Animal Biodiversity and Conservation issue 29.1 (2006)

Formerly Miscel·lània Zoològica

2006

and

Animal Biodiversity Conservation 29.1

"Idée gaura (Idea gaura)" Le Règne Animal par Georges Cuvier; Paris: Fortin, Masson et Cie, Librairies; Pl. 133 Insectes

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 E–mail abc@mail.bcn.es

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 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 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 29.1, 2006 © 2006 Museu de Ciències Naturals, 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 The journal is freely available online at: http://www.bcn.cat/ABC

Animal Biodiversity and Conservation 29.1 (2006)

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Natural history and morphometry of the Cuban iguana (Cyclura nubila Gray, 1831) in Cayo Sijú, Cuba K. Beovides–Casas & C. A. Mancina

Beovides–Casas, K. & Mancina, C. A., 2006. Natural history and morphometry of the Cuban iguana (Cyclura nubila Gray, 1831) in Cayo Sijú, Cuba. Animal Biodiversity and Conservation, 29.1: 1–8.

Abstract Natural history and morphometry of the Cuban iguana (Cyclura nubila Gray, 1831) in Cayo Sijú, Cuba.— The report presents data about the Cuban iguana population (Cyclura nubila nubila) inhabiting Cayo Sijú, an 88 ha island off the southwest coast of Cuba. Population densities estimated using strip transects were higher in xerophytic coastal scrub (6.72 ± 6.25 iguanas/ha) than in typical sand vegetation (3.63 ± 2.71 iguanas/ha) and mangrove forests (2.9 ± 2.9 iguanas/ha). The total population for the cay was estimated at 350 individuals with an adult biomass of approximately 11.67 kg/ha. Densities varied minimally between three habitat types and between the wet and dry seasons. No significant density fluctuations were found one month after Hurricane Ivan affected the cay. Iguana burrows were encountered most frequently in beach dunes. Analysis of 30 scat samples revealed eight species of plants, with the fruits of Chrysobalanum icaco and the leaves of Batis maritima being the most frequently identified items. The remains of crab (Cardisoma guandhumi) and insects of the order Hemiptera were also present in scat samples. Sexual dimorphism was evident in this population, with males being significantly larger in eight morphological variables. The snout–vent length measurements were larger in this population than in those reported in two cays off the south coast of Cuba.

Key words: Cuban iguana, Cyclura nubila nubila, Ecology, Morphometry, Diet.

Resumen Historia natural y morfometría de la iguana cubana (Cyclura nubila Gray, 1831) en Cayo Sijú, Cuba.— En este trabajo se presentan datos sobre una población de iguana cubana (Cyclura nubila nubila) que habita en Cayo Sijú. Este pequeño cayo, de aproximadamente 88 ha, se encuentra al sur de la costa más occidental de Cuba. La densidad de población, estimada mediante transectos, resultaba mayor en el matorral xeromorfo costero (6.72 ± 6.25 iguanas/ha) que en la vegetación típica de la costa arenosa (3.63 ± 2.71 iguanas/ha) y los manglares (2.9 ± 2.9 iguanas/ha). Estimamos que en el cayo existe una población total de 350 iguanas y una biomasa de iguanas adultas de unos 11.67 kg/ha. Las densidades mostraron poca variación entre los tres tipos de hábitat y entre las estaciones seca y húmeda. No se hallaron fluctuaciones significativas un mes después de que el huracán Iván afectara al cayo. Se encontró que la mayoría de los refugios de las iguanas estaba en las dunas de la playa. Se identificaron ocho especies de plantas en 30 muestras fecales analizadas, siendo los frutos de Chrysobalanum icaco y las hojas de Batis maritima los elementos más frecuentes; además se encontraron restos de cangrejos (Cardisoma guandhumi) e insectos del orden Hemiptera. En esta población el dimorfismo sexual era evidente, siendo los machos mayores en ocho variables morfológicas. En ella se daban mayores valores de longitud hocico–cloaca que en otras que habitan en dos cayos de la costa sur cubana.

Palabras clave: Iguana cubana, Cyclura nubila nubila, Ecología, Morfometría, Dieta.

(Received: 21 II 05; Conditional acceptance: 11 IV 05; Final acceptance: 25 VI 05) Karen Beovides–Casas, Empresa para la Protección de la Flora y la Fauna, MINAGRI, Av. Boyeros esquina Capdevila # 12555, Municipio de Boyeros, Ciudad de La Habana, Cuba.– Carlos A. Mancina, Inst. de Ecología y Sistemática, CITMA. Carretera de Varona Km 3 ½, Capdevila, Municipio de Boyeros, Ciudad de La Habana, Cuba.

Corresponding author: Karen Beovides–Casas. E–mail: karen@ffauna.sih.cu

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction West Indian rock iguanas (genus Cyclura) form a unique group of nine species and 15 subspecies inhabiting tropical dry forests in the Greater Antilles, Caiman Islands and the Bahamas (Etheridge, 1982; Alberts, 2000). These iguanas are among the world’s most endangered lizards, primarily as a result of habitat degradation and the negative effects of exotic species (Henderson, 1992; Alberts, 2000). Rock iguanas are the largest native herbivores on many islands; they are therefore important elements of the ecosystems they inhabit for their high biomass and their role in dispersing seeds and enhancing seed germination (Hartley et al., 2000; Iverson, 1985).

Cyclura nubila has two subspecies; C. n. caymanensis is native from two islands, Little Cayman and Cayman Brac, and C. n. nubila (wide) is distributed on Cuba. Mitochondrial DNA analysis, scale characters, color patterns, geographic and reproductive isolation, recently led Burton (2004) to propose that Cyclura nubila lewisi on Grand Cayman, can be considered a distinct species. The Cuban iguana is well distributed around Cuba (Rodríguez–Schettino, 1999), mainly in xerophilic coastal areas, but relatively safe populations are found only in some cays along the north and south and in isolated protected areas of the mainland. Although it is included in the IUCN Vulnerable category (Berovides et al., 1996; Alberts, 1999), Cyclura nubila nubila shows higher abundant populations than the other species of the genus; the total population of this subspecies in Cuba was estimated at 40,000 to 60,000 individuals (Perera, 2000). This subspecies has been also introduced on Islas Magueyes, southwest of Puerto Rico (Christian, 1986).

Given that relative healthy populations still exist in the wild, Cuban iguana can serve as a valuable model to develop conservation strategies for other endangered rock iguanas (Alberts, 2000). The goal of this study was to estimate the density and characterize the morphometry of the Cuban iguana population in Cayo Sijú, as well as to determine aspects of its natural history. This information could be essential for future conservation and management programs of the Cuban iguana on Cayos de San Felipe.

Material and methods Study area Cayos de San Felipe is a microarchipelago off the southwest coast of Cuba; it is comprised of 40 cays and islets with a total area of 42,900 ha (Snap, 2002). Cayo Sijú (fig. 1) is a small cay with an overall area of 88.25 hectares. This cay is characterized by three habitat types: mangrove forests, xerophytic coastal scrub, and sand vegetation. The mangrove forests cover 60% of the cay surface and the predominant plants are Rhizophora mangle and

Beovides–Casas & Mancina

Avicennia germinans. The xerophytic coastal scrub covers 25% and it is located in the central zone of the cay; scrub communities are represented primarily by Chrysobalanum icaco, Metopium toxiferum, and Trinax radiate. The rest of Cayo Sijú consists of beaches where sand vegetation prevails.

Methods We visited Cayo Sijú in February, April, June, July and August, 2004. Twelve transects were made each month: two in the mangrove forest, five in the xerophytic coastal scrub, and five in the sand vegetation. The transects were used to determine the density of iguanas per habitat as well as burrow density; a total of 60 transects were run during the course of the study. The transect was 500 m long and 10 or 20 m wide, depending on the density of the vegetation; transects were made between 10:00 and 13:00 hrs. Density was estimated by dividing the number of iguanas observed by the area of the transect (Iverson, 1979: 334). A trip in October 2004 allowed us to determine the population status of the iguanas one month after the cay was damaged

by Hurricane Iván. This hurricane was a category 5 of the Saffir–Simpson scale, with winds of up to 250 km/h, and a sea level increase of up to 2.5 m.

Thirty scat samples, corresponding to June 2004, were analyzed. The samples were examined under dissecting microscope, and the vegetable remains were compared with reference material collected in the study area.

Morphology Forty–four individuals were captured (26 males and 18 females), by means of fishing nets or by noosing.

All lizards were marked and released after measures. For all specimens, we recorded the following morphological variables to the nearest 0.1 mm: total length, snout–vent length (SVL), tail length, humerus length, femur length, head length, head width, and body mass to the nearest 0.1 kg. The sex of the iguanas was determined by secondary sexual characters and cloacal probing. All individuals without defined secondary sexual characters and those not reaching more than 23 cm of SVL were considered juvenile (Perera, 1984). The morphological analyses examining sexual dimorphism were restricted to adults (over 35 cm SVL in males, and 30 cm SVL in females; see Perera, 1984). Literature data of average snout–vent lengths of adult males and females were used to determine differences in size among four Cuban iguana populations (Cayo Sijú, Beovides–Casas & Mancina, this study; Cayo Rosario, González et al., 2001; Cayo Largo del Sur, Perera, 1984; Cayo Ballenato, Beovides, unpublished data). The SVL was used instead of body mass because the presence of eggs in females and fat bodies in either sex can affect estimates among populations. We used published data only if the mean, standard deviation, and sample size were available.

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Animal Biodiversity and Conservation 29.1 (2006)

N 0

E

W

100

200 km

S

Cayos de San Felipe

Cayo Sijú Fig. 1. Map of Cayos de San Felipe, southwest of Cuba.

Fig. 1. Mapa de los Cayos de San Felipe, al sudoeste de Cuba.

Statistics

Results

A Kruskal–Wallis and Mann–Whitney U test were used to evaluate differences in the density between habitats and across two seasons, respectively. The seasonal analysis was performed combining the data of each month per season (dry: February and April, and wet: June, July and August). We used unpaired two–tailed t–tests to test for sexual size dimorphism; differences in the snout–vent length were estimated for four populations of Cuban iguanas using a one–way ANOVA as well as multiple t–tests (Tukey test). All statistical tests were conducted using Statistical v.

6.0 (StatSoft, 2001).

The density of Cuban iguana on Cayo Sijú was 5.11 ± 5.04 iguanas/ha, varying between 2.43 ± 3.4 in February and 7.75 ± 6.7 in June. The iguanas were observed in the three available habitats, although the xerophytic coastal scrub showed the highest density. No significant differences were found between the three habitats (H = 3.53, df = 2, p = 0.17) (fig. 2). Contrary to the overall density, the density of juvenile iguanas showed significant differences among the habitats (H = 8.89, df = 2, p = 0.011), with higher values in the xerophytic coastal scrub (fig. 2). Based on the density data for each transect and the body mass of all adult

9

Juvenile

Density (iguanas/ha)

8 Adult

7 6 5 4 3 2 1 0 Sand vegetation

Xerophytic scrub

Mangrove forest

Fig. 2. Density of iguanas, Cyclura nubila, in three habitats on Cayo Sijú, Cayos de San Felipe, Cuba. Values are shown as the mean and the vertical line indicates the standard deviation.

Fig. 2. Densidad de iguanas, Cyclura nubila, en tres hábitats de Cayo Sijú, Cayos de San Felipe, Cuba.

Las barras representan los valores medios y las líneas verticales la desviación estándar.

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16 14 Density (iguanas/ha)

iguanas captured (including both sexes), we estimated an adult biomass of approximately 11.67 kg/ha in the cay, with an estimate per habitat of about 13.88 kg/ha in the xerophytic scrub, 10.13 kg/ha in sand vegetation, and 9.03 kg/ha in the mangrove forests.

The density of iguanas was higher in the surveys corresponding to the wet season in the three habitats (fig. 3), although only the sand vegetation showed significant differences in seasonal density (U = 23.5, p = 0.017).

When iguana density in August (before the Hurricane) was compared with that in October (one month after the Hurricane), no statistic differences were observed in the sand vegetation (U = 4.4, p = 0.84) or xerophytic coastal scrub (U = 10.0, p = 0.67). The mangrove forest was not compared statistically because in October only one transect was run; this transect however did show a high value of density (8 iguanas/ha).

The density of burrows was higher in the sand vegetation associated to the beaches (21.9 ± 7.4 burrows/ha) than in the xerophytic coastal scrub (7.1 ± 5.7 burrows/ha) (U = 6.0, p = 0.001); no burrows were observed in the mangrove forest. We examined two burrows; these were 12 m from the coastal line and at 0.5 meters up the sand dune. The length of the main galleries was 1.56 and 1.42 m respectively, there were no lateral galleries in either burrow, and both entrances were oriented southward.

Eight species of plants were found in the scat samples (table 1). Most of the scats (93%) had between one and three items; and only two presented four or five items. The fruits of Chrysobalanum icaco and the leaves of Batis maritima were the most frequently identified material. We found animal remains in 12 samples; the most frequent were the crab Cardisoma guandhumi (16.6%) and another unidentified crab (13.3%). Remains of insects of the order Hemiptera were also found.

The population of Cyclura nubila of Cayo Sijú showed a marked sexual dimorphism; all variables differed significantly between sexes (table 2). The males were greater than females in all the studied variables. We found an overlap in all corporal variables, although this was lower in the snout–vent length, body mass and head width.

Significant differences were found in the snout– vent length of males SVL (F = 15.8; df = 3,69; p < 0.0001) and females (F = 5.65; df = 3,55; p < 0.0019) among four Cuban iguana populations of cays (fig. 4). The males showed a higher variation than females in the SVL. The males of Cayo Sijú were larger in SVL than males of Cayo Rosario and Cayo Largo del Sur (Tukey test, p < 0.001), and they did not differ significantly in relation to those from Cayo Ballenatos (Tukey test, p > 0.05). Little variation was found in the females, although the females of Cayo Ballenatos were larger than Cayo Rosario females (Tukey test, p < 0.001).

Beovides–Casas & Mancina

Mean ± SE ± SD

12 10 8 6 4 2 0 –2

Dry Wet Xerophytic scrub

Dry Wet Sand vegetation

Dry Wet Mangrove forest

Fig. 3. Seasonal variation of the density of iguanas in three habitats on Cayo Sijú, Cayos de San Felipe, Cuba.

Fig. 3. Variación estacional de la densidad de iguanas en tres hábitats de Cayo Sijú, Cayos de San Felipe, Cuba.

Discussion The densities of iguanas in Cayo Sijú were in the range of other populations of Cuban iguana (Perera, 1985a; González et al., 2001; Alberts et al., 2002) and other rock iguanas of the genus Cyclura (Carey, 1975; Gicca, 1980). The higher density of juvenile iguanas in the xerophytic coastal scrub could be related to ecological factors such as the high diversity of food resources and roost sites that would make them less vulnerable to predators. In this cay, eight egret species, two birds of prey (Common Black–Hawk, Buteogallus anthracinus, and American Kestrel, Falco sparverius) and one species of colubrid snake (Alsophis cantherigerus) have been observed (Mancina & Beovides, 2005), all potential depredators of hatchling and juvenile iguanas (Henderson & Sajdak, 1996; Alberts, 2000).

Our estimates of biomass of iguanas in Cayo Sijú were similar to those found for other Cyclura species; i.e. 17.01 kg/ha in Cyclura carinata on Caicos Island (Iverson, 1979), and 11.6 kg/ha in Cyclura pinguis on Anegada, Virgin Island (Carey, 1975). Other estimates show higher values of biomass for Cyclura cychlura on Exuma Cays, Bahamas (Carey, 1976) and Cyclura rileyi nuchalis on Acklin Bight, Bahamas (Hayes et al., 2004), although these studies combined juveniles and adult iguanas.

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Animal Biodiversity and Conservation 29.1 (2006)

Table 1. Items found in 30 scat samples of Cyclura nubila collected on Cayo Sijú, Cayos de San Felipe, Cuba. All samples were collected during the month of June, 2004: 1 Previously reported in the diet of Cuban iguana, Cyclura nubila nubila; 2 Number of scat samples where the item was found; L. Leaves; F. Fruit.

Tabla 1. Elementos encontrados en 30 muestras fecales de Cyclura nubila recolectadas en Cayo Sijú, Cayos de San F e l i p e , C u b a . To d a s l a s m u e s t r a s corresponden al mes de junio del 2004: 1 Encontrada anteriormente en la dieta de la iguana de Cuba, Cyclura nubila nubila; 2 Número de muestras fecales en las que se encontró el elemento; L. Hojas; F. Fruto.

Plant species

L

Chrysobalanum icaco

%

1

F

%

2

96.7

2

6.6

29

Batis maritima

18

60

Strumphia maritima1

1 3.3

Sorghum halepense

1 3.3

Sesuvium portulacastrum 1 3.3 Conocarpus erectus1

1 3.3

1

3.3

1

1 3.3

1

3.3

Metopium toxiferum Erithalis fruticosa

1

1 3.3

The lower values of density observed in the dry season (February and April) may be related to changes in the thermoregulatory behavior of these iguanas. The lowest environmental temperatures were registered during this season (between 13ºC– 25ºC), the rock iguanas, like other ectothermic vertebrates (Bennett, 1983; Christian et al., 1986) could decrease their activity levels during the coldest months being less conspicuous. On the contrary, during the wet months the iguanas show a high activity in relation to breeding behavior. Perera (1985a) found no seasonal difference in the density of iguanas in Cayo Largo del Sur, and he related this to the absence of any marked changes in temperature during the study time.

The higher density of burrows excavated in the beach as compared to other habitats could be related to the development of the dune, the soft soil and moisture in this area, and to a more compact soil in the rest of the key. Burrows for most of the iguanas of Cayo Sijú are concentrated on the beach dune, and when the foraging period starts individuals move to different areas. In Cayo Real, a cay located to the west of Cayo Sijú, the burrows were scarce along the beach (Beovides & Mancina, obs. pers.). In this cay we observed a dune of smaller proportions while the rocks are typically exposed in many parts of the shore, offering natural roosts for the iguanas. Perera (1985a) found that in an area where sandy and rocky soil were available for the iguanas, the reptiles preferred the latter, apparently related with minimizing the energy expenditure in the construction of the burrow.

Table 2. Summary of sexual dimorphism in morphological traits (lengths in mm) in Cyclura nubila nubila from Cayo Sijú, Cayos de San Felipe, Cuba. The last column presents the results from unpaired two–tailed t–tests for sexual size dimorphism.

Tabla 2. Resumen del dimorfismo sexual según las variables morfológicas (longitudes en mm) de Cyclura nubila nubila de Cayo Sijú, Cayos de San Felipe, Cuba. La última columna muestra el valor del estadístico t y el nivel de significación.

Adult male N

Mean±SD

Adult female Range

N

Mean±SD

Two–tailed Range

t–tests

Total length

26 1000.8±110.3 710–1119

18 824.3±62.9 690–910

t = 5.6, p < 0.001

Snout–vent length

26

451.3±46.6

370–520

18 340.0±24.4 305–370

t = 9.1, p < 0.001

Tail length

26

560.7±89.1

320–730

18 485.5±57.2 320–560

t = 2.8, p < 0.006

Humerus length

26

64.5±7.3

49.2–80

18

43–55.5

t = 7.7, p < 0.001

Femur length

26

102.9±11.3

80.5–122

66.6–90

t = 8.1, p < 0.001

Head length

26

103.5±17.2

71.1–123

18

72.5±5.5

61.8–83.1

t = 6.8, p < 0.001

Head width

26

63.8±8.7

48.9–75.8

18

43.3±3.9

35.7–51.6

t = 9.1, p < 0.001

Body mass (kg)

26

4.1±1.08

2.04–5.5

18

1.7±0.4

1.05–2.4

t = 8.1, p < 0.001

(Body mass/ SVL)*100 26

0.89±0.1

0.53–1.19

18

0.43±0.1

0.34–0.64

t = 7.8, p < 0.001

49.3±3.5

18 78.5±6.04

6

Beovides–Casas & Mancina

40 30

550

Males

50

Females A

A A

20

B

B A B

A

A C

10 0 Cayo Sijú

Cayo Cayo largo Cayo Rosario del Sur Ballenato

Fig. 4. Variation in snout–vent length in four populations of Cyclura nubila nubila from Cuba. Values indicate the mean and the vertical line indicates standard deviation; the letters indicate the significant differences using a Tukey Test to p < 0.01.

Fig. 4. Variación de la longitud hocico–cloaca en cuatro poblaciones de Cyclura nubila nubila de Cuba. Las barras reprsentan los valores medios y las líneas verticales la desviación estándar; las letras indican las diferencias significativas utilizando un test de Tukey con p < 0.01.

Hurricanes are very frequent catastrophic disturbances in the West Indies and they play an important role in the structure of animal communities (Wunderle et al., 1992; Spiller et al., 1998; Jones et al., 2001). On September 12th, 2004, Hurricane Ivan, a category 5 cyclone on the Saffir– Simpson scale, hit the west of Cuba, including Cayos de San Felipe. This hurricane notably changed the physiognomy of the cay; the xerophytic coastal scrub was covered by sand in a large area and vegetation was destroyed. Contrary to what was expected, no significant variation was detected in the density of iguanas when we compared iguana populations before and after this climatic event.

Short–term affectation of the iguana population after hurricane could be related to several characteristics of the species: like other lizards, rock iguanas exhibit low resting levels of oxygen consumption compared to mammals and birds.

This low rate of energy demand has the advantage of permitting survival on very little food and enabling periods of tolerance to the limited availability of food (Bennett, 1983). Furthermore, they are herbivorous lizards. We observed that the mangrove forest was the vegetation least affected by the hurricane; it could therefore represent an important roosting and feeding area for the iguanas during stressful times. We did not find scat

Snout–vent length (mm)

Snout–vent length (cm)

60

500 450 400 350 Males Females

300 250 0.5

2.5 4.5 Body mass (kg)

6.5

Fig. 5. Sexual dimorphism in two morphological variables of Cuban iguana, Cyclura nubila, on Cayo Sijú, Cayos de San Felipe, Cuba.

Fig. 5. Dimorfismo sexual en dos variables morfológicas de la iguana cubana, Cyclura nubila, en Cayo Sijú, Cayos de San Felipe, Cuba.

samples during the month of October; but Perera (1985b) found remains of leaves and flowers of the two species of mangroves (Rizophora mangle and Avicenia germinans) in the scat samples of Cyclura nubila on cays near Cayo Largo del Sur. The damage observed in the xerophytic coastal scrub could cause long term changes in the population structure as this habitat is apparently an important site for the survival of juvenile iguanas. Future studies are necessary to determine the effect of this natural disturbance on the population of Cuban iguana on Cayo Sijú.

The Cuban iguana is a generalist phytophagous animal, and its diet depends on the floristic composition of each locality (Perera, 2000). Sixty– two percent of the species of plant that we found in the scat samples had been reported in the diet of the Cuban iguana in other cays of the Cuban archipelago (Perera, 1985b; González et al., 2001).

The iguana could exploit the peak of productivity of some plants; for example in June, 96% of 30 scat samples presented remains of Chrysobalanum icaco and this month coincides with the fructification peak of this plant (Beovides, pers. obs.). Animal matter has been found in the diet of the Cuban iguana (Perera, 1985b) and this could be an important source of nitrogen.

The presence of sexual dimorphism (males larger than females) in the Cuban iguana has been observed by Perera (1984) and González et al. (2001). In Cuban iguanas at Guantánamo Bay, Alberts et al. (2002) found no differences in body mass between nonranking males and females.

We found a light overlap of the body mass be-

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Animal Biodiversity and Conservation 29.1 (2006)

tween sexes in the population of Cayo Sijú, although with approximately the same body mass, the males have a longer snout–vent (fig. 5). In other species of rock iguanas, sexual dimorphism has been previously documented for Cyclura carinata (Iverson, 1979), Cyclura collei (Vogel, 2000) and Cyclura cornuta (Ottenwalder, 2000).

This sexual difference has been related mainly with the home range, territoriality and the mating systems (Stamps, 1983). We observed frequently aggressive behavior among males in all months, although it increased in the reproductive season.

Males with missing fingers were observed, and two individuals had a a forearm completely mutilated. We found an iguana phalange in one scat sample. Such agonistic interaction has been observed in other herbivorous iguanids and it has been related with territoriality (Stamps, 1983; Alberts et al., 2002).

The variation in the snout–vent length in both sexes of the Cuban iguana could be related with variability of the species across a wide geographic range (Rodríguez–Schettino, 1999). However, the higher differences in the males may be the result of collecting bias. In the population of Guantánamo Bay, Alberts et al. (2002) found significant differences in the SVL among males of different social rank; the high–ranking males were larger in SVL than both low and nonranking males. The larger SVL observed in the population of Cayo Ballenato may be the result of higher levels of heterozygosity; in this cay the iguanas were likely reintroduced from nearby coastal zones. Although we have no evidence of such, it is possible that iguanas on cays have a smaller effective population size than on the main island. On the cays, the populations could present lost genetic variation as a consequence of genetic drift (Frankham, 1997; Lacy, 1987), which would account for smaller sizes (e.g. lower SVL) among other effects (Harris & Allendort, 1989). Ecological factors such as the density of iguanas and the food resource abundance could also explain the differences observed among the populations.

We consider that it would be interesting to carry out studies on the genetic structure of the populations of the Cuban iguana. This would allow us to determine the genetic flow of the species, and the presence of isolated subpopulations could play a major role in conservation management of the Cuban iguana in Cuba.

Acknowledgments We are grateful to the staff at Flora y Fauna of La Coloma, Pinar del Rio for logistical support. We thank Lázaro Noel Sánchez, Michel Sánchez and second–year students at the Facultad de Biologia of the Universidad de La Habana for field assistance. Thanks also go to Dr. Lourdes Rodríguez– Schettino and two anonymous referees for commenting on an earlier draft.

References Alberts, A. C., 1999. Developing recovery strategies for West Indian Rock Iguanas. Endangered Species UPDATA, 16(5): 107–110.

– 2000. West Indian Iguanas: Status Survey and Conservation Action Plan: 1–111. IUCN/SSC West Indian Iguanas Specialist Group, IUCN, Gland, Switzerland y Cambridge, UK. Alberts, A. C., Lemm, J. M., Perry, A. M., Morici, L. A. & Phillips, J. A., 2002. Temporary alteration of local social structure in a threatened population of Cuban iguanas (Cyclura nubila). Behavioral Ecology and Sociobiology, 51: 324–335.

Bennett, A. F., 1983. Ecological consequences of activity metabolism. In: Lizard ecology, studies of a model organism: 11–23 (R. B. Huey, E. R. Pianka & T. W. Schoener, Eds.). Harvard Univ.

Press, Cambridge, MA. Berovides, V., Rodríguez, L. & Cubillas, S., 1996.

Cyclura nubila nubila. Conservation assessment and management plan for some Cuban species. IUCN/SSC/GBSG: 93–100.

Burton, F. J., 2004. Revision to Species of Cyclura nubila lewisi, the Grand Cayman Blue Iguana.

Caribbean Journal of Science, 40(2): 198–203.

Carey, W. M., 1975. The rock iguana, Cyclura pinguis, on Anegada, British Virgin Island, with notes on Cyclura ricordi and Cyclura cornuta on Hispaniola. Bulletin of the Florida State Museum of Biological Sciences, 19(4): 189–233.

– 1976. Iguanas of the Exumas. Wildlife, 5: 59–61.

Christian, K., 1986. Aspects of the life history of Cuban iguanas on Isla Magueyes, Puerto Rico.

Caribbean Journal of Science, 22: 159–164.

Etheridge, R., 1982. Checklist of iguanine and Malagasy iguanid lizards. In: Iguanas of the World: 7–37 (G. M. Burghardt & A. S. Rand, Eds.). Noyes, Park Ridge, New Jersey.

Frankham, R., 1997. Do island populations have less genetic variation than mainland pop– ulations? Heredity, 78: 945–959.

Gicca, D., 1980. The status and distribution of Cyclura r. rileyi (Reptilia: Iguanidae) a Bahamas rock iguana. Caribbean Journal of Science, 16: 9–12.

González, A., Berovides, V. & Castañeira, M. A., 2001.

Aspectos de morfometría, abundancia, y alimentación de la iguana cubana (Cyclura nubila nubila) en el Archipiélago de los Canarreos, Cuba. Revista Biología, 15(2): 98–104.

Harris, R. B. & Allendorf, F. W., 1989. Genetically effective population size of large mammals: an assessment of estimators. Conserv. Biol., 3: 181–191.

Hartley, L. M., Glor, R. E., Sproston, A. L., Powell, R. & Parmerlee Jr, J. S., 2000. Germination rates of seeds consumed by two species of rock iguanas (Cyclura spp.) in the Dominican Republic. Caribbean Journal of Science, 36(1–2): 149–151.

Hayes, W. K., Carter, R. L., Cyril, S. & Thorton, B., 2004. Conservation of an endangered Bahamian

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rock iguana: I. Population assessments, habitat restoration, and behavioral ecology. In: Iguanas; Biology and Conservation: 232–257 (A. Alberts, R. Carter, W. Hayes & E. Martins, Eds.). Univ. of California Press, Berkeley, California.

Henderson, R. W., 1992. Consequences of predator introductions and habitat destruction on amphibians and reptiles in the post–colombus West Indies. Caribbean Journal of Science, 28(1–2): 1–10.

Henderson, R. W. & Sajdak, R. A., 1996. Diets of West Indian racers (Colubridae: Alsophis): composition and biogeographic implications.

In: Contributions to West Indian Herpetology: A Tribute to Albert Schwartz: 327–338 (R. Powell & R. W. Henderson, Eds.). Society for the Study of Amphibians and Reptiles, Contributions to Herpetology, volume 12. Ithaca, N.Y. Iverson, J. B., 1979. Behavior and ecology of the rock iguana, Cyclura carinata. Bulletin of the Florida State Museum of Biological Sciences, 24: 175–358.

– 1985. Lizards as seed dispersers? Journal Herpetology, 19: 292–293.

Jones, K. E., Barlow, K. E., Vaughan, N., Rodríguez– Durán, A. & Gannon, M. R., 2001. Short–term impacts of extreme environmental disturbance on the bats of Puerto Rico. Animal Conservation, 4: 59–66.

Lacy, R. C., 1987. Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv. Biol., 1: 143–158.

Mancina, C. A. & Beovides, K., 2005. Aves de Cayo Sijú (Cayos de San Felipe), Cuba. Poeyana, 492: 1–4.

Ottenwalder, J., 2000. Rhinoceros iguana, Cyclura cornuta cornuta. In: West Indian Iguanas: Status Survey and Conservation Action Plan: 22–27 (A. C. Alberts, Ed.). IUCN/SSC West Indian Iguanas Specialist Group, IUCN, Gland, Switzerland y Cambridge, UK.

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Perera, A., 1984. Aspectos de la ecomorfología de Cyclura n. nubila (Sauria Iguanidae). Ciencias Biológicas, 11: 129–141.

– 1985a. Datos sobre la abundancia y actividad de Cyclura nubila (Sauria: Iguanidae) en los alrededores de Cayo Largo del Sur, Cuba.

Poeyana, 288: 1–17.

– 1985b. Datos sobre la dieta de Cyclura nubila (Sauria: Iguanidae) en los alrededores de Cayo Largo del Sur, Cuba. Poeyana, 291: 1–12.

– 2000. Cuban iguana, Cyclura nubila nubila.

In: West Indian Iguanas: Status Survey and Conservation Action Plan: 36–39 (A. C. Alberts, Ed.). IUCN/SSC West Indian Iguanas Specialist Group, IUCN, Gland, Switzerland y Cambridge, UK. Rodíguez–Schettino, L., 1999. The iguanid lizards of Cuba. Univ. Press of Florida, Florida.

Sistema Nacional de Áreas Protegidas (SNAP), 2002. Cuba, Plan 2003–2008. Escandon Impresores, Sevilla, España.

Spiller, D. A., Losos, J. B. & Schoener, T. W., 1998.

Impact of a catastrophic hurricane on island populations. Science, 281: 695–697.

Stamps, J. A., 1983. Sexual selection, sexual dimorphism, and territoriality. In: Lizard ecology, studies of a model organism: 169–204 (R. B. Huey, E. R. Pianka & T. W. Schoener, Eds.).

Harvard Univ. Press, Cambridge.

StatSoft, Inc., 2001. STATISTICA (data analysis software system), version 6. http://www.statsoft.com Vogel, P., 2000. Jamaican iguana, Cyclura collei.

In: West Indian Iguanas: Status Survey and Conservation Action Plan: 19–22 (A. C. Alberts, Ed.). IUCN/SSC West Indian Iguanas Specialist Group, IUCN, Gland, Switzerland y Cambridge, UK. Wunderle, J. M., Lodge, D. J. & Waide, R. B., 1992.

Short–term effects of Hurricane Gilbert on terrestrial bird populations on Jamaica. Auk, 109: 148–166.

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Two new species of Typhlocharis Dieck, 1869 of the silvanoides group from Portugal (Coleoptera, Carabidae) A. R. M. Serrano & C. A. S. Aguiar

Serrano, A. R. M. & Aguiar, C. A. S., 2006. Two new species of Typhlocharis Dieck, 1869 of the silvanoides group from Portugal (Coleoptera, Carabidae). Animal Biodiversity and Conservation, 29.1: 9–18.

Abstract Two new species of Typhlocharis Dieck, 1869 of the silvanoides group from Portugal (Coleoptera, Carabidae).— Two endogean carabid species of Typhlocharis Dieck, 1869 in the T. silvanoides species group are described, Typhlocharis carinata n. sp. and Typhlocharis paulinoi n. sp. T. carinata is characterized by the elytron with four discal setae and one subapical seta, the abdominal sternum II with a median carina, more developed near the posterior margin, stronger in male than in female, the median lobe of aedeagus strongly sickle–shaped and the parameres bisetulose, each with a large apical seta and a short sub–apical seta. T. paulinoi is characterized by the elytron with three discal setae and one subapical seta, the abdominal female sterna II and III without any fovea, the internal sac of median lobe in central area very difuse with one lateral sclerite and the right paramere bisetulose, with a large apical seta and a short sub–apical seta.

Affinities to putative relatives and a key for the identification of the seven known species belonging to the silvanoides group are also given.

Key words: Coleoptera, Carabidae, Anillina, Typhlocharis, New species, Portugal.

Resumen Dos nuevas especies de Typlocharis Dieck, 1869 del grupo silvanoides de Portugal (Coleoptera, Carabidae). — Se describen dos nuevas especies de carábidos endogeos de Typhlocharis Dieck,1869, del grupo de especies T. silvanoides: Typhlocharis carinata n. sp. y Typhlocharis paulinoi n. sp. T. carinata se caracteriza por sus élitros con cuatro sedas discales y una seta subapical, el esternito abdominal II con una carena media, más desarrollada cerca del margen posterior, más fuerte en el macho que en la hembra, el lóbulo medio del edeago más falciforme, y los parámeros bisetulados, cada uno de ellos con una seda apical grande y una seda subapical corta. T. paulinoi se caracteriza por sus élitros con tres sedas discales y una seda subapical, los esternitos abdominales femeninos II y III sin fóvea alguna, el saco interno del lóbulo medio de la zona central muy difuso, con un esclerito lateral y el parámero derecho bisetulado, con una seda apical grande y una seda subapical corta. También se tratan las afinidades con especies supuestamente emparentadas y se da una clave de identificación de las siete especies conocidas del grupo silvanoides.

Palabras clave: Coleoptera, Carabidae, Anillina, Typhlocharis, Especies nuevas, Portugal.

(Received: 4 V 05; Conditional acceptance: 15 VII 05; Final acceptance: 26 VII 05) Artur R. M. Serrano & Carlos A. S. Aguiar, Centro de Biologia Ambiental, Dept. de Biologia Animal, Fac. Ciências da Univ. de Lisboa, R. Ernesto de Vasconcelos C2, 1749–016 Lisboa, Portugal.

Corresponding author: A. R. M. Serrano: aserrano@fc.ul.pt

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction The genus Typhlocharis Dieck, 1869 (Coleoptera, Carabidae, Trechinae, Bembidiini) belongs to the subtribe Anillina, and according to the catalogue of the ground beetles of the Iberian peninsula (Serrano, 2003) is the richest genus in this peninsula, with 37 known species. Representatives of Typhlocharis are distributed throughout the Iberian peninsula (Europe), Morocco and Tunisia (North Africa) (Jeannel, 1963). The genus, considered to be very old, inhabits the vestiges of the Lusitanian, Lionigurian, the Betic Riffian and the Numidian Massifs (Jeanne, 1973). According to Jeannel (1963), the ancestral lucicolous of the Typhlocharis expanded from Africa to the Betic Rriffian Massif 65 million years ago (Montian, Inner Palaeocene), radiating to the present biogeographic limits.

All species of this genus are eyeless (anophthalmous), occur in soil and are endogean. They may also be collected from the lower surface of stones superficially embedded in the soil. Most Typhlocharis species are local or regional endemisms; their distribution is limited, probably because of isolation due to physical barriers and a low capacity of dispersal (e.g. they move very slowly and are wingless carabids). Thus, taking into account their present distribution, they represent a great potential for phylogeographic studies.

Much has been learnt about the systematics and distribution of representatives of the genus Typhlocharis from Portugal has considerably increased in recent years (Serrano & Aguiar, 2000, 2001, 2002; Serrano et al., in press), but our knowledge of the genus in this country is still unsatisfactory. Eight species have been recorded for Portugal to date: T. quadridentatus Coiffait, 1968, T. algarvensis Coiffait, 1971, T. singularis Serrano & Aguiar, 2000, T. sarrius Serrano & Aguiar, 2001, T. elenae Serrano & Aguiar, 2002, T. gomesalvesi Serrano & Aguiar, 2002, T. passosi Serrano & Aguiar and T. fozcoaensis Serrano & Aguiar (Coiffait, 1968, 1971; Serrano & Aguiar, 2000, 2001, 2002; Serrano et al., in press). Two of these species (T. algarvensis and T. sarrius) belong to the silvanoides species group, another two to the gomezi species group and the remainders to the outereloi species group (sensu Zaballos & Ruiz–Tapiador, 1997). The other known species within the silvanoides group are: T. silvanoides Dieck, 1869 (Morocco: Riff), T. armatus Coiffait, 1968 (Spain: Cádiz, San Roque) and T. fancelloi Magrini, 2000 (Spain: Almería, Sierra Almagrera) (Zaballos & Ruiz–Tapiador, 1997; Magrini, 2000). According to Zaballos & Ruiz– Tapiador (1997), adults of the the silvanoides species group are recognized by the following combination of characters: a) umbilicate series of elytra with four setae in the anterior group and four setae in the posterior group (4+4) and b) apical edge of elytra without teeth.

After carefully studying several endogean carabid specimens from Portugal, we concluded that they represent two new species of the genus Typhlocharis,

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belonging to the silvanoides group. This work aims to describe these new species and to provide notes about relationships with the closest forms. Moreover, we provide a key to all known species of the silvanoides species group.

Material and methods Field work was conducted in several areas near the Mértola, Almodovar and Odemira localities in the Province of Baixo Alentejo and in several localities throughout the Province of Algarve (both Provinces of Portugal); this resulted in the collection of specimens of endogean beetle species of the subtribe Anillina. The specimens were collected by hand from under embedded stones in fragments of Mediterranean secondary forest habitat dominated by holm–oaks, rock–roses shrubs and lentisk bushes (Quercus coccifera Linnaeus, Cistus ladanifer Linnaeus and Pistacia lentiscus Linnaeus) with patches of man–induced land uses. Additional specimens were obtained from samples of soil taken from the above–mentioned localities using the Berlese apparatus.

The morphological study of adult specimens was conducted using a scanning electron microscope JEOL JSM–5200 LV. Measurements and drawings were done with a Wild M5 stereoscopic microscope equipped with a dissecting microscope ocular micrometer and a drawing tube.

The distribution of species in the descriptions is given in UTMcoordinates (1 km x 1 km). For practical reasons, the map used for the representation of distributions was 10 km x 10 km squares (fig. 24).

Some localities are therefore enclosed in the same 10 km x 10 km square.

Results Typhlocharis carinata n. sp. (figs. 1–8, 17–18, 21, 24) Diagnosis Anophthalmous, body parallel, depressed, brown or brownish–yellow with integument microreticulate and scattered pubescence. Elytron with four discal setae, one subapical seta, and eight (4+4) marginal umbilicate setae; apical edge sinuate without teeth (males and females), sutural one absent. Hind trochanters inerms in both sexes.

Abdominal sternum II with a median carina, more developed near the posterior margin, stronger in the male than in the female; abdominal female sternum II with one slightly posteriolateral fovea on each side; abdominal female sternum III with one very faint lateral fovea. Aedeagus (figs. 17, 18) with the median lobe strongly sickle–shaped, basal lamina markedly arcuate; internal sac in central area with one twisted sclerite; parameres bisetulose, each with a large apical seta and a short sub–apical seta.

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Description Length of holotype: 2.9 mm.

Length of paratypes: 2.1–2.9 mm {{, 2.3–2.9 mm }}.

Head (figs. 1, 3): robust, slightly wider than long (length: 0.34–0.51 mm {{ and 0.38–0.61 mm }} width: 0.48–0.65 mm {{ and 0.51–0. 57 mm }}) with hexagonal microsculpture and slightly depressed in the middle of the front; anterior region of clypeus with one strong median depression; vertex with transversal microsculpture which, in the area below the anterior margin of the pronotum, is arranged in parallel ridges to form a file (pars stridens) (figs. 1, 2).

Cephalic chaetotaxy (large setae): labrum with three pairs of setae (those on sides longer), one seta on each side of clypeus and two pairs close to frontal sulcus, a pair of supraocular setae (anterior and posterior) present over each eye and two–three posterior pairs of setae between vertex and lateral carinae. Antennae moniliform, mouth–parts (fig. 3) as usual in the genus.

Pronotum (fig. 4): rectangular, slightly longer (1.1– 1.3 times) than wide (length: 0.62–0.88 mm {{ and 0.66–0.81 mm }}, width: 0.56–0.76 mm {{ and 0.59–0.75 mm }}), slightly narrowed towards posterior angles which are marked with one tooth; disk flattened, with three longitudinal slight sulci, one central and one on each side; the lateral sulci only visible in the second half of disk; anterior margin strongly emarginate in the middle region; lateral margins arcuate, with three or four minor denticles near the posterior angles; disk depressed near the posterior margin, this slightly emarginate in the middle region. Chaetotaxy: five longitudinal series of setae between midline and lateral margins, alternatively with minute and large setae directed anteriad; one anterior seta on each side in anterior quarter, one posterior seta on hind angle; anterior margin with three–four pairs of setae.

Elytra (fig. 5): 1.7–1.9 times longer than wide (length: 1.15–1.52 mm {{ and 1.22–1.47 mm }}, width: 0.64–0.83 mm {{ and 0.66–0.86 mm }}), parallel and oval posteriorly, with one slightly longitudinal carina at the beginning of seventh stria; dorso–ventrally flattened on the disk; transverse scutellar organ present near the beginning of suture (fig. 4); scutellar region not punctured; humeral angles rounded, with a small tooth in the beginning of carina; lateral margins serrate, teeth decreasing in size posteriorly; apical margin without any tooth (fig. 5), subsinuate after the end of longitudinal carina. Chaetotaxy: part of the pubescence of the disk is arranged in five lines since the sutural line, these short setae are erect and slightly directed anteriad; four large discal setae stand out close to the third line, one subapical seta coinciding with the end of seventh stria; umbilicate series divided in two groups of four setae each (4+4) (fig. 5).

Legs: with robust femora, inner margin of profemur with a reasonably developed tooth; trochanters of third pair similar in male and female, without special features (figs. 7, 8), protarsus without dilated segments.

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Abdomen (figs. 6–8): with sternum II with one median carina, more developped near the posterior margin (fig. 6), stronger in male than in female; sternum II of female with one slightly posteriolateral fovea on each side, sternum III with one very faint lateral fovea (fig. 8).

Male genitalia (figs. 17, 18): in lateral aspect with a median lobe strongly sickle–shaped, basal lamina markedly arcuate, apex stands out (fig. 17); median lobe in dorsal aspect with rather thin apex thin, bent to left (fig. 18); internal sac in central area with one twisted sclerite; parameres bisetulose, each with a large apical seta and a small one sub–apical seta; left paramere strongly arcuate, with dorso–basal edge very expanded.

Female genitalia (fig. 21): with gonocoxites of ovipositor weakly sclerotized, each one in ventral aspect with one apical seta; internal genital tract with spermathecal duct short and spermatheca spheroid; spermathecal gland long, with proximal region membranous and apical region more or less sclerotized.

Type series Holotype {: Portugal, Odeceixe (UTM: 29SNB2242), 13 I 2004. Paratypes: 9 {{ and 11 }} (2 {{ and 1 } gold coated), same locality and date; Pincho (UTM: 29SNB2218), 9 {{ , 10 I 2004; Alferce (Monchique) (UTM: 29SNB4320), 1 }, 12 I 2004.

Holotype and paratypes deposited in the collection of the senior author, Department of Animal Biology (Lisbon).

Etymology The specific epithet of the new species is the latinized adjectival from the peculiar carina found in the middle region of the abdominal sternum II. Affinities The new species is the largest in the genus Typhlocharis and belongs to the silvanoides group based on the absence of teeth in the apical edge of elytron and the occurrence of four setae in each group of the umbilicate series. However, it is well differentiated within the silvanoides group by the presence of a median carina in the abdominal sternum II (fig. 6), stronger in males than in females. In some species of Typhlocharis (e. g. T. monasticus Zaballos & Wrase, T. peregrinus Zaballos & Wrase and T. navaricus Zaballos & Wrase) the males also present a median tubercle in the same sternum, near the posterior margin (Zaballos & Wrase, 1998). Apparently this structure is found in some species of the same or of different groups (e.g. monasticus and outereloi groups, sensu Zaballos & Ruiz–Tapiador, 1997; Zaballos & Wrase, 1998). The phylogenetic importance of this structure is therefore uncertain with no additional data available. Thee localization of the tubercle suggests / highly suggests that it may be a derivate of the carina now found in the new species. This assumption is corroborated by the fact that the silvanoides group is the most basal group within the

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Figs. 1–8. Typhlocharis carinata n. sp.: 1. Head, dorsal view; 2. Stridulatory organ (pars stridens), dorsal view; 3. Head, ventral view; 4. Posterior part of the head, pronotum and anterior part of elytra, { dorsal view (arrow: tooth in the inner margin of profemur); 5. Right elytron, latero–dorsal view; 6.

Carina in sternum II, { ventral view; 7. Thorax and abdomen, { ventral view; 8. Thorax and abdomen, } ventral view.

Figs. 1–8. Typhlocharis carinata sp. n.: 1. Cabeza, vista dorsal; 2. Órgano estridulador (pars stridens), vista dorsal; 3. Cabeza, vista ventral; 4. Parte posterior de la cabeza, pronoto y parte anterior de los élitros, { vista dorsal (flecha: diente en el borde interno del profemur); 5. Élitro derecho, vista latero– dorsal; 6. Carena del esternito II, { vista ventral; 7. Tórax y abdomen, { vista ventral; 8. Tórax y abdomen, } vista ventral.

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Figs. 9–16. Typhlocharis paulinoi n. sp.: 9. Head and anterior part of pronotum, dorsal view; 10.

Stridulatory organ (pars stridens), dorsal view; 11. Head and anterior part of pronotum, ventral view; 12. Posterior part of the head, pronotum and anterior part of elytra, dorsal view; 13. Left elytron, latero–dorsal view; 14. Elytra, apical view; 15. Thorax and abdomen, { ventral view; 16. Thorax (part) and abdomen, } ventral view.

Figs. 9–16. Typhlocharis paulinoi sp. n.: 9. Cabeza y parte anterior de la cabeza, vista dorsal; 10. Órgano estridulador (pars stridens), vista dorsal; 11. Cabeza y parte anterior del pronoto, vista ventral; 12. Parte posterior de la cabeza, pronoto y parte anterior de los élitros, vista dorsal; 13. Élitro izquierdo, vista latero–dorsal; 14. Élitros, borde apical; 15. Tórax y abdomen, { vista ventral; 16. Tórax y abdomen, } vista ventral.

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Figs. 17–20. Aedeagus. Typhlocharis carinata n. sp.: 17. Median lobe and left and right parameres, lateral view; 18. Median lobe, dorsal view. Typhlocharis paulinoi n. sp.: 19. Median lobe and left and right parameres, lateral view; 20. Median lobe, dorsal view.

Figs. 17–20. Edeagos: 17–18. Typhlocharis carinata sp. n.: 17. Lóbulo mediano y parámeros izquierdo y derecho, vista lateral; 18. Lóbulo mediano, vista dorsal. 19–20. Typhlocharis paulinoi n. sp.: 19.

Lóbulo mediano y parámeros izquierdo y derecho, vista lateral; 20. Lóbulo mediano, vista dorsal.

genus Typhlocharis (Jeanne, 1973). Curiously, within this group, T. carinata is the first species with this type of structure. The quality of T. carinata is probably basal within the silvanoides group based on the presence of one series of four discal setae in elytra, one subapical seta (all absent in all species of the other Typhlocharis´s groups) and on some peculiarities of aedeagus. These peculiarities are the median lobe and left paramere forms, and the location pattern of the setae in both parameres (see description). All these characteristics, on the other hand, reinforce Jeannel’s consideration (1963) that the genera Typhlocharis and Anillus Jacquelin du Val, 1851 are close. Within the silvanoides group, only T. algarvensis Coiffait and the new species present a shiny tegument and a similar conformation of the pronotum. On the other hand, the new species and T. armatus Coiffait have a tooth (more developed in the former than in the latter species) in the inner margin of the male profemur. Besides the presence of one carina in the abdominal sternum II, differences in the shape of median lobe, left paramere and internal sac separate T. carinata n. sp. from all the others belonging to thisgroup. The presence of one pair of posteriolateral foveae in each side of the abdominal female sternum II is also a character within the silvanoides group, only found in the new species. The spermatheca of T. carinata n. sp. has a similar form (spheroid) to that of the other new species described in this work (T. paulinoi n. sp., see next description), but differs from that described for T. fancelloi which is peanut– shaped (see fig. 7, Magrini, 2000). This structure is unknown for the other members of the silvanoides group. The number of apical gonocoxite setae also differs (1 vs. 2) between the latter species, but is

similar between the former species (one seta).

Taking into account the analysed characters, the new species seems to have a closer relationship with T. algarvensis and T. paulinoi n. sp.

Typhlocharis paulinoi new species (figs. 9–16, 19–20, 22, 24) Diagnosis Anophtalmous, body parallel, depressed, brown, with integument microreticulate and scattered pubescence. Elytron with three discal setae, one subapical seta, and eight (4+4) marginal umbilicate setae; apical edge sinuate without teeth ({{ and }}), sutural one absent. Hind trochanters inerms in both sexes. Abdominal female sterna II and III without any fovea. Aedeagus (figs. 19, 20) with the median lobe sickle–shaped, basal lamina markedly arcuate; internal sac in central area very difuse with one lateral sclerite; left paramere with two large apical setae, right paramere bisetulose, with a large apical seta and a short sub–apical seta.

Description Length of holotype: 1.6 mm.

Length of paratypes: 1.3–1.6 mm {{, 1.3–1.8 mm }}.

Head (figs. 9–10): almost as long as wide (length: 0.22–0.30 mm {{ and 0.24–0.34 }}; width: 0.28–0.35 mm {{ and 0.32–0.38 mm }}) with hexagonal microsculpture; vertex with transversal microsculpture arranged in parallel ridges to form a file (pars stridens) in the area below the anterior margin of pronotum (fig. 10). Cephalic chaetotaxy (large setae): Labrum with three pairs of setae (those on sides longer), one pair on sides of

15

Animal Biodiversity and Conservation 29.1 (2006)

22

0.1 mm

0.15 mm

21

Figs. 21–22. Female genitalia (ventral view): 21. Typhlocharis carinata n. sp.; 21. Typhlocharis paulinoi n. sp.

Figs. 21–22. Genitalia femenina (vista ventral): 21. Typhlocharis carinata n. sp.; 21. Typhlocharis paulinoi sp. n.

clypeus and one pair close to frontal sulcus, two pairs of supraocular setae (anterior and posterior) and 1–2 pairs of setae on the posterior region between vertex and lateral carinae. Antennae moniliform and mouth–parts (fig. 11) with no special features, as for other members of the genus.

Pronotum (fig. 12): quadrangular, as long as wide (1.0–1.1 times) (length: 0.35–0.45 mm {{ and 0.35–0.46 mm }}; width: 0.34–0.42 mm {{ and 0.34–0.47 mm }}), narrowed towards posterior angles which are obtuse; disk slightly depressed, with one faint longitudinal sulcus on each side; anterior margin slightly emarginate and posterior margin expanded on each side, emarginate in the middle region; lateral margins arcuate, with 2 or 3 minor denticles near the posterior angles; disk depressed near the posterior margin. Chaetotaxy: three irregular longitudinal series of minute setae between midline and lateral margins directed anteriad; one anterior seta on each side in anterior quarter, one posterior seta on hind angle; four pairs of setae near the anterior margin.

Elytra (fig. 13): 1.8–1.9 times longer than wide (length: 0.70–0.85 mm {{ and 0.78–0.94 mm }}; width: 0.38–0.46 mm {{ and 0.42–0.51 mm }}), parallel and oval posteriorly, with a longitudinal carinae at the beginning of seventh stria; flattened on the disk; transverse scutellar organ present near the base of suture; scutellar region not punctured; humeral angles well marked and rounded, with a tooth in the base of carinae; lateral margins serrate, teeth decreasing in size posteriorly; apical margin without any tooth (figs. 13–14), subsinuate

after the end of longitudinal carina. Chaetotaxy: part of the pubescence of the disk is arranged in five lines from the sutural region, these short setae are erect and slightly directed anteriad; three large discal setae stand out close to the third line, one subapical seta coinciding with the end of seventh stria; umbilicate series divided in two groups of four setae each (4+4) (fig. 13).

Legs: with robust femora, inner margin of profemur inerm; trochanters of third pair similar in male and female, without special features (figs. 15, 16), protarsus of male without dilated segments.

Abdomen (figs. 15, 16): with sternum II of male with no traces of any median special structure (fig. 15), female sterna II and III without any fovea on each side (fig. 16).

Male genitalia (figs. 19, 20): in lateral aspect with median lobe sickle–shaped, basal lamina markedly arcuate (fig. 19); median lobe in dorsal aspect (fig. 20) with apex more or less thin, bent to left; internal sac in central area very difuse, with one lateral sclerite (dorsal aspect) and some tangled membranes; left paramere with two large apical setae, dorso–basal edge very expanded; right paramere bisetulose, with one large apical seta and one short sub–apical seta.

Female genitalia (fig. 22): with gonocoxites of ovipositor weakly sclerotized, each one in ventral aspect with one apical seta; internal genital tract with spermathecal duct short and spermatheca spheroid; spermathecal gland long, with proximal region membranous and apical region more or less sclerotized.

16

Serrano & Aguiar

23 La Coruña Pontevedra

Asturias

Cantabria

Lugo

Vizcaya Guipuzcoa

Francia

Álava Navarra

León

Andorra

Portugal

Burgos Orense Huesca La Rioja Gerona Palencia Viana do Castelo Zamora Lérida Vila Real Soria Braga Barcelona Zaragoza Braganza Valladolid Oporto Segovia Tarragona Viseu Aveiro Salamanca Guadalajara Teruel Guarda Ávila Madrid Coimbra Castellón Castelo Leiria Branco Cuenca Toledo Cáceres Santarém Valencia Portalegre Lisboa Islas Baleares Ciudad Real Albacete Évora Badajoz Alicante Setúbal Córdoba Jaén Beja Murcia Huelva Faro Sevilla Granada 9 Almería Málaga 8 7 Cádiz MC 6 NC S 5 5 6 7 8 94 3 2 1 0 9 8 7 6 5 P 4 P C NB 3 CP 2 A 1 C A 0 Scale UTM 9 10 x 10 km 0 1 2 3 4 5 6 7 8 9 0 1 2 3

España

24

PC

N

Marruecos

PB

4 5

6 7 8

9

Figs. 23–24. Geographic distribution: 23. Silvanoides species group (ellipses); 24: A. T. algarvensis (UTM: 29SNB71, 29SNB90); C. T. carinata n. sp. (UTM: 29SNB21, 29SNB24, 29SNB42); P. T. paulinoi (UTM: 29SNB42, 29SPB15, 29SPB34); S. T. sarrius (UTM: 29SMC95).

Figs. 23–24. Distribución geográfica: 23. Grupo silvanoides (elipses); 24: A. T. algarvensis (UTM: 29SNB71, 29SNB90); C. T. carinata sp. n. (UTM: 29SNB21, 29SNB24, 29SNB42); P. T. paulinoi (UTM: 29SNB42, 29SPB15, 29SPB34); S. T. sarrius (UTM: 29SMC95).

Type series Holotype {: Portugal, Alcoutim (UTM: 29SPB3046), 7 I 2004. Paratypes: 4 }}, same locality and date, 10 {{ and 6 }} (1 { and 2 }} gold coated), same locality, 5 IV 2004; Alferce (Monchique) (UTM: 29SNB4320), 2 }}, 12 I 2004; Espirito Santo (UTM: 29SPB1957), 1 }, 5 IV 2004. Holotype and paratypes deposited in the collection of the senior author, Department of Animal Biology (Lisbon).

Etymology This new species is dedicated to the famous Portuguese entomologist Paulino de Oliveira who elaborated the first catalogue of coleopterous of Portugal and greatly contributed to the taxonomic and faunistic knowledge of these insects in the country.

Affinities The new species also belongs to the silvanoides group. The new species shares with T. sarrius and T. algarvensis the presence and the same location pattern of three discal setae on the elytron. However, the latter species presents a slight carina in the middle region of the pronotum, a character not found in the new species or in any other species of the silvanoides group. The former species differs from T. carinata n. sp. by the number of setae in the left paramere (2 vs 1) and by the number, shape and position of the sclerites of the internal sac (cf. our figs. 19–20 with figs. 1B–1C in Serrano & Aguiar, 2001). T. fancelloi has an equal number of discal setae as T. paulinoi n. sp., but in a different position (see fig. 2 in Magrini, 2000). On the other hand, the absence of a tooth in the inner margin of the male profemur easily segre-

17

Animal Biodiversity and Conservation 29.1 (2006)

gates the new species from T. armatus and T. carinata n. sp. T. paulinoi n. sp. also differs from the latter species by the smaller length of the body, the number of discal setae on elytron (3 vs. 4) and the lack of a carina in the middle region of abdominal sternum II, among other characters. The new species, as well as T. silvanoides and T. fancelloi, do not bear any lateral foveae in the abdominal female sternum II. The new species is akin to T. sarrius, T. carinata n. sp. and apparently to T. armatus by the form of the apical edge of elytron which is subsinuate. The remainder species of the silvanoides group exhibit a round elytron apical edge. Within this group and with the exception of T. carinata n. sp., the conformation pattern of the median lobe of aedeagus of all species is very similar. However, this similitude is more evident between T. silvanoides and T. paulinoi n. sp.

In both species the median lobe is sickle–shaped, ending in a small protuberance slightly bent to the left (cf. our figure 19 with figures 10–13 in Vigna Taglianti, 1972). The internal sacs also exhibit a vestigial sclerite close to the right side (dorsal view) and some tangled membranes. However, several differences can be observed in the aedeagus between these two species: 1. In contrast with with the same structure in T. silvanoides, the median lobe of the new species is not suddenly bent down in the apex; 2. The left paramere of T. paulinoi n. sp. is large (lateral aspect), while the same paramere in T. silvanoides is slender; and 3. The right paramere of the new species has one long apical seta and one

small subapical seta, while the same structure in T. silvanoides exhibits two apical setae. The new species can be easily distinguished from all the others of the same group by details related to the median lobe, the internal sac and the parameres. The form of the spermathecae of T. paulinoi n. sp. and T. carinata n. sp. is similar (spheroid), but the two differ from that described for T. fancelloi which is peanut– shaped. The number of apical gonocoxite setae also differs (1 vs. 2) between the two new species and the latter species, although it is similar to the former species (one seta). Taking the analysed characters into account, namely the features of the median lobe and the female genitalia, the new species seems to have a closer relationship with T. silvanoides and T. carinata n. sp.

As a final remark, we would like to point out that most of the described species of the silvanoides group are confined to Portugal south of the Tejo river (four species of the seven known), with prevalence in the Province of Algarve (three species) (figs. 23, 24).

Key to species of Typhlocharis silvanoides group The silvanoides species group includes the following seven species: T. silvanoides, T. algarvensis, T. armatus, T. fancelloi, T. sarrius, T. carinata n. sp. and T. paulinoi n. sp. The species are distinguished from one another by character states in the key.

Key to species of Typhlocharis silvanoides group.

Clave para las especies del grupo Typhlocahris silvanoides.

1

2 3

4 5

6

Abdominal sternun II with a median carina; elytron with four discal setae, female with one slight pair of posteriolateral foveae. Aedeagus as in figs. 17–18 Abdominal sternun II without a median carina; elytron with or without three discal setae Internal edge of femur of first pair of legs dentate in male Internal edge of femur of first pair of legs not dentate in male Elytron without discal setae. Aedeagus as in figs. 10–13 of Vigna Taglianti (1972) work Elytron with discal setae Pronotum slightly carinate in the middle region of disk Pronotum without any carina in the middle region Apical edge of elytron rounded. Aedeagus as in fig. 4 of Magrini (2000) work Apical edge of elytron subsinuate Median lobe of aedeagus with apex suddenly bent down; left and right parameres with two apical setae each one Median lobe of aedeagus sickle–shaped continuously to apex; right paramere with one apical large seta and one subapical short seta (figs. 19–20)

T. carinata n. sp.

2 T. armatus 3 T. silvanoides 4 T. algarvensis 5 T. fancelloi 6 T. sarrius

T. paulinoi n. sp.

18

Acknowledgments We are grateful to Telmo Antunes and Sónia Proença for photographic assistance. Maria José Boavida helped us to improve the English version. We thank Vicente Ortuño Hernández and one anonym referee, whose comments improved the manuscript.

This work was partially financed by Centro de Biologia Ambiental (CBA).

References Coiffait, H., 1968. Nouveaux Anillini du Maroc et du Sud de la Peninsule Iberique. Bulletin de la Société des Sciences Naturelles et Physiques du Maroc, 48(3–4): 55–66.

– 1971. Contribution a la connaissance du genre Typhlocharis (Col. Carabidae). Description d‘une espèce nouvelle du Portugal. Annales de Spéléologie, 26(2): 463–467.

Jeanne, C., 1973. Sur la Classification des Bembidiides endogés de la Région Euro– Méditerranéenne (Col. Carabidae, Bembidiinae, Anillini). Nouvelle Revue d‘Entomologie, 3(2): 83–102.

Jeannel, R., 1963. Monographie des "Anillini", Bembidiides endogés (Coleoptera Trechidae).

Mémoires du Muséum National D`Histoire Naturelle (N. S.), Série A, Zoologie 28(2): 33–204.

Magrini, P., 2000. Due nuovi Typhlocharis Dieck, 1869 di Spagna (Insecta Coleoptera Carabidae).

Serrano & Aguiar

Quaderno di Studi e Notizie di Storia Naturale della Romagna, 13, suppl.: 1–10.

Serrano, A. R. M. & Aguiar, C. A. S., 2000. Description of two new endogean beetle species (Coleoptera, Carabidae) from Portugal. Boletim da Sociedade Portuguesa de Entomologia, 7(13): 149–158.

– 2001. Three new endogean beetles (Coleoptera, Carabidae) from Portugal. The Coleopterists Bulletin, 55(1): 172–180.

– 2002. The genus Typhlocharis Dieck, 1869 (Coleoptera: Carabidae) in Portugal: description of two new species and faunistic notes. Boletim da Sociedade Portuguesa de Entomologia, 7(16): 181–197.

Serrano, A. R. M., Aguiar, C. A. S. & Proença, S. J. R. (in press). Two new species of Typhlocharis Dieck of the Group gomezi from Portugal (Coleoptera: Carabidae). The Coleopterists Bulletin.

Serrano, J., 2003. Catálogo de los Carabidae (Coleoptera) de la Península Ibérica. Monografias S.E.A., 9: 1–130.

Vigna Taglianti, A., 1972. Un nuovo Typhlocharis di Spagna (Coleoptera Carabidae). Bollettino della Società Entomologica Italiana, 104: 148–156.

Zaballos, J. P. & Ruiz–Tapiador, I., 1997. Nuevos Typhlocharis Dieck (Coleoptera, Caraboidea, Trechidae) de España. Graellsia, 52: 95–106.

Zaballos, J. P. & Wrase, D. W., 1998. Tres nuevos Typhlocharis Dieck, 1869 (Coleoptera, Caraboidea, Trechidae) de Navarra (España). Graellsia, 54: 43–52.

Animal Biodiversity and Conservation 29.1 (2006)

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Impact of different agricultural practices on the genetic structure of Lumbricus terrestris, Arion lusitanicus and Microtus arvalis

R. Kautenburger

Kautenburger, R., 2006. Impact of different agricultural practices on the genetic structure of Lumbricus terrestris, Arion lusitanicus and Microtus arvalis. Animal Biodiversity and Conservation, 29.1: 19–32.

Abstract Impact of different agricultural practices on genetic structure of Lumbricus terrestris, Arion lusitanicus and Microtus arvalis.— Little attention has been given to date to the potential influence of agricultural land use methods or farming practice on the genetic variability of native species. In the present study, we measured the genetic structure of three model species —Microtus arvalis, Arion lusitanicus and Lumbricus terrestris— in an agricultural landscape with a diversity of land use types and farming practices. The aim of the study was to investigate whether different management strategies such as the method of land use or type of farming practice (conventional and ecological farming) have an impact on the species’ genetic structure. We used RAPD markers and multilocus DNA fingerprints as genetic tools. Genetic similarity was based on the presence or absence of bands, which revealed a wide range of variability within and between the analysed populations for each model species. Cluster analysis and Mantel tests (isolation by distance) showed different genetic structures in the populations of M. arvalis from sampling sites with different land use.

However, the main factors influencing the genetic variability of these vole populations were geographic distances and isolation barriers. The genetic variability observed in A. lusitanicus populations correlated with geographic distance and the type of land use method, but no correlation was found with different farming practices. Our preliminary results suggest that the genetic structure of L. terrestris populations is influenced by the agricultural land use method used at the different sampling sites but not by the geographic distance.

Key words: Arion lusitanicus, Genetic structure, Land use, Lumbricus terrestris, Microtus arvalis, DNA fingerprinting.

Resumen La influencia de distintas prácticas agrícolas en la estructura genética de Lumbricus terrestris, Arion lusitanicus y Microtus arvalis.— Hasta la fecha se ha prestado poca atención a la influencia potencial de las distintas formas de uso del suelo o de las prácticas agrícolas en relación a la variabilidad genética de las especies autóctonas. En el presente estudio se analizó la estructura genética de tres especies representativas —Microtus arvalis, Arion lusitanicus y Lumbricus terrestris— en suelos agrícolas sometidos a distintos usos del suelo y prácticas agrícolas. El objetivo de este estudio es evaluar si las distintas estrategias de gestión tales como el método de cultivo o el tipo de práctica agrícola empleada (convencional o ecológica) pueden influir en la estructura genética de las especies. Como herramienta de análisis genético se aplicaron las técnicas RAPD (RAPD markers) y de las huellas genéticas multilocus del DNA (multilocus DNA fingerprinting). La semejanza genética fue evaluada en base a la presencia o ausencia de bandas, que reveló una amplia variabilidad dentro y entre las poblaciones analizadas de cada especie modelo. A través del análisis de conglomerados y del test de Mantel (aislamiento por la distancia) se comprobó que las poblaciones de M. arvalis procedentes de muestreos en suelos con distintos usos presentaban distintas estructuras genéticas. Sin embargo, la distancia geográfica y el aislamiento por barreras fueron los principales factores influyentes sobre la variabilidad genética de estas poblaciones de topillo de campo. En el caso de A. lusitanicus se pudo observar que la variabilidad genética de sus poblaciones estaba correlacionada con las distintas formas de uso del suelo y la distancia geográfica, pero no se halló correlación alguna con las distintas prácticas agrícolas. Nuestros resultados preliminares ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

20

Kautenburger

sugieren que la estructura genética de las poblaciones de L. terrestris se ve influida por el tipo de uso del suelo de los distintos lugares de muestreo, pero no por la distancia geográfica.

Palabras clave: Arion lusitanicus, Estructura genética, Usos del suelo, Lumbricus terrestris, Microtus arvalis, DNA fingerprinting.

(Received: 11 IV 05; Conditional acceptance: 11 VII 05; Final acceptance: 1 IX 05) Ralf Kautenburger, Inst. of Inorganic and Analytical Chemistry and Radiochemistry, Saarland Univ., P. O. Box 151150, D–66041 Saarbrücken, Germany.

E–mail: r.kautenburger@mx.uni–saarland.de

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Animal Biodiversity and Conservation 29.1 (2006)

Introduction Over the last decades, numerous agrarian ecological studies have focused on the impact of land use on animal populations (Hurd & Fagan, 1992; Müller, 1995; Jacob & Hempel, 2003; Gehring & Swihart, 2003, Dauber & Wolter, 2004). The authors of these studies suggest that population dynamics of mainly depend on land use methods and farming systems. Although studies in conservation genetics have been carried out for over 20 years (Soulé, 1980; Frankel & Soulé, 1981; Schonewald–Cox et al., 1983), limited attention has been given to the potential influences of agricultural land use methods and farming practice on the genetic variability of native species living therein. This is of particular interest, for example, to determine whether pest organisms develop genetic resistance to synthetic chemical pesticides (Hawksworth, 1991; Avise & Hamrick, 1995; Dickson & Whitman, 1996; Pons et al., 1998; Nevo, 2001; Pearman, 2001; Weibull et al., 2003).

Native species often face habitat loss and fragmentation in landscapes which have been modified by humans for agriculture (Cale, 2003). Such changes may include a decline in the size of habitat patches and an increase in their spatial and genetic isolation (Saunders et al., 1991). However, it is generally considered essential that levels of genetic diversity remain constant in order to maintain long–term conservation of populations (Frankel & Soulé, 1981; Simberloff, 1988; Opdam, 1990). Decreased levels of genetic variation can lead to inbreeding depression, reducing a population’s ability to adapt to short–term environmental disturbances (Allendorf & Leary, 1986; O’Brien & Evermann, 1988; Milligan et al., 1994), hindering adaptation to long–term environmental changes and possibly leading to extinction (Gilpin & Soulé, 1986; Lacy, 1997). Fragmentation or destruction of habitats, through agriculture for example, is an major cause of the decline of genetic variability and also genetic exchange among populations (Lande & Shannon, 1996; Frankham, 1995; Bjornstad et al., 1998).

The earthworm Lumbricus terrestris (Linneaus 1758) plays a valuable role role in nutrient cycles and energy flows in terrestrial ecosystems. Due to their biology, earthworm populations can indicate the structural, microclimatic, nutritive and toxic situation in soils (Christensen, 1988; Edwards & Bohlen, 1996; Edwards, 1998). They are therefore a suitable model species as their genetic variability should be strongly influenced by diverse agricultural practices such as soil tillage, pesticide use, fertilization and crop rotations (Pfiffner, 2000).

The Spanish slug Arion lusitanicus (Mabille 1868) was originally a local species in the Western Iberian peninsula (Chichester & Getz, 1969).

Distributed by man, it is now introduced in all of Europe. Due to its high reproduction rate and great genetic adaptability to changing environmental conditions, A. lusitanicus is an ideal indi-

cator to detect the effects of short– term land use on genetic structure, particularly because its life expectancy is usually only one year.

Rodents are very suitable as indicators of land use effects as their reproduction rates and ecological valence are generally high. Land management can affect population density, survival and breeding (Jacob & Hempel, 2003). The Common vole Microtus arvalis (Pallas, 1779) commonly uses agroecosystems as its habitat; farming practices such as the use of pesticides and fertilizers, and the removal of shelter, food nesting sites and over– wintering sites may cause the animal considerable stress (Jacob & Brown, 2000). In small isolated populations, genetic diversity may decrease due to genetic drift or inbreeding (Van Treuren et al., 1993).

This can seriously diminish their potential to adapt to changing environments, decrease average individual fitness and consequently increase the extinction risk of populations (Hedrick et al., 1996; Bijlma, 1994, 2000).

In the present study, we measured the genetic variability of the three selected model species (M. arvalis, A. lusitanicus and L. terrestris) in an agricultural landscape which included several types of land use types and different farming practices. Our objective was to analyse whether diverse agricultural management strategies lead to different genetic structure in the selected taxa. As genetic tools, we used RAPD markers to analyse the populations of A. lusitanicus and L. terrestris and multilocus DNA fingerprinting to analyse the genetic structure of M. arvalis because the screened RAPD primers revealed no polymorphic and reproducible RAPD marker.

Materials and methods Site descriptions This study was carried out in two agricultural landscapes in western Germany (fig. 1), one site in northern Saarland (Wahlen) and the other in western Rhineland–Palatinate (Herl/Trier). The sampling sites for the three model species were selected based on different agricultural land types such as arable land (conventional maize, conventional, integrated and ecological barley, forage), meadow and fallow land. The geographic distance between the two sampling sites was about 33 km (the geographic distance between the different sampling locations at each sampling site was 0.1 to 1.8 km).

We created digitalized land use maps (years 1999– 2001) on the basis of the official cadastral maps for both sites.

Sampling design The sampling design for the analyzed populations was generally based based on two different levels.

First, we analyzed populations from geographically separated sites. Second, we analyzed within each site

22

Kautenburger

Germany

6ºE

7ºE

50ºN

50ºN

1

France

2 6ºE

7ºE

Fig. 1. Sampling sites: 1. Herl, near Trier; 2. Wahlen.

Fig. 1. Localidades de muestreo: 1. Herl, cerca de Tréveris; 2. Wahlen.

populations from sampling locations with different land use types (see table 1). Between the two geographically separated sites, Herl and Wahlen, there is no possibility of human–mediated dispersal of the three model species (there is no human– mediated transfer of soil, plants, eggs or organisms between the two sites). Species sampling was carried out during April and October 2000.

Seventeen individuals of L. terrestris were collected from the soil using electrical sampling technique according to a standard operation procedure guideline (Klein & Paulus, 1995). Nineteen individuals of A. lusitanicus were collected by hand from 10 different sampling sites (190 slugs in total) and 12–14 individuals of M. arvalis) were trapped in live capture traps in 5 different fields (65 voles in total). Muscle tissue samples of all collected individuals were stored at –20°C. DNA–techniques Multilocus DNA fingerprinting: all eukaryotic genomes contain many polymorphic loci known as variable number of tandem repeats (VNTRs).

Polymorphisms at such loci are the result of variations in the number of tandem repeats of a short core sequence. DNA probes comprising tandem repeats of a core sequence are used to hybridize multiple variable DNA fragments, and produce an individual–specific multilocus DNA fingerprint (Jeffreys et al., 1985; Epplen et al., 1991; Wan & Fang, 2003). This can be performed by the appli-

cation of a mixture of single locus probes or application of a single probe that identifies multiple similar sequence polymorphisms. In the latter case, one is detecting unidentified fragments of DNA and the result is therefore a DNA phenotype rather than a genotype.

RAPD–PCR fingerprinting: a single 10–base oligonucleotide primer is used to amplify genomic DNA for the RAPD–PCR technique (Williams et al., 1990; Welsh & McClelland, 1990). A DNA amplification product is generated for each genomic region that happens to be flanked by a pair of 10– base priming sites (in the appropriate orientation), which are within about 5,000 base pairs of each other. Amplification products are analysed by gel electrophoresis. Genomic DNA from two different individuals often produces different amplification fragment patterns. A particular DNA fragment, which is generated for one individual but not for another, represents a DNA polymorphism and can be used as a genetic marker.

DNA extraction Genomic DNA from muscle tissue was extracted with a modified salt–chloroform method (Müllenbach et al., 1989). The frozen tissue (10– 20 mg) was ground in liquid nitrogen, transferred to a sterile Eppendorf tube with 0.5 ml of extraction buffer (160 mM Saccharose, 80 mM EDTA, 100 mM Tris/HCl, pH 8.0), 20 µl Proteinase K (20 mg/ml) and incubated for 12–18 h at

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Animal Biodiversity and Conservation 29.1 (2006)

RAPD profiling Table 1. Analysed species, number of analysed individuals (N), and description of the sampling sites (Ss: H. Herl; W. Wahlen) and locations including land use (Sl: Cm. Conventional maize; Eb. Ecological barley; Ef. Ecological forage; Fl. Fallow land [FlH. Fallow land Hohberg; FlZ. Fallow land Zill]; Ib. Integrated barley; Cb. Conventional barley; M. Meadow).

Table 1. Especies analizadas, número de individuos analizados (N) y descripción de los lugares de muestreo (Ss: H. Herl; W. Wahlen) y su localización incluyendo el uso del suelo (Sl: Cm. Maíz convencional; Eb. Cebada ecológica; Ef. Forraje ecológico; Fl. Tierra de barbecho; [FlH. Barbecho Hohberg; FlZ. Barbecho Zill]; Cb. Cebada covencional; M. Prado).

Species

Ss

L. terrestris

H

W A. lusitanicus

M. arvalis

H

Sl

N

Cm

17

Eb

17

Fl

17

Cm

17

Several oligonucleotide primers (Roth GmbH) were surveyed and the most intense and reproducible bands for each species were selected (table 2).

Amplifications were carried out in 25 µl volumes containing 2 µl of template DNA (~100 ng), 18 µl of sterile H 2 O, 2.5 µl of 10 x PCR buffer (DNAzymeTM II), 0.5 Units (0.25 µl) DNAzymeTM II Polymerase (FINNZYMES), 2.5 µl of 10 mM primer and 0.5 µl of 10 mM dNTPs (Amresco).

The DNA amplification was performed in a thermal cycler (TGradient, Biometra) programmed for an initial denaturation of 120s at 94°C, followed by 45 cycles of 30s at 94°C, 60s at 38°C, and 120s at 72°C. The final primer extension step was extended to 10 min at 72°C. Polymerase chain reaction (PCR) products were analysed by electrophoresis on 1.4% agarose gels in 1 x TBE buffer (0.089 M Tris–borate, 2 mM EDTA, pH 8.0) for 4 hours at 70 V (55 mA), visualized by staining with ethidium bromide and photographed under UV light with a Polaroid type 667 film (Polaroid Corp.).

Precautions were taken to ensure PCR reproducibility. PCR conditions were optimized following Bielawski et al. (1995), excluding influence of different concentration of genomic DNA. Concentrations of 50 ng/µl genomic DNA were used. Additionally, one randomly chosen sample was amplified with each PCR as reference and one sample was amplified twice in the same PCR. RAPD profiles were replicated by at least two PCR amplifications for each individual genotype so that irregularities could be detected immediately in amplification and electrophoresis conditions.

Eb 01

19

Ef 02

19

Ef 03

19

Eb 04

19

Ib 05

19

Cb 06

19

Multilocus DNA fingerprinting

Cb 07

19

Fl 08

19

M 09

19

W

M10

19

H

Cb

13

Eb

14

Fl

14

FlH

12

FlZ

12

The DNA (50 mg) was digested to completion with 100 units of the restriction enzyme HinfI. DNA fragments were resolved on a 0.8% agarose gel, stained with ethidium bromide, in TBE buffer (0.089 M Tris, 0.089 M boric acid, 0.002 M EDTA) for 24h at 1.0 V/cm. After electrophoresis, the DNA fragments were transferred to nylon membranes (Zetaprobe, Bio–Rad) by vacuum blotting and baked at 80°C for 2h. Preblocking, prehybridization, hybridization and blocking as well as detection of the hybridization signal were performed according to the manufacturer’s protocol (Roche Diagnostics GmbH). The digoxigeninated multilocus probes (GACA)4 and (GTG)5, (Roche Diagnostics GmbH) were hybridized to the nylon membran at 38°C for (GACA)4 and 40°C for (GTG)5 for 5h.

W

65°C. After the addition of 180 µl 6 M NaCl, proteins and lipids were removed by two extraction steps with 500 µl phenol–chloroform–isoamyl alcohol (25:24:1). DNA was precipitated by the addition of a double volume of cold ethanol. A DNA pellet was recovered by centrifugation, washed in 70% ethanol, dried and dissolved in 300 µl of sterile water.

Statistical analysis The repeatability of the RAPD amplification was checked first, and only fragments with 100% repeatability in amplification reactions were included in further analysis.

Each reproducible band in the RAPD profiles was treated as an independent locus with two

24

Kautenburger

Table 2. Characteristics of the RAPD–primers, oligonucleotide probe and level of polymorphism for the RAPD and multilocus fingerprint markers: Pn. Primer name (Carl Roth GmbH & Co., Karlsruhe, Germany); S(5'–3'). Sequence (5'–3'); G+C. DNA content of Guanine and Cytosine; Fs. Fragment size; Nb. Number of bands; Pb. Polymorphic bands; Re. Restriction enzyme; Op. Oligonucleotide probe.

Table 2. Características de los cebadores (primers) RAPD, la sonda de oligonucleótidos y el nivel de polimorfismo de los marcadores de huellas genéticas multilocus y RAPD: Pn. Nombre del cebador (Carl Roth GmbH & Co., karsruhe, Germany); S(5'–3'). Secuencia (5'–3'); G+C. Contenido de Citosina y Guanina en el ADN; Fs. Tamaño del fragmento; Nb. Número de bandas; Pb. Bandas polimórficas; Re. Enzima de restricción; Op. Prueba del oligonucleótido.

Species

Pn

S(5'–3')

G+C (%)

Fs (bp)

Nb

Pb (%)

L. terrestris

180–08

CGCCCTCAGC

80

320–1500

25

23 (92.0)

L. terrestris

A–10

GTGATCGCAG

60

290–1470

18

16 (88.9)

L. terrestris

B–10

CTGCTGGGAC

70

390–1610

17

16 (94.1)

A. lusitanicus

270–05

GCCCTCTTCG

70

460–1860

26

25 (96.2)

A. lusitanicus

380–3

GGCCCCATCG

80

530–1840

19

18 (94.7)

A. lusitanicus

480–4

CGCCACGAGC

80

510–1860

25

25 (100.0)

A. lusitanicus

Arion lus.

GTAGTCTCGC

60

380–1940

24

24 (100.0)

Species M. arvalis

Re

Op

Fs (kbp)

Nb

Pb (%)

Hinf I

(GACA)4

1.0–23.5

134

134 (100.0)

alleles, presence or absence of a band. RAPD markers (ranging from 0.1 to 2.3 kb) were scored for presence (1) or absence (0) and entered into a binary matrix representing the RAPD phenotype of each individual genotype. The statistical analyses (similarity indices and genetic distances) were calculated according to the methods of Lynch (1991) and Lynch & Milligan (1994). We further investigated genetic relationships within and between populations by cluster analysis based on Euclidean distances (Statistica 5.0 for Windows, StatSoft, Inc.) using UPGMA (unweighted pair group method using arithmetic average, Sneath & Sokal, 1973). Mantel tests (Mantel, 1967) were performed in order to correlate the matrix of genetic distance and the geographical distance (analysis of isolation by distance, GENEPOP software, version 3.1, Slatkin, 1993; Raymond & Rousset, 1995). The significance of matrix correlation was evaluated by comparing the observed Mantel test statistic, Z, with its random distribution obtained after 1,000 permutations. All 10mer oligonucleotide primers for RAPD–PCR (ROTH Kit 170, 180, 270, 280 and Kit A through D, 120 primers in total) were tested on two different individuals of L. terrestris and A. lusitanicus respectively. The primers used for statistics were selected by the same method as described by Bowditch et al. (1993) and Allegrucci et al. (1995). For the statistical analyses, all markers of the selected primers were combined as suggested by Williams et al. (1993).

Multilocus DNA fingerprinting Presence (1) or absence (0) of a band at a particular position in the multilocus DNA fingerprint (ranging from 2.5 to 23 kb) was treated as a discrete character, and banding patterns were converted

Table 3. Mean S ab (based on 60 RAPD markers) within (italic) and between the analysed populations of L. terrestris from the different sampling locations. (For abbreviations see table 1.)

Table 3. Sab media (basada en 60 marcadores RAPD) en cada población (cursiva) y entre las poblaciones analizadas de L. terrestris de diferentes localidades de muestreo. (Para las abreviaturas ver tabla 1.)

Cm(H) Fl(H) Eb(Herl) Cm(W)

Cm(H)

Fl(H)

Eb(H)

Cm(W)

0,735

0,492

0,533

0,537

0,644

0,504

0,482

0,667

0,508 0,605

25

Animal Biodiversity and Conservation 29.1 (2006)

into binary matrices. The total banding number of each isolate and the number of bands shared by each pair of isolates were counted. The similarity index (Sab) was calculated according to the formula: Sab = 2 x nab / (na + nb), where na and nb represent the total number of bands present in the DNA fingerprint patterns of sample a and b, respectively, and nab is the number of bands shared by a and b (Nei & Li, 1979; Lynch, 1991). Subsequently, pairwise genetic distance (D ab) between sample a and b was calculated according to the method of Lynch (1991). The resulting genetic distance values were used as the basis of cluster analysis (UPGMA), and Mantel tests were performed to test isolation by distance.

Results and discussion The selection of primers used for the statistical analysis was based solely on the repeatability of patterns, not on the degree of polymorphism displayed by a primer. The seven informative primers chosen for the analysis of L. terrestris (three primers) and A. lusitanicus (four primers) are listed in table 2. In total, 147 polymorphic bands out of 154 unambiguous and reproducible products were generated with the selected primers, corresponding to 95.5% polymorphism. The primers used in the present study shared no specific motifs and the high percentage of polymorphic bands demonstrate, that the selected primers have generated predominantly independend RAPD markers.

Lumbricus terrestris Based on the reproducibility of the amplified RAPD markers, three primers were chosen for all samples of L. terrestris (table 2). The analysed PCR products ranged from 290 to 1610 bp. In the 68 individuals of the 4 earthworm populations studied, the three RAPD primers amplified a total of 60 scorable fragments; of those, 55 (91.7%) of which were polymorphic. Within all populations of L. terrestris analysed, the similarity indices (Sab, see table 3) were of a relatively similar high value (range between 0.605 and 0.735). Among the populations, Sab were much lower (between 0.482 and 0.537). Using Lynch & Milligan’s (1994) correction for RAPD loci, Nei’s distances (1972) between all pairs of samples were smallest between the earthworm populations of the two maize fields (0.085), although the geographic distances were highest. This finding was confirmed by a UPGMA cluster analysis based on the genetic distances. The UPGMA tree (fig. 2), based on Euclidean distances between the genetic distances Dij of all analysed populations, revealed two main clusters, one of the two populations from the maize fields in Herl and Wahlen and one from the two other fields (fallow and barley, Dij = 0.112) in Herl. To test isolation by distance, the results from genetic distance measures were entered

Maize (Herl)

0.085

Maize (Wahlen) Fallow (Herl)

0.121 0.112

Barley (Herl) Fig. 2. UPGMA dendrogram based on genetic distances Dij for the four populations of L. terrestris from the different farming fields.

Fig. 2. Dendrograma UPGMA basado en las distancias genéticas Dij para las cuatro poblaciones de L. terrestris de los diferentes terrenos agrícolas.

into a Mantel test (1,000 permutations) with geographic distance (fig. 3A). The results from this test revealed no significant correlation between geographic and genetic distance in these populations (Dij vs. geographical distance r = –0.564, P = 0.958). This confirmed the finding obtained from cluster analysis.

The results for earthworms in this study agree with previously published Lumbricides’ findings.

Using RAPD PCR of Aporrectodea spp., Dyer et al. (1998) in Australia showed with that the analysed populations also exhibit a high degree of homogeneity. Stille et al. (1980) found a small amount of genetic variability with enzyme investigations of Aporrectodea tuberculata based only on geographical separation. Several authors (e.g.

Brooks et al., 1995; Pfiffner & Mäder, 1997; Blakemore, 2000) have likewise shown that earthworms populations are strongly influenced by diverse cultural practices, such as soil tillage, use of pesticides, fertilisation and crop rotations (crop residues). Finally, by means of enzyme investigations of L. rubellus in the Faroe Islands, Enckell et al. (1986) determined that geographical barriers or distances have only a slight, or no influence on genetic variation between different populations. In summary, our results coincide with previously published findings reporting that the genetic structure of L. terrestris populations is first dependent on the farming practice and only secondary affected through isolation by distance.

Arion lusitanicus For the populations of A. lusitanicus, the four oligonucleotide primers (Roth GmbH, see table 2) were selected for their intense and reproducible bands.

26

Kautenburger

A

Genetic distance (Dij)

0,12

0,11 r = 0.564 P = 0.958 0,10

0,09

0,08 B

0,24

0

5

10

15

20

25

30

35

40

0,14

Genetic distance (Dij)

0,12

0,20

0,10 0,08 0,06

0,16

0,04

r = 0.907 P = 0.019

0,02

0,12

0,00 0,0

0,4

0,8

1,2

1,6

2,0

0,08 0,04 0,00

0

5

10

15

20

25

30

35

40

C

Genetic distance (Dij)

2,40 2,00 1,60

r = 0.730 P = 0.090

1,20 0,80 0,40 0,00 0

5

10 15 20 25 Geographic distance (km)

30

35

Fig. 3. Relationship (isolation by distance) between genetic distance Dij (Lynch, 1991) and geographic distance of the analyzed populations: A. L. terrestris; B. A. lusitanicus; C. M. arvalis.

Fig. 3. RelaciĂłn (aislamiento por la distancia) entre la distancia genĂŠtica Dij (Lynch, 1991) y la distancia geogrĂĄfica de las poblaciones analizadas: A. L. terrestris; B. A. lusitanicus; C. M. arvalis.

27

Animal Biodiversity and Conservation 29.1 (2006)

Table 4. Mean Sab (based on 94 RAPD markers) within (italic) and between the analysed populations of A. lusitanicus. (For abbreviations see table 1.)

Table 4. Sab media (basada en 94 marcadores RAPD) en cada poblacción (cursiva) y entre las poblaciones analizadas de A. lusitanicus. (Para las abreviaturas ver tabla 1.)

Sampling locations Ib H05 Ib H05

0.710

Cb H06

0.686

Cb H06

Cb H07

Eb H01

Ef H02

Ef H03

Eb H04

Fl H08

M H09

M W10

0.736

Cb H07

0.713

0.733

0.784

Eb H01

0.660

0.672

0.693

0.708

Ef H02

0.684

0.709

0.730

0.680

0.735

Ef H03

0.686

0.725

0.732

0.675

0.715

0.729

Eb H04

0.685

0.720

0.745

0.637

0.706

0.717

0.747

Fl H08

0.668

0.645

0.660

0.632

0.649

0.638

0.638

0.718

M H09

0.674

0.683

0.706

0.637

0.663

0.685

0.685

0.643

0.685

M W10

0.614

0.624

0.637

0.623

0.614

0.617

0.654

0.600

0.608

The statistically evaluated RAPD markers ranged in size from 380 to 1940 bp. In the 190 individuals of the ten populations of A. lusitanicus studied, the primers yielded a total of reproducible 94 fragments. Of those, 92 (97.9%) were polymorphic.

Within all analysed populations, the similarity indices (Sab, see table 4) were of a relatively similar high value (range between 0.685 and 0.784). Between the populations Sab are lower (between 0.632 and 0.733). Values of genetic distance were measured following Lynch (1991).

The highest genetic distances (range from 0.121 to 0.219) can be detected between the geographically most isolated sites from Herl and Wahlen. However, no clear genetic separation between the different farming fields in Herl was seen (values on a relatively low level ranged from 0.015 to 0.088). This result was confirmed by a cluster analysis based on the genetic distances.

The UPGMA tree (fig. 4), based on Euclidean distances between the genetic distances Dij of all analysed populations, revealed one main cluster (all sampling sites in Herl) and one exterior branch (the population of Wahlen). The main cluster can be subdivided into the slug populations of the arable fields (forage and barley sites) and the two analyzed meadow and fallow populations.

Pfenninger (2002) suggested that the population structure of the terrestrial snail Pomatias elegans is mainly a function of the habitat quality and of the spatial arrangement of the habitat network in the landscape and not solely a function of the geographic distance .

0.721

To test isolation by distance in our study, the results from genetic distance measures were entered into a Mantel test (1,000 permutations) with geographic distance (fig. 3B). The results suggest a significant isolation by distance in these populations. (D ij vs. geographical distance r = 0.907, P = 0.019). This agrees with the study of Ross (1999) where genetic distances of the Iowa Pleistocene snail (Discus macclintocki) were strongly related to the geographical distance between all populations; the relationship between genetic distance and watershed distance was especially significant (P = 0.0196). This isolation by distance is also consistent with a study by Pfenninger et al. (1996) with RAPD markers, which found that genetic distance and geographical distance were highly correlated in a similarly sized snail, Trochoidea geyeri (Mantel test: r = 0.567, P < 0.0001, 1,000 permutations). Preliminary results on mtDNA variation in Helix aspersa (Guiller et al., 2001) showed that estimated pairwise correlations between sets of genetic, molecular, morphometric and spatial measurements in northern African colonies indicate that anatomical, and especially biochemical variation is significantly associated with spatial position of sampling localities.

The correlation between geographical and Nei’s distance was r = 0.72 (Madec et al., 1996), while r = 0.50 between geographical and molecular (Kimura 2–parameter) distance. In conclusion, consistent with the literature, we also found an isolation by distance system for the slugs analysed, as well as a distinct influence of the different land use types.

28

Kautenburger

Microtus arvalis Table 5. Comparison of the mean similarity indices (S ab) detected by multilocus DNA fingerprinting within (italic) and between M. arvalis populations from the different sampling locations. (For abbreviations see table 1.)

The structure and amount of genetic variation within and between populations of the common vole M. arvalis were assessed by multilocus DNA fingerprinting. To obtain informative fingerprints, a suitable combination of multilocus minisatellite probes and restriction enzymes had to be found in order to produce the best compromise between a large number of detected bands and minimize the proportions of shared band patterns. As probes we tested (CA)8, (GTG)5, (GACA)4 and (GATA)4, and as restriction enzymes we used EcoR1, Hae III, Hind III and Hinf I. The best variable multibanded pattern was obtained by the combination of Hinf I and (GACA)4. Scorable bands were found ranging from 1.0 to 23.5 kb in all populations. A total of 134 informative bands were detected for all individuals (n = 65), and the mean number of bands per individual was 14.3 ± 0.5. All multilocus fingerprint markers were polymorphic. The genetic similarity within all populations was found relatively low (table 5). Similarity indices within the fallow populations (0.344–0.447) were significantly higher than in the two barley populations (0.152 and 0.202). This result might reflect a smaller effective population size (Ne) in the barley fields in relation to the fallow land. The calculation of mean similarity indices between all analyzed populations was significantly lower (Mann–Whitney U–test, P = 0.005) than values within populations (table 5).

Only the mean similarity index between the two

Table 5. Comparación de los índices de similaridad media (Sab) detectados por huellas genéticas multilocus del DNA en cada población (cursiva) y entre las poblaciones de M. arvalis de diferentes localidades de muestreo. (Para las abreviaturas ver tabla 1.)

FlZ(W) FlH(W) Eb(H) Cb(H) Fl(H) FlZ(W) 0.447 0.264

0.111

0.037 0.069

FlH(W)

0.093

0.092 0.038

0.202

0.091 0.094

Eb(H) Cb(H) F(H)

0.426

0.152 0.115 0.344

fallow populations of Wahlen (0.264) showed a relatively high value. The low similarity indices analyzed in this study agree with values detected in unrelated individuals of pine voles (M. pinetorum, Marfori et al., 1997). These results suggest a high

01 Ecological barley Herl 02 Ecological forage Herl 03 Ecological forage Herl 06 Conventional barley Herl

0.080

07 Conventional barley Herl 05 Integrated barley Herl

0.045 0.121

04 Ecological barley Herl 08 Long storage fallow Herl

0.219

09 Meadow Herl 10 Meadow Wahlen

Fig. 4. UPGMA dendrogram based on genetic distances Dij for the ten populations of A. lusitanicus from different land use and farming types.

Fig. 4. Dendrograma UPGMA basado en las distancias genéticas Dij de las diez poblaciones de A. lusitanicus procedentes de distintos usos del suelo y prácticas agrícolas.

29

Animal Biodiversity and Conservation 29.1 (2006)

Fallow Zill–Wahlen

0.573

Fallow Hoberg–Wahlen Ecological barley Herl

2.310 0.655

Conventional barley Herl

1.031

Ecological fallow Herl

Fig. 5. Genetic relationship (UPGMA tree) between the populations of Microtus arvalis based on genetic distances according Lynch (1991) revealed by multilocus DNA fingerprinting.

Fig 5. Relación genética (árbol UPGMA) entre las poblaciones de Microtus arvalis, basada en las distancias genéticas según Lynch (1991), reveladas por la técnica de las huellas genéticas multilocus del DNA.

level of genetic variability of common voles within populations as well as between geographically separated populations.

Additional insights on genetic structure are offered by a cluster analysis, based on Euclidean distances between the genetic distances (Lynch, 1991) of all populations. The UPGMA tree (fig.

5) revealed two main clusters. The first division of the dendrogram separated the two populations of Wahlen from the sampling sites in Herl according to their geographic distance. The second division of the tree subdivides the different land use types (barley and fallow land) of the sampling site Herl. However, a possible influence of farming practice (ecological or conventional farming) on the genetic structure of M. arvalis cannot be detected. The result observed in this study contrasts with that found for the spatial behavior of common voles in relation to different farming practices (Jacob & Hempel, 2003). However, the results of the cluster analysis are confirmed by the analysis of isolation by distance (fig. 3C). Increased genetic distance was associated with increased geographical distance but the Mantel test revealed no significant correlation (r = 0.730, P = 0.090, 1,000 permutations). A comparison of our results with previously published data might be difficult because no other multilocus DNA fingerprinting findings of M. arvalis are available. Van de Zande et al.

(2000) also observed a high level of genetic variability within root vole (M. oeconomus) populations revealed by microsatellite markers.

In summary, the relatively low genetic similarity of M. arvalis observed in our study agrees with other vole studies. In contrast with other findings, we did not find a clear influence of different farming practices on vole genetics.

In conclusion, populations of M. arvalis from sampling sites with different land use show different genetic structures; however, geographic distances and isolation barriers are the main factors influencing the genetic variability of M. arvalis populations. The genetic variability in A. lusitanicus populations is correlated with geographic distance as well as with different land use methods (i.e. fallow land, meadow land or barley). However, different farming forms (conventionally or ecologically) show no significant influence on the slug genetics. Our results suggest that the genetic structure of L. terrestris populations is influenced by the agricultural land use method practiced on the different sampling sites but not by geographical distance. Although L. terrestris and A. lusitanicus are hermaphrodite species, self–fertilisation could not be detected in this study because no identical RAPD patterns for two individuals were revealed.

Additionally, the level of polymorphism in all three analysed species showed comparably high values, near 100%, so that in spite of the different genetic methods used the statistical results were at least distantly related. For conservation management strategies in agriculturally used landscapes it would be relevant to determine what kind of organism should be protected. Depending on the species analysed, the type of farming practice or changes in land use can cause a severe impact on the genetic structure of populations. The three model organisms analysed in the present study showed high reproduction rates and therefore high effective population sizes so that within each sampling site a high genetic diversity can be observed. However, the loss of genetic variability due to intensive agricultural land use can significantly undermine the viability of populations, particularly for some long– lived species with lower reproductive rates.

30

Acknowledgements The author wish to thank the following persons for supporting this research: Paul Müller as department head of the Institute of Biogeography at the University of Trier, Tanja Rölker, Tanja Peter, Dominik Eisenbarth and Markus Langer for sampling and laboratory work. The German Research Foundation (DFG) financially supported parts of the study (SFB 522, project B7).

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Animal Biodiversity and Conservation 29.1 (2006)

33

Amphibians in the Region of Murcia (SE Iberian peninsula): conservation status and priority areas A. Egea–Serrano, F. J. Oliva–Paterna & M. Torralva

Egea–Serrano, A., Oliva–Paterna, F. J. & Torralva, M., 2006. Amphibians in the Region of Murcia (SE Iberian peninsula): conservation status and priority areas. Animal Biodiversity and Conservation, 29.1: 33–41.

Abstract Amphibians in the Region of Murcia (SE Iberian peninsula): conservation status and priority areas.— The conservation status of amphibian species was studied in the Region of Murcia, taking into consideration 10 variables concerning their biology and distribution. The results obtained show that the amphibian species exposed to the highest risk of extinction in the study area are those with long larval development and a restricted distribution range. According to this species classification, an index is proposed for assessing areas whose conservation is of the highest priority. In the Region of Murcia, most of these areas are located in the main mountain systems, primarily confined to the northwest. Regional Parks and proposed priority conservation areas overlap by only about 12%. The current isolation of these areas makes it necessary to undertake habitat restoration programmes to ensure their interconnection.

Key words: Amphibians, Region of Murcia, Species conservation, Priority areas.

Resumen Anfibios en la Región de Murcia (SE península ibérica): estatus de conservación y áreas prioritarias.— Se ha analizado el estado de conservación de las especies de anfibios presentes en la región de Murcia en función de 10 variables relacionadas con la biología y distribución de dichas especies. Los resultados obtenidos muestran que las especies de anfibios expuestas al mayor riesgo de extinción en el área de estudio son aquéllas que presentan un desarrollo larvario prolongado y una distribución restringida. En función de esta clasificación de las especies, se propone un índice que permita evaluar las áreas cuya conservación es prioritaria. En la Región de Murcia, la mayor parte de estas áreas están localizadas en los principales sistemas montañosos y limitadas principalmente a la comarca nordoccidental del área de estudio. El solapamiento entre los Parques Regionales y las áreas propuestas de conservación prioritaria es sólo del 12%. El aislamiento actual de estas áreas hace necesario emprender programas de restauración del hábitat para garantizar su conexión.

Palabras clave: Anfibios, Región de Murcia, Conservación de especies, Áreas prioritarias.

(Received: 29 VI 05; Conditional acceptance: 20 IX 05; Final acceptance: 10 X 05) A. Egea–Serrano, F. J. Oliva–Paterna & M. Torralva, Dept. de Zoología y Antropología Física, Fac. de Biología, Univ. de Murcia, 30100 Murcia, España (Spain).

Corresponding author: A. Egea–Serrano. E–mail: aegea@um.es

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

34

Egea–Serrano et al.

Introduction

Material and methods

Environmental alteration as a consequence of anthropic activity is considered to have contributed to the decline of numerous amphibian populations throughout the world (Wake, 1991; Galán, 1997; Pechman & Wake, 1997; Marco, 2002a, 2002b). A complete inventory of amphibian species present in a determined territory, as well as its distribution range, is of priority interest. Such information would provide a basic tool to establish the regional conservation status of the different species (UICN, 2003) and consequently, to develop management programmes to ensure their conservation (Palomo & Antúnez, 1992). Monitoring efforts have enabled conservation status to be established on wide spatial scales (Pleguezuelos et al., 2002). Nevertheless, determining distribution and conservation status at a regional scale is also necessary since these parameters can vary greatly for a given species from one region to another (Gärdenfors et al., 1999, 2001).

In addition to species conservation, another target in conservation biology is to prioritize areas on the basis of their biological value (Sutherland, 2000), selecting those which show the highest priority.

Such areas could represent a valuable tool for establishing conservation and management programmes. As regards amphibians, some studies have established important areas for herpetofauna conservation in the Iberian peninsula (Santos et al., 1998; Mateo, 2002). These studies include the Region of Murcia consider amphibian and reptile species together, and no such studies establish priority areas in this territory as a function of amphibian species present alone.

The Region of Murcia in the southern Iberian peninsula is considered one of the most important areas in the Mediterranean region for its amphibian species diversity and/or endemic amphibians (Borkin, 1999). It is characterized by an arid climate (Vidal–Abarca et al., 1992), which makes it unfavorable for amphibians due to hydrological stress and lack of breeding habitats that such climatic conditions represent. Moreover, these factors make the amphibian species present in the Region of Murcia more vulnerable to land use changes affecting this area (Martínez & Esteve, 2003) as they involve a severe habitat degradation process. Several studies dealing with amphibian biology and distribution (Miñano et al., 2003; Egea– Serrano, 2005; Egea–Serrano et al., 2005a, 2005b, 2005c, 2005d, 2005e, 2005f) have been performed.

Nevertheless, to date, there has been no study concerning the risk of extinction of amphibians in the Region of Murcia.

The objectives of the present study were to develop a methodology based on the biological and ecological constraints and distributions of amphibian species to evaluate the risk of extinction of the species present in the Region of Murcia and to establish areas whose conservation should be considered priority.

The study area is restricted to the Region of Murcia (SE Iberian peninsula). This territory includes most of the Segura River basin, one of the most arid of the Iberian peninsula (Vidal–Abarca et al., 1987) and, probably, of Europe (Geiger, 1973). Eleven ecological sectors have been recognised in this basin (Vidal– Abarca et al., 1990), most of them exposed to a dry, hot and arid climate. However, during the last three decades land uses in the study area have been increasingly devoted to extensive agricultural irrigation practices (Martínez & Esteve, 2003), while traditional land uses (non–irrigated agricultural farms) are restricted to the northwestern region of the study area (Pérez & Lemeunier, 2003).

Following Andreone & Luiselli (2000) and Filippi & Luiselli (2000), 10 biological and ecological variables were analysed. These variables include aspects dealing with the distribution, demography, ecology and taxonomy of the species present in the study area. Data for these variables were obtained from the bibliography, as well as from the experience of the authors (table 1). Independent variables were categorised, ranging from the lowest (category 0) to the highest (categories 2, 3, 4, 10, depending on the variable) risk of extinction.

The variables considered in this study are related as follows, as well as their categories and the rationale for the choice of these scores.

Species presence in the Region of Murcia, based on data presented by Egea–Serrano et al. (2005b, 2005c): 0. Present in >50% of the study area surface; 1. Present in 10–50%; 2. Present in 5–10%; 3.

Present in <5% of the study area surface.

Reproductive strategy: 0. Taxon with several reproductive periods throughout the active season; 1. Taxon with 2–3 reproductive periods during active season; 2. Taxon with a single reproductive event each year; 3. Ovoviviparous taxon or showing parental care. It is assumed that species that breed more frequently can recover faster when their habitat is altered. Furthermore, an ovoviviparous taxon (or showing parental care) is expected to be exposed to a higher risk of extinction than an oviparous one in altered habitats. This is because adult individuals carry their embryos for a long period of time and, as a consequence, the probability of some sort of alteration or even death of adults involving the loss of offspring is higher.

Eggs (offspring) number: 0. >200 eggs/ newborns; 1. 50–200; 2. 10–50; 3. <10. Species showing a higher fertility can recover more easily in the face of habitat alteration.

Habitat breadth: based on data presented by Egea–Serrano et al. (2005b, 2005c) and on 11 ecological sectors described by Vidal–Abarca et al.

(1990): 0. Species present in all sectors; 1. Species present in 10 sectors; 2. Species present in nine sectors; 3. Species present in eight sectors; 4. Species present in seven sectors; 5. Species present in six sectors; 6. Species present in five sectors; 7. Species present in four sectors; 8. Spe-

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Animal Biodiversity and Conservation 29.1 (2006)

Table 1. Bibliographic references used to define scores for studied species for each threatening factor: RS. Reproductive strategy; EN. Egg (offspring) number; H. Habits; MA. Maximum age; BH. Breeding habitat; TU. Taxonomic uniqueness; 1. Alcobendas & Buckley, 2002; 2. Arntzen & García– París, 1995; 3. Barbadillo et al., 1999; 4. Bosch, 2003; 5. Busack, 1986; 6. Díaz–Paniagua, 1986; 7. Egea–Serrano et al., 2005e; 8. Egea–Serrano et al., 2005f; 9. Esteban et al., 2004; 10. García– París et al., 2003; 11. García–París, 2004; 12. Guyétant et al., 1999; 13. Lizana et al., 1994; 14.

Martínez–Solano & García–París, 2002; 15. Martínez–Solano et al., 2003; 16. Montori & Herrero, 2004; 17. Nöllert & Nöllert, 1995; 18. Rebelo & Caetano, 1995; 19. Salvador & García–París, 2001; 20. Salvador, 2005; 21. Toxopeus et al., 1993; * Experience of the authors.

Tabla 1. Referencias bibliográficas utilizadas para definir las puntuaciones de las especies de anfibios estudiadas para cada factor de riesgo: RS. Estrategia reproductiva; EN. Número de huevos (descendientes); H. Hábitos; MA. Edad máxima; BH. Hábitat reproductor; TU. Exclusividad taxonómica; * Experiencia de los autores. (Para las otras abreviaturas ver arriba.)

Species

RS

EN

H

MA

BH

Salamandra salamandra

10

*

16

18

7

Rana perezi

TU 1, 10, 16

6

19

11, *

19

8, *

19

15, 20

4

20, 11

4

19, *

2, 11

Alytes obstetricans

4

4

4, 11

4

11, *

2, 11

Bufo calamita

6

19

3, 19

19

19, *

19

Bufo bufo

6

19

3, 19

19

11, *

19

Pelodytes punctatus

6

12, 21

12, 21

9

3, 19, *

19

Discoglossus jeanneae

19

19

19

19

14

5, 11

6, 13

19

11

17, 3

13, 19, *

19

Alytes dickhilleni

Pelobates cultripes

cies present in three sectors; 9. Species present in two sectors; 10. Species present in one sector. This variable reflects species tolerance for environmental variables.

Habits of adult phase: 0. Nocturnal fossorial species or with aquatic activity; 1. Nocturnal species; 2. Diurnal species with cryptic habits; 3.

Diurnal species with obvious habits. It is assumed that obvious species are more exposed to man and predator persecution.

Maximum age: 0. > 15 years; 1. 11–15 years; 2.

6–10 years; 3. 1–5 years.

Adaptability to altered environments: based on the experience of the authors: 0. Species extremely adaptable (found even in urban parks); 1.

Adaptable species (found in suburbia intermingled with small natural fields); 2. Species scarcely adaptable (found in medium sized natural habitat); 3. Unadaptable species (found only in large patches of natural habitat).

Altitudinal distribution: based on data presented

by Egea–Serrano et al. (2005d). 0. Ubiquitous; 1.

Present at high elevations (> 900 m); 2. Species present at a wide range of medium altitudes; 3. Estenohypse species found at medium altitudes; 4. Estenohypse species found at medium altitudes, but restricted to high plateaus. In the study area, sites located at high altitudes are more mountain-

ous than the rest, which makes them inaccessible for most human activies. Species present at high altitudes are therefore more protected from habitat degradation resulting from anthropic activities than those inhabiting less mountainous localities.

Breeding habitat: 0. Taxon which breeds in temporal and permanent water bodies; 1. Taxon which breeds in temporal water bodies; 2. Taxon which breeds in permanent water bodies. It is assumed that species that breed in both permanent and temporal water bodies can better face the pressure resulting from anthropogenic activities than species that only breed in permanent water bodies, most of which in the study area are dedicated to farming activities.

Taxonomic uniqueness: 0. Species of a polytypic genus with more than three recognised subspecies; 1. Species of a polytypic genus with 1–3 recognised subspecies; 2. Monotypic species of a polytypic genus; 3. Species of a monotypic genus.

It is assumed that a species recognised as representing a monotypic genus has more importance from a conservation point of view.

All environmental variables were submitted to a multifactorial analysis to classify different amphibian species depending on their similarities in relation to their risk of extinction, a methodology successfully used in previous studies on amphibians and reptiles (Andreone & Luiselli, 2000; Filippi &

36

Luiselli, 2000). According to these authors, this statistical approach allows studied species to be grouped in a more suitable way than univariate techniques since relations between variables can be established. Anuran and urodele species were analysed together because no information is available concerning the main differences between these two groups in relation to their biology and sensitivity to habitat degradation. The multifactorial analysis used was a multiple correspondence analysis (MCA). This statistical technique allows information provided by original data to be reduced to two dimensions which explain most data variance, and assigns a new coordinate to each case for each dimension extracted by the analysis (Visauta, 1998).

According to the values obtained for each dimension, species have been assigned to one of the following categories, ranging from low to high risk of extinction: 1. Species showing positive values for both dimensions (low risk of extinction); 2. Species showing positive values for dimension 1 and negative values for dimension 2 (low–medium risk of extinction); 3. Species showing negative values for dimension 1 and positive values for dimension 2 (medium–high risk of extinction); 4. Species showing negative values for both dimensions (high risk of extinction).

To establish priority conservation areas from the point of view of the amphibian species present, the surface area of the Region of Murcia was divided into a 5 x 5 km UTM grid. The number of amphibian species present for each square was determined according to information presented by Egea–Serrano et al. (2005b, 2005c). Additionally, the proportion of squares occupied by each species was calculated in relation to the number of 5 x 5 UTM squares into which the study area was divided. This procedure allowed to estimate species extension in the study area, establishing an index of area occupation in Murcia (D) with five categories ranging from high to low presence: 1. Species present in > 30% of the surface of the region. This area corresponds to the area of occupancy of a species considered as Near Threatened or Least Concern according to UICN categories (UICN, 2001). 2. Species present in 10– 30% of the surface of the region. This area corresponds to the area of occupancy of a species whose risk of extinction can be considered intermediate between Near Threatened or Lleast Concern and Vulnerable categories, according to UICN criteria (UICN, 2001). 3. Species present in 5–10% of the surface of the region. This area corresponds to the area of occupancy of a species considered Vulnerable according to UICN categories (UICN, 2001). 4. Species present in 1–5% of the surface of the region. This area corresponds to the area of occupancy of a species whose risk of extinction can be considered intermediate between Vulnerable and Endangered categories, according to UICN criteria (UICN, 2001). 5. Species present in < 1% of the surface of the region. This area corresponds to the area of occupancy of a species considered Endangered according to UICN categories (UICN, 2001).

Egea–Serrano et al.

Considering the calculated amphibian distribution data, number of species per square and the previously calculated risk of extinction for each species, a biological value was calculated for each 5 x 5 km square through the expression:

(MCAi+Di)+Sppj where MCAi is the risk of extinction for species i, Di is the distribution of species i in the Region of Murcia, and Sppj the number of amphibian species for j square.

Squares showing values higher than the 75th percentile for this index were selected as priority conservation squares.

Statistical analysis were performed with the SPSS® statistical package.

Results The scores for the independent variables for the amphibian species in the Region of Murcia are presented in table 2. The results provided by multiple correspondence analysis have enabled identification of three groups of species (fig. 1). Table 3 shows the scores for each variable in each dimension extracted by the MCA. Breeding habitat combined the highest value for dimension 1 (0.770) and the lowest for dimension 2 (0.067), whereas species presence presented the lowest value for dimension 1 (0.682) and the highest for dimension 2 (0.911). This implies that the main variables arranging species through dimension 1 and dimension 2 in the Region of Murcia are, respectively, breeding habitat and species presence.

Table 4 shows the values obtained for variables risk of extinction and extension in the study area for each amphibian species.

The 5 x 5 km UTM squares showing biological value indices higher than the 75th percentile were considered as priority conservation areas. The total number of such areas added up to 103 (fig. 2) and represented 16% of the surface of the Region of Murcia.

Discussion Although Andreone & Luiselli (2000) indicate that both univariate and multivariate methodology sufficiently characterise the conservation status of a species group, multivariate analysis alone was used in the present study as univariate analysis is considered to have the disadvantage of not establishing relationships between variables and therefore not realistically ranking the studied species according to their risk of extinction.

The results obtained show that the species exposed to higher risk of extinction are those which depend on the presence of permanent water bodies to complete their larval development and which, in addition, show a restricted distribution

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Animal Biodiversity and Conservation 29.1 (2006)

Table 2. Scores for the independent variables considered to affect survival of amphibian species in the region of Murcia: P. Presence in the region of Murcia; RS. Reproductive strategy; EN. Egg (offspring) number; HB. Habitat breadth; H. Habits; MA. Maximum age; AE. Adaptability to altered environments; AD. Altitudinal distribution; BH. Breeding habitat; TU. Taxonomic uniqueness.

Tabla 2. Puntuaciones para las variables independientes que se considera que afectan a la supervivencia de las especies de anfibios en la región de Murcia: P. Presencia en la región de Murcia; RS. Estrategia reproductora; EN. Número de huevos (descendientes); HB. Amplitud de hábitat; H. Hábitos; MA. Edad máxima; AE. Adaptabilidad a ambientes alterados; AD. Dsitribución altitudinal; BH. Hábitat reproductor; TU. Exclusividad taxonómica.

Species

P

RS

S. salamandra

3

3

R. perezi

1

A. dickhilleni A. obstetricans

EN

HB

H

MA

AE

AD

BH

2

9

1

0

2

1

2

0

2

0

1

3

2

0

0

0

2

3

2

2

9

1

2

2

1

2

2

3

2

2

10

1

2

2

4

2

0

B. calamita

1

2

0

1

1

1

1

0

1

2

B. bufo

2

2

0

4

1

0

1

2

2

1

P. punctatus

2

2

0

4

1

2

1

2

0

2

D. jeanneae

3

1

0

10

1

2

3

1

2

2

P. cultripes

3

2

0

5

1

1

1

3

0

2

range in the study area. On the other hand, species showing higher plasticity in relation to breeding habitat and a widespread distribution range are less threatened.

High–medium risk of extinction

The studied species can be classified into three groups according to their risk of extinction, as seen from our results. Species facing the highest risk of extinction in the Region of Murcia included S.

Low risk of extinction

3 2

Ss

Ao Ad Dj

Rp Bc

1 Pc

0 –2

–1

0

1

2

Pp

–1 –2

TU

Bb

–3 High risk of extinction

Low–medium risk of extinction

Fig. 1. Bidimensional plot of scores for each studied species in the dimensions extracted by multiple correspondence analysis. Amphibian species groups according to their risk of extinction are identified.

Ss. Salamandra salamandra; Rp. R. perezi; Ad. A. dickhilleni; Ao. A. obstetricans; Bc. B. calamita; Bb. B. bufo; Pp. P. punctatus; Dj. D. jeanneae; Pc. P. cultripes.

Fig. 1. Representación bidimensional de las puntuaciones de cada especie estudiada para las dimensiones extraídas por el análisis de correspondencias múltiple. Los grupos de especies de anfibios se identifican en función de su riesgo de extinción. (Para las abreviaturas, ver arriba.)

38

Egea–Serrano et al.

Table 3. Scores for two dimensions extracted by multiple correspondence analysis for independent variables: E. Eigenvalue. (For abbreviations see table 2.)

Table 4. Scores for amphibian species existing in the region of Murcia for the variables risk of extinction (RE) and extension of distributiion (E).

Tabla 3. Puntuaciones para las dos dimensiones extraídas por el análisis de correspondencia múltiple para las variables independientes. (Para las abreviaturas ver tabla 2.)

Tabla 4. Puntuaciones de las especies de anfibios presentes en la región de Murcia para las variables riesgo de extinción (RE) y extensión de distribución (E).

Dimension 1 (E = 0.63)

Dimension 2 (E = 0.44)

Species

RE

E

S. salamandra

3

P

0.682

4

0.911

RS

A. dickhilleni

3

4

0.369

0.031

A. obstetricans

3

4

EN

0.687

0.059

D. jeanneae

3

5

HB

0.954

0.939

B. calamita

1

2

H

0.234

0.229

B. bufo

2

3

MA

0.308

0.260

P. punctatus

2

3

AE

0.917

0.485

P. cultripes

2

4

AD

0.943

0.937

R. perezi

1

1

BH

0.770

0.067

TU

0.499

0.551

Variable

salamandra, A. dickhilleni, A. obstetricans and D. jeanneae. However, when the IUCN Red List Criteria are applied to these species at a worldwide level (UICN, 2001), only A. dickhhilleni is described as vulnerable (IUCN, 2004). Nevertheless, the group formed by the above species shows a higher risk of extinction than the other studied species when the IUCN Red List Criteria at country level (UICN, 2003) are applied (Pleguezuelos et al., 2002).The degree of agreement between this classification and our results was good. In relation to the remaining species studied, although they have not been evaluated at a worldwide level (IUCN, 2004), when the IUCN Red List Criteria are applied at country level (UICN, 2003) they are not classified separately (Pleguezuelos et al., 2002); they all show a low risk of extinction (Least Concern). In contrast with this classification, the index applied at a regional level in the present study identified a group of species exposed to a low–medium risk of extinction (B. bufo, P. punctatus and P. cultripes) and another group with a low risk of extinction (R. perezi and B. calamita). This difference demonstrates the importance of a spatial scale in evaluating a taxon´s risk of extinction.

If a species in a region is considered threatened (as is the case of S. salamandra, A. dickhilleni, A. obstetricans and D. jeanneae in Murcia) measures must be taken to ensure the conservation of these populations in this territory.

Such measures should include the conservation of traditional farming practices because these would contribute to preserving terrestrial habitats suitable for the adult individuals of many species, as well as water bodies where many species can finish their larval development, as suggested by several authors (París et al., 2002; Martínez– Solano et al., 2004; unpublished data).

The importance of mountain systems in amphibian conservation in the Region of Murcia is clear.

Most areas whose conservation has been considered priority in the present study (80%) are located in the main mountains of the study area, and have been proposed as Sites of Community Interest (Baraza, 1999). However, only 12% of the proposed priority conservation areas are included within Regional Parks (Baraza, 2003), the current legally protected areas.

Mateo (2002) showed some of these mountains were valuable areas for herpetofauna conservation, although amphibian and reptile species were considered together. These areas are characterized by habitats of community interest, such as Tetraclinis articulata, Quercus ilex, Quercus rotundifolia, Juniperus phoenicea, or Juniperus thurifera forests (Baraza, 1999), whose distribution range in the study area is restricted. According to our results, the area showing the most noticeable lack of protection is the north eastern part of the study area, a territory where only three out of the 12 squares established as priority conservation areas are included in Sites of Communitary Interest or Regional Parks.

39

Animal Biodiversity and Conservation 29.1 (2006)

WH

XH

YG N WG XG

UTM 5 x 5 km

Fig. 2. Distribution of areas of the highest conservation priority in the Region of Murcia.

Fig. 2. Distribución de las áreas prioritarias de conservación en la Región de Murcia.

The fact that most priority squares are concentrated in the northwestern area of the region, where they coincide with different protected areas, emphasises the biological value of this territory. In addition, the value of this area increases because of its cultural importance from the point of view of traditional land use conservation (Pérez & Lemeunier, 2003).

Finally, it should be mentioned that most of the priority conservation areas suggested in this work are isolated as a consequence of the severe habitat destruction that the Region of Murcia has undergone, and continues to undergo, as a consequence of irrigation crop expansion (Martínez & Esteve, 2003). Such severe environmental degradation means that only species showing low ecological requirements, such as R. perezi, can survive, and it implies that most of the amphibian populations present in the study area will remain isolated. Since ensuring colonization and genetic flow from nearby populations is an essential measure in amphibian conservation (Semlitsch, 2002), habitat restoration programmes need to be undertaken to provide suitable habitats for different amphibian species. This would form biological corridors that make individual migrations feasible. These aspects should be taken into consideration when amphibian populations in the Region of Murcia are subjected to management and/or recovery programmes.

Acknowledgements Part of this research was supported by the Environmental Service of the Autonomous Government of Murcia, Spain. We thank members of Group of Investigation Aquatic Vertebrates Conservation of the Zoology and Physical Anthropology Department of the University of Murcia for their help in field sampling. We also thank Philip Thomas for the English translation.

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"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 29.1 (2006)

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A new species of the genus Stachorutes Dallai, 1973 from Russia (Collembola, Neanuridae) A. Smolis & J. B. Shvejonkova

Smolis, A. & Shvejonkova, J. B., 2006. A new species of the genus Stachorutes Dallai, 1973 from Russia (Collembola, Neanuridae). Animal Biodiversity and Conservation, 29.1: 43–47.

Abstract A new species of the genus Stachorutes Dallai, 1973 from Russia (Collembola, Neanuridae).— A new species of Stachorutes Dallai, 1973, Stachorutes gracilis n. sp. is described from the forest–steppe area of Russia (Cis–Volga Highland). The new species is characterized by 4+4 eyes and reduced chaetotaxy of labium and legs. It is most similar to S. ruseki Kováč, 1999 from Slovakia. Identification key to species of the genus is given.

Key words: Entomology, Taxonomy, Collembola, Neanuridae, Stachorutes, New species, Russia.

Resumen Nueva especie del género Stachorutes Dallai, 1973 de Rusia (Collembola, Neanuridae).— Se describe una nueva especie de Stachorutes Dallai, 1973, Stachorutes gracilis sp. n., procedente de la zona de bosque– estepa de Rusia (tierras altas del cis–Volga). Esta nueva especie se caracteriza por sus 4+4 ojos y la quetotaxia reducida del labio y las patas. Es muy similar a S. ruseki Kováč, 1999 de Eslovaquia. Se incluye una clave de identificación de las especies del género.

Palabras clave: Entomología, Taxonomía, Collembola, Neanuridae, Stachorutes, Especie nueva, Rusia.

(Received: 27 V 05; Conditional acceptance: 29 VI 05; Final acceptance: 31 X 05) Adrian Smolis, Zoological Inst., Univ. of Wrocław, Przybyszewskiego 63/77, 51–148 Wrocław, Poland.– Julja B. Shvejonkova, State Nature Reserve "Privolzhskaya lesostep", Okruzhnaya 12a, 440031 Penza, Russia.

Corresponding author: A. Smolis. E–mail: adek@biol.uni.wroc.pl

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Smolis & Shvejonkova

Introduction The genus Stachorutes was established by Dallai (1973) for a new species S. dematteisi from Italy.

As presently defined (Thibaud & Palacios Vargas 2000), the genus includes 15 species, 9 of which were described from the Palearctic Region. Species of the genus are most similar to those of Pratanurida Rusek, 1973 and Pseudachorutes Tullberg, 1871, but can be easily separated from these by the reduced number of eyes.

During the research of Collembola fauna in the “Privolzhskaya lesostep” (Cis–Volga Highland) reserve, the second author found an unknown species which can be classified within the genus Stachorutes. The present paper contains its description and an updated key for all members of the genus.

Results Stachorutes gracilis n. sp. (figs 1–9) Studied material Holotype: adult male on slide, Russia, SW of Cis– Volga Highland, forest–steppe zone of Mid–Volga region, Penzenski region, Kuznecki district, "Privolzhskaya lesostep" reserve, Kuncherowski plot, dry steppe (Festuca valesiaca), in sandy soil, 27 IX 2000, leg. J. B. Shvejonkova. Paratypes: adult female on slide, Russia, SW of Cis–Volga Highland, forest–steppe zone of Mid–Volga region, Penzenski region, Kuznecki district, "Privolzhskaya lesostep" reserve, Kuncherowski plot, dry pine forest (Pinus sylvestris with Cladonia sp.), in sand soil, 28 VI 2004, leg. J. B. Shvejonkova; adult female on slide, Russia, SW of Cis–Volga Highland, forest–steppe zone of Mid–Volga region, Penzenski region, Kameshkirsky district, "Privolzhskaya lesostep" reserve, near village Shatkino, xerophytic meadow, on the bank of the Kadada river, in sandy soil, 29 V 2005, leg. J. B. Shvejonkova; adult male and 3 adult females on slide, Russia, SW of Cis–Volga Highland, forest– steppe zone of Mid–Volga region, Penzenski region, Kameshkirsky district, "Privolzhskaya lesostep" reserve, near village Shatkino, xerophytic meadow, on the bank of the Kadada river, in sandy soil, 29 V 2005, leg. J. B. Shvejonkova. Type material is

preserved in the collection of the Department of Biodiversity and Evolutionary Taxonomy, Wrocław University, Poland.

Description Habitus as in fig. 1. Body length (without antennae) 0.40– 0.52 mm (holotype: 0.49 mm). Body colour bluish of variable intensity, eyes dark. Granulation homogenous, rather coarse.

Antennae shorter than head. Antennal segment I with 6 setae, antennal segment II with 12 setae.

Antennal segments III and IV fused dorsally.

Chaetotaxy of antennal segments III and IV as in figures 3 and 4. Antennal III–organ with two small internal curved sensilla and two cylindrical guard sensilla (figs. 3, 4). Ventral microsensillum on antennal segment III present. Antennal segment IV with simple apical vesicle, subapical organite, microsensillum, seta i and 6 cylindrical sensilla (fig. 4).

Postantennal organ composed of 5–7 simple vesicles (holotype–6, 7). Area ocularis with 4+4 relatively large, pigmented eyes (figs. 1, 2).

Buccal cone short. Mandible with two teeth, maxilla styliform. Labium with 9+9 setae (seta E absent) and 1+1 subapical denticles (fig. 5). Labrum chaetotaxy 2/2,4.

Dorsal chaetotaxy as in fig. 1. Seta a0 on the head absent, unpaired seta d1 present. Thoracic tergum II with seta a2 and without m4. Seta m4 on abdominal tergum IV absent. Sensillar formula of the body 022/11111. Sensilla relatively thick and slightly longer than ordinary setae. Thoracic sterna without setae, ventral tube with 4+4 setae. Ventral chaetotaxy of abdominal sterna I–VI as in fig. 8.

Furca short. Dens with 4 setae. Mucro distinctly separated from dens, 3 times shorter than dens (fig. 9). Retinaculum with 3+3 teeth.

Tibiotarsi I, II, III with 13, 13, 12 setae respectively (figs. 6, 7). Femora I, II, III with 10, 10, 9 setae respectively. Trochanters with 5 setae each.

Coxae I, II, III with 3, 7, 7 setae respectively.

Subcoxae 2 I, II, III with 0, 2, 2 setae respectively.

Claws without inner tooth. Empodial appendage absent.

Derivatio nominis The species name is derived from the Latin word "gracilis" – delicate, slender, slim. It refers to the body shape of the new species.

Figs. 1–9. Stachorutes gracilis n. sp.: 1. Habitus and dorsal chaetotaxy; 2. Area ocularis; 3. Antennal segments III–IV of right antenna, ventral view; 4. Antennal segments III–IV of right antenna, dorsal view; 5. Labium; 6. Leg III, ventral view; 7. Leg III, dorsal view; 8. Chaetotaxy of abdominal sterna I– VI; 9. Furca, dorsal view.

Figs. 1–9. Stachorutes gracilis sp. n.: 1. Habitus y quetotaxia dorsal; 2. Área ocularis; 3. Segmentos III–IV de la antena derecha, vista ventral; 4. Segmentos III–IV de la antena derecha, vista dorsal; 5.

Labio; 6. Pata III, vista ventral; 7. Pata III, vista dorsal; 8. Quetotaxia de los esternitos I–VI; 9. Furca, vista dorsal.

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Animal Biodiversity and Conservation 29.1 (2006)

3

2

4

5

0.01 mm

0.01 mm

0.01 mm

6

0.01 mm

8 7

0.1 mm

9 0.01 mm

1

46

Smolis & Shvejonkova

Identification key to the genus Stachorutes.

Clave de identificación para el género Stachorutes.

1

0–3 eyes on each side of head 4–6 eyes on each side of head 2 Eyes absent, tibiotarsi I, II, III with 12, 11, 11 setae Eyes present, tibiotarsi I, II, III with higher number of setae 3 Head with 1+1 eyes Head with 2+2 or 3+3 eyes 4 Antennal segment IV with flame–shaped sensilla dens with 5 setae, mucro absent Antennal segment IV with cylindrical sensilla, dens with 6 setae, mucro present 5 Head with 3+3 eyes, dens with 3 setae Head with 2+2 eyes, dens with 4 or 5 setae 6 Mucro present Mucro absent 7 Dens with 4 setae, retinaculum with 3+3 teeth, tibiotarsi I, II, III with 15, 15, 13 setae Dens with 5 setae, retinaculum with 2+2 teeth tibiotarsi I, II, III with 18, 19, 18 setae 8 Antennal segment IV with hammer–shaped sensilla, dens with 5 setae, retinaculum with 3+3 teeth Antennal segment IV with cylindrical sensilla, dens with 4 setae, retinaculum with 2+2 teeth 9 Head with 4+4 or 6+6 eyes Head with 5+5 eyes 10 Head with 4+4 eyes, dens with 4 setae Head with 6+6 eyes, dens with 5 or 6 setae 11 Mucro present, dens with 6 setae, retinaculum with 3+3 teeth Mucro absent, dens with 5 setae, retinaculum with 2+2 teeth

12 Seta a0 on head present, seta m4 on thoracic tergum II present Seta a0 on head absent, seta m4 on thoracic tergum II absent 13 Thoracic tergum I with 3+3 setae, seta a2 on thoracic tergum II present Thoracic tergum I with 2+2 setae, seta a2 on thoracic tergum II absent 14 Dens with 5 setae, postantennal organ with 8 vesicles Dens with 6 setae, postantennal organ with 9–10 vesicles 15 Seta d1 on head present, seta E on labium present, tibiotarsi I, II, III with 19, 19, 18 setae Seta d1 on head absent, seta E on labium absent, tibiotarsi I, II, III with 18, 18, 17 setae

2 9 S. escobarae (Palacios–Vargas, 1990) 3 4 5 S. jizuensis Tamura, 1997 S. tatricus Smolis & Skarżyński, 2001 S. triocellatus Pomorski & Smolis, 1999 6 7 8 S. maya Thibaud & Palacios–Vargas, 2000 S. dallaii Weiner & Najt, 1998 S. sphagnophilus Sławska, 1996 S. dematteisi Dallai, 1973 10 12 S. gracilis n. sp.

11 S. ruseki Kováč, 1999 S. cabagnerensis Simón Benito, Espantaleón & Garcia–Barros, 2005 (Simón Benito et al., 2005) S. navajellus Fjellberg, 1984 13 14 15 S. valdeaibarensis Arbea & Jordana, 1991 S. scherae Deharveng & Lienhard, 1983 S. longirostris Deharveng & Lienhard, 1983 S. tieni Pomorski & Smolis, 1999

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Animal Biodiversity and Conservation 29.1 (2006)

Discussion

References

Among known members of the genus, only S. gracilis n. sp. has 4+4 eyes and 13, 13, 12 setae on tibiotarsi I, II, III respectively. The presence of slightly reduced mucro (distinctly separated from dens) and absence of setae m4 on thoracic tergum II and abdominal tergum IV place the new species near S. ruseki Kováč, 1999 from Slovakia. Additionally, S. gracilis n. sp. differs from the mentioned species in the following characters: postantennal organ with 5–7 vesicles (in ruseki: 8–10), dens with 4 setae (in ruseki: 6), presence of seta a2 on thoracic tergum II (in ruseki absent), absence of seta E on labium (in ruseki present), trochanters with 5 setae each (in ruseki: 6) and femora I–III with 10, 10, 9 setae respectively (in ruseki: 12, 11, 10).

Dallai, R., 1973. Ricerche sui Collemboli. XVI. Stachorutes dematteisi n. gen., n. sp., Micranurida intermedia n. sp. e considerazioni sul genre Micranurida. Redia, 54: 23–31.

Thibaud, J.–M. & Palacios Vargas, J. G., 2000. Remarks on Stachorutes (Collembola: Pseudachorutidae) with a new Mexican species. Folia Entomol. Mex., 109: 107–112.

Simón Benito, J. C., Espantaleón, D. & Garcia– Barros, E., 2005. Stachorutes cabagnerensis n. sp., Collembola (Neanuridae) from Central Spain, and a preliminary approach to phylogeny of genus. Animal Biodiversity and Conservation, 28.2: 147–155.

"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 29.1 (2006)

49

Osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972 R. I. Ruiz–C. & C. Román–Valencia

Ruiz–C., R. I. & Román–Valencia, C., 2006. Osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972. Animal Biodiversity and Conservation, 29.1: 49–64.

Abstract Osteology of Astyanax aurocaudatus, Eigenmann, 1913 (Pisces, Characidae), with notes on the validity of Carlastyanax, Géry, 1972.— The taxonomic status of Astyanax aurocaudatus is difficult to interpret as no relevant osteological data are available to date. In the present paper we studied the osteological, morphometric and meristic characters of this species. The osteological characters of A. aurocaudatus found include the number and shape of premaxilla, maxilla and dentary teeth, second infraorbital separate from the preopercle, anal fins with pterygiophores that differ as towards the anterior, and presence of supra– orbital. These and other characters, body shape and coloring pattern, coincide with descriptions for the genus Astyanax. The characters describing the genus Carlastyanax therefore correspond to incorrect observations and the studied species is situated in the genus Astyanax. Carlastyanax is here considered a synonym of Astyanax.

Key words: Astyanax aurocaudatus, Teleostei, Osteology, Taxonomic status, Colombia.

Resumen Sobre la osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972.— No hay información osteológica sobre Astyanax aurocaudatus que contribuya a interpretar correctamente su estado taxonómico. En este trabajo se realizaron observaciones osteológicas, morfométricas y merísticas. Entre otros caracteres osteológicos de A. aurocaudatus se encuentran: el número y la forma de los dientes en el premaxilar, maxilar y dentario, segundo infraorbital separado del preopérculo, aleta anal con pterigióforos que se modifican al aproximarse al extremo anterior, y supraorbital presente. Estos y otros caracteres coinciden con los descritos para el género Astyanax: forma del cuerpo y modelo de coloración. Los caracteres planteados para describir el género Carlastyanax corresponden a observaciones incorrectas, por lo que la especie objeto de este estudio se sitúa dentro del género Astyanax. Aquí se considera Carlastyanax sinónimo de Astyanax.

Palabras clave: Astyanax aurocaudatus, Teleostei, Osteología, Estado taxonómico, Colombia.

(Received: 30 VIII 05; Conditional acceptance: 29 X 05; Final acceptance: 4 XI 05) R. I. Ruiz–C.(1) & C. Román–Valencia(2), Univ. del Quindío, Lab. de Ictiología, A. A. 460, Armenia, Quindío, Colombia.

(1) (2)

E–mail: zutana_1@yahoo.com E–mail: ceroman@uniquindio.edu.co

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

50

Ruiz–C & Román–Valencia

Introducción El género Astyanax comprende cerca de 180 especies, que se distribuyen desde el sur de los Estados Unidos de América hasta Argentina (Eigenmann, 1921; Schultz, 1944; Géry, 1977; Miquelarena, 1986; Lozano–Vilano & Contreras– Balderas, 1990; Taphorn, 1992; Schmitter–Soto, 1998; Eschmeyer, 2003). Representa uno de los grupos más abundantes y diversos de esta extensa región (Valdéz–Moreno & Contreras– Balderas, 2003).

La mayoría de los estudios sobre las especies de Astyanax han tratado aspectos ecológicos (Blanco & Cala, 1974; Nomura, 1975a; 1975b; López, 1978; Gutiérrez et al., 1983; Hoenicke, 1983; Huppop, 1986; Barlá et al., 1988; Arcifa et al., 1991; Huppop & Wilkens, 1991; Barbieri et al., 1996; Mora et al., 1997; Luiz et al., 1998; Castro & Vari, 2004; Román–Valencia & Ruiz, 2005).

Son escasos los trabajos sobre aspectos morfológicos, y principalmente sobre osteología.

Entre algunos que citan caracteres osteológicos de las especies de Astyanax, podemos destacar Miquelarena & Arámburu (1983), Miquelarena (1986), Lozano–Vilano & Contreras–Balderas (1990), Valdéz–Moreno & Contreras–Balderas (2003), Malabarba & Weitzman (2003) y Garutti (2003).

Weitzman (1962) analiza la osteología generalizada de la familia Characidae, y cita esqueletos utilizados de Astyanax fasciatus, y A. mexicanus. Otros se refieren a descripciones de nuevas especies y análisis taxonómicos, basados principalmente en morfometría y merísticas (Géry, 1977; Schmitter– Soto, 1998; Zarske & Géry, 1999; Bertaco & Malabarba, 2001).

El género Astyanax es un grupo bastante complejo, que para su reconocimiento requiere de mayor información morfológica, taxonómica y filogenética (Lagler et al., 1990). Respecto al género Carlastyanax, propuesto por Géry (1972), se basa en material tipo de Astyanax aurocaudatus perteneciente a una población natural de carácidos de alta montaña neotropical descrita por Eigenmann (1913).

Los caracteres diagnósticos descritos para Carlastyanax (Géry, 1972, 1977) son externos, expuestos directamente a la variabilidad ambiental, como sucede con la forma curva del tercer diente del dentario, principal carácter diagnóstico de su Carlastyanax, y presente en otras especies de Astyanax (Bertaco & Malabarba, 2001). Por lo tanto, una forma de obtener descripciones detalladas de caracteres diagnósticos en los peces es el análisis y descripción osteológicos, que permiten establecer una clasificación taxonómica apropiada (Weitzman & Fink, 1985; Vari & Harold, 2001).

El objetivo de éste trabajo es describir la osteología de Astyanax aurocaudatus del Río Roble, Alto Cauca, Colombia, y analizar la validez de Carlastyanax basándonos en caracteres osteológicos, merísticos y morfométricos.

pmx n mst f spo

clts

ffp

p

pt

soc eoc 1 mm Fig. 1. Neurocráneo de Astyanax aurocaudatus, vista dorsal: clts. Canal laterosensorial; eoc.

Exoccipital; f. Frontal; ffp. Fontanela frontoparietal; mst. Etmoides; n. Nasal; p. Parietal; pmx. Premaxilar; pt. Pterótico; soc. Supraoccipital; spo. Supraorbital.

Fig. 1. Skull of Astyanax aurocaudatus, dorsal view: clts. Laterosensory canal system; eoc.

Exoccipital; f. Frontal; ffp. Cranial fontanel; mst. Ethmoide ; n. Nasal; p. Parietal; pmx.

Premaxillary; pt. Pterotic; soc. Supraoccipital; spo. Supraorbital.

Material y métodos La toma de datos morfométricos y merísticos se realizó en 40 ejemplares preservados en alcohol al 70%; se utilizó un calibrador digital de precisión 0.01 mm. Los recuentos de radios, escamas y dientes se realizaron sobre el lado izquierdo del ejemplar, utilizando un estereoscopio y una aguja de disección.

Se realizaron modelos sobre las estructuras óseas de cuatro ejemplares de Astyanax aurocaudatus, diafanizados y teñidos con la técnica descrita en Taylor & Van Dyke (1985), Song & Parenti (1995). El material se depositó en el Laboratorio de Ictiología de la Universidad del Quindío, Armenia, Colombia (IUQ) y en el Laboratório de Ictiologia e Colecão de Peixes, Departamento de Zoologia e Botânica, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista–UNESP, Brasil (DZSJRP). Se examinaron radiografías de material

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Animal Biodiversity and Conservation 29.1 (2006)

ef ep eoc mst bo pv

re

oe

pte pe pr ifb

1 mm

Fig. 2. Cráneo de Astyanax aurocaudatus: bo. Basioccipital; ef. Esfenótico; ep. Epioccipital; eoc.

Exoccipital; ifb. Infrafaringobranquial; mst. Etmoides; oe. Orbitoesfenoides; pe. Paraesfenoides; pr.

Proótico; pv. Prevómer; pte. Pteroesfenoides; re. Rinoesfenoides.

Fig. 2. Skull of Astyanax aurocaudatus: bo. Basioccipital; ef. Sphenotic; ep. Epiotic; eoc. Exoccipital; ifb.

Suspensory pharyngeals; mst. Mesethmoid; oe. Orbitosphenoid; pe. Parasphenoid; pr. Prootic; pv.

Prevomer; pte. Pterosphenoid; re. Rhinosphenoid.

tipo de las siguientes especies de Astyanax: A. asuncionensis, A. paranae, A. integer, A. intermedius, A. pellegrini, A. scintillans, A. simulatus, y A. superbus, disponibles en Eschmeyer (2003). Los modelos se realizaron a escala y con ayuda de un estereoscopio. A partir de estos esquemas y observaciones directas sobre el material diafanizado, se realizaron las descripciones y los correspondientes análisis de cada una de las estructuras óseas. La nomenclatura de huesos y cartílagos se basó en Weitzman (1962) y Vari (1995).

Resultados Descripción osteológica Esqueleto axial Neurocráneo (figs. 1, 2) Etmoides: hueso anterior del cráneo, articulado a los extremos anterolaterales del frontal, separado medialmente del frontal por el extremo anterodorsal del rinoesfenoides. La parte basal se inserta en la depresión anteroventral del vómer; a este nivel se extienden dos procesos laterales que articulan el proceso ascendente de los premaxilares. El extremo anterior se extiende ventralmente en medio de los premaxilares.

Frontal: estructura laminar y convexa, que cubre la parte anterodorsal del neurocráneo, y cuya longitud no sobrepasa posteriormente la longitud del supraorbital. La parte anterior se extiende medialmente sobre el etmoides. La superficie posterior está separada medialmente por la fontanela frontoparietal, y el margen posterior se extiende

paralelamente al margen anterior del parietal. No existe un proceso lateroposterior que lo una al proceso del esfenótico. Sobre la superficie dorsal se extiende el canal laterosensorial, que se continúa por el canal supraorbital, parietal y pterótico.

Fontanela frontoparietal: foramen alargado que se extiende desde una corta distancia por delante de la barra epifiseal hasta el borde anterior de la espina supraoccipital.

Parietal: hueso laminar y corto, que cubre la superficie dorsal posterior del neurocráneo, con respecto al frontal; separado medialmente por la fontanela frontoparietal; el extremo lateral posterior se articula al margen superior del pterótico, y el margen posterior se une al supraoccipital. Sobre la superficie ventral se extiende la ramificación parietal del canal laterosensorial.

Supraoccipital: hueso tubular y delgado, cuyo margen anterior se bifurca lateralmente y se une paralelamente al margen posterior del parietal hasta el extremo dorsal posterior del pterótico. El margen posterior se extiende formando una espina alargada horizontalmente y dorsalmente cóncava.

La superficie ventral se une al exoccipital.

Supraorbital: hueso largo, angosto, unido lateralmente al frontal, cuyos extremos anterior y posterior semicóncavos dan lugar al canal supraorbital, superficie dorsal más plana. La superficie anteroventral del supraorbital se articula a la parte dorsal del lateroetmoides, mediante una banda de cartílago que se extiende entre la unión del frontal y el orbitoesfenoides.

Nasal: hueso alargado en forma de porta–canal o tubo, que se continúa con el canal laterosensorial.

El extremo posterior recibe desde el frontal la prolongación del canal supraobital.

52

Antorbital: hueso dorsalmente cóncavo, anterior al lateroetmoides, que ocupa el borde lateral de la fosa nasal, posterior al maxilar; presenta un ensanchamiento en la parte lateromedial.

Etmoides lateral: hueso anterior de la cavidad orbital, posterior al antorbital. El extremo dorsal está unido a la superficie inferoanterior del supraorbital. La superficie posteromedial se ensancha profundamente de forma cóncava. El borde lateral interno se extiende formando un proceso hacia el prevómer; el extremo basal no hace contacto con otras estructuras.

Pterótico: hueso ubicado en la región lateroposterior del neurocráneo. Margen anterodorsal del pterótico unido al frontal, no al supraorbital; la parte anteroventral está unida al esfenótico por una banda de cartílago, mientras que la parte más ventral va unida al proótico y al epioccipital. El extremo posterior presenta tres procesos con canal laterosensorial que se conectan al extraescapular. El margen posterosuperior es plano, unido paralelamente al margen lateral del parietal. El extremo inferior se une al canal esfenótico y al canal epioccipital.

Palatino: hueso rectangular, corto, más ancho que alto, posterior al prevómer; el extremo anterolateral posee una porción de cartílago que se articula con el margen superior del maxilar. El extremo posterior se une al mesopterigoides y el ectopterigoides.

Prevómer: hueso medial de la región anterior y ventral del neurocráneo, cuyo margen posterior se une paralelamente al proceso lateral del etmoides, y cuyo extremo lateral posee una porción de cartílago. La parte posterior del prevómer bordea de forma transversal parte de la región anterior del rinoesfenoides. El extremo dorsal posterior se extiende lateralmente hasta el cartílago inferoanterior del supraorbital, paralelo al lateroetmoides.

Rinoesfenoides: hueso en estado cartilaginoso, cuyo extremo anterior se extiende a través de la parte basal del prevómer hasta alcanzar la superficie de unión entre el frontal y el etmoides. El margen ventral se extiende lateralmente hasta articularse con el cartílago que separa el mesopterigoides del ectopterigoides. El extremo dorsoposterior se une al borde anteroventral del orbitoesfenoides. El extremo posteroventral se extiende sobre la superficie dorsal del paraesfenoides.

Paraesfenoides: hueso horizontalmente alargado ubicado en el eje medio ventral de la cavidad orbital, cuyo extremo anterior se extiende desde la parte anteroventral del rinoesfenoides. El extremo posterior se bifurca y atraviesa la parte ventral del proótico, hasta la parte ventral del basioccipital.

Orbitoesfenoides: hueso laminar, se extiende sobre el eje medio de la cavidad orbital. La parte posteromedial se bifurca de forma arqueada hasta alcanzar los bordes laterales del frontal. El extremo ventral no se une al frontal, pero sí al margen dorsoposterior del rinoesfenoides. La extensión de este hueso desde el eje medio de la cavidad orbital, hasta los bordes laterales del frontal, origina una cavidad o bóveda craneana que se extiende a

Ruiz–C & Román–Valencia

través del orbitoesfenoides, pteroesfenoides y la parte superior del proótico. El extremo ventral se extiende horizontalmente de forma laminar, con un foramen en la superficie posteroventral.

Pteroesfenoides: hueso laminar, separado medialmente por la cavidad que aloja el cerebro, la cual se extiende desde el proótico hasta el prevómer. El pteroesfenoides es posterior al orbitoesfenoides; en los bordes laterales hay bandas de cartílago, que articulan la unión con el orbitoesfenoides y esfenótico.

En el margen ventral hay una apófisis en forma de espina poco desarrollada.

Esfenótico: hueso pequeño, superior al proótico.

Margen anterior unido a la parte posterior del pteroesfenoides hasta alcanzar el extremo posterior del supraorbital, dando origen a la espina esfenótica.

La parte superior posee una rama del canal laterosensorial. Margen posterior unido al canal del pterótico por una banda de cartílago. Parte ventral unida al proceso lateral del proótico, donde se une el borde dorsal del hiomandibular.

Proótico: hueso posterior de la cavidad orbital, cuya superficie basal está unida al borde dorsoposterior del paraesfenoides, formando parte del foramen auditivo, donde se proyecta horizontalmente una lamina ósea que se extiende hasta su margen posterior. El proótico está rodeado por una banda de cartílago que lo une al pterótico, epioccipital, exoccipital y basioccipital; dicha banda de cartílago se ensancha entre el proótico y el paraesfenoides.

Epioccipital: hueso tubular, posteroventral al pterótico. La parte ventral está unida a la superficie dorsal del exoccipital, la parte dorsal se extiende en forma tubular hasta unirse con el borde posteroventral del pterótico. Por detrás de esta unión se extiende dorsal e internamente formando la primera cavidad de la fosa postemporal.

Exoccipital: se encuentra en la parte posterior del cráneo; la superficie dorsal del disco basal es convexa, y está unida ventralmente al basioccipital por una banda de cartílago que se extiende hacia la unión del proótico y el paraesfenoides. El extremo dorsal posterior se separa del epioccipital, formando el arco exoccipital, que se extiende hacia la parte ventral del supraoccipital, formado la segunda cavidad de la fosa postemporal.

Basioccipital: hueso corto, ventralmente convexo, con margen anterodorsal cubierto por una banda de cartílago que se extiende desde la unión del proótico y el paraesfenoides, y en donde se articulan dorsalmente el exoccipital, anteriormente el proótico, e inferiormente al paraesfenoides.

Serie infraorbital (fig. 3) Astyanax aurocaudatus presenta cuatro infraorbitales modificados, estructuras óseas laminares, todos con sistema laterosensorial.

Primer y segundo infraorbitales: de forma triangular, lateralmente convexos, se sitúan por detrás del maxilar. Margen dorsal plano; el extremo anterior no tiene procesos que se extiendan en medio del lateroetmoides y el maxilar; la parte ventral termina en punta y cubre la parte superior del

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Animal Biodiversity and Conservation 29.1 (2006)

fe cso 1 mm

let

pt

ant ino 3

fi

ino 4 Fig. 4. Premaxilar de Astyanax aurocaudatus, vista ventral: fe. Fila externa; fi. Fila interna.

Fig. 4. Premaxillary of Astyanax aurocaudatus, ventral view: fe. Outer row of teeth; fi. Inner row of teeth.

mx 1 mm d

ino 2

Fig. 3. Neurocráneo de Astyanax aurocaudatus, vista lateral: ant. Antorbital; cso. Canal supraorbital; d. Dentario; ino. Infraorbital; let.

Lateroetmoides; mx. Maxilar; pt. Pterótico.

Fig. 3. Skull of Astyanax aurocaudatus, lateral view: ant. Antorbital; cso. Supraorbital canal; d. Dentary; ino. Infraorbital; let. Lateral ethmoid; mx. Maxillary; pt. Pterotic.

dentario y del ángulo articular. Su forma y tamaño indican la fusión del primer y segundo infraorbitales.

Tercer infraorbital: el más ancho de la serie infraorbital, bordeado posteriormente por la apófisis del hiomandibular. Sobre el margen de los individuos de mayor longitud estándar se reconoce una fisura que aumenta de amplitud con relación a la madurez de los ejemplares.

Cuarto y quinto infraorbitales: corto y ancho, el canal laterosensorial se extiende formando el margen anterior. Cubre la porción superior lateral del proótico. Su forma indica la fusión del cuarto y quinto infraorbitales.

Sexto infraorbital: hueso reducido, se extiende dorsalmente hacia el foramen del extremo lateral posterior de la superficie del frontal, dando continuidad al canal laterosensorial.

Branquicráneo Mandíbulas (figs. 3–5) Premaxilar: unido al neurocráneo por los procesos laterales del etmoides. El proceso lateral es corto y curvo, y presenta dos hileras de dientes sobre la superficie inferior. Hilera externa con cinco dientes, todos tricúspides, de los cuales el segundo y el cuarto se inclinan internamente y el tercero está en el borde, con una cúspide central más ancha que los demás dientes. La hilera interna presenta cuatro dientes tricúspides, los laterales de menor tamaño.

Maxilar: hueso alargado con un proceso anterodorsal distinguible y articulado al proceso lateral del premaxilar. Presenta cuatro–seis dientes distribuidos sobre la parte superior del borde lateral del maxilar; este número varía con el tamaño del ejemplar. En la base de cada diente existen alvéolos que albergan dientes de muda. El extremo inferior se pliega sobre la superficie posterolateral del dentario con un extremo redondeado.

Dentario: sobre la superficie lateromedial se extiende horizontalmente el cartílago de Meckel.

En el extremo posteroventral del dentario se ubica el angular, hueso pequeño y rectangular separado del ángulo–articular por una banda de cartílago.

En el extremo dorsal posterior del dentario se localiza el ángulo–articular, hueso alargado que en su región posterior ventral presenta la faceta de articulación del cuadrado. Sobre el margen dorsal del dentario se distribuyen los dientes según su forma y tamaño: la parte anterior presenta tres dientes grandes, los dos primeros tricúspides, el tercero bicúspide con un margen posterior curvo; los siete dientes posteriores son cortos y rectos, y de éstos los tres anteriores son bicúspides y los cuatro posteriores unicúspides.

Suspensorio (fig. 6) Hiomandibular: hueso laminar, anterior al aparato opercular; presenta un borde anterior ligeramente cóncavo; el extremo dorsal se une a la superficie dorsal del proótico, cubriendo así el foramen auditivo. El margen anterior del proceso hiomandibular se une a través de una banda de cartílago al metapterigoides, y en su extremo distal posee una porción de cartílago que se une al interhial y simpléctico.

Cuadrado: hueso alargado, unido horizontalmente sobre la superficie medial del preopérculo.

Sobre el extremo anteroventral se articula el ángulo–articular; no se articula con el simpléctico ni al interhial. El extremo anterior se extiende internamente hasta la banda de cartílago que lo une al metapterigoides y mesopterigoides, pero no al ectopterigoides.

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hd aa

op mes

pa 1 mm

ang

met

ec

cm sp

Fig. 5. Dentario de Astyanax aurocaudatus: aa. Ángulo articular; ang. Angular; cm. Cartílago de Meckel.

Fig. 5. Dentary of Astyanax aurocaudatus: aa.

Anguloarticular; ang. Angular; cm. Meckel‘s cartilage.

Metapterigoides: hueso dorsalmente arqueado; existe una banda de cartílago sobre el margen anterior que lo une ventralmente al cuadrado y dorsalmente al mesopterigoides y ectopterigoides; sobre el margen posterior se extiende una banda de cartílago paralela al proceso del hiomandibular, el cual se extiende hasta el borde dorsal posterior del simpléctico.

Mesopterigoides: hueso alargado, unido posteriormente al metapterigoides. Sobre la superficie ventral se extiende una banda de cartílago que lo une lateralmente al ectopterigoides y posteriormente al cuadrado.

Ectopterigoides: hueso alargado, pegado dorsalmente a una banda de cartílago que lo une al mesopterigoides; la parte inferior se articula en el cuadrado, por delante en el palatino. No posee dientes.

Serie opercular (fig. 3) Opérculo: hueso lateral posterior al neurocráneo, laminar y convexo, unido por cartílago al borde dorsal posterior del preopérculo. La parte dorsal del opérculo cubre estructuras internas como el basioccipital, el exoccipital y parte del epioccipital; al extremo dorsal anterior se une una banda de cartílago. La parte ventral se extiende en forma de punta sobre el preopérculo.

Preopérculo: anterior al opérculo y posteroventral al segundo infraorbital; su parte dorsal se extiende verticalmente entre el hiomandibular y el opérculo; su parte ventral se prolonga de forma arqueada, y dorsoventralmente cóncava, y en ella se encuentran el simpléctico, el interhial y la apófisis del hiomandibular, unidos en sus extremos por cartílago.

Simpléctico: hueso alargado, ubicado perpendicularmente sobre la superficie ventral del preopérculo; los extremos anterior y posterior poseen porciones de cartílago que lo unen anteriormente a la superficie dorsal del cuadrado, y posteriormente a los pequeños cartílagos del interhial y

ih so

1 mm cu io

po

Fig. 6. Arco mandibular de Astyanax aurocaudatus: cu. Cuadrado; ec. Ectopterigoides; hd. Hiomandibular; ih. Interhial; io.

Interopérculo; mes. Mesopterigoides; met.

Metapterigoides; op. Opérculo; pa. Palatino; po. Preopérculo; sp. Simpléctico; so. Subopérculo.

Fig. 6. Mandibular arch of Astyanax aurocaudatus: cu. Quadrate; ec. Ectopterygoid; hd. Hyomandibular; ih. Interhyal; io.

Interopercle; mes. Mesopterygoid; met.

Metapterygoid ; op. Opercle; pa. Palatine; po.

Preopercle ; sp. Symplectic; so. Subopercle.

la apófisis del hiomandibular. Una banda de cartílago que bordea el margen posterior del metapterigoides se une a la superficie dorsoposterior del simpléctico.

Interhial: es corto, lateralmente recto y con una porción de cartílago en la parte superior; se sitúa verticalmente sobre el preopérculo. Las porciones de cartílago del simpléctico y el interhial se unen al extremo cartilaginoso de la apófisis del hiomandibular.

Aparato branquial (fig. 7) Basihial: hueso corto y delgado, unido lateralmente al hipohial ventral y al hipohial dorsal. Sobre su extremo superior existe una porción de cartílago dividida en dos. Extremo ventral separado del primer basibranquial por un espacio.

Hipohial ventral: hueso corto, de superficie dorsal ósea y parte ventral cartilaginosa. Lateralmente se une a través de una banda de cartílago al extremo dorsal del ceratohial y ventralmente al hipohial dorsal.

Hipohial dorsal: hueso cóncavo, unido a cada lado del basihial. Se une por medio de una banda de cartílago al extremo dorsal del ceratohial.

Ceratohial: hueso aplanado dorsolateralmente, de extremo dorsal bifurcado, unido al margen lateral del hipohial ventral y dorsal. Sobre la superficie dorsal se sujetan tres radios branquiostegales. So-

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Animal Biodiversity and Conservation 29.1 (2006)

bre el margen inferior se pliega una banda de cartílago que lo une al epihial.

Epihial: hueso laminar, dorsolateralmente aplanado, unido al ceratohial a través de una banda cartilaginosa. Se extiende desde el borde ventral donde se une al interhial, hueso corto unido al simpléctico por una porción de cartílago. La superficie dorsal sostiene un radio branquiostegal.

Branquiostegios: huesos planos y alargados, que se encuentran en número de cuatro a cada lado del basihial, tres sobre el margen dorsoanterior del ceratohial y uno sobre el margen dorsoanterior del epihial.

Basibranquiales: huesos ubicados verticalmente con respecto al eje central del cuerpo en número de cinco, dos de ellos accesorios, pues no sostienen lateralmente hipobranquiales.

Primer basibranquial: hueso delgado, de extremo dorsal libre, que se extiende hacia el basihial; parte lateroventral unida al primer par hipobranquial.

Segundo basibranquial: hueso tubular, con un foramen sobre el eje medio. La parte dorsal se ensancha en forma arqueada; el borde dorsal está cubierto por una banda de cartílago y no articula hipobranquiales, por lo cual se identifica como un basibranquial accesorio.

Tercer basibranquial: hueso delgado y cartilaginoso. A él se une lateralmente el segundo par hipobranquial.

Cuarto basibranquial: hueso corto y delgado que no articula hipobranquiales, por lo que se asume como el segundo basibranquial accesorio. Su extremo ventral se une a la superficie dorsal del quinto basibranquial.

Quinto basibranquial: hueso ancho y largo, en relación con los demás basibranquiales, en estado cartilaginoso. La parte dorsal se extiende lateralmente y sostiene a cada lado un hipobranquial. La parte media es angosta. La parte ventral se ensancha para articular directamente el cuarto par ceratobranquial.

El extremo ventral se extiende en medio de los extremos dorsales de la placa faríngea ventral.

Hipobranquiales: huesos unidos a cada lado de los basibranquiales. Primer y segundo par de hipobranquiales de forma rectangular, mientras los márgenes dorsal y ventral están bordeados por bandas de cartílago. Tercer par hipobranquial unido al borde dorsolateral del quinto basibranquial; el margen dorsal se extiende perpendicularmente por debajo del segundo par hipobranquial.

Ceratobranquial: hueso alargado, estructurado en cuatro pares a cada lado de los hipobranquiales.

El cuarto par se pliega directamente hacia el basibranquial en ausencia del respectivo par hipobranquial. El primer par carece de cartílago en su extremo dorsal, mientras los tres últimos lo poseen. El hueso ceratobranquial posee una estructura en canal, donde se anclan los filamentos branquiales cartilaginosos, distribuidos a través de los ceratobranquiales hasta los epibranquiales. Los márgenes dorsal y ventral de los ceratobranquiales poseen de cuatro a seis branquispinas cortas muy semejantes a la dentición faríngea.

hpv

bh hpd

cth eph

ith bsb

hpb

ifb epb ctb pfs pfi 1 mm

Fig. 7. Aparato branquial de Astyanax aurocaudatus: bh. Basihial; bsb. Basibranquial; ctb. Ceratobranquial; cth. Ceratohial; epb.

Epibranquial; eph. Epihial; hpb. Hipobranquial; hpd. Hipohial dorsal; hpv. Hipohial ventral; ifb.

Infrafaringobranquial; ith. Interhial; pfi. Placa faríngea inferior; pfs. Placa faríngea superior.

Fig. 7. Hyobranchial apparatus of Astyanax aurocaudatus: bh. Basihyal; bsb. Basibranchial; ctb. Ceratobranchial; cth. Ceratohyal; epb.

Epibranchial; eph. Epihyal; hpb. Hypobranchial; hpd. Dorsal hypohyal; hpv. Ventral hypohyal; ifb. Suspensory pharyngeals; ith. Interhyal; pfi.

Lower pharyngeal; pfs. Upper pharyngeals.

Epibranquiales: huesos alargados y cortos, unidos al ceratobranquial por porciones de cartílago.

Los tres primeros poseen dentículos y se articulan a los suspensorios infrafaringobranquiales. Los dos últimos epibranquiales presentan extremos bifurcados que se aproximan y unen a la placa faríngea superior.

Placa faríngea superior: hueso cartilaginoso y alargado, suspendido al nivel de los infrafaringobranquiales. Su superficie ventral posee una placa de dentición faríngea que se divide en dos para continuar sobre la superficie ventral del cuarto epibranquial.

Placa faríngea inferior: hueso alargado y curvo.

Posee porciones de cartílago en los extremos dorsal y ventral. La superficie dorsal está cubierta de dentición faríngea, consistente en pequeños y numerosos dientes cónicos. La superficie ventral no presenta dentición faríngea y se curva lateroventralmente.

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cmn ae 3 ver ae 4 ver

spn an

1 spn

en

cn

cl es

pzn

ae 5 ver

fph

ct 1 ct 2 int tr cp 1 mm

sus ct 4

epp ph cp

1 mm

Fig. 8. Aparato de Weber de Astyanax aurocaudatus: ae. Arco y espina; cl. Claustrum; cmn. Complejo neural; ct. Centra; cp. Costilla pleural; es. Scaphium; int. Intercalarium; spn.

Supraneural; sus. Suspensorio; tr. Tripus; ver.

Vértebra.

Fig. 9. Vértebras precaudales de Astyanax aurocaudatus: an. Arco neural; cn. Canal neural; cp. Costilla pleural; en. Espina neural; epp. Epineural; fph. Fosa paraapófisis; ph.

Paraapófisis; pzn. Postzigoapófisis neural; spn.

Supraneural.

Fig. 8. Weberian apparatus of Astyanax aurocaudatus: ae. Arch and spine; cl. Claustrum; cmn. Neural complex; ct. Centrum; cp. Pleural rib; es. Scaphium; int. Intercalarium; spn.

Supraneural; sus. Suspensorium; tr. Tripus; ver.

Vertebra.

Fig. 9. Precaudal vertebrae of Astyanax aurocaudatus: an. Neural arch; cn. Neural canal; cp. Pleural rib; en. Neural spine; epp.

Epineural; fph. Fossa for parapophysis; ph.

Parapophysis; pzn. Neural postzigapophysis; spn. Supraneural.

Aparato de Weber (fig. 8) Formado por la fusión de las cuatro primeras vértebras.

Complejo neural: hueso anterior del aparato de Weber, unido en forma de cresta laminar al margen posterior del supraoccipital y el exoccipital. Desde la superficie mediolateral se extiende un proceso hacia el claustrum. La parte posterior se une sobre el margen dorsal anterior de la cuarta vértebra; en el extremo posterior de esta unión existe una pequeña banda de cartílago.

Claustrum: hueso corto y rectangular, cuyo margen dorsal se continúa con el proceso lateral del complejo neural. Se encuentra en medio del exoccipital y la tercera vértebra. El margen ventral del claustrum se continúa con el margen dorsal del scaphium.

Scaphium: hueso corto y ondulado, cuyo margen ventral se une a las centra vertebrales uno y dos.

Intercalarium: hueso alargado, que se extiende desde el origen del proceso lateral del segundo centro, diagonalmente hasta el origen del proceso lateral de la tercera vértebra.

Arco neural y espina de la tercera vértebra: arco neural aplanado, corto y ancho, que se extiende de forma arqueada sobre el margen anterolateral de la cuarta vértebra. Desde el extremo posterior se extiende un proceso o espina de forma arqueada hacia el margen posterior de la scaphium.

Arco neural y espina de la cuarta vértebra: superficie del arco neural liso. Unido anteriormente a la parte dorsal de la tercera vértebra, el dorso se une al margen ventral del complejo neural. Sobre la superficie lateral se fusionan los extremos dorsales del tripus y la costilla pleural.

Vértebras precaudales (fig. 9) Posee de 15 a 16 vértebras precaudales e incluyen a las cuatro primeras fusionadas que conforman el aparato de Weber. Las vértebras 5 a 14 se extienden de forma arqueada hasta las vértebras caudales, dando forma al lomo pronunciado característico de Astyanax aurocaudatus. Sobre la superficie lateral del arco vertebral existen cavidades que alojan la parapófisis, estructura pequeña y laminar encargada de sostener el extremo dorsal de las costillas pleurales. Desde la parte anterodorsal del arco vertebral se extiende la prezigapófisis, estructura laminar y corta, se fusiona al arco neural o canal neural, Sobre el arco neural se extiende la espina neural, que se extiende transversalmente, aún en estado de madurez, cuando el extremo distal alcanza los extremos ventrales de los supraneurales y los pterigióforos de la aleta dorsal; el extremo distal de la espina neural presenta así más de una curva. Sobre el extremo dorsal posterior del arco vertebral se extiende verticalmente y de forma

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Animal Biodiversity and Conservation 29.1 (2006)

epr pne

urn urn

en hpl urs db eh

1 mm

rp

Fig. 10. Esqueleto caudal de Astyanax aurocaudatus: db. Centra; eh. Espinas hemales; en. Espina neural; epr. Epurales; hpl. Hipurales; pne. Proceso neural especializado; rp. Radios procurrentes; urn. Uroneurales; urs. Urostilo.

Fig. 10. Caudal skeleton caudal of Astyanax aurocaudatus: db. Centrum; eh. Haemal spines; en. Neural spine; epr. Epurals; hpl.

Hypurals; pne. Specialized neural process; rp.

Procurrent rays; urn. Uroneurals; urs. Urostyle.

bifurcada la postzigapófisis neural, que en la quinta vértebra es menos desarrollado que en las demás vértebras precaudales. En Astyanax aurocaudatus no existe postzigapófisis hemal. Las costillas pleurales son estructuras alargadas que se extienden transversalmente sobre la superficie lateral de la cavidad celómica; las vértebras 15 y 16 son cortas, con procesos transversales fusionados en la parte posterior de la cavidad celómica, y se continúan con las vértebras caudales. En los machos se observaron de dos a cuatro primeras costillas pleurales con ondulaciones bien definidas.

Supraneurales: posee cinco supraneurales, estructuras delgadas inclinadas perpendicularmente en el sentido de las costillas pleurales. Delgados y curvos, su longitud aumenta hacia el extremo posterior del lomo. A lo largo de la superficie medial se extiende un canal acercándose al primer pterigióforo proximal de la aleta dorsal.

Huesos intermusculares (fig. 9) Epineurales: estructuras delgadas, cortas, similares entre sí, en número de 30 a 31, distribuidas transversalmente sobre la parte superolateral de las costillas pleurales hasta las espinas neurales de las vértebras caudales.

Epipleurales 21 a 22 estructuras similares a los epineurales, pero distribuidos lateralmente respecto a las espinas hemales.

Vértebras caudales (fig. 10) El número de vértebras caudales varía de 19 a 21, y son muy similares entre sí. Sin embargo, las dos últimas se modifican al unir las dos últimas espinas hemales a una banda de cartílago, donde se articulan los radios procurrentes y caudales.

Astyanax aurocaudatus no posee procesos neurales especializados sobre las vértebras caudales, como sucede en otros carácidos. Las vértebras caudales no poseen costillas pleurales pero sí espinas hemales. Estas últimas se unen al cartílago que se extiende sobre el borde distal de los hipurales.

Esqueleto apendicular Cintura y aleta pectorales (figs. 11–12) Extraescapular: estructura delgada con canal laterosensorial, posterior al pterótico; la parte superior es delgada, verticalmente alargada como una espina que atraviesa inferiormente los dos procesos inferiores del pterótico uniéndose con su canal sensorial. La parte inferior se une al extremo superior del postemporal; se articula el neurocráneo con la cintura pectoral.

Postemporal: verticalmente alargado, de superficie plana y lateralmente ondulado. El extremo anterior separado del canal laterosensorial del extraescapular, el extremo inferior se pliega de forma dentada hacia el extremo superior del cleitrum.

Cleitrum: hueso largo, arqueado por delante, posterior al subopérculo. Sobre el margen anterior se pliega paralelamente el supracleitrum, y sobre la superficie ventral se pliega la escápula.

Supracleitrum: hueso alargado, unido al margen dorsal del cleitrum, separado del postemporal. Sobre la superficie ventral se une el extremo dorsal de mesocaracoides. El extremo lateral es puntiagudo y se extiende sobre el margen dorsal del coracoides.

Postcleitrum uno–dos–tres: huesos laminares, situados verticalmente sobre el margen posterior de la cintura pectoral. El postcleitrum uno es corto, delgado y está separado del postcleitrum dos, el cual es más ancho y largo que el primero; su extremo ventral está unido al postcleitrum tres, elemento delgado y alargado que se extiende dorsalmente sobre los radios pectorales.

Escápula: hueso laminar, plegado sobre la superficie ventral del cleitrum, que se extiende de forma angular hasta el margen anterior del coracoides, articulando los radios proximales, que a su vez sostienen los radios pectorales (i, 11–12), en ausencia de foramen.

Mesocaracoides: hueso delgado, se extiende desde la superficie ventral del supracleitrum hasta la superficie dorsal del coracoides.

Coracoides: hueso laminar de superficie lisa, separado del cleitrum por la escápula; borde dorsal unido al margen ventral del supracleitrum.

Aleta dorsal (fig. 13) Posee 8–10 radios, los dos primeros son simples, sostenidos por pterigióforos; el pterigióforo proximal y

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Ruiz–C & Román–Valencia

ex

pst pst

1 mm

pc 1 pc 1

ctm esp

sc mc ctm

pc 2

sc

pc 3

esp pc 2

cr

1 mm

rpx pc 3

Fig. 11. Cintura y aleta pectoral izquierda de Astyanax aurocaudatus, vista lateral: cr.

Coracoides; ctm. Cleitrum; esp. Escápula; ex.

Extraescapular; pc. Postcleitrum; pst.

Postemporal; sc. Supracleitrum.

Fig. 11. Left pectoral girdle and fin of Astyanax aurocaudatus, lateral view: cr. Coracoid; ctm.

Cleithrum; esp. Scapula; ex. Extrascapular; pc. Postcleithrum; pst. Posttemporal;sc.

Supracleithrum.

el pterigióforo medial están fusionados. El pterigióforo distal es una estructura pequeña que articula la unión entre el extremo inferior del radio con el pterigióforo proximal. El pterigióforo proximal aumenta de longitud hacia el extremo anterior, y se dobla al unirse con las espinas neurales de las vértebras precaudales.

Aleta pélvica (fig. 14) Hueso corto, anterior a la aleta anal, conformado por el hueso pélvico. Alargado y cóncavo, el margen lateral se dobla de forma convexa, desembocando en el extremo anterior. El proceso isquial es curvo, se extiende por detrás de los radiales sobre el borde anterior de los radios pélvicos, bifurcándose su extremo distal. El hueso pélvico sostiene 5–6 radios pélvicos, siendo simple el primero.

Aleta anal (fig. 15) Posee de 26 a 28 radios, siendo los cuatro primeros simples. Los pterigióforos distal, medial y proximal, posteriores a partir del octavo radio, diferenciados y cartilaginosos, se modifican al aproximarse al extremo anterior. Así se fusionan el pterigióforo medial y proximal en una sola estructura y el cartílago se reduce a unas pequeñas trazas o banda periférica.

No se observaron espinas en los radios de las aletas anal y pélvica.

cr

Fig. 12. Cintura y aleta pectoral izquierda de Astyanax aurocaudatus, vista interna: cr.

Coracoides; ctm. Cleitrum; esp. Escápula; mc. Mesocaracoides; pc. Postcleitrum; pst.

Postemporal; sc. Supracleitrum; rpx. Radios proximales.

Fig. 12. Left pectoral girdle and fin of Astyanax aurocaudatus, medial view: cr. Coracoid; ctm.

Cleithrum; esp. Scapula; mc. Mesocaracoid; pc. Postcleithrum; pst. Posttemporal; sc.

Supracleithrum; rpx. Proximal rays.

Aleta caudal (fig. 10) Sostenida por el complejo hipural, conformado por el urostilo. Sobre el borde dorsal se extiende el proceso neural especializado, cuyo borde dorsal se extiende en dos procesos, que bordean la inserción de dos epurales. Los radios procurrentes son huesos alargados que bordean los lados dorsal y ventral de los lóbulos caudales.

Posee siete hipurales: primer hipural alargado, ubicado transversalmente sobre el extremo anterior de los hipurales dos, tres y cuatro. El lado externo del primer hipural se continúa con uno de los radios procurrentes del lóbulo superior.

En general la forma de los hipurales es alargada y rectangular, aunque los hipurales cinco y siete tienen forma de abanico: estrecha en el extremo anterior y ancha en el posterior. Sobre el margen posterior de los hipurales dos a siete se extiende una banda de cartílago hasta el extremo distal de la espina hemal del urostilo y las dos últimas de las vértebras caudales. Sobre el extremo dorsal posterior del segundo hipural, y paralelo a los radios procurrentes, se extiende el uroneural, estructura cartilaginosa que separa los radios procurrentes de los radios caudales principales.

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Animal Biodiversity and Conservation 29.1 (2006)

rd

hp

pi er

ptd 1 mm ptp

1 mm

Fig. 14. Cintura y aleta pélvica de Astyanax aurocaudatus: er. Elemento radial; hp. Hueso pélvico; pi. Proceso isquial.

Fig. 14. Pelvic girdle and fin of Astyanax aurocaudatus: er. Radial element; hp. Pelvic bone; pi. Isquial process.

Fig. 13. Aleta dorsal de Astyanax aurocaudatus: ptd. Pterigióforo distal; ptp.

Pterigióforo proximal; rd. Radios distales.

Fig. 13. Dorsal fin of Astyanax aurocaudatus: ptd. Distal pterygiophore; ptp. Proximal pterygiophore; rd. Distal rays.

Morfometría y merística (tabla 1) En la tabla 1 se presentan los datos morfométricos y merísticos. Los que presentan mayor variación son: la altura del cuerpo es mayor en Astyanax aurocaudatu,s con un promedio de 38,47% (30,5–51,92%), mientras especies sintópicas como H. boquiae registran un 27,71% (25,02–31,12%) y B. caucanus 25,20% (21,69– 27,78%). La longitud hocico–aleta anal es mucho menor en Astyanax aurocaudatus 58,62% (39,93– 63,48%) al compararla con A. cremnobates 69,6% (66,6–74,0%). La longitud aleta dorsal–anal es mayor en A. aurocaudatus 38,21% (30,0–52,93%) al confrontarla con especies sintópicas como Hemibrycon boquiae 20,88% (19,90–21,68%).

Longitud de la aleta dorsal–pectoral en A. aurocaudatus 41,04% (24.48–67,5%) mayor que el registrado en H. boquiae 17,94% (17,57– 18,22%). Longitud de la aleta pectoral menor en A. aurocaudatus (26,64–30,75%). Posee cuatro radios simples en la aleta anal, mientras que H. boquiae y B. caucanus registra sólo tres radios simples. Se observa, además, un rango mayor en el número de escamas entre la línea lateral y las aletas: dorsal (6–10 vs. 4–6 en B. caucanus), anal (6–10 vs. 4–5 en H. boquiae y B. caucanus).

La longitud del pedúnculo caudal de A. aurocaudatus es menor, 14,02% (10,73–17,66%), que la correspondiente a H. boquiae, 38,38% (36,19–41,63%). La altura del pedúnculo caudal en A. aurocaudatus, 12,18% (9,09–14,28%), es menor que lo anotado para H. boquiae, 28,41% (tabla 1).

Discusión En la descripción del género Carlastyanax (Géry, 1972) existen inconsistencias en los datos. Además, se fundamenta en observaciones incorrectas, tal como se anota más abajo, y no existen informes previos sobre su osteología. Por lo tanto, basándonos en el conocimiento actual no hay razones para aceptar el género monotípico Carlastyanax, planteado por Géry (1972), sobre la especie tipo Astyanax aurocaudatus. Se mantiene la clasificación inicial de Astyanax aurocaudatus (Román–Valencia & Ruiz, 2005) dada por Eigenmann (1913).

eh

ptp ptm ptd

ra 1 mm

Fig. 15. Aleta anal de Astyanax aurocaudatus: Eh. Espina hemal; ptd. Pterigióforo distal; ptm. Pterigióforo medial; ptp. Pterigióforo proximal; ra. Radios anales.

Fig. 15. Anal fin of Astyanax aurocaudatus: Eh. Haemal spines; ptd. Distal pterygiophore; ptm. Medial pterygiophore; ptp. Proximal medial; ra. Anal fin rays.

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Ruiz–C & Román–Valencia

Tabla 1. Datos morfométricos y merísticos de Astyanax aurocaudatus, A. cremnobates (datos de Bertaco et al., 2001), H. boquiae y B. caucanus: Ls. Longitud estándar; Lt. Longitud total; Pc. Profundidad del cuerpo; L(h–ad). Longitud hocico–aleta dorsal; L(h–apc). Longitud hocico– aletas pectorales; L(h–apv). Longitud hocico–aletas pélvicas; L(h–aa). Longitud hocico–aleta anal; L(ad–h). Longitud aleta dorsal–hipurales; L(ad–aa). Longitud aleta dorsal–aleta anal; L(ad–apc). Longitud aleta dorsal–aletas pectorales; Lad. Longitud aleta dorsal; Lapc. Longitud aletas pectorales; Lapv. Longitud aletas pélvicas; Laa. Longitud aleta anal; Ppc. Profundidad del pedúnculo caudal; Lpc. Longitud del pedúnculo caudal; Lc. Longitud de la cabeza; Lh. Longitud del hocico; Do. Diámetro del ojo; Lpoc. Longitud post–orbital de la cabeza; Lhm. Longitud del hueso maxilar; Ai. Ancho interorbital; Lms. Longitud de la mandíbula superior; Ell. Número de escamas en la línea lateral; E(ll–ad). Escamas línea lateral y la aleta dorsal; E(ll–aa). Escamas lína lateral y la aleta anal; E(ll–apv). Escamas línea lateral y las aletas pélvicas; Epd. Escamas predorsales; Rad. Radios en la aleta dorsal; Raa. Radios en la aleta anal; Rapv. Radios en las aletas pélvicas; Rapc. Radios en las aletas pectorales.

Table 1. Morphometric and meristic data of Astyanax aurocaudatus, A. cremnobates (data from Bertaco et al., 2001), H. boquiae and B. caucanus: Ls. Standard length; Lt. Total length; Pc. Body length; L(h–ad). Snout–dorsal fin distance; L(h–apc). Snout–pectoral fin distance; L(h– apv). Snout–pelvic fin distance; L(h–aa). Snout–anal fin distance; L(ad–h). Dorsal fin–hypurals distance; L(ad–aa). Dorsal–anal fins distance; L(ad–apc). Dorsal–pectoral fins distance; Lad. Dorsal–fin length; Lapc. Pectoral–fin length; Lapv. Pelvic fin length; Laa. Anal–fin length; Ppc. Caudal peduncle depth; Lpc. Caudal peduncle length; Lc. Head length; Lh. Snout length; Do. Orbital diameter; Lpoc. Postorbital distance; Lhm. Maxilla length; Ai. Interorbital distance; Lms. Upper jaws length; Ell. Lateral–line scales; E(ll–ad). Scale rows between dorsal–fin origin and lateral line; E(ll–aa). Scale rows between anal–fin origin and lateral line; E(ll–apv). Scale rows between pelvic–fin and lateral line; Epd. Predorsal median scales; Rad. Dorsal–fin rays; Raa. Anal–fin rays; Rapv. Pelvic–fin rays; Rapc. Pectoral–fin rays.

A. aurocaudatus

A. cremnobates

H. boquiae

B. caucanus

Morfométricos n

39

Ls

20–56 (42,31)

Lt

24,5–68 (51,56)

59

11

168

28,0–81,9 (46,1) 60,43–70,63 (65,01)

27,2–44,3 (30,75)

71,96–76,14 (74,51)

33,7–56,3 (39,95)

Porcentage de la longitud estándar Pc L(h–ad)

30,5–51,92 (38,47)

25,02–31,12 (27,71)

42–57,14 (52,37)

21,69–27,78 (25,20)

48,92–54,47 (51,29)

49,05–56,79 (52,3)

21,08–22,03 (21,49)

23,10–30,56 (30,15)

L(h–apc) 22,44–39,58 (29,18)

25,8–31,5 (28,7)

L(h–apv) 40,69–70,25 (47,35)

48,2–52,4 (50,4)

39,37–43,01 (41,01)

42,67–47,84 (44,91)

66,6–74 (69,6)

53,21–57,89 (55,19)

53,31–62,63 (59,55) 47,47–54,05 (51,35)

L(h–aa)

39,93–63,48 (58,62)

L(ad–h)

40,56–55,76 (51,13)

51,17–58,63 (54,77)

L(ad–aa)

30–52,93 (38,21)

19,90–21,68 (20,88)

29,48–33,67 (31,29)

36,13–40,46 (38,14)

36,85–44,72 (36,34)

L(ad–apc) 24,48–67,5 (41,04) Lad

6,26–29,16 (14,74)

11,82–14,0 (13,09)

18,38–29,67 (24,24)

Lapc

18,92–36 (23,11)

22,4–28,4 (25,2)

10,81–11,20 (10,98)

14,71–23,02 (20,07)

Lapv

10–17,62 (14,69)

12,26–16,60 (14,34)

10,69–15,64 (13,76)

20,58–22,23 (21,41)

14,87–19,51 (17,50)

9,17–11,10 (10,08)

8,82–11,51 (10,44)

Laa

7,14–21 (14,91)

Ppc

9,09–14,28 (12,18)

Lpc

10,73–17,66 (14,02)

11,9–14,2 (13,0)

7,45–12,76 (10,09)

8,03–14,88 (10,59)

Lc

13,95–29,99 (25,08)

27,6–31,9 (29,7)

12,98–15,79 (14,43)

21,07–23,70 (22,47)

14,66–24,70 (20,66)

24,14–33,68 (29,30)

31,02–34,04 (32,80)

35,71–47,62 (39,38)

10,4–14,2 (12,1)

Porcentaje de la longitud de la cabeza Lh

16,66–35 (23,39)

Do

6,05–10,7 (8,13)

22,9–27,4 (25)

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Animal Biodiversity and Conservation 29.1 (2006)

Tabla 1. (Cont.)

A. aurocaudatus

A. cremnobates

H. boquiae

B. caucanus

Lpoc

4,88–15,12 (12,46)

42,29–49,92 (45,96)

33,80–43,75 (41,96)

Lhm

5,71–16 (8,05)

29,24–31,61 (30,62)

32,84–42,86 (38,45)

Ai

7,5–17,85 (9,58)

31,71–36,25 (34,15)

31,03–40,85 (34,23)

6–14,28 (8,25)

24,59–27,01 (25,67)

30,43–39,47 (33,80)

Ell

19–39

37–39

35–43

E(ll–ad)

6–10

6–7

4–6

E(ll–aa)

6–10

4–5

4–5

E(ll–apv)

4–10

4

4–5

Epd

11–18

13

11–15

Lms Merísticos

Rad

ii,6–8

ii,8

ii,8

Raa

x,13–14

iii,23–26

iii,23–27

Rapv

i,6–5

i,7

i–ii.6–7

Rapc

i,10–13

i,11

i,10–13

La forma, número y distribución de los dientes en el maxilar y premaxilar observados en este trabajo coinciden con lo descrito para otras especies del género Astyanax (Eigenmann 1913; 1921; Taphorn, 1992; Bussing, 1998; Bertaco & Malabarba, 2001; Malabarba & Weitzman, 2003; Valdéz–Moreno & Contreras–Balderas, 2003). Además, el carácter tradicionalmente utilizado para reconocer especies de este género, cinco dientes en la fila interna (Eigenmann, 1921), puede encontrarse en especies de Bryconamericus (Román–Valencia, 2003). Por lo tanto, éste carácter no es suficiente para diagnosticar a Astyanax.

La forma curva del tercer diente del dentario no puede ser asumida como un carácter diagnóstico para un nuevo género Carlastyanax, pues la forma curva de los dientes en el dentario se observa en Astyanax, tanto en A. cremnobates como en A. brachypterygium. Además, en estas especies se registra más de un diente curvo en el dentario (Bertaco & Malabarba, 2001).

El nasal es una estructura alargada, doblada levemente hacia el hocico, como sucede en otros caraciformes (Lucena, 1993; Vari, 1995). Por lo tanto, el carácter correspondiente a la forma del nasal propuesto por Géry (1972) no es suficiente para describir un nuevo género, en éste caso Carlastyanax.

El dentario de Astyanax aurocaudatus no se proyecta más allá del premaxilar. El opérculo es casi rectangular. El primer infraorbital de A. aurocaudatus es equivalente a la fusión del primer y segundo infraorbitales de A. mexicanus, y corresponde con la descripción de forma triangular y que

nunca se sobrepone al margen del infraorbital 3, correspondiente en A. aurocaudatus al infraorbital 2, palatino, ectopterigoides y mesopterigoides sin dientes. Estos caracteres coinciden con los diagnósticos de A. mexicanus, la especie tipo del género Astyanax (Valdéz–Moreno & Contreras–Balderas, 2003). El número de dientes en el maxilar, premaxilar, dentario e infraorbitales observados en este trabajo son caracteres bastante variables para ser considerados como diagnósticos para Carlastyanax.

El supraorbital es una estructura presente en Astyanax aurocaudatus, que al unirse al borde lateral del frontal da origen al canal laterosensorial, que se continúa con el nasal; esto no corresponde a lo descrito por Weitzman (1962), quien afirma que esta estructura no está relacionada con el canal laterosensorial en Brycon meeki. Sin embargo, en Astyanax mexicanus se describe la estructura del supraorbital como el frontal (véase Valdéz– Moreno & Contreras–Balderas, 2003). El número característico de infraorbitales en los carácidos es de cinco o seis (Weitzman, 1962; Miquelarena & Arámburo, 1983; Román–Valencia & Muñoz, 2001; Malabarba & Weitzman, 2003); A. aurocaudatus posee cuatro infraorbitales diferenciados así: el primer infraorbital separado anteriormente del maxilar y el etmoides lateral, no unido por detrás al segundo infraorbital. Sin embargo, su tamaño ocupa un espacio importante en el borde anteroventral de la órbita. En este trabajo se asume el tamaño y la posición de este infraorbital como la fusión del primero y segundo infraorbitales, un carácter derivado. El tercer infraorbital corresponde a la fusión del

62

cuarto y quinto infraorbitales. El segundo y quinto infraorbitales conservan la forma y tamaño descritos para los carácidos sin ningún tipo de fusión (Weitzman, 1962; Valdéz–Moreno & Contreras– Balderas, 2003). El opérculo de Astyanax aurocaudatus es estrecho y romboide, y la espina supraoccipital es larga, como se informa en el caso de A. fasciatus (Valdéz–Moreno & Contreras– Balderas, 2003).

La relación de Astyanax aurocaudatus con otros carácidos como Hemibrycon dentatus y H. boquiae, planteada por Géry (1972) no es sustentable, pues a través de nuestras observaciones (Román–Valencia, 2001; Román–Valencia & Ruiz, 2005) se determinó que los modelos de coloración no son semejantes, y los aspectos ecológicos de las especies citadas no corresponden a lo observado en Astyanax aurocaudatus, de hábitos epibentónicos (Román–Valencia & Ruiz, 2005). Todo ello concuerda con lo observado en la longitud y profundidad del pedúnculo caudal de A. aurocaudatus, que es de mayor tamaño con relación a lo observado en H. boquiae. En base a observaciones de Román– Valencia (2002), el engrosamiento del pedúnculo caudal está relacionado con una escasa velocidad, lo que coincide con su actividad gregaria y lenta.

La distancia entre la aleta dorsal y las aletas pectoral y anal es menor en Astyanax aurocaudatus con relación a la registrada para H. boquiae. Ello revela que A. aurocaudatus no es tan alargado como H. boquiae. Esta especie se localiza en la parte media y superior de la columna de agua, como Bryconamericus caucanus (Román–Valencia & Muñoz, 2001).

Astyanax aurocaudatus posee características osteológicas que comparte con otras especies sintópicas como Bryconamericus caucanus y Hemibrycon boquiae: la espina neural de las vértebras precaudales posee un crecimiento indeterminado aun en la madurez, lo que permite que el extremo distal de la espina neural se una a la parte ventral de los supraneurales y de los pterigióforos proximales de la aleta dorsal en ejemplares adultos. Los machos observados en este trabajo presentaron las tres primeras costillas pleurales del lado izquierdo con ondulaciones pronunciadas; este tipo de modificaciones óseas corresponde a la morfología y anatomía de su cuerpo robusto y su lomo pronunciado. Ello no sucede en otras especies de Astyanax como A. asuncionensis, A. paranae, A. integer, A. intermedius, A. pellegrini, A. scintillans, A. simulatus y A. superbus (Eschmeyer, 2003). Algunos caracteres que comparte Astyanax aurocaudatus con otros carácidos son: la presencia de cartílago en medio de la unión del ectopterigoides, mesopterigoides, metapterigoides y cuadrado; una banda de cartílago que bordea al proótico; y la unión de los extremos del simplectico, el interhial y el extremo del proceso del hiomandibular sobre el preopérculo, por las porciones de cartílago que poseen sus extremos.

Además el rinoesfenoides cartilaginoso se extiende de forma ascendente hacia la unión del frontal y el

Ruiz–C & Román–Valencia

etmoides; este carácter presenta un gran variabilidad en cuanto a su distribución en el extremo anterior del neurocráneo y su grado de osificación. Los pterigióforos posteriores de la aleta anal están separados y son cartilaginosos, y se modifican al aproximarse al extremo anterior, con lo que se fusionan el pterigióforo medial y el proximal, y el cartílago transitorio se reduce a unas pequeñas trazas o banda periférica. En este sentido se observa un desplazamiento hacia las estructuras óseas como un carácter posiblemente sinapomórfico.

Agradecimientos Este trabajo se benefició de las correcciones y lectura crítica de Francisco Langeani (UNESP, Brasil), Ricardo A. Ferriz (MACN, Argentina), Francisco Provenzano (MBUCV, Venezuela) y dos revisores anónimos. Le estamos agradecidos a Donald C. Taphorn (MCNG, Venezuela) por la literatura suministrada y sus generosos consejos, y a Carlos A. García (IUQ, Colombia) por la digitalización de las figuras. IDEA WILD financió los reactivos para el proceso de diafanización.

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Taylor, R. W. & Van Dyke, G. C., 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119.

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Skull osteology of the fish Astyanax mexicanus (Teleostei: Characidae). Proceeding of the Biological Society of Washington, 116: 341–355.

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Ctenoluciidae (Teleostei: Ostariophysi: Characiformes): supra and intrafamilial phylogenetic relationship, with a revisionary study. Smithsonian Contributions to Zoology, 564: 1–96.

Vari, R. P. & Harold, A. S., 2001. Phylogenetic study of the neotropical fish genera Creagrutus Günther and Piabina Reinhardt (Teleostei: Ostariophysi: Characiformes), with a revision of the Cis–Andean species. Smithsonian Contribution to Zoology, 613: 1–239.

Weitzman, S. H., 1962. The osteology of Brycon meeki,a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8: 1–77.

Weitzman, S.H. & Fink, S. V., 1985. Xenurobryconin phylogeny and putative pheromone pumps in Glandulocaudine fishes (Teleostei: Characidae).

Smithsonian Contributio to Zoology, 421: 1–121.

Zarske, A. & Géry, J. 1999. Astyanax villwocki sp.nov., a new characid fish from the upper Amazon basin of Peru and Bolivia (Teleostei, Characiformes, Characidae). Mitteilungen aus dem Zoologischen Institut und Zoologischen Museum Hamburgo, 96: 199–206.

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Regression analysis between body and head measurements of Chinese alligators (Alligator sinensis) in the captive population X. B. Wu, H. Xue, L. S. Wu, J. L. Zhu & R. P. Wang

Wu, X. B., Xue, H., Wu, L.S., Zhu, J. L. & Wang, R. P., 2006. Regression analysis between body and head measurements of Chinese alligators (Alligator sinensis) in captive population. Animal Biodiversity and Conservation, 29.1: 65–71.

Abstract Regression analysis between body and head measurements of Chinese alligators (Alligator sinensis) in the captive population.— Four body–size and fourteen head–size measurements were taken from each Chinese alligator (Alligator sinensis) according to the measurements adapted from Verdade. Regression equations between body–size and head–size variables were presented to predict body size from head dimension. The coefficients of determination of captive animals concerning body– and head–size variables can be considered extremely high, which means most of the head–size variables studied can be useful for predicting body length. The result of multivariate allometric analysis indicated that the head elongates as in most other species of crocodilians. The allometric coefficients of snout length (SL) and lower ramus (LM) were greater than those of other variables of head, which was considered to be possibly correlated to fights and prey. On the contrary, allometric coefficients for the variables of obita (OW, OL) and postorbital cranial roof (LCR), were lower than those of other variables.

Key words: Regression analysis, Allometry, Chinese alligator.

Resumen Análisis de regresión entre las mediciones del cuerpo y la cabeza del aligator chino (Alligator sinensis) en las poblaciones en cautividad.— Se tomaron medidas de cuatro dimensiones del cuerpo y catorce de la cabeza de cada uno de los aligatores chinos (Alligator sinensis) según las mediciones de Verdade adaptadas. Se presentaron ecuaciones de regresión entre las variables del tamaño del cuerpo y de la cabeza, para predecir el tamaño corporal a partir de las dimensiones cefálicas. Puede considerarse que los coeficientes de determinación de los animales cautivos, concernientes a las variables del tamaño del cuerpo y la cabeza son muy altos, lo que significa que la mayoría de las variables del tamaño cefálico estudiadas pueden ser útiles para predecir la longitud del cuerpo. Los resultados del análisis alométrico multivariante indicaron que la cabeza se alarga como en la mayoría de especies de cocodrilos. Los coeficientes alométricos de la longitud del hocico (SL) y del ramus inferior (LM) fueron mayores que otras variables de la cabeza, estando correlacionados, posiblemente, con las luchas y la captura de presas; Por el contrario, los coeficientes alométricos para las variables de las óribitas (OW, OL) y del techo craneano postorbital (LCR) son relativamente menores que para otras variables.

Palabras clave: Análisis de regresión, Alometría, Aligator chino.

(Received: 7 I 04; Conditional acceptance: 5 II 04; Final acceptance: 16 XI 05) Xiaobing Wu, Hui Xue & Lusheng Wu, College of Life Science, Anhui Normal Univ., 1 East Beijing Road, Wuhu, 241000 China.– Jialong Zhu & Renping Wang, Anhui Research Center for Chinese Alligator Reproduction, Xuancheng 242000, China.

Corresponding author: Wu Xiaobing. E–mail: wuxb@mail.ahnu.edu.cn ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction The skull is one of the most complicated organs in the body both morphologically and functionally (Pan & Oxnard, 2002). Total skull length was considered the independent variable reflecting overall size (Simpson, et al. 1960; Radinsky, 1981).

Population monitoring of crocodilians usually involves night counts when frequently only the heads of animals are visible. Size–class distribution for the target population is therefore usually based on the relationship between length of head and total body length (Verdade, 1997). Allometric relations can be useful for estimating body size from isolated measures of parts of the body (Schmidt– Nielsen, 1984). As an example, Chabreck (1966) suggests that the distance between the eye and the tip of the snout in inches is similar to the total length of Alligator mississippiensis in feet.

Choquenot & Webb (1987) proposed a photographic method to estimate total length of Crocodylus porosus from head dimensions. Ontogenetic changes in skull structure are of interest to biologists, and wildlife managers can use measurements of discarded skulls to estimate the sizes of hunted animals (Mourão et al., 1996). Relative or allometric growth has been studied in several kinds of crocodiles (Hall, 1994; Verdade, 1999), but as yet there is no comprehensive study on the Chinese alligator.

Allometric analysis can assess the covariation of characters (Cock, 1966) and provide a method to elucidate the relationship between processes of growth and evolution (Blackstone, 1987). Morphometric allometric relationships have been developed for bivariate allometric equations and for a multivariate generalization of the bivariate allometric equation. The formula of bivariate allometry (Huxley, 1932) assumes a power function of the form y = bx where x and y are measurements and the constant is often called the allometric coefficient. The special case when = 1 is called isometry. Jolicoeur (1963) used the first eigenvector extracted from the covariance matrix of log–transformed data to reflect the multivariate allometic coefficients. When all loadings of the first eigenvector equal a value 1 divided by the square root of the number of the variable, the first eigenvector is called the isometry vector. The multivariate allometric coefficients can be easily translated to bivariate allometric coefficients by using the ratio of the coefficients in the first eigenvector for two variables corresponding to the variable in the bivariate allometric analysis (Shea, 1985).

The wild population of Chinese alligator may number < 130 (Thorbjarnarsona et al., 2002), so we studied relative and allometric growth in captive animals. Although the data taken in the paper is not based on wild specimens this is the most feasible way to explore the relationship between skull and body for this species.

OL

CV IOW OW

WN SW

DCL LCR

SL

PXS ML Fig.1. Measurements adapted from Verdade (1999). The picture shows the head–size variables of Chinese alligator (adapted from Wermuth, 1953). (For abbreviationssee material and methods.)

Fig. 1. Mediciones adaptadas de Verdade (1999). La ilustración muestra las variables del tamaño cefálico del aligator chino (adaptado de Wermuth, 1953). (Para las abreviaturas ver material and methods.)

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Animal Biodiversity and Conservation 29.1 (2006)

Materials and methods Samples The samples were taken from the Anhui Research Center for Chinese Alligator Reproduction (ARCCAR). There were animals from five age groups at the centre: 18 individuals were eight months old, 20 individuals were one year old (about 15 months), 20 animals were two years old (about 27 months), 20 animals were three–year old (about 39 month) and 20 animals were four years old (about 51 month). The data from a total of 98 individuals were analyzed.

coefficients on the first principal component (PC1) corresponds to (but does not necessarily equal) the coefficient that would be obtained if those same variables were regressed against one another in a typical bivariate allometry analysis (Huxley, 1932). The isometric vector has the standardized loadings (1/p)1/2, where p is a number of traits. With fourteen traits of head in this study (1/p)1/2 was 0.2673, so that the ratio of each trait’s loading with 0.2673 is the bivariate allometry coefficient of that trait with overall body size (Badyaev, 2000).

Results

Measurements Measurements were taken with a steel electronic digital caliper (0.01 mm precision, third decimal not considered) to take the head–size measurements, a tape (1mm precision) to measure the body–size, a balance (for animals < 1000 g, 0.2 g precision) and a hanging scale (for animals >1000 g, 5 g precision) to weigh the animals. The study began at the onset of the hibernation period.

Four body–size and fourteen head–size variables were taken from Chinese alligators: SVL. Snout– vent length, cm; TTL. Total length, cm; BW. Commercial belly width, mm; BM. Body mass, Kg/g; DCL. Dorsal cranial length: anterior tip of snout to posterior surface of occipital condyle, mm; CW. Cranial width: distance between the lateral surface of the mandibular condyles of the quadrates, mm; SL. Snout length: anterior tip of snout to anterior orbital border, mm; SW. Basal snout width: width across anterior orbital borders, mm; OL. Maximal orbital length, mm; OW. Maximal orbital width, mm; IOW. Minimal interorbital width, mm; LCR. Length of the postorbital cranial roof: orbital border to the posterolateral margin of the squamosal, mm; WN. Maximal width of external nares, mm; PXS. Length of palatal pre maxillary symphysis, mm; ML. Mandible length, mm; LMS. Length of the mandibular symphysis, mm; WSR. Surangular width, mm; LM. Length of lower ramus, mm. The measuremenst of these variables are shown in fig.

1 (Verdade, 1999; Chen, 1985; Cong & Hou, 1998).

One of the measurements, PXS, the length of the premaxillary symphysis, is closely approximated by the distance from the snout tip to the anterior tip of the first tooth posterior to the prominent groove in the snout behind the nares because it is not seen in live animals (Verdade, 1999).

Statistical analysis Bivariate polynomial regression analysis was performed with the snout–vent length (SVL, in cm) value as dependent variables and other variables as independent variables Verdade (1999). We used the first component obtained from a principal components analysis (PCA) as a generalization of simple allometry. In such an analysis, the ratio of

Regression analysis between body length and head length There was a significant correlation between body– and head–size, and relative growth trajectory appears apparently (fig 2). The results were significant with extremely high coefficients of determination (r2) (table 2); except for IOW (r2 = 0.793) they were greater than 0.9 and all of the p–values were significant at 0.001.

Multivariate allometric analysis of head Principal component analysis was applied to fourteen head variables, and the eigenvector of first principle component was calculated. Ten eigenvalues of head traits were greater than the isometric vector (0.2673), indicating these variables show positive allometric growth, and others have negative or no allometry. Among the variables, loadings of SL and LM were higher than all the others, while loadings of OL, OW and LCR were comparatively lower. Coefficients of length variables were all slightly greater than those of width variables (DCL > CW, SL > SW, ML > WSR, see table 3), but differences were slight. This indicates that the skull of Chinese alligator elongates during ontogeny.

Discussion Although most of the researchers have used the model of Huxley (1932) to study allometry, we used polynomial regression rather than the power function to depict the relationship between head and body size, because the allometric function did not improve the regression equations with the exception of body mass in our study. The coefficients of determination of captive animals for body– and head–size variables can be considered extremely high. That is, most of the head–size variables studied can be useful for predicting body length. This can be particularly interesting in the study of museum collections and reconstruction of sizes of hunted animals from skulls left by hunters (e.g. Mourão et al., 1996).

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Wu et al.

80 SVL

80 SVL

80

60

60

60

40

40

40 20

20

20 TTL

0 0 80

40

80

BM

0

120

0

40

80

SVL

80

120

SVL

0 –1.5 –0.7

60

60

40

40

40

20

20

0 0

80

25

50

75

0

80

SVL

40

80

60

40

40

20 0

20

40

60

80

30

20

30

40

CW

0 5

10 15

80 SVL

80 SVL

60

60

60

40

40

40

IOW

0 0

5

10

15

20

LCR

0 10

80

SVL

80

20

30

0

80

60

60

40

40

40

PXS

0 0

10

20

30

ML

0

40

0

80 SVL

80 SVL

60

60

40

40

20

60

120

180

30

SVL

LMS

0 0

10

20

30

20

20 0

10

20

20

30

WN

0

40

SVL

20 25

20

60

20

90

20 CL

0 10

80 SVL

20

60

80 SVL

SVL

60

0

SL 0

40 SW

0.9

0

120

60 20

0.1

20 CW

0

100

log BM

SVL

80

60

DCL

SVL

WSR 0

25

50

75

100

LM

0 0

40

80

120

Fig. 2. Plot between body– and head–size variables for Chinese alligator. (Log BM: log–transformed BM, BM all in kg finally; SVL and TTL in cm, the others in mm). See table 2 for regression equations.

Fig. 2. Gráfico de la relación de las variables del tamaño corporal y cefálico del aligator chino. (Log BM: BM transformado logarítmicamente, BM finalmente en kg; SVL y TTL en cm, los demás en mm).

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Animal Biodiversity and Conservation 29.1 (2006)

Table 2. Regression equations between body and head variables for Chinese alligator: Y = a + bX + cX2 + dX3; N. Sample size. (Log–transformation only was performed on BM to improve the coefficient of determination, r2).

Tabla 2. Ecuación de regresión entre las variables corporales y cefálicas del aligator chino: Y = a + bX + cX2 + dX3; N. Tamaño de la muestra. (La transformación logarítmica sólo se efectuó en el caso de BM, para mejorar el coeficiente de determinación, r2).

r2

N

p–value

0.960

98

0.000

0.0019

0.911

98

0.000

8.3614

0.956

98

0.000

0.4782

0.957

98

0.000

–4.5712

0.7622

0.960

98

0.000

–.8684

0.8427

0.952

98

0.000

0.966

98

0.000

0.929

98

0.000 0.000

Y

X

a

b

SVL

TTL

–1.6566

0.5098

SVL

BW

13.2894

0.1526

SVL

logBM

31.1874

–24.070

SVL

DCL

–5.3251

SVL

CW

SVL

SL

c

d

SVL

SW

–2.3516

0.8722

SVL

OL

65.8007

–9.8093

SVL

OW

–27.2680

3.6849

0.916

98

SVL

IOW

–6.0657

6.8427

0.793

98

0.000

SVL

LCR

–18.398

2.3385

0.915

98

0.000

SVL

WN

–0.9352

2.4374

0.944

98

0.000

SVL

PXS

–2.3766

2.0548

0.933

98

0.000

SVL

ML

–3.1303

0.4185

0.954

98

0.000

SVL

LMS

–11.682

3.8944

0.926

98

0.000

SVL

WSR

–2.0222

0.7125

0.967

98

0.000

SVL

LM

6.9786

0.2388

0.947

98

0.000

0.5596

–0.0392 0.0026

–0.0081

Table 3. Multivariate allometry of morphological trait of Chinese alligator. The table shows the first eigenvectors and the proportion of total variance (%), accounted for by the first eigenvalue from the variance–covariance matrix of log–transformed values: PCI. The ratio of coefficients on the first principal component; P(+) / N(–). Positive (+) / Negative (–) allometric growth.

Tabla 3. Análisis de Componentes Principales de los rasgos morfológicos del aligator chino. La tabla muestra los primeros valores propios y la proporción de varianza total explicada (%), según el primer valor propio de la matriz de varianzas–covarianzas, a partir de los valores transformados logarítimicamente: PCI. Relación de los coeficientes de la primera componente principal; P(+) / N(–).

Crecimiento alométrico Positivo (+) / Negativo (–).

PC I

PC I Variables

Loadings

DCL

0.2705

CW

0.2696

Var % 97.3

P(+)/N(–)

Variables

Loadings

Var %

P(+)/N(–)

+

LCR

0.1911

–

+

WN

0.2940

+

SL

0.3134

+

PXS

0.2827

+

SW

0.2906

+

ML

0.2910

+

OL

0.1954

–

LMS

0.2689

+

OW

0.1581

–

WSR

0.2903

+

IOW

0.2436

–

LM

0.3237

+

70

Verdade (1997) found that determination coefficients of wild and captive broad–snouted Caiman (Caiman latirostris) were extremely high and drew the conclusion that animals lack morphological variation. The phenomenon also appears in Chinese alligator. The conclusion, which is similar to Verdade’s, may be a little arbitrary, but it is an inevitable result that morphological variation would gradually disappear in the captive population due to current conditions, as the genetic variation disappears (Wu, 2002). Efforts should therefore be made to release captive Chinese alligators as soon as possible.

During ontogeny, the skulls of Chinese alligator elongate. The elongation is not particularly obvious as we found no significant differences between coefficients of length and width. Elongation of the skull also appears in Caiman sclerops, Caiman yacare, and Melanosuchus niger, but the skull of the broad–snouted Caiman becomes stout (Monteiro & Soares, 1997). Although the overall skull shape of the Chinese alligator is similar to that of the broad–snouted Caiman (short, broad snouts) the growth trajectory of the head is different. The allometric pattern observed in broad– snouted Caiman is unique among crocodilians (Monteiro & Soares, 1997).

Allometric analyses indicate that the snout and lower ramus grow most compared to other head features. This phenomenon may be associated with the functions of prey capture and fighting (Webb & Messel, 1978).

Acknowledgements We are very grateful to Mr. Mike Brittsan for reviewing the manuscript and correcting the English. We also thank the Anhui Researching Center for Chinese Alligator Reproduction for their kind assistance with the data collection. This study was sponsored by the National Natural Science Foundation of China (NSFC, No. 30270213), the Provincial Excellent Youth Technology Fund of Anhui (No. 04043049) and A Special Scholar Foundation from Anhui Province.

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Factores ambientales condicionantes de la presencia de la lagartija de Carbonell Podarcis carbonelli (Pérez–Mellado, 1981) en la comarca de Doñana J. Román, G. Ruiz, M. Delibes & E. Revilla

Román, J. Ruiz, G. Delibes, M. & Revilla, E., 2006. Factores ambientales condicionantes de la presencia de la lagartija de Carbonell Podarcis carbonelli (Pérez–Mellado, 1981) en la comarca de Doñana. Animal Biodiversity and Conservation, 29.1: 73–82.

Abstract Environmental factors determining the presence of the Carbonell lizard Podarcis carbonelli (Pérez–Mellado, 1981) in the Doñana area.— The Carbonell lizard (Podarcis carbonelli) is an Iberian endemism. The region of Doñana is its southernmost and more isolated stronghold. We used logistic regressions to investigate the factors conditioning the presence of this lizard in Doñana. All selected models retained the distance to the coast as the main variable. This variable is related with less humidity and more continental climatic conditions, including more extreme temperatures, when further from the coast. This climatic factor was observed both spatially and temporarily, with adult lizards drastically reducing their activity both in winter and in summer. We observed juveniles from June to January, with a maximum in September. Scrubland management was another important environmental factor affecting the presence of lizards. The probability of finding this species was higher where the scrubland was partially cleared, and lower in areas with a high plant cover (hygrophytic scrubland) or in areas with sparse vegetation (dune scrubland), probably due to a lower amount of incident light and less protection when moving between refuges, respectively.

Key words: Podarcis carbonelli, Doñana, Isolated populations, Habitat management, Scrubland.

Resumen Factores ambientales condicionantes de la presencia de la lagartija de Carbonell Podarcis carbonelli (Pérez– Mellado, 1981) en la comarca de Doñana.— La lagartija de Carbonell es un endemismo ibérico que encuentra en la comarca de Doñana el reducto más meridional y aislado de su área de distribución. Mediante el uso de regresiones logísticas se ha intentado conocer qué factores condicionan la presencia de la lagartija de Carbonell en Doñana. La variable principal de los distintos modelos fue la distancia a la costa. Ésta se relaciona con un menor grado de humedad y una mayor continentalidad del clima, con temperaturas más extremas, a medida que nos alejamos del mar. Este condicionante climático se ha observado tanto espacial como temporalmente, reduciéndose drásticamente la actividad de los animales adultos en verano e invierno.

Los juveniles se observan desde junio a enero con un máximo en septiembre. Otro de los factores importantes ha resultado ser la gestión del matorral. Se ha observado una mayor probabilidad de encontrar la lagartija de Carbonell en zonas en las que el matorral ha sido parcialmente clareado, ya que evita los lugares con elevadas densidades de plantas (matorral hidrofílico), que reducirían el paso de la luz, o con una densidad muy baja (matorral de las dunas), que no permitiría el tránsito seguro entre refugios.

Palabras clave: Podarcis carbonelli, Doñana, Poblaciones aisladas, Gestión del hábitat, Matorral.

(Received: 13 VI 05; Conditional acceptance: 29 IX 05; Final acceptance: 7 XII 05) Jacinto Román, Miguel Delibes & Eloy Revilla, Dpto. de Biología Aplicada, Estación Biológica de Doñana, Av. María Luisa s/n, 41013–Sevilla, España (Spain).– Gema Ruiz, c/ Giralda 19, 41110 Bollullos de la Mitación, Sevilla, España (Spain).

Corresponding author: J. Román. E–mail: jroman@ebd.csic.es ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

74

Introducción La presencia de lagartijas del género Podarcis en la comarca de Doñana es conocida de antiguo, planteándose desde un principio dudas sobre su asignación taxonómica precisa (Valverde 1960, 1967).

Magraner (1986) es el primer autor que consideró la presencia de dos especies de Podarcis, asignando a Podarcis bocagei carbonelli las lagartijas que ocupan los arenales, y a Podarcis hispanica las restringidas a los pueblos. Aunque Pérez–Mellado (1997a) rechazó estas observaciones, indicando que Podarcis b. carbonelli se encontraría exclusivamente en el sector occidental del Sistema Central (centro de la península ibérica), estudios recientes confirman la presencia de esta lagartija en la comarca de Doñana (Sá–Sousa, 2000, 2001; Sá–Sousa et al., 2001). Por otro lado, la aplicación de técnicas de filogenia y taxonomía molecular ha permitido reconocer que se trata de una especie independiente, que debe denominarse Podarcis carbonelli (Harris & Sá–Sousa, 2001; Sá– Sousa, 2001; Sá–Sousa & Harris, 2002).

Podarcis carbonelli es una lagartija de pequeño tamaño con la zona central del dorso pardo uniforme y líneas dorsolaterales verde brillante, irregulares en los machos y más definidas en las hembras, vientre blanquecino, píleo corto y cabeza alta (Pérez– Mellado, 1981; Pérez–Mellado & Galindo, 1986; Sá– Sousa et al. 2001; Sá–Sousa & Harris, 2002).

Se trata de una especie con una distribución regresiva, que encuentra su núcleo principal de distribución en áreas montañosas forestales del sector occidental del Sistema Central y centro de Portugal (Pérez– Mellado, 1981; Pérez–Mellado, 1997a; Sá–Sousa, 2002). Actualmente no se observa una continuidad en la distribución, estando las poblaciones más meridionales aisladas entre sí. El núcleo de Doñana es el más alejado que se conoce del área principal de presencia de la especie (Sá–Sousa, 2000; Sá–Sousa, 2002). Al ser Doñana la más meridional de estas poblaciones, es razonable suponer que haya sido una de las primeras en segregarse del núcleo principal.

Las particulares condiciones fisiográficas, zona arenosa con escaso relieve, claramente diferentes a las zonas montañosas habitualmente habitadas por la especie, nos inducen a pensar que la subsistencia de esta población es debida a una adaptación a las condiciones ecológicas locales o a una existencia en el límite de las condiciones ecológicas necesarias para su presencia.

Los objetivos del presente trabajo son: (a) conocer los factores limitantes de la presencia de Podarcis carbonelli en la comarca de Doñana, tanto desde el punto de vista climático como desde el del macro y microhábitat; (b) evaluar la influencia de las diferentes prácticas locales de gestión del monte mediterráneo sobre la presencia de Podarcis carbonelli; y (c) analizar el ritmo circanual de actividad de la especie.

Conocer estos parámetros resulta básico para la conservación de estas poblaciones–isla de gran importancia en el mantenimiento de la diversidad biológica, pues éstas se convierten con el tiempo

Román et al.

en lugares de diversificación genética y, a más largo plazo, en centros de especiación (Rojas, 1992; Meffe & Carrol, 1997; Orians, 1997).

Material y métodos Área de estudio La comarca de Doñana ha sido detalladamente descrita (Valverde, 1958; García–Novo et al., 1978).

Se encuentra enclavada en la provincia de Huelva, SO de la península ibérica (fig. 1). Básicamente consiste en una gran marisma limitada al oeste y al sur por un manto eólico arenoso que constituye las zonas de monte, conocidas localmente como “cotos”. Nuestro estudio se centra en estos últimos, puesto que en las zonas de marisma no se localizan especies del género Podarcis (Díaz–Paniagua & Rivas, 1987). Las formaciones vegetales de los cotos están dominadas por el matorral, siendo el único arbolado autóctono unos pocos cientos de alcornoques centenarios (Quercus suber) y zonas de sabinar (Juniperus phoenicea turbinata). Grandes extensiones fueron repobladas a mediados del siglo pasado con pinos (Pinus pinea) y eucaliptos (Eucaliptus globulus y E. camaldulensis, principalmente), pero en la actualidad estas últimas están siendo desmontadas.

Dentro de la comarca se encuadran dos áreas de reserva, los Parques Nacional y Natural de Doñana, con diferente gestión y grado de protección, constituyendo la suma de ambos una de las mayores reservas biológicas de Europa Occidental.

El presente estudio se centra en cinco sectores: los Pinares de Coto del Rey y Abalario, incluidos en el Parque Natural de Doñana, la Reserva Biológica de Doñana y la finca de Matasgordas, en el Parque Nacional de Doñana y los cotos de Cabezudos en áreas no protegidas.

Doñana se encuentra dentro de la Región Bioclimática Mediterránea, caracterizada por presentar sequía estival, y dentro de ésta en el piso Termomediterráneo. La temperatura media anual es de 17–19ºC, estando la media de las mínimas del mes más frío entre 4 y 10ºC y la media de las máximas del mes más cálido entre 14 y 18ºC. Ombroclimáticamente se incluye dentro del tipo subhúmedo, con precipitaciones entre 600– 1000 mm, anuales (Rivas–Martínez, 1987).

Muestreo de animales El estudio se ha basado en el trampeo pasivo de ejemplares en puntos fijos, siendo el esfuerzo de muestreo igual para todos los puntos. En cada uno de ellos se situó una estación de trampeo, consistente en cinco trampas de caída unidas por una valla conductora, diseñadas para la captura de pequeños vertebrados terrestres (anfibios, reptiles y micromamíferos). Cada estación de trampeo constaba de cuatro tubos de PVC de 16 cm de diámetro y uno de 25,5 cm, todos ellos de 50 cm de longitud,

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Animal Biodiversity and Conservation 29.1 (2006)

690000

700000

710000

720000

730000

740000

C

750000

N 4120000

E

4120000

C B 4110000

4110000

D 10 km

Atlantic Ocean 4100000

4100000

A

4090000

4090000

4080000

4080000

690000

700000

710000

720000

730000

740000

750000

Fig. 1. Mapa del área de estudio. Las zonas estudiadas se enmarcan con trazo grueso. A. Reserva Biológica de Doñana; B. Matasgordas; C. Pinares de Coto del Rey; D. Abalario; E. Cotos de Cabezudos. El área ocupada por las zonas arenosas de los Sistemas Eólicos está sombreada. La zona rayada indica la marisma: Lugares donde se ha localizado la especie en el presente estudio; Lugares trampeados en los que no se ha localizado la especie; Otras observaciones de la especie, incluidas anteriores citas publicadas.

Fig. 1. Map of the study area. The thick lines mark the prospected areas. A. Doñana Biological Reserve; B. Matasgordas; C. Pine woods of Coto del Rey; D. Abalario; E. Cotos de Cabezudos. Sandy areas of Aeolian origin are shaded, while the marshland is striped: Sampling point with Carbonell lizard present; Sampling point with Carbonell lizard absent; Other observations of the species, including those reported in other studies.

enterrados en el suelo; hacia estos tubos conducían veintidós metros de valla de poliéster, de 20 cm de altura, sujeta con gavillas y pinzas. Los tubos se situaban formando una cruz griega, con el tubo de mayor tamaño situado en el centro, y los otros cuatro en los extremos de los brazos, a 5,5 m de distancia.

Cuando la estación se encontraba desactivada, los tubos estaban tapados con una tabla, para evitar la captura de animales. Cuando se activaba, se retiraban las tapas y se colocaba la valla de poliéster uniendo los tubos pequeños con el grande.

Elección de los puntos de muestreo Las distintas estructuras y tipos de vegetación que encontramos en la comarca de Doñana tienen una representación superficial muy diferente según las zonas. Con el objeto de abarcar en los muestreos la mayoría de los tipos de vegetación y uso del suelo, independientemente de su extensión, hemos definido una serie de macrohábitats. Éstos surgen de la combinación de tres factores variables, que

son los principales condicionantes de la estructura de la vegetación en la comarca de Doñana: unidades de vegetación (entendidas como grupos de comunidades de plantas leñosas autóctonas reconocibles desde el punto de vista paisajístico; Sousa & García, 1998), grado de protección y la edad de los pinares.

En la tabla 1 se detallan todas las combinaciones encontradas de estos tres factores. En cada una de éstas se eligieron tres puntos de muestreo al azar, separados un mínimo de 500 m. En total se muestrearon 60 puntos, entre septiembre de 1998 y agosto de 1999. Cada punto era muestreado durante cinco días seguidos al mes. Las trampas eran revisadas a diario para evitar la muerte de los animales, que eran retirados y soltados a distancias superiores a 500 m de la trampa más cercana y siempre dentro del mismo macrohábitat. Debido al pequeño tamaño de las trampas, el número de capturas ha sido bajo y no creemos que haya existido un impacto a nivel poblacional sobre la especie, debido a la translocación de los animales.

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Tabla 1. Estratos utilizados durante el estudio, en función del sector, las unidades de vegetación, grado de protección y tipo de gestión forestal.

Table 1. Stratified sampling design as a function of the sector, vegetation, protection and type of forest management.

Sector

Protección

Unidad de vegetación

Repoblaciones forestales

Reserva Biológica

Parque Nacional

matorral xerofítico

sin repoblación

Reserva Biológica

Parque Nacional

matorral hidrófilo

sin repoblación

Reserva Biológica

Parque Nacional

matorral xerofítico

árboles > 3 m de altura clareados

Reserva Biológica

Parque Nacional

sabinar

sin repoblación

Reserva Biológica

Parque Nacional

médano

árboles de 1–3 m de altura

Matasgordas

Parque Nacional

matorral noble

sin repoblación

Coto Rey

Parque Natural

matorral xerofítico

árboles > 3 m de altura sin clarear

Coto Rey

Parque Natural

matorral noble

árboles > 3 m de altura sin clarear

Abalario

Parque Natural

médano

árboles de 1–3 m de altura

Abalario

Parque Natural

sabinar

sin repoblación

Abalario

Parque Natural

matorral xerofítico

árboles > 3 m de altura clareados

Abalario

Parque Natural

matorral noble

árboles > 3 m de altura sin clarear

Abalario

Parque Natural

matorral noble

árboles > 3 m de altura clareados

Abalario

Parque Natural

matorral xerofítico

árboles de 1–3 m de altura

Abalario

Parque Natural

matorral xerofítico

árboles < 1 m de altura

Abalario

Parque Natural

matorral noble

árboles < 1 m de altura

Abalario

Parque Natural

matorral hidrófilo

sin repoblación

Cabezudos

no parques

matorral xerofítico

árboles > 3 m de altura sin clarear

Cabezudos

no parques

matorral xerofítico

árboles < 1 m de altura

Cabezudos

no parques

matorral xerofítico

árboles > 3 m de altura clareados

Estimación de la variación climática

Muestreo de la vegetación a escala de microhábitat

Hemos usado la distancia a la costa de cada una de las estaciones de trampeo como una medida indirecta de la variación climática a nivel comarcal. En Doñana la precipitación primaveral aumenta a medida que nos acercamos a la costa hasta un 28%, mientras que la otoñal disminuye hasta un 27% (Castroviejo, 1993). Por otro lado, el grado de humedad cercano al mar resulta superior al del interior, existiendo un efecto de "precipitaciones ocultas", no cuantificado. Existe también una gradación térmica que favorece una mayor continentalización y amplitud térmica hacia el interior (Rodríguez, 1998; Ojeda, 1987) (fig. 2).

Como estimación del carácter extremo de las temperaturas mensuales se ha utilizado el valor absoluto de la diferencia entre la temperatura media de cada mes y la temperatura media anual. Los datos climáticos mensuales se han tomado de la estación meteorológica del Palacio de Doñana.

Las características de la vegetación se midieron en el entorno inmediato de cada uno de los 60 puntos de muestreo. Para ello se situó una cinta métrica de 10 m en cada una de las bisectrices de los brazos de la trampa, midiéndose en total 40 m por estación. Se tomaron medidas de arbolado, matorral, herbáceas y suelo. Las variables que se tomaron fueron: (1) cobertura de cada estrato: centímetros ocupados por la proyección de cada estrato a lo largo de la cinta métrica; (2) altura media de cada estrato, estimada en un círculo de 20 m de diámetro en torno a la trampa; (3) porcentaje de suelo que aparecía cubierto, a lo largo de la cinta métrica; (4) discontinuidad del matorral, entendida como el número de veces que se pasaba de zona cubierta por matorral a zona descubierta a lo largo de la cinta métrica; (5) número de árboles en un círculo de 20 m de diámetro en torno a la trampa.

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Animal Biodiversity and Conservation 29.1 (2006)

Tabla 2. Variables independientes consideradas en las regresiones logísticas. El primer grupo incluye, las variables de escala de macrohábitat (unidades de vegetación, grado de protección y tipo de gestión forestal) y el segundo a escala de microhábitat.

Table 2. Independent variables studied with the logistic models. The first group includes macrohabitat variables (vegetation units, level of protection and type of forest management) and the second group microhabitat variables.

Variable

Descripción

Rango / valores

Variables a escala de macrohábitat distcosta

distancia a la costa en km

0.6–27.9

protec

presencia de reservas naturales

0: sin protección; 1: parque natural; 2: parque nacional

pinar

edad de los pinares

0: sin pinar; 1: pinares <5 años; 2: pinares de 5–20 años; 3: pinares > 20 años clareados; 4: pinares > 20 años sin clarear

gestión

tratamientos de gestión de matorral

0: sin gestión; 1: eliminación en calles 2: eliminación en superficie

veg_pot

vegetación potencial de la zona

1: matorral xerofítico; 2: matorral hidrófilo 3: sabinar: 4: matorral de dunas; 5: matorral noble

Variables a escala de microhábitat t_arb

cobertura total del arbolado

0–4000

h_arb

altura media del arbolado

0–2000

n_arb

número de árboles en el entorno de la trampa

0–240

per_arb

perímetro medio de los árboles

0–272

t_mat c

obertura del matorral

0–4000

h_mat

altura media del matorral

0–241

het_mat

heterogeneidad del matorral

11–100

herbáceas

cantidad de hierba en suelo

0–4000

cob_sue

cantidad de suelo cubierto por hojas

0–4000

Análisis de los datos Se ha considerado que la especie estaba presente en una trampa cuando al menos existía una captura a lo largo de todo el estudio. Los datos de presencia/ ausencia se analizaron mediante regresiones logísticas con el objeto de estudiar la influencia del macrohábitat, el clima y otros factores en la presencia de la lagartija de Carbonell. Para ello se usaron como variables independientes las unidades de vegetación, el grado de protección y el tipo de gestión forestal (tabla 2), así como la distancia a la costa.

Este mismo análisis permitirá evaluar la influencia de las distintas prácticas de gestión del hábitat en la conservación de esta especie.

A nivel de microhábitat, las regresiones logísticas han incluido como variables independientes los valores de desarrollo de la vegetación (cobertura, altura y discontinuidad) en tres estratos –arbolado, matorral y herbáceas– y la cobertura del suelo. Se

ha incluido asimismo la distancia a la costa por entender que puede ser un factor limitante de la presencia también a esta escala (tabla 2).

Para las correlaciones se han usado las de Pearson, y la comparación entre medianas se ha realizado con la prueba de la U de Mann–Withney.

Todos los tests estadísticos se han realizado usando el paquete de programas SAS (SAS Institute Inc, 1990).

Resultados Entre octubre de 1998 y septiembre de 1999 se capturaron 197 lagartijas de Carbonell, en 30 de las 60 estaciones de captura dispuestas en la comarca de Doñana. Todas las capturas se realizaron en las zonas arenosas del Manto Eólico Litoral al sur del arroyo de la Rocina, lo que supone que se concentraron en los sectores de

78

Román et al.

Tabla 3. Resultados de las regresiones logísticas descritas en el texto, tanto a escala de macrohábitat, como de microhábitat.

Table 3. Final logistic models both on macrohabitat and microhabitat variables.

Variable

Parámetro

(2

g.l.

intercepto

2.8±0.97

distcosta –0.27±0.08

1

8.38 0.004

1 10.82 0.001

manejo nivel1 –1.44±0.74

1

3.78

0.05

nivel2

1

3.51

0.06

2.17±1.16

Escala microhábitat intercepto –0.01±1.21

1 0.0001 0.99

distcosta –0.47±0.19

1

6.55

0.01

het_mat

1

6.17

0.01

0.06±0.02

hierba

0.001±0.0005 1

t_mat

–0.001±0.0005 1

8.75 0.003 3.43

1.0

32

0.8

30

0.6

28

0.4 natural

eliminación eliminación en calles en superficie

26

0.2

24

0.0 0

5

P

Escala regional

10 15 20 Distancia costa (km)

25

30

0.06

Amplitud térmica anual (ºC)

Presencia (P)

Abalario y Reserva Biológica. No se capturó ni un solo ejemplar de Podarcis hispanica, y todos los correspondientes a esta especie observados en la comarca, al margen de este estudio, se encontraron ligados a núcleos urbanos (El Rocío y Matalascañas).

El modelo logístico final en el análisis de macrohábitat (Wald (25 = 10.9; P = 0.01; rmax2 = 0.47) retuvo las variables distcosta y gestión del matorral (tabla 3). La probabilidad de encontrar lagartijas de Carbonell disminuyó con la distancia a la costa, habiéndose capturado la especie hasta 9 km tierra adentro. Para los tres niveles de gestión del matorral la probabilidad de presencia fue mayor en las zonas con el matorral eliminado parcialmente, intermedia en las que el matorral fue eliminado en su totalidad y menor en las zonas no tratadas (fig. 2).

La vegetación potencial, la edad de los pinares y el nivel de protección, no estuvieron relacionados con la presencia de la especie.

El modelo final a escala de microhábitat (Wald (25 = 10.4; P = 0.034; rmax2 = 0.66) incluyó de nuevo como variables más influyentes la distancia a la costa distcosta y la cobertura de herbáceas. Además se incluyeron la cobertura total del matorral, con una menor probabilidad de presencia cuanto mayor es su valor, así como la discontinuidad del matorral con un efecto positivo (tabla 3).

22

Fig. 2. Evolución de la probabilidad de presencia de la lagartija de Carbonell, en función de la distancia a la costa y la gestión del matorral. Los puntos indican los distintos valores de amplitud térmica (media de las máximas del mes más cálido–media de las mínimas del mes más frío) para distintas estaciones meteorológicas de la comarca.

Fig. 2. Probability of presence of Carbonell lizards as a function of the distance to the coast and the management of scrubland. Dots show the thermal amplitude (difference between the mean of the highs of the warmest month and the mean of the lows of the coldest month) for the meteorological stations found in Doñana.

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Animal Biodiversity and Conservation 29.1 (2006)

40

7 6

Nº capturas

30

5 4

20

3 2

10

1 0

(Tª media mensual – Tª media anual)

8 adultos juveniles

0 S

O

N

D

E

F

Mr

Ab

M

Jn

Jl

A

Fig. 3. Evolución anual de las capturas de la lagartija de Carbonell, desde septiembre de 1998 hasta agosto de 1999. Debido a que las capturas son menores en los meses con temperaturas extremas, se ha dibujado la evolución del valor absoluto de la diferencia entre la Tª media mensual y la Tª media anual.

Fig. 3. Evolution of captures of Carbonell lizards from September 1998 to August 1999. To highlight the months with more extreme temperatures we plotted the difference between the mean monthly temperature and the mean annual temperature.

En cuanto a la actividad circanual, se capturó la especie en todos los meses del año, aunque existió un menor número de capturas en los meses con temperaturas extremas (r = –0.610; P = 0.025; n = 12). En adultos se observa el pico mayor de capturas en los meses primaverales y un segundo pico de menor tamaño en los otoñales, con dos valles en invierno y en verano. Los jóvenes empiezan a aparecer en el mes de junio y se detectan hasta enero, con un máximo de capturas en los meses estivales (fig. 3).

Como los estudios realizados hasta la fecha sobre las especies del género Podarcis en Doñana (Mellado, 1980; Díaz–Paniagua & Rivas, 1987) se han desarrollado en las zonas de matorral, sus resultados deben aplicarse a la especie P. carbonelli.

La lagartija de Carbonell se ha localizado siempre en zonas de matorral y, salvo una observación al este de El Rocío (Magraner, 1986), todas las citas se localizan en las zonas cercanas a la costa.

Discusión

El hecho de que la población de Doñana esté situada en el borde de la distribución de la especie y sea la más meridional hace pensar que existen factores climáticos que condicionan su presencia.

Nuestros resultados así lo confirman.

A nivel comarcal, el balance hídrico se caracteriza por la elevada temperatura y la irregularidad de las precipitaciones (Suso & Llamas, 1990), existiendo largos periodos secos. La cercanía al mar atenúa la incidencia de ambos factores, por el efecto tampón que sobre las temperaturas ejerce el mar y por la existencia de una humedad relativa más alta cuanto más cerca de la costa. Pensamos por tanto que el gradiente de aridez, entendido como una relación entre temperatura y humedad,

De las dos especies del género Podarcis que se pueden encontrar en la comarca de Doñana, P. hispanica no ha sido capturada en ninguna ocasión en los macrohábitats estudiados. Ello confirma las menciones previas de que en Doñana está restringida a los núcleos urbanos (Magraner, 1986; Sá– Sousa, 2001). Tratándose de una especie habitualmente ligada a zonas rupícolas (Pérez–Mellado, 1997b), probablemente usa las edificaciones como sustitutivo de las rocas en esta zona completamente arenosa. Ello sugiere que ha debido colonizar la comarca recientemente, siguiendo los poblados y las urbanizaciones de nueva construcción.

El clima como factor limitante en la comarca de Doñana

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que se observa desde la costa hacia el interior, es el principal factor limitante de la presencia de la lagartija de Carbonell.

El clima de la comarca se puede considerar cálido, siendo excepcionales los días con temperaturas bajas, registrándose habitualmente sólo unos 5 días con heladas al año (Castroviejo, 1993). El fuerte calor estival es el único elemento predecible en el clima de Doñana, siendo el resto altamente variables (Ojeda, 1987). Por otro lado, la especie está presente en zonas montañosas del Sistema Central Occidental, donde las temperaturas invernales son claramente inferiores (Pérez–Mellado, 1997a). Por todo ello, el calor parecería ser el principal candidato a factor térmico limitante. No obstante, es poco probable que sólo el calor sea un factor limitante para la lagartija en zonas en las que puede refugiarse poniéndose a la sombra. La inclusión en el modelo de las herbáceas sugiere de nuevo el papel relevante de la humedad. La hierba es un recurso escaso en los cotos de Doñana, creciendo básicamente en zonas bajas en las que el nivel de la capa freática se encuentra relativamente cerca de la superficie (García–Novo et al., 1978), lo que indica una mayor humedad a nivel microclimático.

El efecto del clima sobre la presencia de la lagartija de Carbonell, se ve reflejado también en la dinámica temporal de la especie. Los adultos están claramente más activos en los meses con temperaturas suaves (fig. 3). Por otro lado, la mediana de la distancia a la costa en los 6 meses de mayor número de capturas, resultó ser significativamente mayor que la de los 6 meses con menor número de capturas (U = 1521.5; p = 0.02); esto reflejaría una mayor duración de los periodos de inactividad en las zonas separadas de la costa, con la consiguiente reducción en la eficacia biológica de la especie.

Importancia de la estructura del matorral Las áreas con un gran desarrollo del matorral son evitadas por la lagartija de Carbonell. En Doñana estas áreas se localizan básicamente en zonas con el nivel de la capa freática cercano y donde el matorral hidrófilo se encuentra muy desarrollado (García–Novo et al., 1978). Ello indica que la mera presencia de humedad no es una garantía para la presencia de la especie, sino que son necesarios otros factores probablemente ligados a la termorregulación. El matorral hidrófilo denso, en efecto, crea una densa cúpula que impide la entrada del sol. La termorregulación, que en ausencia de rocas debe ser principalmente heliotérmica, se verá fuertemente mermada en esas condiciones. Las zonas de contacto entre matorrales densos y matorrales clareados sí parecen ser usadas por la especie (Díaz–Paniagua & Rivas, 1987).

En relación con ello, hay que destacar la importancia de la variable "discontinuidad del matorral" a la hora de determinar la presencia de la lagartija de Carbonell. En las zonas de matorrales abiertos, en

Román et al.

los que el matorral es abundante pero permite el tránsito entre plantas, la lagartija de Carbonell encontraría facilidades para solearse y refugios en los que protegerse de los depredadores. Esta especie es la más pequeña de las lagartijas de Doñana (peso medio de las hembras adultas = 1.7 g, n = 29; peso medio de los machos adultos = 2.3 g, n = 76) y es por tanto susceptible de ser capturada por un gran número de depredadores de las comunidades mediterráneas (Valverde, 1967). La importancia de la discontinuidad del matorral para la presencia de la lagartija de Carbonell se ve reflejada en la ausencia de capturas en las zonas de dunas con vegetación más abierta, dónde las matas están separadas por distancias superiores a 5 m y en las que la discontinuidad es por tanto escasa, a pesar de ser los lugares situados más cerca de la costa.

Otros condicionantes La existencia de troncos de alcornoque ha sido mencionada como un factor clave en la presencia de Podarcis carbonelli (Valverde, 1960, 1967; Mellado, 1980). Los alcornoques son árboles relativamente escasos en la comarca y ligados a la cercanía de la marisma (Granados et al., 1987). Debido a la ausencia de alcornoques en la mayor parte del área de estudio, hemos intentado comprobar el papel de la abundancia de troncos de pino en la presencia de la especie, no detectándose ningún efecto. No parece, por tanto, ser un factor necesario para la presencia de la lagartija de Carbonell, pero podría tratarse de un elemento facilitador, creando puntualmente lugares de asentamiento en los que encontrar un refugio seguro. Esta necesidad de refugio se ha observado en el uso de pequeñas estructuras artificiales por parte de la especie, como chapas metálicas y tablas de madera tiradas en el campo (obs. pers.) o losetas de cerámica dispuestas a modo de trampas para anfibios y reptiles (Díaz–Paniagua & Rivas, 1987).

De hecho, el lugar donde más fácil resulta observar a la lagartija de Carbonell es soleándose en las pasarelas de tablas dispuestas para facilitar el tránsito de los turistas por la arena en los lugares de uso público de los espacios protegidos (obs. pers.).

Importancia de la gestión del hábitat Las labores forestales desarrolladas principalmente en el Parque Natural y zonas no protegidas parecen influir en la presencia de la especie, aunque conviene diferenciar el efecto de las distintas técnicas utilizadas.

El desbroce del matorral supone su eliminación cortándolo por el cuello de la raíz o arrancándolo.

Esta eliminación se realiza de dos maneras, o bien abarcando toda la superficie de matorral de un área dada y dejando exclusivamente los pinos con los restos de las plantas arrancadas sobre el suelo, o bien eliminando el matorral por calles. Éstas suelen tener unos 3 m de ancho entre los pinos, de forma que la reducción es de un 50% de la superficie, dejando zonas alternas con matorral

Animal Biodiversity and Conservation 29.1 (2006)

desarrollado y sin él. Estas actuaciones de eliminación del matorral aumentan la producción y riqueza de las herbáceas (López et al., 2003a, 2003b) y han sido usadas históricamente en la comarca con objetivos cinegéticos y ganaderos (Granados et al., 1986; Ojeda, 1987; Moreno & Villafuerte, 1995). El incremento de insolación directa, unido a la reducción de la masa total de matorral y al aumento en la discontinuidad de éste, hacen que la eliminación del matorral por calles sea un método de gestión muy adecuado para la lagartija de Carbonell. La eliminación total del matorral aparece como el segundo tratamiento en importancia, ya que en estas zonas la discontinuidad del matorral es escasa, pero la especie encuentra refugio en las matas arrancadas caídas en la superficie del suelo.

Debido a la importancia del clima para la población de la lagartija de Carbonell en la comarca de Doñana, y al carácter altamente variable de áquel, con periodos de varios años de sequía y varios de abundancia de lluvias (Suso & Llamas, 1990), no es descartable que puedan existir periodos de expansión y contracción en el área de distribución local.

Resulta muy difícil que se habiliten presupuestos y se realicen medidas de gestión tendentes a conservar la lagartija de Carbonell, por varias razones. Por un lado no resulta ser una especie amenazada (Sá–Sousa, 2002) y por otro, es poco atractiva, viéndose eclipsada en Doñana por la presencia de especies emblemáticas amenazadas a nivel mundial, caso en el caso del lince ibérico, Lynx pardinus, y el águila imperial Aquila adalberti (UICN, 2004). Ambos depredadores son fuertemente dependientes de la abundancia de conejos (Delibes & Hiraldo, 1981), lo que ha propiciado que se desarrollen ambiciosos planes de gestión, tendentes a recuperar las poblaciones de esta especie, fuertemente mermadas después de la irrupción de la enfermedad hemorrágica (Villafuerte et al., 1994). Entre estos planes se incluyen tratamientos de reducción de la densidad del matorral, concordantes con los realizados para la gestión forestal y que mejoran las condiciones de hábitat para las poblaciones de conejo (Moreno & Villafuerte, 1995). Ya se ha dicho que, aún cuando se hagan con otra intención, estos tratamientos favorecen asimismo a la lagartija de Carbonell.

Resulta por tanto interesante observar cómo actuaciones destinadas a la mejora del hábitat de unas especies repercuten positivamente en otras notablemente diferentes.

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López, I., del Río, I., Galindo, P., Retamosa, E. C., Jordano, D., Haeger, J. F., Muñoz, J.C. & Villar, R. 2003b. Producción de herbáceas tras desbroces de matorral en el Parque Nacional de Doñana. Estudio sincrónico. VII Congreso Nacional de la Asociación Española de Ecología Terrestre, Barcelona.

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Soc. Herp. Fr., 38: 6–12.

Meffe, G. K. & Carroll, C. R., 1997. Genetics: Conservation of Diversity within Species. In: Principles of Conservation Biology: 161–201 (G. K. Meffe & C. R. Carroll, Eds.). Sinauer Associates, Sunderland.

Mellado, J., 1980. Utilización del espacio en una comunidad de lacértidos del matorral mediterráneo de la Reserva Biológica de Doñana. Doñana, Acta Vertebrata, 7(1): 41–59.

Moreno, S. & Villafuerte, R., 1995. Traditional management of scrubland for the conservation of rabbits Oryctolagus cuniculus and their predators in Doñana National Park, Spain.

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Doñana y su entorno próximo (Almonte). Siglos XVIII–XX. Monografías 49. Ministerio de Agricultura, Pesca de Alimentación.

Orians, G. H., 1997. Global Biodiversity I: Patterns and Processes. In: Principles of Conservation Biology: 161–201 (G. K. Meffe & C. R. Carroll, Eds.). Sinauer Associates, Sunderland.

Pérez–Mellado, V., 1981. Nuevos datos sobre la sistemática y distribución de Podarcis bocagei (Seoane, 1884) (Sauria, Lacertidae) en la Península Ibérica. Amphibia–Reptilia, 2: 259–265.

– 1997a. Podarcis bocagei (Seoane, 1884). En: Reptiles (A. Salvador, Coord.). Fauna Ibérica, vol. 10: 243–257 (M. A. Ramos et al., Eds.).

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– 1997b. Podarcis hispanica (Steindachner, 1870).

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Pérez–Mellado, V. & Galindo, M. P., 1986. Sistemática de Podarcis (Sauria, Lacertidae) ibéricas y norteafricanas mediante técnicas multidimensionales. Serie Manuales Universitarios, Univ. de Salamanca, Salamanca.

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Sá–Sousa, P., 2000. Distribución de la lagartija Podarcis carbonelli (Pérez–Mellado, 1981) en Portugal. Bol. Asoc. Herpetol. Esp., 11(1): 12–16.

– 2001. Comparative chorology between Podarcis bocagei and P. carbonellae (Sauria: Lacertidae) in Portugal. Rev. Esp. Herp, 15: 85–97.

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Sá–Sousa, P. & Harris, D. J., 2002. Podarcis carbonelli Pérez–Mellado, 1981 is a distinct species. Amphibia–Reptilia, 23: 459–468.

Sá–Sousa, P., González de la Vega, J. P. & Barnestein, J. A. M., 2001. Presencia de la lagartija Podarcis carbonelli en Andalucía. Bol. Asoc. Herpetol. Esp., 12(2): 77–79 Sousa, A. & García, P., 1998. Cambios históricos en el avenamiento superficial y la vegetación del Parque Natural de Doñana (Sector Abalario), Huelva. Ería, 46: 165–182.

Suso, J. M. & Llamas, M., 1990. El impacto de la extracción de aguas subterráneas en el Parque Nacional de Doñana. Estudios geol., 46: 317–345.

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– 1960. Vertebrados de las Marismas del Guadalquivir. Archivos del Instituto de Aclimatación, Vol. IX, CSIC, Almería.

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Egg–laying by the butterfly Iphiclides podalirius (Lepidoptera, Papilionidae) on alien plants: a broadening of host range or oviposition mistakes?

C. Stefanescu, J. Jubany & J. Dantart

Stefanescu, C., Jubany, J. & Dantart, J., 2006. Egg–laying by the butterfly Iphiclides podalirius (Lepidoptera, Papilionidae) on alien plants: a broadening of host range or oviposition mistake? Animal Biodiversity and Conservation, 29.1: 83–90.

Abstract Egg–laying by the butterfly Iphiclides podalirius (Lepidoptera, Papilionidae) on alien plants: a broadening of host range or oviposition mistakes?— Iphiclides podalirius is an oligophagous butterfly which feeds on plants of the Rosaceae family. In 2002 and 2005 in NE Spain, we recorded for the first time oviposition on two alien plant species, Cotoneaster franchetii and Spiraea cantoniensis. To ascertain if this unusual behaviour represents a broadening of host range or, alternatively, an oviposition mistake, larval performance on the new plants was investigated in the laboratory and compared with performance on the most common host plants used in the study area. Although larval performance on common hosts differed to some extent, the use of a wide range of plants of different quality at population level may in fact respond to the so-called "spreading of risk" strategy in variable environments. On the other hand, larval performance and survival to adulthood were so low on the two new hosts that our observations probably represent a case of maladaptive oviposition behaviour. This may be due to an evolutionary lag between the newly introduced plants and the insect, although other possible explanations are also taken into account.

Key words: Lepidoptera, Swallowtail butterflies, Iphiclides podalirius, Alien plants, Host plant range, Oviposition mistakes.

Resumen Ovoposición de la mariposa Iphiclides podalirius (Lepidoptera, Papilionidae) en plantas exóticas: ¿ampliación del rango de plantas nutricias utilizadas o errores de puesta?— Iphiclides podalirius es una mariposa oligófaga que se alimenta de plantas de la familia Rosaceae. En 2002 y 2005 se observó, por primera vez en el noreste de España, la puesta sobre dos plantas exóticas, Cotoneaster franchetii y Spiraea cantoniensis. Para poder discernir si este comportamiento inusual representa una ampliación del rango de las plantas nutricias utilizado o, por el contrario, se explica como un error de ovoposición, se investigó el desarrollo larvario sobre estas nuevas plantas en el laboratorio y se comparó con el desarrollo sobre las plantas nutricias más ampliamente utilizadas en la zona de estudio. Aunque se observaron diferencias significativas en el tiempo de desarrollo y el peso pupal entre las plantas nutricias habituales, la utilización de todas ellas por parte de una misma población podría responder a una estrategia de "repartir el riesgo" en un ambiente heterogéneo. Por el contrario, la supervivencia larval, el tiempo de desarrollo y el peso pupal fueron tan bajos en las dos nuevas plantas estudiadas que nuestras observaciones constituyen muy probablemente un ejemplo de comportamiento mal adaptado. Ello podría responder a la existencia de un desajuste evolutivo entre las plantas introducidas y el insecto, si bien otras posibles explicaciones son también consideradas y discutidas.

Palabras clave: Lepidoptera, Papiliónidos, Iphiclides podalirius, Plantas exóticas, Plantas nutricias, Errores de ovoposición.

(Received: 14 IX 05; Conditional acceptance: 11 XI 05; Final acceptance: 11 XII 05) Constantí Stefanescu, Butterfly Monitoring Scheme, Museu de Granollers Ciències Naturals, Francesc Macià, 51, E–08400 Granollers, Spain.– Jordi Jubany, Sant Martí, 1, 1r 1a, E–08470 Sant Celoni, Spain.– Jordi Dantart, Museu de Ciències Naturals de la Ciutadella, Passeig Picasso, s/n, E–08003 Barcelona, Spain.

Corresponding author: Constantí Stefanescu. E–mail: canliro@teleline.es

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction Colonisation of new hosts by phytophagous insects has received much attention in evolutionary and ecological research, as not only is it thought to represent one of the driving forces behind speciation processes, but it may also have marked consequences for the populations of both the insects and the plants concerned (e.g. Strong et al., 1984; Feder, 1998). For butterflies in particular, many studies have focussed on the incorporation of alien plants into the butterfly’s host plant range and the effects this has on aspects such as geographical or habitat range expansion (e.g. Gutiérrez & Thomas, 2000; Shapiro, 2002), population dynamics (e.g.

Tabashnik, 1980; Shapiro & Masuda, 1980) and the evolution of population adaptive traits (e.g. Singer et al., 1993; Camara, 1997).

Colonisation events are almost invariably initiated by ovipositing females which have to decide whether or not a plant is acceptable as an oviposition site. For most species, this decision involves two steps: firstly, and mainly based on visual and volatile chemical cues, she has to decide whether or not to land on the potential host plant; and, secondly, once she has landed on the plant, she has to decide whether or not to oviposit on a basis of the stimulants and deterrents perceived by chemoreceptors located in the tarsi, antennae, proboscis and ovipositor (Feeny et al., 1983; Renwick & Chew, 1994). However, oviposition must be accompanied by the capacity of eggs to hatch and larvae to develop into adults on the new host plant.

Observations of oviposition on new plant species must therefore be complemented by data on the development of immature stages before such behaviour can be regarded as indicative of the broadening of a butterfly’s range of hosts.

The present study was motivated by field observations of egg–laying by the scarce swallowtail butterfly Iphiclides podalirius (L.) on two alien plants that had not been previously reported in the literature as host plants. In this paper we describe the results of laboratory rearing experiments with both the most common host plants used by this butterfly and the two potential new hosts, and discuss the implications of our findings.

Material and methods Study species Iphiclides podalirius is an oligophagous butterfly belonging to the family Papilionidae that feeds on woody plants of the Rosaceae family. According to Tolman & Lewington (1997), species in the genus Prunus (including most cultivated species) are preferred in Europe, although other trees in the genera Pyrus, Crataegus, Sorbus and even Amelanchier are also used. In Catalonia (north–east Iberian peninsula), the following are the most common host plants: blackthorn Prunus spinosa L., fruit trees of

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the genus Prunus (P. dulcis (Miller), P. avium (L.), P. domestica L. and P. persica (L.)), pear tree Pyrus communis L. and hawthorn Crataegus monogyna Jacquin. More rarely, oviposition has been recorded on apple Pyrus malus L. and apricot trees Prunus armeniaca L. and, in other parts of Spain, on Sorbus aucuparia L. (M. L. Munguira, pers. comm.). However, data on larval development on these plants in the wild are not available.

Eggs are laid singly under the leaves of the plants mentioned above, with a predilection for those growing in hedges or in isolated stands. They hatch after one to four weeks, according to temperature. Caterpillars are highly sedentary, especially in the first instars. They spend most of their time on a silk cushion spun on the surface of the leaf selected as a resting site —normally the one on which the egg was laid— and move only to feed upon nearby leaves. Therefore, female choice when egg–laying is crucial for the subsequent survival of the larva.

I. podalirius overwinters in the pupal stage and is usually multivoltine in the Iberian Peninsula. The adult is highly mobile and populations have an open structure (i.e. the breeding areas have no distinct boundaries) as in many other Papilionidae (e.g. Lederhouse, 1983). Mating takes place at special sites selected by males for territorial establishment, mainly hilltops that may be far away from egg–laying sites.

Field observations Observations of oviposition on hitherto unrecorded plants were made at two different Catalan sites: Can Liro (Sant Pere de Vilamajor, 41º 41' 16 N 2º 23' 07 E, 310 m a.s.l.) and Montjuïc (city of Barcelona, 41º 21' 97 N 2º 09' 79 E, 95 m a.s.l.).

At Can Liro, a searching female was followed on 20 VIII 2002 until she detected a medium–sized shrub (ca. 2 m tall) of Cotoneaster franchetii Bois growing in isolation in a sunny hedgerow. She then engaged on a more stationary flight, carefully inspecting the outer branches before landing on one of them, curved her abdomen under the leaf and laid an egg. She immediately moved away in search of another potential host.

In the city of Barcelona, in the Parc de Petra Kelly (Montjuïc), a female was observed on 29 VIII 2002 carefully inspecting a shrub of Spiraea cantoniensis Lour. (ca. 2 m tall) and laying at least seven eggs on the underside of the leaves of the outer branches. In another visit three years later, on 26 VIII 2005, one additional egg and four first instar larvae were found on the same shrub. Finally, on 2 IX 2005, two first instar larvae and two eggs were also found on a small shrub (ca. 75 cm tall) of S. cantoniensis in Can Liro.

Both C. franchetii and S. cantoniensis are exotic shrubs of the family Rosaceae, widely used as ornamental plants in Catalan gardens and urban parks. C. franchetii is originally from western China and S. cantoniensis from eastern Asia.

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Rearing experiments

Results

Two "common–garden" experiments were designed to compare larval growth and survival on some of the most common host plants and also on Cotoneaster franchetii and Spiraea cantoniensis.

All the material used for these experiments was collected at Can Liro. In the first experiment (April– June 1998), larvae hatching from 88 naturally laid eggs on Prunus spinosa, P. domestica, P. persica and Crataegus monogyna were randomly assigned to these four host plants, and larvae were reared in an environmental chamber maintained at a constant temperature of 24ºC under a photoperiod of 16L:8D. In the second experiment (April–May 2005), a total of 72 eggs were collected from the same host plants and the corresponding larvae were divided among P. spinosa (used as a control as a host plant known to be optimum for larval growth), C. franchetii and S. cantoniensis. Rearing took place in the same environmental chamber, under the same conditions.

In both experiments, eggs belonged to many different females and represented a good sample of the genetic diversity of the population. Eggs about to hatch were placed individually on Petri dishes lined with moist paper and with fresh supplies of the food plant. Food for the larvae was collected from plants growing wild at Can Liro. In the case of C. franchetii, we used the same individual on which oviposition had actually been recorded on 2002.

Food plants were replaced every other day in the 1998 experiment and every day in the 2005 experiment to maintain humidity and leaf turgor. Furthermore, to prevent any chamber effect, the relative position of Petri dishes was changed every day in both experiments.

Larvae and pupae were checked daily and their performance was measured by means of three variables: survival to adulthood, development time and pupal weight (measured at the second day of the pupal stage). Wing length and sex of adult butterflies were also recorded.

Unfortunately, ovipositions on S. cantoniensis (recorded on three occasions) and, especially, on C. franchetii (recorded only once) were such rare events that we could not use eggs being laid on these alien plants in the field when performing our second rearing experiment. We were therefore unable to test to see whether possible individual variation in host–choosing tendencies (i.e. females preferring the new hosts) is correlated with physiological variation in larvae in host adaptation (but see Discussion). However, we tried to minimise this problem by collecting and rearing indoors on the same individual plant the six immature larvae found on S. cantoniensis in August 2005, and by comparing the outcome of this small–scale rearing experiment with the results of our second experiment.

Additionally, we marked the position of the eggs from the other two oviposition events on S. cantoniensis and recorded their fate in the wild in subsequent visits.

Larval survival Experiment 1 showed no significant differences in survival between the four common host plants ((2 = 4.62, df = 3, p = 0.20; fig. 1A). Survival ranged from 90.5% on P. spinosa to 63.6% on C. monogyna, with intermediate values of 77.3% and 69.6% for P. persica and P. domestica, respectively. It should be noted, however, that some of the larvae reared on C. monogyna produced crippled adults; given that this may be a common phenomenon in the wild, survival on C. monogyna may be somewhat overestimated in figure 1a.

Most mortality on these common hosts occurred in the final instars, especially in the prepupal and pupal stages. One exception was P. domestica, on which 3 out of 7 recorded losses corresponded to the first instar larvae.

In contrast with the previous results, we found striking differences in survival to adulthood between the common host plant P. spinosa and the two new tested plants ( (2 = 59.15, df = 2, p < 0.001; fig. 1B). Survival was nearly 100% on P. spinosa: all 22 larvae used in the experiment pupated successfully and only one pupa died. On the contrary, only 2 out of 25 larvae reached adulthood when reared on C. franchetii and none survived on S. cantoniensis. Most mortality on the new hosts occurred in the first instar: 100% on S. cantoniensis and 84% on C. franchetii. Of the four larvae that moulted successfully to the second instar on C. franchetii, two died in both the fourth and fifth instars.

Development time Although males tend to develop faster than females (C. Stefanescu & J. Jubany, unpubl. data; see also Lederhouse et al., 1982), a significant difference for total development time (in days) was only found between males and females reared on P. domestica; therefore, we decided to pool the data for both sexes in subsequent analyses.

Development time differed strongly between the four common hosts (F = 35.79, df = 3.61, p < 0.001; fig. 2A). However, most of this variation was accounted for by the lower development rate on C. monogyna, which was roughly 80% of that recorded on the other three hosts (which showed no significant differences in Tukey post–hoc multiple comparisons). On Prunus species, development time to adulthood ranged from 41.3 to 44 days, while on C. monogyna lasted 53.3 days.

Unexpectedly, development time on P. spinosa was shorter in the second experiment than in the first experiment (36.3 days vs. 43.1 days; t–test = 6.54, df = 38, p < 0.001). Perhaps this was due to the fact that the food was replaced every day instead of every other day in the second experiment, thus being overall of better quality. Moreover, the rearing experiment in 2005 took place towards the

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A

Survivorship (%)

100 80 60

P. spinosa P. persica

40

P. domestica 20

C. monogyna

0 L1

L2

L3

L4

L5

pupa

adult

B

Survivorship (%)

100 80 60

P. spinosa C. franchetii

40

S. cantoniensis 20 0 L1

L2

L3

L4 Life stage

L5

pupa

adult

Fig. 1. Survivorship curves of Iphiclides podalirius when reared: A. On the four common hosts Prunus spinosa (n = 21), P. domestica (n = 23), P. persica (n = 22) and Crataegus monogyna (n = 22) (experiment 1); and B. On Prunus spinosa (n = 22) and on the two new plants Cotoneaster franchetii (n = 25) and Spiraea cantoniensis (n = 25) on which oviposition was recorded in the wild (experiment 2). Symbols show the percentage of individuals alive at the beginning of each stage.

Fig. 1. Curvas de supervivencia para Iphiclides podalirius criado: A. Sobre cuatro plantas nutricias comunes Prunus spinosa (n = 21), P. domestica (n = 23), P. persica (n = 22) y Crataegus monogyna (n = 22) (experimento 1); B. Sobre Prunus spinosa (n = 22) y dos plantas nuevas Cotoneaster franchetii (n = 25) y Spiraea cantoniensis (n = 25), cuya ovoposición tuvo lugar en la naturaleza (experimento 2). Los símbolos representan el porcentaje de individuos vivos al inicio de cada fase.

beginning of the season and so the leaves of P. spinosa might have been in better condition than in 1998.

Most importantly, the second experiment showed that larvae reared on C. franchetii developed at a much lower rate than those reared on P. spinosa (fig. 2B). Thus, total development time to adulthood was almost twice as long for C. franchetii (65 days for C. franchetii vs. 36.3 days for P. spinosa; t–test = 13.03, df = 21, p << 0.001). These differences were observed in all the developmental stages except for the pupal stage (although only two pupae survived on C. franchetii), which lasted about the same for both hosts (t–test = 1.19, df = 21, p = 0.25; fig. 2B).

Pupal weight Given that I. podalirius males are regularly smaller in size and weight than females (as confirmed by highly significant t–tests in pair–wise comparisons for all hosts), pupal weights were analysed separately for both sexes.

Experiment 1 showed a significant effect of host in pupal weight for both males (F = 5.31, df = 3,32, p < 0.004; fig. 3) and females (F = 3.45, df = 3,32, p < 0.03; fig. 3). In general, larvae reared on P. domestica and, especially, on P. persica produced heavier pupae than those reared on P. spinosa and C. monogyna. Multiple comparisons indicated that, in females, the mass achieved on P. spinosa was

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A

60 P. spinosa 1998

50

P. domestica 40

P. persica C. monogyna

30 20 10 0

B

total

L1

L2

L3

L4

L5

pupa

80 70 P. spinosa 2005

60

C. franchetii

50 40 30 20 10 0

total

L1

L2

L3 Life stage

L4

L5

pupa

Fig. 2. Mean values (± SE) of total development time (from egg hatching to adult eclosion) and development time for each larval instar and the pupal stage: A. On the four common hosts Prunus spinosa, P. domestica, P. persica and Crataegus monogyna (experiment 1); B. On P. spinosa and C. franchetii (experiment 2). Sample sizes in experiment 1: P. spinosa, n = 21 for L1–L5, n = 19 for pupa and total; P. domestica: n = 19–20 for L1–L5, n = 16 for pupa and total; P. persica: n = 20–21 for L1– L5, n = 16–17 for pupa and total; C. monogyna: n = 18–21 for L1–L5, n = 14 for pupa and total.

Experiment 2: P. spinosa: n = 22 for L1–L5, n = 21 for pupa and total; C. franchetii: n = 4 for L1–L3, n = 3 for L4, n = 2 for L5, pupa and total.

Fig. 2. Valores medios (± EE) del tiempo total de desarrollo (desde la eclosión del huevo hasta la eclosión del adulto) y tiempo de desarrollo para cada fase larvaria y la de pupa: A. Sobre las cuatro plantas nutricias comunes Prunus spinosa, P. domestica, P. persica y Crataegus monogyna (experimento 1); B. Sobre P. spinosa y C. franchetii (experimento 2). Tamaños de la muestra en el experimento 1: P. spinosa: n = 21 para L1–L5 y n = 19 para pupa y total; P. domestica: n = 19–20 para L1–L5, n = 16 para pupa y total; P. persica: n = 20-21 para L1–L5, n = 16–17 para pupa y total; C. monogyna: n = 18–21 para L1–L5, n = 14 para pupa y total. Experimento 2: P. spinosa: n = 22 para L1–L5, n = 21 para pupa y total; C. franchetii: n = 4 para L1–L3, n = 3 para L4, n = 2 para L5, pupa y total.

significantly lower than on the other three hosts, while in males it was lower on C. monogyna and P. spinosa than on P. persica.

There were no differences in pupal mass on P. spinosa between experiments 1 and 2. On the other hand, pupal weights of the only two males

that survived on C. franchetii (0.54 and 0.64 g) were much lower than those values recorded on P. spinosa (fig. 3). Despite the very small sample size, a pair–wise comparison indicated that the observed difference cannot be explained by chance (t–test = 3.24, df = 8, p = 0.012).

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Females Males

Pupal weight (g)

1,25

1

0,75

0,5 P. domestica

P. persica

C. monogyna P. spinosa 1998

P. spinosa 2005

C. franchetii

Fig. 3. Pupal weights (± SE) of males and females reared on the four common hosts Prunus spinosa (data shown for experiments 1 and 2), P. domestica, P. persica and Crataegus monogyna, and the alien plant Cotoneaster franchetii.

Fig. 3. Pesos de las pupas (± EE) de los machos y las hembras criados sobre las cuatro plantas nutricias Prunus spinosa (se incluyen los datos para los experimentos 1 y 2), P. domestica, P. persica y Crataegus monogyna, y la planta exótica Cotoneaster franchetii.

Discussion Iphiclides podalirius is an oligophagous species, feeding on a wide range of plants belonging to the Rosaceae family. The diversity of host plants used

by I. podalirius is maintained at a local scale, in what Wiklund & Ahrberg (1978) have termed a polyphagic strategy within the species’ oligophagy.

This strategy might seem somewhat puzzling in view of the findings of our laboratory experiment, showing significant differences in larval performance between some of the most commonly used hosts. Thus, it is apparent that Crataegus monogyna is a poorer host than Prunus spinosa, P. domestica and P. persica and larvae feeding on this plant tended to have lower survival rates, to develop at a slower rate and to produce generally smaller pupae. On the other hand, host quality was similar in the three Prunus species. Although females achieved lower pupal weights on P. spinosa than on P. persica and P. domestica, the predictable loss of adult fecundity (e.g. Hinton, 1981, but see Leather, 1988) might be compensated by the highest survival to adulthood recorded on the former host.

It is possible that there exists a correlation between the host plant preference of ovopositing females and larval physiological variation in host adaptation that went unnoticed in our "common garden"’ experiment. However, this seems unlikely in a species that uses a variety of hosts

sympatrically and shows an open population structure and a non–resource mating system (i.e. hill– topping behaviour). Under this scenario, gene flow among individuals using different hosts is predictably too high to allow a host–associated differentiation within a population. Moreover, although experiments on oviposition preference have not yet been conducted (and thus no hierarchy of oviposition preference has been established; cf.

Wiklund, 1981; Thompson, 1993), direct observations of egg–laying females in the wild seem to indicate that thresholds of acceptance of alternative plants are usually very low (C. Stefanescu, pers. obs.). For instance, consecutive oviposition events of individual females on two or three different hosts growing side by side in the same hedgerow are a common phenomenon.

We believe that the most plausible scenario to account for the use of a wide range of hosts of different quality at a local scale is provided by the so–called "spreading of risk" strategy in variable environments (Den Boer, 1968). In particular, considering that immature stages are subject to extremely high mortality rates due to predation and parasitism (Stefanescu, 1999, 2000; Stefanescu et al., 2003; see also Feeny et al., 1985), we suggest that females may achieve a greater success by ovipositing on many different plants, even if they are poor hosts.

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This rather generalist behaviour may help to explain the recent incorporation of the American native Prunus serotina in the host diet of a German population of I. podalirius (Landeck et al., 2000) and also our observations of egg–laying on the two alien plants C. franchetii and S. cantoniensis. However, larval performance on these two latter hosts was so low that we might ask if our observations do not represent, in fact, a case of maladaptive oviposition behaviour. Although survival to adulthood was recorded on C. franchetii, larval performance was extremely poor on this plant, at least when compared with that on a wide range of common hosts. Moreover, our rearing experiment seemed to indicate that S. cantoniensis is toxic to larvae, which invariably die in their first instar when feeding on this plant. This seems to be corroborated by the fact that not a single larva was found alive one week later in a careful inspection of the plants on which oviposition was naturally recorded in 2002 and 2005, and also by the death during their first instar —as occurred in all 25 larvae from our second experiment — of all five larvae collected on S. cantoniensis in 2005 and reared indoors. In light of these results, egg–laying on S. cantoniensis may be considered one more example to add to the list of oviposition mistakes documented in the literature (e.g. Chew, 1977; Larsson & Ekbom, 1995; Graves & Shapiro, 2003).

Many authors have discussed the apparent paradox of oviposition on non–hosts or on hosts that confer very poor offspring fitness (e.g. Courtney, 1982; Thompson, 1988; Mayhew, 1997; Nylin et al., 2000). In the context of the present study, a likely explanation is that an evolutionary lag exists between the newly introduced plants and the local insect. Indeed, because of the increasing spread of exotic plants throughout most of the world’s ecosystems, this has become a fairly common phenomenon (e.g. Graves & Shapiro, 2003). Given enough time, however, it is expected that the use of toxic or very poor host plants (such as S. cantoniensis and C. franchetii, respectively) will disappear as a result of natural selection: if oviposition preference responds primarily to selection, then the plants will be excluded from the diet; if the first–responding trait is larval performance, then the plants will be incorporated into the insect’s diet (Singer, 2003). As commented above however, in the case of I. podalirius gene flow between populations is so strong that it makes the existence of local adaptations, for example towards particular hosts, highly unlikely.

There are of course, other possible (not necessarily exclusive) explanations accounting for our observations. For example, low specificity in the oviposition preference hierarchy —as seems to be the case at least in some females of I. podalirius (see above)— may facilitate oviposition on low– ranked host plants or even lethal plants in the absence of the preferred hosts (cf. Wiklund, 1981).

This may be particularly likely in secondary habitats, such as urban areas and gardens, where

common host plants are scarce or non–existent and have been replaced by alien, but still phylogenetically related and chemically similar, plants. Although our observations in the city of Barcelona fit this scenario very well, oviposition on S. cantoniensis and C. franchetii in Can Liro, where preferred host plants are very abundant and commonly used by I. podalirius, points to some other explanation. In the case of C. franchetii, at least, it may be argued that the pressure to ‘spread the risk’ could be so strong as to favour oviposition on such a poor host. Future field experiments would enable us to test this hypothesis and help to elucidate whether this alien plant can be regarded as a true host for I. podalirius or not.

In a more general context, we believe that observations such as the ones reported here are of great interest in the study of the evolution of insects’ host range and add further data to the increasingly important phenomenon of colonisation of newly introduced plants by local fauna (cf. Strong et al., 1984; Nylin & Janz, 1999).

Acknowledgements Thanks are due to the Sant Celoni Town Council for providing laboratory facilities, to Àngel Romo (Institut Botànic de Barcelona) for identifying Cotoneaster franchetii, to Miguel L. Munguira, Sören Nylin and an anonymous referee for useful comments on the MS, and to Mike Lockwood for revising the English version.

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Animal Biodiversity and Conservation 29.1 (2006)

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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 29.1 (2006)

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.es/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@mail.bcn.es). 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. © 2006 Museu de Ciències Naturals

IV

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 fascículos recientes de la revista para seguir sus directrices.

Animal Biodiversity and Conservation 29.1 (2006)

V

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.es/ABC, thus assuring world–wide access to articles published therein.

All manuscripts are screened by the Executive Edi­ tor, 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@mail.bcn.es). The preferred format is a do­ cument 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 consi­deration 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.

© 2006 Museu de Ciències Naturals

VI

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 photographs) must be termed as figures, num­ bered 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.

VII

Animal Biodiversity and Conservation 29.1 (2006)

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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Send this order form by postal mail to: Lluïsa Arroyo

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

"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 29.1 (2006)

IX

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Animal Biodiversity and Conservation joins the recent worldwide Open Access Initiative of providing a permanent online version free of charge and access barriers.

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"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

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, Directory of Open Acces Journals (DOAJ), Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, índex de Sumaris Electrònics del Consorci de Biblioteques de Catalunya, 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, Recent Ornithological Literature, Red de Revistas Científicas Españolas (REVICIEN), Referatirnyi Zhurnal, Science Abstracts, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 29.1 (2006) ISSN 1578–665X

1–8 K. Beovides–Casas & C. A. Mancina Natural history and morphometry of the Cuban iguana (Cyclura nubila Gray, 1831) in Cayo Sijú, Cuba 9–18 A. R. M. Serrano & C. A. S. Aguiar Two new species of Typhlocharis Dieck, 1869 of the silvanoides group from Portugal (Coleoptera, Carabidae) 19–32 R. Kautenburger Impact of different agricultural practices on the genetic structure of Lumbricus terrestris, Arion lusitanicus and Microtus arvalis 33–41 A. Egea–Serrano, F. J. Oliva–Paterna & M. Torralva Amphibians in the Region of Murcia (SE Iberian peninsula): conservation status and priority areas 43–47 A. Smolis & J. B. Shvejonkova A new species of the genus Stachorutes Dallai, 1973 from Russia (Collembola, Neanuridae)

49–64 R. I. Ruiz–C. & C. Román–Valencia Osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972 65–71 X. B. Wu, H. Xue, L. S. Wu, J. L. Zhu & R. P. Wan Regression analysis between body and head measurements of Chinese alligators (Alligator sinensis) in captive population.

73–82 J. Román, G. Ruiz, M. Delibes & E. Revilla Factores ambientales condicionantes de la presencia de la lagartija de Carbonell Podarcis carbonelli (Pérez–Mellado, 1981) en la comarca de Doñana 83–90 C. Stefanescu, J. Jubany & J. Dantart Egg–laying by the butterfly Iphiclides podalirius (Lepidoptera, Papilionidae) on alien plants: a broadening of host range or oviposition mistake?