Animal Biodiversity and Conservation issue 30.1 (2007) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2007

and

Animal Biodiversity Conservation 30.1

Dibuix de la coberta: teixó, tejón (Meles meles) de Jordi Domènech Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

Secretària de redacció / Secretaria de redacción / Managing Editor Montserrat Ferrer

Museu de Ciències Naturals Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 Nou e–mail abc@bcn.cat

Consell assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Ignacio Doadrio Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Antonio Donazar Estación Biológica de Doñana–CSIC, Sevilla, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Juan José Negro Estación Biológica de Doñana–CSIC, Sevilla, Spain Vicente M. Ortuño Univ. de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Univ. de les Illes Balears, Spain Francisco Palomares Estación Biológica de Doñana–CSIC, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Ignacio Ribera Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Barcelona, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway Animal Biodiversity and Conservation 30.1, 2007 © 2007 Museu de Ciències Naturals, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Romargraf S. A. ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://www.bcn.cat/ABC

Animal Biodiversity and Conservation 30.1 (2007)

Census method for estimating the population size of the endemic and threatened land snail Iberus gualtieranus gualtieranus G. Moreno–Rueda & M. Pizarro

Moreno–Rueda, G. & Pizarro, M., 2007. Census method for estimating the population size of the endemic and threatened land snail Iberus gualtieranus gualtieranus. Animal Biodiversity and Conservation, 30.1: 1–5. Abstract Census method for estimating the population size of the endemic and threatened land snail Iberus gualtieranus gualtieranus.— Iberus gualtieranus gualtieranus is an endemic and threatened land snail inhabiting south–eastern Spain. Because it seeks shelter in karstic fissures when inactive, detection is difficult, and censuses may be biased. In this study, a methodology is developed to take an adequate census of this subspecies. The census was performed in the population of Sierra Elvira when the probability of detection was the highest, minimizing the bias. The results show that this population is patchy and has about 500,000 specimens. However, this subspecies is probably vulnerable to extinction as only three isolated populations are known and it is threatened by several factors. The census method in this study may be useful to conserve this endemic species. Key words: Iberus g. gualtieranus, Census technique, Population size, Distribution. Resumen Método de censado para estimar el tamaño poblacional del caracol Iberus gualtieranus gualtieranus, especie endémica y amenazada.— Iberus gualtieranus gualtieranus es un caracol endémico y amenazado que habita en el sudeste de España. Este caracol se refugia en las grietas kársticas cuando está inactivo, lo que dificulta su detección, sesgando las estimas sobre su tamaño poblacional. En este estudio se desarrolla una metodología para censar esta subespecie. El censo fue realizado en la población de Sierra Elvira cuando la probabilidad de detección de los ejemplares fue máxima, minimizando el sesgo de la estima. Los resultados muestran que esta población está parcheada y tiene unos 500.000 ejemplares. Sin embargo, esta subespecie probablemente sea vulnerable a la extinción, ya que su población mundial se reduce a tres poblaciones aisladas y algunos factores ponen en riesgo su supervivencia. El método de censado presentado en este estudio puede ser útil para el manejo y conservación de esta especie endémica. Palabras clave: Iberus g. gualtieranus, Técnica de censado, Tamaño poblacional, Distribución. (Received 3 VIII 06; Conditional acceptance: 3 XI 06; Final acceptance: 29 XII 06) Gregorio Moreno–Rueda & Manuel Pizarro, Dept. de Biología Animal, Fac. de Ciencias, Univ. de Granada, E–18071, Granada, España (Spain). Corresponding author: G. Moreno–Rueda. E–mail: gmr@ugr.es

ISSN: 1578–665X

Introduction Most animal conservation efforts are directed to vertebrates even though these animals represent only about 1% of the extant biodiversity (Ponder & Lunney, 1999). This contrasts with the current extinction risk among invertebrates, less than 0.3% of which have been evaluated for cataloguing in the IUCN lists (Baillie et al., 2004). Molluscs represent the group with the highest number of recorded extinctions, and terrestrial molluscs are especially prone to disappearance as they include many endemisms with restrained distributions and limited dispersion capacity; restoration of locally extinct populations is therefore difficult (Lydeard et al., 2004). The land snail Iberus gualtieranus is an endemic species in Spain, with the subspecies I. g. gualtieranus being endemic to south–east Spain (Elejalde et al., 2005). This species is presently catalogued as "almost threatened" (LR/nt) by the IUCN (www.redlist.org), but the subspecies I. g. gualtieranus has been proposed as “endangered” (Arrébola, 2002) as only three isolated populations have been sighted: in Sierra de Gádor, Sierra de Jaén and Sierra Elvira (Alonso et al., 1985; fig. 1). Because these populations are some distance from each other, a local extinction would be irreversible (Hanski, 1998). Major threats to this subspecies are habitat destruction (Moreno–Rueda & Ruiz–Avilés, 2005), a primary causes of extinction in land snails (Backeljau et al., 2001), and collection by humans for food and ornamental purposes (Arrébola, 2002). Conservation of this subspecies is important not only because it is endemic, but also because of its peculiar evolution (Backeljau et al., 2001; see Elejalde et al., 2005). Its morphology is flattened, presumably, in order to use karstic fissures as refuge against desiccation (López–Alcántara et al., 1983, 1985; Moreno–Rueda, 2002). This adaptation allows it to dwell in semiarid environments with karstic erosion (Alonso et al., 1985). Moreover, this snail plays a significant role in the semi–arid ecosystems in which it dwells. Iberus g. gualtieranus eats a variety of plants (Moreno–Rueda & Díaz–Fernández, 2003) and is consumed by a variety of organisms, such as birds, rodents and insects (Yanes et al., 1991; pers. obs.), making it an important link in trophic chains. As in other arid environments (Shachak et al., 1987), it probably affects soil fertilization and nutrient recycling. This is the first study performed to determine the distribution and population of this endemic species in the mountains it inhabits. Detection is difficult because it frequently shelters inside crevices (Moreno–Rueda, 2007), making censuses unreliable. In this work, we developed a simple census method to gather reliable information on the population size of this subspecies. Material and methods First, we etimated the distribution of Iberus g. gualtieranus in Sierra Elvira based on records of

Moreno–Rueda & Pizarro

presence–absence during numerous trips throughout the complete study area from 1998–2005. These data were marked on 1:25,000 maps, delimiting its distribution in polygons and including minimal distribution of the records. This map was transferred to a Geographic Information System (SAGA; Conrad, 2005) to estimate the surface occupied by Iberus g. gualtieranus. Iberus g. gualtieranus inhabits crevices when inactive, especially during aestivation (Moreno–Rueda, 2007). Its population size would be underestimated if it were censured when inactive and sheltered. To avoid this bias, we performed a study of snail detection during sampling, considering different times throughout the year and the day (day–night). We delimited an area of about 500 m2, where we sampled in 55 plots of 9 m2. During sampling, we recorded the density of adult and immature individuals detected. We used both adult and immature individuals because the immature:adult ratio is relatively constant throughout the year (personal observations). Exhaustive samples were taken from October 2000 to September 2001, covering the 24 h. To determine the appropriate time to sample the snail, we tested whether density varied between two annual periods: spring–summer (n = 109; when the snail was inactive) and autumn–winter (n = 41; when it was active). Within autumn–winter (the activity period), we tested whether the snail density varied between day (n = 63; the snail was inactive) and night (n = 46; it was active). Activity periods were known from previous unpublished studies. Sampling was performed on randomly selected days. With this methodology, we determined that the appropriate sampling time was in autumn–winter (day or night; see Results). For sampling, we randomly assigned 33 points within the distribution area of Iberus g. gualtieranus (fig. 1). During 2002–2004, we reached these points using maps and a GPS, and we delineated a 9 m2 (3 x 3 m) plot at each point. Therefore, a surface area of 297 m2 was sampled. Live specimens (adult or immature) were exhaustively searched for inside the plots, placing special attention to positions inside fissures, under stones, and in vegetation. With these data, we estimated the average density ± standard error of the mean. Assuming that snail density is homogeneous within its distribution area, we estimated the population size (with an associated error according to the standard error of the mean) in Sierra Elvira with a simple multiplication: density × distribution area. Results Iberus g. gualtieranus was distributed primarily on the eastern slope of Sierra Elvira. Its population was divided into sub–populations (fig. 1), but one of them (polygon 1) included 95% of the surface occupied by this land snail. Therefore, in Sierra Elvira, the population of Iberus g. gualtieranus was concentrated in a large sub–population with minor sub–populations to the north and south. In total, it occupied 323.5 hec-

Animal Biodiversity and Conservation 30.1 (2007)

0 750

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Fig. 1. Location of the three populations of Iberus g. gualtieranus in Spain (A. Sierra de Jaén; B. Sierra Elvira; C. Sierra de Gádor), and distribution of this subspecies in Sierra Elvira. Sampling points and density of individuals are showed. Each subpopulation is designated with a number. Fig. 1. Localización de las tres poblaciones de Iberus g. gualtieranus en España (A. Sierra de Jaén; B. Sierra Elvira; C. Sierra de Gádor), y distribución de la subespecie en Sierra Elvira. Se muestran los puntos de muestreo y la densidad de individuos. Cada subpoblación se designa con un número.

tares (3,235,449 m2) in Sierra Elvira. These results are similar to those previously found by G. González and J. M. Gil–Sánchez (unpublished), suggesting that they are reliable. Density of individuals detected during sampling in autumn–winter (0.22 ± 0.23 individuals/m 2 , n = 109 samples) was significantly higher than in spring–summer (0.06 ± 0.12 ind./m2, n = 41) (Mann– Whitney U–test, z = 4.49, p < 0.001), suggesting that the census should be performed during the autumn–winter period. This period showed no significant differences in density during the day (0.19 ± 0.18 ind./m2, n = 63) and the night (0.25 ± 0.28 ind./m2, n = 46) (U–test, z = 0.50, p = 0.62), justifying the census being performed during the day for logistical reasons. These results are due to the different use of refuges between the two periods of activity, with individuals deeply sheltered in crevices during aestivation (Moreno–Rueda, 2007). In the census performed during autumn–winter in the years 2002–2004, we detected 46 specimens. The mean density was 0.155 ± 0.049 individuals per m2. With these data, we estimated a population size in Sierra Elvira of 501,495 ± 158,537 individuals of Iberus g. gualtieranus. With the standard error, this population size may oscillate between 342,958 and 660,032 individuals.

Discussion In this study, we developed a census method for estimating abundance of Iberus g. gualtieranus, an endemic and threatened land snail that is difficult to detect. This is the first census for this subspecies. It is improbable that the results were affected by population dynamics, as density of individuals (both adult and immature) is almost constant throughout the year, especially in autumn–winter (unpublished data). The seasonal use of refuges also could affect the results (Moreno–Rueda, 2007); for this reason, censuses should be performed in autumn–winter. In these seasons, the activity period of this snail (active primarily during the night) did not have significant effects on the density estimated, as they seemed easy to detect during the day. As this methodology appears to be effective it could be used for the other two known populations of this snail, and for other species presenting a similar problem. Information gathered may also be useful to determine the conservation status of this endemic subspecies in Sierra Elvira. Iberus g. gualtieranus showed a patchy distribution in Sierra Elvira (fig. 1). Patchy populations bear a higher risk of extinction, so that re–colonization of locally extinct sub–populations is lower (Schwartz,

1997; Hanski, 1998). This effect is probably higher for snails, because their dispersal capacity is very restricted (Denny, 1980). Some 95% of the population was concentrated in polygon 1, thus this sub– population is probably at lower risk of extinction than the other sub–populations. The small size of the other sub–populations (polygons 2–6) may make them very vulnerable to extinction (Hanski, 1998). Habitat destruction by mining (Moreno–Rueda & Ruiz–Avilés, 2005), excessive collection (Arrébola, 2002), or fire (C. M. A., 2003) could easily drive these sub–populations to extinction. These patches should be protected, for example, by the creation of micro–reserves. The total population size of Iberus g. gualtieranus in Sierra Elvira was about 500,000 individuals. This result is similar to that found in a preliminary study, performed in 1998 in 148 m2 and using the same methodology, in which the population was estimated at about 575,000 individuals (Moreno–Rueda & Cabrera Coronas, 2000). That both studies give very similar results in different years strongly suggests that the methodology gives repeatable findings. This not only supports the method’s reliability, but also suggests that sampling an area of 297 m2 is sufficient for an appropriate estimate. The relatively large number of specimens found may suggest that the population of Sierra Elvira is not endangered. Nevertheless, this population is completely isolated from populations in Jaén and Almería, and this situation of biogeographic isolation implies that it would be irrecoverable if it went extinct. On the other hand, the number of individuals does not define population viability, which is determined by the relationship between the number of extant individuals and those necessary for a viable population. The latter depends on the characteristics of the species. Studies of population dynamics are needed to conclude whether this population is stable or in decline. In conclusion, the low density, geographic isolation and a patchy distribution are risk factors that should be considered in order to conserve this endemic subspecies. Because the worldwide population of this snail is severely patchy, with only three, completely isolated, populations (fig. 1), it can be considered endangered. For these reasons, we suggest that protection measures should be taken in order to avoid excessive exploitation and habitat destruction. We also recommend that the methodology employed in the present study be used in future censuses in the three populations in order to update information on the status of this endemic subspecies. Any population decline could thus be detected and appropriate measures could be taken. Acknowledgements Amelia Ocaña enthusiastically supported this study from its beginning. Pablo Cabrera Coronas, David F. Díaz Fernández, Francisco A. Ruiz Avilés, Rocío

Moreno–Rueda & Pizarro

Márquez Ferrando and Rubén Rabaneda Bueno collaborated in the field work. Comments by José María Gil–Sánchez, José Ramón Arrébola and an anonymous referee improved the manuscript. David Nesbitt improved the English. References Alonso, M. R., López–Alcántara, A., Rivas, P. & Ibáñez, M., 1985. A biogeographic study of Iberus gualtierianus (L.) (Pulmonata: Helicidae). Soosiana, 13: 1–10. Arrébola, J. R., 2002. Caracoles terrestres de Andalucía. Consejería de Medio Ambiente–Junta de Andalucía, Cádiz. Backeljau, T., Baur, B. & Baur, A., 2001. Population and conservation genetics. In: The biology of terrestrial molluscs: 383–412 (G. M. Barker, Ed.). CAB International, Wallingford. Baillie, J. E. M., Hilton–Taylor, C. & Stuart, S. N., 2004. 2004 IUCN Red List of Threatened Species. A Global Species Assessment. IUCN, Gland and Cambridge. C. M. A., 2003. Suelta de un caracol endémico de Andalucía en un área de la sierra almeriense de Gádor. Quercus, 209: 11. Conrad, O., 2005. SAGA 2.0.0b (System for Automated Geoscientific Analyses) [computer program]. GNU, General Public License (GPL). Geographisches Institut, Göttingen. Denny, M., 1980. Locomotion: the cost of Gastropod crawling. Science, 208: 1288–1290. Elejalde, M. A., Muñoz, B., Arrébola, J. R. & Gómez– Moliner, B. J., 2005. Phylogenetic relationship of Iberus gualtieranus and I. alonensis (Gastropoda: Helicidae) based on partial mitochondrial 16S rRNA and COI gene sequences. Journal of Molluscan Studies, 71: 349–355. Hanski, I., 1998. Metapopulation dynamics. Nature, 396: 41–49. López–Alcántara, A., Rivas, P., Alonso, M. R. & Ibáñez, M., 1983. Origen de Iberus gualtierianus. Modelo evolutivo. Haliotis, 13: 145–154. – 1985. Variabilidad de Iberus gualtierianus (Linneo, 1758) (Pulmonata, Helicidae). Iberus, 5: 83–112. Lydeard, C., Cowie, R. H., Ponder, W. F., Bogan, A. E., Bouchet, P., Clark, S. A., Cummings, K. S., Frest, T. J., Gargominy, O., Herbert, D. G., Hershler, R., Perez, K. E., Roth, B., Seddon, M., Strong, E. E. & Thompson, F. G., 2004. The global decline of nonmarine mollusks. BioScience, 54: 321–330. Moreno–Rueda, G., 2002. Selección de hábitat por Iberus gualtierianus, Rumina decollata y Sphincterochila candidissima (Gastropoda: Pulmonata) en una sierra del sureste español. Iberus, 20: 55–62. – 2007. Refuge selection by two sympatric species of arid–dwelling land snails: Different adaptive strategies to achieve the same objective. Journal of Arid Environments, 68: 588–598. Moreno–Rueda, G. & Cabrera Coronas, P., 2000.

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La situación de Iberus gualtieranus ecotipo gualtieranus (Gastropoda: Stylomathophora: Helicidae) en Sierra Elvira (Granada, España). I Jornadas de Fauna Andaluza, Víznar. Moreno–Rueda, G. & Díaz–Fernández, D. F., 2003. Notas sobre la alimentación de Iberus gualtierianus gualtierianus (Linnaeus, 1758) (Gastropoda: Helicidae). Acta Granatense, 2: 89–92. Moreno–Rueda, G. & Ruiz–Avilés, F. A., 2005. Impacto de las canteras en el monte granadino de Sierra Elvira. Quercus, 233: 4. Ponder, W. F. & Lunney, D. (Eds.), 1999. The other 99%. The conservation and biodiversity of inver-

tebrates. Royal Zoological Society of New South Wales, Mosman. Schwartz, M. W. (Eds.), 1997. Conservation in highly fragmented landscapes. Chapman & Hall, New York. Shachak, M., Jones, C. G. & Granot, Y., 1987. Hervibory in rocks and the weathering of a desert. Science, 236: 1098–1099. Yanes, M., Suárez, F. & Manrique, J., 1991. La cogujada montesina, Galerida theklae, como depredador del caracol Otala lactea: comportamiento alimenticio y selección de presa. Ardeola, 38: 297–303.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 30.1 (2007)

Area selection for the conservation of butterflies in the Iberian Peninsula and Balearic Islands H. Romo, M. L. Munguira & E. García–Barros

Romo, H., Munguira, M. L. & García–Barros, E., 2007. Area selection for the conservation of butterflies in the Iberian Peninsula and Balearic Islands. Animal Biodiversity and Conservation, 30.1: 7–27. Abstract Area selection for the conservation of butterflies in the Iberian Peninsula and Balearic Islands.— Coverage provided by the network of protected areas in the Iberian Peninsula and Balearic Islands was tested by measuring the coincidence between the squares protected by the network and the butterfly species recorded for such UTM grid squares. Five species were found to be absent in the network. The protected areas with the highest numbers of butterfly species were Ordesa National Park and Monte Perdido and the Posets– Maladeta Natural Park. Priority areas were selected using WORLDMAP software and showed that the all species of butterflies in the Iberian Peninsula and Balearic Islands can be found within 16 squares of 10 x 10 km (nine of them not within the network of protected areas). More specific area selections were also carried out: eight squares supported the total number of threatened species, five hosted all the Iberian endemisms and 13 harboured the rare butterfly species. This study detected 16 squares that are not currently protected but are important for butterfly conservation in the Iberian Peninsula and Balearic Islands. Key words: Conservation, Butterflies, Gap analysis, Protected areas, Iberian Peninsula, Balearic Islands. Resumen Selección de áreas para la conservación de las mariposas diurnas de la Península Ibérica e Islas Baleares.— Se ha analizado el nivel de cobertura que proporciona la red de espacios protegidos en la Península Ibérica e Islas Baleares comprobando la coincidencia entre éstos y el número de especies de mariposas registrado. Cinco especies quedan excluidas de la red. Los espacios protegidos con mayor número de especies fueron el Parque Nacional de Ordesa y Monte Perdido y el Parque Natural de Posets– Maladeta. Se realizó también una selección de áreas utilizando el programa WORLDMAP en la que 16 cuadrículas de 10 km de lado albergan a la totalidad de mariposas de la Península Ibérica y Baleares (nueve de ellas no se encuentran dentro de la red de espacios protegidos). También se realizaron selecciones de áreas más específicas: ocho cuadrículas fueron suficientes para albergar la totalidad de especies amenazadas, cinco para los endemismos ibéricos y 13 para las especies de mariposas raras. Basándonos en estos resultados se seleccionaron 16 cuadrículas en el área de estudio que son importantes para la conservación de mariposas y que actualmente no están protegidas. Palabras clave: Conservación, Mariposas diurnas, Análisis de huecos, Espacios protegidos, Península Ibérica, Islas Baleares. (Received: 31 X 06; Conditional acceptance: 24 XI 06: Final acceptance: 16 I 07) Helena Romo Benito, Miguel L. Munguira & Enrique García–Barros, Depto. de Biología (Zoología), Univ. Autónoma de Madrid, Carretera de Colmenar km. 15, 28049 Madrid, España (Spain). Corresponding author: H. Romo. E–mail: helena.romo@uam.es

ISSN: 1578–665X

Introduction The Lepidoptera is the third most diverse insect order (following Coleoptera and Diptera: Gullan & Cranston, 2000), with ca. 70 families and 140,000 species, 20,000 of which are butterflies (Heppner, 1991). Butterflies are strongly climate–dependent (e.g. Dennis, 1993; Stefanescu et al., 2003), and their phytophagous larvae favor specific plant taxa. Hence, they are generally believed to be good environmental indicators (New, 1991; Kremen, 1992; Cleary, 2004). A remarkable decline in butterfly diversity is becoming increasingly evident, especially in central western Europe (Konvicka et al., 2006). Local or regional losses are largely caused by human activity (e.g. Warren et al., 2001; Hill et al., 2002; Pullin, 2002; Pennisi, 2004; Thomas et al., 2004; Pounds et al., 2006). For instance, the distribution range of some British species has decreased by 46% in recent times (Asher et al., 2001), and 21% of the Dutch species vanished during the last century (Van Swaay, 1990). There is some evidence that changes in elevational limits associated with climate warming might be occurring in Central Spain (Wilson et al., 2005). Spanish policy for the preservation of biodiversity includes the creation of four main categories of natural preserved areas (Ley 4/89 de Conservación de los Espacios Naturales y de la Flora y Fauna Silvestres, artículo 12), i.e.: "Parques" (National and Natural Parks), "Reservas Naturales" (Nature Reserves), "Monumentos Naturales" (Natural Monuments) and "Paisajes Protegidos" (Protected Landscapes). These categories are also applicable in Portugal (ICN–Instituto da Conservação da Natureza, http://www.icn.pt/). On a more communitarian level, there is an additional array of legally protected sites and areas. These areas co–exist with the Natura 2000 Network which includes the Sites of Community Importance (SCIs) and the Special Protection Areas (SPAs) (Múgica de la Guerra & Gómez–Limón, 2002; Múgica de la Guerra et al., 2005). The conservation status of Iberian species and evaluations of the coverage offered by the network of protected areas have been dealt with in some detail for the flora (Castro et al., 1996; Araújo, 1999; Martínez et al., 2001; Cerrillo et al., 2002; Moreno et al., 2003) and the vertebrate fauna (Araújo, 1999; Carrascal et al., 2002; De la Montaña & Rey Benayas, 2002; Carrascal & Lobo, 2003; Lobo & Araújo, 2003; Rey Benayas & De la Montaña, 2003; Filipe et al., 2004; Carrascal et al., 2006; Egea–Serrano et al., 2006; Razola et al., 2006; Rey Benayas et al., 2006). Invertebrates have been far less profusely dealt with (e.g. Rosas et al., 1992; Ribera, 2000). Red Books available include those by Gómez Campo (1987), Palomo & Gisbert (2002), Pleguezuelos et al. (2002), and Verdú & Galante (2006). An "economy" criterion to design networks of protected areas would require the selection of a minimal number of area units with a maximal number

Romo et al.

of species. This can be done in several ways (Cabeza & Moilanen, 2001). One technique is Gap Analysis (Burley, 1988; De la Montaña & Rey Benayas, 2002; Méndez, 2003), which first involves setting a hierarchy of area units (e.g. land squares) ordered by decreasing species richness until the set of geographic units hosts the full set of species considered. The selection is then contrasted with the network of preserved areas (using the same geographic units), to detect the squares not included in the protected network ("gaps"; see e.g. Burley, 1988; Pullin, 2002). Gap analysis has been applied to Iberian plants (Castro et al., 1996) and vertebrate animals (Williams et al., 1996; De la Montaña & Rey Benayas, 2002; Rey Benayas & De la Montaña, 2003; Rodrigues et al., 2004a; Rodrigues et al., 2004b; Wall et al., 2004). Several quantitative analyses have been used for the selection of priority areas for conservation (hotspots of rarity, hotspots of richness, random selection and area complementarity: Williams et al., 1996; Araújo, 1999; Ramírez, 2000; Cerrillo et al., 2002; Lobo & Araújo, 2003). Area complementarity seems to be best suited to maximise the full representation of species and to supplement pre–existing networks of protected spaces (Williams et al., 1996; Balmford & Gaston, 1999; Méndez, 2003). Accordingly, complementarity–based approaches have been applied in several geographic contexts (e.g. Ando et al., 1998; Howard et al., 1998; Rodrigues & Gaston, 2002a; Gaston & Rodrigues, 2003; Roig–Juñent & Debandi, 2004) including the Iberian Peninsula (Araújo, 1999; Martín–Piera, 2001; Carrascal & Lobo, 2003; Lobo & Araújo, 2003). Although the outputs obtained by different methods were tested in the present study, we chose area complementarity using richness because this method has proven to be more suitable in butterfly studies. Analyses of the Iberian butterfly fauna intended for conservation purposes have concentrated either on analysing the species status, or on qualifying land cells by means of species diversity at a regional scale (Viejo et al., 1989; Moreno, 1991; García–Barros et al., 1998), for the Spanish territory (De Viedma & Gómez–Bustillo, 1976, 1985; Munguira & Martín, 1993; Carrión & Munguira, 2001, 2002), Portugal (Garcia–Pereira, 2003) or the whole of the Iberian Peninsula (Munguira, 1989; Munguira et al., 1991, 2003). A preliminary gap–analysis based on selected species was attempted by Carrión & Munguira (2002) for the Spanish butterflies. However, none of these works has used a detailed and extensive database from the whole Iberian butterfly fauna. Comprehensive faunistic information on the Ibero–Balearic butterflies has recently been compiled (García–Barros et al., 2004), allowing an exhaustive evaluation based on updated data. Thus the main aim of this study was to provide, for the first time, a test for the coverage of the Spanish–Portuguese network of protected areas in terms of butterfly species richness. For the reasons mentioned above, this was primarily attempted using richness–based complementarity (although alternative options are

Animal Biodiversity and Conservation 30.1 (2007)

briefly discussed). More specifically, our objectives were: 1) to determine how many and which species are not represented within the network of protected areas, 2) to estimate how much land surface and what sites should be added to the set of preserved areas so that the network provide coverage to all the butterfly species, 3) to identify the most outstanding protected areas from two points of view: for their species diversity or for hosting relevant (threatened, rare, endemic) butterfly species, 4) to select the best subsets of squares for the rare, endemic and threatened Iberian and Balearic species, and finally, 5) based on the former results, to determine which area units (among those not currently protected) should be considered for inclusion in the present network of protected areas. Material and methods Study area The study area was the Iberian Peninsula and the Balearic Islands. The total area is of 584,192 km2, of which 49,900 km2 (8.5%) are formally protected by law. The operative geographic units were the UTM (Universal Transverse Mercator) 10 x 10 km grid squares, a system which has previously been used in conservation studies (Viejo et al., 1989; Munguira et al., 1991; Rey Benayas & De la Montaña, 2003). As an operative criterion, the number of the UTM grid squares that totally or partially include a protected area of any extent was calculated. Species, occurrence data and rarity We used an updated version of the data described by García–Barros et al. (2004), consisting of 290,329 records assigned to 10 x 10 km UTM grid squares for 223 species of butterflies (Lepidoptera, superfamilies Papilionoidea & Hesperioidea). The number of species present in the protected areas was determined by compiling all the species present in the 10 x 10 km squares that had some part of their area within the boundaries of the protected areas. The status and list of threatened species follows Verdú & Galante (2006), endemicity status is taken from García–Barros et al. (2000, 2002) and both lists are shown in table 1. Species rarity was calculated as (1 / n), where n is the number of 10 km grid squares where the species has been recorded (table 1). Species with an estimated rarity 15% below the maximum value were treated as "rare" in the analyses (e.g. Rey Benayas & De la Montaña, 2003). Network of protected areas Information on the limits and extent of the Spanish natural protected areas was gathered from the Ministerio de Medio Ambiente (www.mma.es) and Europarc (www.europarc–es.org) and from the

Instituto da Conservação da Natureza (http:// www.icn.pt/) and Garcia–Pereira (2003) in the case of Portugal. We took into account 205 Natural Monuments, 10 National Parks, 130 Natural Parks and 209 Nature Reserves. Overall, this network comprised 1,282 10 km squares, which represents roughly 20% of the total number of squares in the study area. An analysis of the most outstanding protected areas was carried out, i.e. those that hosted the highest number of species or threatened species. Data analysis The package WORLDMAP 4.17.08 (Williams, 1997) was used. This application was developed to estimate and represent patterns of diversity, rarity and species richness and to facilitate the area selection for management and conservation purposes (Ghillean, 2000). It performs analyses based in complementarity criteria (Méndez, 2003) and has been applied to a wide range of organisms at varied locations and geographic scales (Castro et al., 1996; Araújo, 1999; Williams & Araújo, 2000; Balmford et al., 2001; Lobo et al., 2001; Lobo & Araújo, 2003). Some of the cartographic results were represented using MapInfo software (MapInfo, 1994); and AutoCAD (AutoCAD, 2004) was used for complementary estimates of area and coverage. Priority area selection and Gap Analysis To define the minimum number of squares that are necessary to host the total number of butterfly species in the Iberian Peninsula and Balearic Islands, an area selection was performed with the automatic option and using richness as criteria with the function Greedy area set of the WORLDMAP program (Williams, 1997), which uses the algorithm designed by Kirkpatrick (1983). This procedure uses a complementarity criterion, with a species richness map as a starting point and adding new squares according to their contribution to the total number of species already included in the previous selection. When there is a conflict between two squares adding the same number of species the program chooses the option with higher richness value. The squares are added until the selected squares are representative of the total number of species. The selected areas were then matched with the protected areas map to spot which squares were outside the current network of protected areas. This protocol (Gap Analysis; Pullin, 2002) identified the priority squares for butterfly conservation in the studied area and their possible interest as new conservation areas. As a validation for our method, we tested whether random area selections (made ten times with 1,000 replicas each) produced a better performance as far as the number of species hosted by the same number of squares is concerned. We also identified

Romo et al.

Table 1. List of threatened, endemic (E) and rare (R) species considered in this work. Threatened species follow the Red Data Book of the Spanish Invertebrates (RDB, Verdú & Galante, 2006: EN. Endangered; VU. Vulnerable; NT. Near threatened; LC. Least concern), European Red Data Book (ERDB, Van Swaay & Warren, 1999: SPEC 1. Species of global conservation concern; SPEC 3. Species threatened in Europe, but with headquarters both within and outside Europe; SPEC 4a. Global distribution restricted to Europe, but no threatened; SPEC 4b. Global distribution concentrated in Europe, but no threatened) and the Bern Convention (BC) and Habitats Directive (HD) annexes II and IV are also given. P. apollo is protected by CITES Convention; and M. nausithous (VU) and P. golgus (EN) are protected by the Spanish National Catalogue of Threatened Species. Endemic species are shown with a cross (X). If the distribution of endemic species comprises the North of Pyrenees, this is indicated by an asterisk (*). The last column details the number of 10 x 10 km UTM grid squares in which the rare species are present. Tabla 1. Lista de las especies consideradas como amenazadas, endémicas (E) y raras (R) en este trabajo. Se muestran las especies consideradas amenazadas según el Libro Rojo de los Invertebrados de España (RDB, Verdú & Galante, 2006: EN. En peligro; VU. Vulnerable; NT. Casi amenzada; LC. Preocupación menor), las categorías SPEC del European Red Data Book (ERDB, Van Swaay & Warren, 1999: SPEC 1. Especies amenazadas a escala mundial; SPEC 3. Especies amenazadas en Europa, cuyas poblaciones no se encuentran mayoritariamente en este continente; SPEC 4a. Especies cuya distribución se encuentra restringida a Europa pero no se encuentran amenazadas; SPEC 4b. Especies no amenazadas en Europa que presentan una distribución global aunque concentrada en este continente), y las mariposas protegidas en los anexos II y IV del Convenio de Berna (BC) y la Directiva de Hábitats (HD). P. apollo además se encuentra dentro del convenio de CITES y M. nausithous (VU) y P. golgus (EN) dentro del Catálogo Nacional de Especies Amenazadas de España. Los endemismos aparecen representados con una cruz (X). En el caso de que el endemismo se encuentre en el Norte de los Pirineos se representa con un asterisco (*). Se muestra el número de cuadrículas de 10 km de lado en las que se encuentran las especies consideradas raras.

Threatened species

RDB

Agriades glandon (Prunner, 1798)

SPEC 4a

Agriades pyrenaicus (Boisduval, 1840) Agriades zullichi Hemming, 1933

ERDB SPEC 4a

Aricia morronensis Ribbe, 1910

SPEC 4a

Aricia nicias (Meigen, 1829)

SPEC 4a

R 36

* 16

Azanus jesous (Guérin, 1849)

Boloria eunomia (Esper, 1799)

Boloria napaea (Hoffmannsegg, 1804)

Borbo borbonica (Boisduval, 1833)

Carterocephalus palaemon (Pallas, 1771)

Carchadorus tripolinus (Esper, [1780])

Chazara prieuri (Pierret, 1837)

SPEC 4b

Erebia epistygne (Hübner, [1824])

SPEC 1 VU

Erebia gorgone (Boisduval, [1833])

SPEC 4a

Erebia hispania Butler, 1868

SPEC 4a

Erebia lefebvrei (Boisduval, 1828)

SPEC 4a

Erebia manto (Denis & Schiffermüller, 1775)

SPEC 4a

Erebia oeme (Hübner, [1804])

SPEC 4a

Erebia palarica Chapman, 1903

Erebia pandrose (Borkhausen, 1788)

Erebia pronoe (Esper, [1780])

SPEC 4a

Erebia sthennyo (Graslin, 1850)

SPEC 4a

25 28

Erebia zapateri Oberthür, 1875

SPEC 4a

Animal Biodiversity and Conservation 30.1 (2007)

Table 1. (Cont.) Threatened species Euchloe charlonia (Donzel, 1842)

RDB

ERDB

Gegenes pumilio (Hoffmannsegg, 1804)

Lasiommata petropolitana (Fabricius, 1787) Lopinga achine (Scopoli, 1763)

13 VU

SPEC 3 VU

Lycaena bleusei Oberthür, 1884 Lycaena helle (Denis & Schiffermüller, 1775)

SPEC 3 VU

Maculinea rebeli (Hirschke, 1904)

SPEC 1 VU

Melitaea aetherie (Hübner, [1826])

SPEC 3 EN

Parnassius apollo (Linnaeus, 1758)

SPEC 3 VU

Parnassius mnemosyne (Linnaeus, 1758)

Plebejus hespericus (Rambur, 1839)

Polyommatus fabressei (Oberthür, 1910)

4 II

II, IV

Polyommatus nivescens (Keferstein, 1851)

SPEC 1 VU

SPEC 4a

Polyommatus fulgens (Sagarra, 1925)

Pseudochazara hippolyte (Esper, 1784)

6 X

Maculinea nausithous (Bergsträsser, [1779])

Polyommatus golgus (Hübner, [1813])

SPEC 4a SPEC 4a

II, IV

Pseudophilotes panoptes (Hübner, [1813])

Pyrgus andromedae (Wallengren, 1853)

SPEC 4a

Pyrgus bellieri (Oberthür, 1910)

SPEC 4a

SPEC 4a NT

Pyrgus cacaliae (Rambur, [1840]) Pyrgus cinarae (Rambur, [1840])

Pyrgus sidae (Esper, [1782])

Satyrium pruni (Linnaeus, 1758)

Satyrus ferula (Fabricius, 1793)

Tarucus theophrastus (Fabricius, 1793)

the 16 squares with higher species richness (hotspots of richness), the 16 with higher rarity (hotspots of rarity) and made an area selection using complementarity based on rarity (Near minimum area set, NMS). The latter uses a rarity algorithm that is based on Margules et al. (1988), that gives priority to squares that have the highest number of rare species. Then it adds the squares that host the largest amount of rare species to the previous set, until the total number of species is represented. When two squares add the same number of new rare species, the program selects that with the highest number of overall rare species, and if even these are similar it makes a random selection choosing the square with the lowest label number. The same set of analyses was performed using only the data with threatened, endemic or rare species.

Species not included in the network of protected areas To spot the species that were completely excluded from the current network of protected areas a map with these areas was superimposed with the distribution map for each species (depicted with data of the ATLAMAR database). Each species was then tested for presence in the network of protected areas and the species with no representation in this network were selected. The distribution of these excluded species was then represented in a map and an area selection with these species was performed. This selection resulted in areas that needed to be added to the network of protected areas. Conservation of such areas would assure that all the species have at least one population within the network of protected areas.

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139 94 76 67 58 50 45 40 36 32 29 27 24 22 19 16 14 12 9 8 6 5 4 3 2 1

Fig. 1. Geographic distribution of butterfly species richness in the Iberian Peninsula and Balearic Islands obtained with the use of the WORLDMAP program. The highest number of species in each 10 x 10 km UTM square is shown in darker grey tones. Fig. 1. Mapa de riqueza de especies de mariposas de la Península Ibérica e Islas Baleares obtenido mediante la aplicación del programa WORLDMAP. El mayor número de especies diferentes por cuadrícula UTM de 10 km de lado se muestra con tonalidades de gris más oscuras.

Results Species richness The maximum species richness (139 species, 62.33% of the total) was detected in the squares in the National Park of Ordesa y Monte Perdido (Huesca Province) and in Viella (Lérida) (fig. 1; table 2). Highest species numbers concentrate in mountain ranges. The Portuguese territory is overall dominated by a high proportion of low–richness squares.

29SNB70, 29TNF25, 31SDD68) would still not fall within any protected area. Alternative selections of squares based on random selection, hotspots of richness, hotspots of rarity, or complementary areas based on rarity were compared with complementary areas based on richness (table 4). The selection based on rarity criterion generally pointed out similar squares that were used as alternatives to the 16 formerly identified. The most relevant difference was the square in Sierra de Baza instead of the formerly selected one in Los Monegros, both supported by the presence of Euchloe charlonia.

Selection of priority areas The use of WORLDMAP with the species richness criterion resulted in a selection of 16 squares (fig. 2A) which altogether would host the whole set of Iberian butterflies, with each species represented in at least one square (table 3). Only seven of these squares (43.8%) belong to the present network of protected areas (fig. 2A), although one of them includes a Protected Landscape. If the Sites of Community Importance (SCIs) were considered as an effective figure for butterfly conservation, the figure would rise to 13 squares; similarly, 12 squares are included in Special Protection Areas (SPAs). In the best of these combinations, three squares (i.e.

Species not included in the network of protected areas The number of species present in each of the main protected areas is summarised in table 5. Five species are not represented in any of the actual protected areas, i.e.: Gegenes pumilio (rare), Pyrgus cinarae (vulnerable, rare), Euchloe charlonia (near threatened, rare), Boloria napaea (rare) and Satyrium pruni (rare) (details and conservation status in table 1). These five butterflies have been recorded from different (non–coincident) subsets of a total of 38 squares; a selection of areas based solely on these species is given in table 6.

Animal Biodiversity and Conservation 30.1 (2007)

3 8

7 12 2

6 4

B 5

8 4

3 7 1

Fig. 2. Selection of high–priority squares for the conservation of butterfly species in the Iberian Peninsula and Balearic Islands, using the complementarity criteria based on richness with the WORLDMAP program. The numbers show the hierarchical position of the areas. The network of protected areas is shown in grey. Stars represent the coincidence between the priority areas selected by the program and the network of protected areas. Circles show the gaps where this selection does not match the network: A. Selection with all the species, the 16 selected squares together host all the Peninsular and Balearic butterfly species; B. The eight selected squares jointly host the total number of threatened species in the study area. Fig. 2. Selección de cuadrículas prioritarias para la conservación de mariposas en la Península Ibérica e Islas Baleares, utilizando el criterio de complementariedad basado en la riqueza con el programa WORLDMAP. Las selecciones se presentan de forma jerárquica indicada por la numeración. En gris se representa la red de espacios protegidos. Las estrellas muestran la coincidencia de las áreas seleccionadas por el programa con la red de espacios naturales protegidos. Los círculos indican los huecos donde la selección no coincide con la red de espacios: A. Selección con todas las especies, las 16 cuadrículas, consideradas en conjunto, contienen la totalidad de especies de mariposas iberobaleares; B. Selección con las especies amenazadas, ocho cuadrículas UTM de 10 km de lado presentan, en conjunto, la totalidad de especies de mariposas diurnas amenazadas en el área de estudio.

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Table 2. Analysis of butterfly species richness in the Iberian Peninsula and Balearic Islands performed using the WORLDMAP program. Values of relative richness (in percentage) referring to the total (223) species are given. Six of these 10 x 10 km UTM grid squares are listed with their respective localities. They account for the highest values in the number of different species (N). Tabla 2. Análisis de riqueza de especies de mariposas en la Península Ibérica e Islas Baleares realizada con el programa WORLDMAP, en el que se obtienen los valores de riqueza relativa (en porcentaje) respecto al total (223 especies). Se muestran las seis cuadrículas UTM de 10 km de lado, con sus respectivas localidades, que presentan los valores más altos de número de especies (N) diferentes que albergan. N

Richness (%)

UTM square

Locality

Province

139

61.78%

30TYN32

P. N. Ordesa

Huesca

139

61.78%

31TCH13

Viella

Lérida

136

60.44%

30TXK37

Albarracín

Teruel

132

58.67%

30TUN57

Fuente De

Cantabria

132

58.67%

30TYN23

Panticosa

Huesca

131

58.22%

30TWM92

Sierra del Moncayo

Zaragoza

Table 3. Results obtained in the selection (S) of high–priority squares for the conservation of butterfly species in the Iberian Peninsula and Balearic Islands, using the complementarity criteria based on richness with the WORLDMAP program. Localities are shown according to the hierarchical selection order. The number of species registered in each square (SR), the number of new species added in the selection (SA) and their presence (yes) or absence (no) in the network of protected areas (PA) are also shown. Tabla 3. Resultados obtenidos en la selección de cuadrículas prioritarias para la conservación de mariposas en la Península Ibérica e Islas Baleares, utilizando el criterio de complementariedad basado en la riqueza con el programa WORLDMAP. Se muestran: las localidades según el orden de selección, el número de especies citadas en esa cuadrícula (SR), el número de especies nuevas que añaden en la selección (SA) y su presencia (yes) o ausencia (no) en la red de espacios naturales protegidos (PA). S

UTM square

Locality

30TYN32

P. N. Ordesa (Huesca)

139

Yes

30TXK37

Albarracín (Teruel)

136

Yes

31TCH13

Viella (Lérida)

139

30STF70

Algeciras (Cádiz)

30TUN57

Fuente De (Cantabria)

30SVG90

7 8 9

30TTK66

La Garganta (Cáceres)

30TUN39

Covadonga (Asturias)

Yes

30TVN06

Reinosa (Cantabria)

Yes

30TWK96

Tragacete (Cuenca)

127

30TWN21

Montoria (Álava)

115

29SNB70

Faro (Algarve)

Yes

132

Yes

Puerto de la Ragua (Granada)

Yes

29TNF25

Porto (Douro Litoral)

31TDG39

Nuria (Gerona)

102

31TBF59

Los Monegros (Huesca)

31SDD68

Son Espanyolet (Mallorca)

Animal Biodiversity and Conservation 30.1 (2007)

Table 4. Assessment of the efficiency of the current network of protected areas (regarding UTM squares with any percentage of protected surface, or UTM grid squares with more than 15% of their surface protected). We compared the number of threatened, endemic, rare species and the total of butterfly species in the Iberian Peninsula and Balearic Islands by several area selections based on different criteria (random selection, hotspots of richness and rarity, and complementarity). The number of UTM squares considered for each selection, the number of species recorded in these squares and the relative percentage in relation to the total in each case are shown. The asterisk (*) represents average ± standard deviation. Tabla 4. Valoración de la efectividad de la red de espacios protegidos actualmente existente (considerando las cuadrículas UTM con cualquier porcentaje de espacio protegido, y aquellas cuadrículas UTM que tengan más del 15% de su superficie protegida) y comparación con la representatividad que ofrecen las selecciones de áreas aleatorias, los puntos de máxima riqueza y rareza y las selecciones de áreas complementarias a las especies amenazadas, endémicas, raras y a la totalidad de las especies de mariposas de la Península Ibérica e Islas Baleares. Se muestra el número de cuadrículas UTM de 10 km de lado consideradas en cada caso, el número de especies que reúnen y el porcentaje de estas especies respecto al total de especies consideradas en el área de estudio en cada caso. El asterisco (*) indica la media ± la desviación estándar.

No. of squares All species

Threatened

Protected areas

1,282

218

97.76

718

211

94.62

Hotspots of richness

197

88.34

Hotspots of rarity

202

90.58

Complementarity (1 representation)

223

100

Complementarity with rarity (NMS)

223

100

Random selection*

133 ± 0,9

59.64

1,282

87.5

Protected areas

718

68.75

Hotspots of richness

62.50

Hotspots of rarity

62.50

Complementarity (1 representation)

100

Complementarity with rarity (NMS)

100

Random selection*

6 ± 0,5

37.5

1,282

100

718

87.5

Hotspots of richness

Hotspots of rarity

43.75

Complementarity (1 representation)

100

Complementarity with rarity (NMS)

100

Protected areas Protected areas (> 15%)

Random selection* Rare

% Species

Protected areas (> 15%)

Endemic

Species

5±0

31.25

1,282

81.82

Protected areas (> 15%)

718

63.64

Hotspots of richness

57.58

Hotspots of rarity

69.70

Complementarity (1 representation)

100

Complementarity with rarity (NMS)

100

Random selection*

12 ± 0

36.36

Protected areas

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Table 5. Number of different butterfly species (N) present in the richest protected areas in the Iberian Peninsula and Balearic Islands. The percentage shows the species present in the protected areas with regard to the total number of diurnal butterflies in the study area (223). The protected areas with percentages above 50% are those included in the table. Tabla 5. Número de especies diferentes de mariposas (N) que presentan los espacios protegidos de mayor riqueza en la Península Ibérica e Islas Baleares. El porcentaje indica las especies que están presentes en el espacio protegido respecto al número total de especies de mariposas diurnas del área de estudio (223). Las áreas protegidas con porcentajes mayores del 50% son las incluidas en la tabla.

Protected area

Ordesa y Monte Perdido

160

71.7

Posets–Maladeta

159

71.3

Parque Regional de los Picos de Europa

152

68.2

Parque Nacional de los Picos de Europa

148

66.4

Massís del Montseny

144

64.6

Cadí–Moixeró

144

64.6

La Sierra y Cañones de Guara

138

61.9

Fuentes Carrionas y Fuente Cobre

137

61.4

Moncayo

132

59.2

Urbasa y Andia

132

59.2

Cuenca Alta del Manzanares

130

58.3

Zona Volcánica de La Garrotxa

129

57.8

Gorbeia

126

56.5

Sierra de Cebollera

125

56.1

Sierras de Cazorla, Segura y Las Villas

122

54.7

Cumbre, Circo y Lagunas de Peñalara

121

54.3

Sierra Nevada

120

53.8

Alto Tajo

119

53.4

Table 6. Results of the square selection (S) using the richness criteria, performed with the WORLDMAP program for the butterfly species that are not present within the network of protected areas in the Iberian Peninsula and Balearic Islands. The selected localities and the name of the species added in the selection are shown. Tabla 6. Resultados de la selección de cuadrículas (S) realizada con criterio de riqueza, con el programa WORLDMAP para las especies de mariposas que se encuentran fuera de la red de espacios protegidos en la Península Ibérica e Islas Baleares. Se muestran las localidades seleccionadas y el nombre de las especies que se añaden en la selección.

UTM square

Locality

Species registered

30SWG24

Baza (Granada)

Euchloe charlonia

31SDD67

Cas Catalá (Mallorca)

Gegenes pumilio

30TWK73

Cuenca

Pyrgus cinarae

30TXM48

Sadaba (Zaragoza)

Satyrium pruni

31TDG49

Setcases (Gerona)

Boloria napaea

Animal Biodiversity and Conservation 30.1 (2007)

Endemic species, area selection and Gap Analysis Table 7. Protected areas with the highest number of threatened butterfly species (T) in the Iberian Peninsula and Balearic Islands and the number of these species in each area. Tabla 7. Espacios naturales protegidos que presentan el mayor número de especies de mariposas amenazadas (T) en la Península Ibérica e Islas Baleares y el número de estas especies en cada área.

Protected area

Sierra Nevada

Posets–Maladeta

Picos de Europa

Alto Tajo

Sierra de María–Los Velez

Sierra de Baza

Sierra Espuna

Oodesa y Monte Perdido

Dehesa del Moncayo

Cadí–Moixeró

Aigüestortes i Estany de Sant Maurici

Threatened species, area selection and Gap Analysis The distribution of threatened species was compared with the network of protected areas (tables 4, 7). Only 46.8% of the records of threatened species and 34.5% of the squares hosting any of the threatened species fell within the protected network. Two squares (31TCH02 in the Pyrenees and 30SVG60 in Sierra Nevada) represented the top hotspots from the point of view of threatened species, with five of these species per square. Comparatively important numbers of threatened species were concentrated in parts of the Iberian System, Cantabrian Mountains and the Sierra del Moncayo. The minimum selection needed to cover the threatened species would be eight squares (fig. 2B, table 8), six of which are within the protected network. The remaining two are those selected by the presence of Pyrgus cinarae and Euchloe charlonia (i.e.: Cuenca in Central and Baza in Southern Spain). The complementarity selection based on rarity pointed out several alternative sites such as Los Monegros (NE Spain, instead of Sierra de Baza); Béjar (not protected, instead of the presently protected Navarredonda, both in Western Spain) based on the presence of Pyrgus sidae; and Cacém (Estremadura, Portugal, not protected) instead of Sierra Espuña (SE Spain protected), due to the occurrence of Melitaea aetherie (tables 4, 9).

Richness analysis showed three squares with seven Iberian endemic species each (30TYN04, 31TCH02, 30SVG60). The results showed a similar pattern with threatened species, although in this case the Central System was detected for its endemic species richness. Five squares together hosted the 16 Iberian endemic butterflies (fig. 3A, table 8). Three of these squares were within the network of protected areas. The complementarity selection based on rarity resulted in one additional square (Puerto del Escudo, Burgos, N Spain) chosen for the presence of Polyommatus fulgens (table 4). The main differences encountered using this selection were the square for Sierra del Moncayo (Zaragoza) instead of Navacerrada (Central Spain, both squares outside the network of protected areas) as a result of the presence of Lycaena bleusei; and the selection of Candanchú (Pyrenees, not protected) instead of Benasque (Pyrenees, protected) due to the occurrence of several species of the genus Erebia (table 9). Rare species, area selection and Gap Analysis The highest number of rare species (11 species) was concentrated in the square 31TCH02 (Pyrenees). The areas with higher number of these species were Sierra Nevada and Cádiz in Southern Spain, the Cantabrian Range and the Iberian System. An area selection resulted in 13 squares which altogether hosted all the rare species (fig. 3B, table 8). Seven of these squares were within the network of protected areas. Complementarity selection based on rarity analysis resulted in one square less in the Pyrenees than that based on richness (table 4); one square in Los Monegros replaced that in Sierra de Baza as a consequence of the presence of Euchloe charlonia (table 9). Summary of analyses The results show that 16 squares are important for the conservation of diurnal butterflies and are not represented in the existing network of protected areas (fig. 4). Nine further squares may be worth considering because of the relevance of the species recorded therein (table 9). Discussion Species richness and protected areas in the Iberian Peninsula and Balearic Islands The 223 butterfly species considered showed differences in their conservation status, abundance and distribution in the study area. According to Rey Benayas & De la Montaña (2003), rarity can be defined as the inverse value of the number of squares in which a species is present (1 / n). There

Romo et al.

Table 8. Selection of high–priority squares (S) for the conservation of butterfly species in the Iberian Peninsula and Balearic Islands, using the complementarity criteria based on richness with the WORLDMAP program with the threatened, endemic and rare species (present in less than 37 UTM grid squares). Localities are shown according to the hierarchical selection order, the number of threatened, endemic and rare species registered in that grid (SR), the number of new species added in the selection (SA) and their presence (yes) or absence (no) in the network of protected areas (PA). Tabla 8. Selección de cuadrículas prioritarias (S) para la conservación de mariposas en la Península Ibérica e Islas Baleares, utilizando el criterio de complementariedad basado en la riqueza con el programa WORLDMAP con las especies amenazadas, endémicas y raras (presentes en menos de 37 cuadrículas UTM). Se muestran: las localidades según el orden de selección, el número de especies amenazadas, endémicas o raras citadas en esa cuadrícula (SR), así como el número de especies nuevas que se añaden en la selección (SA) y su presencia (yes) o ausencia (no) en la red de espacios naturales protegidos (PA).

Threatened

Endemic

Rare

UTM square

Locality

30SVG60

Veleta (Granada)

31TCH02

Benasque (Huesca)

Yes

30SXG29

Sierra Espuña (Murcia)

Yes

30TWK73

Cuenca

30TUN57

Fuente De (Cantabria)

Yes

30TVN95

Puerto de Orduña (Burgos)

Yes

30SWG24

Baza (Granada)

30TUK26

Navarredonda (Ávila)

Yes

30SVG60

Veleta (Granada)

Yes

31TCH02

Benasque (Huesca)

Yes

30TXK64

Sierra de Javalambre (Teruel)

30TUN47

Puerto de Pandetrave (León)

Yes

30TVL10

Navacerrada (Madrid)

31TCH02

Benasque (Huesca)

Yes

31TCH23

Salardú (Lérida)

30STF70

Algeciras (Cádiz)

Yes

30SVG90

Puerto de la Ragua (Granada)

Yes

31TDG39

Nuria (Gerona)

30TUN57

Fuente De (Cantabria)

Yes

30TWK84

Valdecabras (Cuenca)

30TUN96

Puerto de Palombrera (Cantabria) 2

Yes

31TCH14

Les (Lérida)

30TUN48

Cordiñanes (León)

Yes

30SWG24

Baza (Granada)

31SDD67

Cas Catalá (Mallorca)

30TUK26

Navarredonda (Ávila)

Yes

is, however, no generalized criterion in the classification of Spanish species through the use of their geographic ranges. The percentage of squares that can be designed as relevant for having at least some part of their

Yes

surface as a protected area is relatively low (20%). However, this figure is larger than the 15% considered in the European Union as a guideline for nature conservation (79/409/ECC Bird Directive and 92/43/ ECC Habitat Directive) (European Commission, 1996;

Animal Biodiversity and Conservation 30.1 (2007)

Table 9. Selection of important squares for butterfly conservation, taken from the analyses of all area selections based on richness with the WORLDMAP program. These squares are not present within the current network of protected areas. The asterisk (*) indicates squares that are alternative to previous proposals, as a result of the area selection based on rarity (Near Minimum Area Set) performed with the WORLDMAP program. Localities are shown together with the species responsible for the selection of the squares: VU. Vulnerable; NT. Near threatened; R. Rare; E. Endemic; LC. Least concern. Tabla 9. Selección de cuadrículas importantes para la conservación de las mariposas obtenidas a partir de los resultados de todos los análisis de selecciones de áreas basados en riqueza realizados con el programa WORLDMAP y que no se encuentran dentro de la red de espacios protegidos existente. Con un asterisco (*) se marcan las cuadrículas obtenidas con el programa WORLDMAP basado en rareza (Near Minimum Area Set), consideradas como cuadrículas alternativas a las propuestas. Se muestran las localidades y las especies por las que esas cuadrículas son elegidas en la selección de áreas: VU. Vulnerable; NT. Casi amenazada; R. Rara; E. Endémica; LC. Preocupación menor. UTM square

Locality

Species

30SWG24 31TBF59

Hoya de Baza (Granada) Los Monegros (Huesca)

Euchloe charlonia (NT, R)

30TWK73 30TWK96

Cuenca Serranía de Cuenca

30TXM48 31TCH14

Sadaba (Zaragoza) Les (Lérida

Satyrium pruni (R)

31TDG49 31TDG39

Setcases (Gerona) Nuria (Gerona)

Boloria napaea (R)

31SDD67 31SDD68 31SDD79*

Cas Catalá (Mallorca) Son Espanyolet (Mallorca) Bunyola (Mallorca)

Gegenes pumilio (R)

Pyrgus cinarae (VU, R) Erebia epistygne (LC) Chazara prieuri (VU)

29TNF25

Porto (Douro Litoral)

Pseudophilotes panoptes (E)

29SNB70

Faro (Algarve)

Melitaea aetherie (NT) Carchadorus tripolinus (R)

29SMC89*

Cacém (Estremadura)

Melitaea aetherie (NT)

31TCH13

Viella (Lérida)

139 species

30TTK66

La Garganta (Cáceres)

Pyrgus sidae (VU, R) Lycaena bleusei (E)

30TTK67*

Béjar (Salamanca)

Pyrgus sidae (VU, R)

30TXM03*

Sierra del Moncayo (Zaragoza)

Lycaena bleusei (E)

30TXK64

Sierra de Javalambre (Teruel)

Erebia zapateri (E, R) Plebejus hespericus (VU, E) Polyommatus fabressei (E) Polyommatus nivescens (E) Pseudophilotes panoptes (E)

30TVL10

Navacerrada (Madrid)

Aricia morronensis (E) Lycaena bleusei (E) Polyommatus nivescens (E) Pseudophilotes panoptes (E)

30TUP41*

Nueva (Asturias)

Maculinea alcon

30TVN36*

Puerto del Escudo (Burgos)

Polyommatus fulgens (E, R)

30TWN14*

Nanclares de la Oca (Álava)

Callophrys avis

30TYN04*

Candanchú (Huesca)

Erebia gorgone (E) Erebia lefebvrei (E) Erebia sthennyo (E, R)

31TCH81*

Encamp Cortals (Andorra)

Aricia nicias (R) Boloria eunomia (R)

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4 2

5 3

1 2

7 12

11 4 3

Fig. 3. Selection of high–priority squares for the conservation of butterfly species in the Iberian Peninsula and Balearic Islands, using the complementarity criteria based on richness with the WORLDMAP program. The numbers show the hierarchical position of the areas. The network of protected areas is shown in grey. The stars indicate the coincidence between the priority areas selected by the program and the network of protected areas. The circles show the gaps where this selection does not match the network: A. The five UTM grid squares selected jointly host the total number of endemic species in the study area; B. The 13 UTM grid squares selected together contain all the rare species (present in less than 37 100 km2 UTM grid squares) in the study area. Fig. 3. Selección de cuadrículas prioritarias para la conservación de mariposas en la Península Ibérica e Islas Baleares, utilizando el criterio de complementariedad basado en la riqueza con el programa WORLDMAP. Las selecciones se presentan de forma jerárquica indicada por la numeración. En gris se representa la red de espacios protegidos. Las estrellas indican la coincidencia de las cuadrículas seleccionadas por el programa con la red de espacios naturales protegidos. Los círculos indican los huecos donde no coincide la selección con la red de espacios: A. Se presentan las cinco cuadrículas UTM que, en conjunto, albergan a la totalidad de especies endémicas en el área de estudio; B. Se presentan las 13 cuadrículas UTM que albergan, en conjunto, la totalidad de especies raras (presentes en menos de 37 cuadrículas UTM de 100 km2) en el área de estudio.

Animal Biodiversity and Conservation 30.1 (2007)

Fig. 4. Selection of the important UTM grid squares for butterfly conservation in the Iberian Peninsula and Balearic Islands obtained in the different analyses in this paper. The network of protected areas is represented in grey. The selected squares are shown in black. Fig. 4. Selección de cuadrículas UTM importantes para la conservación de las especies de mariposas diurnas a la luz de los resultados obtenidos en los diferentes análisis. En gris se representa la red de espacios protegidos. Los cuadrados negros indican las cuadrículas seleccionadas.

Rey Benayas & De la Montaña, 2003). The use of 10 km grid squares can nevertheless bias this percentage, giving a higher value than the real percentage of protected areas (8.5%). It has also been suggested that it is not appropriate to favour a universal basis for the proportion of conserved land, because this percentage should depend on the faunistic composition of the considered territory (Rodrigues & Gaston, 2001). Species richness is higher in the Central Pyrenees, the Cantabrian Mountains, the Central System, Sierra Nevada, Sierras Béticas and the Serra de Gerês. These results are highly consistent with previous studies carried out with butterflies (García–Barros et al., 2000) and with other plant or animal groups (Castro et al., 1996; Lobo & Araújo, 2003; Rey Benayas & De la Montaña, 2003; Rey Benayas et al., 2006). The Pyrenees are a typical area for lepidopterological studies due to the ample knowledge of their important species richness (García–Barros & Munguira, 1999). Sierra Nevada is also a relevant site for its diversity and the number of threatened and endemic species it hosts (Carrión & Munguira, 2002; Munguira et al., 2003). The altitudinal gradient has a major influence on butterfly diversity in a given area (Martín & Gurrea, 1990), and our results clearly show higher diversities in mountains. The

fact that most protected areas in the Iberian Peninsula have been declared in mountain ranges produces a coincidence between hotspots for butterflies and nature reserves that is favourable for conservation purposes. This is the case in regions like Andalusia, the Oriental Pyrenees, Cantabrian Mountains, part of the Central System and the mountains in Northern and Central Portugal. The richness of threatened, endemic and rare species regularly follows similar patterns: the Pyrenees and Sierra Nevada show the highest values and are followed by the Cantabrian Mountains and the Southern part of the Iberian System. For the endemic species the Central System is also important. This geographic pattern is very similar to that previously obtained with endemic vascular plants (Castro et al., 1996) and with endemic butterflies using 100 km grid squares (Martín et al., 2000). As far as butterflies are concerned, it was already known that the number of endemic species is correlated with the total number of species (García–Barros et al., 2000). Selection of priority areas Gap Analysis is an efficient tool that can be used as a first step in the selection of priority areas for conservation purposes (Scott et al., 1993). The

areas selected by this procedure need to be analysed carefully in order to obtain detailed knowledge of the fauna they can preserve and its conservation needs. Using the presence of a species in at least one 10 km square as a basis for the Iberian Peninsula and Balearic Islands, the minimum number of squares to cover all the species would be 16. This figure is rather low and in other animal groups the necessary area is larger with 13 (50 km) squares necessary to protect the 252 Spanish bird species (Carrascal & Lobo, 2003), five 50 km squares for amphibians, and nine for all the reptiles (Lobo & Araújo, 2003; note the scale difference). In Portugal, 27 squares (10 km) are necessary to cover a population of all the amphibians and reptiles and lower plants (Araújo, 1999). The selected squares are scattered right throughout the Iberian Peninsula and Mallorca but at the same time they are concentrated in areas with diversity hotspots or areas with larger numbers of endemic species. The selection thus covers areas such as the Pyrenees, the Cantabrian Mountains and the Iberian System, as well as areas in Portugal, the South of Andalusia and Balearic Islands. Three squares in the selection are not protected in the network of protected areas or in the Natura 2000 Network (SCIs and SPAs) and have species of interest such as Melitaea aetherie (NT, see table 1), Pseudophilotes panoptes (endemic species) and Gegenes pumilio (rare following the criteria used in this analysis). Some squares have been selected in the different analyses because they host species whose records need to be confirmed, such as Azanus jesous that has not been recorded again since its discovery and can be considered a casual immigrant. The square selected for this species is also interesting, however, for hosting other butterflies, and in fact adds eight new species in the selection process. The species Gegenes pumilio has not been found in the Balearic Islands (its distribution area) since its last record in 1978. Species not covered by protected areas and fauna in these areas The species that are excluded from the protected area network are different to those pointed out by Carrión & Munguira (2002). Euchloe charlonia, Satyrium pruni, and Pyrgus cinarae were detected in both studies as excluded from the network, and Gegenes pumilio and Boloria napaea are only excluded in our analysis. The reasons for this are that the present study considers a larger amount of protected areas than that of Carrión & Munguira (2002) and also the database from which data come is more detailed. Besides, the threatened species considered for both analyses differ slightly because the Red Data Book of the Spanish Invertebrates (Libro Rojo de los Invertebrados de España, Verdú & Galante, 2006) had not been published when the first study was performed and

Romo et al.

the status of these species has now been better assessed. The protected parks that show the largest number of species are concentrated in the Pyrenees and the Cantabrian Mountains. This confirms the altitudinal effect in butterfly richness described by Martín & Gurrea (1990). The protected areas with the largest number of species in our study are consistent with those in the literature (Carrión & Munguira, 2001, 2002), stressing the importance of some traditional and relevant areas for the conservation of butterflies in the study region. Area selection with threatened, endemic and rare species The areas selected for hosting all the threatened, endemic or rare species show a very similar pattern, with squares scattered all throughout the Peninsula with the exception of Portugal. Sierra Nevada is the first selected area for both threatened and endemic butterfly species as it is for vascular plants (Castro et al., 1996). On the other hand, the first square selected for rare species is in the Pyrenees. The second selected area for all these species is also in the Pyrenees. The area selection for threatened species has an overall similarity with that in the proposal of Prime Butterfly Areas (PBAs) with the exception of Portugal, where the number of PBAs was five (Van Swaay & Warren, 2006), while our analysis did not select priority areas for threatened species in Portugal. Threatened species are concentrated in mountain areas, a pattern different that contrasts with other groups such as amphibians (concentrated in the Northern coast and Balearic Islands) and reptiles (South and East of the Peninsula) (Rey Benayas & De la Montaña, 2003; Razola et al., 2006). Threatened birds and mammals are, on the other hand, mainly found in the centre of the Peninsula and are not abundant in mountain areas as butterflies are (Rey Benayas & De la Montaña, 2003). It is well known that mountain areas are important for endemic butterfly species (Balleto, 1995; Martín et al., 2000; García–Barros, 2003). Our results show similar patterns to those made with 50 km UTM squares (García–Barros et al., 2000), although there were some differences with some areas in the Pyrenees that were not relevant for their endemicity in other studies (Martín et al., 2000). It is also interesting to note that the butterfly pattern is similar to that of endemic collembolan, with the exception of Sierra Nevada (Martín et al., 2000). Rare species of butterflies follow a similar pattern to other animal groups (amphibians, reptiles, birds and mammals), with a high priority for the Pyrenees and Cantabrian Mountains (Rey Benayas & De la Montaña, 2003). The areas selected in this analysis that are not otherwise protected should be considered in further conservation plans due to their important rare species accumulation (table 8).

Animal Biodiversity and Conservation 30.1 (2007)

A problem that should not be overlooked is the difference between the size of the squares in which the data were taken compared with the size of the squares from the network of protected areas that is usually in the range of one or more orders of magnitude (Hopkinson et al., 2000). Another drawback is the fact that we only have butterfly data from 4,114 (10 km) of the total of 6,395 squares for the Iberian Peninsula and only between 6.8% and 9.8% have been properly sampled (Romo & García– Barros, 2005). This could affect the conclusions of this study, but it is also true that most areas that are rich in butterfly species are well studied and sampled. Squares selected in different analyses Because the networks of protected areas designed using criteria for other animal groups might not be efficient in protecting insect species (Araújo, 1999; Rodrigues & Gaston, 2001), it is important to take into account the information gathered from the latter. Nevertheless, the protected areas in the Iberian Peninsula provide coverage for the majority of butterfly species. The figures are more favourable than for other taxa such as plant species, in which a gap analysis needed 97 new 10 km squares to achieve a total coverage of the species in the Iberian Peninsula (Castro et al., 1996). In all the analyses performed for the conservation of the near threatened (NT) and rare (R) species E. charlonia, two squares are highlighted: Hoya de Baza (Granada, 30SWG24, table 9) and Los Monegros (Huesca, 31TBF59). The former results in four different selections (the area selection with species not covered by protected areas, with threatened and rare species and with the complementarity analysis based on rarity); this square was previously suggested for the conservation of E. charlonia by Carrión & Munguira (2002). Area selections based on species richness (taking into account all the butterfly species) and those based on rarity with rare and threatened species highlight an area in Los Monegros for the same species. The conservation of both areas would be necessary for this threatened species because its distribution range within Europe is restricted to Spain. Regarding the squares from Cas Catalá (31SDD67) and Son Espanyolet (31SDD68) in Mallorca, selected for G. pumilio, it would be necessary to review the distribution and species’ status because the records are rather old and from isolated populations. Finally, Viella (31TCH13) in the Pyrenees is one of the locations with highest species richness in the study area (139). It is not within any protected area and is selected in the third position in the area selection process. Species richness has been used as a criterion for the selection of conservation areas, although not all authors consider it is the most efficient method (Viejo et al., 1989; Williams et al., 1996; Araújo, 1999; Balmford & Gaston, 1999; Reyers et al., 2000; Méndez, 2003; Rey Benayas & De la

Montaña, 2003). Threatened and endemic species are also important targets in conservation proposals, but they do not always warrant the representation of the total number of species (Bonn et al., 2002). Our results show that the richest areas are also those with most endemic and threatened species, a conclusion verified in previous studies (Williams et al., 1996; Cofré & Marquet, 1999; Bonn et al., 2002). Therefore, a selection based on species richness and a complementarity criterion can be considered a reasonable preliminary approach. It is also true that this preliminary analysis could be improved with other more complex techniques such as linear programming, which allows the assignation of a specific conservation value for each species. This would result in an optimization of the design of a protected area network (Carrascal & Lobo, 2003; Rodrigues & Gaston, 2002b) through the elaboration of more realistic selections among all the used methods. Although some authors have shown with other taxa that complementarity selections based on rarity (NMS) are more effective (Csuti et al., 1997), in the case of butterflies the selections based on richness provide an interesting alternative in the set of squares that host the total fauna under consideration. Selection based on rarity showed a tendency to aggregate the squares in particular areas, while the richness selection produced a more scattered pattern. Thus the richness option seems to be more adequate when considering the minimization of extinction risk, because it spreads the localities in wider areas and therefore makes them less vulnerable to any given impacts. However, in some cases the rarity selection is useful, because it detects squares outside the protected areas, while richness selection chooses a protected square for the same species. In these cases we have proposed both options as the best conservation strategy (see table 9). Random selections have in all cases produced a lower percentage of total considered species than the complementarity area selections or the already existing network of protected areas. The latter options are thus more suitable than random selections for conservation strategies. Rarity and richness hotspots also showed low percentage of species and tended to aggregate the selected squares in the Pyrenees and Sierra Nevada and in the Iberian System or Central System in some analyses. They are not thus a good strategy for conservation because concentrating all efforts in the same area is not the best alternative if there are other possible choices. With the analysis of the information available we can say that the conservation status of Iberian and Balearic butterflies is relatively good, particularly when compared with the countries in our geographical vicinity. Comparisons with the number of species now extinct in other European countries (Konvicka et al., 2006) and the number of threatened species per country (Van Swaay & Warren, 1999) seem to support this statement. In our study,

a high percentage of the butterfly species is within the network of protected areas, and a few UTM squares hosts all the butterfly species, but full protection of these insects in the Iberian Peninsula and Balearic Islands is not guaranteed. Our study highlights the necessity to add new areas to the currently existing network and suggests a first approach in complementing this network. Acknowledgements We would like to thank Paul Williams and Juan Carlos Moreno for providing a version of the WORLDMAP program adapted to the study area. The members of the Project ATLAMAR (REN2000– 0466 GLO), José Martín Cano, Patrícia Garcia– Pereira and Ernestino Maravalhas, helped us to compile the data that were the origin of the database on which this study was based. We are also grateful to the biology students from the Universidad Autónoma de Madrid, Juan López Pajarón, Ana Isabel Moraga Quintanilla and Belén García Pérez, who worked on degree projects related with butterfly conservation and whose analyses were useful in the development of parts of our study. Finally, we wish to express our gratitude to José María Rey Benayas and an anonymous referee who kindly read our manuscript and made suggestions which improved it considerably. References Ando, A., Camm, J., Polasky, S. & Solow, A., 1998. Species distributions, land values, and efficient conservation. Science, 279: 2126–2128. Araújo, M. B., 1999. Distribution patterns of biodiversity and the design of representative network in Portugal. Diversity and Distributions, 5: 151–163. Asher, J., Warren, M. S., Fox, R., Harding, P. T., Jeffcoate, G. & Jeffcoate, S., 2001. The Millennium Atlas of Butterflies in Britain and Ireland. Oxford Univ. Press, Oxford. AutoCAD, 2004. User’s Guide AutoCAD. Autodesk, Inc. Paris, Francia. Balleto, E., 1995. Endemism, areas of endemism, biodiversity and butterfly conservation in the Euro– Mediterranean area. Bollettino del Museo Regionale di Scienze Naturali–Torino, 13: 445–491. Balmford, A. & Gaston, K. J., 1999. Why biodiversity surveys are good value. Nature, 398: 204–205. Balmford, A., Moore, J. L., Brooks, T., Burgess, N., Hansen, L. A., Williams, P. & Rahbek, C., 2001. Conservation Conflicts Across Africa. Science, 291: 2616–2619. Bonn, A., Rodrigues, A. S. L. & Gaston, K. J., 2002. Threatened and endemic species: are they good indicators of patterns of biodiversity on a national scale? Ecology Letters, 5: 733–741. Burley, F. W., 1988. Monitoring biological diversity for setting priorities in conservation. In:

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Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

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Animal Biodiversity and Conservation 30.1 (2007)

Birds and fish as bioindicators of tourist disturbance in springs in semi–arid regions in Mexico: a basis for management J. Palacio–Núñez, J. R. Verdú, E. Galante, D. Jiménez–García & G. Olmos–Oropeza

Palacio–Núñez, J., Verdú, J. R., Galante, E., Jiménez–García, D. & Olmos–Oropeza, G., 2007. Birds and fish as bioindicators of tourist disturbance in springs in semi–arid regions in Mexico: a basis for management. Animal Biodiversity and Conservation, 30.1: 29–41. Abstract Birds and fish as bioindicators of tourist disturbance in springs in semi–arid regions in Mexico: a basis for management.— Tourist disturbance in semi–arid springs was analysed; birds and fish were selected as bioindicators. Media Luna spring is the biggest and most spatially complex system in the region, with the highest biodiversity levels and tourist use. Areas with the highest bird species richness and abundances showed highest structural heterogeneity and least direct human impact. No differences in species richness of fish were observed between sectors and the most abundant species were found in the sectors least perturbed by human activity. Factors that explained the bird distribution were the species´ tolerance to the effects of direct tourism (noise and direct presence of people) and habitat quality, mainly riparian vegetation. Aquatic vegetation condition was very important for fish. Six bird species and two fish species were relevant as indicators of the habitat quality related to human impact. Anthropic disturbance such as tree plantation favoured some bird species, whereas aquatic vegetation removal was favourable for some fish species, such as the endemic Cichlasoma bartoni, however, both types of disturbance were unfavourable for other species; riparian vegetation removal was negative for both groups. Controlled tourism promotes good conditions for C. bartoni establishment. Efficient conservation measures such as limiting touristic distribution are necessary for all species, especially for the fish community, in order to conserve biodiversity in general. Key words: Wetlands, Species distribution, Threatened species, Endemism, Habitat loss, Spatial heterogeneity, Bioindicators. Resumen Aves y peces como bioindicadores de las alteraciones debidas al turismo en manantiales de zonas semiáridas en México: bases para la gestión.— Para analizar las alteraciones por el turismo en manantiales de zonas semiáridas se utilizaron aves y peces como bioindicadores. Se seleccionó el manantial de la Media Luna por ser el más grande y complejo, y por incluir la más alta biodiversidad y el mayor impacto turístico en la zona. Los sectores con alta diversidad y abundancias de aves fueron los que tienen la mayor heterogeneidad estructural y menor impacto humano directo. Las mayores abundancias de peces se encontraron en los sectores menos perturbados sin diferencias para la riqueza de especies. Los factores que explicaron la distribución de las aves fueron la tolerancia de las especies a los efectos directos del turismo (ruido y presencia directa de gente) y la calidad del hábitat, principalmente la vegetación ribereña. La condición de la vegetación acuática fue muy importante para los peces. Seis especies de aves y dos de peces fueron relevantes como indicadores de la calidad del hábitat en función del impacto humano. Las alteraciones antrópicas tales como la plantación de árboles favoreció a algunas especies de aves mientras que la eliminación de la vegetación acuática fue favorable para algunos peces como el endémico Cichlasoma bartoni, pero estas alteraciones fueron negativas para otras especies; la eliminación de la vegetación ribereña tuvo efectos negativos para ambos grupos. El turismo controlado crea condiciones favorables para C. bartoni. Para la conservación de la biodiversidad en general, se requieren medidas eficientes de conservación tales como la restricción geográfica del turismo especialmente importante para la comunidad de peces. ISSN: 1578–665X

Palacio–Núñez et al.

Palabras clave: Humedales, Distribución de las especies, Especies amenazadas, Endemismos, Pérdida de hábitat, Heterogeneidad espacial, Bioindicadores. (Received: 6 IX 06; Conditional acceptance: 31 X 06; Final acceptance 7 II 07) Jorge Palacio–Núñez & Genaro Olmos–Oropeza, Colegio de Postgraduados en Ciencias Agrícolas, Campus San Luis Potosí, Iturbide 73, Salinas de Hidalgo, S. L. P., 78600, México.– José R. Verdú & Eduardo Galante, Inst. de Biodiversidad–CIBIO, Univ. de Alicante, 03080 Alicante, España (Spain).– Daniel Jiménez– García, Dept. de Ecología, Univ. de Alicante, 03080 Alicante, España (Spain). Corresponding author: J. Palacio–Núñez, Inst. de Biodiversidad–CIBIO, Univ. de Alicante, 03080 Alicante, España (Spain). E–mail: jpalacio@colpos.mx

Animal Biodiversity and Conservation 30.1 (2007)

Introduction Arid and semi–arid zones have limited water resources. The few existing springs are usually isolated, relict in nature, and in poor condition. They may contain endemic fish species with restricted distribution, sometimes limited to a single spring (Contreras–Balderas, 1969). Freshwater environments are especially susceptible to modifications such as overexploitation, pollution and aloctone species introduction, the main factors affecting biodiversity (Cooperrider & Noss, 1994; Curtis et al., 1998). The increasing transformation that such environments are subjected to has negative consequences for ictiofauna and riparian biodiversity in general (Mensing et al., 1998; Fu et al., 2003), as well as for local biodiversity (Angermeier & Schlosser, 1995). An important source of disturbance is tourism. Tourism is an important means of income in Mexico but it is causing increasing environmental degradation in many places due to the lack of planning and preventive measures. Ecotourism strategies related to natural resources, participation of local people and visitor education (e.g. Boo, 1992; Ross & Wall, 1999; Burger, 2000) must be established and adapted to the particular conditions such as the Media Luna system. Media Luna has been used increasingly by tourists since the 1950s (Michelet, 1996), leading to continuous disturbances and transcendental changes during the 1960s and 1970s with the introduction of exotic fish and trees species (Palacio–Núñez, 1997). The state of an area’s conservation can be well evaluated on the basis of bioindicators selected from previous data (Randall, 1992), but this is not usually possible for most protected ecosystems (Heino et al., 2005). Consequently, threatened or endemic species, or other sensitive species are frequently used as indicators (Rubinoff & Powell, 2004). Different indicators cannot lead to the same responses (Duelli & Obrist, 2003) and different combinations of biological and ecological groups have been used (Van Rensburg et al., 2000; Heino et al., 2005; Pineda et al., 2005). Birds (Pyrovetsi & Papastergiadou, 1992; Browder et al., 2002) and fish (Heino et al., 2005; Fu et al., 2003) are important groups as indicators as both have at least the following points in common: 1) individual species are associated with singular habitats, 2) most are short– lived species so any change in their composition may manifest shortly after a disturbance, and 3) some species groups can be used to develop habitat associations which are predictors of relative human disturbance levels, and both groups may be affected by some tourist activities (e.g. Tershy et al., 1997; Higginbottom et al., 2003; Newsome et al., 2004). Bioindicators most commonly used to estimate effects of habitat transformation on biodiversity are arthropods (Micó et al., 1998; Verdú et al., 2000; Bestelmeyer & Wiens, 2001) or vertebrates (e.g. Flather et al., 1997) such as birds (e.g. Fleishman et al., 2001), mammals (e.g. Lomolino et al., 1989) or fish (e.g. Heino et al., 2005). The location we chose

was the Media Luna spring because it is the biggest and the most representative spring in the Rioverde valley, with high tourist affluence and biodiversity (Miller, 1984; Palacio–Núñez, 1997). It includes several bird species and some endemic fish species, mainly the monospecific Cualac and Ataeniobius genus (Miller, 1984; Contreras–Balderas, 1969). Media Luna was declared a State Park in 2003 due to its biological importance and state of conservation (SEGAM, 2003), but more basic management and ecological research are required. This paper aims to determine the impact of tourism and management on springs in semi–arid areas, using birds and fish as bioindicators, and to propose suggestions for management strategies which should be followed in order to preserve biodiversity in such locations. Methods Study area The Media Luna system is located in the Rioverde Valley, San Luis Potosí, Mexico (between X UTM: 393723 & 395317 and Y UTM: 2417647 & 2418070 coordinates, zone 14 N), at an average altitude of 1,000 m a.s.l. It is a complex of spring–lakes (Media Luna and Los Anteojitos) and channels or rivers with permanent water, two seasonal lakes, and flooding zones with lateral infiltrations which maintain a wet environment at variable distances from the source. This effect contrasts with the aridity of the plain. Media Luna is the largest spring lake (with 15 springs) in the valley and consists of six spring craters that provide a constant flow of about 5,000 l s–1 crystalline thermal water (Miller, 1984; Labarthe et al., 1989) that flows through three main channels (fig. 1). These wetlands are an important refuge for many aquatic and riparian bird species (IIZD, 1994). A total of 13 sectors were established for the lake and channels, according to their vegetation and environmental variability, and they are subject to variable anthropic pressure (Palacio–Núñez, 1997). Riversides contain zones with dense and scarce allochthonous woodland and other zones with native vegetation dominated by Panicum bulbosum Kunth and Andropogon glomeratus (Walt) BSP grasses (table 1). Riparian vegetation has previously been classified in a range between 0 (bare ground) to 5 for excellent conditions. Aquatic vegetation has been classified between 0 to 3. This vegetation is highly dominated by Nymphaea sp. and has two structural forms: 1) big size plants with isolated bases and floating leaves, and 2) small size plants with high population density, creating a close dense layer at leaf level (Palacio–Núñez et al., 1999). Sampling design Increasing relevance is being given to the use of spatial scales as bioindicators and the effect of habitat structure on the dynamics of animal and vegeta-

Palacio–Núñez et al.

Woodland

12 13

1 2

4 Undisturbed grassland

Aquatic vegetation Plants with floating leaves Small size plants

Wet and semi–wet disturbed grassland

Bare ground 0

500 m

Fig. 1. Study area map with aquatic vegetation and adjacent grassland and woodland vegetation. Circled numbers indicate sectors and white lines indicate sector limits. Fig. 1. Mapa del área de estudio mostrando la vegetación acuática y la vegetación adyacente de pastizal y de arbolado. Los círculos con número indican los sectores y las líneas blancas indican los límites de los sectores.

tion populations, but bioindicators can only show some environmental peculiarities (Duelli & Obrist, 2003). As bird and fish species in Media Luna have different origins, habitat requirements and risks of extinction (table 2) they were used to seek the widest possible environmental representation. Bird sampling was carried out on monthly field visits between November 1996 and May 1997. Under seasonal variability and two conditions of tourist presence, a single transect was repeated 39 times across the entire 2,498 m distance covering all the Media Luna System sectors. Transect repetitions were made in an inflatable boat and we counted the total number of birds observed through binoculars in each transect. The two cited conditions were based on visitor presence: without people (WP, when there was nobody in the area), with n = 24 transects, and with people (P, when there were people present), with n = 15 transects. Fish sampling considered three factors: 1) the population of some fish species was very low so it was not appropriate to carry out captures; 2) fish were not distributed among different levels of the water column, but always near the bottom or the banks between Nymphaea sp. stems, or over the vegetation cover (fish do not go under leaves of small plants); and 3) the great clarity of the water and the few visual obstacles allowed species sighting and count, even in the case of juveniles (Palacio– Núñez, 1997). Faced with this situation and to avoid altering populations, we carried out the sampling in 54 subaquatic transects; these transects were repeated five times on seasonal visits in spring and

summer 1998, winter 1998–99, and summer and autumn 1999. We adapted the Finland transect of Järvinen & Väisänen (Tellería, 1986) for subaquatic use in free diving, determining each transect as 10 m long and 2 m fixed width (20 m2). We traced each transect with orange cord in a perpendicular position to the riparian line. We made three repetitions per riverside, per sector. Biodiversity analysis We constructed species–accumulation curves to assess the adequacy of our sampling. Species– accumulation curves relate sampling effort to the cumulative number of species to evaluate sampling effectiveness (e.g. Longino & Colwell, 1997; Gering et al., 2003). Species accumulation curves and richness estimators (Chao 2, Jack 1 and ACE) were calculated using EstimateS 7.0 (Colwell, 2000). The rarefaction technique corrects unbalanced sample sizes, the main problem in diversity comparisons (Gart et al., 1982). For different sample sizes for birds, we calculated species richness expected for each situation WP or P through rarefaction curves for 1,000 randomizations, using EcoSim 7.0 software (Gotelli & Entsminger, 2001). For fish, sampling size was identical (see above), so rarefaction was not used. Statistical analysis To evaluate population distribution of the bioindicator groups in the sectors, we used the

Animal Biodiversity and Conservation 30.1 (2007)

Kruskal–Wallis non–parametric test (KW) with the STATISTICA package (StatSoft, 2001), and multiple comparisons of average range pairs using the Dunn test (Gardiner, 1997). We analysed bird and fish abundance and richness; in both WP and P conditions for birds. Interrelationships among birds and fish in each sector (for both WP and P conditions) were analysed by a Factorial Correspondence Analysis (FCA), using the STATISTICA software. For each sampling site we used the relative abundance of each species. FCA is an ordination– multivariate technique which simultaneously arranges species and habitats. As there was no discontinuity between habitats, they were grouped in ecological series, thus reducing complex patterns into simple and interpretable forms (Braak, 1985; Moreno, 2000). Results Species richness Accumulation curves showed 20 bird species for both conditions WP and P. Eleven fish species were present in the 13 sectors of the Media Luna. There are two particular species of the Cichlasoma genus that could not be differentia t e d a n d w e r e thereforeanalysed together (C. labridens + Cichlasoma sp.). Our inventories showed 100% completeness for both bioindicator groups according to the Chao 2, Jack 1 and ACE estimators. Bird species richness was statistically different between both WP and P conditions (fig. 2). Species distribution among sectors Species richness and abundance of bird species distribution were statistically different among sectors. Differences in fish abundance were also significant but species richness was statistically indistinguishable among sectors (see table 3 for KW probabilities). The largest differences in the Dunn and KW test in bird species richness and abundance were between sectors 9 and 4 (highest figures), and sectors 13, 11 and 12 (the poorest; fig. 3). In these five sectors there is woodland presence but, in sectors 9 and 4 there is little human impact and riparian grassland. Sectors 13, 11 and 12 have no grassland and human impact is very high (see table 1, fig. 1). Species richness between sectors 8 and 3 (without woodland and low human impact) was statistically non–significant compared with the high richness sectors, whereas sectors 1 and 10 (with woodland and very high human impact) were similar to the poorest sectors. For fish abundance the greatest differences were observed between sector 4, with dense aquatic vegetation coverage and highest abundance values, and the poorest 12, 13 and 1 sectors (fig. 4) with scarce Nymphaea sp. coverage. Species distribution among sectors was con-

Table 1. Characteristics of the sectors (S) of Media Luna system for aquatic area (A, in ha), physical variables (W, woodlands), estimated human environmental impact (HI), state of riparian vegetation (RV) and terrestrial vegetation (TV) (qualification average). Sectors with low human impact show high riparian and aquatic vegetation quality. Tabla 1. Características de los sectores del sistema de la Media Luna para el área acuática (A, en ha), variables físicas (W, bosques), impacto ambiental antrópico estimado (HI) y estado de la vegetación ribereña (RV) y de la vegetación terrestre (TV) (calificación media). En general los sectores con bajo impacto humano mostraron los valores más altos en la calificación de ambos tipos de vegetación.

1.379

Yes

0.619

0.637

Very high

2.35

0.86

Very low

4.75

2.78

Very low

4.90

2.66

0.389

Yes

Very low

5.00

2.78

0.687

Yes

Very low

4.63

2.79

0.607

Very low

3.65

2.93

1.219

Very low

3.45

2.96

1.513

Low

2.90

2.78

0.606

Yes

Very low

5.00

2.35

0.251

Yes

High

3.65

2.10

0.216

Yes

Very high

0.40

0.20

0.271

Yes

Very high

2.18

0.45

0.235

Yes

Very high

2.17

0.43

firmed by species grouping in the FCA analysis. Bird species ordination showed three main groups for both WP and P conditions related to axis 1 (fig. 5). In the WP plot the first two axes accounted for 64.6% of the variance in the data (fig. 5A). According to the distribution of sectors and species, axis 1 could be explained as the level of disturbance originated by tourists. In this sense, the first species group was determined by low human impact (sectors 6, 7 and 8, see table 1) with the more intolerant species such as Bubulcus ibis and Anas diazi. The second species group (Ardea herodias and Casmerodius albus) corresponded to intolerant species and was related to the well– conserved sector 5, whereas the third group containd generalist species such as Phalacrocorax olivaceus and Podylimbus podiceps in the most disturbed sectors (1, 11, 12 and 13) and well conserved (2, 3, 4, 9 and 10) sectors. In the P plot, the first two axes

Palacio–Núñez et al.

Table 2. List of the 20 bird and 11 fish species and taxonomic family found in the Media Luna system. Abbreviations (Abbr) used in this study, origin information (O) and extinction risk (ER) according to the Mexican Red List NOM 059 (INE, 2002) and IUCN Red List (2004). Bird list based on Peterson & Chalif (1989), and fish list based on List for Mexican Fish of Espinosa Pérez et al. (1993). For birds habitat requirements (HR): SW. Superficial water; DP. Open water for dive with close rocks or trunks for perching; OW. Open water; P. Branches or rocks close to the water; FV. Floating vegetation; BT. Big trees near the water. For population status (PS): T. Threatened; E. Endangered; CR. Critically endangered; V. Vulnerable. 1These two species of fish are reported together Tabla 2. Lista de las 20 especies de aves y las 11 de peces habitantes del sistema de la Media Luna. Se señalan las abreviaturas (Abbr) utillizadas en este trabajo, información sobre el origen (O) de las especies así como su situación de riesgo de extinción (ER) de acuerdo con la NOM 059 (INE, 2002) y la lista roja de UICN (2004). El listado de aves está basado en Peterson & Chalif (1989) y el de peces está basado en la Lista de Peces Mexicanos de Espinoza Pérez et al. (1993). (Para otras abreviaturas ver arriba.)

Family Birds Ardeidae

Species

Casmerodius albus L Nycticorax nycticorax L Ardea herodias L Butorides striatus Rackett Bubulcus ibis L Egretta thula Medina E. caerula L E. tricolor Müller N. violacea L Ciconiidae Mycteria americana L Phalacrocoracidae Phalacrocorax olivaceus Humboldt Anhingidae Anhinga anhinga L. Anatidae Dendrocygna autumnalis L Anas diazi Ridgway Podicipedidae Podylimbus podiceps L Rallidae Fulica americana Gmelin Alcedinidae Ceryle alcyon L C. torquata L Jacanidae Jacana spinosa L Pandionidae Pandion haliaetus L Fish Characidae Astyanax mexicanus Filippi Cyprinidae Dionda dichroma Hubbs y Miller Cyprinodontidae Cualac tessellatus Miller Goodeidae Ataeniobius toweri Meek Cichlidae Cichlasoma bartoni Bean C. labridens Pellegrin Cichlasoma sp. C. cyanoguttatum Bird and Girard Oreochromis sp. Poecilidae Gambusia panuco Hubbs Poecilia mexicana Steindachner P. latipunctata Meek

Abbr

ER NOM IUCN

alb nyc her str ibi thu cae tri vio mam oli anh aut dia pod fam alc tor spi hal

Native Native Native Native Exotic Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native

SW SW SW SW SW SW SW SW SW SW DP DP OW OW OW OW B B FV BT

– – – – – – – – T T – – – – – – – – – –

– – – – – – – – – – – – – – – – – – – –

Af Dd Ct At Cb Cl1 Cl1 Cc Ta Gp Pm Pl

Native Endemic Endemic Endemic Endemic Endemic Endemic Introduced Exotic Introduced Introduced Introduced

None Unknown Unknown Unknown Unknown Unknown Unknown Unknown None Unknown Unknown Unknown

– T E E E T E – – – – E

– V E E V E – – – – – CR

Expected species richness

Animal Biodiversity and Conservation 30.1 (2007)

25 20 15 10 WP condition P condition 95% confidence Interval

5 0

5 10 Transect number

Fig. 2. Rarefaction curves for birds in the sectors of Media Luna in P (with people) and WP (without people) conditions. Comparisons were made for n = 15 transects and 1,601 individuals observed in WP condition, with 20 bird species in both conditions. There was no statistical difference; both conditions are in the confidence interval of 95% curves. Fig. 2. Curvas de rarefacción para las aves de la Media Luna en condiciones P (con gente) y WP (sin gente). Las comparaciones fueron hechas para n = 15 transectos y 1.601 individuos observados en condición sin gente, con 20 especies en ambas condiciones. No se encontró diferencia estadística; ambas condiciones se encuentran dentro de las curvas del intervalo de confianza al 95%.

accounted for 55.35% of variance (see fig. 5B). Sectors 5 and 6 were the least susceptible to people presence and some intolerant species such as Fulica americana and Pandion haliaetus from the first group (in WP condition), and Dendrocygna autumnalis from the third group were redistributed in the second group in condition P. The first two axis from FCA accounted for 66.7% of the variance in the fish data (fig. 6). The fish community showed three main groups. The first group was represented by Cichlasoma bartoni and Oreochromis sp. and was related to the most disturbed sectors (1, 11, 12 and 13). A second group corresponded to the most generalist species such as Astyanax mexicanus, Cichlasoma labridens and C. cyanoguttatum, and is related to sectors 2 and 10; these species did not show special requirements. Dionda dichroma was only observed in sector 10. The third group contained the best conserved sectors; Ataeniobius toweri only appeared related to sectors with well established sub–aquatic vegetation (sector 3, 4, 5, 6, 7, 8 and 9). Discussion Sector characteristics were reflected by species distribution and abundance of bioindicator groups. Vegetation and other structural habitat variables are important to determine bird abundance (Read

Table 3. Kruskal–Wallis results for specific richness and abundance distribution of birds and fish among sectors in the Media Luna. All results were significant except fish species richness: Bg. Bioindicator group; C. Condition; Dv. Dependent variable (Sr. Species richness; A. Abundance). Tabla 3. Resultados de las pruebas de Kruskal– Wallis para la distribución de la riqueza específica y la abundancia de aves y peces entre los sectores de la Media Luna. Con excepción de la riqueza específica de peces, todos los resultados fueron significativos: Bg. Grupo bioindicador; C. Condición; Dv. Variable dependiente (Sr. Riqueza específica; A. Abundancia).

d.f.

Birds

129.4

0.0001

Birds

119.6

0.0001

Birds

129.4

0.0001

Birds

113.9

0.0001

Fish

–

20.80

0.0534

Fish

–

23.39

0.0022

Palacio–Núñez et al.

Birds abundance

Birds species richness

WP birds condition 10

a a

ab ab

6 abc

4 2 0 70 60

P birds condition

abc

bcd

abc

bcde

cd cde

cde

d e

a a

50 40

abc

bc abc

10 0

cd abc

bcd

abc

bcde cd cd

6 7 Sectors

cd cd

d d

Fig. 3. Results of Dunn test for bird species in Media Luna sectors, in both WP and P conditions for: A. Species richness; B. Mean individual abundance. The letters over the bars indicates the statistical group for each condition; similar letters indicate statistical similarity between sectors. There were strong statistical differences between sectors 9, 4 and 8 in contrast with 10 to 13 for bird richness and abundance. Fig. 3. Resultados de la prueba de Dunn para las especies de aves en los sectores de la Media Luna en las condiciones sin gente (WP) y con gente (P) para: A. Riqueza de especies; B. Abundancia media de individuos. Las letras sobre las barras indican el grupo estadístico para cada condición; las letras similares indican similitud estadística entre los sectores. Existen fuertes diferencias significativas entre los sectores 9, 4 y 8 en contraste con los sectores del 10 al 13 tanto para la riqueza como para la abundancia de aves.

et al., 2000). Although birds can move openly into Media Luna sectors, some sectors do not have the appropriate conditions for all species observed. Our results showed statistical differences in the spatial distribution of birds among sectors, with lowest abundance and richness values when there was visitor presence (fig. 3). We suggest that this presence creates environmental stress that accounts for the different responses to tolerance among birds throughout the Media Luna system. FCA confirmed the observations that bird distribution changes between conditions of human presence. Some bird species benefit from anthropic modifications which tend to disguise some impact (Read et al., 2000). Species such as P. olivaceus,

A. anhinga, most Ardeidae species, all Alcedinidae species, P. haliaethus and M. americana benefit from riparian woodlands. C. albus, A. herodias and N. nycticorax benefit from trees but are affected by border changes and P. podiceps which do not benefit are affected by riparian grassland destruction. Bird groups or particular species which are affected by any kind of change are usually considered the indicator species for this particular change (Read et al., 2000; Paillison et al., 2002; Veraart et al., 2004). The best example of a close relation with habitat structure and high quality of aquatic vegetation was J. spinosa. This species lives on floating vegetation and is very territorial (Peterson & Chalif,

Animal Biodiversity and Conservation 30.1 (2007)

Fish mean abundance (20 m2)

abc abc

abc

abc abc

abc

bc bc

6 7 Sectors

Fig. 4. Results of Dunn test for fish species abundance in Media Luna sectors. The letters above the bars indicate the statistical group; similar letters indicate statistical similarity between sectors. There are significant differences in the abundance between sectors number 4 and 1, 12 and 13. Fig. 4. Resultados de la prueba de Dunn para la abundancia de peces en los sectores de la Media Luna. Las letras sobre las barras indican el grupo estadĂstico; las letras similares indican similitud estadĂstica entre los sectores. Existen diferencias significativas en la abundancia entre los sectores 4 y los sectores 1, 12 y 13.

1989). It appears to be tolerant as it attempts only small escape movements from human presence. This behaviour is related to avoiding encroaching on another territory; its vocalizations, however, indicate stress. We consider this species to be the best environmental quality bird indicator. The most intolerant species to direct human impact were A. diazi, B. ibis, F. americana, P. haliaetus and D. autumnalis. These five species were the best indicators of tourist disturbance caused by direct human presence in the Media Luna. For fish, species richness and spatial distribution show a complex relation with the geographic location, size of the river or creek and the habitat characteristics in these system parts (Heino et al., 2005). Media Luna sectors have enough habitat conditions for most fish species and there are no significant differences in species richness between sectors (fig. 4). These results were confirmed by few relations between most fish species and habitat particularities as shown in the FCA results (fig. 6). This ordination method emphasizes opposite habitat structure preferences between two endemic species: C. bartoni related to bare ground and A. toweri related only to dense subaquatic vegetation. We considered these species as fish indicators for tourist impact and habitat changes in Media Luna.

Conservation policies may underestimate the value of small fragments. Each small fragment of unique and isolated native habitat can be important not only to maintain, but also to generate endemic biodiversity, and it must be carefully evaluated (Rubinoff & Powell, 2004). We emphasize the importance of small wetlands in semiâ&#x20AC;&#x201C;arid regions with fish endemism and the need for good management planning in order to avoid a critical situation. The use of bioindicators helps us to analyse the impact of direct and indirect effects of tourism on biodiversity (e.g. Mancini et al., 2005). We observed altered conditions in Media Luna, such as abrupt riverside and areas > 1 m deep (non anthropized sectors have gentle slopes and gradual deep increases) which are now completely unusable for some riparian bird species, such as Ardeidae. Among fish groups, we observed that cichlids have parental care and their young are sure to be found anywhere, but the other young fish species need shallow waters (< 0.5 m) and dense vegetation coverage for survival. Only cichlids were observed breeding successfully in the most disturbed sectors; for C. bartoni and Oreochromis sp. these sectors were the best places.

Palacio–Núñez et al.

1.5

Axis 2 (20.06% of variance)

vio thu tri cae

ibi

0.0

nyc S10

dia S6 fam

her alb

hal

S11

aut

alc S5

S1 S3

tor

pod str

spi

–1.0

Bird species Sector –2.0

anh

oli mam

–2.0

S12 S13

–1.0 0.0 Axis 1 (44.54% of variance)

1.0

1.5 tor

Axis 2 (19.95% of variance)

dia S8

hal

S5 S6 her

0.0

man alc aut alb

spi nyc oli

S11 anh tri pod S10

S9 fam

S12

thu

S13 S3 str cae vio

–1.5

ibi S7

–3.0 –3.0

–2.0 –1.0 Axis 1 (35.40% of variance)

0.0

0.5

Fig. 5. FCA plot for birds in Media Luna system showing relationships between sectors and bird species for axis 1 and 2: A. For WP condition; B. For P condition. In the principal axis, species group according to direct anthropic tolerance. Some species change sector if the condition varies from WP to P, but most tolerant species do not move. Fig. 5. Resultados de FCA para las aves del sistema de la Media Luna mostrando la relación entre los sectores y las especies de aves para los ejes 1 y 2: A. Para la condición sin gente (WP); B. Para la condición con gente (P). Algunas especies cambian de sector si la condición varía de WP a P, sin embargo las especies más tolerantes no cambian.

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1.0

0.0

S11

S12

S13

S2 Cl

S4 S9

Axis 2 (23.59% of inertia)

Gp S5 S7 S6

S8 At

S10

–2.0

Endangered endemic fish species Other fish species Sector

–4.0

–1.0

–0.8

–0.4 0.0 Axis 1 (43.09% variance)

0.4

0.8

Fig. 6. FCA plot for fish in Media Luna system showing relationships between sectors and fish species for axis 1 and 2. Strong contrast is shown in axis 1 between two endangered endemic fish: Ataeniobius toweri (At) and Cichlasoma bartoni (Cb), the first lives in dense vegetation and the second prefers bare portions. Fig. 6. Resultados de FCA para los peces del sistema de la Media Luna mostrando la relación entre los sectores y las especies de peces para los ejes 1 y 2. Se observan fuertes contrastes entre dos especies amenazadas y endémicas: Ataeniobius toweri (At) y Cichlasoma bartoni (Cb), la primera habitante de zonas con vegetación densa y la segunda que mostró preferencia por sitios sin vegetación.

Both indicator groups are important elements in this ecosystem, but management and conservation actions should focus mainly on the fish group, considering the arrival of visitors and their implication in habitat structure and quality (e.g. Root, 1998; Currie, 2003). We observed that the best riparian grassland conservation, with and without trees, was related to the maximum bird diversity and abundance, and the best subaquatic quality and abundance was related to the best fish density. Grassland and aquatic vegetation constitute barriers as few visitors cross them. As long as these barriers remain this system can be maintained. These habitat structures are the basis of conservation of the entire system. Restriction of sector 10 is especially important for conservation of D. dichroma, and tourist use should be kept moderate in altered channels in view of the con-

servation implications with C. bartoni. Finally, subaquatic coverage is especially important for A. toweri. Media Luna spring shares species, environmental variables and problems with several other semiarid springs (Palacio–Núñez, 1997) and our present findings may provide helpful information for their management. Acknowledgements We thank J. Jesús Enríquez–Fernández who collaborated in the field research in all phases. This study was partially supported by grants (A–1870/04, A–1870/05) from the AECI (Agencia Española de Cooperación Internacional); Becas MAE No. 32342 and by a CONACyT pre–doctoral grant No. 187777.

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cal conservation implications of water level fluctuations in wetlands of international importance: Lake Kerkini, Macedonia, Greece. Environmental Conservation, 19: 235–243. Randall, T. R., 1992. Effect of the focal taxon on the selection of nature reserves. Ecological Applications, 2: 404–410. Read, J. L., Reid, N. & Venables, W. N., 2000. Which birds are useful bioindicators of mining and grazing impacts in arid South Australia? Environmental Management, 26: 215–232. Ross, S. & Wall, G., 1999. Ecotourism: towards congruence theory and practice. Tourism Management, 20: 123–132. Root, K. V., 1998. Evaluating the effects of habitat quality, connectivity, and catastrophes on a threatened species. Ecological Applications, 8(3): 854– 865. Rubinoff, D. & Powell, J. A., 2004. Conservation of fragmented small populations: endemic species persistence on California’s smallest channel island. Biodiversity and Conservation, 13: 2537– 2550. SEGAM, 2003. Declaratoria de Área Natural Protegida bajo la modalidad de Parque Estatal denominado “Manantial de la Media Luna”. Diario Oficial de San Luis Potosí. 7 de junio del 2003. http://www.segam.gob.mx/ StatSoft, Inc., 2001. STATISTICA (Data Analysis Software System) Version 6. Tulsa, Oklahoma. Tellería, J. L., 1986. Manual para el censo de los vertebrados terrestres. Ed. Raíces, Madrid. Tershy, B. R., Breese, D., & Croll D. A., 1997. Human perturbations and conservation strategies for San Pedro Mártir Island, Islas del Golfo de California Reserve, México. Environmental Conservation, 24(3): 261–270. Van Rensburg, B. J., McGeoch, M. A., Matthews, W., Chown, S. L. & Van Jaarsveld, A. S., 2000. Testing generalities in the shape of patch occupancy frequency distributions. Ecology, 81: 3163– 3177. Veraart, J. A., de Groot, R. S., Perelló, G., Riddiford, N. J. & Roijackers, R., 2004. Selection of (bio) indicators to assess effects of freshwater use in wetlands: a case study of Albufera de Mallorca, Spain. Regional Environmental Change, 4: 107–117. Verdú, J. R., Crespo, M. B. & Galante, E., 2000. Conservation strategy of a nature reserve in Mediterranean ecosystem: the effects of protection from grazing biodiversity. Biodiversity and Conservation, 9: 1707–1721.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

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Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 30.1 (2007)

Species diversity and morphometrics of tardigrades in a medium–sized city in the Neotropical Region: Santa Rosa (La Pampa, Argentina) J. R. Peluffo, A. M. Rocha & M. C. Moly de Peluffo

Peluffo, J. R., Rocha, A. M. & Moly de Peluffo, M. C., 2007. Species diversity and morphometrics of tardigrades from a medium–size city in the Neotropical Region: Santa Rosa (La Pampa, Argentina). Animal Biodiversity and Conservation, 30.1: 43–51. Abstract Species diversity and morphometrics of tardigrades in a medium–size city in the Neotropical Region: Santa Rosa (La Pampa, Argentina).— Tardigrade diversity was studied in a medium–sized city in the Neotropical Region: Santa Rosa (La Pampa, Argentina). Samples were collected between February 1999 and January 2000 from lichens and mosses growing on sidewalk trees of the urban and periurban area. Five species of tardigrades were found, i.e., Echiniscus rufoviridis du Bois–Reymond Marcus, 1944, Macrobiotus areolatus Murray, 1907, Ramazzottius oberhaeuseri (Doyère, 1840), Milnesium cf. tardigradum and a non–described species of Macrobiotus. Only one species, M. cf. tardigradum, was found in areas with high levels of vehicle traffic. Results are compared with those from cities in the Nearctic and Palearctic regions. Measurements and pt index values (percentage ratios between the length of the structure considered and the buccal tube length) are provided for M. areolatus, R. oberhaeuseri and M. cf. tardigradum. Amongst the characters considered, the pt index for the stylet support insertion shows the least intraspecific variation. This character is also independent from body length and buccal–tube length. Key words: Tardigrades, Neotropical fauna, Urban environment, Biotic homogenization, Morphometric analysis, Medium–size cities. Resumen Diversidad y morfometría de tardígrados de una ciudad mediana de la región Neotropical: Santa Rosa (La Pampa, Argentina).— Se estudió la diversidad de tardígrados en una ciudad mediana de la Región Neotropical: Santa Rosa (La Pampa, Argentina). Las muestras se recolectaron entre febrero de 1999 y enero de 2000 de líquenes y musgos que crecían sobre árboles de vereda de áreas urbanas y periurbanas. Se encontraron cinco especies de tardígrados: Echiniscus rufoviridis du Bois–Reymond Marcus, 1944, Macrobiotus areolatus Murray, 1907, Ramazzottius oberhaeuseri (Doyère, 1840), Milnesium cf. tardigradum y una especie no descrita de Macrobiotus. M. cf. tardigradum fue la única especie encontrada en áreas con alto tránsito vehicular. Los resultados se comparan con los de ciudades de las Regiones Neártica y Paleártica. Se brindan medidas y valores del índice pt (relación porcentual entre la longitud de la estructura considerada y la longitud del tubo bucal) para M. areolatus, R. oberhaeuseri y M. cf. tardigradum. Entre los caracteres considerados, el índice pt correspondiente a la inserción del soporte de los estiletes es el que muestra la menor variabilidad intraespecífica. Además, este carácter es independiente del largo total del cuerpo y del largo del tubo bucal. Palabras clave: Tardígrados, Fauna neotropical, Ambiente urbano, Homogenización biótica, Análisis morfométrico, Ciudades medianas. (Received: 2 XII 05; Conditional acceptance: 26 V 06; Final acceptance: 16 II 07) Julio R. Peluffo, Alejandra M. Rocha & María C. Moly de Peluffo, Fac. de Ciencias Exactas y Naturales, Univ. Nacional de La Pampa, Uruguay 151, 6300 Santa Rosa, La Pampa, Argentina. Corresponding author: J. R. Peluffo. E–mail: molpel@speedy.com.ar ISSN: 1578–665X

Introduction The phylum Tardigrada includes meiofaunal organisms that live in all environments. These include terrestrial environments where they can be found to colonise in the soil, in leaf litter and turf, and in lichen and moss communities growing on rocks, trees or other suitable substrates. These communities and their tardigrades have been well studied in non–urban environments (e.g. Nelson, 1975; Ito, 1995; Bertolani & Rebecchi, 1996; Jönsson, 2003; Michalczyk & Kaczmarek, 2003). Conversely, urban tardigrades are less known. The works of Séméria (1981, 1982) in France, Meininger et al. (1985) in the USA, Utsugi (1986) in Japan and Steiner (1994a, 1994b, 1994c) in Switzerland are among the few that have been published world–wide. In Argentina, the tardigrade fauna is known mainly from papers of the 1980’s (Claps & Rossi, 1981, 1984, 1988; Maucci, 1988; Rossi & Claps, 1980, 1989), but none of them deals with urban tardigrades. During the past few years some work has been carried out on city–dwelling tardigrades (Peluffo et al., 2002; Rocha et al., 2002; Moly de Peluffo et al., 2006). Increasingly rapid urbanization, with the peculiar conditions it imposes upon organisms living in urban areas, has become a major concern in conservation biology (Shochat et al., 2006). A consequence of this process is the global decrease in diversity and the increased biota similarity among cities. McKinney & Loockwood (1999) defined biotic homogenization as "the replacement of local biota with non–indigenous species". His concept was later extended by Olden & Rooney (2006) to describe "the broader, overarching ecological process by which formerly disparate biotas lose biological distinctiveness at any level of organization, including in their genetic, taxonomic and functional characteristics". The effects of urbanization differ according to the class of organism involved. Urban tardigrades elicit a number of questions on this issue, such as, a) what is the diversity of tardigrades in a city? b) is it different from that in the surrounding rural areas? c) can an internal gradient or intersite differences be detected within a city? d) do different cities host different faunas? e) if so, how different are these faunas? f) do populations of the same species living in different cities show morphometric variations? and g) are such differences due to phenotypic plasticity or genetic differences? Exact identification of the species considered is required to answer these questions. The taxonomic status of several taxa therefore needs to be clarified before any further work can be undertaken. Many wide–ranging species that are considered cosmopolitan, such as Milnesium tardigradum Doyère, 1840, may in fact be species complexes (Nelson, 2002). Besides, as many original descriptions are based on a small number of specimens,

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the range of intraspecific, ontogenetic, and sexual variation remains unknown (Kinchin, 1994). Such systematic problems increase when the South American tardigrade fauna is considered, as knowledge of this group is still very limited (Pilato et al., 2003). The aim of this paper was to provide data on tardigrade species found in a medium–sized city in central Argentina, i.e., Santa Rosa (La Pampa), and compare them to those found in other cities, providing data for a preliminary "biogeography of urban tardigrades". We also performed a morphometric analysis in an attempt to contribute elements towards a better characterization of the urban tardigrades inhabiting the Neotropical Region. Material and methods Between February 1999 and January 2000 samples were collected from mosses and lichens growing on different tree species in the city of Santa Rosa. Trees in public areas mainly include specimens of Robinia pseudoacacia and several species of Fraxinus. Also, and mainly in non–paved areas, there are specimens of the autochthonous Prosopis caldenia. Samples were treated following the usual methodology (e.g., Ramazzotti & Maucci, 1983). Specimens were mounted in Faure’s medium or polyvinyl–lactophenol. Tardigrades were measured with an eyepiece micrometer. Measurements were taken following Pilato (1981), Binda & Pilato (1990), Bertolani & Rebecchi (1993) and Kinchin (1996). Percentage ratios between the length of the structure considered and the buccal tube length (pt) were calculated according to Pilato (1981). Study area Santa Rosa (36° 39' S, 64° 17' W) is located in the central–eastern part of the province of La Pampa (fig. 1), at 177 m a.s.l. According to the bioclimatic classification of Argentina (IRAM 11.603, 1996), it corresponds to zone IIIa, defined as warm–temperate. Within this zone, it is placed in the southernmost sector, near the boundary with zone IVc (cold–temperate). The average maximum temperatures in summer are in the 30º range 30º and the average minimum temperatures in winter are around 0ºC. The daily thermal ranges are over 15ºC. Annual average rainfall is approximately 640 mm. The stable population is around 100,000. Santa Rosa is a regional commercial and administrative centre and has over 24 industrial enterprises spread over an area of 134 hectares. Its characteristics are those of an intermediate or medium–sized city: according to Llop Torné & Bellet Sanfeliu (1999), an intermediate city is defined by its population — 20,000 to 200,000— and the role it plays in the surrounding regions for which it serves as a reference centre.

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Results Tardigrades were found in 127 of the 157 samples studied. Active individuals and free laid eggs were found as well as exuvia with and without eggs. This allowed specific identification of tardigrades. They belonged to five species: Echiniscus rufoviridis du Bois–Reymond Marcus, 1944, Macrobiotus areolatus Murray, 1907, Ramazzottius oberhaeuseri (Doyère, 1840), Milnesium cf. tardigradum and Macrobiotus sp. The last species, which was present in 18% of the samples, is new to science and will be fully described in a forthcoming paper. The greatest specific richness per sample was 4 and was recorded in a bush placed in the central square. Class: Heterotardigrada Marcus, 1927 Order: Echiniscoidea Marcus, 1927 Family: Echiniscidae Thulin, 1928 Genus: Echiniscus Schultze, 1840 Echiniscus rufoviridis du Bois–Reymond Marcus, 1944 Observations: present in 32% of the samples. This is a Neotropical species based on specimens collected in Brazil in 1944 and recently rediscovered and mentioned for several localities in Argentina by Peluffo et al. (2002). Class: Eutardigrada Marcus, 1927 Order: Parachela Schuster, Nelson, Grigarick and Christenberry, 1980 Family: Macrobiotidae Thulin, 1928 Genus: Macrobiotus Schultze, 1834 Macrobiotus areolatus Murray, 1907 Observations: cosmopolitan species. In Santa Rosa it was found in a non–systematic sampling of a paved area with medium to heavy vehicle traffic. The eggs are typical for the species. Table 1 and figures 2A and 3A illustrate morphometric data and results of statistical analysis. The pt index with the smallest coefficient of variation corresponds to the insertion level of stylet supports on the buccal tube followed by the row length of placoids and the width of the buccal tube. On the other hand, the pt index values of the insertion level of the stylet support show the highest independence with respect to the body length (y = –0.0009x + 77.585; r2 = 0.0004) and with respect to the buccal tube length (y = – 0.0284x + 78.564; r2 = 0.0075). Family: Hypsibiidae Pilato, 1969 Genus: Ramazzottius Binda and Pilato, 1986 Ramazzottius oberhaeuseri (Doyère, 1840) Observations: cosmopolitan species, present in 18% of the samples. Egg morphology coincides perfectly with that described for this species. It was absent from samples collected in areas with

Santa Rosa 0

300 km

Fig. 1. Map of South America, Argentina and La Pampa indicating the location of Santa Rosa. Fig. 1. Mapa de América del Sur, Argentina y La Pampa indicando la ubicación de Santa Rosa.

heavy vehicle traffic. Table 2 and figures 2B and 3B illustrate morphometric data and results of statistical analysis. The pt index with the smallest coefficient of variation corresponds to the insertion level of stylet supports on the buccal tube. The values of pt index for this character show the greatest independence respect to body length (y = 0.0005 x + 56.184; r2 = 0.0002) and respect to buccal tube length (y = 0.0189 x + 55.768; r2 = 0.0014). Order: Apochela Schuster, Nelson, Grigarick and Christenberry, 1980 Family: Milnesiidae Ramazzotti, 1962 Genus: Milnesium Doyère, 1840 Milnesium cf. tardigradum Observations: Milnesium tardigradum Doyère, 1840 is a cosmopolitan species. Milnesium cf. tardigradum is present in 89% of the samples. In areas with heavy vehicle traffic it was the only species recorded. Table 3 and figures 2C and 3C illustrate morphometric data and results of statistical analysis. The pt index with the smallest coefficient of variation corresponds to the insertion level of stylet supports on the buccal tube followed by those corresponding to claw length of the fourth pair of legs. The values of pt index that show the greatest independence from the body length are those of the main branch length of the claws of the fourth pair of legs (y = 0.0047x + 55.298; r2 = 0.0083). They are

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Macrobiotus areolatus 80

60 40 20 200

250

300 350 Body length (µm)

ssi

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C 80

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70 60 50 40 30 250

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450 550 Body length (µm) ssi

sb4

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750

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Fig. 2. The pt index values plotted against body length. The tendency lines are shown: ssi. Insertion level of stylet supports on the buccal tube; btd. Diameter of the buccal tube; pl. Macroplacoid row length; sb4. Basal claws + secondary branch length of the fourth pair of legs; mb4. Main branch length of claws of the fourth pair of legs. Fig. 2. Valores del índice pt obtenidos en función de la longitud total del cuerpo. Se muestran las líneas de tendencia: ssi. Nivel de la inserción del soporte de los estiletes sobre el tubo bucal; btd. Diámetro del tubo bucal; pl. Longitud de la hilera de macroplacoides; sb4. Longitud de la uña basal + longitud de la rama secundaria del cuarto par de patas; mb4. Longitud de la rama principal de la uña del cuarto par de patas.

Animal Biodiversity and Conservation 30.1 (2007)

Macrobiotus areolatus 80

60 40 20 0

35 40 45 50 Buccal tube length (µm) ssi

btd

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24 26 28 30 32 µm) Buccal tube length (µ ssi

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65 55 45 35 25 22

30 34 38 42 Buccal tube length (µm) ssi

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Fig. 3. The pt index values plotted against buccal tube length. The tendency lines are shown. (For abbreviations see fig. 2.) Fig. 3. Valores del índice pt obtenidos en función de la longitud del tubo bucal. Se muestran las líneas de tendencia. (Para las abreviaturas, ver la fig. 2.)

Peluffo et al.

Table 1. Summary of morphometric data (in µm, except pt) for Macrobiotus areolatus: bl. Body length; btl. Buccal tube length; btd. Diameter of the buccal tube; ssi. Insertion level of stylet supports on the buccal tube; pl. Macroplacoid row length; 1° pl. First macroplacoid length; 2° pl. Second macroplacoid length; 3° pl. Third macroplacoid length; C. Character; Min. Minimum; Max. Maximum; SD. Standard deviation; CV. Coefficient of variation. Tabla 1. Resumen de datos morfométricos (en µm, excepto para pt) de Macrobiotus areolatus: bl. Longitud total del cuerpo; btl. Longitud del tubo bucal; btd. Diámetro del tubo bucal; ssi. Nivel de la inserción del soporte de los estiletes sobre el tubo bucal; pl. Longitud de la hilera de macroplacoides; 1° pl. Longitud del primer macroplacoide; 2° pl. Longitud del segundo macroplacoide; 3° pl. Longitud del tercer macroplacoide; C. Carácter; Min. Mínimo; Max. Máximo; SD. Desviación estándar; CV. Coeficiente de variación.

Mean

Min.

Max.

pt mean

pt min.

pt max.

pt SD

pt CV

329.24

207.40

439.20

64.27

btl

44.31

27.30

59.66

8.06

btd

6.55

3.03

9.61

1.54

14.44

11.11

16.33

1.31

9.07

ssi

34.23

21.74

46.52

6.26

77.31

72.50

83.22

2.64

3.41

22.49

12.14

31.35

4.97

50.88

44.44

55.47

3.14

6.71

1° pl

6.71

3.40

9.80

1.71

15.12

12.37

18.23

1.61

10.62

2° pl

5.18

2.02

8.43

1.57

11.57

7.41

15.09

1.73

14.95

3° pl

7.54

3.70

10.11

1.95

16.97

11.44

20.85

2.16

12.73

followed by the pt index values of the secondary branch length of the same claws (y = 0.0056x + 41.823; r2 = 0.0224) and the insertion level of the stylet supports (y = 0.0058x + 64.447; r2 = 0.1539). As to the buccal tube length, the pt index values that show the greatest independence are those of the secondary branch length of claw IV (y = –0.167x + 50.825; r2 = 0.0592), followed by the pt index values of the insertion level of the stylet supports (y = 0.0737x + 64.644; r2 = 0.0739).

Discussion Two of the species found in Santa Rosa —Milnesium cf. tardigradum and Ramazzottius oberhaeuseri— were also recorded by Moly de Peluffo et al. (2006) in General Pico; M. tardigradum and R. oberhaeuseri were recorded in Europe by Séméria (1981) in Nice and by Steiner (1994b) in Zurich. M. areolatus is a species that has not been recorded within the cities except in the Neotropical

Table 2. Summary of morphometric data (in µm, except pt) for Ramazzottius oberhaeuseri. (For abbreviations see table 1.) Tabla 2. Resumen de datos morfométricos (en µm, excepto para pt) de Ramazzottius oberhaeuseri. (Para las abreviaturas, ver tabla 1.)

Mean

Min.

Max.

pt mean

pt min.

pt max. pt SD

pt CV

252.74

128.22

356.30

54.89

btl

29.37

20.61

37.26

4.63

btd

1.61

1.27

2.38

0.28

5.50

3.81

7.50

0.89

16.2

ssi

16.55

11.65

20.61

2.83

56.14

51.72

60.71

2.29

4.1

6.33

4.76

7.93

0.63

21.72

16.67

30.00

3.22

14.8

39 36

Animal Biodiversity and Conservation 30.1 (2007)

Table 3. Summary of morphometric data (in µm, except pt) for Milnesium cf. tardigradum: mb4. Main branch length of claws of the fourth pair of legs; sb4. Basal claws + secondary branch length of the fourth pair of legs. (For other abbreviations see table 1.) Tabla 3. Resumen de datos morfométricos (en µm, excepto para pt) de Milnesium cf. tardigradum: mb4. Longitud de la rama principal de la uña del cuarto par de patas; sb4. Longitud de la uña basal + la rama secundaria del cuarto par de patas. (Para las otras abreviaturas, ver tabla 1.)

Mean

Min.

Max.

pt mean

pt min. pt max.

pt SD pt CV

508.11

288.9

770.37

139.61

btl

37.00

23.78

49.94

7.55

btd

13.72

7.13

25.37

4.24

36.99

23.68

59.26

7.96

21.5

ssi

24.62

15.90

31.90

5.48

67.37

63.11

70.53

2.05

3.0

mb4

21.17

13.48

31.71

4.23

57.72

46.43

74.07

7.24

12.5

sb4

16.43

11.1

22.20

3.48

44.65

34.67

57.89

5.18

11.6

Region. In Argentina, it was recorded in urban samples of General Pico (Moly de Peluffo et al., 2006) and in non–systematic surveys in other cities. As pointed out by Séméria (1982) for some species found in Nice, Echiniscus rufoviridis and Macrobiotus sp, even if not cosmopolitan show such tolerance to urban conditions that it allows them to appear in cities. Echiniscus rufoviridis has been recorded in several cities ranging from its original locality in Brazil to central Argentina (Peluffo et al. 2002). However, non–systematic surveys in other Neotropical cities have rendered negative results. In the city of Santa Rosa there are none of the species with high tolerance to urban pollution that have been mentioned for northern hemisphere cities, i.e., Macrobiotus hufelandi Schultze, 1833 (Séméria, 1981, 1982), Diphascon (Adropion) scoticum Murray, 1905 (Meininger et al., 1985) and Macrobiotus persimilis Binda & Pilato, 1972 (Steiner, 1994b). In Santa Rosa the species that shows the greatest tolerance to urban pollution due to vehicle transit is M. cf. tardigradum. This coincides with data from General Pico (Moly de Peluffo et al., 2006). The low diversity of tardigrades in Santa Rosa and the maximum specific richness for any one site are common to those of other cities studied (Moly de Peluffo et al., 2006). Santa Rosa and General Pico share their five species of tardigrades, while Nice and Zurich share four. One of them, i.e., R. oberhaeuseri, appears in all four cities. Upon observation of tardigrade distribution in Santa Rosa, the statement —for other animals— by Jokimäki & Kaisanlahti–Jokimäki (2003), applies, i.e., "Urbanization cannot be seen as a process that monotonically increases the similarity of bird communities". Thus, the maximum richness of four species of tardigrades occurs in the central area of the city, i.e., the central square of c. 1 ha. This suggests that the negative effect of intense vehicle traffic on

species richness observed in the epiphytic communities on sidewalk trees, decreases rapidly with increased distance from the street. It may be possible that the strong seasonal winds characteristic of this region have a dispersant effect on the potential atmospheric pollutants produced by vehicles. This and other particular cases seem to confirm the need to enrich the traditional gradient analysis with consideration of other factors, including socio–economic variables (Kinzig et al., 2005). Similarities among tardigrade taxocenoses in cities suggest that these animals are also undergoing a process of biotic homogenization linked to urbanization, although in a different measure according to the level of organization and spatial scale considered. It appears that homogenization reaches a taxonomic level at a regional scale. At a global scale there appears to be a functional homogenization that produces the following similarities: a) reduced specific richness, b) different tolerant species in cities of different biogeographic regions, and c) tolerant species common to different cities in a same biogeographic region. The last case requires study if these species show intercity population similarities regarding density, relative abundance and morphometric characteristics. In the three species recorded in Santa Rosa for which morphometric data was analyzed, M. areolatus, R. oberhaeuseri and M. cf. tardigradum, the pt index with the lowest variation coefficient was clearly that corresponding to the insertion level of stylet supports on the buccal tube (3–4.1%). This confirms the low variability mentioned for this character by Pilato (1981). The same was recorded by Bertolani & Rebecchi (1993) for species of the Macrobiotus hufelandi group. In his study in tardigrades from the Caucasus, Biserov (1997) did not provide the variation coefficient of pt indices. However, calculation of such coefficients based on

the data provided in his tables shows that the pt index of the insertion level of stylet supports on the buccal tube is also that which varies the least, except for one species of Ramazzottius. As recorded by Pilato (1981) for Isohypsibius elegans, in the three species analyzed in this study, the values of pt index for the insertion level of stylet supports on the buccal tube were independent from the body length and the length of buccal tube. Morphometric analysis of the data presented herein provides a foundation for a better characterization of the tardigrade species living in cities of the Neotropical Region and adds to our knowledge of the morphometric differences amongst their populations. Future studies should allow the degree of similarity among the urban tardigrade taxocenoses to be measured at different organization levels and different spatial scales. If morphometric differences were detected among populations of species common to different cities, molecular studies should be useful to elucidate whether the differences are due to phenotypic plasticity or genetic differences. Such investigation should also contribute towards the uncovering of distribution patterns of urban tardigrades and the underlying mechanisms that produce them, as well as towards the testing of any such hypotheses. Acknowledgements The authors wish to thank M. Claps (UNLP, Argentina), G. Rossi (CEPAVE, Argentina) and E. Quirán (UNLPam, Argentina) for their bibliographic help. They also thank. M. Griffin (UNLPam, Argentina) for his suggestions and help with the English version of the paper. This research was partially supported by Universidad Nacional de La Pampa, (Argentina). References Bertolani, R. & Rebecchi, L., 1993. A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica Scripta, 22(2): 127–152. – 1996. The tardigrades of Emilia (Italy). II. Monte Rondinaio. A multihabitat study on a high altitude valley of the northearn Apennines. Zoological Journal of the Linnean Society, 116: 3–12. Binda, M. G. & Pilato, G., 1990. Tardigradi di Terra del Fuoco e Magallanes. I. Milnesium brachyungue, nuova specie di tardigrado Milnesiidae. Animalia, 17: 105–110. Biserov, V., 1997. Tardigrades of the Caucasus with a taxonomic analysis of the genus Ramazzottius (Parachela: Hypsibiidae). Zoologischer Anzeiger, 236: 139–159. Claps, M. C. & Rossi, G. C., 1981. Contribución al conocimiento de los tardígrados de Argentina. II.

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Revista de la Sociedad Entomológica Argentina, 40: 107–114. – 1984. Contribución al conocimiento de los tardígrados de Argentina. IV. Acta Zoológica Lilloana, 38: 45–50. – 1988. Contribución al conocimiento de los tardígrados de Argentina. VI. Iheringia, 67: 3–11. IRAM 11.603., 1996. Acondicionamiento térmico de edificios. Clasificación bioambiental de la República Argentina. Instituto Argentino de Normalizaciones. Ito, M., 1995. Taxonomic study on the Eutardigrada from the Northern Slope of Mt. Fuji, Central Japan, II. Family Hypsibiidae. Proceedings of the Japanese Society of Systematic Zoology, 53: 18–39. Jokimäki, J. & Kaisanlahti–Jokimäki, M–L. 2003. Spatial similarity of urban bird communities: a multiscale approach. Journal of Biogeography, 30(8): 1183–1193. Jönsson, K., 2003. Population density and species composition of moss–living tardigrades in a boreo–memoral forest. Ecography, 26: 356–364. Kinchin, I., 1994. The Biology of Tardigrades. Portland Press, London. – 1996. Morphometric analysis of Ramazzottius varieornatus (Hypsibiidae: Eutardigrada). Zoological Journal of the Linnean Society, 116: 51–60 Kinzig, A. P., Warren, P., Martin, C., Hope, D. & Katti, M., 2005. The effects of human socio– economic status and cultural characteristics on urban patterns of biodiversity. Ecology and Society, 10(1): 23. [online] URL: http://www.ecologyandsociety.org/vol10/ iss1/art23/ Llop Torné, J. M. & Bellet Sanfeliu, C., 1999. Ciudades intermedias y urbanización mundial. Ajuntament de Lleida, UNESCO, UIA, Ministerio de Asuntos Exteriores. Maucci, W., 1988. Tardigrada from Patagonia (Southern South America) with description of the three new species. Revista Chilena de Entomología, 16: 5–13. McKinney, M. L. & Loockwood, J. L., 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution, 14(11): 450–453. Meininger, C. A., Vetz, G. W. & Snider, J. A., 1985. Variation in epiphytic microcommunities (tardigrade–lichen–bryophyte assemblages) of the Cincinnati, Ohio area. Urban Ecology, 9: 45–61. Michalczyk, L. & Kaczmarek, L., 2003. Water bears (Tardigrada) of the Bieszczady Mountains (Poland, West Carpathians). Zootaxa, 242: 1–24. Moly de Peluffo, M. C., Peluffo, J. R., Rocha A. M & Doma, I. L., 2006. Tardigrade distribution in a medium–sized city of central Argentina. Hydrobiologia, 558(1): 141–150. Nelson, D., 1975. Ecological distribution of tardigrades on Roan Mountain, Tennessee – North Carolina. Memorie dell’ Istituto Italiano di Idrobiologia, 32: 225–276. – 2002. Current status of the Tardigrada: Evolution and ecology. Integrative and Comparative Biol-

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ogy, 42: 652–659. Olden, J. D. & Rooney, T. P., 2006. On defining and quantifying biotic homogenization. Global Ecology and Biogeography, 15: 113–120. Peluffo, J. R., Moly de Peluffo M. C. & Rocha A. M., 2002. Rediscovery of Echiniscus rufoviridis du Bois–Raymond Marcus, 1944 (Heterotardigrada, Echiniscidae). New contributions to the knowledge of its morphology, bioecology and distribution. Gayana, 66: 97–101. Pilato, G., 1981. Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia, 8: 51–57. Pilato, G., Binda M. G. & Lisi, O., 2003. Remarks on some species of tardigrades fron South America with the description of Minibiotus sidereus n. sp. Zootaxa, 195: 1–8. Ramazzotti, G. & Maucci, W., 1983. Il Phylum Tardigrada. III. Edizione riveduta e aggiornata. Memorie dell’ Istituto Italiano di Idrobiologia, 41: 1–1012. Rocha, A. M., Izaguirre M. F., Moly de Peluffo, M. C., Peluffo J. R. & Casco V. H., 2002. Ultraestructura de la cutícula de Echiniscus rufoviridis du Bois–Raymond Marcus, 1944 (Tardigrada). In: VIII Jornadas Pampeanas de Ciencias Naturales: 195–197. Consejo Profesional de Ciencias Naturales de La Pampa (Argentina). Rossi, G. C. & Claps, M. C., 1980. Contribución al conocimiento de los tardígrados de Argentina. I. Revista de la Sociedad Entomológica Argentina, 39: 243–250.

– 1989. Contribución al conocimiento de los tardígrados de Argentina. V. Revista de la Sociedad Entomológica Argentina, 47: 133–142. Séméria, Y., 1981. Recherches sur la faune urbaine et sub–urbaine des tardigrades muscicoles et lichenicoles. 1. Nice–Ville. Bulletin Mensuel de la Société Linnéenne de Lyon, 50: 231–237. – 1982. Recherches sur la faune urbaine et sub– urbaine des tardigrades muscicoles et lichenicoles. 2. L’espace sub–urbain: les hauteurs orientales de Nice–Ville. Bulletin de la Société Linnéenne de Lyon, 51: 315–328. Shochat, E., Warren, P. S., Faeth, S. H., McIntyre, N. E. & Hope, D., 2006. From patterns to emerging processes in mechanistic urban ecology. Trends in Ecology and Evolution, 21(4): 186–191. Steiner, W. A., 1994a. The influence of air pollution on moss–dwelling animals: 1. Methodology and composition of flora and fauna. Revue de Zoologie, 101: 533–556. – 1994b. The influence of air pollution on moss– dwelling animals: 2. Aquatic fauna with emphasis on Nematoda and Tardigrada. Revue de Zoologie, 101: 699–724. – 1994c. The influence of air pollution on moss– dwelling animals: 4. Seasonal and long–term fluctuations of rotifer, nematode and tardigrade populations. Revue de Zoologie, 101: 1017–1031. Utsugi, K., 1986. Urban tardigrades in Kyushu. Zoological Science, 3: 1110.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 30.1 (2007)

Nuevas especies de los géneros Trichodesma LeConte, 1861 y Gastrallus Jacquelin du Val, 1860, del África Austral (Coleoptera, Anobiidae) A. Viñolas & G. Masó

Viñolas, A. & Masó, G., 2007. Nuevas especies de los géneros Trichodesma LeConte, 1861 y Gastrallus Jacquelin du Val, 1860, del África Austral (Coleoptera, Anobiidae). Animal Biodiversity and Conservation, 30.1: 53–70. Abstract New species of the genus Trichodesma LeConte, 1861 and Gastrallus Jacquelin du Val, 1860, from South Africa (Coleoptera, Anobiidae).— Continuing the review of the Anobiidae collection at the Transvaal Museum of Pretoria, we describe the following species of Anobiinae: Trichodesma endroedyyoungai n. sp., Gastrallus omedesae n. sp., G. jeremiasi n. sp., G. strydomi n. sp., G. pafuriensis n. sp., G. skukuzaensis n. sp., G. ndumuensis n. sp. and G. krugerensis n. sp. Most of these species were collected at the National Kruger Park, South Africa. As we found specimens of males of the Xyletininae, Xyletinastidius tessellatus (Español, 1971) and of the Dorcatominae, Stagetodes australis Español & Viñolas, 1995, these are described here as only females of genus Xyletinastidius (Español & Comas, 1991) and the two species were described previously. Key words: Coleoptera, Anobiidae, Anobiinae, Xyletininae, Dorcatominae, New species, South Africa. Resumen Nuevas especies del género Trichodesma LeConte, 1861 y Gastrallus Jacquelin du Val, 1860, del sur de África (Coleoptera, Anobiidae).— Continuando la revisión de la colección de Anobiidae del Transvaal Museum de Pretoria, se describen las siguientes especies de Anobiinae: Trichodesma endroedyyoungai sp. n., Gastrallus omedesae sp. n., G. jeremiasi sp. n., G. strydomi sp. n., G. pafuriensis sp. n., G. skukuzaensis sp. n., G. ndumuensisn. sp. n. y G. krugerensis sp. n. Especies procedentes, en su mayoría, del Parque Nacional Kruger, República de Sudáfrica. Así mismo, al localizar en la misma, machos del Xyletininae, Xyletinastidius tessellatus (Español, 1971) y del Dorcatominae, Stagetodes australis Español & Viñolas, 1995, nos permite realizar la descripción de los mismos, ya que el género Xyletinastidius Español & Comas, 1991 y ambas especies fueron descritas anteriormente sólo con hembras. Palabras clave: Coleoptera, Anobiidae, Anobiinae, Xyletininae, Dorcatominae, Nuevas especies, República de Sudáfrica. (Received: 16 XI 06; Conditional acceptance: 6 II 07; Final acceptance: 19 II 07) Amador Viñolas & Gloria Masó, Museu de Ciències Naturals de la Ciutadella (edifici de Zoologia), Passeig Picasso s/n., 08003 Barcelona, Espanya (Spain).

ISSN: 1578–665X

Viñolas & Masó

Introducción En 1989 Español inició la revisión de los Anobiidae, pendientes de estudio, de la colección del Transvaal Museum de Pretoria, con la descripción de un gran número de especies y géneros nuevos (Español, 1990, 1992a, 1992b, 1993; Español & Blas, 1992; Español & Comas, 1992; Español & Viñolas, 1995a, 1995b, 1995c; 1996). Hoy, gracias a la colaboración de la mencionada institución, podemos continuar con el estudio de los ejemplares que quedaron pendientes de revisar tras la lamentable defunción de los doctores F. Español y E. Younga. En este primer trabajo se estudia la subfamilia Anobiinae, en el género Trichodesma LeConte, 1861, con la descripción de la primera especie conocida, de éste género, en el África austral, claramente diferenciada del resto de sus congéneres africanos y en el género Gastrallus Jacquelin du Val, 1860, del que ya se habían descrito tres especies nuevas de Sudáfrica (Español & Comas, 1992), con la descripción de siete más, todas ellas muy bien caracterizadas, a parte de pequeños detalles de la morfología externa muy constante en el género, por las antenas, palpos maxilares y sobre todo por la conformación del edeago que las separa del resto de especies del género. Así mismo se amplia la distribución, hasta ahora conocida, de las tres primeras. Es de destacar que la mayor parte de las especies han sido capturadas, durante diferentes campañas, en el Parque Nacional Kruger y alrededores. Se comenta la nueva localización de Trichodesmina nana Español, 1982, en Ruanda, descrita y sólo conocida hasta el presente de la República Democrática del Congo. Hemos podido estudiar dos hembras procedentes de las capturas en este país del Dr. Th. Wagner. En 1971 Español describió el Xyletininae, Xyletinastes tessellatus, con una hembra procedente de Ngomeni, región de Tana en Kenya. La separó, básicamente, del resto de especies del género por la conformación de las antenas, única en el mismo, así como por otros caracteres del cuerpo que hacen que sea una especie aberrante dentro de los Xyletinastes Español, 1966. Posteriormente Español & Comas (1992) la separaron creando para ella el género Xyletinastidius, por los mencionados caracteres y por la armadura del saco interno del edeago, no estando representados en el mencionado trabajo. En la colección del Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia) de Barcelona, hemos localizado otro ejemplar procedente de Jkutha, Kenya, con la indicación "org. extraido, {". Ha sido imposible localizar este edeago dentro de las preparaciones microscópicas de la colección de anóbidos "F. Español" del Museu. Por suerte, hemos localizado un macho procedente de Sudáfrica, lo que amplia notablemente su área y nos permite efectuar la descripción del mismo, así como la representación del órgano copulador. La localización de varios ejemplares machos del Dorcatominae, Stagetodes australis (Español &

Viñolas, 1995a), descrito de Zululand con un sólo ejemplar hembra, pero con muy buenos caracteres diferenciales, nos permite realizar la descripción del macho y de su órgano copulador, validando así la especie. Resultados Subfamilia Anobiinae Género Trichodesma LeConte, 1861 Especie tipo: Anobium gibossum Say, 1825, designación original. Descrito por LeConte (1861) para el Anobium gibossum Say, 1825 (Say, 1825), procedente del valle del Mississipi, cuenta en la actualidad con un gran número de especies distribuidas por todo el continente americano, Japón y Asia meridional, conociéndose sólo tres especies de África (Español, 1966a; Pic, 1903) (fig. 25), pudiéndose hoy describir una nueva del África austral. Trichodesma endroedyyoungai sp. n. Diagnosis Las tibias con el borde externo no ensanchado, la distribución de la pubescencia pronotal y elitral (figs. 14–15), la talla media mayor y la conformación del edeago (figs. 9–10) lo diferencian de T. dentitibia Español, 1966. Bien separado también de T. nigrofasciata Español, 1966, por la distribución de la pubescencia pronotal y elitral (fig. 14 y 16) y por la muy diferente conformación del edeago. Más próxima a T. lateritia Pic, 1903, pero bien separada de ésta por el menor tamaño de las manchas pronotales de pubescencia (figs. 13–14), por las zona elitral desprovista de pubescencia blanca no alcanzando nunca el borde marginal (figs. 13–14), por el último artejo de los palpos maxilares y labiales de diferente contorno y poco o nada escotado en el ápice (figs. 3–6) y por el edeago más robusto y de diferente conformación (figs. 9–12). Descripción Longitud: 5,5–6,9 mm. Cuerpo subparalelo, convexo y muy robusto, superficie cubierta irregularmente de corta, densa y acostada pubescencia blanca, mezclada con otra más larga y erecta de reflejos amarillento castaños (fig. 1). Cabeza cubierta en parte por el protórax, totalmente pubescente; ojos muy grandes; antenas de once artejos, con maza terminal de tres, ésta más larga que la suma del resto de artejos (fig. 2); último artejo del palpo maxilar fusiforme, ligeramente truncado en el ápice (fig. 3), el labial fusiforme y nada truncado en el ápice (fig. 5). Protórax transverso, estrechado y redondeado en la base y ápice, con el disco giboso, los márgenes explanados y la superficie fuertemente

Animal Biodiversity and Conservation 30.1 (2007)

Fig. 1. Habitus del { de Trichodesma endroedyyoungai sp. n., de Ndumu camp, KwaZulu Natal. Fig. 1. Habitus of the { of Trichodesma endroedyyoungai n. sp., of Ndumu camp, KwaZulu Natal.

granulosa, cubierta totalmente por la pubescencia acostada blanca, sin zonas libres de ella y provista, en el disco, de cuatro manchas de pubescencia larga y erecta, de color castaño (fig. 14). Élitros con la superficie cubierta de pubescencia acostada blanca, mezclada con una de larga, erecta y dispersa de reflejos amarillento castaños, salvo una gran mancha, media, desprovista de la pubescencia blanca, que no alcanza nunca el borde marginal (fig. 14), los húmeros redondeados, con series longitudinales de puntos gruesos, muy

impresos, con los intervalos poco anchos y algo crenulados, la superficie junto a la base con granulación igual a la del protórax. Abdomen según modelo del género (fig. 8); patas cortas y robustas, nada ensanchadas en el borde externo; tarso con los artejos dilatados progresivamente; uñas con un saliente basal anchamente rectangular (fig. 7). Edeago (figs. 9–10) con el lóbulo medio basalmente muy dilatado y con el ápice, visto lateralmente, muy saliente y dirigido hacia abajo,

Viñolas & Masó

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Figs. 2–12. Trichodesma endroedyyoungai sp. n.: 2. Antena; 3. Último artejo del palpo maxilar; 5. Último artejo del palpo labial; 7. Uñas tarsales; 8. Abdomen; 9. Edeago en visión ventral; 10. Edeago en visión lateral. Trichodesma lateritia Pic, 1903, de la República Democrática del Congo: 4. Último artejo del palpo maxilar; 6. Último artejo del palpo labial; 11. Edeago en visión ventral; 12. Edeago en visión lateral. Figs. 2–12. Trichodesma endroedyyoungai n. sp.: 2. Antenna; 3. Last segment of maxillary palps; 5. Last segment of labial palps; 7. Claws; 8. Abdomen; 9. Aedeagus in ventral view; 10. Aedeagus in lateral view. Trichodesma lateritia Pic, 1903, of the Democratic Republic of the Congo: 4. Last segment of maxillary palps; 6. Last segment of labial palps; 11. Aedeagus in ventral view; 12. Aedeagus in lateral view.

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Figs. 13–16. Esquema de la pubescencia de la parte superior del cuerpo de: 13. Trichodesma lateritia Pic, 1903; 14. Trichodesma endroedyyoungai sp. n.; 15. Trichodesma dentitibia Español, 1966; 16. Trichodesma nigrofasciata Español, 1966. Figs. 13–16. Plan of pubescence of the upper part of the body of: 13. Trichodesma lateritia Pic, 1903; 14. Trichodesma endroedyyoungai n. sp.; 15. Trichodesma dentitibia Español, 1966; 16. Trichodesma nigrofasciata Español, 1966.

lacinias estrechas, curvadas regularmente y bastante salientes apicalmente, párameros muy gruesos y anchos lateralmente, con el ápice redondeado y provisto de larga y densa pubescencia. Hembra sin caracteres diferenciales apreciables. Material estudiado Holotypus: 1 {, "S. Afr. KwaZulu Natal / Ndumu camp / 26.55 S–32.18 E" "21–11–2002, E–Y:3553 / light trap / leg. J. Harrison, R. Müller". Depositado en el Transvaal Museum, Pretoria. Paratypus: 11 { }; 1 ex., "S. Afr. KwaZulu–Natal / Tembe Elephant Park / 27.03 S–32.25E" "17–11– 2002, E–Y:3545 / light trap at camp / leg. J. Harrison, R. Müller"; 1 ex., "S. Afr. KwaZulu Natal / Tembe Nat. Res. / 27.03 S–32.25 E" "18–11–2002, E–Y:3549 / light trap / leg. J. Harrison, R. Müller"; 1 ex., "S. Afr. KwaZulu Natal / Ndumu camp / 26.55 S–32.18 E" "21–11–2002, E–Y:3553 / light trap / leg. J. Harrison, R. Müller"; 8 ex., "S. Afr. KwaZulu Natal / Ndumu camp / 26.55 S–32.18 E" "22–11–2002, E–Y:3556 / light trap / leg. J. Harrison, R. Müller". Depositados en el Transvaal Museum, Pretoria, en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona y en la colección A. Viñolas. Biología Desconocida, todos los ejemplares fueron capturados con trampas de luz U.V.

Etimología Especie dedicada en memoria del Dr. Endrödy Younga, en homenaje a su gran labor como entomólogo y como persona. Distribución Conocido, de momento, sólo de la región de KwaZulu Natal en la República de Sudáfrica en su linde con Mozambique y Swaziland (fig. 17). El macho de T. lateritia Pic, 1903, citado por Español & Comas (1992) de Ndumu Zululand, probablemente deberá incluirse en la nueva especie.

Género Trichodesmina Español, 1982 Especie tipo: Trichodesmina nana Español, 1982, designación original. Trichodesmina nana Español, 1982 Género y especie descritos con un macho procedente de Congo da Lemba, República Democrática del Congo y una hembra de Albercorn, Zambia. Separado del género Trichodesma por la forma de las antenas, iguales en ambos sexos, con todos los artejos del funículo, excepto el octavo que es muy pequeño, aserrados y por la conformación tan característica del edeago (Español, 1982).

Viñolas & Masó

Trichodesma lateritia Pic Trichodesma dentitibia Español Trichodesma nigrofasciata Español Trichodesma endroedyyoungai sp. n. Xyletinastidius tessellatus Español Stagetodes australis Español & Viñolas

50 200 400 0 100 300

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Fig. 17. Distribución, en el continente africano, de los géneros Trichodesma LeConte, 1861, Xyletinastidius Español & Comas, 1992 y Stagetodes australis Español & Viñolas, 1994. Fig. 17. Distribution, in the African continent, of the genus Trichodesma LeConte, 1861, Xyletinastidius Español & Comas, 1992 and Stagetodes australis Español & Viñolas, 1994.

Hemos podido estudiar dos hembras procedentes de Cyamudongo, Ruanda, idénticas al tipo en cuanto a talla, conformación de las antenas y detalles de la morfología del cuerpo. No obstante, cabe señalar que Español (1982) indica para el cuerpo una coloración rojiza oscura uniforme y, por contra, los ejemplares de Ruanda tienen los élitros provistos de manchas, bastante uniformes, más claras y oscuras. Sin poder estudiar la genitalia masculina, es por el momento, imposible apreciar si existen diferencias específicas entre ellos.

Material estudiado 2 }, "Rwanda, Karengera / Cyamudongo, 1700 m / Th. Wagner leg. X.93", colección A. Viñolas.

Género Gastrallus Jacquelin du Val, 1860 Especie tipo: Anobium immarginatum Müller, 1821, designación original. Definido por el cuerpo subparalelo y alargado, cilíndrico, con la pubescencia aparente pero corta y

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Figs. 18–24. 18. Abdomen de Gastrallus. Edeago en visión ventral de: 19. Gastrallus varii Español & Comas, 1992; 20. Gastrallus minutus Español & Comas, 1992; 21. Gastrallus rorkei Español & Comas, 1992; 22. Gastrallus omedesae sp. n.; 23. Gastrallus jeremiasi sp. n.; 24. Gastrallus strydomi sp. n. Figs. 18–24. 18. Abdomen of the Gastrallus. Aedeagus in ventral view of the: 19. Gastrallus varii Español & Comas, 1992; 20. Gastrallus minutus Español & Comas, 1992; 21. Gastrallus rorkei Español & Comas, 1992; 22. Gastrallus omedesae n. sp.; 23. Gastrallus jeremiasi n. sp.; 24. Gastrallus strydomi n. sp.

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acostada; por la cabeza cubierta por el borde anterior del protórax; por las antenas de diez artejos, con maza terminal de tres, muy diferenciada del funículo (figs. 29–38); por el protórax convexo, con el borde lateral sólo marcado por detrás; por los élitros paralelos, provistos de series de puntos poco o nada impresos, a veces sólo lateralmente; por las procoxas muy separadas; por el mesosternón fuertemente excavado en el medio, para alojar las antenas en estado de reposo; metasternón grande y con surco longitudinal medio; por el abdomen con los dos primeros esternitos soldados (fig. 18) y por el edeago simétrico, con la forma de los parámeros y lóbulo medio muy variable segun la especie (figs. 19–28). Sin diferencias sexuales apreciables. La indicación del menor tamaño del cuerpo y la mayor longitud de las antenas en el macho, cuando se observan grandes series, es dificil de mantener como valor específico. De amplia distribución, se le conoce de gran parte de Europa y Asia, de todo el continente africano, donde hay la representación más numerosa, Madagascar y dos especies de Estados Unidos (California, Colorado y Nuevo Mexico) (Español, 1963a, 1963b, 1966b, 1992c; Español & Comas, 1992; Español & Viñolas, 1996). Las especies descritas como Gastrallus de Nueva Guinea, deberán permanecer en duda genérica hasta su comprobación.

último artejo de los palpos maxilares (fig. 40) y sobre todo por la conformación del edeago (fig. 21), sin igual en el resto de especies del género. El material ahora estudiado amplia su área de distribución a gran parte del Parque Nacional Kruger, norte y sur. Material estudiado 7 { y 4 }: 1 {, "S. Afr. Kruger Nat. Pk / Malonga sands / 22.38 S– 31.17 E" "2–2–1994; E–Y:2973 / UV light & trap / leg. Endrödy–Younga"; 3 { y 1 }, "S. Afr. Kruger Nat. Pk / Malonga sands / 22.38 S– 31.17 E" "9–2–1994; E–Y:2994 / UV light collection / leg. Endrödy–Younga"; 1 }, "S. Afr. Kruger Nat. Pk / Pafuri res ca. 3kmW / 22.25 S– 31.10 E" "9–2– 1994; E–Y:2994 / UV light collection / leg. Endrödy– Younga"; 1 { y 1 }, "S. Afr. Kruger Nat. Pk / Skukuza res / 24.59 S– 31.36 E" "22–1–1995; E– Y:3090 / UV light & trap / leg. Cl. Bellamy"; 1 }, "S. Afr. Kruger Nat. Pk / Pafuri research ca / 22.25 S– 31.12 E" "25–1–1995; E–Y:3098 / beating / leg. Cl. Bellamy"; 2 {, "S. Afr. Kruger Nat. Pk / Lebombo mt / 25.10 S– 32.02 E" "23–2–1995; E–Y:3118 / beating / leg. Endrödy–Younga". Depositados en el Transvaal Museum, Pretoria y en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona.

Gastrallus minutus Español & Comas, 1992 Gastrallus varii Español & Comas, 1992 Descrito con 1 { y 1 } procedentes del campo Letaba, Parque Nacional Kruger y bien caracterizado por la conformación de las antenas (fig. 29), último artejo de los palpos maxilares (fig. 39) y la conformación muy característica del edeago (fig. 19). Todos los ejemplares estudiados proceden de la región norte de dicho parque. Material estudiado 10 { y 1 }: 1 {, "PUNDA MILIA / K. N. P. Survey / 21–23.XI.1961 / Vári & Rorke"; 7 {, "S. Afr : Kruger Nat. Pk / Pafuri res. Camp / 22.25 S–31.12 E" "30.1.1994; E–Y:2954 / UV light & trap / leg. Endrödy–Younga"; 1 { y 1 } "S. Afr : Kruger Nat. Pk / Pafuri res. Camp / 22.25 S–31.12 E" "5.2.1994; E–Y:2982 / UV light collection / leg. Endrödy– Younga"; 1 {, "S. Afr : Kruger Nat. Pk / Pafuri res. Camp / 22.25 S–31.12 E" "25.1.1995; E–Y:3098 / beating / leg. Cl. Bellamy". Depositados en el Transvaal Museum, Pretoria y en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona.

Descrito con un sólo ejemplar macho procedente del Northen Transvaal, Mmabolela State, próximo a G. varii Español & Comas, 1992, pero diferenciado de éste por la conformación de las antenas (fig. 31), del último artejo de los palpos maxilares (fig. 41) y por la diferente estructura de los parámeros del edeago (fig. 20). La diferencia, dada en la descripción, de sólo 6 artejos en el funículo, no es cierta, los dos ejemplares estudiados poseen, como el resto de especies del género, 7 artejos en el funículo, siendo el quinto muy pequeño y poco diferenciado del sexto, pareciendo una continuación del mismo (fig. 31). La longitud, 2,0–2,2 mm, de los ejemplares estudiados, superior a los 1,8 mm del tipo, lo colocan aun más en las proximidades de G. varii (2,5–2,9 mm). Extendido al parecer por gran parte del Parque Nacional Kruger. Material estudiado 2 {: 1 {, "S. Afr. Kruger Nat Pk / Skukuza res camp / 24.59 S–31–36 E" "29.1.1994; E–Y:2953 / UV light & trap / leg. Endrödy–Younga"; 1 {, "S. Afr: Kruger Nat Pk / Pafuri res camp / 22.25 S– 31.12 E" "5.2.1994; E–Y:2982 / UV light collection / leg. Endrödy–Younga". Depositados en el Transvaal Museum, Pretoria.

Gastrallus rorkei Español & Comas, 1992 Descrito con una numerosa serie de ejemplares, 6 { y 4 }, procedentes todos ellos del Northen Transvaal, Mmabolela state. Bien definido por la forma del protórax, de las antenas (fig. 30), del

Gastrallus omedesae sp. n. Diagnosis Próximo a Gastrallus vrydaghi Español, 1963, G.

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gabonicus Español, 1963, G. basilewskyi Español, 1963 y G. kaszabi Español, 1966, por su talla y contorno del cuerpo, pero bien separado de todos ellos por la conformación de las series elitrales de puntos y granulación de la superficie de los élitros, asimismo por la particular estructura del último artejo de los palpos maxilares y sobre todo por la del órgano copulador. Éste último lo sitúan al lado de su vecino geográfico G. rorkei Español & Comas, 1992, ambos provistos de lacinias y de espinas muy desarrolladas en el lóbulo medio, separados no obstante por la diferente conformación de dicho órgano (figs. 22–22) y sobre todo por el contorno muy diferente del último artejo de los palpos maxilares (figs. 40, 42). Descripción Longitud: 2,50–2,77 mm. Cuerpo subparalelo, de color castaño rojizo muy oscuro y con la superficie cubierta de corta pubescencia acostada, poco visible y de un color grisáceo claro. Antenas de diez artejos (fig. 32), con maza terminal de tres artejos muy dilatados lateralmente, octavo y noveno por igual, sin diferencias apreciables en los artejos del funículo; último artejo de los palpos maxilares securiforme (fig. 42), con el borde apical bisinuado; protórax transverso, 1,37 veces más ancho que largo, de lados estrechados en el medio y salientes hacia el ápice y la base, con la mayor anchura junto a ésta, lados y base finamente bordeados, ángulos posteriores muy redondeados, nada marcados, sin gibosidad manifiesta en la región discal, superficie cubierta de granulosidad bien indicada, regular y nada contigua. Élitros con sólo seis series de puntos apreciables, más impresas las dos laterales junto al borde marginal, superficie cubierta de granulación muy densa y confusa. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 22) con los parámeros largos y gráciles, terminados en punta recurvada, lóbulo medio provisto de dos espinas muy bien caracterizadas, lacinias notablemente largas y desarrolladas. Hembra sin diferencias sexuales aparentes. Material estudiado Holotypus: 1 {, "S. Afr.; Kruger Nat. Pk / Pafuri around / 22.25 S– 31.12 E c" "1.2.1994; E–Y:2969 / air plankton / leg. Endrödy Younga". Depositado en el Transvaal Museum, Pretoria. Paratypus: 1 }, "S. Afr.; Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "5.2.1994; E–Y:2982 / UV light collection / leg. Endrödy Younga". Depositado en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona. Etimología Dedicado a la Dra. Anna Omedes, directora del Museu de Ciències Naturals de la Ciutadella de Barcelona, por su gran disposición y ayuda en nuestras labores entomológicas.

Biología Desconocida, los ejemplares han sido capturados con trampa aérea de plancton y a la luz ultravioleta. Distribución Sólo conocido, de momento, de la localidad típica, la reserva Pafuri, en el extremo norte del Parque Nacional Kruger, en la República de Sudáfrica en su linde con Zimbabwe y Mozambique (fig. 52).

Gastrallus jeremiasi sp. n. Diagnosi Especie muy bien caracterizada por diferentes detalles de su morfología externa, tales como: su gran talla; la gracilidad de sus antenas (fig. 33); las series de puntos de los élitros completas, incluida la escutelar, profundamente impresas y marcando verdaderas estrías elitrales. También la conformación de los parámeros y sobre todo del lóbulo medio del edeago (fig. 28) lo separan de todos los Gastrallus conocidos. Descripción Longitud: 3,45–4,80 mm. Cuerpo subparalelo, de color castaño rojizo muy oscuro y con la superficie cubierta de pubescencia grisácea, corta, acostada y muy densa Antenas de diez artejos (fig. 33), muy gráciles, con maza terminal de tres artejos, estrechos, tan larga como el funículo, éste con sólo el sexto artejo ligeramente dentado; último artejo de los palpos maxilares securiforme (fig. 48); protórax algo transverso, 1,22 veces más ancho que largo, de lados sinuosos junto a la base y estrechados por delante, con la máxima anchura en la mitad basal, lados y base bordeados, sin gibosidad aparente en la región discal, superficie cubierta de granulación muy marcada, regular, nada contigua. Élitros con todas las series de puntos, incluida la escutelar, muy marcadas, formando verdadera estriación, superficie cubierta de granulación menor que la del protórax, pero mucho más densa. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 23) simétrico, con los parámeros cortos y de estructura muy particular, con el lóbulo medio ancho, muy quitinizado en el ápice y provisto este, en ambos lados, de dos dientes muy marcados. Hembra sin diferencias sexuales aparentes. Material estudiado Holotypus: 1 {, "S. Afr : Kruger Nat. Pk / Pafuri res camp / 22.25 S– 31.12 E" "30.1.1994; E–Y:2954 / UV light & trap / leg. Endrödy–Younga". Depositado en el Transvaal Museum, Pretoria. Paratypus: 13 { y 5 }: 1 }, "S. Afr; Tvl. Nelspruit / Nat. Res., Koppee / 25.29 S– 30.55 E" "19.12.1986; E–Y:2403 / beating / leg. Endrödy Younga"; 2 {, "S. Afr: Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "30.1.1994; E–Y:2954 / UV light & trap / leg. Endrödy Younga"; 1 { y 2 }, "S. Afr: Kruger Nat.

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37 38

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Figs. 25–38. Edeago en visión ventral de: 25. Gastrallus pafuriensis sp. n.; 26. Gastrallus skukuzaensis sp. n.; 27. Gastrallus ndumuensis sp. n.; 28. Gastrallus krugerensis sp. n. Antena de: 29. Gastrallus varii Español & Comas, 1992; 30. Gastrallus rorkei Español & Comas, 1992; 31. Gastrallus minutus Español & Comas, 1992; 32. Gastrallus omedesae sp. n.; 33. Gastrallus jeremiasi sp. n.; 34. Gastrallus strydomi sp. n.; 35. Gastrallus pafuriensis sp. n.; 36. Gastrallus skukuzaensis sp. n.; 37. Gastrallus ndumuensis sp. n.; 38. Gastrallus krugerensis sp. n. Figs. 25–38. Aedeagus in ventral view of the: 25. Gastrallus pafuriensis n. sp.; 26. Gastrallus skukuzaensis n. sp.; 27. Gastrallus ndumuensis n. sp.; 28. Gastrallus krugerensis n. sp. Antenna of the: 29. Gastrallus varii Español & Comas, 1992; 30. Gastrallus rorkei Español & Comas, 1992; 31. Gastrallus minutus Español & Comas, 1992; 32. Gastrallus omedesae n. sp.; 33. Gastrallus jeremiasi n. sp.; 34. Gastrallus strydomi n. sp.; 35. Gastrallus pafuriensis n. sp.; 36. Gastrallus skukuzaensis n. sp.; 37. Gastrallus ndumuensis n. sp.; 38. Gastrallus krugerensis n. sp.

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Figs. 39–51. Último artejo de los palpos maxilares de: 39. Gastrallus varii Español & Comas, 1992; 40. Gastrallus rorkei Español & Comas, 1992; 41. Gastrallus minutus Español & Comas, 1992; 42. Gastrallus omedesae sp. n.; 43. Gastrallus jeremiasi sp. n.; 44. Gastrallus strydomi sp. n.; 45. Gastrallus pafuriensis sp. n.; 46. Gastrallus skukuzaensis sp. n.; 47. Gastrallus ndumuensis sp. n.; 48. Gastrallus krugerensis sp. n. Xyletinastidius tesellatus (Español, 1971): 49. Parte anterior del segmento genital; 50. Edeago en visión ventral; 51. Detalle de las espinas del saco interno del edeago. Figs. 39–51. Last segment of maxillary palps of the: 39. Gastrallus varii Español & Comas, 1992; 40. Gastrallus rorkei Español & Comas, 1992; 41. Gastrallus minutus Español & Comas, 1992; 42. Gastrallus omedesae n. sp.; 43. Gastrallus jeremiasi n. sp.; 44. Gastrallus strydomi n. sp.; 45. Gastrallus pafuriensis n. sp.; 46. Gastrallus skukuzaensis n. sp.; 47. Gastrallus ndumuensis n. sp.; 48. Gastrallus krugerensis n. sp. Xyletinastidius tesellatus (Español, 1971): 49. Genital segment; 50. Aedeagus in ventral view; 51. Detail of the spines of the internal sack of the aedeagus.

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Pk / Pafuri res. camp 4KmW / 22.25 S– 31.09 E" "1.2.1994; E–Y:2970 / UV light & trap / leg. Endrödy Younga"; 4 { y 1 }, "S. Afr: Kruger Nat. Pk / Pafuri research ca. / 22.25 S– 31.12 E" "18.11.1994; E– Y:3053 / beating / Endrödy & Bellamy"; 5 {, "S. Afr: Kruger Nat. Pk / Pafuri research ca. / 22.25 S– 31.12 E" "25.1.1995; E–Y:3098 / beating / leg. Cl. Bellamy"; 1 { y 1 }, "S. Afr : Kruger Nat. Pk / Pafuri research ca. / 22.25 S– 31.12 E" "26.1.1995; E–Y:3100 / UV light & trap / leg. Cl. Bellamy". Depositados en el Transvaal Museum, Pretoria, en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona y en la colección A. Viñolas. Etimología Dedicado al Dr. Xavier Jeremias, buen entomólogo y sobre todo excelente amigo, por la gran ayuda, totalmente desinteresada, prestada a todos a lo largo de los años. Biología Desconocida, los ejemplares estudiados han sido capturados con trampa de luz ultravioleta y también batiendo la vegetación. Distribución Conocido del Parque Nacional Kruger, República de Sudáfrica; de la reserva Pafuri situada en el extremo norte en su linde con Zimbabwe y Mozambique, y de Koppe en el extremo sur, en las cercanias de Nelspruit (fig. 52).

Gastrallus strydomi sp. n. Diagnosis Por la forma del cuerpo y talla se debe colocar en la vecindad de Gastrallus vrydaghi Español, 1963 y G. kaszabi Español, 1966, diferenciado de ellos por las series de puntos de los élitros totalmente visibles, sólo las laterales en ellos, por el desarrollo de primer artejo de la maza antenal (fig. 34), carácter que también lo separan del resto de Gastrallus. La conformación del último artejo del palpo maxilar (figs. 39, 40, 44) lo sitúan al lado de G. varii Español & Comas, 1992 y de G. rorkei Español & Comas, 1992, separado de ambos por la muy diferente conformación de los parámeros del órgano copulador (figs. 19, 21, 24), sin igual en el resto de especies del género. Descripción Longitud: 1,80–2,15 mm. Cuerpo subparalelo, de color castaño rojizo claro y con la superficie cubierta de muy larga, acostada y no muy densa pubescencia de un color grisáceo. Antenas de diez artejos (fig. 34), con maza terminal de tres artejos muy dilatados lateralmente, sobre todo el octavo, ésta bastante más larga que el funículo que tiene los artejos cuarto y sexto dentados; último artejo de los palpos maxilares securiforme (fig. 44); protórax transverso, 1,28 veces más ancho que largo, de lados estrechados en el medio y salien-

tes hacia el ápice y la base, con la mayor anchura junto a ésta, lados y base bordeados, ángulos posteriores redondeados, pero bien indicados, sin gibosidad manifiesta en la región discal, superficie cubierta de granulosidad poco indicada y confusa. Élitros con todas las series de puntos apreciables, más las laterales junto al borde marginal, superficie cubierta con la misma granulación que el protórax. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 24) con los parámeros con un contorno propio muy bien caracterizado y con el lóbulo medio corto y ancho, poco quitinizado. Hembra sin diferencias sexuales aparentes. Material estudiado Holotypus: 1 {, "S. Afr.; N. Transvaal / Waterberg, Farm 223 / 24.11 S– 27.50 E" "11.2.1976; E– Y:1030 / at light / leg. A. Strydom". Depositado en el Transvaal Museum, Pretoria. Paratypus: 1 { y 1 }, "S. Afr., N. Transvaal / Mmabolela estate / 22.40 S– 28.15 E" "9.3.1973; E–Y:33 / mercury vap. light / leg. Endrödy Younga". Depositados en el Transvaal Museum, Pretoria y en el Museu de Ciències Naturals (edificio de Zoologia), Barcelona. Etimología Dedicado al Dr. A. Strydom, recolector del ejemplar tipo de ésta interesante especie. Biología Desconocida, los ejemplares estudiados fueron capturados con diferentes trampas de luz. Distribución Coloniza el Northern Transvaal, en la República de Sudáfrica.

Gastrallus pafuriensis sp. n. Diagnosis La conformación del cuerpo, antenas y edeago lo acercan a Gastrallus gabonicus Español, 1963, aun que el contorno del protórax, en línea recta de la base al ápice, los artejos tercero a séptimo de las antenas iguales y sin diferencias apreciables (fig. 35), la diferente estructura de los parámeros y sobre todo la del lóbulo medio del órgano copulador, lo alejan del mismo. Descripción Longitud: 2,00–2,32 mm. Cuerpo subparalelo, de color castaño claro y con la superficie cubierta de pubescencia muy corta, acostada y de un color grisáceo. Antenas de diez artejos (fig. 35), con maza terminal de tres artejos, los dos primeros dilatados, lateralmente, por igual, ésta bastante más larga que el funículo, con los artejos tercero a séptimo del funículo iguales y nada dilatados lateralmente; último artejo de los palpos maxilares securiforme

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(fig. 45), bastante dilatado lateralmente; protórax transverso, 1,3 veces más ancho que largo, de lados en línea de la base al ápice y con la mayor anchura en la base, lados y base bordeados, ángulos posteriores redondeados y poco marcados, sin gibosidad manifiesta en la región discal, superficie provista de granulación poco destacada y nada contigua. Élitros con todas las series de puntos apreciables, aunque sólo bien impresas las dos laterales junto al borde marginal, superficie cubierta de granulación pequeña y muy irregular en tamaño y densidad. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 25) con los parámeros grandes, largos y apicalmente aguzados, lóbulo medio redondeado en el ápice y con el saco interno poco desarrollado. Hembra sin diferencias sexuales aparentes. Material estudiado Holotypus: 1 {, "S. Afr: Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "30.1.1994; E–Y:2954 / UV light & trap / leg. Endrödy Younga". Depositado en el Tranvaal Museum, Pretoria. Paratypus: 2 { y 1 }, "S. Afr: Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "30.1.1994; E– Y:2954 / UV light & trap / leg. Endrödy Younga". Depositados en el Tranvaal Museum, Pretoria, en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona y en la colección A. Viñolas. Etimología Nombre de la reserva natural donde ha sido capturado el tipo de la especie. Biología Desconocida, todos los ejemplares fueron capturados con trampa de luz ultravioleta. Distribución Localizado en la reserva Pafuri, en el extremo norte del Parque Nacional Kruger, en la República de Sudáfrica en su linde con Zimbabwe y Mozambique (fig. 52).

Gastrallus skukuzaensis sp. n. Diagnosis La conformación del cuerpo, antenas y edeago lo acercan a Gastrallus gabonicus Español, 1963, G. basilewskyi Español, 1963 y G. pafuriensis sp. n. La granulosidad doble de la superficie del protórax lo separa de ellos, así como por la diferente conformación del funículo de las antenas y también por el contorno de los parámeros y estructura del lóbulo medio del órgano copulador.

Antenas de diez artejos (fig. 36), con maza terminal de tres artejos bastante dilatados lateralmente y algo más larga que el funículo, éste con sólo el sexto artejo más desarrollado, pero no más saliente, lateralmente, que el resto; último artejo de los palpos maxilares securiforme (fig. 46), poco dilatado lateralmente; protórax transverso, 1,32 veces más ancho que largo, de lados ligeramente sinuosos en la mitad apical, algo redondeados hacia la base y con la máxima anchura en ésta, lados y base bordeados, ángulos posteriores redondeados, pero bien marcados, sin gibosidad discal manifiesta, superficie con granulosidad grande, aparente y muy dispersa en la mitad apical, menor y muy densa en la mitad basal. Élitros con sólo dos series de puntos, muy impresas, junto al borde marginal, superficie cubierta de densa e irregular granulación, igual, en tamaño, a la de la mitad basal del protórax. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 26) con los parámeros muy largos y paralelos, con el ápice terminado en un doble diente, externo–interno, muy característico, lóbulo medio largo y ancho, pudiéndose apreciar en el saco interno unas pequeñas e irregulares espinas, poco quitinizadas. El ejemplar procedente de Pafuri, aunque externamente indiferenciable del ejemplar tipo de Skukuza, presenta unas ligeras diferencias en la conformación del edeago, que creemos se deben a una malformación del mismo. Hembra desconocida. Material estudiado Holotypus: 1 {, "S. Afr: Kruger Nat. Pk / Skukuza research ca / 24.59 S– 31.35 E" "28.1.1994; E– Y:2952 / UV light & trap / leg. Endrödy Younga". Depositado en el Transvaal Museum, Pretoria. Paratypus: 1 {, "S. Afr.: Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "30.1.1994; E– Y:2954 / UV light & trap / leg. Endrödy Younga". Depositado en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona. Etimología Nombre del campo de investigación donde ha sido capturado el tipo de la especie. Biología Desconocida, los ejemplares examinados fueron capturados con trampa de luz ultravioleta. Distribución Propio del Parque Nacional Kruger, en la República de Sudáfrica (fig. 52).

Gastrallus ndumuensis sp. n. Descripción Longitud: 2,05–2,10 mm. Cuerpo subparalelo, de color castaño claro y con la superficie cubierta de pubescencia relativamente larga, acostada y de color grisáceo.

Diagnosis El protórax con los ángulos posteriores muy marcados y salientes, nada redondeados y con una ligera gibosidad discal, así como la estructura del

Viñolas & Masó

30º 30'

31º

1º 30'

32º

32º 30'

Zimbabwe

22º 30'

Pafuri 1 Punda Milia 2

Malonga 3 Nayandu 4

23º

23º 30'

Mozambique

República de Sudáfrica

24º

24º 30'

25º Skukuza 5 Lebombo 6

G. varii Español & Comas 1–2 G. rockei Español & Commas 1–3–5–6 G. minutus Español & Comas 1–5 G. omedesae sp. n. 1 G. jeremiasi sp. n. 1–7

25º 30'

Nelspruit 7

Swaziland

G. pafuriensis sp. n. 1 G. skukuzaensis sp. n. 1–5 G. krugerensis sp. n. 4

Fig. 52. Distribución del género Gastrallus Jacquelin du Val, 1860, en el Parque Nacional Kruger, República de Sudáfrica. Fig. 52. Distribution of the genus Gastrallus Jacquelin du Val, 1860, in the Kruger National Park, South Africa.

edeago (fig. 27) lo alejan de todos sus congéneres africanos, acercándolo a los europeos (Español, 1963a), pero también diferenciado de ellos por el órgano copulador y otros pequeños detalles. Descripción Longitud: 2,95–3,30 mm. Cuerpo subparalelo, de color castaño rojizo ligeramente oscurecido y con la superficie cubierta de corta, acostada y densa pubescencia amarillenta. Antenas de diez artejos (fig. 37), con maza termi-

nal de tres artejos, los dos primeros dilatados, lateralmente, por igual, bastante más larga que el funículo, éste con sólo el sexto artejo más desarrollado que el resto; último artejo de los palpos maxilares securiforme (fig. 47), proporcionalmente muy grande y desarrollado; protórax nada transverso, de lados casi en línea de la base al ápice, con la máxima anchura junto a ésta, lados y base bordeados, ángulos posteriores muy marcados, con una ligera gibosidad en el disco, superficie cubierta de granulación muy aparente, regular y bastante densa.

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0,25 mm

0,1 mm

0,25 mm

0,5 mm

Figs. 53–58. Stagetodes australis Español & Viñolas, 1995: 53. Antena; 54. Ojo en visión lateral; 55. Último artejo del palpo maxilar; 56. Último artejo del palpo labial; 57. Abdomen; 58. Edeago en visión ventral. Figs. 53–58. Stagetodes australis Español & Viñolas, 1995: 53. Antenna; 54. Eye in lateral view; 55. Last segment of maxillary palp; 56. Last segment of labial palp; 57. Abdomen; 58. Aedeagus in ventral view.

Élitros con sólo tres series de puntos, poco indicadas, junto al borde marginal, superficie cubierta de granulación bien impresa, irregular y muy densa. Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 27) con los parámeros grandes, redondeados lateralmente en el ápice y con el lóbulo medio poco desarrollado, provisto de lacínias más largas que él. Hembra sin diferencias sexuales aparentes.

Material estudiado Holotypus: 1 {, "S. Afr.; KwaZulu–Natal / Ndumu / 36.55 S– 32.18 E" "21.11.2002; E–Y:3553 / light trap / leg. J. Harrison. R. Müller". Depositado en el Transvaal Museum, Pretoria. Paratypus: 2 { y 2 }: 1 { y 1 }, "S. Afr.; KwaZulu–Natal / Kosi Bay / 26.58 S– 32.50 E" "13.11.2002; E–Y:3532 / at light / Burger, Harrison, Müller"; 1 }, "S. Afr.; KwaZulu–Natal / Kosi Bay

Viñolas & Masó

camp / 26.58 S– 32.50 E" "15.11.2002; E–Y:3540 / light trap / leg. J. Harrison. R. Müller"; 1 {, "S. Afr.; KwaZulu–Natal / Ndumu / 36.55 S– 32.18 E" "21.11.2002; E–Y:3553 / light trap / leg. J. Harrison. R. Müller". Depositados en el Transvaal Museum, Pretoria, en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona y en la colección A. Viñolas. Etimología Nombre de la localidad donde ha sido capturado el tipo de la especie. Biología Desconocida, los ejemplares estudiados fueron capturados con diferentes trampas de luz. Distribución Conocido sólo de la región de KwaZulu Natal en la República de Sudáfrica en su linde con Mozambique y Swaziland.

Gastrallus krugerensis sp. n. Diagnosis Especie muy bien caracterizada por su pequeña talla, por la granulación diferente de la zona discal de la superficie del protórax y sobre todo por la conformación muy particular del edeago (fig. 28), caracteres todos ellos que lo separan del resto de especies conocidas del género.

Material estudiado Holotypus: 1 {, "S. Afr.; Kruger Nat. Pk / Nyandu sands / 22.38 S– 31.23 E" "9.2.1994; E–Y:2990 / ground & vegetation / leg. Endrödy Younga". Depositado en el Transvaal Museum, Pretoria. Paratypus: 1 { y 2 }: 1 { y 1 }, "S. Afr.; Kruger Nat. Pk / Pafuri, around / 22.25 S– 31.12 E c" "1.2.1994; E–Y:2969 / air plankton / leg. Endrödy Younga"; 1 }, "S. Afr.; Kruger Nat. Pk / Pafuri res. camp / 22.25 S– 31.12 E" "5.2.1994; E–Y:2982 / UV light collection / leg. Endrödy Younga". Depositados en el Transvaal Museum, Pretoria, en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona y en la colección A. Viñolas. Etimología Nombre del Parque Nacional donde fueron capturados todos los ejemplares estudiados. Biología Desconocida, pero recolectada por diferentes procedimientos, con luz ultravioleta, con trampa aérea de plancton y sobre el campo y vegetación. Distribución Propio de la zona norte del Parque Nacional Kruger, en la República de Sudáfrica (fig. 52).

Subfamilia Xyletininae Género Xyletinastidius Español & Comas, 1992

Descripción Longitud: 1,36–1,73 mm. Cuerpo subparalelo, de color castaño rojizo claro y con la superficie cubierta de larga, acostada y no muy densa pubescencia de un color grisáceo. Antenas de diez artejos (fig. 38), con maza terminal de tres artejos no muy dilatados lateralmente y bastante más larga que el funículo, sin diferencias apreciables en los artejos de éste; último artejo de los palpos maxilares securiforme (fig. 48), poco ensanchado apicalmente; protórax ligeramente transverso, 1,15 veces más ancho que largo, de lados estrechados en el medio y salientes hacia el ápice y la base, con la mayor anchura junto a ésta, lados y base bordeados, ángulos posteriores redondeados, pero bien indicados, sin gibosidad manifiesta en la región discal, superficie densa y regularmente granulada, excepto en la zona discal anterior en la que los gránulos son mayores y muy dispersos. Élitros con sólo tres series de puntos, bien indicadas, junto al borde marginal, superficie cubierta de granulación casi igual, a la basal, del protórax Pro–, meso–, metasternón y abdomen según el modelo del género. Edeago (fig. 28) con los parámeros largos y finos, terminados en punta recurvada en el ápice, lóbulo medio no muy desarrollado y poco quitinizado. Hembra sin diferencias sexuales aparentes.

Especie tipo: Xyletinastes tessellatus Español, 1971, designación original. Definido básicamente por la conformación de las antenas (Español, 1971, fig. 2) de diez artejos, del cuarto al décimo fuertemente flabelados y el tercero triangular, también por la forma del último artejo de los palpos maxilares (Español, 1971, fig. 3) y por la pubescencia elitral. Caracteres que lo separan de Xyletinastes Español, 1966, a los que podríamos añadir el protórax con el disco poco giboso y una mayor riqueza en la escultura de la superficie del cuerpo.

Xyletinastidius tessellatus (Español, 1971) Xyletinastes tessellatus Español, 1971: 49. Xyletinastidius tessellatus (Español): Español & Comas, 1992: 28.

Hoy al poseer un { procedente de Ndumu, KwaZulu–Natal, República de Sudáfrica, al compararlo con el tipo de la especie, una } de Ngomeni, Tana, Kenia y observar la coincidencia total de todos sus caracteres externos procedemos a su descripción, recordar lo comentado en la introducción a lo sucedido al { de Jkutha, Kenya, de la colección del Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia) de Barcelona.

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Aunque Español (1972), en su trabajo sobre los Xyletininae del Gabón, al describir una nueva especie del género Xyletinastes Español, 1966, en la página 185 representa las antenas de las especies conocidas del género con el siguiente pie de figura [23–26. Gén. Xyletinastes Esp., antenas del { : 23. X. tessellatus Esp.; 24. X. basilewsky Esp.; 25. X. hastatus sp. n.; 26. X. decelli Esp.], la figura 23 perteneciente a la antena de X. tessellatus corresponde al de la hembra y es el mismo empleado pocos meses antes en la descripción de la especie. Descripción del macho Longitud 5,2 mm. (5 mm la hembra) Cuerpo ligeramente oval, de un color castaño rojizo no muy oscuro, superficie cubierta de pubescencia dorada bastante larga, acostada y densa, formando sobre los élitros un dibujo de bandas longitudinales, muy regular y bien delimitado. Toda la parte superior del cuerpo esta cubierta de fuerte granulación, variable en tamaño, pero siempre muy visible, igual a la hembra tipo, aunque en la descripción original (Español, 1971) se indica un fuerte punteado para dicha superficie. Cabeza con la superficie cubierta de gruesos gránulos, nada contiguos, con ojos grandes y salientes; antenas de diez artejos, con el tercero triangular y del cuarto al décimo flabelados; último artejo del palpo maxilar alargado. Antenas y palpos sin diferencias apreciables con la hembra de Kenia. Protórax muy transverso, 1,44 veces más ancho que largo, de lados estrechados hacia delante y ligeramente sinuados en la mitad apical y con la máxima anchura en la base, lados, base y borde apical completamente bordeados, ligeramente giboso en el disco, ángulos posteriores obtusos y redondeados, superficie cubierta de gruesos gránulos, muy destacados del fondo y dispersamente distribuidos. Élitros paralelos, redondeados en el ápice y con el borde marginal, en el tercio apical, provisto de pequeños dientes, sin estrías ni series de puntos manifiestas, superficie cubierta totalmente de pequeños gránulos, muy destacados y densamente dispuestos. Pro–, meso–, metasternón y abdomen iguales a la hembra. Edeago (fig. 58) con el modelo propio de la subfamilia y con el saco interno (fig. 52) provisto de pequeñas espinas; segmento genital (fig. 49) inerme. Distribución Conocido hasta el presente de Kenia, hoy podemos añadir a su distribución la de Ndumu, KwaZulu– Natal en la República de Sudáfrica (fig. 17).

Subfamilia Dorcatominae Género Stagetodes Español, 1970 Especie tipo: Theca breviuscula Fairmaire, 1886, designación original.

Español & Viñolas (1995a) describieron una nueva especie del género, con una hembra procedente de Sudáfrica, por sus buenos caracteres diferenciales que la alejaban de sus congéneres asiáticos y la colocaban en la vecindad de S. breviusculus (Fairmaire, 1886) y S. africanus (Pic, 1929) (Español, 1970), pero bien separada de ellos por la conformación de las antenas, último artejo de los palpos maxilares, escotadura lateral de los ojos y también por pequeños detalles morfológicos ventrales. Al haber podido localizar machos de la misma, procedemos a su descripción y representación de su edeago, confirmando la validez específica de la misma.

Stagetodes australis Español & Viñolas, 1995 Descripción del macho Longitud 2,65–3,25 mm. Cuerpo convexo, subparalelo, de color castaño muy oscuro a negruzco y con la superficie cubierta de larga pubescencia, erecta, de color dorado. Cabeza cubierta en gran parte por el borde anterior del protórax; antenas de once artejos, con maza terminal de tres, fuertemente desarrollada (fig. 53) y con los artejos quinto y séptimo del funículo muy salientes lateralmente; ojos muy escotados, casi divididos (fig. 54); último artejo de los palpos maxilares grande y muy tranverso (fig. 55); ultimo artejo de los palpos labiales, algo menor y menos transverso (fig. 56). Protórax transverso, de lados regularmente estrechados hacia el ápice y con la máxima anchura en la base, ésta con el lóbulo medio saliente hacia atrás, superficie con el punteado fuerte, bien impreso, más denso hacia los márgenes. Élitros paralelos con el calo humeral poco indicado, superficie con el punteado fuerte, bien impreso, pero algo menor que el del protórax, provistos de diez estrías y una escutelar corta, todas muy indicadas, punteado de las mismas fuerte y grande, desbordando el contorno de las laterales, intervalos discales planos, los laterales algo convexos. Abdomen (fig. 57) con la superficie cubierta de punteado grande, bien impreso y bastante pubescente. Edeago (fig. 58) simétrico, con los parámeros muy cortos y el lóbulo medio provisto en el ápice de espinas asimétricamente colocadas. Las diferencias frente al tipo (hembra) son: una talla media menor, un mayor desarrollo de la maza antenal y una ligera modificación del contorno del último artejo de los palpos maxilares y labiales. Material estudiado 4 {: 1 {, "S. Afr.: Kruger Nat. Pk / Skukuza research ca / 25.00 S– 31.35 E" "1.12.1988; E–Y: 2593 / forest floor litter / leg. Endrödy – Younga"; 1 {, "S. Afr. N Zululand / Ndumu Game Reserve / 26.54 S– 32.17 E" "2.12.1992; E–Y: 2875 / UV light at vie / leg. Endrödy – Younga"; 1 {, "S. Afr.: Kruger Nat. Pk / Skukuza research ca / 25.00 S– 31.35 E" "19.2.1995; E–Y: 3102 / UV light & trap / leg.

Endrödy – Younga"; 1 {, S. Afr.: KwaZulu–Natal / Tembe Elephant Park / 27.03 S– 32.25 E" "19.11.2002; E–Y: 3549 / light trap at camp / leg. J. Harrison, R. Müller". Depositados en el Transvaal Museum, Pretoria y en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia), Barcelona. Distribución Conocida de una pequeña zona de Sudáfrica en su linde con Mozambique, extremo sur del Parque Nacional Kruger y noreste de KwaZulu Natal, por lo que es probable que también habite en Swaziland (fig. 17). Agradecimientos Agradecemos a la Dra. Ruth Müller, del Transvaal Museum de Pretoria, las facilidades prestadas para poder continuar con el estudio de los Anobiidae de las colecciones de dicho Museo. También al Dr. Th. Wagner, del Museum Alexander Konig de Berlín, la donación para estudio del material de Anobiidae por el capturado en sus campañas por Ruanda. Referencias Español, F., 1963a. Notas sobre anóbidos. VIII. Los Gastrallus mediterráneos. Publicaciones del Instituto de Biología Aplicada, 35: 5–21. – 1963b. Notas sobre anóbidos. IX–X (Coleoptera Anobiidae). IX. Contribución al conocimiento de los Gastrallus del África tropical. X. Un nuevo género y especie de Dorcatominae del África tropical. Rev. Zool. Bot. Afr., 67(3–4): 189–202. – 1966a. Notas sobre anóbidos (Coleoptera). XVII . Las Trichodesma del África tropical. Eos, 41(2–3): 215–222. – 1966b. Notas sobre anóbidos. 23. Descripción de un nuevo Xyletininae del África central. 24. Sobre el género Deroptilinus Lea. 25. Un nuevo Gastrallus del norte de Ghana. Eos, 42(1–2): 265–273. – 1970. Nota sobre Anóbidos. 36. Sobre la disparidad genérica del complejo Stagetus Woll. Anales de la Escuela Nacional de Ciencias Biológicas, México, 17(1968) 157–168. – 1971. Notas sobre Anóbidos. 53: Más datos sobre el género Xyletinastes Español, con la descripción de un nuevo representante del África Oriental. Miscelánia Zoológica, 3(1): 49–52. – 1972. Contribución al conocimiento de los Xyletininae (Col. Anobiidae) del Gabón (Mision H. Coiffait, 1963). Biologia Gabonica, 8(2): 175–189. – 1982. Sobre algunos Anobiidae (Col.) del Museo Real del Africa Central, Tervuren (Nota 97). Publicaciones del Departamento de Zoología, 8:

Viñolas & Masó

65–72. – 1990. Contribución al conocimiento de los Anobiidae (Coleoptera) del Africa Austral; 2ª nota: la sección Petalium. Elytron, 4: 111–124. – 1992a. Contribución al conocimiento de los Anobiidae del África Austral (Coleoptera, Bostrychoidea). 3ª nota: sobre un nuevo género a colocar en la vecindad de Trichodesmina Español, 1982. Elytron, 5(1991): 129–133. – 1992b. Anobiidae del África Austral (Coleoptera, Bostrychoidea). 4ª nota. Nuevos datos sobre las secciones Mirosternus Sharp y Dorcatoma Herbst. Miscel·lània Zoològica, 15(1991): 121–132. – 1992c. Tres nuevos Gastrallus Jacq. du Val (Coleoptera. Anobiidae) de la fauna del África Central. Miscel·lània Zoològica, 15(1991): 133–136. – 1993. Anobiidae del África Austral (Coleoptera, Bostrychoidea). 5ª nota. Primeros datos sobre la subfamilia Trycoryninae: Scottanobium africanum gen. n., sp. n. Miscel·lània Zoològica, 16(1992): 61–72. Español, F. & Blas, M., 1992. Contribución al conocimiento de los Anobiidae del África Austral (Coleoptera: Bostrychoidea). 6ª nota: A propósito de las subfamilias Ernobiinae y Ptilininae. Elytron, 5(1991): 331–336. Español, F. & Comas, J., 1992. Contribución al conocimiento de los Anobiidae del África austral (Coleoptera: Bostrychoidea). Primera nota. Elytron suppl., 5(1)(1991): 15–38. Español, F. & Viñolas, A., 1995a. Tres nuevos Anobiidae micetófagos de Zululand, República de Sudáfrica (Coleoptera). Miscel·lània Zoològica, 17(1993–1994): 153–158. – 1995b. Anobiidae del África Austral (Coleoptera, Bostrychoidea). 9ª nota. Subfamilia Trycoryninae, géneros Mesocoelopus Jacquelin du Val, 1860, Mesothes Mulsant & Rey, 1864 y Rhamna Peyerimhoff, 1912. Miscel·lània Zoològica, 17(1993–1994): 159–172. – 1995c. Dryophilastes crassipunctatus gen. n., sp. n. de Dryophilinae LeConte, 1861, de la República de Sudáfrica, con revisión y clave genérica de la subfamilia (Coleoptera: Anobiidae). Boletín de la Asociación Española de Entomología, 19(3–4): 23–33. – 1996. Género y especies nuevas de Anobiidae del África tropical (Coleoptera). Miscel·lània Zoològica, 19(1): 75–98. LeConte, J. L., 1861. Classification of the Coleoptera of North America. Prepared for the Smithsonian Institution. Part 1. Smithsonian Miscellaneous Collection, 3: 1–208. Pic, M., 1903. Coléoptères exotiques nouveaux. L’Echange, 19, 218: 106–107. Say, T., 1825. Descriptions of new species of coleopterous insects inhabiting the United States. Journal of the Academy of Natural Sciences of Philadelphia, 5(1): 160–204.

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Un método para cuantificar las contribuciones de los colaboradores en las publicaciones científicas S. Guallar

Guallar, S., 2007. Un método para cuantificar las contribuciones de los colaboradores en las publicaciones científicas. Animal Biodiversity and Conservation, 30.1: 71–81. Abstract A method for quantifying collaborators’ contributions in scientific publications.— Authorship has become a hot topic in the past decades, especially in the field of biomedical sciences. Concern about this issue is increasing in other sciences as well, due to the importance of authorship for scientific careers and funding. I propose a method to quantify collaborators’ relative contributions to scientific publications, from which contributorship (collaborators who sign the publication and their order of appearance) can be established. This method begins with an initial agreement among collaborators based on principles of distribution of credit and weighting contributions to the design, data gathering, analysis, interpretation, writing and administration phases involved in scientific publication. Standardized application of this method with tables showing the percentage of each collaborators’ involvement would contribute to the assessment of scientists’ productivity and the construction of citation indexes Editorials, indexing services, university departments and laboratories should coordinate policies for the attainment of standardized, unified criteria. Key words: Contributorship, Authorship, Scientific contributions quantification, Quantification method, Scientific publications. Resumen Proceso de evaluación y método para cuantificar las contribuciones de los colaboradores en las publicaciones científicas.— El tema de la autoría en las publicaciones científicas se ha convertido en un problema en las últimas décadas, especialmente en las ciencias de la salud; no obstante, ha empezado también a serlo en otras ciencias debido a la importancia que se otorga a las autorías en las carreras científicas y en las obtención de fondos. Se propone un método para cuantificar las contribuciones que abandona la figura tradicional del autor y emplea la del colaborador. Este método se inicia con un acuerdo inicial sujeto a una revisión final y se basa en los principios de reparto del crédito entre los colaboradores y la ponderación de sus respectivas participaciones en las diversas fases que implica una publicación científica (diseño, toma de datos, análisis, interpretación, redacción, etc). Tanto para el cálculo de la producción de los científicos como para el de los índices de citación, sería de gran utilidad que junto a la lista de colaboradores se adjuntara una tabla con el porcentaje de sus contribuciones al trabajo de investigación. Editoriales, servicios de indexado, departamentos universitarios y laboratorios deberían coordinar sus políticas con el fin de unificar y estandarizar criterios. Palabras clave: Contribución, Autoría, Cuantificación de las contribuciones científicas, Método de cuantificación, Publicaciones científicas. (Received: 28 VIII 06; Conditional acceptance: 28 XI 06; Final acceptance: 28 II 07) Santiago Guallar, Depto. de Biología Animal, Fac. de Biología, Univ. de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Espanya (Spain).

ISSN: 1578–665X

Las autorías El tema de la determinación de los autores en las publicaciones de trabajos científicos continúa siendo insuficientemente conocido entre los investigadores en general (Hoen et al., 1998; Pignatelli et al., 2005). En España su difusión es escasa, reciente y restringida al ámbito biomédico (Arranz, 2003; Pérez–Hoyos & Plasència, 2003; Pulido, 2004). Con el presente escrito se quiere presentar este tema de carácter ético, laboral y social (Santana, 1990; Wilcox, 1998; Arranz, 2003) a la consideración de los ecólogos y biólogos de la conservación. Aunque la aparición de las colaboraciones científicas está ligada a la profesionalización de la ciencia hacia principios del siglo XIX (Beaver & Rosen, 1978), el fenómeno de las coautorías múltiples (más de dos autores) en las publicaciones científicas data de apenas unas décadas. Tradicionalmente los trabajos de investigación eran firmados por un único autor, pero el incremento tanto en el número de científicos como en la complejidad de los trabajos de investigación parece haber detonado la proliferación de artículos científicos con múltiples coautores (Drenth, 1998). Aunque en las ciencias de la salud ha llegado a extremos hiperbólicos (McDonald, 1995; Regalado, 1995), como los 2000 autores de un estudio sobre supervivencia tras un infarto (ISIS–4, 1995), la tendencia es generalizada (Endersbyi, 1996; Bird, 1997; Slafer, 2004). Sin embargo, esta inflación no es básicamente debida al aumento de trabajos de colaboración o interdisciplinarios (Benson, 1991; Epstein, 1993; Kahn et al., 1999; Slafer, 2004) sino al sistema de valoración de la producción de los investigadores que se basa en su número de publicaciones. Este es el principal parámetro, la moneda de cambio que se usa para, entre otros beneficios personales, obtener promociones académicas y recursos financieros para llevar a cabo proyectos de investigación (Rennie & Flanagin, 1994; Cronin, 1996). Este sistema da lugar a abusos flagrantes como en el caso de Yury Struchkov que publicó ¡un artículo cada 3,9 días durante 10 años! (Anderson, 1992). El número de querellas sobre coautorías ha aumentado con el paso del tiempo (Wilcox, 1998) y se sigue debatiendo sobre la aplicación de los criterios que se han de emplear para determinarlas (Kassirer, 1995; Rennie, 2001; Cronenwett & Seeger, 2005; Fizpatrick, 2005). Organizaciones como el Institut for the Health Policy Studies, el Commitee on Publication Ethics y la American Medical Association han promovido la implantación de sistemas con el fin de evitar el fraude en las publicaciones científicas y establecer normas que determinen quién ha de firmarlas y en qué orden (White, 2004; JAMA, 2005). A mediados de los años 80 del siglo pasado un grupo de editores de revistas biomédicas (el grupo de Vancouver) instituyó el International Commitee of Medical Journal Editors y redactó un manuscrito donde marcaban las directrices éticas y editoriales para poder publicar trabajos de investigación en ellas. Este docu-

Guallar

mento ha sido actualizado en sucesivas ocasiones, la última de las cuales (ICMJE, 2005) recomienda tres criterios para que un investigador que haya participado en un trabajo de investigación conste como coautor en una publicación: 1. Contribución sustancial en la concepción y diseño o en la adquisición de datos o en su análisis e interpretación; 2. Redacción del artículo o revisión crítica de su contenido; 3. Aprobación final del artículo a publicar. También explicita que la adquisición de fondos, la recogida de datos o la supervisión general del grupo de investigación por sí mismos no justifican la coautoría, y que cada coautor tiene que haber participado suficientemente en el trabajo para tomar responsabilidad pública de su contenido, o por lo menos de la parte de la que se encargó. Más de 500 publicaciones dedicadas a la difusión de trabajos de investigación en las ciencias de la salud han adoptado estas recomendaciones como criterios para establecer las coautorías, a pesar de lo cual, gran parte de los investigadores piensa que es difícil reunir los criterios y muchos de los autores aún no lo hacen (Van Rooyen et al., 2001). Las autorías fantasma y de regalo continúan siendo muy frecuentes (Rennie & Flanagin, 1994; Rennie et al., 1997; Flanagin et al., 1998; Mowatt et al., 2002; Pignatelli et al., 2005), incluso la publicación repetida de un mismo trabajo y el fraude (Marshall, 1996; Al–Marzouki et al., 2005). Factores y actores que intervienen en el proceso de publicación de los trabajos científicos. Algunas soluciones propuestas Horton & Smith (1996) ya llamaron la atención sobre la necesidad de cambiar las prácticas y concepciones sobre autorías y organizaron una conferencia en Nothingham, Inglaterra, en junio de 1996, de la cual nacieron ideas e iniciativas para adaptar aquéllas a la realidad actual (Scott & Smith, 1996; Smith, 1997). Meses después, Rennie et al. (1997) hicieron la revisión más completa de la problemática asociada a la publicación y acreditación de las contribuciones en los trabajos científicos. No solamente hicieron una presentación concisa y clara de los elementos que están implicados, también hicieron una propuesta innovadora y sensata para resolver los problemas que surgen en las diferentes etapas del proceso. Este epígrafe hace eco de sus ideas y propuestas (véase Cronin, 2001 para una revisión crítica). La responsabilidad de lo que se publica es la otra cara de la moneda de la publicación. Con el actual sistema de autorías la responsabilidad se diluye y puede ser eludida alegando desconocimiento de lo que han hecho los otros coautores. La única manera de resolver esto es hacer público quién ha hecho qué y, a ser posible, cuánto en cada publicación. El orden en que aparecen los autores está lejos de ser consistente y los criterios empleados para determinarlo continúan siendo muy variables: jerárquicos, alfabéticos, aleatorios o fijados median-

Animal Biodiversity and Conservation 30.1 (2007)

te reglas tácitas (por ejemplo, el estadístico siempre es segundo autor, el jefe del equipo ocupa el último por aquello de que la "nobleza obliga", etc.). El punto en común entre todos estos sistemas es que sus criterios no se hacen públicos en el momento de la publicación y, lógicamente, su diversidad hace imposible compararlos; además, su vaguedad deja abierta la puerta a prácticas no éticas. Algunos editores ayudaron a mejorar este problema comenzando a establecer criterios para las autorías y obligando a los coautores a tomar responsabilidad por escrito de lo que publicaban (Huth, 1986). Sin embargo, no es esta la solución al problema, puesto que el propio concepto de autoría es el que falla: el modelo de autor tradicional no encaja en la práctica actual de la investigación científica en la cual intervienen múltiples investigadores (Shapiro et al., 1994; Eastwood et al., 1996; Scott & Smith, 1996). Como Van Rooyen et al. (2001) suscriben, la realidad actual queda mejor reflejada asumiendo que la responsabilidad ha de ser dividida entre los múltiples colaboradores de un proyecto, en el que cada uno se responsabiliza solamente de ciertas partes del mismo, aunque se produzca solapamiento entre las contribuciones realizadas, como suele ser el caso habitual. Pero la responsabilidad no solo ha de ser asumida de forma parcial entre los colaboradores, también ha de haber uno o más investigadores que den garantía por el todo. En este escenario las figuras del colaborador, del firmante y del garante son más apropiadas que la del coautor. Colaborador será cualquier investigador que haya hecho una contribución al trabajo de investigación. Firmante será cualquier colaborador que alcance el porcentaje de contribución mínimo (ver siguiente apartado) y sea, consecuentemente, nombrado en la línea de encabezamiento bajo el título de la obra; en casos como los de trabajos con colaboradores multitudinarios, cada uno de los cuales ha hecho una contribución muy pequeña, el firmante o firmantes serán exclusivamente los garantes. Garante será todo colaborador que pueda tomar plena responsabilidad de lo que se publica porque puede responder sobre el contenido de la totalidad del proyecto. En el resto del artículo se adopta esta concepción y su terminología asociada. Como ha quedado antes apuntado, el punto clave de todo el sistema es que los colaboradores hagan público en qué actividades de la investigación han estado implicados y cuantificar su contribución para establecer su orden de citación. Esto puede llevarse a cabo, por ejemplo en el caso de los artículos, añadiendo una nota en el pie de la primera o última páginas donde se muestre una tabla (como la tabla 4) con el desglose de las contribuciones finales de cada colaborador por actividad (ver siguiente apartado) pero agrupando todos los no firmantes. Aunque Rennie et al. (1997) consideran que la cuantificación es útil para determinar el orden de los colaboradores, opinan que su publicación es innecesaria y que solamente debería aparecer la descripción de las actividades obje-

to de su contribución. Lo cierto es que la presentación de esta información en una tabla ahorraría espacio y descripciones farragosas (como las que se presentan en su propio artículo), pero lo más interesante es que permitiría establecer de forma directa el peso de cada firmante en la publicación, con las consecuencias que esto tendría para el otorgamiento del crédito real, y para calcular la producción en la carrera de los investigadores. Por ejemplo, evitaría fijar de manera arbitraria los coeficientes de reparto y la fracción del crédito total en la fórmula de Trueba & Guerrero (2004). En este sentido se han realizado avances. La American Medical Association (JAMA, 2005), el British Medical Journal (BMJ, 2005), el Commitee on Publication Ethics (White, 2004), entre otras prestigiosas instituciones, han redactado directrices para todos los autores en las que se requiere la firma de una declaración sobre sus contribuciones, transferencia de copyright y la procedencia de los fondos de financiación (muy importante en el caso de los ensayos clínicos de fármacos). Los criterios editoriales y los de los propios investigadores deberían de converger (Bhopal et al., 1997). Aunque muchas ya lo han hecho, todas las editoriales tendrían que establecer un número máximo de firmantes en una publicación mediante la definición de la contribución mínima, de manera que aquellos colaboradores que no lo alcanzaran solo aparecerían en la sección de agradecimientos. De cualquier forma, los porcentajes de sus contribuciones no deberían ser repartidos entre los firmantes, las contribuciones de los cuales no variarían. La contribución mínima tendría que estar próxima al 10% y el número máximo de firmantes en las publicaciones tendría que estar en torno a los 8 (esta cifra se deduce del método de puntuación propuesto más adelante). La definición apriorística de la contribución mínima tiene la virtud de definir quien consta como firmante y eliminar las fórmulas para su determinación cuantitativa. Pero investigadores y editoriales no son los únicos actores en el proceso de publicación de trabajos de investigación, los organismos que indexan los artículos y autores calculando el número de citaciones que reciben (Science Citation Index, National Library of Medicine, etc.) también juegan un papel destacado porque el número máximo de firmantes en las publicaciones debería coincidir con el número máximo que estos servicios citan. Los elementos del trabajo de investigación Según Dickson et al. (1978) los trabajos científicos están divididos básicamente en cinco bloques o áreas de actividad: concepción, diseño, ejecución, análisis e interpretación de datos, y preparación del manuscrito. A este esquema se debería añadir un sexto bloque que engloba las actividades de tipo logístico y administrativo sin las cuales pocos proyectos podrían realizarse con éxito. Una descripción de las áreas de actividad es la siguiente: 1. La

concepción o planteamiento engloba la idea original y exploración de las respuestas que puede aportar el estudio, así como la determinación para emprender el proyecto y la asunción de la iniciativa; 2. El diseño comprende la redacción del proyecto, la determinación de los tamaños de muestra, la selección de la metodología a emplear, el cálculo presupuestario y otras tareas preparatorias; 3. La ejecución se halla integrada por la recogida de datos de campo y/o laboratorio; 4. El análisis e interpretación de datos es la aplicación de tratamientos matemáticos, estadísticos y gráficos y la interpretación y discusión de los resultados que se obtienen; 5. La preparación del manuscrito consta no solo de su redacción sino también de la revisión y seguimiento del proceso de corrección para la imprenta o de la correspondencia con revisores en revistas, y, normalmente, es responsabilidad del primer autor; 6. Las tareas logístico– administrativas comprenden la búsqueda de financiamiento y otras como la contratación de personal, la gestión de permisos y la obtención de equipamiento en general. Los bloques 1, 2, 4 y 5 constituyen el núcleo intelectual de la contribución científica. El bloque 6 per se no debería otorgar crédito porque no constituye ninguna contribución científica como tal. El personal administrativo, el de búsqueda de recursos financieros o el de mantenimiento no realizan contribuciones científicas (Altmann, 1994, 1995). El bloque 3 incluye desde actividades que entran dentro del ejercicio laboral habitual de colaboradores que no se involucran en el proyecto de investigación y que solo aportan mano de obra hasta faenas muy especializadas que exigen observar, interpretar y reajustar esquemas y procedimientos sobre la marcha. La recogida de datos que llevan a cabo técnicos de campo y de laboratorio tendría que ser ponderada de acuerdo a su dificultad y su grado de integración en el estudio, de manera que la lectura de controles que hacen los operarios de máquinas o la extracción de sangre que llevan a cabo las enfermeras, por poner algunos ejemplos, deberían tener un peso muy bajo en relación al resto de bloques. Así pues, la ponderación de los diferentes bloques depende de la importancia relativa que los colaboradores les concedan, teniendo presente que la dificultad y el mérito de los trabajos de investigación radica principalmente en las aportaciones de carácter intelectual y creativo. Este esquema general se tendría que adaptar a cada caso teniendo en cuenta que hay proyectos en los que uno o más de estos bloques tiende a ser nulo y que hay otros en que las actividades implicadas se tendrían que dividir aún en más bloques (hasta el punto de detallar cada tarea si se considera oportuno). Por ejemplo, en las publicaciones compilatorias el trabajo de campo es nulo, en los encargos que realizan las editoriales el planteamiento y concepción puede ser casi nulo por parte de los firmantes del trabajo final, muchos artículos que se publican como subproductos no planificados al inicio de un proyecto y, por tanto, su diseño es nulo, etc.

Guallar

Método de cuantificación propuesto La determinación de los firmantes y la secuencia en que aparecen en las publicaciones debería basarse en las contribuciones efectivas de cada investigador en cada faceta de la investigación, no solo por motivos de reconocimiento del esfuerzo invertido, sino también para mantener la buena relación entre las partes. La mayoría de los escritos sobre este tema (Dickson et al., 1978; Altmann, 1995; Kassirer, 1995; Galindo–Leal, 1996; ICMJE, 2005) coinciden en que todos ellos deberían hacer una contribución sustancial en la redacción, cuando menos una revisión de la misma, y en una área adicional del trabajo de investigación; sin embargo, no existe un consenso (Culliton, 1988; Anderson, 1992). Todo colaborador la participación del cual no alcanzara el mínimo tendría que ser únicamente reconocido en el apartado de agradecimientos en el caso de los artículos o como asistente a la edición, por ejemplo, en el caso de la edición de un libro; es decir, no deberían constar como firmantes. En el caso de que quienes aparecieran en la sección de agradecimientos fueran poco numerosos y de que sus contribuciones fueran sustanciales, los porcentajes de las mismas podrían acompañar a la descripción de las tareas por ellos ejercidas. Entre muchos otros, Kassirer & Angell (1991) han planteado esta cuestión concomitante de los agradecimientos. No reconocer como firmantes a colaboradores que han realizado contribuciones pequeñas pero importantes puede reducir su disposición a continuar donando su trabajo en el futuro. Propuestas como la de Cronin & Weaver–Wozniak (1993) para otorgar un reconocimiento adecuado a las "subautorías" mediante la creación de un índice de agradecidos paralelo al Science Citation Index podrían mejorar esta situación pero de compleja resolución práctica (Giles & Councill, 2004). Los acuerdos sobre la puntuación de las contribuciones individuales han de ser tomados al comienzo del proyecto o en sus etapas iniciales (Riesenberg & Lundberg, 1990), una vez se aclara el compromiso que puede asumir cada uno de los investigadores implicados. Se pueden dar numerosas circunstancias durante la gestación de los trabajos de investigación que obliguen a alterar este esquema inicial, entre los cuales se pueden citar el abandono del proyecto y la entrada de nuevos investigadores. De acuerdo con Galindo–Leal (1996) debería tratarse de un proceso en dos etapas: 1. Las partes han de llegar a un acuerdo escrito en el que se describan sus roles y responsabilidades, incluyendo los porcentajes de contribución esperados y los coeficientes de ponderación mediante la tabla de acuerdo inicial (tabla 2); en muchos casos esto se hará cuando ya se ha pasado la fase de concepción y se sabe quienes son los colaboradores definitivos; los baremos de puntuación de las contribuciones y compromisos habrían de ser revisados periódicamente o, por lo menos, cuando se produjeran modificaciones a lo largo de la ejecución del proyecto; 2. Al finalizar la investigación las

Animal Biodiversity and Conservation 30.1 (2007)

partes deberían revisar el acuerdo para valorar los porcentajes de contribución efectivos y modificar, si hace falta, los coeficientes de ponderación para lograr el acercamiento más realista posible a la relevancia de cada bloque y al esfuerzo invertido por cada colaborador; esto queda reflejado en la tabla de valoración final (tablas 1, 3). La ponderación de las contribuciones y la determinación de cuál es la mínima puntuación necesaria para constar como firmante en una publicación en el caso de que haya más de dos colaboradores se complica, sobre todo si las disciplinas involucradas en el estudio son varias, con colaboradores independientes en cada una de ellas. Para cada tipo de estudio cada bloque debería puntuarse siguiendo diferentes baremos de forma que se otorgara un peso adecuado a cada uno. En el caso hipotético en que la recogida de datos o trabajo de campo constituyesen una parte más importante que el diseño del proyecto en sí se debería conceder más peso al primero que al último. En el caso de proyectos interdisciplinarios la contribución del representante de cada disciplina será imprescindible y los pesos de sus contribuciones deberían de ser iguales, aunque, también, haría falta evaluar sus participaciones. Lógicamente, la subjetividad es un elemento inevitable y la flexibilidad en el momento de reconocer el grado de participación entre los colaboradores es esencial para alcanzar el beneplácito entre estos. Se discutirá la influencia sobre la evaluación de las contribuciones una vez expuesto el método. Este, aunque desarrollado de forma independiente, concuerda con la línea ya propuesta por otros autores. Su principal aportación consiste en adecuarse al marco conceptual expuesto sobre las colaboraciones científicas. Los principios en que se basa son: 1. Reparto, el crédito total otorgado ha de ser repartido entre todos los colaboradores; 2. Ponderación, el crédito se reparte entre los colaboradores en proporción aritmética a sus contribuciones. Como se ha apuntado anteriormente, el proceso comienza con la redacción de un acuerdo inicial. El resultado se condensa en la tabla de acuerdo inicial (tabla 2). Al terminar, se han de reevaluar las contribuciones realizadas por cada colaborador. Esto queda reflejado en la tabla de valoración final (tablas 1, 3). Ambas tablas forman matrices de porcentajes cuyas filas y columnas han de sumar 100. Los coeficientes de ponderación (Ci), que varían entre 0 y 1, constituyen otra matriz con igual número de columnas. La puntuación final del colaborador j sería: Pj =

3 Xji ·

donde Xji es la puntuación en el bloque i del colaborador j. Para obtener porcentajes, la puntuación Pj se corrige según la fórmula Pj Pj =

La puntuación mínima debería ser un valor límite estandarizado en el mundo editorial. De forma tentativa se propone que contribuciones ≈ 10% otorguen crédito como firmante. La principal dificultad en el momento de evaluar la aportación de cada investigador es la falta de objetividad del proceso. La única forma de fijar el peso que se da a cada bloque es pactar los valores del esquema de puntuación a priori. Las fuentes de subjetividad son dos: 1. El valor que toman los coeficientes de ponderación de cada bloque; 2. El sistema que emplea para valorar los porcentajes finales de contribución: estimación pactada entre los colaboradores, contabilidad de horas invertidas, el volumen de trabajo aportado, etc. Tanto el coeficiente de ponderación como los porcentajes de contribución contienen en gran medida apreciaciones personales Además, cada colaborador es más consciente de su propio esfuerzo que del ajeno. Una forma de limitar la subjetividad en la valoración de las contribuciones es contabilizar las horas invertidas o el volumen de trabajo realizado. Si se emplean las horas será difícil estandarizar el trabajo realizado porque, por razones muy diversas (experiencia, conocimientos, tipo de tarea, etc.), el ritmo de trabajo de cada colaborador es diferente. El volumen de trabajo soluciona en parte esta complicación, pero continúa limitado por la necesidad de ponderar las actividades. Por todo esto, la definición y el acuerdo iniciales son necesarios al llegar el momento de la valoración definitiva de las aportaciones individuales. Dos problemas adicionales asociados a la determinación de los firmantes son: la decisión de incluir los colaboradores "umbral" (aquellos que quedan muy cerca de la puntuación mínima para constar como firmantes) y el orden de citación cuando los porcentajes de las contribuciones son muy similares. Aunque en el proceso definitivo de cuantificación de las contribuciones no se puede evitar que los colegas con más poder inclinen la balanza hacia su lado ni que haya desacuerdos y disputas (Rennie et al., 2000), estos problemas deberían de minimizarse con la aceptación del acuerdo inicial y de las sucesivas revisiones. La resolución de estas cuestiones radica en la buena voluntad de las partes y en la búsqueda del beneficio colectivo. Una técnica que puede ayudar a establecer el consenso es la de los quáqueros (McKearnan, 1999; Quaker Foundations of Leadership, 1999), según la cual las diferencias se resuelven mediante la discusión y no mediante el voto, evitando así las rupturas y el tomar decisiones que excluyan a algunos miembros del grupo. El cálculo de las contribuciones totales debería seguir un patrón de tipo iterativo. Se puede comenzar por los colaboradores que han tenido una menor intervención en todo el proceso y proseguir en orden ascendente; una vez se obtienen los primeros porcentajes de contribución se ajustan los Ci y las Xji hasta consensuarlos entre todos. Otra opción es lograr este consenso definiendo las contribuciones de los colaboradores en cada bloque.

Guallar

Tabla 1. Valoración final realizada para cada uno de los colaboradores del artículo a posteriori. Los colaboradores que no alcanzarían la puntuación mínima para firmar el trabajo ( < 10%) aparecen en minúsculas. Pj es la puntuación final del colaborador j ; es la puntuación corregida del colaborador j. Table 1. Final a posteriori evaluation for each of the paper collaborators. Collaborators that would not reach a minimum contribution for signing the publication ( < 10%) are shown in lower case. Pj is the final score for the collaborator j; is the final corrected score for the collaborator j.

Actividades de la investigación

Total

Planificación y concepción

100

Ejecución

Colaboradores C d e

100

Análisis

0,5

100

Interpretación

0,5

100

400

163

100%

41%

20%

13%

15%

Preparación del manuscrito Pj

Teóricamente cualquiera de los colaboradores que poseyera suficiente conocimiento del trabajo desarrollado a lo largo de todo el proyecto podría ser garante. Sin embargo, en la práctica, y aunque no necesiten haber participado en todos los bloques de actividades, para asumir responsabilidad de la integridad de lo que se publica, han de haber parti-

cipado, por lo menos, en aproximadamente un 50% de los tres bloques más importantes en el trabajo de investigación (normalmente serán los 2, 3 y 5), es decir que siempre alcanzarían puntuaciones ≥ 30% (se puede demostrar a partir de la sustitución de valores en las tablas 1 y 3). Teniendo esto en cuenta, el número máximo de garantes sería de tres

Tabla 2. Acuerdo inicial. Solo cinco colaboradores participan en el inicio del proyecto y cuatro de ellos se comprometen a realizar contribuciones sustanciales (en mayúsculas). Los colaboradores que no alcanzarían la puntuación mínima para firmar el trabajo ( < 10%) aparecen en minúsculas. Pj es la puntuación final del colaborador j; es la puntuación corregida del colaborador j. Table 2. Initial agreement. Only five collaborators participate at the beginning of the project, four of them commit to make substantial contributions (shown in upper case). Collaborators that would not reach a minimum contribution for signing the publication ( < 10%) are shown in lower case. Pj is the final score for the collaborator j; is the final corrected score for the collaborator j.

Actividades de la investigación

Total

Colaboradores C D

Diseño

100

Ejecución

100

Análisis

0,5

100

Interpretación

0,5

100

0,2

100

420

163

100%

11%

39%

Preparación del manuscrito Tareas administrativas Pj

Animal Biodiversity and Conservation 30.1 (2007)

Tabla 3. Valoración final. Se incorporan cinco colaboradores más y se decide que la trascendencia de la interpretación y del análisis de datos requiere incrementar sus coeficientes de ponderación. Se decide dar a los nuevos colaboradores la categoría de asistentes a la edición y pasar a e (un colaborador novato) delante de g (un colega de prestigio) por generosidad. En minúsculas los colaboradores no firmantes. Los colaboradores que no alcanzarían la puntuación mínima para firmar es la el trabajo ( < 10%) aparecen en minúsculas. Pj es la puntuación final del colaborador j; puntuación corregida del colaborador j. Table 3. Final evaluation. Five more collaborators join the project, and it is decided to raise the coefficients of weighting for data analysis and results due to their relevance of their interpretation. It is also decided to designate the new collaborators as editor assistants, and to place e (a novel collaborator) before g (a prestigious colleague) for reasons of generosity. Non–signatory collaborators are shown in lower case. Collaborators that would not reach a minimum contribution for signing the publication ( < 10%) are shown in lower case. Pj is the final score for the collaborator j; is the final corrected score for the collaborator j.

Actividades de la investigación

Total

Firmantes B C

Diseño

100

Ejecución

100

Análisis

100

0,75

100

0,2

100

495

174

104

100%

18%

35%

18%

21%

Interpretación Preparación del manuscrito Tareas administrativas Pj

y el número máximo teórico de firmantes en el caso de que hubiese tres garantes sería de cuatro, para dos garantes sería de cinco y en el caso de un solo garante sería de ocho. Esta última cifra debería proporcionar una guía a las editoriales para limitar el número máximo de firmantes. No obstante, la dificultad de establecer esta cifra en estudios como los ensayos clínicos aleatorizados demuestra que este es un tema muy complejo (Carbone, 1992; Cronin, 2001). Han sido varios los métodos de evaluación de las contribuciones propuestos hasta hoy, pero pocos han intentado cuantificarlas. Davis & Gregerman (1969) expusieron el suyo en clave irónica asumiendo que el reparto del crédito total entre los diferentes colaboradores había de seguir la regla del picoteo: a mayor rango jerárquico mayor crédito. Ayiomamitis (1987) propuso un sistema de puntuación corregido para repartir el crédito entre los colaboradores de una publicación en función del orden en que aparecen citados pero que no permite comparar la producción entre autores. Hunt (1991), Galindo–Leal (1996) y Ahmed et al. (1997) hicieron propuestas muy prácticas basadas en la asignación de valores tabulados para cada una de las categorías de contribuciones que consideren. No obstante, la hoja de cálculo

Resto de colaboradores f g h i

diseñada por Schmidt (1987) constituye el sistema de determinación de las contribuciones relativas y del orden en que han de aparecer los diferentes colaboradores más elaborado y es un precursor del método aquí propuesto. Ejemplo 1. Artículo que será publicado próximamente entre siete colaboradores (tabla 1) Es este un artículo que nace a propósito de un fenómeno observado durante la recogida de otro tipo de datos en el estudio de un ave en peligro de extinción. Por tanto su diseño es casi nulo. Los colaboradores, sin evaluar sus contribuciones, pactaron el siguiente orden de aparición: A, B, G, E, D, F y C. Aplicando el método propuesto, el orden de citación de los colaboradores solo sufriría un cambio: C tendría que pasar a la cuarta posición. C, como jefe del equipo, decidió ocupar la última posición por "nobleza obliga", alterando así el segundo principio en que se basa el método. Así mismo, el número de firmantes que debería aparecer variaría sustancialmente, de siete a solo cuatro, con el colaborador E cercano al umbral de citación; su inclusión debería estudiarse, aunque sería aconsejable hacer un esfuerzo de realocación de las contribuciones para comprobar si es factible.

Guallar

Tabla 4. Tabla de contribuciones a publicar. Las contribuciones de los colaboradores no firmantes se suman a la columna e. Estos colaboradores son mencionados en la sección de agradecimientos. Pj es la puntuación final del colaborador j; es la puntuación corregida del colaborador j. Table 4. Table of contributions to be published. Contributions of non signatory collaborators add up in column e. These collaborators are the acknowledgees. Pj is the final score for the collaborator j; is the final corrected score for the collaborator j.

Actividades de la investigación

Total

Firmantes B C

Diseño

100

Ejecución

100

Análisis

100

0,75

100

0,2

100

495

174

104

100%

18%

35%

18%

21%

Interpretación Preparación del manuscrito Tareas administrativas Pj

Ejemplo 2. Edición de un libro sobre zoogeografia (tablas 2, 3 y 4)

Hacia una estandarización del proceso de evaluación de la producción científica

Es este un caso en que el proyecto nace como un encargo y, por tanto, el bloque de planteamiento y concepción tiene un origen ajeno a los colaboradores finales. Por su relevancia, la interpretación de los datos se ha considerado un bloque aparte del análisis de los mismos. Al finalizar, los firmantes decidieron agradecer a ciertos colaboradores su contribución otorgándoles el título de asistentes a la edición. Resultado: según el acuerdo inicial los colaboradores habían de ser B, D, A, C (este último preliminarmente como firmante umbral) en este orden y la previsión se cumplió. Sin embargo, tras la valoración final, la contribución definitiva de cada uno varía: C traspasa el porcentaje umbral y el reparto de los créditos varía sustancialmente. Los editores asistentes deberían haber sido citados en este orden G, E, F, H y I pero los firmantes decidieron que el orden fuera E, G, F, H y I. Es interesante comprobar que el método da resultados muy semejantes a los que los propios colaboradores habían pactado sin cuantificar sus contribuciones. Esto hace pensar que, a pesar de ser solamente probado a partir de dos casos, parece acercarse a lo que sugiere el sentido común. Su utilidad radica en la determinación de los firmantes pero sobre todo en la determinación del orden de los colaboradores a partir de la cuantificación de sus contribuciones.

La transparencia, coordinación y unificación de criterios de todos los factores y actores implicados en el proceso de la producción científica es esencial para que el sistema funcione de forma apropiada y justa. La política interna de departamentos y laboratorios debería estar regulada de tal manera que no promoviera prácticas deshonestas e inapropiadas en el reconocimiento del trabajo de investigación. Una manera de lograrlo sería implantando estándares internacionales sobre evaluación de las contribuciones científicas. Sin embargo, la comercialización del trabajo científico con el surgimiento del Contract Research Organization supone una corriente muy poderosa en contra de cualquier intento de estandarización (Mirowski & Van Horn, 2005). En otro ámbito, las editoriales deberían adoptar los mismos estándares y aplicar criterios universales sobre contribuciones mínimas y declaraciones sobre la veracidad de estas. Finalmente los organismos que indexan publicaciones científicas tendrían que coordinarse con las editoriales para mantener los mismos criterios acerca del número de colaboradores citados y tener en cuenta, al calcular los índices de citación, los porcentajes de contribución que reciben los firmantes de cada publicación. Esta unificación permitiría a los comités que otorgan becas, promociones académicas y contratos disponer de parámetros más precisos (y reales) sobre los cuales basar sus decisiones. El

Animal Biodiversity and Conservation 30.1 (2007)

cambio en las prácticas de publicación tendría como consecuencias directas un aumento de la honestidad, un reconocimiento más justo del trabajo realizado y la disminución del fraude. Los colaboradores tendrían más protección ante el abuso por parte de colegas más poderosos y los engaños y fraudes serían más difíciles de ocultar. Uno de los cambios que esto propiciaría sería el de liberar a los jefes de departamento y otros responsables que habitualmente reciben coautorías de regalo o que, por política de departamento, imponen su nombre en las publicaciones que genera el equipo de investigación bajo su cargo de la obligación de publicar (Marshall, 1996). La productividad de las personas que ocupan estos puestos de responsabilidad debería medirse por el número de publicaciones y de citaciones que genera su equipo y no por las suyas propias. Los congresos internacionales sobre "peer review" (revisión por colegas expertos) en las publicaciones biomédicas sirven para tomar el pulso a temas como autoría versus contribución, proceso de revisión por colegas, políticas editoriales, criterios de transparencia para los investigadores que publican, ética científica, propiedad intelectual, sistemas de citación, factores de impacto, sesgos en las publicaciones en función de la esponsorización y regulación de las prácticas editoriales (Kaandorp, 2002). A pesar de que muchos artículos se hacen eco de la reunión de Nottingham, todavía se continúa trabajando en el marco conceptual de la autoría (Bates et al., 2004; Hren et al., 2005). Las ramificaciones (Blumenthal et al., 1997; Bodenheimer, 2000; Smith, 2001), la complejidad y la magnitud de una empresa como esta son demasiado grandes para ser optimistas sobre los avances que puedan lograrse en un futuro a corto y medio plazo. Agradecimientos Sergi Herrando, Gerard Bota y Gabriel Gargallo ayudaron con sus comentarios a mejorar este trabajo. Sara Blanquer colaboró en la búsqueda bibliográfica. Referencias Ahmed, S. M., Maurana, C. A., Engle, J. A., Uddin, D. E. & Glaus, K. D., 1997. A method for assigning authorship in multiauthored publications. Family Medicine, 29: 42–44. Al–Marzouki, S., Evans, S., Marshall, T. & Roberts, I., 2005. Are these data real? Statistical methods for the detection of data fabrication on clinical trials. BMJ, 331: 267–270. Altmann, S., 1994. The problem of multiple authorship. Anim. Behav. Soc. Newsletter, 39: 5–6. – 1995. On authorship and intellectual property. Anim. Behav. Soc. Newsletter, 41(1): 4–7.

Anderson, C., 1992. Writer’s cramp. Nature, 355: 101. Arranz, M., 2003. Ni son todos los que están, ni están todos los que son. Algunas consideraciones sobre la autoría de los autores. Rev. Calidad Asistencial, 19(1): 1–2. Ayiomamitis, A., 1987. Multiple authorship: a mathematical sanctuary. Can. Med. Assoc. J., 137: 1077–1078. Bates, T., Anić, A., Marušić, M. & Marušić, A., 2004. Authorship criteria and disclosure of contributions. Comparison of 3 general medical journals with different author contribution forms. JAMA, 291(1): 86–88. Beaver, D. B. & Rosen, R., 1978. Studies in scientific collaboration. Part I: the professional origins of scientific coauthorship. Scientometrics, 1: 65–84. Benson, K. R., 1991. Science and the single author: historical reflections on the problem of authorship. Cancer Bull., 43: 324–330. Bhopal, R. S., Rankin, J. M., Mccoll, E., Thomas, L., Kaner, E., Stacy, R., Pearson, P., Vernon, B. & Rodgers, H., 1997. The vex question of authorship: views of researchers in a British medical faculty. BMJ, 314: 1009–1010. Bird, J. E., 1997. Authorship patterns in marine mammal science, 1985–1995. Scientometrics, 39: 19–27. Blumenthal, D., Campbell, E. G., Anderson, M. S., Causino, N. & Louis, K. S., 1997. Withholding research results in academic life science. JAMA, 277: 1224–1228. Bodenheimer, T., 2000. Uneasy alliance–clinical investigators and the pharmaceutical industry. N. Engl. J. Med., 342: 1284–1286 BMJ, 2005. Submitting articles to the journal [editorial]. [Consultado el 18/11/05]. Disponible en: http:// bmj.bmjjournals.com/advice/article submission.shtml Carbone, P. P., 1992. On authorship and acknowledgments. N. Engl. J. Med., 326(16): 1084. Cronenwett, J. L. & Seeger, J. M., 2005. Criteria for authorship. J. Vascular Surgery, 42(4): 599. Cronin, B., 1996. Rates of return to citation. J. Documentation, 52: 188–197. – 2001. Hyperauthorship: a postmodern perversion or evidence of a structural shift in scholarly communication practices? J. Amer. Soc. Information Science and Technology, 52(7): 558–569. Cronin, B. & Weaver–Wozniak, S., 1993. Online access to acknowledgements. In: Proceedings of the 14th International Online Meeting 1993, New Jersey, May 4–6: 93–97 (M. E. Wiliams, Ed.). Learned Information, Inc., New York. Culliton, B. J., 1988. Authorship, data ownership examined. Science, 242: 658. Davis, P. J. & Gregerman, R. I., 1969. Parse analysis: a new method for the evaluation of the investigators’ bibliographies. N. Engl. J. Med., 281: 989–990. Dickson, J. D., Conner, R. N. & Adair, K. T., 1978. Guidelines for authorship of scientific articles. Wildl. Soc. Bull., 6(4): 260–261.

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Guallar

cal publication: Fourth International Congress, 14–16 September 2001, Barcelona. Science Editor, 25(2): 44–45. Kahn, K. S., Nwosu, C. R., Kahn, S. F., Dwarakanath, L. S. & Chien, P. F. W., 1999. A controlled analysis of authorship trends over two decades. Am. J. Obstetrics and Gynecology, 181: 503–507. Kassirer, J. P., 1995. Authorship criteria. Science, 268: 785–786. Kassirer, J. P. & Angell, M., 1991. On authorship and acknowledgments. N. Engl. J. Med., 325(21): 1510–1512. Marshall, E., 1996. Fraud strikes top genome lab. Science, 274: 908–910. Mcdonald, K. A., 1995. Too many co–authors? Chronicle of Higher Education, 28: A35–A36. Mckearnen, S., 1999. The consensus building handbook. Consensus Building Institute, Richmond. Mirowski, P. & Van Horn, R., 2005. The contract research organization and the commercialization of scientific research. Social Studies of Science, 35(4): 503–548. Mowatt, G., Shirran, L., Grimshaw, J. M., Rennie, D., Flanagin, A., Yank, V., Maclennan, G., Gøtzsche, P. C. & Bero, L. A., 2002. Prevalence of honorary and ghost authorship in Cochrane reviews. JAMA, 287(21): 2769–2771. Pérez–Hoyos, S. & Plasència, A., 2003. Aspectos éticos en la publicación de manuscritos en revistas de salud médica. Gac. Sanit., 17(4): 266–267. Pulido, M., 2004. Nueva revisión de los requisitos de uniformidad para los manuscritos enviados a revistas biomédicas: ¡atención a la ética! Med. Clin. (Bar), 122(17): 661–663. Pignatelli, B., Maisonneuve, H. & Chapuis, F., 2005. Authorship ignorance: views of researchers in French clinical settings. J. Medical Ethics, 31(10): 578–581. Quaker foundations of Leadership, 1999. A Comparison of Quaker–based Consensus and Robert’s Rules of Order. Earlham College, Richmond. Regalado, A., 1995. Multiauthor papers on the rise. Science, 268: 25. Rennie, D., 2001. Who did what? Authorship and contribution in 2001. Muscle and Nerve, 24: 1274–1277. Rennie, D. & Flanagin, A., 1994. Authorship! Authorship! Ghosts, guests and grafters, and the two–sided coin. JAMA, 271: 469–471. Rennie, D., Yank, V. & Emanuel, L., 1997. When authorship fails. A proposal to make contributors accountable. JAMA, 278(7): 579–585. – 2000. The contributions of authors. JAMA, 284(1): 89–91. Riesenberg, D. & Lundberg, G. D., 1990. The order of authorship: who’s on first? JAMA, 264: 1857. Santana, E., 1990. Consideraciones éticas sobre la determinación de autores y el otorgamiento de

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Trueba, F. J. & Guerrero, H., 2004. A robust formula to credit authors for their publications. Scientometrics, 60(2): 181–204. Van Rooyen, S., Goldbeck–Wood, S. & Goodle, F., 2001. What makes an author? A comparison between what authors say, they did and what editorial guidelines require. Fourth International Congress on Peer Review in Medical Publication. Barcelona, September 2001 [consultado el 16/11/05]. Disponible en: http://www.ama-assn.org/public/ peer/prc_program2001.htm. White, C., 2004. The COPE Report 2003. Annual Report of the Committee on Publication Ethics. BMJ Books, London. Wilcox, L. J., 1998. Authorship. The coin of the realm, the source of complaints. JAMA, 280(3): 216–217.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 30.1 (2007)

Convergences and divergences between two European mountain dung beetle assemblages (Coleoptera, Scarabaeoidea) J. M. Lobo, B. Guéorguiev & E. Chehlarov

Lobo, J. M., Guéorguiev, B. & Chehlarov, E., 2007. Convergences and divergences between two European mountain dung beetle assemblages (Coleoptera, Scarabaeoidea). Animal Biodiversity and Conservation, 30.1: 83–96. Abstract Convergences and divergences between two European mountain dung beetle assemblages (Coleoptera, Scarabaeoidea).— We analyzed the altitudinal change in dung beetle species richness and the relative proportion of higher taxa, as well as the turnover in the type of distribution and range size of species in two mountain chains located at the two extremes of Europe (Western Rhodopes Mountains and the Iberian Central System). Both mountain ranges showed a clear substitution among higher taxa (Aphodiinae–Geotrupinae vs. Scarabaeidae) and species richness variation with the altitude was similar. We suggest that East European dung beetle assemblages are conditioned by a horizontal colonization process in which mountains had been reached in relatively recent geological time by elements coming from different latitudes. In spite of these convergences, Rhodopes dung beetle assemblages are characterized by a significantly lower proportion of narrowly distributed species and a lower relevance of Aphodiinae species in lowland places. Although these divergences can be partially attributed to the dissimilar sampling effort accomplished in both regions, we suggest that the low number on narrowly distributed species could be due to the different role of these two mountain zones as refuges during glaciar–interglaciar Pleistocene cycles. Key words: Scarabaeoidea, Dung beetles, Altitudinal variation, Rhodopes mountain range, Iberian Central System, Refuges. Resumen Convergencias y divergencias entre dos comunidades coprófagas de montaña europeas (Coleoptera, Scarabaeoidea).— Compilando toda la información faunística disponible sobre los coleópteros coprófagos de dos zonas montañosas desconectadas, ubicadas a ambos extremos de Europa (los Rhodopes Occidentales y el Sistema Central Ibérico), hemos analizado el cambio altitudinal en la riqueza de especies, la modificación en la proporción relativa de los principales grupos taxonómicos implicados, así como el relevo en el tipo de distribución y el tamaño del rango geográfico de las especies implicadas. Ambas zonas de montaña muestran un patrón evidente de sustitución entre taxones de alto rango (Aphodiinae–Geotrupinae vs. Scarabaeidae) y también parecidas tasas de variación en la riqueza de especies con la altura. Sugerimos que las comunidades coprófagas del este de Europa están también condicionadas primordialmente por un proceso de colonización horizontal, en el cual las montañas serían colonizadas en periodos geológicos recientes por elementos procedentes de latitudes septentrionales. A pesar de estas convergencias, las comunidades de los Rhodopes se caracterizan por una significativa menor presencia de especies con rangos de distribución restringidos y una escasa relevancia de las especies de Aphodiinae en las zonas de menor altitud. Aunque estas divergencias pueden atribuirse parcialmente a diferencias en el esfuerzo de colecta realizado en ambas regiones, consideramos el escaso número de especies con distribución restringida estaría relacionado con el distinto papel ejercido por estas montañas como refugio durante los ciclos glaciares del Pleistoceno. Palabras clave: Scarabaeoidea, Escarabajos coprófagos, Variación altitudinal, Rhodopes, Sistema Ibérico Central, Refugios. (Received: 16 X 06; Conditional acceptance: 23 I 07; Final acceptance: 9 III 07) Jorge M. Lobo, Depto. de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, C.S.I.C., Madrid, Spain.– Borislav Guéorguiev, National Museum of Natural History, BAS, Blvd. Tzar Osvoboditel 1, 1000 Sofia, Bulgaria.– Evgeni Chehlarov, Inst. of Zoology, BAS, Blvd. Tzar Osvoboditel 1, 1000 Sofia, Bulgaria. Corresponding author: J. M. Lobo. E–mail: mcnj117@mncn.csic.es

ISSN: 1578–665X

Introduction Altitudinal variations in species richness and faunistic composition are unavoidably related with the environmental gradients provided by differences in elevation. However, it is currently widely accepted that historical factors such as recent Pleistocene climatic cycles have played an important role in the conformation of mountain assemblages (Brown, 1995; Brown & Lomolino, 1998; Hewitt, 2000; Lobo & Halffter, 2000). The relevance of these historical factors is based on the degree of isolation of mountain areas (i.e., on the accessibility for the biota of surrounding regions; Janzen, 1967; Brown & Lomolino, 1998; Channell & Lomolino, 2000). Study of elevational variation in West Palaearctic dung beetle assemblages has shown that mountain faunas are influenced by a horizontal colonization process; the geographical displacement of some taxa or ancestors in relatively recent geological times seems to have generated a clear pattern of altitudinal substitution among higher taxa with different evolutionary histories (Martín–Piera et al., 1992; Jay– Robert et al., 1997; Errouissi et al., 2004). Three dung beetle lineages are present in Palaearctic dung beetle assemblages: Scarabaeidae, Geotrupinae and Aphodiinae. Scarabaeidae are largely restricted to the southern Mediterranean part of Europe, whereas Geotrupinae and Aphodiinae dominate northern assemblages, although they are also present in south temperate localities (Hanski, 1986, 1991; Lumaret & Kirk, 1991; Hortal–Muñoz et al., 2000; Lobo et al., 2002). The latitudinal turnover between these taxa (Scarabaeidae vs. Geotrupinae–Aphodiinae) is analogous to the altitudinal gradient observed in Central and Southern European mountain ranges (Jay–Robert et al., 1997), and also in the Mexican Transition Zone (Halffter et al., 1995; Lobo & Halffter, 2000). This pattern is probably the result of the southward shift of northern lineages during Quaternary climate changes (Elias, 1994), highlighting the important role of spatial shifts in species ranges (Hengeveld, 1997) and the minor influence of adaptive evolutionary changes promoted by the isolation of populations after these colonization events (Cruzan & Templeton, 2000; Hewitt, 2000; Moritz et al., 2000). In contrast, such a turnover pattern does not appear at dung beetle assemblages of Southeastern Asia islands (Hanski, 1983; Hanski & Niemelä, 1990; Hanski & Krikken, 1991), at the Andean communities of South America (Escobar et al., 2005), or even at the southernmost mountain assemblages of the Iberian Peninsula (see Jay–Robert et al., 1997). This is probably a consequence of the isolation of these areas from northern temperate zones. Unfortunately, due to the lack of standardized studies of dung beetles at elevational gradients in Asia and East Europe we can not ascertain whether the altitudinal replacement of high level lineages with those of a different origin and evolutionary history is general for the Palaearctic region. Here, we analyzed the elevational turnover of the dung beetle assemblages located near of the eastern

Lobo et al.

border of the Euro–Mediterranean region. To do this, we compiled all the available faunistic information of a mountain range located in Eastern Europe, for the first time (Western Rhodopes mountains). We analyzed the change in species richness, the relative proportion of high level taxonomic groups, the turnover in distribution and the range size of species. Finally, we compared these results with those obtained in a Western European mountain range (the Iberian Central System) which is also located in the boundary between Mediterranean and Eurosiberian domains. Methods We studied two distant European mountain regions (separated by 4,000 km approximately): the Western Rhodopes (South–Central Bulgaria) and the Iberian Central System. The Rhodopes mountain range covers an area of around 14.000 km2 (from 200 to 2,000 m in altitude) while the area studied in the Iberian Central System covers approximately 34,000 km2 (see fig. 1) (from 500 to 2,200 m in altitude). We compiled all the faunistic information available for both regions. The information compiled for Bulgarian Rhodopes comes from 17 works, comprising the period between 1904 and 2005 (Ioakimov, 1904; Nedelkov, 1905, 1909; Stolfa, 1938; Pittioni, 1940; Goljan, 1953; Mikšić, 1957, 1959; Angelov, 1965; Zacharieva, 1965a, 1965b; Zacharieva & Dimova, 1975; Mariani, 1980; Král & Malý, 1993; Bunalski, 2001a, 2001b; Rossner, 2005). All data taken from those references refers to precise localities, except for Mariani (1980), where Aphodius montanus is cited without an exact location. In addition, we included the data from twelve localities placed along an altitudinal transect (662–2,016 m) in three seasons: 10–19 V 04; 14–21 X 04; 15–21 VII 06 (Lobo et al., in press). Five of these localities were sampled by 10 baited pitfall traps (see Lobo et al., 1988; Veiga et al., 1989) in each season, while the other seven were sampled using a standardized (and comparable) sampling effort: over a 45–minute period, three investigators (JML, BG and ECh) collected all beetles found within and beneath cattle, sheep or horse excrements. Localities were selected on the basis of the presence of cattle. The non–parametric estimates of total species richness for this study indicate that around 94% of the total regional species pool had been collected, while the mean percentage of completeness for the localities is 83% (see Lobo et al., in press). In the case of the Iberian Central System data came from several publications (Martín–Piera et al., 1986; Martín–Piera et al., 1992; Lobo, 1992; Lobo & Hortal, 2006; Hortal et al., 2006) as well as from BANDASCA, a database which originally compiled all the available biological and geographical information from museums, private collections, published and unpublished data about Iberian Scarabaeidae dung beetles (Lobo & Martín– Piera, 1991). This database has recently been updated to include a large amount of records on

Animal Biodiversity and Conservation 30.1 (2007)

<0 156 313 469 625 781 938 1094 1250 1406 1563 1719 1875 2031 2186 2344 2500+ < 150 297 444 591 738 884 1031 1178 1325 1472 1619 1766 1913 2059 2206 2353 2500+

Site 1 2 3 4 5 6 7 8 9 10 11 12

X UTM 309431 313834 306903 311760 315303 302769 299345 313655 307221 312034 302767 300119

Y UTM 4640325 4612921 4608422 4615672 4618756 4609895 4608747 4612148 4608452 4615697 4609898 4609729

2 12 11 3 10 7 6 9 8

Fig. 1. Location of the two studied mountain areas in Europe (Iberian Central System and Western Rhodopes); darkest areas represent mountain areas, and white lines are the main rivers. The continuous line in the map of Bulgaria represents the Mediterranean–Eurosiberian climate boundary. The location of sites with faunistic data in both regions is shown on a topographic map with grey tones varying in accordance to altitude. Squares in the Western Rhodopes identify recently sampled localities (Lobo et al., in press), specifically located (reference system UTM–36n) and numbered on the lower part of the figure (black areas, more than 1,500 m altitude; grey areas, 1,000–1,500 m altitude). Fig. 1. Localización general de las dos zonas de montaña estudiadas en Europa (Sistema Central Ibérico y Rhodopes Occidentales). Las áreas más oscuras correspondes a zonas montañosas, mientras que los principales ríos se muestran como líneas blancas. La línea continua en el mapa de Bulgaria representa le límite entre el clima Mediterráneo y el Eurosiberiano. Situación de las localidades con datos faunísticos dentro de un mapa topográfico en el que los tonos de gris reflejan la altitud. Los cuadrados en el mapa de los Rhodopes Occidentales identifican aquellas localidades recientemente muestreadas (Lobo et al., in press), las cuales aparecen localizadas (sistema de referencia UTM–36n) y numeradas en la parte inferior de la figura (áreas oscuras, más de 1.500 m de altitud; áreas grises, entre 1.000 y 1.500 m de altitud).

Zacharieva 1965b

Lobo et al. unpublished X

A. (Acrossus) luridus (Fabricius)

A. (Acrossus) rufipes (Linnaeus)

A. (Ammoecius) brevis Erichson

A. (Amidorus) obscurus (Fabricius)

A. (Agrilinus) scybalarius (Fabricius)

A. (Amidorus) cribrarius Brullé

A. (Agrilinus) ater (De Geer)

A. (Agoliinus) satyrus Reitter

X X

A. (Acrossus) depressus (Kugelann)

Angelov 1965

X X

Zacharieva & Dimova 1975 X

Král & Malý 1993 X

Bunalski 2001b

Bunalski 2001a

Zacharieva 1965a

Mikšić 1957

Golian 1953

Pittioni 1940

Stolfa 1938

Nedelkov 1909

Nedelkov 1905

Ioakimov 1904

Mikšić 1959 X

Rossner 2005 EA

Distribution

Aphodius (Acanthobodilus) immundus Creutzer

Species

Rs 6

700

1900

1800

1700

1600

1500

1400

1300

1200 1100

1000 900

800

600

500

400

300

200

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

2000

Tabla 1. Listado de las especies presentes en los Rhodopes occidentales de acuerdo a la literatura disponible y un reciente estudio de campo realizado en una docena de localidades (J. M. Lobo, B. Guéorguiev & E. Chehlarov, datos inéditos). El gradiente altitudinal para cada especie fue establecido asumiendo que la especie aparece en todas aquellas altitudes situadas entre la mínima y máxima altitud en que ha sido observada. El tipo de distribución se estimó de acuerdo al criterio de La Greca (1964): EU. Eurosiberiana; EA. Euroasiática; E. Europea; M. Mediterránea; CA. Centroasiática; EM. Euromediterránea; ET. Euroturanica; T. Turanica; H. Holártica. El tamaño de la distribución de cada especie (Rs) se estimó considerando seis categorías de distribución que consideran el porcentaje del área de distribución de cada especie respecto al área total del Paleártico occidental (12 x 106 km2) (ver Lumaret & Lobo, 1996). * A. (Neagolius) montanus fue citada por Mariani (1980) sin localidad específica.

Table 1. Checklist of the species present at the Western Rhodopes mountain chain according to available bibliography and a recent survey carried out in twelve localities (J. M. Lobo, B. Guéorguiev & E. Chehlarov, unpublished). The altitudinal range of each species was established assuming that the species occurs along the whole range between minimum and maximum recorded altitude. The type of distribution of each species is included according to the criteria of La Greca (1964): EU. Eurosiberian; EA. Euroasiatic; E. European; M. Mediterranean; CA. Centralasiatic; EM. Euromediterranean; ET. Euroturanian; T. Turanian; H. Holarctic. Distribution range size (Rs) was estimated taking six classes into account and considering the percentage of the total western Palaearctic region area (12 x 106 km2) occupied by each species (see Lumaret & Lobo, 1996). * A. (Neagolius) montanus is cited at the Rhodopes by Mariani (1980), but without any specific locality.

86 Lobo et al.

Lobo et al. unpublished

Golian 1953 Mikšić 1959

Nedelkov 1905

Ioakimov 1904

X X X

A. (Melinopterus) consputus Creutzer

A. (Melinopterus) prodromus (Brahm)

A. (Melinopterus) sphacelatus (Panzer)

A. (Nimbus) obliteratus Panzer

A. (Nobius) serotinus (Panzer)

X X

A. (Nimbus) contaminatus (Herbst)

A. (Nialus) varians Duftschmid

A. (Neagolius) montanus Erichson

A. (Limarus) maculatus Sturm

A. (Eupleurus) subterraneus (L.)

A. (Euorodalus) paracoenosus Bal. & Hru.

A. (Eudolus) quadriguttatus (Herbst)

A. (Esymus) pusillus (Herbst)

A. (Coprimorphus) scrutator (Herbst)

X X

A. (Colobopterus) erraticus (Linnaeus)

A. (Esymus) merdarius (Fabricius)

A. (Chilothorax) sticticus (Panzer)

X X X

A. (Chilothorax) melanosticticus W. Schmidt

Nedelkov 1909

Stolfa 1938

Pittioni 1940

A. (Chilothorax) distinctus (Müller)

Mikšić 1957

A. (Calamosternus) granarius (L.)

Angelov 1965

X X X

Zacharieva 1965a X

Zacharieva 1965b

A. (Bodilus) lugens Creutzer

A. (Aphodius) foetens (Fabricius)

A. (Aphodius) fimetarius (Linnaeus)

Species

Table 1. (Cont.) Zacharieva & Dimova 1975 X

Král & Malý 1993 X

Bunalski 2001b X

Distribution ES

ET–M

EM–CA

ET–M

T–M

Rs 4

2000

1900

1800

1700

1600

1500

1400

1300

1200

1100

1000

900

800

700

600

500

400

300

200

1 1

1 1 1 1 1 1 1 1 1 1

1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1

1 1 1 1 1 1 1 1

1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

Animal Biodiversity and Conservation 30.1 (2007) 87

Rossner 2005

Bunalski 2001a

A. (Teuchestes) fossor (L.)

Ioakimov 1904

Copris umbilicatus Abeille de Perrin

Copris lunaris (L.)

Caccobius schreberi (L.)

Copris hispanus (L.)

Trypocopris vernalis (L.)

Lethrus schaumi Reitter

X X

Angelov 1965 X

Zacharieva 1965a X

X X

Thorectes punctulatus (Jekel)

Geotrupes stercorarius (Linnaeus)

Geotrupes spiniger Marsham

Nedelkov 1905

Nedelkov 1909

Geotrupes mutator Marsham

Stolfa 1938

Pittioni 1940

Golian 1953

Mikšić 1957

Anoplotrupes stercorosus (Scriba)

Zacharieva 1965b X

X X X X

Mikšić 1959

Pleurophorus caesus (Creutzer)

Oxyomus silvestris (Scopoli)

Euheptaulacus sus (Herbst)

Euheptaulacus carinatus (Germar)

A. (Sigorus) porcus (Fabricius)

A. (Trichonotulus) scrofa (Fabricius)

X X

A. (Pseudoacrossus) thermicola Sturm

Lobo et al. unpublished

A. (Planolinus) uliginosus (Hardy)

A. (Planolinus) borealis Gyllenhal

A. (Phalacronothus) biguttatus Germar

A. (Otophorus) haemorrhoidalis (L.)

Species

Table 1. (Cont.)

Zacharieva & Dimova 1975 X

Bunalski 2001a X

Distribution E

CA–M

ET–M

East M

East E

EM–CA

CA–ET–M

Rs 5

400

1500

1400

1300

1200

1100

1000

900

800

700

600

500

1800

1700

1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1

1 1 1 1 1 1 1 1 1

1 1 1 1

1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1

200

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1900

1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

300

1 1 1

2000

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1600

1 1 1 1 1 1 1 1 1 1 1 1 1

88 Lobo et al.

Rossner 2005

Bunalski 2001b

Král & Malý 1993

Lobo et al. unpublished Nedelkov 1905

O. (Onthophagus) taurus (Schreber)

Golian 1953

O. (Palaeonthophagus) verticicornis (Lairch.)

Sisyphus schaefferi (L.)

S. (Scarabaeus) typhon Fischer–Waldheim

Scarabaeus (Scarabaeus) pius (Illiger)

O. (Palaeonthophagus) ruficapillus Brullé

O. (Palaeonthophagus) ovatus Linnaeus

O. (Palaeonthophagus) vacca (L.)

O. (Palaeonthophagus) lemur (Fabricius)

O. (Palaeonthophagus) similis (Scriba)

O. (Palaeonthophagus) joannae Goljan

X X

Angelov 1965

X X X

X X

X X X X

O. (Palaeonthophagus) grossepunctatus Reit.

X X

X X X X

Mikšić 1957

O. (Palaeonthophagus) fracticornis (Preyssler)

Zacharieva 1965a X

Zacharieva 1965b

X X X X

Mikšić 1959

O. (Palaeonthophagus) coenobita (Herbst) X

O. (Onthophagus) illyricus (Scopoli) X

Onthophagus (Furconthophagus) furcatus (F.)

Ioakimov 1904

Nedelkov 1909 X

Stolfa 1938

Gymnopleurus sturmi McLeay

Pittioni 1940

Gymnopleurus mopsus (Pallas)

Gymnopleurus geoffroyi (Fuessly)

Euonthophagus gibbosus (Scriba)

Euonthophagus amyntas (Olivier)

Euoniticellus pallipes (Fabricius)

Euoniticellus fulvus (Goeze)

Species

Table 1. (Cont.)

Distribution CA–E–M

CA–M

East M

EA–M

ET–M

CA–M

ET–M

EA–M

ET–M

Rs 6

1400

1300

1200

1100

1000

900

800

700

600

500

400

300

200

1500

2000

1900

1800

1700

1600

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

Animal Biodiversity and Conservation 30.1 (2007) 89

Rossner 2005

Bunalski 2001b

Bunalski 2001a

Král & Malý 1993

Zacharieva & Dimova 1975

Lobo et al.

Geotrupinae and Aphodiinae Iberian species (around 8,000 database records). The information compiled for the Iberian Central System also involves a long period of samplings: from 1872 to 2004. All these data are freely available in the GBIF web page (http://www.gbif.org/). We established the range of altitudes for each species assuming that they occur along the whole range between minimum and maximum recorded altitude. This procedure implies the existence of two assumptions: i) that the species generally have a Gaussian symmetric or skewed unimodal response along the elevational environmental gradients, and ii) that the detected upper and lower limits of species occurrence are related with true altitudinal limits. While much evidence supports the occurrence of such response curves in most species (McKenzie et al., 2003; Sanders et al., 2003; McCain, 2004; Austin, 2005), the second assumption clearly relies on the existence of reliable sampling inventories along the altitudinal interval. Here, we assume that the analysis of a long period of data collection has allowed detection of the potential altitudinal distribution of species, a similar supposition to that generally established in the estimation of species range distributions. To do this, we divided the altitudes into 100 m intervals at both regions. For each species we also considered information on its range size and type of distribution. Geographic range size was estimated considering the six classes of geographic range size suggested by Lumaret & Lobo (1996), according to the percentage of the total western Palaearctic region area covered by the distribution range of each species’ (12 x 106 km2). Those species with range–size classes 1–4 (i.e., ranges of approximately the same area as the Iberian Peninsula or smaller) were considered narrowly distributed. The type of distribution was defined according to the criteria of La Greca (1964) calcu-

lating the number of species with Euroturanian and Mediterranean distributions (herein, Mediterranean–centred species). Species nomenclature followed the taxonomic criteria of Dellacasa (1983) and Baraud (1992). For each higher taxa and region we calculated the one hundred altitudinal interval with most species (i.e., the mode). Two linear regressions were calculated using two groups of data defined by this modal score (above and below) to estimate whether the increase and/or decrease in species richness with altitude (the slope) depart significantly from zero. The significance (p–level) for the difference between proportions has been calculated taking into account the sample size of each of region (total number of species) according to the t–value for the respective comparison (see StatSoft, 2003). Results Seventy–nine dung beetle species have been cited for the Western Rhodopes (table 1), although many of the localities surveyed were situated in the western part of this mountain chain (fig. 1). Recent field work (Lobo et al., in press) recorded 48 species (60% of total), adding seven new species to the regional inventory. In contrast, the dung beetle fauna of the Iberian Central System was richer (121 species). Almost half of these species (57 species) were present in both regions (fig. 2). Interestingly, although 57% of all the species collected in both regions were Aphodiinae (82 species) and 30% Scarabaeidae (44 species), 44% of the shared species belonged to the latter family while most of the species exclusive of the Rhodopes or the Iberian Central System were Aphodiinae (58% and 73%, respectively; see fig. 2). In the Western Rhodopes 45% of the species (36 species) had a distribution centred in the Mediterranean basin, while only 4%

Iberian Central System 17

10 25

3 2

Western Rhodopes Fig. 2. Number of species shared by both regions and number of species exclusive to each of them. Scarabaeidae (dark grey), Aphodiinae (clear grey), Geotrupinae (white). Fig. 2. Número de especies compartidas y número de especies propias de cada una de las regiones analizadas. Scarabaeidae (gris oscuro), Aphodiinae (gris claro), Geotrupinae (blanco).

Animal Biodiversity and Conservation 30.1 (2007)

Table 2. Number of species (S) belonging to each of the three main dung beetle taxonomic groups for the two mountain chains considered (the percentage of the total is shown in brackets), the 100 m altitude interval with the highest number of species (according to the Mode), and slope scores of the linear relationship between altitude and species richness, calculated considering the data above (B+) and below (B–) modal values (change in the number of species for each 100 m); t–value and resulting p–value test the hypothesis that the slope equals to 0. Tabla 2. Número de especies (S) de cada uno de los tres principales grupos de escarabajos coprófagos en las dos regiones montañosas analizadas (porcentajes entre paréntesis), valor modal del número de especies en los intervalos de 100 m utilizados y valores de la pendiente de regresión linear entre el numero de especies y la altitud según se consideren los datos por encima (B+) y por debajo (B–) de los valores modales (número de especies por cada 100 m de altitud). Los valores de t tratan de comprobar si estas pendientes puede considerarse significativamente diferentes de cero.

Mode

B+

B–

Total species

121

900

6.1 (t = 3.68; p = 0.02)

– 8.2 (t = 22.05; p < 0.0001)

Scarabaeidae

42(35%)

900

2.8 (t = 9.90; p = 0.002)

– 2.7 (t = 19.20; p < 0.0001)

Aphodiinae

66(54%)

1,000

3.2 (t = 8.61; p = 0.001)

– 4.7 (t = 25.18; p < 0.0001)

Geotrupinae

13(11%)

1,450

0.6 (t = 2.49; p = 0.03)

– 1.3 (t = 15.39; p < 0.0001)

Total species

1,000

3.9 (t = 5.14; p = 0.001)

– 3.7 (t = 12.75; p < 0.0001)

Scarabaeidae

27(34%)

700

1.1 (t = 1.71; p = 0.16)

– 1.7 (t = 10.42; p < 0.0001)

Aphodiinae

46(57%)

1,100

2.3 (t = 6.96; p = 0.0001)

– 1.4 (t = 9.97; p < 0.0001)

Geotrupinae

7(9%)

1,500

0.3 (t = 5.43; p = 0.0002)

– 0.5 (t = 5.00; p = 0.02)

Iberian Central System

Western Rhodopes

could be considered narrowly distributed (3 species). The proportion of Mediterranean–centred species was similar in the Iberian Central System (58 species; 48%, p = 0.34) as was the percentages of species of the three main taxonomical groups (table 2). However, the percentage of narrowly distributed species was higher than in Rhodopes (16% of total; p = 0.005). The elevational pattern derived for Rhodopes (fig. 3) showed a mid–elevational peak between 700 and 1,400 m. All relationships between richness and altitude (except Scarabaeidae in the 200– 700 m interval) differed significantly from zero, with negative slopes above the modal altitude and positive slopes up to this modal altitude (table 2). The increase in species richness towards the modal altitude was more pronounced in Aphodiinae than in Scarabaeidae, while the two groups showed similar decays in species richness from the modal altitude. Thus, a manifest elevational turnover among the two taxonomical groups occurred (fig. 3).

A mid–elevational peak in species richness was also observed at the Iberian Central System (between 800–1,000 m), with very similar modal altitudes for each of the three dung beetle groups (table 2). Here, the rates of increment and decrease in species richness were more pronounced than at Rhodopes Mountains, probably due to the higher number of species considered. In spite of this, the emerged altitudinal pattern was quite similar (table 2). Although the relevance of Aphodiinae species in lower altitudinal levels seemed comparatively higher, the increase in the contribution of Aphodiinae and Geotrupinae species with altitude was also evident (fig. 2). The occurrence of Mediterranean–centred species clearly diminished with altitude, both at the Rhodopes and the Iberian Central System (fig. 4), showing similar slopes. On the contrary, the number of narrowly–distributed species increased slightly but significantly with altitude in both regions (fig. 4).

Lobo et al.

Iberian Central System

100

Species richness

120

50 40

35 30

25 20

5 2000 1900 1800 1700 1600 1500 1400 1300 1200 1100 1000 900 800 700 600 500 400 300 200

2200 2100 2000 1900 1800 1700 1600 1500 1400 1300 1200 1100 1000 900 800 700 600 500 %

Western Rhodopes

Altitude

2000 1900 1800 1700 1600 1500 1400 1300 1200 1100 1000 900 800 700 600 500 400 300 200

2200 2100 2000 1900 1800 1700 1600 1500 1400 1300 1200 1100 1000 900 800 700 600 500

Altitude

Fig. 3. Relationships between altitude and number of collected species in both mountain regions, and relationships between altitude and percentage of species from the three taxonomic groups. All dung beetles (white circles), Scarabaeidae (black triangles), Aphodiinae (black circles) and Geotrupinae (black squares). Fig. 3. Relaciones entre altitud y el número total de especies (círculos blancos), numero de especies de Scarabaeidae (triángulos negros), Aphodiinae (círculos negros) y Geotrupinae (cuadrados negros) para cada una de las dos regiones montañosas y relaciones entre altitud y el porcentaje de especies de estos tres grupos taxonómicos.

Discussion Our results suggest that Eastern European dung beetle assemblages have similar patterns of compositional turnover and species richness variation with altitude as those observed in Western Europe and North America (Martin–Piera et al., 1992; Jay–Robert et al., 1997; Errouissi et al., 2004, Halffter et al. 1995; Lobo & Halffter, 2000). In spite of the relatively low proportion of shared species (40%), dung beetle assemblages at the Iberian Central System and Rhodopes Mountains show: (i) relatively similar proportions of species belonging to their three main taxonomic lineages

(Scarabaeidae, Aphodiinae and Geotrupinae), (ii) comparable frequencies of species with Mediterranean–centred distribution (around 45%–48%), (iii) analogous modal species richness altitudes, and (iv) similar rates of richness increase and/or decrease with altitude (both for total species and for Mediterranean or narrowly distributed species). The evident pattern of altitudinal substitution among higher level taxa (Aphodiinae–Geotrupinae vs. Scarabaeidae) at Rhodopes Mountains suggests that East European dung beetle assemblages are also conditioned by a horizontal colonization process, where mountains were colonized in relatively recent geological times by elements coming from

Animal Biodiversity and Conservation 30.1 (2007)

Iberian Central System B = –2.2; t = 20.22; p < 0.0001

B = –2.3; t = 18.92; p < 0.0001

Western Rhodopes

B = 0.2; t = 5.15; p < 0.0001

B = 0.5; t = 3.95; p < 0.004

2000

1500

1000

500

Altitude

2000

1500

0 1000

500

Altitude

Fig. 4. Altitudinal variation in the number of Mediterranean–centred species (circles) and narrowly distributed species (squares) for both mountain areas. B is the slope of the linear relationship between altitude and the number of species, while t–value and resulting p–value test the hypothesis that the slope is equal to 0. Fig. 4. Variación altitudinal en el número de especies con una distribución centrada en la region Mediterránea (círculos) y en el número de especies con rangos de distribución restringidos (cuadrados) para ambas regiones. B es el valor de la pendiente de la regresión linear entre altitud y número de especies, mientras los valores de t tratan de comprobar si esta pendiente puede considerarse significativamente diferente de cero.

different latitudes (Lobo & Halffter, 2000). These convergences are difficult to explain by sampling effort differences because they would imply that future new citations in Western Rhodopes should belong to taxonomically and geographically biased species. Several differences can be observed between these two regions. Rhodopes dung beetle assemblages are characterized by a significantly lower proportion of narrowly distributed species than those of the Iberian Central System, and also by a lower relevance of Aphodiinae species in lowland places. Some of these divergences can be attributed to differences in area and differences in sampling techniques between the two regions. There is a marked variation among the area of both regions (almost 2.4 times higher in the Iberian Central System). However, species area curves for dung beetles demonstrate that the rate of species–accumulation with increasing area is low (around 0.098 species by km2; see Lobo & Martín– Piera, 1999), so the inventory of Western Rhodopes could increase approximately in seven species if this region had a similar area to that of the Iberian Central System. Thus, the important difference in the total number of species at each region (41 species) would only be partially due to differences in area. The disparity in the survey techniques for the inventory in the two regions and the differences in the location of surveyed localities (few surveys in the southern part of Western Rhodopes) may also

partly explain this difference in regional species richness. For example, a recent exhaustive survey partly devoted to the Iberian Central System (Hortal, 2004) added only one new species to the regional catalogue. In contrast, our recent field work in Western Rhodopes yielded seven new citations, and sampling did not encompass a whole year. The scarcity of faunistic data from the southernmost Rhodopes localities under Mediterranean conditions probably influences the low number of species recorded for the lowlands (mainly Aphodiinae and/or species with Mediterranean distribution). The forthcoming addition of faunistic data from these places could allow us to assess the reliability of the differences in species richness between the two regions. In spite of these limitations, we consider that the main divergence found between the two regions in this study (the lower proportion of narrowly distributed species) can not be explained by sampling effort differences (all seven new citations for the Western Rhodopes belong to the maximum range– size category; over 10% of the total area of the Western Palaearctic region; see Lumaret & Lobo, 1996). There are nineteen narrowly distributed species in the Iberian Central System, some of them widely distributed in the region and with abundant populations (Lobo, 1992), but there are only three in Western Rhodopes. In our opinion, this remarkable divergence can be partially explained by the different degree of isolation and biogeographical

history of these two mountain areas. Both Iberian and Balkan Peninsulas acted as refuges during Pleistocene glacial–interglacial cycles (see Bennet et al., 1991; Hewitt, 1996; Taberlet et al., 1998; Brewer et al., 2002; Olalde et al., 2002; Petit et al., 2002 for the former and Hewitt, 2000; Bordács et al., 2001; Petit et al., 2002; Heuertz et al., 2004; Schmitt et al., 2006; Ursenbacher et al., 2006 for the latter). However, recent phylogeographic data demonstrate that, at least for butterflies, the Pyrenees could have acted as a barrier for post–glacial recolonization of European lineages, contrary to the pattern found for Italian and Balkan Peninsulas (Habel et al., 2005). Thus, the connection of Rhodopes Mountains with other European mountain chains could have hindered the isolation and subsequent speciation of the lineages sheltered there during Pleistocene climate changes. This could explain the notable divergence between eastern and western European dung beetle assemblages found in this study: the low number of narrowly distributed species inhabiting the eastern Rhodopes mountain chain. Acknowledgements Special thanks to Joaquín Hortal for his valuable suggestions. This study has been supported by two research projects financed jointly by CSIC (Spain) and BAS (Bulgaria) (2004BG0012 and 2005BG0022). References Angelov, P., 1965. Mistkäfer (Coprinae, Scarabaeidae) aus Bulgarien. Travaux scientifique de l’ecole normale superieure, Plovdiv, Biologie, 3(1): 95–109 (In Bulgarian, German summary). Austin, M. P., 2005. Vegetation and environment: discontinuities and continuities. In: Vegetation Ecology: 52–84 (E. van der Maarel, Ed.). Blackwell Publishing, Oxford. Baraud, J., 1992. Coleóptères Scarabaeoidea d’Europe. Faune de France 78. Fédération Française des Sociétés de Sciences Naturelles, Lyon. Bennet, K. D., Tzedakis, P. C. & Willis, K. J., 1991. Quaternary refugia of north European trees. Journal of Biogeography, 18: 103–115. Bordács, S., Popescu, F., Slade, D., Csaikl, U. M., Lesur, I., Borovics, A., Kézdy, P., König, A. O., Gömöry, D., Brewer, S., Burg, K. & Petit, R. J., 2001. Chloroplast DNA variation of white oaks in northern Balkans and in the Carpathian Basin. Forest Ecology and Management, 156: 197–209. Brewer, S., Cheddadi, R., De Beaulieu, J. L., Reille, M. & Data contributors, 2002. The spread of deciduous Quercus throughout Europe since the last glacial period. Forest Ecology and Management, 156: 27–48. Brown, J. H., 1995. Macroecology. University of

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Chicago Press, Chicago. Brown, J. H. & Lomolino, M. V., 1998. Biogeography. Sinauer Associates, Sunderland, Massachusetts. Bunalski, M., 2001a. Contributions to the knowledge Scarabaeoidea (Coleoptera) of Bulgaria. Part II. Species not recorded from Bulgaria before. Wiadomosti Entomologiczne, 20: 29–32. – 2001b. Checklist of Bulgarian Scarabaeoidea (Coleoptera) {Fourth contribution to the knowledge of Scarabaeoidea of Bulgaria}. Polskie Pismo Entomologiczne, 70: 165–172. Channell, R. & Lomolino, M. V., 2000. Trajectories toward extinction: dynamics of geographic range collapse. Journal of Biogeography, 27: 169–179. Colwell, R. K., 2005. EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5. Persistent URL: purl.oclc.org/estimates Cruzan, M. B., & Templeton, A. R., 2000. Paleoecology and coalescence: phylogeographic analysis of hypotheses from the fossil record. Trends Ecology and Evolution, 15: 491–496. Davis, A. L. V., Scholtz, C. H. & Chown, S. L., 1999. Species turnover, community boundaries, and biogeographical composition of dung beetle assemblages across an altitudinal gradient in South Africa. Journal of Biogeography, 26: 1039–1055. Dellacasa, G., 1983. Sistematica e nomenclatura degli Aphodiini italiani (Coleoptera Scarabaeidae: Aphodiinae). Monografie del Museo Regionale di Scienze Naturale di Torino, Torino. Elias, S. A., 1994. Quaternary insects and their environments. Smithsonian Institution Press, Washington. Errouissi, F., Jay–Robert, P., Lumaret, J. P. & Piau, O., 2004. Composition and Structure of Dung Beetle (Coleoptera: Aphodiidae, Geotrupidae, Scarabaeidae) assemblages in Mountain Grasslands of the Southern Alps. Annals of the Entomological Society of America, 97(4): 701–709. Escobar, F., Lobo, J. M. & Halffter, G., 2005. Altitudinal variation of dung beetle (Scarabaeidae: Scarabaeinae) assemblages in Colombian Andes. Global Ecology and Biogeography, 14: 327–337. Goljan, A., 1953. Studies on Polish beetles of the Onthophagus ovatus (L.) group with some biological observations on coprophagans (Coleoptera, Scarabaeidae). Annales Musei zoologici Polonici, 15: 55–81. Habel, J. C., Schmitt, T. & Müller, P., 2005. The fourth paradigm pattern of post–glacial range expansion of European terrestrial species: the phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera). Journal of Biogeography, 32: 1489–1497. Halffter, G., Favila, M. E. & Arellano, L., 1995. Spatial distribution of three groups of Coleoptera along and altitudinal transect in the Mexican Transition Zone and its biogeographical implications. Elytron, 9: 151–185. Hanski, I., 1983. Distributional ecology and abundance of dung beetles and carrion feeding beetles

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(Coleoptera) from Bulgaria. Acta Societatis Zoologicae Bohemoslovacae, 57: 17–29. La Greca, M., 1964. Le categorie corologiche degli elementi faunistici italiani. Atti dell’ Academia Nazionale Italiana di Entomologia. Rendiconti, 11: 231–253. Lobo, J. M., 1992. Biogeografía de los Scarabaeoidea coprófagos (Coleoptera) del Macizo Central de Gredos (Sistema Central Ibérico). Ecologia Mediterranea, 18: 69–80. Lobo, J. M., Chehlarov, E. & Guéorguiev, B. (in press). Dung beetle assemblage variation with altitude in the Bulgarian Rhodopes Mountains: a comparison. European Journal of Entomology. Lobo, J. M. & Halffter, G., 2000. Biogeographical and ecological factors affecting the altitudinal variation of mountainous communities of coprophagous beetles (Coleoptera: Scarabaeoidea): a comparative study. Annals of the Entomological Society of America, 93: 115–126. Lobo, J. M. & Hortal, J., 2006. Los Escarabeidos y Geotrúpidos de la Comunidad de Madrid: Lista de especies, distribución geográfica y patrones de diversidad (Coleoptera, Scarabaeoidea, Scarabaeidae y Geotrupidae). Graellsia, 62: 419–438. Lobo, J. M., Lumaret, J.–P. & Jay–Robert, P., 2002. Modelling? the species richness distribution of French dung beetles and delimiting the predictive capacity of different groups of explanatory variables (Coleoptera: Scarabaeidae). Global Ecology and Biogeography, 11: 265–277. Lobo, J. M. & Martín–Piera, F., 1991. La creación de un banco de datos zoológico sobre los Scarabaeidae (Coleoptera: Scarabaeoidea) Ibero– Baleares: Una experiencia piloto. Elytron, 5: 31–37. – 1999. Between–group differences in the Iberian dung beetle species–area relationship (Coleoptera: Scarabaeidae). Acta Oecologica, 20: 587–597. Lobo J. M., Martín–Piera F. & Veiga, C. M., 1988: Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeidae (Col.). I. Características determinantes de su capacidad de captura. Revue d’écologie et de biologie du sol, 25: 77–100. Lumaret, J. P. & Kirk, A. A., 1991. South temperate dung beetles. In: Dung Beetle Ecology: 97–115 (I. Hanski & Y. Cambefort, Eds.). Princeton Univ. Press, Princeton. Lumaret, J. P. & Lobo, J. M., 1996. Geographic distribution of endemic dung beetles (Coleoptera, Scarabaeoidea) in the Western Palearctic region. Biodiversity Letters, 3: 192–199. Mariani, G., 1980. Gli Aphodius italiani del sottogenere Agolius Muls. (Coleoptera, Aphodiidae). Memorie della Società Entomologica Italiana, 58: 41–94. Martín–Piera, F., Veiga, C. M. & Lobo, J. M., 1986. Contribución al conocimiento de los Scarabaeoidea (Col.) coprófagos del Macizo Central de Guadarrama. Eos, 62: 103–123.

– 1992. Ecology and biogeography of dung–beetle communities (Coleoptera, Scarabaeoidea) in an Iberian mountain range. Journal of Biogeography, 19: 677–691. McCain, C. M., 2004. The mid–domain effect applied to elevational gradients: species richness of small mammals in Costa Rica. Journal of Biogeography, 31: 19–31. McKenzie, D., Peterson, D. W., Peterson, D. J & Thornton, P. E., 2003. Climatic and biophysical controls on conifer species distributions in mountain forests of Washington State, USA. Journal of Biogeography, 30: 1093–1108. Mikšić, R., 1957. Zweiter Nachtrag zur "Fauna Insectorum Balcanica–Scarabaeidae". (Coleoptera, Lamellicornia). (24. Beitrag zur Kenntnis der Scarabaeidae). Acta Musei Macedonici scientiarum naturalium, 4: 139–214. – 1959. Dritter Nachtrag zur "Fauna Insectorum Balcanica–Scarabaeidae". (30. Beitrag zur Kenntnis der Scarabaeiden). Godišniakbioloctaškog instituta univerziteta u Sarajevu, 12(1–2): 47–136. Moritz, C., Patton, J. L., Schneider, C. J. & Smith, T. B., 2000. Diversification of rainforest faunas: An integrated molecular approach. Annual Review in Ecology and Systematics, 31: 533–563. Nedelkov, N., 1905. Contribution to the entomological fauna of Bulgaria. Periodichesko spisanie na bulgarskoto knizhovno druzhestvo v Sofia, 66: 404–439 (In Bulgarian). – 1909. Fifth contribution to the fauna of insects of Bulgaria. Sbornik za narodni umotvorenia, nauka i kni•nina, 25: 3–37 (In Bulgarian). Olalde, M., Herrán, A., Espinel, S. & Goicoechea, P. G., 2002. White oaks phylogeography in the Iberian peninsula. Forest Ecology and Management, 156: 89–102. Petit, R. J., Brewer, S., Bordács, S., Kornel, B., Cheddadi, R., Coart, E., Cottrell, J. E., Csaikl, U. M., Van Dam, B., Deans, J. D., Espinel, S., Fineschi, S., Finkeldey, R., Glaz, I., Goicoechea, P. G., Jensen, J. S., König, A. O., Lowe, A. J., Madsen, S. F., Mátyás, G., Munro, R. C., Popescu, F., Slade, D., Tabbener, H. E., De Vries, S. G. M., Ziegenhagen, B., De Beaulieu, J. L. & Kremer, A., 2002. Identification of refugia and post–glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecology and Management, 156: 49–74. Pittioni, B., 1940. Die Arten der Unterfamilie Coprinae (Scarabaeidae, Coleoptera) in der Sammlung des Kgs. Naturh. Museum in Sofia. Mitteilungen aus den Königlichen Naturwissenschaftlischen

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Instituten, Sofia, 13: 211–238. Rossner, E., 2005. Die Verbreitung von Aphodius (Eurodalus) coenosus (Panzer, 1798) und Aphodius (Eurodalus) paracoenosus Balthasar & Hrubant, 1960 in Deutschland und Mittelung von Funddaten zu den Gesamtarealen beider Arten (Coleoptera: Scarabaeidae). Entomologische Zeitschrift, Stuttgart, 115(2): 59–69. Sanders, N. J., Moss, J. & Wagner, D., 2003. Patterns of ant species richness along elevational gradients in an arid ecosystem. Global Ecology & Biogeography, 12: 92–102. Schmitt, T., Habel, J. C., Zimmermann, M. & Müller, P., 2006. Genetic differentiation of the marbled white butterfly, Melanargia galathea , accounts for glacial distribution patterns and postglacial range expansion in southeastern Europe. Molecular Ecology, 15: 1889–1901 StatSoft, Inc. 2003. STATISTICA (data analysis software system), version 6. www.statsoft.com. Stolfa, E., 1938. Revisione delle specie papearctiche del sottogenere Scarabaeus s. str. Atti del Museo civico di Storia naturale Trieste, 13: 141–156. Taberlet, P., Fumagalli, L., Wust–Saucy, A. G. & Cosson, J. F., 1998. Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7: 453–464. Ursenbacher, S., Carlsson, M., Herfer, V., Tegelström, H. & Fumagalli, L., 2006. Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Molecular Ecology, 15: 3425–3437. Veiga, C. M., Lobo, J. M. & Martín–Piera, F., 1989: Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeidae (Col.). II. Análisis de efectividad. Revue d’écologie et de biologie du sol, 26: 91–109. Zacharieva, B., 1965a. Beitrag zur erforschung der coprophagen Scarabaeoidae (Coleoptera) aus den Ostrhodopen. Bulletin de l’Institut de Zoologie et Musée, 19: 129–134 (In Bulgarian, German summary). – 1965b. Scarabaeidae (Coleoptera) aus Thrakien. In: Die Fauna Thrakiens. Sofia, 2: 229–254 (A. K. Valkanov, Ed.). Bulgarian Academy of Sciences, Sofia. (In Bulgarian, German summary). Zacharieva B., V. Dimova 1975. Fauniscthe untersuchungen über die Scarabaeidae (Coleoptera) aus den Rhodopen. In: La faune des Rhodopes. Materiaux. Sofia. 183–196 (G. Peshev, Ed.). Bulgarian Academy of Sciences, Sofia. (In Bulgarian, German summary).

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Evaluating factors affecting amphibian mortality on roads: the case of the Common Toad Bufo bufo, near a breeding place X. Santos, G. A. Llorente, A. Montori, M. A. Carretero, M. Franch, N. Garriga & A. Richter–Boix

Santos, X., Llorente, G. A., Montori, A., Carretero, M. A., Franch, M., Garriga, N. & Richter–Boix, A., 2007. Evaluating factors affecting amphibian mortality on roads: the case of the Common Toad Bufo bufo, near a breeding place. Animal Biodiversity and Conservation, 30.1: 97–104. Abstract Evaluating factors affecting amphibian mortality on roads: the case of the Common Toad, Bufo bufo, near a breeding place.— The Common Toad Bufo bufo is the amphibian with the highest rates of road mortality in many European countries. This elevated incidence of road kills has frequently been associated with migration to breeding sites. In this study, we analysed the mortality of the Common Toad in the road network in Catalonia (NE Spain), and investigated the related causative factors on four roads near a breeding site in the Pyrenees. Results suggest that the high mortality rate is due to a combination of factors: toad abundance, traffic density and quality of water bodies for breeding. On the road with the highest incidence of road kills we investigated whether deaths occurred at specific spots or in a random manner. The road was divided into 500 m sections and each section was classified according to biotic (type of vegetation) and abiotic (presence of streams, roadside topography) variables. Multiple correspondence analysis showed that sections with streams crossing under the road had the highest mortality rate, suggesting that such water bodies flowing into the breeding pond are the toads’ main migratory pathways for hibernation and breeding. As toads use the same migratory routes each year, it is critical to identify areas with a high potential mortality so that efficient measures can be designed to increase wildlife permeability, and thereby reduce habitat fragmentation. This methodology could be applied in other areas with high amphibian mortality. Key words: Amphibian, Common Toad, Bufo bufo, Landscape fragmentation, Migration, Mortality, Road permeability, Pyrenees. Resumen Evaluando los factores que afectan a la tasa de mortalidad en la carretera: el caso de Sapo Común Bufo bufo, cerca de un área de reproducción.— El Sapo Común Bufo bufo, es el anfibio con mayor tasa de mortalidad en la carretera en numerosos países de Europa. Esta elevada mortalidad se debe principalmente a las migraciones que realiza hacia las zonas de reproducción. En este estudio se analiza la mortalidad del Sapo Común en la red de carreteras de Cataluña (NE España) y más específicamente qué factores influyen sobre dicha mortalidad en cuatro carreteras cercanas a un punto de reproducción en los Pirineos. Los resultados sugieren que la alta tasa de mortalidad se debe a la combinación de tres factores: abundancia de sapos, densidad de tráfico y calidad de los puntos de agua para la reproducción. En la carretera con mayor índice de atropellos, se analizó si existía agregación en los animales atropellados o estos se distribuían al azar. Para ello, la carretera se dividió en tramos de 500 m, cada uno de los cuales se caracterizó por el tipo de vegetación circundante, así como otros factores que pudieran influir sobre la migración de los sapos (p. e. inclinación del margen de la carretera, presencia de riachuelos, etc.). El análisis de correspondencias múltiple demostró que los tramos con torrentes cruzando bajo la carretera presentaban mayor mortalidad. Esto sugiere que dichos torrentes son las vías principales usadas por los sapos para acudir a los puntos de reproducción. Dado que los sapos utilizan cada año las mismas vías migratorias, es fundamental identificar dichos puntos para predecir cuáles presentan mayor mortalidad potencial y así diseñar más eficazmente los mecanismos de permeabilidad para la fauna en las vías de comunicación. Esta metodología puede ser aplicada a otras zonas con elevada mortalidad de anfibios en la red de carreteras. ISSN: 1578–665X

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Palabras clave: Anfibio, Sapo Común, Bufo bufo, Fragmentación del paisaje, Migración, Mortalidad, Permeabilidad de la carretera, Pirineos. (Received: 13 XII 06; Conditional acceptance: 14 II 07; Final acceptance: 18 III 07) X. Santos, G. A. Llorente, A. Montori, M. Franch, N. Garriga & A. Richter–Boix, Dept. de Biologia Animal (Vertebrats), Univ. de Barcelona, Av. Diagonal 645, 08028 Barcelona, Espanya (Spain).– X. Santos, Parc Natural de Sant Llorenç del Munt i l’Obac, Oficina Tècnica de Parcs Naturals, Diputació de Barcelona, c/ Urgell 187, Edifici del Rellotge, 3ª planta, 08015 Barcelona, Espanya (Spain).– M. A. Carretero, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485–661 Vairão, Portugal. Corresponding author: X. Santos. E–mail: xsantos1@ub.edu

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Introduction Wildlife road mortality has been extensively studied and there is general consensus that it dramatically affects amphibians (Ehmann & Cogger, 1985; Fahrig et al., 1995; Hels & Buchwald, 2001; Montori et al., 2001; PMVC–CODA, 2003; Seiler, 2001; Trombulak & Frisell, 2000). Studies devoted to amphibian road kills have detected the most vulnerable species, identified "black spots" in the road network (for Spain, see Lizana, 1993; Lizana & Barbadillo, 1997; PMVC–CODA, 2003) and proposed strategies to reduce mortality on roads (see Langton, 1989a). Mortality of amphibians, reptiles and other vertebrates has recently been assessed in short segments of roads by standardized field surveys (Carretero & Rosell, 2000; Clevenger et al., 2003; Montori et al., 2004). This methodological approach identifies the species most vulnerable to road traffic, predicts the possible demographic effects of road mortality on species (i.e. population reduction, extinction, fragmentation) (Fahrig et al., 1995; Seiler, 2001; Trombulack & Frissell, 2000; Wilson, 1988) and provides useful information for developing correction measures to reduce mortality (Langton, 1989b; Vogel & Puky, 1995). The Common Toad Bufo bufo, present in most parts of Europe, is the amphibian with the widest Palaearctic distribution (Lizana, 2002). It is abundant and unfortunately the amphibian most frequently found dead on roads in many European countries (Langton, 1989a). Bufo bufo mortality has frequently been associated with migration to breeding sites (Feldmann & Geiger, 1989; Orlowski, 2007; Van Gelder, 1973), when hundreds of specimens are killed by traffic during the reproductive period (Cooke, 1995; Frétey et al., 2004). However, reports on biotic (i.e. vegetation) and abiotic (i.e. roadside topography) data related to toad mortality are scarce (Clevenger et al., 2003). This aspect is relevant, since every year toads use the same migratory pathways from hibernation to breeding sites. Areas with migratory routes that present potentially high mortality should be determined and efficient measures should be adopted to reduce road kills. The aims of this study were: 1) to detect road mortality of the common toad in the study area, 2) to determine the influence of traffic density on toad mortality and, 3) to examine whether road kills occurred randomly or at specific spots related to toad migratory pathways. Material and methods The study was conducted in La Pobla de Segur (542 m a.s.l., Lleida province, Spain), a mountainous region located in the Pyrenees (41º 15’ N and 0º 58’ E, fig. 1). Field work was carried out in the valley of the Noguera Pallaresa River, in an area where the river forms the Sant Antoni reservoir (267 hm3). The topography is moderately abrupt

with several streams that flow into the reservoir. Potential vegetation is composed of oak (Quercus faginea) although often replaced by pine plantations (e.g. Pinus nigra) and, in areas with low slope, by agricultural fields. All the roads studied in this work were surveyed by car at 20 km/h speed and recently killed common toads and other amphibians were recorded. At this speed it is possible to observe all kind of road–kills, hence avoiding biases due to the size of the amphibian species sampled (see Montori et al., 2001 for methodological details). To determine whether the common toad mortality was important with respect to other amphibian causalities in the study area a 20–km stretch of a road near La Pobla de Segur was surveyed every two weeks from May 2000 to April 2001, to detect the species with highest mortality rates. Bufo bufo road kills in the study area were compared with respect to results on another 45 roads in the Catalan road network , using the same methodology (Montori et al., 2004). To find whether traffic density and size of breeding sites were relevant factors to explain toad mortality dead toads were searched in four stretches of road around La Pobla de Segur. These roads differed in traffic density and type of breeding pond (fig. 1): a. C–13, between La Pobla de Segur and Tremp (11 km), the main road, running alongside the dam, with high traffic density as it links big cities further south (Barcelona, Lleida) with the tourist area of the Pyrenees; b. N–260, from La Pobla de Segur in the direction of Sort (5 km), with the same traffic density but running close to the Noguera Pallaresa River; c. N–260, from La Pobla de Segur going towards Senterada (5 km), with half the former traffic density and running close to the Flamisell River, a medium–size river which flows into the Noguera Pallaresa River in La Pobla de Segur, and d. A local road from La Pobla de Segur to Aramunt (7 km), with low traffic density, running alongside the dam on the opposite side to that of the C–13. No correction measures to reduce wildlife mortality (e.g. drift fences and tunnels) have been adopted on these roads to date. The common toad is an explosive breeder (Wells, 1977) that selects spring periods with high temperature and rainfall to move from hibernation to breeding sites (Sinsch, 1988; Zuiderwijk, 1989). For this reason, these four roads were surveyed during the peak of migratory activity, which occurred on 5–7 April 2001, during a rainy episode, when hundreds of specimens migrated from hillsides to the dam for breeding. Mortality on these four roads was compared by the number of killed toads per km, IKA (see Carretero & Rosell, 2000). To assess whether toad road kills were randomly distributed on roads running close to breeding points we studied only the C–13 stretch between La Pobla de Segur and Tremp as it runs alongside the dam (fig. 1) and showed the highest IKA score. The 11 km section between these two localities was divided into 500–meter segments and toads were

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counted in each of them. Segments were separately characterized according to the type of vegetation, type of roadside, roadside slope, presence of local roads and presence of streams that cross under the road. Association between these variables and the abundance of toads was assessed by a multiple correspondence analysis.

vegetation and agricultural lands. The variable best associated with mortality was the presence of streams crossing under the road. Segments with a stream had more kills than those without (median = 5, mean = 8.9 ± 2.8 toads in 7 segments with stream; median = 2, mean = 2.5 ± 0.4 toads in 14 segments without stream; Z = 10, p = 0.004).

Results

Discussion

Common toad mortality in the Pyrenees

Differences in the numbers of amphibians killed on different roads may be due to several factors as toad abundance and quality of breeding ponds in the road vicinity. Stretches of N–260 exhibited fewer road kills than C–13 and the local road (table 1). These differences suggest that toad populations are smaller in the vicinity of mountainous rivers like the Noguera Pallaresa and the Flamisell than in the hills around the dam. In Poland, road–kills were closely related to toad abundance and to the size of water bodies for breeding (Orlowski, 2007). Our results agree with these conclusions as the Sant Antoni reservoir is the biggest water body for breeding in the study area as mountainous rivers have only small ponds for breeding due to the water– speed. This finding supports the fact that the presence of quiet or slow–moving water seems to be Bufo bufo’s only requirement for breeding (Augert & Guyetant, 1995; Lizana, 1997). Reservoirs in the Pyrenees like the Sant Antoni dam seem to be suitable water bodies to maintain important breeding populations of the common toad. Differences in toad road kills between the two roads that run alongside the dam (C–13 and the local road, fig. 1 and table 1) support the role of traffic density in toad mortality as has been extensively reported (Fahring et al., 1995). Intensive surveys of roads near the breeding ponds proved an effective method to detect migratory paths from hibernation sites to reproductive ponds. In the study area, we detected that common toads followed small streams to move from hibernation to breeding sites. Generally, toads exhibit a high fidelity to their natal pond (Sinsch, 1989) and, like other amphibians, non–random migratory routes through specific corridors are followed every year (Langton, 1989b; Dodd & Cade, 1998; De la Torre & Sobrino, 2001). The streams that flow into the Sant Antoni reservoir in La Pobla de Segur seem suitable routes for toad migration because amphibian displacements are sensitive to all barriers, both natural and anthropic (Sinsch, 1988, 1992; Ray et al., 2002), whereas natural routes originated by rivers present few obstacles. Measures to minimise toad mortality should focus on spots where streams cross under roads near the breeding sites. The section with the highest number of killed toads in the C–13 road includes a hillside of 40º slope with herbaceous and shrub vegetation. In this section, a stream crosses under the road through a 30 m long, 10 m wide, and 8 m high tunnel. High mortality in this spot was detected in previous visits, most

On the road surveyed from May 2000 to April 2001, we found three species of amphibians in road kills: the midwife toad Alytes obstetricans, the common toad Bufo bufo and the common frog Rana temporaria. Most of the species present in this area (Llorente et al., 1995) were thus affected, although the common toad was that most frequently killed (92% of occurrence). Consistent with these results, preliminary data of standardized transects on 45 roads in Catalonia (NE Spain) showed that the common toad Bufo bufo is the amphibian most frequently killed on roads (29% of observations, n = 1,240, unpublished data from the authors) in this area. Half–mountainous and rainy regions as our study area showed the highest mortality rates of common toads in Catalonia. Toad mortality related to traffic density and breeding sites The numbers of Bufo bufo found killed on the four roads surveyed is shown in table 1. The IKA scores revealed differences between roads according to traffic density and potential reproductive sites. Roads with high density traffic reached high IKA scores when they ran close to the dam (C–13 road), whereas they showed lower values running alongside rivers (N–260 from La Pobla de Segur to Sort). Furthermore, the local road from La Pobla de Segur to Aramunt ran close to the reservoir and, despite its low traffic density, the IKA score was higher than in the N–260 road. Factors affecting toad mortality In the C–13 road (La Pobla de Segur–Tremp), 99 common toads recently killed in the 11 km section were recorded. Toads did not appear randomly along the road. The number of toads did not increase from the closest to the farthest segment to the head of the dam (Spearman r = 0.04, p = 0.8, n = 21). Although there were toads in all the segments, the distribution differed significantly between them (range from 1 to 23 toads), suggesting that certain spots concentrated many specimens. The multiple correspondence analysis (fig. 2) revealed that segments with high mortality were characterized by: 1) the presence of streams crossing under the road, 2) low slope of the roadside, and 3) vegetation characterized by a mosaic of natural

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Sort

Por tu gal

Senterada

Spain

Flamisell River

c La Pobla de Segur a

Noguera Pallaresa River

b d Aramunt Sant Antoni Reservoir

Tremp

Fig. 1. Map of the breeding pond and the four roads around La Pobla de Segur surveyed for toads: a. C–13 from La Pobla de Segur to Tremp (11 km); b. N–260 from La Pobla de Segur in the direction of Sort (7 km); c. N–260 from La Pobla de Segur going towards Senterada (5 km); d. A local road from La Pobla de Segur to Aramunt (5 km). (For more information see Material and methods.) Fig. 1. Mapa del punto de reproducción y las cuatro carreteras alrededor de La Pobla de Segur donde se han buscado sapos atropellados: a. C–13 desde La Pobla de Segur a Tremp (11 km); b. N–260 desde La Pobla de Segur en dirección a Sort (7 km); c. N–260 desde La Pobla de Segur hacia Senterada (5 km); d. Carretera local desde La Pobla de Segur a Aramunt (5 km). (Para más información ver Material y métodos.)

toads were dry carcasses which persisted for weeks after death although corvids and other scavengers had removed part of the specimens (Slater, 1989, 1994, pers. obs.). In April 1998, 2000 and 2001, this point had been visited and 64, 46 and 82 kills were detected, respectively implying that multiple road kills occurred every year at this point and suggesting that the stream crossing the road in this section could be a key migratory pathway for common toads. Unfortunately, we lack information concerning the proportion of the breeding populations which were killed by traffic. However, the fact that the road is not new suggests that a sufficient number of specimens manage to cross the road annually and road kills are not of particular relevance for the breeding population. Other results are, however, interesting in other ways. Despite the existence of tunnels for streams, many toads climbed the embankment onto the road and were killed by traffic. This observation suggests that road permeability by big tunnels is not always an effective measure to prevent toad mortality during migration. The use of some sort of low fencing or barrier to prevent road access for migrating amphibians and ideally guide them to a tunnel entrance may contribute to decreasing toad mortality (Galet, 1995; Marshall et al., 1997; Rosell et al.,

Table 1. Number of common toads Bufo bufo killed and IKA scores (no. / km) of four roads in La Pobla de Segur (Lleida, Spain): R. Road; L. Length, in km; Td. Traffic density; N. Number of killed toads; IKA. Number of killed toads per km. (For other abbreviations see fig. 1.) Table 1. Número de sapos comunes Bufo bufo muertos y valor IKA (nº individuos / km) en cuatro carreteras alrededor de La Pobla de Segur (Lleida, España): R. Carretera; L. Longitud, en km; Td. Densidad de tráfico; N. Número de sapos muertos; IKA. Número de sapos muertos por km (Para otras abreviaturas ver fig. 1.)

IKA

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Dimension 2 Eigenvalue: 0.39; 27.7% of inertia

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–0.5 0.0 0.5 Dimension 1 Eigenvalue: 0.43; 31.0% of inertia

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Fig. 2. Plot of the multiple correspondence analyses to detect the variables linked to the presence of killed common toads Bufo bufo in the C–13 road. Variables (categories): Toad presence (yes, no); Presence of streams (yes, no); Presence of local ways (yes, no); Slope of the road side (high, medium, low); Type of vegetation (natural vegetation, fields, nat. veget. + fields). Fig. 2. Análisis de correspondencias multiples que muestra las variables relacionadas con la presencia de sapos comunes Bufo bufo atropellados en la carretera C–13. Variables (categorías): Presencia de sapos (sí, no); Presencia de arroyos (sí, no); Presencia de caminos (sí, no); Pendiente del margen de la carretera (alto, medio, bajo); Tipo de vegetación (vegetación natural, cultivos, vegetación natural + cultivos).

1997; SCV, 1997; Rosell & Velasco, 1999). Moreover, new infrastructures like highways and high speed railways use viaducts when they cross threatened ecosystems. This seems to be a suitable solution to increase wildlife permeability and reduce landscape fragmentation. In short, the present study shows that streams that flow into breeding points may be effective migratory routes for common toads to follow between breeding and terrestrial hibernation sites. Once detected, these natural pathways, partially blocked by roads, should be given high attention and taken into account when applying measures to reduce mortality (Schlupp & Podloucky, 1994). Although the common toad is a widespread species in Spain, its high mortality rate and the increasing road network suggest it is necessary to pay attention to breeding areas, particularly in very disturbed regions. Acknowledgements We thank German Pascual and Ester Berniola for their hospitality during the field work and Marta Pascual for her assistance during the field work. The present study is part of a project to study

amphibian and reptile mortality on Catalan roads and is funded by the Departament de Medi Ambient of the Generalitat de Catalunya (FBG301492). X.S. was supported by a Beatriu de Pinós grant (Generalitat de Catalunya). M.A.C. also thanks Fundação para a Ciência e a Tecnologia (Portugal) for funding (PhD position SFRH/BPD/27025/ 2006). References Augert, D. & Guyetant, R., 1995. Space occupation for egg deposition in amphibians living in plain woodland and pasture land (east of France). In: Scientia Herpetologica: 165–169 (G. A. Llorente, A. Montori, X. Santos & M. A. Carretero, Eds.). Asociación Herpetológica Española, Barcelona. Carretero, M. A. & Rosell, C., 2000. Incidencia del atropello de anfibios, reptiles y otros vertebrados en un tramo de carretera de construcción reciente. Boletín de la Asociación Herpetológica Española, 11: 40–44. Clevenger, A. P., Chruszcz, B. & Gunson, K. E., 2003. Spatial patterns and factors affecting small

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vertebrate fauna road–kill aggregations. Biological Conservation, 109: 15–26. Cooke, A. S., 1995. Road mortality of common toads (Bufo bufo) near a breeding site 1974– 1994. Amphibia–Reptilia, 16: 87–90. De la Torre, J. G. & Sobrino, E., 2001. Dispositivos para evitar el atropello de anfibios. Quercus, 183: 20–22. Dodd, C. K. & Cade, B. S., 1998. Movement patterns and the conservation of amphibians breeding in small, temporary wetlands. Conservation Biology, 12: 331–339. Ehmann, H. & Cogger, H., 1985. Australia’s endangered herpetofauna: a review of criteria and policies. In: The biology of Australasian frogs and reptiles: 435–447 (G. Grigg, R. Shine & H. Ehmann, Eds.). Royal Zoological Society of New South Wales, Sydney. Fahrig, L., Pedlar, J. H., Pope, S. E., Taylor, P. D. & Wegner, J. F., 1995. Effect of road traffic on amphibian density. Biological Conservation, 73: 177–182. Feldmann, R. & Geiger, A., 1989. Protection for amphibians on roads in Nordrhein–Westphalia. In: Amphibian and roads: 51–57 (T. E. S. Langton, Ed.). Proceedings of the Toad Tunnel Conference, Rendsburg, Germany. Frétey, T., Cam, E., Le Garff, E. & Monnat, J. – Y., 2004. Adult survival and temporary emigration in the common toad. Canadian Journal of Zoology, 82: 859–872. Galet, M., 1995. Autoroute A71, crossing of the Sologne. Devices to protect amphibians. Habitat fragmentation and infrastructure. Maastrich, The Netherlands. Hels, T. & Buchwald, E., 2001. The effect of road kills on amphibian populations. Biological Conservation, 99: 331–340. Langton, T. E. S. (Ed.), 1989a. Amphibian and roads. Proceedings of the Toad Tunnel Conference, Rendsburg, Germany. – 1989b. Reasons for preventing amphibian mortality on roads. In: Amphibian and roads: 75–80 (T. E. S. Langton, Ed.). Proceedings of the Toad Tunnel Conference, Rendsburg, Germany. Lizana, M., 1993. Mortalidad de anfibios y reptiles en carreteras: Informe sobre el estudio AHE– CODA. Boletín de la Asociación Herpetológica Española, 4: 37–41. – 1997. Bufo bufo (Linnaeus, 1758). In: Distribución y biogeografía de los Anfibios y Reptiles en España y Portugal: 152–154 (J. M. Pleguezuelos, Ed.). Monografías de Herpetología 3, Universidad de Granada y Asociación Herpetológica Española, Granada. – 2002. Bufo bufo (Linnaeus, 1758). In: Atlas y libro rojo de los Anfibios y Reptiles de España: 109–112 (J. M. Pleguezuelos, R. Márquez & M. Lizana, Eds.). Dirección General de Conservación de la Naturaleza, Asociación Herpetológica Española, Madrid. Lizana, M. & Barbadillo, L. J., 1997. Legislación, protección y estado de conservación de los

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anfibios y reptiles españoles. In: Distribución y biogeografía de los Anfibios y Reptiles en España y Portugal: 477–516 (J. M. Pleguezuelos, Ed.). Monografías de Herpetología 3, Universidad de Granada y Asociación Herpetológica Española, Granada. Llorente, G. A., Montori, A., Santos, X. & Carretero, M. A., 1995. Atlas dels amfibis i rèptils de Catalunya i Andorra. Editorial El Brau, Figueres, Spain. Marshall, I. C., Corner, A. & Tattersfield, P., 1997. An amphibian mitigation scheme for the A34 Wilmslow and Handforth Bypass, Chesire, United Kingdom. In: Habitat fragmentation and infrastructure: 227–237 (K. Canters, A. Piepers & D. Hendriks–Heersma, Eds.). Proceedings of the international conference on habitat fragmentation, infrastructure and the role of ecological engineering. Maastricht and The Hague, The Netherlands, Delft. Montori, A., Llorente, G. A., Carretero, M. A. & Santos, X., 2001. La gestión forestal en relación con la herpetofauna. In: Conservación de la biodiversidad y gestión forestal. Su aplicación en la fauna vertebrada: 251–289 (J. Camprodon & E. Plana, Eds.). Edicions de la Universitat de Barcelona, Barcelona. Montori, A., Santos, X., Llorente, G. A., Richter– Boix, A. & Garriga, N., 2004. Incidència dels atropellaments sobre l’herpetofauna al Parc Natural del Garraf: eix viari Olivella. Rat–penat. IV Trobada d’Estudiosos del Garraf, Monografies, 37: 107–112. Orlowski, G., 2007. Spatial distribution and seasonal pattern in road mortality of the common toad Bufo bufo in an agricultural landscape of south–western Poland. Amphibia–Reptilia, 28: 25–31. PMVC–CODA, 2003. Mortalidad de vertebrados en carreteras. Proyecto provisional de seguimiento de la mortalidad de vertebrados en carreteras (PMVC). Documentos Técnicos de Conservación, 4: 1–346. SCV, Madrid. Ray, N., Lehmann, A. & Joly, P., 2002. Modelling spatial distribution of amphibian populations: a GIS approach based on habitat matrix permeability. Biodiversity and Conservation, 11: 2143– 2165. Rosell, C., Parpal, J., Campeny, R., Jové, S., Pasquina, A. & Velasco, J. M., 1997. Mitigation of barrier effect of linear infrastructures on wildlife. In: Habitat fragmentation and infrastructure: 367–371 (K. Canters, A. Piepers A & D. Hemdriks–Heersma, Eds.). Proceedings of the international conference on habitat fragmentation, infrastructure and the role of ecological engineering. Maastricht and The Hague, The Netherlands, Delft. Rosell, C. & Velasco, J. M., 1999. Manual de prevenció i correcció dels impactes de les infraestructures viàries sobre la fauna. Documents dels Quaderns de Medi Ambient, 4: 1–95. Generalitat de Catalunya, Departament de Medi

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Ambient, Barcelona, Spain. Schlupp, I. & Podloucky, R., 1994. Changes in breeding site fidelity – a combined study of conservation and behavior in the common toad Bufo bufo. Biological Conservation, 69: 285–291. SCV, 1997. Primeras soluciones a los atropellos de anfibios en España. Boletín de la Asociación Herpetológica Española, 8: 51–52. Seiler, A., 2001. Ecological effects of roads. A review. Introductory research essay, 9: 1–40. Uppsala. Sinsch, U., 1988. Seasonal changes in the migratory behaviour of the toad Bufo bufo: direction and magnitude of movements. Oecologia, 76: 390–398. – 1989. Migratory behaviour of the common toad Bufo bufo and the natterjack toad Bufo calamita. In: Amphibian and roads: 113–115 (T. E. S. Langton, Ed.). Proceedings of the Toad Tunnel Conference, Rendsburg, Germany. – 1992. Structure and dynamics of a natterjack toad metapopulation (Bufo calamita). Oecologia, 90: 489–499. Slater, F. M., 1989. Amphibian barrier in mid–Wales. In: Amphibian and roads: 175–180 (T. E. S. Langton, Ed.). Proceedings of the Toad Tunnel

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Conference, Rendsburg, Germany. – 1994. Wildlife road casualties. British Wildlife, 5: 214–221. Trombulak, S. C. & Frissell, C. A., 2000. Review of ecological effects of roads on terrestrial and aquatic communities. Conservation Biology, 14: 18–30. Van Gelder, J. J., 1973. A quantitative approach to the mortality resulting from traffic in a population of Bufo bufo. Oecologia, 13: 93–95. Vogel, Z. & Puky, M., 1995. A fast environmental assessment method for the evaluation of road constuction effects on amphibian communities, In: Scientia Herpetologica: 349–351 (G. A. Llorente, A. Montori, X. Santos & M. A. Carretero, Eds.). Asociación Herpetológica Española, Barcelona. Wells, K. D., 1977. The social behaviour of anuran amphibians. Animal Behaviour, 25: 666–693. Wilson, E. O., 1988. Biodiversity. National Academy Press, Washington D.C. Zuiderwijk, A., 1989. Amphibian and reptile tunnels in the Netherlands. In: Amphibian and roads: 67–74 (T. E. S. Langton, Ed.). Proceedings of the Toad Tunnel Conference, Rendsburg, Germany.

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Lack of genetic structure of Cypriot Alectoris chukar (Aves, Galliformes) populations as inferred from mtDNA sequencing data M. Guerrini, P. Panayides, P. Hadjigerou, L. Taglioli, F. Dini & F. Barbanera

Guerrini, M., Panayides, P., Hadjigerou, P., Taglioli, L., Dini, F. & Barbanera, F., 2007. Lack of genetic structure of Cypriot Alectoris chukar (Aves, Galliformes) populations as inferred from mtDNA sequencing data. Animal Biodiversity and Conservation, 30.1: 105–114. Abstract Lack of genetic structure of Cypriot Alectoris chukar (Aves, Galliformes) populations as inferred from mtDNA sequencing data.— The Chukar (Alectoris chukar cypriotes) is the most common game bird in Cyprus. Since 1990 the Cypriot Government has established a restocking program with captive–reared birds. However, this program has not been guaranteed by checking the genetic nature of wild and farmed samples, either in the areas controlled by the Cypriot Government or in northern Cyprus. The sequencing of both Cytochrome–b and Control Region of the mitochondrial DNA was carried out for 61 Cypriot representatives and 14 specimens of the same subspecies from Crete and Israel. Only the A. chukar maternal lineage was found. A partitioning of Cypriot specimens among different clades was not reliably supported, whereas robust bootstrap values weighted for an evolutionary divergence between Cypriot and Cretan Chukars. An overall genetic homogeny of the Cypriot populations was disclosed, whatever their status (captive vs. wild stocks) and origin (Government controlled vs. occupied areas) would be, a higher nucleotide diversity of the wild vs. captive representatives notwithstanding. Key words: Chukar, Control Region, Cytochrome–b, Genetic diversity, mtDNA, Partridges. Resumen Falta de estructura genética en las poblaciones chipriotas de Alectoris chukar (Aves, Galliformes), deducida de los datos de secuenciación del ADNmt.— Una subespecie de la perdiz chucar (Alectoris chukar cypriotes) es el ave de caza más común de Chipre. A partir de 1990 el gobierno chipriota estableció un programa de repoblación utilizando aves criadas en cautividad. No obstante, dicho programa no ha sido avalado mediante la comprobación de la naturaleza genética de muestras tanto de ejemplares salvajes como de granja, ni en las zonas controladas por el gobierno chipriota ni en el norte de Chipre. Se ha llevado a cabo la secuenciación del citocromo–b y de la región de control del ADN mitocondrial de 61 ejemplares chipriotas y de 14 especimenes de la misma subespecie de Creta y de Israel. Sólo se encontró el linaje materno de A. chukar. No se pudo demostrar con fiabilidad el reparto de los especimenes chipriotas en distintos clados, mientras que unos valores bootstrap muy consistentes sustentaban una divergencia evolutiva entre las perdices chucar chipriotas y cretenses. Se reveló la existencia de una homogeneidad genética en las poblaciones chipriotas, cualquiera que fuera su estatus (linajes cautivos frente a salvajes) o su origen (zonas controladas por el gobierno frente a zonas ocupadas), por más que se diera una mayor diversidad de nucleótidos de los ejemplares salvajes frente a los cautivos. Palabras clave: Perdiz chucar, Región de control, Citocromo–b, Diversidad genética, ADNmt, Perdices. (Received: 19 II 07; Conditional acceptance: 14 III 07; Final acceptance: 20 III 07) M. Guerrini, F. Dini & F. Barbanera, Dept. of Biology, Protistology–Zoology Unit, Via A. Volta 6, 56126 Pisa, Italy.– P. Panayides & P. Hadjigerou, Cypriot Game Fund Service, Ministry of Interior, 1453 Nicosia, Cyprus.– L. Taglioli, Dept. of Biology, Anthropology Unit, Via S. Maria 55, 56126 Pisa, Italy. Corresponding author: F. Barbanera. E–mail: fbarbanera@biologia.unipi.it ISSN: 1578–665X

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Introduction The Chukar partridge (Alectoris chukar, Galliformes) is the most common and most popular game bird in Cyprus, the third largest island in the Mediterranean after Sicily and Sardinia. Cyprus also harbours the A. c. cypriotes Hartert, a 1,917 subspecies, which is reported to inhabit the Aegean islands (Crete included), southern Turkey and Israel (Madge & McGowan, 2002). Records of the Chukar in Cyprus date back to the Bronze Age (Watson, 1962). It inhabits a wide area, covering rocky habitats with maquis and/or phrygana between the coastal area and the forested peaks of the Troodos Mountains. Cyprus has the largest A. chukar population in Europe, with a yearly harvest estimated at 254,000–600,000 hunted birds (1986–2006: P. Panayides, pers. comm.). Hunting occurs throughout the Chukar’s large distribution range that is claimed to extend from the eastern Mediterranean throughout central Asia and up to Manchuria (Madge & McGowan, 2002). Due to its limited range within Europe, A. chukar is a Species of European Conservation Concern. The Cypriot population, in particular, is listed as vulnerable (BirdLife International, 2004). The situation was made worse in Cyprus following the severe social–economic changes of 1974, when 37% of the island came under the occupation of Turkey and about 200,000 people were forced to move to the southern region, thus causing considerable stress to wildlife resources in terms of population crowding and land–use changes. Indeed, since that time, Cyprus has experienced a rapid economic growth that has largely contributed to habitat loss because of resort building sprawl, construction of dense road networks, and expansion of agriculture with increased mechanization and pesticide use (World Research Institute, 1992; Panayides, 2005). In addition, there is no doubt that hunting pressure is another important factor accounting for the current status of the Cypriot A. chukar, as since the 1970’s the number of suitable hunting territories has decreased while the number of hunters has almost doubled (presently close to 50,000: Kassinis, 2001). In response to these challenges, in 1990 the Cypriot Game Fund Service launched a Chukar release program using local A. c. cypriotes birds reared at the Stavrouvoni state farm. A genetic study based on Short Tandem Repeats (STR) markers was recently undertaken to evaluate the situation (Tejedor et al., 2005). Despite its heuristic value, several shortcomings were detected in the above–mentioned study: (i) the number of both the specimens (n = 33) and nuclear loci (n = 4) taken into consideration was a serious constraint, (ii) no accurate geographic records for the studied populations were provided, (iii) no comparison between farmed and wild birds was carried out, and (iv) no specimens from Turkish occupied territory were analysed. The present work employed genetic markers whose effectiveness in comparing genetic

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relationships among neighbouring and even geographically distant Alectoris chukar populations has been consistently proved for both their nature and pair–base lengths: the Cytochrome b (Cyt–b) and Control Region (CR) markers of the mitochondrial DNA (mtDNA) (Barbanera et al., 2005; Randi et al., 2006; Barbanera et al., in press). Our results support a close genetic relationships between the A. c. cypriotes populations and provide insights into the general variation characterizing the species Alectoris chukar throughout its range of distribution. Material and methods Sampling Seventy–five A. chukar cypriotes specimens were investigated. Samples (liver) were obtained from wild birds (n = 24) hunted in two Government– controlled regions of Cyprus, namely the Alykes coastal wetland area near Larnaca (n = 12) and the mountains of the Paphos Forest (n = 12). Samples of wild birds hunted in the Turkish controlled part of northern Cyprus (Karpas Peninsula, n = 8) were also collected (fig. 1). The above–mentioned populations were originally considered wild, as they have never been restocked with captive specimens (P. Panayides, pers. com.). We also collected samples (feathers) of captive birds (n = 29), obtained from both state (Stavrouvoni, Larnaca District, n = 12) and private game farms (Theodosis: Ayious Trimithias, Nicosia District, n = 6; Sam: Alassa, Limassol District, n = 6; Vorvoromitas, Agrokipia, Nicosia District: n = 5; see fig. 1). Samples obtained from shot birds were carefully collected in order to avoid the analysis of specimens from the same covey. In order to do so, only one sample per hunting trip was kept for genetic analysis. Samples (liver) from A. chukar specimens hunted in Crete (Greece, n = 7) and in Israel (n = 7) were also investigated to estimate their possible genetic differentiation with respect to the Cypriot populations. Additional samples from Red–legged Partridge (Alectoris rufa, n = 3, liver, Spain), Rock Partridge (A. graeca, n = 2, feathers, Italy) and Barbary Partridge (A. barbara, n = 1, liver, Italy) were also used as references for the remaining Mediterranean Alectoris partridges. The Gene Bank accession codes of the sequences employed in this work are as follows: Cyt–b, from AM492908 to AM492953, from AM084553 to AM084575, AJ586141, AJ586147, AJ586150, AJ586157 and AJ586158; CR: from AM084616 to AM084645, from AM492954 to AM492998, AJ586190, AJ586196, AJ586198, AJ586206 and AJ586207. DNA extraction, PCR amplification and sequencing The total genomic DNA was extracted from liver fragments using Puregene7 Genomic DNA Isolation Kit (Gentra Systems, USA) and from feathers as reported by Barbanera et al. (2005). For each

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Black Sea Republic of Cyprus Mediterranean Sea Crete (Greece)

Cyprus Israel

Northern Cyprus (Turkish controlled area) 3 2 6 1 5 4

15 km

Fig. 1. The studied area in the Mediterranean: A. The relative positions of Crete, Cyprus and Israel are indicated; B. The localities of the sampled Cypriot A. chukar populations are indicated (1. Stavrouvoni state farm; 2. Theodosis private farm; 3. Vorvoromitas private farm; 4. Sam private farm; 5. Alykes Larnaca coastal wetland area; 6. Paphos Forest; 7. Karpas Peninsula, in the Turkish occupied territory). Fig. 1. El área mediterránea estudiada: A. Se indican las situaciones relativas de Creta, Chipre e Israel; B. Se indican las localidades de muestreo de las poblaciones chipriotas de A. chukar: (1. Granja estatal Stavrouvoni; 2. Granja privada Theodosis; 3. Granja privada Vorvoromitas; 4. Granja privada Sam; 5. Humedal costero Alykes Larnaca; 6. Bosque de Paphos; 7. Península de Karpas, en el territorio ocupado por Turquía.

specimen almost the entire Cyt–b gene (1,092 bp, total length = 1,143 bp) and the whole CR were amplified (Barbanera et al., 2005). PCR products were purified using BioRad Kleen Spin Columns and both DNA strands were directly sequenced on an ABI 310 automated sequencer (Applied Biosystems, USA). In order to assess the authenticity of the mtDNA amplifications, possible nuclear sequences of mitochondrial origin were checked by comparing sequences with those directly obtained from purified mtDNA (Barbanera et al., 2005). Specifically, mtDNA was isolated from the following samples: n. 6, 10, 27 and 42 (A. chukar) from Cyprus; n. 4 (A. chukar) from Crete; P01 (A. rufa) from Spain; Uro01 (A. graeca) and Ier03 (A. barbara) from Italy. Phylogenetic data analysis The alignments of Cyt–b and CR sequences from 81 specimens were completed with Clustal (Thompson et al., 1994). The Partition–Homogeneity test as implemented in PAUP* 4.0b10 (Swofford, 2002) was applied to 1,000 replications of an heuristic search with character partitions to determine the statistical validity of combining the two mtDNA genes for the phylogenetic analysis. As the test detected no significant differences among mtDNA gene partitions (P = 0.667), the Cyt–b and CR sequences were analysed as combined mtDNA dataset.

The phylogenetic signal was evaluated (i) by means of the index of substitution saturation (Iss, Xia test with 1,000 replicates: Xia et al., 2003) using DAMBE 4.2.13 software (Xia & Xie, 2001), and (ii) by plotting the number of transitions (Ti) and transversions (Tv) against a corrected genetic distance that was obtained by exporting the relative matrix produced by PAUP into Microsoft Excel. Finally, the software MEGA 3 (Kumar et al., 2004) was employed to compute nucleotides composition, genetic distances and nucleotide diversity ( ). Phylogenetic relationships were inferred using both distance and parsimony methods as implemented in PAUP. Concerning the distance method , the model of DNA substitution that best fitted the data was selected using the software FindModel (Los Alamos National Laboratory, New Mexico, USA: http://hcv.lanl.gov/content/hcv–db/findmodel/ findmodel.html). FindModel is a weighted neighbour joining–based (NJ) procedure set up by Bruno et al. (2000). It was developed as web implementation of the program Modeltest (Posada & Crandall, 1998). The HKY85 algorithm (Hasegawa et al., 1985) with gamma distribution was then singled out according to the Akaike Information Index criterion (Posada & Buckley, 2004), and the calculation of the shape parameter was performed as reported by Sullivan et al. (1995). The Maximum parsimony (MP) procedure was set up as follows: unweighted, with TBR swapping algorithm and random addition

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0.10

Ti and Tv (n)

0.08

0.06

0.04

0.02

0 0

0.02 0.04 0.06 0.08 0.10 0.12 Corrected genetic distance ( –HKY85)

Fig. 2. The number of transitions (ordinates: Ti. Solid square) and transversions (ordinates: Tv. Open square) plotted versus the corrected genetic distance (abscissas: –HKY85 evolutionary model). Fig. 2. Número de transiciones (ordenadas: Ti. Cuadrados sólidos) y transversiones (ordenadas: Tv. Cuadrados huecos) representadas frente a la distancia genética corregida (abscisas: modelo evolutivo –HKY85).

sequence limited to 10 rearrangements per bootstrap replicate. Gaps were treated as fifth base. Multiple MP trees were collapsed to obtain a 50% majority– rule consensus tree. For both kinds of reconstruction a Barbary Partridge sequence was employed as outgroup and the statistical support was evaluated by bootstrapping (BP, with 1,000 resampling steps: Felsenstein, 1985). The partition of the genetic diversity among and within A. chukar populations was investigated by means of the analysis of molecular variance (AMOVA, Arlequin 3.01 software package: Excoffier et al., 2005) using pairwise FST distances of Wright’s (1965) F–statistics. Distance values were plotted on the first two axes of a Principal Components Analysis (PCA) carried out using the Statistica7 ver. 5.0/W Statistica package (Statsoft Inc., USA). The software Arlequin was also used to calculate the haplotype diversity (h) and to check for neutral evolution of the investigated mtDNA sequences (Tajima neutrality test). Results Phylogenetic data The alignment of joint Cyt–b and CR sequences defined a set of 2,256 characters, indels included

(only in the CR). More particularly, the A. chukar Cyt–b sequences were all 1,092 bp long whereas the CR sequences were all 1,154 bp (cf., Randi & Lucchini, 1998). The real mitochondrial nature of the PCR products obtained from total genomic DNA was assessed by (i) comparison with the sequences from isolated mtDNA, (ii) the detected under–representation of guanine (13.4%), and (iii) the absence of indels and/or internal stop codons (only in the Cyt–b). The analysis of the phylogenetic signal did not disclose any saturation. The average number of Ti was 4.4 higher than Tv, outgroup excluded. In the plot of the number of the Ti and Tv versus divergence measured by the –HKY85 evolutionary model, the Ti/Tv ratio was > 1 in the whole distance range (fig. 2). The Iss value (= 0.299) was found to be highly significantly smaller (P < 10–5) than that of the critical Iss (Iss.c, the Iss value at which the sequences begin to fail to recover the true tree) assuming either symmetrical or asymmetrical topology for the phylogenetic reconstructions (Iss.c = 0.843 and Iss.c = 0.820, respectively). Genetic distance analysis with –HKY85 algorithm ( = 0.152) produced the NJ tree (92 variable sites) in figure 3. The BP values calculated by MP procedure were added below internodes, as MP produced a 50% majority–rule consensus

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Animal Biodiversity and Conservation 30.1 (2007)

100 100

A. rufa P 01 Spain A. rufa RP548 Spain A rufa A01 Spain A. graeca Uro01 Italy A. graeca Uro02 Italy

100 100

A. chukar Cyp05,13,17,19,27*,31,34,35,45,48,50,51,54,55,59–60 Cyprus 64 62 62 65

A. chukar Cyp10,24 Cyprus A. chukar Cyp29 Cyprus A. chukar Cyp27,53 Cyprus A. chukar Cyp49 Cyprus A. chukar Cyp09,11,14,22 Cyprus

54 –

64 82

A. chukar Cyp30,32,56 Cyprus A. chukar Cyp20,23,40 Cyprus

66 65

A. chukar Cyp44 A. chukar Cyp25,37,47 Cyprus A. chukar Cyp21,41 Cyprus

A. chukar Cyp18 Cyprus A. chukar Cyp52 Cyprus A. chukar Cyp15 Cyprus 64 A. chukar Cyp36 Cyprus 63 A. chukar Cyp57 Cyprus 100 100 63 A. chukar Cyp12 Cyprus A. chukar Cyp16 Cyprus A. chukar Cyp58 Cyprus A. chukar Cyp02 Cyprus A. chukar Cyp03 Cyprus A. chukar Cyp07 Cyprus A. chukar Cyp39 Cyprus A. chukar Cyp04 Cyprus A. chukar Cyp38 Cyprus A. chukar Cyp42 Cyprus A. chukar Cyp28 Cyprus 73 – 93 92

Alectoris barbara Ier03 Italy

A. chukar Cyp01,04,06,08,26,46 Cyprus A. chukar Isr61,63,67 Israel

A. chukar Isr53 Israel A. chukar Isr64 Israel A. chukar Isr51 Israel

A. chukar Isr58 Israel

0.001 substitutions / site 66 84 73 87

A. chukar Cre05,07 Greece

A. chukar Cre01,04 Greece A. chukar Cre06 Greece

Fig. 3. The neighbour–joining tree computed by PAUP using HKY85 –genetic distances ( = 0.152) among the aligned 2,256 characters (indels included) of the joint Cyt–b and CR sequences. Numbers at the internodes indicate all the bootstrap percentage values computed in both the NJ (above internodes) and 50% majority–rule consensus MP (below internodes) tree. Rectangular boxes show identical sequences. The phylogenetic trees were rooted using an A. barbara sequence. Abbreviations: Cyp. Cyprus; Cre. Crete; Isr. Israel; P01. Mallorca, Spain; A01. Seville, Spain; RP548. Ciudad Real, Spain; Uro01–02. Southern Apennines, Italy; Ier03. Sardinia, Italy. Fig. 3. Árbol de proximidad calculado mediante PAUP utilizando las distancias genéticas –HKY85 ( = 0,152) entre los 2.256 caracteres alineados (incluyendo indels) de las secuencias ensambladas del citocromo–b y la región de control. Las cifras de los internodos indican los valores porcentuales bootstrap calculados mediante NJ (por encima de los internodos) y MP de consenso de la regla de la mayoría del 50% (debajo de los internodos). Los rectángulos indican secuencias idénticas. Los árboles filogenéticos se establecieron utilizando una secuencia de A. barbara. (Para las abreviaturas ver arriba.)

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Guerrini et al.

tree with the same topology as the NJ tree (152 parsimony informative characters; length, L = 372; consistency index, CI = 0.720; retention index, RI = 0.806). All specimens from Cyprus, Israel and Crete clustered in the same clade (NJ, MP: BP = 100%), showing only the mtDNA lineage corresponding to the Chukar phenotype. Both the A. rufa and A. graeca clades clearly diverged with respect to the A. chukar clade (cf., Randi & Lucchini, 1998). Within the A. chukar clade, four clusters supported by BP ranging around 65% and including only Cypriot specimens were found. There was no geographic consistency within these groups, each cluster being formed by specimens from different regions of Cyprus. Most of the A. chukar specimens from Israel had a basal position within the clade, with the exception of three specimens clustering apart (A. chukar Isr61,63,67: NJ, BP = 93%; MP, BP = 92%). All of the specimens from Crete grouped together in the A. chukar clade (NJ, BP = 84%; MP, BP = 87%).

Table 1. Results of the AMOVA analysis for the A. chukar populations: Sv. Source of variation (in %, Ap. Among populations, Wp. Within populations); Cy. Cyprus; I. Israel; Cr. Crete. Tabla 1. Resultados del análisis AMOVA de las poblaciones de A. chukar: Sv. Origen de la variación (en %, Ap. Entre poblaciones, Wp. Dentro de poblaciones); Cy. Chipre; I. Israel; Cr. Creta.

Sv Region

FST

6.5

93.5

0.065

0.078

Cy + I

22.1

77.9

0.221

< 10–5

Cy + Cr

40.5

59.5

0.405

< 10–5

Cy + I + Cr

42.3

57.7

0.420

< 10–5

Cytochrome–b heteroplasmy A mtDNA heteroplasmic event was disclosed in the Cyt–b sequence of the A. chukar Cyp27 specimen. Amplification was obtained from purified mtDNA and direct sequencing disclosed a double peak on the chromatogram of both DNA strands, revealing a single nucleotide polymorphism (Gene Bank accession codes: AM084572 and AM084573). Indeed, at

pos. 504 (cf., Randi, 1996), either guanine or adenine was found (3rd codon pos., no aminoacidic change), the latter being present in all of the Chukars sequenced in this work.

Second component (11.26%)

1.5 Israel

1.1

0.7

0.3

–0.1 –1.2

Cyprus

Crete –0.8

–0.4 –0 0.4 First component (84.50%)

0.8

1.2

Fig. 4. PCA performed using the pairwise FST distances calculated for all A. chukar ingroups of the phylogenetic reconstructions provided in figure 3. Single specimens were grouped according to each population as reported in table 2. Fig. 4. PCA llevado a cabo utilizando las distancias FST en grupos de dos, calculadas para todos los grupos homogéneos de A. chukar de las reconstrucciones filogenéticos de la figura 3. Los ejemplares aislados se agruparon por poblaciones, tal como se indica en la tabla 2.

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Animal Biodiversity and Conservation 30.1 (2007)

Table 2. Estimates of genetic diversity computed using 2,256 characters of joint Cyt–b and CR sequences from nine A. chukar populations: PpS. Population sample size; Pl. Polymorphic sites; T. Tajima neutrality test; H. Haplotypes; Uh. Unique haplotypes; Hd. Haplotype diversity; Nd. Nucleotide diversity. (Standard deviation is reported in brackets.) Tabla 2. Estimas de la diversidad genética calculadas utilizando 2.256 caracteres de secuencias ensambladas del citocromo–b y la región de control de nueve poblaciones de A. chukar: PpS. Tamaño de la muestra de la población; Pl. Lugares polimórficos; T. Test de neutralidad de Tajima; H. Haplotipos; Uh. Haplotipos únicos; Hd. Diversidad de haplotipos; Nd. Diversidad de nucleótidos. (La desviación estándar se indica entre paréntesis.)

PpS (n) Pl (n) Sam farm, Cyprus Stavrouvoni farm, Cyprus

T (D; P)

H (n) Uh (n)

Hd (h)

Nd ( , %)

– 1.010; 0.214

0.800 (0.172)

0.114 (0.044)

– 1.769; 0.013

0.859 (0.087)

0.081 (0.026)

Theodosis farm, Cyprus

– 1.337; 0.054

0.800 (0.172)

0.075 (0.034)

Vorvoromitas farm, Cyprus

0.273; 0.680

0.900 (0.161)

0.090 (0.042)

Alykes Larnaca, Cyprus

– 1.388; 0.082

0.924 (0.057)

0.130 (0.037)

Paphos Forest, Cyprus

0.209; 0.620

0.879 (0.075)

0.125 (0.047)

Karpas Peninsula, Cyprus

– 0.229; 0.439

0.964 (0.077)

0.166 (0.051)

Crete, Greece

– 0.876; 0.267

0.667 (0.160)

0.060 (0.030)

Israel

0.225; 0.597

0.857 (0.137)

0.248 (0.076)

Genetic diversity As reported in table 1, AMOVA indicated that, when only the Cypriot populations were taken into account, 93.5% of the total genetic variability was distributed within populations, and 6.5% among populations (FST index = 0.065). When Israeli or Cretan populations were also analysed, the FST value increased to 0.221 and 0.405, respectively. When all of the A. chukar populations were considered, 57.7% of the total genetic variability was distributed within populations, and 42.3% among populations (FST = 0.420). When the FST distances calculated for the A. chukar sequences were plotted on the first two axes of a PCA (fig. 4), the first two components explained 96% of the total genetic diversity. A significant divergence between the populations from Cyprus, Israel and Crete was disclosed. The genetic distance value calculated between Cypriot and Israeli populations ranged around 0.14%, whereas that between Cypriot and Cretan populations ranged around 0.34%. The alignment of the A. chukar sequences disclosed a total of 35 haplotypes defined by 77 polymorphic sites (table 2). More particularly, 22 haplotypes were unique, most of them (17) being restricted to Cyprus. The haplotype diversity (h) was high, its average value ranging around 0.85. The lowest value (h = 0.67) showed by the Cretan population was different from those of the other populations (Bonferroni post–hoc multiple compari-

sons: one way ANOVA, P < 10–5 and Bonferroni test, P < 0.05). The Israeli population showed the highest value of nucleotide diversity ( = 0.25%: ANOVA, P < 10–5; Bonferroni test, P < 0.05 versus all populations). Among Cypriot representatives, the nucleotide diversity of the Karpas Peninsula population ( = 0.17%, the highest value) differed significantly from those calculated for the Stavrouvoni, Theodosis and Sam farmed stocks (ANOVA, P < 10–5; Bonferroni test, P < 0.05). Finally, with the exception of the mtDNA sequences obtained from the Stavrouvoni population, all the others evolved neutrally (Tajima’s D: table 2). Discussion A great number of travellers’ notes reported that Chukar was abundant in the eastern Mediterranean until the 19th century. Nowadays, Chukar populations have disappeared from several Greek islands. There are a few exceptions, but surviving populations are small and suffering decline due to abandonment of traditional wheat crops, illegal hunting and habitat disappearance or deterioration (Papavangelou et al., 2001). Furthermore, genetic studies dealing with Mediterranean A. chukar populations are scarce (Tejedor et al., 2005; Barbanera et al., in press) when compared to those referring to A. rufa and A. graeca, the only exception being the A. chukar populations colonizing Israel (see Randi et al.,

112

2006 for a review). Disappointingly, such a poor genetic knowledge is potentially harmful for the conservation of the species. As discussed by Frankham (2005), it can lead to misguided management plans because of the risk of introduction of non–endemic, invasive genotypes or subspecies through restocking with captive stocks. Since 1990 the Cypriot A. c. cypriotes populations have been subjected to restocking by the Game Fund (Ministry of Interior, Cyprus). Such a release program originally involved captive stock from Stavrouvoni state farm that originated from eggs collected in the wild. The program was later extended to a restricted number of private farms, which started to rear Chukars under the supervision of the Game Fund. A 2,256 character dataset provided by sequencing of Cyt–b and CR mtDNA markers from 75 partridges that showed the outwardly identifying features of the A. chukar species, was analysed to gain insight into the genetic kinship of Cypriot, Cretan and Israeli populations. According to the "total evidence" approach stating that the phylogenetic analysis should be performed on a combined dataset using all of the possible evidence (Kluge & Wolf, 1993), the tree reconstruction was accomplished using previously jointed Cyt– b and CR sequences. The results showed a flawless correlation between the mtDNA lineage and the outward Chukar appearance of the analyzed representatives (fig. 3). Taking into account that anthropogenic hybridization between A. chukar and A. rufa is a widespread phenomenon even in small islands, whatever the parental origin of the introgressive swarms could be (Barbanera et al., 2005; Barbanera et al., in press), the absence of allochthonous mtDNA lineages is a promising result for the conservation of the native A. chukar genome in the eastern Mediterranean. Further, no robust genetic differentiation between farmed and wild Cypriot populations was found (BP < 70%, fig. 3; cf., Felsestein, 2004), also when specimens from north Cyprus were considered. Within the A. chukar clade, only a few Israeli representatives clearly clustered apart from the remaining ingroups (BP > 90%, fig. 3). This might be related to the known genetic differentiation due to geographical isolation of Israeli Chukar populations occurring across the north Negev ecotone (Randi et al., 2006). The AMOVA analysis of the Cypriot A. chukar showed that the very large majority of the genetic variability was distributed among individuals, the populations thus representing a largely homogeneous group. Only when Cretan and Israeli Chukars were also taken into account in the analysis, was an overall, significant divergence found (table 1). On one hand, the differentiation that was disclosed between Cypriot and Cretan populations (figs. 3, 4: average genetic distance = 0.34%) was in agreement with the morphological evidence reporting that Cretan A. c. cypriotes specimens are smaller and darker than Cypriot specimens (Cramp & Simmons, 1980). Such a slightly variant phenotype has accounted for the past assignation of the Cre-

Guerrini et al.

tan population to the A. c. scotti subspecies, which is no longer considered valid taxon (Madge & McGowan, 2002). On the other hand, the differentiation between Israeli and Cypriot populations (table 1; average genetic distance = 0.14%) was likely due to the robust divergence showed by a few Israeli representatives coupled to the limited size of the relative sampling (figs. 3, 4). Hence, a deeper investigation is needed to definitively clarify the genetic relationships between Cypriot and Israeli A. chukar. The genetic information was gained from the total number of haplotypes (n = 35, unique haplotypes = 22; table 2), which was comparable to that found in a similar work where several Israeli A. chukar populations were analyzed (Randi et al., 2006). However, this result was obtained with a lower number of samples and a longer segment of sequenced mtDNA (Randi et al., 2006: 216 samples from five populations, 444 characters, only CR; this study: 75 samples from nine populations, 2,256 characters, Cyt–b and CR). Moreover, in the present work, a single nucleotide polymorphism for the Cyt–b sequence of the A. chukar Cyp27 specimen was found. To our knowledge, this represents the first case of mtDNA heteroplasmy for a coding gene in birds, the other event recorded in the literature dealing with the CR sequence of a razorbill (Alca torda: Moum & Bakke, 2001). To sum up, the Cypriot populations showed a large haplotype diversity that, however, did not differ significantly from the Israeli representatives. Although the nucleotide diversity of the wild Cypriot populations was significantly higher than that disclosed in the captive birds, the whole range of detected variation (between 0.07%, Theodosis farm population, and 0.17%, Karpas Peninsula population) dealt with very low percentages (table 2). Hence, the high rates of the haplotype diversity coupled to the low values of the nucleotide diversity confirmed once more the genetic homogeny of the Cypriot populations. The data provided in this work suggest that Cypriot A. chukar should be considered as a single unit for conservation purposes; whether their representatives (i) are captive or wild, (ii) inhabit southern or northern part of the island, or (iii) belong or not to restocked populations does not appear to be of relevance. Although the genetic markers used in the present work follow a maternal inheritance, our results support a high rate of genetic flux among the studied Chukar populations throughout the entire island of Cyprus (cf., Tejedor et al., 2005). This, in turn, might be related to the actions undertaken by the Cypriot Government to preserve the local A. chukar breeding stock, such as, for instance, the creation of well–distributed game reserves working as breeding banks. These areas, where hunting is strictly forbidden, occupy 30% of Government– controlled territory. Nevertheless, the value of the nucleotide diversity index estimated for the wild populations was found to be higher than that calculated for the captive populations. Conventional wis-

Animal Biodiversity and Conservation 30.1 (2007)

dom suggests that a regular renewal of the captive breeding stocks by means of selected drawing from wild populations would not be just an academic exercise. Finally, the occurrence of genetic differentiation particularly between Cypriot and Cretan A. chukar populations suggests that translocation of birds throughout the eastern Mediterranean should not be recommended, although Cyprus and southern Aegean islands officially harbour the same subspecies (Madge & McGowan, 2002). In conclusion, a large data set will hopefully be available following the STR markers–based study that the University of Pisa is developing in collaboration with the Cypriot Ministry of the Interior, the Greek Hunting Federation of Macedonia–Thrace and the Bahauddin Zakariya University (Multan, Pakistan). The goal of this study is the identification of both Mediterranean and Asian A. chukar populations in order to bring the exchange of commercial stocks into line with knowledge of the genetic kinship, thus conferring to their management the status of a scientific process. Acknowledgements The authors are particularly grateful to: M. Miltiadou (BirdLife Cyprus) and M. Xenophontos for their helpful comments on this paper; C. Sokos and P. Birtsas (Hunting Federation of Macedonia–Thrace, Thessaloniki, Greece) for the A. chukar samples from Crete; E. Randi (National Wildlife Institute, Bologna, Italy) for the A. chukar samples from Israel; J. J. Negro (Estación Biologica de Doñana, Seville, Spain) for the A. rufa samples Spain; M. Paganin (Urogallo stock–farm, Asiago, Italy) for the A. graeca samples from Italy; M. Muzzeddu (Wildlife Recovery Centre, Sassari, Italy), and T. Corrias for the A. barbara sample from Sardinia (Italy). This work was supported by grants from the Cypriot Game Fund Service, the Ministry of the Interior, Nicosia, Cyprus and the Province of Leghorn, INTERREG III Toscana–Corsica–Sardegna. References Barbanera, F., Negro, J. J., Di Giuseppe, G., Bertoncini, F., Cappelli, F. & Dini, F., 2005. Analysis of the genetic structure of red–legged partridge (Alectoris rufa, Galliformes) populations by means of mitochondrial DNA and RAPD markers: a study from central Italy. Biological Conservation, 122: 275–287. Barbanera, F., Guerrini, M., Hadjigerou, P., Panayides, P., Sokos, P., Wilkinson, P., Khan, A. A., Khan, B. Y., Cappelli, F. & Dini, F. (in press). Genetic insight into Mediterranean chukar (Alectoris chukar, Galliformes) populations inferred from mitochondrial DNA and RAPD markers. Genetica. Birdlife International, 2004. Birds in Europe: population estimates, trends and conservation status.

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BirdLife Conservation Series, vol. 12. BirdLife International, Wageningen, The Netherlands. Bruno, W. J., Socci, N. D. & Halpern, A. L., 2000. Weighted Neighbor Joining: A Likelihood–Based Approach to Distance–Based Phylogeny Reconstruction. Molecular Biology and Evolution, 17: 189–197. Cramp, S. & Simmons, K. E. L., 1980. Handbook of the Birds of Europe, the Middle East and North Africa, vol. 2, The Birds of the Western Paleartic. Oxford Univ. Press, Oxford. Excoffier, L., Laval, G. & Schneider, S., 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47–50. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783–791. – 2004. Inferring Phylogenies. Sinauer Associates, Inc. Publishers Sunderland, Massachusetts. Frankham, R., 2005. Genetics and extinction. Biological Conservation, 126: 131–140. Hasegawa, M., Kishino, H., Yano, T.–A., 1985. Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22: 160–174. Kassinis, N., 2001. Chukar partridge status and conservation in Cyprus. In: Proceedings of the Symposium on the status, management and conservation of the species Alectoris, Black Francolin, Thrush, Quail and Turtle Dove in the Mediterranean Region: 84–89 (N. Kassinis & P. Panayides, Eds). The Cypriot Game Fund Service, Ministry of Interior, Nicosia, Cyprus. Kluge, A. G. & Wolf, A. J., 1993. Cladistics: What’s in a word ? Cladistics, 9: 183–199. Kumar, S., Tamura, K. & Nei, M., 2004. MEGA3: Integrated Software for Molecular Evolutionary Genetics Analysis and Sequence Alignment. Briefings in Bioinformatics, 5: 150–163. Madge, S. & McGowan, P., 2002. Pheasants, partridges and grouse. A and C Black Ltd., London. Moum, T. & Bakke, I., 2001. Mitochondrial control region structure and single site heteroplasmy in the razorbill (Alca torda; Aves). Current Genetics, 39: 198–203. Panayides, P., 2005. Six Aspects of Land Use and Development Activity that Result in Adverse Effects to Cypriot Wildlife Resources. In: Proceedings of the XXVth International Congress of the International Union of Game Biologists and the IXth Symposium Perdix: 76–90 (E. Hadjisterkotis, Ed.). Government Printing Office, Ministry of Interior, Cyprus. Papaevangelou, E., Thomaides, C., Handrinos, G. & Haralambides, A., 2001. Status of partridges (Alectoris and Perdix) species in Greece. Game and Wildlife Science, 18: 253–260. Posada, D. & Crandall, K. A., 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14: 817–818. Posada, D. & Buckley, T. R., 2004. Model selection and model averaging in phylogenetics: advan-

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Animal Biodiversity and Conservation 30.1 (2007)

Animal Biodiversity and Conservation

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Els treballs seran presentats en format DIN A–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manuscrits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat. El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona. Els caràcters cursius s’empraran per als noms científics de gèneres i d’espècies i per als neologis mes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona. Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú. Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri. Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase. Les dates s’indicaran de la forma següent: 28 VI 99; 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30). S’evitaran sempre les notes a peu de pàgina.

Normes de publicació Els treballs s'enviaran preferentment de forma electrònica (abc@bcn.cat). El format preferit és un document Rich Text Format (RTF) o DOC que inclo gui les figures (TIF). Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció. Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investiga cions originals no publicades anteriorment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors. Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el progra ma utilitzat (preferiblement en Word). Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat. El primer autor rebrà 50 separates del treball sense càrrec a més d'una separata electrònica en format PDF. ISSN: 1578–665X

Format dels articles Títol. El títol serà concís, però suficientment indicador del contingut. Els títols amb designacions de sèries numèriques (I, II, III, etc.) seran acceptats previ acord amb l'editor. Nom de l’autor o els autors. Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva. Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància. Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellanoparlants. Palabras clave en castellà. Adreça postal de l’autor o autors. (Títol, Nom, Abstract, Key words, Resumen, Pala bras clave i Adreça postal, conformaran la primera pàgina.)

Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball. Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mèto des d’estudi i d’anàlisi de les dades i zona d’estudi. Resultados. En aquesta secció es presentaran úni cament les dades obtingudes que no hagin estat publicades prèviament. Discusión. Es discutiran els resultats i es compa raran amb treballs relacionats. Els suggeriments de recerques futures es podran incloure al final d’aquest apartat. Agradecimientos (optatiu). Referencias. Cada treball haurà d’anar acompanyat de les referències bibliogràfiques citades en el text. Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. La relació de referències bibliogràfiques d’un treball

serà establerta i s’ordenarà alfabèticament per autors i cronològicament per a un mateix autor, afegint les lletres a, b, c,... als treballs del mateix any. En el text, s’indicaran en la forma usual: "...segons Wemmer (1998)...", "...ha estat definit per Robinson & Redford (1991)...", "...les prospeccions realitzades (Begon et al., 1999)..." Taules. Les taules es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista. Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3, etc. i han de ser sempre ressen yades en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels au tors. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es reprodueixen bé. Peus de figura i capçaleres de taula. Els peus de figura i les capçaleres de taula seran clars, concisos i bilingües en la llengua de l’article i en anglès. Els títols dels apartats generals de l’article (Intro ducción, Material y métodos, Resultados, Discusión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols. Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules). Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una institució pública. Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

Animal Biodiversity and Conservation 30.1 (2007)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter disciplinar, publicada desde 1958 por el Museo de Zoología de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxonomía, morfología, biogeografía, ecología, etología, fisiología y genéti ca) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con especies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos. Animal Biodiversity and Conservation está re gistrada en todas las bases de datos importantes y además está disponible gratuitamente en internet en http://www.bcn.cat/ABC, lo que permite una difusión mundial de sus artículos. Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siem pre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo. Una vez aceptado, el trabajo pasará a ser propie dad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reprodu cida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@bcn.cat). El formato preferido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras (TIF). Si se opta por la versión im presa, deberán remitirse cuatro copias juntamente con una copia en disquete a la Secretaría de Redacción. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre investigaciones originales no publicadas anteriormente y que se somete en exclusiva a Animal Biodiversity and Conservation. En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesa rios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores. Cuando el trabajo sea aceptado los autores de berán enviar a la Redacción una copia impresa de la versión final junto con un disquete del manuscrito preparado con un procesador de textos e indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán ISSN: 1578–665X

III

remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modifica ciones sustanciales en las pruebas de imprenta, intro ducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en formato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado. El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofrece, sin cargo ningu no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitándose siempre la primera persona. Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común. Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo. Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase. Las fechas se indicarán de la siguiente forma: 28 VI 99; 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30). Se evitarán siempre las notas a pie de página. Formato de los artículos Título. El título será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designaciones de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consen timiento del editor. Nombre del autor o autores. Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esencia del manuscrito (introducción, material, métodos, resulta dos y discusión). Se evitarán las especulaciones y las citas bibliográficas. Irá encabezado por el título del trabajo en cursiva. Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia. © 2007 Museu de Ciències Naturals

Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablantes. Palabras clave en castellano. Dirección postal del autor o autores. (Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.) Introducción. En ella se dará una idea de los ante cedentes del tema tratado, así como de los objetivos del trabajo. Material y métodos. Incluirá la información referente a las especies estudiadas, aparatos utilizados, me todología de estudio y análisis de los datos y zona de estudio. Resultados. En esta sección se presentarán úni camente los datos obtenidos que no hayan sido publicados previamente. Discusión. Se discutirán los resultados y se compara rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado. Agradecimientos (optativo). Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publicaciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773 * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University.

* Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. Las referencias se ordenarán alfabéticamente por autores, cronológicamente para un mismo autor y con las letras a, b, c,... para los trabajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospecciones realizadas (Begon et al., 1999)..." Tablas. Las tablas se numerarán 1, 2, 3, etc. y se reseñarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista. Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc. y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto. Deben evitarse las figuras tridimensionales. Tanto los mapas como los dibujos deben incluir la escala. Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien. Pies de figura y cabeceras de tabla. Los pies de figura y cabeceras de tabla serán claros, concisos y bilingües en castellano e inglés. Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Discusión, Agradecimientos y Referencias) no se numerarán. No utilizar más de tres niveles de títulos. Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas. Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública. Se recomienda a los autores la consulta de fascícu los recientes de la revista para seguir sus directrices.

Animal Biodiversity and Conservation 30.1 (2007)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal which has been published by the Zoological Mu seum of Barcelona since 1958. It includes empirical and theoretical research in all aspects of Zoology (Systematics, Taxonomy, Morphology, Biogeography, Ecology, Ethology, Physiology and Genetics) from all over the world with special emphasis on studies that stress the relevance of the study of Conservation Biology. The journal does not publish catalogues, lists of species (with no other relevance) or punctual records. Studies about rare or protected species will not be accepted unless the authors have been granted all the relevant permits. Each annual volume consists of two issues. Animal Biodiversity and Conservation is registered in all principal data bases and is freely available online at http://www.bcn.cat/ABC, thus assuring world–wide access to articles published therein. All manuscripts are screened by the Executive Editor, an Editor and two independent reviewers in order to guarantee the quality of the papers. The process of review is rapid and constructive. Once accepted, papers are published as soon as practicable, usually within 12 months of initial submission. Upon acceptance, manuscripts become the prop erty of the journal, which reserves copyright, and no published material may be reproduced without quoting its origin.

Manuscripts must be presented on A–4 format page (30 lines of 70 spaces each) with double spacing. Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been accepted. The text may be written in English, Spanish or Catalan. Authors are encouraged to send their con tributions in English. The journal provides a FREE service of correction by a professional translator specialized in scientific publications. Care should be taken in using correct wording and the text should be written concisely and clearly. Wording should be impersonal, avoiding the use of the first person. Italics must be used for scientific names of genera and species as well as untranslatable neologisms. Quotations in whatever language used must be typed in ordinary print between quotation marks. The name of the author following a taxon should also be written in small print. The common name of the species should be writ ten in capital letters. When referring to a species for the first time in the text, both common and scientific names must be given when possible. Place names may appear either in their original form or in the language of the manuscript, but care should be taken to use the same criteria throughout the text. Numbers one to nine should be written in full in the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence. Dates must appear as follows: 28 VI 99, 28,30 VI 99 (days 28th and 30th), 28–30 VI 99 (days 28th to 30th). Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (abc@ bcn.cat). The preferred format is a document Rich Text Format (RTF) or DOC, including figures (TIF). In the case of sending a printed version, four copies should be sent together with a copy on a computer disc to the Editorial Office. A cover letter stating that the article reports on original research not published elsewhere and that it has been submitted exclusively for consi deration in Animal Biodiversity and Conservation is also necessary. When animal manipulation has been necessary, the cover letter should also especify that the authors follow current norms on the protection of animal species and that they have obtained all relevant permissions. Authors may suggest referees for their papers. Once an article has been accepted, authors should send a printed copy of the final version together with a disc. Please identify software (preferably Word). Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days. Expenses due to any substantial alterations of the proofs will be charged to the authors. The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format.

ISSN: 1578–665X

Formatting of articles Title. The title must be concise but as informative as possible. Part numbers (I, II, III, etc.) should be avoided and will be subject to the Editor’s consent. Name of author or authors. Abstract in English, no longer than 12 typewritten lines (840 spaces), covering the contents of the article (introduction, material, methods, results and discussion). Speculation and literature citation must be avoided. Abstract should begin with the title in italics. Key words in English (no more than six) should express the precise contents of the manuscript in order of importance. Resumen in Spanish, translation of the Abstract. Summaries of articles by non–Spanish speaking authors will be translated by the journal on request. Palabras clave in Spanish. Address of the author or authors. (Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.) Introduction. The introduction should include the historical background of the subject as well as the aims of the paper.

Material and methods. This section should provide relevant information on the species studied, materials, methods for collecting and analysing data and the study area. Results. Report only previously unpublished results from the present study. Discussion. The results and their comparison with related studies should be discussed. Suggestions for future research may be given at the end of this section. Acknowledgements (optional). References. All manuscripts must include a bibliogra phy of the publications cited in the text. References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. References must be set out in alphabetical and

chronological order for each author, adding the letters a, b, c,... to papers of the same year. Bibliographic citations in the text must appear in the usual way: "...according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the prospections that have been carried out (Begon et al., 1999)..." Tables. Tables must be numbered in Arabic numerals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal. Figures. All illustrations (graphs, drawings or pho tographs) must be termed as figures, numbered consecutively in Arabic numerals (1, 2, 3, etc.) and with reference in the text. Glossy print photographs, if essential, may be included. Colour photographs may be published but its publication will be charged to authors. Maximum size of figures is 15.5 cm width and 24 cm height. Figures will not be tridimensional. Both maps and drawings must include scale. The preferred shadings are white, black and bold hatching. Avoid stippling, which does not reproduce well. Legends of tables and figures. Legends of tables and figures must be clear, concise, and written both in English and Spanish. Main headings (Introduction, Material and methods, Results, Discussion, Acknowledgements and Refe rences) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages including figures and tables. If the article describes new taxa, type material must be deposited in a public institution. Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 30.1 (2007)

VII

Animal Biodiversity and Conservation Subscription Form  Please enter our subscription to Animal Biodiversity and Conservation  66 e Spain  69 e Europe  76 e rest of world  Single use subscription:  21 e Spain  24 e Europe  31 e rest of world  Please despatch my issues by air mail (supplement of 6 e for outside Europe)

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Dept. of Scientific Publications Museu de Ciències Naturals de la Ciutadella Psg. Picasso s/n 08003 Barcelona, Spain

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 30.1 (2007)

Welcome to the electronic version of Animal Biodiversity and Conservation

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http://www.bcn.cat/ABC

Animal Biodiversity and Conservation joins the recent worldwide Open Access Initiative of providing a permanent online version free of charge and access barriers. This is the result of the growing point of view that open access to research is essential for efficient and rapid scientific communication.

ABC alert, a free alerting service, provides eâ&#x20AC;&#x201C;mail information on the latest issue. To sign on for this service, please send an eâ&#x20AC;&#x201C;mail to: abc@bcn.cat

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Les cites o els abstracts dels articles d’Animal Biodiversity and Conservation es resenyen a / Las citas o los abstracts de los artículos de Animal Biodiversity and Conservation se mencionan en / Animal Biodiversity and Conservation is cited or abstracted in: Abstracts of Entomology, Agrindex, Animal Behaviour Abstracts, Anthropos, Aquatic Sciences and Fisheries Abstracts, Behavioural Biology Abstracts, Biological Abstracts, Biological and Agricultural Abstracts, Current Primate References, DIALNET (Difusión de Alertas en la Red), DOAJ (Directory of Open Access Journals), Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, RACO (Revistes Catalanes amb Accés Obert), Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 30.1 (2007) ISSN 1578–665X

1–5 G. Moreno–Rueda & M. Pizarro Census method for estimating the population size of the endemic and threatened land snail Iberus gualtieranus gualtieranus

71–81 Forum S. Guallar Un método para cuantificar las contribuciones de los colaboradores en las publicaciones científicas

7–27 H. Romo, M. L. Munguira & E. Gracía–Barros Area selection for the conservation of butterflies in the Iberian Peninsula and Balearic Islands

83–96 J. M. Lobo, B. Guéorguiev & E. Chehlarov Convergences and divergences between two European mountain dung beetle assemblages (Coleoptera, Scarabaeoidea)

29–41 J. Palacio–Núñez, J. R. Verdú, E. Galante, D. Jiménez–García & G. Olmos–Oropeza Birds and fish as bioindicators of tourist disturbance in springs in semi–arid regions in Mexico: a basis for management

97–104 X. Santos, G. A. Llorente, A. Montori, M. A. Carretero, M. Franch, N. Garriga & A. Richter–Boix Evaluating factors affecting amphibian mortality on roads: the case of the Common Toad Bufo bufo, near a breeding place

43–51 J. R. Peluffo, A. M. Rocha & M. C. Moly de Peluffo Species diversity and morphometrics of tardigrades from a medium–size city in the Neotropical Region: Santa Rosa (La Pampa, Argentina)

105–114 M. Guerrini, P. Panayides, P. Hadjigerou, L. Taglioli, F. Dini & F. Barbanera Lack of genetic structure of Cypriot Alectoris chukar (Aves, Galliformes) populations as inferred from mtDNA sequencing data

53–70 A. Viñolas & G. Masó Nuevas especies de los géneros Trichodesma LeConte, 1861 y Gastrallus Jacquelin du Val, 1860, del África Austral (Coleoptera, Anobiidae)