Animal Biodiversity and Conservation issue 27.2 (2004) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2004

and

Animal Biodiversity Conservation 27.2

Dibuix de la coberta de Jordi Domènech Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

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

Museu de Ciències Naturals Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 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 Xavier Domingo–Roura Univ. Pompeu Fabra, Barcelona, 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 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, 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 27.2, 2004 © 2004 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 27.2 (2004)

A new orthoclad species of Rheocricotopus Thienemann & Harnisch (Diptera, Chironomidae) from the Darjeeling–Sikkim Himalayas in India N. Hazra & P. K. Chaudhuri

Hazra, N. & Chaudhuri, P. K., 2004. A new orthoclad species of Rheocricotopus Thienemann & Harnisch (Diptera, Chironomidae) from the Darjeeling–Sikkim Himalayas in India. Animal Biodiversity and Conservation, 27.2: 1–4. Abstract A new orthoclad species of Rheocricotopus Thienemann & Harnisch (Diptera, Chironomidae) from the Darjeeling–Sikkim Himalayas in India.— The adults and pupa of a new species, Rheocricotopus rarispina are described from the Darjeeling–Sikkim Himalayas in India. The species is distinguished by the few spines on the thoracic horn, anal lobe without fringe and bristle–like L setae and presence of ovoid humeral pit, nine squamal setae, structure of anal point and triangular and subterminal crista dorsalis in the adult male. With this new species, the number of Indian species of the genus rises to six. Key words: Chironomidae, New species, Tiger Hill, Darjeeling, India. Resumen Una nueva especie de ortocladino de Rheocricotopus Thienemann & Harnisch (Diptera, Chironomidae) de Darjeeling–Sikkim, en el Himalaya indio.— En este trabajo se describen los ejemplares adultos y las crisálidas de una nueva especie, Rheocricotopus rarispina, procedente de Darjeeling–Sikkim, en el Himalaya indio. Dicha especie se identifica por la existencia de algunas espinas en el cuerno torácico, el lóbulo anal sin franja y sin setas parecidas a cerdas en forma de L, la presencia de una cavidad humeral ovoide, nueve setas escamosas, la estructura de la cresta anal y cresta dorsal triangular y subterminal en el macho adulto. Con ésta, el número de especies de origen indio del género asciende ya a seis. Palabras clave: Chironomidae, Nueva especie, Tiger Hill, Darjeeling, India. (Received: 9 IV 03; Conditional acceptance: 5 VI 03; Final acceptance: 17 VII 03) Niladri Hazra & P. K. Chaudhuri, Dept. of Zoology, Univ. of Burdwan, Burdwan 713 104, India.

ISSN: 1578–665X

Hazra & Chaudhuri

Introduction

Results

Rheocricotopus Thienemann & Harnisch is one of the best known orthoclad genera, established by Thienemann & Harnisch (1932) on the basis of pupa (Sæther, 1985). Five species of the genus are recorded in India (Chaudhuri et al., 2001), but their biology remains unknown except R. valgus Chaudhury & Sinharay (1983) of which some aspects of its ecology are studied by Hazra et al. (1998). Following investigation of the chironomid fauna in the Darjeeling–Sikkim Himalayas in India, two pupae and one male adult were identified as a new member of Rheocricotopus Thienemann & Harnisch. Descriptions and terminologies of the pupa and the adult are made after Langton (1991) and (Sæther, 1985).

Rhecricotopus (Psilocricotopus) rarispina n. sp. (figs. 1–6)

Material and methods Types are deposited in the National Zoological Collections (NZC), Calcutta, and will be forwarded to the Natural History Museum (BMNH), London.

Pupa (n = 2) Pale brown. Total length 3.95 mm. Cephalothorax: frontal seta weak, short 41 µm long on prefrons (fig. 1). Antennal sheath 960 µm long. Ocular field without any Postorbital (Po) seta. Median antepronotals 185 µm and 100 µm long, lateral antepronotal 100 µm long, other one small peg–like. Thoracic horn (fig. 2) 315 µm long, club-shaped, anterior end serrate, covered by sparse spinules. Thoracic horn ratio (Thr) 5.25; precorneal setae 3 (fig. 2); anterior seta fine, 90 µm long, median one stouter, prominent 189 µm long; posterior one fine, minute 41 µm long, all arranged in triangular fashion. Of 4 dorsocentrals (Dc) only Dc3 and Dc 4 grouped together; length of Dc1 78, Dc2 41, Dc3 26 and Dc4 59; distance between Dc1 and Dc2 89, between Dc2 and Dc3 52, and between Dc3 and Dc 4, 15. Prealar seta 1,37 µm long. Abdomen (fig. 3): tergite I without shagreen; tergites II–V with few shagreen; tergites VI–VIII with extensive shagreen; tergite IX with antero-

Figs. 1–3. Pupa of Rheocricotopus (Psilocricotopus) rarispina n. sp.: 1. Cephalic area; 2. Thoracic horn and precorneals; 3. Tergites of pupa. Figs. 1–3. Pupa de Rheocricotopus (Psilocricotopus) rarispina sp. n.: 1. Región cefálica; 2. Cuerno torácico y precorneal; 3. Terguito de la pupa.

Animal Biodiversity and Conservation 27.2 (2004)

Figs. 4–6. Adult male of Rheocricotopus (Psilocricotopus) rarispina n. sp.: 4. Wing; 5. Thorax; 6. Hypopygium. Figs. 4–6. Macho adulto de Rheocricotopus (Psilocricotopus) rarispina sp. n.: 4. Ala; 5. Tórax; 6. Hypopigium.

median shagreen. Pedes spurii A on sternite VI; pedes spurii B absent. Tergite II with rows of 24 hooklets. Number of caudal spines on tergites III–VII as: 18, 22, 24, 26, 25, 25; maximal length of caudal spines on tergites III–VIII as: 67, 70, 52, 52, 45, 45. Number of caudal spines on sternites V–VII as: 20, 18, 17; maximal length of caudal spines on sternites V–VII as: 34, 32, 18. Lateral (L) setae hair like on segments I–VIII as: 2, 3, 3, 3, 3, 3, 3, 3. Anal lobe elongated, fusiform 300 µ long and 300 µ wide without any fringe; anal macrosetae subequal, apically hooked, 270 µ long. Genital sac 330 µ long and 225 µ wide; Anal lobe ratio (ALR) 2.00, G/F 1.10. Male imago (n = 2) Total length 3.75 mm; wing length 1.96 mm; total length/wing length 1.91; wing length/length of profemur 2.20. Head: antennal ratio (AR) 0.93, ultimate

flagellomere 389 µm long. Temporal setae 2 including Inner vertical (IV) 0, Outer vertical (OV) 2 and Postorbital 0. Clypeus roughly with 14 setae. Maxillary palp brown, length of palpomeres (I–V): 35, 60, 156, 180, 345; third palpal segment with 3 short sensilla clavata. Cibarial pump 495 µm long. Tentorium 195 µm long and 30 µm wide. Head–antennal ratio (CA) 0.55, Head–palpal ratio (CP) 0.75. Thorax (fig. 4): antepronotum with 3 lateral antepronotals; humeral pit large, oval in shape; acrostrichals 9; dorsocentrals 10, uniserial; prealers 3; scutellum with 8 setae, unserial. Wing (fig. 5): venarum ratio (VR) 1.03, costal ratio (CR) 0.96; brachiolum with 1 seta; anal lobe absent; squama with 9 setae; R2+3 ending midway between the ends of R and R 4+5, Cu1 straight and ending distal to Fcu; R with 5 setae; costal extension 44 µm long; sensilla campaniformia 20.

Table 1. Length and proportion of leg segments: LR. Leg ratio; BV. Beiverhältnisse; SV. SchenkelSchiene–Verhältnis; BR. Bristle ratio. Tabla 1. Longitud y proporción de los segmentos de la pata: LR. Proporción de la pata; BV. Beiverhältnisse; SV. Schenkel-Schiene–Verhältnis; BR. Proporción de la cerda.

Length segment fe

ta1

ta2

ta3

ta4

888

1017

777

814

462

851

1017

592

296

ta5

444

333

240

222

148

0.76

2.41

2.86

2.95

0.57

4.03

5.5

2.7

222

111

0.58

3.39

4.35

3.6

Hazra & Chaudhuri

Legs (table 1): the spur of fore tibia 44 µm long, spurs of mid tibia 18 µm and 11 µm long, of hind tibia 48 µm and 26 µm long; width at apex of fore tibia 42 µm, of mid tibia 41 µm and of hind tibia 55 µm long; hind tibial comb with 12 setae, longest seta being 52 µm long and shortest seta 22 µm long; pseudospurs absent from all the legs. Hypopygium (fig. 6): Anal point tapering to a sclerotized point, 48 µm in length with 4 lateral setae on each side; tergite IX with 1 seta, laterosternite with 1 seta on each side; gonocoxite 226 µm long, inferior volsella prominent, triangular, slightly curved at the tip, setose; distance between two legs of lateral sternapodeme base is 133; phallapodeme 44 µm long, coxapodeme 48 µm; virga absent; gonostylus 85 µm long, crista dorsalis triangular and subterminal, megaseta 11 µm long. Hypopygium ratio (HR) 2.65, Hypopygium value (HV) 4.41. Holotype: { with pupa (reared) (type no. B.U. Ent. 249), West Bengal, Tiger Hill (Darjeeling), 06 III 1996, Coll. N. Hazra. Paratype: { with pupa (reared) data same as holotype; Sikkim: Selep, 08 III 1996, Coll. S. K. Pradhan. Discussion The name "rarispina" has been proposed due to presence of a few spinules on the thoracic horn of pupa of this new species. The adult and pupa appear to closely resemble Rheocricotopus (Psilocricotopus) tirolus Lehmann (1969) in absence of anal fringe and G/ F, but it is distinguished from the above by L setae of segments V–VIII as: 3, 3, 3, 3 and bristle–like. The male imago of R. (P.) frequens Bhattacharyay et al. (1991) shows similarities with the new species in thoracic chaeotaxy, AR, squamal setae and hind tibial comb, but the hypopygial features are quite different in the two species. In chaetotaxy of thorax, absence of distinct anal lobe of wing, well developed crista dorsalis and megaseta of gonostylys of the proposed species comes closer to Rheocricotopus (Psilocricotopus) himalayensis Chaudhuri & Sinharay (1983) and R.( P.) chapmani (Edwards). The following combination of features shows its distinctness from all other species of the subgenus Psilocricotopus: Pupa 1. Thoracic horn covered with few spinules; 2. Dc3 and Dc4 grouped together, distance between

them 15; 3. L setae of segments V–VIII as 3 : 3 : 3 : 3 and all bristle–like; 4. Anal lobe without fringe; 5. G/F 1.2). Male imago 1. Ovoid humeral pit; 2. R with 5 setae; 3. Anal point 52 µm long with 4 setae on each side. The proposed species belongs to the Chalybeatus –species group of Sæther (1985) on the basis of large ovoid humeral pit and may be considered to form a group with R. (P.) chapmani and R. (P.) tirolus Lehman (Lehman, 1969). Acknowledgements The authors are grateful to the Department of Science & Technology, Govt. of India, for financial assistance and to the Head of the Department of Zoology, University of Burdwan for laboratory facilities. References Bhattacharyay, S. A. A. & Chaudhuri, P. K., 1991. Orthoclads of tribe Orthocladiini (Diptera: Chironomidae) from India. Beitr. Ent. Berlin, 41: 333–349. Chaudhuri, P. K. & Hazra, N., 2001. A Checklist of chironomid midges (Diptera: Chironomidae) of the Indian subcontinent. Orient. Ins., 35: 335–372. Chaudhuri, P. K. & Sihnaray, D. C., 1983. A study on Orthocladiinae (Diptera, Chironomidae) of India. The Genus Rheocricotopus Thienemann and Harnisch. Ent. Basil., 8: 398–407. Hazra, N., Som, D. K. & Chaudhuri, P. K., 1998. Immatures of Rheocricotopus (Psilocricotopus) valgus Chaudhuri & Sinharay of Darjeeling Himalaya with notes on ecology (Diptera: Chironomidae). Annals Limnol., 34(1): 75–82. Langton, P. H. (Ed.), 1991. A Key to the pupal exuviae of West Palaearctic Chironomidae. Huntingdon, Cambridgeshire. Lehman, J., 1969. Die europaischen Arten der Gattung Rheocricotopus Thien. und Harn. Und drie neue Artvertreter dieser Gattung aus der Orientalis (Diptera: Chironomidae). Arch. Hydrobiol., 66: 348–381. Sæther, O. A., 1985. A Review of the genus Rheocricotopus Thienemann & Harnisch, 1932, with the description of three new species (Diptera: Chironomidae). Spixiana Suppl., 11: 59–108. Thienemann, A. & Harnisch, O., 1932. Chironomiden– Metamorphosen. IV. Die Gattung Cricotopus v. d. Wulp. Zool. Anz., 99: 138–143.

Animal Biodiversity and Conservation 27.2 (2004)

General bat activity measured with an ultrasound detector in a fragmented tropical landscape in Los Tuxtlas, Mexico A. Estrada, C. Jiménez, A. Rivera & E. Fuentes

Estrada, A., Jímemez, C., Rivera, A. & Fuentes, E., 2004. General bat activity measured with an ultrasound detector in a fragmented tropical landscape in Los Tuxtlas, Mexico. Animal Biodiversity and Conservation, 27.2: 5–13. Abstract General bat activity measured with an ultrasound detector in a fragmented tropical landscape in Los Tuxtlas, Mexico.— Bat tolerance to neotropical forest fragmentation may be related to ability by bats to use available habitats in the modified environmental matrix. This paper presents data on general bat activity (for three hours starting at dusk) measured with an ultrasound detector in a fragmented landscape in the region of Los Tuxtlas, Mexico. Bat activity was measured in continuous forest, forest fragments, forest–pasture edges, forest corridors, linear strips of vegetation, citrus groves, pastures and the vegetation present in local villages. The highest bat activity rates were recorded in the villages, in forest fragments and in linear strips of vegetation. The lowest activity rates were detected in pasture habitats. Data suggest that native and man–made arboreal vegetation may be important for sustaining bat activity in fragmented landscapes. Key words: Chiroptera, Tropical forest fragmentation, Bat conservation, Bat ultrasounds, Los Tuxtlas, Mexico. Resumen Actividad general en los murciélagos registrada mediante un detector de ultrasonidos en una zona de selva fragmentada de Los Tuxtlas (México).— La tolerancia de los murciélagos a la fragmentación de las selvas neotropicales parece estar relacionada con su capacidad para utilizar los hábitats disponibles en la matriz ambiental modificada. En este trabajo se presentan datos sobre la actividad general de los murciélagos (durante las tres horas siguientes al atardecer) medida con un detector de ultrasonidos en una zona con fragmentos aislados de selva de la región de Los Tuxtlas (México). La actividad de los murciélagos se midió en una zona de selva continua, fragmentos aislados de selva, límites de la selva con zonas de pastos, corredores de vegetación, cercas vivas, plantaciones de cítricos, pastizales y la vegetación presente en los asentamientos humanos. Las mayores tasas de actividad se registraron en los asentamientos humanos, fragmentos de selva y cercas vivas. Las tasas más bajas de actividad se registraron en los pastizales. Los datos sugieren que las zonas con vegetación arbórea autóctona e introducida por el hombre pueden constituir un factor importante para sostener la actividad de los murciélagos en los fragmentos aislados de selva. Palabras clave: Quirópteros, Fragmentación de la selva, Conservación de murciélagos, Ultrasonidos, Los Tuxtlas, México. (Received: 24 IV 03; Conditional acceptance: 27 VI 03; Final acceptance: 16 VII 03) A. Estrada & E. Fuentes, Estación de Biología "Los Tuxtlas", Inst. de Biología, Univ. Nacional Autónoma de México, Apdo. Postal 176, San Andrés Tuxtla, Veracruz, México.– C. Jíménez, Colegio de la Frontera Sur, San Cristóbal de las Casas, Chiapas, México.– A. Rivera, Colegio de la Frontera Sur, Chetumal, Quintana Roo, México. Corresponding author: A. Estrada. E–mail: aestrada@primatesmx.com ISSN: 1578–665X

Estrada et al.

Introduction Members of the order Chiroptera are of particular importance in neotropical rain forests because they constitute about 40–50% of mammal species, greatly influencing the species richness and diversity of mammals in these ecosystems and have, as a result of their feeding habits, an important impact on the ecology of pollen and seed dispersal (Fleming et al., 1972; Heithaus et al., 1975; Fleming, 1982; Heithaus, 1982; Bonaccorso & Gush, 1987; Fleming, 1988; Charles–Dominique, 1991; Medellín & Gaona, 1999). Insectivorous bats may play an important role in regulating the populations of some invertebrates in the tropical ecosystem (MCNAB, 1982). In spite of their mobility, neotropical bats seem to be sensitive to loss and fragmentation of their natural habitat, locally undergoing decreases in species diversity and size of populations (Gallard et al., 1989; Estrada et al., 1993; Brosset et al., 1996; Granjou et al., 1996; Schulze et al., 2000). Other studies suggest that bat tolerance to habitat loss and fragmentation may be related to an ability to traverse open areas to reach other forest fragments or other vegetation types and use resources within the matrix (Law et al., 1999; Schulze et al., 2000). However, documentation of bat activity in fragmented landscapes in the Neotropics is scanty. The few published studies available have been limited to trapping bats with mist nets and/or traps reporting presence or absence of species and describing aspects of bat assemblage structure and composition (Estrada et al., 1993; Brosset et al., 1996; Granjou et al., 1996; Cosson et al., 1999; Schulze et al., 2000; Estrada & Coates–Estrada, 2001a, 2001b, 2002). These studies have inferred activity of bats at various habitats from the number of bats captured at the sites investigated and have expanded our understanding of neotropical bat tolerance to habitat loss and fragmentation. However, to increase our understanding of bat responses to changes in the distribution of their natural habitat —additional evidence relating bat presence to bat activity at the habitats investigated is needed. Ultrasound detectors have been successfully used to study patterns of habitat use by bats in North America (Krusic et al., 1996; Thomas & Laval, 1988), in Britain (Vaughan et al., 1997), in New South Wales, Australia (Law et al., 1999) and in highly modified landscapes in Europe (Limpens & Kaptyen, 1991; Walsh & Harris,1996; Kalko & Schnitzler, 1993). The use of ultrasound detectors in the study of Paleotropical bats has been documented in several localities (Fenton & Thomas, 1980; Fenton, 1982). In the Neotropics, the use of ultrasound detectors has been restricted to a few inventories of bat vocal signatures (O´Farrel & Miller, 1997, 1999), to studies of assessment of intraspecific variation with respect to habitat and behavior and studies of location of food by frugivorous bats (Thies et al., 1998). The central goal of this paper is to present data on bat activity measured with an ultrasound detec-

tor in a series of habitats that are part of a fragmented landscape located in the northeastern section of the region of Los Tuxtlas in southern Mexico: continuous forest, isolated forest fragments, forest–pasture edges, forest corridors, linear strips of vegetation, citrus groves, pastures and in the vegetation present in local villages. The data reported herein expands on earlier work based on trapping bats with mist nets at some of these habitats. These data and the results presented here are aimed at assessing which landscape scenarios may favor persistence of bat species assemblages in areas where the forest has been fragmented (Estrada et al., 1993; Estrada & Coates–Estrada, 2001a, 2001b, 2002). Methods Study area The tropical rain forest of Los Tuxtlas, in southeastern Veracruz, Mexico, represents the northernmost limit of the lowland rainforests in the American continent. Bat diversity in these forests is high with about 50 species reported (Coates–Estrada & Estrada, 1986). Human activity in this region has converted large extensions of the original forest surface (2,500 km2) to pastures, but constellations of forest fragments have remained in the lowlands (Estrada & Coates–Estrada, 1996). Some of the pasture land is used to cultivate arboreal cash crops such as citrus and allspice. These crops appear sporadically as islands of vegetation amidst the pastureland. Weather monitoring stations in the area indicate a mean annual temperature of 27oC (range 20 to 28oC). Average annual rainfall is 4,900 mm but from March to May average monthly rainfall is 111.7 SD ! 11.7 mm and from June to February this average equals 486.25 SD ! 87.0 mm. Study habitats The sites in which we sampled bat activity were located in a 126 km2 landscape in the north–eastern section of the region of Los Tuxtlas where the altitudinal gradient ranges from sea level to about 500 m above sea level (fig. 1). The continuous tract of lowland rainforest comprised part of the land of the biological research station "Los Tuxtlas" of Universidad Nacional Autónoma de México (95o 00’ W, 18o 25’ N). The forest of this reserve (700 ha) is connected to about 4,000 ha of pristine rainforest that forms part of the Los Tuxtlas Biosphere Reserve. Three locations separated by 2.0 km within the continuous forest tract were used to sample bat activity. In the three locations in the interior of the continuous forest distance to the edge was 400–500 m. The forest–pasture edges consisted of three 1.0 km long sections of the edge that bordered the continuous forest tract in its northern boundary. These sections were separated from each other by about 1.5–2.0 km.

Animal Biodiversity and Conservation 27.2 (2004)

Gulf of Mexico

L F

C P

Lake P

E E

I I

F 1000 m

Fig. 1. Study sites in the region of Los Tuxtlas, Veracruz, Mexico. The fragmented landscape (forest fragments shown in black) north of the extensive forest tract that forms part of the biological field station Los Tuxtlas is shown: I. Forest interior sites; C. Corridors; E. Forest edges; F. Forest fragments; P. Pastures; L. Live fences; circles with a cross are villages and shaded squares are citrus groves. Fig. 1. Áreas de estudio en la región de Los Tuxtlas, Veracruz, México. Se muestran los fragmentos de selva (indicados en negro) al norte de la selva extensa que forma parte de la Estación de Biología Los Tuxtlas: I. Emplazamientos del interior de la selva; C. Corredores; E. Límites de la selva; F. Fragmentos de selva; P. Pastizales; L. Setos vivos; los círculos con una cruz indican los asentamientos humanos y los cuadrados sombreados corresponden a las plantaciones de cítricos.

The original lowland rainforest immediately north of the continuous forest was gradually converted to pasture lands between 1960–1970, but clusters of forest fragments have remained in the 126 km 2 area. Three forest fragments, 10, 30 and 80 ha in size and located about 1, 3 and 6 km from the continuous forest were used to sample bats with the ultrasound detector. The linear strips of vegetation running across the pastures were of two types. One consisted of three corridors of remnant rainforest along the sides of three streams while another consisted of three live fences. The former habitats had an average length of 1.2 ! 0.10 km and an average

width of 10.2 ! 3.5 m) and were located about 0.5–3 km from the forest edge sites. The residual forest vegetation at these sites was dominated by trees of the Lauraceae, Moraceae, Cecropiaceae, Boraginaceae and Fabaceae plant families. The sites had a few representatives of the forest palms Astrocaryum mexicanum and Bactris trichophylla, which are common in the understorey of undisturbed forest vegetation in this region (Bongers et al., 1988) reflecting the residual nature of the vegetation found at the site. The three live fence sites, formed by a single row of grown live posts of Bursera simaruba (Burseraceae) and Gliricidia sepium (Leguminosae) planted at one

Estrada et al.

Table 1. Number of bat passes recorded at each habitat investigated. Each habitat was sampled for 1,620 minutes: S. Sampling points; Cf. Continuous forest; E. Forest pasture–edge; F. Forest fragments; C. Corridors; L. Live fences; Ci. Citrus; V. Villages; P. Pastures. Tabla 1. Número de pases registrados en los hábitats investigados. En cada hábitat se realizó un muestreo durante 1.620 minutos: S. Puntos de muestreo; Cf. Selva continua; E. Límite de la selva con zonas de pasto; F. Fragmentos de selva; C. Corredores de vegetación; L. Setos vivos; Ci. Cítricos; V. Asentamientos humanos; P. Pastizales.

105

112

Total

664

879

1036

855

1038

957

1245

Mean

44.3

58.6

69.1

69.2

63.8

83.0

4.0

! SD

24.6

11.7

26.2

18.3

13.0

10.6

7.0

2.0

meter intervals a few years back by ranchers to hold the barbed wire, were separated from each other by about 2.5 km. The three citrus groves were located 2.5 km northeast of the continuous forest. These sites were rectangular in shape and each about 10 ha in size. The citrus trees arranged in rows were 3– 4 m in height and fruit productive. The vegetation on the ground consisted of grass actively grazed by cattle. The vegetation patches forming part of three villages were located at 2, 5 and 8 km from the continuous forest. The vegetation in these sites consisted of planted tree species such as B. simaruba, G. sepium, coconut palms, citrus trees, almonds, avocados, and various other ornamental and shade providing trees and non tree plants such as papayas and bananas that people planted in their yards and to fence their house lots. The pastures sites were three open areas about 100 ha in size located at 1, 2 and 6 km from the continuous forest. The pastures consisted of 10–15 cm high African star grass (Cynodon plectostachyus), grazed by free–ranging cattle.

Bat activity Bat activity was monitored at each site using a Pettersson ultrasound detector model D230 (Pettersson Elektronic AB, Upsala, Sweden) in the broadband frequency division mode (10–120 kHz). The directional microphone had a reach of about 25 m. At each site a 750 m long sinuous transect was set up and sampling points were marked at 50 m intervals for a total of 15 points. In the forest fragments the transects ran sinuously through the middle of each site. In the corridors and live fences the sampling transects ran under the shadow of the tree vegetation and under the crown of the row of trees, respectively. In the citrus groves, three parallel transects were set up, separated from each other by 100 m, about 250 in length each. In the villages, the transect was established along one of 2–3 existing streets. No street lamps were present in the villages only indoor houselights were used by the inhabitants. In the pasture sites, the transects ran in a straight line N–S for 750 m.

Animal Biodiversity and Conservation 27.2 (2004)

100 90

Passes/100min

80 70 60 50 40 30 20 10 0

C Sites

Fig. 2. Bat activity rates of bats (! SE), measured as passess/100 min with the ultrasound detector, at the habitats investigated. (For abbreviations see table 1.) Fig. 2. Tasa de actividad de los murciélagos (! EE), indicada como el número de pases cada 100 minutos en los hábitats investigados. (Para las abreviaturas ver tabla 1.)

Each site was visited three times between May and August of 2000. Echolocation calls were monitored at each site for three hours starting at dusk. At each of the 15 points in each site, we counted the number of bat passes, defined as a sequence of m 2 echolocation calls including feeding buzzes (Thomas, 1988; Law et al., 1999) for a total of 12 minutes. The ultrasound detector was held at elbow height at a 45 degree angle with respect to the ground and aerial space at each cardinal point was scanned for three minutes. Samples were conducted on moonless nights and on non rainy days at all sites. Measures of habitat clutter To obtain an indirect measure of vegetation clutter at the habitats investigated, a light meter at knee height was used to measure the amount of light illuminating the ground at each of the 15 points in each site where sampling of bat activity was carried out with the ultrasound detector. Readings were taken between 12:00–14:00 hrs on sunny and clear days. Data were expressed as mean number of lumens per square meter. Data analysis Bat activity recorded with the ultrasound detector was standardized as number of passes per 100 min (Thomas, 1988). The non–parametric Kruskal–Wallis (data could not be transformed to fit a normal distribution) or the Mann–Whitney tests were used to determine whether bat activity differed among

habitats and between pairs of habitats (MINITAB for Windows, version12). Results A total of 216 hours was accumulated monitoring the activity of bats at all habitats (1620 min per habitat) and a total of 6,734 passes was recorded. Bat activity was not homogeous among habitats (Kruskal– Wallis H = 62.97; df = 7; P = 0.001) (table 1). The lowest bat activity rates were recorded at the pasture habitats (3.7 passes/100 min) (fig. 2). The highest bat activity rates (76.9 passes/100 min) were recorded in villages followed by the forest fragments, live fences, citrus groves, forest pasture edges, corridors and the continuous forest sites (fig. 2). A pair–wise comparison in activity rates between the continuous forests and the non–pasture habitats showed that non–significant differences in bat activity rates existed only with respect to the forest pasture-edge and the corridors (U–test P > 0.05). In all other cases, bat activity rates were significantly higher at the other habitats than in the continuous forest (U–test P = 0.002) All habitats differed significantly in activity rates from the pasture sites (U–test P < 0.001 in all cases) (table 1). Measures of habitat clutter Light meter readings (lumens/m2) were lower at the forest sites than at the other habitats investi-

Estrada et al.

1600 1400

80 70

1200

1000

50 800

600

400

200

L Sites

Mean passes/100 min

Mean lumens/m2

Mean number of lumens Mean number of passes

Fig. 3. Reading (lumens/m2) recorded with a lightmeter at the sites investigated. (For abbreviations see table 1.) Fig. 3. Luminosidad (lúmenes/m2) registrada por medio de un exposímetro en los emplazamientos investigados. (Para las abreviaturas ver tabla 1.)

gated. Average light meter readings were 196 lumens/m2 and 442 lumens/m2 in the corridors and live fences, respectively (fig. 3). Higher readings were recorded at the villages and the citrus groves, 812 lumens/m2 and 840 lumens/m2, respectively. Maximum readings were obtained at the pasture sites (1200 lumens/m2). Bat activity roughly paralleled the observed increases in luminosity from forest to the villages, dropping sharply in the pastures (fig. 3). Discussion While a catalogue of vocal signatures for the bat species present in Los Tuxtlas does not yet exist, mist netting of bats in the continuous forest, forest fragments, live fences and citrus grove sites used in this study indicated the presence of a rich species pool represented by 39 species of bats (about 80% of species historically recorded; Estrada et al., 1994). The proportion of bat species captured with mist nets in the habitats sampled with the ultrasound detector were 77% in the continuous forest, 85% in forest fragments, 46% in citrus groves, 31% in live fences and zero percent in pastures. This indicates a high diversity of bat species in the arboreal habitats investigated and the likelihood that bat activity measured with the ultrasound detector reflects the activity of many of the bat species identified with the use of mist nets in these habitats. For example, C. brevicauda, S. lilium, Artibeus spp., Dermanura spp. and G. soricina dominant bat species in continuous forest and forest fragments are fast fliers and have been reported to forage in or above the canopy and

in open spaces (Brosset et al., 1996) and frequent the edges and interior of small forest fragments (Fleming, 1988), live fences and citrus groves (Estrada et al., 1993). Even bat species with more specialized feeding habitats and habitat requirements (e.g., Leptonycteris curasoae, S. ludovici, V. spectrum; Fleming, 1982) are present in these habitats (Estrada et al., 1994; Estrada & Coates–Estrada, 2001a, 2001b, 2002). Our study showed that bat activity rates were higher in the non–pasture habitats examined than in the continuous forest. While habitat clutter in the continuous forest habitats may have influenced detection of echolocation calls produced by bats, our results nevertheless suggest that bats living in fragmented landscapes in Los Tuxtlas, regularly use linear strips of vegetation, forest fragments and human–made vegetation patches (including the vegetation of home gardens in human settlements) (Estrada et al., 1993; Estrada & Coates–Estrada, 2001a, 2001b). As feeding rates of bats have been reported to be positively correlated with aerial insect densities (Racey & Swift, 1985), areas where bats may achieve high rates of activity may be good quality habitats for movement and/or foraging, and deserve protection (Vaughn et al., 1997). The high activity rates of bats recorded at the forest fragments suggest that even small or poor quality remnants constitute a significant conservation resource for bats (Shafer, 1995; Law et al., 1999). The intense bat activity recorded in the live fence sites and in the corridors of residual forest vegetation suggests the presence of resources used by bats in these habitats. It has been noted that wind speed affects the distribution of nocturnal insects (Peng et al., 1992a,

Animal Biodiversity and Conservation 27.2 (2004)

1992b) and linear strips of vegetation such as hedgerows and wind breaks affect insect distribution, probably because of their effect on local wind speed (Lewis, 1969). Bats are usually loyal to foraging sites and may find new roosts if the sites where roosts were located disappear (Brinham & Fenton, 1986), suggesting that the conservation of foraging and flyway habitats such as corridors of residual forest vegetation and live fences is important. The presence of linear strips of residual forest or of man–made vegetation may also reduce isolation distances between forest fragments and between these habitats and other types of vegetation patches, a feature that may facilitate movement of bats in the landscape and may also function as foraging trap–lines for bats (Fleming, 1982; Estrada et al., 1993; Estrada & Coates– Estrada, 2001a). Similarly, the high bat activity rates recorded at the forest–pasture edges may stress the importance of linear landscape elements to bats for commuting and navigating across the landscape (Krusic et al., 1996). Some fruit–eating neotropical bats use echolocation to locate their food, as studies have shown for species of Carollia (Thies et al., 1998) and Phyllostomus (Kalko & Condon, 1998). It is thus possible that some of our records in the linear strips of vegetation and at the forest–asture edge may be of fruit–eating bats tracking food resources such as fruits of Piper and Solanum, plants that become established in these environments (Fleming, 1988). Readings of light illumination at the sites investigated suggest less cover is available at live fences, citrus groves and villages when compared to the other non–pasture habitats studied. Increases in bat activity roughly paralleled the presence of less vegetation clutter in these habitats, suggesting that, in spite of greater exposure of bats to potential predators (e.g., bat falcons, Falco rufigularis and owls, Tyto alba) in these habitats, bats were active in these sites. While bats may face potential predation and higher time and energy expenditure due to exposure and distances flown when visiting different habitat patches in the landscape, by reaching various vegetation patches available in the matrix, outside the forest fragment in which they reside, they may encounter a greater variety of habitats in which to find resources and meet survival requirements, avoiding over exploitation of resources and increased competition (Offerman et al., 1995). General implicatons The use of ultrasonic detectors to record bat activity may detect soft–calling species (whispering bats, e.g., Phyllostomidae) less frequently than loud calling species (e.g. Pteronotus parnelli). In addition, these devices do not provide data that can be translated directly into estimates of population density (Thomas, 1988). However, ultrasound detectors provide a relatively unbiased index of levels of use among habitats (Thomas & Laval, 1988) and, in contrast to ground level nets, the devices may detect

canopy and high flying taxa (O´Farrel & Miller, 1999). The low record of bat activity in the pasture habitats corresponds well with the lack of captures of bats using mist nets in these habitats (Estrada et al., 1994). Although we observed bats in pastures at dawn or dusk but flying high (> 20 m) toward scattered groups of forest fragments), it is possible that some species may forage on insects in high grass. Two factors may mitigate against use of pastures by bats. One is the scarcity of food resources (fruit/ insects) and lack of roost sites in these habitats, while the other could be potential predation. During the study, bat falcons (Falco rufigularis) and owls (Tyto alba) were observed preying on bats at dusk as they flew out of forest fragments into the pasture, suggesting that exposure to predators may be greater in these habitats (see Fenton & Thomas, 1980). Surely, the ability to fly and to traverse open areas using patches of native and introduced vegetation as well as linear strips of vegetation, seems to allow bat species more flexibility in their responses to habitat fragmentation as compared to non–flying mammals (Estrada et al.,1993; Estrada et al., 1994; Cosson et al., 1999; Schulze et al., 2000). The high diversity of the bat assemblages still present in the investigated landscape, attested by our ealier studies using mist nets, and the data presented here suggest that bats not only pass through native and man–made habitats in the landscape, but that they are active in these habitats searching and harvesting food, thus enhancing their capacity to persist in landscapes modified by man and in which arboreal agricultural vegetation is an important component (Laurance, 1991; Estrada & Coates–Estrada, 1994; Walsh & Harris, 1996; Turner, 1996; Law et al., 1999). Clearly, in this scenario, conservation of isolated forest fragments is incomplete and consideration must also be given to the value, as stepping–stones and as foraging sites, of other types of vegetation in the matrix, including the vegetation found in the home gardens of local villages, for bats (Lindenmayer & Nix, 1993; Neiman et al., 1993; Turner, 1996; Estrada & Coates– Estrada, 2002). The fact that not only insectivorous bats and those that feed on vertebrates use echolocation to locate their food, but also that frugivorous bats employ these tactics (Thies et al., 1998; Kalko & Condon, 1998) suggests that bat activity in the human–modified landscape investigated involves a great number of bat species that differ in dietary and habitat requirements. These species may be important in the natural control of insect populations as well as in the natural process of forest regeneration via the pollen and seed dispersal services bat species provide for forest plants in human–modified landscapes. Acknowledgements We are grateful to the Scott Neotropic Fund of the Cleveland Metropark Zoo for support and to the Universidad Nacional Autónoma de México for additional support and logistical aid.

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1993.The role of riparian corridors in maintaining regional biodiversity. Ecological Applications, 2: 209–212. O´Farrel, M. J. & Miller, B. W., 1997. A new examination of echolocation calls of some neotropical bats (Emballonuridae and Mormoopidae). Journal of Mammalogy, 78: 954–963. – 1999. Use of vocal signatures for the inventory of free–flying neotropical bats. Biotropica, 31: 507–516. Offerman, H. L., Dale, V. N., Pearson, S. M., Bierregaard, O. Jr. & O’Neill, R. V., 1995. Effects of forest fragmentation on neotropical fauna: current research and data availability. Environmental Review, 3: 190–211. Peng, R. K., Fletcher, C. R. & Sutton, S. L., 1992a. The effects of microclimate on flying dipterans. International Journal of Bioeteorology, 36: 69–76. Peng., R. K., Sutton, S. L. & Fletcher, C. R., 1992b. Spatial and temporal distribution patterns of flying Diptera. Journal of Zoology London, 228: 329–340. Racey, P. A. & Swift, S. M., 1985. Feeding ecology of Pipistrellus pipistrellus (Chiroptera, Vesper– tilionidae) during pregnancy and lactation. I. foraging behaviour. Journal of Animal Ecology, 54: 205–215. Schulze, M. D., Seavy, N. E. & Whitacre, D. F., 2000.

A comparison of phyllostomid bat assemblages in undisturbed neotropical forest and in forest fragments of a slas–and–burn farming mosaic in Petén, Guatemala. Biotropica, 32: 174–184. Shafer, C. L., 1995. Values and shortcomings of small reserves. Bioscience, 45: 80–88. Thies, W., Kalko, E. & Schmitzler, H. U., 1998. The roles of echolocation and olfaction in two neotropical fruit–eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behavioral Ecology and Sociobiology, 42: 397–409. Thomas, D. W., 1988. The distribution of bats in different ages of Douglas–fir forest. Journal of Wildlife Management, 52: 619–626. Thomas, D. W. & Laval, R. K., 1988. Census and survey techniques. In: Ecological and behavioral methods for the study of bats: 77–87 (T. H. Kunz, Ed.). Smithsonian Institution Press, Washington, DC. Turner, I. M., 1996. Species loss in fragments of tropical rain forest: a review of the evidence. Journal of Applied Ecology, 33: 200–209. Vaughan, N., Jones, G. & Harris, S., 1997. Habitat use by bats (Chiroptera) assessed by means of a boad–band acoustic method. Journal of Applied Ecology, 34: 716–730. Walsh, A. L. & Harris, S., 1996. Foraging habitat preferences of vespertilionid bats in Britain. Journal of Applied Ecology, 33: 508–518.

"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 27.2 (2004)

Patrones de diversidad de la fauna de mariposas del Parque Nacional de Cabañeros y su entorno (Ciudad Real, España central) (Lepidoptera, Papilionoidea, Hesperioidea) A. Jiménez–Valverde, J. Martín Cano & M. L. Munguira

Jiménez–Valverde, A., Martín Cano, J. & Munguira, M. L., 2004. Patrones de diversidad de la fauna de mariposas del Parque Nacional de Cabañeros y su entorno (Ciudad Real, España central) (Lepidoptera, Papilionoidea, Hesperioidea). Animal Biodiversity and Conservation, 27.2: 15–24. Abstract Diversity patterns of the butterfly fauna of the Parque Nacional de Cabañeros and its surroundings (Ciudad Real, Central Spain) (Lepidoptera, Papilionoidea, Hesperioidea).— The butterfly species richness and faunistic composition in six plots with different land uses and dissimilar environmental diversity is studied in the Parque Nacional de Cabañeros and its surroundings (Ciudad Real, Central Spain). The holm–oak forest is the richest sampling plot, with a butterfly species composition that clearly differs from the rest of more humanized sampling plots. The pine plantation has the lowest values of species richness and abundances, with a faunistic composition quite similar to those of the sampling plots with a dominance of hostile habitats for butterflies (grasslands and crops), so the need to create clearings is emphasised. The importance of environmental diversity in humanized habitats and the need for proper management and conservation of woodlands is stressed in order to conserve butterfly biodiversity. Key words: Lepidoptera, Parque Nacional de Cabañeros, Central Spain, Biodiversity, Land uses, Habitat improvements. Resumen Patrones de diversidad de la fauna de mariposas del Parque Nacional de Cabañeros y su entorno (Ciudad Real, España central) (Lepidoptera, Papilionoidea, Hesperioidea).— Se estudia la riqueza en especies de mariposas y la composición faunística en seis parcelas representativas de distintos usos del monte mediterráneo y con distinto valor de diversidad ambiental, en el Parque Nacional de Cabañeros y su entorno (Ciudad Real, España central). La parcela representativa del bosque mediterráneo resulta ser la más rica en mariposas y presenta una composición faunística que la diferencia claramente del resto de parcelas con mayor grado de antropización. La parcela representativa de la plantación de coníferas es la más pobre en cuanto a número de especies e individuos, y su composición faunística la asemejan a las parcelas más hostiles para las mariposas, como son las parcelas con dominancia de zonas para pastos y agrícolas. Por ello, se recalca la necesidad de crear espacios aclarados para mejorar estas masas arbóreas y hacerlas más atractivas para la fauna lepidopterológica. Se pone en relevancia la importancia de la diversidad ambiental en los hábitats antropizados y la necesidad de una gestión y conservación adecuadas de zonas boscosas de cara a mantener la biodiversidad lepidopterológica. Palabras clave: Lepidoptera, Parque Nacional de Cabañeros, España central, Biodiversidad, Usos del territorio, Mejora de hábitats. (Received: 18 II 03; Conditional acceptance: 6 V 03; Final acceptance: 6 X 03) Alberto Jiménez–Valverde*, José Martín Cano & Miguel López Munguira, Univ. Autónoma de Madrid, Dept. Biología (Zoología), 28049 Cantoblanco, Madrid, España (Spain). *Dirección actual: Museo Nacional de Ciencias Naturales (CSIC), Dept. Biodiversidad y Biología Evolutiva, c/ José Gutiérrez Abascal 2, 28006 Madrid, España (Spain). E–mail: mcnaj651@mncn.csic.es ISSN: 1578–665X

Jiménez–Valverde et al.

Introducción Las principales causas del declive de la riqueza de mariposas en Europa son los cambios en el uso y manejo del territorio (New et al., 1995) y la pérdida de hábitats favorables (Mousson et al., 1999; Swaay & Warren, 1999). A pesar del aumento del número de espacios protegidos en las últimas décadas, la desaparición de especies de mariposas sigue un ritmo que Swaay & Warren (1999) consideran progresivo. Este hecho, general en la vida silvestre, probablemente se acentúe en el caso de las mariposas debido, entre otras causas, a que los planes de manejo de los espacios protegidos no tienen en cuenta a su fauna lepidopterológica (Rodríguez González, 1991). Para evitar esto es necesario un conocimiento de los patrones de diversidad de mariposas en las reservas, identificando cómo influyen los diferentes usos del territorio en estos patrones. Además, al tratarse de animales fitófagos de requerimientos bastante específicos pueden, dentro de unos límites razonables, reflejar las necesidades ecológicas de otros grupos de artrópodos (Martín Cano et al., 1996). Los montes del entorno de Cabañeros empezaron a sufrir una intensa presión antrópica a partir del siglo XIII. La ganadería, la agricultura y las actividades relacionadas con el carboneo provocaron la transformación de un territorio con una eminente vocación forestal (V.V.A.A., 1997). Fruto de estas actividades es el actual paisaje del Parque Nacional de Cabañeros, donde alternan formaciones boscosas, matorrales y pastos con distintos grados de desarrollo y complejidad estructural. En su entorno, fuera de los límites del Parque, los terrenos destinados a labores agrícolas y de pastoreo contribuyen al mosaicismo paisajístico tan característico de este territorio del centro peninsular. El trabajo de Jiménez–Valverde et al. (2002) aporta los primeros datos sobre la fauna de mariposas del Parque Nacional de Cabañeros y de su entorno. Los autores presentan un listado faunístico, procedente de muestreos sistemáticos y ocasionales, con un total de 49 especies, y estudian la fenología de la lepidopterocenosis destacando su marcado carácter mediterráneo, con mínimos de riqueza y abundancia durante la sequía estival. En este trabajo nos planteamos, como principal objetivo, determinar la variación en los patrones de diversidad y composición de mariposas en relación con los principales hábitats presentes en el Parque Nacional de Cabañeros y su entorno. Material y métodos El Parque Nacional de Cabañeros, declarado como tal en el año 1995, se sitúa en el sistema orográfico de los Montes de Toledo, entre las provincias de Ciudad Real y Toledo. El Parque se encuentra en el piso mesomediterráneo medio-superior de ombroclima seco–subhúmedo. Se eligieron seis parcelas de 1 km2 en el conjunto de las cuales

0 3 km

Navas de Estena

Toledo

2 3 6 Alcoba

Pueblonuevo de Bullaque

Ciudad Real Fig. 1. Mapa del Parque Nacional de Cabañeros con la situación de las parcelas de muestreo. Fig. 1. Location of the sampling plots in the Parque Nacional de Cabañeros.

estuvieran representados los ecosistemas y usos del territorio más característicos del Parque Nacional y de su entorno (ver fig. 1): Parcela 1: encinar (Quercus ilex ballota) situado sobre una pedriza, en una ladera de umbría, ya que es en estas situaciones donde se localizan los bosques mediterráneos mejor conservados de la región analizada (Costa Tenorio et al., 1998; V.V.A.A., 1997). Parcela 2: plantación de Pinus pinaster que data de finales de los años 60. Estrato arbustivo formado, básicamente, por Erica arborea. Un cortafuegos en el interior de la plantación presenta brotes de Cistus ladanifer y E. arborea Parcela 3: en esta parcela predomina el jaral de C. ladanifer. también hay una zona de raña (pastizales adehesados, ecosistema característico del Parque Nacional) y de tierras aradas. Parcela 4: dominada por tierras dedicadas a cultivos con zonas de pastos y jaral y una zona más húmeda con presencia de un arroyo temporal. Parcela 5: extensa zona adehesada en la que actualmente pasta ganado ovino. Existe un retazo de encinar. Parcela 6: esta parcela contiene una mezcla de distintos usos: tierras aradas, barbechos, jaral y raña. Los porcentajes de cada hábitat en cada parcela se exponen en la tabla 1. Estas proporciones han sido empleadas para calcular un índice de diversidad ambiental para cada parcela utilizando para ello el índice de diversidad de Shannon–Wiener (tabla 1). Se realizaron muestreos semanales, desde abril hasta septiembre del año 2001, mediante el conteo de las mariposas observadas dentro de los prime-

Animal Biodiversity and Conservation 27.2 (2004)

Tabla 1. Descripción de las parcelas especificando la proporción que ocupa cada hábitat en cada una de ellas. Se ha empleado el índice de diversidad de Shannon–Wiener para calcular la diversidad ambiental de cada parcela. Table 1. Description of the sampling plots pointing out the proportion of each habitat in each sampling plot. The Shannon–Wiener index has been used to calculate the environmental diversity of each sampling plot.

Parcela

Hábitats representados y proporción relativa de cada uno sobre el total

Bosque Querqus ilex ballota (93%); pedreras (3%)

Plantación Pinus pinaster (90%); cortafuegos (10%)

0,47

Jaral (60%); raña (25%); tierras aradas (15%)

1,35

Tierras aradas y cultivadas con maiz (55%); pastos de ribera (20%); jaral (10%); encinar adehesado (15%)

1,68

Encinar adehesado para pastos (75%); encinar (25%)

0,81

Jaral (35%); raña (25%); barbechos (15%); tierras aradas (25%)

1,94

ros 5 m por delante del investigador y 2.5 m a cada lado suyo, a lo largo de seis transectos (uno en cada parcela; fijos durante todo el estudio) de 1 km de longitud, siguiendo la metodología de Pollard (1977). En total se han llevado a cabo 144 transectos. En la parcela 1 los muestreos se comenzaron en el mes de mayo. Las mariposas eran identificadas al vuelo, capturando y volviendo a soltar las de difícil identificación y estudiando en el laboratorio los caracteres morfológicos y/o la genitalia de los individuos que así lo requiriesen. Para la denominación de las especies se ha seguido a Karsholt & Razowski (1996), excepto para Lycaena bleusei, la cual se ha elevado a categoría de especie (Cassulo et al., 1989). Para analizar si las diferencias en el número medio de especies y de individuos colectados en cada parcela eran estadísticamente significativos se efectuó un análisis de la varianza (ANOVA), transformando los datos del número de individuos mediante la expresión log (n+1) para ajustarlos a una distribución normal, y realizando posteriormente un test de Tukey (HDS) para detectar los pares con diferencias significativas (p < 0,05). Para cada parcela se ha calculado el índice de equitabilidad de Pielou, y para agruparlas en función de su composición de especies se ha realizado un análisis de agrupamiento (Cluster Analysis) empleando el Porcentaje de Disimilitud como medida de proximidad y el método de Ward como estrategia de agrupamiento (Legendre & Legendre, 1998). Se han estudiado las curvas de acumulación de especies para cada parcela con el fin de conocer el grado de precisión de los inventarios faunísticos y ofrecer estimas de su riqueza de especies (Colwell & Coddington, 1994). Estas curvas posibilitan la com-

Diversidad ambiental 0,37

paración de inventarios de lugares diferentes ya que hacerlo exclusivamente mediante el valor del número de especies encontradas, sin hacer referencia al esfuerzo invertido, puede producir resultados engañosos (Gotelli & Colwell, 2001). El número de transectos se empleó como medida del esfuerzo de muestreo, y su orden se aleatorizó 100 veces con el fin de construir curvas suavizadas empleando el programa Estimates 6.0 (Colwell, 2000). Las asíntotas de las curvas se estimaron ajustando la ecuación de Clench a las curvas de acumulación (Soberón & Llorente, 1993; Colwell & Coddington, 1994) mediante el método de Quasi–Newton (StatSoft, 1999), y el valor asintótico predicho se empleó para estimar el grado de precisión de los seis inventarios. También se ha realizado la curva de acumulación para el conjunto de las seis parcelas con el fin de estimar la fiabilidad del inventario total del Parque Nacional de Cabañeros. Resultados Ninguna de las curvas de acumulación de especies alcanza la asíntota (fig. 2). Sin embargo, la ecuación de Clench se ajusta bastante bien a las seis curvas con porcentajes de varianza explicada que oscilan entre el 98.7 y el 99.9%. En todos los casos la asíntota predicha no difiere mucho del valor de riqueza observado, oscilando los porcentajes de especies colectadas entre el 81% y el 85% (tabla 2), estando además los valores estimados y los reales altamente correlacionados (r = 0,997, p < 0,0001). Estos resultados indican que, a pesar de no ser unos inventarios completos, los valores obtenidos permiten hacer comparaciones fiables entre las

Jiménez–Valverde et al.

Nº de especies observadas

35 30 25 20 15 10 5 0

15 Transectos

Fig. 2. Curvas de acumulación de especies en las diferentes parcelas, efectuadas con el programa EstimateS 6.0 (Colwell, 2000), y ajuste de la ecuación de Clench (línea continua). ! Parcela nº 1; " Parcela nº 2; # Parcela nº 3; • Parcela nº 4; $ Parcela nº 5; % Parcela nº6. Fig. 2. Species accumulation curves of the different sampling plots calculated with EstimateS 6.0 software (Colwell, 2000), and Clench equation fitted. ! Sampling plot nº 1; " Sampling plot nº 2; # Sampling plot nº 3; • Sampling plot nº 4; $ Sampling plot nº 5; % Sampling plot nº 6.

seis parcelas. Para el conjunto de la región, la curva se muestra bastante asintótica, alcanzándose un porcentaje de especies colectadas del 91% (fig. 3). Es decir, según las estimas quedarían 4 especies por inventariar en la zona. Jiménez– Valverde et al. (2002) observan 7 especies más de las aparecidas en los transectos en visitas esporádicas a zonas de interés lepidopterológico en el área. Por tanto, la estima de la función de Clench para el conjunto de los seis transectos se ajusta bastante bien al número de especies observado en el área de Cabañeros. El número medio de especies difiere significativamente entre las parcelas (F = 9,6; g. l. = 5; p < 0,01), presentando la parcela 1 una mayor riqueza de especies que el resto y la parcela 2 menor riqueza que las parcelas 1, 4 y 6 (test HDS de Tukey, fig. 4A). Son, además, las parcelas que muestran mayor y menor número total observado y predicho de especies respectivamente (tabla 2). El número medio de individuos también varía significativamente entre las parcelas (F = 11,4; g. l. = 5; p < 0,01), presentando las parcelas 1 y 2 mayor y menor número que el resto, respectivamente (fig. 4B), al igual que ocurre con el total de individuos observados (tabla 2). No existe correlación significativa entre el número de especies o individuos y la diversidad ambiental de las parcelas (r = 0,394; p > 0,9 y r = 0,184; p > 0,7, respectivamente).

En las seis parcelas se repite un patrón de dominancia (tabla 3). Hay unas pocas especies muy abundantes, típicas de pastizales y zonas abiertas, y una mayoría de especies escasamente representadas. Llama la atención la fuerte dominancia de Aricia cramera en la parcela 1, con el 43,5% del total de los individuos. En esta misma parcela Maniola jurtina, especie típica de prados, muestra un valor similar a otras especies eminentemente forestales como Pyronia bathseba, Satyrium esculi o Neozephyrus quercus y, a pesar de que las estimaciones realizadas para las dos últimas especies no sean muy precisas debido al método de muestreo empleado (Stefanescu, 2000), consideramos que el dato sigue siendo relevante. De la misma manera, hay una fuerte presencia de otras especies típicas de zonas abiertas y herbazales como Coenonympha pamphilus y Lycaena phlaeas. Celastrina argiolus, Coenonympha dorus y Melanargia lachesis son especies exclusivas de esta parcela y son propias de zonas boscosas bien conservadas. En la parcela 2 es P. bathseba la especie dominante, con el 33.6% de los individuos, seguida de M. jurtina y A. cramera. En la parcela 3, Pyronia cecilia representa por sí sola el 42.3% del total de los individuos, seguida de C. pamphilus y M. jurtina. En el resto de parcelas son especies dominantes P. cecilia, L. phlaeas, A. cramera, M. jurtina y C. pamphilus, componiendo estas dos últimas especies el 69,4% del total en la parcela 5. Esta es, de hecho, la parcela con el índice de equidad más bajo (tabla 2).

Animal Biodiversity and Conservation 27.2 (2004)

Tabla 2. Número de visitas, especies e individuos, índice de equidad de Pielou (EP), valor asintótico de la función de Clench (VC) y tanto por ciento de especies colectadas para las distintas parcelas (%). Table 2. Number of visits, species and individuals, Pielou equitability index (EP), asymptotic value of the Clench function (VC) and percentage of collected species for the different sampling plots (%).

Parcela 2

Nº visitas

1 21

Nº especies

1498

304

856

836

709

684

Nº individuos EP

0,63

0,73

0,61

0,59

0,72

36,5

24,7

29,4

29,5

26,1

30,6

84,93

80,97

85,03

84,74

84,29

84,97

La abundancia relativa de Lycaenidae, Pieridae y Satyrinae difiere significativamente entre las parcelas (P2 = 1206,1; g. l. = 10; p < 0,01; fig. 5), siendo los licénidos especialmente abundantes en la parcela 1 (debido a la elevada densidad de A. cramera), los piéridos en la parcela 4 y los satirinos en las parcelas 2, 3 y 5. El análisis de agrupamiento genera dos grupos principales (fig. 6). El primer grupo está compuesto únicamente por la parcela 1, la que representa el hábitat con menor grado de alteración y más homogéneo: el encinar. El segundo

grupo está formado por el resto de parcelas que han sufrido una mayor antropización del medio. Este segundo grupo se divide, a su vez, en dos subgrupos. El primero lo forman las parcelas 2, 4 y 5. Son parcelas que tienen en común una alta proporción de hábitat hostil para las mariposas (tabla 1) presentando además, las dos primeras, bajos valores de diversidad ambiental. El segundo subgrupo está formado por las parcelas 3 y 6, ambas con una elevada proporción de matorral y con un alto valor de diversidad ambiental (tabla 1).

Nº de especies observadas

45 40 35 30 25 20 15 10 5 0

15 Transectos

Fig. 3. Curva de acumulación de especies para el conjunto de las parcelas con la ecuación de Clench ajustada (valor de la asíntota = 46,1; R2 = 99,9). Fig. 3. Species accumulation curve for the six sampling plots alltogether with Clench equation fitted (asymptotic value = 46.1; R2 = 99.9).

Jiménez–Valverde et al.

A Nº medio de individuos

Nº medio de especies

10 9 8 7 6 5 4 3 2

3 4 Parcela

100 90 80 70 60 50 40 30 20 10 0

3 4 Parcela

Fig. 4. Número medio de especies (A) e individuos (B) en las diferentes parcelas (± intervalo de confianza 95%). Fig. 4. Mean total species richness (A) and abundances (B) at the different sampling plots (± 95% confidence interval).

Discusión Los niveles de sombra afectan negativamente a la abundancia de mariposas ya que son animales que necesitan cierto nivel de insolación para volar. Por otra parte, el grado de insolación de una zona va a condicionar la presencia de flores para que liben los adultos y de plantas nutricias para la alimentación de las larvas (Pollard & Yates, 1993). En el interior de las formaciones boscosas el grado de insolación es un factor crítico que gobierna la selección de hábitat de muchas especies, cada una da las cuales puede presentar asociaciones con niveles de sombra específicos (Warren, 1985). Así, es normal encontrar especies propias de prados en las zonas abiertas (caminos y claros) de los bosques (Warren, 1985). La fuerte abundancia de especies típicas de herbazales en el encinar estudiado se debe a que es un bosque con presencia de zonas aclaradas, donde junto a las especies forestales aparecen especies típicas de prados que encuentran en estos lugares hábitats adecuados intercalados entre el dosel arbóreo. Martín Cano & Ferrín (1998) encuentran el mismo fenómeno al comparar una plantación de Pinus sylvestris en Valsaín (Sierra de Guadarrama, España central) con un bosque cercano de Quercus pyrenaica. En su estudio, la especie oportunista Melanargia lachesis alcanzaba elevadas densidades en los claros del bosque de quercinias, haciendo descender el índice de equitabilidad de éste por debajo del de la plantación. Según García–Barros et al. (1998), la relación de dominancia de las comunidades de formaciones pratenses difiere marcadamente de la que puede encontrarse en zonas dominadas por bosques y matorrales mediterráneos. En el primer

caso, hay una marcada dominancia de unas pocas especies típicas de prados, dominancia que no se observa en zonas con vegetación más boscosa. En Cabañeros, estas diferencias no se aprecian tan claramente como en el estudio de García–Barros et al. (1998). El encinar presenta una elevada abundancia de A. cramera, de manera similar a lo observado en el robledal de Valsaín por Martín Cano & Ferrín (1998) con M. lachesis, provocando que la abundancia de licénidos sea significativamente alta. En la parcela 3, con dominancia de matorral, P. cecilia, C. pamphilus y M. jurtina se encuentran en elevadas densidades, resultando en una abundancia de satirinos significativamente alta. De esta manera, el encinar aparece claramente diferenciado respecto a su composición, riqueza y abundancia de especies del resto de parcelas que se han visto sometidas a una mayor presión antrópica. Así, el mantenimiento de masas boscosas bien conservadas es esencial para asegurar la protección de la biodiversidad de mariposas, viéndose enriquecida ésta gracias a la presencia de caminos y claros que favorecen el crecimiento de plantas para la alimentación de las orugas, para la ovoposición y de flores para la alimentación de los imagos. En el conjunto de las parcelas 2, 3, 4, 5 y 6 están representadas 11 especies que no se presentan en el encinar. Estas especies aparecen en muy baja frecuencia, aunque su presencia es indicadora de ciertas condiciones ambientales. Así, por ejemplo, los piéridos Pieris rapae y Pontia daplidice son especies propias de áreas destinadas a labores agrícolas, como demuestran sus elevadas y significativas densidades en la parcela 4. Vanesa cardui prefiere parajes abiertos y secos y Papilio machaon

Animal Biodiversity and Conservation 27.2 (2004)

Tabla 3. Frecuencia total de las especies en las seis parcelas muestreadas. Table 3. Total species frequencies in the six sampling plots.

Parcela Especie Aporia crataegi

0,1

–

0,1

–

Argynnis pandora

1,2

1,0

0,2

0,1

2,5

2,2

Aricia cramera

43,5

10,9

5,6

18,9

8,3

10,7

Brintesia circe

0,5

1,0

3,4

0,1

0,3

3,7

Callophrys rubi

–

0,3

0,1

–

0,3

Celastrina argiolus

0,3

–

Charaxes jasius

0,3

–

1,1

0,1

–

0,1

Coenonympha dorus

0,2

–

Coenonympha pamphilus

3,6

15,1

38,2

36,1

11,3

Colias croceus

0,1

5,9

0,5

4,2

0,8

0,6

Euchloe belemia

–

0,1

0,3

Euchloe crameri

0,1

1,3

0,9

1,3

1,6

2,9

Euphydryas aurinia

0,7

–

4,2

–

Gonepteryx cleopatra

0,5

–

0,9

0,1

1,3

0,3

Heodes bleusei

0,7

0,3

–

Hipparchia alcyone

0,3

9,9

–

0,1

–

Hipparchia semele

–

0,7

0,4

–

0,1

0,4

Hipparchia statilinus

4,1

6,9

6,8

0,4

2,0

5,3

Hyponephele lupinus

0,4

0,3

1,3

0,7

1,0

–

Issoria lathonia

0,3

–

0,2

–

Lampides boeticus

0,1

–

0,1

Lasiommata megera

0,5

6,6

0,1

–

Leptidea sinapis

–

0,1

–

0,1

Lycaena phlaeas

2,7

0,7

1,4

6,8

5,2

14,9

Maniola jurtina

8,6

14,1

13,0

14,5

33,3

15,4

Melanargia ines

0,2

–

0,1

Melanargia lachesis

0,1

–

0,1

–

7,3

–

0,2

2,8

–

Muschampia proto Neozephyrus quercus Papilio machaon

–

0,1

Pieris rapae

–

0,3

–

4,4

0,3

0,9 0,4

Pontia daplidice

–

0,4

2,3

0,1

Pyronia bathseba

8,7

33,6

–

0,1

–

Pyronia cecilia

2,2

–

42,3

4,4

2,4

23,2

Pyronia tithonus

1,5

1,0

0,1

–

Satyrium esculi

8,3

–

0,1

0,2

0,6

0,7

Thymelicus acteon

0,3

–

0,1

–

Thymelicus lineola

–

0,2

–

1,7

–

1,6

0,5

0,3

2,0

–

0,1

–

1,0

–

1,6

0,4

0,9

0,7

0,1

0,3

3,2

Thymelicus sylvestris Tomares ballus Vanessa cardui Zerynthia rumina

Jiménez–Valverde et al.

Parcelas

5 4 3 2 1 0%

20%

40% 60% Proporción relativa

80%

100%

Fig. 5. Abundancia relativa de Lycaenidae (en negro), Pieridae (en blanco) y Satyrinae (en gris) en cada parcela. Fig. 5. Relative abundance of Lycaenidae (black), Pieridae (white) and Satyrinae (grey) in each sampling plot.

vuela en los bordes de caminos y barbechos donde crecen sus plantas nutricias. Es decir, las transformaciones que el hombre realiza en el medio benefician a ciertas especies que prefieren territorios abiertos y ruderales a los bosques más cerrados. Se observa, por tanto, que las áreas fragmentadas agrícolas y ganaderas con explotación extensiva,

que mantienen zonas con el bosque original y pastos seminaturales junto con cultivos, pueden conservar una buena representación de la biodiversidad de mariposas. Precisamente el tamaño y calidad de la red de las superficies boscosas es el factor fundamental para el mantenimiento de esta biodiversidad.

1 2 5 4 3 6

0,50

0,55 0,60 0,65

0,70 0,75

0,80 0,85

0,90 0,95

1,00

Fig. 6. Dendrograma de clasificación de las parcelas muestreadas en función de su composición de especies. Se ha empleado el Porcentaje de Disimilitud como medida de proximidad y el método de Ward como estrategia de agrupamiento (Legendre & Legendre, 1998). Fig. 6. Classification tree of the sampling plots based on species composition. The percent disagreement has been used as distance measure and Ward´s method as linkage rule (Legendre & Legendre, 1998).

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Sin embargo, una estructura forestal no es garantía de una mayor diversidad. La plantación de coníferas parece no diferir del resto de parcelas con intensa presión antrópica, presentando incluso una menor riqueza específica y un menor número de individuos que éstas. Las plantaciones de coníferas son sistemas complejos cuya naturaleza se ve influenciada por numerosos factores: localización geográfica, especie arbórea empleada, técnica usada de reforestación y el posterior manejo y uso del territorio. En general, las plantaciones hacen decrecer la riqueza faunística de mariposas, en mayor o menor grado dependiendo del porte del dosel arbóreo y de la estructura y composición de los estratos subarbóreos (Martín Cano & Ferrín, 1998). Greatorex–Davis et al. (1992) comprobaron cómo, en varias plantaciones de coníferas, tanto el número de especies de mariposas como el número de individuos estaban correlacionados negativamente con el grado de sombra de los diferentes caminos. La composición faunística de las plantaciones de coníferas suele consistir en especies comunes y de amplia distribución (Pollard & Yates, 1993). La plantación de este estudio es una plantación antigua y con un dosel arbóreo muy desarrollado, por lo que el interior del pinar tiene un bajo grado de insolación y una diversidad vegetal baja. En este caso es Pyronia bathseba la especie oportunista que alcanza densidades significativamente elevadas. El hecho de que de las 20 especies encontradas, 6 aparezcan exclusivamente en el cortafuegos, subraya la pobreza de la plantación y pone de relieve la importancia de los cortafuegos como elementos fundamentales para enriquecer la fauna de mariposas de las plantaciones de coníferas, además de la importancia de las estructuras lineales en el movimiento de las mariposas (Dover et al., 1997). La riqueza del cortafuegos muestra la importancia de facilitar la existencia de espacios abiertos en este tipo de biotopos. Sería interesante establecer una red de caminos, de diferentes anchuras, con el fin de crear nichos adecuados para distintas especies. También resultaría útil aclarar este tipo de plantaciones antiguas que poseen un dosel arbóreo muy denso que impide la llegada del sol al piso inferior del bosque, provocando la escasez de zonas apropiadas para las mariposas y la reducción de la diversidad vegetal. Es interesante el agrupamiento de la plantación de coníferas junto a las parcelas 4 y 5. Las tres son parcelas en las que domina un hábitat poco adecuado para las mariposas. La parcela 5 tiene una dominancia de pastos adehesados y la parcela 4 una dominancia de tierras dedicadas a cultivos. Las zonas abiertas no ofrecen protección a las mariposas frente a las inclemencias temporales (Dover et al., 1997). El viento y, en áreas mediterráneas, el seco y caluroso verano obligan a los lepidopteros a buscar refugio en la vegetación, refugio que no encuentran en los hábitats mencionados. El agrupamiento de la plantación de coníferas con estas otras dos apoya la idea de lo desfavorables que resultan las plantaciones de coníferas para la fauna lepidopterológica.

Agradecimientos Al personal del Parque Nacional de Cabañeros y especialmente a su director, José Jiménez García Herrera, por permitirnos llevar a cabo este estudio. Al propietario y personal de la finca “Las Póvedas”, especialmente a Daniel, por su amabilidad y por todas las facilidades dadas. Este estudio ha sido financiado por el proyecto europeo Biodiversity Assessment Tools (BioAssess) EUK4– 1999–00280. Referencias Cassulo, L., Mensi, P. & Balletto, E., 1989. Taxonomy and evolution in Lycaena (subgenus Heodes) (Lycaenidae). Nota lepidopterologica, Suppl. 1: 23–25. Colwell, R. K., 2000. Estimates: Statistical Estimation of Species Richness and Shared Species from Samples (Software and User´s Guide), Versión 6.0. En: http://viceroy.eeb.uconn.edu/estimates Colwell, R. K. & Coddington, J. A., 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society, series B, 345: 101–118. Costa Tenorio, M., Morla Juaristi, C. & Sainz Ollero, H. (Eds.), 1998. Los bosques ibéricos. Una interpretación geobotánica. Geoplaneta, Barcelona. Dover, J. W., Sparks, T. H. & Greatorex–Davies, J. N., 1997. The importance of shelter for butterflies in open landscapes. Journal of Insect Conservation, 1: 89–97. García–Barros, E., Martín, J., Munguira, M. L. & Viejo, J. L., 1998. Relación entre espacios protegidos y la diversidad de la fauna de mariposas (Lepidoptera: Papilionoidea et Hesperiodea) en la Comunidad de Madrid: una evaluación. Ecología, 12: 423–439. Gotelli, N. J. & Colwell, R. K., 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4: 379–391. Greatorex–Davis, J. N., Sparks, T. H., Hall, M. L. & Marrs, R. H., 1992. The influence of shade on butterflies in rides of coniferised lowland woods in England and implications for conservation management. Biological Conservation, 63: 31–41. Jiménez–Valverde, A., Martín Cano, J. & Munguira, M. L., (2002). Fauna de mariposas del Parque Nacional de Cabañeros y su entorno (Ciudad Real) (Lepidoptera: Papilionoidea, Hesperioidea). SHILAP, Revista de Lepidopterología, 30(120): 271–279. Karsholt, O & Razowski, J., 1996.The Lepidoptera of Europe. A distributional Checklist. Apollo Books, Stenstrup, Denmark. Legendre, P. & Legendre, L., 1998. Numerical Ecology. Elsevier, Amsterdam. Martín Cano, J. & Ferrín, J. M., 1998. Changes in

butterfly diversity in three reforested areas in Spain. Journal of the Lepidopterists´Society, 52(2): 151–165. Martín Cano, J., Ferrín J. M., García–Barros, E., García–Ocejo, A., Gurrea, P., Lucianez, M. J., Munguira, M. L., Perez Barroeta, F., Ruiz Ortega, M., Sanz Benito, M. J., Simon, J. C. & Viejo, J. L., 1996. Las comunidades de insectos del Parque Regional de la Cuenca Alta del Manzanares (centro de España): estado de conservación. Graellsia, 51: 101–111. Mousson, L., Nève, G., & Baguette, M., 1999. Metapopulation structure and conservation of the cranberry fritillary Boloria aquilionaris (Lepidoptera, Nymphalidae) in Belgium. Biological Conservation, 87: 285–293. New, T. R., Pyle, R. M., Thomas, J. A., Thomas, C. D. & Hammond, P. C., 1995. Butterfly conservation management. Annual Review of Entomology, 40: 57–83. Pollard, E., 1977. A method for assessing changes in the abundance of butterflies. Biological Conservation, 12: 115–134. Pollard, E. & Yates, T. J., 1993. Monitoring butterflies for ecology and conservation. Chapman &

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Hall, Londres. Rodríguez González, J., 1991. Las mariposas del Parque Nacional de Doñana. Biología y ecología de Cyaniris semiargus y Plebejus argus. Tesis doctoral, Univ. de Córdoba. Soberón, J. & Llorente, B. J., 1993. The use of species accumulation functions for the prediction of species richness. Conservation Biology, 7: 480–488. StatSoft, 1999. Statistica for Windows, Computer program manual. StatSoft, Inc., Tulsa, OK. Stefanescu, C., 2000. El Butterfly Monitoring Scheme en Catalunya: los primeros cinco años. Treballs de la Societat Catalana de Lepidopterologia, 15: 5–48. Swaay , C. A. M. van & Warren, M. S., 1999. Red Data Book of European butterfies (Rhopalocera). Nature and Environment 99. Council of Europe Publishing, Strasbourg. V.V.A.A., 1997. Parque Nacional de Cabañeros. Ecohábitat, Ciudad Real. Warren, M. S., 1985. The influence of shade on butterfly numbers in woodland rides, with special reference to the Wood White Leptidea sinapis. Biological Conservation, 33: 147–164.

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Seasonal change in pupation behaviour and pupal mortality in a swallowtail butterfly C. Stefanescu

Stefanescu, C., 2004. Seasonal change in pupation behaviour and pupal mortality in a swallowtail butterfly. Animal Biodiversity and Conservation, 27.2: 25–36. Abstract Seasonal change in pupation behaviour and pupal mortality in a swallowtail butterfly.— Phenotypic plasticity in pupal colour has evolved to render cryptic pupae. Apart from characteristics of the pupation site, the photoperiod experienced by larvae is important in determining pupal colour, long and short photophases eliciting the formation of green and brown pupae, respectively. This seasonal polyphenism is often correlated with developmental pathway, green pupae developing directly and brown pupae entering into diapause. From 1996 to 2000, immature stages of Iphiclides podalirius were monitored on natural hostplants in NE Spain. Larvae were followed to the pupation site and pupal colour, characteristics of the pupation site and the fate of pupae were recorded. Before August, pupae were non–diapausing green while in early August they were dimorphic, after which, they were brown and overwintered. As theory predicts, differences in pupation sites in successive generations were found in relation to pupal colour. Green pupae occurred on the hostplants and brown pupae were found among the leaf litter. Mortality ranged from 14.3 to 100%. Bird predation was the major mortality factor for green pupae and was also important for brown pupae. Results suggest that preference for pupation sites in the litter in diapausing broods evolved to avoid strong bird predation on the hostplants. Preference for sites above ground level in summer generations may have evolved in response to both non–visual (small mammals) and visual (avian) predators. Key words: Lepidoptera, Swallowtail butterflies, Iphiclides podalirius, Pupal colour, Pupation behaviour, Pupal mortality. Resumen Cambios estacionales en el comportamiento de pupación y en la mortalidad de las pupas en un papiliónido.— La plasticidad fenotípica en el color de las pupas es el resultado de un proceso evolutivo que permite a las pupas ser crípticas. Además de las características del lugar de pupación, el color de la pupa viene determinado por el fotoperíodo que experimenta la larva. Los fotoperíodos largos y cortos favorecen, respectivamente, la formación de pupas verdes y marrones. Este polifenismo estacional frecuentemente se correlaciona con el tipo de desarrollo, de manera que las pupas verdes siguen un desarrollo directo mientras que las marrones entran en diapausa. Entre 1996 y 2000, se controlaron los estadios inmaduros de Iphiclides podalirius sobre sus plantas nutricias naturales en una localidad del noreste de España. Se siguió a las larvas hasta su lugar de pupación, y se anotaron las características de dichos lugares y el destino final de las pupas. Antes de agosto, todas las pupas observadas fueron verdes y de desarrollo directo; a principios de agosto, las pupas fueron dimórficas; posteriormente, todas fueron marrones y entraron en diapausa. Tal como predice la teoría, las diferencias entre generaciones sucesivas respecto los lugares de pupación se relacionaron con el color de las pupas. Las pupas verdes se localizaron sobre la planta nutricia, mientras que las marrones se localizaron entre la hojarasca. La mortalidad osciló entre el 14,3 y el 100%. La predación por parte de aves insectívoras fue el principal factor de mortalidad para las pupas verdes y también fue importante para las pupas marrones. Los resultados sugieren que la preferencia por la hojarasca como lugar de pupación en las generaciones que entran en diapausa ha evolucionado para reducir la gran mortalidad que tendría lugar sobre la planta nutricia. En las generaciones de verano, la preferencia por lugares alejados del suelo podría ser el resultado de una respuesta evolutiva tanto frente a los depredadores no visuales (micromamíferos) como visuales (aves). ISSN: 1578–665X

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Palabras clave: Lepidoptera, Papiliónidos, Iphiclides podalirius, Color pupal, Comportamiento pupal, Mortalidad pupal. (Received: 28 V 03; Conditional acceptance: 28 VIII 03; Final acceptance: 6 X 03) Constantí Stefanescu, Butterfly Monitoring Scheme, Museu de Granollers Ciències Naturals, Francesc Macià, 51, E–08400 Granollers, Spain. E–mail: canliro@teleline.es

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Introduction The pupal stage is critical in the survival of any holometabolous insect, including Lepidoptera (Cornell & Hawkins, 1995), above all because its lack of mobility makes it very vulnerable to predation. To a large extent its survival is based on a “primary anti-predator defence”, that is to say, on the avoidance of detection by predators (Brakefield et al., 1992). Therefore, it comes as no surprise that the pupa is the hardest stage of a butterfly’s life cycle to locate and few studies have included detailed data on the nature of pupation sites (e.g. West & Hazel, 1996) or on pupal mortality (e.g. White, 1986). Since the pioneering work of Poulton (1887, 1892), it has repeatedly been shown that pupal colour can vary within swallowtail butterflies. Thus, the pupae of many species are dimorphic, either brown or green, exhibiting phenotypic plasticity or environmentally cued polymorphism for colour (reviewed in Hazel, 1995). Both the colour and texture of the pupation site have been recognised as the most important environmental cues governing polymorphism (Smith, 1978; Hazel & West, 1979). The upshot is that pupae match the background of their resting sites, which, in turn, leads to enhanced survival (e.g. Wiklund, 1975; Sims & Shapiro, 1984; Hazel et al., 1998). An additional factor, the photoperiod experienced by larvae, can also be important in determining pupal colour (Smith, 1978; Hazel & West, 1979, 1983). Thus, under a short photophase, the larvae of some species produce almost exclusively brown pupae. Because diapause in many insects is also influenced by the larval photoperiod (Leather et al., 1993), a phenotypic correlation between pupal colour and diapause strategy may be a common phenomenon. This kind of seasonal polyphenism (Shapiro, 1976) seems to apply in the scarce swallowtail butterfly, Iphiclides podalirius (L.). Under laboratory conditions, larvae exposed to long day lengths produce green pupae that do not diapause, while those exposed to short day lengths produce brown pupae that overwinter (Wohlfahrt, 1954, 1957; Friedrich, 1986; Tolman & Lewington, 1997). Available data thus suggest that pupae are seasonally monomorphic, with colour being correlated to the developmental pathway. According to Clarke & Sheppard (1972) and Wiklund (1975), monomorphic pupae have evolved in stable predictable environments where larvae can develop strong preferences for a particular kind of substratum, whereas the reverse is true for polymorphic pupae. A seasonal polyphenism would arise in cases of differences in the pupation sites in successive generations. Hence, a first prediction regarding I. podalirius is that diapause and nondiapause pupae should be found at different sites (see also West & Hazel, 1979). Second, it has been hypothesized that green pupae evolved from monomorphic brown pupae

that suffered from high levels of non–visual predation (mainly by small mammals) at their pupation sites in the leaf–litter. Green coloration would have been selected in the event of pupation site preference changing to sites among green vegetation above ground levelwhich render pupae more cryptic to visual (mainly avian) predators (e.g. West & Hazel, 1982; Hazel, 1995; Hazel et al., 1998). According to this hypothesis, green non–diapausing pupae of I. podalirius should be found on green sites above ground level, where avian predators would play a significant role in overall mortality. On the other hand, brown overwintering pupae should occur near the ground, where they would mainly be preyed upon by non–visual predators. In the present paper, these two predictions are tested, having first confirmed the existence of seasonal polyphenism in I. podalirius pupae (and the correlation between pupal colour and developmental pathway) under natural conditions. Material and methods Study species Iphiclides podalirius is a swallowtail butterfly which is widespread in the Palaearctic region (Tolman & Lewington, 1997). It overwinters in the pupal stage and, in the Iberian peninsula, is usually multivoltine. Hostplants are shrubs and trees of the Rosaceae family, mainly blackthorn Prunus spinosa, fruit trees of the genus Prunus, and hawthorn Crataegus monogyna. Eggs are laid singly on the underside of leaves. Caterpillars are sedentary and live on a silk cushion spun onto the surface of the leaf selected as a resting site. They pass through five instars with a total developmental time of three to six weeks, depending on the temperature and host plant (C. Stefanescu, unpublished data). Study site and sampling The study was carried out in Can Liro (Sant Pere de Vilamajor, 41º 41' 16" N 2º 23' 07" E, 310 m a.s.l., NE Spain), an agricultural area surrounded by evergreen oak Quercus ilex forest. The climate is Mediterranean, with rainfall of ca. 650 mm per year and summer drought. Immature stages of I. podalirius were monitored on their natural hostplants, and an attempt was made to follow any larva reaching the prepupal stage to the pupation site. Pupal colour, characteristics of the pupation site and the fate of pupae were subsequently recorded. From 1996–1999, four blackthorns, two peach trees Prunus persica and one hawthorn were monitored in a hedgerow between two fields. All these plants were at least two years old in 1996. Their height ranged from 180–200 cm (trees) and 50– 215 cm (shrubs). In 1999, 14 additional blackthorns in another hedgerow were also monitored. They

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were young shoots resulting from the cutting, in February 1999, of a dense stand of blackthorn, and their mean height in April was 45.4 ± 8.1 cm (mean ± SD, range: 35–64 cm). Their appearance differed strongly from that of shrubs, as they mainly consisted of a stem and a few branches. Of over 700 larvae successfully hatched from 1033 naturally laid eggs, only 72 completed their development and were monitored throughout the pupal stage (see Stefanescu et al., 2003). To increase this sample, 65 fifth instar larvae were collected on nearby blackthorns and peach trees in 1998–2000 and released on the monitored host plants. These larvae were allowed to select a pupation site once their development was completed. Correlates of pupal colour To confirm that pupal colour and diapause are induced by the photoperiod and are correlated traits in I. podalirius, field data were complemented with data from the captive rearing of 112 larvae. Larvae were collected as eggs in 1996 and 1997 and were reared in clear plastic boxes in an outdoor yard (i.e. not exposed to direct sunshine but experiencing naturally fluctuating air temperatures and photoperiod). Larvae were allowed to pupate freely on the stems provided together with the food (blackthorn) or on the box sides. Preliminary rearings had shown that neither kind of substrate elicited differences in pupal colour (see Hazel & West, 1979, for a different situation), and therefore no attempt was made to control for this factor. As noted by Hazel (1995), the colour of the green morph varies little in the pupae of swallowtail butterflies, while the brown morph can show considerable variation in accordance with the darkness of the pupation site (the so–called phenotypic modulation). In the present paper, however, pupae were classified as either green or brown, without taking into account the degree of darkness of brown pupae. Because the definitive colour appeared soon after pupation and then remained unchanged until adult emergence, colour assignment could be performed within the first 24 h after a larva had pupated. Those factors most likely to influence (or to be associated with) pupal colour were measured: 1. Photoperiod, calculated at the pupation date (i.e. during the most sensitive period of the larval stage, according to Hidaka, 1961) from tables published by the Instituto Nacional de Meteorología (1991); 2. The generation to which the larva belonged, as deduced from the monitoring of immature specimens and from adult transect counts as part of the Catalan Butterfly Monitoring Scheme (Stefanescu, 2000a); 3. The developmental pathway, considering a pupa to have entered diapause if eclosion was delayed for more than 120 days (the shortest time necessary for passing the winter period, in the hypothetical case in which pupation and adult emergence occurred, respectively, by late October and early March); 4. The pupation site, its height off the ground and the diameter of the site measured at

the point of girdle attachment (following West & Hazel, 1979, 1996; West, 1995); and 5. Whether pupation occurred on or off the hostplant. Pupal mortality Once larvae selected pupation sites, positions were marked with plastic tags to allow subsequent relocation. Non–overwintering and overwintering pupae were inspected daily and at one–weekly intervals, respectively, and their fates were recorded as follows: 1. Alive and intact; 2. Attacked by a predator, remains found; 3. Gone and presumed preyed upon; 4. Dead but intact (physiological death); 5. Stepped on; or 6. Eclosed. Although the identity of predators could not always be established with certainty, indirect evidence from characteristic forms of damage allowed the main sources of mortality to be estimated. Similar pupal remains to those described by Frank (1967) were considered to be the result of invertebrate predation. Bird predation was assessed by means of direct observation (a full account of observations is reported in Stefanescu, 2000b). Also, between 8 and 15 December 1997, 10 Sherman traps were placed in the experimental area from dusk to early morning to determine the most common small mammal predators. Experiments on bird predation pressure In non–overwintering broods, pupation mostly occurred on the foodplants, except for one–year–old blackthorn shoots, in which case it predominantly occurred on the ground. On the other hand, in diapausing broods, larvae always pupated among the leaf litter (see Results). Because swallowtail pupae above ground level are commonly preyed upon by birds (e.g. West & Hazel, 1982; Stefanescu, 2000b), two field experiments were designed to test the possibility that larvae leaving the hostplant might have been selected to avoid bird predation. Non–overwintering pupae Four out of 10 larvae occurring on one–year old blackthorns in June–July 1999 pupated on the hostplants (one left its original foodplant but finally pupated on another sapling), at heights of 20– 40 cm above the ground. To increase this sample, eight pupae were artificially glued on nearby shoots with a dab of colourless “Evo–stick” impact adhesive, using the same kind of pupation sites naturally selected (woody stems and the underside of leaves) within the same height range (20–40 cm). Their survival was compared with that of those pupae produced by the six larvae that left the same shoots and pupated among green grasses, plus another four pupae glued to grass stems to increase this data set. Survival was also compared with that of those pupae naturally occurring on shrubs in summers 1996–1999. All pupae monitored in this experiment (both naturally occurring and artificially placed) were green.

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Overwintering pupae The survival of two sets of overwintering pupae was compared in each of the winters 1997–98, 1998–99 and 1999–2000. One set was composed of pupae naturally occurring among the leaf-litter (i.e. those coming from larvae that could be followed to their pupation sites) and the other of pupae glued to hostplants at heights of 50–150 cm. To rule out the possibility that highly visible plastic tags on leafless shrubs and trees increased attraction for visual predators, relocation of artificially placed pupae was made with the help of a sketch showing their positions instead of the plastic tags. On 9 XI 97, 16 pupae were placed on three blackthorns and one peach tree to simulate the situation that would have arisen if the 17 wild larvae that survived to the prepupal stage had pupated on their hostplant instead of leaving to pupate among the leaf litter. This design prevented attaining an unnatural pupal density in the monitored hedgerow that might have led to an abnormally high level of predation. The same design was used in the following years. On 1 XI 98, 13 pupae were placed on two blackthorns, two peach trees and one hawthorn, and their survival was compared with that of 23 wild pupae. On 16 X 99, 25 pupae were placed on four blackthorns, one peach tree and one hawthorn and their survival was compared with that of 30 wild pupae. Wild pupae were inspected at weekly intervals, while artificially placed pupae were checked daily, and their fates recorded as described above. All pupae in this experiment (both naturally occurring and artificially placed) were brown.

The null hypothesis “pupal survival is unaffected by bird predation whether the pupa is on or off the hostplant” was tested by comparing proportions of successfully eclosed pupae by means of 2 x 2 contingency tables. In overwintering pupae, however, mortality was so high that the power of the test was much reduced; therefore, a second analysis was performed to compare another variable correlated with pupal survival: elapsed time (in days) before a pupa died. Non– parametric tests were used because this variable was not normally distributed even after data transformation. Results Seasonal polyphenism First generation butterflies peaked in early May (fig. 1). Their offspring developed into green pupae (fig. 2A) that gave rise to a second generation of adults emerging from late June to early August (fig. 1). The earliest offspring of the second generation produced green pupae that developed into a partial third generation of adults from early August to early September (fig. 1). The proportion of larvae entering the direct–developmental pathway decreased from 8:2 (non–diapausing green: diapausing brown) in 3–9 August to 4:12 in 10–16 August. The remaining pupae of the second generation and all those of the third generation (which appeared in early October) were diapausing brown

Weekly count

16 14 12 10 8 6 4 2 0

3 5 7 9 11 13 15 17 19 21 23 25 27 29 Weeks March April May June July August Sept

Fig. 1. Seasonal abundance of Iphiclides podalirius as recorded by weekly transect counts of adults at the study site in 1994–2000 (n = 110). Week 1 corresponds to 1–7 March and week 30 to 20–26 September. Fig. 1. Abundancia estacional de Iphiclides podalirius en la zona de estudio entre 1994–2000 (n = 110), según los contajes semanales a lo largo de un transecto. La semana 1 corresponde a 1–7 de marzo y la semana 30 a 20–26 de septiembre.

pupae (fig. 2A). Very similar results were obtained in the rearing experiment, with the single exception of a non–diapausing brown pupa occurring in early July (fig. 2B). Photoperiods are shown in fig. 2C. The data confirm the existence of a seasonal polyphenism, with the colour and developmental pathway of the pupae being correlated traits. Mean duration (in days) of non–diapausing green pupae was 16.82 ± 0.46 (mean ± SD, n = 17; range: 14– 21) and 18.18 ± 0.59 (n = 37; range: 13–25) for wild and captive pupae, respectively. For brown diapausing pupae, these values were 214.13 ± 13.8 (n = 8; range: 167–269) and 258.73 ± 2.3 (n = 74; range: 209–302), respectively. There was no difference in the duration of this stage between captive and wild non–diapausing pupae (t test = 1.82, df = 53, p = 0.074), but captive diapausing pupae took longer to develop than wild diapausing pupae (t test = 3.19, df = 80, p = 0.014). Pupation site Pupal colour and whether pupation site was on or off the hostplant were strongly associated (table 1). Although the plant species did not affect the behaviour shown by non–diapausing broods, the size of the hostplant did. Prepupal larvae tended to leave their hostplants when these consisted of small one– year old blackthorns (78.9% of green pupae stayed on shrubs vs. 27.2% on shoots; Fisher’s exact test, p = 0.009). The main pupation sites are summarized in table 2. Green pupae occurred much higher above ground level and on broader substrates than brown pupae. Twigs and thorns hidden by dense foliage were chosen on blackthorns while the underside of leaves were preferred on peach trees. In eight out of 13 cases in which larvae left the hostplant, they pupated on woody stems of nearby blackthorn shrubs. The background colour of pupation sites was always green (including those cases in which pupation occurred off the hostplant) and hence pupae were cryptically coloured. Brown pupae strongly preferred slender grass stems (mainly dry stems of Cynodon dactylon) and weed stalks (mainly brown stems of Medicago sativa from a nearby field) close to the ground. They were cryptically coloured during the winter because pupation sites consisted of predominantly dead vegetation. Pupal mortality Non–overwintering pupae Of 46 non–diapausing pupae, 29 successfully eclosed (63%) and 17 died (fig. 3). Survival ranged from 42.9% to 85.7% in 1996–1999, but differences among years were not significant (P2 = 6.174, df = 3, p = 0.1). It should be noted, however, that there might well have occurred differences in survival that were undetected due to the small sample sizes and the reduced statistical power of the test. Bird predation was the main mortality factor, accounting for at least 47% of losses. Included in

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this estimation are confirmed records of predation by the Great Tit Parus major, as well as pupae that disappeared in the early morning leaving no trace other than the broken girdle (see Stefanescu, 2000b, for details). Impact by avian predators could indeed be much higher (nearly 80% of total losses), if pupae disappearing without trace had also been preyed upon by birds. Invertebrate predation was apparently unimportant and was only recorded once when the wasp Polistes gallica killed a second day prepupa. Comparison of pupal survival on blackthorn shrubs as opposed to shoots (including experimental data of glued pupae) revealed strong differences: 13 out of 19 green pupae on shrubs successfully eclosed, but none of 12 green pupae on shoots survived (Fisher’s exact test, p = 0.0001). Difference in survival rates between green pupae occurring on shoots (0 out of 12) and those that naturally left from the same shoots and pupated among the leaf litter (7 out of 10, the latter including four green pupae glued to equivalent sites on grass stems) was also significant (Fisher’s exact test, p = 0.02). On the other hand, neither the survival of pupae occurring on blackthorn shrubs as opposed to the leaf litter (Fisher’s exact test, p = 1), nor between blackthorn shrubs and peach trees and hawthorn (Fisher’s exact test, p = 1) were significantly different. The data indicate that the experimental manipulation did not produce a bias in the results. Survival rates among the leaf litter did not differ between naturally occurring and glued pupae (Fisher’s exact test, p = 0.67). Similarly, no differences in elapsed time before a pupa died were found between those pupae naturally occurring and those artificially placed on shoots (Mann–Whitney U test = 9, df = 4,8; p = 0.22). Overwintering pupae Three ground sites could not be relocated; of the remaining 88 overwintering pupae, eight eclosed (9.1%) and 80 were killed as the result of several mortality factors (fig. 3). Predation by the Great Tit was observed in one occasion. In another 15 cases, bird predation by several species was the most plausible explanation (see Stefanescu, 2000b). 50 pupae disappeared leaving no remains, birds and small mammals (mainly the shrew Crocidura russula, the only species trapped in the area in December 1997, and the hedgehog Erinaceus europaeus, a common species at the studied site) being the most probable predators. Minor mortality factors included physiological death during the abnormally rainy winter of 1997–98 (in which some pupae were submerged for long periods following winter flooding), trampling by humans and invertebrate predation. Pupal survival was 0% in 1996 (eclosed/total monitored: 0/11), 1998 (0/23) and 2000 (0/7), 13.3% in 1999 (4/30) and 23.5% in 1997 (4/17). Even though the sample sizes were small, differences in these proportions were marginally significant among years

Animal Biodiversity and Conservation 27.2 (2004)

A Number of pupae

18 15 12 9 6 3 0

f g Weeks

f g h i j k l Weeks brown, 2nd gen brown, 3rd gen

Number of pupae

15 12 9 6 3 0

green, 1st gen

green, 2nd gen

brown, 1st gen

Photoperiod (hours light)

C 16.0 15.0 14.0 13.0 12.0 11.0 10.0 a

f g Weeks

Fig. 2. Seasonal distribution of pupal colour in Iphiclides podalirius as recorded from the monitoring of: A. One hundred thirty–seven wild larvae; B. The rearing outdoors of 112 larvae; C. Changes in day length during the pupation period. All surviving green pupae from (A) and (B) developed into adults in # 21 and # 25 days, respectively (i.e. were non–diapausing). All brown pupae with the exception of the single captive pupa from the first generation entered in diapause: a. 1–7 June; b. 15–21 June; c. 29– 5 July; d. 13–19 July; e. 27–2 August; f. 10–16 August; g. 24–30 August; h. 7–13 September; i. 21– 27 September; j. 5–11 October; k. 19–25 October; l. 2–8 November. Fig. 2. Distribución estacional del color de la pupa de Iphiclides podalirius obtenida a partir de: A. Ciento treinta y siete larvas seguidas en el campo; B. La cría en el exterior de 112 larvas; C. Cambios en la duración del día durante el período de pupación. Todas las pupas verdes supervivientes de (A) y (B) dieron lugar a adultos en # 21 y # 25 días, respectivamente (es decir, no entraron en diapausa). Todas las pupas marrones, con la excepción de la única pupa de este color criada en cautividad y perteneciente a la primera generación, entraron en diapausa: a. 1–7 junio; b. 15–21 junio; c. 29–5 julio; d. 13–19 julio; e. 27–2 agosto; f. 10–16 agosto; g. 24–30 agosto; h. 7–13 septiembre; i. 21–27 septiembre; j. 5–11 octubre; k. 19–25 octubre; l. 2–8 noviembre.

Stefanescu

Table 1. Green (non–overwintering) and brown (overwintering) pupae of Iphiclides podalirius recorded on or off the hostplant. Significance for G test of independence between pupal colour and pupation site: * p < 0.05; *** p < 0.001; # Including one pupa monitored in 1998. (Abbreviations: G. Green pupae; B. Brown pupae; S. Significance; Bs. Blackthorn (shrubs); B1. Blackthorn (one–year old shoots); Pt. Peach tree; Hs. Hawthorn (shrub); T. Total.) Tabla 1. Número de pupas verdes (no hibernantes) y marrones (hibernantes) de Iphiclides podalirius halladas sobre la planta nutricia o entre la vegetación circundante. Se indica la significación de un test G para la independencia entre el color de la pupa y el lugar de pupación: * p < 0,05; *** p < 0.001; # incluye una pupa estudiada en 1998. (Abreviaturas: G. Pupas verdes; B. Pupas marrones; S. Significación estadística; Bs. Endrinos (arbustivos); B1. Endrinos (rebrotes de un año); Pt. Melocotonero; Hs. Majuelo (arbusto); T. Total.)

Tabla 2. Lugares de pupación, altura desde el suelo y diámetro de lugar de pupación en el punto de fijación con el cíngulo para pupas verdes (no hibernantes) y marrones (hibernantes) de Iphiclides podalirius. Significación de un test de U Mann–Whitney: *** p < 0.001. (Abreviaturas: G. Pupas verdes; B. Pupas marrones; Lugar de pupación: Ul. Reverso de una hoja; Gs. Gramínea; We. Tallo de planta herbácea; Wo. Tallo de planta leñosa; Ull. Reverso de una hoja viva; Udl. Reverso de una hoja muerta; Ur. Bajo una roca.)

off

***

Table 2. Pupation sites, height from the ground and diameter of the site at the point of girdle attachment for green (non– overwintering) and brown (overwintering) pupae of Iphiclides podalirius. Significance for Mann–Whitney U test: *** p < 0.001. (Abbreviations: G. Green pupae; B. Brown pupae. Pupation sites: Ul. Underside of leaf; Gs. Grass stem; We. Weed stalk; Wo. Woody stem; Ull. Underside of living leaf; Udl. Underside of dead leaf; Ur. Underside of rock.)

Twig

–

Total

Pupation site On the hostplant

Off the hostplant

(P2 = 9.042, df = 4, p = 0.06), indicating, most probably, a real variation in overwintering survival depending on the season. Pupae artificially placed on hostplants disappeared within a few days in all three years, as a result of bird predation (fig. 4). The Great Tit was repeatedly observed inspecting the hedgerow in search of food and, occasionally taking pupae for consumption. Another very common forager was the Sardinian Warbler Sylvia melanocephala, although no direct observations confirmed that it was actually a predator. Survival of pupae naturally occurring among the leaf litter and those artificially placed on the hostplants was significantly different when data were pooled for all years (Fisher’s exact test, p = 0.009), but not for individual years. Nevertheless, elapsed time before a pupa died was always much longer for pupae in the leaf litter (fig. 4). When comparisons were restricted to pupae presumably preyed upon by birds or small mammals (i.e. after discarding the few cases of invertebrate

Ull

Udl

–

Total

Height above the ground (cm) mean±SD 63.66±9.32 median range n

4.09±0.51 ***

33.5

1–180

1–35

Diameter of substrate (mm) mean±SD 10.09±1.26 median range n

3.49±0.62

1–30

2–50

***

Animal Biodiversity and Conservation 27.2 (2004)

Fates of wild pupae

100 % 80 % 60 % 40 % 20 % 0% Non–overwintering

Overwintering

No remains

Probable bird predation

Predation by Great Tit

Invertebrate predation

Physiological death

Stepped on

Successful emergence

Fig. 3. Fates of 46 non–overwintering and 88 overwintering wild pupae of Iphiclides podalirius monitored in 1996–2000 (see text for more details). Fig. 3. Destino de 46 pupas no hibernantes y de 88 pupas hibernantes de Iphiclides podalirius, seguidas en el campo entre 1996–2000 (ver el texto para más detalles).

Surviving pupae

75 100 125 150 175 200 225 250 275

Among the litter

Hostplant

Days

Successful pupae

Fig. 4. Elapsed time before death for 62 pupae of Iphiclides podalirius naturally overwintering among the leaf litter and 54 pupae artificially placed on the hostplant in 1997–1999. The emergence time of eight successful pupae naturally overwintering among the leaf litter during the same period, is also indicated for comparison. Fig. 4. Tiempo transcurrido antes de la muerte de 62 pupas de Iphiclides podalirius hibernantes entre la hojarasca, y de 54 pupas colocadas artificialmente sobre las plantas nutricias, entre 1997–1999. Se indica también, con fines comparativos, el tiempo de emergencia de los imagos procedentes de ocho pupas hibernantes entre la hojarasca, durante el mismo período.

predation, trampling and physiological deaths), the median of the elapsed time for pupal death was 109 days (n = 52; range: 2–238) and 11 days (n = 54; range: 2–36) for litter (wild) and host (artificially placed) pupae, respectively (Mann– Whitney U test = 4017.5, df = 52, 54; p < 0.0001; p < 0.001 in each year). Discussion This study supports Wohlfahrt’s (1957) general conclusion that green non–diapausing and brown diapausing pupae of I. podalirius are produced when larvae are reared under long and short day length conditions, respectively. However, the occurrence of a single brown non–diapausing pupa in the rearing experiment (fig. 2b) suggests that pupal colour is not entirely controlled by photoperiod under long day conditions. This finding may be interpreted in the context of what is known from Papilio polyxenes and P. troilus (Hazel & West, 1979, 1983), in which short photophases cause the obligate production of brown pupae, while long photophases allow for pupal colour to vary depending on the pupation site. Therefore, though a seasonal polyphenism with respect to pupal colour seems to be the rule in I. podalirius, further research is required to determine which environmental cues may elicit the production of brown pupae under long day length conditions. In I. podalirius, fifth–instar larvae seem to be the most sensitive to photoperiod, with the critical day length for diapause induction being positively correlated with latitude (Friedrich, 1986). In northern Spain, at a latitude of 41º 41’ N, field data showed that the critical photoperiod lies between 13.7 and 14.5 h (corresponding to the first three weeks of August). In this area, the population is bivoltine with a partial third generation. Offsprings of the first generation pupate before August and produce monomorphic green pupae (but see above), while offsprings of the third generation pupate by the end of September at the earliest and produce monomorphic brown pupae. On the other hand, offsprings of the second generation pupate in August and September and produce a mixture of green and brown pupae. This situation provided an excellent opportunity to test and confirm the prediction raised by Clarke & Sheppard (1972), that is, the existence of differences in pupation sites in successive generations related to differences in pupal colour (first and third generation) and, by extension, between green and brown pupae of the second generation. Green and brown pupae strongly differed in their pupation sites: the first were usually found on the hostplant, well above ground level, while the second were always found on the ground, among the leaf litter (tables 1 and 2). It is broadly accepted that pupal colour in swallowtails has evolved in relation to pupation site preference (Hazel & West, 1979) and pupae are thus cryptically camouflaged in their habitats, thereby

Stefanescu

increasing their chances of survival (Wiklund, 1975; West & Hazel, 1982; Hazel et al., 1998). In the present study, pupal mortality was very high and ranged from 14.3–57.1% for green pupae and 76.5– 100% for brown pupae. However, mortalities would have been even higher if pupation site selection had not occurred. For instance, larvae that left the hostplant to produce green pupae did so mainly when they fed on one–year–old blackthorns, on which no pupal survival was recorded. Data from the second field experiment also indicate that natural sites for overwintering pupae are adaptive: all brown pupae artificially placed on the hostplants in three consecutive years disappeared within the first month, while most of those naturally occurring among the leaf litter survived for much longer periods. Although mortality was very high in wild overwintering pupae, it is important to note that each year a considerable proportion (ca. 25%) survived long enough to have eclosed, at least in theory (fig. 4). Habitat selection also meant that pupation usually occurred in the warmer south–facing side of the hedgerow (C. Stefanescu & J. Navarro, unpublished data), allowing a faster post–diapause development of pupae, reducing their time of exposure to predation. Although many wild pupae disappeared without trace (especially during the winter, fig. 3), direct observations and indirect evidence seem to indicate that bird predation was the major mortality factor for non–diapausing pupae and may also have a strong impact on diapausing pupae (Stefanescu, 2000b). In particular, the Great Tit regularly includes Lepidopteran pupae in its diet (e.g. Baker, 1970; Cowie & Hinsley, 1988; Cramp & Perrins, 1993); in the present study, it was the main predator of green pupae but it was also observed capturing a brown pupa among the leaf litter. Visual (avian) predators have long been recognised as the main source of mortality for swallowtail pupae above ground–level, while non–visual predators (small mammals) are thought to be the primary predators of pupae on the ground (West & Hazel, 1982). Hazel (1995) and Hazel & West (1996) further developed this idea and reconstructed the possible events leading to the evolution of plasticity in pupal colour in swallowtail butterflies, starting with the ancestral condition of brown pupae occurring among the leaf litter. Results in the present study somewhat contradict this view: though non–visual predators (especially the shrew and hedgehog) may be responsible for a substantial part of the losses experienced by overwintering pupae, field observations indicate that birds are also probably a very important cause of mortality (see also Stefanescu, 2000b). In my study, other insectivorous birds in addition to the Great Tit (e.g. Anthus pratensis, Turdus merula, Turdus philomelos and Sylvia melanocephala) also spent many hours searching in the vegetation around overwintering pupae and should be consid-

Animal Biodiversity and Conservation 27.2 (2004)

ered as serious potential predators. Furthermore, it should be noted that the role of invertebrate predators (e.g. carabid beetles and ants) as potential predators of pupae among the leaf litter cannot, of course, be disregarded. In relation to the hypothesis of Hazel (1995) and Hazel & West (1996), this study suggests that the selection pressure for pupation sites above groundlevel in summer generations was the combination of non–visual (by invertebrates and small mammals) and visual (avian) predation that affected pupae among the leaf litter. Moreover, selective pressure would also have favoured prepupal larvae staying on the hostplant, thereby reducing mortality during the critical period of wandering in search of another pupation site (e.g. Baker, 1970; C. Stefanescu, unpublished data). The opposite behaviour, however, would have been selected in diapausing broods, taking into account the extremely high mortality to which pupae artificially placed on the hostplant are subject during the winter. Further insight into the mechanisms leading to the selection of distinct pupation sites may be gained from detailed studies on the behaviour exhibited by larvae from either developmental pathway during the wandering phase. For instance, in another related species, Papilio machaon L., the duration of the pre–pupation larval wandering phase seems to be much longer for larvae of the diapausing pathway as compared to larvae of the non– diapausing pathway (C. Wiklund, pers. comm.). A similar behaviour in I. podalirius may well result in larvae from the non–diapausing pathway pupating on and off the hostplants when the plants are large and small, respectively, as indeed occurs. On the other hand, long wandering phases in larvae from the diapausing pathway would always result in pupae away from the hostplant. This and other aspects of the wandering phase (e.g. the timing at which it takes place and the larval orientation) will be considered in a future paper. Acknowledgements I am grateful to Sergi Herrando, Michael Lockwood, José Navarro, Marko Nieminen, Christer Wiklund, two anonymous referees and, especially, Toomas Tammaru and Chris Thomas for useful comments on the manuscript. Jordi Jubany helped in the field work, Ferran Páramo gave technical assistance and Marta Miralles assisted me in many ways. The Butterfly Monitoring Scheme in Catalonia is funded by the Departament de Medi Ambient de la Generalitat de Catalunya. References Baker, R. R., 1970. Bird predation as a selective pressure on the immature stages of the cabbage butterflies, Pieris rapae and P. brassicae. J. Zool., 162: 43–59.

Brakefield, P. M., Shreeve, T. G. & Thomas, J. A., 1992. Avoidance, concealment, and defence. In: The ecology of butterflies in Britain: 93–119 (R. L. H. Dennis, Ed.). Oxford University Press, Oxford. Clarke, C. A. & Sheppard, P. M., 1972. Genetic and environmental factors influencing pupal colour in the swallowtail butterflies Battus philenor (L.) and Papilio polytes L. J. Entom. A, 46: 123–133. Cornell, H. V. & Hawkins, B. A., 1995. Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am. Nat., 145: 563–593. Cowie, R. J. & Hinsley, S. A., 1988. Feeding ecology of Great Tits (Parus major) and Blue Tits (Parus caeruleus), breeding in suburban gardens. J. Anim. Ecol., 57: 611–626. Cramp, S. & Perrins, C. M., 1993. The Birds of the Western Palaearctic. Vol. VII: Flycatchers to Shrikes. Oxford University Press, Oxford. Frank, J. H., 1967. The insect predators of the pupal stage of the winter moth Operophtera brumata (L.) (Lepidoptera: Hydriomenidae). J. Anim. Ecol., 36: 375–389. Friedrich, E., 1986. Breeding butterflies and moths. Harley Books, Essex. Hazel, W. N., 1995. The causes and evolution of phenotypic plasticity in pupal color in swallowtail butterflies. In: Swallowtail Butterflies: Their Ecology & Evolutionary Biology: 205–210 (J. M. Scriber, Y. Tsubaki & R. C. Lederhouse, Eds.). Scientific Publishers, Gainesville. Hazel, W. N., Ante, S. & Stringfellow, B., 1998. The evolution of environmentally–cued pupal colour in swallowtail butterflies: natural selection for pupation site and pupal colour. Ecol. Entom., 23: 41–44. Hazel, W. N. & West, D. A., 1979. Environmental control of pupal colour in swallowtail butterflies (Lepidoptera: Papilioninae): Battus philenor (L.) and Papilio polyxenes Fabr. Ecol. Entom., 4: 393–400. – 1983. The effect of larval photoperiod on pupal colour and diapause in swallowtail butterflies. Ecol. Entom., 8: 37–42. – 1996. Pupation site preference and environmentally cued pupal colour dimorphism in the swallowtail butterfly Papilio polyxenes Fabr. (Lepidoptera: Papilionidae). Biol. J. Linn. Soc., 57: 81–87. Hidaka, T., 1961. Recherches sur le mécanisme endocrine de l’adaptation chromatique morphologique chez les nymphes de Papilio xuthus L. J. Fac. Sci. Tokyo Univ., Sect. IV, 9: 223–261. Instituto Nacional de Meteorología, 1991. Calendario Meteorológico 1991. Ministerio de Transportes, Turismo y Comunicaciones, León. Leather, S. R., Walters, K. F. A. & Bale, J. S., 1993. The Ecology of Insect Overwintering. Cambridge University Press, Cambridge. Poulton, E. B., 1887. An enquiry into the cause and extent of a special colour–relation between certain exposed lepidopterous pupae and the sur-

faces which immediately surround them. Phil. Trans. R. Soc. B, 178: 311–441. – 1892. Further experiments upon the colour relations between certain lepidopterous larvae, pupae, cocoons and imagines and their surroundings. Trans. Entom. Soc. Lond. B, 1892: 293–487. Shapiro, A. M., 1976. Seasonal polyphenism. Evol. Biol., 9: 229–253. Sims, S. R. & Shapiro, A. M., 1984. Pupal color dimorphism in California Battus philenor (L.) (Papilionidae): mortality factors and selective advantage. J. Lepid. Soc., 37: 236–243. Smith, A. G., 1978. Environmental factors influencing pupal colour determination in Lepidoptera I. Experiments with Papilio polites, Papilio demoleus and Papilio polyxenes. Proc. R. Entom. Soc. Lond. B, 200: 295–329. Stefanescu, C., 2000a. El Butterfly Monitoring Scheme en Catalunya: los primeros cinco años. Treb. Soc. Cat. Lepid., 15: 3–46. – 2000b. Bird predation on cryptic larvae and pupae of a swallowtail butterfly. Butll. GCA, 17: 39–49. Stefanescu, C., Pintureau, B., Tschorsnig, H.–P. & Pujade–Villar, J., 2003. The parasitoid complex of the butterfly Iphiclides podalirius feisthamelii (Lepidoptera: Papilionidae) in north–east Spain. J. Nat. Hist., 37: 379–396. Tolman, T. & Lewington, R., 1997. Butterflies of Britain and Europe. Harper Collins, London. West, D. A., 1995. Comparative pupation behavior in the Papilio glaucus group: studies of Papilio glaucus, Papilio eurymedon and their hybrids (Lepidoptera: Papilionidae). In: Swallowtail Butterflies:

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Their Ecology & Evolutionary Biology: 93–99 (J. M. Scriber, Y. Tsubaki & R. C. Lederhouse, Eds.). Scientific Publishers, Gainesville. West, D. A. & Hazel, W. N., 1979. Natural pupation sites of swallowtail butterflies (Lepidoptera: Papilioninae): Papilio polyxenes Fabr, P. glaucus L. and Battus philenor (L.). Ecol. Entom., 4: 387–392. – 1982. An experimental test of natural selection of pupation site in swallowtail butterflies. Evolution, 36: 152–159. – 1996. Natural pupation sites of three North American swallowtail butterflies: Eurytides marcellus (Cramer), Papilio cresphontes Cramer, and P. troilus L. (Papilionidae). J. Lepid. Soc., 50: 297–302. White, R. R., 1986. Pupal mortality in the Bay Checkerspot butterfly (Lepidoptera: Nymphalidae). J. Res. Lepid., 25: 52–62. Wiklund, C., 1975. Pupal colour polymorphism in Papilio machaon and the survival in the field of cryptic versus non–cryptic pupae. Trans. R. Entom. Soc. Lond., 127: 73–84. Wohlfahrt, T., 1954. Beobachtungen über Färbung und Zeichnung an Raupen und Puppen des Segelfalters Iphiclides podalirius (L.) and über die Ursache des Auftretens seiner Sommergeneration in Mitteleuropa. Entom. Z., 64: 161–175. – 1957. Über den Einfluss von Licht, Futterqualität und Temperatur auf Puppenruhe und Diapause des mitteleuropäischen Segelfalters Iphiclides podalirius (L.). Wanderversamml. dt. Entom., 8: 6–14.

Animal Biodiversity and Conservation 27.2 (2004)

Landform resources for territorial nettle–feeding Nymphalid butterflies: biases at different spatial scales R. L. H. Dennis

Dennis, R. L. H., 2004. Landform resources for territorial nettle–feeding Nymphalid butterflies: biases at different spatial scales. Animal Biodiversity and Conservation, 27.2: 37–45. Abstract Landform resources for territorial nettle–feeding Nymphalid butterflies: biases at different spatial scales.— Observations of perch sites for three territorial nymphalid butterflies reveals a bias in landform use at two spatial scales: at macro–scale, sunlit wood edges at the top of slopes; at micro– scale, molehills and bare ground compared to vegetation substrates. There is a hierarchy in landform exploitation; slope and edge position outweighs micro–landform feature use. Landforms for territories tend to be prominent landmarks. This is especially the case at macro–scale (e.g., wood edges and corners); though also the case at micro–scale (e.g., molehills, earth bank edge) it is not invariably the case and highly apparent substrates (white boards) entered into territories were ignored. The predominant characteristic of all landforms chosen is that they are all hotspots: warm and sheltered sites. Substrates used for perching change with ambient conditions. In cool spring weather warm sites are essential for territorial defence, acquisition of females and predator evasion. As air temperatures increase there is an increasing propensity for territorial incumbents to use non–apparent, vegetation substrates. Bare earth sites are suggested to be important habitat components for butterfly biology as is their continued renewal through human activity. Key words: Thermoregulation, Territoriality, Micro–landforms, Molehills, Habitat, Utility–resources. Resumen Utilización de las formas del terreno por los ninfálidos que se nutren de ortigas: sesgos en distintas escalas espaciales.— La observación de los lugares donde se posan tres ninfálidos territoriales revela un sesgo en el uso de las formas del terreno en dos escalas espaciales: a macroescala, en los linderos soleados de los bosques, en la parte superior de las laderas; a microescala, en las toperas y terrenos áridos en comparación con sustratos con vegetación. Existe una jerarquía en lo que respecta a la explotación de las formas del terreno; las laderas y los bordes prevalecen sobre el uso de las microcaracterísticas del terreno. Las formas de terreno empleadas para definir los territorios tienden a ser importantes puntos de referencia. Esto es especialmente cierto a macroescala (por ejemplo, los lindares de los bosques y recodos) y, aunque también es válido a microescala (por ejemplo, toperas, franjas de tierra), se dan excepciones; así, los sustratos muy aparentes (tableros blancos) introducidos en los territorios fueron ignorados. La característica predominante que compartían todas las formas de terreno escogidas es que eran puntos calientes: cálidos y resguardados. Los sustratos empleados para posarse cambian con las condiciones ambientales. Con el clima fresco de la primavera, los lugares cálidos resultan esenciales para la defensa territorial, la adquisición de hembras y la evasión de los predadores. Pero a medida que la temperatura del aire aumenta, quienes han ocupado el territorio tienden a utilizar sustratos con vegetación no aparente. Se ha sugerido que los lugares de terreno árido son importantes componentes del hábitat para la biología de las mariposas, como también lo es su continua renovación a través de la actividad humana. Palabras clave: Termorregulación, Comportamiento territorial, Microcaracterísticas de las formas del terreno, Toperas, Hábitat, Recursos funcionales. ISSN: 1578–665X

Dennis

(Received: 6 VIII 03; Conditional acceptance: 16 X 03; Final acceptance: 10 XI 03) Roger L. H. Dennis, Dept. of Entomology, Manchester Museum, Manchester Univ., Oxford Road, Manchester M13 9PL; and School of Biological and Molecular Sciences, Oxford Brookes Univ., Headington, Oxford OX3 0BP, U K. Eâ&#x20AC;&#x201C;mail: rlhdennis@aol.com

Animal Biodiversity and Conservation 27.2 (2004)

Introduction Males of nettle–feeding Nymphalid butterfly species Inachis io (Linnaeus), Aglais urticae (Linnaeus) and Polygonia c–album (Linnaeus) are known to defend territories, limited areas, to acquire females (Baker, 1972; Dennis & Shreeve, 1988; Rutowski, 1991). Baker (1969) argues that territorial behaviour seems likely to evolve when some requirement, in this case females, is obtained in greater quantity as a result of staying a certain length of time in one suitable area rather than spending some of that time in voluntary displacement from area to area and when the quantity of this requirement is further increased by defending the area against competing individuals. He also argues that male territories are likely to be found in species in which some requirement of the female (e.g., feeding or oviposition sites) occurs in relatively concentrated areas and less likely to be found in species in which female requirements are diffusely scattered through the environment (Baker, 1972). Baker (1972) has explored various aspects of territories, including territory size and territorial behaviour, in the two nymphalids, Inachis io and Aglais urticae (e.g., territory: male ratio; territorial decisions, timing of territorial behaviour; territorial interactions). From this research, we know that these territories are found in distinctive areas; many of the features are shared by the two species. Both select territories on the ground in direct sunlight and both prefer to have some vertical edge on the side away from the sun, typically a line of trees in Inachis io and a wall or hedge in Aglais urticae. The advantage of an edge site is suggested to be that migrating females, searching for oviposition sites, tend to fly along edges for some distance in their search. Corners seem most advantageous to Inachis io. Male A. urticae more typically establish territories in areas with hostplant patches (e.g., nettle patches). Nectar source availability in the territory is not important. However, we have limited information about the nature of the ground occupied by territorial males, the physical features used for perching. The use of different terrain micro–features at the current study site by territorial Inachis io was first noticed in April 1999; male territories were established on earth mounds (molehills) created by moles (Talpa europaea), a burrowing animal, rather than the cut grass surfaces. These observations were repeated in early May 2000 (Dennis, unpublished observations) for Inachis io and Aglais urticae, including the use of an abandoned concrete seat base in the same area. Here I explore several issues associated with territorial perches. Are there consistent patterns in choice of landforms for territorial perches? Is landform choice taking place at several scales, at meso/macro–scale (e.g., hillslopes, edge structures, corner sites) and micro–scale (e.g., molehills)? Which spatial scale is dominant in perch choice? Is there differential use of micro landforms

by different Nymphalid species? If so, what is this related to? Also, does micro-terrain use relate primarily to thermal conditions, to feature prominence (i.e., visual stimuli) (Dennis & Williams, 1987) or to areas where consumable resources (viz., host plants, nectar) occur? The latter finding has relevance for the integration of resources comprising habitats (Dennis et al., 2003).

Methods The study has been undertaken in part of a public park, The Carrs, Wilmslow, Cheshire UK (fig. 1). The area chosen (grid reference: SJ8481), 340 m long by 110 m wide (12,538 m2), comprises a south-west facing slope above the river Bollin, bounded by the river’s north bank at the foot of the slope and by a narrow woodland separating the Carrs from housing at the top of the slope. The south–eastern extremity of the study area effectively forms a large sloping clearing with woodland on three sides. The north west end terminates in an abrupt reflex angle in the wood edge, the corner distinguished by a low bank of rough grass (Dactylis glomerata Linnaeus) centred on a hollow (> 50 cm deep), the previous site of a tree trunk. Most of the study area comprises short mown grass divided up by small copses of trees, though a very narrow strip of uncut grass and scrub borders the wood upslope and a wider (2 to 3 m wide) strip of vegetation including trees, scrub and tall herbs forms the river levée. The host plant for all three nymphalids, Urtica dioica Linnaeus, is restricted to these borders and is substantially more abundant along the river bank (incidence 163 m, 13 m overtopped by vegetation) than along the wood edge at the top of the slope (incidence 58 m, 27 m overtopped). A single path traverses the length of the study area but other, unofficial paths of movement —evident in the flattening of the grass and bare earth patches from foot wear and scuffing— run along the wood edge and riverside. Molehills are concentrated in seven zones, two at the top of the slope (127 molehills) and five at the base of it (835 molehills); The clearing also comprises a concrete rectangle (116 x 167 cm), a disused seat base, 5m from the top of the slope and cut horizontally into it. The mean diameter of molehills is 50.1 ± 1.3 cm and their total area 193.7 m2, occupying 1.54% of the study area. Owing to differences in age and compaction, molehills in the distinct zones contrast in dimensions (F(6,92) = 10.6, P < 0.0001) and their respective total dimensions have been calculated for each zone separately. Uniform transects (N = 36) were conducted over the entire area (N = 12) and the clearing (N = 24) afternoon BST between March 18 and 31, 2003 during dry conditions, in sunshine and when shade air temperatures > 14oC. Wind, varying in strength between 1.5 to 8 m/s, was predominantly from the south (mean 182o ± 42o, minimum 134o and maximum 322o) during the survey. Territories at the study location were identified from fidelity to

sites following voluntary patrols and interactions with intruders (Baker, 1972). Distinct zones of the study area were used repeatedly for perching (fig. 1); territorial interactions (Baker, 1972), between the three species as well as between conspecifics, were observed to occur within each of these zones with one exception at the base of the slope. Records were noted for six classes of perch sites for males in established territories: concrete seat base, molehill, bare earth scuff, vegetation debris (dried leaves and twigs), dead grass and live grass. Observations were also made of behaviour on perches. As it was not possible to establish a secure control site in the park, temperature contrasts for the valley slope and perch sites were taken using repeated (> 10 times) alternate paired measurements with a fast–response thermistor (accuracy ± 0.5oC) between transects. Two white boards (each 25 cm2) were used to test the response of butterflies to enhanced stimuli in the clearing; these presented a cool, glossed white exposed surface. Observations were carried out on two further dry, sunny days (April 15 and 16) when shade air temperatures > 23oC to test perch site use in much hotter conditions. To avoid influencing behaviour, individuals were not marked but identified by distinctive markings. Comparisons of perching sites have been processed for two sets of data, for all records (observations) of perching and separately for all individuals. In the second case, only the first observation of perching has been used. Individual results are coined in terms of null hypotheses. Micro–scale refers to features of < 1 m and macroscale to features at least an order of magnitude greater (> 10 m).

Results Selection of large scale landforms. A comparison of slope base and top Hypothesis: no distinctions exist in territorial perching between the top and base of slope. Five territorial sites were identified at the top of the slope compared to three at the base (fig. 1). However territorial occupancy was substantially greater at the top of the slope for all three nymphalid species. Altogether, almost 10 times more individuals used the top of the slope by the wood edge than the base of it near the river (all records: N = 126 and 11; %2(1) = 31.7, P < 0.0001, single records for individuals: N = 87 and 9; %2(1) = 19.6, P < 0.0001 tests standardised for number of territories). A similar frequency of Inachis io and Polygonia c– album were found at the base and top of the slope; however, significantly more Aglais urticae were found at the base of the slope than for the other two species (all records: I. io versus A. urticae: Fisher exact test, P = 0.0003; P. c–album versus A. urticae: Fisher P = 0.002; Single records for individuals: I. io versus A. urticae, Fisher P = 0.008, P. c–album versus A. urticae, Fisher P = 0.019).

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Selection of micro landforms. Biased use of molehills Hypothesis: no bias occurs in the use of molehills as territorial perches. The three species use molehills significantly and substantially more often than expected by chance based on the area of surfaces available to them (all species lumped together and all records: %2(1) = 85.4, P < 0.0001; all species lumped together and one record per individual, %2(1) = 59.3, P < 0.0001; for the three species separately (all records and one record per individual), %2 tests and Fisher Exact tests, P < 0.001). These results were obtained applying a conservative test, based on the area of molehills as perch sites compared to the area of other sites potentially available to territorial butterflies. This is a conservative test as perches are included for territorial areas at the top of the slope lacking molehills altogether. Comparison of large scale and micro land forms Hypothesis: numbers of perch sites corresponds with the number of molehills. Dominance of the use of molehills over slope position should produce a distribution of perch sites equating with the abundance of molehills. However, perch sites dominated the slope top compared to the slope base despite the fact that favoured perch sites (i.e., molehills) were far more abundant (6.6 times) at the bottom of the slope than at the top of it (all species lumped together and all records: %2(1) = 167.6, P < 0.0001; all species lumped together and one record per individual, %2(1) = 111.2, P < 0.0001). Comparison of perch sites used by the three nymphalid species Hypothesis: there are no distinctions in perch sites among species. Direct comparisons have been made of perch sites by the three nymphalid species. These were found to differ in their exploitation of the six available perch site categories (table 1). They differ significantly in a comparison of bare ground sites versus vegetated sites (all records: %2(2) = 9.12, P < 0.02; one record per individual: %2(2) = 6.13, P < 0.05). However, this distinction may be caused by the dominant use of the concrete seat base by Inachis io (see below). Comparisons with data adjusted for removal of the concrete base showed homogeneity among species in perch type use for molehills (all records and single records per individual, P > 0.10) and bare earth sites (all records and single records for individuals, P > 0.05). Comparisons of the thermal environment and other resources within the study site Hypothesis: the distribution of resources (nectar, host plants and warm areas) does not influence the distribution of perches. At the time of the survey very few nectar sources were available in the study area

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Concrete seat base

A 1

4 5

th Pa

G River Bollin Clearing

Fig. 1. Schematic map of the Carrs study site: Horizontal shading. Woodland and copse; Unshaded areas. Cut grass; Cross hatching. Rough ground dominated by rank herbs and willow carr; Stippled areas. Molehill zones in 2003 (boxes 1 to 7 indicating number of molehills: 1, 66; 2, 61; 3, 209; 4, 128; 5, 250; 6, 62; 7, 186); Pecked lines. Territories for nymphalids labelled A to H (bold, occupancy in > 50% surveys); Star in territory A. Hollowed out tree trunk; Fine arrows. Slope gradient (degrees). Probability of territory occupancy during surveys (multiple occupancy by one or more species): A, 0.75 (0.33); B, 0.83 (0.17); C, 0.08 (0); D, 0.5 (0); E, 0.96 (0.69); F, 0.04 (0); G, 0.33 (0); H, 0.25 (0.08). Fig. 1. Mapa esquemático del lugar de estudio situado en Carrs: Sombreado horizontal. Bosque y soto; Áreas sin sombrear. Forraje; Entramado. Terreno agreste dominado por maleza y zona pantanosa con sauces; Áreas punteadas. Zonas de toperas en 2003 (los recuadros 1–7 indican el número de toperas: 1, 66; 2, 61; 3, 209; 4, 128; 5, 250; 6, 62; 7, 186); Líneas discontinuas. Territorios para los ninfálidos etiquetados A–H (en negrita: ocupación en > 50% de los estudios); Estrella en el territorio A. Tronco de árbol hueco; Flechas delgadas. Pendiente (grados). Probabilidad de ocupación del territorio durante los estudios (ocupación múltiple por una o más especies): A, 0,75 (0,33); B, 0,83 (0,17); C, 0,08 (0); D, 0,5 (0); E, 0,96 (0,69); F, 0,04 (0); G, 0,33 (0); H, 0,25 (0,08).

and none in the vicinity of territories. The host plant for all three nymphalids, Urtica dioica Linnaeus, is substantially more abundant (2.8 times) along the river bank than along the wood edge at the top of the slope. Nettles occurred in the vicinity (but not in) of only two territories (fig. 1, labelled G and H) largely occupied by A. urticae. Macro–site thermal contrasts exist within the study site. In the clearing, air temperatures recorded at the top of the slope, 5 m from the wood edge, are slightly higher than those at the base of the slope (exposed bulb: mean difference = 1.25oC, t = 4.8,

P < 0.002; shaded bulb: mean difference = 0.89oC, t = 2.99, P = 0.02). The difference is greater for ground temperatures, taken from the summit of molehills (mean difference = 3.15 o C, t = 5.2, P = 0.0006). The bias in warmth corresponds with the selection of slope position by nymphalids. Micro–site thermal contrasts also exist within the site. Ground temperatures are substantially warmer than air temperatures (mean 22.0oC versus 16.1oC, difference 5.9oC, t = 8.8, P = 0.00001). Temperatures of the boundary air immediately above the surface of molehills is similar to that of grass sur-

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faces (t = –0.87, P = 0.40) as is that of molehills and the concrete seat base in the clearing (t = 1.05, P = 0.32). However, probe measurements of ground surfaces reveals that the substrates of molehills are significantly warmer than the surrounding grass surfaces and their underlying soil substrates (mean difference = 2.83 oC, t = 10.29, P < 0.00001) or the concrete seat base (mean difference = 1.65oC, t = –4.34, P = 0.002) during the period of the survey. In the former case, the difference in surface probe temperatures decreases as ground temperatures rise (r = –0.56, P = 0.011). Temperature contrasts favour bare earth areas, including molehills, on which biased perching occurs. Thermoregulatory behaviour of nymphalids at the study site Hypothesis: the species show no thermoregulatory (warmth enhancing) behaviour on perches. Individuals of all three nymphalid species display clear thermoregulatory behaviour on perch sites (see Dennis, 1993). Almost invariably males align themselves to the sun’s azimuth when taking up perch stations; one exception was observed for a single event when the sun became obscured. In this position, the wings are generally held open or closed and the body tilted to be orthogonal to the sun’s rays (see Shreeve, 1992). Often the hindwing inner margins and abdomen, referred to as hindwing appression, are in contact with the substrate. Full wing appression to the substrate was witnessed in all species on a number (N = 14) of occasions with the wings wrapped around the cone of the molehill (Shreeve, 1992; Dennis, 1970, 1993). One individual was observed shivering on the day with highest wind speeds and ambient air temperature at 16oC. Some form of shelter from the wind was observed on 70 occasions (51.5%); this took the form of exploiting hollows in the substrate and/or locating on slopes (e.g., of molehills) away from the wind direction. There was no significant difference among species in the use of shelter (%2(2) = 2.8, P = 0.24). Although, together, the two forms of wing appression to substrates were more commonly observed on exposed perches, this was not quite significant (%2(1) = 3.54, P = 0.06). However, hindwing appression also tends to occur, if only inadvertently, when individuals orient towards (body tilt) the sun’s azimuth and hollows were often shallow and may have given inadequate shelter. Landforms as visual landmarks Hypothesis: perch sites are not distinctive land marks. At macro–scale, all perch sites were in the vicinity of prominent structures: edges or corners; none were located in the centre of the study site in open grassland. At micro–scale, territories were not invariably sited where prominent landforms such as molehills were available (see above). Molehills were not exclusively used when they were present nor was the concrete seat base used exclusively in the clearing (table 1). Nevertheless,

biased use was made of the concrete seat base in the clearing by I. io compared to A. urticae and P. c–album (all records: %2(2) = 13.7, P < 0.001; single records per individual: %2(2) = 11.6, P . 0.001). White boards variously placed, singly and together, near and on the concrete base at the top of the clearing within the permanently occupied territories there during one afternoon session of survey were ignored by incumbent territorial Inachis io. Change of perch sites in relation to changing ambient conditions Hypothesis: no changes in type of perch sites used occur with changes in ambient temperatures. Perch usage is influenced by ambient temperature conditions. During two days of much warmer conditions in mid April (> 23oC), when shade air temperatures matched ground temperatures of the main survey period in March, I. io was found to use vegetated surfaces significantly more frequently in the clearing (all surfaces: vegetation use rises from 16% to 45%, %2(1) = 12.9, P = 0.0003; exclusion of concrete base: vegetation use rises from 19% to 61%, %2(1) = 18.3, P < 0.0001). Discussion Landform bias for territories at different spatial scales The current findings demonstrate that the three nymphalid species, I. io, A. urticae and P. c–album are biased, for the purposes of territorial activity and perching, in their use of landscape features at two different scales. At the macro scale they clearly prefer a wood edge or corner at the top of a southfacing slope compared to the base of it along the riverbank. This confirms Baker’s (1972) observations of a bias for sunlit wood edges, a common cue in nymphalids (Watanabe, 2002). At a micro–terrain scale, the species show a substantial bias in using molehills compared to other features. In the case of I. io preference is also shown for a concrete slab though not in A. urticae nor P. c– album but this may be a feature of their being out– competed by I. io for this unique site and substrate. At a higher resolution still, observations revealed finer adjustments to positions on micro–terrain features, for instance to hollows on molehills and molehill slopes (aspect). So, terrain exploitation extends to the infra–molehill level. Hierarchy in landform selection across spatial scales A hierarchy in landscape exploitation exists; decisions at a macro–scale outweigh those at a micro scale, slope position dominating micro–landform (molehill) choice. Some large molehill zones at the foot of the slope were ignored whereas territories were established where no molehills and little bare ground occurred.

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Table 1 Perch sites adopted by three nymphalid species in the study site during spring 2003: Cs. Concrete seat base; M. Molehills; B. Bare earth; Vd. Vegetation debris; Dg. Dead grass; Lg. Live grass. Mean number of territorial males encountered per survey: Inachis io, 1.42; Aglais urticae, 0.78; Polygonia c–album, 0.53; all species, 2.72. Tabla 1. Lugares escogidos para posarse por tres especies de ninfálidos en el lugar del estudio durante la primavera de 2003: Cs. Base de cemento; M. Toperas; B. Terreno árido; Vd. Restos vegetales; Dg. Hierba muerta; LG. Hierba viva. Promedio de machos territoriales encontrados en cada estudio: Inachis io, 1,42; Aglais urticae, 0,78; Polygonia c–album, 0,53; todas las especies, 2,72.

Perch sites All records Species

Total

I. io

A. urticae

P. c–album

All groups

137

Single record for each individual Species

Total

I. io

A. urticae

P. c–album

All groups

Consumer resource distributions and territories Territories (perch sites) were not associated with nectar sources and the host plant occurred near only two of the (weaker) eight territories. Compared to the other two nymphalids, the significantly greater propensity of Aglais urticae for riverbank sites (as opposed to the wood edge) tends to support Baker’s (1972) finding of a greater tendency for territories in Aglais urticae to occur near host plants. The incidence of nettle along the river bank is nearly three times that along the wood edge. Are landforms used for perching landmarks or look–out posts? Territorial sites often provide visual cues for resident males (Dennis & Shreeve, 1988; Rutowski, 1991). However, a distinction necessarily has to be made between sites providing visual cues to enhance conspecific contacts and sites enhancing visibility for resident males (Dennis & Williams, 1987). The findings in this study support Baker’s (1972) observations that macro–scale sites (woodland edges, hedge lines and field corners) provide visual landmarks, locations where females are likely to pass in movement across the countryside. Other species (pierids such as Pieris napi L., Anthocharis

cardamines L. and Gonepteryx rhamni L.) were using the same features (i.e., wood edges in sunshine) as flyways during the survey. At a micro–scale, features such as molehills, the earth bank in territory A and the concrete seat base are clearly distinctive landmarks, in the sense of being visually apparent structures. Yet, by no means were all micro–scale sites prominent from the surrounding matrix (e.g., cut grass, dead leaves) and enhanced visual stimuli (e.g., white boards; discarded magazines by the public, Dennis, personal observation) in territories were ignored. Yet, such stimuli are highly effective in other species (e.g., Ochlodes venata Bremer & Grey; Dennis & Williams, 1987). Although some micro–scale sites may provide prominent look– out posts (e.g., molehill summits) for passing females and intruders, again many do not. Many molehills chosen were flattened and depressed below the grass surroundings. An example of an important site presenting poor visibility was the deep hollow on the earth bank at the apex of territory A. During the strong breeze on March 31 the resident male I. io perched deep inside (> 30cm) this hollow; although still in sunshine, its arc of detection was very restricted. As is frequently the case anyway from perches, this male undertook voluntary patrols to search its

territory returning to this hollow. Such observations suggest that visibility is compromised by ambient conditions and requires an experimental approach to determining which factors dominate under specific conditions. Are landforms used for perching hot spots? Perch biases for the landscape features at different scales all have a common climatic component. They are warmer areas or more sheltered, which amounts to the same thing. It is likely that there are no terrain features that do not have climatic implications, and thus fitness consequences for butterflies as regards mate location. Warmer sites ensure greater motility and mobility, particularly important in the scramble for mates and defence of sites as well as evasion of predators (Shreeve, 1992; Stutt & Willmer, 1998). At the macro–scale, it is not possible to distinguish the impact of the wood edge as a potential visual cue for mate location from its influence as a warmer area enhancing flight and mobility. Light and warmth are inextricably linked, shaded wood edges at one and the same time lack the contrast and warmth of wood edges in sunshine. At the micro–scale, molehills and bare ground substrates are warmer (or provide more shelter) than vegetation surfaces and the bias for bare soil sites supports the notion that they are chosen as hot spots. It was noticeable that sunlight to two of the molehill areas (fig. 1, zones 4 and 6) ignored by perching nymphalids was filtered by trees. Although the concrete base presented a cooler surface than molehills, it provided more shelter from prevailing winds up the slope. Two further observations corroborate this suggestion for hot spots. First, there is a substantial and significant increase in the use of vegetation substrates by I. io in warmer conditions (shade temperature 7oC increase). This observation can be coupled with another for the difference in temperature between ground surfaces for bare soil and grass–covered soil that diminishes as air temperatures increase. In effect, as overall air temperatures rise, the area of ground with minimum suitable temperatures for perching increases and the difference between soil (molehills) and vegetation becomes less critical for perching males. Second, warmth is critical for butterfly activity. For sustained flight, butterfly species with moderate to fast wings beat frequencies typically require thorax temperatures in the range of 28–40oC and for vigorous flight 33–38oC (Kingsolver, 1985), temperatures well above those experienced in the study area during March and early April. Nymphalid males show a range of thermoregulatory behaviour on the micro–scale perch sites: wing and body adjustments to sun azimuth, hindwing, full wing and abdomen appression to substrates, shivering and seeking shelter (i.e., hollows and lee slopes of molehills) in relation to wind (Shreeve, 1992; Maier & Shreeve, 1996; Dennis, 1993; Kemp & Krockenberger, 2002). It was noticeable that wing

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and body appression could not be achieved, and difficulties were experienced in wing orientation to the sun, when vegetation surfaces were used instead of the soil substrates. Butterflies are known to change their mate location behaviour with changing air temperatures (Fischer & Fiedler, 2001; Ide, 2002); this finding now confirms that they may also change their perching sites as temperatures change (Rutowski, 2000). Although just what perch sites they use is affected by what is available, these need to be warm enough for individuals to function efficiently (Maier & Shreeve, 1996). Nymphalids are known to use taller vegetation for territorial perching (e.g., Polygonia comma, P. c–album, Vanessa atalanta) (Bitzer & Shaw, 1979, 1983; Hardy, personal observations), especially during the summer emergence in the UK (Wiltshire, 1997; Dennis, personal observation), further suggesting that access to bare ground in suitable locations becomes less critical as ambient conditions become warmer. Macro– and micro–scale landforms are important resources for butterflies Macro–terrain cues for mate location are common to a number of butterfly species. Both Pieridae (e.g., Pieris napi L., Pieris brassicae L., Anthocharis cardamines L., Gonepteryx rhamni L.) and Nymphalinae share the physical cue of the south– facing wood edge for mate location, but the former invariably patrol along its length whereas the latter perch as well as patrol (Dennis & Shreeve, 1988). At the micro–scale, other Nymphalids are known to use bare ground for territorial perches (e.g., Vanessa atalanta L. and V. cardui L.) (Bitzer & Shaw, 1979; Dennis, personal observations). Nevertheless, bare ground is an important utility resource for a range of activities by butterflies in cool temperate regions; it is part of the habitat (Dennis et al., 2003) and is a component of the hostplant biotopes of at least 24 British butterflies (Shreeve et al., 2001). Because of rapid vegetation succession it is a short– lived resource and needs to be continuously created by disturbance. The use of molehills for mate location forms one of several examples of butterflies using micro– terrain created by animals for its activities (e.g., egglaying by Lasiommata megera L. Satyrinae in recesses caused by rabbits and cattle hoof marks) (Dennis, 1983). However, by far the greatest number of relief features used by butterflies, as currently known, is created by human activity. These range from "hills" and "hollows" at the macro–scale (e.g., Neolithic burial tombs, hill fort ramparts and ditches, spoil heaps, quarries and bomb craters) to similar features at a micro–scale (e.g., field ridge and furrow, drainage lines, piles of gravel) associated with agriculture and construction, including elements of landscape furniture (e.g., fences, walls) all of which are known to be used by butterflies for different activities. Bearing in mind how important,

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but short–lived, a resource bare ground is for butterfly biology, the creation of bare ground is one area where human activity is clearly beneficial to butterfly persistence, especially as it triggers early seral vegetation for butterflies dependent on pioneer host plants.

Acknowledgements My thanks to Peter Hardy for his comments on the paper and observations on perching nymphalids and to two referees and Dr. Adolfo Cordero Rivera for their helpful comments on an earlier draft.

References Baker, R. R., 1969. The evolution of the migratory habit in butterflies. J. Anim. Ecol., 38: 703–746. – 1972. Territorial behaviour of the Nymphalid butterflies, Aglais urticae (L.) and Inachis io (L.). J. Anim. Ecol., 41: 453–469. Bitzer, R. J. & Shaw, K. C., 1979. Territorial behaviour of the red admiral Vanessa atalanta (Lepidoptera: Nymphalidae). J. Res. Lep., 18: 36–49. – 1983. Territorial behaviour of Nymphalis antiopa and Polygonia comma. J. Lepid. Soc., 37: 1–13. Dennis, R. L. H., 1970. Note on the relation of Aglais urticae L. to direct and shade temperatures. Ent. Rec. J. Var., 82: 302. – 1983. Egg–laying cues in the wall brown butterfly, Lasiommata megera (L.) (Lep., Satryidae). Ent. Gaz., 34: 89–95. – 1993. Butterflies and Climate Change. Manchester University Press, Manchester, UK. Dennis, R. L. H. & Shreeve, T. G., 1988. Hostplanthabitat structure and the evolution of butterfly mate–location behaviour. Zool. J. Linn. Soc., 94: 301–318. Dennis, R. L. H., Shreeve, T. G. & Van Dyck, H., 2003. Towards a functional resource–based concept for habitat: a butterfly biology viewpoint. Oikos, 102: 417–426. Dennis, R. L. H. & Williams, W. R., 1987 Matelocation behaviour in the butterfly Ochlodes

venata (Br. and Grey) (Hesperiidae). Flexible strategies and spatial components. J. Lepid. Soc., 41: 45–64. Fischer, K. & Fiedler, K., 2001. Resource-based territoriality in the butterfly Lycaena hippothoe and environmentally induced behavioural shifts. Anim. Behav., 61: 723–732. Ide, J. Y., 2002. Seasonal changes in the territorial behaviour of the satyrine butterfly Lethe Diana are mediated by temperature. J. Ethol., 20: 71–78. Kemp, D. J. & Krockenberger, A. K., 2002. A novel method of behavioural thermoregulation in butterflies. J. Evol. Biol., 15: 922–929. Kingsolver, J. G., 1985. Butterfly thermoregulation: organismic mechanisms and population consequences. J. Res. Lep., 24: 1–20. Maier, C. & Shreeve, T. G., 1996. Endothermic heat production in three species of Nymphalidae. Nota Lepid., 18: 127–137. Rutowski, R. L., 1991. The evolution of male matelocating behavior in butterflies. Amer. Nat., 138: 1121–1139. – 2000. Postural changes accompany perch location changes in male butterflies (Asterocampa leilia) engaged in visual mate searching. Ethol, 106: 453–466. Shreeve, T. G., 1992. Adult behaviour. In: The Ecology of Butterflies in Britain: 22–45 (R. L. H. Dennis, Ed.). Oxford University Press, Oxford, UK. Shreeve, T. G., Dennis, R. L. H., Roy, D. B. & Moss, D., 2001 An ecological classification of British butterflies: ecological attributes and biotope occupancy. J. Insect Conserv., 5: 145–161. Stutt, A. D. & Willmer, P., 1998. Territorial defence in speckled wood butterflies: do the hottest males always win? Anim. Behav., 55: 1341–1347. Watanabe, M., 2002. The existence and its function of territorialism in overwintering population of Polygonia c–aureum (Linnaeus) (Lepidoptera, Nymphalidae). Trans. Lepid. Soc. Japan., 53: 83–102. Wiltshire, E. P., 1997. Territorial red admirals: behaviour of Vanessa atalanta (Lepidoptera: Nymphalidae) in a Berkshire garden during the 1995 heatwave. Entomologist, 116: 58–65.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Animal Biodiversity and Conservation 27.2 (2004)

The relationship between haematocrit and some biological parameters of the Indian shad, Tenualosa ilisha (Family Clupeidae) L. A. Jawad, M. A. Al–Mukhtar & H. K. Ahmed

Jawad, L. A., Al–Mukhtar, M. A. & Ahmed, H. K., 2004. The relationship between haematocrit and some biological parameters of the Indian shad, Tenualosa ilisha (Family Clupeidae). Animal Biodiversity and Conservation, 27.2: 47–52. Abstract The relationship between haematocrit and some biological parameters of the Indian shad, Tenualosa ilisha (Family Clupeidae).— Haematological parameters have been recognised as valuable tools for the monitoring of fish health. Here we analyse the relationship between haematocrit and body length, sex and reproductive state in the Indian Shad Tenualosa ilisha. Haematocrit value showed a quadratic relationship to fish size (body length), incrementing as the fish body length increased up to 400 mm, after which it decreased. Male fish showed a higher haematocrit value than females. Haematocrit appeared to be higher in the pre–spawning period than in the spawning phase, but then increased slightly in the post– spawning period. Key words: Haematology, Tenualosa ilisha, Basrah, Iraq. Resumen Relación entre el hematocrito y algunos parámetros biológicos del sábalo de la India, Tenualosa ilisha (Familia Clupeidae).— Se ha demostrado que los parámetros hematológicos constituyen una valiosa herramienta para controlar la salud de los peces. En este artículo se analiza la relación entre el hematocrito y la longitud del cuerpo, el sexo y el estado reproductivo del sábalo de la India Tenualosa ilisha. Se ha encontrado una relación cuadrática entre el valor del hematocrito y el tamaño del pez (longitud del cuerpo), en aumento con la longitud del cuerpo, hasta los 400 mm, para después empezar a disminuir. Los valores del hematocrito de los peces machos son más elevados que los de las hembras. Parece que el hematocrito es más elevado en el periodo anterior al desove que durante el mismo, aunque en el período posterior se registra un ligero aumento. Palabras clave: Hematología, Tenualosa ilisha, Basora, Irak. (Received: 1 II 00; Conditional acceptance: 8 II 01; Final acceptance: 10 XI 03) L. A. Jawad, Museum of New Zealand, Te Papa, 169 Tory St., Wellington, New Zealand.– M. A. Al– Mukhtar, Dept. of Marine Vertebrates, Marine Science Centre, Univ. of Basrah, Basrah, Iraq.– H. K. Ahmed, Halton College, Kingsway, Widnes, Cheshire, WA8 6AH, UK.

ISSN: 1578–665X

Jawad et al.

Introduction Haematological parameters have been recognised as valuable tools for the monitoring of fish health (Bhaskar & Rao, 1984; Schuett et al., 1997) and in helping fishery biologists interpret physiological responses to environmental stress, information which is specially relevant when comparing studies of different fish species living in contrasted habitats (Fasihuddin & Kumari, 1990; Ivanc et al., 1996; Zhiteneva et al., 1997; Leonard & McCormick, 1999; Zhiteneva, 1999). It has been observed that blood parameters such as haematocrit, haemoglobin concentration and RBC count are related to environmental factors such as water temperature and salinity (Graham, 1997). Additionally, the relationship between haemoglobin and oxygen differs between loading and unloading sites and shows adaptations not only to environmental conditions but also to metabolic requirements, both of which govern oxygen availability and transport to tissues (Weber & Wells, 1989). Such adaptations may involve quantitative changes in total Hb content, or qualitative changes in Hb–oxygen– binding properties, and may appear both at the inter– and intra–specific level (Weber & Wells, 1989). Thus, the remarkable diversity of oxygen transport properties results from evolutionary processes through subtle sequence differences in haemoglobin that appear to match the varied metabolic demands of animals with the environmental oxygen supply (Wells, 1999). In spite of the vast number of reports on the haematology of the different species of fish, only a few studies have investigated the relationship between haematological parameters and aspects of fish biology such as body length, sex and the reproductive period (Pandy et al., 1976; Zhiteneva & Goroslovskaya, 1986; Canfield et al., 1994). The aim of this work was to determine the relationship between haematocrit and biological parameters in the Indian shad T. ilisha.

marsh area just north of Basrah city, Iraq. The upper limit of its northern distribution is Al-Hammar Marsh (180 km north of Basrah city). T. ilisha has a multispawn ability and has a long spawning season, which may last from May to August (Husain et al., 1991). Its absolute fecundity has been estimated to be in the range of 450,000–1,600,000 eggs per female (Jabir & Faris, 1989). It may reach 2,000,000 depending on the size of the fish (Hussain et al., 1991). It is well known that fecundity of the fish correlates positively with the square length of the fish (Wootton, 1990). Maturing individuals entering the Shatt al– Arab River range between 200 mm and 550 mm in total length, while a few immature fish enter the same waterway as small as 220 mm in length (Jabir & Faris, 1989). Fish specimens (N = 400) were collected from Shatt al–Arab River at Basrah city, Iraq, in 1990. Immediately after capture, blood was sampled at the collection site by cutting the caudal peduncle without anaesthesia in small fish, and by direct sampling from the heart with a hypodermic needle for the larger specimens. They were later measured to the nearest mm. To determine haematological values, the blood was kept in tubes containing EDTA as an anticoagulant and in an icebox with ice. They were processed within a few hours of collection. The haematocrit value or packet cell volume was determined with a microhematocrit pipette. Blood samples were centrifuged for 5 min (12,000 rpm). Haematocrit value was determined according to the method described in Al–Abood & Al–Hassan (1988). Haematocrit was measured for each individual fish. Specimens (389) were dissected to determine sex and stage of maturity. Three stages were recognised, pre–spawning (fish with developing gonads that might contain eggs of sperms), spawning (fish with fully developed gonads containing well–developed eggs or sperms) and post–spawning individuals (fish with spent gonads).

Materials and methods

Results

The Shatt al–Arab River is formed by the confluence of the two major rivers in Mesopotamia, the Tigris and Euphrates at Qarmat Ali, 160 km north of the Arabian Gulf. This river flows in a south–eastern direction toward the Arabian Gulf. Water temperature shows a marked seasonal variation reaching a maximum in July (32oC) and a minimum in December (15oC) (Al–Hassan & Hussain, 1985). The Indian shad, Tenualosa ilisha, is an anadromous clupeid fish, and represents one of the most important fisheries in the estuarine waters and some distance up stream (Sarma, 1984). In the Arabian Gulf area, this species is found along the Iranian side of the gulf and moving northward toward the estuary of Shatt al–Arab River in Iraq and other rivers in Iran (Al–Hassan, 1993). T. ilisha ascends Shatt al–Arab River and reaches the great

The relationship between body length and haematocrit The haematocrit value differed according to the total length of the fish (ANOVA, F 5,381 = 5136, P < 0.001) (table 1). Multiple pair–wise comparisons suggested that all the length groups differed from each other (Tukey tests all P < 0.001) with the exception of the 200+mm length group in comparison with the 500+mm group (TUKEY test, P = 0.99). Haematocrit value showed a polynomial relationship (quadratic regression) to the length of the fish (Ht = –5.7 + 0.2801 x L – 0.000387 x L2; R2 = 0.78, P < 0.001, F2,384 = 6.78, P < 0.001). Fish in the smallest size group (0–100 mm) had the lowest values for haematocrit (table 1). This increased as the fish length increased up to a certain level, so

Animal Biodiversity and Conservation 27.2 (2004)

that the fishes in the size group 301–400 mm showed the highest haematocrit values, after which no further increase was noted. The relationship between fish haematocrit, sex and spawning period Males showed a higher haematocrit value than females, independently of body length (tables 2, 3). Haematocrit value was higher at the beginning of maturation, it then decreased in April when the fish started to spawn, and increased slightly in the post-spawning period (tables 3, 4). Pre– and post–spawning periods had a higher Ht level than the spawning period (table 5). Pre– and post– spawning periods did not differ in Ht level (table 5). This seasonal variation was similar in both sexes (two–way ANOVA, interaction Sex x Period not significant; F–value 0.03; df 2,69; p. 97; table 3, fig. 1). When sex and spawning period were taken into account, the relationship of haematocrit and fish length disappeared (table 3).

Table 1. Total length and blood haematocrit value of Tenualosa ilisha: BL. Body length groups (in mm); N. Number of fishes; ML. Mean length (in mm ± SE); Ht. Haematocrit value (% ± SE). Tabla 1. Longitud total y valor del hematocrito sanguíneo de Tenualosa ilisha: BL. Grupos de longitug corporal (en mm); N. Número de peces; ML. Longitud media (en mm ± EE); Ht valor del hematocrito (% ± EE). BL

Ht %

0–100

78.65 ± 0.84

13.22 ± 0.83

101–200

85 137.15 ± 0.85

24.85 ± 0.70

201–300

90 262.40 ± 0.07

37.74 ± 0.08

301–400

74 330.19 ± 0.81

52.05 ± 0.80

401–500

35 445.53 ± 0.18

43.23 ± 0.19

501–600

30 534.50 ± 0.12

24.17 ± 0.13

Discussion The general trend in the relationship between blood haematocrit and body length is the longer the fish, the higher the haematocrit in Cyprinus carpio, for example, Murachi (1959) found that haematocrit increased as the fish length increased. Similar results were obtained for Clarius batrachus (Joshi & Tandon, 1977). Male T. ilisha showed higher blood haematocrit values than females in all the length groups studied. This is in agreement with results from other fish species (Telapia zilli, Ezzat et al. (1973) [Ezzat et al., 1973]; Cyprinus carpio Fourie & Hattingh (1976) [Fourie & Hattingh, 1976]; Cyprinion macrostomus Al–Mehdi & Khan (1984) [Al–Mehdi & Khan, 1984];

Amphiprous cuchia Banerjee (1986) [Banerjee, 1986]. Fouri & Hattingh (1976) suggested that the differences in haematocrit between the two sexes are genetically determined, although Raizada et al. (1983) considered that the differences might be due to the higher metabolic rate of males compared to females. Our results support this suggestion, which has been related to an increase in fish activity with an increase in size (Chaudhuri et al., 1986). It is generally stated that the blood haematocrit value in fish increases during the spawning season (Joshi & Tandon, 1977; Khan, 1977; Leonard &

Table 2. Sex and blood haematocrit value, Ht (% ± SE) of Tenualosa ilisha: BL. Body length; N. Number of fishes. Tabla 2. Sexo y valor del hematocrito sanguíneo, Ht (% ± EE) de Tenualosa ilisha: BL. Longitud corporal; N. Número de peces.

N BL

0–100

12.42 ± 0.04

101–200

24.87 ± 0.85

201–300

34.67 ± 0.07

301–400

401–500

501–600

t–test

11.08 ± 0.05

2.34

< 0.05

23.28 ± 0.05

2.41

< 0.05

33.62 ± 0.08

2.22

< 0.05

52.78 ± 0.83

50.73 ± 0.08

2.35

< 0.05

45.22 ± 0.12

41.91 ± 0.03

2.19

< 0.05

23.79 ± 0.18

23.49 ± 0.09

2.24

< 0.05

Jawad et al.

McCormick, 1999). This increase has been interpreted in relation to the high–energy requirements of fish during the breeding season. On the other hand, Sano (1963) and Einszporn–Orecka (1970) reported a marked reduction in haematocrit during gonadal development in both sexes of cultured trout, interpreted as a result of the depletion of nutritive substances during spawning. This agrees with the finding in the present study in T. ilisha. During the spawning season, the water temperature in Shatt al–Arab River is at its highest level (July, 32oC), resulting in less oxygen content in the water which might cause the rise in haematocrit value. Hence, two factors are probably responsible for the rise in haematocrit value: a physiological factor evoked by a high energy demand during the breeding season and an environmental factor induced by the rise in water temperature. Several authors have shown how environmental factors such as water temperature have a direct effect on different blood parameters such as haematocrit through their effect on the haemoglobin oxygen–binding properties and thus on oxygen trans-

Table 3. ANCOVA on the relationship between fish sex, spawning period and length (as covariate) of Tenualosa ilisha: S. Sex; Sp. Spawning period; L. Length. Tabla 3. ANCOVA de la relación entre sexo, el período de desove y la longitud (como covariable) de Tenualosa ilisha: S. Sexo; Sp. Periodo de desove; L. Longitud.

Factors

F–value

266.74

1,46

139.17

2,46

0.04

2,45

0.95

P 0

S x Sp

0.03

2,69

0.97

SxL

0.01

2,62

0.97

Sp x L

0.03

2,60

0.98

S x Sp x L

0.02

2,68

0.97

Table 4. Blood haematocrit, Ht (% ± SE), fish sex and different spawning periods of Tenualosa ilisha: Pre–Sp. Pre–spawning period; Sp. Spawning period; Pst–Sp. Post–Spawning period. Tabla 4. Hematocrito sanguíneo, Ht (% ± EE), sexo y distintos períodos de desove de Tenualosa ilisha: Pre–Sp. Periodo previo al desove; Sp. Periodo de desove; Pst–Sp. Periodo posterior al desove.

Ht Sex

Pre–Sp

Males

34.36 ± 0.18

33.38 ± 0.15

34.29 ± 0.18

Pst–Sp

Females

33.52 ± 0.16

31.12 ± 0.16

33.45 ± 0.16

Table 5. Post hoc comparisons (Tukey test) within and between spawning periods and within and between sexes: Pre–Sp. Pre–spawning period; Sp. Spawning period; Pst–Sp. Post–Spawning period. Tabla 5. Comparaciones post hoc (test de Tukey) en los períodos de desove y entre los mismos, y en los sexos y entre los mismos: Pre–Sp. Periodo previo al desove; Sp. Periodo de desove; Pst–Sp. Periodo posterior al desove. Male Pre–Sp

Female

Pst–Sp

Pre–Sp

0.0003

1.0000

0.0012

Pst–Sp

Male Pre–spawning Spawning

0.0003

0.0009

Post–spawning

0.0004

Female Pre–spawning Spawning

0.0000

0.9992 0.0001

Animal Biodiversity and Conservation 27.2 (2004)

Females

24 Ht level

Ht level

Males

21 20

20 120

130 140 150 160 Length (mm)

170

180

120

140 160 180 Length (mm)

200

Fig. 1. Length versus haematocrit value by gender and spawning period of T.ilisha: a. Pre–spawning period; b. Spawning period; c. Post–spawning period. Fig. 1. Longitud según el valor del hematocrito, por género y período de desove de T. ilisha: a. Período anterior al desove; b. Período de desove; c. Período posterior al desove.

port (Di Prisco & Tamburrini, 1992; Wells, 1999). On the other hand, T. ilisha is a migratory fish and enters rivers at the stage when the fish are ready to lay their eggs. Such activity leads this fish species to face changes in the external salinity which in turn produces changes in the distribution of water masses and in the total amount of haemoglobin (Parry, 1961). Increases in osmoregulatory work might be expected to produce an increase in the blood oxygen carrying capacity, which in turn would bring about a significant change in the haematocrit value, by the same reasoning as for temperature. However, changes in water balance will cause an osmotic effect in the red blood cell, finally increasing haematocrit (Cameron, 1970). Different rates of fish activity demand different levels of metabolic activity. Such activity requires several physiological adjustments. These include haematological parameters (Putman & Freel, 1978), which play a significant role in the increase of blood supply to the muscle through their variation. Haematocrit is one of those parameters that showed a general correlation with fish activity. T. ilisha might need to be more active and thus increase its metabolic rate if environmental changes such as water quality or destruction of breeding niches occur in its natural habitat. The recent diversions in Shatt al–Arab River directions have led not only to changes in the water quality of the lower reaches, ultimately changing water salinity, but also to the disappearance of major marsh areas where T. ilisha usually lay their eggs (Munro

& Towron, 1997). Haematological parameters may therefore be of value in monitoring the effects of habitat changes on fish biology. References Al–Abood, A. Y. & Al–Hassan, L. A. J., 1988. Haematocrit value in some freshwater fishes of Iraq. Basrah J. Agri. Sci., 1: 31–34. Al–Hassan, L. A. J., 1993. Additional synopsis of biological data on Tenualosa ilisha. Marina Mesopotamica (Suppl. No. 2): 1–23. Al–Hassan, L. A. J. & Hussain, N. A., 1985. Hydrological parameters influencing the penetration of Arabian Gulf fishes into the Shatt Al–Arab River, Iraq. Cybium, 9(1): 7–16. Al–Mehdi, M. I. A. & Khan, A. A., 1984. Haematology of a freshwater carp, Cyprinion macrostomus from northern Iraq. Envirn. Ecol., 2(3): 222–226. Banerjee, V., 1986. Haematology of a freshwater eel, Amphipnous cuchia (Hamilton): Erythrocyte dimensions with special reference to body length, sex and season. Comp. Physiol. & Ecol., 2(2): 68–73. Bhaskar, B. R. & Rao, K. S., 1984. Influence of environmental variables on haematological ranges of milkfish, Chanos chanos (Forskal), in brackish–water culture. Aquaculture, 83(1–2): 123–136. Cameron, J. N., 1970. The influence of environmental variables on the hematology of pinfish, Lagodon

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Animal Biodiversity and Conservation 27.2 (2004)

Taxonomic notes on Amarodytes duponti (Aubé, 1838) (Dytiscidae, Hydroporinae, Bidessini) with redescription of male genitalia C. J. Benetti & J. A. Régil Cueto

Benetti, C. J. & Régil Cueto, J. A., 2004. Taxonomic notes on Amarodytes duponti (Aubé, 1838) (Dytiscidae, Hydroporinae, Bidessini) with redescription of male genitalia. Animal Biodiversity and Conservation, 27.2: 53–56. Abstract Taxonomic notes on Amarodytes duponti (Aubé, 1838) (Dytiscidae, Hydroporinae, Bidessini) with redescription of male genitalia.— The male genitalia of the water beetle Amarodytes duponti (Aubé, 1838) are described and illustrated. The species was collected in small pools of rainwater on the margins of a river. A. duponti is distinguished from other species of the genus by the presence of bi–segmented parameres. This species is related to Bidessodes Régimbart, Hypodessus Guignot and Tepuidessus Spangler. Key words: Coleoptera, Dytiscidae, Bidessini, Amarodytes duponti, Brazil. Resumen Notas taxonómicas sobre Amarodytes duponti (Aubé, 1838) (Dytiscidae, Hydroporinae, Bidessini) con redescripción de la genitalia masculina.— Se describe e ilustra la genitalia masculina del coleóptero acuático Amarodytes duponti (Aubé, 1838). Los especímenes fueron capturados en pequeñas pozas de origen pluvial, en los márgenes de un río. A. duponti se distingue de otras especies del género por presentar parámeros con dos segmentos. Esta especie está relacionada con Bidessodes Régimbart, Hypodessus Guignot y Tepuidessus Spangler. Palabras clave: Coleópteros, Dytiscidae, Bidessini, Amarodytes duponti, Brasil. (Received: 3 VII 03; Conditional acceptance: 2 X 03; Final acceptance: 1 XII 03) Cesar João Benetti*, Dept. de Ecología y Biología Animal, Fac. de Ciencias, Univ. de Vigo, 36200 Vigo, España (Spain).– Juan Antonio Régil Cueto(2), Dept. de Biología Animal, Fac. de Biología, Univ. de León, 24071 León, España (Spain). * Corresponding author: C. J. Benetti. E–mail: cjbenetti@uvigo.es

ISSN: 1578–665X

Introduction The Neotropical genus Amarodytes Régimbart, 1900 is made up of 10 species, all from South America (Biström, 1988; Nilsson, 2001; Young, 1969). Although it has been considered a typical Bidessini to date, Biström (1988) places it in a separate group as “Insertae sedis” together with the also Neotropical genus Hydrodessus J. Balfour–Browne, taking into account the presence of one–segmented parameres. This characteristic is not present in other genera of Bidessini. Following the study of an unidentified species of Amarodytes, Miller (2001) confirms its placement in the tribe Bidessini, based on the presence of a spermathecal spine. However, the phylogenetic analysis places Amarodytes sp. at the base of the tribe Bidessini, apart from the other genera, according to the author. Amarodytes duponti described by Aubé (1838), was mentioned by several authors, cited in catalogues or lists of species (Gemminger & Harold, 1868; Zimmermann, 1920; Blackwelder, 1944; Tremouilles, 1995). Diagnoses can be found in Sharp (1882), Regimbart (1900) and Gschwendtner (1935). However, only external morphological characteristics have been considered and no description of male genitalia has been given or illustrated to date. Costa et al. (1988) described the larvae of a bidessine, which they claim to be A. duponti. An adult specimen of this species is also illustrated in their paper. The analysis of the male genitalia of A. duponti allowed us to clearly observe the presence of twosegmented parameres, different from A. percosioides Régimbart, the type species of Amarodytes, which has simple parameres. Therefore, A. duponti is considered a typical Bidessini, according to the paramere segmentation, proposal by Biström (1988). Results Amarodytes duponti (Aubé, 1838) Hydroporus Duponti Aubé, 1838: 568 (original description); Gemminger & Harold, 1868: 432. Bidessus duponti (Aubé), Sharp, 1882: 369; Blackwelder, 1944: 76. Amarodytes Duponti (Aubé), Régimbart, 1900: 527; Gschwendtner, 1935: 151. Bidessus (Amarodytes) Duponti (Aubé), Zimmermann, 1920: 61. Amarodytes duponti (Aubé), Young, 1969: 1; Biström, 1988: 36; Costa et. al., 1988: 82; Tremouilles, 1995: 47; Nilsson, 2001: 110.

Type locality: “Brazil” Description Body form ovate, constricted between pronotum and elytra, with general coloration reddish–black, total length: 2.6 to 3.0 mm. Head without a cervical line; black with one pale cervical patch, near pronotum, pointed in part, with

Benetti & Régil Cueto

two longitudinal lines of strongly printed punctures between the eyes and with microreticulation regular. Antennae slender, with 11 subconical antennomeres, the hind antennomer enlarged; coloration reddish brown, with hind antennomer darkened, clypeus not margined; Palpi with apical segment darkened, enlarged and bifid. Pronotum with lateral margin curved, broader near the head, with basal striae oblique and deeply marked, and with a basal depression in the middle, without transverse carina, broad anteriorly, near the head; posterior edge broken, projected slightly backwards (fig. 1). Pronotum dark, with two pale transverse marks in the antero–lateral region, near the head; pubescent and regularly pointed. Elytra without basal, sutural or accessory striae; but with oblique depression extending to suture; elytral apex slightly depressed, rounded, not truncate. Elytra pubescent, with punctuation very marked and regular, without micro–reticulation. Black, with three or four small pale marks, with the following arrangement: one basal–median small mark; two sub median lateral marks, sometimes joined, the external oval with one projection apical and the internal smaller, rounded; one third apical mark, small, sometimes absent (fig. 2). Ventral side completely black, with punctuation very marked in the hind coxae and the two first abdominal sternite. Prosternum and mesosternum smooth, metasternum with punctures scattered and with some setae. Prosternal process with apical portion acuminate and deeply emarginate. Epipleura basally without a pit posteriorly delimited by a transverse carina, only slightly depressed and smooth, finely punctate and with short setae. Metacoxal lines slightly divergent in front. Abdominal sternites III and IV finely punctate and setae mainly in the middle; sternites IV–VI with hind margin pointed and with setae short. Anal sternite not emarginated, making it sexually dimorphic: in the male with punctures in the posterior edge and a group of setae present, not depressed; in the female only scattered punctures, without a group of setae and with depression rounded and folded in middle. Fore and middle tarsi pseudotetramerous, the fourth segment concealed by the lobes of the third. Legs reddish brown, hind and middle tibia with long swimming setae. Male genitalia: aedeagus subtriangular with apex narrow and very tapering in dorsal view (fig. 3A); slightly curved to the ventral side in lateral view (fig. 3B). Parameres two–segmented, with the superior segment smaller and narrower than the basal (fig. 3C). Variation: some specimens possess a distinct elytral pattern consisting of three or four pale elongated marks in the basal region, sometimes joined; one lateral mark near the apex, sometimes absent and one small apical mark. Material studied Brazil, Gramado, State of Rio Grande do Sul, River Cai, 340 m of altitude, 25 II 2001 (37 exx.: 24

Animal Biodiversity and Conservation 27.2 (2004)

Fig. 1. Dorsal view of Amarodytes duponti (Aubé) (SEM). Fig. 1. Vista dorsal de Amarodytes duponti (Aubé) (MEB). Fig. 2. Right elytra of A. duponti (Aubé). Fig. 2. Élitro derecho del A. duponti (Aubé). males and 13 females), deposited in Laboratory of Entomology of Universidade do Vale do Rio dos Sinos, São Leopoldo, Brazil; Brazil, Rio Claro, State of São Paulo (2 males), deposited in Museum of Zoology of Universidade de São Paulo. Distribution Brazil, states of Rio Grande do Sul, São Paulo and Santa Catarina (Gschwendtner, 1935). Ecologic notes This species was collected in small rainwater pools

on the margins of a river. A plant–free rock substrate is characteristic of these pools. The specimens were collected with individuals of Desmopachria nitida Babington and Copelatus longicornis Sharp. Costa et al. (1988) stated that Amarodytes duponti was collected in pools in the rock bed of “Rio Claro”, São Paulo, Brazil.

0.4 mm

Fig. 3. A. duponti (Aubé): A. Aedeagus, dorsal view; B. Aedeagus, lateral view; C. Paramere, lateral view. Fig. 3. A. duponti (Aubé): A. Edeago, vista dorsal; B. Edeago, vista lateral; C. Parámero, vista lateral.

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Discussion

Acknowledgements

A. duponti differs from A. percosioides, type species of Amarodytes, mainly in the form of the aedeagus and parameres. In A. duponti, the aedeagus is subtriangular an parallel with the apex tapering and slightly curved in lateral view; the parameres are slender with two segments. In A. percosioides, the aedeagus is slender and subparallel, with the apex rounded and strongly curved in lateral view; the parameres are very broad and simple, and not segmented (Biström, 1988). Other than genitalia, A. duponti differs from A. percosioides in its very narrow pronotum in relation to the elytra; the pronotum without a transverse carina with a concave centre; non–excavated epipleura, and the shape of the prosternal process. This species appears to be closely related to genus Bidessodes Régimbart, Hypodessus Guignot and Tepuidessus Spangler, considering its external and internal morphologic characteristics, specially the presence of two–segmented parameres and lack of cervical line. It differs from these other genera based on the following characters: very marked pronotal striae, absence of elytral striae (basal, sutural and accessory), distinctive coloration and marks on the pronotum and elytra, an emarginated prosternal process, the epipleura not excavated and lacking transverse carinae, the anal sternite not emarginate, and genitalic characters. New studies with the other species of the genus Amarodytes are necessary, in addition to other species of near genus in order to clarify important taxonomic aspects. An alternative could be the creation of a new genus, that is justified based on the divergent characteristics of A. duponti in relation to the A. percosioides (type species of Amarodytes) and other genera of the Bidessini tribe, in addition to Amarodytes and Hydrodessus. Following the key proposed by Biström (1988), the species A. duponti would be classified as pertaining to the Bidessodes genus, but the analysis of different character diagnostics does not allow to include A. duponti in Bidessodes. A phylogenetic analysis of the genera of Bidessini, including Amarodytes and Hydrodessus, based on their species type, is necessary to discover relationships among them.

We wish to thank Dr. Olof Biström (University of Helsinki) and Dr. Ignacio Ribera (Museo Nacional de Ciencias Naturales, Madrid) for their cooperation; the Departamento de Biología Animal of the Universidad de León, Spain, for the use of the scanning electron microscope and the images analyzer and Deyse Cristina Queiroz Silva and Nicolás Perez Hidalgo for the drawings. References Aubé, C. A., 1838. Species general des Hydrocanthares et Gyriniens. Spec. Col., 6: 1–804. Biström, O., 1988. Generic review of the Bidessini (Coleoptera, Dytiscidae). Acta zool. fenn., 184: 1–41. Blackwelder, R., 1944. Checklist of the Coleopterous Insects of Mexico, Central america, the West Indies and South America. Bull. U. S. nat. Mus., 185(1): 72–82. Costa, C., Vanin, S. A. & Casari–Chen, S. A., 1988. Larvas de Coleoptera do Brasil. Museu de Zoologia, Universidade de São Paulo, São Paulo. Gemminger, M. & Harold, E. von, 1868. Dytiscidae. Catalogus Coleopterorum synonymicus et systematicus, 2: 425–467. Gschwendtner, L., 1935. Neue sudamerikanische Dytisciden. Ent. Anz., 15: 151–152. Miller, K. B., 2001. On the phylogeny of the family Dytiscidae (Insecta: Coleoptera) with an emphasis on the morphology of the female reproductive tract. Insect Syst. Evol., 32: 45–92. Nilsson, A. N., 2001. Dytiscidae. World Catalogue of Insects, 3: 1–395. Regimbart, M., 1900. Sur quelques dytiscides nouveaux de l´Amérique Méridionale. Annali Mus. civ. Stor. nat. Genova, 40: 524–530. Sharp, D., 1882. On aquatic carnivorous Coleoptera or Dytiscidae. Scient. Trans. R. Dubl. Soc., (2)2: 179–1003. Tremouilles, E. R., 1995. Coleoptera. Dytiscidae, Subfam. Methlinae–Hydroporinae. Fauna de Agua Dulce de la Republica Argentina, 37(1): 1–82. Young, F. N., 1969. A checklist of the American Bidessini (Coleoptera: Dytiscidae–Hydroporinae). Smithson. Contr. Zool., 33: 1–5. Zimmermann, A., 1920. Dytiscidae, Haliplidae, Hygrobiidae, Amphizoidae. In: Coleopterorum Catalogus, 71: 1–326 (W. Junk & S. Schenkling, Eds.). W. Junk, Berlin.

Animal Biodiversity and Conservation 27.2 (2004)

Effects of natural phenomena and human activity on the species richness of endemic and non–endemic Heteroptera in the Canary Islands J. M. Vargas, J. C. Guerrero & R. Real

Vargas, J. M., Guerrero, J. C. & Real, R., 2004. Effects of natural phenomena and human activity on the species richness of endemic and non–endemic Heteroptera in the Canary Islands. Animal Biodiversity and Conservation, 27.2: 57–66. Abstract Effects of natural phenomena and human activity on the species richness of endemic and non–endemic Heteroptera in the Canary Islands.— The geographical patterns of Heteroptera species diversity in the Canary Islands were analysed, and endemic and non–endemic species were studied both together and separately. Causal processes most likely controlling these patterns, as well as the theory of island biogeography, hypotheses about evolutionary time, habitat heterogeneity, climatic stability, intermediate disturbances, energy, environmental favourableness–severity, productivity and human influence were investigated. The combination of habitat heterogeneity and human influence accounted for the total number of species. However, when endemic and non–endemic species were analysed separately, habitat heterogeneity and favourableness–severity explained the richness of endemic species, whereas habitat heterogeneity and human influence explained that of non–endemic species. Key words: Canary Islands, Heteroptera, Species richness, Biogeography. Resumen Efectos de los fenómenos naturales y la actividad humana sobre la riqueza específica de heterópteros endémicos y no endémicos de las Islas Canarias.— En el presente trabajo se analiza la distribución geográfica de los heterópteros en las Islas Canarias, tomando en consideración las especies endémicas y no endémicas juntas y por separado. Asimismo se investigan los procesos causales que con mayor probabilidad controlan los patrones de distribución resultantes, poniendo a prueba la teoría de la biogeografía insular y las hipótesis del tiempo evolutivo, de la heterogeneidad de hábitats, de la estabilidad climática, de las perturbaciones a escala intermedia, de la energía, de la favorabilidad–severidad ambiental, de la productividad y de la influencia humana. El número total de especies sobre las islas queda explicado por una combinación de la heterogeneidad de hábitats y de la influencia humana. Sin embargo, cuando se analizan las especies endémicas y no endémicas por separado, la heterogeneidad de hábitats y la favorabilidad–severidad explican la riqueza específica de las endémicas mientras que la heterogeneidad de hábitats y la influencia humana explican la riqueza específica de las especies no endémicas. Palabras clave: Islas Canarias, Heteroptera, Riqueza específica, Biogeografía. (Received: 18 VI 02; Conditional acceptance: 13 IX 02; Final acceptance: 3 XII 03) J. Mario Vargas, José C. Guerrero & Raimundo Real, Dept. de Biología Animal, Fac. de Ciencias, Univ. de Málaga, 29071 Málaga, España (Spain). Corresponding author: J. M. Vargas. E–mail: jmvy@uma.es

ISSN: 1578–665X

Vargas et al.

Introduction The description and analysis of the geographical trends in species diversity and the testing of explanatory hypotheses are of major concern when assessing the biodiversity of an area. Several practical and philosophical problems must be solved to approach these analyses adequately. Regarding insular faunas, most studies about species diversity are based on the theory of island biogeography of MacArthur & Wilson (1967) which considers area and isolation as the determinant factors of the number of species that inhabit the islands (see, for example, Sfenthourakis, 1996; Dennis & Shreeve, 1997; Hanski & Gyllenberg, 1997). However, Williamson (1989) encouraged the search for explanations of biodiversity patterns beyond the theory of MacArthur and Wilson. Haila (1990) and Fox & Fox (2000), for example, suggested that a realistic vision of insular ecology should include the development of alternative hypotheses about the dynamics that may have an important role in the system studied. Some authors, such as Brown & Lomolino (2000), consider that a new paradigm shift is currently in the making regarding island biogeography (Lomolino, 2000). Human presence is prevalent in nearly all islands, and biogeographical interpretations and conservation efforts must take into account that the interconnection between human activity and natural phenomena explains the current patterns of insular biodiversity (Chown et al., 1998). Insular biotas are more vulnerable to human influence than those of continental regions, as the proportion of endemic species, with small distribution areas, is higher in the islands (Sadler, 1999). Kitchener (1982) showed that the best predictors for species richness might differ for endemic species when compared to the predictors for introduced species (see also Chown et al., 1998; Fox & Fox, 2000). The concept of native species is ambiguous, as ecologists do not use this term consistently (Callicott et al., 1999; Shrader–Frechette, 2001). In islands which have been inhabited by humans for a long time it is almost impossible, given the scarcity of palaeoecological data, to distinguish between non–endemic native species and those species introduced by humans (Willerslev et al., 2002). Particularly in oceanic islands, the only operational distinction is between endemic species, which are generally native, and non–endemic species, which are generally colonizers. Human impact on islands tends to jeopardize endemic species while providing new habitats and means of dispersion for colonizers (Sadler, 1999). Therefore, it is necessary to consider endemic and non–endemic species separately when assessing the influence of human activity on species richness in islands. Heteroptera of the Canary Islands are well recollected and understood taxonomically (Heiss & Báez, 1990; Heiss & Ribes, 1992; Ribes & Ribes, 1997; Heiss, 1997). The Canary Islands are characterized by a rather diverse fauna of Heteroptera, which comprises more than 350 species, over

25% of which are endemic to the archipelago (Ribes & Ribes, 1997). Becker (1992) analysed the number of species of Heteroptera in the Canary Islands, but did not take into account the influence of human activity or consider endemic species separately. In this paper, geographical patterns of heteropterous species diversity in the Canary Islands are identified, and endemic and non–endemic species are studied together and separately, in an attempt to detect the causal processes, whether natural or human–induced, that most likely control those patterns. Material and methods Study area The Canary Islands, constituted by seven major islands and a set of small islets, are located off the north–western coast of Africa. Along with the archipelagos of Azores and Hawaii, they are one of the largest strings of volcanic islands worldwide (Schmincke, 1976). Although the genesis of the Canary Islands is similar to that of other oceanic islands, their eruptive history has been longer and more complex, comprising a time span of more than 20 m.y. in contrast with the few million years of other island groups (López–Ruíz, 1985). As a result, endemic species and genera make up a significant proportion of their biota. The Canary Islands have a heterogeneous climate which, according to the bioclimatic classification of Rivas–Martínez (1993), belongs to the Mediterranean macrobioclimate, showing at least two months of aridity after the summer solstice. Precipitation tends to decrease from north to south and from west to east, increasing considerably with elevation (Vega, 1992). The variables and hypotheses Table 1 shows the list of variables used and their sources. The numbers of species of Heteroptera (total and endemic) for the Canary Islands were taken from Heiss & Báez (1990), Heiss & Ribes (1992), Ribes & Ribes (1997), Heiss (1997), and Báez & Zurita (2001). There are a total of 363 heteropterous species in the archipelago, 105 of which are endemic. The following explanatory hypotheses were tested: Evolutionary time (Pianka, 1966; Rohde, 1992) A new habitat or niche that becomes available, not used previously by any species, will be occupied if there is sufficient time for a suitable species to evolve. Older islands are more likely to have undergone a more complex history (Margalef, 1963). The history of volcanic islands has a special influence on the evolution of insular fauna;

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Table 1. Ejército, Instituto Instituto

List of variables and their sources. Sources: Juan et al., 2000 (1); Servicio Geográfico del 1975 (2); Quirantes–González & Pérez–González, 1991 (3); Rivas–Martínez, 1987 (4); Nacional de Meteorología, 2000 (5); Font, 1983 (6); Vega, 1992 (7); Coma, 1979 (8); Canario de Estadística, 1995 (9); Martín et al., 2001 (10).

Tabla 1. Listado de variables y su procedencia. (Ver arriba.)

Variables

Geological Age (1) Elevation range–ER (2) Distance to the continent (2) Minimum distance between islands (2) Surface area (2) Number of ecosystems–NE (3) Number of phytoclimatic regions–PR (4) Number of successional vegetation series–VS (4) Number of bioclimatic elevation belts–BB (4) Temperature range (5) Precipitation range (5) Maximum precipitation recorded in 24 hours (5) January temperature (5) July temperature (5)

January humidity (5) July humidity (5) Mean annual days with precipitation–DP (6) Hours of sunshine (6) Potential evapotranspiration (6) Number of days with fog–DF (6) Mean Annual Temperatures ((7) Mean Annual Precipitation (7) Actual evapotranspiration (8) Number of inhabitants–NI (9) Population density (9) Cropland surface percentage (9) Total cropland surface–CS (9) Number of plant species–NP (10)

some islands could have begun as smaller isles and later joined, and eruptions may have divided an island into isolated parts which might favour the allopatric differentiation of vagile species (Machado, 1992). A direct relationship between the number of endemic species and the geological age of each island is expected according to this hypothesis. Habitat heterogeneity (Pianka, 1966) The more heterogeneous and complex the physical environment, the more complex and diverse the animal communities that inhabit it. This hypothesis predicts direct relationships between species richness and number of plant species, elevation range, number of ecosystems on each island, number of phytoclimatic regions, number of ecological successions of vegetation, and number of bioclimatic elevation belts, as these variables indicate different levels of habitat heterogeneity. Climatic stability (Klopfer, 1959) A climatically stable environment allows the existence of more niches with predictable resources on which rare species can specialize, thus favouring an increase in faunal diversity. On the contrary, a fluctuating environment may increase the extinction rate in the island or preclude specialization, thereby decreasing the species richness of the island (Brown & Lomolino, 1998). According to this hypothesis, inverse relationships between the number of species and temperature range and precipitation range are expected.

Intermediate disturbances (Connell, 1978) Disturbances of intermediate magnitudes and frequencies maintain higher levels of diversity. The maximum precipitation recorded in 24 hours, as an estimate of the intensity of floods, and the maximum precipitation recorded in 24 hours/mean annual days with precipitation, as an estimate of their severity, are variables related to disturbances. The relationship between species richness and the associated variables could be direct, inverse or unimodal. Energy Hutchinson (1959) proposed that energy might determine the species richness of an area. This idea was further developed by Connell & Orias (1964), Brown (1981), and Wright (1983). The main argument is that a population requires a minimum amount of energy to subsist. In this way, the energy available limits the number of populations that may share this energy in a specific region. This hypothesis may be tested by searching for direct relationships between the number of species and certain variables related to solar energy, such as mean annual temperature, annual hours of sunshine, potential evapotranspiration, January temperature, and July temperature. Environmental favourableness–severity (Richerson & Lum, 1980) When the environmental parameters are close to optimal values for the physiological requirements

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of the species, organisms may specialize with respect to more physical gradients, and may use a higher amount of energy, matter, and genome to make co–adaptive adjustments to other species. The mean values of the environmental variables are suitable indices to test this hypothesis (Richerson & Lum, 1980). Direct, inverse or unimodal responses of species richness are expected with respect to mean annual days with precipitation, number of days with fog, January humidity, and July humidity; inverse or unimodal responses are expected with respect to the variables related to energy, namely mean annual temperature, annual potential evapotranspiration, annual number of sunshine hours, January temperature, and July temperature. Productivity hypothesis of Tilman (1982) Over a range of resources that goes from extremely poor to low, the greater the availability of resources, the higher the number of species. In a moderate range of resources the species richness will be maximum, and it will decrease as the resources become more abundant. Annual precipitation and evapotranspiration have been used as predictors of productivity (see Rosenzweig, 1968; Leith, 1975). According to Mittelbach et al. (2001), species richness is expected to show direct, inverse or unimodal responses to the associated variables. Island biogeography theory (MacArthur & Wilson, 1967) The number of species is directly related to the surface area and inversely to the degree of isolation of the islands. The distance to the continent, the minimum distance between islands, and the surface area of each island were used to test this hypothesis. Human influence (Simberloff, 1986) Human presence and activity may jeopardize the survival of some species but may favour others by providing suitable habitats for them. In particular, agricultural systems often consist of many species of introduced plants that constitute new habitats for phytophagous insects, which, in turn, constitute new habitats for entomophages. In this study, the number of heteropterous species, as well as the number of endemic and non–endemic species separately, was related to the number of inhabitants, population density, cropland surface percentage, and total cropland surface of each island. Direct or inverse relationships would be in accordance with the hypothesis. Statistical analyses The total number of heteropterous species, the number of heteropterous species endemic to the archipelago, and the total number of non–endemic heteropterous species were analysed separately.

The normality of the variables was tested by means of the Kolmogorov–Smirnov test. Each hypothesis was studied separately relying on bivariate analyses as stepwise variable selection techniques make some questionable assumptions and their results may be of doubtful biological validity (James & McCulloch, 1990; Chown et al., 1998). Linear regressions to detect monotonic responses (either direct or inverse) of the species richness to each variable analysed, and second–degree polynomial regressions to detect unimodal responses were performed. To prevent the increase of the error type II that may be caused by testing several hypotheses simultaneously, the Bonferroni sequential test was used (Rice, 1989), starting with a significance level = 0.05 divided by the number of hypotheses. A stepwise multiple regression of the species richness was performed to explain species richness (S) by a combination of several hypotheses only on the variables that remained significant after applying the Bonferroni test in the bivariate analysis (James & McCulloch, 1990). The variables selected by the multiple regression in the variance partitioning procedure called partial regression analysis (Legendre, 1993) were then used. The part of the variance in species richness explained by the multhat is due to each selected tiple regression hypothesis exclusively and the part due to the shared action of different hypotheses was thus specified. To do this, each selected environmental variable related to a hypothesis was regressed in turn onto the subset of selected variables related to other hypotheses, and only the regression residuals, which represent the part of the variation that is not explained by other hypotheses, were retained. The was assessed pure effect of each hypothesis by regressing S on the residuals of the variables related to the hypothesis. The variation due to the sharedaction of two hypotheses was obtained by subtracting from the pure effect of the two hypotheses involved .The unexplained variation of S was . Results Total number of heteropterous species Significant linear regressions of the number of heteropterous species (S) on nine variables were found. However, only four remained significant after applying the Bonferroni sequential test. The variables involved were, in decreasing order of explanatory power, the number of plant species (NP), the number of inhabitants (NI), total cropland surface (CS), and number of natural ecosystems (NE), all directly related with the number of species (fig. 1). These relations were predicted by the hypotheses of habitat heterogeneity and human influence. According to the Bonferroni test, the number of species of heteroptera (S) followed a lineal regresión with NP, NI, CS and NE (directly related)

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300

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200000 400000 600000 800000 NI

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Fig. 1. Bivariate linear regressions of the number of heteropterous species (S) on environmental variables that remained significant after applying Bonferroni’s sequential test. (Abbreviations of environmental variables as in table 1; FU. Fuerteventura; GC. Gran Canaria; GO. Gomera; HI. El Hierro; LA. Lanzarote; PA. La Palma; TE. Tenerife.) Fig. 1. Regresiones lineales bivariantes del número de especies de heterópteros (S) sobre las variables ambientales que permanecieron significativas tras aplicar la prueba secuencial de Bonferroni. (Abreviaturas de las variables ambientales como en la tabla 1; FU. Fuerteventura; GC. Gran Canaria; GO. Gomera; HI. El Hierro; LA. Lanzarote; PA. La Palma; TE. Tenerife.)

according to the test of the following paragraph (stepwise multiple regression) the number of species of heteroptera (S) on the Canary Islands depends directly on the combination of NE and CS according to the equation. Using stepwise multiple regression, the number of heteroptera species (S) was significantly explained by the combination of the number of natural ecosystems (NE) and the total cropland surface (CS), which are included in the model in this order, according to the following equation: S = 0.158021 x NP + 0.049346 x CS – 9.152072 R2 = 0.99342; p = 0.00001 The hypotheses of habitat heterogeneity and human influence are not therefore mutually exclusive, but they combine to explain the species richness of Heteroptera in the Canary Islands. Partial regression analysis showed the following partition of the variance of S:

Part of variance explained exclusively by NP: = 0.14838; Part of variance explained exclusively by CS: = 0.02798; Part of variance explained by the SharedAction of NP and CS: = 0.81706; Unexplained variance: 1 – R2 = 0.00658. Endemic heteroptera species Linear regressions of the number of heteroptera species endemic to the Canary Islands (ES) were significant with twelve variables, although only eight of these passed the Bonferroni sequential test, namely, in decreasing order of explained variance, number of natural ecosystems (NE), elevation range (ER), number of plant species (NP) number of days with fog (DF), number of ecological successions of vegetation (VS), number of bioclimatic elevation belts (BB), number of phytoclimatic regions (PR) and mean annual days with precipitation (DP)

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(fig. 2), all directly related with the number of endemic species. No significant unimodal model was obtained. The hypotheses selected were therefore those of habitat heterogeneity and environmental favourableness–severity, with six and two variables involved, respectively. Using stepwise multiple regression the number of endemic heteropterous species (ES) was significantly explained by the combination of the number of natural ecosystems (NE), and number of days with fog (DF), which are included in the model in this order, according to the following equation: ES = 4.973214 x NE + 2.294643 x DF – 13.491071 R2 = 0.99038; p < 0.0001 The hypotheses of habitat heterogeneity and environmental favourableness–severity were not thus mutually exclusive, but when combined they accounted for the species richness of endemic Heteroptera species in the Canary Islands. The result of the partial regression analysis showed the following partition of the ES variance: Part of variance explained exclusively by NE: = 0.13463; Part of variance explained exclusively by DF: = 0.03561; Part of variance explained by the sharedaction of = 0.82014; NE and DF: Unexplained variance: 1 – R2 = 0.00962. Non–endemic heteropterous species Linear regressions of the number of non–endemic heteropterous species (NES) were found for nine variables, although only three remained significant after applying the Bonferroni test, namely number of plant species (NP), number of inhabitants (NI), and total cropland surface (CS), all directly related to the number of species (fig. 3). These relations were predicted by the habitat heterogeneity hypothesis and the human influence hypothesis. Using stepwise multiple regression, the number of non–endemic heteropterous species was significantly explained by the combination of the number of plant species (NP), and the total cropland surface (CS), which is included in the model according to the following equation: NES = 0.100187 x NP + 0.051906 x CS + 8.349266 R2 = 0.98473; p = 0.0002 The hypotheses of habitat heterogeneity and human influence were not mutually exclusive, but in combination they explained the species richness of Heteroptera in the Canary Islands. The result of the partial regression analysis showed the following partition of the variance of NES: Part of variance explained exclusively by NP: = 0.10333; Part of variance explained exclusively by CS: = 0.05364;

Part of variance explained by the sharedaction of = 0.82776; NP and CS: Unexplained variance: 1 – R2 = 0.01527. Discussion Different processes for endemic and non–endemic species Results from the present study show that factors accounting for the richness of endemic and nonendemic Hereroptera species differ. Becker (1992) found that the species richness of both predatory and herbivore Heteroptera in the Canary Islands was significantly related to plant species richness. However, Becker (1992) did not distinguish between endemic and non–endemic species in Heteroptera. Our results show that, although both groups of species are related to vegetation, endemic species respond to natural habitat heterogeneity while non–endemic species respond to the number of plant species, which included introduced plant species, and to the availability of new habitats due to agricultural activity. This is consistent with the results of Kitchener (1982), who showed that for some groups of vertebrates, the best predictors for species richness were different for those species recorded only in natural vegetation when compared to those for species found in disturbed situations. The variance partitioning analysis revealed a high proportion of sharedaction of the cropland surface of the islands and the number of natural ecosystems or the number of plant species. This may be due to the effect of area, because larger islands support more diverse ecosystems, more plant species and larger cropland surface. This would be consistent with the finding of Becker (1992) that the number of species of predatory Heteroptera in the Canary Islands was significantly related to the area of the islands. However, after taking into account the effect of habitat heterogeneity and human activity, the effect of area is negligible. This might be a rather common pattern for insects. Abbott (1974), for example, found that area was of minor importance in explaining insect species richness on the southern ocean islands while plant species richness accounted for most variation in insect species richness, and Williams (1982) found that plant species richness was an important predictor of insect richness but that area was less important. The role of habitat heterogeneity Insular habitat heterogeneity has been reported to have an effect on species richness for other groups of arthropods as well. Owen & Smith (1993) found that the total number of species and the number of endemic species of lepidoptera in the Canary Islands, Azores and Madeira were significantly cor-

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Fig. 2. Bivariate linear regressions of the number of endemic heteropterous species (ES) on environmental variables that remained significant after applying the Bonferroni sequential test. (For abbreviations of environmental variables see table 1, for other abbreviations see figure 1.) Fig. 2. Regresiones lineales bivariantes del número de especies de heterópteros endémicos (ES) sobre las variables ambientales que permanecieron significativas tras aplicar la prueba secuencial de Bonferroni. (Para las abreviaturas de las variables ambientales ver tabla 1, para otras abreviaturas ver figura 1.)

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Fig. 3. Bivariate linear regressions of the number of non–endemic heteropterous species (NES) on environmental variables that remained significant after applying the Bonferroni sequential test. (For abbreviations of environmental variables see table 1, for other abbreviations see figure 1.) Fig. 3. Regresiones lineales bivariantes del número de especies de heterópteros no endémicos (NES) sobre las variables ambientales que permanecieron significativas tras aplicar la prueba secuencial de Bonferroni. (Para las abreviaturas de las variables ambientales ver tabla 1, para otras abreviaturas ver figura 1.)

related with vegetation diversity, and Sfenthourakis (1996) considered that habitat diversity was the most important factor determining terrestrial isopod species richness in the Aegean archipelago. Natural habitat heterogeneity also plays a role for non–endemic Heteroptera. Such a role has been reported for other groups of species; Chown et al. (1998), for instance, found that indigenous vascular plant species richness was important in determining alien insect species richness in southern ocean islands, although this relationship was modified by the extent of human activity, as an increase in both plant species richness and human activity provoked an increase in alien insect species richness. The role of human activity on non–endemic species Invading species have been shown to be more successful in habitats altered by human activities

than in undisturbed habitats inhabited by locally adapted native species (Elton, 1958; Sax & Brown, 2000). Simberloff (1986) suggested that new plants introduced into islands constitute food or shelter for new insects, and some of these new insects become prey species for yet other predatory and parasitic insects. In this way, habitat change in islands, such as those created by agriculture, may increase the probabilities of success for many alien species. In natural ecosystems the resident insect community may present predatory or competitive resistance to alien invasions that are not exerted in agricultural systems, which are novel for native species. Notwithstanding this, the presence of introduced species in natural ecosystems could be of concern for the conservation of endemic fauna, since Fox & Fox (2000) considered the presence of invasive species as a form of disturbance for indigenous species (see also Fox & Fox, 1986).

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References Abbott, I., 1974. Numbers of plants, insect and land bird species on nineteen remote islands in the Southern hemisphere. Biological Journal of the Linnean Society, 6: 143–152. Báez, M. & Zurita, N., 2001. Hemiptera Heteroptera. In: Lista de especies silvestres de Canarias (hongos, plantas y animales terrestres): 182–197 (I. Izquierdo, J. L. Martín, N. Zurita & M. Arechavaleta, Eds.). Consejería de Política Territorial y Medio Ambiente, Gobierno de Canarias, La Laguna. Becker, P., 1992. Colonization of islands by carnivorous and herbivorous Heteroptera and Coleoptera: effects of island area, plant species richness, and "extinction" rates. Journal of Biogeography, 19: 163–171. Brown, J. H., 1981. Two decades of homage to Santa Rosalía: toward a general theory of diversity. American Zoologist, 21: 877–888. Brown, J. H. & Lomolino, M. V., 1998. Biogeography. Sinauer, Sunderland. – 2000. Concluding remarks: historical perspective and the future of island biogeography theory. Global Ecology and Biogeography, 9: 87–92. Callicott, J. B., Crowder, & Mumford, A. K., 1999. Current Normative Concepts in Conservation. Conservation Biology, 13: 22–35. Chown, S. L., Gremmen, N. J. M. & Gaston, K. J., 1998. Ecological biogeography of southern ocean islands: Species–area relationships, human impacts, and conservation. American Naturalist, 152: 562–575. Coma, J. E. (Ed.),1979. Mapa Hidrogeológico Nacional. Explicación de los mapas de lluvia útil, de reconocimiento hidrogeológico y de síntesis de los sistemas acuíferos. Memoria del Instituto Geológico y Minero de España, División de Aguas Subterráneas, Madrid. Connell, J. H., 1978. Diversity in tropical rain forest and coral reefs. Science, 199: 1302–1310. Connell, J. H. & Orias, E., 1964. The ecological regulation of species diversity. American Naturalist, 98: 399–414. Dennis, R. L. H. & Shreeve, T. G., 1997. Diversity of butterflies on British Islands: ecological influences underlying the roles of area, isolation and the size of the faunal source. Biological Journal of the Linnean Society, 60: 257–275. Elton, C. S., 1958. The ecology of invasions by animals and plants. Methuen, London. Font, I., 1983. Atlas climático de España. Instituto Nacional de Meteorología, Madrid. Fox, B. J. & Fox, M. D., 2000. Factors determining mammal species richness on habitat islands and isolates: habitat diversity, disturbance, species interactions and guild assembly rules. Global Ecology and Biogeography, 9: 19–37. Fox, M. D. & Fox, B. J., 1986. The susceptibility of natural communities to invasion. In: The ecology of biological invasions: 57–66 (R. H. Groves & J. Burdon, Eds.). Australian Academy of Science,

Camberra. Haila, Y., 1990. Toward an ecological definition of an island: a northwest European perspective. Journal of Biogeography, 17: 561–568. Hanski, I. & Gyllenberg, M., 1997. Uniting two general patterns in the distribution of species. Science, 275: 397–400. Heiss, E., 1997. Nachtrag zur Heteropterousnfauna der Kanarischen Inseln. V (Insecta, Heteroptera). Bericht des Naturwissenschaftlich–medizinischen Vereins in Innsbruck, 84: 359–369. Heiss, E. & Báez, M., 1990. A preliminar catalog of the Heteroptera of the Canary Islands. Vieraea, 18: 281–315. Heiss, E. & Ribes, J., 1992. Additions to the Heteroptera–fauna of the Canary Islands. I. Boletim do Museu Municipal do Funchal, 44: 77–102. Hutchinson, G. E., 1959. Homage to Santa Rosalía, or why are there so many kinds of animals? American Naturalist, 93: 145–159. Instituto Canario de Estadística, 1995. Anuario Estadístico de Canarias. http://www.istac.rcanaria.es. Instituto Nacional de Meteorología, 2000. Guía resumida del clima en España (1971–2000). Plan Estadístico Nacional 2001–2004. Centro de Publicaciones del Instituto de Medio Ambiente, Madrid. James, F. C. & McCulloch, C. E., 1990. Multivariate analysis in ecology and systematics: panacea or Pandora’s box. Annual Review of Ecology and Systematics, 21: 129–166. Juan, C., Emerson, B. C., Oromí, P & Hewitt, G., 2000. Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends in Ecology & Evolution, 15: 104–109. Kitchener, D. J., 1982. Predictors of vertebrate species richness in nature reserves in the Western Australia wheatbelt. Australian Wildlife Research, 9: 1–7. Klopfer, P. H., 1959. Environmental determinants of faunal diversity. American Naturalist, 93: 337–342. Legendre, P., 1993. Spatial autocorrelation: trouble or new paradigm? Ecology, 74: 1659–1673. Leith, H., 1975. Modeling the primary productivity of the world. In: Primary productivity of the biosphere: 237–263 (H. Leith & R. H. Wittaker, Eds.). Springer–Verlag, New York. Lomolino, M. V., 2000. A call for a new paradigm of island biogeography. Global Ecology and Biogeography, 9: 1–6. López–Ruíz, J., 1985. El volcanismo de las Islas Canarias. Mundo Científico, 17: 892–900. MacArthur, R. H. & Wilson, E. O., 1967. The theory of island biogeography. Princeton University Press, Princeton. Machado, A., 1992. Monografía de los Carábidos de las Islas Canarias. Instituto de Estudios Canarios, La Laguna. Margalef, R., 1963. On certain underlying principles in ecology. American Naturalist, 97: 357–374. Martín, J. L., Izquierdo, I., Arechavaleta, M., Delgado, M. A., García Ramírez, A., Marrero, M. C., Martín, E., Rodríguez, L., Rodríguez Núñez, A. & Zurita,

N., 2001. Las cifras de la biodiversidad taxonómica terrestre de Canarias. In: Lista de especies silvestres de Canarias (hongos, plantas y animales terrestres): 15–26 (I. Izquierdo, J. L. Martín, N. Zurita & M. Arechavaleta, Eds.). Consejería de Política Territorial y Medio Ambiente, Gobierno de Canarias, La Laguna. Mittelbach, G. G., Steiner, C. F., Scheider, S. M., Gross, K. L., Reynolds, H. L., Waide, R. B., Willig, M. R., Dodson, S. I. & Gough, L., 2001. What is the observed relationship between species richness and productivity? Ecology, 82: 2381–2396. Owen, D. F. & Smith, D. A. S., 1993. The origin and history of the buttefly fauna of the North Atlantic Islands. Boletim do Museu Municipal do Funchal, 45 (Supl. 2): 211–241. Pianka, E. R., 1966. Latitudinal gradients in species diversity: a review of concepts. American Naturalist, 100: 33–46. Quirantes–González, F. & Pérez–González, R., 1991. Canarias. Parte 2. In: Geografía de España, volumen 8: 411–589. Editorial Planeta, Barcelona. Ribes, J. & Ribes, E., 1997. Adiciones a los Heterópteros de las Islas Canarias. III. Sessió Conjunta d’Entomologia de la Institució Catalana d’Història Natural y de la Societat Catalana de Lepidopterologia (ICHN–SCL), 9: 161–173. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution, 43: 223–225. Richerson, P. J. & Lum, K., 1980. Patterns of plant species diversity in California: relation to weather and topography. American Naturalist, 116: 504–536. Rivas–Martínez, S., 1987. Memoria del mapa de series de vegetación de España. 1:400000. ICONA, Madrid. – 1993. Clasificación bioclimática de la Tierra. Folia Botanica Matritensis, 10: 1–13. Rohde, K., 1992. Latitudinal gradients in species diversity: the search for the primary cause. Oikos, 65: 514–527. Rosenzweig, M. L., 1968. Net primary productivity of terrestrial communities: prediction from climatological data. American Naturalist, 102: 67–74.

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Sadler, J. P., 1999. Biodiversity on oceanic islands: a palaeoecological assessment. Journal of Biogeography, 26: 75–87. Sax, D. F. & Brown, J. H., 2000. The paradox of invasion. Global Ecology and Biogeography, 9: 363–371. Schmincke, H.–U., 1976. The geology of the Canary Islands. In: Biogeography and ecology in the Canary Islands: 67–84 (G. Kunkel, Ed.). Dr. W. Junk Publishers, B. V., The Hague. Servicio Geográfico del Ejército, 1975. Mapa militar de España, escala 1:800000. S.E.E., Madrid. Sfenthourakis, S., 1996. The species-area relationship of terrestrial isopods (Isopoda; Oniscidea) from the Aegean archipelago (Greece): a comparative study. Global Ecology and Biogeography, 5: 149–157. Shrader–Frechette, K., 2001. Non-Indigenous Species and Ecological Explanation. Biology & Philosophy, 16: 507–519. Simberloff, D., 1986. Introduced insects: a biogeographic and systematic perspective. In: Ecology of biological invasions of North America and Hawaii: 3–26 (H. A. Mooney & J. A. Drake, Eds.). Springer–Verlag, New York. Tilman, D., 1982. Resource competition and community structure. Princeton University Press, Princeton. Vega, R. D., 1992. La meteorología en las Islas Canarias. Canarias Copypress, Santa Cruz de Tenerife. Willerslev, E., Hansen, A. J., Nielsen, K. K. & Adsersen, H., 2002. Number of endemic and native plant species in the Galápagos Archipelago in relation to geographical parameters. Ecography, 25: 109–119. Williams, G. R., 1982. Species–area and similar relationships of insects and vascular plants on the southern outlying islands of New Zealand. New Zealand Journal of Ecology, 5: 86–96. Williamson, M., 1989. The MacArthur and Wilson theory today: true but trivial. Journal of Biogeography, 16: 3–4. Wright, D. H., 1983. Species–energy theory: an extension of species–area theory. Oikos, 41: 496–506.

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Impact of power lines on bird mortality in a subalpine area K. Bevanger & H. Brøseth

Bevanger, K. & Brøseth, H., 2004. Impact of power lines on bird mortality in a subalpine area. Animal Biodiversity and Conservation, 27.2: 67–77. Abstract Impact of power lines on bird mortality in a subalpine area.— Four sections of power lines, amounting to 4,000 km, in a subalpine area of southern Norway were patrolled from April 1989 to June 1995 to record birds killed when colliding with the overhead wires. A total of 399 dead birds and bird remains were identified as collision victims. At least 24 species were identified among the victims, the majority only represented by a few individuals. Ptarmigan (Lagopus spp.), particularly Willow ptarmigan (Lagopus lagopus), made up 80% of the victims. Season, power–line section and ptarmigan abundance affected the collision rate of this species. The highest rate was found in winter, marginally higher than in spring. Few collided with the power lines in autumn, and none were identified as victims in summer. On average, the annual minimum ptarmigan collision rate was found to be 5.3 birds km–¹ power line. The only parameter with a predictable effect on the probability of ptarmigan collisions was the height of the trees, as collision spots tended to be in places with low trees. Mortality due to power lines was, on average, at least 2.4 times higher than the annual ptarmigan hunting bag in the area during this 6–year study. Key words: Collision, Hunting, Lagopus spp., Norway, Wildlife management. Resumen Impacto del tendido eléctrico de alta tensión en la mortalidad de las aves de una región subalpina.— Entre abril de 1989 y junio de 1995, se estudiaron cuatro secciones de tendido eléctrico de alta tensión de una zona subalpina de Noruega meridional, con una extensión total de 4.000 km. El objetivo era registrar el número de aves que habían perecido tras haber colisionado con los cables aéreos. Se identificaron un total de 399 de cadáveres y restos de aves como víctimas de colisiones. Se determinaron un mínimo de 24 especies distintas, que en la mayoría de los casos sólo estaban representadas por unos pocos individuos. Los lagópodos (Lagopus spp.), en especial el lagópodo común (Lagopus lagopus), constituyeron el 80% de las víctimas. La estación del año, la sección del tendido eléctrico y la abundancia de lagópodos influyeron en la tasa de colisión de esta especie. La tasa más elevada se registró en invierno, con valores marginalmente más altos que en primavera. En otoño, fueron pocos los lagópodos que colisionaron con el tendido eléctrico, mientras que en verano no se registró ninguna víctima. Por término medio, la tasa mínima anual de colisión de lagópodos fue de 5,3 aves por km–1 de tendido eléctrico. El único parámetro con un efecto predecible sobre la probabilidad de colisión de los lagópodos fue la altura de los árboles, puesto que en los lugares donde se registró un mayor número de colisiones abundaban los árboles de poca altura. Durante los sies años que duró el estudio, la mortalidad de lagópodos ocasionada por el tendido eléctrico de alta tensión fue, por término medio, 2,4 veces mayor que aquélla generada por la caza. Palabras clave: Colisión, Caza, Lagopus spp., Noruega, Gestión de la Fauna. (Received: 6 IX 03; Conditional acceptance: 22 XII 03; Final acceptance: 14 I 04) Kjetil Bevanger* & Henrik Brøseth, Norwegian Institute for Nature Research, Tungasletta 2, NO 7485 Trondheim, Norway. *Corresponding author: Dr. K. Bevanger. E–mail: kjetil.bevanger@nina.no ISSN: 1578–665X

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Introduction Flying birds generally depend on free air space for their movements. Over time, several species have evolved sophisticated behavioural and biomechanical adaptations for moving around in structurally complex habitats, although flight in obstructed terrain is a finely tuned balance, with an everpresent risk of collisions taking place. Over more than 100 years, a steadily growing number of man– made obstacles have increased the collision hazards for birds, particularly through the erection of overhead wires for energy transmission and telecommunication (Avery et al., 1980; Hebert et al., 1995; Trapp, 1998). Research on bird mortality caused by collisions with power lines has been published around the world, for instance in Australia (Winning & Murray, 1997), India (Sundar & Choudhury, 2001), Europe (Scott et al., 1972; Renssen et al., 1975; Heijnis, 1980; Ferrer & Riva, 1987; Rose & Baillie, 1992; Bevanger et al., 1998; Janss, 2001), Southern Africa (Royen & Ledger, 1999), South America (Zerda & Rosselli, 1997) and the United States (Brown & Drewien, 1995; Savereno et al., 1996). The results of these studies confirm earlier data indicating that many different species are involved in collisions with overhead wires, and there is increasing evidence of a disproportionate representation of species with restricted biomechanical qualities (“poor flyers” sensu Rayner, 1988), for instance gallinaceous birds (Bevanger, 1998). Several studies in Europe have confirmed that resident tetraonid species, like ptarmigan (Lagopus spp.), are particularly prone to collide with overhead wires (Watson, 1982; Bevanger, 1988, 1993a, 1995a; Miquet, 1990; Bevanger et al., 1998), and fences (Baines & Summers, 1997; Bevanger & Brøseth, 2000). The ecological, economic and recreational importance of these birds (Bevanger, 1995b) has prioritized the need to understand the effect of collision mortality at the population level. More knowledge about the factors that trigger collisions would provide essential guidelines for routing and constructing power lines that would be optimal from an ornithological point of view. In general, bird deaths due to collisions with power lines have been considered an unimportant source of mortality at the population level (Bevanger, 1994). Awareness is now increasing regarding the possible additive effects of human related mortality factors. For example, whether hunting mortality is compensated for, or whether it occurs in addition to natural mortality (Bergerud, 1985; Ellison, 1991). New research on ptarmigan in Scandinavia does not support the idea of compensation of hunting mortality under the conditions studied (Smith & Willebrand, 1999; Pedersen, in press). There is little reason to believe that mortality caused by collisions with power lines should differ, given the same conditions. We initiated a long–term study in subalpine habitats in southern Norway in 1989, primarily to as-

sess the extent of bird collision mortality and, specifically for ptarmigan populations, its possible implications compared with mortality from hunting. We also tried to identify possible connections between collisions and ptarmigan behaviour, topographical characteristics and power–line configuration or technical construction. Material and methods Study area The study area is located in Mørkedalen, a valley in the county of Buskerud, southern Norway (61o 54' N, 8o 30' E), in an approximately 50 km2 area where small–game hunting takes place each autumn (fig. 1). About half of the area is typical Willow ptarmigan (Lagopus lagopus) habitat, located below the tree line, which is at about 1200 m a.s.l. here; the higher parts of the area are a more typical Rock ptarmigan (Lagopus mutus) habitat. The power– line sections patrolled to assess the extent of bird collisions are located 950–1000 m a.s.l. in subalpine habitats dominated by northern boreal birch woodland mixed with small mires (Bevanger, 1990a; Bevanger & Sandaker, 1993; Bevanger et al., 1998). Power–line characteristics Three power lines with a total length of 30 km cross the study area, a single circuit 300 kV high–tension transmission line and two distribution lines (22 and 66 kV, single circuit). All the lines have flat configurations with simplex phase conductors. The transmission line has two parallel earth wires about three meters above the phase conductors and the 22 kV distribution line has one earth wire about two meters below the phase conductors (table 1). Data recording Four selected sections of the power lines were patrolled from April 1989 to June 1995 to assess the impact on bird mortality. Section one was a five km segment of the 300 kV power line, section two was a 2.5 km segment of the 66 kV power line, and sections three and four were segments of 2.5 and 1 km, respectively, of the 22 kV power line (fig. 1, table 1). Patrols were carried out at five–day intervals from September to May and 10–day intervals from June to August. During the study period about 4000 km of power lines were patrolled. The data– collecting routine was to patrol the power-line corridor to find and collect dead birds and their remains (Bevanger, 1999). One person accompanied by pointer dogs searched the area beneath the power line and 5–10 m on each side of the terminal phase conductor, that is a 16–32 m transect (table 1). The use of pointers obviously increased the efficiency of the search for collision victims. It should be stressed that the dogs should be specially trained for the task, as pointers are generally most interested in

Animal Biodiversity and Conservation 27.2 (2004)

ede

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Fig. 1. The subalpine area in southern Norway used to study bird collisions with power lines. Patrolled power–line sections are shown and the limit of the ptarmigan hunting area is indicated in grey. Fig. 1. La zona subalpina de Noruega meridional donde se han estudiado las colisiones de aves con el tendido eléctrico de alta tensión. Se muestran las secciones de tendido eléctrico que fueron estudiadas se indican en negrita, mientras que el límite del área de caza de lagópodos se indica en gris.

Table 1. Technical specifications for the four power–line sections searched for bird collision victims in southern Norway in 1989–1995. Tabla 1. Especificaciones técnicas de las cuatro secciones de tendido eléctrico de alta tensión en la Noruega meridional donde se habían estudiado las muertes de aves por colisión entre los años 1989 y 1995.

Voltage (kV) Distance patrolled (m) Patrols Time and distance patrolled (km) April–May June–August September–October November–March Total distance patrolled (km) Patrol period (first/last patrol) Phase conductors/levels Earth wires/levels Phase conductor diameter (mm) Earth wire diameter (mm) Pylon/pole height (m) Distance between phase conductors (m) Construction year Width of clear–felled area (m)

1 300 5000 376 405.5 320.0 323.0 809.4 1857.9 1 IV 1989/ 31 V 1995 3/1 2/1 35.10 18.27 20–30 9.2 1974 35

Power–line section 2 3 66 22 2500 2500 376 375 204.1 158.7 160.7 407.5 931.0 1 IV 1989/ 31 V 1995 3/1 0/0 12.33 – 10–12 3.0 1971/1972 20

205.0 160.0 160.0 412.5 937.5 1 IV 1989/ 31 V 1995 3/1 1/1 12.33 12.33 8–10 1.5 1977 10

4 22 1000 279 56.0 37.0 51.0 134.9 278.9 5 X 1990/ 31 V 1995 3/1 1/1 12.33 12.33 8–10 1.5 1990 10

Bevanger & Brøseth

Table 2. Ptarmigan collision rates (n collisions per km–¹ per month–¹) recorded during patrols beneath four power–line sections in southern Norway in 1989–1995. A total of 279 ptarmigan were recorded as casualties of collisions with the power lines. During April–June 1989, another 39 ptarmigan found along sections 1, 2 and 3 were classified as having collided during the winter of 1988–1989. The winter (November–March) collision rate is given from one year to the next (i.e. 1989 = 1989–90, 1990 = 1990–91, etc.): * Collision rates affected by an experimental removal of the earth wire on power– line section 3 in this period (BEVANGER & BRØSETH, 2001). Tabla 2. Tasas de colisión de lagópodos (n colisiones por km–¹ por mes–¹) registradas durante los estudios llevados a cabo en cuatro secciones de tendido eléctrico de alta tensión de la Noruega meridional entre 1989 y 1995. Se registraron un total de 279 lagópodos como víctimas por colisión con el tendido eléctrico de alta tensión. Entre abril y junio de 1989, se determinó que otros 39 lagópodos encontrados a lo largo de las secciones 1, 2 y 3 habían colisionado con las líneas de alta tensión durante el invierno de 1988–1989. La tasa de colisiones correspondiente a la estación invernal (noviembre–marzo) se expresa de un año para otro (es decir, 1989 = 1989–90, 1990 = 1990–91, etc.): * Tasas de colisión afectadas por una eliminación experimental del alambre de tierra en la sección 3 de las líneas de tendido electrico de alta tensión durante este periodo (BEVANGER & BRØSETH, 2001).

Season Spring Year/Section

Summer 4

Autumn

Winter

1989

0.2 0.2

0.4

–

0.6

–

0.6

0.5

–

1990

0.2 0.2

0.4

–

0.2

0.8

0.3

1.2

2.2

1991

0.2 0.2

1.4

0.1

0.4

0.8

0.5

0.9

1.8

1992

0.3 0.2 0.2*

0.5

0.6 0.3* 0.6

1993

0.2 0.4 0.6* 1.5

0.1

0.4*

0.2

0.6 0.2* 0.2

1994

1.0 1.0 1.2* 2.5

0.5

0.2* 1.0

0.5

0.2 0.2* 0.4

1995

0.4 0.4 0.6* 1.0

–

live birds. However, young, inexperienced dogs can be useful, as they are curious about dead animals lying on the ground. All bird remains were collected for detailed examination. It may be difficult to distinguish collision victims from raptor kills by visual examination at a collision site. However, only the Golden Eagle (Aquila chrysaetos) and Gyrfalcon (Falco rusticolus) are present in winter in mountainous areas of Norway, and only the Golden Eeagle was observed in the study area. This heavy bird will always leave its footprints in snow. The Golden Eagle was never observed to scavenge birds killed by the power line beneath the conductors, although its footprints and feather–tip marks were occasionally observed in the snow beneath the conductors, indicating that some power–line victims could have been removed. The topographical and technical parameters of the power line were recorded at each collision spot. We calculated the ptarmigan collision rate as the number of victims found per kilometre of power line per month for each power–line section each year (table 2). To assess the impact of a potential seasonal

0.4 0.4* 0.5

–

0 –

–

effect on the collision rate we separated the material into four biologically meaningful seasons (spring: April–May; summer: June–August; autumn: September–October; winter: November– March). Live birds flushed by the observer or the pointer in the transect and in adjacent sites were recorded and used to calculate a ptarmigan population index as the number of observations per 10 km of patrol (table 3). Willow ptarmigan may form flocks, and 50 or more birds can sometimes be seen together in winter. When a large flock was flushed by the observer, it was impossible to count the number of birds exactly. Therefore, when calculating the number of observations, single birds and flocks were treated as one observation in the ptarmigan population index, which may have decreased the accuracy of the index. To assess the relative impact of ptarmigan mortality caused by power lines in this area, we compared it with another anthropogenic mortality factor, hunting, by recording the number of ptarmigan shot in the study area during the hunting season each year.

Animal Biodiversity and Conservation 27.2 (2004)

Table 3. Ptarmigan population index (n observations per 10 km–¹ per patrol) along four power–line sections patrolled in southern Norway in April 1989–June 1995. Tabla 3. Índice poblacional de lagópodos (n observaciones por 10 km–¹ por patrulla) a lo largo de cuatro secciones de tendido eléctrico de alta tensión estudiadas en la Noruega meridional entre abril de 1989 y junio de 1995.

Season Spring Year/Section

Summer 3

1 0.1

1989

1.8 1.2

7.1

–

1990

1.8

1.3

–

1991

2.7 1.3

3.7 3.3

1.6

1992

2.8 2.0

7.7 2.5

0.2

1993

1.4 2.3

9.0 2.7

1994

1.7 1.4

1995

2.7 2.2

1.6

Autumn

Winter

0.4 3.8

–

0.2

2.2

–

1.3 0.6

1.0

–

1.8

–

1.0

2.3

2.2 1.5

3.7 6.4

0.8 1.6

0.6 0.4 1.8

3.1 1.2

3.1 1.3

2.7

0.7

2.3 1.5

2.6 3.2

0.9

0.5 4.9

0.7

2.0

1.4 0.9

4.8 3.6

5.0 4.2

1.6

0.9 4.0

1.5

4.4

1.8 1.1

2.6

5.8 2.2

–

Factors affecting the rate of collisions with power lines To test for the effect of different factors on the rate of ptarmigan collisions with power lines, we applied a GLM–Univariate analysis procedure (SPSS for Windows, Release 10.0.5, © 1999 SPSS Inc., Chicago, Illinois) with power–line section, season (spring, summer, autumn or winter), and power– line category (300 kV, 66 kV or 22 kV) as fixed factors, year as a random factor, and the ptarmigan population index as a covariate. We tested for both the main effects and the interaction effects of all the parameters. To find the best model, we applied the model–building strategy of stepwise forward inclusion or alternate exclusion of independent variables. Only variables significant at P < 0.05 were accepted in the model. The collision rate on powerline section three in 1992–1995 was excluded from the GLM–analysis because the collision hazard on this section was influenced by the experimental removal of the earth wire during this period (table 2; Bevanger et al., 1998; Bevanger & Brøseth, 2001). Factors affecting the probability of collisions with power lines To test whether we were able to predict the probability of ptarmigan colliding with the power lines using the power–line characteristics, vegetation, and topography as parameters, we performed a binary logistic regression analysis based on a comparison of collision spots and stratified random places without any recorded collisions (SPSS for Windows, Release 10.0.5, © 1999 SPSS INC., Chicago, Illinois). A stepwise forward conditional model–building strategy was applied to find the best logistic model

Table 4. Seasonal bias correction factors used to adjust the estimate of the number of Ptarmigan killed by colliding with high– tension power–lines in southern Norway: spring, April–May; autumn, September– October; winter, November–March. Total correction denotes the cumulative correction used to adjust the absolute minimum number of collision victims found during the patrols (tdb) (Bevanger, 1995b). Tabla 4. Factores de corrección del sesgo estacional empleados para ajustar la estimación del número de lagópodos que perecieron al colisionar con el tendido eléctrico de alta tensión en la Noruega meridional: primavera, abril–mayo; otoño, septiembre–octubre; invierno, noviembre– marzo. La corrección total indica la corrección acumulativa empleada para ajustar el número mínimo absoluto de victimas por colisión encontradas durante el estudio (tdb) (Bevanger, 1995b).

Seasonal correction factors Spring

Autumn

Winter

Search bias

0.05

Scavenger bias

0.25

0.30

0.20

Habitat bias

0.20

Crippling bias

0.05

Total correction 1.85 tdb 1.98 tdb 1.73 tdb

Bevanger & Brøseth

to predict ptarmigan collisions based on the parameters tested. In the logistic analysis, we tested whether the height of the earth wire above the ground, the distance to the woodland and the height of trees affected the probability of collision taking place. We also tested whether topographical parameters like slope and habitat type had a significant effect on the probability of collision. Estimating total losses The numbers of dead ptarmigan found during power–line patrols are absolute minimum values, no matter how frequently patrols are performed, or how thoroughly the corridor is searched for victims (Bevanger, 1999). Therefore, several important biasing factors connected with the fieldwork procedure have to be taken into account when trying to estimate the real number of collision victims (Aplic, 1994; Bevanger, 1995b, 1999). The four biasing factors commonly accounted for are crippling, habitat, scavenger and search biases (review in Bevanger, 1999). Let N denote the total number of collision victims along a patrolled power-line section, and 1–pbk the proportion of these that are undetected because of the crippling bias (pbk = "percentage of birds colliding that were killed and fell on the search area" (Meyer, 1978)). Let 1–ps denote the proportion of the remaining pbk × N victims that are undetected because of the habitat bias (ps = "proportion of line section which is searchable" (James & Haak, 1979)). Let 1–pnr denote the proportion of the remaining ps × pbk × N victims that are undetected because of the scavenger bias (pnr = "percentage of dead birds not removed by scavengers– derived from a removal rate study" (Meyer, 1978)). Finally, let 1–pbf denote the proportion of the remaining pnr × ps × pbk × N victims that are undetected because of the search bias (pbf = "percentage of dead birds found based on a dead bird plant study" (Meyer, 1978)). The total number of dead birds found, tdb, is given by the equation tdb = pbf × pnr × ps × pbk × N. Thus, the real, total loss, N, is tdb / (pbf × pnr × ps × pbk). To estimate the total annual losses in the area, we applied the estimating procedure and correction factors used in earlier studies on ptarmigan collisions to adjust the observed collision rate recorded during the patrols (table 4; Bevanger et al., 1994, 1998; Bevanger, 1995b, 1999; Bevanger & Brøseth, 2000). Year–round fieldwork in Norwegian alpine habitats is difficult due to bad weather and snow conditions for about six months of the year. We performed experiments in the study area to improve the scavenger removal bias, which is site specific and quite important in some areas (Bevanger et al., 1998). The results showed that 15% of the dummy ptarmigan were removed within five days, and tracks indicated that the Red fox (Vulpes vulpes), Stoat (Mustela erminea) and Golden eagle were the most active scavengers, particular the Red fox.

Results Species composition of collision victims A total of 399 dead collision victims were recorded during the six–year study, 390 of which were identified at the species or genus level. At least 24 different species were identified among the collision victims, 318 (80%) of which were ptarmigan. Most species were represented by a few individuals: Mallard (Anas plathyrhynchos), Rough–legged buzzard (Buteo lagopus), Kestrel (Falco tinnunculus), Black grouse (Tetrao tetrix), Golden plover (Pluvialis apricaria), Tringa sp., Lapwing (Vanellus vanellus), Ruff (Philomachus pugnax), Snipe (Gallinago gallinago), Arctic tern (Sterna paradisea), Wood pigeon (Columba palumbus), Long–eared owl (Asio otus), Anthus sp., Blackcap (Sylvia atricapilla), Bluethroat (Luscinia svecica), Fieldfare (Turdus pilaris), Ring ouzel (Turdus torquatus), Blackbird (Turdus merula), Redwing (Turdus iliacus), Song thrush (Turdus philomelos), Wheatear (Oenanthe oenanthe), and Redpoll (Carduelis flammea). It was rarely possible to identify the species of ptarmigan as most consisted of feather clusters and other remains. However, 42 undisturbed ptarmigan bodies were found, the majority (95%) of which were Willow ptarmigan. Ptarmigan mortality due to power lines The observed variation in the ptarmigan collision rate was significantly affected by the season and power–line section, together with the ptarmigan population index which also entered the GLM model (table 2 and table 3, F7,81 = 9.0, P < 0.001). These three parameters accounted for 46% of the observed variation. We found no significant interaction effect between the parameters tested, and nor did the power–line category or year explain a significant part of the observed variation (P > 0.10). On average, the annual minimum ptarmigan collision rate was estimated to be 5.3 ± 1.1 SE birds per kilometre of power line (section one: 3.7, section two: 3.1, section three: 6.5 and section four: 7.8). The ptarmigan collision rate peaked in the winter with 0.7 birds per km–¹ per month–¹ (fig. 2, seasonal effect: F3,81 = 4.8, P < 0.01). However, there was also a high collision rate in spring (0.6 birds per km–¹ per month–¹), whereas far fewer ptarmigan collided in autumn (0.2 birds per km–¹ per month–¹). During the summer months, we found no ptarmigan collision victims. Of the four power-line sections, section four had a much higher ptarmigan collision rate than the other three, which were quite similar (fig. 3, section effect: F3,81 = 4.8, P < 0.01). In general, the collision rate increased as the population index increased (population index covariate effect: F1,81 = 9.0, P < 0.01). Based on the recorded collision rate of the patrolled sections, we found that, on average, collisions with power lines killed at least 159 ptarmigan annually in this area. When the observed collision

Collision rate (n km–1 month–1)

Animal Biodiversity and Conservation 27.2 (2004)

1.5

Spring Summer Autumn Winter

1.0

0.5

0.0 Section 1

Section 2

Section 3

Section 4

Fig. 2. Seasonal variation in ptarmigan collision rates (n collisions per km–¹ per month–1) ± SE for the four power–line sections studied in a subalpine area in southern Norway during a 6–year period from April 1989 to June 1995. Fig. 2. Variación estacional en las tasas de colisión de los lagópodos (n colisiones por km–¹ por mes–1) ± EE para las cuatro secciones de tendido eléctrico de alta tensión de una zona subalpina de Noruega meridional estudiadas durante un período de 6 años comprendido entre abril de 1989 y junio de 1995.

Estimated marginal mean

1.0

0.8

Section Section Section Section

1 2 3 4

0.6

0.4

0.2

0.0

Spring

Summer

Autumn

Winter

Fig. 3. Estimated marginal means of ptarmigan collision rates (n collisions per km–¹ per month–¹) in different seasons to compare the four power–line sections studied. These mean values are adjusted for the ptarmigan population index as a covariate in the GLM analysis in a fixed–effects model. Fig. 3. Medias marginales estimadas de las tasas de colisión de los lagópodos (n colisiones por km–1 por mes–¹) en distintas estaciones del año para comparar las cuatro secciones de tendido eléctrico estudiadas. Estos valores medios se han ajustado para el índice poblacional de los lagópodos como una covarianza en el análisis GLM de un modelo de efectos fijos.

Bevanger & Brøseth

Table 5. The absolute minimum annual number of ptarmigan collision victims recorded during patrols beneath four power–line sections in southern Norway in 1989–1995, and the total hunting yield in 1989–1994 in the same area. The number is given from one year to the next, i.e. 1989–1990, 1990– 1991, etc. Tabla 5. El número mínimo absoluto anual de víctimas de lagópodos por colisión registrado durante el estudio realizado entre 1989 y 1995 en cuatro secciones de tendido eléctrico de alta tensión de la Noruega meridional, y el rendimiento total de caza entre 1989 y 1994 en la misma área. El número se indica de un año para otro; es decir, 1989–1990, 1990–1991, etc.

Year 1989 Minimum no. of collision victims Hunting bag

1990

1991

1992

1993

1994

108

216

183

117

107

173

101

rate was adjusted for biasing factors connected with the fieldwork procedure (table 4), we estimated that, on average, collisions killed 282 ptarmigan annually. This indicates that the annual collision rate was probably was as high as 9.4 birds per kilometre of power line during the study period. The only significant parameter in the binary logistic regression analysis affecting the probability of ptarmigan colliding was the height of trees (P²1 = 13.5, P < 0.001). Collision spots generally had lower trees than places along power lines without any recorded ptarmigan collisions. Neither the height of power-line wires, the distance to woodland, the slope nor the habitat type had any significant predictive effect on the probability of collision. Power line versus hunting mortality During the six hunting seasons (1989–1994), 422 ptarmigan were shot in the study area (table 5). The minimum power–line collision mortality recorded each year was on average at least 2.4 times higher than the hunting mortality during this period (range 1.3–4.2 times higher). The estimated mean minimum number of ptarmigan killed annually by colliding with the power lines during 1989–1994 was 151 birds, whereas only 70 were harvested each year (table 5). Compared with the estimated total losses due to power lines in the area (289 birds year-1), this is, on average, as much as four times higher than the hunting mortality. Discussion Few bird species are adapted to survive the harsh environmental conditions in Norwegian alpine habitats during the winter. In summer, however, migrants increase the number of species significantly. The majority of bird species run a risk of colliding with man–made obstacles like overhead wires, although

in most species only a few individuals are recorded (Avery, 1980; Bevanger, 1993a, 1995a, 1998; Brown & Drewien, 1995; Munkejord 1996). A similar pattern occurs also in the present study where ptarmigans are the dominating victims. The migrant Fieldfare was the only species other than the ptarmigan that had a noticeable collision mortality (6% of the victims). The Fieldfare is quite common, and numerous individuals gather in flocks during autumn when the southward migration starts. The migrant species of collision victims was mainly found during restricted periods in spring and autumn, reflecting the fact that the valley is draining an east–west bird migration in autumn and a west–east migration in the spring. The victim number of these species is, however, too small and fragmental for an assessment based on statistical treatment. The considerable number of ptarmigan victims found confirms the findings of earlier studies, which showed that tetraonid species are particularly prone to collide with man–made obstacles (Watson, 1982; Bevanger, 1988, 1993a, 1995a; Miquet, 1990; Baines & Summers, 1997; Bevanger & Brøseth, 2000). The majority of the ptarmigan we were able to classify to the species level were Willow ptarmigan, and only two verified Rock ptarmigan victims were found. Rock ptarmigan only temporarily migrate from higher altitudes down to Willow ptarmigan habitats in the birch woods, where the four power–line sections were located, when snowstorms and icing of food resources occur in their alpine habitat. Willow ptarmigan and Rock ptarmigan are monogamous, territorial, medium sized grouse (0.4–0.6 kg), with a circumpolar distribution inhabiting mainly heather moor, treeless tundra and alpine habitats of North America and northern parts of Eurasia (Johnsgard, 1983). Ptarmigan populations exhibit major fluctuations in numbers, with large spatio–temporal variations in density of the breeding and autumn population (Myrberget, 1988; Hudson, 1992; Lindström, 1994). The number of ptarmigan victims found during spring (April–May) and winter (November–March)

Animal Biodiversity and Conservation 27.2 (2004)

indicates that these are the most dangerous periods of the year with respect to collisions. The winter and early spring activity of the species combined with the poor light and bad weather conditions in this period particularly seem to contribute to the collision hazard. During the winter, ptarmigan make short, preferably gliding, flights downhill, from one food patch to another, depending on the combination of prevailing winds and falling and drifting snow covering the vegetation. The males have a display period in April and May flying between the boundaries of their territory, the activity peaking during evening twilight. In summer, ptarmigan scarcely fly at all because food is plentiful and the birds are caring for their chicks. Autumn, before snow covers the vegetation, is also a period with abundant food resources and the birds may stay within restricted areas. The data collected on topography and vegetation structure indicate some highly hazardous situations. The tree height effect on collision probability supports the assumption that ptarmigan prefer open terrain when flying between food patches. Thus, the collision hazard must be expected to decrease if a power line is routed through dense woodland or forest with tall trees, forcing the birds to fly above the wires (Thompson, 1978; Bevanger, 1990b, 1993a). Northern boreal birch woodland does not develop into tall trees (normally less than 7–8 m high), but the distribution and height of trees play an important role in regulating the flight lanes of birds. It would, however, have been preferable to use multidimensional terrain models to get a better picture of how to route a power line to minimize the collision hazard. The high mortality values on section four are interesting, as the section was built in 1990 (Bevanger & Sandaker, 1993). It has earlier been suggested that power lines are particularly dangerous for birds shortly after they are constructed, implying that birds may “learn” to avoid collisions with air obstacles in the area they inhabit. An alternative hypothesis would be that a possible decrease in collisions over time reflects a reduction in the population size due to increased mortality caused by the power lines. Power lines may negatively influence the population development, and contribute to population limitation. Watson (1982) reported the local extinction of Rock Ptarmigan in Scotland due to overhead ski–lift cables, and in France cables have been reported to be a threat to Black grouse populations (Miquet, 1990). Whether such mortality is compensatory or additive to natural mortality is questionable (Ellison, 1991). Traditionally, wildlife biologists have rejected density independent mortality factors like hunting and power lines as being important for species with a short life span and high reproduction potential. However, this has recently been questioned, and hunting has been shown to be important for the population trajectory (Pedersen, in press). The present study indicates that the majority of ptarmigan are killed in winter and spring, i.e. when

most natural mortality occurs (Hudson, 1992), and these birds would be going to reproduce. Hence, power–line induced mortality may have a significant demographic effect. Hunting, on the other hand, takes place in September and October (Kastdalen, 1992). Moreover, hunting mortality can be spread over a much wider area (Brøseth & Pedersen, 2000), whereas birds in the vicinity of a power line run a greater risk of becoming collision victims than an "average" bird. However, the impact area, i.e. the area where power lines have a behavioural or ecological effect (Cassel, 1978), must be considered according to species-specific movement patterns. These two mortality factors might thus affect a local population in two ways. An interesting aspect of the present findings, particularly from a management point of view, is that the mortality caused by the power lines was 2–3 times higher than that caused by hunting. It is, however, difficult to assess the significance of hunting and power-line induced mortality in the area because the present data are insufficient for judging the population development in the study period. Acknowledgements We want to thank Odd and Marianne Sandaker for carrying out the fieldwork, and several Norwegian power companies, the Directorate for Nature Management, the County Governor in Buskerud and the Norwegian Institute for Nature Research for funding the study. John D. C. Linnell made valuable comments on an earlier version of the manuscript. References Avery, M. L., Springer, P. F. & Dailey, N. S., 1980. Avian mortality at man–made structures: an annotated bibliography (Revised). US Fish and Wildlife Service. Biological Services Program, National Power Plant Team, FWS/OBS–80/54. Avian Power Line Interaction Committee (Aplic), 1994. Mitigating bird collisions with power lines: the state of the art in 1994. Edison Electric Institute, Washington, DC. Baines, D. & Summers, R. W., 1997. Assessment of bird collisions with deer fences in Scottish forests. J. Appl. Ecol., 34: 941–948. Bergerud, A. T., 1985. The additive effect of hunting mortality on the natural mortality rates of grouse: In: Game harvest management: 345–366 (S. L. Beasom & S. F. Robertson, Eds.). Caesar Kleberg Wildlife Research Institute, Kingsville, Texas. Bevanger, K., 1988. Transmission line wirestrikes of Capercaillie and Black grouse in central Norwegian coniferous forest. Økoforsk Report, 9: 1–53. [In Norwegian, English summary.] – 1990a. Willow grouse and power–line wire strikes in Hemsedal. Norwegian Institute for Nature Research, Project Report 49: 1–15. [In Norwegian,

English summary.] – 1990b. Topographic aspects of transmission wire collision hazards to game birds in the Central Norwegian coniferous forest. Fauna norvegica Serie C, 13: 11–18. – 1993a. Bird collisions with a 220 kV transmission line in Polmak, Finnmark. Norwegian Institute for Nature Research, Research Report, 40: 1–26. [In Norwegian, English summary.] – 1993b. Hunting mortality versus wire–strike mortality of Willow grouse Lagopus lagopus in an upland area of Southern Norway. In: Avian interactions with utility structure. Proc. Int. workshop EPRI TR–103268, Project 3041: 11.1–11.10. – 1994. Bird interactions with utility structures; collision and electrocution, causes and mitigating measures. Ibis, 136: 412–425. – 1995a. Tetraonid mortality caused by collisions with power lines in boreal forest habitats in central Norway. Fauna norvegica Serie C, 18: 41–51. – 1995b. Estimates and population consequences of tetraonid mortality caused by collisions with high tension power lines in Norway. J. Appl. Ecol., 32: 745–753. – 1998. Biological and conservation aspects of bird mortality caused by electricity power lines: a review. Biological Conservation, 86: 67–76. – 1999. Estimating bird mortality caused by collision with power lines and electrocution, a review of methodology. In: Birds and power lines. Collision, electrocution and breeding: 29–56 (M. Ferrer & G. F. E. Janss, Eds.). Quercus, Madrid. Bevanger, K., Bakke, Ø. & Engen, S., 1994. Corpse removal experiments with Willow ptarmigan (Lagopus lagopus) in power–line corridors. Ökolgie der Vögel (Ecology of Birds), 16: 597–607. Bevanger, K. & Brøseth, H., 2000. Reindeer Rangifer tarandus fences as a mortality factor for ptarmigan Lagopus spp. Wildlife Biology, 6: 121–127. – 2001. Bird collisions with power lines–an experiment with ptarmigan (Lagopus spp.). Biological Conservation, 99: 341–346. Bevanger, K., Brøseth, H. & Sandaker, O., 1998. Bird mortality due to collisions with power lines in Mørkedalen, Hemsedalsfjellet, Norway. Norwegian Institute for Nature Research, Project Report, 531: 1–41. [In Norwegian, English summary.] Bevanger, K. & Sandaker, O., 1993. Power lines as a mortality factor for Willow grouse in Hemsedal. Norwegian Institute for Nature Research, Project Report, 193: 1–25. [In Norwegian, English summary.] Brown, W. M. & Drewien, R. C., 1995. Evaluation of two power line markers to reduce crane and waterfowl collision mortality. Wildl. Soc. Bull., 23: 217–227. Brøseth, H. & Pedersen, H. C., 2000. Hunting effort and game vulnerability studies on a small scale: a new technique combining radio–telemetry, GPS and GIS. J. Appl. Ecol., 37: 182–190. Cassel, F., 1978. Behaviour. Working group summa-

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ries. In: Impacts of transmission lines on birds in flight: 167–171 (M. L. Avery, Ed.). Oak Ridge Associated Universities, Oak Ridge, Tennessee. Ellison, L. N., 1991. Shooting and compensatory mortality in tetraonids. Ornis Scandinavica, 22: 229–240. Ferrer, M. & Riva, M. de la, 1987. Impact of power lines on the population of birds of prey in the Donana National Park and its environment. Mediterranean Birds of Prey III. National Institute of Game Biology 12, Sevilla. Hebert, E., Reese, E, Mark, L., Anderson, R. & Brownell, J. A., 1995. Avian collision and electrocution: An annotated bibliography. California Energy Commission, Sacramento, CA. Publication No. P700–95–001. Heijnis, R., 1980. Bird mortality from collision with conductors for maximum tension. Ökolgie der Vögel (Ecology of Birds), (Sonderheft), 2: 111–129. Hudson, P., 1992. Grouse in space and time. The population biology of a managed gamebird. The Game Conservancy. Matthew Gloag & Son, Hampshire. Janss, G. F. E., 2001. Birds and power lines: a field of tension. Ph. D. thesis, Univ. of Utrecht. James, B. W. & Haak, B. A., 1979. Factors affecting avian flight behavior and collision mortality at transmission lines. Bonneville Power Administration Report. US Dept. of Energy, Oregon. Johnsgard, P. A., 1983. The grouse of the world. Croom Helm, London. Kastdalen, L., 1992. Skogshøns og jakt. Norges Bondelag, Norsk skogbruksforening, Norges skogeierforbund, Norges jeger–og fiskerforbund. Oslo. [In Norwegian.] Lindström, J., 1994. Tetraonid population studies– state of the art. Annales Zoologici Fennici, 31: 347–364. Meyer, J. R., 1978. Effects of transmission lines on bird flight behavior and collision mortality. Bonneville Power Administration Report. U S Dept. of Energy, Oregon. Miquet, A., 1990. Mortality in Black grouse Tetrao tetrix due to elevated cables. Biological Conservation, 54: 349–355. Munkejord, A., 1996. Kraftledninger og fugledød på Jæren. Fylkesmannen i Rogaland, Miljøvernavdelingen, Miljørapport, 2. [In Norwegian.] Myrberget, S., 1988. Demography of an island population of willow ptarmigan in northern Norway. In: Adaptive strategies and population ecology of northern grouse. Volume I. Population studies: 379–419 (A. T. Bergerud & M. W. Gratson, Eds.). Univ. of Minnesota Press, Minneapolis. Pedersen, H. C., Steen, H., Kastdalen, L., Brøseth, H., Ims, R. A., Svendsen, W. & Yoccoz, N. G., 2004. Weak compensation of harvest despite strong density–dependent growth in willow ptarmigan. Proceedings of the Royal Society of London Series B., 271: 381–385. Rayner, J. M. V., 1988. Form and function in avian flight. Current Ornithology, 5: 1–66.

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Renssen, T. A., Bruin, A. de, Doorn, J. H. van, Gerritsen, A., Greven, N. G., Kamp, J. van de, Linthorst, H. D. M. & Smith, C. J., 1975. Vogelsterfte in Nederland tengevolge van aanvaringen met hoogspannings–lijnen. Rijksinstituut voor Natuurbeheer, Arnhem. Rose, P. & Baillie, S., 1992. The effects of collisions with overhead wires on British birds: an analysis of ringing recoveries. BTO Res. Rep., 42: 1–227. Royen, C. S. van & Ledger, J. A., 1999. Birds and utility structures: developments in Southern Africa. In: Birds and power lines. Collision, electrocution and breeding: 205–229 (M. Ferrer & G. F. E. Janss, Eds.). Quercus, Madrid. Savereno, A. J., Savereno, L. A., Boettcher, R. & Haig, S. M., 1996. Avian behavior and mortality at power lines in coastal South Carolina. Wildl. Soc. Bull., 24: 636–648. Scott, R. E., Roberts, L. J. & Cadbury, C. J., 1972. Bird deaths from power lines at Dungeness. British Birds, 65: 273–286. Smith, A. & Willebrand, T., 1999. Mortality causes and survival rates of hunted and unhunted Willow grouse. J. Wildl. Manage., 63: 722–730. Sundar, K. S. G. & Choudhury, B. C., 2001. A note on Sarus crane (Grus antigone) mortality

due to collision with high–tension power lines. Journal of Bombay Natural History Society, 98: 108–110. Thompson, L. S., 1978. Transmission line wire strikes: mitigation through engineering design and habitat modification. In: Impacts of transmission lines on birds in flight: 51–92 (M. L. Avery, Ed.). Oak Ridge Associated Universities, Oak Ridge, Tennessee. Trapp, J. L., 1998. Bird kills at towers and other man–made structures: an annotated partial bibliography (1960–1998). U S Fish and Wildlife Service, Office of Migratory Bird Management, Arlington, Virginia. Watson, A., 1982. Effects of human impact on Ptarmigan and Red grouse near skilifts in Scotland. Institute of Terrestrial Ecology, Annual Report 1981. Cambridge. Winning, G. & Murray, M., 1997. Flight behaviour and collision mortality of waterbirds flying across electricity transmission lines adjacent to the Shortland Wetlands, Newcastle. NSW. Wetlands,17: 29–40. Zerda, S. de la & Rosselli, L., 1997. Colombian fauna and transmission lines. ISA, Interconexión Eléctrica S. A., Final Report, Columbia. [In Spanish, English summary provided by the authors.]

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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Animal Biodiversity and Conservation 27.2 (2004)

Nutrient richness of wood mould in tree hollows with the Scarabaeid beetle Osmoderma eremita N. Jönsson, M. Méndez & T. Ranius

Jönsson, N., Méndez, M. & Ranius, T., 2004. Nutrient richness of wood mould in tree hollows with the Scarabaeid beetle Osmoderma eremita. Animal Biodiversity and Conservation, 27.2: 79–82. Abstract Nutrient richness of wood mould in tree hollows with the Scarabaeid beetle Osmoderma eremita.— Trunk hollows with wood mould harbour a rich invertebrate fauna with many threatened species, and it has been suggested that the beetle Osmoderma eremita (Coleoptera, Scarabaeidae) is a keystone species in this community. We estimated the amount of nitrogen and phosphorus in wood mould and compared the coarse fraction which constitutes frass of O. eremita with the finer fraction of wood mould, and found that the nutrient richness was higher in frass. O. eremita larvae have a fermentation chamber that harbours nitrogen fixing bacteria. As the levels of absorbable nitrogen are a limiting factor in insect growth, an increase in nutrient richness is one of several possible explanations why the species richness of saproxylic beetles is higher in hollow oaks where O. eremita is present in relation to similar trees where the beetle is absent. Key words: Nitrogen, Oak, Phosphorous, Scarabaeoidea, Wood decay. Resumen Riqueza en nutrientes del mantillo de la madera en cavidades arbóreas donde está presente el escarabeideo Osmoderma eremita.— Las cavidades de los troncos con mantillo de la madera albergan una rica fauna de invertebrados, entre los que se incluyen numerosas especies amenazadas. Se ha sugerido que Osmoderma eremita (Coleoptera, Scarabaeoidea) constituye una especie clave de esta comunidad. Se estimó la cantidad de nitrógeno y fósforo presentes en el mantillo de la madera, y se comparó la fracción gruesa formada por las deyecciones de O. eremita con la fracción más fina del mantillo de la madera y se vió que la riqueza en nutrientes era más elevada en la fracción gruesa. Las larvas de O. eremita contienen una cámara de fermentación que alberga el nitrógeno fijado por las bacterias. Puesto que los niveles de nitrógeno absorbible constituyen un factor limitador del crecimiento de insectos, un aumento de la riqueza en nutrientes es una de las posibles explicaciones del porqué la riqueza en especies de los escarabajos saproxílicos es más elevada en los robles huecos donde O. eremita está presente que en otros árboles similares donde está ausente. Palabras clave: Nitrógeno, Roble, Fósforo, Scarabaeoidea, Descomposición de la madera. (Received: 6 IX 03; Conditional acceptance: 17 XII 03; Final acceptance: 9 II 04) Niklas Jönsson & Thomas Ranius*, Dept. Entomology, Swedish Univ. of Agricultural Sciences, P. O. Box 7044, SE – 750 07 Uppsala, Sweden.– Marcos Méndez**, Botanical Inst., Stockholm Univ., SE – 106 91 Stockholm, Sweden; *Corresponding author: Thomas Ranius. E–mail: thomas.ranius@entom.slu.se ** Present address: Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y Tecnologia, Univ. Rey Juan Carlos, c/ Tulipan s/n., E–28933 Móstoles, Madrid, Spain.

ISSN: 1578–665X

Jönsson et al.

Introduction When deciduous trees age, hollows with wood mould often form in the trunks. Wood mould is loose wood colonised by fungi, often with remains from bird nests and insects. Trunk hollows with wood mould harbour a specialised fauna, mainly consisting of beetles, flies, mites and pseudoscorpions (Dajoz, 2000; Ranius, 2002a). Among these species, the Scarabaeid beetle Osmoderma eremita has received much attention in the last few years because it is among those species with the highest priority in the European Union’s Habitats Directive (Luce, 1996). Species richness of beetles associated with tree hollows is considerably higher in tree hollows with O. eremita present than in those hollows where it is absent (Ranius, 2002b). This may be because several species have similar habitat requirements and thus prefer the same trees (Ranius, 2002c). To some extent it may also be because they are all limited by the spatio– temporal structure of suitable trees in a similar way, and therefore have colonised the same trees. A third possibility is that O. eremita improves the habitat for other species. Up to 100 adult O. eremita beetles emerge from a suitable tree hollow every year (Ranius, 2001), implying that there may be several hundreds of larvae present. O. eremita larvae eat large amounts of rot wood, thereby increasing the volume of the trunk hollow. As their frass is often a dominant content of tree hollows (Martin, 1993), it has been suggested that O. eremita is a keystone species which influences a whole community of species associated with tree hollows (Ranius, 2002b). O. eremita increases the size of the hollow, and its frass also changes the structure of the wood mould by making it more grainy. Moreover, larvae of O. eremita have a fermentation chamber which harbours nitrogen fixing bacteria (Wiedemann, 1930). Because levels of absorbable nitrogen are a limiting factor in insect growth (Haack & Slansky, 1985; Dajoz, 2000), it is possible that O. eremita improves the habitat for other species by increasing the nutrient richness of the rot wood. This study estimated the nutrient richness (content of nitrogen and phosphorus) in wood mould, comparing hollows with and without O. eremita. When O. eremita was present, we compared the fraction of wood mould consisting of O. eremita frass with the finer fraction. Material and methods The content of nitrogen and phosphorus was measured in samples with wood mould taken from trunk hollows in 20 oaks Quercus robur. The possibility to obtain large sample sizes is restricted because hollow oaks are a rare habitat and many tree hollows are out of reach, even by ladder. The oaks had a trunk circumference of 2.2–4.8 m and were situated at half–open or regrown pasture woodlands on the island Hallands Väderö, southern

Sweden. The age of oaks at Hallands Väderö has been measured by counting tree rings and almost all very old oaks are between 280 and 350 years old (Lannér, 2003). Probably all the trees in our study were this age. Brown rot was unmistakably the dominant rot type in the hollows. Only in five of twenty hollows there was also wood decayed by white rot, but this was not the dominating rot type in any tree. All hollows contained a sufficient amount of wood mould for larval development of O. eremita (at least 10 litres, according to data in Hedin & Mellbrand [2003]). Frass of O. eremita was found in 15 of the hollows, while it was absent in five. Samples were taken from each tree 10 cm below the wood mould surface. When frass of O. eremita was present, it was separated from the finer fraction of wood mould by sieving. The finer fraction consists of rotten wood which has become pulverized, possibly due to activity by insects other than O. eremita (for instance, beetles and ants). It may also contain pulverized frass from O. eremita. Larval frass can be present for a long time after the species has disappeared from the tree (Martin, 1993; Ranius & Nilsson, 1997), which suggests that the sampled frass may have been years old. For the chemical analyses, about 60 mg of the dried samples were used. Samples were ground to a fine powder and oven–dried at 60°C for five days. Samples were digested by a micro–Kjeldahl digestion (boiled at 415°C in 2 ml concentrated sulphuric acid plus a catalyser until the sample turned clear, taking approximately 1h). The digested material was diluted to 100 ml with distilled water and analysed for N (organic plus ammonical) and P using a Flow Injection Analyzer (FIA; Tecator, Höganäs, Sweden). FIA carries out an automatized colorimetric assessment of N and P by measuring absorbance of the sample at 540 nm and 650 nm respectively. Results The content of N and P was significantly higher in larval frass than in the finer fraction of wood mould (fig. 1). This was analysed with the paired sample ttest (for N: p < 0.001, for P: p = 0.001). There was no significant difference in nutrient richness in wood mould with O. eremita absent in comparison with the finer fraction of wood mould in trunks where O. eremita was present (for N: p = 0.404, for P: p = 0.151). Discussion A study by Kelner–Pillault (1974) in chestnut trees, revealed that the level of organic nitrogen was higher in wood mould (0.79–0.97%) than in other kind of wood (healthy wood – 0.24%; dry rotten – 0.31%; damp rotten wood – 0.47%). In our study, we found an N concentration of about 1% dry mass in wood mould with no O. eremita present, which means that the level of N concentration was similar

Animal Biodiversity and Conservation 27.2 (2004)

to the wood mould studied by Kelner–Pillault (1974). Viejo Montesinos et al. (1996) measured an N concentration of between 0.5 and 0.8% dry mass in rotten wood of different Quercus species. Frass of O. eremita was N and P enriched when compared to the finer fraction of wood mould. A similar finding has been reported for the longhorn beetle Phymatodes maaki (Ikeda, 1979). The enrichment is probably due to the nitrogen fixing bacteria which occur in the fermentation chamber of O. eremita larvae. Another less likely explanation is that O. eremita larvae selectively feed on a certain fraction of the rotten wood with a much higher nutrient richness than the rest. However, in many trees almost all loose material consists of O. eremita frass, which suggests that O. eremita larvae eat on the inner walls without leaving any fraction of the rot wood. When Kelner–Pillault (1974) studied the content of the wood mould and frass of the Scarabaeid beetle Gnorimus variabilis in chestnut trees, there was a trend towards a higher level of organic nitrogen in the frass in comparison to the wood mould (1.17% in comparison to 1.09%). Trees with O. eremita generally have a higher species richness than those without O. eremita, and several explanations have been suggested (see Introduction). This study adds another possible explanation: higher nutrient richness may improve the situation for decomposing invertebrates, and increase the total species richness of invertebrates in the tree hollow. However, one weakness of this explanation is that we do not know the decomposition rate of the frass and to what extent it is actually utilised by the invertebrate community in tree hollows. Some observations indicate that larval frass of O. eremita may remain in tree hollows, for instance in old stumps, for several decades after O. eremita has disappeared. However, we do not know whether it is only a very small proportion that remains after a few decades or if the volume of frass is more or less intact after that time. Therefore, studies of decomposition rate of frass and wood mould should be carried out, as well as experimental studies on the effect of O. eremita frass on the abundance of other invertebrates. Present knowledge on habitat requirements of invertebrates in tree hollows is mainly based on correlations observed between presence/absence of species and easily measurable variables reflecting the quality of tree hollows (Ranius 2002a; 2002c). This study suggests that to go one step further, and understand the mechanism behind the correlation patterns, analyses oh how wood mould forms and decomposes are required, based on studies both in the field and in the laboratory. During the successional change of a tree hollow, the wood mould habitat also changes. The volume of wood–mould in known to change (Kelner–Pillault, 1974), but the physical and chemical characteristics likely change as well, and this may affect the invertebrate community. The present study shows that invertebrates such as Osmoderma eremita may affect the rotten wood habitat not only physically, but also chemically.

A 1.4

1.2

1.0 0.8 0.6 0.4 0.2 0.0

B 0.040

0.035 13

0.030 0.025

0.020 0.015 0.010 0.005 0.000 Lf

F Abs Type of wood mould

Fig. 1. Concentration of nitrogen (organic + ammoniacal) (A) and phosphorus (B) (mean and standard deviation, units in mmol per g) in three types of dried wood mould: Lf. Larval frass; F. Finer wood mould; Abs. Wood mould taken from trunk hollows with O. eremita absent. (Lf and F are fractions taken from the same trees.) Fig. 1. Concentración de nitrógeno (orgánico + amoniacal) (A) y fósforo (B) (media y desviación estándard, en mmol por g) en tres tipos de mantillo de la madera seca: Lf. Deyecciones larvales; F. Mantillo más fino en la madera; Abs. Mantillo de la madera tomado de cavidades formadas en troncos sin presencia de O. eremita. (Lf y F son fracciones tomadas de los mismos árboles.)

Acknowledgements This study was financially supported by Stiftelsen Lars Hiertas minne (to Thomas Ranius) and Sällskapet Hallands Väderös Natur (to Niklas Jönsson).

References Dajoz, R., 2000. Insects and forests. Intercept, London. Haack, R. A. & Slansky Jr., F., 1985. Nutritional ecology of wood–feeding Coleoptera, Lepidoptera, and Hymenoptera. In: Nutritional ecology of insects, mites, spiders, and related invertebrates: 449–486 (F. Slansky Jr., J. E. Rodríguez, Eds.). Wiley–Interscience, New York. Hedin, J. & Mellbrand, K., 2003. Population size of the threatened beetle Osmoderma eremita in relation in habitat quality. In: Metapopulation ecology of Osmoderma eremita – dispersal, habitat quality and habitat history: 101–112. Ph D. Thesis, Lund University. Ikeda, K., 1979. Consumption and food utilization by individual larvae and the population of a wood borer Phymatodes maaki Kraatz (Coleoptera: Cerambycidae). Oecologia, 40: 287–298. Kelner–Pillault, S., 1974. Étude écologique de peuplement entomologique des terraux d’arbres creux (chataigners and saules). Bull. Ecol., 5: 123–156. Lannér, J., 2003. Landscape openness. A longterm study of historical maps, tree densities, tree regeneration and grazing dynamics at Hallands Väderö. Licentiate thesis, Swedish Univ. of Agricultural Sciences, Alnarp. Luce, J.–M., 1996. Osmoderma eremita (Scopoli, 1763). In: Background information on invertebrates of the Habitats Directive and the Bern Convention. Part I: Crustacea, Coleoptera and Lepidoptera: 64–69 (P. J. van Helsdingen, L.

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Willemse, M. C. D. Speight, Eds.). Council of Europe, Strasbourg. Martin, O., 1993. Fredede insekter i Danmark. Del 2: Biller knyttet til skov. Entomologiske Meddelelser, 57: 63–76 [In Danish, English Summary.] Ranius, T., 2001. Constancy and asynchrony of populations of a beetle, Osmoderma eremita living in tree hollows. Oecologia, 126: 208–215. – 2002a. Population ecology and conservation of beetles and pseudoscorpions living in hollow oaks in Sweden. Animal Biodiversity and Conservation, 25.1: 53–68. – 2002b. Osmoderma eremita as an indicator of species richness of beetles in tree hollows. Biodiversity and Conservation, 11: 931–941. – 2002c. Influence of stand size and quality of tree hollows on saproxylic beetles in Sweden. Biological Conservation, 103: 85–91. Ranius, T. & Nilsson, S. G., 1997. Habitat of Osmoderma eremita Scop. (Coleoptera: Scarabaeidae), a beetle living in hollow trees. Journal of Insect Conservation, 1: 193–204. Viejo Montesinos, J. L., Molino Olmedo, F. & Martín Martín, J., 1996. Variación del contenido en carbono y nitrógeno a lo largo del proceso de putrefacción de la madera de Quercus, Pinus y Abies en Andalucía. Tomo Extraordinario, 125 Aniversario de la RSEHN. Boletín de la Real Sociedad de Historia Natural: 455–458. Wiedemann, K., 1930. Die Zelluloserverdauung b e i L a m e l l i c o r n i e r l a r v e n . Z e i ts c h r i ft f ü r Morphologie und Ökologie der Tiere, 19: 228–258.

Animal Biodiversity and Conservation 27.2 (2004)

When morphology and molecular markers conflict: a case history of subterranean amphipods from the Pilbara, Western Australia T. L. Finston, J. H. Bradbury, M. S. Johnson & B. Knott

Finston, T. L., Bradbury, J. H., Johnson, M. S. & Knott, B., 2004. When morphology and molecular markers conflict: A case history of subterranean amphipods from the Pilbara, Western Australia. Animal Biodiversity and Conservation, 27.2: 83–94. Abstract When morphology and molecular markers conflict: a case history of subterranean amphipods from the Pilbara, Western Australia.— Fifteen species of groundwater amphipods in the genus Chydaekata have been described from the Pilbara, Western Australia, each restricted to a single bore. Dewatering at a local mine site was halted while a second survey was undertaken. Newly collected samples were identified using the existing key, and allozyme analysis was used to test species boundaries. Allozymic diversity was not associated with single bores, and only two distinct genetic groups (one of which was very rare), were identified. Based on these results, and the finding that species were found to be more widespread, the Western Australian Environmental Protection Authority recommended that dewatering continue with caution at the site. This study provides an example of the problems associated with incongruent data sets, and the difficulties inherent in working with rare species, namely, interpreting the results of studies based on small samples or incomplete collections. Key words: Conservation, Genetics, Morphology, Species, Amphipods. Resumen Cuando la morfología y los marcadores moleculares entran en conflicto: el ejemplo de los anfípodos subterráneos de la región de Pilbara, Australia Occidental.— Se han descrito quince especies de anfípodos de aguas subterráneas del género Chydaekata que habitan en la región de Pilbara, Australia Occidental, restringiéndose cada una de ellas a una única perforación. Mientras se elaboraba un segundo estudio, se interrumpió el desagüe que se estaba llevando a cabo en un emplazamiento minero local. Las nuevas muestras recolectadas se identificaron utilizando la clave existente, mientras que para verificar los límites de la especie se recurrió a un análisis alozimático. La diversidad alozimática no se asoció con perforaciones únicas y sólo se identificaron dos grupos genéticos bien diferenciados (uno de los cuales era muy poco común). Basándose en estos resultados y en el hallazgo de que la especie estaba más extendida, el Organismo de Protección Medioambiental de Australia Occidental recomendó que se actuara con cautela al proceder con el desagüe. El presente estudio brinda un ejemplo de los problemas asociados con conjuntos de datos incongruentes, así como las dificultades que conlleva trabajar con especies poco comunes, especialmente en lo que respecta a la interpretación de los resultados de estudios basados en pequeñas muestras o recolecciones incompletas. Palabras clave: Conservación, Genética, Morfología, Especie, Anfípodos. (Rebut: 9 I 04; Conditional acceptance: 6 V 04; Final acceptance: 11 V 04) Terrie L. Finston, Michael S. Johnson & Brenton Knott, The Univ. of Western Australia, School of Animal Biology (M092), 35 Stirling Hwy., Crawley, WA 6009, Australia.– John H. Bradbury, The Univ. of Adelaide, Dept. of Environmental Biology, Adelaide, SA 5005, Australia.

ISSN: 1578–665X

Finston et al.

Introduction The groundwater of the Pilbara, Western Australia, is inhabited by a diverse and endemic assemblage of stygofauna (Humphreys, 1999, 2001). This fauna is dominated by crustaceans, although other groups such as annelids are occasionally represented. The region is particularly rich in amphipods, and recent morphological analyses of the ostracode and copepod fauna also suggest high levels of species diversity in these groups (Koranovic & Marmonier, 2003; Koranovic, 2004). Since 1995, five genera and 26 species of amphipods have been described from the Pilbara and Cape Range Peninsula, based on variation in morphological characters (Bradbury & Williams, 1996, 1997; Bradbury, 2000). The richness of the fauna is associated with the unique geology of the region (Humphreys, 2001). The Pilbara has an abundance of calcrete deposits, associated with current and paleo–river channels, within which form a network of fissures and chambers (Mann & Horwitz, 1979). Much of the region contains outcrops of banded iron ore and silica formations (Twidale et al., 1985), making the Pilbara an important producer of iron ore. High levels of species diversity and endemicity have major implications for mining industries in Western Australia, where much mining occurs beneath the local water table. Mining activity was halted during 2001 at one Pilbara mine site, Orebody 23 in the Ethel Gorge (23º 2’ S, 119º 5’ E), due to the discovery of a locally endemic stygofaunal community, and the concurrent introduction of the Environment Protection and Biodiversity Conservation Act in 1999, protecting threatened fauna and communities. This paper describes a genetic study and the associated series of events following the description of 15 species of Chydaekata from the Ethel Gorge and Fortescue Valley region, and highlights the difficulties involved in making decisions when sampling is incomplete and data sets are not congruent. Morphological analysis indicated that the amphipod fauna of the Ethel Gorge is characterised by high levels of local endemism and narrow species distributions (Bradbury, 2000). Fourteen of the 15 species of the genus Chydaekata were described from single sampling locations (bores) over a distance of approximately 35 km along the Fortescue River catchment north of Newman, WA (23º 4’ S, 119º 8’ E), while the remaining species was described from a site more than 100 km downstream. Three bores were located within the region to be dewatered for the extraction of iron ore from the Orebody 23 site. One of these contained six species of Chydaekata (Bradbury, 2000). Many evolutionary, ecological, and practical issues arise from these findings. In particular, high levels of local species diversity lead to several areas of investigation, including identifying the mechanisms behind the generation of diversity, the ecological factors that maintain sympatric species, and, most relevant to this paper, the implications for human activities on an endemic fauna.

The present study used allozyme electrophoresis to provide an independent evaluation of species boundaries in the genus Chydaekata within the Ethel Gorge, in keeping with the directive from the Minister for the Environment in Western Australia to “assess the conservation significance” of the local fauna (Humphreys & Armstrong, unpublished report). The decision–making process for the future of the mine was dependent upon two key factors: whether genetic data supported the species deliniations described by Bradbury (2000), and whether species were recorded from areas both within and outside of the area of dewatering. This study is the first step towards bringing a combined morphological and genetic approach to conservation issues for the largely undescribed stygofauna of the extensive Pilbara region. It is also an example of an application of the “taxonomic revolution” (see Trends in Ecology and Evolution, vol. 18 for a summary), a growing trend toward reliance on molecular data in making taxonomic decisions. Methods Samples were obtained from ten bores in the vicinity of the mine site, two within, five outside, and one on the boundary of the area to be dewatered. Amphipods were collected with a plankton net of mesh size 200 ✙m fitted with a glass vial. Upon being brought to the surface, the samples were placed in an insulated container to maintain ambient water temperature (approximately 28oC) and darkness. Effort was made to collect specimens of Chydaekata from their type localities, however only two (C. acuminata and C. brachybasis) were re– collected. In particular, bore WB23–4, the source of six of the described species, yielded no animals. Instead a sample was collected from a nearby bore in the same series of production bores (WB23–1) with similar depth and lithology. Specimens were treated in three ways. Approximately two–thirds were frozen whole in liquid nitrogen for allozyme electrophoresis, and the others were processed in two ways: approximately half of these were placed into 70% ethanol for morphological identification using the key for Chydaekata (Bradbury, 2000), and the remainder were dissected. For each dissected specimen, a small piece of tissue from the abdomen was placed in liquid nitrogen for allozyme analysis, and the head, gnathopods, and the last three body segments (urosomes) and their associated uropods were placed in ethanol. In this way, allozyme phenotypes could be matched with morphological phenotypes. The sites and the number of samples used for allozyme electrophoresis are shown in fig. 1. The amphipods were analysed for allozyme variation at 31 loci, using standard methods of cellulose acetate electrophoresis (Richardson et al., 1986), following a pilot study to identify polymorphic and readily interpretable loci. The present study included all 11 of the most commonly used enzymes compiled from more than 20 studies of allozyme variation in

Animal Biodiversity and Conservation 27.2 (2004)

W126 (29) W126NR (21) W126NRE (45)

WP116 (29) W152 (30)

Pilbara Ethel Gorge

W245 (121) W262 (0)

Western Australia

WB23–1 (55) W270 (21) W013 (5) 5 km

Perth 250 km

Fig. 1. Map showing the bores sampled in the present study and their placement in the mine site. Line indicates area of impact from dewatering activities; sample sizes for the allozyme analysis are in parentheses. Bore W262 yielded too few animals for electrophoresis. Fig. 1. Mapa en el que se indican las perforaciones muestreadas durante la realización del presente estudio, así como su localización en el emplazamiento minero. La línea indica el área de impacto de las actividades de desagüe; los tamaños de las muestras para el análisis alozimático se indican entre paréntesis. La perforación W262 produjo muy pocos animales para electroforesis.

amphipods (Stewart, 1993). Because of their small size, individuals were not screened for all 31 loci, but samples from a bore were split and run in two sets. The majority of specimens were analysed for loci in set I, which contained the following 17 loci: Amino aspartate transferase (Aat–m and Aat–s loci), Alkaline phosphatase (Alp), Arginine kinase (Apk1, Apk2, and Apk3 loci), Esterase (Est), Leucine amino peptidase (Lap), Malate dehydrogenase (Mdh–1 and Mdh–2 loci), Malate dehydrogenase NADP+ (Me–1 and Me– 2 loci), Mannose phosphate isomerase (Mpi), Peptidase leu–ala (Pep–1 and Pep–2 loci), Phosphoglucose isomerase (Pgi), and Phosphoglucomutase (Pgm). Between five and 15 individuals from each bore were analysed for loci in set II, which contained the following 14 loci: Aconitase (Acon–1, Acon–2 loci), Adenosine deaminase (Ada), Fructose–1,6–Diphosphatase (Fdp–1, Fdp–2 loci), Glycerol–3–Phospate dehydrogenase (Gpdh), Glyceraldehyde–3–Phosphate dehydrogenase (G3Pdh), Glucose–6–Dehydrogenase (G6pdh–1, G6pdh–2 loci), Isocitrate dehydrogenase (Idh–1, Idh–2 loci), 6–Phosphogluconate dehydrogenase (6Pgdh–1, 6Pgdh–2), and Triose phosphate isomerase (Tpi). The only exception was in the case of W013, where only five individuals were collected; these were run for set I loci only. To maintain continuity between the two data sets, loci at which on average, the frequency of the most common allele was < 0.90 (Aat, Mpi, Pgi, Pgm) were analysed in both sets. A second locus appeared for 6–Phosphogluconate dehydrogenase, the origin of which is uncertain, and is listed here as 6Pgdh–2. Alleles were scored relative to a common mobility standard of Chydaekata sp. from bore W245 in the Ethel Gorge.

To identify the presence of co–occurring species, we first considered the possibility of multiple species within bores, then considered the issue of differences between bores. To look for the presence of more than one species in a sample, the data sets were sorted into multi–locus genotypes, using only those individuals with no missing data. The multi– locus genotypes were inspected for multiple allelic substitutions among individuals. Second, tests for Hardy–Weinberg equilibrium and linkage disequilibrium were run for samples containing $ 30 individuals. Hardy–Weinberg equilibrium was tested in the HDYWBG module in BIOSYS (Swofford & Selander, 1989), and linkage disequilibrium was tested using Option 2 in Genepop on the web (http://wbiomed.curtin.edu.au/genepop/ adapted from Raymond & Rousset, 1995). Significance values were assessed using the sequential Bonerroni technique as described by Rice (1989), in order to reduce the incidence of Type I errors. All populations were assessed for heterozygote deficiency or excess using the fixation index, F, calculated in the STATS module of GDA (Lewis & Zaykin, 2001). F was averaged across variable loci. We would anticipate deviations from Hardy– Weinberg expectations, association of alleles, and heterozygote deficits if more than one species were present in a sample. Next, the data were inspected for evidence of variation between bores. Genic differentiation between pairs of bores was tested for all populations with samples $ 30, using a contingency test on the total number of copies of each allele at each variable locus. This was done using Option 3 in Genepop, and Fisher’s combined

probability method. Genetic distances and identities (Nei, 1972) were calculated among multi–locus genotypes and among bores in the DIST module of GDA (Lewis & Zaykin, 2001). Genetic distances were used in the MDS module in SYSTAT (Wilkenson, 1988). Multi–dimensional scaling was used to look for associations of genotypes with bores, indicating the presence of cryptic species. Data sets I and II were treated separately. The dissected portions of 13 amphipods were suitable for morphological identification, the remainder being too damaged to permit proper study. These dissected specimens were identified as belonging to five species (C. anophelma, C. acuminata, C. brachybasis, C. dolichodactyla, and C. tetrapsis) and were sampled from four of the nine bores. The specimens were analysed for the 17 loci from set I. Nei’s genetic identities and distances were calculated between each pair of individuals using the DIST module in GDA. This module was also used to produce a UPGMA dendogram of the distance values to investigate possible associations between genotypes and morphotypes. Results It was not possible to identify all specimens, because many appeared to possess mixtures of morphological characteristics of more than one species. However, some specimens could be identified, and in all, eight species were present in the ethanol preserved specimens (table 1). These examinations indicated that species had broader distributions than were indicated by the initial survey (Bradbury, 2000). Importantly, following the second survey, only one species, C. transversa, appeared to be restricted to the dewatering zone. Thirteen of the 31 loci were found to be variable, and 12 of these were from data set I (table 2). The majority had only two or three alleles, but two loci (Mpi, Pgi) had five alleles. There were 75 multi–locus genotypes among the 242 individuals analysed for set I loci, and 21 genotypes among the 48 individuals analysed for set II loci (table 3). Some genotypes were very common and widespread. Eight of the nine bores possessed genotype "n" from set I, comprising 22% of all individuals. Indeed, 47% of all individuals were represented by just four genotypes (n, x, ag, aq). However, many genotypes (56/75 in set I and 13/21 in set II) were represented by single individuals. The number of unique genotypes within bores ranged from 0 to 17 in set I and from 0 to 5 in set II. First we examined the possibility that more than one species was present in a bore. A single case was immediately detectable by allelic substitutions at six loci in the sample from W245 (table 2). Multi– dimensional scaling showed both the distinctiveness of one individual and the comparative cohesiveness of the others (fig. 2). The stress for this analysis was 0.106, indicating that the plot is a good representation of genetic variation. This population also showed linkage disequilibrium at six

Finston et al.

pairs of loci and Hardy–Weinberg disturbances at five loci. The divergent individual (W245–b) was removed from the data set, and the remaining individuals were examined for cryptic variation. Of the remaining 25 tests for HW equilibrium, there were no further deviations from expectations. Of 108 tests for linkage disequilibrium, there was only a single case of significant association between alleles. In W245–a, association was found between alleles at the Pep–1 locus and the Pgm locus. The fixation index was positive in the majority of samples (table 2). An examination of the multi–locus genotype data does not coincide with the morphological patterns. The proportion of unique genotypes in samples containing single and multiple species were not substantially different. We might expect to see more unique genotypes in populations containing multiple species, but the opposite occurred. WP116 and W270 each were identified as containing single species, and had 50% and 53% unique genotypes, respectively. In contrast, WB23–1 and W245 were identified as containing multiple species, yet had 49% and 44% unique genotypes. Next we addressed the possibility of differences among bores. Over all 31 loci, Nei’s genetic identity among bores was very high, ranging from 0.984 to 0.999 (table 4). Multi–dimensional scaling of data set I showed no discrete clusters to indicate the presence of multiple species, i.e., there was no association of genotypes with bores, as individuals from single bores were distributed throughout the scatter plot (fig. 3, Set I, stress = 0.198). In contrast, multi–dimensional scaling of data set II appeared to show association of genotypes with bores (fig. 3, Set II, stress = 0.142). However, inspection of the data for this less polymorphic set of loci indicated that this divergence was attributable to allele frequency differences at single loci, such that the individuals clustered into homozygote and heterozygote classes. For example, WP116 appears distinct due to a high frequency of the Mpi4 allele. Of the four unique genotypes shown (the fifth was not unique to the bore and is indicated by a + in the plot), three were Mpi44 homozygotes, while one was an Mpi34 heterozygote. The other genotype was an Mpi33 homozygote. The Mpi44 homozygote is also present in bore WP126NRE. The distinctiveness of the genotypes from W270 is due to a high frequency of Aat–s44 homozygotes. The Aat–s4 allele appears in two other populations (range from 0.04 to 0.09; see table 2), however W270 lacks Aat–s34 heterozygotes, despite the presence of Aat–s33 homozygotes in the population. Although genetic identities were very high, frequency differences were detected in the contingency tests of genic differentiation. Using Fisher’s combined probabilities, differences in allelic frequencies at a locus were significant between all three pairs of populations tested (W245, WB23–1, and WP126NRE). These differences were usually attributable to the presence of rare alleles in one of the pairs (table 2). Although there were subtle genetic differences among bores, the genetic variation did not corre-

Animal Biodiversity and Conservation 27.2 (2004)

Table 1. Identifications based on the morphological key for Chydaekata (Bradbury, 2000) for specimens from ten bores in the Ethel Gorge, and their location with respect to the dewatering zone. Adapted from Humphreys (unpublished data). Tabla 1. Identificaciones basadas en la clave morfológica correspondiente a Chydaekata (Bradbury, 2000), para especímenes procedentes de diez perforaciones en Ethel Gorge, y su emplazamiento con respecto a la zona de desagüe. Adaptado de Humphreys (datos no publicados).

Bore

Identification

Location

W013

Undetermined, showing characteristics of: C. ovatosetosa, C. acuminata and C. brachybasis

outside

W116

C. ovatosetosa

outside

W126

Undetermined, showing characteristics of: C. diagonalis and C. carscutica

outside

W126NR (type locality Undetermined, showing characteristics of: C. brachybasis) C. diagonalis and C. carscutica

outside

W126NRE

Undetermined, showing characteristics of: C. tetrapsis, C. anophelma and C. scopula

outside

W152 (type locality C. acuminata)

C. acuminata

outside

WB23–1

C. dolichodactyla, C. scopula, C. diagonalis and C. transversa

W245

C. brachybasis, C. anophelma and Undetermined, showing characteristics of: C. scopula and C. nudula

W262

Undetermined, showing characteristics of: C. acuminata and C. brachybasis

W270

C. dolichodactyla

spond to morphology. Not all samples were unequivocally assigned to species, but where definitive identifications were made, there was no corresponding genetic support. For example, WP116 appeared to contain a single species, C. ovatosetosa, a species not definitively found in any other bore, yet four of the five genotypes in WP116 were distributed amongst six other bores. Likewise, C. dolichodactyla was the sole species identified from the ethanol collections in bore W270, appearing in only one other bore (WB23–1; with three other species), yet five of the eight genotypes found in W270 also occurred in six other bores. Five species were identified from the dissected portions of specimens. UPGMA clustering of genetic distances between dissected specimens showed three main clusters (fig. 4A). However, the genetic distances between clusters were not large, ranging from 0.0 to 0.14 (identities ranged from 0.78 to 1.0), and the clusters did not correspond to morphological species. For example, the most distinct cluster (A) contained two individuals whose morphology placed them with C. anophelma and C. brachybasis. The two other major clusters, B

inside outside

inside boundary

and C, also contained individuals that keyed to C. anophelma. Cluster B consisted of several smaller clusters that showed no correspondence to morphology —all five morphospecies were represented in this cluster. Cluster C contained two morphospecies that were also found in clusters A and B. To look for frequency differences among species instead of individuals, multilocus genotypes belonging to the same species were pooled and genetic distances were reanalysed. Genetic distances were even lower among groups, ranging from 0.012 to 0.072 (fig. 4B). Identities ranged from 0.91 to 0.98. Discussion The patterns of variation produced by analysis of allozyme markers differed from that of the original morphology–based taxonomy. In contrast to high levels of localised diversity and narrow distributions, i.e. endemism associated with individual bores, we found a high degree of overlap among individual genotypes from different bores. However,

Finston et al.

Table 2. Allele frequencies for samples of amphipods from nine bores in the Pilbara, Western Australia: * Type locality for C. brachybasis; ** Type locality for C. acuminata; N. Number of individuals screened for loci in set I and set II, respectively; F. Mean fixation index, averaged across loci. Allele frequencies were pooled for loci common to both surveys; n.d. No data. The following loci were monomorphic for all individuals screened: Acon–1, Acon–2, Ada, Apk–2, Fdp–1, Fdp–2, Gpdh, G6pdh– 1, G6pdh–2, Idh–1, Idh–2, Lap, Mdh–1, Mdh–2, Me–2, 6Pgdh–1, 6Pgdh–2, Pgm–2. Tabla 2. Frecuencia de alelos para muestras de anfípodos procedentes de nueve perforaciones en la región de Pilbara, Australia Occidental: * Localidad tipo para C. brachybasis; ** Localidad tipo para C. acuminata; N. Número de individuos investigados para cada loci en los conjuntos de datos I y II respectivamente; F. Índice de fijación media, variación entre los loci. Las frecuencias de alelos se agruparon para aquellos loci que apaarecieron en ambos muestreos; n.d. Sin datos. Los siguientes loci fueron monomórficos para todos los individuos analizados: Acon–1, Acon–2, Ada, Apk–2, Fdp–1, Fdp–2, Gpdh, G6pdh–1, G6pdh–2, Idh–1, Idh– 2, Lap, Mdh–1, Mdh–2, Me–2, 6Pgdh–1, 6Pgdh–2, Pgm–2.

Site

W013

WP116

W126

W126NR

W126NRE* W152** WB23–1

W245–a W245–b

5 /0

20 / 9

24 / 5

11 / 10

30 / 15

20 / 10

47 / 8

104 / 16

0.000

0.378

0.047

–0.052

0.150

0.130

0.100

0.101

****

0.12

****

1.00

0.88

1.00

****

1.00

0.91

1.00

****

0.09

****

W270

1 / 0 11 / 10 0.000

0.376

0.01

****

1.00

0.98

1.00

0.93

****

0.01

****

0.07

****

0.01

1.00

****

0.96

1.00

0.99

****

0.81

0.04

****

0.19

Aat–m

Aat–s

Alp 2

****

0.05

****

0.05

1.00

0.87

0.91

0.89

0.85

0.93

0.98

1.00

0.95

****

0.13

0.09

0.11

0.10

0.07

0.02

****

1.00

****

1.00

****

1.00

****

1.00

****

1.00

****

1.00

****

Apk–1

Apk–3

Est 2

****

0.05

****

1.00

0.97

1.00

0.98

0.95

0.96

0.95

1.00

****

0.03

****

0.02

0.05

0.04

****

0.04

****

0.01

****

1.00

0.97

1.00

0.96

1.00

0.99

1.00

****

1.00

****

0.03

****

1.00

****

0.02

0.01

****

1.00

0.29

0.76

0.91

0.87

0.70

0.69

0.81

****

0.81

****

0.71

0.24

0.09

0.13

0.26

0.25

0.18

1.00

0.19

****

0.02

0.03

****

0.02

0.01

****

Me–1

Mpi

Animal Biodiversity and Conservation 27.2 (2004)

Table 2. (Cont.)

Site

W013

WP116

W126

W126NR W126NRE* W152** WB23–1

W245–a W245–b W270

Pep–1 2

0.10

****

0.07

****

0.90

1.00

0.99

0.93

1.00

****

0.01

****

0.07

0.02

****

1.00

0.94

0.98

1.00

****

1.00

****

0.01

****

0.03

0.90

1.00

0.84

0.91

0.98

0.67

0.88

0.97

****

0.80

0.10

****

0.16

0.09

0.02

0.33

0.09

0.03

****

0.17

****

0.02

****

Pep–2

Pgi

Pgm 2

****

0.13

0.05

0.02

****

0.06

0.01

0.50

****

1.00

0.53

0.77

0.26

0.73

0.61

0.75

0.50

0.73

****

0.47

0.34

0.18

0.72

0.27

0.33

0.24

****

0.27

n.d.

****

0.06

****

n.d.

****

0.71

1.00

0.94

1.00

0.29

****

Tpi

Table 3. Multi–locus genotypes found in each bore for data sets I and II: * Unique genotype. Tabla 3. Genotipos multilocus hallados en cada perforación para los conjuntos de datos I y II: * Genotipo único.

Bore

Set I

W013

n, s

WP116

q, aa, ax, bn, bt*

WP126

a*, c, e*, n, q, r*, s, aa, ag, ah, ai*, ak, aq, bn, bq*

W126NR

c, n, t*, y, ag, as*

Set II

d, f, h*, n*, q*

b, e, g, k, p*

a*, b, e, i*, k, m*

WP126NRE 28

g, m*, n, aa, ag, am*, ap*, aq, bb*, bh, bi*, bj*, bk*, bl*, bm, bn, bu*

c, f, j*, l*, o

W152

n, s, v, x, y, z*, ac*, ad*, ak, ar*, at*, au*, av, ax, bw*

b, c, e

WB23–1

b*, c, d*, g, h*, i*, j*, n, o, p*, s, u*, v, x, ag, ah, aj*, an*, aq, av, aw*, ay*, ba*, bd*, be*, bm, bn, bo*, bp*, bs*

c, d, e, f, g

W245

f*, g, k*, l*, n, o, s, w*, x, aa, ab*, af*, ag, ak, al*, ao*, aq, ax, az*, bc*, bf*, bg*, bh

W270

n, x, ae*, ag, ak, aq, br*, bv*

15 7

b, c, e, k b, k, r*, s*, t*, u*, v*

Finston et al.

Stress = 0.106 2 Axis 2

there was also considerably more overlap in morphological characters among specimens collected for this study, blurring species boundaries, and making species identifications difficult. The group shows extreme morphological diversity. The original taxonomy was based on a limited amount of material, and many of the specimens were juveniles. This precluded a study of character variation within species. Additional sampling associated with this study, while increasing the number of specimens examined, also revealed greater complexity and new combinations of characters. The most common multi–locus genotype was found in eight of the nine bores, representing nearly 25% of all individuals sampled. The presence of an apparently common, widespread species contradicts the most recent morphological identifications, where no species was definitively found in more than two bores. The same common alleles were present in all samples, and genetic identities among samples were very high. These values are typical of those associated with conspecifics, both for animals in general (Thorpe, 1982) and amphipods in particular (Stewart, 1993). Samples of Chydaekata, with identity values ranging from 0.984 to 0.999, are even less differentiated than typical allopatric populations of other amphipod species, showing differentiation that might be expected among individuals sampled from the same population. While there were small frequency differences among bores at some loci, including the occurrence of a few unique rare alleles, we could not find evidence to support the hypothesis that each bore contained a distinct species. The only exception was the presence of a single individual in bore W245 that showed substitutions at six of 17 loci, and large frequency shifts at two additional loci. However,

–2 –10

–8

–6

–4 –2 Axis I

Fig. 2. Multi–dimensional Scaling (MDS) plot of genetic distances among multilocus genotypes, showing distinctiveness of a single genotype at W245. Fig. 2. Representación gráfica mediante escalamiento multidimensional (MDS) de distancias genéticas entre genotipos multilocus, indicándose el carácter distintivo de un solo genotipo en W245.

without a morphological specimen, it is difficult to ascertain whether this represents a case of sympatry between species of Chydaekata, or between species in different genera. Of potentially greater relevance is the trend toward deficits of heterozygotes within bores, which suggests the mixing of genetically different groups. Notable diversity was detected in bore W270, where no

Table 4. Matrix of Nei's (1972) genetic identities (above the diagonal) and distances (below the diagonal) among bores, excluding the genetically distinctive individual W245–b. Tabla 4. Matriz de identidades genéticas (por encima de la diagonal) y de distancias (por debajo de la diagonal) de Nei (1972) entre las diversas perforaciones, sin incluir los individuos genéticamente diferentes W245–b.

W013

WP116

WP126

WP126NR WP126NRE W152

WB23–1

W245

W270

W013

*****

0.981

0.993

0.997

0.984

0.992

0.991

0.997

0.991

WP116

0.016

*****

0.989

0.987

WP126

0.006

0.009

*****

0.999

0.989

0.990

0.994

0.991

0.988

0.997

0.999

0.997

0.996

WP126NR

0.002

0.009

0.000

*****

0.994

0.997

0.998

0.996

WP126NRE

0.015

0.011

0.003

W152

0.006

0.009

0.002

0.005

*****

0.992

0.997

0.994

0.993

0.002

0.008

*****

0.997

0.996

0.995

WB23–1

0.008

0.004

0.001

0.002

*****

0.998

0.994

W245

0.002

0.007

0.002

0.001

0.006

0.004

0.002

*****

0.994

W270

0.008

0.010

0.003

0.006

0.004

0.005

*****

Animal Biodiversity and Conservation 27.2 (2004)

Set I

Set II

2 1 %

Axis 2

1 0

–1 –1 –2 –3 –3

Stress = 0.142

Stress = 0.198 –2

–1

0 Axis I

WP126NR WP126 multiple

WP116 WB23–1 W245

–2 –2

–1

0 Axis I

WP152 WP126NRE W270

Fig. 3. Multi–dimensional Scaling (MDS) plot of genetic distances among multilocus genotypes (divergent genotype, W245–b, removed). Fig. 3. Representación gráfica mediante escalamiento multidimensional (MDS) de distancias genéticas entre genotipos multilocus (genotipo divergente, W245–b, eliminado).

heterozygotes for Aat–s were found. One explanation of the trend towards deficits of heterozygotes could be the co–occurrence of subtly different species. Sampling from bores could also result in the artificial mixing of genetically divergent conspecific populations from different aquifers. However, sample sizes were small, particularly for set II loci, which may have affected our ability to pick up polymorphisms. Thus, although we cannot exclude the possible presence of multiple species, neither the minor genetic differences among samples nor the possible deficits of heterozygotes provide convincing evidence for multiple species. Hence, the allozyme data do not support the current taxonomy of endemism associated with individual bores. Even though mixture of genetically similar species would be more difficult to detect, especially in small samples, the bores purported to contain multiple species contained similar proportions of unique genotypes to those purportedly containing only one species. While small samples and limitations in the collections (i.e. lack of type specimens and definitive species identifications) mean these conclusions are provisional, these results make sense in light of the

recent morphological ambiguities, as well as the hydrological structure of the aquifer. The Fortescue River transects the borefield in the Ethel Gorge. A thin layer of alluvium overlays an extensive dolomite–calcrete deposit, which contains the aquifer. It is considered to be a continuous flow system, with recharge from the Fortescue River and rainfall (Barnett & Commander, 1985). Thus, hydrologically it behaves as a single, alluvial aquifer, and this connectivity would support the explanation of the presence of a common, widely distributed species. Still, we must consider the possibility that the allozyme data were not adequate for detecting species differences. Chydaekata may be a recent radiation, and may not have evolved allozymic divergence that corresponds to morphological variation. Shared polymorphisms do occur between closely related species due to common ancestry or introgression (Clark, 1997; Clarke et al., 1996; Morrow et al., 2000). Models predict that random drift will drive polymorphic sites to fixation. This can happen relatively quickly in small populations (Clark, 1997), but these polymorphisms may persist in large populations. The use of a large number of allozyme

Finston et al.

C. anophelma C. brachybasis C. anophelma C. brachybasis C. dolichodactyla C. acuminata C. dolichodactyla

0.14

C. tetrapsis C. anophelma C. acuminata

C. anophelma C. tetrapsis C. tetrapsis

0.105

0.07 Nei's D

0.035

0.00

C. anophelma C. tetrapsis C. brachybasis C. dolichodactyla C. acuminata

0.07

0.03 Nei's D

0.00

Fig. 4. UPGMA (Unweighted Pair Group Method with Arithmetic Average) diagram of Nei’s genetic distances among 13 individuals of Chydaekata with complementary allozyme phenotypes and morphological identifications: A. All individuals treated separately; B. Pooling of individuals belonging to the same species. Fig. 4. Diagrama UPGMA (Método de agrupamiento por parejas no ponderado con media aritmética) de las distancias genéticas de Nei entre 13 individuos de Chydaekata con fenotipos alozimáticos complementarios e identificaciones morfológicas: A. Todos los individuos tratados por separado; B. Conjunto de individuos pertenecientes a la misma especie.

loci should however, be able to overcome the signal of shared polymorphisms (Ting et al., 2000). Finally, morphological variation needs to be re–examined in this group. Many crustaceans, including amphipods, are known to exhibit variable morphological and life history characters (Dickson, 1977; Holsinger & Culver, 1970; Culver et al., 1990). Incongruous combinations of morphological characters and blurring of species boundaries in the present collections suggest that this may be the case, and that a taxonomic revision may be called for. Other approaches, such as a thorough investigation of character variation within species, and the use of more sensitive markers (e.g. rapidly evolving mtDNA genes), need to be undertaken in order to investigate further the relationship between genetic and morphological variation.

Despite ambiguities among data sets, a decision on the issue was requested by the mine operators, because of the cost to industry associated with an interruption to operations. The Department of Conservation and Land Management, the state government body responsible for advising the Environmental Protection Authority (EPA), took the position that dewatering would not lead to the extinction of a species. This was based on the following three factors: (1) most species previously thought to be restricted to the dewatering zone were found to have broader distributions outside the area of impact; (2) morphological boundaries between species were ambiguous; and (3) the allozymes provided no supporting evidence for distinct species. Consequently, the EPA advised the Minister for the Environment to allow mining activity to resume at Orebody 23, with the

Animal Biodiversity and Conservation 27.2 (2004)

condition that regular monitoring of the bores for stygofauna would continue. This case is an example of the difficulties scientists and managers face when studying rare and endangered fauna, that of small samples and incomplete collections. It highlights the dilemma posed by non–congruent data sets, underlining the need for guidelines for action when such circumstances arise. There are several examples where uncertainties in taxonomy have led to misdirected conservation efforts (see O’Brien & Mayr, 1991; Avise & Hamrick, 1996 for summaries; also see Daugherty et al., 1990; Bowen et al., 1991). The current thrust of governmental policy in Western Australia is to protect and conserve species and ecological communities (Humphreys & Armstrong, unpublished report). In response, mining and other companies planning to develop an area are required to conduct intensive Environmental Impact Assessments, which can be logistically difficult and expensive in remote areas of the state. Hence, what the companies require is certainty of procedure. This is further complicated by a potentially major and contentious issue: how are species defined and recognised for the purpose of meeting the legal requirements? Mayden (1997) observes that there are at least 22 concepts of species currently in use. Two sets of information often lead to congruent results, but how should decisions be made when the two data sets are incongruent, as in the present case? The most reasonable biological resolution, namely to conduct properly designed cross–breeding experiments at least to the F2 stage will, in most if not all situations involving stygofauna, be practically impossible to execute. Consequently, we suggest that a number of actions be taken, to establish a framework from which science and industry can develop suitable protocols. First, and most importantly, comprehensive systematic studies of the stygobitic fauna of the Pilbara are urgently needed. The real issue facing managers is how to manage something about which very little is known. Secondly, there needs to be informed and substantive debate directed towards developing an acceptable definition of a legal "operational species concept" which has sound biological basis. There have been recent arguments for a strictly molecular approach to taxonomy —i.e., a phenetic concept based on genetic distance or phylogeny (Tautz et al., 2003). While there are reasonable arguments against this extreme approach to the problem (see commentaries by Lipscomb et al., 2003; Seberg et al., 2003), the utility of molecular data as additional characters in making taxonomic decisions is not refuted. Finally, a regional approach needs to be adopted to place local findings in a broader context. This study demonstrates the complexity of issues facing government, industry and the scientific community, and makes clear the need for action in order to establish the framework within which to make well–informed decisions on issues of environmental concern.

Acknowledgements Funding for this project was provided by BHP– Billiton Pty. Ltd., and Hamersley Iron Pty. Ltd. Permits to collect samples were issued by the Department of Conservation and Land Management, Western Australia. Kyle Armstrong and Garth Humphreys (Biota Environmental Sciences) and David Kaljuste (BHP–Billiton) assisted with field collections, and Murray Eagle and David Porterfield (both BHP–Billiton) provided logistical support at the mine sites. The manuscript was improved through discussions with Garth Humphreys and Kyle Armstrong, and by comments from Stuart Halse (Department of Conservation and Land Management) and Bill Humphreys (Western Australian Museum), and several anonymous reviewers. References Avise, J. C. & Hamrick, J. L., 1996. Conservation Genetics: Case Histories from Nature. Chapman and Hall, New York, New York. Barnett, J. C. & Commander, D. P., 1985. Hydrogeology of the Western Fortescue Valley, Pilbara Region, Western Australia. Western Australia Geological Survey, Record 1986/8. Bowen, B. W., Meylan, A. B. & Avise, J. C., 1991. Evolutionary distinctiveness of the endangered Kemp’s ridley sea turtle. Nature, 352: 709–711. Bradbury, J. H., 2000. Western Australian stygobiont amphipods (Crustacea: paramelitidae) from the Mt Newman and Millstream regions. Records of the Western Australian Museum Supplement No., 60: 1–102. Bradbury, J. H. & Williams, W. D., 1996. Freshwater amphipods from Barrow Island, Western Australia. Records of the Australian Museum, 48: 33–74. – 1997. The amphipod (Crustacea) stygofauna of Australia: Description of new taxa (Melitidae, Neoniphargidae, Paramelitidae), and a synopsis of known species. Records of the Australian Museum, 49: 249–341. Clark, A. G., 1997. Neutral behavior of shared polymorphism. Proceedings of the National Academy of Sciences, 94: 7730–7734. Clarke, B., Johnson, M. S. & Murray, J., 1996. Clines in the genetic distance between two species of island land snails: how ‘molecular leakage’ can mislead us about speciation. Philosophical Transactions of the Royal Society of London B, 351: 773–784. Culver, D. C., Kante, T. C., Fong, D. W., Jones, R., Taylor, M. A. & Sauereisen, S. C., 1990. Morphology of cave organisms – Is it adaptive? Mémoires de Biospéologie, Tome XVII: 13–26. Daugherty, C. H., Cree, A., Hay, J. M. & Thompson, M. B., 1990. Neglected taxonomy and continuing extinctions of tuatara (Sphenodon). Nature, 347: 177–179.

Dickson, G. W., 1977. Variation among populations of the troglobitic amphipod crustacean Crangonyx antennatus Packard living in different habitats I. Morphology. International Journal of Speleology, 9: 43–58. Holsinger, J. R. & Culver, D. C., 1970. Morphological variation in Gammaruns minus Say (Amphipoda, Gammaridae) with emphasis on subterranean forms. Postilla, 146: 1–24. Humphreys, W. F., 1999. Relict stygofaunas living in sea salt, karst and calcrete habitats in arid northwestern Australia contain many ancient lineages. In: The Other 99%. The Conservation and Biodiversity of Invertebrates: 219–227 (W. Ponder & D. Lunney, Eds.). Royal Zoological Society of New South Wales, Mosman. – 2001. Groundwater calcrete aquifers in the Australian arid zone: the context to an unfolding plethora of stygal biodiversity. Records of the Western Australian Museum, Supplement No., 64: 63–83. Karanovic, T., 2004. Subterranean copepods (Crustacea, Copepoda) from arid Western Australia. Crustaceana Supplement, 3: 1–366. Karanovic, I. & Marmonier, P., 2003. Three new genera and nine new species of the subfamily Candoninae (Crustacea, Ostracoda, Podocopida) from the Pilbara region (Western Australia). Beaufortia, 53: 1–51. Lewis, P. O. & Zaykin, D., 2001. Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0 (d16c). Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/ software.html Lipscomb, D., Platnick, N. & Wheeler, Q., 2003. The intellectual content of taxonomy: A comment on DNA taxonomy. Trends in Ecology and Evolution, 18: 65–66. Mann, A. W. & Horwitz, R. C., 1979. Groundwater calcrete deposits in Australia: some observations from Western Australia. Journal of the Geological Society of Australia, 26: 293–303. Mayden, R. L., 1997. A hierarchy of species concepts: The dénouement in the saga of the species problem. In: Species: The Units of Biodiversity: 381–424 (M. F. Claridge, H. A. Dawah & M. R. Wilson, Eds.). Chapman and Hall, Melbourne. Morrow, J., Scott, L., Congdon, B., Yeates, D.,

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Frommer, M. & Sved, J., 2000. Close genetic similarity between two sympatric species of tephritid fruit fly reproductively isolated by mating time. Evolution, 54: 899–910. Nei, M., 1972. Genetic distance between populations. American Naturalist, 106: 283–292. O’Brien, S. J. & Mayr, E., 1991. Bureaucratic mischief: Recognising endangered species and subspecies. Science, 251: 1187–1188. Raymond, M. & Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86: 248–249. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution, 43: 223–225. Richardson, B. J., Baverstock, P. R. & Adams, M., 1986. Allozyme Electrophoresis. A handbook for animal systematics and population studies. Academic Press, Melbourne. Seberg, O., Humphries, C. J., Knapp, S., Stevenson, D. W., Peterson, G., Scharff, N. & Anderson, N. M., 2003. Shortcuts in systematics? A commentary on DNA–based taxonomy. Trends in Ecology and Evolution, 18: 63–65. Stewart, B. A., 1993. The use of protein electrophoresis for determining species boundaries in amphipods. Crustaceana, 65: 265–277. Swofford, D. L. & Selander, R. B., 1989. BIOSYS. A Computer Program for the Analysis of Allelic Variation in Genetics. Department of Genetics and Development, University of Illinois at Urbana–Champaign. Tautz, D., Arctander, P., Minelli, A., Thomas, R. H. & Vogler, A. P., 2003. A plea for DNA taxonomy. Trends in Ecology and Evolution, 18: 70–74. Thorpe, J. P., 1982. The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Annual Review of Ecology and Systematics, 13: 139–168. Ting, C., Tsaur, S. & Wu, C., 2000. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proceedings of the National Academy of Sciences, 97: 5313–5316. Twidale, C. R., Horwitz, R. C. & Campbell, E. M., 1985. Hamersley landscapes of the northwest of Western Australia. Revue de Geologie Dynamique et de Geographie Physique, 26: 173–186. Wilkenson, L., 1988. SYSTAT: The System for Statistics. SYSTAT Inc., Evanston, IL.

Animal Biodiversity and Conservation 27.2 (2004)

Animal Biodiversity and Conservation

Manuscrits

Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista interdisciplinària publicada, des de 1958, pel Museu de Zoologia de Bar celona. Inclou articles d'investigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxonomia, morfologia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfasis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica catàlegs, llistes d'espècies o cites puntuals. Els estudis realitzats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles. Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a internet a http://www.bcn.es/ABC, de manera que permet una difusió mundial dels seus articles. Tots els manuscrits són revisats per l'editor execu tiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció. Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

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

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

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

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

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

III

Animal Biodiversity and Conservation 27.2 (2004)

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

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. © 2004 Museu de Ciències Naturals

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

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

Animal Biodiversity and Conservation 27.2 (2004)

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.

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 Referen ces) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages including figures and tables. If the article describes new taxa, type material must be deposited in a public institution. Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 27.2 (2004)

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Animal Biodiversity and Conservation 27.2 (2004)

Arxius de Miscel·lània Zoològica vol. 1 (2003) 2003 Museu de Ciències Naturals de la Ciutadella ISSN: 1698-0476

Índex/Índice/Contents Uribe, F. & Ferrer, M., 2003. La revista Miscel·lània Zoològica: apunts per a la seva història. Arxius de Miscel·lània Zoològica, 1: 1–6. Abstract Miscel·lània Zoològica: some remarks for the history of this journal.— In a little over four decades the journal Miscel·lània Zoològica published some 900 papers. A simple review of the contents of these articles reveals several characteristics: the issues most commonly dealt with were faunistics and taxonomy, with insects making up the most frequently analyzed group. The geographical range was centred on the Iberian peninsula, mainly Catalonia. The intellectual heritage of Miscel·lània Zoològica has been continued since 2001 by the journal Animal Biodiversity and Conservation and by Arxius de Miscel·lània Zoològica as of this current volume. It is now time to start writing the history of Miscel·lània Zoològica. Key words: History, Miscel·lània Zoològica, Scientific journal. Benetti, C. J. & Régil Cueto, J. A., 2003. Hydrovatus caraibus Sharp, 1882 (Dytiscidae, Hydroporinae, Hydrovatini) nuevo para la fauna de Sudamérica. Arxius de Miscel·lània Zoològica, 1: 7–11. Abstract Hydrovatus caraibus Sharp, 1882 (Dytiscidae, Hydroporinae, Hydrovatini) new for the fauna of South America.— The species Hydrovatus caraibus Sharp, 1882 is registered for the first time for South America, after the captures in the municipality of Gramado, state of Rio Grande do Sul, Brazil. Of this form the rank of distribution of the specie, before restrict of the Caribbean, is extended up to the latitude 29º 26’ South, approximately. Key words: Hydrovatus caraibus, New record, South America. Baehr, M., 2003. New records of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae). Arxius de Miscel·lània Zoològica, 1: 12–17. Abstract New records of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae).— New records of species of the carabid genus Dolichoctis Schmidt–Göbel from New Guinea and several surrounding islands are dealt with. Apart from two new species that were described in another recent paper (Baehr, 2003), records of the following species from New Guinea are annotated: D. aculeata Chaudoir, D. biak Baehr, D. dentata Darlington, D. laticollis Baehr, D. striata Schmidt–Göbel, D. subquadrata Darlington, D. subrotunda Darlington, and D. suturalis Darlington. D. aculeata Chaudoir is also recorded for the first time from the island of New Britain. Additional material of D. spinipennis Chaudoir corroborates its status as a separate species, being particular for the Moluccas. Key words: Dolichoctis, New records, New Guinea, New Britain, Moluccas. Cadevall, J., Hernández, E., Nebot, J., Orozco, A., Uribe, F. & Bros, V., 2003. Influència de l'altitud en la riquesa d'especies de mol·luscs: variacions a la vall d'Alinyà, Alt Urgell, Lleida. Arxius de Miscel·lània Zoològica, 1: 18–45. Abstract Influence of elevation on the species richness in molluscs: variations in the Alinyà valley, Lleida (Northeast Spain).— The species richness of land molluscs is negatively correlated with altitude, while the altitudinal range of the species inhabiting at higher elevations is greater than in low levels. At the low scale of this study factors other than elevation may account better for the species richness. Key words: Altitudinal gradient, Elevation, Species richness, Mollusca.

web: http://www.bcn.es/arxiusMZ

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

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

Índex / Índice / Contents Animal Biodiversity and Conservation 27.2 (2004) ISSN 1578–665X

1–4 Hazra, N. & Chaudhuri, P. K. A new orthoclad species of Rheocricotopus Thienemann & Harnisch (Diptera, Chironomidae) from the Darjeeling–Sikkim Himalayas in India 5–13 Estrada, A., Jímemez, C., Rivera, A. & Fuentes, E. General bat activity measured with an ultrasound detector in a fragmented tropical landscape in Los Tuxtlas, Mexico 15–24 Jiménez–Valverde, A., Martín Cano, J. & Munguira, M. L. Patrones de diversidad de la fauna de mariposas del Parque Nacional de Cabañeros y su entorno (Ciudad Real, España central) (Lepidoptera, Papilionoidea, Hesperioidea) 25–36 Stefanescu, C. Seasonal change in pupation behaviour and pupal mortality in a swallowtail butterfly 37–45 Dennis, R. L. H. Landform resources for territorial nettle–feeding Nymphalid butterflies: biases at different spatial scales 47–52 Jawad, L. A., Al–Mukhtar, M. A. & Ahmed, H. K. The relationship between haematocrit and some biological parameters of the Indian shad, Tenualosa ilisha (Family Clupeidae)

53–56 Benetti, C. J. & Régil Cueto, J. A. Taxonomic notes on Amarodytes duponti (Aubé, 1838) (Dytiscidae, Hydroporinae, Bidessini) with redescription of male genitalia 57–66 Vargas, J. M., Guerrero, J. C. & Real, R. Effects of natural phenomena and human activity on the species richness of endemic and non–endemic Heteroptera in the Canary Islands 67–77 Bevanger, K. & Brøseth, H. Impact of power lines on bird mortality in a subalpine area 79–82 Jönsson, N., Méndez, M. & Ranius, T. Nutrient richness of wood mould in tree hollows with the Scarabaeid beetle Osmoderma eremita 83–94 Finston, T. L., Bradbury, J. H., Johnson, M. S. & Knott, B. When morphology and molecular markers conflict: a case history of subterranean amphipods from the Pilbara, Western Australia IX Abstracts del volum 1 (2003) d'Arxius de Miscel·lània Zoològica Abstracts del volumen 1 (2003) de Arxius de Miscel·lània Zoològica Abstracts of volume 1 (2003) of Arxius de Miscel·lània Zoològica