Animal Biodiversity and Conservation issue 26.1 (2003) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2003

and

Animal Biodiversity Conservation 26.1

Mallarenga emplomellada Parus cristatus. Dibuix de Francesc Jutglar publicat al Butll. GCA, 6: 116 (1989).

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 (Zoologia) 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 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 The Natural History Museum, London, United Kingdom 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 26.1, 2003 © 2003 Museu de Ciències Naturals (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 The journal is freely available online at: http://bcn.cat/ABC

Animal Biodiversity and Conservation 26.1 (2003)

Further new species of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae) M. Baehr

Baehr, M., 2003. Further new species of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae). Animal Biodiversity and Conservation, 26.1: 1–7. Abstract Further new species of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae).— Two new species of the carabid genus Dolichoctis Schmidt–Göbel from New Guinea and New Ireland are described: D. glabripennis of the striata–group (sensu Baehr, 1999) of the nominate subgenus, from New Guinea, and D. novaeirlandiae of the subgenus Spinidolichoctis Baehr, from the island of New Ireland. In New Guinea, D. glabripennis replaces D. microdera Andrewes of the Greater Sunda Islands and Moluccas that apparently does not occur in New Guinea. D. novaeirlandiae is the first record of a Dolichoctis from this island and it is outstanding due to its very short, only dentate elytra apex. Key words: Dolichoctis, New species, D. glabripennis n. sp., D. novaeirlandiae n. sp., New Guinea, New Ireland. Resumen Dos nuevas especies del género Dolichoctis Schmidt–Göbel de Nueva Guinea e islas cercanas (Insecta, Coleoptera, Carabidae, Lebiinae).— Se describen dos nuevas especies del género de carábidos Dolichoctis Schmidt–Göbel de Nueva Guinea y Nueva Irlanda: D. glabripennis del grupo striata (sensu Baehr, 1999) del subgénero nominal de Nueva Guinea, y D. novaeirlandiae del subgénero Spinidolichoctis Baehr, de la isla de Nueva Irlanda. En Nueva Guinea, D. glabripennis sustituye a D. microdera Andrewes de las islas de la Gran Sonda y de las Molucas, lo que aparentemente no ocurre en Nueva Guinea. D. novaeirlandiae constituye la primera cita de un Dolichoctis en esta isla y resulta excepcional por su ápice elitral muy corto y dentado. Palabras clave: Dolichoctis, Nueva especie, D. glabripennis sp. n., D. novaeirlandiae sp. n., Nueva Guinea, Nueva Irlanda. (Received: 19 XI 02; Conditional acceptance: 17 II 03; Final acceptance: 26 III 03) Martin Baehr, Zoologische Staatssammlung, Münchhausenstr. 21, D–81247 München, Germany. E–mail: Martin.Baehr@zsm.mwn.de

ISSN: 1578–665X

Introduction Since my revision of the New Guinean species of the lebiine genus Dolichoctis (BAEHR, 1999) additional material from New Guinea and several neighbouring islands has accumulated that includes two new species and several new records, the latter of which are enumerated in a separate paper to be published in Arxius de Miscel·lània Zoològica, published by the Museu de Ciències Naturals of Barcelona. Therein, inter alia, the specific status of a doubtful species from the Moluccas whas corroborated that was known to date only from the type series. The new species and records are due to the sampling efforts of several collectors, namely M. Balke (Berlin, now London), O. Missa (Brussels), A. Riedel (München, now Lincoln, Nebraska), and A. Weigel (Pößneck).

Methods Format and style of the descriptions, as well as measurements and ratios follow those used in my revision (BAEHR, 1999). Measurements were made under a stereo microscope using an ocular micrometer. Length was measured from apical margin of labrum to apex of elytra including the apical spines, hence, length measurements may slightly differ from those of DARLINGTON (1968). Length of prothorax was taken along midline, width of base of prothorax at position of posterior marginal seta, width of apex between the most advanced points of apex. The full list of synonymies of the already described species may also be taken from this revision. For dissection of the male genitalia the specimens were soaked in a wet jar overnight, the genitalia were then cleaned for a short time in hot 4% KOH. The habitus photographs were obtained using SPOT Advanced, version for Windows 3.5, and were subsequently worked using MS Corel Photo Paint 10. Abbreviations of collections: CBM. Working collection M. Baehr, München; CWP. Collection A. Weigel, Pößneck; IRSNB. Institut Royal des Sciences Naturelles, Bruxelles; ZSM–CBM. Zoologische Staatssammlung, München, as permanent loan in working collection M. Baehr.

Results

Dolichoctis glabripennis n. sp. (figs. 1, 2) Note This species had been noted by BAEHR (1999, p. 128) for New Guinea under the name D. microdera Andrewes, although some differences in shape and in structure of the surface between

Baehr

the holotype of the latter species (from Sumatra) and the New Guinean specimens were noted but regarded as being due to geographic variation. In the meantime, additional material of D. microdera from Sumatra, Borneo, and Sulawesi was available, and during examination it became evident that the mentioned differences are substantial and, thus, the New Guinean specimens belong to a separate species that with high probability is endemic to New Guinea. Presumably DARLINGTON (1968, p. 127) likewise included in D. microdera specimens of this new species that were mentioned by him from New Guinea, though D. microdera most probably does not occur in New Guinea. As a consequence, it should be removed from the checklist of the genus Dolichoctis occurring in New Guinea (BAEHR, 1999, p. 160) and be replaced by the new species. Nevertheless, D. microdera still occurs on Sulawesi. Types Holotype: {, INDONESIA or. Irian Jaya 170 km S Nabire Epomani 1,150m, 6 I 1996, leg. A. Weigel (ZSM–CBM). Paratypes: 3{, 1}, same data (CBM, CWP); 2{, INDONESIA or. Irian Jaya 50 km S Nabire Pusspensaat, 30 XII 1996 leg. A. Weigel (CBM, CWP); 1}, Canopy mission P. N. G. Madang province Baiteta Light AR52, 20 V 1996 Leg. Olivier Missa (IRSNB). Diagnosis Easily distinguished from all other New Guinean species by the narrow pronotum bearing a narrow lateral channel. From the closely related species D. microdera Andrewes it differs by anteriorly wider, therefore shorter, far less coarse microreticulate pronotum, almost completely reduced elytral striation, and remarkably glabrous, non–microreticulate elytra. Description Measurements: length 4.55–5.0 mm; width 2.05– 2.30 mm. Ratios: width/length of prothorax: 1.33– 1.36; width base/apex of prothorax: 0.98–1.00; width prothorax/head: 1.09–1.10; length/width of elytra: 1.36–1.40; length elytra/prothorax: 3.81– 3.86. Colour (fig. 2): glossy black, only labrum, mandibles, palpi, four basal antennomeres, legs, and the narrow margin of the elytra dark yellowish, pronotum more indistinctly margined yellow. Elytra with two rather small though conspicuous, yellow spots, the anterior one situated just behind humerus between 5th or lateral part of 4th and 8th intervals, respectively, if striae and intervals were distinct. Spot about circular though medio–posteriad with a triangular extension. The circular posterior spot situated in apical third of elytra between 2nd–5th intervals. Head: about as wide as or even wider than pronotum. Eyes very large though laterally but

Animal Biodiversity and Conservation 26.1 (2003)

1 3

0.25 mm

Fig. 1. Male genitalia of Dolichoctis glabripennis n. sp.: 1. Aadeagus; 2. Parameres; 3. Genital ring. Fig. 1. Genitalia masculina de Dolichoctis glabripennis sp. n.: 1. Edeago; 2. ParĂĄmeros; 3. Anillo genital.

moderately protruding. Labrum elongate, apically transverse and slightly excised, 6â&#x20AC;&#x201C;setose, lateroapically with a fringe of hairs. Mandibles moderately elongate. Palpi, labium and mentum as in D. microdera. Antennae of moderate size, surpassing base of pronotum by about 2 antennomeres. Median antennomeres c 2.5x as long as wide. Surface with distinct though slightly superficial, isodiametric microreticulation, fairly glossy. Pronotum: rather similar to that of D. microdera. Narrow, somewhat cordiform, fairly depressed, apex as wide as base, widest diameter slightly in front of middle. Lateral margin regularly convex, near base shortly excised. Apex fairly deeply excised, apical angles projecting, obtuse at tip. Base straight, laterally obliquely rounded, basal angles wide, >100Â°, rather obtuse. Apex indistinctly margined, base margined only laterally. Median line distinct, almost complete, slightly deepened towards base, complete. Anterior transverse impression absent, basal impression moderately impressed. Lateral channel narrow throughout, but slightly widened immediately in front of base. Basal grooves rather deep, more or less linear, slightly oblique, anteriorly and posteriorly merging into transverse basal sulcus and into lateral channel. Anterior lateral seta absent, posterior lateral seta situated at basal angle. Surface with fine transverse wrinkles and with highly superficial, isodiametric to slightly transverse microreticulation, almost impunctate, rather glossy. Elytra: rather wide and short, somewhat quadrate, dorsal surface highly convex. Humeri widely rounded, lateral margin gently convex, apical

Fig. 2. Habitus of Dolichoctis glabripennis n. sp., length 4.8 mm. Fig. 2. Habitus de Dolichoctis glabripennis sp. n., longitud 4,8 mm.

margin oblique, straight or even very gently concave. Apical angle rounded. Marginal channel narrow, slightly widened at anterior third. Striae barely indicated or almost lacking, usually only inner striae basally perceptible as fine lines or rows of extremely faint punctures. Intervals absolutely depressed, impunctate. Two extremely fine discal punctures present in middle of third interval slightly behind middle and in apical fourth of elytra, bearing almost invisible, extremely short setae. Marginal series consisting of eight punctures behind humerus, two punctures behind middle, four more widely spaced punctures in apical third, and a single puncture at end of 3rd stria. Humeral and apical punctures widely separated. Marginal setae remarkably elongate. Microreticulation absent, surface highly glossy. Inner wings fully developed. Lower surface: metepisternum elongate, almost 2x as long as wide. Abdomen impunctate. Terminal sternite bisetose in male, quadrisetose in female. Legs: elongate, tarsi very slender. Tarsal claws elongate, with 4 fairly large teeth. Male genitalia (fig. 1): genital ring oval– shaped, rather asymmetric, with large apical plate. Aedeagus short and stout, depressed in apical half, lower surface gently bisinuate. Apex rather short and stout, wide, triangularly narrowed towards tip, though tip obtuse. Orificum short, slightly turned to the left side, internal sac at bottom with two large, polydentate sclerites which both end in an acute tooth that is directed towards apex. Parameres very dissimilar, right paramere small, fairly short, left paramere large, rather short, at apex evenly convex. Variation: Slight variation noted only in distinctness of elytral striae, as these are almost lacking in all Irian Jaya specimens, though yet perceptible but highly superficial in the single Papua New Guinea specimen. Distribution So far known from western central Irian Jaya and northern central Papua New Guinea. Collecting circumstances Largely unknown. Irian Jaya specimens probably sieved from litter on or under logs in rain forest, the Papua New Guinea specimen collected at light in lowland rain forest. Some specimens sampled at median altitude, at about 1,150 m. Etymology The name refers to the remarkably glabrous elytra. Relationships D. glabripennis is closely related to D. microdera Andrewes which is widely distributed through the Greater Sunda Islands from Sumatra to Sulawesi. Recognition For recognition of D. glabripennis the key in my

Baehr

revision (BAEHR, 1999, p. 124) scarcely needs alteration. Under caption 2. just replace microdera Andrewes by glabripennis n. sp.

Dolichoctis novaeirlandiae n. sp. (figs. 3–6) Types Holotype: }, PNG, New Ireland prov. Schleinitz Range, 15 km S. E. Fissoa, 100m 03° 02’ 58'’S, 151° 34’ 88'’E, 7 III 2000 leg. A. Weigel (CBM–ZSM). Paratype: }, same data (CBM). Diagnosis Easily distinguished from all other species of subgenus Spinidolichoctis Baehr except for S. dentata Darlington by the dentate rather than aculeate sutural apex of the elytra. Distinguished from D. dentata by the wide, not cordate pronotum and the oval-shaped rather than quadrate elytra. Description Measurements: length 6.1 mm; width 2.70– 2.75 mm. Ratios: width/length of prothorax 1.78–1.81; width base/apex of prothorax 1.30– 1.33; width prothorax/head 1.44–1.51; length/ width of elytra 1.42–1.47; length elytra/ prothorax 3.83–3.85. Colour: deep black, only borders of labrum, mandibles, palpi, antennae, tarsi and apex of tibiae reddish, lateral margin of pronotum very indistinctly translucent. Apical denticle of elytra black. Abdomen dark piceous to black. Head: generally as in related species of subgenus Spinidolichoctis . Labrum elongate, anteriorly slightly convex. Frons in middle behind clypeal suture with an extremely shallow, about circular impression. Eyes of average size, almost semicircular, laterally markedly projecting, orbits short, rather oblique, neck rather narrow. Only the posterior supraorbital seta present, anterior seta absent, though the pore present. Antenna rather short, slightly surpassing base of pronotum, subapical antennomeres about 1.5x as long as wide. Surface with fairly distinct though somewhat superficial isodiametric microreticulation, with extremely fine and scattered puncturation, and on vertex with fine wrinkles, moderately glossy. Pronotum (fig. 4): very wide, depressed, base considerably wider than apex. Lateral margin evenly convex, in apical half markedly incurved, towards base gently convex to almost straight. Apex rather deeply excised, excision almost transverse, apical angles produced but evenly rounded. Basal angles very obtuse, base straight, laterally obliquely convex. Apex margined throughout, though faintly in middle, base not margined. Median line fairly impressed, almost reaching apex and base, basal grooves fairly deep, about linear, obliquely oval–shaped. Lateral explanation wide throughout, even widened towards

Animal Biodiversity and Conservation 26.1 (2003)

4 0.25 mm

Figs. 3–5. Dolichoctis novaeirlandiae n. sp.: 3. Female stylomeres; 4. Pronotum; 5. Apex of elytra. Figs. 3–5. Dolichoctis novaeirlandiae sp. n: 3. Estilómero femenino; 4. Pronoto; 5. Ápice del élitro.

base, lateral margins not perceptibly upturned though widely explanate. Anterior lateral seta absent, posterior seta situated at basal angle. Surface with some fine, irregular wrinkles and fine, scattered punctures, with fine and very superficial microreticulation that is composed of transverse lines and meshes, rather glossy. Elytra (figs. 5, 6): comparatively elongate, rather depressed, gently oval, widest in middle, lateral margins almost evenly convex. Lateral apical angles obtusely angulate, sutural angles slightly dehiscent, triangularly dentate. Striation complete, striae rather lightly impressed, impunctate, intervals very gently convex, impunctate. Two very fine discal punctures situated considerably behind middle and at apical fifth. The anterior puncture in middle of 3rd interval, the posterior one near 2nd stria. Surface with very fine and superficial though remarkably regular microreticulation composed of transverse lines and meshes, rather glossy, even slightly iridescent. Inner wings fully developed. Lower surface: metepisternum moderately elongate, c 1.8x as long as wide. Abdomen impunctate. Terminal abdominal sternum in female bisetose. Legs: elongate, slender. Tarsal claws elongate, with 3–4 rather delicate teeth. Male genitalia: unknown. Female genitalia (fig. 3): apex of stylomere 1 asetose. Stylomere 2 elongate, curved, with 2 elongate latero–ventral ensiform seta and one elongate medio–dorsal ensiform seta. Apparently without any nematiform seta. Variation: faint variation noted in relative shape of pronotum and elytra.

Fig. 6. Habitus de Dolichoctis novaeirlandiae n. sp., length 6.1 mm. Fig. 6. Habitus de Dolichoctis novaeirlandiae sp. n., longitud 6,1 mm.

Baehr

Partial identification key of Dolichoctis novaeirlandiae n. sp. (see BAEHR, 1999). For recognition of both new species the key in my revision (BAEHR, 1999, p. 124) is changed up to caption 10 from there (the key has not been altered and will not be repeated here). Clave parcial para la identificación de Dolichoctis novaeirlandiae sp. n. (ver BAEHR, 1999). Para reconocer las dos nuevas especies, la clave de mi revisión (BAEHR, 1999, p. 124) se ha cambiado hasta el punto 10 (el resto de la clave no se ha cambiado y no se incluye).

Apex of elytra rounded, not dentate or aculeate at sutural angle Apex of elytra dentate or aculeate at sutural angle 2 Prothorax wide, marginal channel wide (BAEHR, 1999, fig. 29) Prothorax narrow, marginal channel narrow (fig. 2) 3 Elytra wide, ovate; marginal channel wide, explanate Elytra narrow, lateral margin parallel; marginal channel narrow, not explanate 4 Head and pronotum with microreticulation; colour either unicolourous, blackish or dark piceous, or elytra blackish with reddish sutural stripe, or bimaculate in posterior half with maculae situated near suture Head and pronotum without microreticulation; colour either distinctly bicolourous with head and prothorax reddish and elytra darker, or light brownish throughout 5 Eyes small but abruptly prominent, frons swollen on either side; prothorax semicircular, >2x as wide as long Eyes normal, not abruptly prominent, frons normal; prothorax not semicircular, <2 x as wide as long 6 Elytra either with reddish sutural stripe or bimaculate in posterior half Elytra unicolorous 7 Elytra with reddish sutural stripe Elytra bimaculate in posterior half 8 Pronotum narrower, cordiform, without distinct reddish margins, basal angles rectangular (BAEHR, 1999, fig. 49); elytral spots broadly joined at suture, forming a common elliptical transverse spot (BAEHR, 1999, fig. 102) Pronotum wider, laterally evenly convex, with distinct reddish margins, basal angles obtuse (BAEHR, 1999, fig. 50); elytral spots separated at suture, somewhat irregularly shaped (BAEHR, 1999, fig. 103) 9 Both supraorbital setae present; in the case of broken anterior seta, lateral margins of pronotum wide and distinctly reddish translucent, elytra with very weak and superficial microreticulation and with distinct iridescent lustre; aedeagus (BAEHR, 1999, fig. 5) Anterior supraorbital seta absent, though pore present; lateral margins of pronotum more or less wide but usually not distinctly reddish translucent, elytra usually with more distinct microreticulation and without or with less distinct iridescent lustre 10 Sutural apex of elytra only dentate (fig. 5; BAEHR, 1999, fig. 62) Sutural apex of elytra aculeate (BAEHR, 1999, figs 59, 60, 63–77) 10a Elytra rather quadrate; pronotum not much wider than head, rather cordiform (BAEHR, 1999, fig. 32). New Guinea Elytra oval–shaped (fig. 6); pronotum much wider than head, not cordiform (fig. 4). New Ireland

Dolichoctis s. str. 4

3 glabripennis n. sp. striata Schmidt–Göbel

elongata Baehr

Spinidolichoctis n. subgen.

Papuadolichoctis n. subgen.

distorta Darlington 6 7 9 suturalis Darlington 8

angustemaculata Baehr

riedeli Baehr

bisetosa Baehr

10 10a 11

dentata Darlington novaeirlandiae n. sp.

Animal Biodiversity and Conservation 26.1 (2003)

Distribution Central New Ireland. Known only from type locality. Collecting circumstances Largely unknown. Probably collected under bark of logs in rain forest at low altitude. Etymology The name refers to the range of this species, the island of New Ireland. Relationships Although D. novaeirlandiae has in common the short, dentate apex of the elytra with D. dentata Darlington from New Guinea, most probably it is not closely related to the latter species, because the mentioned similarity presumably is a plesiomorphic character state still present in both species. Recognition For recognition of D. novaeirlandiae the key in my revision (BAEHR, 1999, p. 124) can be followed to caption 10 which subsequently must be altered as the adjoined partial identification key. Remarks The new species communicated herein in some ways alter distribution and species inventory of the genus Dolichoctis in the Papuan Subregion. The new species D. novaeirlandiae extends the range of the genus Dolichoctis to New Ireland. The new species Dolichoctis glabripennis underlines the status of New Guinea as a stronghold of endemism for the genus Dolichoctis, because the number of species common to New Guinea and Southeast Asia again is reduced and apparently now only includes the widespread D. striata Schmidt–Göbel of the nominate subgenus, and D. aculeata Chaudoir of the predominantly Papuan subgenus Spinidolichoctis, The latter species occurs in New Guinea, New Britain, and northern Australia, but also on Sulawesi and Buru Islands. However, even the common "species" Dolichoctis striata remains doubtful in some ways, because specimens at my disposal from the Philippine Islands, the Moluccas, various parts of New Guinea, and Australia differ rather in certain aspects of their external shape and structure from those of the Sunda Islands and continental South Asia, and thus, it is quite uncertain whether this

complex can be maintained as a single "species" in future. Presumably, it would be better —or even should be— dismembered into subspecies or even separate species. This survey, however, is not yet finished and to date, no clear picture has been gathered. Nevertheless, the thoughts about colonization of New Guinea by species–groups and species of the genus Dolichoctis expressed in BAEHR (1999) do not need much alteration, because the evolution of D. glabripennis and/or the immigration of its ancestor must indeed have been a rather recent event, with respect to the still close relationship between this New Guinean species and the Oriental D. microdera. In view of its only dentate instead of aculeate elytral apex, Dolichoctis novaeirlandiae seems to be rather remotely related to any New Guinean species of the subgenus Spinidolichoctis. Such structure of the elytral apex only occurs in D. dentata Darlington from New Guinea which, however, does not seem to be closely related to D. novaeirlandiae . The question how D. novaeirlandiae evolved and/or from where it or its ancestor arrived on New Ireland, still remains open. However it must be closely related to the original stock of the present subgenus Spinidolichoctis that is restricted to the Moluccas, the New Guinean region, and northern Australia.

Acknowledgements My sincere thanks to Dr. M. Balke, London; Mr. A. Drumont, Brüssels; Dr. A. Riedel, München, now Lincoln, Nebraska; and Mr. A. Weigel, Pößneck for lending or donating the material.

References BAEHR, M., 1999. The genus Dolichoctis SchmidtGöbel, 1846 in New Guinea and surrounding areas (Coleoptera: Lebiinae). Coleoptera , (1998): 121–169. CHAUDOIR, M. de, 1869. Mémoire sur les Coptodérides. Ann. Soc. Ent. Belg., 12: 163–256. DARLINGTON, P. J. Jr., 1968. The Carabid beetles of New Guinea. Part III. Harpalinae continued. Perigonini to Pseudomorphini. Bull. Mus. Comp. Zool., 139: 1–253.

"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 26.1 (2003)

Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria B. C. Emerson

Emerson, B. C., 2003. Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria. Animal Biodiversity and Conservation, 26.1: 9–20. Abstract Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria.— High levels of floral and faunal diversity in the Canary Islands have attracted much attention to the archipelago for both evolutionary and ecological study. Among the processes that have influenced the development of this diversity, the volcanic history of each individual island must have played a pivotal role. The central island of Gran Canaria has a long geological history of approximately 15 million years that was interrupted by violent volcanism between 5.5 and 3 million years ago. Volcanic activity is thought to have been so great as to have made all plant and animal life virtually extinct, with survival being limited to some coastal species. The implication from this is that the higher altitude laurel forest and pine woods environments must have been re–established following the dramatic volcanic period. This paper reviews the evidence for this using recent molecular phylogenetic data for a number of plant and animal groups on the island of Gran Canaria, and concludes that there is general support for the hypotheses that the forest environments of Gran Canaria post–date the Roque Nublo eruptive period. Key words: Gran Canaria, Phylogeography, Biodiversity, Ecology, Evolution. Resumen Genes, geología y biodiversidad: diversidad de la fauna y flora de la isla de Gran Canaria.— La extensa diversidad de la flora y fauna de las Islas Canarias ha convertido el archipiélago en un centro de especial interés para los estudios sobre evolución y ecología. De entre los procesos que han influido en el desarrollo de esta diversidad, cabe destacar el importante papel que ha desempeñado la historia volcánica de cada una de las islas. La isla principal del archipiélago, Gran Canaria, tiene una larga historia geológica de aproximadamente unos 15 millones de años, que fue interrumpida por un violento volcanismo que tuvo lugar hace entre 5,5 y 3 millones de años. Se considera que la actividad volcánica fue de tal magnitud, que prácticamente extinguió toda la vida vegetal y animal de las islas, a excepción de unas pocas especies costeras que lograron sobrevivir. De ello puede deducirse que los entornos de mayor altitud, como los bosques de laureles y pinos, seguramente se reestablecieron tras el dramático período volcánico antes mencionado. En este trabajo, se revisa la evidencia de ello mediante el análisis de datos filogénicos moleculares recientes de una serie de grupos de plantas y animales de la isla de Gran Canaria, y se demuestra la validez general de la hipótesis que sostiene que los entornos forestales de Gran Canaria son posteriores al ciclo eruptivo de Roque Nublo. Palabras clave: Gran Canaria, Filogeografía, Biodiversidad, Ecología, Evolución. (Received: 28 V 02; Conditional acceptance: 27 IX 02; Final acceptance: 4 XI 02) B. C. Emerson, Centre for Ecology, Evolution and Conservation (CEEC), School of Biological Sciences, Univ. of East Anglia, Norwich NR4 7TJ, United Kingdom (U.K.). E–mail: b.emerson@uea.ac.uk

ISSN: 1578–665X

Emerson

Introduction The Canary Islands (fig. 1) are increasingly being utilised for evolutionary studies of colonisation and speciation (for a review see JUAN et al., 2000), the attraction stemming from the great diversity within the flora and fauna of the archipelago. The Canary Islands are characterised by a high level of species endemism, and groups of closely related species are often characterised by a diversity of both morphological and ecological types. The rich biodiversity of the Canarian archipelago is undoubtedly attributed in part to the diversity of habitats present. The Canary Islands have a subtropical climate with warm temperatures that show little seasonal variation. The climate is strongly influenced by the humid trade winds from the northeast, which in combination with the altitude of the volcanoes and the drier northwest winds blowing at higher levels produce an inversion zone and marked vegetational zones. Five vegetational zones can be recognised: 1. Arid subtropical scrub up to 250m; 2. Humid and semi–arid subtropical scrub and woods from 250 to 600m; 3. Humid laurel forest in the cloud belt from 600 to 1,000 m; 4. Humid to dry temperate pine forest from 1000 to 2,000 m; 5. Dry subalpine scrub over 2,000 m. Although individual islands are characterised by a diversity of habitats the extent of these on each island differs, and this can be attributed to both natural and non–natural causes. For example, due to their low elevation the eastern islands of Fuerteventura and Lanzarote are naturally lacking forest habitats. In contrast forest environments occur naturally on the island of Gran Canaria, but the extent of these has been drastically reduced by human activity. Only a small percentage of the

20º

Iberian peninsula

original Pinus canariensis forest, totalling about 12,000 ha remains, and this is fragmented (PÉREZ DE PAZ et al., 1994). There is now almost no lowland thermophilous forest and of the once extensive laurel forest there remain only two fragments amounting to approximately 130 ha. Not surprisingly, Gran Canaria is characterised by a large number of plant species recognised as endangered or threatened (AIZPURU et al., 2000). The laurel forest and pine woods have been viewed as a relict flora (CIFFERI, 1962), proper to the Tertiary and thus constituting the oldest island environments (MACHADO, 1976). In fact many plant genera from Macaronesia (Canary Islands, Madeira, Azores, Selvagens, and Cape Verde Islands) have been considered relict survivors from the Tertiary period. This hypothesis of a relict origin for many elements of the Macaronesian flora can be traced back to the end of the last century (ENGLER, 1879) and has continued to win favour with more modern biogeographers (e.g. WULF, 1943; LEMS, 1960; CIFERRI, 1962; MEUSEL, 1965; TAKHTAJAN, 1969; BRAMWELL, 1972, 1976; HUMPHRIES, 1976; SUNDING, 1979; CRONK, 1992). Evidence for a relict origin comes from fossil data suggesting that many groups now found in the laurel forests and sclerophilous zones of Macaronesia were apparently lost from the flora of Europe at the end of the Tertiary and in the Pleistocene due to climate change. The woody habit of many Macaronesian plants has also been viewed as an ancestral trait that identifies them as a relict flora. Recent molecular phylogenetic studies have sought to test this hypothesis of a relict origin for a number of plant groups and, perhaps surprisingly, little evidence has come to light (see EMERSON, 2002 for a review). This does not rule out the possibility of a component of the Canary Island

Lanzarote (15.5) La Palma (2)

Madeira

Tenerife (11.6)

Salvages Africa Canary Islands

Fuerteventura (20)

Gran Canaria (14–16) La Gomera (10) El Hierro (1)

Fig. 1. The Canary Islands. Numbers in parentheses refer to the proposed maximum geological ages for each of the Canary Islands, estimated in millions of years. Fig. 1. Las islas Canarias. Los números entre paréntesis se refieren a los máximos períodos geológicos propuestos para cada una de las islas, estimados en millones de años.

Animal Biodiversity and Conservation 26.1 (2003)

flora being relicts from the tertiary, and indeed molecular data can not exclude this for the laurel forest endemic Ixanthus viscosus (Gentianaceae) (THIV et al., 1999) and molecular phylogenetic data support a relict origin for the monotypic genus Allagopappus (FRANCISCO–ORTEGA, 2001). Similar to Allagopappus, molecular data also describe basal phylogenetic positions for the monotypic genus Plocama (BREMER, 1996; ANDERSSON & ROVA, 1999) and Lavatera phoenicea (RAY, 1995) supporting a possible relict origin for these taxa. An old age for the forest environments may also lead to older associations within these environments for the animal species inhabiting them. It is interesting that in the laurel forests of the Canarian archipelago many insect groups reach their maximum of endemicity (MACHADO, 1976), an observation supporting the antiquity of the laurel forest environment (EMERSON et al., 1999). However, this observation of high endemicity is just that, suggestive but not conclusive. To test the general hypothesis that the forest environments are relictual a molecular phylogenetic approach is required to generate age estimates for the origin of species groups confined to the forest environments. A suitable island for testing this general hypothesis is that of Gran Canaria. The island of Gran Canaria has a maximum subaerial age of approximately 15 million years (My) (HOERNLE et al., 1991), making it the geologically oldest island with forest environments. One may argue that the limited laurel forest remaining may introduce a bias due to a concomitant species loss with deforestation. This analysis is restricted to laurel forest data for Coleoptera, for which it has been noted that there is frequent sympatry of closely related species (MACHADO, 1976), and for which many species have managed to survive in deforested areas, through use of alternative humid habitat (P. Oromí, pers. comm.). It is generally accepted by geologists that the recent eruptive period that formed the Roque Nublo agglomerate complex (from 5.5 million years ago (Mya) to 3 Mya) was very explosive (PÉREZ–TORRADO et al., 1995). It is very probable that the whole vegetation of this island, except possibly some coastal species, went extinct (ARAÑA & CARRACEDO, 1980; MARRERO & FRANCISCO–ORTEGA, 2001). Given this consideration we can define two hypotheses with regard to the antiquity of the forest environments in Gran Canaria that can be tested with molecular phylogenetic data: Hypothesis 1 (H1): The forest environments of Gran Canaria are ancient and survived through the Roque Nublo eruptive period. If this is true then sequence divergence estimates for some species groups inhabiting the forests should pre– date the end of the Roque Nublo eruptive period (3 My). Hypothesis 2 (H2): The forest environments of Gran Canaria post–date the Roque Nublo eruptive period. If this is true then no age estimates for species groups inhabiting the forests should

pre–date the end of the Roque Nublo eruptive period (3 My). Recent molecular phylogenetic analyses of plant and animal groups on the Canary Islands provide a number of data sets for testing which of the two hypotheses (H1, H2) best fit the forest environments of Gran Canaria. What follows is a review of these studies with an assessment of their support for H1 or H2, and a comparative assessment of data for non–forest organisms.

Flora and fauna of the pine and laurel forests

Laurus azorica Laurus azorica (Canary Island laurel) is one of two species in the genus and is native to the Canary Islands, Madeira and the Azores. The second species, L. nobilis, is found in southern and western Europe, including all the Mediterranean area and the Atlantic coast of France and the Iberian peninsula (ARROYO–GARCÍA et al., 2001). The common ancestor of both species was broadly distributed in Europe from the Miocene until the Pleistocene (BARBERO et al., 1981). Laurus azorica is one of the defining species of the laurel forests of the Canary Islands. Recently ARROYO–GARCÍA et al., 2001 have undertaken an amplified fragment length polymorphism (AFLP) analysis to establish genetic similarities among populations of both species of Laurus. Genetic similarities between each pair of samples were calculated using the number of shared amplification products using the Dice (SNEATH & SOKAL, 1973) which were then represented as a dendrogram (fig. 2). From figure 2 it is clear that the genetic diversity encompassed by L. azorica falls within the greater genetic diversity exhibited by L. nobilis. In fact allelic variation exhibited by L. azorica is nested within that of L. nobilis from the Iberian peninsula and it appears that Laurus in Madeira and the Canary Islands may have been the result of two recent independent colonisations from Iberia. Although there is no means of calibrating divergence times from the dendrogram in figure 2, the genetic patterning is indicative of the Macaronesian Laurus being recently derived from L. nobilis. ARROYO–GARCÍA et al. (2001) suggest that laurel in the Canary Islands is more likely to be the result of a recent range expansion from the continent, and although the evidence is indirect, it is more consistent with H2. Calathus The genus Calathus (Coleoptera) is represented by 24 species in the Canary Islands. Most species are in the monteverde, which is composed of laurel forest and fayal–brezal (the vegetation occurring above and around the laurel forest proper), and a few are found in pine forest. Several species are

Emerson

Laurus nobilis continental

Laurus azorica Madeira Laurus azorica Canary Islands

Laurus nobilis continental

Persea indica Apollonias barbujana

Fig. 2. Dendrogram constructed from AFLP data for genotypes of Laurus nobilis (black bars) and L. azorica (gray bars). Modified from ARROYO–GARCÍA et al. (2001). Fig. 2. Dendrograma construido a partir de los datos AFLP para genotipos de Laurus nobilis (barras negras) y de L. azorica (barras grises). Modificado de ARROYO–GARCÍA et al. (2001).

found below these montane forest environments in the lowland thermophilous forest (now open areas due to deforestation). Three species occur on the island of Gran Canaria, two occurring in the laurel forest (C. canariensis and C. appendiculatus) and one occurring outside the laurel forest (C. angularis). Recent phylogenetic analyses by EMERSON et al. (1999, 2000a), using mitochondrial DNA (mtDNA) cytochrome oxidase I and II genes (COI and COII), have identified these three species as monophyletic. Studies by DESALLE et al. (1987) and BROWER (1994) have shown that mtDNA in arthropods evolves at a rate of 2 and 2.3% per My respectively. EMERSON et al. (1999) have applied an average of these, 2.15% per My, leading them to conclude that the observed mtDNA diversity among the species dates back only some 750,000 years (yr). Although it can not be ascertained with any certainty when the island of Gran Canaria was

colonised, the phylogenetic relationships of the three species lend support to H2.

Nesotes The genus Nesotes (Coleoptera) is represented on the Canary Islands by 19 species and 2 subspecies, but recent molecular phylogenetic analyses indicate that alpha taxonomy underestimates the real number of species (REES et al., 2001a, 2001b). There are five species on the island of Gran Canaria inhabiting a range of niches, including xeric coastal areas (N. lindbergi and N. fusculus), open areas and pine forests (N. quadratus and N. piliger) and laurel forest (N. conformis). The molecular phylogenetic analyses of REES et al. (2001a, 2001b), using mtDNA COII gene sequences, have identified the Gran Canarian species to be a monophyletic group resulting from a

Animal Biodiversity and Conservation 26.1 (2003)

conformis

conformis quadratus conformis conformis

conformis 96 76 lindbergi lindbergi quadratus conformis conformis conformis conformis conformis

conformis piliger piliger 97 quadratus quadratus piliger quadratus 73

fusculus fusculus fusculus quadratus 94 quadratus quadratus 90 quadratus quadratus quadratus 70 quadratus 76 quadratus quadratus 82 95 quadratus quadratus quadratus congestus–EH 78

aethiops–FV 0.005

0.003

0.001 0

Fig. 3. Neighbour joining tree of maximum likelihood distances for N. conformis, N. quadratus, N. piliger, N. lindbergi and N. fusculus using mtDNA sequence data. Bootstrap values are indicated for nodes gaining more than 70% support (1,000 reps). Nesotes conformis lineages are shown in gray. Age estimates for nodes A and B are discussed in the text. Modified from REES et al. (2001b). Fig. 3. Árbol por agrupación de vecinos de distancias máximas de verosimilitud para N. conformis, N. quadratus, N. piliger, N. lindbergi y N. fusculus, utilizando la secuenciación de ADNmt. Los valores iniciales de ceba (valores "bootstrap") se indican para los nodos que cuentan con un apoyo de más del 70% (1.000 reps). Los linajes de Nesotes conformis se indican en gris. Las estimaciones de edad para los nodos A y B se discuten en el texto. Modificado de REES et al. (2001b).

single colonisation event. Their conclusion is that this group is the result of a recent diversification of a widespread N. quadratus type ancestor, typical of open areas, followed by morphological adaptation to laurel, pine and coastal environments. The maximum genetic distance

(maximum likelihood) within the Gran Canarian clade is 7.1% (Tamura Nei model with invariant sites and gamma shape parameter). For the purposes of this paper it is useful to apply the 2.15% per My rate estimate for arthropods (DESALLE et al., 1987; BROWER, 1994) to test sup-

Emerson

remaining Gran Canarian species has a maximum genetic divergence of 4.7 % (Emerson et al., unpublished data). Applying the 2.15% per My rate for arthropod mtDNA evolution suggests an age estimate of 2.2 My for the MRCA of the three remaining species. Although it can not be ascertained when the island of Gran Canaria was colonised, the recent diversification of the three species lends support to H2.

port for each of the two hypotheses. Ideally one would like to use specific rate estimates for each group of species analysed, for the particular mitochondrial gene analysed. In the absence of such specific rate estimates the general rate estimate of 2.15% per My is used with the caveat that individual groups analysed are likely to have specific rate estimates that vary around the general rate estimate, and should thus be viewed with caution. The 7.1% maximum divergence of the Gran Canarian Nesotes gives an estimated age of 3.3 My for the most recent common ancestor (MRCA) of this group. To estimate the approximate ages of laurel forest lineages from the tree in figure 3, the tree has been calibrated with the 3.3 My age estimate for the MRCA, and the non parametric rate smoothing (NPRS) method of SANDERSON (1997) has been applied (see EMERSON et al., 2000b). This method smoothes local transformations in rate as rate changes over the tree. Essentially this method replaces the constraint of a constant rate across a tree with a much weaker constraint on how rates vary, but one that is still sufficient to allow the estimation of divergence times. This generates maximum age estimates of 1 My and 0.9 My for nodes A and B on figure 3, indicating that the laurel forest of Gran Canaria has only recently been colonised by Nesotes, and supporting H2.

Oribatid mites of the genus Steganacarus are macrophytophages requiring forest soils rich in organic substances (RAJISKI, 1967). The genus comprises approximately 50 species, with three endemic to the Canary Islands, two of which occur on Gran Canaria. Steganacarus guanarteme is endemic to Gran Canaria, while S. carlosi is also found on the islands of Tenerife and La Gomera. A molecular phylogenetic analysis using mtDNA COI gene sequences (SALOMONE et al., 2002) has identified S. guanarteme and S. carlosi from Gran Canaria to be monophyletic. Although it can not be concluded when Gran Canaria was colonised, applying the 2.15% per My rate for arthropod mtDNA evolution suggests an age estimate of 1.6 My for the MRCA, supporting a post–Roque Nublo origin.

Tarphius

Pinus canariensis

The genus Tarphius (Coleoptera) is represented by 29 species on five of the Canary Islands. The Tarphius are hygrophilic fungivorous beetles, intimately associated with the monteverde forest, with some species also occurring in the pine forests, and a few species in other mesic environments (e.g T. supranubius in subalpine Adenocarpus viscosus shrubs). Four species occur on Gran Canaria; T. moyanus is known only from the laurel forest, T. huggerti is known only from areas of monteverde that have now been deforested, T. piniphilus occurs in the pine forest of Tamadaba, and T. canariensis occurs in the laurel forest. Of the four, the first three are restricted to Gran Canaria but T. canariensis also occurs on Tenerife, and La Palma. Recent molecular phylogenetic analyses of the Tarphius using mtDNA COI and COII gene sequence data (EMERSON et al., 2000c and unpublished data) have identified that the four species of Gran Canaria are the result of two independent colonisation events, one involving T. canariensis and the other giving rise to the other three species. Using a combination of the phylogeographic pattern for T. canariensis, geological data, the biogeography of the remaining species and estimated divergence times, EMERSON et al. (2000c) have estimated that the genetic diversity present within Gran Canarian T. canariensis dates back 1.8 My, and the maximum age for the colonisation of Gran Canaria by T. canariensis is, at the most, 2.4 My suggesting a post–Roque Nublo origin. The clade of the three

Pinus canariensis is endemic to the central (Gran Canaria, Tenerife) and western (La Palma, El Hierro and La Gomera) Canary Islands, where it comprises one of the two dominant forest types in the archipelago. Distinctive features of the species are the thick bark, underlain by epicormic buds, and the capacity for basal resprouting; adaptations that enable this pine to survive the moderately intense fires associated with the ongoing volcanic activity of the islands (KEELY & ZEDLER, 1998). A recent molecular phylogenetic assessment of Eurasian pines (WANG et al., 1999) using sequence data from 4 chloroplast genes (rbcL, matK, trnV intron, and rp120–rp18 spacer) identifies P. canariensis to belong to clade of six closely related species including P. heldreichii, P. pinea, P. pinaster, P. brutia and P. halepensis. Within the Pinaceae several conflicting attempts have been made to calibrate from the fossil record. WANG et al. (2000) have used a 140 My age for the split of the genus Pinus from the other Pinaceae to calibrate their phylogeny of the Pinaceae. However the same estimate derived from MILLER (1988) has also been used by SAVARD et al. (1994) to date the origin of the Pinaceae itself. KUTIL & WILLIAMS (2001) suggest the genus Pinus probably emerged within the Pinaceae during the Jurassic period approximately 195 million years ago, but there is no fossil evidence supporting this conjecture. The earliest known pine from the fossil record, P. belgica (ALVIN, 1960) dates back to the Early

Steganacarus

Animal Biodiversity and Conservation 26.1 (2003)

Cretaceous approximately 130 Mya, and I use this as a conservative calibration for the origin of the genus Pinus for dating divergence times within the genus. Using sequence data for rbcL and matK from WANG et al. (1999) maximum likelihood distances were calculated using PAUP* v.4.0b10 with parameters obtained from Modeltest v.3.06 (POSADA & CRANDALL, 1998). The Modeltest program tests the fit of 56 models of DNA sequence evolution using likelihood values obtained from PAUP* for each of the models (SWOFFORD, 1998). Genetic divergences between P. canariensis and two non–Pinus members of the Pinaceae, Picea abies and Pseudotsuga menziesii are 4.540% and 4.291% respectively. Using the average of these (4.415%) and calibrating with the 130 My fossil record for P. belgica gives an estimated absolute nucleotide substitution rate of 0.034% per My. Genetic divergence between P. canariensis and the continental species P. pinaster is 0.085%, and applying the divergence rate of 0.034% per My generates an estimated divergence time of 2.5 Mya between P. canariensis and P. pinaster. A genetic divergence of 0.17% between P. canariensis and P. pinea generates an estimated divergence time between these two lineages of 5 Mya. Although these age estimates indicate nothing specifically about P. canariensis on Gran Canaria, they do suggest the P. canariensis forest ecosystem is rather young (2.5–5 My) compared with the geological age of the archipelago.

Brachyderes The genus Brachyderes (Coleoptera) is found predominantly in the Iberian peninsula and North Africa, with some species extending their ranges into France and northern Italy. The genus is also represented on four of the seven Canary Islands, and current taxonomy describes these as four subspecies of B. rugatus (PALM, 1976), although previous treatments have described the four as distinct species (LINDBERG & LINDBERG, 1958). Brachyderes rugatus is primarily associated with Pinus canariensis and its distribution is broadly correlated with the range of P. canariensis. A recent molecular phylogenetic analysis of the Canary Island Brachyderes using mtDNA COII gene sequence data (EMERSON et al., 2000b) has been able to use a combination of phylogeographic pattern and the geological ages of islands to estimate the ages of origin of each subspecies on each island, indicating that Gran Canaria was colonised by the ancestor of B. r. calvus at least 2.6 Mya. Brachyderes rugatus, along with eight other species, belongs to the subgenus Brachyderes, and limited sampling of the eight continental congenerics suggests the colonisation of Gran Canaria could be much older than 2.6 My. Sequence data for three of these other species, B. pubescens, B. grisescens (EMERSON et al., 2000b), and B. incanus (Emerson, unpublished data) indicate a deep divergence of

the B. rugatus lineage. Using the minimum genetic distance (maximum likelihood with parameters determined by Modeltest) between B. rugatus and the continental species (32%), and applying the 2.15% per My rate for arthropod mtDNA evolution, suggests a conservative age estimate of 15 My for the MRCA of B. rugatus and the continental species. However, it is inappropriate to draw such conclusions with less than 40% of the continental species having been sequenced (EMERSON, 2002). It is interesting that the minimum age estimate of 2.6 My for the colonisation of Gran Canaria by Brachyderes (EMERSON et al., 2000b) is surprisingly similar to the 2.5 My minimum age estimate for the divergence of P. canariensis from continental Pinus species (see above). The phylogeographic pattern for B. r. calvus on Gran Canaria suggests the contemporary population is the result of a much more recent expansion out of a geographically restricted area in the region of Juncal (fig. 4). Although it can not be ascertained when the island of Gran Canaria was colonised, the phylogeographic pattern for B. r. calvus, and the recent age estimate for its host plant, P. canariensis lend support to H2. Non–forest flora and fauna It could be argued that measures of genetic diversity observed within the laurel and pine forest ecosystems of Gran Canaria may be typical for the flora and fauna of Gran Canaria as a whole. A number of recent molecular phylogenetic analyses of Gran Canarian taxa occurring exclusively outside the forest ecosystems provide a comparative assessment of the genetic diversities of the forest and non–forest ecosystems.

Pimelia The genus Pimelia (Coleoptera) has 14 taxa described in the Canary Islands, with all endemic to single islands with the exception of one species that occurs on two islands. Five taxa occur on the island of Gran Canaria, three are strictly coastal ( P. estevezi , P. granulicollis , P. sparsa albohumeralis), one occurs in dry lowland environments (P. sparsa serrimargo), and the fifth inhabits dry high altitude environments (P. sparsa sparsa). A molecular phylogenetic analysis using mtDNA COI gene sequence data has identified these five taxa and P. fernandezlopezi from La Gomera to be monophyletic, indicating the five Gran Canarian taxa resulted from within island diversification following a single colonisation event (JUAN et al., 1995). Using the maximum genetic distance (maximum likelihood with parameters determined by Modeltest) between Gran Canarian species (19.6%), and applying the 2.15% per My rate for arthropod mtDNA evolution, suggests an age estimate of 9 My for the MRCA of the Gran Canarian taxa. This age estimate indicates

Emerson

Fig. 4. Phylogeography of Brachyderes rugatus calvus haplotypes on Gran Canaria. Branch lengths are not proportional to maximum likelihood branch lengths which are given in the top left inset. Modified from EMERSON et al. (2000b). Fig. 4. Filogeografía de los haplotipos de Brachyderes rugatus calvus de Gran Canaria. Las longitudes de las ramas no son proporcionales a las longitudes de las ramas de máxima probabilidad, que se indican en el recuadro izquierdo superior. Modificado de EMERSON et al. (2000b).

that the genus Pimelia was established on Gran Canaria prior to the Roque Nublo eruptive period. Further to this the genetic distance of 8.15% between the high altitude species P. sparsa sparsa and the closely related P. sparsa serrimargo suggests an age estimate of 3.8 Mya for the divergence of these two species, close to the end of the Roque Nublo eruptive period.

Hegeter The genus Hegeter (Coleoptera) is endemic to Macaronesia with 23 species, 21 of which occur exclusively on the Canary Islands. Most species are xerophilic and present at low altitudes, but some are present in the high altitude volcanic zones (JUAN et al., 1996). A molecular phylogenetic analysis of

100 97 B 100

A 100

T. b. boettgeri T. b. boettgeri 100

T. b. hierrensis T. b. hierrensis T. b. bischof fi bischoffi

T T.. b. boettgeri

Fig. 5. A neighbour joining tree of phylogenetic relationships among species of Tarentola from Gran Canaria, El Hierro and the Selvages, with bootstrap values (1,000 reps). Age estimates for nodes A and B are discussed in the text. Modified from CARRANZA et al. (2000). Fig. 5. Árbol por agrupación de vecinos de relaciones filogenéticas entre varias especies de Tarentola de Gran Canaria, El Hierro y las Islas Selvagens, con valores iniciales de ceba (valores "bootstrap", 1.000 reps.). Las estimaciones de edad para los nodos A y B se discuten en el texto. Modificado de CARRANZA et al. (2000).

Animal Biodiversity and Conservation 26.1 (2003)

Table 1. Estimated ages in millions of years (My) for Gran Canarian taxa analysed in this study, and their correspondence to the Roque–Nublo eruptive period occurring from 5.5–3.0 million years ago: Ae. Age estimate; PstRN. Post–Roque Nublo; RN. Roque–Nublo; PreRN. Pre-Roque Nublo. Tabla 1. Estimaciones de edades expresadas en millones de años (My) para los taxones de la isla de Gran Canaria analizada en este estudio, y su correspondencia con el ciclo eruptivo de Roque-Nublo que tuvo lugar hace 5,5–3,0 millones de años: Ae. Edad estimada; PstRN. Posterior a Roque Nublo; RN. Roque Nublo; PreRN. Previo a Roque Nublo.

Environments / taxa

PstRN

PreRN

Pine and laurel forest not calibrated

Calathus

0.75 My

Nesotes

1 My

Tarphius

2.4 My

Laurus azorica

Steganacarus Pinus canariensis Brachyderes

1.6 My

2.5–5 My

2.6 My

Non–forest

Pimelia

9 My

Hegeter

10.9 My

Tarentola

5.3–6.7 My

Chalcides

4.8–5.6 My

the Canary Island Hegeter using mtDNA COI gene sequence data included five of the six species from Gran Canaria. Although lacking bootstrap support, monophyly for the Gran Canarian species is favoured. Using the maximum genetic distance (maximum likelihood with parameters determined by Modeltest) between Gran Canarian species (23.5%), and applying the 2.15% per My rate for arthropod mtDNA evolution, suggests an age estimate of 10.9 My for the MRCA of the Gran Canarian taxa. Similarly to the result for the Pimelia, this age estimate indicates that the genus Hegeter was established on Gran Canaria prior to the Roque Nublo eruptive period. Although two of the five species can be found in mountainous, deforested areas, they are not restricted to this habitat and also occur in xerophilous low or medium altitude habitats (JUAN et al., 1996). The species not included in the study of JUAN et al. (1996), H. abbreviatus, is recorded as only occurring in humid forest environments (JUAN et al., 1996), and it would be interesting with regard the hypotheses being tested here to know the phylogenetic placement, and approximate divergence time of this species.

Tarentola The gekkonid genus Tarentola comprises around 22 species that occur in North Africa, the coastal

districts of the Mediterranean sea and Macaronesia, with an isolated species in Cuba and the Bahamas, and a further recently described species in Jamaica that is probably extinct. A single species of Tarentola, T. boettgeri boettgeri occurs on the island of Gran Canaria, and typical of species within this genus it is found in dry, non–forest environments, from sea level to altitudes of 1500 m (BARBADILLO et al., 1999). Several recent molecular phylogenetic analyses of the Tarentola using mtDNA 12S and cytb sequence data, and sequence data from the nuclear c–mos gene (CARRANZA et al., 2000, 2002) have helped to clarify the origins of the Macaronesian taxa. Within the Macaronesian islands DNA sequence diversity within T. b. boettgeri on Gran Canaria clearly indicates an origin by a single colonisation event, with T. b. hierrensis from El Hierro, and T. b. bischoffi from the Selvages being included within this clade (fig. 5). Using sequence data for the mtDNA cytb gene, the greatest genetic distance among Gran Canarian haplotypes (maximum likelihood with parameters determined by Modeltest) is 16.8%. CARRANZA et al. (2000) conclude that T. b. hierrensis from El Hierro is the result of a colonisation from the Selvages involving the ancestor of T. b. bischoffi. Assuming El Hierro was colonised not long after its appearance, node A in figure 5 provides a maximum age estimate for this event,

Emerson

allowing for unsampled or extinct lineages from the Selvages (see EMERSON et al., 2000b, EMERSON, 2002). Calibrating this node with the estimated 1.1 My age of El Hierro (GUILLOU et al., 1996) generates a cytb divergence rate estimate of 2.5% per My for Tarentola. Applying this rate to the observed 16.8% divergence within Gran Canarian T. b. boettgeri generates an age estimate of 6.7 My for the MRCA of this species. This compares well with an estimate of 5.3–6.7 My for the MRCA of T. b. boettgeri generated by CARRANZA et al. (2002). Both of these age estimates suggest that T. b. boettgeri was established on Gran Canaria prior to the Roque Nublo eruptive period.

Chalcides The skink genus, Chalcides, contains at least 19 species, with the majority occurring in Morocco, and three endemic species in the Canary Islands. A single species, C. sexlineatus, occurs on the island of Gran Canaria, occurring in dry and mesic open areas from the coast to elevations over 1,000 m. The monophyly of C. sexlineatus has been verified by a molecular phylogenetic analysis using mtDNA sequence data from 12S RNA, 16S RNA, and cytb (BROWN & PESTANO, 1998), revealing substantial within island genetic diversity of C. sexlineatus. A follow–up study using only 12S RNA sequence data (PESTANO & BROWN, 1999) sampled C. sexlineatus more intensively and identified three deep mitochondrial lineages within the island. The authors suggest that C. sexlineatus may have survived through the Roque Nublo eruptive period with a restricted distribution in the south–east of the island. Genetic distance estimates (maximum likelihood with parameters determined by Modeltest) for taxa spanning the root of the tree for C. sexlineatus are typically between 6–7% (with a maximum value of 12.6%). Although it is understood that 12S rRNA evolves at a slower rate than many protein coding mtDNA genes, rate estimates within the reptiles are lacking. However a recent study of grass lizards (Takydromus), LIN et al. (2002) have estimated a divergence rate of 1.25% per My for the 12srRNA gene. Applying this rate to genetic divergence estimates within C. sexlineatus generates an approximate age of 4.8–5.6 My for the MRCA (with a maximum estimate of 10.1 My), suggesting C. sexlineatus was already established on Gran Canaria in the early part of the Roque Nublo eruptive period.

Conclusion The violent eruptions on the island of Gran Canaria that formed the Roque Nublo agglomerate complex, 5.5–3 Mya, were very explosive (P ÉREZ– TORRADO et al., 1995), leading to the speculation that they would have led to massive extinction within the island, with species survival being limited

to the coastal environment (ARAÑA & CARRACEDO, 1980; MARRERO & FRANCISCO–ORTEGA, 2001). The implication from this is that the higher altitude laurel forest and pine wood environments must have been re–established following the dramatic volcanic period. An assessment of recent molecular phylogenetic analyses for plant and animal groups associated with these forest ecosystems finds general support for the hypothesis that the forest environments of Gran Canaria post–date the Roque Nublo eruptive period (table 1). No definitive evidence exists for these species groups predating the end of the Roque Nublo eruptive period (3 My). Four species groups occurring exclusively outside the forest ecosystems have also been analysed. Three of these provide evidence for an origin predating the Roque Nublo eruptive period, and the fourth, Chalcides, may have an origin at the beginning of the Roque Nublo eruptive period. These results are compatible with a general prediction, based on the volcanic history of the island, that biodiversity on Gran Canaria, as measured by genetic diversity, is lower within the laurel forest and pine wood ecosystems compared to that of non–forest ecosystems. It will be interesting to see whether future molecular phylogenetic analyses of other species groups on the island of Gran Canaria add further support to the findings of this paper.

Acknowledgements I am grateful to Pedro Oromí and three anonymous referees whose comments greatly improved the manuscript.

References

AIZPURU, I., 2000. Lista Roja de Flora Vascular Española. Unidad de Botánica, Dept. de Biologia, Univ. Autónoma de Madrid, Madrid, Spain. ALVIN, K. L., 1960. Further conifers of the Pinaceae from the Wealden Formation of Belgium. Mem. Inst. Roy. Sci. Nat. Belgique, 146: 1–39. A NDERSSON , L., & R OVA , J. H. E., 1999. The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Syst. Evol., 214: 161–186. ARAÑA, V., & CARRACEDO, J. C., 1980. Canarian Volcanoes, III. Gran Canaria. Rueda, Madrid. A RROYO –G ARCÍA , R., MARTÍNEZ –Z APATER, J. M.., FERNÁNDEZ PRIETO, J. A., & ÁLVAREZ–ARBESÚ, R., 2001. AFLP evaluation of genetic similarity among laurel populations (Laurus L.). Euphytica, 122: 155–164. BARBADILLO, L .J., LACOMBA, J. I., PÉRE–MELLADO, V., SANCHO, V., & LOPEZ–JURADO, L. F., 1999. Anfibios y reptiles de la Península Ibérica, Baleares y Canarias. Ed. Planeta S. A., Barcelona. BARBERO, M., BENABID, A., PEYRE, C., & QUÉZAL, P.,

Animal Biodiversity and Conservation 26.1 (2003)

1981. Sur la presence au Maroc de Laurus azorica (Seub.) Franco. Anales Jardín Botánico de Madrid, 37: 467–472. BRAMWELL, D., 1972. Endemism in the flora of the Canary Islands. In: Taxonomy, Phytogeography and Evolution: 141–159 (D. H. Valentine, Ed.). Academic Press, London. – 1976. The endemic flora of the Canary Islands; distribution, relationships and phytogeography. In: Biogeography and Ecology in the Canary Islands: 207–240 (G. Kunkel, Ed). Dr. W. Junk, The Hague. BREMER, B., 1996. Phylogenetic studies within Rubiaceae and relationships to other families based on molecular data. Opera Botanica Belgica, 7: 33–50. BROWER, A. V. Z., 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA, 91: 6,491–6,495. BROWN, R. P., & PESTANO, J., 1998. Phylogeography of skinks (Chalcides) in the Canary Islands inferred from mitochondrial sequences. Mol. Ecol., 7: 1,183–1,191. CARRANZA, S., ARNOLD, E. N., MATEO, J. A., & GENIEZ, P., 2002. Relationships and evolution of the North African geckos, Geckonia and Tarentola (Reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Mol. Phylogenet. Evol. (in press). CARRANZA, S., ARNOLD, E. N., MATEO, J. A., & LÓPEZ– JURADO, L. F., 2000. Long–distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: gekkonidae), revealed by mitochondrial DNA sequences. Proc. R. Soc. Lond. B, 267: 637–649. CIFERRI , R., 1962. La Laurisilva Canaria: Una paleoflora vivente. Ricercha Scient., 32: 111–134. CRONK, Q. C. B., 1992. Relict floras of Atlantic Islands: patterns assessed. Biol, J. Linn. Soc., 46: 91–103. DESALLE, R., FREEDMAN, T., PRAGER, E. M., & WILSON, A. C., 1987. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J. Mol. Evol., 26: 157–164. EMERSON, B. C., 2002. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol. Ecol., 11: 951–966. EMERSON, B. C., OROMÍ, P., & HEWITT, G. M., 1999. MtDNA phylogeography and recent intra–island diversification of Canary Island Calathus beetles (Carabidae). Mol. Phylogenet. Evol., 13: 149–158. – 2000a. Interpreting colonisation of the Calathus (Coleoptera: Carabidae) on the Canary Islands and Madeira through the application of the parametric bootstrap. Evolution, 54: 2,081–2,090. – 2000b. Colonisation and diversification of the species Brachyderes rugatus (Coleoptera) on the Canary Islands: evidence from mtDNA COII gene sequences. Evolution, 54: 911–923.

– 2000c. Tracking colonisation and diversification of insect lineages on islands: MtDNA phylogeography of Tarphius canariensis (Coleoptera: Colydiidae) on the Canary Islands. Proc. R. Soc. Lond. B, 267: 2,199–2,205. E NGLER, A., 1879 Versuch einer Entwickllungsgeschichte, insbesondere der Florengebiete seit der Tertiärperiode. I. Die extratropischen Gebiete der nördlichen Hemisphäre. Leipzig, W. Engelmann. FRANCISCO–ORTEGA, J., PARK, S–J., SANTOS–GUERRA, A., BENABID, A., & JANSEN, R. K., 2001. Origin and evolution of the endemic Macaronesian Inuleae (Asteraceae): evidence from the internal transcribed spacers of nuclear ribosomal DNA. Biol. J. Linn. Soc., 72: 77–97. GUILLOU, H., CARRACEDO, J. C., PÉREZ TORRADO, F., & RODRÍGUEZ BADIOLA, E., 1996. K–Ar ages and magnetic stratigraphy of a hotspot–induced, fast grown oceanic island: El Hierro, Canary Islands. J. Volcanol. Geotherm. Res., 73: 141–155. HOERNLE, K., TILTON, G., & SCHMINKE, H. U., 1991. Sr–Nd–Pb isotopic evolution of Gran Canaria: evidence for shallow enriched mantle beneath the Canary Islands. Earth Planet. Sci. Lett., 106: 44–63. HUMPHRIES, C. J., 1976. Evolution and endemism in Argyranthemum Webb ex Schultz Bip. (Compositae: Anthemideae). Bot. Macar., 1: 25–50. JUAN, C., EMERSON, B. C., OROMÍ, P., & HEWITT, G. M., 2000. Colonisation and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends Ecol. Evol., 15: 104–109. JUAN, C., OROMÍ, P., & HEWITT, G. M., 1995. Mitochondrial DNA phylogeny and sequential colonization of Canary Islands by darkling beetles of the genus Pimelia (Tenebrionidae), Proc. R. Soc. London Ser. B, 261: 173–180. – 1996. Phylogeny of the genus Hegeter (Tenebrionidae, Coleoptera) and its colonization of the Canary Islands deduced from Cytochrome Oxidase I mitochondrial DNA sequences. Heredity, 76: 392–403. KEELY, J. & ZEDLER, P., 1998. Evolution and life histories in Pinus. In: Ecology and Biogeography of Pinus: 219–250 (D. M. Richardson, Ed.). Cambridge University Press, Cambridge, U. K. KUTIL, B. L., & WILLIAMS, C. G., 2001. Triplet–repeat microsatellites shared among hard and soft pines. J. Hered., 92: 327–332. LEMS, K., 1960. Botanical notes on the Canary Islands. 2. The evolution of plant forms in the Islands: Aeonium. Ecology, 41: 1–17. LIN, S–M., CHEN, C. A., & LUE, K–Y., 2002. Molecular phylogeny and biogeography of the grass lizards genus Takydromus (Reptilia: Lacertidae) of East Asia. Mol. Phylogenet. Evol., 22: 276–288. LINDBERG, H., & LINDBERG, H., 1958. Coleoptera Insularum Canariensium. I. Aglycyderidae und Curculionidae. Comm. Biol., 30: 278–287. MACHADO, A., 1976. Introduction to a faunal study of the Canary Islands’ Laurisilva, with special

reference to the ground–beetles (Coleoptera, Caraboidea). In: Biogeography and Ecology in the Canary Islands: 347–411 (G. Kunkel, Ed.). Dr. W. Junk, The Hague. M ARRERO , A., & F RANCISCO –O RTEGA , J., 2001. Evolución en islas: la metáfora especio–tiempo– forma. In: Naturaleza de las Islas Canarias: ecología y conservación: 133–140 (J. M. Fernández–Palacios & Martín–Esquivel, Eds.). Turquesa, Santa Cruz de Tenerife. M EUSEL , H., 1965. Die reliktvegetation der kanarischen Inseln in ihren Beziehungen zur süd– und mitteleuropäischen Flora. In: Gesammelte Vorträge über moderne Probleme der Abstammungslehre, 1: 117–136 (M. Gersch, Ed.). Friedrich–Schiller–Universität. – 1988. The origin of modern conifer families. In Origin and Evolution of Gymnosperms: 448– 487 (C. B. Beck, Ed.). Colombia University Press, New York. PALM, T., 1976. Zur kenntnis der käferfauna der Kanarischen Inseln, 20. Die Gattung Brachyderes Schönherr (Coleoptera: Curculionidae). Ent. Scand., 7: 309–311. PÉREZ–TORRADO, F. J., CARRACEDO, J. C., & MANGAS, J., 1995. Geochronology and stratigraphy of the Roque Nublo cycle, Gran Canaria, Canary Islands. J. Geol. Soc. Lond., 152: 807–818. PÉREZ DE PAZ, P. L., SALAS, M., RODRÍGUEZ, O., ACEBES, J. R., DEL ARCO AGUILAR, M. J., & WILPREDT, W., 1994. Atlas cartográfico de los pinares canarios: IV. Gran Canaria y plantaciones de Fuerteventura y Lanzarote. Viceconsejería de Medio Ambiente, Gobierno de Canarias, Santa Cruz de Tenerife, Spain. PESTANO, J., & BROWN, R. P., 1999. Geographical structuring of mitochondrial DNA in Chalcies sexlineatus within the island of Gran Canaria. Proc. R. Soc. Lond. B., 266: 805–812. POSADA, D., & CRANDALL, K. A., 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14: 817–818. RAJISKI, A., 1967. Autoecological–zoogeographical analysis of moss mites (Acari Oribatei) on the basis of fauna in the Poznan environs. Part 1. Polskie Pismo Entomologiezne, 37: 69–166. RAY, M. F., 1995. Systematic of Lavatera and Malva (Malvaceae, Malvae) —a new perspective. Plant Syst. Evol., 198: 29–53. REES, D. J., EMERSON, B. C., OROMÍ, P. & HEWITT, G. M., 2001a. Mitochondrial DNA phylogeography of the genus Nesotes (Coleoptera: Tenebrio-

Emerson

nidae) on the Canary Islands. Mol. Phylogenet. Evol., 21: 321–326. – 2001b. Morphology, ecology, and mtDNA: interpreting the phylogeography of the Nesotes (Coleoptera: Tenebrionidae) of Gran Canaria (Canary Islands). Mol. Ecol., 10: 427–434. SALOMONE, N., EMERSON, B. C, HEWITT, G. M. & BERNINI, F., 2002. Phylogenetic relationships among the Canary Island Steganacaridae (Acari, Oribatida) inferred from Mitochondrial DNA sequence data. Mol. Ecol., 11: 79–90. SANDERSON, M. J., 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol., 14: 1,218–1,231. SAVARD, L., LI, P., STRAUSS, S. H., CHASE, M. W., MICHAUD, M., & BOUSQUET, J., 1994. Chloroplast and nuclear gene sequences indicate Late Pennsylvanian time for the last common ancestor of extant seeded plants. Proc. Natl. Acad. Sci. USA, 91: 5,163–5,167. SNEATH, P. H. A., & SOKAL, R. R., 1973. The principles and practice of numerical classification. W. H. Freeman, San Francisco. SUNDING, P., 1979. Origins of the Macaronesian fauna. In: Plants and islands : 13–40 (D. Bramwell, Ed.). Academic Press, London. SWOFFORD, D., 1998. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachussetts. TAKHTAJAN, A., 1969. Flowering plants: origin and dispersal. Smithsonian Institution Press, Washington, D.C. THIV, M., STRUWE, L., KADEREIT, .J. W., 1999. The phylogenetic relationships and evolution of the Canarian laurel forest endemic Ixanthus viscosus (Aiton) Griseb. (Gentianaceae): evidence from matK and ITS sequences, and floral morphology and anatomy. Plant Syst. Evol., 218: 299–317. W ANG , X–Q, T ANK , D. C., & S ANG , T., 2000. Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol. Biol. Evol., 17: 773–781. WANG, X–R, TSUMURA, Y., YOSHIMARU, H., NAGASAKA, K., & SZMIDT, A. E., 1999. Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, matK, rp120–rps18 spacer, and trnV intron sequences. Am. J. Bot., 86: 1,742–1,753. WULFF, E. V., 1943 An introduction to historical plant geography. Chronica Botanica, Waltham.

Animal Biodiversity and Conservation 26.1 (2003)

Two new species of the genus Laemostenus (Pristonychus) Bonelli from Bulgaria and notes on L. (P.) euxinicus Nitzu (Coleoptera, Carabidae) B. Guéorguiev

Guéorguiev, B., 2003. Two new species of the genus Laemostenus (Pristonychus) Bonelli from Bulgaria and notes on L. (P.) euxinicus Nitzu (Coleoptera, Carabidae). Animal Biodiversity and Conservation, 26.1: 21–29. Abstract Two new species of Laemostenus (Pristonychus) Bonelli from Bulgaria and notes on L. (P.) euxinicus Nitzu (Coleoptera, Carabidae).— Two new species of subgenus Pristonychus Dejean, 1828, of the genus Laemostenus Bonelli, 1810, are described and illustrated: L. stoevi n. sp. from northern Bulgaria and L. derventicus n. sp. from southeastern Bulgaria. Both new species are distinguished from the closely related L. euxinicus Nitzu, 1998, L. tichyi (Kult, 1946) and L. punctatus (Dejean, 1828). This work contributes to both the faunistics and taxonomy of L. euxinicus from Romania. The assumed adaptive trend and origin of the most modified characters of the two new species are discussed, and the systematic place, taxonomic status and formation of more divergent species of the “terricola” group are presented. Key words: Coleoptera, Carabidae, Laemostenus, L. stoevi n. sp., L. derventicus n. sp., Bulgaria. Resumen Dos nuevas especies del género Laemostenus (Pristonychus) Bonelli de Bulgaria y notas sobre L. (P.) euxinicus Nitzu (Coleoptera, Carabidae).— Se describen e ilustran dos nuevas especies del subgénero Pristonychus Dejean, 1828, del género Laemostenus Bonelli, 1810: L. stoevi sp. n. del norte de Bulgaria y L. derventicus sp. n. del sudeste de Bulgaria. Las dos nuevas especies se diferencian de las estrechamente relacionadas con ellas L. euxinicus Nitzu, 1998, L. tichyi (Kult, 1946) y L. punctatus (Dejean, 1828). Este trabajo es una contribución a la faunística y a la taxonomía de L. euxinicus de Bulgaria. Se discuten y asumen las tendencias adaptativas y el origen de la mayoría de caracteres modificados de las dos nuevas especies y se presentan la ubicación sistemática, el estatus taxonómico y la formación de especies más divergentes del grupo “terricola”. Palabras clave: Coleoptera, Carabidae, Laemostenus, L. stoevi sp. n., L. derventicus sp. n., Bulgaria. (Received: 6 IV 01; Conditional acceptance: 16 X 01; Final acceptance: 13 IX 02) Borsilav Guéorguiev, Natural Museum of Natural History, 1 blvd. Tzar Osvoboditel, 1000 Sofia, Bulgaria. E–mail: bobivg@yahoo.com

ISSN: 1578–665X

Guéorguiev

Introduction

Results

During a recent study of the specimens from the genus Laemostenus deposited in the collections of the National Museum of Natural History–Sofia (NMNHS), specimens belonging to two new species from two different regions of Bulgaria (fig. 1) were found. Their diagnostic characters and descriptions are given below. Further on, based on two male specimens from two new localities, a contribution to the taxonomy of L. euxinicus is given. Finally, the systematic position of the new taxa is discussed, as the presence of some apotypic external characters suggests an adaptive trend to live in subterranean habitats.

Laemostenus (Pristonychus) stoevi n. sp. (figs. 1–2, 6, 10, 14, 18, 20, 22)

Material and methods In the description of L. stoevi n. sp. comparative material of L. punctatus (Dejean, 1828) from the cave “Devetashka peshtera” was used, collected simultaneously with two females of the first taxon, as well as two males of L. euxinicus Nitzu, 1998 (see below). L. derventicus n. sp. was compared with the above–mentioned specimens of L. stoevi n. sp. and L. euxinicus, with some individuals of L. punctatus, collected from different regions in Bulgaria, and with few specimens of L. cimmerius (Fisher–Waldheim, 1823), found around the type locality of this new species. The sclerites and setae of the ovipositor are named after BALL & SHPELEY (1983). The data for the geological age of the various types of limestone are in accordance with POPOV (1970).

Type material Holotype: 1{, Bulgaria, Nikopol District, v. Muselievo, cave “Nanin kamik”, 12 X 1986, leg. P. Beron, U. T. M. grid co–ordinates LJ23 (preserved in coll. NMNH). Paratypes: 1{, 2} (original labels in Cyrillic) Bulgaria, Lovech District, cave “Vodnata peshtera”, 16 IV 1926, leg. N. Radev, U. T. M. grid co–ordinates LH 39 (a male and a female in coll. A. Casale, other female in coll. NMNHS); 2{, 1}, Bulgaria, Nikopol District, v. Muselievo, cave “Nanin kamik”, 12 VIII 1994, leg. P. Stoev & T. Ivanova, coll. NMNHS; 2}, Bulgaria, Lovech District, cave Devetashka 13 VIII 1994, leg. P. Stoev, U. T. M. grid co–ordinates LH 28, coll. NMNHS. Diagnostic features L. stoevi n. sp. differs from L. euxinicus, L. derventicus n. sp., and L. punctatus by shape of the male genitalia (figs. 2, 6, 10, 14). The median lobe in lateral view is that which curves most downwards (fig. 2), the right paramere has the roundest mid part and the most bent apex (fig. 10), and the left paramere is different (fig. 14) in comparison with males of the other three taxa. The new species differs from L. derventicus n. sp., L. punctatus and L. tychyi (genital characters unknown) in the protibia which has accessory pubescence on the anteriormargin distally (fig. 22). Further on, L. stoevi n. sp. can be distinguished from L.

Romania

"" "

! !! Black Sea

Bulgaria

• Turkey Greece Fig. 1. Map of Bulgaria and southern Romanian Dobrudja showing the distribution of: Laemostenus (Pristonychus) stoevi n. sp. (!); Laemostenus (Pristonychus) euxinicus Nitzu ("); Laemostenus (Pristonychus) derventicus n. sp. (•). Fig. 1. Mapa de Bulgaria y el sur de Rumanía (región de Dobrudja) que muestra la distribución de: Laemostenus (Pristonychus) stoevi sp. n. (!); Laemostenus (Pristonychus) euxinicus Nitzu ("); Laemostenus (Pristonychus) derventicus sp. n. (•).

Animal Biodiversity and Conservation 26.1 (2003)

1 mm

Figs. 2–5. Shape of lateral aspect of the median lobe of: 2. Laemostenus (Pristonychus) stoevi n. sp. holotype, cave “Nanin kamik”, v. Muselievo, Nikopol District, Bulgaria; 3. Laemostenus (Pristonychus) punctatus, cave “Devetashka peshtera”, v. Devetaki, Lovech District, Bulgaria; 4. Laemostenus (Pristonychus) euxinicus Nitzu, military bunker in Hagieni Forest, v. Albeshti, Mangalia District, Romanian Dobrudja; 5. Laemostenus (Pristonychus) derventicus n. sp., holotype, a small precipice near v. Krajnovo, Elhovo District, Bulgaria. Figs. 2–5. Configuración del aspecto lateral del lóbulo medio de: 2. Laemostenus (Pristonychus) stoevi sp. n. holotipo, cueva “Nanin kamik”, Muselievo, distrito de Nikopol, Bulgaria; 3. Laemostenus (Pristonychus) punctatus, cueva “Devetashka peshtera”, Devetaki, distrito de Lovech, Bulgaria; 4. Laemostenus (Pristonychus) euxinicus Nitzu, búnker militar en el bosque de Hagieni, Albeshti, distrito de Mangalia, Dobrudja rumana; 5. Laemostenus (Pristonychus) derventicus sp. n., holotipo, en un pequeño precipicio cerca de Krajnovo, distrito de Elhovo, Bulgaria.

derventicus n. sp. by the different ratio width of elytra / width of pronotum, and from L. punctatus in colour of the tegument, lack of denticles on the claws inside, and both shape of sternum eight in female (figs. 18–19) and stylus of the ovipositor (figs. 20–21). Etymology The new species is named after one of its collectors, the young specialist of Balkan Chilopoda and enthusiastic cave explorer (Pavel Stoev). Description Colour varied from piceous–ferrugineus to nearly black, without metallic lustre. Length 12.8– 19 mm (holotype 19 mm); width 4.7–6.8 mm (holotype 6.8 mm). Microsculpture on elytra isodiametric, absent on head and pronotum. Head smooth, antennae exceeding first quarter of elytra; eyes slightly prominent, shorter than temporae; frontal furrows very shallow; mentum with a bifide tooth. Pronotum cordate, 1.13– 1.24 times wider than long (mean 1.17, of holotype 1.24) and 1.34–1.43 times wider than

head with eyes (mean 1.39, of holotype 1.43), broadest in first third, with some punctures along lateral margins and at base; disc towards base with more or less conspicuous transversal microstirae; median furrow long and straight; anterior margin concave, anterior angles prominent, sub–acuminate; bead of lateral margins before anterior angles disappears; sides strongly sinuated towards, with somewhat projecting posterior angles; posterior margin almost straight and slightly curved towards posterior angles; bead of posterior margin interrupted in middle; base with a single fovea from each side. Legs are long and slender; posterior ventral margins of profemora with three or four setae, smooth (absent obvious tubercles); protibia with accessory pubescence on distal end of anterior margin; first three male protarsi with adhesive bristles ventrally; mesotibia slightly curved distally in males, and almost straight in females; mesotibiae and metatibiae inside distally with brush of hairs; first article of tarsus densely pubescent on all sides; onychium with four or five pairs of setae on ventral surface; claws smooth

Guéorguiev

1 mm Figs. 6–9. Shape of the dorsal aspect of the apex of the median lobe of: 6. Laemostenus (Pristonychus) stoevi n. sp., holotype; 7. Laemostenus (Pristonychus) punctatus; 8. Laemostenus (Pristonychus) euxinicus Nitzu; 9. Laemostenus (Pristonychus) derventicus n. sp., holotype. (For more information on locations of these species, see the legend of figs. 2–5.) Figs. 6–9. Visión dorsal del ápice del lóbulo medio de: 6. Laemostenus (Pristonychus) stoevi sp. n. holotipo; 7. Laemostenus (Pristonychus) punctatus; 8. Laemostenus (Pristonychus) euxinicus Nitzu; 9. Laemostenus (Pristonychus) derventicus sp. n., holotipo. (Para más información sobre las localizaciones de estas especies, ver el pie de las figs. 2–5.)

inside. Elytra dilated towards posterior half, 1.43– 1.59 times longer than broad mean 1.515, of holotype 1.51) and 1.41–1.53 times wider than pronotum (mean 1.49, of holotype 1.41); two elytron coalesced from scutellum to beginning of posterior half; angle of shoulder protruding, but absent clear denticle; both scutellar stria and

scutellar setiferous pore present, other striae delicately punctate, intervals flat; umbilicate marginal series of 21–23 pores; end of seventh stria with three apical pores. Apterous. Ventrum smooth; apophysis of prosternum indistinctly bordered; exterior margin of metaepisterna longer than anterior; last visible sternum with single mar-

1 mm Figs. 10–13. Shape of the right paramere of: 10. Laemostenus (Pristonychus) stoevi n. sp., holotype; 11. Laemostenus (Pristonychus) punctatus; 12. Laemostenus (Pristonychus) euxinicus Nitzu; 13. Laemostenus (Pristonychus) derventicus n. sp., holotype. (For more information on locations of these species, see the legend of figs. 2–5.) Figs. 10–13. Forma del parámero derecho de: 10. Laemostenus (Pristonychus) stoevi sp. n. holotipo; 11. Laemostenus (Pristonychus) punctatus; 12. Laemostenus (Pristonychus) euxinicus Nitzu; 13. Laemostenus (Pristonychus) derventicus sp. n., holotipo. (Para más información sobre las localizaciones de estas especies, ver el pie de las figs. 2–5.)

Animal Biodiversity and Conservation 26.1 (2003)

1 mm

Figs. 14–17. Shape of the left paramere of: 14. Laemostenus (Pristonychus) stoevi n. sp., holotype; 15. Laemostenus (Pristonychus) punctatus; 16. Laemostenus (Pristonychus) euxinicus Nitzu; 17. Laemostenus (Pristonychus) derventicus n. sp., holotype. (For more information on locations of these species, see the legend of figs. 2–5.) Figs. 14–17. Forma del parámero izquierdo de: 14. Laemostenus (Pristonychus) stoevi sp. n. holotipo; 15. Laemostenus (Pristonychus) punctatus; 16. Laemostenus (Pristonychus) euxinicus Nitzu; 17. Laemostenus (Pristonychus) derventicus sp. n., holotipo. (Para más información sobre las localizaciones de estas especies, ver el pie de las figs. 2–5.)

ginal pore in each side. Sternum eight of female sex with slightly slanting and hardly wavy distal border (fig. 18) whereas in female of L. punctatus same has well–expressed slanting and wavier distal border (fig. 19). Male genitalia are illustrated on figs. 2, 6, 10, 14. Apical stylomere of left stylus (fig. 20) having blade with dorsal side evidently concave, widened before rounded apex, one dorsal ensiform seta medially, two different in size dorsolateral ensiform setae (apical stylomere of left stylus, fig. 21, of female of L. punctatus from “Devetashka peshtera” has a blade with dorsal side slightly concave before pointed apex, one dorsal ensiform seta medially, and two dorsolateral ensiform setae different regarding size).

height, 102 m width and mote than 2000 m length) is located in the vicinity of Devetaki Village (Lovech District). The direct line between the two caves is 10 km, whereas the distance between them and the cave “Nanin kamik” is 42–44 km approximately. Perhaps the specimens from the two closer caves should be regarded as population of a single species, but not geographical race.

Distribution The “Nanin kamik” cave is 200 m long and it is buried in Sarmatic limestone. It lies on the right side of the Osam River at 100 m altitude and the nearest village is Muselievo (Nikopol District). The other two caves, “Vodnata peshtera” and "Devetashkata peshtera”, also lie on the right side of the Osam River at elevation of 250– 300 m in Early Cretaceous limestone. The first cave (25 m height, 60 m width, 450 m length) is situated between the villages of Chavdartsi and Alexandrovo (Lovech District). The second (57 m

Notes Part of the type series of L. stoevi n. sp. has been previously studied and published. The male specimen captured in the cave “Nanin kamik”, 12 X 1986, leg. P. Beron bears label: “ L. (Pristonychus) cimmerius weiratheri Müll. det. A. Casale 1988” and it was recorded by BERON (1994). One {, 2}, individuals collected from the cave “Vodnata peshtera” (original labels in Cyrillic) were identified as “L. (P.) terricola punctatus (Dej.) det. A. Casale 1994”.

Geographical affinities In the limits of the “terricola” species group, this strict troglophile beetle is sympatric and syntopic of L. punctatus, and is allopatric (e. g. isolated genetically from) of L. euxinicus, L. derventicus n. sp. and L. tychyi.

Guéorguiev

1 mm Figs. 18–19. Ventral line drawings of sternum eight of: 18. Laemostenus (Pristonychus) stoevi n. sp., female paratype; 19. Laemostenus (Pristonychus) punctatus, female. Both specimens from cave “Devetashka peshtera”, v. Devetaki, Lovech District, Bulgaria. Figs. 18–19. Dibujos de la línea ventral del esternón ocho de: 18. Laemostenus (Pristonychus) stoevi sp. n., paratipo, hembra; 19. Laemostenus (Pristonychus) punctatus, hembra. Ambos especímenes procedentes de cueva “Devetashka peshtera”, Devetaki, distrito de Lovech, Bulgaria.

Laemostenus (Pristonychus) derventicus n. sp. (figs. 1, 5, 9, 13, 17)

The { specimen from the same locality also has a second label: “Laemostenus terricola? det. V. Guéorguiev”. Two } specimens, collected from the cave “Devetashka”, 13 VIII 1994, leg. P. Stoev, bear labels: “L. (P.) terricola punctatus (Dej.) det. B. Guéorguiev 1994” and they were cited by BERON (1994).

Type material Holotype: 1{, small nameless pothole, 350– 400 m, v. Krajnovo (Elhovo District), U. T. M. grid co–ordinates MG 85, 22 IV 1991, leg. P. Stoev, coll. NMNHS.

0.5 mm

b.s

d.m.e.s.

d.l.e.s

a.s

Figs. 20–21. Ventral aspect of the left stylus (stylomeres 1–2) of the ovipositor of: 20. Laemostenus (Pristonychus) stoevi n. sp., female, paratype; 21. Laemostenus (Pristonychus) punctatus, female. Both specimesn from cave “Devetashka peshtera”, v. Devetaki, Lovech District, Bulgaria: b.s. Basal stylomere; a.s. Apical stylomere; d.l.e.s. Dorsolateral ensiform setae; d.m.e.s. Dorsomedial ensiform seta. Figs. 20–21. Aspecto ventral del estilo izquierdo (estilómero 1–2) del ovopositor de: 20. Laemostenus (Pristonychus) stoevi sp. n., paratipo hembra; 21. Laemostenus (Pristonychus) punctatus, hembra. Ambos especímenes procedentes de cueva “Devetashka peshtera”, Devetaki, distrito de Lovech, Bulgaria: b.s. Estilómero basal; a.s. Estilómero apical; d.l.e.s. Sedas ensiformes dorsolaterales; d.m.e.s. Seta ensiforme dorsomedial.

Animal Biodiversity and Conservation 26.1 (2003)

1 mm

Figs. 22–23. Presence of accessory pubescence on the distal end on the anterior margin of the right protibia of: 22. Laemostenus (Pristonychus) stoevi n. sp., male paratype, cave “Nanin kamik”, v. Muselievo, Nikopol District, Bulgaria; 23. Laemostenus (Pristonychus) euxinicus Nitzu, male specimen, cave “Limanu", v. Limanu, Mangalia District, Romanian Dobrudja. Figs. 22–23. Presencia de la pubescencia accesoria en el extremo distal del margen anterior de la protibia derecha: 22. Laemostenus (Pristonychus) stoevi sp. n., paratipo macho, cueva “Nanin kamik”, Muselievo, distrito de Nikopol, Bulgaria; 23. Laemostenus (Pristonychus) euxinicus Nitzu , macho, cueva "Limanu", Limanu, distrito de Mangalia, Dobrudja rumana.

Diagnostic features This species is quite similar to L. stoevi n. sp., L. euxinicus, and L. punctatus, but differs from all cited species by the shape of median lobe and two parameres (figs. 5, 9, 13, 17). The median lobe in the lateral aspect is somewhat like that of L. punctatus but its apex is not so bent downwards (fig. 5). Compared with males of the three other species, the right paramere of L. derventicus n. sp. seems the most slender with the basal part almost at a right angle to the apical one (fig. 13), whereas the left paramere has the left front margin evidently bent downwards (fig. 17). In particular, the new species can be distinguished from L. stoevi n. sp. in protibia without accessory pubescence on the distal end of the anterior margin and different ratio of width of elytra / width of pronotum. L. derventicus n. sp. is distinct from L. euxinicus in protibia without accessory pubescence on the distal end of the anterior margin, colour of the tegument is lighter, and fewer pores of umbilicate series. L. derventicus n. sp. differs from L. punctatus in depigmentation of tegument, smaller number of marginal pores of umbilicate series, and reduction of the denticulation on claws inside. Etymology This species is named after the region (the Derventski Vazvisheniya Hills) where the holotype was found.

Description Colour piceous–ferrugineus, without metallic lustre; head somewhat darker, palpi lighter. Total length 14.5 mm; width 5.8 mm. Microsculpture on elytra isodiametric, absent on head and pronotum. Head smooth, antennae exceeding first quarter of elytra; eyes slightly prominent, as long as temporae; frontal furrows very shallow; mentum with a bifide tooth. Pronotum cordate, 1.11 times wider than long and 1.41 times wider than head (with eyes), broadest in first third, with a few fine punctures along lateral margins; disc smooth; median furrow well expressed; anterior margin concave, its angles prominent, with rounded apex; lateral margins strongly sinuated towards somewhat projecting posterior angles, bead of lateral margins before both anterior and posterior angles disappears; posterior margin almost straight and slightly curved towards angles; bead of posterior border interrupted in middle; basal surface with single shallow fovea from each side. Legs long and slender; posterior ventral margins of profemora with four setae, alternating with three small, but tubercles not so evident; protibia without accessory pubescence on distal end of anterior margin; first three male protarsi with adhesive bristles ventrally; mesotibia almost straight; mesotibia and metatibia inside distally with brush of hairs; first article of tarsus densely pubescent on all sides; onychium with

Guéorguiev

five pairs of setae on ventral surface; claws smooth inside. Elytra dilated towards posterior half (1.48 times longer than broad and 1.62 broader than pronotum); angle of shoulder protruding, but no clear denticle; scutellar stria and setiferous puncture present, other striae scarcely punctate, intervals flat; umbilicate marginal series of left elytron of 21 pores, right one (of 20 pores); end of seventh stria with three apical pores (two large and one further), hardly visible and rather smaller. Apterous. Ventrum smooth; apophysis of prosternum indistinctly bordered; exterior margin of metaepisterna longer than anterior; last visible sternum with a single marginal pore on each side. Male genitalia shown in figs. 11–14. Type locality The single specimen of this beetle was found in a small precipice at eight–nine m depth, which is situated in Middle Triassic limestone. This precipice is located among the Derventski vazvisheniya Hills, on three–four km west of v. Krajnovo and next to the Bulgarian–Turkish border. Geographical affinities This troglophile species is allopatric of the other species of the “terricola” group here examined (L. stoevi n. sp., L. euxinicus, L. punctatus and L. tychyi), e. g. the population to which these specimens belong is isolated reproductively from the most related taxa. L. derventicus n. sp. is sympatric of L. cimmerius (a beetle belonging to other phyletic trend of the “terricola” group). The latter species is common in microcavernicolous limestone habitats of the Derventski vazvisheniya Hills and adjacent to these regions (unpublished information). Three other ground–beetles taxa were collected together with L. derventicus n. sp.: Platyderus cf. rufus (Duftschmid), Amara saphirea Dej., and Amara lucida (Duft.).

variations in the shape of the sclerites of male genitalia in both specimens (figs. 4, 8, 12, 16) are within the limits of digressions normally observed in samples of separate populations of the same species.. However, some of the characters, mentioned by N ITZU (1998), merit noting with the diagnosis of L. euxinicus. These are: flatter temporae, the evident frontal foveae near to the clypeal suture, angulated carina of the front profemori, more acute front angles, much thinner lateral margins of pronotum, and basal margin of the elytra oblique towards scutellum. Such features are either lacking with the two individuals examined by the present author, or their state is very unstable. The presence of some of the above–mentioned characters can even be observed in single specimens of L. punctatus inhabiting North Bulgaria. These features are not therefore accurate for differentiation. More reliable diagnostic characters in L. euxinicus are probably the shape of male genitalia, the smooth claws, the number of pores of the umbilicate marginal series of elytron, the darker colour of the tegument, practically reduced bead of the base of pronotum, and almost the straight mesotibiae (in the order of enumeration). A fairly important (and stable) external diagnostic character available with this taxon, but omitted by N ITZU (1998), is the presence of accessory pubescence on the distal end of the anterior margin of the protibia (fig. 23). The state of this feature in L. euxinicus , in comparison with L. stoevi n. sp., appears more advanced. Finally, there are no distinct humeral teeth of elytra in either male studied. Geographical affinities L. euxinicus is sympatric of L. punctatus only (cfr. Nitzu, 1998, sub L. terricola p.), and is allopatric of the other three studied here members of the species group “terricola”.

Laemostenus (Pristonychus) euxinicus Nitzu, 1998 (figs. 1, 4, 8, 12, 16, 23) Discussion Material examined 1{, Romanian Dobrudja, v. Limanu (Mangalia District), cave “Limanu", U. T. M. grid co–ordinates PG 25, under stone on clay & guano, 3 VIII 2000, leg. B. Petrov & T. Ivanova, coll. A. Casale; 1{, Romanian Dobrudja, v. Albeshti (Mangalia District), military bunker in Hagieni Forest, U. T. M. grid co–ordinates PG 15, under stone, 1 VIII 2000, leg. B. Petrov & T. Ivanova, coll. NMNHS. Both places are new established for this taxon, after its description (fig. 1). Taxonomic comments After examining the males and studying the original description, the author considers that L. euxinicus is clearly a distinct species. The

L. stoevi n. sp. and L. derventicus n. sp., included in the "terricola” species group of subgenus Pristonychus, with L. euxinicus, L. tichyi and L. punctatus, should be considered as separate species of the “superspecies” L. terricola (Herbst, 1783), after CASALE (1988). At present, Casale (personal communication), an authority on the Sphodrini carabids, continues considering that “the question about the species of the “terricola” group is not easy (species, semispecies, subspecies?)”. This problem apparently requires further research. In comparison with L. terricola and L. punctatus, both new species are particularly interesting for the presence of some modified characters (depigmentation of the tegument, reduction of the

Animal Biodiversity and Conservation 26.1 (2003)

number of pores of the umbilical series, lack of obvious tubercles between the setae on the posterior ventral margins of the profemora, presence of accessory pubescence on the distal end of the anterior margin of the protibia, mesotibia slightly curved or almost straight distally, and reduction of the denticulation of the internal side of claws). These presumably apotypic special features would be regarded as further adaptation to a subterranean manner of living. On account of convergence, most of the modifications mentioned above, including the lengthening of antennae and legs, seem adaptive rather than phyletic characters, which cannot differentiate the subgenera of Laemostenus (Casale, 1988). For example, similar adaptive characters appear also in Actenipus Jeannel, 1937. In two species from the last subgenus, e.g. Laemostenus (Actenipus) acutangulus (Schaufuss, 1862) from south Italy (C ASALE , 1988) and Laemostenus (Actenipus) dubaulti Lassale, 1989 from the Peloponessos (LASSALE, 1989), there is accessory pubescence on the distal end of the anterior margin of the protibia. The reasons for such adaptation are probably to a great extent similar to those discussed by NITZU (1998). The lack of specimens captured from epigeous, lapidicolous or stratobios microhabitats shows that the most appropriate microclimatic conditions for the survival of two new species lies in the net of cracks of limestone. In the underground microhabitat, the variation of either or both of the most important abiotic factors (humidity and temperature) for the existence of these mesophillous beetles is considerably less than on ground, under stones or in the superficial soil stratum.. I suggest that L. stoevi n. sp., L. derventicus n. sp., L. euxinicus and L. tichyi are formed as the result of preadaptation brought about in several local Pleistocene populations of an eutopic (not so specialized, and arboreal) South–European species. It seems also that all four taxa present independent divergent lines from this ancestor, which was comprised during the Pleistocene both recent morphospecies (or semispecies?) [L. terricola (in the north–west) and L. punctatus (in the south–east)]. In the shape of the male genitalia (figs. 2–17) and the lower number of setae on the posterior margin of the profemora, all the four abovementioned species, are more similar to L. terricola than to

L. cimmerius. The apices of the median lobes dorsally (figs. 6–9) in three of them (the male genitalia of L. tichyi are as yet unknown) are wholly rounded (like L. terricola ) but not subacuminate (like L. cimmerius). The number of setae on the posterior margin of the profemori of the four species is three or four (figures closer to L. terricola rather than to L. cimmerius).

Acknowledgements My special thanks to Prof. Dr. Achille Casale (Sassari, Italy) who confirmed both new species, critically examined the preliminary draft and made valuable suggestions to improving the work. I would also like to thank my colleagues Dr. Petar Beron, Mrs. Teodora Ivanova, Mr. Pavel Stoev, and Mr. Boyan Petrov, all from NMNHS, for the opportunity to study the specimens here included, as well as Mr. P. Petrov (Sofia) and A. Zarichinov (NMNHS) for their technical assistance.

References BALL, G. E. & SHPELEY, D., 1983. The species of eucheloid Pericalina: Classification and evolutionary considerations (Coleoptera: Carabidae: Lebiini). Can. Entomol., 115: 743–806. B ERON , P., 1994. Résultats des recherches biospéléologiques en Bulgarie de 1971 à 1994 et liste des animaux cavernicoles bulgares. Tranteeva, 1: 1–137. C ASALE , A., 1988. Revisione degli Sphodrina (Coleoptera, Carabidae, Sphodrini). Monogr. Mus. Reg. Sci. Nat. Torino, 5: 1–1,024. LASSALE, B., 1989. Un nouveau Laemostenus de Gréce (Col. Carabidae, Sphodrini). Nouv. Revue Ent. (N. S.), 6(4): 437–438. N ITZU , E., 1998. Laemostenus (Pristonychus) euxinicus n. sp. (Coleoptera: Carabidae) in the subterranean habitat from southern Dobrogea, Romania. Trav. Mus. Natl. Hist. nat. “Grigore Antipa”, 40: 337–346. POPOV, V., 1970. Aire d’extension du calcare (karst) en Bulgarie et quelques–unes de ses particularités. Bull. Inst. Géogr. Sofia, 13: 5–19 (In Bulgarian).

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 26.1 (2003)

Some observations on the life history of the freshwater amphipod Echinogammarus longisetosus Pinkster, 1973 (Gammaridae) from Catalonia (Spain, N Iberian peninsula) G. Guerao

Guerao, G., 2003. Some observations on the life history of the freshwater amphipod Echinogammarus longisetosus Pinkster, 1973 (Gammaridae) from Catalonia (Spain, N Iberian peninsula). Animal Biodiversity and Conservation, 26.1: 31–39. Abstract Some observations on the life history of the freshwater amphipod Echinogammarus longisetosus Pinkster, 1973 (Gammaridae) from Catalonia (Spain, N Iberian peninsula).— Aspects of the population structure and reproductive biology of the freshwater amphipod Echinogammarus longisetosus were studied in the northeastern Iberian Peninsula (Catalonia, Spain). Amphipods were sampled at approximately monthly intervals from September 1999 to October 2000. Pairs in precopula and ovigerous females were present all year round. The sex ratio was not significantly different from 1:1. Juveniles were abundant in all samples (> 40%). The number of eggs carried by females (N) was related to the size of the females (LP3) (range: 9–68, mean value: 28.2): N = 0.594 LP33.141 (n = 80, r 2 = 0.7136, LP3 were measured from the anterior part of the head to the posterior edge of the third pereional segment; total length was approximately 3.5 times greater than LP3 ). The mean embryo diameter was 0.45 mm (mean of measurements of the long and short axes of recently laid eggs). The egg volume increased during development (2 fold by eggs close to hatching). Key words: Echinogammarus longisetosus, Amphipoda, Life cycle, Population structure, Reproduction, Fecundity. Resumen Algunas observaciones sobre el ciclo biológico del anfípodo de agua dulce Echinogammarus longisetosus Pinkster, 1973 (Amphipoda: Gammaridae) en Cataluña (España, N de la península ibérica).— Se estudian varios aspectos relacionados con la estructura poblacional y la biología reproductiva del anfípodo Echinogammarus longisetosus, basándose en muestras obtenidas en el nordeste de la península ibérica (Cataluña, España). Los anfípodos se muestrearon a intervalos de aproximadamente un mes desde septiembre de 1999 hasta octubre de 2000. Se capturaron parejas en precópula y hembras ovígeras en todas las muestras obtenidas durante el período estudiado. La relación de sexos no fue significativamente diferente de 1:1. Los individuos jóvenes eran abundantes en todas las muestras (> 40%). El número de huevos transportados por las hembras ovígeras (N) estaba relacionado con el tamaño de éstas (LP3) (rango: 9–68, valor medio: 28,2): logN= 3,142LP3 – 0,226 (n = 80, r = 0,845; LP3 = longitud del céfalon más los tres primeros pereionitos; la longitud total era aproximadamente 3,5 veces LP3). El diámetro medio de los huevos era de 0,45 mm (media de la longitud del eje mayor y del eje menor de los huevos al principio del desarrollo embrionario). El volumen de los huevos se incrementaba durante el desarrollo embrionario (2 veces en los huevos a punto de eclosionar). Palabras clave: Echinogammarus longisetosus, Amphipoda, Ciclo vital, Estructura poblacional, Reproducción, Fecundidad. (Received: 9 IV 02; Conditional acceptance: 30 VII 02; Final acceptance: 31 XII 02) Guillermo Guerao, Dept. de Biologia Animal (Artròpodes), Fac. de Biologia, Univ. de Barcelona, Av. Diagonal 645, 08028 Barcelona, Espanya (Spain). E–mail: guilleg@porthos.bio.ub.es.

ISSN: 1578–665X

Guerao

Introduction The genus Echinogammarus Stebbing, 1899 is found in a wide area extending from Europe and Northern Africa to Asia Minor (PINKSTER, 1993). E. longisetosus Pinkster 1973, is a freshwater amphipod endemic of the Iberian peninsula. It is known from Guipúzcoa, Vizcaya, Navarra, Álava, Burgos, Zaragoza, Valencia, Teruel, Guadalajara, Cuenca, Madrid, Lleida, Girona, Tarragona and Barcelona (P INKSTER , 1993). Knowledge of E. longisetosus to date has been limited to its description and a few ecological and zoogeographical notes (PINKSTER, 1993); its biological cycle and reproduction was unknown. The aim of the present work was to study the life cycle and reproduction of E. longisetosus and to compare it with literature data concerning freshwater species of the genus Echinogammarus and Gammarus.

Material and methods The population studied inhabits the Torrent de Vallbardina (near Font Freda) in the locality of Gelida (CÓRDOBA, 1999), about 28 km southwest of Barcelona (Catalonia, Spain, 41.437º N, 1.839º E) (fig. 1). Specimens for the present study were collected once a month from October 1999 to October 2000. Samples were taken with a fine–meshed hand– net along the detritus and vegetal debris. On each occasion the water temperature was measured and the presence of pairs in precopula was noted. Echinogammarus longisetosus individuals were counted and classified into four demographic categories: juveniles without distinctive characteristics; non–ovigerous females with oostegites; ovigerous females with fully developed setose

oostegites and carrying embryos in their marsupium; males with ventral genital apophyses (penial papillae) in the 7th segment of the pereion. Amphipods were sorted from the samples with the aid of a dissecting microscope and measured with an ocular micrometer to the nearest 0.1 mm. Individuals were measured from the anterior part of the head (front) to the posterior edge of the third pereional segment (L P3 ). In addition, 80 amphipods were measured for total length (Lt ) measured from the front of the head to the base of the telson. In order to determine the relationship between female size and brood size, 80 females with recently laid eggs were examined and the number of eggs counted. Diameter of three axes (length, width and height) of live eggs was measured with a binocular microscope incorporating an ocular micrometer. Embryo diameter (ED) was the mean of measurements of the length (long axis) and short axis of recently laid eggs (width = height in recently laid eggs). Egg volume was calculated assuming their shape to be ellipsoidal (V = 4/3πr1r2r3). Results Water temperature in the sampling locality varied from 8ºC in December 1999 to 16ºC in September 2000 (fig. 2). The substrate consists mainly of sand and stones with detritus and vegetal debris. Depth ranges from 0.1–0.5 m. The relationship between LP3 and total length (Lt ) is expressed as: Lt = 3.5303 LP30.9978 (r2 = 0.9917, n = 80) LP3 was used as individual size reference because it can be measured more accurately than total

Llobregat River

Martorell

N 42

Llobregat River Gelida

Anoia River Barcelona Gelida

Mediterranean Sea 100 km

Torrent de Vallbardina

Font Freda 5 km

Fig. 1. Sampling area inhabited by a population of Echinogammarus longisetosus. Fig. 1. Zona de muestreo habitada por una población de Echinogammarus longisetosus.

Animal Biodiversity and Conservation 26.1 (2003)

18 Temperatura (ºC)

16 14 12 10 8 6 S O 1999

J F 2000

Fig. 2. Monthly water temperature of the investigated area: S. September; O. October; N. November; D. December; J. January; F. February; M. March; A. April; M. May; J. June; J. July; A. August. Fig. 2. Temperatura mensual del agua de la zona muestreada: S. Septiembre; O. Octubre; N. Noviembre; D. Diciembre; J. Enero; F. Febrero; M. Marzo; A. Abril; M. Mayo; J. Junio; J. Julio; A. Agosto.

body length. Total length was approximately 3.5 times greater than LP3. Males reached larger sizes than females. Maximum LP3 was observed in specimens collected in April 2000 and December 1999: 5.1 mm (~17.7 mm Lt) and 4.05 mm (~14.1 mm Lt) for males and females, respectively. Males of ~1.5 to 1.8 mm LP3 were already recognisable by the presence of genital apophyses, while females of ~1.6 to 1.9 mm LP3 had just begun to develop oostegites. The minimum LP3 of ovigerous females was 2.6 mm (~9.1 mm Lt). The minimum LP3 of juveniles was 0.5 mm (~1.9 mm Lt). The size of juveniles hatched from eggs produced by females maintained in the laboratory was ~1.8 mm Lt. The life cycle of Echinogammarus longisetosus is illustrated by data presented in figure 3, together with the water temperature. Pairs in precopula and ovigerous females were recorded in all samples; the percentage of ovigerous females reared a maximum in July 2000 (72.7%) and a minimum in October 1999 (12.5%). The structure of the E. longisetosus population was similar throughout the year and no discrete generations were evident because of the intensive periods of breeding. Juveniles were abundant in all samples (> 40%). The percentage of juveniles reached a maximum in February (74.6%) and spring (72.2% in April and 73.9% in June). The sex ratio was not significantly different from 1:1 (χ2 test, P < 0.05) for all months. However, males outnumbered females in all samples except in September 2000 (fig. 4). The number of eggs (N ) carried by the female of E. longisetosus was related to the size (LP3 )

(fig. 5): N = 0.594 LP33.141 (n = 80, r 2 = 0.7136). The highest number of eggs was 68 from a female of 4 mm LP3 (~13.9 mm Lt). The lowest number of eggs was 9, from a female of 2.6 mm L P3 (~9.12 mm Lt). The mean number of eggs was 28.2 (σ = 12.1, n = 80). The long axis length of recently laid eggs varied from 0.48 to 0.53 mm, with a mean value of 0.51 mm (σ = 0.02, n = 100); the small axis length ranged from 0.400 to 0.425 mm, with a mean value of 0.39 mm (σ = 0.02, n = 100); the mean embryo diameter was 0.45 mm, with a mean volume of 0.0420 mm3. The eggs showed an increase in volume of the order of 100% during development: the mean volume of the eggs close to hatching was 0.0854 mm3 (length = 0.675 mm; width = 0.537 mm; height = 0.450 mm). Seasonal differences in egg size were not observed.

Discussion The life history types of amphipods were distributed according to latitudinal gradients: longevity, breeding periods, body size at maturity, brood size, and size of embryos in gammarid amphipods seem to be clearly related to temperature (GABLE & CROKER, 1977; MORINO, 1978; KOLDING & FENCHEL, 1981; WILDISH, 1982; SAINTE–MARIE, 1991). High– latitude gammaridean amphipods are characterized in general by univoltinism, delayed maturity, large embryos, and few broods in a lifetime. Iteroparous or semiannual population types, with high reproductive potentials, are more characteristic of low latitude habitats (SAINTE–MARIE, 1991).

Guerao

% 45

30 16 IX 1999 16ºC n = 108

25 20

22 XII 1999 8ºC n = 64

5 5

0 5

10 15

15 50

15 X 1999 15ºC n = 202

02 II 2000 9ºC n = 83

55 45

35 25

5 0

26 XI 1999 9ºC n = 66

40 30

8 III 2000 9ºC n = 146

50 40 30

10 0

20 0.4

1.4 2.4 3.4 LP3 length (mm)

4.4

0.4

1.4 2.4 3.4 L P3 length (mm)

4.4

Fig. 3. Monthly distribution of LP3 length in juveniles, males and females of Echinogammarus longisetosus. Fig. 3. Distribución mensual de clases de talla (LP3) de individuos jóvenes, machos y hembras de Echinogammarus longisetosus.

Animal Biodiversity and Conservation 26.1 (2003)

% 35

50 26 IV 2000 12.5ºC n = 95

1 IX 2000 16ºC n = 344

30 25 20

15 10

5 10

0 5

10 15

10 60

2 VI 2000 14ºC n = 142

19 X 2000 12ºC n = 79

30 25

20 15

10 20

0 5

10 15

0.4

1.4 2.4 3.4 4.4 L P3 length (mm)

50 11 VII 2000 15ºC n = 128

juveniles

males

nonovigerous females

ovigerous females

0 10

0.4

1.4 2.4 3.4 L P3 length (mm)

4.4

There is a tendency towards an extended reproductive season with decreasing latitude in freshwater gammarid species (SAINTE–MARIE, 1991). Moreover, there is a relationship between the length of the

breeding period and the altitude of the sampling locality (ZIELI¼SKI, 1995). In localities of constant water temperature amphipods may have an acyclic breeding without a winter pause (table 1). ZIELI¼SKI

Guerao

Sex ratio (F/F+M)

0,55 0,5 0,45 0,4 0,35 0,3 S O 1999

M 2000

Fig. 4. Monthly sex ratio females / (females + males) of the E. longisetosus in the study area: S. September; O. October; N. November; D. December; J. January; F. February; M. March; A. April; M. May; J. June; J. July; A. August. Fig. 4. Distribución mensual de la proporción de sexos hembras / (hembras + machos) de E. longisetosus en la zona muestreada: S. Septiembre; O. Octubre; N. Noviembre; D. Diciembre; J. Enero; F. Febrero; M. Marzo; A. Abril; M. Mayo; J. Junio; J. Julio; A. Agosto.

(1995) reported that low temperatures (below 4– 7ºC) stop the breeding of Gammarus balcanicus. The population of Echiogammarus longosetosum from Torrent de Vallbardina (Catalonia, Spain) sampled on the present study showed continuous reproduction throughout the year and the maximum percentage

70 60

of ovigerous females appeared in spring and summer. During the sampling period, the water temperatures in winter months were from 9ºC to 8ºC (fig. 2). In contrast, KONOPACKA & JESIONOWSKA (1995) noted the presence of ovigerous females of E. ischnus only from February to October in Liche½skie lake

y = 0.5943 X3.141 r 2 = 0.7136

Fecundity

50 40 30 20 10 0 2.5

3.5 LP3 length (mm)

4.5

Fig. 5. Relationship between fecundity (number of eggs) and female size (LP3) on E. longisetosus. Fig. 5. Relación entre la fecundidad (número de huevos) y el tamaño de la hembra (LP3) en E. longisetosus.

Animal Biodiversity and Conservation 26.1 (2003)

Table 1. Breeding period of several freshwater and brackish gammarid amphipods: WT. Range of water temperature (ºC). Tabla 1. Periodo de puesta en varias especies de amfípodos gammáridos de agua dulce y salobre: WT. Rango de temperaturas del agua (ºC).

Species

Breeding period

Reference

E. longisetosus

8–16

Continuous

Present study

E. ischus

10–12

Continuous

KONOPACKA & JESIONOWSKA (1995)

E. ischus

5.2–29

February–October

KONOPACKA & JESIONOWSKA (1995)

February–October

ZIELI¼SKI (1998)

2–7.4

April–October

ZIELI¼SKI(1995)

G. fossarum

8–10

Continuous

BRZEZI¼SKA–BLASZCZYK & JAòDòEWSKI (1980)

G. troglophilus

11–13

Continuous

JENIO (1980)

G. leopoliensis G. balcanicus

0.2–15.3

G. palustris

-2–20

April–November

GABLE & CROKER (1977)

G. lacustris

4.5–11

April–October

HYNES & HARPER (1972)

G. lacustris

2–12

May–August

HYNES & HARPER (1972)

February–October

HYNES & HARPER (1972)

G. pseudolimnaeus

0–19.5

(Poland) (table 1). Similar life cycles were found in several freshwater species of the genus Gammarus from high latitudes (table 1). The percentage of juveniles in the studied Echinogammarus longisetosus population may indicate a high mortality due to predation. In the sampled stream, there was a great density of benthic predators (Guerao, pers. obs.): mainly sala-

mander larvae (Salamandra salamandra ) and naiads of anisopter odonats. JENIO (1980) indicated that salamander larvae can be potential predators of gammarids. In amphipods, it is usual that the sex ratio shows seasonal fluctuations and the females are more numerous than males (FISH & PREECE, 1979; HUGHES, 1978; MOORE, 1981). Sexually biased pre-

Table 2. Fecundity and egg size of several freshwater and brackish gammarid amphipods: FL. Female total length (max.); MNE. Mean number of eggs (range); ED. Embryo diameter (in mm). Tabla 2. Fecundidad y tamaño del huevo en varias especies de amfípodos gammáridos de agua dulce y salobre: FL. Longitud total de la hembra (max.); MNE. Número medio de huevos (rango); ED. Diámetro del embrión (en mm). Species

MNE

Reference

0.45

Present study

E. longisetosus

14.1

28 (9–68)

E. ischnus

12.0

14 (3–27)

–

G. fasciatus

15.0

29 (1–86)

0.46

G. lacustris

16.0

22 (1–40)

–

HYNES & HARPER (1972)

G. duebeni

18.0

25.4

0.56

STEELE & STEELE (1969)

–

15 (5–27)

–

G. pseudolimnaeus

15.0

39 (10–91)

–

HYNES & HARPER (1972)

G. mucronatus

15.5

34.6

0.42

FREDETTE & DÍAZ (1986)

G. leopoliensis

12.3

16.7 (8–31)

–

ZIELI¼SKI (1998)

G. balcanius

14.0

9.4 (2–20)

–

ZIELI¼SKI (1995)

G. minus

KONOPACKA & JESIONOWSKA (1995) CLEMENS (1950)

JENIO (1980)

Guerao

dation has been used as a hypothesis to explain the female–biased sex ratio. MOORE (1981) emphasized the impact of predation on the active sex (male). However, in E. longisetosus a sex ratio is not biased in favour of females and males are slightly more abundant than females. GABLE & CROKER (1977) also showed an unusual sex ratio for Gammarus palustris; males are more abundant than females throgouth the year. The sex ratio is also influenced by physical environmental factors. KINNE (1961) suggested that sex determination in Gammarus duebeni is temperature–dependent. In the laboratory young G. duebeni became predominantly male under long– day conditions and predominantly female under short–day conditions (BULNHEIM , 1978; WATT, 1994). Future studies in the laboratory should be carried out to clarify the factors influencing E. longisetosus sex ratio. The number of eggs produced per female increases with female size in E. longisetosus, as in many other gammarid amphipods (NELSON, 1980; KOLDING & FENCHEL, 1981; FREDETTE& DÍAZ, 1986; SAINTE–MARIE, 1991; KONOPACKA & JESIONOWSKA, 1995; ZIELI¼SKI, 1995, 1998). The mean number of eggs carried by E. longisetosus females are not markedly different from other freshwater and brackish gammarid species (SUTCLIFFE, 1993; ZIELI¼SKI, 1998) (table 2). The mean embryo size (ED) obtained from E. longisetosus is similar to that reported for many other freshwater gammarid amphipods (SAINTE– MARIE, 1991) (table 2). The eggs of amphipods increase in size during development and the size increment varies according to the amphipod species (MOORE, 1981; SHEADER, 1983, 1996). Eggs of gammarids generally show an increase in volume of the order of 140–200% during development (SHEADER, 1996). In E. longisetosus, the eggs volume increment is lower than in other gammarid amphipods (about 100%). Seasonal changes in egg volume are common in many species of amphipods (SHEADER, 1983, 1996). The length of the intermoult period is important in determining the size of oocytes; therefore, egg size is related to the temperature during oocyte development (SHEADER, 1996). SHEADER (1996) showed a seasonal cycle in egg size of Gammarus insensibilis, with small egs in the warmer summer months and large eggs in winter; the temperature values of the sampling area ranges from ~5ºC in winter to ~25ºC in summer. In the present study, seasonal differences in egg size were probably not been detected because of the relatively small yearly range of stream water temperature (fig. 2).

Acknowledgements I wish to thank Dr. Joan Pretus and Mr. Joaquim Margarit for their valuable help in locating necessary references and documentation.

References BRZEZI¼SKA–BLASZCZYK, E. & JAòDòEWSKI, K., 1980. Reproductive cycle of Gammarus fossarum Koch (Crustacea, Amphipoda) in different thermic conditions. Acta Univ. Lodz., 33: 129–153. B ULNHEIM , H. P., 1978. Interaction between genetic, external and parasitic factors in sex determination of the crustacean amphipod Gammarus duebeni. Helgoländer wiss. Meeresunters., 31: 1–33. CLEMENS, H. P., 1950. Life cycle and ecology of Gammarus fasciatus Say. Ohio State Univ., Contr. Franz Theodore Stone Inst. Hydrobiologia, 12: 1–61. CÓRDOBA, M., 1999. Les fonts del Panadès i els seus voltants. Ed. El Cargol Publicacions s. l., Vilafranca del Penedès, Barcelona. FISH, J. D. & PREECE, G. S., 1979. The annual reproductive patterns of Bathyporeia pilosa and Bathyporeia pelagica (Crustacea: Amphipoda). J. mar. biol. Ass. U. K., 50: 475–488. FREDETTE, T. J. & DÍAZ, R. J., 1986. Life history of Gammarus mucronatus Say (Amphypoda: Gammaridae) in warm temperature estuarine habitat, York River, Virginia. J. Crust. Biol., 6(1): 57–78. GABLE, M. F. & CROKER, R. A., 1977. The salt marsh amphipod, Gammarus palustris Bousfield, 1969 at the northern limit of its distribution. Estuar. cstl. mar. Sci., 5: 123–134. HUGHES, R. G., 1978. Life-histories and abundance of epizoites of the hydroid Nemertesia antennina (L.). J. mar. biol. Ass. U. K., 58: 313–332. HYNES, H. B. N. & HARPER, F., 1972. The life histories of Gammarus lacustris and G. pseudolimnaeus in southern Ontario. Crustacena, Suppl. 3: 329–341. JENIO, F., 1980. The life cycle and ecology of Gammarus troglophilus Hubricht & Mackin. Crustaceana, Suppl. 6: 204–215. KINNE, O., 1961. Die Geschlechtsbestimmung des Flohkrebses Gammarus duebeni Lillj (Amphipods) ist temperaturabhängig —eine Entgegnung. Crustaceana, 3: 56–69. KOLDING, S. & FENCHEL, T. M., 1981. Patterns of reproduction in different populations of five species of the amphipod genus Gammarus. Oikos, 37: 167–172. KONOPACKA , A. & JESIONOWSKA , K., 1995. Life history of Echinogammarus ischnus (Stebbing, 1898) (Amphipoda) from artificially heated Lichenskie Lake (Poland). Crustaceana, 68(3): 341–349. MOORE, P. G., 1981. The life histories of the amphipods Lembos websteri Bate and Corophium bonnellii Milne Edwards in Kelp Holdfasts. J. exp. mar. Biol. Ecol., 49: 1–50. M ORINO, H., 1978. Studies on the Talitridae (Amphipoda, Crustacea) in Japan. III. Life history and breeding activity of Orchestia platensis Kroyer. Publ. Seto Mar. Biol. Lab., 24: 245–267. NELSON, W. G., 1980. Reproductive patterns of

Animal Biodiversity and Conservation 26.1 (2003)

gammaridean amphipods. Sarsia, 65: 61–71. P INKSTER , S.,1993. A revision of the genus Echinogammarus Stebbing, 1899 with some notes on related genera. Memorie del Museo Civico di Storia Naturale (serie 2) Sezione Scienze della Vita. SAINTE–MARIE, B., 1991. A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history with latitude, depth, salinity and superfamily. Hydrobiologia, 223: 189–227. SHEADER, M., 1983. The reproductive biology and ecology of Gammarus duebeni (Crustacea: Amphipoda) in southern England. J. mar. biol. Ass. U. K., 63: 517–540. – 1996. Factors influencing egg size in the gammarid amphipod Gammarus insensibilis. Mar. Biol., 124: 519–526. STEELE, D. H. & STEELE, V. J.,1969. The biology of Gammarus (Crustacea, Amphipoda) in the

northwestern Atlantic. I. Gammarus duebeni Lillj. Can. J. Zool., 47: 235–244. SUTCLIFFE, D. W., 1993. Reproduction in Gammarus (Crustacea: Amphipoda): female strategies. Freshwater Forum, 3(1): 26–64. W ATT, P. J., 1994. Parental control of sex ratio in Gammarus duebeni , an organism with environmental sex determination. J. Evol. Biol., 7: 177–187. WILDISH, D. J., 1982. Evolutionary ecology of reproduction in gammaridean Amphipoda. Int. J. Invert. Reprod., 5: 1–19. Z IELI¼SKI, D., 1995. Life history of Gammarus balcanicus Schäferna, 1922 from the Biesócóady mountains (eastern Carpathians, Poland). Crustaceana, 68(1): 61–72. – 1998. Life cycle and altitude range of Gammarus leopoliensis Jaó dóewski & Konopacka, 1989 (Amphipoda) in south–eastern Poland. Crustaceana, 71(2): 129–143.

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 26.1 (2003)

A new larval trombidiid, Calctrombidium nikolettae n. gen., n. sp. (Acari, Prostigmata, Trombidiidae, Trombidiinae) from India R. Haitlinger

Haitlinger, R., 2003. A new larval trombidiid, Calctrombidium nikolettae n. gen., n. sp. (Acari, Prostigmata, Trombidiidae, Trombidiinae) from India. Animal Biodiversity and Conservation, 26.1: 41–44. Abstract A new larval trombidiid, Calctrombidium nikolettae n. gen., n. sp. (Acari, Prostigmata, Trombidiidae, Trombidiinae) from India.— Calctrombidium nikolettae n. gen., n. sp. is described from Calcutta in India. Larvae were obtained from plants. The new genus has the following main features: anterior dorsal scutum sensillae placed between setae AL and PL; PL setae placed posterior and lateral to bases of sensilla. Posterior dorsal scutum absent. Bf 5, 4, 4, Tr 1, 1, 1, Cx 2, 2, 1, all barbed. Posterior claw III reduced to a hooked conical spur. Key words: Acari, Trombidiidae, Calctrombidium nikolettae n. gen., n. sp., India. Resumen Una nueva forma larval de trombidio, Calctrombidium nikolettae gen. n., sp. n. (Ácari, Prostigmata, Trombidiidae, Trombidiinae) de la India.— Se describe una nueva forma larval de trombidio Calctrombidium nikolettae gen. n., sp. n. procedente de Calcuta, India. Las larvas se obtuvieron de plantas. El nuevo género se caracteriza por: sensilios del scutum anterior dorsal situados entre las sedas AL y PL; Sedas PL situadas posterior y lateral a la base de los sensilios. Scutum dorsal posterior ausente. Bf 5, 4, 4, Tr 1, 1, 1, Cx 2, 2, 1, todas barbuladas. Uña posterior III reducida a un espolón cónico ganchudo. Palabras clave: Ácari, Trombídiidae, Calctrombidium nikolettae gen. n., sp. n., India. (Received: 12 VI 01; Conditional acceptance: 29 X 01; Final acceptance: 3 X 02) Ryszard Haitlinger, Dept. of Zoology, Agricultural Academy, 50–205 Wroclaw, Cybulskiego 20, Poland. E–mail: rhait@ozi.ar.wroc.pl

ISSN: 1578–665X

Introduction The subfamily Trombidiinae Leach consists of 12 genera; some of them were described based only on postlarval instars; five genera were described based on larvae. Now, in this subfamily the following genera based on larvae or adults with known larval instars have been reported: Trombidium Fabricius, Paratrombium Bruyant, Dinothrombium Southcott, Clinotrombium Southcott and Pollicotrombium Southcott. According to SOUTHCOTT (1986), 7 genera based on larvae (or larvae and adults) belonged to this subfamily; later ZHANG & XIN (1992) synonymized the genus Nippotrombium Southcott with the genus Allothrombium Berlese and the genus Acritotrombium Southcott was transferred to the subfamily Allothrombiinae Thor. In this paper, a new genus Calctrombidium for new species C. nikolettae is described from India. To date only two species were known in India, both belonging to the family Trombidiidae: Dinothrombium gigas (Trouessart) based on adults and Allothrombium muscaparasiticae Vishnupriya & Mohanasundaram based on larvae (THOR & WILLMANN, 1947; VISHNAUPRIYA & MOHANASUNDARAM, 1988).

Material and methods Two specimens of Calctrombidium nikolettae n. gen., n. sp., were obtained from plants in Calcutta, India. They were mounted in Berlese fluid. The terminology is based on ROBAUX (1974) and SOUTHCOTT (1986). All measurements are given in micrometers (µm). The holotype will be deposited in the Museum of Natural History, Wroclaw University (MNHWU).

Results Fam. Trombidiidae Leach, 1815 Subfam. Trombidiinae Leach, 1815

Calctrombidium n. gen. Diagnosis Anterior dorsal scutum sensillae placed between setae AL and PL; PL setae placed posterior and lateral to bases of sensilla. Posterior dorsal scutum absent, but two setae are present in place where scutellum usually is. Basifemur 5, 4, 4, Trochanteralae 1, 1, 1, Coxalae 2, 2, 1, all barbed. Seta 1a (on coxa I) and seta 2a (on coxa II) both placed at anterior margin of these coxae. Posterior claw III reduced to a hooked conical spur. Palptarsus with only short setae, without long and barbed setae. Hypostomalae distally branched. Type species Calctrombidium nikolettae n. sp.

Haitlinger

Etymology Generic name is derived from the first part of the name: Calcutta, the place of type species collection, and "–tromb–" as a root word of the superfamily. Remarks Calctrombidium n. gen. is similar to genera Trombidium, Dinothrombium and Clinotrombium. It differs from Dinothrombium by PL placed beyond bases of scutal sensilla, proximal coxala II placed near anterior margin of coxa; from Clinotrombium by PL situated at posterior angle of scutum, proximal coxalae I placed at anterior margin of coxae and coxalae II placed near anterior margin of coxae; from Trombidium by barbed coxala 1a and proximal coxala II placed near anterior margin of coxa.

Calctrombidium nikolettae n. sp. (figs. 1–8) Examined material Holotype larva, Calcutta, India, 30 II 2001, from herbaceous plants on large recreation ground near centre of Calcutta; paratype, the same data as in holotype; leg. R. Haitlinger; MNHWU. Description Larva Idiosoma elongate. Dorsal surface of idiosoma with 20 very slightly barbed setae, arranged 4, 6, 4, 4, 2. Setae without platelets (fig. 1). Two pairs of eyes, both on platelet; the anterior eye larger than the posterior eye. Dorsal scutum with very weakly barbed AL and PL and distinctly barbed AM. Setae AL about half the length of setae PL. AM = AL. Sensillae distally with setules (fig. 3). Scutellum absent but two setae present in its place. Ventral surface of idiosoma with two intercoxal setae 3a, present between coxae III. Beyond coxae III six setae; two posterior setae weakly barbed (fig. 2). Gnathosoma with palpfemur and palpgenu without setae, palptarsus with seven short and nude setae (with solenidion). Hypostomalae distally branched (figs. 4, 5). Leg lengths (with coxae, without claws) I 300 holotype, 310 paratype; II 274, 284; III 288, 296. Ip = 862, 890. Legs setal formula Leg I. Ta–1ω, 2ζ, 14B; Ti–2ϕ, 5B; Ge–2δ, 4B; Fe– 5B; Tr–1B. Coxa with two barbed setae; seta 1a placed at anterior margin of coxa and seta 1b placed in angle at posterior and lateral margins of coxa (fig. 6). Leg II. Ta–1ω, 1ζ, 11B; Ti–2ϕ, 5B; Ge–1δ, 3B; Fe–4B; Tr–1B. Coxa with two barbed setae; seta 2a near anterior margin of coxa and seta 2b near posterior margin of coxa. Solenidion δ relatively long (36 µm) (fig. 7).

Animal Biodiversity and Conservation 26.1 (2003)

5 ω ω σ

ϕ ϕ

σ σ

ζ ω

Figs. 1–8. Calctrombidium nikolettae n. sp.: 1. Idiosoma, dorsal view, eyes and dorsal seta detailed; 2. Idiosoma, ventral view and ventral seta detailed; 3. Scutum; 4. Gnathosoma and hypostoma detailed; 5. Palptarsus; 6. Leg I, tarsus–coxa; 7. Leg II, tarsus–coxa; 8. Leg III, tarsus– coxa: ω. Solenidion on tarsi I, II; ϕ. Solenidion on tibiae I, II; σ. Solenidion on genu I–III; ζ. Eupathidium. Figs. 1–8. Calctrombidium nikolettae sp. n.: 1. Idiosoma, vista dorsal, ojos y sedas dorsales en detalle; 2. Idiosoma, vista ventral y sedas ventrales en detalle; 3. Scutum; 4. Detalle del gnatosoma y del hipostoma; 5. Palpotarso; 6. Pata I, tarso–coxa; 7. Pata II, tarso–coxa; 8. Pata III, tarso–coxa: ω. Solenidio de los tarsos I, II; ϕ. Solenidio de las tibias I, II; σ. Solenidio del genu I–III; ζ. Eupatidio.

Leg III. Ta–11B; Ti–5B; Ge–1δ, 3B; Fe–4B; Tr–1B. Coxa with one barbed seta 3b placed in median part of coxa. Anterior claw strong, recurved; empodium long, slender; posterior claw strong, curved (fig. 8). Measurements IL (length of idiosoma) 1,695 holotype, 1,511 paratype, IW (width of idiosoma) 707, 774, L 80, 78, W 96, 94, AW 80, 80, PW 80, 84, AA 44, ?, SB 54, 58, ASB 62, 60, PSB 18, 18, ISD 50, 42, AP 22, 28, AL 28, 30, PL 58, 54, AM 28, 28, MA 36, 40, S 60, 64, DS 42–52, 44–54, GL 84, 86, SA 16, 16, SP 20, 20, Ocular sclerite 26, –, TaI 82, 80, TiI 44, 48, GeI 34, 30, FeI 50, 60, TrI 36, 36, CxI 54, 56, TaII 66, 70, TiII 42, 44, GeII

26, 26, FeII 50, 48, TrII 36, 40, CxII 54, 56, TaIII 70, 70, TiIII 48, 50, GeIII 26, 28, FeIII 54, 56, TrIII 38, 44, CxIII 52, 48. Remarks This species has common features with Trombidium telletxeae Goldarazena et al. provisionally included with the genus Trombidium. T. telletxeae also has seta 2a situated at anterior margin of coxa, but differs by the presence of scutellum, nude setae 1a and normal claws on tarsus III (GOLDARAZENA et al., 2000). Etymology The name of the species has been derived from the name Nikoletta.

References GOLDARAZENA, A., ZHANG, Z.–Q. & JORDANA, R., 2000. A new species and a new record of ectoparasitic mites from thrips in Turkey (Acari: Trombidiidae and Erythraeidae). Systematic Parasitology, 45: 75–80. ROBAUX, P., 1974. Recherches sur le developpement et la biologie des acariens Thrombidiidae. Memoires du Museum National d’Histoire Naturelle (n. s.) Serie A Zoologie, 85: 1–186. SOUTHCOTT, R. V., 1986. Studies on the taxonomy and biology of the subfamily Trombidiinae

Haitlinger

(Acarina: Trombidiidae) with a critical revision of the genera. Australian Journal of Zoology, Supplementary Series, 123: 1–116. THOR, S. & WILLMANN, C., 1947. Trombidiidae. Das Tierreich, 71b: 187–541. VISHNUPRIYA, R. & MOHANASUNDARAM, M., 1988. Mites associated with insects in Tamil Nadu, India. Entomon, 12: 247–257. ZHANG, Z.–Q. & XIN, J.–L., 1992. Review of larval Allothrombium (Acari: Trombidioidea), with description of a new species ectoparasitic on aphids in China. Journal of Natural History, 26: 383–393.

Animal Biodiversity and Conservation 26.1 (2003)

A case study of species assessment in invasion biology: the Village Weaverbird Ploceus cucullatus D. C. Lahti

Lahti, D. C., 2003. A case study of species assessment in invasion biology: the Village Weaverbird Ploceus cucullatus. Animal Biodiversity and Conservation, 26.1: 45–55. Abstract A case study of species assessment in invasion biology: the Village Weaverbird Ploceus cucullatus.— Application of recent insights gained in invasion biology to particular species may aid in addressing a central problem of the field, that of prediction of the dynamics of future introduction and invasion. The Village Weaverbird (Ploceus cucullatus) is concluded to be a potential invader of concern in several regions, especially the Mediterranean, Caribbean, and southeastern United States. This conclusion is supported by the introduction and invasion history of the species, factors concluded in recent reviews and quantitative studies to correlate with introduction success or invasiveness in birds, the species’ agricultural pest status in its current range, and a published rating system. A proactive stance is recommended since control efforts have met with little success, but certain characteristics of the Village Weaver may provide opportunities for management. Key words:: Invasive species, Introduction success, Agricultural pests, Birds, Ploceidae, Ploceus cucullatus. Resumen Estudio de un caso de evaluación biológica de una especie invasora: el tejedor Ploceus cucullatus.— La aplicación a determinadas especies de los últimos resultados obtenidos en el campo de la biología de las invasiones podría ayudarnos a abordar un problema clave: predecir cuál será la dinámica de la futura introducción e invasión de ciertas especies. Se ha llegado a la conclusión de que el tejedor Ploceus cucullatus constituye un importante invasor potencial en determinadas áreas geográficas, especialmente en el Mediterráneo, el Caribe y el sudeste de Estados Unidos. Esta conclusión se basa en la historia de la introducción e invasión de determinadas especies, así como en los factores recogidos en distintos análisis y estudios cuantitativos orientados a establecer una correlación entre el éxito de la introducción o invasión de estas aves, la situación de las plagas agrícolas causadas actualmente por esta especie, y un sistema de valoración publicado. Dado que los intentos de control no han resultado muy satisfactorios, se recomienda adoptar una actitud proactiva, si bien cabe la posibilidad de que determinadas características de este tejedor brinden ciertas oportunidades de control. Palabras clave:: Especies invasoras, Éxito de la introducción, Plagas agrícolas, Aves, Ploceidae, Ploceus cucullatus. (Received: 8 II 02; Conditional acceptance: 2 V 02; Final acceptance: 4 XI 02) David C. Lahti, Museum of Zoology and Dept. of Ecology and Evolutionary Biology, Univ. of Michigan, Ann Arbor, MI 48109, U.S.A.

ISSN: 1578–665X

Introduction For decades ecologists have recognized the importance of invasive species, organisms that expand into a new geographical areas and subsequently spread from their points of entry (ELTON, 1958; WILLIAMSON, 1996). A central theme in the political and scientific response to the invasive species problem has been a call for focused research on prediction of the likelihood of an invasion’s occurrence and impact: the “Holy Grail of invasion biology” (ENSERINK, 1999). One way in which research may proceed in this area is to apply knowledge about particular candidate species and sites of potential introduction or spread, to our understanding of typical characteristics of invaders and invasion sites. This paper provides such a case study. The Village Weaver (Ploceus cucullatus) is a common passerine bird native to sub–Saharan Africa (BANNERMAN, 1949; MACLEAN, 1993; BARLOW et al., 1997). The Village Weaver builds elaborate, enclosed nests in often dense colonies, and prefers the proximity of human habitation and agriculture (COLLIAS & COLLIAS, 1971; LAHTI et al., 2002). Its ecological generalism and its successful establishment on islands to which it has been introduced, along with the agricultural damage it causes (e.g., ADEGOKE, 1983a; MANIKOWSKI, 1984), indicate it as an important candidate for applying recent work in invasion biology. Moreover, in the last two decades this species has been sighted with increasing frequency in the southern United States and Europe, which are outside of its current breeding range (e.g., HIPP, 1988; PEZZO & MORELLINI, 1999). This case study aims to: 1. Assemble what is known about the Village Weaver relevant to invasion biology; 2. Assess the likelihood that this species will be an invader of concern in the future; and 3. Determine whether its biology warrants actions to deal with ecological or agricultural problems.

Regions of past and possible future naturalization History of introductions and sightings The West African form of the Village Weaver (P. c. cucullatus) was introduced to the island of Hispaniola long before 1920, when the first specimens were collected (WETMORE & SWALES, 1931). Most researchers believe that the Village Weaver is among those birds described by the eighteenth century historian Moreau de Saint–Méry as having been imported to Haiti from Senegal as cage birds (WETMORE & S WALES, 1931). One source claims a colony to have been established in that country in 1783 (LONG, 1981), and in fact the species could have existed there before that time. By the 1930’s the weaverbird was still mainly known from Haiti, and had only been found in

Lahti

two locations in western Dominican Republic (WETMORE & SWALES, 1931; BOND, 1936). It remained at low densities on the island, and maintained its restricted distribution, through the middle of the twentieth century. As late as 1962 the Dominican Republic was not considered part of its range by MAYR & GREENWAY (1962). In the early 1960’s, however, “a population explosion caused it to become so abundant that it became a serious pest to rice crops” (LONG, 1981). Recently the species has been described as widespread and common in both countries on the island (LEVER, 1987; RAFFAELE et al., 1998), although on no other island in the Greater Antilles. Some indication exists that the Hispaniolan population may be currently undergoing a decline, and some areas that have been known to support large colonies no longer do so (personal observation, IV–VI 01; J. W. Wiley, personal communication, III 01). In about 1880 the western South African form of the Village Weaver (called there the Spotted– Backed Weaver, P. c. spilonotus) was introduced to the Mascarene Island of Réunion. In 1886 it was introduced to nearby Mauritius (CHEKE, 1987; JONES, 1996). These introductions were probably due to escapes from captivity (BARRÉ & BARAU, 1982), and researchers are confident that no reintroductions have followed those events (B ERLIOZ , 1946; SIMBERLOFF, 1992). As of 1946 the Réunion population was still restricted to the cultivated plains near the coast, but already had a reputation as an agricultural pest (BERLIOZ, 1946). By 1982 it was considered with the House Sparrow ( Passer domesticus) to be the worst agricultural pest on the island, and was abundant throughout the island in low elevations. On Mauritius the species spread slowly from its point of initial introduction (CHEKE, 1987) and steadily increased in population size through the 1950s when it began to be considered a pest there as well. Village Weaver specimens were collected from the Cape Verde Islands off the west coast of Africa in 1924 and a breeding attempt was documented in 1993 (HAZEVOET, 1995). Their origin, and whether their presence there has been continuous or intermittent, is unknown, though they are usually presumed to be introduced (LONG, 1981; LEVER, 1987; CRAMP & PERRINS, 1994). A bird established on São Tomé Island has been claimed to be an introduced Village Weaver (MAYR & GREENWAY, 1962). In fact its origin is unknown, and differences in plumage from the mainland Village Weaver have led many to view it as a distinct species (HALL & MOREAU, 1970; NAUROIS, 1994). The first record of the Village Weaver nesting on Martinique was in 1980 (PINCHON & BENITO– ESPINAL, 1980). The species was described as well established a few years later (BARRÉ & BENITO– ESPINAL, 1985). Though common, it is still reported to be localized in the same area to which it was introduced, at the northern end of the island (RAFFAELE et al., 1998).

Animal Biodiversity and Conservation 26.1 (2003)

In the past two decades the Village Weaver has been found in the wild for the first time in North and South America, and Europe. A single male was seen and photographed in South Carolina in 1988, apparently the first record from the continental United States (HIPP, 1988). The closest population to South Carolina is on Hispaniola, 1600 km away, although the bird could also have been an escape. The distance from Hispaniola to Florida is 750 km, although no records exist from that state. Hispaniola is of course close to other Caribbean islands, although the weaver is at most a vagrant in Cuba, Jamaica and Puerto Rico. (Despite the claim in LONG (1981) and LEVER (1987) that it exists on Puerto Rico, there is no support for this in the relevant regional works (e.g., BOND, 1936; RAFFAELE et al., 1998)). Recently the Village Weaver has been seen breeding in Venezuela (R. Restall, personal communication, VII 00). Specimens have been collected from the vicinity of Lake Maracaibo, which is 800km south of the Dominican Republic, or 1,200 km east–southeast of Martinique. In Europe, the Village Weaver has been sighted at least six times in Italy, three of which involved breeding attempts (males building nests) (PEZZO & MORELLINI, 1999). PEZZO & MORELLINI (1999) suggest that the species may survive in the wild in Siena province, and could eventually become established in Central Italy. A breeding attempt has also been documented in the vicinity of Paris (LE MARÉCHAL, 1985). These individuals survived the winter, which suggests that the species may be able to persist in that region. Other breeding attempts in the wild, some successful, are reported from France and Germany (PEZZO & MORELLINI, 1999). In Portugal breeding colonies have reportedly been established (VOWLES & VOWLES, 1994), although whether they persist is unknown. No sources are known for the birds in any of these localities, but they are often assumed to be escapes. The distance from the northern African range limit to Portugal or Italy is approximately 2,500 km. In sum, three attempts at introduction are known in this species: Hispaniola, Réunion, and Mauritius. All of these were successful, although the Hispaniolan introduction is likely to have consisted of several events over a long period of time. One further naturalized population (Martinique) is of unknown origin. Establishment in Cape Verde, Venezuela, and Portugal is possible but not yet adequately documented. There are no known failed introductions of the Village Weaver, but escapes may have gone unnoticed. No single pattern of population growth characterizes the species in the several areas to which it has been introduced or spread. In the Mascarene Islands the populations have grown and spread steadily, whereas on Hispaniola the density remained low until a population boom and rapid spread occurred. On Martinique the population has grown but remained localized.

Commercial bird trade The cage bird trade is probably responsible for much of the Village Weaver’s existence outside of its native range; historical records indicate this method of introduction to the islands of Hispaniola, Mauritius, and Réunion over a century ago (WETMORE & SWALES, 1931; BARRÉ & BARAU, 1982; CHEKE, 1987). Data collected between 1974 and 1981 on annual exports of cage birds from Senegal, 13% of which were Ploceids, indicate France as the top importer. France, Spain, Belgium, Holland, Italy, and West Germany accounted for 75% of Senegal’s bird trade during that period. The United States was a rising market, overtaking France in 1980 (BRUGGERS, 1983). However, in the U. S. the Village Weaverbird in particular is said to be “seldom kept in captivity, mainly because of its aggressivity” (HIPP, 1988), and the captive populations that do exist are subject to legislated standards of confinement (BROSSET, 1985). In France the species has been reported to be common merchandise and susceptible to escape due to lack of restrictions (BROSSET, 1985). Some researchers believe that the Village Weaver’s recent establishment on the island of Martinique was due to recent bird trade (BARRÉ & BENITO–ESPINAL, 1985), whereas others see this species as one of several that may have been carried to the West Indies by storms from Africa (NORTON, 1989; WAVER, 1996). Given the nature of the Ploceid trade and the history of this species’ introductions and sightings, the southern United States, the West Indies to northern South America, and southwestern Europe might be considered the regions of most probable introduction.

Factors influencing introduction and invasion success The ecology and behavior of the Village Weaver were determined from the literature and from observations of natural populations in its natural and introduced ranges during 1999–2001 (see, e.g., LAHTI & LAHTI, 2002). These characteristics, along with habitat information from regions of most probable introduction, were compared with attributes of species and introduction sites that were found in recent reviews and quantitative studies to correlate with the likelihood of introduction success or invasiveness (table 1). Here "introduction" refers to population establishment, whereas "invasion" refers to spread beyond the local area of introduction (KOLAR & LODGE, 2001b). Both intrinsic and extrinsic factors were considered, in the sense of factors that respectively are or are not species–specific traits of the Village Weaver. In general the Village Weaver fits the characterization of a successfully introduced and invasive bird as described by recent studies (table 1). Of 14 factors found to correlate with introduc-

Lahti

Table 1. Factors correlated with introduction success and invasiveness in birds, and relation to the Village Weaverbird Ploceus cucullatus (VW). Factors in the first column exhibit a correlation with introduction or invasion success. In the second column, numbers following KL are the numbers of quantitative studies testing each factor (number of studies with a significant result / total number of studies), adapted from KOLAR & LODGE (2001b) and subsequent adjustments (based on SOL, 2001; KOLAR & LODGE, 2001a). These studies may not be independent tests of the hypotheses because four of the eight were of New Zealand birds. Other initials in the second column refer to the following studies: LMA. LOCKWOOD et al. (1993); C. CASE (1996); SMC. SORCI et al. (1998); MMS. MCLAIN et al. (1999); BD. BLACKBURN & DUNCAN (2001); STL. SOL et al. (2002). No two studies had significant results opposed to each other; 1 CASE (1996) actually measured number of native extinctions, but considered this a proxy for “degree of human activity and habitat destruction and deterioration…”. 2 LOCKWOOD et al. (1993) actually measured morphological overdispersion of introduced relative to native species, which they consider to be an indicator of competition. 3 Both of the two significant studies had mixed results (SOL, 2001). 4 BLACKBURN & DUNCAN (2001) actually measured latitudinal difference and proportion of introductions within the same biogeographic region as the source population, but considered these proxies for “climatic and habitat features”. 5 No quantitative study has tested whether successfully established or invasive exotic birds tend to become established or invasive in subsequent introductions as well. The factor is included here because of its plausibility (SIMBERLOFF & BOECKLEN, 1991; VERMEIJ, 1996). Tabla 1. Factores correlacionados con el éxito de la introducción y el carácter invasivo de las aves, y su relación con el tejedor Ploceus cucullatus (VW). Los factores indicados en la primera columna muestran correlación con el éxito de la introducción o invasión. En la segunda columna, los números que figuran a continuación de KL corresponden a estudios cuantitativos que verifican cada factor (número de estudios que ofrecen un resultado significativo / número total de estudios), adaptado de KOLAR & LODGE (2001b) y adaptaciones subsiguientes (según SOL, 2001; KOLAR & LODGE, 2001a). Es posible que dichos estudios no constituyan ensayos independientes de la hipótesis, dado que cuatro de los ocho estudios presentados corresponden a aves de Nueva Zelanda. Las otras iniciales de la segunda columna se refieren a los siguientes estudios: LMA. LOCKWOOD et al. (1993); C. CASE (1996); SMC. SORCI et al. (1998); MMS. MCLAIN et al. (1999); BD. BLACKBURN & DUNCAN (2001); STL. SOL et al. (2002). En ningún caso dos estudios ofrecen resultados significativos opuestos entre sí; 1 CASE (1966) midió en realidad el número de extinciones de especies nativas, pero la consideró una variable sustitutiva para el "grado de actividad humana y destrucción y deterioro del hábitat..."; 2 LOCKWOOD et al. (1993) midieron en realidad la sobredispersión morfológica de las especies introducidas con respecto a las especies nativas, al considerarla como un indicador de competencia; 3 Los dos estudios significativos obtienen resultados diversos (SOL, 2001); 4 BLACKBURN & DUNCAN (2001) midieron en realidad la diferencia de latitud y la proporción de introducciones en una misma región biogeográfica como la población de origen, pero lo consideraron como una variable sustitutiva para las "características climáticas y de hábitat"; 5 Ningún estudio cuantitativo ha comprobado si las aves exóticas establecidas o con éxito en su acción invasiva tienden a establecerse o convertirse en invasivas del mismo modo en introducciones subsiguientes. El factor está incluido aquí por su plausibilidad (SIMBERLOFF & BOECKLEN, 1991; VERMEIJ, 1996).

Studies

Consistent with VW?

Comments regarding probable influence on VW introduction and invasion success

More individuals released

KL 8/8

Introductions most likely from scapes, propagule size small

More introduction events

C, KL 5/7

yes

Several recent sightings in Europe and New World; active trade

Biogeographic region

yes/no Palearctic high success/Nearctic low (Caribbean intermediate)

More human activity1

yes

VW associates with human settlement and agriculture (see text)

Less intersp. competition2

LMA

Competitors widespread; but VW a fierce competitor (see text)

Extrinsic Factors Introduction success

Animal Biodiversity and Conservation 26.1 (2003)

Table 1. (Cont.)

Consistent Comments regarding probable influence on Studies with VW? VW introduction and invasion success Invasiveness More individuals released

KL 1/1

Introductions most likely from escapes, propagule size small

More introduction events

KL 1/1

yes

Several recent sightings in Europe and New World; active trade

Higher body mass

KL 2/53

VW small (mass 31–45 g) (MACLEAN, 1985)

Plumage monomorphism

MMS, no SMC, STL

VW conspicuously dimorphic

Lack of migration

KL 1/4

yes

VW not known to migrate (CROOK, 1963; ADEGOKE, 1983a; PARKER, 1999)

More broods per season

KL 1/2

yes

VW breeding season 3–12 months (CYRUS & ROBSON, 1980; BARRÉ & BARAU, 1982; CRAIG, 1997). Mean four breeding attempts in a 75–day period (DA CAMARA–SMEETS, 1982)

Higher nest site

MMS

yes

VW usually nests 2–15m high throughout range (pers. obs.)

Broader diet

MMS

yes

VW will eat seeds and insects (ADEGOKE, 1983a); will also eat fruit (pers. obs.)

Commensalism with humans

STL

yes

VW associates with human settlement and agriculture (see text)

Larger geographic range size

yes?

Introduced birds range from 0.25 to 68,625 degrees2, mean 1386 (T. M. Blackburn, pers. comm.). VW range ~3715 degrees2.

Better habitat/climate match

BD4, KL 1/1

yes

E.g., West Indies, southern U.S., and Mediterranean (see text)

yes

Established in three of three known introductions; but failed introduction events (escapes) may go unnoticed.

Intrinsic Factors Introduction success

Successful introduction history5

Invasiveness Presence of migration

KL 1/1

VW not known to migrate (CROOK, 1963; ADEGOKE, 1983a; PARKER, 1999)

Smaller body mass

KL 1/1

yes

VW small (mass 31–45 g) (MACLEAN, 1985)

Smaller egg mass

KL 1/1

yes

VW small (mass 2.3–3.6 g, N = 94 clutches)

Shorter juvenile period

KL 1/1

Juvenile period uncertain for VW

More broods per season

KL 1/1

yes

VW breeding season 3–12 months (CYRUS & ROBSON, 1980; BARRÉ & BARAU, 1982; CRAIG, 1997). Mean four breeding attempts in 75–day period (DA CAMARA–SMEETS, 1982)

Greater longevity

KL 1/1

Longevity uncertain for VW

Better habitat/climate match

KL 1/1

yes

E.g., West Indies, southern U.S. and Mediterranean (see text)

yes

Invasive in three of three known introductions; but at least one noninvasive naturalized population exists.

Successful invasion history5

tion success in birds, 11 are consistent with success of the Village Weaver, at least in some regions of probable introduction. Of eight factors correlated with invasiveness for which relevant information about the Village Weaver exists, six are consistent with the Village Weaver. Intrinsic factors strongly favor both introduction success and invasiveness. The only thorough exception to this is plumage dimorphism, although migratory behavior and body mass appear to have opposite effects on introduction success versus invasiveness. The contribution of extrinsic factors is more ambivalent. The pattern of introduction is likely to consist of common releases of a very small number of individuals, and the likelihood of success also varies with the region of introduction. Two factors whose contribution is complex will be described in more detail: habitat and climate match, and competition. Habitat and climate requirements Successful introductions are associated with similarity of habitat and climate between the area of introduction and that to which the bird species is adapted (KOLAR & LODGE, 2001b; BLACKBURN & DUNCAN, 2001). Although general indicators are quantitative and convenient, such as latitudinal differences and proportion of introductions in the same biogeographic region (BLACKBURN & DUNCAN, 2001), each bird species is likely to have particular habitat or climatic limitations. Among these can be elevation, ecoystem type, temperature, and precipitation. The Village Weaverbird is not usually found above 300 m in elevation (CHEKE, 1987; personal observation), although CLANCEY (1964) reports it to exist up to 1500 m in KwaZulu–Natal, South Africa. Its tendency to be a lowland bird is especially evident on volcanic islands to which it has been introduced, such as Mauritius where even irrigated agricultural fields on the central plateau were devoid of colonies in early 2001. Elevation is below 300 m in nearly all of the American southeast up to the Appalachians, and on several islands near Hispaniola, particularly Cuba. Large tracts of land exist within the Village Weaver’s accustomed elevation range in the western and southern portions of the Iberian peninsula. Italy, tends to be more mountainous, which suggests that a naturalized population of the Village Weaver there might be more localized. Landscapes converted from natural ecosystems to either development or agriculture are more likely to contain introduced birds (CASE, 1996). Village Weavers in particular exhibit diversity in their preference of ecosystem type. Their broad distribution in subsaharan Africa indicates the habitat generalism of this species (BATES, 1930). However, several generalizations hold throughout their range. On a local scale, they are most abundant near agricultural fields and water sources (B ANNERMAN , 1949; C YRUS & R OBSON , 1980;

Lahti

MACLEAN, 1985; RAFFAELE et al., 1998; LAHTI & LAHTI, 2002). The Village Weaver is particularly noted for its tendency to dwell among human habitations, from which it may gain some protection from predators (BATES, 1930; MOREAU, 1942; DA CAMARA– SMEETS, 1982; BARRÉ & BARAU, 1982; LAHTI et al., 2002). For example, BATES (1909) writes, “No sooner is a clearing made and stakes set in the ground for a new village than ‘Benga’a’ begin to build in the nearest tree…The more populous the village and the greater the hubbub of village life, the better are the birds pleased”. They avoid dense forests, although they can be found in small woodlots or forests open enough to permit grasses. Trees are preferred for nesting, although in areas of abundant food (e.g. near ricefields) they occasionally nest in shrubs or even herbaceous vegetation (personal observation). The Village Weaver’s preference for disturbed or agricultural lands is reflected in its reported range expansion in Africa over the last century, “due to the opening up of forests through increasing desiccation, fire, the relentless spread of human cultivation and the concomitant encroachment of savannah into what was previously homogenous forest land” (CROOK, 1963: 222). Based on these habitat preferences, the Village Weaver seems well suited to Cuba and much of the southeastern U.S. (especially Florida, whose land is almost completely converted to development or agriculture). By the same considerations the largely agricultural European countries of Spain and Portugal, as well as southern France and Italy, provide appropriate Village Weaver habitat (data obtained from USDA NRCS–NATURAL RESOURCES CONSERVATION SERVICE , 1992; SEI–S TOCKHOLM ENVIRONMENT INSTITUTE, 1999). The Village Weaver is a tropical to subtropical species, so temperature may be a factor governing its distribution. A comparison of the Village Weaver’s current global distribution with average annual temperatures and minimum annual temperatures of 30 cities in and near the bird’s range (NOAA–NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION, 1991) reveals that the Village Weaver tends to exist only near cities where the average annual temperature exceeds 20°C, and only where the minimum annual temperature is above 0°C. However, the Village Weaver has recently expanded its range into the vicinity of Gabarone, Botswana (PETERSEN, 1991; HERREMANS et al., 1994), where the minimum annual temperature does dip below freezing (–2°C in 2001). If temperature is a range–limiting factor in this species, various areas in the southern U.S.A. (southern half of Florida, south Texas, southwestern Arizona, and the coast of California), and the Caribbean Islands fit the weaver’s accustomed average and minimum annual temperature regime (CPC–CLIMATE PREDICTION CENTER, 2002). In general the coastal areas of Spain and Portugal, the southern coast of France, and portions of the Italian coast (particularly near the French border and in the south) are also warm enough. Much of

Animal Biodiversity and Conservation 26.1 (2003)

the interior of these countries, however, including Spain, dip readily below freezing. Nevertheless, an attitude of caution is still warranted in colder areas. The average annual temperature in Los Angeles, CA, U.S.A. is below 20°C, yet Village Weavers have survived for years in aviaries there with no climate control, exhibiting no apparent variation in behavior with temperature fluctuation, except for more resting at higher temperatures (COLLIAS et al., 1971). Moreover, temperature does not explain the absence of the weaver from many areas near its range which do have appropriate temperatures, such as much of Somalia, South Africa, and the northern Sahel. The length of the rainy season determines the length of the Village Weaver’s breeding season (DA CAMARA–SMEETS, 1982). In fact, in the moister areas of Africa they breed in every month of the year and the males might never molt into their nonbreeding plumage (CHAPIN, 1954). There is evidence that rain is important in initiating colonies, and partly also in establishing subsequent breeding synchrony within the colony (HALL, 1970). Not surprisingly, therefore, precipitation provides a more accurate indicator of the range of the Village Weaver than temperature. For instance, a map of the Village Weaver’s range in Africa coincides at all borders with a map of the areas which receive at least a millimeter of rain per day on annual average (GPCP–GLOBAL PRECIPITATION CLIMATOLOGY PROJECT, 2000). The precipitation contour explains, for instance, the Village Weaver’s range in Southern Africa, which skirts Namibia and most of Botswana and terminates in a finger curving along the eastern coast of South Africa. It also explains the weaver’s absence from the region of Somalia southeast of the Red Sea, as well as the drier latitudes of the continent north of about 15°N. Comparing this one mm/day rule with the regions of probable introduction, all of the areas fit this criterion except for the far west of Mexico and the United States. Captive Village Weavers, of course, may breed all summer regardless of rainfall if provided with food, water and nesting materials by caretakers (COLLIAS & COLLIAS, 1970). Likewise, in the uncommon case in nature where a dependable food and water supply and drought–resistant vegetation persist despite a lack of rainfall, Village Weavers may breed where they would not otherwise be expected. For example, in the Dominican Republic in V–VI 2001, weavers were observed breeding in large colonies in the northwestern desert, where the watercourses were completely dry and where no rain fell for at least a month, but where juicy cactus fruits were available and regularly consumed (personal observation). Several areas of Europe and North America, then, in addition to the Caribbean, apparently provide appropriate climate and habitat for the Village Weaver, according to comparisons of elevation, ecosystem type, temperature and precipitation. Specifically, Florida and the Gulf Coast, much of Portugal, lowlying areas of Spain, southern France, and the northwestern and southern coastal areas of Italy fit the Village Weaver’s

current range in all these respects. Moving inland or northward from these areas tends to compromise one or more of the factors. Competition Evidence suggests that competition with other introduced species may affect introduction success (LOCKWOOD et al., 1993). This is difficult to test adequately (SIMBERLOFF & BOECKLEN, 1991), and is likewise difficult to assess for any given species or region of probable introduction. With regard to the Village Weaver in particular, introduction success in the Mascarenes in the 1880’s would have been considered unlikely according to the competition hypothesis, due to the high numbers of introduced species that already existed on those islands (MOULTON et al., 1996). Despite competition, and despite a small propagule size, both introductions succeeded. Nevertheless, Village Weavers may yet encounter and be affected by competitors whose effects on their population size and invasiveness are difficult to predict. The Village Weaver forms large foraging flocks and nesting colonies, and is often involved in synchronized competitive actions such as displacing other bird species in foraging areas and mobbing intruders near and within colonies (personal observation). Individually also they are aggressive, appropriately called “chasers and fighters” in one study (DIN, 1992). The individual sighted in North Carolina was observed supplanting a Boat–tailed Grackle (Quiscalus major), a species over twice as long, at a feeder (HIPP, 1988). Together with its compact and enclosed nest structure, aggression in this species functions as a defense against enemies such as brood parasites or predators (COLLIAS & COLLIAS, 1964; MACDONALD, 1980; DIN, 1992). These aggressive or competitive characteristics of the Village Weaver may function to enhance its establishment and population growth in new areas.

Agricultural pest status The extent of concern due to a potential invasive species and the necessity for proactivity depend not only on the species’ likelihood of establishment and spread, but also on its probable ecological or environmental impact. The Village Weaver’s habits of nesting in raucous colonies and denuding the vegetation have been troublesome in Africa (BATES, 1930; CHAPIN, 1954; personal observation). There are also likely to be ecological effects of invasion that do not directly affect human economies. However, by far the most important and immediate concern in areas with Village Weaver populations is the effect of the bird’s foraging in agricultural areas. From the earliest accounts of its behavior the species has been known as a destroyer of cereal crops in Africa (BATES, 1909; 1930) and Réunion (BERLIOZ, 1946). Recent accounts of

Lahti

Table 2. Expected ratings of concern for invasion, according to the Smallwood–Salmon Rating System (SMALLWOOD & SALMON 1992). Values in the interior of the table range from 0 to 1, with a high score representing a high rating of concern in the respective area. Total values (bottom row) range from 9 to 27, with high scores denoting species of generally high concern as invaders. Other known invasive species are provided for comparison with the Village Weaver. Tabla 2.. Índices de preocupación previstos con respecto a la invasión, según el sistema de valoración de Smallwood–Salmon (SMALLWOOD & SALMON 1992). Los valores incluidos en la tabla oscilan entre 0 y 1, donde una puntuación alta representa un alto índice de preocupación en el área respectiva. Los valores totales (fila inferior) oscilan entre 9 y 27, refiriéndose las puntuaciones altas a especies que sugieren una alta preocupación en términos de invasión. También se facilitan otras especies invasoras conocidas, a efectos de establecer una comparación con el tejedor.

Village Weaver

Pig

House Mouse

Monk Parakeet

House Sparrow

Starling

Quelea

Introduction

0.6

0.82

0.93

0.89

0.64

0.57

0.37

Establishment

0.75

0.25

Damage

0.75

0.89

0.84

0.64

0.66

0.81

0.72

Uncontrollability

0.84

0.43

0.41

0.54

0.41

0.84

Total rating

the species in both its native and introduced ranges nearly always mention the damage it causes to local agriculture (e.g., JENSEN & KIRKEBY, 1980; MICHEL, 1992; RAFFAELE et al., 1998). This dietary preference has been supported by analysis of stomach contents, mainly in West Africa (CHAPIN, 1954; ADEGOKE, 1983a; MANIKOWSKI, 1984; personal observation). A recent survey of more than sixty evaluations of crop damage due to birds in West Africa has concluded that the Village Weaver is in some areas the single worst avian pest, and takes second place in the region as a whole, after the Red–billed Quelea (MANIKOWSKI, 1984). It is the biggest threat to agriculture in The Gambia, where a third of some farmers’ rice crops have been destroyed (LAHTI & LAHTI, 2000). It has also been called the worst avian pest in Mauritius (BARRÉ & BARAU, 1982), and in Haiti, where losses of 20– 35% to rice are sustained because of this species (BRUGGERS, 1983). An adult consumes on average 250 g of cultivated seeds in 30 days; one thousand birds therefore consume a third of the production of a typical Chadian field of sorghum in one month (DA CAMARA–SMEETS, 1981). An exception is South Africa, where the species is not considered a major pest (CRAIG, 1997). There are also regions such as central Uganda where weaver damage to crops has been relatively light (KASOMA, 1987). Determining the correlates of such variation in crop damage could provide a basis on which to predict its probable impact in new areas. For instance, neither central Uganda nor eastern South Africa raise rice or similarly sized grains as a major crop, whereas a study in Nigeria found that rice was the most

significant element in the bird’s diet when available (ADEGOKE, 1983a). In fact, consistent availability of suitable grains, especially in the breeding season, is suggested to be the factor limiting the size of Village Weaver populations, and in turn, agricultural damage (DA CAMARA–SMEETS & MANIKOWSKI, 1981; ADEGOKE, 1983a).

Smallwood–Salmon rating system SMALLWOOD & SALMON (1992) developed a rating system for invasive species which has been used to corroborate California’s "most unwanted exotic species" list. The system utilizes questions about a species’ invasive history and environmental impact to derive a series of values between 0 and 1 which estimate the relative probability of introduction, establishment, damage, and resistance to control methods. The Village Weaver’s scores place it among the most dangerous invasive species, having the maximum total score of 27 (table 2). These values, bolstered with the results of the application of recent studies, permit some bold suggestions. The Village Weaver may be predicted to have the Red–billed Quelea’s (Quelea quelea) resistance to control, yet nearer to the Starling’s (Sturnus vulgaris) ease of introduction and establishment. No other exotic bird or mammal species in or near North America has this combination of strengths according to this rating system (SMALLWOOD & SALMON, 1992). The rating system has not yet been applied in the literature to many species in or near other regions. The rating system’s final score results from a double weighting of establishment, and a triple

Animal Biodiversity and Conservation 26.1 (2003)

weighting of damage and uncontrollability. Therefore, the post–invasion impact of the species, regardless of its likelihood of introduction or invasion, is responsible for two thirds of the final score. Since the weaverbird is such a pest in its native range, the system may have inflated the invasiveness potential of this species on that basis. If an effective method were developed for control of the species, the adjustment to the final score would decrease it to 24. Nevertheless, the system is robust to changes in certain parameters: if the questions were answered such that the weaverbird was estimated to be two–thirds as damaging, or half as uncontrollable, the final score would not change.

population growth, than others; it can also aid in maximizing efficiency of control methods in the event that they are required. Recall, however, that the provision of water and other resources to the weavers (e.g., by humans) can lead to an extension of their breeding season despite a lack of rain (COLLIAS & COLLIAS, 1970). Much has been written on the pest status and control prospects of the top African bird pest, the Red–billed Quelea (e.g. MANYANZA, 1983; ALLAN, 1983; BRUGGERS & ELLIOTT, 1989). Since this species has similar behaviors and agricultural impacts to the Village Weaver, building upon this research base and appropriating its results may aid in preparedness and control efforts for the more invasive Village Weaver.

Suggestions for prevention and control Acknowledgments In light of the agricultural impact of the Village Weaver and its likelihood of invasion, proactive measures seem in order. Regulating the international trade of these birds is probably the best strategy (BROSSET, 1985). Control methods such as fire, scarecrows, rattles, shooting, nest–robbing, and the felling of trees have not met with much success in Africa, the Mascarenes, or Hispaniola. Poison has been too expensive for most areas and is at best temporary anyway since local birds are responsible for most agricultural damage, and roaming populations can quickly fill in the gaps created by culls (LONG, 1981; ADEGOKE, 1983b). Matters do not seem to have improved in this respect since BATES (1909: 44) noted that “the number killed by man does not seem to affect the population of the colonies. Killing numbers of them will not frighten them away, and tearing down their nests only makes them build the more furiously.” The introduction history of this species suggests that, even where there is a population boom, there is a preceding period of lag (SAKAI et al., 2001) where population sizes are low and probably more manageable. Therefore, in areas where new breeding colonies are reported, proactive control methods, perhaps including removal of the population, may be advisable. Given the Village Weaver’s reliance on rain, those concerned with invasion might use rainfall and breeding season data from the species’ current range to predict breeding seasons in new areas. For instance, Portugal receives very little rain between June and September, so Village Weavers introduced to that country will not be likely to breed during that time period. In general the one mm/day rule that on an average annual basis accords well with the species’ range, also broadly matches the bird’s breeding season when calculated on an average monthly basis (GPCP–G L O B A L P R E C I P I TAT I O N C L I M AT O L O G Y PROJECT, 2000). This information can be useful in predicting what areas are likely to have longer breeding seasons, and therefore perhaps higher

For aid in research and the formation of ideas I thank April R. Lahti and Robert B. Payne. For helpful comments I am grateful to Shannon Bouton, John Carroll, Beverly Rathcke, Sheila Schueller, Lindsay Whitlow, and an anonymous referee. Personal communications cited in this article were received from Tim M. Blackburn (School of Biosciences, University of Birmingham, Birmingham, U.K.), Robin Restall (Phelps Ornithological Collection, Caracas, Venezuela), and James W. Wiley (Maryland Cooperative Fish and Wildlife Research Unit, University of Maryland Eastern Shore, Princess Anne, MD, U.S.A.).

References ADEGOKE, A. S., 1983a. Diet of the village weaver Ploceus cucullatus. Malimbus, 5: 79–89. – 1983b. The pattern of migration of village weaverbirds (Ploceus cucullatus) in southwestern Nigeria. Auk, 100: 863–870. ALLAN, R., 1983. The strategy for protecting crops from the depredations of quelea birds in Kenya. In: Proceedings of the Ninth Bird Control Seminar: 307–316. Bowling Green State University, Bowling Green, OH. BANNERMAN, D. A., 1949. The Birds of Tropical West Africa, Volume 7. Oliver and Boyd, Edinburgh. BARLOW, C., WACHER, T. & DISLEY, T., 1997. A Field Guide to the Birds of The Gambia and Senegal. Pica Books, Mountfield, U.K. BARRÉ, N. & BARAU, A., 1982. Oiseaux de la Réunion. Imprimerie Arts Graphiques Modernes, St. Denis, France. BARRÉ, N. & BENITO–ESPINAL, E., 1985. Oiseaux granivores exotiques implantés en Guadeloupe, á Marie–Galante et en Martinique (Antilles françaises). L’Oiseau et la Revue Française d’Ornithologie, 55: 235–241. BATES, G. L., 1909. Field–notes on the birds of southern Kamerun, West Africa. Ibis, 3 (9th

Series): 1–74. – 1930. Handbook of the Birds of West Africa. John Bale, Sons, & Danielsson, London. BERLIOZ, J., 1946. Oiseaux de la Réunion. Librarie La Rose, Paris. BLACKBURN, T. M. & DUNCAN, R. P., 2001. Determinants of establishment success in introduced birds. Nature, 414: 195–197. BOND, J., 1936. Birds of the West Indies. The Academy of Natural Sciences of Philadelphia, Philadelphia, PA. BROSSET, A., 1985. Construction de nids par an Tisserin gendarme (Ploceus cucullatus) sur l'Etang de Saclay (France). Alauda, 53: 231. BRUGGERS, R. L., 1983. Senegal’s trade in cage birds. In: Proceedings of the Ninth Bird Control Seminar: 321–323Ed.) Bowling Green State University, Bowling Green, OH. BRUGGERS, R. L. & ELLIOTT, C. C. H., 1989. Quelea quelea: Africa’s Bird Pest. Oxford University Press, Oxford. CASE, T. J., 1996. Global patterns in the establishment and distribution of exotic birds. Biological Conservation, 78: 69–96. CHAPIN, J. P., 1954. The Birds of the Belgian Congo, part 4. American Museum of Natural History Bulletin, 75. CHEKE, A. S., 1987. An ecological history of the Mascarene Islands, with particular reference to extinctions and introductions of land vertebrates. In: Studies of Mascarene Island Birds: 5–89 (A. W. Diamond, Ed.) Cambridge University Press, Cambridge, U.K. CLANCEY, P. A., 1964. The Birds of Natal and Zululand. Oliver and Boyd, Edinburgh. COLLIAS, N. E. & COLLIAS, E. C., 1964. Evolution of nest–building in the weaverbirds (Ploceidae). University of California Publications in Zoology, 73: 1–239. – 1970. The behavior of the West African village weaverbird. Ibis, 112: 457–480. – 1971. Comparative behaviour of West African and South African subspecies of Ploceus cucullatus. Ostrich, Supplement 9: 41–52. COLLIAS, N. E., VICTORIA, J. K., COUTLEE, E. L. & GRAHAM, M., 1971. Some observations on behavioral energetics in the village weaverbird II. All–day watches in an aviary. Auk, 88: 133–143. CPC (CLIMATE PREDICTION CENTER), 2002. Regional Climate Maps: Ed.) National Center for Environmental Prediction (NCEP), National Weather Service (NWS), and National Oceanic and Atmospheric Administration (NOAA), Washington, D.C., U. S. A. CRAIG, A. J. F. K., 1997. Spottedbacked Weaver. In: The Atlas of Southern African Birds, vol. 2: 554–555 (J. A. Harrison, D. G. Allan, L. G. Underhill, M. Herremans, A. J. Tree, V. Parker & C. J. Brown, Eds.) BirdLife South Africa, Johannesburg, South Africa. CRAMP, S. & PERRINS, C. M. (Eds.), 1994. Handbook of the Birds of Europe, the Middle East and North Africa, vol. 8. Oxford University Press, Oxford.

Lahti

CROOK, J. H., 1963. Comparative studies on the reproductive behaviour of two closely related weaver bird species (Ploceus cucullatus and Ploceus nigerrimus) and their races. Behaviour, 21: 177–232. CYRUS, D. & ROBSON, N., 1980. Bird Atlas of Natal. University of Natal Press, Pietermaritzburg, South Africa. DA CAMARA–SMEETS, M., 1981. Les bilans énergétiques pendant la reproduction du tisserin gendarme, Ploceus cucullatus. Nature et importance des prélèvements sur le milieu. Gerfaut, 71: 415–431. – 1982. Nesting of the village weaver Ploceus cucullatus. Ibis, 124: 241–251. DA CAMARA–SMEETS, M. & MANIKOWSKI, S., 1981. Preferences alimentaires de Ploceus cucullatus au Tchad. Malimbus, 3: 41–48. DIN, N. A., 1992. Hatching synchronization and polymorphism in the eggs of Ploceus cucullatus and P. nigerrimus with data on nest parasitism. African Journal of Ecology, 30: 252–260. ELTON, C. S., 1958. The Ecology of Invasion by Plants and Animals. Methuen, London. ENSERINK, M., 1999. Biological invaders sweep in. Science, 285: 1834–1836. GPCP (GLOBAL PRECIPITATION CLIMATOLOGY PROJECT), 2000. GPCP Color Precipitation Maps. World Data Centre for Meterology, National Climatic Data Center (NCDC), Asheville, N.C., U.S.A. HALL, B. P. & MOREAU, R. E., 1970. An Atlas of Speciation in African Passerine Birds. Trustees of the British Museum (Natural History), London. HALL, J. R., 1970. Synchrony and social stimulation in colonies of the blackheaded weaver Ploceus cucullatus and Veillot’s black weaver Melanopteryx nigerrimus. Ibis, 112: 93–104. HAZEVOET, C. J., 1995. The Birds of the Cape Verde Islands. British Ornithological Union, Tring, U.K. HERREMANS, M., BORELLO, W. & HERREMANS–TONNOEYR, D., 1994. New cases of the spottedbacked weaver Ploceus cucullatus breeding near Gaborone. Babbler, 26–27: 29–30. HIPP, J., 1988. Village weaver photographed on Seabrook Island, S. C. Chat, 52: 81. JENSEN, J. V. & KIRKEBY, J., 1980. The Birds of the Gambia. Aros Nature Guides, Arhus, Denmark. JONES, C., 1996. Bird introductions to Mauritius: status and relationships with native birds. In: The Introduction and Naturalisation of Birds: 113–123 (J. S. Holmes & J. R. Simons, Eds.) HMSO, London. KASOMA, P. M. B., 1987. Is the black–headed weaver a pest? African Journal of Ecology, 25: 107–116. KOLAR, C. S. & LODGE, D. M., 2001a. Predicting invaders: Response from Kolar and Lodge. Trends in Ecology & Evolution, 10: 546. – 2001b. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution, 16: 199–204. LAHTI, D. C. & LAHTI, A. R., 2000. The village weaverbird: A common bird of uncommonly great concern. In: Daily Observer: 11. Banjul, The Gambia.

Animal Biodiversity and Conservation 26.1 (2003)

– 2002. How precise is egg discrimination in weaverbirds? Animal Behaviour, 63: 1,135–1,142. LAHTI, D. C., LAHTI, A. R. & DAMPHA, M., 2002. Nesting associations of the village weaver (Ploceus cucullatus) with other animal species in The Gambia. Ostrich, 73: 59–60. LE MARÉCHAL, P., 1985. Construction de nids par un Tisserin gendarme (Ploceus cucullatus) sur l’Etang de Saclay (France). Alauda, 53: 228–231. LEVER, C., 1987. Naturalized Birds of the World. Longman Scientific & Technical, Harlow, England. LOCKWOOD, J. L., MOULTON, M. P. & ANDERSON, S. K., 1993. Morphological assortment and the assembly of communities of introduced passeriforms on oceanic islands: Tahiti versus Oahu. American Naturalist, 141: 398–408. LONG, J. L., 1981. Introduced Birds of the World. Universe Books, New York. MACDONALD, M. A., 1980. Observations on the diederik cuckoo in southern Ghana. Ostrich, 51: 75–9. MACLEAN, G. L., 1985. Roberts’ Birds of Southern Africa, 5th edition. Trustees of John Voelcker Bird Book Fund, Cape Town, South Africa. – 1993. Roberts’ Birds of Southern Africa, 6th edition. Trustees of John Voelcker Bird Book Fund, Cape Town, South Africa. MANIKOWSKI, S., 1984. Birds injurious to crops in West Africa. Tropical Pest Management, 30: 379–387. MANYANZA, D. N., 1983. Quelea control operations in Tanzania. In: Proceedings of the Ninth Bird Control Seminar: 317–320. Bowling Green State University, Bowling Green, OH. MAYR, E. & GREENWAY, J. C. JR. (Eds.), 1962. Check– ist of Birds of the World, vol. 15. Museum of Comparative Zoology, Cambridge, MA. MCLAIN, D. K., MOULTON, M. P. & SANDERSON, J. G., 1999. Sexual selection and extinction: the fate of plumage–dimorphic and plumage–monomorphic birds introduced onto islands. Evolutionary Ecology Research, 1: 549–565. MICHEL, C., 1992. Birds of Mauritius, 3rd edition. Editions de l’Ocean Indien, Rose Hill, Mauritius. MOREAU, R. E., 1942. The nesting of African birds in association with other living things. Ibis, 6 (14th Series): 240–263. MOULTON, M. P., SANDERSON, J. G. & SIMBERLOFF, D., 1996. Passeriform introductions to the Mascarenes (Indian Ocean): An assessment of the role of competition. Ecologie, 27: 143–152. NAUROIS, R. D., 1994. Les Oiseaux des Iles du Golfe de Guinee. Instituto de Investigação Científica Tropical, Lisbon, Portugal. NOAA (NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION), 1991. Climates of the World. National Climatic Data Center, Asheville, N.C., U.S.A. NORTON, R. L., 1989. West Indies region. American Birds, 43: 174–175. PARKER, V., 1999. The Atlas of the Birds of Sul do

Save, Southern Mozambique. Avian Demography Unit and Endangered Wildlife Trust, Cape Town and Johannesburg, South Africa. P ETERSEN, S. E., 1991. Spottedbacked Weaver Ploceus cucullatus breeding at Gaborone Dam. Babbler, 21–22: 74–76. P EZZO, F. & MORELLINI, M., 1999. Breeding attempt of the village weaver, Ploceus cucullatus, at Montepulciano Lake (Sienna, central Italy). Rivista Italiana di Ornitologia, 69: 142–145. PINCHON, R. & BENITO–ESPINAL, E., 1980. Installation de nouvelles espèces à la Martinique. L’Oiseau et la Revue Française d’Ornithologie, 50: 347–348. RAFFAELE, H., WILEY, J., GARRIDO, O., KEITH, A. & RAFFAELE, J., 1998. Birds of the West Indies. Christopher Helm, London. SAKAI, A. K., ALLENDORF, F. W., HOLT, J. S., LODGE, D. M., MOLOFSKY, J., WITH, K. A., BAUGHMAN, S., CABIN, R. J., COHEN, J. E., ELLSTRAND, N. C., MCCAULEY, D. E., O’NEIL, P., PARKER, I. M., THOMPSON, J. N. & WELLER, S. G., 2001. The population biology of invasive species. Annual Review of Ecology and Systematics, 32: 305–332. SEI (S TOCKHOLM E NVIRONMENT I NSTITUTE ), 1999. Land Cover Map of Europe. University of York, York, U.K. SIMBERLOFF, D., 1992. Extinction, survival, and effects of birds introduced to the Mascarenes. Acta Oecologica, 13: 663–678. SIMBERLOFF, D. & BOECKLEN, W., 1991. Patterns of extinction in the introduced Hawaiian avifauna: a reexamination of the role of competition. American Naturalist, 138: 300–327. SMALLWOOD, K. S. & SALMON, T. P., 1992. A rating system for potential exotic bird and mammal pests. Biological Conservation, 62: 149–159. SOL, D., 2001. Predicting invaders. Trends in Ecology & Evolution, 16: 544. SOL, D., TIMMERMANS, S. & LEFEBVRE, L., 2002. Behavioural flexibility and invasion success in birds. Animal Behaviour, 63: 495–502. SORCI, G., MØLLER, A. P. & CLOBERT, J. 1998. Plumage dichromatism of birds predicts introduction success in New Zealand. Oikos, 90: 599–605. USDA NRCS (NATURAL RESOURCES C ONSERVATION S ERVICE), 1992. Dominant Cover/Use Types. Natural Resources Inventory (NRI), Washington, D.C. VERMEIJ, G. J., 1996. An agenda for invasion biology. Biological Conservation, 78: 3–9. WAVER, R. H., 1996. A Birder’s West Indies: An Island–by–Island Tour. University of Texas Press, Austin. WETMORE, A. & SWALES, B. H., 1931. The birds of Haiti and the Dominican Republic. U.S. Museum of Natural History Bulletin, 155: 1–459. WILLIAMSON, M. H., 1996. Biological Invasions. Chapman and Hall, London.

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 26.1 (2003)

An indirect assessment of the effects of oil pollution on the diversity and functioning of turtle communities in the Niger Delta, Nigeria L. Luiselli & G. C. Akani

Luiselli, L. & Akani, G. C., 2002. An indirect assessment of the effects of oil pollution on the diversity and functioning of turtle communities in the Niger Delta, Nigeria. Animal Biodiversity and Conservation, 26.1: 57–65.

Abstract An indirect assessment of the effects of oil pollution on the diversity and functioning of turtle communities in the Niger Delta, Nigeria.— There are many documented cases of oil spillage in the Niger Delta region, southern Nigeria (West Africa). Due to both habitat characteristics and omnivorous habits, the freshwater turtles are important vertebrates species in the trophic chain. They are therefore considered to play a significant role as ecological indicators for areas subjected to oil spillage events. The aim of this study was to evaluate the effects of oil spillage and consequent pollution on the abundance, complexity and functioning of freshwater turtle communities of the Niger Delta, by comparing the turtle fauna found in two areas with similar environmental characteristics, one unpolluted and the other polluted by a case of oil spillage in 1988. A total of 510 turtle specimens belonging to four different species (Trionyx triunguis, Pelusios castaneus, Pelusios niger, and Pelomedusa subrufa) were captured in the unpolluted area, whereas 88 specimens, from two different species (P. castaneus and P. niger) were captured in the polluted area. The dominant species was P. castaneus followed by P. niger in the unpolluted area, and P. niger in the polluted area. A marked shift in habitat use was observed in one species (P. niger) after the oil spillage event. This study revealed both direct and indirect effects of oil pollution on the complexity and habitat use of Nigerian freshwater communities of turtles. The main direct effect was a considerable reduction in the specific diversity of the turtles; 50% of species were lost after oil spillage and there was a very strong decline in the numbers of turtle specimens also for those species which were able to survive the catastrophic pollution event. The shift in habitat use after oil spillage by P. niger may have a significant effect on the long–term persistence of this species, independently of the pollution effects of the oil spillage event, because it considerably reduced habitat niche separation between this species and the closely related P. castaneus, a potential competitor. It is therefore stressed that eco–ethological modifications in populations of animals subjected to catastrophic events such as oil pollution should be taken into account when evaluating the long–term effects of these devastating phenomena. Key words: Turtles, Community ecology, Habitat, Pollution, Oil industry, Tropical, Nigeria. Resumen Evaluación indirecta de los efectos de la contaminación por petróleo en la diversidad y funcionamiento de las comunidades de tortugas del delta del Níger, Nigeria.— Existen numerosos casos documentados de vertidos de petróleo en la región del delta del Níger, al sur de Nigeria (África Occidental). Tanto por las características del hábitat como por sus costumbres omnívoras, las tortugas de agua dulce constituyen importantes especies de vertebrados en la cadena trófica. Por consiguiente, se considera que desempeñan un papel fundamental como indicadores ecológicos en las áreas sujetas a vertidos de petróleo. El presente estudio tiene por objeto evaluar los efectos de los vertidos de petróleo y la consiguiente contaminación en la abundancia, complejidad y funcionamiento de las comunidades de tortugas de agua dulce del delta del Níger. Para ello se han comparado con las especies de tortugas halladas en dos áreas con características medioambientales muy similares, una no contaminada y la otra contaminada, tras un caso de vertido de petróleo en 1998. En el área no contaminada se capturaron un total de 510 de ejemplares de tortugas pertenecientes a cuatro especies distintas (Trionyx triunguis, Pelusios castaneus, Pelusios niger y Pelomedusa subrufa), mientras que en el área ISSN: 1578–665X

Luiselli & Akani

contaminada se capturaron 88 ejemplares procedentes de dos especies (P. castaneus y P. niger). La especie dominante en el área no contaminada fue P. castaneus, seguida de P. niger, y en el área contaminada fue P. niger. En una de las especies (P. niger) se observó un pronunciado cambio en el uso del hábitat tras el vertido de petróleo. Este estudio revela los efectos directos e indirectos de la contaminación por petróleo en la complejidad y uso del hábitat de las comunidades de tortugas de agua dulce de Nigeria. El principal efecto fue una considerable reducción en la diversidad específica de las tortugas; el 50% de las especies se perdieron, produciéndose una importante disminución en el número de ejemplares de las especies que lograron sobrevivir a la catastrófica contaminación. Es posible que el cambio en el uso del hábitat experimentado por P. niger repercuta de forma significativa en la persistencia a largo plazo de esta especie, con independencia de los efectos de la contaminación provocada por el vertido de petróleo, puesto que se redujo considerablemente la separación del nicho ecológico entre esta especie y otra especie estrechamente relacionada con ella y posible competidora, P. castaneus. Por consiguiente, se destaca el hecho de que para evaluar los efectos a largo plazo de fenómenos tan devastadores como los causados por los vertidos de petróleo y la subsiguiente contaminación, habría que tener en cuenta las modificaciones ecoetológicas generadas en poblaciones de animales sometidas a episodios catastróficos. Palabras clave: Tortugas, Ecología de comunidades, Hábitat, Contaminación, Industria petrolera, Trópico, Nigeria. (Received: 26 VII 02; Conditional acceptance: 4 XI 02; Final acceptance: 4 XII 02) Luca Luiselli, F. I. Z. V. (Ecology), Via Olona 7, I–00198 Rome, Italy. G. C. Akani, Dept. of Biological Sciences, Rivers State Univ. of Science and Technology, P. M. B. 5080, Port Harcourt (Rivers State), Nigeria. Corresponding author: L. Luiselli. E–mail: lucamlu@tin.it

Animal Biodiversity and Conservation 26.1 (2003)

Introduction With a crude oil production of 2.04 mb/d, the Federal Republic of Nigeria is an Oil Producers Economic Community (OPEC) country, and is the main oil producer country in sub–Saharan Africa. Most of the oil–related industry of Nigeria is found in the Niger Delta region (DE MONTCLOS, 1994; EMBASSY OF NIGERIA, 2001). Natural environments of crucial ecological relevance such as swamp–rainforest and large portions of mangrove forest, as well as many endemic species of divergent faunal and floral groups (KINGDON, 1990), are found within the Niger Delta region. There is no doubt that the oil–related industry may be a prominent cause of habitat loss and a threat to the conservation of many important plant and animal species. Therefore, the impact of oil–related industries on the natural ecosystems of Niger Delta merits careful research. However, the constant friction between the main oil companies operating in the region and the local inhabitants has led to chronic civil instability which in turn has caused further political problems. For example, at the time of Ken Saro Wiva’s execution by the military regime of the late General Sani Abacha (1995) [Ken Saro Wiva was an internationally famous Nigerian writer who defended the opinion of the Niger Delta inhabitants (mainly the Ogoni tribe) who claimed they were the rightful owners of the crude oil. The Federal Government was accused of stealing their oil to sell to companies (Agip, Shell, ExxonMobil, etc). The late General Abacha ordered the execution of Ken Saro Wiwa and youth groups protested by destroying pipelines, causing significant economic loss to the oil companies] demonstrators broke oil pipelines to steal crude oil and petroleum, frequently causing oil spillage and pollution. As for cases of oil spillage, the "Niger Delta Environmental Survey" (NDES, 1998) and environmentalists such as ODU et al. (1989) have documented evidence of oil spillage in the region, especially in mangrove zones with brackish water rivers. The following cases are examples of temporal constancy of spillage events, which may have adversely affected the ecosystems and ecological biodiversity of the Niger Delta region: Bonny oil spillage (1993; brackish water), Rumuekpe oil spillage (1995; freshwater swamp), Bille oil spillage (early July, 2000; brackish water, with over 250,000 barrels lost), and the Ogbodo–Isiokpo oil spill (2001; freshwater stream). Unfortunately, many other spillage events have occurred and their impact on the fragile ecosystem of the region has not yet been documented. Despite previous studies on the effects of oil spillage on natural ecosystems and their plant and animal communities, no scientific research is available for the Niger Delta other than relatively terse comments available in local grey literature [mainly Environmental Impact Assessment (EIA) studies conducted by local industries].

Due to both habitat characteristics and omnivorous habits, the freshwater turtles are important vertebrates species in the trophic chain (AKANI et al., 2001). They are therefore considered to be significant ecological indicators for areas subjected to oil spillage events. In this regard, it is unfortunate that chelonians have not been popular subjects for community ecology studies (e.g., TOFT, 1985). Little is known on the organisation of their communities or assemblages of species (but see WILLIAMS & CHRISTIANSEN, 1981; VOGT & GUZMAN, 1988; MOLL, 1990; STONE et al., 1993; TERAN et al., 1995; KENNETT & TORY, 1996; ALLANSON & GEORGES, 1999; PRITCHARD, 2001). The aim of this study was to evaluate the effects of oil spillage and consequent pollution on the abundance, complexity and functioning of freshwater turtle communities in the Niger Delta. The methodology compares two very close turtle communities (a polluted area and a non–polluted area) with very similar ecological conditions. In particular, in the above–mentioned comparative approach, the following issues were addressed: 1. Is there any loss in terms of specific turtle diversity and abundance after oil spillage events? 2. Is there any species–specific change in habitat selection after oil spillage events? If so, which habitats are favoured by surviving turtle populations?

Materials and methods Study areas Two study areas were used for our comparisons, both with similar environmental conditions (i.e. a main river tract with banks covered by dense gallery forest, and with seasonal swamps into the riverine forest, and almost permanent marshes with rich aquatic vegetation). Among the plant species found in both areas, we may cite Pterocarpus sp., Raphia sp., Triumphetta eriophlebia, Mitragyna stipulosa, Triplichiton scleroxylon, Khaya sp., Terminalia superba, Mitragyna ciliata, and others. The linear distance between the two areas was approximately 20 km. Both areas presented very similar surfaces (1 km of main river tract with its forested banks), to avoid eventual differences in terms of the numbers of observed specimens being caused by a different surface surveyed. Both study areas appeared to have adequate micro–habitats (i.e. forested banks, spots with rich aquatic vegetation, and a number of basking sites) to house rich populations of semiaquatic chelonians. Unpolluted area The unpolluted study area was situated along a tributary of Sambreiro River (Rivers State), approximately 7 km east of Degema town (Kula,

Luiselli & Akani

Degema Local Government Area). There is no data about the water volumes of this site. This area was characterized by a portion of shallow, lentic, seasonally flooded, galloping swamp forest with several mounds, and by a deeper river with forested banks. Polluted area The polluted study area was situated along Sakie Stream and Baki Creek (Bayelsa State), where a well–known case of oil spillage had occurred. On January 27th, 1988, a spillage of crude oil (estimated at about 1,026 barrels) was detected along the Nun River delivery line of Shell Petroleum Developmental Company. This was the result of a pipeline burst caused by an internal tear. The oil flowed down an area of seasonally flooded galloping swamp forest (Sakie Stream) into the Baki Creek which links up to the Nun River into Igeibiri Creek during the rainy season (ODU et al., 1989). There are no data about the water volumes of the Sakie stream and Baki Creek. The Sakie stream is a shallow, lentic, seasonally flooded, galloping swamp forest with several mounds. Baki Creek, on the other hand, is deeper and tidal. According to ODU et al. (1989) report, oil pollution affected the galloping forest to a width of about 12–25 m and a length of about 350 m. Only the bottom sediment of the Baki Creek was affected but not the banks, while the banks of Eniwari Creek and aspects of Igeibiri Creek were oiled. The vegetation affected was heterogeneous and consisted of broad leaved, tall trees like Mitragyna stipulosa, Harungana madagascariensis, Atiopicus communis, Musanga cercopoides, Eupatorium odoratus, Costus afer, Alchornea sp., Triumphetta eriophlebia, etc, all characteristic of freshwater swamp. In Baki Creek the damaged vegetation was predominantly mangrove, dominated by Rhizophora racemosa and Avicennia africana. Around Igeibiri Creek some fallow species showed chlorotic symptoms, and phytoplankton abundance and productivity as well as a number of benthic organisms were adversely affected in the high and impacted areas of the galloping forest as well as the Baki and Eniwari Creek areas (ODU et al., 1988). Four different species of freshwater turtles ( Trionyx triunguis, Pelusios niger, Pelusios castaneus, Pelomedusa subrufa) were found in this river before the spillage, but their relative abundance was not studied (POLITANO, 1985; ODU et al., 1989). During 30 days of field work in 1984, a team of scientists headed by Dr Edoardo Politano recorded 48 Pelusios niger, 31 Pelusios castaneus, 4 Pelomedusa subrufa and 2 Trionyx triunguis (POLITANO, 1985), from exactly the same study area. It should be pointed out that these scientists did not specifically study freshwater turtles, and came across these animals purely by chance. Several specimens were collected at that time, and they are now stored in the collections of the Environmental Centre "Demetra", Rome.

Table 1. Summary of the data on total hydrocarbon content (THC, in ppm), in surface as well as in bottom water, measured at the site of oil spillage for the "polluted study area", and at some neighbouring localities along the River Nun (Bayelsa State, southern Nigeria). See also the study by ODU et al. (1989): ND. Not detected. (For more details on the methods, see the text.) Tabla 1. Resumen de los datos sobre contenido total en hidrocarburos (THC, en ppm), tanto en la superficie como en el fondo del agua, medido en el emplazamiento donde se produjo el vertido de petróleo para el "área de estudio contaminada", así como en algunas localidades vecinas situadas a lo largo del río Nun (estado de Bayelsa, sur de Nigeria). Véase también el estudio de ODU et al. (1989): ND. No detectado. (Para más detalles acerca de los métodos empleados, consultar el texto.)

THC Location

Top

Bottom

Aguobiri

0.3

Ekowe

1.3

3.2

Eniwari

0.5

1.2

Nangigbene

2.5

2.4

The spillage event at this site was devastating, resulting in crude oil pollution upstream up to a distance of 1 km. Total hydrocarbon content for several sites along the River Nun, where this oil spillage event occurred, are presented in table 1 (see also ODU et al., 1989). Water Samplers were used to sample the surface and bottom water at each station. Aliquots of each sample were collected in plastic bottles and transported to the laboratory in ice–loaded chambers. The oil spill occurred on 27th January, 1988 and on the following day, “Shell Petroleum Development Company” sent containment booms and anchors to check the flow of oil into Igeibiri Creek. However, before this could be done, crude oil had escaped into the creek. Post–Impact Studies of the spill (aimed at quantifying the extent and degree of pollution and damage) were carried out over the period, September 10–22, 1988. Laboratory analysis of Total Hydrocarbon content (THC) in the soil and water samples were carried out by extraction method using toluene and the extracted oil determined by the absorbance of the extracts at 420 nm in a spectronic 70 Spectrophotometre. The concentration was consequently read off from a standard curve and multiplied by the appropriate dilution factor.

Animal Biodiversity and Conservation 26.1 (2003)

with H representing Shannon’s index and S the total number of species. Shannon index is:

Methods Data were gathered mainly during the years 2000 and 2001, but some additional observations were also made in the two study areas between 1996 and 1999. In total, these two study areas were surveyed for 20 field days at each locality, both in dry and in wet seasons. Each field day lasted at least 12 hours. Thus, in total, 80 field days (40 in dry and 40 in wet seasons) were done. The search for free–ranging turtles along non–linear transects was conducted along three main habitats, known to be frequented by these species (see LUISELLI et al., 2000): main river tract, forest swamps, and permanent marshes surrounded by grassy vegetation. Several standard turtle–collecting techniques were used, including baited hoop traps, dipnetting, trawling [see also GIBBONS et al. (2001) for a similar procedure], and many additional specimens were brought in by local villagers specifically employed for the purpose of this research project. The numbers of villagers employed at the two sites and also the number of traps (200 at each site, all situated along the main rivers) was standardized to avoid any potential bias in the methodology. Once the turtles were captured, they were measured (plastron length), sexed, identified to species, and permanently individually marked by unique sequences of notches filed into the marginal scutes. To avoid statistical problems due to "pseudo– replication" of the data (MATHUR & SILVER, 1980; HURLBERT, 1984), data (on habitat use, diet, etc) was recorded only once from individual turtles, i.e. the recaptured turtles were never used again for data recording and analyses. For uniformity, data relative to the first time a given specimen was encountered were recorded. Quantitative biodiversity analyses were made according to the following indexes: species diversity was calculated using Margalef’s Diversity Index (MAGURRAN, 1988):

DMg = (S – 1) ln N where S is the total number of species and N is the total number of individuals. Species dominance was assessed using the Berger–Parker index (MAGURRAN, 1988):

H = – 3[n / N log (n / N)] where n is the number of individuals observed for each species and N is the total number of individuals observed in each study area. Habitat niche breadth was assessed by the Simpson’s diversity index (SIMPSON, 1949):

B = 1 / 3(pi2) where pi is the frequency of utilization of the ith resource. All data were statistically analysed by STATISTICA (version 5.0, for Windows) PC+package (STATSOFT INC., 1996), with all tests being two– tailed and alpha set at 5%.

Results Community composition in pristine habitat and in oil–polluted habitat A total of 510 turtle specimens, belonging to four different species (Trionyx triunguis, Pelusios castaneus, Pelusios niger, and Pelomedusa subrufa), were captured in the unpolluted area, whereas 88 specimens, belonging to two different species (Pelusios castaneus and Pelusios niger), were captured at the polluted area. The dominant species was Pelusios castaneus followed by Pelusios niger in the unpolluted area, and Pelusios niger in the polluted area. In the villages around the polluted area smoked shells of both Trionyx triunguis and Pelomedusa subrufa were found, which testifies that these two species were certainly also present in this latter area before the various pollution events. The values of the biodiversity indexes calculated for both the unpolluted and the polluted areas are given in table 2. A linear correlation Mantel test revealed that DMg was significantly higher in the unpolluted area (P < 0.0001), and that E was significantly higher in the polluted area (P = 0.038), whereas no statistical difference was found between areas regarding the indexes d (P = 0.352) and H (P = 0.117). Habitat use

d = Nmax / N where Nmax is the total number of individuals of the most abundant species. An increase in the value of the reciprocal form of the index (1/d) indicates an increase in diversity and reduction in dominance (MAGURRAN, 1988). Evenness index was calculated using Pielou’s formula:

E = H / log S

The distribution of captured species in three different habitats at both the unpolluted and the polluted areas is presented in figure 1. The percentage of occurrence of turtles (all species cumulated) in the three habitats is presented in figure 2. Values of niche breadth, calculated for each species both in the polluted and unpolluted environments are presented in table 3. In both species of Pelusios there was a significant (at least P < 0.005, Mantel test) reduction in the

Luiselli & Akani

Table 2. Values of the biodiversity indexes calculated for both the unpolluted and the polluted areas: S. Total number of species; N. Total number of individuals; Nmax. Total number of individuals of the most abundant species; DMg. Margalef’s diversity index; D. Berger–Parker’s dominance index; E. Pielou’s evenness index; H. Shannon’s index. Tabla 2. Valores de los índices de biodiversidad, calculados tanto para las áreas no contaminadas como para las contaminadas: S. Número total de especies; N. Número total de individuos; Nmax. Número total de individuos de la especie más abundante; DMg. Índice de diversidad de Margalef; D. Índice de dominancia de Berger–Parker; E. Índice de uniformidad de Pielou; H. Índice de Shannon.

Nmax

Unpolluted area

510

314

Polluted area

habitat niche breadth at the polluted area in comparison with the unpolluted area. A factorial plan of a Principal Component Analysis (PCA) on the habitat similarities across turtle species [VARIMAX standardized rotation model; log10 det. Corr. Matrix = –46.977, eigenvalues: 3.656 (60.9% of total variance exlained), 1.842 (30.7% of total variance explained)] based on the proportion of specimens found in each habitat type, including in the analysis only the adults (fig. 3), showed that: 1. Pelusios castaneus in polluted area, Pelusios

Main river

18.703

0.616

0.387

0.643

4.477

0.648

0.281

0.937

niger in polluted area, and Trionyx triunguis, are arranged in the same zone of the multidimensional spacing; 2. Pelusios castaneus in unpolluted area, Pelusios niger in unpolluted area, and Pelomedusa subrufa are arranged in divergent zones of the multidimensional spacing each another; 3. Factor 1 correlated significantly with Pelusios niger in unpolluted area, Pelusios niger in polluted area, and Pelusios castaneus in polluted area; 4. Factor 2 correlated significantly with Pelusios castaneus in unpolluted area, and Pelomedusa subrufa .

Forest ponds

Marsh

B 250

Number of specimens

DMg

200 150 100 50 0

Pc Species

60 50 40 30 20 10 0

Pn Species

Fig. 1. Number of turtle specimens observed in the unpolluted area (A) and in the polluted area (B) during the present research study, in the three different habitat types. For this figure, the various species are entered separately: Tt. T. triunguis; Pc. P. castaneus; Pn. P. niger; Ps. P. subrufa. Fig. 1. Número de ejemplares de tortugas observados en el área no contaminada (A) y en el área contaminada (B) durante el presente estudio, en los tres tipos de hábitat distintos. En esta figura, las distintas especies se indican por separado. Tt. T. triunguis; Pc. P. castaneus; Pn. P. niger; Ps. P. subrufa.

Animal Biodiversity and Conservation 26.1 (2003)

% of specimens

Unpolluted area 100 90 80 70 60 50 40 30 20 10 0

Main river

P olluted area

Forest ponds Habitat type

Marsh

Fig. 2. Percent of occurrence of turtles (all species cumulated) found in the three different habitat types in the unpolluted area (n = 510) and in the polluted area (n = 88). Fig. 2. Porcentaje de la presencia de tortugas (todas las especies acumuladas) halladas en los tres tipos de hábitat distintos del área no contaminada (n = 510) y de la contaminada (n = 88).

Table 3. Values of the Simpson’s niche breadth indexes calculated for all the study species in both the unpolluted (Unpoll) and the polluted (Poll) areas. Tabla 3. Valores de los índices de amplitud de nicho de Simpson, calculados para todas las especies del estudio, tanto en las áreas no contaminadas (Unpoll) como en las contaminadas (Poll).

Species

Unpoll

Poll

Trionyx triunguis

1.189

***

Pelusios castaneus

1.965

1.280

Pelusios niger

2.075

1.156

Pelomedusa subrufa

1.000

***

Discussion Our study revealed both direct and indirect effects of oil pollution on the complexity and habitat use of Nigerian freshwater communities of turtles, even though over ten years had elapsed between the pollution event and the present study. The main direct effect was a considerable reduction in the turtle specific diversity, with 50% of the species being lost after oil spillage, and with a very strong decline in the numbers of turtle specimens also for those species which were

able to survive the catastrophic pollution event. It should be pointed out that the two species which disappeared were the largest one (Trionyx triunguis), with a basically carnivorous diet (AKANI et al., 2001), and the smallest one (Pelomedusa subrufa), which is typically a savanna species, and which only marginally enters the swamp–forest habitat of Niger Delta (IVERSON , 1991, 1992; LUISELLI et al., 2000). Thus, it seems likely that extinction of these two species occurred mainly due to a decline also in prey species (mass mortality of fish caused by the oil pollution of waters) in the case of the former species, and due to a suboptimal adaptation to forest environments, aggravated by the catastrophic oil spillage event, in the case of the latter species. Another direct consequence of the oil spillage event is that the habitat use changed considerably in one species, i.e. Pelusios niger, which shifted from an intensive use of swamps into the rainforest before spillage to an almost complete abandonment of this habitat type after the spillage event. It was most probably a consequence of the fact that at least several of the swamps became strongly polluted after the oil spillage event, with nearly complete extirpation of the flora and small fauna inhabiting them. Unfortunately, there are no contaminant analytical data available to confirm this, but only a number of empirical evidences (ODU et al., 1989). The shift in habitat use by Pelusios niger may have strong effects on the long–term persistence of this species, independently of the pollution effects of the oil spillage event. Indeed, this species is certainly a strong competitor with Pelusios castaneus, a species which is phylogenetically closely

Luiselli & Akani

1.2 1

Pc (unpoll)

•

Factor 2

0.8 0.6 0.4

Pc (poll) • Tt • Pn•(poll)

0.2 0

Pn ((un un poll) unpoll)

-0.2 -0.4 -0.4

Pc. P. castaneus Pn. P. niger Ps. P. subrufa Tt. T. triunguis

•

-0.2

0.2 0.4 0.6 Factor 1

0.8

1.2

Fig. 3. Factorial plan of a Principal Component Analysis (PCA) on the habitat similarities across turtle species (VARIMAX standardized rotated model), based on the proportion of specimens found in each habitat type, including in the analysis only the adults, selected after Fisher exact test across species: (unpoll). Sample observed in the unpolluted area; (poll). Sample observed in the polluted area. Fig. 3. Plano factorial de un análisis de componentes principales (PCA) sobre las similitudes que presentan los hábitat de distintas especies de tortugas (método normalizado de rotación VARIMAX), basado en la proporción de ejemplares hallados en cada tipo de hábitat, incluyendo en el análisis sólo los ejemplares adultos, seleccionados tras el test exacto de Fisher realizado en distintas especies: (unpoll). Muestra observada en el área no contaminada; (poll). Muestra obsevada en el área contaminada.

related, of similar size, and with similar dietary habits (LUISELLI et al., 2000). Based on observations and statistical modelling of the distribution of these species, LUISELLI et al. (2000) concluded that the most likely niche difference between these potential competitors is divergent habitat use, with one species being more linked to permanent water bodies than the other, which is conversely linked to seasonal swamps and marshes. Presently in our study area, the oil spillage event constrained the two species to coexist on the same habitat resource (as clearly explained by the factorial plan of PCA in fig. 3), and thus to strengthen their competitive relationships. It is likely that, under these conditions, the species least adapted to permanent water bodies would decline, thus augmenting the direct negative effects of the pollution event. Apart for direct killing to adults and juveniles, it is most likely that oil contamination had serious effects also on the eggs. Turtles lay their eggs on sandy beaches (LUISELLI et al., 2000), which are common around this area in focus, and oil readily permeates into sandy beaches. It implies that turtle eggs could easily be destroyed by this contaminant. Our study fully reinforces the few published observations on mortality of herpetofuna following oil spills. For instance, BURY (1972) observed that after a diesel oil spill into a Californian stream, 36 garter snakes and a single pond turtle of the genus Clemmys were killed, while others were in a moribund state. Following a huge oil spill on St. Lawrence River,

many frogs and turtles were also found dead (PALM, 1979; ALEXANDER et al., 1981). A significant implication of this study is that eco–ethological modifications in populations of animals subjected to catastrophic events of oil pollution should always be studied in order to properly understand the long–term effects of these devastating phenomena.

Acknowledgements This study was financially supported by Chelonian Research Foundation (Lunenburg, Massachusetts), through its Linnaeus Annual Turtle Research Awars (year 2001, awarded to L. Luiselli), with some logistical assistance from companies of the ENI Group (Rome) and the Rivers State University of Science and Technology, Port Harcourt. The Federal Department of Forestry (Port Harcourt) released authorizations to capture the study animals, and Dr F. M. Angelici and Dr E. Politano critically commented upon a previous draft of the manuscript. Dr E. Filippi is especially thanked for the data he provided and for help with the manuscript.

References AKANI, G. C., CAPIZZI, D. & LUISELLI, L., 2001. Diet of the softshell turtle, Trionyx triunguis, in an

Animal Biodiversity and Conservation 26.1 (2003)

Afrotropical forested region. Chel. Cons. Biol., 4: 200–201. ALEXANDER, M. M., LONGABUCCO, P. & PHILLIPS, D. M., 1981. The Impact of oil on marsh communities in the St. Lawrence River. In: Oil Spill Conference: 333–340. American Petroleum Institute, Washington D.C. ALLANSON, M. & GEORGES, A., 1999. Diet of Elseya purvisi and Elseya georgesi (Testudines: Chelidae), a sibling species pair of freshwater turtles from eastern Australia. Chel. Cons. Biol., 3: 473–477. BURY, R. B., 1972. The Effects of Diesel Fuel on a Stream Fauna. Calif. Fish Game, 58: 291–295. DE MONTCLOS, M.–A., 1994. Le Nigéria. Kurthala, Paris. EMBASSY OF NIGERIA, 2001. Nigeria’s profile: political and economical. Embassy of Nigeria Italy Quarterly Newsletter, 3(2000): 11–12. G IBBONS, J. W., LOVICH , J. E., T UCKER, A. D., FITZSIMMONS, N. N. & GREENE, J. L., 2001. Demographic and ecological factors affecting conservation and management of the Diamondback Terrapin (Malaclemys terrapin) in South Carolina. Chel. Cons. Biol., 4: 66–74. HURLBERT, S. H., 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr., 54: 187–211. IVERSON, J., 1991. Global correlates of species richness in turtles. Herpetol. J., 2: 77–81. – 1992. A revised checklist with distribution maps of the turtles of the world. Privately Printed, Richmond. KENNETT, R. & TORY, O., 1996. Diet of two freshwater turtles, Chelodina rugosa and Elseya dentata (Testudines: Chelidae) from the wet–dry tropics of northern Australia. Copeia, 1996: 409–419. KINGDON, J., 1990. Island Africa. Academic Press, New York. LUISELLI, L., POLITANO, E. & ANGELICI, F. M., 2000. Ecological correlates of the distribution of terrestrial and freshwater chelonians in the Niger Delta, Nigeria: A biodiversity assessment with conservation implications. Rev. Ecol. (Terre et Vie), 55: 3–23. MAGURRAN, A. E., 1988. Ecological diversity and its measurement. Princeton University Press,

Princeton (New Jersey). MATHUR, D. & SILVER, C. A., 1980. Statistical problems in studies of temperature preferences of fishes. Can. J. Fish. Aquat. Sci., 37: 733–737. MOLL, D., 1990. Population sizes and foraging in a tropical freshwater stream turtle community. J. Herpetol., 24: 48–53. NDES, 1998. Environment and Socio–economic Characteristics. Vol 1. Niger Delta Environmental Survey, Port Harcourt. ODU, C. T. I., NWBOSHI, L. C., FAGADE, S. O. & AWANI, P. E., 1989. Final Report on Post–Impact Study of SPDC "8" Nun River Delivery Line Spillage. Report to Shell Petroleum Developmental Company, Port Harcourt. PALM, D. J., 1979. Damage Assessment Studies Following the NEPCO–140 Oil Spill on the St. Lawrence River. EPA 600/7–79–256. Industrial Environment Research Laboratory EPA, Cincinnati, Ohio. POLITANO, E., ED. 1985. Studio dell’ecosistema di un’area del Delta del Fiume Niger, Nigeria, con riferimento allo sfruttamento industriale petrolifero. ENI S.p.A., Rome. PRITCHARD, P. C. H., 2001. Observations on body size, simpatry, and niche divergence in softshell turtles (Trionychidae). Chel. Cons. Biol., 4: 5–27. SIMPSON, E. H., 1949. Measurement of diversity. Nature, 163: 688. STATSOFT INC., 1996. STATISTICA for Windows, release 5.0. Statsoft Inc, Tulsa. STONE, P. A., HAUGE, J. B., SCOTT, A. F., GUYER, C. & DOBIE, J. L., 1993. Temporal changes in two turtle assemblages. J. Herpetol., 27: 13–23. TERAN, A. F., VOGT, R. C. & GOMEZ, M. F. S., 1995. Food habits of an assemblage of five species of turtles in the Rio Guapore, Rondonia, Brazil. J. Herpetol., 29: 536–547. TOFT, C. A., 1985. Resource partitioning in amphibians and reptiles. Copeia, 1985: 1–21. VOGT, R. C. & GUZMAN, S., 1988. Food partitioning in a neotropical freshwater turtle community. Copeia, 1988: 37–47. WILLIAMS, T. A. & CHRISTIANSEN, J. L., 1981. The niches of two sympatric softshell turtles, Trionyx muticus and Trionyx spiniferus, in Iowa. J. Herpetol., 15: 303–308.

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 26.1 (2003)

Edad, crecimiento y reproducción de Gobio gobio L. (Pisces, Cyprinidae) en un tramo regulado del río Segura (SE España) P. A. Miñano, A. García–Mellado, F. J. Oliva–Paterna & M. Torralva

Miñano, P. A., García–Mellado, A., Oliva–Paterna, F. J. & Torralva, M., 2003. Edad, crecimiento y reproducción de Gobio gobio L. (Pisces, Cyprinidae) en un tramo regulado del río Segura (SE España). Animal Biodiversity and Conservation, 26.1: 67–76. Abstract Age, growth and reproduction of Gobio gobio L. (Pisces, Cyprinidae) in a regulated stretch of the Segura river (SE Spain).— The age, growth and reproduction of Gobio gobio, were studied during a period of two years in a section of the Segura River regulated by the effect of a small upstream hydroelectric power station. A total of 254 specimens were caught monthly by electrofishing. The studied population showed a maximum of six age classes in females (0+–5+) and five in males (1+–5+). All females were mature at 2+ age class, whereas only 62.5% 2+ males showed mature gonads. During the studied period, both sexes showed maximum values of Gonadosomatic Index in May and spawn was different between the two studied periods. Compared with other populations, the studied population from a regulated locality is characterized by a non– seasonal body condition cycle and low captures of juvenile fish (0+, 1+) probably due to the effect of washing produced by drastic and unpredictable flow changes. Key words: Gobio gobio, Life–history, Growth, Reproduction. Resumen Edad, crecimiento y reproducción de Gobio gobio L. (Pisces, Cyprinidae) en un tramo regulado del río Segura (SE de España).— La edad, crecimiento y reproducción de Gobio gobio, ha sido estudiada a lo largo de dos años en un tramo del río Segura regulado por una pequeña central hidroeléctrica. Mediante pesca eléctrica fueron capturados, mensualmente, un total de 254 ejemplares. Las hembras presentaron seis clases de edad (0+–5+) mientras que los machos presentaron cinco clases (1+–5+). Todas las hembras de clase de edad 2+ resultaron maduras mientras que los machos 2+ resultaron maduros en un 62,5% de los casos. Durante el periodo de estudio, ambos sexos presentaron los máximos valores del Índice Gonadosomático durante los meses de mayo aunque el desove resultó diferente entre los dos periodos estudiados. En comparación con otras poblaciones, la población estudiada en un tramo regulado del río se caracteriza por no presentar un ciclo estacional en la condición somática y bajas capturas de ejemplares juveniles (0+, 1+) debido, probablemente, al efecto de lavado provocado por los drásticos e impredecibles cambios en el caudal. Palabras clave: Gobio gobio, Estrategias de vida, Crecimiento, Reproducción. (Received: 9 IV 02; Conditional acceptance: 22 VII 02; Final acceptance: 3 II 03) P. A. Miñano*, A. García–Mellado, F. J. Oliva–Paterna & M. Torralva, Dept. de Zoología y Antropología Física, Fac. de Biología, Univ. de Murcia, 30100–Murcia, España (Spain). Corresponding author: P. A. Miñano. E–mail: paminano@um.es

ISSN: 1578–665X

Miñano et al.

Introducción Gobio gobio (Linnaeus, 1758), es un ciprínido de pequeño tamaño que raramente supera los 150 mm de longitud. Su hábitat más característico es el curso medio de los ríos donde tiene preferencia por tramos de corriente con fondos arenosos o de grava, siendo indicador de una buena calidad de las aguas (DOADRIO, 2001). No obstante, también puede encontrarse en ambientes lénticos y someros como las colas de ciertos embalses. Es una especie gregaria y bentónica que se alimenta básicamente de macroinvertebrados. Su distribución nativa ocupa la mayor parte de Europa, siendo introducido en la península ibérica en el siglo XIX, donde se aclimató extendiéndose rápidamente por nuestros ríos (LOBÓN–CERVIÁ et al., 1991). Si bien, DOADRIO (2001) atribuye un carácter autóctono a las poblaciones de las cuencas del Ebro y Bidasoa, la presencia de Gobio gobio en la Cuenca Hidrográfica del Segura es, al igual que la de Carassius auratus L., 1758 (MA S, 1986; GARCÍA DE J ALÓN et al., 1992) y Chondrostoma polylepis Steindachner, 1864 (TORRALVA & OLIVA–PATERNA , 1997), resultado de la transferencia de agua entre la Cuencas Hidrográficas del Tajo y el Segura (Trasvase Tajo–Segura). El carácter de especie introducida en la Cuenca del Segura hace que el estudio de su estrategia de vida presente una importancia notable debido, principalmente, a las posibles repercusiones o influencias que pueda tener sobre las especies autóctonas de dicha Cuenca (ELVIRA , 1998b). A su vez, si bien existen antecedentes de estudios sobre las estrategias que presentan poblaciones de la especie localizadas en otras cuencas hidrográficas de la península (LOBÓN–CERVIÁ & TORRES, 1983; LOBÓN– CERVIÁ et al., 1991), en el presente estudio se presentan los primeros datos sobre el crecimiento y la reproducción de la especie en la Cuenca del Segura. Asimismo, a pesar de que la regulación del caudal en los ríos de la península ibérica ha sido puesto de manifiesto en sucesivas ocasiones como uno de los principales problemas sobre su ictiofauna (ELVIRA , 1996, 1998a), pocos son los estudios sobre los efectos provocados por este tipo de perturbación sobre las poblaciones de peces (CAMARGO & GARCÍA DE JALÓN, 1990; GARCÍA DE J ALÓN et al., 1992; 1994; TORRALVA et al., 1997; ALMODÓVAR & NICOLA , 1999). En el presente estudio se analiza la estrategia de Gobio gobio en un área donde las condiciones del medio se ven afectadas por continuas sueltas de agua, procedentes de una central hidroeléctrica, y caracterizada por la predominancia de una especie autóctona de la cuenca, Barbus sclateri Günther, 1868. Material y métodos El área de estudio se encuentra localizada en un tramo de 500 m del río Segura a 44 km de la cabecera en el Sector 2 de los definidos por VIDAL–

ABARCA et al. (1990). Dicha zona se encuentra sometida a una fuerte regulación de su caudal debido a las descargas de agua procedentes de una central hidroeléctrica, localizada aguas arriba de la zona de estudio, la cual regula el flujo de agua en función de las necesidades de fluido eléctrico. Los cambios provocados por dicha regulación en el hábitat acuático de la localidad de estudio son drásticos. Así, con determinadas descargas de agua se pasa de una anchura media del cauce de 12,5 m y una profundidad media de 19 cm a una anchura media de 17,5 m de ancho y 1,5 m de profundidad al procederse la descarga (TORRALVA, 1996). En la figura 1 se puede observar la evolución diaria de los caudales, provocados por dicha central eléctrica, durante el periodo de estudio. Para más detalles sobre la localidad de muestreo revisar TORRALVA et al. (1997). Mediante pesca eléctrica (200–350 V, 1–3 A) fueron capturados un total de 254 ejemplares de la especie Gobio gobio (101 machos y 153 hembras). Las muestras fueron tomadas con periodicidad mensual entre el mes de septiembre de 1989 y septiembre de 1991. Sin embargo, no fueron capturados ejemplares de esta especie durante los meses de octubre de 1989, agosto de 1990 y febrero, marzo y junio de 1991. Tras su captura los especímenes fueron fijados en formaldehído al 4% y transportados al laboratorio donde fueron medidos [longitud furcal (Lf) y longitud estándar (Ls) ± 1 mm], pesados [peso húmedo total (Pt) y peso húmedo eviscerado (Pe) ± 0,01 g] y sexados mediante observación directa de las gónadas. De cada ejemplar se obtuvo una muestra de escamas (obtenidas del flanco izquierdo entre el inicio de la aleta dorsal y la línea lateral) para la determinación de la edad. El análisis del retrocálculo ha sido realizado aplicando el criterio de BAGENAL & TESCH (1978). El cálculo de las tasas instantáneas de crecimiento en longitud (g) se realizó según WO O T TON (1998): g = (log e Lt2 – log e Lt1) / (t2 – t1) siendo L t2 la longitud media retrocalculada final, L t1 la longitud media retrocalculada inicial y t2 – t1 el periodo de tiempo transcurrido. La relación entre la longitud y el peso se calculó para el total de los ejemplares capturados y para machos y hembras sexualmente maduros por separado, según la relación: Pe = a Lfb siendo Pe el peso húmedo eviscerado, Lf la longitud furcal, “a” una constante y “b” el exponente. La existencia de diferencias significativas en esta relación entre los sexos fue determinada mediante análisis de covarianzas (ANCOVA, p < 0,05) (SOKAL & R OHLF, 1981). A su vez, la isometría (b = 3) o alometría (b ≠ 3) de la curva fue contrastada mediante un test de Student (SOKAL & R OHLF, 1981).

Animal Biodiversity and Conservation 26.1 (2003)

-1

Fig. 1. Tasa diaria del caudal (m s ) y temperatura media mensual (ºC) en el área de muestreo durante el periodo de estudio. Se muestra en detalle el caudal diario durante los meses de diciembre de 1989 y junio de 1990: S. Septiembre; O. Octubre; N. Noviembre; D. Diciembre; E. Enero; F. Febrero; M. Marzo; A. Abril; M. Mayo: J. Junio; J. Julio; A. Agosto. 3

-1

Fig. 1. Daily flow rate (m s ) and mean; monthly temperature (°C) in sampling area along the study period. Daity flow during December 1989 and June 1990 detailed in inset: S. September; O. October,; N. November; D. December; E. January; F. February; M. March; A. April; M. May; J. June; J. July; A. August.

La condición somática (K) se ha obtenido mediante una modificación del índice de condición de Fulton (BAGENAL & TESCH, 1978; VAZZOLER, 1996): b

K = Pe / Lf (10 ) donde "b" es el exponente de la relación longitud-peso, Pe y Lf son el peso húmedo eviscerado y la longitud furcal respectivamente. A su vez, se comprobó la independencia del índice con la longitud de los ejemplares (Análisis de regresión, p > 0,05) (SOKAL & ROHLF, 1981). Las gónadas de cada ejemplar fueron clasificadas como inmaduras, en proceso de maduración, maduras y post-reproductoras, mediante los caracteres visuales que presentaron según la escala propuesta por VAZZOLER (1996) para la determinación del estado de madurez gonadal. De esta forma, la longitud y edad de primera maduración han sido determinadas mediante la representación por

edades y tallas del estado de madurez gonadal y del índice gonadosomático durante el periodo reproductor. El desarrollo gonadal ha sido estudiado mediante el cálculo del índice gonadosomático (Ig) (WOOTTON, 1998): Ig= 100 Pg / Pt donde Pg es el peso de la gónada y Pt el peso húmedo total. El estudio del ciclo ovular se ha realizado mediante el método gravimétrico propuesto por BAGENAL (1978). No han sido detectadas diferencias significativas en el diámetro y número de huevos según su localización en la gónada o entre ambos ovarios (ANOVA, p > 0,05) por lo que los oocitos presentes en una submuestra de la zona media del ovario (5% del peso total de la gónada) fueron contados y medidos (± 0,05 mm). Para ello, cada muestra fue

Miñano et al.

tratada con solución de Gilson (BAGENAL, 1978) con la finalidad de reblandecer el tejido gonadal y, de esta forma, disgregar los oocitos. Finalmente, la muestra era procesada en una lupa binocular cuyo ocular izquierdo presentaba una regleta calibrada de 10 mm para facilitar la medición de los oocitos observados. Resultados Edad y crecimiento anual La estructura poblacional de los ejemplares capturados muestra seis clases de edad para las hembras (0+ – 5+) y cinco clases para los machos (1+ – 5+). El mayor número de ejemplares capturados, en ambos sexos, fueron los pertenecientes a la clase de edad 3+, representando un 39,8% de las capturas en los machos y un 45,3% en las hembras (tabla 1). Las longitudes máximas observadas han sido de 98 mm (Lf) en un macho capturado en el mes de diciembre de 1989 y de 101 mm (Lf) para una hembra capturada en el mes de octubre de 1990. La relación entre la longitud furcal y el radio total de la escama resultó lineal en ambos sexos (Lf = 1,541 + 0,135Rt; r = 90%; F(1,230) = 887,416; p < 0,0005). No fueron detectadas diferencias significativas en esta relación entre ambos sexos (ANCOVA, F(1,231) = 0,322, p = 0,571 de la pendiente) por lo que fueron tratados de forma conjunta. De esta forma, la ecuación obtenida para el retrocálculo es la siguiente: Ln = [Rn / Rt (Lf – 1,541)] + 1,541 siendo Ln la longitud a la edad “n”, Rt el radio total de la escama, Rn el radio de la escama a la edad “n” y “1,541” la ordenada en el origen de la relación

Tabla 1. Distribución de machos (M) y hembras (H) de G. gobio capturados en el río Segura por clases de edad. Table 1. Distribution of Gobio gobio males (M) and females (H) caught in the Segura River grouped in age classes. Edad 0+

M (%) –

H (%) 2,9

11,8

11,5

35,5

31,7

39,8

45,3

11,8

7,9

1,1

0,7

lineal obtenida entre el radio total de la escama (Rt) y la longitud furcal (Lf). De esta forma, en la tabla 2 se muestran las longitudes retrocalculadas para machos y hembras de forma independiente ya que fueron detectadas diferencias significativas entre ambos sexos en las longitudes retrocalculadas de las clases de edad 1+ y 2+ (t de Student, t1+ = – 8,044, gl = 226, p < 0,0005; t2+ = –2,363, gl = 199, p = 0,019). El cálculo de las tasas instantáneas de crecimiento muestra un elevado crecimiento de los ejemplares más jóvenes descendiendo a medida que avanzan en edad. Los machos presentaron tasas superiores a las hembras durante los primeros años de vida, estabilizándose a los 3 años, edad a la cual el 100% de ejemplares fueron maduros (tabla 2). Relación longitud–peso La relación entre la longitud y el peso que mejor ajuste presentó viene dada por la siguiente ecuación:

(R2

Pe = 0,014 Lf 2,8437 = 0,885; p < 0,05; n = 228)

Ambos sexos se estudiaron conjuntamente ya que no fueron detectadas diferencias significativas entre ellos (ANCOVA, F(1,227) = 0,01, p = 0,920). Los datos reflejaron un crecimiento alométrico de la población estudiada (b ≠ 3; t = –2,294, gl = 226, p < 0,05). Condición somática Ambos sexos mostraron una dinámica temporal similar en el ciclo de la condición somática (Análisis de correlaciones, r = 0,890, p < 0,0005). No obstante, los machos presentaron valores superiores en condición para el total de los ejemplares capturados (ANOVA, F(1,227) = 7,668, p = 0,006). Sin embargo, no se ha observado un patrón estacional claro en el ciclo de la condición somática en ninguno de los dos sexos (fig. 2). Únicamente se observa un incremento significativo (ANOVA, F(3,51) = 18,696, p < 0,001) en las hembras durante los meses previos a la reproducción (enero–abril) del año 1990. Dicho incremento no ha sido observado en los machos (ANOVA, F(3,21) = 2,593, p > 0,05). Proporción de sexos En la zona de estudio la proporción de sexos para el total de ejemplares capturados ha resultado significativamente favorable a las hembras (χ2 = 10,64; 1 gl; p < 0,05), siendo la proporción resultante de 0,66:1. Longitud y edad de primera madurez Del total de ejemplares estudiados durante el periodo reproductor, el 100% de individuos 1+ de

Animal Biodiversity and Conservation 26.1 (2003)

Tabla 2. Longitudes medias retrocalculadas (mm), incremento anual del crecimiento y tasas instantáneas de crecimiento de los machos y hembras de G. gobio. Los números romanos indican las edades a las que han sido retrocalculadas las longitudes: g. Tasa instantánea de crecimiento. Table 2. Mean back–calculated lengths (mm), annual growth increment and instantaneous growth rates of G. gobio males and females. Roman numbers indicate ages of back–calculated lengths: g. Instantaneous growth rate. Longitud a cada edad (mm) Edad de captura

III

1+ 2+

11 33

31,9 33,9

55,1

34,4

55,4

70,2

34,0

54,0

69,4

82,9

32,0

47,2

63,7

76,3

86,5

33,85

54,99

69,93

82,37

86,5

0,48

0,10

0,16

0,43

Machos

Media L.C. 95% Incremento anual g Hembras 1+

21,14

14,94

12,44

4,13

0,48

0,24

0,16

0,05

35,2

37,0

57,6

36,5

56,0

69,9

36,8

55,8

69,8

Media L.C. 95% Incremento anual g

81,3

36,1

56,0

71,9

87,8

95,7

36,52

56,57

69,94

81,86

95,7

0,43

0,83

1,16

4,24

20,05

13,38

11,92

13,84

0,44

0,21

0,16

ambos sexos resultaron inmaduros. De los ejemplares 2+ analizados, el 37,5% de los machos resultaron inmaduros, mientras que el 62,5% ya se encontraban con capacidad reproductora, presentando el ejemplar más pequeño capturado con dicha capacidad una talla de 62 mm (Lf). Las hembras de esta edad resultaron maduras en el 100% de los casos, siendo la talla mínima de los ejemplares capturados con esta edad de 58 mm (Lf). El total de machos 3+ capturados resultaron maduros. Índice gonadosomático Ambos sexos presentaron dinámicas temporales similares del índice gonadosomático (Análisis de correlación, r = 0,682, p < 0,01) (fig. 3). Asimismo, conforme a lo habitualmente observado en ciprínidos, las gónadas de las hembras mostraron un mayor desarrollo de forma significativa (ANOVA, F(1,226) = 92,787, p < 0,0005).

Con referencia al ciclo temporal que presentan los machos (fig. 3a), el periodo de quiescencia o reposo gonadal se produce entre los meses de agosto/septiembre y febrero (finales del verano, otoño e invierno), detectándose la reactivación gonadal al inicio de la primavera (marzo de 1990, abril de 1991) que culmina con el máximo desarrollo de la gónada en los meses de mayo de ambos años. A su vez, se puede observar como el periodo reproductor que presentan durante el año 1990 es algo más dilatado en el tiempo (mayo–agosto) que el observado para el año 1991 (mayo–julio). En las hembras se observa un periodo de quiescencia similar a los machos (fig. 3b). Sin embargo, de forma antagónica a lo presentado por los machos, el periodo reproductor de las hembras correspondiente al año 1990 (mayo–junio) abarcó menos tiempo que en 1991 (mayo–julio), año en el que se detectó una elevada proporción de hembras maduras.

Miñano et al.

Fig. 2. Variación temporal en la condición somática de los machos (o) y hembras (•) de G. gobio durante el período de estudio. Medias para muestras de cinco o más individuos. Límites de confianza omitidos para mayor claridad de la figura. (Para las abreviaturas ver el pie de la fig. 1.) Fig. 2. Seasonal changes in somatic condition in G. gobio males (o) and females (•) in the study period. Mean for samples of five or more specimens. Confidence limits have been omitted for clarity. (For abbreviations see the legend of fig. 1.)

Fig. 3. Variación estacional del índice Gonadosomático (Ig) en las machos (A) y hembras (B) de G. gobio. Media y límites de confianza al 95% para muestras de cinco o más individuos. (Para las abreviaturas ver el pie de la fig. 1.) Fig. 3. Seasonal changes in gonadosomatic index (Ig) for (A) males and (F) females of G. gobio. Mean and 95% CL. for samples of five or more fish. (For abbreviations see the legend of fig. 1.)

Animal Biodiversity and Conservation 26.1 (2003)

Ambos sexos presentaron los valores máximos del Ig durante los meses de mayo de 1990 (Ig machos = 0,96 ± 0,14; Ig hembras = 8,86 ± 1,92; L.C. 95%) y 1991 (Ig machos = 0,72 ± 0,18; Ig hembras = 5,19 ± 1,5; L.C. 95%).

obtienen mayores capturas de ejemplares juveniles (1+, 2+) en los ríos Ucero y Moros, mientras que la población analizada en el presente estudio se caracteriza por una mayor abundancia en las capturas de ejemplares 3+. Las continuas e impredecibles sueltas de agua procedentes de la central hidroeléctrica podrían estar provocando el arrastre de ejemplares, principalmente de tallas inferiores (0+, 1+), aguas abajo del área de estud i o (COPP , 1990; COPP et al., 1991; JURAJDA, 1995, ALMODÓVA R & N ICOLA, 1999). Pese a la presencia de un número elevado de clases de edad, en la población de Gobio gobio estudiada se observa un crecimiento inferior al descrito en otras poblaciones peninsulares de la misma especie. Así, en sistemas fluviales con mayor latitud como los ríos Ucero, Moros y Matarraña se han obtenido longitudes máximas de 140, 110 y 115 mm, respectivamente (LOBÓN CERVIÁ et al., 1991), mientras que en nuestro caso los ejemplares no superaron los 101 mm. De la misma forma, LOBÓN–CERVIÁ & TORRES (1983) obtienen en el río Jarama y embalse de Pinilla longitudes máximas superiores a las obtenidas en el presente estudio. Sin embargo, las longitudes máximas descritas en todos estos sistemas peninsulares resultan inferiores a las observadas en ríos del resto de Europa caracterizados por dinámicas más estables (KENNEDY & FITZMAURICE , 1972; MANN, 1980). Los medios afectados por fuertes fluctuaciones ambientales pueden provocar en esta especie respuestas adaptativas que provocan una temprana madurez y elevado esfuerzo reproductor con la intención de asegurar la supervivencia de la progenie (MANN, 1980; LOBÓN -CERVIÁ & TORRES, 1983). Al tiempo que se alcanza un bajo número de clases de edad (GRANADO–LORENCIO, 1992). La población de estudio no ha mostrado un patrón claro en la dinámica temporal de la condición somática de sus individuos. Sin embargo, LOBÓN– CERVIÁ & T ORRES (1983), en el río Jarama, sí detectan un patrón claro en la dinámica mensual de la condición somática con dos máximos al comienzo y final del período reproductor y valores mínimos en el mes de octubre. Una ausencia de un patrón claro en el ciclo de condición somática se observó también para Barbus sclateri e n l a m i s m a l o c a l i d a d d e muestreo ( TORRALVA et al ., 1997), en contraste con el ciclo temporal claro que presentaron poblaciones de la misma especie en localidades sometidas a una dinámica natural de la misma cuenca hidrográfica (TORRALVA et al., 1997) y en otras cuencas (HERRERA et al., 1988; HERRERA & FERNÁNDEZ– DELGADO, 1992; ENCINA & GRANA DO –L ORENCIO, 1997). En este sentido, el estrés ambiental, dadas las continuas sueltas de agua procedentes de la central hidroeléctrica, al que se encuentran sometidas las poblaciones de Gobio gobio y Barbus sclateri de la localidad de estudio puede ser la causa principal de la variación azarosa en la condición de sus individuos (TORRALVA et al., 1997).

Ciclo oocitario Si bien no todas las hembras presentaron una sincronía en el desarrollo de sus ovarios, en la figura 4 se muestra una secuencia temporal representativa del desarrollo oocitario en 12 hembras de longitudes similares durante los años 1990 y 1991. Durante el periodo de quiescencia del año 1990, los ovarios se caracterizan por presentar una única moda de oocitos translúcidos (∅ max = 0,3 mm). Con el inicio de la actividad gonadal en marzo, se observa el desarrollo de un elevado número de oocitos opacos (∅ = 0,39 ± 0,006 mm; L.C. 95%), los cuales, probablemente, constituirán el stock de huevos a desovar durante los siguientes meses. En el mes de abril se aprecia la división del grupo de oocitos anteriormente mencionado en dos grupos, uno de oocitos opacos con un diámetro similar al detectado (∅ = 0,38 ± 0,01 mm; L.C. 95%), y otro de nueva aparición constituido por oocitos vitelados (∅ = 0,68 ± 0,01 mm; L.C. 95%). A partir de que estos oocitos vitelados alcanzan su máximo desarrollo, durante el mes de junio (∅ = 0,89 ± 0,01 mm; L.C. 95%) se produce el desove de los mismos, aspecto que se observa claramente en la distribución oocitaria detectada para el mes de julio (fig. 4). Durante el año 1991 se aprecia un proceso similar al año anterior salvo en el hecho de que el máximo desarrollo de los oocitos vitelados se detecta en el mes de julio (∅ = 0,89 ± 0,04 mm; L.C. 95%), produciéndose el desove en meses posteriores (fig. 4). Finalmente, se detectó una correlación significativa entre el diámetro oocitario y la longitud (Lf) de las hembras (Análisis de correlación, r = 0,484, p < 0,0005), denotando que las hembras de la población objeto de estudio tienden a presentar oocitos de mayor diámetro cuanto mayor es la longitud. Discusión La estructura por edades de la población de Gobio gobio estudiada en el río Segura es similar a la encontrada por LOBÓN –CE RVIÁ et al. (1991) en el río Ucero, donde los ejemplares más longevos que fueron capturados en ambos estudios correspondieron con la clase de edad 5+. A su vez, esta estructura poblacional presenta un número de clases de edad superior al descrito en otros puntos de la península ibérica: ríos Matarraña y Moros donde la clase de edad máxima encontrada fue la 3+ (LOBÓN–CERVIÁ et al., 1991) o río Jarama y embalse de Pinilla donde la edad máxima alcanzada fue la 4+ (LOBÓN –CE RVIÁ & TORRES, 1983). Sin embargo, LOBÓN –CERVIÁ et al. (1991)

Miñano et al.

enero 1990

100 80

100

0 100

abril 1990 n = 386

100

mayo 1990 n = 268

80 60

Número de oocitos

20 0 100

60 40

0 100

0 100 junio 1990 n = 288

0 julio 1990 n = 101

100

20 0,1

0,3

0,5 0,7 0,9 ∅ oocitario

1,1

1,3

septiembre 1991

julio 1991 n = 270

100

mayo 1991 n = 448

abril 1991 n = 719

enero 1991

Número de oocitos

100

marzo 1990 n = 440

septiembre 1990

100

0,1

0,3

0,5 0,7 0,9 ∅ oocitario

1,1

1,3

Fig. 4. Distribución de frecuencias oocitarias de 12 hembras de G. gobio de tamaño similar: n. Oocitos opacos + oocitos vitelados (∅ > 0,3 mm); Oocitos inmaduros; Oocitos opacos; Oocitos vitelados. Fig. 4. Size–frequency distribution of oocytes from ten similar size G. gobio females: n. Opaque oocytes + yolky oocytes (∅ > 0.3 mm); Immature oocytes; Opaque oocytes; Yolky oocytes.

Animal Biodiversity and Conservation 26.1 (2003)

LOBÓN–CERVIÁ et al. (1991) describe el alcance de la madurez sexual de Gobio gobio a edades muy tempranas, de forma similar a la población del río Segura, mientras que LOBÓN –C ERVIÁ & TORRES (1983) observan que la mayor parte de los individuos son sexualmente maduros un año después, al igual que sucede en otras poblaciones europeas de la especie (BANARESCU et al., 1999). Los resultados del análisis de la reproducción muestran un periodo reproductor de la población en estudio muy extenso, abarcando desde el mes de abril, en el que ya encontramos en las gónadas oocitos vitelados, hasta el mes de junio (año 1990) y julio (año 1991), en el que se alcanza el máximo desarrollo de los mismos, momento a partir del cual se produce el desove. La duración del periodo reproductivo, en esta especie, varía de unas poblaciones a otras. Así, en poblaciones europeas, se han detectado periodos reproductores de dos meses, abril–mayo, en los ríos Frome y Themes, en Inglaterra (MATHEWS , 1971; MANN, 1980) y mayo–junio en Czechia y Eslovaquia (PENAZ & P ROKES, 1978). Sin embargo, en la península ibérica se han observado periodos de tres meses, mayo–julio, en el embalse de Pinilla, e incluso de cuatro meses, mayo–agosto en el río Jarama (LOBÓN– CE RVIÁ & T ORRES, 1983). Esta misma situación se ha observado en el río Nivelle, en Francia (BERNET , 1960). De esta forma, la población del presente estudio junto con la población del río Jarama presentan, al igual que los ciprínidos que son capaces de poner dos e incluso tres o más lotes de huevos en una misma estación reproductora, periodos reproductores extensos (MANN , 1980; LOBÓN–C ERVIÁ et al., 1991; MI L L S, 1991). Este aspecto, sumado al hecho de que en las especies de ciprínidos con puesta múltiple es frecuente encontrar que los pesos de las gónadas, durante el periodo reproductor, representan en torno al 10% del peso del cuerpo (MI L L S, 1991) nos hace inclinarnos hacia la presencia de dicha puesta múltiple, con las ventajas que conlleva en ambientes fluctuantes (CAMBRA Y & B RUTON, 1984), en la población de estudio. No obstante, ha resultado difícil, mediante el análisis del ciclo oocitario en esta población, la determinación de una segunda puesta debido a la periodicidad mensual de los muestreos que puede provocar la no visualización de la misma, siendo necesario realizar muestreos semanales para su confirmación, como ha sido expuesto para otras especies (HERRERA & F ERNÁNDEZ– DELGADO, 1992). En resumen, las alteraciones provocadas por la regulación de las aguas en los ecosistemas fluviales someten a las comunidades de peces a un estrés añadido que se ve reflejado en una falta de coherencia y sincronía en la dinámica estacional de sus estrategias de vida en un intento de adaptarse al nuevo ambiente (T ORRALVA, 1996). Así, la población de Gobio gobio analizada, en condiciones de regulación

de caudal drásticas, se caracteriza por presentar ejemplares con tallas bajas, con una madurez sexual a edades tempranas, primando la supervivencia de la especie ante el crecimiento en un intento por adaptarse y permanecer en este medio de gran inestabilidad. Finalmente, la puesta fraccionada a lo largo del periodo reproductor puede ser una estrategia, presente en otras poblaciones de la especie, que en este ambiente le confiere la ventaja de no arriesgar toda la progenie en un solo evento reproductor. Agradecimientos Mostrar nuestro agradecimiento a Asunción Andreu, Paloma Sánchez y Mónica Faraco por su colaboración en el procesado y análisis del material utilizado. Dichas tareas han sido realizadas en el Departamento de Zoología y Antropología Física de la Universidad de Murcia, al cual agradecemos su inestimable ayuda. Referencias ALMODOVAR, A. & NICOLA, G. G., 1999. Effects of a small hydropower station upon brown trout Salmo trutta L. in the river Hoz Seca (Tagus Basin, Spain) one year after regulation. Regulated rivers: Research and Investigation, 15: 477–484. BAGENAL , T., 1978. Methods for assessment of fish production in fresh waters. Blackwell Scientific Publications, London. BAGENAL, T. & TESCH, F. W., 1978. Age and Growth. In: Methods for assessment of fish production in fresh waters: 101–136 (T. Bagenal, Ed.). Blackwell Scientific Publications. London. BANARESCU, P. M., SORIC, V. M. & ECONOMIDIS, P. S., 1999. Gobio gobio (Linnaeus, 1758). In: The Freshwater Fishes of Europe: 81–134. (P. M. Banarescu, Ed.). Aula–Verlag Gmbh, Wiebelsheim. BERNET , B., 1960. Recherches biologiques sur les populations du Gobio gobio (Linne, 1758) a la Nivelle fleuve cotier du Pays Basque. Ann. St. Centr. Hydrobiol. Appl., 8: 127–180. CAMARGO , J. A. & GARCÍA DE JALÓN, D., 1990. The downstream impact of the Burgomillodo reservoir, Spain. Regulated Rivers: Research and Management, 5: 305–317. CAMBRAY, J. A. & BRUTON, M., 1984. The reproductive strategy of a barb, Barbus anoplus (Pisces, Cyprinidae), colonizing a man made lake in South Africa. J.Zool.Lond., 204: 143–168. COPP , G. H., 1990. Effect of regulation on 0+ fish recruitment in the Great Ouse, a lowland river. Regulated Rivers: Research and Management, 5: 251–263. COPP, G. H., OLIVER, J. M., PENÁZ, M. & ROUX , A. L., 1991. Juvenile fishes as functional describers of fluvial ecosystem dynamics: applications on the River, Rhone, France. Regulated Rivers: Re-

search and Management, 6: 135–145. DOADRIO, I., 2001. Atlas y Libro Rojo de los peces continentales de España. CSIC, Madrid. ELVIRA , B., 1996. Endangered freshwater fish of Spain. In: Conservation of Endangered Freshwater Fish in Europe: 55–61 (A. Kirchhofer & D. Hefti, Eds.). Bassel: Birkhäuser Verlag. – 1998a. El declive de los peces fluviales en España. Ecosistemas, 22: 66–71. – 1998b. Peces introducidos. Un cáncer en nuestros ríos. Biológica (Septiembre): 42–51. ENCINA , L. & GRANADO–LORENCIO, C., 1997. Seasonal changes in condition, nutrition, gonad maturation and energy content in barbel, Barbus sclateri, inhabiting a fluctuating river. Env. Biol. Fish., 50: 75–84. GARCÍA DE JALÓN, D., GONZÁLEZ DEL TÁNAGO , M. & CASADO, C., 1992. Ecology of regulated streams in Spain: An overview. Limnética, 8: 161–166. G ARCÍA DE J ALÓN , D., SANCHEZ , P., C AMARGO , J. A., 1994. Downstream effects of a new hydropower impoundment on macrophyte, macroinvertebrate and fish communities. Regulated Rivers: Research and Managem e n t, 9: 253–261. G RANADO – LORENCIO, C., 1992. Fish species ecology in Spanish Freshwater ecosystems. Limnetica, 8: 255–261. HERRERA , M. & FERNÁNDEZ–DELGADO, C., 1992. The life-history patterns of Barbus bocagei sclateri (Günther, 1868) in a tributary stream of the Guadalquivir River Basin, southern Spain. Ecology of Freshwater Fish, 1: 42–51. H ERRERA , M., HERNANDO, J. A., FERNÁNDEZ – DELGADO, C. & BELLIDO , M., 1988. Age, growth and reproduction of the barbel, Barbus sclateri (Günther, 1868), in a first order stream in southern Spain. J. Fish Biol., 33: 371–381. JURAJDA , P., 1995. Effect of channelization and regulation on fish recruitment in a flood plain river. Regulated Rivers: Research and Management, 10: 207–215. KENNEDY , M. & FITZMAURICE, P., 1972. Some aspects of the biology of gudgeon Gobio gobio (L.) in Irish waters. J. Fish Biol., 4: 425–440. LOBÓN– CERVIÁ, J., MONTAÑÉS C. & DE SOST OA A., 1991. Influence of environment upon the life history of gudgeon, Gobio gobio (L.): a recent and successful colonizer of the Iberian Peninsula. Journal of Fish Biology, 39: 285–300.

Miñano et al.

LOBÓN–CERVIÁ, J. & TORRES, S., 1983. On the growth and reproduction of two populations of gudgeon (Gobio gobio L.) in Central Spain. Acta. Hydrobiol., 1: 101–115. MANN, R. H. K., 1980. The growth and reproductive strategy of the gudgeon, Gobio gobio (L.), in two hard–water rivers in southern England. J. Fish Biol., 17: 163–176. MAS, J., 1986. La ictiofauna continental de la cuenca del Río Segura, evolución histórica y estado actual. Anales de Biología , 8(2): 3–17. MATHEWS , C. P., 1971. Contribution of young fish to total production of fish in the River Thames near Reading. J. Fish Biol., 3: 157–180. MILLS, C. A., 1991. Reproduction and Life History. In: Cyprinid fishes. Systematics, biology and exploitation: 483–508 (I. J. Winfield & J. S. Nelson, Eds.) Chapman & Hall. Fish and Fisheries Series, 3. Great Britain. PENAZ, M. & PROKES , M., 1978. Reproduction and early development of the gudgeon, Gobio gobio L. 1. Spawning and embryonic period. Folia Zool., 27: 257–267. SOKAL, R. R. & R OHLF, F. J., 1981. Biometry. W. H. Freeman & Co., San Francisco, California. TORRALVA, M., 1996. Biología de Barbus sclateri Günther, 1868 (Pises, Cyprinidae) en dos cursos de agua con distinto grado de regulación en la Cuenca del Río Segura (S.E. de España). Tesis doctoral, Universidad de Murcia. TORRALVA, M. & OLIVA-PATERNA , F.J., 1997. First record of Chondrostoma polylepis Steindachner, 1865 (Ostariophysi, Cyprinidae) in the basin of the river Segura, S.E. of Spain. Limnetica, 13(1): 1–3. TORRALVA, M., PUIG, M. A. & FERNÁNDEZ–DELGADO , C., 1997. Effect of river regulation on the lifehistory patterns of Barbus sclateri in the Segura river basin (south-east Spain). Journal of Fish Biology, 51: 300–311. VAZZOLER , A. E. A. DE M., 1996. Biologia da reproduçao de peixes Teleósteos: Teoría e práctica. EDUEM, Maringa, PR. VIDAL–ABARCA , M.R., MONTES, C., SUÁREZ, M. L. & RAMÍREZ–D ÍAZ, L., 1990. Sectorización ecológica de cuencas fluviales: aplicación a la cuenca del río Segura (SE España). Anales de Geografía de la Universidad Complutense, 10: 149–182. WOOTTON, R. J., 1998. Ecology of Teleost Fishes. Chapman & Hall. London.

Animal Biodiversity and Conservation 26.1 (2003)

Can taxonomic richness be used as a surrogate for phylogenetic distinctness indices for ranking areas for conservation? M. Pérez–Losada & K. A. Crandall

Pérez–Losada, M. & Crandall, K. A., 2003. Can taxonomic richness be used as a surrogate for phylogenetic distinctness indices for ranking areas for conservation? Animal Biodiversity and Conservation, 26.1: 77–84. Abstract Can taxonomic richness be used as a surrogate for phylogenetic distinctness indices for ranking areas for conservation?— Several methods have been proposed for evaluating area conservation priorities. Here the performance of traditional approaches (taxonomic richness) versus newer methods of phylogenetic distinctness is compared using the results and data from three different molecular studies: crayfish from the central United States and Australia, and Aeglidae freshwater crabs from Chile. To a large extent rankings based on species and genus richness agree with rankings based on taxonomic, phylogenetic and genetic diversity, thus suggesting that taxonomic richness methods may be used as a surrogate for the phylogenetic distinctness methods for the purpose of prioritizing reserve areas for conservation. Key words: Conservation priorities, Phylogenetic distinctness, Taxonomic richness. Resumen ¿Puede utilizarse la riqueza taxonómica como un indicativo de diferenciación filogenética para evaluar áreas de conservación?— Se han propuesto varios métodos para evaluar prioridades de conservación de áreas. En este trabajo se compara el funcionamiento de métodos tradicionales (riqueza taxonómica) frente a métodos más recientes de diferenciación filogenética utilizando los resultados y datos de tres estudios moleculares diferentes: cangrejos de agua dulce de los estados centrales de Estados Unidos y Australia, y cangrejos de agua dulce Aeglidae de Chile. En gran medida los ordenamientos basados en riqueza específica y genérica coinciden con los basados en diversidad taxonómica, filogenética y genética, sugiriendo por lo tanto que la riqueza taxonómica puede ser utilizada como un indicativo de diferenciación filogenética con el objetivo de priorizar reservas para su conservación. Palabras clave: Prioridades de conservación, Diferenciación filogenética, Riqueza taxonómica. (Received: 15 V 02; Conditional acceptance: 3 X 02; Final acceptance: 24 I 03) Marcos Pérez–Losada & Keith A. Crandall, Dept. of Integrative Biology, 401 Widtsoe Building, Brigham Young Univ., Provo UT 84602–5181, U. S. A. Corresponding author: Dr. M. Pérez–Losada. E–mail: mp323@email.byu.edu

ISSN: 1578–665X

Pérez–Losada & Crandall

Introduction

Material and methods

The most effective way of preserving biodiversity is by maintaining self–sustaining populations of native species in their natural ecosystems (RODRIGUES & GASTON, 2002). This often requires the designation of nature reserves, areas where conservation of biodiversity is a priority over other forms of land use. However, because maintaining the integrity of these areas often imposes restrictions to other economically and/or socially important human activities, there will always be limitations to the total amount of land that can be set aside for conservation purposes (VANE–WRIGHT et al., 1991; FAITH, 1992). Methods for ranking areas for the selection of reserve networks have been proposed as a response to these concerns. Traditional approaches such as species and genus richness (MAY, 1981; BROWN, 1988; SCHLUTER & RICKLEFS, 1993), assume that all units are taxonomically equivalent, and assign the same value for conservation. But is it appropriate to regard all species as equal in this matter? If faced with saving either a species not closely related to any other extant taxa (such as the tuataras or Welwitshia) or a species with many close relatives (such as species of grass snake and Taraxacum), it would look more reasonable to keep the former because its extinction would represent a much greater loss of evolutionary history and genetic diversity. Taxonomically distinct species and the places where they occur, should therefore be given priority in the allocation of conservation resources. This can be achieved by using a currency of biological diversity which takes the phylogenetic relationships between species (hence evolutionary history) into account. Over the last ten years several methods have been proposed for measuring taxonomic distinctness using phylogenetic information, and presently they are mostly applied to molecular data (see HUMPHRIES et al., 1995 and CROZIER, 1997 and references therein; and MORITZ & FAITH, 1998; OWENS & BENNETT, 1999; POSADAS et al., 2001). Phylogenetic distinctness is defined quantitatively either by reference to the topology (VANE–WRIGHT et al., 1991; NIXON & WHEELER, 1992; POSADAS et al., 2001), genetic divergence (SOLOW et al., 1993; WEITZMAN, 1992), or both (CROZIER, 1992; FAITH, 1992, 1994). In spite of the appeal of phylogenetic methods, several studies have recently been published that suggest that traditional indices such as taxonomic richness could be a good surrogate for phylogeny– based methods in ranking and prioritizing areas for conservation (WILLIAMS & HUMPHRIES, 1996; CRANDALL, 1998; HACKER et al., 1998; WHITING et al., 2000; POLASKY et al., 2001; PÉREZ–LOSADA et al., 2002; RODRIGUES & GASTON, 2002). In this study this question is addressed by comparing different biodiversity indices using data from three studies on freshwater invertebrates (CRANDALL, 1998; WHITING et al., 2000; PÉREZ–LOSADA et al., 2002).

Results from three different studies on freshwater macroinvertebrates including crayfish from the Ozark Plateaus (CRANDALL, 1998) and Australia (WHITING et al., 2000), and crabs of the family Aeglidae from Chile (PÉREZ–LOSADA et al., 2002) are compared. The Ozark Plateau is located in the central United States and encompasses much of southern Missouri and northern Arkansas. It has been subdivided into six regions characterized by the major river drainages within each as Neosho, White, Black, Southeast, Mississippi, and Missouri. Australia has been subdivided in forty–eight areas according to the Interim Biogeographic Regionalisation for Australia (IBRA) representing unique habitats and ecosystems (THACKWAY & CRESSWELL, 1995). Finally, temperate Chile encompasses twenty different main basins which have been divided in six hydrographic regions, named here with letters from A to F (see table 1). These studies have been chosen for several reasons: 1) the studied organisms represent different taxonomic levels (populations, species, and genera); 2) the areas of concern have been extensively studied and represent three well-known regions with very different ecological, faunistic, and geological characteristics; 3) all of them use different traditional and molecular phylogenetic indices for assessing conservation priorities and provide adequate information for estimating new indices if necessary; 4) the phylogenetic trees (fig. 1) representing the relationships among the studied taxa are fairly well supported and are based on different phylogenetic approaches (maximum parsimony, minimum evolution, and maximum likelihood) that make different assumptions about the evolutionary process. In the previous studies phylogenetic assessments of conservation priorities were performed using two distinct approaches: the topological dependent methods of taxonomic diversity (TD; VANE–WRIGHT et al., 1991), and the distance and branch length dependent methods of genetic diversity (GD; CROZIER, 1992) and phylogenetic diversity (PD; FAITH, 1992), respectively. Topology dependent methods rely on a rooted phylogeny and reflect the branching order and, therefore, rank those organisms that evolved earliest with the highest priority regardless of divergence between species (NIXON & WHEELER, 1992; POSADAS et al., 2001). Distance or branch length dependent methods sum the branch lengths to derive a phylogenetic diversity for an organism and strive to represent the genetic diversity or divergence between each organism (FAITH, 1994; KRAJEWSKI, 1994). Estimates of species and generic phylogenetic diversity (S.PD and G.PD, respectively), and generic genetic diversity (G.GD) were separately calculated for the Australian IBRA areas. Non–phylogenetic methods as species (SR) and genus (GR) richness (total number of species presented in each area) were also estimated.

Animal Biodiversity and Conservation 26.1 (2003)

Table 1. Ozark (A), Australian (B), and Chilean (C) area ranks for different indices and complimentarity analysis. For Australia, only the twelve areas representing most of the top ten rankings are shown. Species richness (SR), genus richness (GR), taxonomic diversity (TD), phylogenetic diversity (PD), species phylogenetic diversity (S.PD), generic phylogenetic diversity (G.PD), and generic genetic diversity (G.GD) values are also indicated. Australian areas: SEH. South Eastern Highlands; WSW. West and South West; WOO. Woolnorth; VM. Victorian Midlands; SEQ. South Eastern Queensland; NNC. NSW North Coast; NCP. Naracoorte Coastal Plain; SCP. South East Coastal Plain; VVP. Victorian Volcanic Plain; SEC. South East Corner; WAR. Warren; NSS: NSW South Western Slopes. Chilean hydrographic areas: A. Rivers of snowy and pluvious regimen; B. Rivers of snowy regimen with torrential draining; C. Rivers with snowy regimen and fast flood; D. Transition rivers; E. Rivers of constant flow and light slope; F. Patagonian rivers. n. a. Data not available. Tabla 1. Clasificación de las áreas Ozark (A), Australia (B) y Chile (C) para diferentes indices y análisis de complementaridad. Para Australia, solamente se muestran las doce áreas más representadas en los diez primeros puestos. Se indican también los valores de riqueza específica (SR), riqueza genérica (GR), diversidad taxonómica (TD), diversidad filogenética (PD), diversidad filogenética específica (S.PD), diversidad filogenética genérica (G.PD) y diversidad genética genérica (G.GD). Áreas australianas: SEH. South Eastern Highlands; WSW. West y South West; WOO. Woolnorth; VM. Victorian Midlands; SEQ. South Eastern Queensland; NNC. NSW North Coast; NCP. Naracoorte Coastal Plain; SCP. South East Coastal Plain; VVP. Victorian Volcanic Plain; SEC. South East Corner; WAR. Warren; NSS. NSW South Western Slopes. Áreas hidrográficas chilenas: A. Ríos de régimen ligado a las nieves y lluvias; B. Ríos de régimen ligado a las nieves y con lluvias torrenciales; C. Ríos de régimen ligado a las nieves y con crecidas rápidas; D. Ríos de transición; E. Ríos con caudal constante y desnivel poco pronunciado; F. Ríos de Patagonia. n. a. Datos no disponibles.

A. Ozark areas SR

Neosho 5

TD PD SR Rank TD Rank PD Rank Complementarity SR TD PD SR Rank TD Rank PD Rank

8.0 73 4 4 4 analysis 2 4.3 57 4–5 3 4

White 9

Black 8

Southeast 3

Mississippi Missouri 8 2

18.5 114 1 1 3

13.0 117 2–3 3 2

3.4 48 5 5 5

15.5 159 2–3 2 1

2.2 18 6 6 6

9 18.5 108 1 1 2

4 4.0 89 3 4 3

2 2.2 7 4–5 5 5

7 14.3 159 2 2 1

1 1.0 0 6 6 6

B. Australian areas SR GR S.PD G.PD G.GD SR Rank GR Rank

SEH WSW WOO 26 16 14 4 4 4 66.4 78.0 46.9 12.5 15.2 15.2 16.2 17.8 17.8 1 3 6 3–6 3–6 3–6

VM SEQ 9 15 5 3 25.7 42.4 15.1 8.8 19.5 12.2 9–10 4–5 1–2 $7

NNC 17 3 31.4 8.8 12.2 2 $7

NCP 5 5 15.1 15.1 19.5 >10 1–2

SCP 15 3 39.3 7.2 10.8 4–5 $7

VVP 8 4 23.0 12.2 15.9 >10 3-6

SEC WAR NSS 13 9 3 3 2 3 25.9 37.1 8.9 6.8 7.9 8.9 7.1 6.4 11.4 7 9–10 >10 $7 $10 =7

S.PD Rank G.PD Rank

2 5

1 1–2

3 1–2

10 3–4

$10

>10 3–4

5 >10

>10 6

9 >10

6 >10

>10 9

G.GD Rank

3–4

1–2

7–8

1–2

>10

Pérez–Losada & Crandall

Table 1. (Cont.) SEH WSW WOO Complementarity analysis

SEQ

NNC

NCP

SCP

VVP

SEC

WAR NSS

S.PD

n.a.

G.PD

15.2

8.9

2.5

8.9

2.6

G.GD

9.7

19.5

4.2

19.5

1.0

SR Rank

$10

5–6

$10

GR Rank

>10

3–6

1–2

7–10 7–10

1–2

>10

7–10 >10

S.PD Rank

n.a.

G.PD Rank

$10

1–2

3–5

8–9

3–5

$10

3–5

$10

6–7

$10

G.GD Rank

>10

3–6

1–2

7–8

1–2

>10

9–10 >10

C. Chilean hydrographic areas A

8.0

12.6

11.1

17.9

13.3

8.7

4.65

12.58

9.28

16.56

13.84

7.12

2.55

8.09

6.99

11.88

9.76

5.12

SR Rank

4–5

TD Rank

PD Rank

GD Rank

Complementarity analysis SR

8.0

10.6

5.1

17.9

5.6

2.0

4.65

10.52

4.16

16.56

5.72

1.63

2.55

6.58

3.17

11.88

4.29

1.37

SR Rank

5–6

2–3

5–6

TD Rank

PD Rank

GD Rank

Fig. 1. De izquierda a derecha: 1. Árbol de máxima parsimonia obtenido a partir de la secuenciación del ADNmt 16S de especies de cangrejos de agua dulce procedentes de Ozark Plateaus estudiadas por CRANDALL (1998). Los números sobre las ramas del árbol indican el número de cambios no ambiguos a lo largo de cada rama. 2. Árbol de evolución mínima basado en la secuenciación del ADNmt 16S de cangrejos de agua de Australia según WHITING et al. (2000). 3. Árbol de máxima verosimilitud basado en los genes del ADNmt 12S, 16S, COI y COII de los cangrejos de agua dulce Aeglidae de Chile (PÉREZ–LOSADA et al., 2002). Bajo las ramas se indican los valores iniciales de ceba (valores "bootstrap") basados en 200 (árbol 1), 1.000 (árbol 2) y 100 (árbol 3) réplicas.

Animal Biodiversity and Conservation 26.1 (2003)

O. luteus 2 A. papudo O. medius A. af finis affinis 8 2 O. neglectus A. bahamondei 54 12 O. quadruncus 1 98 Aegla sp. 70 3 O. ozarkae 6 A. hueicollensis 4 74 O. punctimanus A. alacalufi 82 15 O. longidigitus A. denticulata denticulata 1 7 O. peruncus 100 12 A. denticulata lacustris 6 O. hylas 2 100 65 A. mani 4 1 O. ozarkae 56 A. laevis laevis 7 O. neglectus 100 A. laevis talcahuano 8 100 1 O. harrisonii 3 61 A. laevis talcahuano 52 14 O. eupunctus 5 A. cholchol 10 O. meeki 60 9 A. cholchol O. nana 1 2 68 92 26 A. rostrata O. macrus 100 26 A. cholchol 4 O. palmeri 2 56 20 O. lancifer A. pewenchae 12 A. araucaniensis O. williamsi 98 18 A. spectabilis C. maculatus 10 3 100 14 A. abtao C. hubbsi Astacopsis franklinii P. acutus 76 Astacopsis gouldi 0.01 substitutions / site 100 Astacopsis tricornis Euastacus rieki Euastacus spinifer Euastacus bispinosus 82 Euastacus yarraensis Euastacus armatus Euastacus bidawalus 50 Euastacus hystricosus 63 Euastacus suttoni 53 Euastacus australasiensis Paranephrops planifrons Parastacoides sp. 62 100 Parastacoides sp. Cherax cuspidatus 71 Cherax sp. nov nov.. 1 Cherax dispar Cherax rotundus 62 Cherax destructor 99 Cherax albidus 56 Cherax quadricarinatus 99 Cherax quinquecarinatus 98 Cherax tenuimanus 84 Cherax glaber Engaeus fossor 65 57 Engaeus cunicularius 70 Engaeus sericatus Geocharax falcata 97 100 Geocharax falcata T enuibranchiurus glypticus Tenuibranchiurus Gramastacus sp. 96 Gramastacus sp. Engaewa similis Engaewa subcoerulea 93 0.05 changes 6

Fig. 1. From left to right: 1. Maximum parsimony tree inferred from 16S mtDNA sequence data for the crayfish species from the Ozark Plateaus studied by CRANDALL (1998). Numbers above branches indicate the number of unambiguous changes along that branch. 2. Minimum evolution tree based on 16S mtDNA sequence data for the crayfish from Australia in WHITING et al. (2000). 3. Maximum likelihood tree based on 12S, 16S, COI, and COII mtDNA genes for the freshwater crabs Aeglidae from Chile (PĂ&#x2030;REZâ&#x20AC;&#x201C;LOSADA et al., 2002). Bootstrap values based on 200 (tree 1), 1000 (tree 2), and 100 (tree 3) replications are indicated below branches.

Because not all of these indices were estimated by the previous authors in their studies, some phylogenetic indices were calculated here for every area using information on taxa geographical distributions and phylogenetic relationships. For conservation purposes it is important to identify areas that represent similar species richness thereby eliminating redundancy. Moreover, ranking areas according to their faunistic complementarity may alter the initial ordination based on non-complementarity information. In this study, we have therefore compared the resulted rankings from both phylogenetic and non– phylogenetic methods performed under both non–complementarity and complementarity analyses using the Spearman rank correlation coefficient.

Results and discussion Phylogenetic and non–phylogenetic indices, as well as the area rankings derived from them, are shown in table 1 for the Ozark Plateaus, the top ten ranking Australian IBRA areas, and the Chilean hydrographic regions. Phylogenetic and non– phylogenetic indices showed significant positively correlated rankings (P < 0.001) within the Ozark (four comparisons) and the Chilean regions (six comparisons) for both the non–complementarity (initial ranks) and the complementarity analyses (Spearman rank correlation rs = 0.71 – 0.99). All of these comparisons remained significant at P < 0.01 after sequential Bonferroni correction. Within the forty–eight IBRA Australian regions, there was also strong positive correlation between the rankings based on the number of genera per area (GR) and the generic PD and GD, as well as between the species richness (SR) and the species PD for the non–complementarity and the complementarity analyses (Spearman rank correlations rs = 0.76 – 0.99, P < 0.001). All of these comparisons remained significant at P < 0.01 after sequential Bonferroni correction. But when the species–based methods are compared directly with the genus–based methods, there are strong disparities in the resulting conservation rankings (rs < 0.001). WILLIAMS et al. (1994), BALMFORD et al. (1996), and RICOTTA et al. (2002) addressed the question of whether it is reasonable to use higher taxon richness as a surrogate for species richness in evaluating conservation priorities. They found that there is generally a good correlation between genus richness and species richness, but this correlation decreases as the number of species increases (BALMFORD et al., 1996). The results of this study show that the disparity between genus and species richness occurs in those areas with the greatest species richness (SEH, NNC, SEQ, SCP, and SEC). All of the three compared studies show that there is little difference between the traditional biodiversity measures and the newer

Pérez–Losada & Crandall

phylogenetic approaches, estimated from maximum parsimony, minimum evolution or maximum likelihood trees either performed under non–complementarity or complementarity analyses. The largest deviations between taxon richness and phylogeny–based methods were the WAR and the NNC areas from the Australian IBRA regionalisation, and region B from the Chilean hydrographic regions. Areas WAR and NNC have nine and seventeen species, respectively, but species PD of 37.1 and 31.4, respectively. Region B has only four species, but a PD of 12.58 (see table 1B, 1C). This reflects the fact that the species in areas WAR and B represent more phylogenetically distinct taxa than those found in other regions. Similar results were found by WILLIAMS & HUMPHRIES (1996), HACKER et al. (1998), POLASKY et al. (2001), and RODRIGUES & GASTON (2002) when comparing taxon richness versus taxonomic diversity and phylogenetic diversity (with branch lengths estimated assuming a molecular clock) using bird species from North America and African primates. They concluded that the congruence of methods is certainly not perfect, but when these methods are used for ranking areas for conservation priorities the general ranks tend to be the same. Therefore, our results also support the assertion that taxon richness is a good surrogate for phylogenetic diversity. It has been graphically illustrated that either measure based on the number of branching nodes (e.g. taxonomic diversity) or branch lengths (e.g. phylogenetic diversity) increases as taxa are added and are positively correlated to taxonomic richness (NEE & MAY, 1997; POLASKY et al., 2001; RODRIGUES & GASTON, 2002). However, extreme taxon richness is not the only way in which an area could make a large contribution to phylogenetic diversity. Scenarios can be proposed where both measures lead to different area rankings. If the tree is unbalanced with some of the branches being ramified (e.g. recent speciation process) while others correspond to older monophyletic taxa, and if there is a spatial segregation between sites where these two types of branches occur (e.g. due to a vicariance event), one would expect that taxonomic richness indices will tend to select sites with many closely related species while phylogenetic indices will tend to select sites with more distinct taxa. For example in the minimum evolution tree depicted in fig. 1 (2nd tree), an area represented by the twelve species in the top clade (Atacopsis and Euastacus) would have a PD of 1.0, while an area represented by the 3 species in its sister clade (Paranephrops and Parastacoides) would have a PD of 1.22. These two areas would clearly rank different for both indices. A parallel situation may also occur if the study area includes sites with marked differences in taxonomic structure (GASTON, 2000). The radiation of lemurs in Madagascar could be an example (HACKER et al., 1998).

Animal Biodiversity and Conservation 26.1 (2003)

Therefore, the use of phylogenetic–based information indices could help to assist decisions concerning conservation priorities because they consider the evolutionary component of biodiversity and allow identification of those areas that will ensure the preservation of evolutionary potential and phylogenetically different species (BROOKS et al., 1992). Indeed, as preserving genetic diversity is often a goal in conservation biology (TEMPLETON, 1991; CROZIER, 1992), it seems pertinent to include some measure of genetic distinctness into a weighting scheme for habitat preservation (CRANDALL, 1998). However, it has been suggested that no single measure is adequate for complete evaluation of biodiversity, so it seems more adequate to integrate different approaches to yield a broad perspective on conservation priorities (POSADAS et al., 2001). Either combining different biodiversity indices or developing measures that integrate ecological considerations of abundance, endemicity, and geographic distribution with the evolutionary history of the taxa as both topology and genetic divergence, will allow for a more accurate ranking of areas for conservation priorities. In this latter sense new biodiversity measures such as the “taxonomic endemicity standardized weight” index proposed by POSADAS et al. (2001) appears to be a promising rationale. A modification of this index to include genetic distinctiveness as genetic distances into the equation would be desirable.

Recommendations Given unlimited resources, the optimal way to compute conservation rankings is to use every species in reconstructing a phylogeny. In this way, the PD for every species present in an area could be summed up, resulting in an accurate representation of both species richness and genetic diversity. One of the major functional constraints of phylogenetic diversity measures is sampling (FAITH, 1992). Branch lengths are dependent on sister taxa, therefore if sampling is incomplete the resulting conservation priorities will vary greatly depending on the taxa chosen. If there is not an option of complete sampling a method must be chosen that best represents the available information. The subtle differences between the traditional and phylogenetic methods does not seem to be sufficient to warrant the added expense of obtaining sequence data for every taxon. However, phylogenetic distinctness measures appear to be very useful in providing information concerning which genera or species are the most genetically distinct. When one area or taxon must be chosen over another, information from PD values are extremely useful. Therefore, in ranking areas for conservation, we suggest that in cases of limited resources a species count be taken first, and then sufficient sequence data be obtained to compute phylogenetic diversity values.

Acknowledgements During the realization of this study M. Pérez– Losada was supported by the Fulbright Commission for Cultural, Educational and Scientific Exchange between the United States of America and Spain. This study was funded by a grant from National Science Foundation (NSF 0075600).

References BALMFORD, A., GREEN, M. J. B. & MURRAY, M. G., 1996. Using higher–taxon richness as a surrogate for species richness: I. Regional tests. Proceedings of the Royal Society of London, 263: 1,267–1,274. BROOKS, D. R., MAYDEN, R. L. & MACLENNAN, D. A., 1992. Phylogeny and biodiversity: conserving our evolutionary legacy. Trends in Ecology and Systematics, 7: 55–59. BROWN, J. H., 1988. Species diversity. In: Analytical biogeography: 57–89 (A. A. Myers & P. S. Giller, Eds.). London, Chapman & Hall. CRANDALL, K. A., 1998. Conservation phylogenetics of Ozark crayfishes: assigning priorities for aquatic habitat protection. Biological Conservation, 84: 107–117. CROZIER, R. H., 1992. Genetic diversity and the agony of choice. Biological Conservation, 61: 11–15. – 1997. Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annual Review of Ecology and Systematics, 28: 243–268. FAITH, D. P., 1992. Conservation evaluation and phylogenetic diversity. Biological Conservation, 61: 1–10. – 1994. Genetic diversity and taxonomic priorities for conservation. Biological Conservation, 68: 69–74. GASTON , K. J., 2000. Biodiversity: higher taxon richness. Progress in Physical Geography , 24: 117–127. HACKER, J. E., COWLISHAW, G. & WILLIAMS, P. H., 1998. Patterns of African primate diversity and their evaluation for the selection of conservation areas. Biological Conservation, 84: 251–262. HUMPHRIES, C. J., WILLIAMS, P. H. & VANE–WRIGHT, R. I., 1995. Measuring biodiversity value for conservation. Annual Review of Ecology and Systematics, 26: 93–111. KRAJEWSKI, C., 1994. Phylogenetic measures of biodiversity: a comparison and critique. Biological Conservation, 69: 33–39. MAY, R. M., 1981. Patterns in multiple species communities. In: Theoretical ecology, 2nd edition: 197–227 (R. M. May, Ed.). Sinauer Associates, Sunderland, Massachusetts. MORITZ, G. & FAITH, D. P., 1998. Comparative phylogeography and the identification of ge-

netically divergent areas for conservation. Molecular Ecology, 7: 419–429. N EE, S. & M AY , R. M., 1997. Extinction and the loss of evolutionary history. Science , 278: 692–694. NIXON, K. C. & WHEELER, Q. D., 1992. Measures of phylogenetic diversity. In: Extinction and phylogeny : 216–234 (M. J. Novacek & Q. D. Wheleer, Eds.) . Columbia University Press, New York. OWENS, I. P. F. & BENNETT, P. M., 1999. Quantifying biodiversity: a phenotipic perspective. Conservation Biology, 14: 1,014–1,022. PEREZ–LOSADA, M., JARA, C. G., BOND–BUCKUP, G. & CRANDALL, K. A., 2002. Conservation phylogenetics of Chilean freshwater crabs Aegla (Anomura, Aeglidae): assigning priorities for aquatic habitat protection. Biological Conservation, 105: 345–353. POLASKY, S., CSUTI, B., VOSSLER, C. A. & MEYERS, S. M., 2001. A comparison of taxonomic distinctness versus richness as criteria for setting conservation priorities from North American birds. Biological Conservation, 97: 99–105. POSADAS, P., MIRANDA ESQUIVEL, D. R. & CRISCI, J. V., 2001. Using phylogenetic diversity measures to set priorities in conservation: an example from southern South America. Conservation Biology, 15: 1325–1334. RICOTTA, C., FERRARI, M. & AVENA, G., 2002. Using the scaling behaviour of higher taxonomic taxa for the assessment of species richness. Biological Conservation, 107: 131–133. RODRIGUES, A. S. L. & GASTON, K. J., 2002. Maximising phylogenetic diversity in the selection of networks of conservation areas. Biological Conservation, 105: 103–111. S CHLUTER, D. & RICKLEFS, R. E., 1993. Species

Pérez–Losada & Crandall

diversity: an introduction to the problem. In: Species diversity in ecological communities: 1–10 (R. E. Ricklefs & D. Schluter, Eds.). Chicago University Press, Chicago. SOLOW, A., POLASKY, S. & BROADUS, J., 1993. On the measurement of biological diversity. Journal of Environmental Economics and Management, 24: 60–68. TEMPLETON, A. R., 1991. Genetics and conservation biology. In: Species conservation: a population–biological approach: 15–29 (A. Seitz & V. Loeschcke, Eds.). Birkhauser Verlag, Basel. THACKWAY, R. & CRESSWELL, I. D., 1995. An interim biogeographic regionalisation for Australia: a framework for establishing the national system of reserves. Australian Nature Conservation Agency, Canberra. VANE–WRIGHT, R. I., HUMPHRIES, C. J. & WILLIAMS, P. H., 1991. What to protect? Systematics and the agony of choice. Biological Conservation, 55: 235–254. WEITZMAN, M. L., 1992. On diversity. The Quarterly Journal of Economics, 107: 363-405. W HITING , A. S., LAWLER , S. H., HORWITZ, P. & CRANDALL, K. A., 2000. Biogeographic regionalization of Australia: assigning conservation priorities based on endemic freshwater crayfish phylogenetics. Animal Conservation, 3: 155–163. WILLIAMS, P. H. & HUMPHRIES, C. J., 1996. Comparing character diversity among biotas . In: Biodiversity: a biology of numbers and difference: 54–67 (K. J. Gaston, Ed.). Blackwell, Oxford. WILLIAMS, P. H., HUMPHRIES, C. J. & G ASTON, K. J., 1994. Centers of seed plant diversity: the family way. Proceedings of the Royal Society, Biological Sciences, 256: 67–70.

Animal Biodiversity and Conservation 26.1 (2003)

Consideraciones sobre la identidad de Onychochaeta elegans (Cognetti, 1905) (Oligochaeta, Glossoscolecidae) C. Rodríguez, A. G. Moreno & G. Cabrera

Rodríguez, C., Moreno, A. G. & Cabrera, G., 2003. Consideraciones sobre la identidad de Onychochaeta elegans (Cognetti, 1905) (Oligochaeta, Glossoscolecidae). Animal Biodiversity and Conservation, 26.1: 85–91. Abstract Considerations on the identity of Onychochaeta elegans (Cognetti, 1905) (Oligochaeta, Glossoscolecidae).— Anatomical variability of Onychochaeta elegans in Cuban populations was studied. A comparison among these populations and O. elegans cubana Michaelsen, 1924 and O. cubana Zicsi, 1995 from Cuba, as well as the descriptions of the typical form of Cognetti (1905) from Panama and Colombian specimens (Righi, 1995) was made. Besides, new materials from Mexico and Panama were added. Variations in anatomical characters in Cuban populations included those present in continental forms, so, there were not any character that justifies the division of O. elegans nor subspecies neither in distinct insular and continental species. Key words: Oligochaeta, Glossoscolecidae, Onychochaeta elegans, Anatomy, Taxonomy. Resumen Consideraciones sobre la identidad de Onychochaeta elegans (Cognetti, 1905) (Oligochaeta, Glossoscolecidae).— Se realizó un estudio de la variabilidad anatómica de Onychochaeta elegans (Cognetti, 1905) en poblaciones cubanas y se hizo una comparación con las poblaciones de O. elegans cubana Michaelsen, 1924 y de O. cubana Zicsi, 1995 de Cuba, así como las descripciones de la forma típica de Cognetti (1905) de Panamá y de Righi (1995) de Colombia. Además se adicionaron nuevos materiales colectados en México y Panamá. Las variaciones de los caracteres anatómicos analizados en las poblaciones cubanas incluyen las presentadas por las continentales por lo que no se evidencia carácter alguno que justifique la división de O. elegans en subespecies ni en una especie insular y otra continental. Palabras clave: Oligochaeta, Glossoscolecidae, Onychochaeta elegans, Anatomía, Taxonomía. (Received: 19 XI 02; Conditional acceptance: 31 I 03; Final acceptance: 21 II 03) Carlos Rodríguez, Dept. de Biología Animal y Humana, Fac. de Biología, Univ. de La Habana, Calle 25 entre J e I, Vedado, C. P. 10 400, C. de La Habana, Cuba. E–mail: crodri@fbio.uh.cu Ana G. Moreno, Dept. de Biología Animal I (Zoología), Fac. de Biología, Univ. Complutense, c/ José Antonio Novais, s/n, 28040 Madrid, España (Spain). Grisel Cabrera, Inst. de Ecología y Sistemática, Carretera de Varona, Km. 14, Capdevila, C. de La Habana, Cuba. Corresponding author: Ana G. Moreno. E–mail: agmoreno@bio.ucm.es

ISSN: 1578–665X

Rodríguez et al.

Introducción

Material y métodos

El género Onychochaeta fue establecido por BEDDARD (1891) para acomodar a O. windlei (Beddard, 1890), una especie de Venezuela que el propio autor había ubicado inicialmente en Diachaeta Benham, 1886. El género quedó definido por la presencia de setas distribuidas irregularmente en la parte posterior del cuerpo, poros masculinos "ubicados probablemente" en la zona clitelar, espermatecas localizadas antes de los segmentos de los testículos, molleja desarrollada en el segmento 6, el último par de corazones en el 11, nefridios con esfínter terminal, dos pares de testículos, dos pares de vesículas seminales en los segmentos 11 y 12 y la porción distal de los conductos deferentes sin modificaciones. Con posterioridad, CORDERO (1945) redefinió el género y adicionó los siguientes caracteres: setas dispuestas en 8 series longitudinales regulares o por lo menos en parte, presencia de tres pares de glándulas calcíferas en los segmentos 7–9 de estructura tubular simple o compuesta y metagino. El género Onychochaeta cuenta actualmente con cinco especies: O. windlei (Beddard, 1890), O. elegans (Cognetti, 1905), O. serieia Righi, 1971, O. borincana Borges, 1994 y O. cubana Zicsi, 1995. Se diferencian fundamentalmente por la disposición de las setas, la localización del clitelo, de los tubérculos pubertarios, de las espermatecas y por el patrón de papilas genitales. Según MICHAELSEN (1924), las poblaciones cubanas de O. elegans estaban representadas por una subespecie, O. elegans cubana que difería de la forma típica de COGNETTI (1905) de Panamá por la posición de los tubérculos pubertarios, la extensión del clitelo, la localización de las papilas genitales y la presencia o ausencia de vesículas seminales. RIGHI (1995) citó vesículas seminales en poblaciones colombianas y basó las diferencias entre las dos subespecies sólo en la posición de los tubérculos pubertarios. Por su parte, ZICSI (1995) elevó la subespecie cubana a la categoría de especie, apoyándose en la presencia de vesículas seminales, en el número de muescas en las setas genitales y en la posición de los poros masculinos. Sin embargo, para establecer estas categorías taxonómicas, ni MICHAELSEN (1924) ni ZICSI (1995) ni el propio COGNETTI (1905) tuvieron en cuenta la variabilidad intraespecífica de las poblaciones locales; de hecho las descripciones de COGNETTI (1905) y de MICHAELSEN (1924) se basaron, aparentemente, en un único ejemplar. En el presente artículo se hace una descripción de O. elegans y se estudian las variaciones intraespecíficas en poblaciones de Cuba con el objetivo fundamental de esclarecer el estatus taxonómico de esta especie. Además, se reunifica la información dispersa publicada sobre la misma. Por último, se incluye una diagnosis del género y se da una clave actualizada para sus especies.

Se realizaron colectas en diferentes tipos de ecosistemas a lo largo de la isla de Cuba, en México y en Panamá entre 1981 y 1999. Los ejemplares cubanos y mexicanos se encuentran depositados en la colección del laboratorio de Fauna del Suelo de la Facultad de Biología de la Universidad de La Habana (FBUH) y los panameños en la colección personal de la Dra. Ana G. Moreno en la Facultad de Biología de la Universidad Complutense de Madrid. Relación de ejemplares estudiados Cuba: 35 clitelados y 40 no clitelados procedentes de las provincias de Pinar del Río (Sierra del Rosario y San Cristóbal), Ciudad de La Habana (Capdevila y Santiago de las Vegas) y Matanzas (Jovellanos y Ciénaga de Zapata). México: 9 clitelados y 6 no clitelados colectados en Chetumal, Quintana Roo. Panamá: 28 clitelados recogidos en las provincias de Panamá (Ciudad de Panamá y Summit Garden), Coclé (El Caño y Santa Clara) y Los Santos (Parque Nacional Sarigua y Pocri). Los ejemplares de México y Panamá no se incluyeron en la descripción y sólo se usaron para compararlos con las poblaciones cubanas. Los animales se extrajeron manualmente del suelo. Los ejemplares cubanos y mexicanos se fijaron y conservaron en una solución de formalina al 4% (10 % de la solución comercial). Los animales panameños se fijaron en una mezcla a partes iguales de alcohol 96º y formalina al 4% y se conservaron en una solución de formalina al 4%. Para determinar las distancias setales en los segmentos donde se presenta una distribución irregular de las setas, se tomaron sólo las distancias entre las hileras regulares y la medida de la circunferencia del cuerpo en el mismo segmento (RODRÍGUEZ et al., en prensa).

Resultados y discusión

Onychochaeta elegans (Cognetti, 1905) Onychochaeta elegans (Cognetti, 1905). Sporadochaeta elegans Cognetti, 1905: 5. Onychochaeta elegans Michaelsen, 1918: 232. Onychochaeta elegans cubana Michaelsen, 1924: 4. Onychochaeta cubana Zicsi, 1995: 59.

Descripción Anatomía externa Longitud de 42 a 78 mm; diámetro postclitelar de 3 a 5 mm. Número de segmentos: 120–135. Peso: de 0,6 a 1,7 g. Cuerpo de forma cilíndrica en sección transver-

Animal Biodiversity and Conservation 26.1 (2003)

sal. No pigmentados; en individuos vivos se observa la región anterior de color amarillento, el clitelo amarillo verdoso y los tubérculos pubertarios de color blanco cremoso; el contenido intestinal se puede observar por transparencia. Los ejemplares conservados son beige a gris pálidos. Prostomio prolóbico, surge del techo de la cavidad bucal. Peristomio pequeño e invaginado con surcos longitudinales, al igual que los segmentos 2 y 3. Anillación doble en los segmentos de la región media del cuerpo, poco evidente en la zona preclitelar y ausente en el clitelo y en la región final del cuerpo. Setas lumbricinas, 8 por segmento, se inician en 3 a 5, distribuidas regularmente en la región preclitelar, cercanamente pareadas; en la región postclitelar las hileras b, c y d son irregulares. Las setas a se mantienen alineadas hasta pocos segmentos antes del pigidio desplazándose hacia la región dorsal. Distancias relativas entre las setas: segmento 10 (aa:ab:bc:cd:dd): 12,5:1:9:1:28,5; en la parte media del cuerpo (segmento 30) aa = 17,85 % de la circunferencia. Las setas somáticas están ornamentadas, presentando cuatro hileras alternas de excavaciones semilunares; dos a tres excavaciones por hileras. La longitud de las setas en la región media y posterior del cuerpo es de 250–270 µm. Las setas a o b de las papilas de los segmentos clitelares 18 y 22 son genitales, su longitud es aproximadamente de 1.280 µm y el diámetro de 60 µm, son ligeramente arqueadas hacia la base con el extremo apical aguzado; la mitad distal presenta cuatro hileras alternas de excavaciones semilunares que constituyen una depresión cuyo borde superior se hace continuo con la superficie de la seta. Las muescas de las hileras enfrentadas entre si forman pares, que alternan en posición con los pares formados por las de las otras dos hileras; cada hilera presenta de 7 a 10 excavaciones. Clitelo anular, con la región ventral menos desarrollada que la dorsal, ligeramente cóncava; se extiende del segmento 1/n 16, 16, 17 al 24; mantiene los surcos intersegmentarios, las setas ab y los poros nefridiales. Tubérculos pubertarios en la región ventrolateral de los segmentos 1/n19, 19–22, 23, laterales a b, en forma de una banda que se estrecha hacia los últimos segmentos de manera que los tubérculos en su conjunto adoptan una forma lanceolada, con el extremo más aguzado dirigido hacia atrás. Poros dorsales ausentes. Poros nefridiales conspicuos, dispuestos regularmente; en la región preclitelar se alinean con las hileras de setas cd. Los poros masculinos, femeninos y espermatecales no pueden distinguirse externamente por su pequeño tamaño, pero pueden localizarse mediante disección. Los poros masculinos desembocan en el intersegmento 19/20 a la altura de los tubérculos pubertarios; los

oviductos desembocan en la parte anterior del segmento 14 y los poros espermatecales se abren a nivel de cd en 6/7–8/9. Papilas genitales, redondeadas–elípticas, con distribución variable, pares o impares, en los segmentos 12, 13, 16, 18 y 22, asociadas a las setas a o b. Anatomía interna Primer septo 6/7, septos 6/7 al 13/14 musculares y distendidos hacia la parte posterior del cuerpo, de manera que forman conos imbricados, septo 14/15 menos grueso, el resto membranosos. Molleja en 6. La mucosa esofágica forma criptas amplias y ligeramente ramificadas (tejido calcífero) en 7–11. Tres pares de glándulas calcíferas de estructura tubular en 7, 8 y 9, ubicadas en la parte ventrolateral de cada segmento dirigidas hacia abajo y hacia delante. Comienzo del intestino en el segmento 16 ó 17. El tiflosol comienza, de una forma brusca, a partir del segmento 27 y termina entre el 80 y el 82, adelgazándose progresivamente. Es una lámina gruesa, simple y plegada; su profundidad en la porción media del intestino, es aproximadamente el diámetro del lumen del intestinal. Ciegos ausentes. Dos pares de grandes corazones intestinales en 10 y 11 y tres pares de finos corazones laterales de 7–9. Vaso dorsal moniliforme, alcanza su mayor desarrollo en el segmento 18. Vaso supraesofágico comienza en 7 y se mantiene hasta el 12. Vaso subneural presente. Holonefridios con esfínteres terminales voluminosos y cónicos; consisten en un simple embudo preseptal y tres lazos postseptales, uno medio y dos laterales al lado de la vejiga. En la parte anterior se presentan ramilletes de meganefridios sobre la faringe y la molleja. Holándrica, con un par de testículos y de embudos seminales de aspecto iridiscente en cada uno de los segmentos 10 y 11. Sin sacos testiculares (gimnorquídica). Dos pares de vesículas seminales, en 11 y 12, cortas, confinadas en sus segmentos de origen. Vasos deferentes intraparietales, los de cada lado se fusionan en el segmento 13 y desembocan en el intersegmento 19/20 a la altura de los tubérculos pubertarios. Un par de ovarios y de embudos ováricos en el segmento 13; los oviductos desembocan en la parte anterior del segmento 14. Tres pares de espermatecas intracelómicas, en 7, 8 y 9 que abren a nivel de cd en 6/7–8/9; ampollas piriformes, aplanadas y sin divertículo; conducto algo más largo que la ampolla y se transforma gradualmente en ésta, ambos contienen espermatozoides. Variabilidad intraespecífica La longitud y el peso de O. elegans fueron los caracteres morfométricos más variables (tabla 1),

Rodríguez et al.

Tabla 1. Morfometría de individuos clitelados N = 35 y no clitelados (entre paréntesis) N = 40, de O. elegans en poblaciones cubanas: X. Media; d.e. Desviación estándar; C.V. Coeficiente de variación.

Table 1. Morphometry of clitellate N = 35 and non clitellate individuals (in brackets) N = 40, of O. elegans in Cuban populations: X. Mean; d.e. Standard deviation; C.V. Coefficient of variation.

Caracteres Longitud total (mm) Diámetro postclitelar (mm) o

N de segmentos Peso (g)

Mínimo

Máximo

d.e.

42(25)

78 (70)

56,20 (47,32)

3 (2)

5 (4)

4,17 (3, 42)

0,51 (0,59)

C.V.

8,97 (12,17) 15,98 (25,73) 12,31 (17,35)

120 (94)

135 (135)

130 (125)

3,94 (10,78)

3,02 (8,63)

0,51 (0,15)

1,69 (1,43)

1,08 (0,69)

0,36 (0,40)

33,08 (57,49)

encontrándose individuos en las poblaciones con tallas y pesos pequeños pero con caracteres sexuales externos desarrollados. En las poblaciones de las lombrices de tierra se encuentran con frecuencia especímenes que alcanzan la madurez sexual con un grado de crecimiento variable; así lo han demostrado las observaciones en Eudrilus eugeniae (Kinberg, 1867), Eisenia fetida (Savigny, 1826), Polypheretima elongata (Perrier, 1872) y Millsonia anomala Omodeo, 1954, entre otras (RODRÍGUEZ & REINÉS, 1986; RODRÍGUEZ et al., 1986; RODRÍGUEZ & ROCHA, 1993; REINECKE & VILJÖEN, 1988; LAVELLE et al., 1989). Este hecho podría estar relacionado con las condiciones ambientales (humedad y alimento, fundamentalmente) donde ha vivido el individuo (EDWARDS & BOHLEN, 1996; SIERRA & RODRÍGUEZ, 1996). El número de segmentos es el carácter con menos variación (tabla 1), lo que supone que la longitud del animal depende más del tamaño de los segmentos que no de su número. Respecto a otros caracteres externos, el material revisado mostró que el clitelo se extiende del segmento 17 al 24, pero en individuos muy maduros sexualmente puede abarcar además el 16; mientras que los tubérculos pubertarios se observaron con constancia entre el 19 y el 23, excepto pocos casos que sólo comprendieron hasta el 22. Todos los ejemplares estudiados presentaron papilas genitales en los segmentos 12, 13, 16, 18 ó 22. El patrón de su distribución constituye uno de los caracteres que exhibe mayor variabilidad, presentando un elevado número de combinaciones que involucran la presencia o ausencia de papilas y su condición de imparidad o duplicidad en el segmento (tabla 2). Las papilas se localizan en un sólo segmento (4,5% de la población), en dos segmentos (58%), en tres (27,5%), en cuatro (6,4%) o en cinco (3,6%). Las papilas de los segmentos 12 y 18 se presentan en más del 80% de los ejemplares y la mayoría de las veces son

Tabla 2. Patrón de distribución de las papilas genitales de O. elegans en poblaciones cubanas: S. Segmento; P. Presencia (%); Pp. Papilas pares (%); Pi. Papilas impares (%); D. Derecha; I. Izquierda.

Table 2. Distribution of genital marks in cuban populations of O. elegans: S. Segment; P. Presence; Pp. Pair papillae; Pi. Odd papillae; D. Right; I. Left. Pi S

16,5

33,3

21,7

41,7

58,3

100

pareadas, mientras que las del segmento 16 se encuentran en algo más de la mitad de la población, de forma par o impar. La presencia de papilas en los segmentos 13 y 22 es baja. Taxonomía La separación entre O. elegans y O. cubana se basa en la presencia o ausencia de las vesículas seminales, la posición de los poros masculinos y el número de muescas de las setas genitales. La colecta de animales con vesículas seminales en poblaciones de Colombia (RIGHI, 1995), de México: Quintana Roo y Calakmul (Fragoso, com.

Animal Biodiversity and Conservation 26.1 (2003)

Tabla 3. Caracteres anatómicos comparativos de O. elegans procedentes de diferentes poblaciones: Oee. O. e. elegans Cognetti, 1905 de Panamá; Oe. O. elegans, este estudio de Panamá; Oec. O. e. cubana Michaelsen, 1924 de Cuba; Oc. O. cubana Zicsi, 1995 de Cuba; Oe. O. elegans, este estudio de Cuba; Oee. O. e. elegans Righi, 1995 de Colombia; Oe. O. elegans, este estudio de México; N. Número de ejemplares; L. Longitud (en mm); A. Ancho (en mm); Nºseg. Número de segmentos; Tp. Tubérculos pubertarios; Pg. Papilas genitales; Vs. Vesículas seminales; Pm. Poros masculinos; Msg. Muescas setas genitales; Dsg18. Dimensiones de las setas genitales del segmento 18 (en µm).

Table 3. Anatomic characters of O. elegans in different populations: Oee. O. e. elegans Cognetti, 1905 from Panamá; Oe. O. elegans, this study from Panamá; Oec. O. e. cubana Michaelsen, 1924 from Cuba; Oc. O. cubana Zicsi, 1995 from Cuba; Oe. O.elegans, this study from Cuba; Oee. O. e. elegans Righi, 1995 from Colombia; Oe. O. elegans, this study from México; N. Number of specimens; L. Length (in mm); A. Width (in mm); Nºseg. Number of segments; Tp. Tuberculum; Pg. Genital markings; Vs. Seminal vesicles; Pm. Male pores; Msg. Genital setae excavations; Dsg18. Genital setae size of segment 18th (in µm).

Panamá

Cuba

Colombia

México

Oee

Oec

Oee

50,00

A Nºseg

50–80

75,00

–

4,50

4–6

4,50

–

4,12(3–5)

3,5–6,1

3–4,5

130

117–145

128

–

130(120–135)

155–162

119–143

Clitelo

16–24

16,17–24

17–24

16,17–23,24

16–24 y 17–24

19–23

19–22

19–23

19–22,23

1/n 19–23

19–23

12,13, 18 y 22

Sin papilas 12,13,16 y 18

12 y 16

12 y 18

12,13,16 18 y 22

16,18 22 y 23

12,13,16 18 y 22

11 y 12

19/20

–

20/21

19/20

Msg

7–10

10–12

–

Dsg18

–

1.400x50

1.200x50

–

1.200x 60

1.852–1.993

–

pers.) y fundamentalmente de Panamá (tabla 3) no justifica ya la separación de ambas especies. La ausencia de vesículas seminales en el ejemplar de Panamá descrito por COGNETTI (1905) podría interpretarse como una anomalía, teniendo en cuenta además, que los ejemplares panameños de Pocri presentaron una parasitación masiva de gregarinas, lo que suele provocar castración parasitaria e impide el desarrollo de las vesículas seminales (GATES, 1956). ZICSI (1995) ubica los poros masculinos en 20/21, lo cual no coincide con la localización de los mismos en el resto de los ejemplares citados por los demás autores (tabla 3). Teniendo en cuenta además, que los materiales trabajados por Zicsi proceden, en parte, de las mismas localidades que las incluidas en este artículo, se considera que la posición de los poros masculinos tampoco es un criterio válido para la separación de ambas especies; así mismo ocurre con el número de muescas de las setas genitales, ya que las diferencias están

56,20(42–78)

95–115

38–81

1/n 16–24 1/n16,16,17–23,4

comprendidas en el rango de variabilidad de este carácter (tabla 3). Se sugiere como hipótesis que el número de muescas podría estar relacionado con el tamaño de los ejemplares y por lo tanto con el de sus setas (tabla 3), esto implicaría que este carácter sería poco útil para la diferenciación de especies. Por lo anteriormente expuesto, se concluye que no existe ningún criterio para separar ambas especies y, por lo tanto, se considera que O. cubana Zicsi, 1995 es una sinonimia de O. elegans (Cognetti, 1905). Distribución de la especie El número entre paréntesis detrás de cada localidad denota los individuos colectados y representan: Juveniles, sin caracteres sexuales externos; No clitelados, con caracteres sexuales externos, pero sin clitelo; Clitelados, adultos con el clitelo desarrollado.

Rodríguez et al.

Clave para las especies del género Onychochaeta (fig. 1). Key for the species of genera Onychochaeta (fig. 1).

1. Tubérculos pubertarios en 19 ó 20 al 22 ó 23. Sin sacos testiculares Tubérculos pubertarios del 22 al 26. Con sacos testiculares 2. Setas a dispuestas regularmente a través del cuerpo y setas b, c y d dispuestas irregularmente por detrás del clitelo Todas las setas están dispuestas irregularmente 3. Tubérculos pubertarios 20–22. Espermatecas en 7, 8 y 9 Tubérculos pubertarios 19–21. Espermatecas en 6, 7 y 8

Cuba: Pinar del Río, Sierra del Rosario (4–3–5) FBUH 100; San Cristobal (0–0–4) FBUH 215, Candelaria, La Caridad (9–0–6) FBUH 226, Candelaria, Soroa (0–0–4) FBUH 276; Ciudad de La Habana, Santiago de las Vegas (25–38–31) FBUH 007, Capdevila (0–0–3) FBUH 079, Vedado (1–0–2) FBUH 094; Parque Almendares (3–0–6) FBUH 217; San-

O. serieia O. elegans 3 O. windlei O. borincana

tos Suárez (2–0–6) FBUH 247, El Sevillano (0–0– 1) FBUH 248; La Habana, San José de Las Lajas (6–3–7) FBUH 235; El Rincón (MICHAELSEN, 1924); Matanzas, Ciénaga de Zapata (0–0–2) FBUH 096, Jovellanos (1–0–4) FBUH 169; Villa Clara, Encrucijada (2–1–1) FBUH 236; Cienfuegos, Palmira (0– 0–1) FBUH 174; Sancti Spíritus, Márgenes de la

22 21

1 mm

C 19

22 26

1 mm 1 mm Fig. 1. Vista ventral del clitelo: A. O. borincana; B. O. windlei; C. O. elegans; D. O. serieia. Fig. 1. Clitellum, ventral view: A. O. borincana; B. O. windlei; C. O. elegans; D. O. serieia.

Animal Biodiversity and Conservation 26.1 (2003)

presa Zaza (0–2–3) FBUH 066; Camagüey, La Paz (Zicsi, 1995); Holguín, Pinares de Mayarí (5–1–0) FBUH 315; Santiago de Cuba, Gran Piedra; Santiago de Cuba (ZICSI, 1995). México: Quintana Roo, Chetumal (35–0–15) FBUH 286. Panamá: Panamá (Ciudad de Panamá y Summit Garden), Coclé (El Caño y Santa Clara), Los Santos (Parque Nacional Sarigua y Pocri) (0–0–28); Darien (COGNETTI, 1905). Colombia: Tolima, Venadillo (RIGHI, 1995). Género Onychochaeta Beddard, 1891 emend. Cordero, 1945 Diagnosis Con 8 setas por segmento, dispuestas en hileras irregulares. Un par de poros masculinos intraclitelares. Molleja en 6. Tres pares de glándulas calcíferas en los segmentos 7–9, de estructura tubular y origen ventral. Holándrico. Con o sin sacos testiculares (cleistorquídica o gimnorquídica). Con vesículas seminales cortas. Sin cámaras copulatorias. Metagino. Espermatecas presentes. Lista de especies y distribución:

O. elegans (Cognetti, 1905) (Cuba, Panamá, México y Colombia) O. serieia Righi, 1971 (Brasil) O. borincana Borges, 1994 (Puerto Rico) O. windlei (Beddard, 1890) (Bermudas, Cuba, La Española, Islas Vírgenes, Venezuela y Surinam). Se adjunta clave de identificación de las especies del género Onychochaeta.

Agradecimientos Los autores agradecen a CYTED (Programa de Cooperación Iberoamericana, Ciencia y Tecnología para el Desarrollo) mediante el proyecto precompetitivo XII. 3 "Diversidad de la Macrofauna de Invertebrados del Suelo: Implicaciones Ecológicas" (Subprograma Diversidad Biológica), por el apoyo financiero otorgado a C. Rodríguez para realizar una estancia de trabajo en la Universidad Complutense de Madrid con el fin de revisar las colecciones de la Dra. A. G. Moreno y escribir el presente artículo.

Referencias BEDDARD , F. E., 1891. The classification and distribution of earthworms. Proc. Phys. Soc. Edinb., 10: 235–290.

COGNETTI , L., 1905. Oligocheti raccolti nel Darien dal Dr. E. Festa. Boll. Mus. Torino, 20(495): 1–7. CORDERO, E. H., 1945. Oligoquetos sudamericanos de la familia Glosssoscolecidae, VI. Los géneros de la Subfamilia Glossoscolecinae, sus probables relaciones filéticas y su distribución geográfica actual. Comun. Zool. Mus. Hist. Nat. Montevideo, 1(22): 1–28. EDWARDS, C. A. & BOHLEN, P. J., 1996. Biology and Ecology of earthworms. Chapman and Hall, 3th edition, London. GATES, G. E., 1956. Reproductive organ polymorphism in earthworms of the oriental Megascolecine genus Pheretima Kinberg 1867. Evolution, 10(2): 213–227. LAVELLE, P., BAROIS, I., MARTÍN, Z. & SCHAEFER, R., 1989. Management of earthworms population in agroecosystems: a possible way to maintain soil quiality? In: Ecology of arable land: 109122 (M. Clarholm & L. Bergström, Eds.). Kluwer Academic Publishers., Dordrecht, The Netherlands. M ICHAELSEN , W., 1924. Oligocheten von der warmeren Amerikas und des Atlantische Ozean. Mitt. Zool. Mus. Hamburg, 41: 74–76. REINECKE, A. J. & VILJÖEN, S. A., 1988. Reproduction of the African earthworms, Eudrilus eugeniae (Oligochaeta) cocoons. Biol. Fertil. Soils., 7: 23–27. RIGHI, G., 1995. 16 Colombian earthworms. In: Studies on tropical Andean Ecosystems 4: 485– 607 (T. Van der Hammen & A. G. Santos, Eds.) Cramer (Bomtraeger), Berlin–Stuttgart. RODRÍGUEZ, C., CANETTI, M. E., REINÉS, M. & SIERRA, A., 1986. Ciclo de vida de Eudrilus eugeniae (Oligochaeta: Eudrilidae) a 30 C. Poeyana, 326: 1–13. RODRÍGUEZ, C. A. MORENO, G. & BORGES, S. (en prensa). Aproximación a la filogenia y biogeografía del género Diachaeta Benham, 1886 (Oligochaeta: Glossoscolecidae). Caribbean Journal of Science. RODRÍGUEZ, C. & REINÉS, M., 1986. Morfología de Polypheretima elongata (Oligochaeta: Megascolecidae) en una población cubana. Poeyana, 325: 1–10. RODRÍGUEZ, C. & ROCHA, I., 1993. Crecimiento en peso, longitud y número de segmentos de Eudrilus eugeniae (Oligochaeta: Eudrilidae). Rev. Biología, 6(3): 215–221. SIERRA, A. & RODRÍGUEZ, C., 1996. Influencia del alimento en el desarrollo embrionario de Eudrilus eugeniae (Oligochaeta: Eudrilidae). Rev. Biología, 10: 12–21. Z ICSI , A., 1995. Ein weiterer Beitrag zur Regenwurm–fauna der Karibischen Region (Oligochaeta). Regenwürmer aus Südamerika 24. Mitt. Hamb. Zool. Mus. Inst., 92: 53–64.

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 26.1 (2003)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter disciplinària publicada, des de 1958, pel Museu de Zoologia de Barcelona. 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 énfa sis 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 inter net a http://www.museuzoologia.bcn.es/servis/servis3. htm, de manera que permet una difusió mundial dels seus articles. Tots els manuscrits són revisats per l'editor executiu, 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.

Normes de publicació Els treballs s'enviaran preferentment de forma electrò nica (abc@mail.bcn.es). El format preferit és un do cument 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 investi gacions 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 programa 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 ISSN: 1578–665X

sense càrrec a més d'una separata electrònica en format PDF. Manuscrits 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 cien tífics de gèneres i d’espècies i per als neologismes 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. Format dels articles Títol. El títol serà concís, però suficientment indi cador del contingut. Els títols amb designacions de sèries numèriques (I, II, III,...) 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. © 2003 Museu de Ciències Naturals

(Títol, Nom, Abstract, Key words, Resumen, Palabras 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, mètodes 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 species 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 con servation 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 tre ball 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)...” Quan en el text s’anomeni un autor de qui no es dóna referència bibliogràfica el nom anirà en rodona: “...un altre autor és Caughley...” 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,... i han de ser sempre ressenya des 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 autors. 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, Discu sión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols. Els autors procuraran que els seus treballs origi nals 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 26.1 (2003)

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, morfolo gía, biogeografía, ecología, etología, fisiología y genética) 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 registrada en todas las bases de datos importan tes y además está disponible gratuitamente en internet en http://www.museuzoologia.bcn.es/servis/ servis3.htm, 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 siempre 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 pro piedad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reproducida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@mail.bcn.es). El formato prefe rido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras (TIF). Si se opta por la versión impresa, deberán remitirse cuatro co pias 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 publi cadas 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 necesarios 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 deberán enviar a la Redacción una copia impresa de la versión final junto con un disquete del ma nuscrito preparado con un procesador de textos e ISSN: 1578–665X

indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modificaciones sustanciales en las prue bas de imprenta, introducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del tra bajo 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 espa cio 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 ninguno, 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 comi llas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el tra bajo, 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 escri birán 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 consentimiento 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, resultados y discusión). Se evitarán las © 2003 Museu de Ciències Naturals

especulaciones y las citas bibliográficas. Irá enca bezado 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. 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 antecedentes del tema tratado, así como de los objetivos del trabajo. Material y métodos. Incluirá la información refe rente a las especies estudiadas, aparatos utilizados, metodología 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 publica ciones 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 species 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 con servation 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 prospeccio nes realizadas (Begon et al., 1999)..." Cuando en el texto se mencione un autor no incluido en la bibliografía el nombre irá en redonda: "...otro autor es Caughley..." Tablas. Las tablas se numerarán 1, 2, 3, etc. y se re señarán 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 26.1 (2003)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal which has been published by the Zoolo gical Museum 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 on line at http://www.museuzoologia.bcn.es/servis/ABCag. htm, 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 written in capital letters. When referring to a spe cies for the first time in the text, both common and scientific names must be given when possible. Place names may appear either in their origi nal 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 document Rich Text Format (RTF) or DOC, including figures (TIF). In the case of sending a printed version, four copies should be sent together with a copy on a computer disc to the Editorial Office. A cover letter stating that the article reports on original research not published elsewhere and that it has been submitted exclusively for 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,...) 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 au thors 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 © 2003 Museu de Ciències Naturals

aims of the paper. Material and methods. This section should provide relevant information on the species studied, ma terials, 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 bi bliography 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 species 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 con servation 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. Biblio graphic 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)..." When an author is mentioned in the text but no bibliographical reference is given, the name must appear in ordinary print: "...another of these authors is Caughley..." Tables. Tables must be numbered in Arabic nu merals 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 photo graphs) must be termed as figures, numbered conse cutively in Arabic numerals 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 me thods, Results, Discussion, Acknowledgements and References) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages inclu ding 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 26.1 (2003)

VII

Animal Biodiversity and Conservation Subscription Form  Please enter our subscription to Animal Biodiversity and Conservation  66.11 € Spain  68.52 € Europe  69.12 € rest of world  Single use subscription:  21.04 € Spain  23.4 4 € Europe  24.04 € rest of world  Please despatch my issues by air mail (supplement of 6.01 € for outside Europe)  Please send me the Instructions to authors

Name Institution

Address

Payment method  Cheque payable to Associació d'Amics del Museu de Zoologia de Barcelona and drawn against a Spanish bank  Visa credit card Card number Valid until  Please send a proforma invoice

Date

Send this order form to: Associació d'Amics del Museu de Zoologia de Barcelona Museu de Ciències Naturals Psg. Picasso s/n 08003 Barcelona, Spain Fax: +34–93–3104999

Signature

VIII

Welcome to the electronic version of Animal Biodiversity and Conservation

ele

ctr on

lib

http://www.museuzoologia.bcn.es/servis/ABCag.htm

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

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

Les cites o els abstracts dels treballs d’aquesta publicació es resenyen a / Las citas o los abstracts de los trabajos de esta publicación se mencionan en / This publication 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 26.1 (2003) ISSN 1578–665X

1–7 Baehr, M. Further new species of the genus Dolichoctis Schmidt–Göbel from New Guinea and surrounding islands (Insecta, Coleoptera, Carabidae, Lebiinae) 9–20 Emerson, B. C. Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria 21–29 Guéorguiev, B. Two new species of the genus Laemostenus (Pristonychus) Bonelli from Bulgaria and notes on L. (P.) euxinicus Nitzu (Coleoptera, Carabidae)

45–55 Lahti, D. C. A case study of species assessment in invasion biology: the Village Weaverbird Ploceus cucullatus 57–65 Luiselli, L. & Akani, G. C. An indirect assessment of the effects of oil pollution on the diversity and functioning of turtle communities in the Niger Delta, Nigeria 67–76 Miñano P. A., García–Mellado, A., Oliva–Paterna, F. J. & Torralva, M. Edad, crecimiento y reproducción de Gobio gobio L. (Pisces, Cyprinidae) en un tramo regulado del río Segura (SE España)

31–39 Guerao, G. Some observations on the life history of the freshwater amphipod Echinogammarus longisetosus Pinkster, 1973 (Gammaridae) from Catalonia (Spain, N Iberian peninsula)

77–84 Pérez–Losada, M. & Crandall, K. A. Can taxonomic richness be used as a surrogate for phylogenetic distinctness indices for ranking areas for conservation?

41–44 Haitlinger, R. A new larval trombidiid, Calctrombidium nikolettae n. gen., n. sp. (Acari, Prostigmata, Trombidiidae, Trombidiinae) from India

85–91 Rodríguez, C., Moreno, A. G. & Cabrera, G. Consideraciones sobre la identidad de Onychochaeta elegans (Cognetti, 1905) (Oligochaeta, Glossoscolecidae)