Animal Biodiversity and Conservation issue 31.2 (2008) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2008

and

Animal Biodiversity Conservation 31.2

Dibuix de la coberta: escurçó ibèric, víbora hocicuda, Lataste's viper (Vipera latasti) de Jordi Domènech Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

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

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

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

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

Animal Biodiversity and Conservation 31.2, 2008 © 2008 Museu de Ciències Naturals, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Romargraf S. A. ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://www.bcn.cat/ABC

Animal Biodiversity and Conservation 31.2 (2008)

Branchiosyllis salazari sp. n. (Polychaeta, Syllidae) del Caribe noroccidental y comentarios sobre el material tipo de B. exilis (Gravier, 1900) J. D. Ruiz–Ramírez & L. H. Harris

Ruiz–Ramírez, J. D. & Harris, L. H., 2008. Branchiosyllis salazari sp. n. (Polychaeta, Syllidae) del Caribe noroccidental y comentarios sobre el material tipo de B. exilis (Gravier, 1900). Animal Biodiversity and Conservation, 31.2: 1–9. Abstract Branchiosyllis salazari n. sp. (Polychaeta, Syllidae) from Northwestern Carribean with notes on type material of B. exilis (Gravier, 1900).— On the basis of 195 specimens from the Northwestern Caribbean Sea, a new species of Branchiosyllis Ehlers, 1887 is described. Branchiosyllis salazari n. sp. has three pairs of eyes (two small pairs above the anterior margin of the prostomium, the third pair in a transverse line), without branchia, setae with large hooked blades in median setigers, and proventricle without middorsal line. The type material of B. exilis (Gravier, 1900), an apparently circumtropical species, was revised to clarify its presence in the Caribbean Sea. Its diagnostic features are: two pairs of eyes in a transverse line, no branchia, setae with large hooked blades in posterior setigers only, and proventricle with a middorsal line of diamond–shaped cells. A key for the seven species of Branchiosyllis in the Grand Caribbean is included. Key words: Branchiosyllis salazari n. sp., Taxonomy, Grand Caribbean, Syllidae, Polychaeta. Resumen Branchiosyllis salazari sp. n. (Polychaeta, Syllidae) del Caribe noroccidental y comentarios sobre el material tipo de B. exilis (Gravier, 1900).— Basándonos en el estudio de 195 ejemplares procedentes del Caribe Noroccidental, se describe una nueva especie de Branchiosyllis Ehlers, 1887. Branchiosyllis salazari sp. n. tiene tres pares de ojos (dos pares pequeños en el margen anterior del prostomio, el tercer par está en una línea transversal), sin branquias, sedas con artejo en forma de ganchos grandes ya en los setígeros medios, y proventrículo sin línea mediodorsal. El material tipo de B. exilis (Gravier, 1900), una especie aparentemente circuntropical, fue revisado para clarificar su presencia en el Mar Caribe. Sus características diagnósticas son: dos pares de ojos en una línea transversa, sin branquias, sedas con artejo en forma de gancho grande restringidas a los setígeros posteriores y proventrículo con una línea mediadorsal de células en forma de diamante. Se anexa una clave para las siete especies de Branchiosyllis en el Gran Caribe. Palabras clave: Branchiosyllis salazari sp. n., Taxonomía, Gran Caribe, Syllidae, Polychaeta. (Received: 22 X 07; Conditional acceptance: 10 I 08; Final acceptance: 15 IV 08) Jenifer D. Ruiz–Ramirez(1), Depto. de Ciencias, Univ. de Quintana Roo (dirección actual) y Laboratorio de Bentos, El Colegio de la Frontera Sur–Unidad Chetumal (dirección anterior). Boulevard Bahía esquina Ignacio Comonfort, C. P. 77019 Quintana Roo, México.– Leslie H. Harris(2), LACM–Allan Hancock Foundation Polychaete Collection, National History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, U.S.A. (1) (2)

E–mail: jenifer@uqroo.mx E–mail: lhharris@bcf.ucr.ac.cr

ISSN: 1578–665X

Ruiz–Ramírez & Harris

Introducción El género Branchiosyllis fue propuesto por Ehlers (1887) con B. oculata Ehlers, 1887 como especie tipo. Sus características diferenciales son poseer antenas (tres) y cirros tentaculares y cirros dorsales articulados, parápodos con o sin lóbulos pre– y postsetales largos y digitiformes, y faringe eversible. Algunas o todas sus sedas poseen artejos en forma de gancho (Fauchald, 1977; Uebelacker, 1984). El nombre genérico Branchiosyllis, implica la presencia de branquias. Entre los poliquetos, las branquias se definen como expansiones del tegumento, distinguiendo entre las huecas y conectadas al celoma (celobranquias) y las provistas de un vaso sanguíneo o eubranquias (Fauvel, 1959). Las primeras observaciones de poliquetos vivos, mostraron que las branquias eran dorsales y se asociaban por lo general con los parápodos. Por ello, Ehlers consideró que las expansiones presentes en su especie tenían función respiratoria y, por su rareza en la familia, que constituían un argumento suficiente para proponer un nuevo género. Sin embargo, hasta donde sabemos, no se ha estudiado la estructura fina de estas proyecciones o lóbulos por lo que su función branquial no se ha confirmado. Según Fauchald (1977) y San Martín & Bone (1999) se conocen seis especies de Branchiosyllis: B. abranchiata Hartmann–Schröder, 1965 (Samoa), B. diazi Rioja, 1958 (Golfo y Caribe mexicano), B. exilis (Gravier, 1900) (Mar Rojo y aparentemente circuntropical?), B. lorenae San Martín & Bone, 1999 (Venezuela), B. oculata Ehlers, 1887 (Mar Caribe) y B. pacifica Rioja, 1941 (Pacífico mexicano). Aunque Licher (1999) menciona en su revisión a B. maculata (Imajima, 1966) (Japón), B. salina (Hartman–Schröder, 1959) (El Salvador) y B. verruculosa (Augener, 1913) (Australia) y coincide con el número San Martín (2003) en su revisión para la fauna ibérica. Las especies del género se separan por la disposición de los ojos, el patrón de las antenas, la presencia de las branquias y por la presencia de sedas falcígeras compuestas combinadas con grandes sedas compuestas con artejos en forma de gancho, bien en todo el cuerpo o sólo en una parte. Sin embargo, estas características merecen revisarse en una comparación con materiales tipo y adicionales, de distintas localidades del mundo, para estandarizar su variación y definir la presencia de especies de amplia o limitada distribución. En particular, B. exilis es la especie de aparentemente mayor área de distribución, incluyendo al Gran Caribe, y podría tratarse de un complejo de especies, por lo que consideramos necesario revisar el material tipo. Material y métodos El material tipo de Branchiosyllis exilis (Gravier, 1900) se estudió en el Museum National d´Histoire Naturelle (MNHN) de París. El paratipo de Branchiosyllis salazari sp. n. se encuentra depositado en el National History Museum of Los Angeles (LACM–AHF). Los 195 ejemplares examinados pertenecen a la Colec-

ción de Referencia del Laboratorio de Bentos de El Colegio de la Frontera Sur. Las hileras de células musculares del proventrículo se abrevian HCM y las proporciones (L/AM) se refieren a la relación entre la longitud y la anchura máxima del artejo de las sedas falcígeras compuestas. Se consultó la lista de especies registradas en el Gran Caribe para la elaboración de la clave a especies de Branchiosyllis (Salazar–Vallejo, 1996). Resultados Familia Syllidae Grube, 1850 Subfamilia Syllinae Grube, 1850 Género Branchiosyllis Ehlers, 1887 Branchiosyllis exilis (Gravier, 1900) (figs. 1A–1F)

Syllis (Typosyllis) exilis Gravier, 1900: 160–162, lám. 9, fig. 9. Syllis (Typosyllis) fusco–suturata Augener, 1924: 43. Syllis (Typosyllis) fusco–suturata Augener, 1927: 52. Syllis (Typosyllis) exilis Hartmann, 1959: 230. Branchiosyllis exilis Westheide, 1974: 62–64, fig. 26 (sinonimia); Uebelacker, 1982: 583–584; Uebelacker, 1984: 30–105–30–106, fig. 30–100.

Diagnosis Basada en la descripción original (Gravier, 1900), se resaltan únicamente los caracteres más importantes. Holotipo (MNHN–A74) con 60 setígeros, la parte posterior estaba en regeneración (fig. 1B). Coloración ausente. Prostomio acorazonado posteriormente por la presencia de órganos nucales, antenas laterales situadas frente a los ojos, moniliformes, la izquierda con 15 artejos; la derecha ausente, antena central, entre los ojos internos. Cuatro ojos aparentemente dispuestos en una sola línea, los exteriores de mayor tamaño (fig. 1A). Cirros tentaculares, dorsales y anales ausentes. Palpos separados en la base con un amplio espacio entre ellos, de tamaño similar al prostomio. Faringe ocupando seis setígeros; proventrículo con 35 HCM, con una fila mediodorsal de células romboidales, a partir de la quinta HCM y hasta la cuarta HCM posterior (fig. 1C). Parápodos anteriores con diez sedas falcígeras largas (L/AM 5:1) y dos acículas, una en forma de L y otra oblicua distalmente hinchada (fig. 1D); parápodos medios con cuatro medias, sedas falcígeras largas (L/AM = 2.5:1) y dos acículas, una en forma de L y otra oblicua, con una ligera constricción subdistal (fig. 1E); parápodos posterioes con dos sedas en forma de gancho (L/AM = 2:1) y una acícula aguzada con punta oblicua (fig. 1F). Branchiosyllis exilis, junto con otras especies de distintas localidades, fue sinonimizado con la especie antillana Syllis (Typosyllis) fuscosuturata Augener, 1922, siendo considerada circuntropical (Westheide, 1974). Sin embargo, la comparación con ejemplares del Pacífico americano, incluyendo Galápagos, permitió reconocer varias diferencias con la especie antillana (Monro, 1933a), por lo que es posible que las formas ubicadas a ambos lados de Panamá sean distintas. Por ejemplo, la pigmentación es variable; los ejemplares de Curaçao

Animal Biodiversity and Conservation 31.2 (2008)

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Fig. 1. Branchiosyllis exilis (Gravier, 1900), holotipo (MNHN–A74): A. Parte anterior: B. Parte posterior; C. Proventrículo; D. Sedas falcígeras y acículas anteriores; E. Sedas falcígeras y acículas medias; F. Ganchos y acículas posteriores. Fig. 1. Branchiosyllis exilis (Gravier, 1900), holotype (MNHN–A74): A. Anterior part; B. Posterior part; C. Proventriculum; D. Anterior falcigers and aciculae; E. Middle falcigers and aciculae; F. Posterior hooks and aciculae.

pueden tener o no las líneas dorsales transversas características en los segmentos (Augener, 1927), mientras que en el material del Pacífico de Panamá se encontraron ejemplares con 2–3 líneas transversales color cafés por segmento en la región anterior que en la mitad del cuerpo se combinan formando bandas transversas, las cuales tienden finalmente a descolorarse pasando a ser pequeños puntos y manchas (que, sin embargo, dan un efecto continuo). En otro ejemplar, en cambio, se observó una sola

línea oscura transversal en medio de cada segmento anterior. La presencia de sedas con artejo en forma de gancho serrados en la parte posterior del cuerpo, hizo que dichos ejemplares fuesen atribuidos a S. fuscosuturata (Monro, 1933a). Esta especie también se encontró en Tortugas, si bien sin coloración, con dos pares de ojos (tres en la descripción de Augener) y las grandes sedas con artejo en forma de gancho localizadas en los setígeros medios y posteriores (Monro, 1933b).

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Fig. 2. Branchiosyllis salazari sp. n.: A. Parte anterior; B. Parte posterior. Fig. 2. Branchiosyllis salazari n. sp.: A. Anterior part; B. Posterior part.

Branchiosyllis salazari sp. n. (fig. 2A–2B, fig. 3C–3H)

Branchiosyllis exilis (non Gravier) Uebelacker, 1984: 30–105–30–106, figs. 30–100. Branchiosyllis exilis (non Gravier) Russell, 1987: 214–216 (sin figuras).

Material examinado AK1 (3), AK2 (1), AV1 (1), BA1 (1), BA2 (1), BC1 (1), BO1 (4), BP1 (2), BP2 (2), BP3 (2), BP4 (3), BP5 (7), BP6 (3), BP7 (19), BP8 (4), BP9 (1), BP10 (3), BP11 (6), CCA1 (1), CCE1 (29), DA1 (1), DA2 (1), E1M1T1 (1), E1M3T1 (1), E2M1T1 (7), E2M2T1 (1), E2M3T1 (1), E3M2T1 (1), E3M2T1 (1), E4M1T1 (1), E4M1T1 (1), E4M7T1 (2), E5M1T1(1), E6M4T1 (1), E7M1T1 (3), E7M2T1 (1), E7M5T1 (2), E8M2T1 (3), E8M6T1 (3), EL1 (1), EL2 (1), EL3 (1), F1 (1), IC1 (1), IC2 (1), ITM RM2 NI (1), ITM RM3 NS (1), M1 (1), PA1 (1), PA2 (5), PA3 (4), PA4 (3), PA5 (4), PG1 (2), PG2 (1), PGA1 (1), PGA2 (1), PH1 (2), PH2 (1), PH3 (14), PH4 (1), PH5 (2), S1 (1), SC1 (1), SM1 (3), T1 (2), Y1 (1), Y2 (1), Y3 (1), XA1 (1), XC1 (1), XC2 (1) y XCY1 (3). Material tipo Paratipo (LACM–AHF–00) Punta Nizuc, Cancun, 20º 02' N y 86º 44' W, II 2001, cols. JDRR y LHH; Holotipo (ECOSUR–Syll–27). Descripción Holotipo completo, largo y delgado, con 79 setígeros. Segmentos anteriores sin coloración, a partir del setígero 18 y hasta los más posteriores

con una banda dorsal media (central) abarcando todo el setígero; algunos artejos de las antenas, cirros tentaculares, cirros dorsales y cirro anal con manchas oscuras (fig. 2A). Prostomio oval, más ancho que largo, con una pequeña muesca posterior central hacia adentro (órganos nucales). Cuatro ojos casi en línea, los externos grandes y los internos menores y un par de ojos anteriores muy pequeños, todos con lentes. Antenas y cirros moniliformes. Antena central inserta en medio del prostomio, dos veces más larga que las laterales, con 25 artejos; antenas laterales situadas en el borde anterior del prostomio, externamente a las manchas oculares, con 21 artejos, ligeramente más largas que el prostomio más los palpos. Palpos anchos, 1.5 veces más largos que el prostomio, fusionados en la base. Segmento tentacular ligeramente más largo que el resto; dos pares de cirros tentaculares, el dorsal dos veces más largo que el ventral, con 34 artejos; el ventral con 21. Primer cirro dorsal muy largo (44 artejos); el resto alternando largos y cortos, los anteriores entre 32–42 artejos, los medios entre 35 y 24–28 artejos, y los posteriores entre 22 y 17. Parápodos cónicos con dos lóbulos distales triangulares, la anterior más larga que la posterior. Cirro ventral corto, cónico, ancho en la base y delgado hacia la punta. Parápodos anteriores con 5–6 sedas compuestas con cuatro artejos largos (L/AM 4:1), ligeramente curvos, serrados, bidentados, con el diente distal más largo que el subdistal, y dos cortos (L/AM 3:1),

Animal Biodiversity and Conservation 31.2 (2008)

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Fig. 3. Branchiosyllis salazari sp. n.: C. Sedas falcígeras anteriores; D. Acículas anteriores; E. Sedas falcígeras del setígero 18; F. Acículas del setígero 35; G. Sedas falcígeras y gancho del setígero 35; H. Sedas falcígeras y gancho posteriores. Fig. 3. Branchiosyllis salazari n. sp.: C. Anterior falcigers; D. Anterior aciculae; E. Falcigers of setiger 18; F. Aciculae of setiger 35; G. Falcigers and hook of setiger 35; H. Posterior falcigers and hook.

similares a los largos (fig. C). El setígero 17 con cuatro sedas compuestas de artejo corto (L/ AM 2:1), curvo, serrado, bidentado, con el diente distal más grande que el subdistal y tres sedas de artejo corto (L/AM 2:1), curvo, ligeramente serrado y unidentado. Desde el setígero 18, seis sedas compuestas de artejo corto (L/AM 2:1), cuatro con artejos curvos, serrados, bidentados, con el diente subdistal tan pequeño que parece unidentado, y dos con artejos muy curvos, parecidos a ganchos, unidentados (fig. 3E). Setígero 35 con seis sedas compuestas, cinco con artejos cortos (L/AM 2:1), curvos, serrados y unidentados y uno en forma de gancho muy grueso (L/AM 3:1) (fig. 3G). Setígeros posteriores conservaron 3–5 sedas, una con artejo en forma de gancho muy grueso L/AM 3:1) y 2–4 con artejos cortos (L/AM 1.5–2:1), curvos, serrados y unidentados (fig. 3H). Sedas simples dorsales y ventrales ausentes. Tres acículas en los parápodos anteriores, dos aguzadas y una con una pequeña prolongación distal lateral (oblicua) (fig. 3D), pasando a dos en los setígeros medios y posteriores, una aguzada y una con la pequeña prolongación distal lateral (fig. 3F). Pigidio muy corto, redondeado, se conserva un único cirro anal largo, con 19 artejos

(fig. 2B). Faringe larga, ocupando los setígeros 2–8, con papilas en el margen anterior y un diente mediodorsal anterior muy grande. Proventrículo largo, ocupando los setígeros 8–13, con 40 HCM y la línea mediodorsal indistinta. Variación Los ejemplares estudiados pueden poseer 1–5 acículas anteriores, de 27 a 48 HCM y 1–3 ganchos a partir de los setígeros 13–48, aunque pueden aparecer desde el tercero. Discusión Branchiosyllis salazari sp. n. se distingue fácilmente de B. abranchiata Hartmann–Schroder, 1965, B. pacifica Rioja, 1941 y B. oculata Ehlers, 1887 porque todas poseen ganchos compuestos en todo el cuerpo. Sólo tres especies poseen a la vez sedas falcígeras y ganchos compuestos: Branchiosyllis exilis (Gravier, 1900), B. diazi Rioja, 1958 y B. lorenae San Martín & Bone, 1999. Branchiosyllis salazari sp. n. difiere de B. exilis en la forma de las acículas anteriores y medias, las sedas falcígeras medias son bidentadas, con el diente distal 3 veces más grande que el subdistal y el proventrículo presenta una línea central de células romboidales. También difiere de B. diazi porque posee ojos

Ruiz–Ramírez & Harris

Clave de identificaación para las especies de Branchiosyllis del Gran Caribe. Identification key for the the species of Branchiosyllis from the Great Caribbean.

1 Con branquias

Sin branquias

2 Antena media central; palpos separados; branquia vesiculosa y pigmentada, cerca de la base del cirro dorsal

B. diazi

Antena media anterior; palpos fusionados en la base; branquias diferentes

3 Branquia en forma de saco; con 3 acículas; faringe ocupa 3–7 segmentos; proventrículo ocupa 9–15 segmentos (105–112 setígeros)

B. oculata

Branquia variada, muy vascularizada; con una acícula; faringe ocupa

4 segmentos; proventrículo ocupa 4–7 segmentos (31–36 setígeros)

B. pacifica

4 Antena media central; 4 ojos medios en línea

Antena media posterior; 4 ojos en trapecio

5 Sedas falcígeras unidentadas; con dos acículas aguzadas, derechas; faringe ocupa 3 segmentos; proventrículo ocupa 8–15 segmentos; [con banda oscura transversa media y trazas en cada segmento] (61 setígeros)

B. exilis

Sedas falcígeras bidentadas; con tres acículas, dos aguzadas y truncada oblicua; faringe ocupa 7 segmentos; proventrículo ocupa 8–13 segmentos;

[con una banda oscura tranversa media en cada segmento] (79 setígeros)

B. salazari sp. n.

6 Cirros dorsales con 30–33 artejos; proventrículo con 30 HCM; 1–3 sedas compuestas anteriores y 7–10 medias y posteriores; dientes proximales

sin espinas; acícula capitada y otra en forma de L, en setígeros posteriores semeja una bota corta; (54 setígeros)

B. lorenae

Cirros dorsales con 9–44 artejos; proventrículo con 35 HCM; 8 sedas compuestas anteriores y 1 posterior; dientes proximales con espinas; acícula truncada oblicua y 2 multidentadas; (68 setígeros)

en disposición trapezoidal, branquias vesiculosas y pigmentadas, sedas falcígeras anteriores curvas, y una acícula aguzada y otra truncada, con dos salientes en los extremos de la superficie truncada, el superior más pequeño y agudo que el inferior. Finalmente difiere de B. lorenae porque tiene ojos en arreglo trapezoide, sedas falcígeras medias y posteriores bidentadas, con el diente distal mayor (los posteriores hasta 3–4 veces que el subdistal). También difiere de B. maculata (Imajima, 1966) de Japón y B. salina (Hartmann–Schroder, 1959) de El Salvador porque poseen ojos en arreglo trapezoide. Además, B. salina posee sedas falcígeras unidentadas y sólo la mitad de los artejos serrados y B. verruculosa (Augener, 1913) de Australia posee sedas falcígeras unidentadas. Los ejemplares de B. exilis (non Gravier) de Uebelacker (1984) se parecen a B. salazari sp. n. en la posición de los ojos, en la ausencia de branquias y en la presencia de sedas falcígeras anteriores bidentadas

B. noviseta

que hacia setígeros medios y posteriores pasan a ser unidentadas, y de ganchos compuestos en la región media del cuerpo. El ejemplar de Russell (1987) posee el mismo arreglo de pigmentación y sedas falcígeras con proporciones similares a las de B. salazari sp. n. Consideramos que ambos ejemplares quedan dentro de la misma especie, pero nuestra apreciación se basa únicamente en las descripciones de estos autores. B. pacifica se ha descrito de Acapulco, México (Rioja, 1941) y reportado posteriormente en el Atlántico por Hartmann–Schröder (1980) en las Antillas y en la lista de especies de Salazar–Vallejo (1992) en Sian Ka´an, Quintana Roo, México. Su distribución es cuestionable, las formas asignadas a esta especie no pueden ser parte de la misma especie biológica; debe revisarse con detalle. Localidad tipo Punta Nizuc, Cancún (20º 02' N y 86º 44' W).

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Etimología El nombre específico se ha escogido en honor del Dr. Sergio I. Salazar–Vallejo, profesor y amigo, por su ardua labor y su contribución al conocimiento de los poliquetos en el Gran Caribe. Distribución Caribe noroccidental: Sabancuy, Campeche hasta Bacalar Chico, situado en la frontera México–Belice. Hábitat Asociada a macroalgas, arenales, esponjas y praderas submarinos; raíces de mangle rojo, fondos mixtos y sedimento de conchas de caracol abandonadas. Agradecimientos Este documento fue parte del programa sobre Poliquetos del Caribe mexicano y de la tesis de Maestría de la primera autora. Las autoras agradecen a Sergio I. Salazar–Vallejo por invitarlas a participar en su Seminario Doctoral Avanzado y Talleres Intensivos sobre Poliquetos y por todas las facilidades otorgadas para la realización de este trabajo. La primera autora agradece a CONACyT por una beca para la realización de estudios de Maestría en El Colegio de la Frontera Sur–Unidad Chetumal. A Fredrik Pleijel (Museum National d´Histoire Naturelle) por facilitarme el espacio y equipo suficiente para la revisión del material tipo, así como a Marie–José d´Hondt por su paciencia y tiempo dedicado en la búsqueda del material durante mi estancia en París. A Miguel Angel García Salgado, Roberto Ibarra Navarro y Belem Ramírez Avalos de la SEMARNAT por permitirnos colectar material en el Parque Nacional de Cancún y brindarnos el espacio suficiente para el procesamiento del material. A Mario Londoño–Mesa por su tiempo dedicado a la edición de las figuras. A Norma Emilia González Vallejo por la información sobre la Colección de Referencia de ECOSUR. A Montserrat Ferrer, Guillermo San Martín y a Daniel Martín por la revisión, comentarios y sugerencias a este documento, con lo cual se mejoró en gran medida la presentación final. Referencias Augener, H., 1913. Polychaeta I, Errantia. In: Die Fauna Südwest–Australiens, Band 4, Lief 5: 65–304 (W. Michaelsen & R. Hartmeyer, Eds.). Gustav Fischer. Jena. – 1924. Ueber litorale Polychaeten von Westindien. Sitzber. Ges. Naturforsch. Fr. Berlin., 1922: 38–53. – 1927. Bijdragen tot de Kennis der Fauna van Curaçao. Resultaten eener Reis van Dr C. J. van der Horst in 1920. Zool. Genoots. Nat. artis Magistra Amsterdam, 25: 39–82. Ehlers, E., 1887. Reports on the Annelids. Reports on the results of dredging, under the direction of Pourtalès & Agassiz, in the Gulf of Mexico. Mem. Mus. Comp. Zool. Harvard, 15: 1–335.

Fauchald, K., 1977. The Polychaete Worms. Definitions and Keys to the Orders, Families and Genera. Publ. Nat. Hist. Mus. Los Angeles Cty, Sci. Ser., 28: 1–188. Fauvel, P., 1959. Classe des Annélides Polychètes, Annelida, Polychaeta (Grube 1851). In: Traité de Zoologie, vol. 5: 12–196 (P. P. Grassé, Ed.). Masson et Cie., Paris. Gravier, M. C., 1900. Contribution a l’étude des annélides polychétes de la Mer Rouge. Bull. Nouv. Arch. Mus. Hist. Nat. Paris 4 ème sér., 2(2): 137–282. Hartman, O. 1959. Catalogue of the Polychaetous Annelids of the World, Pt. 1. Allan. Hancock Found. Occ. Pap., 23: 1–353. Hartmann–Schroder, G., 1959. Zur Ökologie der Polychaeten des Mangrove–Estero–Gebietes von El Salvador. Beiträge zur neotropischen Fauna, 1: 70–183. – 1965. Zur Kenntnis der Eulitoralen Polychaeten Fauna von Hawaii, Palmyra und Samoa. Abhand. Verhand, Naturwissen. Vereins (Hamburg): 81–161. – 1980. Die Polychaeten der Amsterdam–Expeditionen nach Westindien. Bijdragen tot de Dierkunde, 50, 387–401. Imajima, M., 1966. The Syllidae (Polychaetous Annelids) from Japan, IV. Syllinae (1). Publ. Seto Mar. Biol. Lab., 14: 219–252. Licher, F., 1999. Revision der Gattung Typosyllis Langerhans, 1879 (Polychaeta: Syllidae) Morphologie, Taxonomie und Phylogenie. Abh. Senckenberg. Naturforsch Ges., 551: 1–336. Monro, C. C. A., 1933a. The Polychaeta Errantia collected by Br. C. Crossland at Colón, in the Panama Region, and the Galapagos Islands during the Expedition of the S.Y. "St. George". Proc. Zool. Soc. Lond., 1933(1): 1–96. – 1933b. On a Collection of Polychaeta from Dry Tortugas, Florida. Ann. Mag. Nat. Hist. ser. 10, 12: 244–69. Rioja, E., 1941. Estudios anelidológicos, 3. Datos para el conocimiento de la fauna de poliquetos de las costas del Pacífico de México. An. Inst. Biol., 12: 669–746. – 1958. Estudios anelidológicos, 22. Datos para el conocimiento de la fauna de anélidos de las costas orientales de México. An. Inst. Biol., 29: 219–301. Russell, D., 1987. The taxonomy and distribution of Syllidae (Annelida: Polychaeta) inhabiting mangrove and adjacent shallow–water habitats of Twin Cays, Belize. Ph. D. dissertation, The George Washington Univ. Salazar–Vallejo, S. I., 1996. Lista de especies y bibliografía de poliquetos (Polychaeta) del Gran Caribe. An. Inst. Biol. UNAM, Ser. Zool., 67(1): 11–50. – 1992. Updated checklist of polychaetes (Polychaeta) from the Gulf of Mexico, the Caribbean Sea and adjacent areas in the Western Atlantic Ocean. In: Diversidad Biológica en la Reserva de la Biosfera de Sian Ka'an, Quintana Roo, México: 43–76 (D. Navarro & E. Suárez–Morales, Eds.). CIQRO & SEDESOL, México.

San Martín, G., 2003. Annelida, Polychaeta II: Syllidae. En: Fauna Ibérica, vol. 21: 1–554 (Ramos, M. A. et al., Eds.). Museo Nacional de Ciencias Naturales–CSIC, Madrid. San Martín, G. & Bone, D., 1999. Two new species of Dentatysyllis and Branchiosyllis (Polychaeta: Syllidae: Syllinae) from Venezuela. Proc. Biol. Soc. Wash., 112(2): 319–326. Uebelacker, J. M., 1982. Review of some little–know species of syllids (Annelida: Polychaeta) described from the Gulf of Mexico and Caribbean by Hermann

Ruiz–Ramírez & Harris

Augener in 1924. Proc. Biol. Soc. Wash., 95(3): 583–593. – 1984. Family Syllidae Grube, 1850. In: Taxonomic guide to the polychaetes of the Northern Gulf of Mexico, 30.3: 30–151 (J. M. Uebelacker & P. G. Johnson, Eds.). Minerals Management Service, Barry A. Vittor An. Mobile. Westheide, W., 1974. Interstitielle Fauna von Galapagos, 11. Pisionidae, Hesionidae, Pilargidae, Syllidae (Polychaeta). Milkrofauna Meeres, 44: 193–338.

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Apéndice 1. Datos de las estaciones de recolecta de los ejemplares analizados. Las iniciales indican los colectores son: Eduardo Donath (ED), Iloín Pelayo (IP), Jennifer Denisse Ruiz Ramírez (JDRR), Juan José Oliva (JJO), Julio Espinoza–Avalos (JEA), Leslie H. Harris (LHH), Luis Fernando Carrera–Parra (LFCP), María de los Angeles Díaz–Marín (MADM), María Soledad Jímenez–Cueto (MSJC), y Sergio I. Salazar–Vallejo (SISV). Appendix 1. Sampling station data on the specimens analysed. Items are identified by the collector's initials: Eduardo Donath (ED), Iloín Pelayo (IP), Jennifer Denisse Ruiz Ramírez (JDRR), Juan José Oliva (JJO), Julio Espinoza–Avalos (JEA), Leslie H. Harris (LHH), Luis Fernando Carrera–Parra (LFCP), María de los Angeles Díaz–Marín (MADM), María Soledad Jímenez–Cueto (MSJC), and Sergio I. Salazar–Vallejo (SISV). Materiales recolectados en Bajo Pepito por MADM y JEA BP1. Bajo Pepito, en Penicillus dumetosus, II 97; BP2. Bajo Pepito, en Halimeda incrassata, II 97; BP3. Bajo Pepito, blanquizal, en Lobophora variegata, II 97; BP4. Bajo Pepito, blanquizal, en algas, 5 II 97; BP5. Bajo Pepito, III 97; BP6. Bajo Pepito, banquizal, en Udotea, III 97; BP7. Bajo Pepito, IV 97; BP8. Bajo Pepito, en Lobophora variegata, IV 97; BP9. Bajo Pepito, en Sargassum vulgaris, V 97; BP10. Bajo Pepito en Halimeda incrassata, VI 97; BP11. Bajo Pepito, en algas, VI 97. Materiales recolectados por el submarino Edwin Link EL1. 2774, 170 f, 20 VIII 90 Cayo Norte Chinchorro (18º 45.63' N, 87º 15.84' W), 16.9ºC; EL2. 2777, 218 f, 21 VIII 90 Al sur de Chinchorro (18º 26.02' N, 87º 18.82' W), 18.5ºC; EL3. 2780, 201 f, Esponja, 22 VIII 90 al norte de Cayo Blackford (18º 30.94' N, 87º 26.61' W), 18ºC. Materiales recolectados en la Laguna de Nichupté por MSJC y JJO E1M1T1, 22 IV 88; E1M3T1, 5 VII 88; E2M1T1, 18 IV 88; E2M2T1, 29 X 87; E2M3T1, 5 VII 88; E3M2T1, 20 IV 88; E3M2T1, 5 VII 88; E4M1T1, 19 IV 88; E4M1T1, 7 VII 88; E4M7T1, 18 X 87; E5M1T1, 7 VII 88; E6M4T1, 6 VII 88; E7M1T1, 20 IV 88; E7M2T1, 6 VII 93; E7M5T1, 6 VII 88; E8M2T1, 6 VII 88; E8M6T1, 29 X 87. Materiales diversos AK1. Akumal, 23 II 86 MA; AK2. Akumal, 12 IV 86; AV1. Aventuras, 18 V 86, ED; BA1. B. Ascensión entre Thalassia, 28 I 86; BA2. B. Ascensión, CV RM3, 29 IV 87; BC1. Bacalar chico, desembocadura, en raíz de Rhizophora mangle, 9 X 97, JEA; BO1. Bocontica, M. 92 I 91; CCA1.Cabo Catoche, +5 Norte, Arr. Red. Cam.; CCE1.Cayo Cedros, RM2, 6 III 87; DA1. DIF–Aventuras, QR–4, roca mixta, 21 IV 92; DA2. DIF–Aventuras, QR–5 roca; 22 III 92; F1. Faro Xcayal, B. 110, 4 XI 90; IC1. Isla Contoy, barlovento sur, 28 II 2001; IC2. Isla Contoy, MF–camping, en sedimento de caracol abandonado, LFCP; ITM RM2 NI, 29 IV 87; ITM RM3 NS, 28 IV 87; M1. Mahahual, XII, 2000; PA1. P. Allen, 24 II 86, ED; PA2. P. Allen, en T. turbinata, 27 II 86; PA3. P. Allen, 10 VI 86, ED; PA4. P. Allen, 11 VI 86, ED; PA5. PA RM1 NM, 29 IV 87; PG1. P. Gavilán, I. Pelayo, 15 VII 92; PG2. P. Gavilán, I. Pelayo, 26 X 92; PGA1. P. Gorda, 27 VII 84; PGA2. Gorda E. 27 VII 84; PH1. P. Hualostoch, 26 II 86; PH2. PH RM1, 2 VII 87; PH3. PH RM1 NM, 2 VII 87; PH4. PH RM1 NS, 28 IV 87; PH5. PH RM3 NI, 28 IV 87; S1. Sabancuy, D. 28 VII 84; SC1. San Carlos 21 V 91, MDEM; SM1. Sol y Mar, 9 I 2001; T1. Tulum, 24 II 86; Y1. Yalahau, asociada a macroalgas, 9 IX 93; Y2. Yalahau JEA 8 IX 93; Y3. Yalahau, P. Vista Alegre, M. 26, I 91; XA1. Xamach, 28 II 86, E.D.; XC1. Xcacel 13; XC2. Xcacel, 17 IV 96 SISV–LFCP; XCY1. Xcayal, 4 XI 90.

"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 31.2 (2008)

Hyphessobrycon ocasoensis sp. n. (Teleostei, Characidae) una nueva especie para el Alto Cauca, Colombia C. A. García–Alzate & C. Román–Valencia

García–Alzate, C. A. & Román–Valencia, C., 2008. Hyphessobrycon ocasoensis sp. n. (Teleostei, Characidae) una nueva especie para el Alto Cauca, Colombia. Animal Biodiversity and Conservation, 31.2: 11–23. Abstract Hyphessobrycon ocasoensis n. sp. (Teleostei, Characidae) a new species from the Alto Cauca, Colombia.— Hyphessobrycon ocasoensis n. sp. (Characiformes, Characidae) from heterorhabdus group (Gery, 1977) is described from the upper Cauca River in Colombia. The new species is distinguished from all other known species by the following combination of characters: three unbranched and eight branched fins in the dorsal fin; short maxillary bone with one or no teeth; four small foramens in the maxillary bone, and five in the premaxillary; 5–17 scales with pores in the lateral line, six between the lateral line and anal–fin origin, six between the lateral line and pelvic–fin origin, and nine predorsals; depth of the caudal peduncle has a mean of 16.7% in standard length; interorbital width 50.6% in head; a dark spot on caudal peduncle and a dark lateral band that extends vertically from the dorsal–fin origin to the tips of the middle caudal fin rays. Physical and chemical data of their habitat are included. Key words: Hyphessobrycon ocasoensis n. sp., Characid fish, Alto Cauca, Colombia. Resumen Hyphessobrycon ocasoensis sp. n. (Teleostei, Characidae) una nueva especie para el Alto Cauca, Colombia.— Se describe Hyphessobrycon ocasoensis sp. n. (Characiformes, Characidae) perteneciente al grupo heter orhabdus (Gery, 1977) de la cuenca alta del río Cauca, Colombia. La nueva especie se distingue de las otras especies descritas por la siguiente combinación de caracteres: tres radios simples y ocho radios ramificados en la aleta dorsal; un maxilar corto con un diente o sin dientes; cuatro pequeños forámenes en el maxilar, y cinco en el premaxilar; 15–17 escamas con poros en la línea lateral, seis entre la línea lateral y el origen de la aleta anal, seis entre la línea lateral y el origen de la aleta pélvica, y nueve predorsales; la altura media del pedúnculo caudal es 16,7% en la longitud estándar; la anchura interorbital 50,6% en la longitud de la cabeza; una mancha oscura en el pedúnculo caudal y una banda lateral oscura que se extiende desde una vertical trazada al inicio de la aleta dorsal hasta los radios medios caudales. Se incluyen datos físicos y químicos sobre el hábitat acuático propio del nuevo taxón. Palabras clave: Hyphessobrycon ocasoensis sp. n., Pez carácido, Alto Cauca, Colombia. (Received: 16 X 07; Conditional acceptance: 13 III 08; Final acceptance: 4 IX 08). Carlos A. García–Alzate(1) & C. Román–Valencia(2), Lab. de Ictiología, Univ. del Quindío, A. A. 2639, Armenia, Quindío, Colombia. (1) (2)

E–mail: cagarcia@uniquindio.edu.co E–mail: ceroman@uniquindio.edu.co

ISSN: 1578–665X

Introducción El género Hyphessobrycon Durbin, 1908 constituye actualmente una gran subunidad dentro de la familia Characidae, con cerca de 110 especies nominales (Lima et al., 2003; Lima & Moreira, 2003; Lucena, 2003; Almirón et al., 2004; Bertaco & Malabarba, 2005) ampliamente distribuidas desde el sur de México hasta el Rio de la Plata en Argentina. El género Hyphessobrycon se define por la combina ción de los siguientes caracteres: línea lateral con poros incompleta, presencia de aleta adiposa, pocos dientes en el maxilar o sin ellos, tercer infraorbital sin contacto con el preopérculo, dos series de dientes en el premaxilar teniendo su fila interna 5 o más dientes y aleta caudal desnuda sin escamas; éste ultimo carácter lo diferencia del género Hemigrammus. La diagnosis del género Hyphessobrycon no se ha realizado desde una perspectiva filogenética, por lo que no se considera un género monofilético (Weitz man & Palmer, 1997; Malabarba & Weitzman, 2003; Bertaco & Malabarba, 2005). Los problemas en su sistemática radican en la incertidumbre con respecto a la taxonomía de la mayoría de las especies que lo componen, y no se dispone de un análisis filogené tico que la aclare. Uno de las mayores dificultades se presenta porque no hay evidencia que explique la relación de la especie tipo Hyphessobrycon compressus, con las especies de Centroamérica y con algunas especie del noreste de Colombia y norte de los Andes (Weitzman & Palmer, 1997). Para Colombia se reconocen trece especies, de las cuales cinco pertenecen al grupo heterorhabdus Géry, 1977: H. heterorhabdus (Ulrey, 1894) en Alto amazonas, H. metae Eigenmann y Henn, 1914 (Ei genmann & Henn, 1914) y H. diancistrus Weitzman, 1977 en el río Orinoco, H. poecilioides Eigenmann, 1913 en el Alto Cauca, H. proteus Eigenmann, 1913 (Eigenmann, 1913) drenajes del Caribe Colombia no, Cuenca media y baja del Magdalena y Atrato (fig. 1). Este grupo se caracteriza por presentar una banda lateral oscura en la parte lateral del cuerpo. El objetivo de éste trabajo es describir una nueva especie de Hyphessobrycon del grupo heterorhabdus para el Alto Cauca, Colombia. Se utilizan caracteres morfométricos, merísticos y además osteología para ilustrar su diagnosis. Material y métodos Las colectas de los peces se realizaron utilizando un método consistente en arrastres con una malla fina (ojo de malla 6,0 por 3,5 mm) de 3,85 m de longitud por 1,65 m de ancho. Los arrastres se hi cieron en un solo biotopo: zona litoral de remanso, a favor de la corriente. Se registró la coloración en vivo y se fijaron con formol al 10%, posteriormente se preservó en alcohol al 70%, y los ejemplares se alojaron en la colección de peces del laboratorio de Ictiología del Departamento de Biología, Universidad del Quindío, Armenia, Colombia (IUQ); en el Museo de Biología de la Universidad Central de Venezuela,

García–Alzate & Román–Valencia

Caracas (MBUCV) y en el Museo Ciencias Naturales, Universidad Experimental de los Llanos Occidentales "Ezequiel Zamora", Guanare, Venezuela (MCNG). Además, se examinó material alojado en el Museo de Ciencias Naturales de Filadelfia, USA (ANSP), The Natural History Museum, London, formerly Bri tish Museum (Natural History) (BMNH), la colección de peces del Instituto de biología de la Universidad Nacional Autónoma de México (IBUAM–P), Museo de Ciencia y Tecnología, Pontificia Universidad Católica de Rio Grande del Sur, Porto Alegre, Brasil (MCP), Instituto de Ciencias Naturales–Museo de Historia Natural, Universidad Nacional de Colombia, Bogotá (ICN–MNH), de la colección Ictiológica, Instituto de Biología de la Universidad de Antioquia, Medellín, Colombia (CIUA) y Museo de Ciencias Naturales, del Instituto para la Investigación y la Preservación del Patrimonio Cultural del Valle del Cauca INCIVA, Cali, Colombia (IMCN). Las medidas de los ejemplares se tomaron con un calibre digital, hasta décimas de milímetro. Todas las medidas fueron obtenidas punto a punto. Los recuentos de radios, escamas y dientes empleando estereoscopio y aguja de disección. Las medidas y recuentos (tabla 1) se realizaron sobre el lado izquierdo de los ejemplares, excepto cuando éstos estaban deteriorados en tal lado. Medidas y conteos siguen a Weitzman & Malabarba (1999), se expresaron como porcentaje de la longitud estándar (%LE) y porcentaje longitud cabeza (%LC). Los 21 caracteres morfométricos utilizados en éste trabajo (tabla 1) fueron útiles para efectuar un análisis de componentes principales (ACP) usando Log10 para eliminar la influencia del tamaño en la forma con el programa Past, versión 1,82 (Hammer et al., 2001). Los conteos de escamas analizados mediante diagrama de cajas (Box Plot) con el paquete estadístico Spss versión 9,0 de Windows. Las observaciones de estructuras óseas y cartílagos se hicieron sobre ejemplares transparentados y teñidos (CyT) de acuerdo a los métodos descritos por Taylor & Van Dyke (1985), Song & Parenti (1995). La nomen clatura de huesos se basó en Weitzman (1962), Vari (1995) y Ruiz–Calderón & Román–Valencia (2006), el rango de medidas mínimas y máximas de cada lote examinado se presento en paréntesis. En la localidad tipo, se hicieron determinaciones diurnas de las siguientes variables: oxígeno disuelto (OD), porcentaje de saturación, temperatura super ficial del agua y del ambiente con oxímetro, pH con potenciómetro y conductividad con conductímetro, tipo de sustrato y color del ambiente acuático, calificado por observación directa, la dureza (total, cálcica y magnésica), alcalinidad, demanda química de oxígeno (DQO), demanda bioquímica de oxíge no (DBO), cloruros, sólidos (totales, suspendidos y disueltos), alcalinidad y acidez se determinaron en los dos periodos climáticos de la región (sequia y lluvias) (tabla 2) de acuerdo con la metodología recomendada por la APHA (1998) y Wetzel & Likens (2000) en el laboratorio de aguas de la Universidad del Quindío, Armenia. Con métodos numérico (Hyslop, 1980; Hynes, 1950), y volumétrico (Capitoli, 1992) se realizó el análisis de los organismos presentes de

Animal Biodiversity and Conservation 31.2 (2008)

Fig. 1. Distribución geográfica de Hyphessobrycon grupo heterorhabdus para Colombia: H. ocasoensis sp. n. (•), H. diancistrus ([), H. proteus ( ), H. poecilioides (Ì), H. metae ( ) y H. heterorhabdus (—). Fig. 1. Geographical distribution of Hyphessobrycon heterorhabdus group from Colombia: H. ocasoensis n. sp. (•), H. diancistrus ([), H. proteus ( ), H. poecilioides (Ì), H. metae ( ) and H. heterorhabdus (—).

los estómagos del material transparentado y teñido. Coordenadas y altitud con un sistema electrónico portátil de posición global (GPS) 4,000XL. Material de comparación examinado Hyphessobrycon compressus BMNH 1905.12.6.4–5, paratipos, 2; México, Obispo, Vera Cruz, 31,38–33,55 mm LE. ANSP 124774; México, 12, río Usumacinta casi unido con Pasión, cerca Sayache, 18 VIII 1961, 30,29–35,58 mm LE. IBUAM–P 8538, 2; México, trinitaria, Flor de Café, Chris, 03 VII 1993, 24,48–26,32 mm LE. IUQ 1690; México, 3 CyT, río Usumacinta casi unido con Pasión, cerca Sayache, 18 VIII 1961. Hyphessobrycon poecilioides IUQ 718, 1, Colombia, Quebrada La Picota, Quindío, 29 IX 2004, 64,29 mm LE. IUQ 519, 46; Colombia, quebrada El Indio, 100 m en el peaje vía Alambrado– Corozal, Valle, 5 XII 2003, 65,95–75,85 mm LE. IUQ 517, 33; Colombia, quebrada El Indio, 100 m en el peaje vía Alambrado–Corozal, Valle, 12 IX 2004, 27,12–71,03 mm LE. IUQ 719, 13; Colombia, que brada Naranjal, Vallejuelo, Valle, 28 VI 1994. IUQ 718, 1; Colombia, quebrada La Picota, 29 IX 2004, 23,33–61,66 mm LE. IUQ 1959, 2 CyT; Colombia, quebrada El Indio, 100 m en el peaje vía Alambrado– Corozal, Valle, 12 IX 2004, 27,19–63,66 mm LE. Hyphessobrycon proteus

IUQ 1009, 2 CyT; Colombia, ciénaga de capote, en Soplaviento, bajo Magdalena, 31 V 2003, 35,60–38,78 mm LE. IUQ 583, 3; Colombia, frente a Santa Lucia, Atlántico, 5 VIII 1991, 33,15–49,74 mm LE. IUQ 736, 2; Colombia, Jagüey frente izquierdo de Puerto Colombia, Atlántico, 15 IV 1990, 46,01– 52,86 mm LE. IUQ 1965, 36; Colombia, ciénaga de Capote, en Soplaviento, Bajo Magdalena, 31 V 2003, 35,56–54,87 mm LE. CIUA 790, 8; Colombia, la guna Villa Sonia área de conexión minera carbones de la Jagua, Cesar, 27 VIII 07, 35,86–40,58 mm LE. CIUA 296, 38; Colombia, estuario del río San Juan, San Juan de Uraba, Antioquia, 23 IX 2005, 47,08–53,86 mm LE. Hyphessobrycon heterorhabdus ICNMNH 5063, 10; Colombia, Río Puré, Leticia, Amazonas, 02º 07' 05'' S y 69º 37' 50'' O, 8 I 2000, 27,17–35,88 mm LE. MCP 41577, 5; Brazil, Para, Igarapé Acuí Igarapçe Acuí, 01º 35' 46'' S y 48º 44' 26'' W, 26,30–30,37 mm LE. IUQ 1961, 3 CyT; Colombia, río Puré, Leticia, Amazonas, 02º 07' 05'' S y 69º 37' 50'' O, 8 I 2000, 28,32–34,58 mm LE. IUQ 1963, 1 CyT; Brazil, Para, Igarapé Acuí Igarapçe Acuí, 01º 35' 46'' S y 48º 44' 26'' W, 33,05 mm LE. Hyphessobrycon diancistrus BMNH 1977.1.12.1–2, paratipos, 2; Colombia, río Vichada, 23,13–23,53 mm LE. MBUCV–V 902, 3 CyT; Venezuela, río Cataniapo, aguas abajo del

García–Alzate & Román–Valencia

Tabla 1. Datos morfométricos y merísticos de Hyphessobrycon ocasoensis sp. n. (Longitud estándar y total en mm; promedios entre paréntesis.) Table 1. Morphometric and meristic data of Hyphessobrycon ocasoensis n. sp. (Standard and total lengths in mm; mean values within parenthesis.)

Holotipo

Paratipos (n = 23)

Longitud estándar

44,0

33,8–51,7 (39,4)

Longitud total

55,0

42,9–60,7 (49,4)

Profundidad del cuerpo

41,3

32,1–43,8 (39,6)

Longitud hocico–aleta dorsal

54,0

41,7–55,7 (52,7)

Longitud hocico–aletas pectorales

29,0

23,5–33,5 (28,8)

Longitud hocico–aletas pélvicas

49,5

39,2–54,3 (49,9)

Longitud hocico–aleta anal

65,0

20,8–68,2 (56,9)

Longitud aleta dorsal–hipurales

51,4

41,8–56,0 (50,7)

Longitud aleta dorsal–aleta anal

42,2

34,6–44,1 (40,5)

Longitud aleta dorsal–aletas pectorales

45,1

34,2–46,9 (42,9)

Longitud aleta dorsal

28,2

23,0–30,4 (27,7)

Longitud aletas pectorales

22,9

16,6–24,0 (21,2)

Longitud aletas pélvicas

18,2

12,6–19,7 (16,8)

Longitud aleta anal

17,9

15,0–23,0 (19,6)

Profundidad del pedúnculo caudal

15,3

11,9–18,7 (16,7)

Longitud del pedúnculo caudal

10,5

7,7–10,9 (9,2)

Longitud de la cabeza

28,3

21,9–30,4 (27,0)

Longitud del hocico

24,8

18,7–32,5 (24,7)

Diámetro del ojo

37,1

29,0–46,7 (37,9)

Longitud post–orbital de la cabeza

44,9

32,5–50,3 (45,4)

Longitud del hueso maxilar

29,1

26,7–40,2 (31,8)

Ancho interorbital

54,8

41,9–63,6 (50,6)

Longitud de la mandíbula superior

29,3

25,6–34,6 (29,6)

En la serie lateral

31–32

Morfometría Porcentaje de la longitud estandar

Porcentaje longitud cabeza

Merística Escamas En la linea lateral con poros

15–17

Entre la línea lateral y la aleta dorsal

5–6

Entre la línea lateral y la aleta anal

Entre la línea lateral y las aletas pélvicas

Predorsales

Dorsales

iii, 8

Anales

iii, 22

iii, 21–22

Radios

Pélvicos

ii, 6

Pectorales

ii, 12

Animal Biodiversity and Conservation 31.2 (2008)

Tabla 2. Variables fisicoquímicas analizadas para el hábitat de rio Roble de Hyphessobrycon ocasoensis sp. n.: OD. Oxigeno disuelto; DBO. Demanda bioquímica de oxígeno; DQO. Demanda química de oxígeno. Table 2. Physico–chemical variables analyzed for the Roble River habitat of Hyphessobrycon ocasoensis n. sp.: OD. Dissolved oxygen; DBO. Biochemical oxygen demand; DQO. Chemical oxygen demand. Variables OD mg/l

Sequía

Lluvias

4,3

6,32

DBO mg/l

150

230

DQO mg/l

65,34

73,68

Dureza cálcica mg/l CaCO3 23

Dureza total mg/l CaCO3

Dureza magnésica mg/l CaCO3 22 Alcalinidad mg/l CaCO3

26,45

31,32

Acidez mg/l

30,98

Sólidos totales mg/l

120

–

Sólidos disueltos mg/l

–

Sólidos suspendidos mg/l

Cloruros mg/l

25 FAU

31 FAU

Turbidez Profundidad

1,10 m

1,70 m

Ancho

16,76 m

19,30 m

Color Sustrato

cristalino marron rocoso

rocoso,

fangoso

Velocidad de corriente

0,63 m/s

0,49 m/s

caño Colorado, río abajo de la comunidad de San Pedro, Amazonas, 26 IV 2002, 28,94–29,74 mm LE. MBUCV–V 14298, 4; Venezuela, río Cataniapo, 200 m río arriba del puerto de la comunidad de Las Pavas, Amazonas, 05° 36' 00'' N y 67° 30' 37'' W, 16 III 1984, 29,26–33,65 mm LE. MBUCV–V 14484, 373; Venezuela, río Cataniapo, 200 m río arriba del puerto de la comunidad de Las Pavas, Amazonas, 05° 36' 0'' N y 67° 30' 37" O, 30 III 1984, 21,65– 31,33 mm LE. MBUCV–V 14644, 7; Venezuela, río Cataniapo, 200 m río arriba del puerto de la comunidad de Las Pavas, Amazonas, 05° 36' 00" N y 67° 30' 37" O, 24 XII 1983, 30,38–33,65 mm LE. MBUCV–V 24479, 17; Venezuela, río Cataniapo, rau dal Rabipelado, carretera Puerto Ayacucho–Gavilán, Amazonas, 05° 33' 08" N y 67° 20' 52" O, 29 III 1993, 27,30–33,06 mm LE. MBUCV–V 30747, 2; Venezuela, río Cataniapo, caño Gavilán, playa arenosa, Ama

zonas, 20 XI 2001 25,50–28,67 mm LE. MBUCV–V 30835, 17; Venezuela, río Cataniapo, aguas abajo del caño Colorado, río abajo de la comunidad de San Pedro, Amazonas, 26 IV 2002, 28,50–35,70 mm LE. MBUCV–V 30852, 2; Venezuela, río Cataniapo, playa fango–arenosa, río arriba de Gavilán, Amazonas, 26 V 2002, 26,17–27,60 mm LE. MBUCV–V 30867, 6; Venezuela, caño Gavilán, laja en Cucurital, aproxi madamente 1/2 h de Gavilán, Amazonas, 30 IV 2002, 28,94–32,28 mm LE. Hyphessobrycon metae IMCN 3751, 15; Colombia, caño payara, afluente de caño Negro, puerto Carreño, Vichada, 27 IV 2005, 28,09–34,34 mm LE. IUQ 1964, 2 CyT; Colombia, caño Payara, afluente de caño Negro, puerto Carreño, Vichada, 27 IV 2005, 29,80–30,33 mm LE. Hyphessobrycon sovichthys MBUCV–V 906, 2 CyT; Venezuela, préstamo de la hacienda Berlín, municipio Bartolomé de las Casas, Zulia, 12 VI 1974, 36,68–40,32 mm LE. MBUCV–V 18331, 465; Venezuela, río Santa Ana, Estado Perijá, Zulia, 10 XII 982, 22,42–39,01 mm LE. MBUCV–V 9212, 5; Venezuela, préstamo de la hacienda Berlín municipio Bartolomé de las Casas, Zulia, 12 VI 1974, 21,31–33,03 mm LE. MBUCV–V 29776, 48; Venezuela, caño La Guardia, balneario debajo del puente en carretera Casigua–Maracaibo, Zulia, 12 I 2001, 22,33–29,59 mm LE. MBUCV–V 18318, 10; Venezuela, lago de Maracaibo departamento Rosas noroeste de Carrasquero, Zulia, 5 XII 1982, 21,12–23,59 mm LE. ICNMNH 2360, 5; Colombia, rio la Gabarra cuenca del río Catatumbo, norte de Santander, 1 II 1995, 22,32–30,01 mm LE. Hyphessobrycon fernandezi MBUCV–V 2716, 1; Venezuela, caño Boca la Vieja, carretera boca de Aroa–Tucacas, Falcón, 7 II 1965, 24,94 mm LE. MBUCV–V 904, 4 CyT; Venezuela, caño pequeño margen izquierdo de la carretera Puerto Cabello–Morón, detrás de la estación de electricidad, Yaracuy, 11 X 1985, 25,78–28,84 mm LE. MBUCV– V 15078, 14; Venezuela, caño pequeño margen izquierdo de la carretera Puerto Cabello–Morón, detrás de la estación de electricidad, Carabobo, 11 X 1985, 18,80–28,85 mm LE. MBUCV–V 24222, 1; Venezuela, río Yaracuy, bajo el puente Yaracuy, Yaracuy, 6 II 1987, 24,60 mm LE. MBUCV–V 24232, 6; Venezuela, río Yaracuy, Yaracuy, 05 XI 1987, 21,94–26,32 mm LE. Resultados Hyphessobrycon ocasoensis sp. n. (tabla 1, figs. 1–6) Holotipo: IUQ 1635, macho 44,03 mm LE; Colombia, río Roble, afluente río La Vieja, 100 m abajo del puente peatonal Playa Azul, reserva natural "Mon te del Ocaso", Quimbaya, Quindío, 4° 35' 68" N y 75° 52' 81" O, 1100 m snm, 2 VIII 2007. Paratipos: IUQ 1634, 11, colectados con el holotipo. IUQ 1636, 2 CyT, colectados con el holotipo; MBUCV–V

García–Alzate & Román–Valencia

33746, 2, colectados con el holotipo; MCNG 55846, dos colectados con el holotipo. IUQ 1414, 2; Co lombia, río Roble en el puente hacienda playa azul, reserva natural Monte El Ocaso, Quimbaya, Quindío, 4° 35' 68'' N y 75° 52' 81'' O, 1100 m snm, 23 IX 2001. IUQ 1636, 2; Colombia, Quebrada las cañas, afluente río Cauca, vía La Paila–Zarzal, valle, 4° 21' 09'' N y 76° 04' 11'' O, 941 m snm, 6 VIII 2007. IMCN 3377, 2; Colombia, rio Risaralda en la confluencia con el rio Mapa, La Virginia, Risaralda, 24 II 2005. Diagnosis Hyphessobrycon ocasoensis se distingue por presentar tres radios simples y ocho ramificados en la aleta dorsal (vs. dos radios simples y nueve ramificados, excepto H. notidanos con iii, 8), por un maxilar corto sin dientes o con un diente (vs. maxilar largo con dos a cinco dientes), por cuatro pequeños forámenes en el maxilar (vs. sin forámenes), 15 a 17 escamas con poros en la línea lateral (vs. 8–13 escamas con poros en la línea lateral, excepto H. proteus con 17 a 22 y H. heterorhabdus con 23 a 24), seis escamas entre la línea lateral y la aleta anal (vs. cuatro a cinco, excepto H. poecilioides con cinco a seis), seis escamas entre la línea lateral y la aleta pélvica (vs. cuatro a cinco escamas entre la línea lateral y la aleta pélvica), ocho escamas predorsales (vs. 10–14 escamas predorsales) (figs. 4–5), por el ancho interorbital X = 50,6% en la longitud de la cabeza (vs. X = 38–47,4% el ancho interorbital en la longitud de la cabeza) y por registrar una mancha oscura en la base del pedúnculo caudal y una banda lateral oscura que se extiende desde la parte poste rior de la mancha humeral hasta los radios medios caudales (vs. sin una mancha oscura en la base del pedúnculo caudal y sin banda lateral oscura desde el borde postero–superior del preopérculo hasta los radios medios caudales).

Descripción Datos morfométricos y merísticos se consignan en la tabla 1. Cuerpo corto y profundo; parte dorsal de las órbitas convexo. Perfil dorsal de la cabeza y del cuerpo oblicuo desde el hocico hasta el supra occipital, y desde el supraoccipital hasta el origen de la aleta dorsal, y desde el último radio de la aleta dorsal hasta la base de la aleta caudal. Perfil ventral del cuerpo plano desde el hocico hasta la base de la aleta anal. Cabeza y hocico corto; mandíbulas iguales; boca subterminal; labios blandos y flexibles, no cubren externamente la hilera externa de dientes del premaxilar; parte ventral de la mandíbula superior plana; extremo posterior del maxilar alcanza el borde anterior de la orbita. Premaxilar con el proceso lateral largo y puntiagudo se inserta sobre el etmoides, presenta cuatro pequeños forámenes en la margen ventro– medial, con dos filas de dientes (fig. 3); fila externa con tres dientes tricúspides, orientados en zig zag; la fila interna con cinco dientes multicúspides. Los dientes disminuyen gradualmente de tamaño del di ente interno al externo. Maxilar corto, anteriormente cóncavo sin dientes o con un diente multicúspide, el extremo posterior alcanza el borde ventral del seg undo infraorbital. El dentario presenta un foramen redondeado en la región medial anterior, presenta diez dientes localizados en su borde supero–anterior; tres grandes dientes frontales con siete cúspides, seguido por un diente lateral pentacúspides, le siguen cuatro pequeños dientes tricúspides y final mente dos dientes cónicos. Seis huesos infraorbitales presentes, el tercer in fraorbital más largo y ancho, en contacto con el canal latero sensorial del preopérculo, el sexto infraorbital es el más pequeño de la serie. Anterorbital con el borde anterior cóncavo de igual tamaño que el primer infraorbital. Supraorbital ausente. El etmoides lateral

1 cm

Fig. 2. Hyphessobrycon ocasoensis sp. n.: IUQ 1635, holotipo, macho, 44,03 mm LE, Colombia. Fig. 2. Hyphessobrycon ocasoensis n. sp.: IUQ 1635, holotype, male, 44.03 mm SL, Colombia.

1 mm

Animal Biodiversity and Conservation 31.2 (2008)

1 mm

Fig. 3. Mandíbulas superior (A) e inferior (B) de Hyphessobrycon ocasoensis sp. n., IUQ 1636, paratipo. Mandíbulas superior (C) e inferior (D) de H. proteus IUQ 1009. Fig. 3. Upper (A) and lower (B) jaws of Hyphessobrycon ocasoensis n. sp., IUQ 1636, paratype. Upper (C) and lower (D) jaws of H. proteus IUQ 1009.

es un hueso largo y cóncavo que se conecta por cartílago al margen lateral del frontal. Rinosfenoides cartilaginoso, unido al orbito esfenoides. Orbitoesfenoides óseo alargado anteri ormente, con una apófisis redondeada en la parte ventral–anterior. Paraesfenoides no dividido, unido a la superficie ventral del vómer por medio de cartílago; extremo posterior del paraesfenoides en contacto por una banda de cartílago con el proótico y el basioccipital. Metapterigoideo con el borde superior ancho y con cresta, presenta un gran foramen en la región postero medial, presenta banda de cartílago en el lado anterior para unirse con el cuadrado y ventro–posteriormente para plegarse con el hiomandibular. Ectopterogoideo alargado y angosto, en contacto con el borde supero– anterior del cuadrado. Hueso nasal presente. Basihial cartilaginoso y no dividido. Placa farín gea alargada y curva, posee porciones de cartílago en los extremos dorsal y ventro–dorsal, 18 espinas branquiales. Borde de la aleta dorsal oblicuo. Pteriogóforos proximales de los radios de la aleta dorsal insertados entre las espinas neurales 9 y 15; 22 pterigóforos proximales en la aleta anal, los cinco iniciales insertados entre las espinas hemales 16 y 17. Cuatro supraneurales alargados, con cartílago entre el extremo inferior, insertados sobre la quinta y octava espinas neurales. Cintura pectoral con un

proceso dorsal puntiagudo sobre el cleitro, articulada a la parte postero lateral del cráneo por la fusión del supracleitro y el extremo ventral del postemporal, unidos al borde dorsal del cleitro. Cleitro alargado con el borde posterior ondulado, se ubica bajo el borde ventral del opérculo. Escápula anteriormente recta. El primer postcleitro ovoide no en contacto con el segundo, el tercer postcleitro alargado y recto con una prolongación ósea laminar en el borde postero medial. Cuatro radiales proximales. Aleta pélvica larga, su extremo alcanza el origen de la aleta anal. El hueso pélvico es una estructura alargada, se localiza paralelo al área central del cu erpo; hueso pélvico largo, recto y angosto, se observa cartílago en sus extremos anterior y postero lateral; el proceso isquial es una estructura larga, curva y con una apófisis puntiaguda cartilaginosa. Aleta caudal bifurcada con lóbulos largos y redondeados. Radios caudales principales 10/10 y 8/8 radios procurrentes, aleta caudal sin escamas. Número total de vértebras 28–29. Dimorfismo sexual secundario: Los machos tienen una hilera de cinco a doce espinas cortas sobre los primeros cuatro radios ramificados y del primer radio simple de la aleta pélvica, ubicadas sobre la rama interna del radio en cada segmento, con un par de espinas sobre cada porción. Aleta anal con los tres

García–Alzate & Román–Valencia

Especies

3 4 5 6 7 8 5,00 10,00 15,00 20,00 25,00 30,00 Escamas con poros en la línea lateral

Especies

3 4 5 6 7 8

4,00

6,00 8,00 10,00 Escamas predorsales

12,00

Fig. 4. Gráfico de cajas para la variación del número de escamas con poros en la línea lateral (A) y de las escamas predorsales (B) de Hyphessobrycon ocasoensis sp. n. y demás especies de Colombia: 1. H. ocasoensis sp. n.; 2. H. sovichthys; 3. H. proteus; 4. H. poecilioides; 5. H. metae; 6. H. heterorhabdus; 7. H. fernandezi; 8. H. diancistrus. Fig. 4. Box plot showing variations in the numbers of scales with pores on the lateral line (A) and of predorsal scales (B) of Hyphessobrycon ocasoensis n. sp. and other species from Colombia. (For abbreviations of species see above.)

primeros radios simples, los siguientes nueve ramifi cados, con tres a once espinas puntiagudas. Color en vivo: cuerpo verde amarillento sobre fondo plateado en la parte dorso–lateral; área latero– ventral, a partir de la cabeza hasta el orificio anal,

blanco amarillento; banda lateral plateada presente. Se observa mancha rojiza sobre el margen dorsal del ojo. Con mancha peduncular oscura, la cual se pro longa sobre los radios medios caudales. Sin mancha opercular. Aletas pectoral, pélvica, dorsal y adiposa

Animal Biodiversity and Conservation 31.2 (2008)

1 2

Especies

3 4 5 6 7 8 3,00 4,00 5,00 6,00 Escamas entre la línea lateral y la aleta anal Fig. 5. Gráfico de cajas para la variación del número de escamas entre la línea lateral y la aleta anal de Hyphessobrycon ocasoensis sp. n. y demás especies de Colombia. (Para las abreviaturas de las especies ver fig. 4.) Fig. 5. Box plot showing variation in the numbers of rows of scales between anal–fin origin and lateral line of Hyphessobrycon ocasoensis n. sp. and other species from Colombia. (For abbreviations of species see fig. 4.)

amarillas, sus extremos oscuros; primeros radios de la aleta anal blancos, seguidos de una pequeña mancha rojiza, sus extremos oscuros; lóbulos de la aleta caudal anaranjados. Los bordes posteriores de las aletas dorsal y caudal oscuros. Color en alcohol: cuerpo amarillo claro, verde oscuro en el borde dorsal, con una mancha oscura en la base del pedúnculo caudal. La parte lateral del cuerpo con una banda oscura, posterior a la mancha humeral, se extiende hasta la mancha caudal, y se ensancha a nivel de una línea trazada desde el origen de la aleta dorsal. Mancha opercular oscura, verticalmente alargada. El área posterior de las es camas oscuras. Bordes de la aleta dorsal y caudal oscuras. Aletas pectorales, pélvicas y anales hialinas; aleta anal con pigmentación oscura entre sus radios, en las membranas interradiales. Área dorsal de la cabeza oscura. Distribución En el río Roble un afluente del río La Vieja y en la quebrada de Las Cañas afluente río Cauca pertene cientes a la cuenca del Alto río Cauca (fig. 1). Etimología Epíteto especifico alusivo para la Reserva Natural Montaña el Ocaso, donde se colectaron los primeros ejemplares.

Comentarios H. ocasoensis es similar a H. proteus, se diferencian además de los caracteres diagnósticos, por la proyec ción del extremo postero ventral del primer infraorbital no en contacto con el segundo infraorbital vs. en con tacto; tres dientes en la fila externa del premaxilar vs. cinco dientes, tres dientes frontales pentacúspides en el dentario vs. cuatro dientes frontales heptacuspides, maxilar corto vs. maxilar alargado (fig. 3). El análisis de componentes principales (fig. 6) para todas las especies de Colombia no fue significativo, sin embargo, se encontró que el nuevo taxón se distingue de H. proteus en el eje I por la longitud de la mandibula superior con relación a la longitud postorbital de la cabeza y la profundidad del cuerpo; en el eje II, por la longitud del pedúnculo caudal y la longitud del maxilar. El primer componente explicó el 78,45% de la varianza total, y entre el primero y segundo componente explican el 85,80% de la va riabilidad total (tablas 3, 4). Así mismo, se distingue de H. poecilioides por la longitud del hueso maxilar (26,7–40,2% LC vs. 17,1–26,3% LC en H. poecilioides), por la longitud del hocico (18,7–32,5% LC vs. 10,4–17,8% LC en H. poecilioides). Notas ecológicas Datos obtenidos en dos estómagos de ejemplares transparentados y teñidos. Dieta predominantemente

García–Alzate & Román–Valencia

2,4

Componente 2

1,8 1,2 0,6 –3,0

–2,4

–1,8

–1,2

–0,6 –0,6

0,6

1,2

1,8

2,4

–1,2 –1,8 –2,4 –3,0 Componente 1 Fig. 6. Representación de los dos componentes principales para Hyphessobrycon ocasoensis sp. n. (+) y H. proteus (G). Fig. 6. Diagram showing the two principal components of Hyphessobrycon ocasoensis n. sp. (+) and H. proteus (G).

Tabla 3. Valores propios de los componentes principales (Cp) entre Hyphessobrycon ocasoensis sp n. y H. proteus: V. Varianza. Table 3. Eigenvalue for principal components (Cp) between Hyphessobrycon ocasoensis n. sp. and H. proteus: V. Variance.

Valores propios

0,131275

78,452

0,00037853

0,22622

0,0123658

7,3899

0,00024106

0,14406

0,00573485

3,4272

0,00022442

0,13412

0,00018661

0,11152

0,0041574

2,4845

0,00310447

1,8553

0,00018538

0,11078

0,00249431

1,4906

0,00011424

0,068268

0,00184802

1,1044

0,00010073

0,060196

6,34E–05

0,037888

0,00155413

0,92877

0,00104438

0,62413

5,37E–05

0,032072

0,00099203

0,59285

3,04E–05

0,018138

0,00065334

0,39045

2,45E–05

0,014618

0,00050577

0,30225

Animal Biodiversity and Conservation 31.2 (2008)

Tabla 4. Vectores propios de los componentes principales (Cp) entre Hyphessobrycon ocasoensis sp. n. y H. proteus. Table 4. Eigenvector for principal components (Cp) between Hyphessobrycon ocasoensis n. sp. and H. proteus. Medidas

Cp1

Cp2

Cp3

Cp4

–0,2211

0,01873

–0,003075

0,05539

–0,2055

0,03696

0,003873

0,07806

–0,2533

–0,03498

0,002862

0,262

H–AD

–0,2179

–0,0008243

0,02114

0,07099

H–AP

–0,1829

–0,08608

0,08564

0,0614

H–APL

–0,2023

–0,04081

0,02635

0,1692

H–AA

–0,2215

–0,004916

0,02356

0,129

AD–HY

–0,2261

–0,007034

–0,005928

0,08858

AD–P

–0,2477

0,02468

0,02843

0,237

AD–AA

–0,248

0,07492

0,01079

0,124

–0,1852

0,07317

0,0732

0,1144

–0,1852

0,1113

0,25

–0,02029

APL

–0,1805

0,007345

0,08339

–0,1387

–0,02747

0,01624

–0,07123

PPC

–0,2028

–0,1921

0,007996

0,133

LPC

–0,1736

–0,437

0,2948

–0,1218

–0,197

0,1521

0,1506

0,01568

–0,03768

–0,2231

–0,08615

–0,005439

–0,6361

–0,1388

0,04254

0,06223

0,02532

LPC

–0,2537

0,5165

0,304

–0,3675

LMX

–0,1623

–0,6051

–0,06656

–0,3044

AIO

–0,157

–0,1684

–0,2587

0,2471

LMS

–0,2915

0,2039

–0,7985

–0,2047

compuesta por algas, se alimenta de material alóctono principalmente Desmidiaceae Gonatozigon (55,31% Numérico y 8,92% Volumétrico), aunque también se observó restos de insectos (17,02% N y 15,17% V), larvas de Trichoptera (8,51% N y 9,82% V), larvas de Díptera (4,25% N y 5,35% V) y material no identificado (14,91% N y 60,74% V). Su hábitat se caracteriza por presentar un sustrato de piedras y detrito, el agua cristalina, una concentración de oxigeno disuelto de 5,32 mg/l, así como conductividad (126 µs) y porcen taje de saturación (76%), pH neutro (7,2). La marcada variación de la DQO, DBO, acidez, alcalinidad, turbidez y el oxigeno disuelto entre periodos climáticos (lluvias y sequía), a su vez los valores altos de DQO y DBO (230 mg/l y 73,68 mg/l respectivamente) sumados a to das las variables analizadas, indicaron que el rio Roble corresponde a un ambiente oligotrófico con tendencia a la eutroficación en época de sequia (tabla 2).

Discusión Una nueva especie de Characidae se describe como Hyphessobrycon bajo la definición propuesta por Durbin en Eigenmann (1908), adoptada por Eig enmann (1918) como primer revisor del género y recientemente ampliada por Miquelarena & López (2006). Dos de los caracteres útiles para definir al género son: 1) el tercer infraorbital no en contacto con el preopérculo y 2) cinco dientes en la fila interna del premaxilar. El primer carácter no se observó en la nueva especie y en otras especies del género como H. sovichthys, H. agulha, H. bentosi, H. sweglesi, H. fernandezi, H. proteus e H. poecilioides, a su vez, el segundo carácter no se observo en los paratipos y en el material examinado de la especie tipo H. compressus la cual presentó de 8 a 9 dientes en la fila interna premaxilar; este

conteo no reportado en ninguna de las especies definidas como Hyphessobrycon para Sudamérica, por consiguiente su diagnosis debe ser reevaluada desde una perspectiva filogenética. El número de los radios en la aleta dorsal (iii, 8) presente también en H. notidanos (Carvalho & Bertaco, 2006) (véase diagnosis), es un conteo raro para Hyphessobrycon, inclusive otros géneros de Characidae, a su vez el segundo diente del dentario expuesto frontalmente por fuera de la hilera de dientes (fig. 3) podrían sugerir sinapomorfias para este grupo. Géry (1977) en su clave de especies del género Hyphessobrycon reconoce seis grupos artificiales basados en la combinación de modelos de coloración. Esta agrupación no es aplicable para H. ocasoensis porque el modelo de coloración cambió posterior a su fijación en vivo presentó sólo una mancha caudal; que lo ubicaría dentro del grupo minimus; mientras que una vez fijado mostró una banda lateral oscura que lo incluye dentro del grupo heterorhabdus. Es tos resultados demuestran la poca utilidad de la diferenciación entre especies basados en modelos de coloración. Algunos autores ya han señalado este hecho especialmente Lima & Moreira (2003) y Carvalho & Bertaco (2006) al describir cinco especies del género Hyphessobrycon que fueron adscritos en grupos extremadamente heterogéneos. Se demuestra que las especies trans–interandinas se caracterizan por ser de gran tamaño y extremada mente robustas, comparadas con las demás especies cisandinas. Para el Alto Cauca se reportaba H. poecilioides como endémica (Román–Valencia, 1995) y se confirma que la mayor riqueza de especies de éste género ocurre en las áreas cisandinas. Agradecimientos Se recibió financiación de la Universidad del Quindío– Vicerrectoría de Investigaciones (proyecto 357) y programa Académico de Biología. Donald C. Taphorn (MCNG) y tres revisores anónimos por la lectura crí tica del manuscrito, por sus generosos comentarios y excelentes correcciones. A las siguientes personas por el préstamo, donación o acceso a material bajo su cuidado: Mark Sabaj Pérez (ANSP), Janeth Mu ñoz Saba (ICMNH), Armando Ortega–Lara (IMCN); Francisco Provenzano (MBUCV), Carlos Alberto Lu cena (MCP), Carlos A. Lasso y Oscar Lasso–Alcalá (MHNLS), Luz Fernanda Jiménez (CIUA) y Héctor Espinoza (IBUAM–P). John Fong (CAS) y James Maclain (BMNH) por el amable y oportuno envío de las imágenes de los tipos. Dahiana K. Arcila Mesa, Alejandro Londoño y Anyelo Vanegas R. (IUQ) cola boraron durante el trabajo de campo. Referencias Almirón, A., Casciotta, J., Bechara, J. & Ruiz–Díaz, F., 2004. A new species of Hyphessobrycon (Characiformes,Characidae) from the Esteros del Iberá wetlands, Argentina. Revue Suisse de

García–Alzate & Román–Valencia

Zoologie, 111(3): 673–682. Bertaco, V. A. & Malabarba, L. R., 2005. A new species of Hyphessobrycon (Teleostei: Characidae) from the upper–Rio Tocantins drainage, with bony hooks on fins. Neotropical Ichthyology, 3(1): 83–88. Capitoli, R., 1992. Método para estimar volúmenes do conteúdo alimentar de peixes e macroinverte brados–Atlantica. Rio Grande, 4: 17–120. Carvalho, T. P. & Betarco, V. A., 2006. Two new spe cies of Hyphessobrycon (Teleostei: Characidae) from upper rio Tapajós basin on Chapada dos Parecis, Central Brazil. Neotropical Ichthyology, 4(3): 301–308. Eigenmann, C. H., 1908. Zoological results of the Thayer Brazilian expedition. Preliminary descrip tion of new genera and species of tetragonopterid characins. Bulletin of Museum of Comparative Zoology, 52(6): 93–106. – 1913. Some results from an ichthyological recon naissance of Colombia, South America, Part II. Indiana University Studies, 18: 1–32. – 1918. The American Characidae. Part 2. Memoirs of Museum of Comparative Zoology, 43: 103–208. Eigenmann, C. H. & Henn. A. W., 1914. On new species of fishes from Colombia, Ecuador, and Brazil. Contribution Zoology Lab. Indiana University, 24: 231–234. Géry, J., 1977. Characoids of the World. TFH Publi cation Neptune City, NJ. Hammer, Ø., Harper D. A. T. & Ryan, P., 2001. PAST: Paleontological Statistics Software Package For Education And Data Analysis. Palaeontologia Electronica, 4(1): 1–9. Hynes, H. B. N., 1950. The food of Fresh–water Sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius) with a review of methods used in studies of the food of fishes. Journal Animal Ecology, 19: 36–58. Hyslop, E. J., 1980. Stomach contents analysis – a review and methods and their application. Journal Fish Biology, 17: 411–429. Lima, F., Malabarba, L., Buckup, P., Pezzi Da Silva, J., Vari, R., Harold, A., Benine, R., Oyakawa, O., Pavanelli, C., Menezes, N., Lucena, C., Malabarba, M., Lucena, Z., Reis, R., Langeani, F., Casatti, L., Bertaco, V., Moreira, C. & Lucinda, P., 2003. Genera Incertae Sedis in Characidae. In: Check List of the Freshwater Fishes of South and Central America: 106–169 (R. Reis, S. Kullander & C. Ferraris, Eds.). Edipucrs, Porto Alegre. Lima, F. & Moreira, C., 2003. Three new species of Hyphessobrycon (Characiformes: Characidae) from the upper río Araguaia basin in Brazil. Neotropical Ichthyology, 1(1): 21–33. Lucena, C., 2003. New characid fish, Hyphessobrycon scutulatus, from the rio Teles Pires drainage, upper Rio Tapajós system (Ostariophysi: Chara ciformes: Characidae). Neotropical Ichthyology, 1(2): 93–96. Malabarba, L. & Weitzman, S., 2003. Description a new genus with new species from southern Brazil, Uruguay and Argentina, with a discussion of a putative characid clade (Teleostei: Characiformes:

Animal Biodiversity and Conservation 31.2 (2008)

Characidae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, Porto Alegre, 16(1): 67–151. Miquelarena, A. M. & Lopez, H. L., 2006. Hyphes sobrycon togoi, a new species from the La Plata basin (Teleostei: Characidae) and comments about the distribution of the genus in Argentina. Revue Suisse de Zoologie, 113(4): 817–828 Román–Valencia, C., 1995. Lista anotada de los peces de la cuenca del río La Vieja, alto Cauca, Colombia. Boletín Ecotrópica, 29: 11–20. Ruiz–Calderón R. I. & Román–Valencia, C., 2006. Osteología de Astyanax aurocaudatus, Eigenn man, 1913 (Pisces: Characidae), con notas sobre la validez de Carlastyanax, Géry, 1972. Animal Biodiversity and Conservation, 29(1): 49–51. Song, J. & Parenti, L. R., 1995. Clearing and staining whole fish specimens for simultaneous demostration of bone, cartilage and nerves. Copeia: 114–118. Taylor, W. R. & Van Dyke, G. C., 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119. Ulrey, A., 1894. Preliminary descriptions of some new South American Characinidae. American Naturalist, 610–611.

Vari, R. P., 1995. The neotropical fish family Cteno luciidae (Teleostei: Ostariophysi: Characiformes) supra and intrafamilial phylogenetic relationships, with a revisionary study. Smithsonian Contribution to Zoology, 564: 1–96. Weitzman, S. H., 1962. The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological. Bulletin, 8(1): 03–77. – 1977. A new species of Characoid fish, Hyphessobrycon diancistrus, from the Río Vichada, Orinoco river drainage, Colombia, South America (Teleostei: Characidae). Proceedings of the Biological Society of Washington, 90(2): 348–357. Weitzman, S. H. & Malabarba L. R., 1999. Syste matics of Spintherobolus (Teleostei: Characidae: Cheirodontinae) from eastern Brazil. Ichthyological Exploration of Freshwaters, 10: 1–43. Weitzman, S. H. & Palmer, L., 1997. A new spe cies of Hyphessobrycon (Teleostei: Characidae) from the Neblina region of Venezuela and Brazil, with comments on the putative, rosy tetra clade. Ichthyological Exploration of Freshwaters, 7(3): 209–242. Wetzel, R. & Likens, G., 2000. Limnological analyses, 3 ed. Nueva York: Springer–Verlag.

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 31.2 (2008)

Population genetic structure in natural and reintroduced beaver (Castor fiber) populations in Central Europe R. Kautenburger & A. C. Sander

Kautenburger, R. & Sander, A. C., 2008. Population genetic structure in natural and reintroduced beaver (Castor fiber) populations in Central Europe. Animal Biodiversity and Conservation, 31.2: 25–35. Abstract Population genetic structure in natural and reintroduced beaver (Castor fiber) populations in Central Europe.— Castor fiber Linnaeus, 1758 is the only indigenous species of the genus Castor in Europe and Asia. Due to extensive hunting until the beginning of the 20th century, the distribution of the formerly widespread Eurasian beaver was dramatically reduced. Only a few populations remained and these were in isolated locations, such as the region of the German Elbe River. The loss of genetic diversity in small or captive populations through genetic drift and inbreeding is a severe conservation problem. However, the reintroduction of beaver populations from several regions in Europe has shown high viability and populations today are growing fast. In the present study we analysed the population genetic structure of a natural and two reintroduced beaver populations in Germany and Austria. Furthermore, we studied the genetic differentiation between two beaver species, C. fiber and the American beaver (C. canadensis), using RAPD (Random Amplified Polymorphic DNA) as a genetic marker. The reintroduced beaver populations of different origins and the autochthonous population of the Elbe River showed a similar low genetic heterogeneity. There was an overall high genetic similarity in the species C. fiber, and no evidence was found for a clear subspecific structure in the populations studied. Key words: Beaver, Castor fiber, Castor canadensis, Genetic diversity, RAPD, Reintroduction. Resumen Estructura genética en poblaciones naturales y reintroducidas de castor (Castor fiber) en Europa Central.— El castor euroasiático (Castor fiber Linnaues, 1758) es la única especie autóctona del género Castor en Europa y Asia. Debido a la intensa presión cinegética a la que fue sometido hasta principios del siglo XX, su amplia distribución se vio drásticamente reducida. Tan sólo sobrevivieron algunas poblaciones en áreas aisladas, como por ejemplo en la zona del río Elba en Alemania. La pérdida de diversidad genética en poblaciones pequeñas o criadas en cautividad, causada por la deriva genética y la endogamia, supone un grave problema para la conservación de esta especie. Por otro lado, los ensayos de su reintroducción en distintas zonas de Europa han puesto de manifiesto que las poblaciones poseen una gran viabilidad y altas tasas de crecimiento. En el presente estudio se ha analizado la estructura genética de una población natural y dos reintroducidas en Alemania y Austria. Además, se muestra la diferenciación genética entre dos especies de castor, el castor euroasiático y el castor americano (C. canadensis), utilizando RAPD (polimorfismo de fragmentos de ADN amplificados al azar) como marcador genético. La población de castor reintroducida a partir de diferentes orígenes y las poblaciones autóctonas del río Elba muestran una baja heterogeneidad genética. Existe una alta semejanza genética en la especie C. fiber, no hallándose evidencias de una estructura subespecífica en las poblaciones estudiadas. Palabras clave: Castor, Castor fiber, Castor canadensis, Estructura genética, RAPD, Reintroducción. (Received: 11 I 08; Conditional acceptance: 13 III 08; Final acceptance: 9 IX 08) Ralf Kautenburger, Inst. of Inorganic and Analytical Chemistry and Radiochemistry, Saarland Univ., D–66041 Saarbrücken, Germany.– Anna–Christine Sander, Dept. of Animal Ecology, Justus–Liebig Univ., Heinrich–Buff– Ring 26–32 (IFZ), D–35392 Gießen, Germany. Corresponding author: R. Kautenburger. E–mail: kautenburger@mx.uni–saarland.de ISSN: 1578–665X

Introduction The genus Castor is the only living representative of the family Castoridae, with two species: Castor fiber, Linnaeus 1758 and Castor canadensis, Kuhl 1820 (Heidecke, 1998). C. fiber was once widespread in the holarctic, from Europe to northern Asia, as the result of glacial and postglacial climatic changes (Veron, 1992). However, populations in western Europewere limited to a few isolated sites (in the Elbe River in Germany, the Rhône River in France, and southern Norway) by the end of the 19th century due to over–hunting for pelts, meat and castoreum (a secretion from their scent glands). Habitat loss was also probably a contributory factor. A few small populations survived further east in Belarus, Russia and Mongolia. Only a local population of approximately 200 individuals survived in Germany, in the region of the Elbe River. Since 1966 extensive reintroduction programs have reinstated beavers in many European countries. In western Germany, the first reintroduction program took place in the 1960s when beavers from Poland and Russia were released into the Danube watershedin Bavaria. In total, 120 beavers (C. fiber) of different origins were reintroduced along the rivers Danube and Inn between 1966 and 1975. By 2000, their numbers had increased to over 5000 individuals (Schwab & Lutschinger, 2001). Reintroduction programmes were also started in Austria and between 1976 and 1988 a total of 42 beavers, including 5 C. canadensis, were released along the Danube River east of Vienna. (Kollar, 1992). The population size in 2001 was estimated at approximately 1300 animals (Schwab & Lutschinger, 2001), but it is unknown how many of these were C. canadensis (Kollar & Seiter, 1990; Sieber, 1998). Nowadays, reintroduced populations in several regions in Europe are highly viable and growing fast, with beavers emigrating from Bavaria and Austria to adjacent areas (Halley & Rosell, 2002). It is generally accepted that the local extinction of a species is followed by a bottleneck effect, implementing a reduction in the genetic diversity of the population (Avise, 1994). Reintroduction of a species with a few individuals leads to an artificial bottleneck, and this also reduces genetic diversity. The genetic impact of a potential bottleneck in the natural population and a founder effect in the reintroduced populations of C. fiber are still unclear. Nevertheless, successful reintroduction suggests that C. fiber is not sensitive to inbreeding and population growth does not appear to have been reduced due to any potential loss of genetic diversity (Nolet & Baveco, 1996). For conservation management strategies, it is necessary to analyse the genetic structure of natural and reintroduced beaver populations in order to ensure long–term viability of this key–species in riverine ecosystems, to preserve genetic diversity within the species and to prevent sensitivity to potential disease and parasitism (Nolet et al., 1997; Babik et al., 2005). In the present study, we analysed the population genetic structure of two reintroduced beaver populations in the Danube River system east of Vienna

Kautenburger & Sander

(Austria) and in Bavaria (Germany) and one natural population of C. fiber in the Elbe River system in eastern Germany, using random amplified polymorphic DNA (RAPD) (Welsh & McClelland, 1990; Williams et al., 1990). Multilocus DNA markers are important for population studies, because they reveal many polymorphic loci distributed over the genome (Zhivotovsky, 1999; Krauss, 2000). Despite some methodological shortcomings (e.g. Bielawski et al., 1995; Grosberg et al., 1996), this fast and low–cost approach of RAPD–PCR has proven to deliver very useful information on population genetic structure and taxonomy without previous sequence information (e.g. Nebauer et al., 2000; Vucetich et al., 2001; Callejas & Ochando, 2002; Vandewoestijne & Baguette, 2002; Kautenburger, 2006a, 2006b). This study addresses the following questions: Has the natural population of C. fiber in the Elbe River system undergone a loss in genetic diversity due to the severe bottleneck over the 19th century as compared to the reintroduced C. fiber populations from different origins in the Danube River system, and can RAPD markers reveal a genetic differentiation among the analysed beaver populations? Material and methods Study species The genus Castor consists of two species: the Eurasian beaver C. fiber and the American beaver C. canadensis. The two species have a semi–aquatic life–style and are very similar in appearance and behaviour (Nolet, 1997). Beavers live in freshwater habitats lined by rich vegetation and they use trees to build dams and lodges (Macdonald et al., 2000). They are monogamous and live in small colonies, typically an adult pair and their offspring. They produce up to three young per year in a single litter (Wilsson, 1971). Beavers have an average life expectancy of seven to eight years. Dispersal usually takes place at a year and a half to two years of age and maximum distance recorded is about 170 km (Heidecke, 1984). DNA samples C. fiber is a protected animal species in Germany and Austria, as in many parts of Europe, and it is still under threat of extinction (IUCN red list category: NT. Near threatened; European Union red list category: LC. Least concern). Muscle tissue is therefore collected from dead animals (accident, or natural death). A total of 35 individuals were sampled for DNA typing as shown in table 1. Tissue samples were taken from 31 C. fiber and four C. canadensis). The C. fiber samples were collected from three different populations: 11 animals from the autochthonous Elbe River population (two that had been reintroduced into the Kinzig River in Hessen, Germany, and one that had been reintroduced into the Prims River in Saarland, Germany; 13 individuals from the reintroduced Bavarian Danube population;

Animal Biodiversity and Conservation 31.2 (2008)

Table 1. Overview of the analysed beaver samples: Pop. Population; Ss. Sample size. Tabla 1. Muestras de castores analizadas: Pop. Población; Ss. Tamaño de la muestra. Pop

Origin

Austria

Austria/Danube

Ss 7

Castor fiber spp.

Canada

Austria/Danube

Castor canadensis

Elbe

Germany/Kinzig–Prims

Castor fiber albicus

Elbe

Germany/Elbe

Castor fiber albicus

Bavaria

Germany/Danube

Canada

Germany/Danube

and seven from the reintroduced Austrian Danube population east of Vienna (fig. 1) For comparison, four American beavers, three from Bavaria and one from Austria, were included as the out–group for the statistical analysis. All samples were stored at –20°C until further DNA analyses.

Species/Subspecies

Castor fiber spp. Castor canadensis

DNA extraction Genomic DNA was extracted from muscle tissue using the salt–chloroform method adapted from Mullenbach et al. (1989). Frozen tissue (50–60 mg) was grounded in liquid nitrogen, transferred to a sterile

Elbe

Germany Kinzig Prims

Bavaria

100 km

Austria

Sampling regions Sampling sites

Fig. 1. Geographic distribution of the sampling sites (individual beaver samples marked with an asterisks were assigned to the Elbe population) in Austria and Germany. Fig. 1. Distribución geográfica de los lugares de muestreo (las muestras de castores individuales marcadas con un asterisco se asignaron a la población del Elba) en Austria y Alemania.

Kautenburger & Sander

Table 2. RAPD primers used in the study, size and number of amplified DNA–fragments for each primer, number of polymorphic bands, and percentage of polymorphic bands in brackets: B. Bands in total; P. Polymorphic bands (%). Tabla 2. RAPD primers utilizados en el estudio, tamaño y número de los fragmentos de ADN amplificados para cada primer, número de bandas polimórficas, y entre paréntesis porcentaje de bandas polimórficas: B. Bandas totales; P. Bandas polimórficas (%).

Primer

Sequence (5´–3´)

Roth 180–01

Castor fiber

Castor canadensis

Size (bp)

P (%)

GCACCCGACG

250–1,600

9 (69.2)

4 (50.0)

Roth 180–04

CGCCCGATCC

300–1,900

11 (64.7)

5 (38.5)

Roth 180–06

GCACGGAGGG

400–1,080

8 (66.7)

2 (16.7)

Roth 180–08

CGCCCTCAGC

400–1,100

8 (61.5)

4 (40.0)

36 (65.5)

15 (34.9)

Total

tube with 0.5 ml of extraction buffer (160 mM saccharose, 80 mM EDTA, 100 mM Tris/HCl, pH 8.0), and 20 µl proteinase K (20 mg/ml) and incubated for 16 hours overnight at 60°C. After the addition of 180 µl 6 M NaCl, proteins and lipids were removed using two extraction steps with 700 µl phenol–chloroform– isoamyl alcohol (25:24:1). DNA was precipitated by addition of twice the volume of ice–cold ethanol. The DNA pellet was recovered by centrifugation, washed in 70% ethanol, dried and dissolved in 500 µl H2O. DNA was quantified and qualified with a photometer (260 nm for the concentration, ratio of 260 nm and 280 nm for the purity); additionally, samples were checked on a 1.4% agarose gel. RAPD reactions Ten oligonucleotide (10mer) primers (Carl Roth GmbH & Co., Karlsruhe, Germany; kit 180–01 to –10) were tested. Amplifications were carried out in 25 µl volumes containing 10 mM Tris–HCl, pH 8.8 at 25°C, 1.5 mM MgCl2, 150 mM KCl, 0.1% Triton X–100 (1 x PCR– buffer, Finnzymes, Espoo, Finland), 0.5 U DNAzymeTM II Polymerase (Finnzymes, Espoo, Finland), 1 mM of primer, 0.2 mM dNTPs (Amresco, Solon, USA) and 100 ng template DNA. The DNA was amplified in a thermal cycler (Progene 02, Techne, Cambridge, UK) programmed for an initial denaturation of 120 s at 94°C, followed by 45 cycles of 30 s at 94°C, 60 s at 42°C, and 120 s at 72°C. The final primer extension step was extended to 10 min at 72°C. PCR products were analysed by electrophoresis on 1.4% agarose gels in 1 x TBE buffer (89 mM Tris–borate, 2 mM EDTA, pH 8.0) for approximately 4 hours at 70 V (55 mA), visualized by staining with ethidium bromide and photographed under UV radiation with a Polaroid type 667 film (Polaroid, Waltham, USA). PCR–conditions were optimized following Bielawski et al. (1995). In order to ensure reproducible results and minimise errors one beaver sample was randomly

chosen and amplified with each PCR as positive control, another sample was amplified twice in the same PCR. Duplicate amplifications (PCR runs) were conducted for each sample. Bands which could not be reproduced in both assays were not considered for analysis. Statistical analysis DNA fragments generated by RAPD analysis were scored as an individual locus and each locus represents a two–allele system. The banding patterns were converted into a binary matrix based on presence (1) or absence (0) of RAPD markers. Bands with the same size were regarded as homologous (Grosberg et al., 1996) and differences in intensity were not considered. Faint or irregularly appearing bands were not included (Williams et al., 1993). The estimation of allele frequency for dominant markers presents some statistical difficulties. However, estimates of allele frequency can generally be applied in highly polymorphic dominant markers (Krauss, 2000; Tero et al., 2003). Similarity indices (S) according to Nei & Li (1979) were calculated, where S = 2mxy / (mx + my), with mxy being the number of shared markers between two individuals, while mx and my are the number of markers for each individual. The mean values of the similarity index and the mean genetic distances (Nei, 1972) were statistically compared using Mann– Whitney U–test (Spss 10.0.7 for Windows, Spss Inc., Chicago, USA). Because the reintroduced beaver populations were not expected to have Hardy–Weinberg–Equilibrium, the method by Lynch & Milligan (1994) was not appropriate in this case. Therefore, we alternatively treated the multilocus phenotype as a haplotype in the programs Popgene 1.31 (Yeh & Boyle, 1997) and Arlequin 2.000 (Schneider et al., 2000), as suggested by Huff et al. (1993), Holsinger et al. (2002) and Jimenez et al. (2002). Intrapopulational genetic diversity h (Nei,

Animal Biodiversity and Conservation 31.2 (2008)

Table 3. Similarity index S (Nei & Li, 1979) within populations (in italics) and between populations. Means are given with their standard deviations. Tabla 3. Índice S de similitud (Nei & Li, 1979) dentro de las poblaciones (en cursiva) y entre las poblaciones. Se dan las medias junto con sus desviaciones estándar.

Austria (n = 7)

Elbe (n = 11)

Bavaria (n = 13)

Austria

0.853 ± 0.053

Elbe

0.837 ± 0.055

0.889 ± 0.051

Bavaria

0.852 ± 0.050

0.860 ± 0.069

0.932 ± 0.029

C. canadensis

0.746 ± 0.078

0.744 ± 0.033

0.761 ± 0.022

1987) and genetic distances D (Nei, 1972) among the analysed populations were evaluated using Popgene. Population structure was checked by an analysis of molecular variance (AMOVA; Excoffier et al., 1992) using Arlequin. Standard variance components and f– statistics were calculated using AMOVA. We performed this analysis first with the C. fiber samples only, and in the next step we included the C. canadensis as a separated outgroup to the AMOVA analysis. We produced a set of 1000 genetic distance (Nei, 1972) matrices by bootstrapping (with randomised data entry) over all RAPD loci using the program Rapddist 1.0 (Black, 1996). Phylogenetic relationships (majority rule consensus tree) between all individuals were constructed based on a Neighbor– Joining algorithm (Saitou & Nei, 1987) using the Neighbor and Consense program in Phylip 3.57c (Felsenstein, 1995). In addition, the 0/1–matrix was subjected to a principal component analysis (PCA; Statistica 5.0, StatSoft, Tulsa, USA). The PCA achieves an ordination of the individuals according to the presence or absence of RAPD markers along principal component axes (Manly, 1994). Results The four best performing primers (Roth 180–01, –04, –06 and –08), according to reproducibility and polymorphic banding pattern, were chosen for all samples. Sequences and detailed information on the RAPD primers used are listed in table 2. PCR– products ranged from 250 bp to 1900 bp. In total, 55 reproducible bands were obtained for C. fiber, 36 of which (65.5%) were polymorphic. C. canadensis showed a total of 43 reproducible bands, fifteen of these markers (34.9%) were polymorphic. We found one diagnostic RAPD marker (180–04 1000 bp) that was monomorphic for C. fiber and absent in the C. canadensis samples. Furthermore, we identified four other diagnostic markers (180–01 250 bp, 180–04 1350 bp, 180–08 450 bp, 180–08 400 bp) that were only fixed in the C. fiber samples.

C. canadensis (n = 4)

0.891 ± 0.059

Similarity indices (S) within and among the C. fiber populations were generally high (table 3). Overall, the similarity indices within the beaver populations (mean: 0.891 ± 0.032 SD) were not significantly higher (U–test: P = 0.13) than the genetic similarity among the C. fiber populations (mean: 0.850 ± 0.012 SD), while the similarity indices were significantly higher among these populations and the analysed C. canadensis samples (mean: 0.750 ± 0.009 SD; U–test: P = 0.05). Within the populations, individuals from Bavaria showed the highest similarity, whereas the Austrian population showed the lowest value for genetic similarity. The comparison between the Austrian beavers and samples from the Elbe River showed the lowest similarity among the C. fiber populations. The three C. fiber populations showed a moderate genetic differentiation (AMOVA: 18.2% of the variation among the three analysed populations, table 4). Furthermore, adding C. canadensis as a second group, the analysis of the genetic structure of the populations by AMOVA analysis revealed that over 44% of the genetic variance was situated within the single populations. However, there was still a significant differentiation between population units (> 9%), suggesting slightly phenotypic variation among the C. fiber populations. The portion of molecular variances among the C. fiber populations and the C. canadensis individuals amounted to over 45%. All three levels are highly significant (P < 0.001). The average intrapopulational genetic diversity h calculated following Nei (1987) within C. fiber populations was 0.183, whereas the samples from Bavaria showed a lower value, and the individuals from Austria the highest value (table 5). The C. fiber populations showed overall low genetic distances (table 5) and again C. canadensis was significantly distinguished from the C. fiber populations (mean: 0.291 ± 0.046 SD; U–test: P = 0.046). The consensus tree (fig. 2) that resulted from the Neighbor–Joining cluster analyses of all beaver samples revealed three groups: the C. canadensis samples, three C. fiber samples (A2, A3 and A7)

Kautenburger & Sander

Table 4. Results of the hierarchical analysis of molecular variance (AMOVA) within and among the beaver populations sampled, using 55 RAPD markers. Notice that the analysed C. canadensis individuals were regarded as one population. Among populations within groups are the individuals of C. canadensis as one group and the three C. fiber populations as the second group. The level of significance is based on 1,023 random permutations: Df. Degree of freedom; Sq. Sum of squares; Vc. Variance components; Pv. Percentage of variation; Fi. Fixation indices (NC. Not computed; fCT. Correlation of random RAPD phenotypes within groups relative to total; fSC. Correlation within populations relative to group; fST. Correlation within populations relative to total). Tabla 4. Resultados del análisis jerárquico de la varianza molecular (AMOVA) dentro y entre las poblaciones de castor muestreadas, utilizando los marcadores RAPD 55. Obsérvese que los individuos analizados de C. canadensis se consideraron como una población. En el análisis entre poblaciones, los individuos de C. canadensis se consideraron como un grupo, y las tres poblaciones de C. fiber como un segundo grupo. El nivel de significación se basa en 1.023 permutaciones al azar: Df. Grados de libertad; Sq. Suma de cuadrados; Vc. Componentes de la varianza; Pv. Porcentaje de variación; Fi. Índices de fijación (NC. No computado; fCT . Correlación entre los fenotipos RAPD tomados al azar dentro de los grupos en relación con el total; fSC. Correlación dentro de las poblaciones en relación con el grupo; fST. Correlación dentro de las poblaciones en relación con el total). Source of variation

P–value

Three C. fiber populations Among C. fiber populations

28.28

0.974

18.23

Within C. fiber populations

122.30

4.368

81.77

< 0.0001 fST = 0.1823 NC

Two groups (beaver species) Among groups

40.98

4.512

45.97

< 0.0001 fCT = 0.4597

Among populations within groups

28.28

0.978

9.97

< 0.0001 fSC = 0.1845

Within populations

134.05

4.324

44.06

< 0.0001 fST = 0.5594

from the Austrian population and the remaining C. fiber samples from Austria, Bavaria and from the Elbe River. Bootstrapping supported these groups. To gain more detailed insight into the multidimensional relationships among individuals of C. fiber and C. canadensis, we constructed a three–dimensional plot of the PCA from the 35 RAPD phenotypes (fig. 3). The first three principal components accounted for 43.1%, 10.3% and 9.6% (= 63.0%) of the total variance. Among the other 17 principal components greater than zero, none accounted for more than 5.3% of the variation. Individuals of C. canadensis were clearly separated from the individuals of the C. fiber populations. Additionally, a small group of three Austrian beaver samples was detected in an intermediate range between the C. canadensis and the C. fiber clusters, confirming the results above. No separation between individuals from the Elbe River, Bavaria or Austria was detected among the remaining C. fiber samples. Discussion This paper reports initial findings on the genetic structure in populations of Castor fiber in Germany and Austria. The genetic similarity (S) of the three European populations analysed was relatively high

within populations (mean values ranging from 0.853 to 0.932) and among populations (from 0.744 to 0.860). C. canadensis samples showed a similar small genetic

Table 5. Genetic distance D (Nei, 1972) among the analysed populations of C. fiber and C. canadensis (below diagonal, italic) and intrapopulational genetic diversity h (Nei, 1987): A. Austria; E. Elbe; B. Bavaria. Tabla 5. Distancia genética D (Nei, 1972) entre las poblaciones analizadas de C. fiber y C. canadensis (por debajo de la diagonal, en cursiva) y diversidad genética intrapoblacional h (Nei, 1987): A. Austria; E. Elba; B. Baviera. Pop

Austria

0.225

Elbe

0.050

0.177

Bavaria

0.056

0.071

0.111

C. canadensis

0.238

0.318 0.318 0.142

Animal Biodiversity and Conservation 31.2 (2008)

Bavaria B12 Bavari B9

Bavaria B13 Bavaria B11 Austria A6 Bavaria A7 Elbe E4 Bavaria B10 Bavaria B2 Bavaria B1

Elbe E3 Bavaria B4 Bavaria B3

Bavaria B5 55

Austria A1 Bavaria B6 Elbe E9

Austria A5 Austria A4 Bavaria B8 Elbe E1

Elbe E11 Elbe E7 Elbe E8 Elbe E2

Elbe / Prims ER10 Elbe / Kinzing ER5

92 59

Elbe / Kinzing ER6 Austria A7 Austria A2 Austria A3

C. canadensis C4 97

C. canadensis C2 C. canadensis C3 C. canadensis C1

Fig. 2. Neighbour–joining tree based on Nei’s (1972) genetic distance among all analysed beaver samples. Bootstrap support of the nodes (1,000 permutations) is only included if they exceed 50%. The C. canadensis sample C1 served as outgroup. Fig. 2. Árbol filogenético de unión de vecinos ("neighbour–joining") basado en la distancia genética de Nei (1972) entre todas las muestras de castor analizadas. Sólo se incluye el muestreo ("bootstrap") soporte de los nodos (1.000 permutaciones) si superan el 50%. La muestra C1 de C. canadensis sirvió de grupo de comparación ("outgroup").

Kautenburger & Sander

1.0

C. fiber

0.8 0.6 0.4 C. canadensis

0.2 0.0

1.0

0.8

0.6

0.4

0.2

0 0. 2 0. 0.0 – –0 4 . .2 0 –

0 1. 8 . 0 .6 0 .4 0 2 0.

Fig. 3. Principal components analysis (Varimax normalised factor rotation) of the binary RAPD data of the different beaver samples: C. C. canadensis; E. C. fiber from Elbe; ER. Kinzig and Prims (reintroduced samples from Elbe); A. Austria; B. Bavaria. Fig. 3. Análisis de componentes principales (rotación de factores normalizados Varimax) de los datos RAPD binarios de las distintas muestras de castores: C. C. canadensis; E. C. fiber del Elba; ER. Kinzig y Prims (muestras del Elba reintroducidas); A. Austria; B. Baviera.

variation, probably because our sample was small. Lizarralde et al. (2008) have recently analysed a total of 30 specimens (with 5 specimens from Alaska as an outgroup) of C. canadensis, which was introduced into Isla Grande de Tierra del Fuego, Argentina in 1946. They found a high genetic variation in partial sequences of Cytochrome b, 12S rRNA genes and the main non–coding D–loop region. We did not find population specific RAPD markers for C. fiber, but there was a clear difference in the banding pattern (in form of "diagnostic markers") in C. canadensis individuals. Tamate et al. (1995) interpret the absence of population–specific markers as evidence of kinship between the individuals of the different populations. Our findings agree with previously published data on protein polymorphisms of American beavers (Hoppe et al., 1984) and with allozyme analysis of reintroduced C. fiber populations from Kirov and Novosibirsk in Russia (Milishnikov & Savel’ev, 2001; Milishnikov, 2004). These studies revealed only relatively low levels of enzyme variation, and genetic differences between the analysed

beaver populations in all studied loci were very small. Using DNA fingerprinting population genetic studies of reintroduced Scandinavian beavers displayed a similar low heterogeneity, with a mean similarity coefficient of 0.80, and only monomorphic MHC loci (Ellegren et al., 1993). Kappe et al.’s (1997) studies on harbour seal subspecies (Phoca vitulina ssp.) with multilocus DNA fingerprinting by revealed similar results. The subspecies P. vitulina vitulina also revealed high values of similarity coefficients both within and among the analysed populations of the Dutch Wadden Sea and the east coast of Scotland (S = 0.79 to 0.87 and 0.74–0.79 respectively), as a result of a severe bottleneck during the last glaciation. Our results also agree with Durka et al. (2005) and Ducroz et al. (2005) who analysed the nucleotide variation in the mitochondrial DNA control region (mtDNA CR) from 152 specimens of Castor fiber from 39 localities in France, Germany, Norway, Poland, Lithuania, Russia and Mongolia. Over this large geographical scale, they found an extreme genetic structuring as the result of an apparent cessation of gene flow. As

Animal Biodiversity and Conservation 31.2 (2008)

in our study, they also found no or only a little genetic variation for the analysed beaver populations from Central Europe (beaver populations from Germany, France and Norway clustering together and distinct from populations east of the Oder and Vistula Rivers). On the intrapopulational level the sequence variation of the assayed fragment of the mtDNA CR within the relict Castor fiber populations was also very low. The authors conclude that this very low level of intrapopulational variation may be attributed to a recent bottleneck. In our study, there was no significant differentiation among the original local beaver population of the Elbe River and the reintroduced animals of the Danube River system and the overall genetic similarity was relatively high. No specific bottleneck effect was detected, and the overall within–species genetic variation was low. It stands out, however, that the Austrian population, established from individuals of different origins, showed the lowest genetic similarity among all C. fiber populations, displaying a relatively high genetic heterogeneity of the reintroduced individuals and no evidence for a founder effect. These results are consistent with the assumption that loss of heterozygosity is very slow and depends on the population size and the length and the depth of a potential population reduction (Amos & Balmford, 2001). The overall high genetic similarity of C. fiber might be due to other factors, such as postglacial colonisation, and it does not seem to reduce recolonisation success. Regarding the cluster analysis and the PCA in more detail, we propose that the three Austrian beavers, grouped among the other C. fiber and C. canadensis samples, show a genetic structure in between the two species. These results suggest that these three intermediate individuals are possible offspring from reintroduced eastern C. fiber subspecies or perhaps hybrids between different beaver subspecies. This is also supported by the genetic diversity of the analysed populations, as only the beaver samples from the reintroduced population in Austria show a relatively high value, compared to the other two populations. Hybridisation between C. fiber and C. canadensis seemed to be unlikely because breeding experiments were not successful in captivity (Djoshkin & Safonow, 1972; Kuehn et al., 2000; Halley & Rosell, 2002) and the karyotypes of the two species are different (Lizarralde et al., 2004). For long–term conservation strategies, the autochthonous C. fiber populations might be the hot spots of beaver conservation, as Durka et al. (2005) suggested. New reintroduction programs of beavers in Europe should be accompanied by a clear genetic identification of reintroduced individuals so as to prevent reintroduction of C. canadensis in Europe. Further analyses using co–dominant techniques in a larger sample of individuals should be performed to confirm these first results of an interspecific gene flow. Acknowledgments This project was financially supported by the "Hessische Gesellschaft für Ornithologie und Naturschutz"

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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 31.2 (2008)

Autumn–winter diet of three carnivores, European mink (Mustela lutreola), Eurasian otter (Lutra lutra) and small–spotted genet (Genetta genetta), in northern Spain S. Palazón, J. Ruiz–Olmo & J. Gosálbez

Palazón, S., Ruiz–Olmo, J. & Gosálbez, J., 2008. Autumn–winter diet of three carnivores, European mink (Mustela lutreola), Eurasian otter (Lutra lutra) and small–spotted genet (Genetta genetta), in northern Spain. Animal Biodiversity and Conservation, 31.2: 37–43. Abstract Autumn–winter diet of three carnivores, European mink (Mustela lutreola), Eurasian otter (Lutra lutra) and small–spotted genet (Genetta genetta), in northern Spain.— This study describes the autumn–winter diet of three carnivores (Mustela lutreola, Lutra lutra and Genetta genetta) in northern Spain. Diet composition was analysed from 85 European mink, 156 otter and 564 spotted genet fecal samples The European mink diet was based on small mammals (relative frequency of occurrences 38.1%), fish (30.9%) and birds (16.7%). Spotted genet consumed mainly small mammals, birds and fruits, whilst otter predated practically only fish (95%). Using Levins’ index, trophic–niche widths in European mink, small–spotted genet and Eurasian otter were 3.76, 3.77 and 1.10, respectively. The trophic niche overlap by Pianka index for autumn–winter was 0.77 for European mink vs. small–spotted genet, and 0.60 for European mink vs. otter. The average size of brown trout taken by otter was larger than those consumed by European mink. Key words: European mink (Mustela lutreola), Eurasian otter (Lutra lutra), Small–spotted genet (Genetta genetta), Diet, Spain. Resumen Dieta otoño–invernal de tres carnívoros, visón europeo (Mustela lutreola), nutria euroasiática (Lutra lutra) y gineta común (Genetta genetta), en el norte de España.— Se describe la dieta otoño–invernal de tres carnívoros (Mustela lutreola, Lutra lutra y Genetta genetta) en el norte de España. La dieta fue analizada a partir de 85 muestras de visón europeo, 156 de nutria euroasiática y 564 de gineta común. El visón europeo basó su dieta en micromamíferos (38,1% de frecuencia relativa), peces (30,9%) y aves (16,7%). La gineta común consumió principalmente micromamíferos, aves y frutos, mientras la nutria predó casi exclusivamente peces (95%). Los índices de Levins de la anchura del nicho trófico del visón europeo, la gineta común y la nutria fueron 3,76, 3,77 y 1,10 respectivamente. Los solapamientos del nicho trófico durante otoño–invierno del visón europeo (índice de Pianka) respecto a la gineta común y la nutria euroasiática fueron 0,77 y 0,60, respectivamente. El tamaño medio de las truchas consumidas por las nutrias fue mayor que el de las consumidas por el visón europeo. Palabras clave: Visón europeo (Mustela lutreola), Nutria euroasiática (Lutra lutra), Gineta común (Genetta genetta), Dieta, España. (Received: 24 X 03; Conditional acceptance: 4 II 04; Final acceptance: 29 IV 08) Santiago Palazón & Jordi Ruiz–Olmo, Servei de Protecció de la Fauna, Flora i Animals de Companyia, Direcció General del Medi Natural, Dr. Roux 80, 08017 Barcelona, Espanya (Spain).– Joaquim Gosálbez, Dept. de Biologia Animal, Univ. de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Espanya (Spain).

ISSN: 1578–665X

Palazón et al.

Introduction Eurasian otter (Lutra lutra) and European mink (Mustela lutreola), both members of the family Mustelidae, are semi–aquatic mammals. The Eurasian otter is the most widely distributed otter species in the world, and it can be found in Europe, North Africa and Asia. European mink, however, is one of the most critically endangered mammals in the world (Schreiber et al., 1989). Furthermore, its distribution in Europe has declined dramatically since the 19th century (Youngman, 1982; Braun, 1990; Camby, 1990; Tumanov, 1999) and its range has been greatly fragmented. There remain only a few isolated populations in Eastern Europe and one population in south–west France / northern Spain, over 2,300 km away (Palazón & Ruiz–Olmo, 1997; Palazón, 1998; Palazón et al., 2003). The small–spotted genet (Genetta genetta), family Viverridae, is widely distributed in Africa and the Middle East, but it is also found in the Iberian peninsula and southern France. It generally inhabits forested areas, but in northern Spain it lives in riparian habitats, sharing habitat with Eurasian otter and European mink. In this range the small–spotted genet feeds not only on terrestrial prey but also on aquatic prey (Ruiz– Olmo & López–Martín, 1993), potentially competing with the native European mink, that consumes both terrestrial and aquatic prey, and the otter, that feeds mainly on aquatic prey (Ruiz–Olmo & Palazón, 1997; Clavero et al., 2003). The aim of this study was to show the diet of three species that share the same riparian habitat and whose ranges overlap. Understanding the factors that may affect European mink populations is specially important due to their endangered status. In this study, we investigated the diets of the American mink, the spotted genet, and the Eurasian otter in an area of northern Spain in order to determine their trophic niche breadth and overlap, and examine the potential for these species to compete. Material and methods The study area is located in Navarra and La Rioja in Northern Spain (latitude: 42o 10' N–43o 14' N; longitude: 1o 30' O–3o 03' O) (fig. 1), and the samples were collected from Mediterranean and Atlantic rivers. These Mediterranean rivers have a low flow during the summer. They are bordered by dense riparian cover, but surrounded by extensive dry and irrigated agricultural lands. In the Atlantic basin, the water flow is more constant year around. In both areas, the riparian vegetation is composed of black alders (Alnus glutinosa), white (Populus alba) and black poplars (P. nigra), white willows (Salix alba), ashes (Fraxinus angustifolia) and elms (Ulmus minor). The fish present in the study area are Cyprinidae, Cobitidae, Anguillidae and Salmonidae (Doadrio, 2002). Amphibians and reptiles are common (Pleguezuelos et al., 2002) and in the Mediterranean rivers, American crayfish (Procambarus clarckii) are found. The riparian vegetation in the study area is also the

habitat of several species of waterfowl, raptors, and small birds. Besides the three species of carnivores studied here, fox (Vulpes vulpes), weasel (Mustela nivalis), stoat (Mustela erminea), European polecat, stone marten (Martes foina) and badger (Meles meles) are also present (Palomo & Gisbert, 2002). Other mammals in the area are lagomorphs (the European rabbit Oryctolagus cuniculus and hares Lepus europaeus and L. granatensis), rodents (Arvicolids, Murids and Glirids) and insectivores (Palomo & Gisbert, 2002). To study the autumn–winter diet of the three study species we used 85 European mink and 564 spotted genet faecal samples collected between 1992 and 1996 in the Ega River (Navarra), and 156 otter scats collected in the Ebro, Najerilla and Iregua (La Rioja) Rivers between 1996 and 1997 (fig. 1). All the samples came from within the range of this isolated population of European mink. Samples were collected at different sites and times. Genet samples were gathered from latrines typically used for scent communication. Otter and European mink samples were easily differentiated by smell. Besides, most European mink samples were collected inside traps or from the dens of radio–tracked minks. Samples were cleaned, classified and identified to the level of major taxa, according to the authors’ own field collections and published keys: fish pharyngeal teeth, vertebrae and flakes (Conroy et al., 1993; Ruiz–Olmo, 1995), amphibian skeletons (Rage, 1974), mammalian hairs (Debrot et al., 1982) and mammalian teeth and bones (Gosálbez, 1987), assuming the errors associated to this analysis, especially for otters (Carss & Parkinson, 1996). To quantitatively describe the diet of three species we used the index: relative frequency of occurrence of each food item RFi =

Number of prey–items of prey taxa i Total prey–items

Fork length and weight of three consumed fish species (Barbus sp., Salmo trutta, and Chondrostoma miegii) were estimated using the functional relationship found by Ruiz–Olmo (1995). To compare the food–niche breadth of three mammals species, the B index was calculated for the nine established food categories, according to Levins (1968): B=1/

Spi2

ranging from 1 to 9 prey groups, where pi is the relative frequency of prey–category i in the diet, and n is the number of prey–categories. Trophic niche overlap between the three species (European mink, spotted genet and otter) was calculated by means of the Pianka (1976) index:

a = S (pi . qi ) x (S pi2 · S qi2 )–1/2 where pi is the proportion of prey–item i in the diet of the predator p, and qi is the proportion of prey item i

Animal Biodiversity and Conservation 31.2 (2008)

Cantabric Sea France

Basque Country Navarra

Burgos La Rioja

European mink range

Ebro River

European mink (Mustela lutreola) Eurasian otter (Lutra lutra) Small–spotted genet (Genetta genetta) Fig. 1. Map of study area where the samples of European mink (Mustela lutreola), Eurasian otter (Lutra lutra) and small–spotted genet (Genetta genetta) were collected. Fig. 1. Mapa del área de estudio donde se recolectaron las muestras de visón europeo (Mustela lutreola), nutria euroasiática (Lutra lutra) y gineta común (Genetta genetta).

in the diet of predator q. It ranges from 0 (exclusive niches) to 1 (complete overlap). Student t–test was used to compare the weight and length of different species of fish consumed by European mink and otter. Results Autumn–winter diet overlap between European mink and spotted genet was 0.77, between mink and otter 0.60, and between spotted genet and Eurasian otter 0.09. The autumn–winter food–niche breadth index (B) was 3.76 for European mink, 3.77 for spotted genet, and 1.10 for Eurasian otter (table 1). The three main prey categories in the European mink diet were small mammals (38%), fish (31%) and birds (17%) (table 1). All three together reached a relative frequency of 85.3%. Like European mink, small–spotted genet based their diet on three main items: small mammals

(39%), birds (18%) and fruits (26%) (table 1). In contrast, Eurasian otter almost exclusively consumed fish (95%), a prey–item category which only represented a third of the prey–items consumed by European mink. In the case of the otter, the remaining prey–items were of minor importance. Fish caught by Eurasian otter were longer than those consumed by European mink, but we only found differences in fork length and in weight of brown trout (table 2). The average size of trout consumed by mink and otter was 16.36 cm (range = 11.9–21.6) and 23.52 cm (range = 7.7–48.0), respectively (table 2, fig. 2). There was a large difference between average weight of trout consumed by mink (59.52 g, range = 18.71–124.5) and by otter (234.68 g, range = 3.3–1,578.0) (table 2, fig. 2). Most brown trout consumed by otter (60.6%) were longer than the longest trout consumed by European mink, while 56.5% of brown trout consumed by otter were heavier than the heaviest samples consumed by European mink.

Palazón et al.

Table 1. European mink (Mustela lutreola), small–spotted genet (Genetta genetta) and otter (Lutra lutra) autumn–winter diet (relative frequencies of occurrences, RF) and food–niche breadth (B index) (Levins, 1968) in northern Spain. Tabla 1. Dieta otoño–invernal (frecuencia relativa de aparición, RF) de visón europeo (Mustela lutreola), gineta común (Genetta genetta) y nutria euroasiática (Lutra lutra) y anchura del nicho trófico (índice B) (Levins, 1968) en el norte de España.

M. lutreola

G. genetta

(n = 85) Prey

L. lutra

(n = 564)

(n = 156)

Small mammals

38.1

589

39.4

0.2

Birds

16.7

267

17.8

1.1

Fish

30.9

4.1

430

95.3

Reptiles

0.8

1.8

2.0

Amphibians

3.2

0.1

1.1

Crayfish

0.0

1.0

0.0

Insects

2.4

147

9.8

0.2

Fruits

4.0

386

25.8

0.0

Garbage

4.0

0.1

0.01

Total

124

1,496

451

B index

3.76

3.77

1.10

Table 2. Comparison of fork length (FL) and weight of barbels (Barbus sp.), brown trout (Salmo trutta) and nase (Chondrostoma miegii) consumed by European mink (Mustela lutreola) and otter (Lutra lutra) in northern Spain: N. Number of samples; X. Mean; SD. Standard deviation; * Significant differences. Tabla 2. Comparación de la longitud forcal (FL) y del peso de barbo (Barbus sp.), trucha común (Salmo trutta) y madrilla (Chondrostoma miegii) consumidas por el visón europeo (Mustela lutreola) y la nutria euroasiática (Lutra lutra) en el norte de España: N. Número de muestras; X. Media; SD. Desviación estándar; * Diferencias significativas.

Mustela lutreola

Student t–test

Lutra lutra

Barbus sp. FL

12.52

4.24

13.78

6.80

1.660

0.201

Weight

24.34

21.88

46.24

76.81

3.487

0.065

193

23.52

8.11

3.724

0.055

193 234.68 251.18

3.938*

0.049

Salmo trutta FL

16.36

3.79

Weight

59.52

43.53

11.83

3.86

10.82

3.19

0.230

0.634

Weight

10.58

3.98

9.69

3.15

0.418

0.521

Chondrostoma miegii

Animal Biodiversity and Conservation 31.2 (2008)

A Lutra lutra

Mustela lutreola

Percentage

35 30 25 20 15 10 5 0

<10

10–15

15–20 20–25 Fork length (cm)

25–30

>30

B Lutra lutra

Percentage

Mustela lutreola

40 30 20 10

<10

10–20

20–50 50–100 Weight (g)

100–200 200–500

>500

Fig. 2. Comparison of fork length (A) and weight (B) of brown trout (Salmo trutta) consumed by European mink (Mustela lutreola) and otter (Lutra lutra) in northern Spain. Fig. 2. Comparación de la longitud forcal (A) y del peso (B) de trucha común (Salmo trutta) consumidas por el visón europeo (Mustela lutreola) y la nutria euroasiática (Lutra lutra) en el norte de España.

Discussion Our results have shown that the American mink and the small–spotted genet tend to have a similar diet, partitioned between aquatic and terrestrial prey, while the otter fed almost exclusively on aquatic prey. These findings are similar to those in Belarus, where the food–niche breadth was higher for the European mink

than for the otter (Sidorovich, 2000). In Spain the diet overlap between Eurasian otter and European mink was similar (Sidorovich, 2000), with otter consuming more than 50% fish, and European mink consuming more than 50% frogs. The diet overlap between European mink and spotted genet was slightly higher. The study of diet overlap should not be confused with competition in the diet.

Otters have a higher rate of fish capture than mink. This is likely because they are better adapted to an aquatic life–style due to their larger surface of interdigital membranes, greater diving capacity, better under–water vision, higher percentage of milk fat, and the vibrissae on muzzle and elbows that help them detect fish in murky waters. (Dunstone, 1993; Conroy & Jenkins, 1986; Estes, 1989; Kemenes & Nechay, 1990; Brzezinski et al., 1993). There are no studies on the swimming behaviour of European mink, although it is likely similar to American mink (Dunstone, 1993). Due to their larger size, and their adaptations to aquatic life, otter can prey on fish of different species and sizes. European mink, however, have a limited capacity for swimming and can only prey on small fish. Otter and European mink share some fish. When they concur on the same river, could there be a competitive relationship between the two species? Could otter attack or predate on European mink? Since the 1990s Spanish otter populations are increasing and spreading (Ruiz–Olmo & Delibes, 1998). Could this lead to a decrease in European mink populations in a similar way to the American mink in England (Strachan & Jefferies, 1996; Crawford, 2003)? We consider it would be interesting to study the ecological relations between European mink, otter and small–spotted genet in the Mediterranean areas of sympatry in depth. Such studies should also be extended to the European polecat and American mink in Spain as in the near future, this invasive species could become a major competitor of European mink not only in Spain but also in other European countries (Maran et al., 1998; Sidorovich et al., 1998, 2000, 2001). Acknowledgements We would like to thank Dr. Enrique Castién, Javier Ochoa, Dr. José María López–Martín, Asun Gómez– Gayubo, Dr. Oscar Arribas and Jordi Palazón for their help in the study. We are grateful to Carolyne Newey for the English revision. The research was financed by the autonomous governments of Navarra, Catalonia and La Rioja, and the Spanish Environment Ministry. References Braun, A. J., 1990. The European mink in France: past and present. Mustelid & Viverrid Conservation, 3: 5–8. Brzezinski, M., Jedrzejewski, W. & Jedrzejewska, B., 1993. Diet of otters (Lutra lutra) inhabiting small rivers in the Bialowiza National Park, eastern Poland. J. Zool. Lond., 230: 495–501. Camby, A., 1990. Le Vison d’Europe (Mustela lutreola Linnaeus, 1761). In: Encyclopédie des Carnivores de France, vol 13: 1–18. Societé Francaise pour l'´Étude et le Protection des Mamifères (SFEPM), París. Carss, D. N. & Parkinson, S. G., 1996. Errors associated with otter Lutra lutra faecal analysis: I.

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Assessing general diet from spraints. Journal of Zoology (London), 238: 301–317. Clavero, M., Prenda, J. & Delibes, M., 2003. Trophic diversity of the otter (Lutra lutra) in temperate and Mediterranean fresh habitat. J. Biogeog., 30: 761–769. Conroy, J. W. H. & Jenkins, D., 1986. Ecology of otters in northern Scotland. VI. Diving times and hunting sucess of otter (Lutra lutra) at Dinnet lochs, Aberdeen and in Yell Sound, Shetland. J. Zool. Lond., 209: 341–346. Conroy, J. W. H., Watt, J., Webb, J. B. & Jones, A. P., 1993. A guide to the identification of prey remains in otter spraint. An Occasional Publication of the Mammal Society, 16: 1–52. Crawford, A., 2003. Fourth Otter Survey of England 2000–2002. Environment Agency, Bristol. Debrot, S., Fivaz, G., Mermod, C. & Weber, J. M., 1982. Atlas des Poils de Mammifères d'Europe. Institut de Zoologie de l”Université de Neuchatel, Neuchatel. Doadrio, I., 2002. Atlas de los Peces Continentales de España. DGCNA–SECEM–SECEMU, Madrid. Dunstone, N., 1993. The mink. T. & A. D. Poyser, London. Estes, J. A., 1989. Adaptations for Aquatic Living by Carnivores. In: Carnivores, Behavior, Ecology and Evolution: 242–282 (J. L. Gittleman, Ed.). Cornell University Press, Cornell. Gosàlbez, J., 1987. Insectívors i Rossegadors de Catalunya. Metodologia d”estudi i Catàleg faunístic. Ketres, Barcelona. Kemenes, I. & Nechay, G., 1990. The food of otters Lutra lutra in different habitats in Hungary. Acta Theriologica, 35: 17–24. Levins, R., 1968. Evolution in changing environments. Princeton University Press, Princeton. Maran, T., Kruuk, H., MacDonald, D. W. & Polma, M., 1998. Diet of two species of mink in Estonia: displacement of Mustela lutreola by M. vison. J. Zool. Lond., 245: 218–222. Palazón, S., 1998. Distribución, morfología y ecología del visón europeo (Mustela lutreola L. 1761) en la Península Ibérica. Ph. D. Thesis, Universitat de Barcelona. Palazón, S. & Ruiz–Olmo, J., 1997. El visón europeo (Mustela lutreola) y el visón americano (Mustela vison) en España. Ministerio de Medio Ambiente, Madrid. Palazón, S., Ruiz–Olmo, J., Gosálbez, J, Gómez– Gayubo, A., Ceña, J. C. & Ceña, A., 2003. Trends in distribution of the European mink (Mustela lutreola L., 1761) in Spain: 1950–1999. Mammalia, 67(4): 473–484. Palomo, J. & Gisbert, J., 2002. Atlas de los Mamíferos Terrestre de España. DGCNA–SECEM–SECEMU, Madrid. Pianka, E. R., 1976. Competition and niche theory. In: Theoretical ecology, Principles and aplications: 114–141 (R. M. May, Eds.) Oxford Blackwell Scientific Publications, Oxford. Pleguezuelos, J. M., Márques, R. & Lizana, M., 2002. Atlas y Libro Rojo de los Anfibios y Reptiles de

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España. DGCNA–SECEM–SECEMU, Madrid. Rage, J. C., 1974. Batraciens fossiles du quaternaire. Bull. Soc. Linn. Lyon, 43: 276–289. Ruiz–Olmo, J., 1995. Estudio bionómico de la nutria (Lutra lutra L., 1758) en el nordeste de la Península Ibérica. Ph. D. Thesis, Universidad de Barcelona. Ruiz–Olmo, J. & Delibes, M., 1998. La nutria en España. SECEM, Barcelona–Sevilla–Málaga. Ruiz–Olmo, J. & López–Martín, J. M., 1993. Note on the diet of the Common Genet (Genetta genetta L.) in mediterranean riparian habitats of N.E. Spain. Mammalia, 57(4): 607–610. Ruiz–Olmo, J. & Palazón, S., 1998. The diet of the European otter (Lutra lutra L., 1758) in Mediterranean freswater habitats. Journal of Wildlife Research, 2(2): 171–181. Ruiz–Olmo, J., Palazón, S., Bueno, F., Bravo, C., Munilla, I. & Romero, R., 1998. Distribution, status and colonization of the American mink Mustela vison in Spain. Journal of Wildlife Research, 2(1): 30–36. Saint–Girons, M. C., 1991. Le vison sauvage (Mustela lutreola) en Europe. In: Collection Sauvegarde de la nature. Consejo de Europa, Strasburgo, 54: 1–41. Conseil d'Europe, Strasburg. Schreiber, A., Wirth, R., Riffel, M. & Van Rompaey, H., 1989. Weasels, Civets, Mongooses and Their relatives: An Action Plan for the Conservation of Mustelids and Viverrids. UICN, Gland.

Sidorovich, V. E., 2000. Seasonal variation in the feeding habits of riparian mustelids in river valleys of NE Belarus. Acta Theriologica, 45(2): 233–242. Sidorovich, V. E., Kruuk, H., MacDonald, D. W. & Maran, T., 1998. Diets of semi–aquatic carnivores in northern Belarus, with implications for populations changes. In: Behaviour and ecology of riparian mammals: 177–189 (N. Dunstone & M. L. Gorman, Eds.). Symposia of the Zoological Society of London 71, London. Sidorovich, V. E., MacDonald, D. W., Kruuk, H. & Krasko, A., 2000. Behavioural interactions between the naturalized American mink Mustela vison and the native riparian mustelids, NE Belarus, with implications for population changes. Small Carnivore Conservation, 22: 1–5. Sidorovich, V. E., MacDonald, D. W., Pikulik, M. M. & Kruuk, H., 2001. Individual feedings specializations in the European mink, Mustela lutreola and the American mink Mustela vison in north–eastern Belarus. Folia Zool., 50(1): 27–42. Strachan, R. & Jefferies, D. J., 1997. Otter survey of England 1991–1994. The Vincent Wildlife Trust, London. Tumanov, I. L., 1999. The modern state of European mink (Mustela lutreola L.) populations. Small Carnivore Conservation, 21: 9–11. Youngman, P. M., 1982. Distribution and systematics of the Europen Mink, Mustela lutreola Linnaeus, 1761. Acta Zool. Fenn., 166: 1–48.

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 31.2 (2008)

Bias in density estimations using strip transects in dry open–country environments in the Canary Islands L. M. Carrascal, J. Seoane & D. Palomino

Carrascal, L. M., Seoane, J. & Palomino, D., 2008. Bias in density estimations using strip transects in dry open–country environments in the Canary Islands. Animal Biodiversity and Conservation, 31.2: 45–50. Abstract Bias in density estimations using strip transects in dry open–country environments in the Canary Islands.— We studied bias in density estimations derived from strip transects in dry open–country in the Canary Islands. We also present some critical remarks on García–del–Rey’s (2005) paper regarding strip transects and the validity of comparisons based on population densities of birds in scrublands on Tenerife island using two different methods: territory mapping and strip transect sampling. Although strip transects with census belts of 25 m do not account for detectability, this method only slightly undervalues true density estimates, and allowed to detect more than 85% of birds present in poorly vegetated environments in the Canary Islands. Previously published works on distribution and abundance of terrestrial birds in the Canary Islands using the strip transect sampling with belts of 25 m on both sides of the observer, thus provide reliable information that only slightly underestimates true densities. Key words: Birds, Canary Islands, Census methods, Strip transects, Open–country environments, Population density, Territory mapping. Resumen Sesgos en la obtención de estimas de densidad obtenidas por medio de transectos lineales en ambientes estepáricos de las Islas Canarias.— Se estudian los sesgos derivados del empleo del método del taxiado (transectos lineales con bandas de 25 m a cada lado del observador) para obtener densidades en ambientes estepáricos de las Islas Canarias. También se presentan algunos comentarios críticos al trabajo de García– del–Rey (2005) que compara estimas de densidad obtenidas en Tenerife utilizando dos métodos diferentes: mapeo de territorios y transecto lineal. Aunque el método del taxiado estima densidades relativas no corregidas por la detectabilidad de las especies, este método proporciona valores de densidad muy parecidos a los reales, ya que permite detectar en ambientes con poca cobertura vegetal a más del 85% de los individuos dentro de bandas de 25 m a cada lado del observador. Por tanto, los trabajos previamente publicados sobre densidades de aves en Canarias proporcionan estimas fiables sólo ligeramente infravaloradas. Palabras clave: Aves, Islas Canarias, Métodos de censo, Transecto lineal, Ambientes estepáricos, Densidad de población, Mapeo de territorios. (Received: 31 III 08; Conditional acceptance: 9 V 08; Final acceptance: 4 VII 08) Luis M. Carrascal, Dept. Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales–CSIC, c/ José Gutiérrez Abascal 2, 28006 Madrid, Spain.– Javier Seoane, Dept. Interuniversitario de Ecología, Fac. de Ciencias, Univ. Autónoma de Madrid, 28049 Madrid, Spain.– David Palomino, Área de Estudio y Seguimiento de Aves, SEO/BirdLife, c/ Melquiades Biencinto 34, 28053 Madrid, Spain.

ISSN: 1578–665X

Carrascal et al.

Introduction Macroecology and ecological biogeography require reliable information concerning the distribution and abundance of organisms. Much of the presently available information was obtained decades ago when sampling methods were not well established or calibrated, or it was gathered following pragmatic sampling protocols over large areas. As a result, abundance measurements may be biased and lack precision and exactitude. One of the most commonly used methods to estimate bird abundance for large–scale monitoring programmes is the strip transect method (also named fixed-width method; i.e., counting all objects within a predeterminated distance of the line travelled, Thomas et al., 2002). This approach provides relative densities that are perfectly comparable within–species across different environments, but biased in interspecific comparisons (Franzeb, 1981; Tellería, 1986; Bibby et al., 2000). The lack of exactitude is mainly due to the fact that this method does not account for detectability, and although it produces abundance estimates that are highly correlated with "true" densities, these are lower than those obtained by variable–width estimates (e.g., Shankar, 2003), and the magnitude of the difference is species–specific. Carrascal & Palomino (2005) studied the species–specific habitat preferences, density and species richness of bird communities in Tenerife (Canary Islands). They used strip transects with census belts of 25 m on each side of the observer to obtain population densities in 26 different habitats. García–del–Rey (2005) estimated the population density of passerine bird species in coastal scrublands of Tenerife island using two different methods: territory mapping and the strip transect method (which he labelled the line transect method). Comparing previously published bird abundance estimates in Tenerife (Carrascal & Palomino, 2005) with his own work, he concluded that strip transects using census belts of 25 m on both sides of the observer gave skewed density estimates and questioned the validity of previous published works. The author recommended a more reliable approach should be used in future studies to estimate abundance and advocated the use of distance sampling (Buckland et al., 2001). In this short paper we provide new insights on density bias estimates when working with strip transects, and analyse the detectability patterns of the three most common bird species in the dry open–country environments of Tenerife: Anthus berthelotii, Sylvia conspicillata and Lanius meridionalis. These three passerines have very different foraging strategies (cursorial on the ground, sit–and–wait on perches of good visibility, or gleaners ambushed within bushes) in dry and poorly vegetated areas in the Canary Islands. Our main goal was to determine the degree to which density estimates made with strip transects using belts of 25 m on each side of an observer differ from "good" densities obtained

by more precise methods. The paper also includes critical comment on García–del–Rey’s (2005) paper regarding the experimental design he used and the validity of comparisons made therein. Material and methods We used the data obtained in an extensive survey program in Lanzarote and Fuerteventura in 2005 and 2006 (1,071 km of line transects; see Carrascal et al., 2006, 2007; Palomino et al., 2008). Line transect sampling was used; this technique is frequently applied in extensive assessments of abundance, distribution patterns and habitat preferences of birds (Bibby et al., 2000). The transects were carried out on windless, rainless days, walking cross country or following little–used dirt tracks at a low speed (1–3 km/h approximately), in the 4 hours after dawn and the 2.5 hours before dusk. For each detected bird, the distance perpendicular to the observer’s trajectory was estimated. Training with a laser range–finder (Leica Rangemaster LRF 900) helped to improve distance estimates and to reduce inter–observer variability. Detectability was estimated with the sampled distances (Thomas et al., 2002). To model detectability, we fitted three canonical models (half–normal, negative exponential and hazard–rate, trying to include a suitable series expansion in each one) that are commonly used to explain the loss of detectability as a function of the distance from the transect line (the further the distance the lower the probability of detecting an individual). We also built more elaborate models to take possible observer effects into account (adding a factor with five levels corresponding to five observers) and vegetation structure (adding a continuous covariate calculated as mean shrub cover multiplied by mean shrub height). These models were used to estimate the probability of detection and the effective census strip width. Models were evaluated according to AICc. AICc is a second order correction of AIC for small sample sizes. Since AICc converges to AIC as n increases, AICc should be employed regardless of sample size. We calculated a weighted average of the detection probabilities derived from the models according to weights (W) obtained from AICc values, where Wi = exp [–0.5 · DAICci] / S exp [–0.5 · DAICci] Burnham & Anderson, 2002). Detectability models were built with Distance 5.0 software (Thomas et al., 2004). Using this approach, it was also possible to calculate the probability of detection within 25 m–wide belts on both sides of the observer. Results Figure 1 shows the variation of birds detected with the perpendicular distance to the observer. We

Animal Biodiversity and Conservation 31.2 (2008)

450

Anthus berthelotii

400

# of contacts

350 300 250 200 150 100 50 0

120

20 35 50 65 80

95 110 125 140 155

Sylvia conspicilata

# of contacts

100 80 60 40 20 0

35 50 65 80 95 110 125 140 155 Distance to observer (m)

60 Lanius meridionalis

# of contacts

50 40 30 20 10

45 65 85 105 125 145 165 185 205 225 245 265 # of contacts

Fig. 1. Number of birds at a different distance to the observer in 1,071 km of transects in dry open–country areas of Fuerteventura and Lanzarote. We obtained 3,217 records for Anthus berthelotii, 961 for Sylvia conspicillata and 541 for Lanius meridionalis. The curves represent the models fitted to the truncated data (see truncated distances in table 1). Fig. 1. Variación del número de aves detectadas a diferentes distancias del observador en 1.071 km de transectos en ambientes estepáricos de Fuerteventura y Lanzarote. Se obtuvieron 3.217 contactos para Anthus berthelotii, 961 para Sylvia conspicillata y 541 para Lanius meridionalis. Las curvas sobre los histogramas representan los modelos ajustados a los datos truncados (véase la tabla 1).

Carrascal et al.

Table 1. Models fitted to the detection distances of Anthus berthelotii, Sylvia conspicillata and Lanius meridionalis, following the order of their AICc values (i.e., from greater to less reliability). More elaborate models were also built to take the possible effects of observer (o) and/or vegetation structure (v) into account. W is the weight given to each model according to the formula Wi = exp [–0.5 · DAICci] / S exp [–0.5 · DAICci] (Burnhman & Anderson, 2002): TD. Detection distances were right–truncated excluding outliers as recommended by Buckland et al. (2001), i.e., disregarding the 5% of the longest perpendicular distances from the transect line; P. Detection probability and its 95% confidence interval within the truncated distances of observation (2,866 contacts for Anthus berthelotii excluding those farther than 73 m; 950 for Sylvia conspicillata, truncated at 95 m; and 526 for Lanius meridionalis, truncated at 145 m). Tabla 1. Modelos ajustados a las distancias de detección de Anthus berthelotii, Sylvia conspicillata y Lanius meridionalis, ordenados de acuerdo a los valores de AICc. También se han construido otros modelos más elaborados que incluyeron los posibles efectos del observador (o) y/o la estructura de la vegetación (v). W es el peso dado a cada modelo de acuerdo con la fórmula Wi = exp [–0.5 · DAICci] / S exp [–0.5 · DAICci]; (Burnhman & Anderson, 2002): TD. Distancias de detección truncadas que excluyen observaciones muy lejanas, según recomendaciones de Buckland et al. (2001); P. Probabilidad de detección y su intervalo al 95% dentro de las bandas definidas por las distancias de observación truncadas (2.866 contactos para Anthus berthelotii excluyendo aquellos más distantes de 73 m; 950 para Sylvia conspicillata, truncados a 95 m; y 526 para Lanius meridionalis, truncados a 145 m).

DAICc

P (95% CI)

0.00

1.00

0.660 (0.646–0.675)

Half–normal (cosine adjustments)–ov

0.00

0.72

0.563 (0.538 –0.588)

Hazard–rate (cosine adjustments)–ov

1.91

0.28

0.558 (0.534–0.583)

Anthus berthelotii Hazard–rate (cosine adjustments)–ov Sylvia conspicillata

Weighted average

0.561 (0.537–0.587)

Lanius meridionalis Hazard–rate (polynomial adjustments)–o

145

0.00

0.25

0.420 (0.390–0.453)

Half–normal (cosine adjustments)–ov

145

0.48

0.20

0.443 (0.415–0.474)

Half–normal (cosine adjustments)–o

145

0.98

0.15

0.443 (0.415–0.474)

Hazard–rate (polynomial adjustments)–ov

145

1.08

0.15

0.421 (0.391–0.454)

Half–normal (polynomial adjustments)–ov

145

1.11

0.14

0.459 (0.415–0.508)

Hazard–rate (cosine adjustments)–o

145

1.54

0.12

0.440 (0.408–0.475)

Weighted average

obtained 3,217 contacts for Anthus berthelotii, 961 for Sylvia conspicillata and 541 for Lanius meridionalis. Table 1 shows the best models fitted to the detection distances for the three species (considering only those with DAICc lower than 2). According to these models, the probabilities of detection within census belts of 25 m on each both sides of the observer were 0.86 for Anthus berthelotii, 0.96 for Sylvia conspicillata and 0.90 for Lanius meridionalis. All these values were higher than 0.85 and demonstrate that strip transects with census belts of 25 m on each side of the observer are very efficient censusing birds in poorly vegetated dry areas of the Canary Islands.

0.436 (0.404–0.471)

Discussion Although line transects with fixed census belts –strip transects– do not account for detectability, this method only slightly undervalued true density estimations. It allowed detection of more than 85% of birds present while sampling densities in poorly vegetated environments in the Canary Islands. Similar results have been found for larger species in semi–desert environments of the Canary Islands, such as Cursorius cursor (0.94 for detection probability within census belts of 25 m; a figure obtained from fitted detection models in Carrascal et al., 2007) and Chlamydotis undulata (0.98; Carrascal et al., 2006). Therefore, previously

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published works on distribution and abundance of terrestrial birds in the Canary Islands, using the strip transect method with belts of 25 m on each side of the observer, provide reliable information that only slightly underestimates true densities. The comparison between census methods in a paper by García–del–Rey (2005) is questionable as the experimental design does not adequately take important sources of variation into account. Spatial variability, for example, was not considered because García–del–Rey compared strip transects in four localities with territory mapping in just one (the study plot for territory mapping is in site 4, far from the rest of the sites, according to figure 1 in García–del–Rey [2005]). Besides, when the author used data from the same site, it was not stated whether the survey line transects and territory mapping were made over exactly the same area. Furthermore, the size of the area surveyed differed between the two methods because the 5.2 km of transects using belts of 25 m in site 4 covered a surface of 26 ha (5.2 km x 50 m = 26 ha), while with territory mapping the author covered 68 ha. More problematic is the fact that García–del–Rey made the strip transect in site 4 only on one date (5 March), and this did not overlap with the timing of territory mapping at the same site (3, 11, 18, 25 January, 1, 8, 15, 22 February). It is also surprising that García–del–Rey’s (2005) density estimations derived from the territory mapping method were nearly 100% lower than those obtained by means of strip transects in the two species that were most abundant and had most data (Anthus berthelotii and Sylvia conspicillata). This finding contradicts that found in previous works comparing the two methods (Emlen, 1977; Järvinen, 1978; Tellería, 1986; Shankar, 2003). It is not unusual to find spatial variation in density when counting birds due to changes in habitat structure (see Illera, 2001, Carrascal et al., 2006, Illera et al., 2006, and Palomino et al., 2008 for some examples with open–country canary birds). In view of the lack of information on habitat structure in García–del–Rey’s (2005) study no conclusion can be reached regarding the validity of any one method or survey program when comparing density estimations obtained in different studies (Carrascal & Palomino [2005] provide detailed information on habitat structure of the environments censused). We therefore consider that García–del–Rey's criticisms (2005) on the line transect method with belts of 25 m are flawed by the experimental design to compare two methods. The differences they found in density estimations may be due to phenological shifts in detectability, seasonal or spatial changes in densities, or differences in habitat structure. Based on our findings indicate that strip transect sampling with narrow census belts is a good survey method to estimate bird abundance for large–scale monitoring programmes as it only slightly undervalues true density estimations.

References Bibby, C. J., Burgess, N. D. & Hill, D. A., 2000. Bird Census Techniques (2nd edition). Academic Press, London. Buckland, S. T., Anderson, D. R., Burham, K. P., Laake, J. L., Borchers, D. L. & Thomas, L., 2001. Introduction to Distance Sampling. Oxford University Press, New York. Burnham, K. P. & Anderson, D. R., 2002. Model selection and multimodel inference. A practical information–theoric approach. Springer–Verlag, New York. Carrascal, L. M. & Palomino, D., 2005. Preferencias de hábitat, densidad y diversidad de las comunidades de aves en Tenerife (islas Canarias). Animal Biodiversity and Conservation, 28: 101–119. Carrascal, L. M., Seoane, J., Palomino, D. & Alonso, C. L., 2006. Preferencias de hábitat, estima y tendencias poblacionales de la Avutarda Hubara (Chlamydotis undulata) en Lanzarote y La Graciosa (Islas Canarias). Ardeola, 53: 251–269. – 2007. El corredor sahariano en España. I Censo Nacional (2005–2006). Monografía nº 14. SEO/ BirdLife, Madrid. Emlen, J. T., 1977. Estimating breeding season bird densities from transect counts. Auk, 94: 455–468. Franzeb, K.E. 1981. The determination of avian densities using the variable–strip and fixed–width transect surveying methods. Stud. Avian Biol., 6: 139–145. García–del–Rey, E., 2005. Density estimates of passerine bird species in Tenerifean coastal scrub using two different methods (Canary Islands). Vieraea, 33: 193–199. Illera, J. C., 2001. Habitat selection by the Canary Islands stonechat (Saxicola dacotiae) (Meade– Waldo, 1889) in Fuerteventura Island: a two–tier habitat approach with implications for its conservation. Biological Conservation, 97: 339–345. Illera, J. C., Diaz, M. & Nogales, M., 2006. Ecological traits influence the current distribution and range of an island endemic bird. Journal of Biogeography, 33: 1192–1201. Järvinen, O., 1978. Species–specific census efficiency in line transects. Ornis Scandinavica, 9: 164–167. Palomino, D., Seoane, J., Carrascal, L. M. & Alonso, C. L., 2008. Competing effects of topographic, lithological, vegetation structure and human impact in the habitat preferences of the Cream– coloured Courser. Journal of Arid Environments, 72: 401–410. Shankar, T. R., 2003. Assessment of census techniques for interspecific comparisons of tropical rainforest bird densities: a field evaluation in the Western Ghats, India. Ibis, 145: 9–21. Tellería, J. L., 1986. Manual para el censo de los vertebrados terrestres. Raíces, Madrid. Thomas, L., Buckland, S. T., Burnham, K. P., Anderson, D. R., Laake, J. L., Borchers, D. L. & Strind-

berg, S., 2002. Distance sampling. In: Encyclopedia of Environmetrics: 544â&#x20AC;&#x201C;552 (A. H. Elâ&#x20AC;&#x201C;Shaarawi & W. W. Piegorsch, Eds.). John Wiley & Sons, Chichester. Thomas, L., Laake, J. L., Strindberg, S., Marques, F.

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F. C., Buckland, S., Borchers, D. L., Anderson, D. R., Burnham, K. P., Hedley, S. L., Pollard, J. H. & Bishop, J. R. B., 2004. Distance 5.0, Release Beta 2. Research Unit for Wildlife Population Assessment, St. Andrews.

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Microhabitat occupation and functional morphology of four species of sympatric agamid lizards in the Kyzylkum Desert, central Uzbekistan N. Clemann, J. Melville, N. B. Ananjeva, M. P. Scroggie, K. Milto & E. Kreuzberg

Clemann, N., Melville, J., Ananjeva, N. B., Scroggie, M. P., Milto, K. & Kreuzberg, E., 2008. Microhabitat occupation and functional morphology of four species of sympatric agamid lizards in the Kyzylkum Desert, central Uzbekistan. Animal Biodiversity and Conservation, 31.2: 51–62. Abstract Microhabitat occupation and functional morphology of four species of sympatric agamid lizards in the Kyzylkum Desert, central Uzbekistan.— We examined microhabitat occupation and functional morphology of four sympatric agamid lizards (Phrynocephalus helioscopus helioscopus, P. interscapularis, P. mystaceus galli and Trapelus sanguinolentus) at three sites in the arid zone of central Uzbekistan. At two sites located in sand dunes, substrate attributes played a key role in habitat selection by three syntopic species. At a third flat, stony site, P. helioscopus selected habitat non–randomly, tending to occur close to sparse, low vegetation. Syntopic taxa were separated in morphospace, and there was a trend for taxa with proportionally longer limbs to have faster field escape speeds. Field escape distances and predator avoidance tactics differed between species, with two main escape strategies (crypsis or sand–diving following an escape sprint). We caution that broad–scale threatening processes such as over–grazing and salinity may be having a detrimental effect on microhabitat features important to terrestrial reptiles in Uzbekistan. Key words: Agamidae, Central Asia, Microhabitat occupation, Functional morphology. Resumen Ocupación del microhábitat y morfología funcional de cuatro especies de lagartos agámidos simpátridas del desierto de Kyzylkum, en Uzbekistán central.— Examinamos la ocupación del microhábitat y la morfología funcional de cuatro lagartos agámidos simpátridas (Phrynocephalus helioscopus helioscopus, P. interscapularis, P. mystaceus galli y Trapelus sanguinolentus) en tres localizaciones de la zona árida del Uzbekistán central. En dos localizaciones, situadas en una zona de dunas de arena, las características del sustrato tuvieron un papel clave en la selección del hábitat por parte de tres especies sintópicas. En una tercera zona, una llanura pedregosa, P. helioscopus no seleccionaba su hábitat al azar, con una clara tendencia a situarse cerca de vegetación baja y dispersa. Los taxa sintópicos estaban separados en el morfoespacio, y existía la tendencia entre los taxa con las extremidades proporcionalmente más largas a tener una mayor velocidad de huida. Las distancias de huida de campo y las tácticas de evitación de los depredadores diferían según las especies, con dos estrategias de huida principales (cripsis o enterramiento en la arena, seguidos de una carrera de escape). Hemos de advertir que los procesos amenazadores a gran escala, tales como el sobrepastoreo y la salinización pueden tener un efecto perjudicial sobre las características del microhábitat que son importantes para los reptiles terrestres de Uzbekistán. Palabras clave: Agamidae, Asia central, Ocupación del microhábitat, Morfología funcional. (Received: 30 VI 08; Conditional acceptance: 4 IX 08; Final acceptance: 6 X 08) Nick Clemann & Michael P. Scroggie, Arthur Rylah Inst. for Environmental Research, Dept. of Sustainability and Environment, P. O. Box 137, Heidelberg, Victoria 3084, Australia.– Jane Melville, Museum Victoria, G. P. O. Box 666, Melbourne, Victoria 3001, Australia.– Natalia B. Ananjeva & Konstantin Milto, Zoological Inst., Russian Academy of Sciences, St. Petersburg 199034, Universitetskaya nab. 1, St. Petersburg, Russia.– Elena Kreuzberg, 212–2100 Scott Str., Ottawa, Ontario K1Z 1A3, Canada. Corresponding author: Jane Melville. E–mail: jmelv@museum.vic.gov.au ISSN: 1578–665X

Clemann et al.

Introduction Central Asia, which encompasses the desert regions of Kazakhstan, Kyrgyzstan, Uzbekistan, Turkmenistan, has pronounced landscape heterogeneity, from high mountain ranges, to pebble, sand and steppe deserts. The deserts of Central Asia have some of the highest levels of biological richness of all the Eurasian deserts (Szczerbak, 2003). Despite this high biodiversity we still have limited understanding of the biogeography and ecology of the constituent reptile species, which show high levels of regional endemism. Qualitative descriptions of the general habitats of most of these taxa have been synthesised in field guides (Szczerbak, 2003; Ananjeva et al., 1998, 2006). However, very limited quantitative data exist on their microhabitat use (Bogdanov, 1960; Ananjeva & Tuniyev, 1992; Brushko, 1995), and few studies have investigated the functional link between morphology and microhabitat for lizards in this region (Sukhanov, 1974; Ananjeva, 2003). Of the Central Asian countries, the Republic of Uzbekistan has a particularly diverse vertebrate fauna that includes approximately 60 reptile species. Uzbekistan is facing considerable natural resource management challenges. Extensive agricultural development and natural resource demands around highly populated areas have led to large–scale environmental problems such as desertification, water and soil pollution, and increased soil salinity (UNEP, 1999; UNDP, 2001). These processes have undoubtedly affected vital habitat attributes for numerous wildlife taxa. Detailed knowledge of the conservation status of wildlife in Central Asia is limited, and concern for the future of some reptiles in Uzbekistan is mounting (NBSAP, 1998). Sixteen reptile taxa have been listed by the International Union for Conservation of Nature and Natural Resources as threatened in The Red Data Book of Uzbekistan (2003; see also Ananjeva et al., 2006). Many lizard species in Central Asia occur in geographically restricted habitats such as desert dunes, and are considered habitat specialists (Szczerbak, 2003; Ananjeva et al., 2006). Quantification of microhabitat utilisation and functional morphology can provide important information for conservation strategies and management actions, by affording a greater understanding of an animal’s ecological niche and resource requirements. We present the first study to investigate microhabitat utilisation and functional morphology of Central Asian agamid lizards. To do this we quantify microhabitat use, escape speed and morphology, and discuss the functional link between escape behaviour and habitat, as has been undertaken for other reptile species (e.g., Irschick & Losos, 1999; Melville & Swain, 2000; Irschick & Garland, 2001). We studied four species that inhabit the Kyzylkum Desert in central Uzbekistan. These species included two sand substrate specialists (Phrynocephalus interscapularis and P. mystaceus) and two species that are not known to have specialised substrate preferences (P. helioscopus and T. sanguinolentus).

Numbers of P. mystaceus are in sharp decline, and there is serious concern regarding the conservation status of some populations of P. helioscopus (The Red Data Book of Uzbekistan, 2003). This study provides a greater understanding of habitat use by agamid lizards in this little–studied region, and provides a basis for future ecological, conservation and evolutionary studies. Materials and methods Site location and description Sampling was conducted at three sites in the Kyzylkum Desert in central Uzbekistan. The first (41° 45' N, 64° 02' E) and second sites (41° 48' N, 64° 38' E, near the village of Tamdi) consisted of undulating sand dunes, whilst the third site (41° 43' N, 64° 28' E, also near Tamdi) consisted of flat topography and a gravel substrate. The region is characterised by a cold winter from December to February, and a hot, dry summer from June to August. Extremes of temperature are common during the peaks of these seasons. Annual precipitation in the Middle Asian deserts is extremely low (100–200 mm). Study species Phrynocephalus helioscopus helioscopus is a small (body length to 70 mm) agamid that inhabits hard earthy soils and, less commonly, the sands of semideserts. It emerges from winter hibernation in late February or early March, produces two or three clutches of 2–7 eggs each year, and reaches maturity at one year (Bogdanov, 1960; Brushko, 1995; Szczerbak, 2003). Phrynocephalus interscapularis is a very small (body length to 42 mm) agamid that inhabits sandy deserts with sparse vegetation. In the Kyzylkum this species emerges from hibernation in the second half of March, produces single eggs four times a season, and reaches maturity by the end of the first year of life with a body length of around 37 mm (Bogdanov, 1960; Szczerbak, 2003). Phrynocephalus mystaceus galli is a large (body length to 120 mm) agamid that inhabits sandy desert with sparse grass and shrubs. It is active from late March or early April until October, has two mating periods in a season, produces 1–4 eggs per clutch, and reaches maturity at two years (Szczerbak, 2003). Trapelus sanguinolentus aralensis is a common, large (body length to 188 mm), semi–arboreal agamid that inhabits a variety of habitats, ranging from sandy, earthy and rocky deserts to mountain slopes up to 1,200 m above sea level, and river and canal banks. It shelters beneath stones and in rodent burrows. It emerges from hibernation between late February and early April and remains active until October. Two clutches of 4–18 eggs are produced each season, and maturity is attained at two years and a body length of 65–80 mm (Szczerbak, 2003).

Animal Biodiversity and Conservation 31.2 (2008)

Habitat variables

Escape speed

The data were recorded by walking throughout each field site from approximately 07.00 until 19.00 hours. This method ensured coverage of the entire range of structural and thermal microhabitats available. This was done over a 2–week period from April to May 2003, with approximately 4 days spent at each location. Data were only collected on sunny, warm days when lizards could be fully active. At the time and place that each lizard was captured, we recorded eleven structural characteristics of the microhabitat: relative vertical position on dune [top (3); mid–dune (2); swale (1) and no dune (0)]; distance (cm) to the nearest vegetation; distance (cm) to the nearest shelter; height (cm) above ground that the lizard was perched; diameter of perch (cm); visual estimate of the percentage of shrub cover in a 3 m radius surrounding the lizard; visual estimate of the percentage of ground and grass cover in a 3 m radius surrounding the lizard; visual estimate of the percentage of litter cover in a 3 m radius surrounding the lizard; average shrub height (cm) in a 3 m radius surrounding the lizard; visual estimate of percentage rock cover in a 3 m radius surrounding the lizard; visual estimate of percentage gravel cover in a 3 m radius surrounding the lizard. We could not evaluate interspecific differences in microhabitat occupation at the gravel site near Tamdi, as we captured only P. helioscopus and a single T. sanguinolentus at this location. Consequently, in order to determine whether these lizards were selecting microhabitats non–randomly, we plotted a randomly positioned grid of 50 x 100 m (encompassing the full range of microhabitats used by the lizards) and recorded microhabitat variables as we would for an actual lizard capture every 5 m within the grid (resulting in 55 data points). The grid data points were only recorded at times of the day when lizards were active, allowing comparable measurements of thermal conditions.

Average escape speed was used as a measure of the functional link between morphology and the microhabitat occupied by each species. Our measurement of escape speed is not intended as a proxy for maximum performance ability, but rather an estimate of escape speed in an ecologically natural setting. There have been numerous studies that have measured running and locomotion in natural settings (e.g., Irschick & Jayne, 1999; Irschick & Losos, 1999), including the video techniques that we employ. It has been found that substrate and slope can alter the speed and behaviour of lizards (Irschick & Garland, 2001). Thus, our field–based measurements provide an ecologically relevant estimate of escape speed in a species' natural environment. At the time of release, the lizard was aligned with a line marked in the substrate, and the escape sprint was recorded on a Sony Digital video camera for later analysis. The distance the lizard ran was measured to the nearest centimetre. To reduce the possibility of displacement and provide an accurate estimate of escape speed in their microhabitat, lizards were released for videoing at the point where they were first observed. To ensure differences in escape speed were not related to temperature, the body temperature of all lizards were measured prior to videoing. As all lizards had active body temperatures (range: 25.1– 35.2°C; mean = 30.1; SE = 0.28), there was no relationship between the body temperature and speed of the lizard (n = 48, r2 = 0.03, P = 0.278). Even when analysed within species there was no relationship between escape speed and body temperature (Phrynocephalus helioscopus n = 14, r2 = 0.03, P = 0.475, P. interscapularis n = 16, r2 = 0.03, P = 0.538, P. mystaceus n = 9, r2 = 0.03, P = 0.644 and Trapelus sanguinolentus n = 9, r2 = 0.31, P = 0.118). Videoed escapes were analysed using Quicktime 4.1.2 software (Apple Computers Inc., Cupertino, California, USA). We determined the duration of all runs by counting the number of frames (30 frames.s–1) elapsed between the beginning and end of the escape movement. Speed was measured in m.s–1 for each escape.

Morphology Active lizards were caught by hand or with a noose– pole. Immediately upon capture the lizard’s body temperature was measured to provide an estimation of active body temperatures of each species in its preferred habitat. Each lizard’s gender was determined and nine morphological measurements were recorded: 1. Snout–vent length (SVL); 2. Tail length (only individuals with intact tails were included); 3. Pelvis width (distance between hip joints on dorsal surfaces); 4. Humerus length (distance from shoulder to apex of elbow); 5. Antebrachium length (distance from elbow apex to center of wrist); 6. Forefoot length (distance from center of wrist to claw tip of longest toe, IV); 7. Femur length (distance from insertion of hindleg at pelvis to apex of knee); 8. Crus length (distance from apex of knee to heel); and 9. Hindfoot length (distance from heel to claw tip of longest toe, IV).

Data analyses Principal components analyses (PCA) were used to reduce the dimensionality of the morphological data (FACTOR procedure of SYSTAT). Prior to analysis, all morphological variables were log–transformed, and the effect of body size was removed from all measurements by using the residuals for each of the log–transformed variables regressed on logSVL. In each case the principal components (PCs) were extracted from a correlation matrix of the raw data. Principal components axes were named by the correlations of the original variables to the PC: correlations with absolute values greater than 0.5 were considered important (following Tabachnick & Fidell, 1989). Resultant PC axes were explored using analy-

Clemann et al.

Table 1. Gender, field body temperature, presence at each field site, general description of habitats in which each species occurs, escape distance and speed of agamid lizards from the Kyzylkum Desert, Uzbekistan: G M/F. Gender M/F; Bt. Body temperature [ºC,  ± (SE)]; Fs. Field site number; Hc. Habitat category; Ghd. General habitat description; Med. Maximum escape distance [m,  ± (SE)]: Es. Escape speed [m.s–1,  ± (SE)]; a Note that two of the T. sanguinolentus presented here were not captured at the sites where habitat attributes where assessed, and were not included in habitat analyses. Tabla 1. Género, temperatura corporal de campo, presencia en cada localización, descripción general de los hábitats en los que se encuentra cada especie, distancia de escape y velocidad de huida de los lagartos agámidos del desierto de Kyzylkum, Uzbekistán: G M/F. Género M/H; Bt. Temp. corporal [oC,  ± (EE)]; Fs. Número de localización; Hc. Categoría de habitat; Ghd. Descripción general del hábitat; Med. Distancia máxima de huida [m,  ± (EE)]; Es. Velocidad de escape [m.s–1,  ± (EE)]; a Nótese que dos de los T. sanguinolentus que aquí presentamos no fueron capturados en lugares en los que se habían valorado los atributos del hábitat, y no han sido incluidos en los análisis del hábitat.

Species

G M/F

Ghd

Med

Phrynocephalus helioscopus

3/11

33.1 (0.70)

Ground–dwelling

Flat gravel desert

0.94 (0.12)

1.49 (0.13)

32.4 (0.65)

Ground–dwelling

Undulating sand dunes

1.46 (0.14)

2.26 (0.16)

32.3 (0.87)

1, 2

Ground–dwelling

Dune tops in

6.23 (0.81)

4.12 (0.29)

35.4 (0.79)

1, 2, 3

Semi–arboreal

All habitats except

3.69 (0.60)

2.70 (0.31)

Phrynocephalus interscapularis

10/6

Phrynocephalus mystaceus

4/5

undulating sand dunes

Trapelus sanguinolentusa

7/4

sis of variance (anova) with multiple comparisons (Tukey’s procedure) to determine whether there were interspecific differences in morphological and microhabitat variables. For each taxon, field body temperature, escape distance and speed were compared using anova with multiple comparisons (Tukey’s procedure). Maximum escape distance was regressed against SVL, and escape speed was regressed against limb length (i.e. the sum of the three limb measures for fore– and hindlimbs) whilst controlling for body size (SVL) by using the residuals of the various leg length variables. We used SYSTAT Version 10.2 (SYSTAT Software Inc., Richmond, California, USA) for analyses. For the available habitat variables at each site (range–standardised), we computed a matrix of pairwise Euclidean distances between data points. We employed non–metric multi–dimensional

dune tops

scaling (NMDS) ordination in two dimensions, and plotted the resulting ordination diagram as a scatterplot. Subsequently, convex hulls were drawn around the groups of data points according to which species had been captured there (or whether they were random points, in the case of the gravel site). We then fitted linear vectors of the original habitat variables to the ordination space, displayed as arrows overlayed on the plot showing direction of steepest gradient in each habitat variable. Significant differences between habitat attributes of lizard sites and random sites were determined using an Analysis of Similarity (ANOSIM) test, with 1000 random permutations. NMDS and ANOSIM procedures were implemented in the R statistical programming environment (R Development Core Team, 2004), with the aid of the add–in libraries MASS (Venables & Ripley, 2002) and vegan (Oksanen, 2005).

Animal Biodiversity and Conservation 31.2 (2008)

Table 2. Summary statistics of the 11 structural microhabitat variables recorded for each species of agamid lizards from the Kyzylkum Desert, Uzbekistan ( ± SE): Pd. Position on dune (a estimate of relative vertical position on dune: top (3), mid–dune (2), swale (1) and no dune (0)); Nv. Nearest vegetation (cm); Ns. Nearest shelter (cm); Ph. Perch height (cm); Pd. Perch diameter (cm); Sc. Shrub cover (%); Ggc. Ground/grass cover (%); Lc. Litter cover (%); Sh. Shrub height (cm); Rc. Rock cover (%); Gc. Gravel cover (%). Tabla 2. Resumen estadístico de las 11 variables de microhábitats estructurales estudiadas para cada especie de lagarto agámido del desierto de Kyzylkum, Uzbekistán ( ± EE): Pd. Posición en la duna (a Estimación de la posición vertical relativa en la duna: cima (3), mitad de la duna (2), parte baja (1) y sin duna (0); Nv. Vegetación más cercana (cm); Ns. Refugio más cercano (cm); Ph. Altura de la percha (cm); Pd. Diámetro de la percha (cm); Sc. Cubierta arbustiva (%); Ggc. Suelo/cubierta herbácea (%); Lc. Cubierta de mantillo (%); Sh. Altura de los arbustos (cm); Rc. Suelo rocoso (%); Gc. Capa de grava (%). Species n

Pda

Ggc

Phrynocephalus helioscopus

0.0 ± 0.0

30.7 ± 4.50

103.2 ± 23.05

0.0 ± 0.0

2.4 ± 0.49

6.4 ± 1.25

0.9 ± 0.28

36.4 ± 5.09

12.6 ± 3.52

24.3 ± 4.29

Phrynocephalus interscapularis 16

2.1 ± 0.23

94.7 ± 35.26

167.8 ± 38.64

0.0 ± 0.0

1.9 ± 0.26

1.8 ± 0.46

0.2 ± 0.11

75.0 ± 12.04

0.0 ± 0.0

Phrynocephalus mystaceus

3.0 ± 0.0

124.4 ± 28.49

170.0 ± 30.64

0.0 ± 0.0

2.9 ± 0.54

0.3 ± 0.24

0.7 ± 0.29

102.2 ± 10.90

0.0 ± 0.0

Trapelus sanguinolentusa

0.8 ± 0.30

51.8 ± 14.5

63.4 ± 18.8

9.1 ± 4.76

12.7 ± 7.15

4.4 ± 0.72

6.0 ± 1.21

1.5 ± 0.25

70.9 ± 8.47

3.6 ± 2.68

8.9 ± 4.76

Results Habitat selection Mean field body temperatures ranged from 32.3°C (P. mystaceus) to 35.4°C (T. sanguinolentus) (table 1). An ANOVA of these temperatures indicated significant differences among species (F3,46 = 3.49, P = 0.023). Trapelus sanguinolentus had a significantly higher body temperature than P. interscapularis (Tukey’s HSD post hoc test, P = 0.025). Phrynocephalus spp. had similar mean field body temperatures that were all slightly lower than T. sanguinolentus (table 1). Although the latter species is semi–arboreal (versus ground–dwelling for the Phrynocephalus spp.), all specimens that we measured were first encountered either on the ground or perched on small mounds of sand or gravel. The summary statistics for the 11 structural microhabitat characteristics for each species are provided in table 2. At the two sand dune sites we recorded data for 16 P. interscapularis, nine P. mystaceus and eight T. sanguinolentus. Analysis

of Similarities indicated significant differences in the habitat features associated with each species (ANOSIM statistic: R = 0.3371, P < 0.001). At the two sand dune sites P. interscapularis and P. mystaceus were associated with low shrub heights, long distances to vegetation and shelter, and occurred towards the tops of dunes (fig. 1). However, P. mystaceus occurred in a much more restricted range of habitat associations than P. interscapularis (most notably, position on dune, where P. mystaceus was only found on dune tops, and P. interscapularis tended to occur mid–slope and in swales between dunes). The generalist species, T. sanguinolentus, was associated with a wide range of habitat factors, although it occurred closer to shelter and vegetation than the other species and was found in areas with more vegetation and rock cover. For the gravel site, we recorded data for 14 P. helioscopus, one T. sanguinolentus and 55 random points. A NMDS ordination of these data is given in figure 2. The result of the ANOSIM indicates that there are significant differences between the habitat features

Clemann et al.

Distance to shelter

Distance to vegt.

0 % Ground cover % Rock cover % Gravel

–10

Position on dune

Shrub height

Perch height Perch diameter

% Shrub cover % Litter cover

–20 –30

–20

–10

Fig. 1. Scatterplot of the non–metric multi–dimensional scaling ordination for species occurring at the sand dune sites, with arrows indicating the linear gradients of significant habitat factors. The stress of the ordination configuration is 0.088. Convex hulls have been drawn around data points of each species: Trapelus sanguinolentus (¢, solid line); Phrynocephalus interscapularis ( , dashed line); and Phrynocephalus mystaceus (£, dotted line). Fig. 1. Diagrama de dispersión de la ordenación ajustada multidimensional y no métrica de las especies que habitan en las localizaciones de las dunas arenosas; las flechas indican el gradiente lineal de los factores del hábitat significativos. El estrés de la configuración de ordenación es 0,088. Se han dibujado signos convexos alrededor de los puntos de los datos de cada especie: Trapelus sanguinolentus (¢, línea continua); Phrynocephalus interscapularis ( , línea discontinua); y Phrynocephalus mystaceus (£, línea de puntos).

for each of these lizards and the random data points (ANOSIM statistic: R = 0.2338, P = 0.007). The vector plot indicates that P. helioscopus and the single T. sanguinolentus were associated with areas of higher vegetation cover than that typically found at random habitat points. Phrynocephalus helioscopus occurred in a much more restricted range of habitat associations than the randomly measured data points. Functional morphology and escape speed A summary of morphometric characters for each species is presented in table 3. Principal components analysis of the morphological variables revealed that limb proportions explained most of the variance in the data. This first axis (PC1) explained 42.8% of the variance in morphology. Lizards scoring high on

this axis had long limbs and hands / feet, and a wide pelvis. Lizards scoring low on this axis had short limbs (table 4). The second principal component axis (PC2) explained 17.5% of variance in morphology. Lizards scoring high on this axis had long tails and long upper hindlimbs, whilst lizards scoring low in this axis had short tails and upper hindlimbs (table 4). An anova indicated a significant difference between species on PC1 (F3,46 = 24.15, P < 0.001) and a Tukey’s HSD post hoc test showed that P. mystaceus scored significantly higher on this axis than the other three species (all Ps < 0.001), and that P. helioscopus scored significantly higher than P. interscapularis (P  = 0.031). Thus, P. mystaceus had longer limb proportions than the other species, relative to body size. An anova of PC2 also indicated a significant difference between species (F3,46 = 18.86, P < 0.001). A Tukey’s HSD post hoc test indicated that, on this axis, T. sanguinolentus

Animal Biodiversity and Conservation 31.2 (2008)

Distance to shelter Distance to vegt.

Perch diameter Perch height

% Gravel % Rock (5–20 cm) % Rock (< 5 cm)

Substrate type % Litter cover

–5

% Rock (20–50 cm)

% Ground cover % Shrub cover

–10

–5

Shrub height

Fig. 2. Scatterplot of the non–metric multi–dimensional scaling ordination analysis for species occurring at the gravel site, with arrows indicating the linear gradients of significant habitat factors. The stress of the ordination configuration is 0.166. Convex hulls have been drawn around data points: Phrynocephalus helioscopus (¢, solid line) and random habitat points ( , dashed line). A single Trapelus sanguinolentus was recorded at this site and is indicated by a single data point (£). Fig. 2. Diagrama de dispersión del análisis de la ordenación ajustada multidimensional y no métrica de las especies que habitan en las localizaciones con suelo cubierto de grava; las flechas indican el gradiente lineal de los factores del hábitat significativos. El estrés de la configuración de ordenación es 0,166. Se han dibujado signos convexos alrededor de los puntos de los datos de cada especie: Phrynocephalus helioscopus (¢, línea continua) y puntos del hábitat al azar ( , línea discontinua). Sólo se localizó un único Trapelus sanguinolentus en este habitat, y ha sido consignado mediante un solo punto (£).

scored significantly higher than all of the other taxa (Ps < 0.001). There was clear separation of these species in morphospace (fig. 3). The three species that were syntopic at the two dune sites, P. mystaceus, P. interscapularis and T. sanguinolentus, did not overlap in morphospace. Similarly, the two species occurring at the site with gravel substrate (P. helioscopus and T. sanguinolentus) did not overlap. Thus, even after the effects of body size were removed, there was morphological separation of all study species in limb proportions, pelvis dimensions and tail length. The functional significance of each species’ morphology in their respective habitat was quantified using escape speed and escape distance. Upon release, the two larger taxa, P. mystaceus and T. sanguinolentus, ran further than the other species (table 1; anova of maximum escape distance, F3,46 = 31.14, P < 0.001).

After controlling for body size, P. mystaceus ran significantly further than all the other taxa (Tukey’s HSD post hoc test, P < 0.001 for P. helioscopus and P. interscapularis, and P = 0.001 for T. sanguinolentus), and both P. helioscopus and P. interscapularis ran relatively further than T. sanguinolentus (P < 0.001 and = 0.001 respectively). Regression of maximum escape distance against SVL showed a significant positive relationship between longer–bodied taxa and escape distance (F1,48 = 78.71, P < 0.001). However, a similar test of distance versus combined fore– and hindlimb dimensions (controlled for body size) showed no significant relationship between leg length and escape distance (F2,47 = 0.50, P = 0.610). The two larger taxa also displayed greater outright speed than the smaller species (table 1, anova of escape speed, F3,46 = 23.26, P < 0.001). A Tukey’s HSD post hoc test showed that, after controlling

Clemann et al.

Table 3. Summary of morphometric characters for each agamid species (mm,  ± SE): SVL. Snout– vent length; T. Tail; Pw. Pelvis width; Uf. Upper forelimb; Lf. Lower forelimb; Hl. Hand length; Tf. Total forelimb; Uh. Upper hindlimb; Lh. Lower hindlimb; Fl. Foot length; Th. Total hindlimb; a Note that two of the T. sanguinolentus presented here were not captured at the sites where habitat attributes where assessed, and were not included in habitat analyses. Tabla 3. Resumen de las características morfométricas de cada especie de agámido (mm,  ± EE): SVL. Longitud hocico–cola, T. Cola; Pw. Amplitud pélvica; Uf. Pata delantera superior; Lf. Pata delantera inferior; Hl. Longitud de la mano; Tf. Longitud total de la pata delantera; Uh. Pata trasera superior; Lh. Pata trasera inferior; Fl. Longitud del pie; Th. Longitud total de la pata trasera; a Nótese que dos de los T. sanguinolentus que aquí presentamos no fueron capturados en lugares en los que se habían valorado los atributos del hábitat, y no han sido incluidos en los análisis del hábitat. Species

SVL

Phrynocephalus helioscopus

43.6 (1.66)

47.9 (1.80)

7.9 (0.33)

8.6 (0.26)

8.6 (0.54)

8.4 (0.21)

25.68 (0.92)

11.5 (0.38)

14.3 (0.38)

39.57 (1.14)

Phrynocephalus interscapularis

31.1 (0.76)

33.0 (1.03)

4.7 (0.15)

5.7 (0.10)

5.2 (0.13)

5.8 (0.19)

16.63 (0.31)

8.6 (0.20)

10.3 (0.21)

12.3 (0.24)

31.22 (0.54)

Phrynocephalus mystaceus

102.9 (2.58)

112.2 (2.01)

15.6 (0.38)

18.9 (0.66)

20.1 (0.51)

20.7 (0.66)

59.67 (1.26)

23.4 (0.69)

30.1 (0.61)

34.8 (0.83)

88.33 (1.70)

Trapelus sanguinolentus a

94.5 (2.65)

156.4 (4.22)

12.0 (0.54)

16.8 (0.57)

16.9 (0.36)

15.1 (0.54)

48.82 (1.33)

21.6 (0.61)

27.2 (0.54)

27.4 (0.63)

76.18 (1.49)

for body size, P. mystaceus ran significantly faster than all the other taxa (P < 0.001), and that P. helioscopus was relatively faster than P. interscapularis (P = 0.037) and T. sanguinolentus (P = 0.001). Regression of escape speed against combined fore– and hindlimb measures (controlled for body size) was marginally non–significant (F2,47 = 3.084, P = 0.055), indicating a trend for species with proportionally longer limbs to have faster escape speeds. However, the interspecific relationship between escape speeds is confounded by the fact that species were escaping on different substrate types. Thus, rather than direct interspecific comparisons, these results should be interpreted as escape speed relevant to habitat occupation. Discussion Habitat selection Thermal ecology plays an important role in habitat selection by agamid species (Izhaki & Haim, 1996; Melville & Schulte, 2001). The field body temperatures of agamids in the present study were within the range

recorded for arid–zone agamids from other continents (e.g. Greer, 1989; Melville & Schulte, 2001), but the mean body temperatures we recorded were slightly lower than those reported in these other studies. Other research on Central Asian agamid species found that Phrynocephalus mystaceus and P. interscapularis in the Karakum Desert were active at maximal body temperatures of 43–44 and 43.5–44oC respectively (Cherlin & Muzychenko, 1983). Melville & Schulte (2001) suggested that the field body temperatures they recorded for Australian arid–zone agamids were slightly lower than previously recorded for these taxa because they conducted their study in spring, when ambient and substrate temperatures are cooler than in summer. It is likely that the same situation applies to the present study; we conducted fieldwork in spring during relatively mild conditions, and it is plausible that the mean field body temperatures of the species that we studied may be higher later in the active season. Our study species preferentially selected particular microhabitats. At each site a number of habitat characteristics were found to be important in distinguishing the habitats occupied by each species. For the three species occupying the two sand dune sites, Phrynocephalus interscapularis, P. mystaceus and Trapelus

Animal Biodiversity and Conservation 31.2 (2008)

Table 4. Principal components analysis (PCA) of lizard morphology. The eigenvalues, the proportion of the variance explained by the eigenvalue for each axis, and the loadings for the morphology variables are given. Tabla 4. Análisis de componentes principales (PCA) de la morfología de los lagartos. Se dan los valores propios, la proporción de la varianza explicada por el valor propio para cada eje, y los pesos de las variables morfológicas.

Eigenvalue % of total variance explained

PCA 1

3.852

1.573

42.8

17.5

Cumulative % of total variance explained Snout–vent length Tail residuals Pelvis residuals

that proximity to vegetation played an important role in microhabitat selection for these iguanid species. At our third study site, which was stony and had patchily–distributed ground cover, the proximity of vegetation played an important role in microhabitat selection. We found that, compared to the random data points, Phrynocephalus helioscopus preferred stony microhabitats close to shrubs. However, this species has a large geographic range in Central Asia, occupying hard earthy soils and, infrequently, the sands of semideserts, so whilst our study site may be typical, further comparative study is warranted. Functional morphology and escape speed

42.8

60.3

Loadings 0.374

0.227

–0.436

0.806

0.640 –0.475

Upper hindlimb residuals

0.542

0.620

Lower hindlimb residuals

0.705

0.431

Foot residuals

0.778 –0.022

Upper forelimb residuals

0.683

0.173

Lower forelimb residuals

0.758

0.008

Hand residuals

0.823 –0.215

sanguinolentus, substrate played a significant role in microhabitat selection, whereas at the stony site near Tamdi the proximity of vegetation appeared to be the important factor for microhabitat selection for P. helioscopus. The three species that occurred at the sand dune sites occupied different microhabitats. We found P. mystaceus only on dune tops, whereas P. interscapularis tended to occur mid–slope and in swales between dunes. In contrast, T. sanguinolentus tended towards habitat generalism at the sand dune sites, although it was never observed on the top of large dunes. Differential habitat use of swale versus dune tops has been recorded in studies of other desert lizard species. For example, in the Simpson Desert, Australia, differences have been found in the use of dunes tops, sides and swales between the agamid species Ctenophorus isolepis and C. nuchalis (Dickman et al., 1999). Similarly, in the White Sands National Monument, New Mexico, the iguanid species Holbrookia maculata and Sceloporus undulatus have also been found to select dune, hardpan or transitional substrates differentially (Hager, 2001). This latter study also found

There were considerable differences in the relative morphology of the study species, most notably between Trapelus sanguinolentus and the three species of Phrynocephalus. We found relative tail length (PC2) to be significantly different between these two groups, where T. sanguinolentus had a relatively longer tail than the three species of Phrynocephalus. This difference may have a phylogenetic basis, which the current study is unable to address. The interspecific differences between PC1 (limb proportions) shows that P. mystaceus has significantly longer limbs than all of the other species. However, the remaining two species within the same genus (P. interscapularis, P. helioscopus) do not differ significantly in relative limb proportions to the more distantly related T. sanguinolentus, which indicates phylogenetic relatedness is not playing an important role. Thus, we are able to look at these traits in a functional framework. Measuring escape speed in the field provides a direct and functional link between morphology and habitat use. Previous studies have shown that field escape speed is significantly less than the speed recorded in laboratory tests (e.g., Avery et al., 1987; Braña, 2003). A similar trend is likely for the species that we studied. The only direct previous measure of speed for any of our study species is for P. mystaceus (Sukhanov, 1974), where attempts to record speed both in the field and laboratory were largely unsuccessful, with only two brief speed cycles recorded in the laboratory. These speeds were 1.2 ms–1 for a cycle of about 0.09 seconds, and 1.8 ms–1 for 0.1 second (Sukhanov, 1974). The escape speeds we recorded in the field were comparable to those of two iguanid species studied in the laboratory that have similar habitat preferences and body shape to P. mystaceus (Callisaurus draconoides SVL = 76 mm, speed = 4.4 ms–1; Uma scoparia SVL = 80 mm, speed = 4.0 ms–1; Irschick & Jayne, 1998). However, these species have a smaller body size than P. mystaceus (SVL = 103 mm, speed = 4.12 ms–1). This possible reduction in speed relative to body size in the field is unlikely to be due to temperature differences, as there was no correlation between body temperature and speed in the present study. However, it is likely that habitat plays a significant role in escape speed. Locomotor performance is highly context–dependent, so that factors such as habitat selection can interpose filters that diminish potential per-

Clemann et al.

P. helioscopus P. interscapularis P. mystaceus T. sanguinolentus

PC1

–1

–3

–2

–1

PC2

Fig. 3. The distribution of four study species along the first two morphological principal components axes. Fig. 3. Distribución de las cuatro especies estudiadas a lo largo de los dos primeros ejes de componentes principales morfológicos.

formance (Braña, 2003; Irschick & Losos, 1999). In the loose sand habitats that Phrynocephalus interscapularis and P. mystaceus occupy, escape speed would be reduced due to an unstable and movable substrate that would dampen propulsive force, despite the possession by these species of specialised morphological features to assist in locomotion, such as toe fringes. Similarly, the habitat of P. helioscopus in the present study (stony valley with scattered ground cover) would also provide challenges to locomotor speeds. Thus, by measuring escape speed in the field we are able to directly examine the relationship between habitat occupation, morphology and locomotion. The escape behaviour observed in a species, as well as its escape speed, can provide insight into habitat utilisation. A number of studies have found that there is a correlation between behaviour, morphology, performance ability and habitat use (e.g., Melville & Swain, 2000; Herrel et al., 2002). We found that escape distance varied significantly between the species. Phrynocephalus interscapularis and P. helioscopus escaped over very short distances, while P. mystaceus escaped over long distances. Trapelus sanguinolentus, on the other hand, had variable escape distances. This species occupied a wider range of habitats than the other species, was semi–arboreal, and was often observed perching

above or close to a burrow entrance. Consequently, T. sanguinolentus is likely to have a greater range of retreat options when fleeing predators, and often may not need to travel as far along the ground as the strictly terrestrial species. Within the three Phrynocephalus species we observed two main escape behaviours: crypsis and sand–diving. Crypsis was used by Phrynocephalus helioscopus, which initially flee a short distance before freezing. This behaviour has been observed in other arid–zone species occupying stony plains, including the agamid Tympanocryptis cephalus and the iguanid Phynosoma modestum (Melville, pers. obs.). Phrynocephalus mystaceus and P. interscapularis used sand–diving when escaping. When approached, P. mystaceus would sprint away from the observer until it had just cleared the next rise, where they would rapidly bury themselves in the sand using lateral oscillatory movements. This sand–diving technique has previously been observed in members of this genus, and is known to be an adaptive trait in lizards occupying loose sand habitats (Arnold, 1995). Although P. interscapularis used a similar sand–diving strategy to avoid capture, it usually relied upon short bursts of sprinting and erratic changes of direction before eventually burying itself if pursuit continued. This sand–diving appeared to be a "last resort" strategy for this species.

Animal Biodiversity and Conservation 31.2 (2008)

Other studies of terrestrial lizards living in open, sparsely vegetated habitats have suggested that there are two possible behavioural escape strategies (Schulte et al., 2004): (1) running long distances at high speed to a potential shelter; or (2) remaining motionless and flattening the body against the ground. Whilst we observed both of these behaviours in Phrynocephalus, it is apparent from our observations that there may be a third and possibly intermediate category, where a species flees over short distances, using evasive techniques such as rapid changes in direction. Clearly there is scope for further comparative work on the agamid lizards of Uzbekistan. Conservation Studies such as this demonstrate the importance of microhabitat features for many small, terrestrial animals, particularly those with specialised habitat requirements. Many of these habitat attributes are vulnerable to threatening processes such as trampling by domestic stock, overgrazing, firewood collection, increasing salinity and desertification. The paucity of field research on vertebrate fauna in Central Asia means that there is little quantitative data with which to assess their current or former distribution, abundance or conservation status. Based on anecdotal accounts of declines in some taxa (Szczerbak, 2003), we suggest that there is an urgent need for surveys to determine the current geographic range of these species, and to establish programs to monitor the status of the species and their habitats. Such programs should address issues such as population trends over time, and the impact and mitigation of threatening processes. Acknowledgements We thank Artur Nuridjanov, Alexandr Kreuzberg, Djamshid and Kamal for companionship and help before and during fieldwork. Financial support was provided by an Australian Research Council grant (ARC 00104045). Dave Duncan provided a useful critique of an earlier draft of the manuscript. References Ananjeva, N. B., 2003. Comparative analysis of limb proportions in five sympatric species of Eremias genus. Russian Journal of Herpetology, 10: 140–145. Ananjeva, N. B., Borkin, L. Y., Darevsky, I. S. & Orlov, N. L., 1998. Amphibia and reptilia. Encyclopedia of the nature of Russia. (Field Guide of amphibians and reptiles of Russia and adjacent countries). ABF Publishing Company, Moscow, Russia. Ananjeva, N. B., Orlov, N. L., Khalikov, R. G., Darevsky, I. S., Ryabov, S. A. & Barabanov, A. V., 2006. The Reptiles of Northern Eurasia. Pensoft Series, Faunistica No. 47, Pensoft Publishers, Russia.

Ananjeva, N. B. & Tuniyev, B. S., 1992. Historical biogeography of Phrynocephalus of USSR fauna. Asiatic Herpetological Research, 4: 76–98. Anderson, S. C., 1999. The lizards of Iran. Contribution to Herpetology. Vol. 15. SSAR. Arnold, E. N., 1995. Identifying the effects of history on adaptation – origins of different sand–diving techniques in lizards. Journal of Zoology, 235: 351–388. Avery, R. A., Mueller, C. F., Jones, S. M., Smith, J. A. & Bond, D. J., 1987. Speed and movement patterns of European lacertid lizards: a comparative study. Journal of Herpetology, 21: 324–329. Bogdanov, O. P., 1960. Amphibians and Reptiles. Fauna of Uzbek SSR. Vol. 1. Tashkent. Braña, F., 2003. Morphological correlates of burst speed and field movement patterns: the behavioural adjustment of locomotion in wall lizards (Podarcis muralis). Biological Journal of the Linnean Society, 80: 135–146. Brushko, Z. K., 1995. Lizards of the deserts of Kazakhstan. Almaty, Konzhyk. Cherlin, V. A. & Muzychenko, I. V., 1983. Thermobiology of Eremias grammica, Phrynocephalus mystaceus and Phrynocephalus interscapularis in east Karakumy in summer. Zoologicheskii Zhurnal, 62: 897–908. Dickman, C. R., Letnic, M. & Mahon, P., 1999. Population dynamics of two species of dragon lizards in arid Australia: the effects of rainfall. Oecologia, 119: 357–366. Greer, A. E., 1989. The Biology and Evolution of Australian Lizards. Surrey Beatty & Sons Pty Ltd, New South Wales, Australia. Hager, S. B., 2001. Microhabitat use and activity patterns of Holbrookia maculata and Sceloporus undulates at White Sands National Monument, New Mexico. Journal of Herpetology, 35: 326–330. Herrel, A., Meyers, J. J. & Vanhooydonck, B., 2002. Relations between microhabitat use and limb shape in phrynosomatid lizards. Biological Journal of the Linnean Society, 77: 149–163. Irschick, D. J. & Garland Jr., T., 2001. Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annual Review of Ecology and Systematics, 32: 367–96. Irschick, D. J. & Jayne, B. C., 1998. Effects of incline on speed, acceleration, body posture and hindlimb kinematics in two species of lizard Callisaurus draconoides and Uma scoparia. Journal of Experimental Biology, 201: 273–287. – 1999. A Field Study of the Effects of Incline on the Escape Locomotion of a Bipedal Lizard, Callisaurus draconoides. Physiological and Biochemical Zoology, 72: 44–56. Irschick, D. J. & Losos, J. B., 1999. Do lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean Anoles. The American Naturalist, 154: 293–305. Izhaki, I. & Haim, A., 1996. Adaptive morphometric variation in lizards of the genus Agama in Israel.

Israel Journal of Zoology, 42: 385–394. Melville, J. & Schulte II, J. A., 2001. Correlates of active body temperatures and microhabitat occupation in nine species of central Australian agamid lizards. Austral Ecology, 26: 660–669. Melville, J. & Swain, R., 2000. Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lygosominae). Biological Journal of the Linnean Society, 70: 667–683. NBSAP, 1998. Republic of Uzbekistan Biodiversity Conservation. National Strategy and Action Plan. National Biodiversity Strategy Project Steering Committee. Tashkent, Uzbekistan. Oksanen, J., 2005. Vegan: Community Ecology Package. R package version 1.6–7. URL: http://cc.oulu.fi/~jarioksa/ R Development Core Team, 2004. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07–0. URL: http://www.R–project.org. Schulte, J. A., Losos, J. B., Cruz, F. B. & Nunez, H., 2004. The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini). Journal of Evolutionary Biology

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17: 408–420. Sukhanov, B. V., 1974. General system of symmetrical locomotion of terrestrial vertebrates and some features of movement of lower tetrapods. Amerind Publishing, New Delhi. (Translated from the Russian version, published in 1968 by Nauka Publishers, Leningrad, Russia.) Szczerbak, N. N., 2003. Guide to the Reptiles of the Eastern Palearctic. Krieger Publishing Company, Malabar, Florida, U.S.A. Tabachnick, B. G. & Fidell, L. S., 1989. Using Multivariate Statistics. Harper & Row, New York, U.S.A. The Red Data Book of the Republic of Uzbekistan 2003. Vol. 2. Animals. Tashkent. Chinor ENK. UNDP, 2001. Supporting Drylands Development. Report of the United Nations Development Programme (UNDP) to the Fifth Conference of the Parties to the Convention to Combat Desertification. Geneva, Switzerland. UNEP, 1999. National Action Programme to Combat Desertification in Republic of Uzbekistan. United Nations Environment Programme (UNEP) and Cabinet of Ministers Main Administration of Hydrometeorology (GLAVGIDROMET). Venables, W. N. & Ripley, B. D., 2002. Modern Applied Statistics with S. Fourth Edition. Springer, New York, U.S.A.

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Population and conservation srategies for the Chinese crocodile lizard (Shinisaurus crocodilurus) in China C. M. Huang, H. Yu, Z. J. Wu, Y. B. Li, F. W. Wei & M. H. Gong

Huang, C. M., Yu, H., Wu, Z. J., Li, Y. B., Wei, F. W. & Gong, M. H., 2008. Population and conservation strate gies for the Chinese crocodile lizard (Shinisaurus crocodilurus) in China. Animal Biodiversity and Conservation, 31.2: 63–70. Abstract Population and conservation strategies for the Chinese crocodile lizard (Shinisaurus crocodilurus) in China.— The Chinese crocodile lizard (Shinisaurus crocodilurus) is an unusual anguimorph lizard found mainly in China. Transect surveys estimate a total wild population of about 950 individuals in China. This is a dramatic decrease compared with previous surveys. At present, there are only eight areas of distribution. No Chinese crocodile lizards have been found in four former areas for several years. Investigations have demonstrated that poaching has contributed directly to the population decline. Habitat destruction, and in particular water flow, is the second most important factor. Mining, small scale dam construction, electro–fishing and poisoning of fish in the stream also contribute to population decline. Therefore, educating local people, punishing illegal poaching, and strengthening scientific research are urgent. Key words: Chinese crocodile lizard (Shinisaurus crocodilurus), Population survey, Threatening factors, Con servation strategy. Resumen Población y estrategias para la conservación del lagarto cocodrilo chino (Shinisaurus crocodilurus) en China.— El lagarto cocodrilo chino (Shinisaurus crocodilurus) es un lagarto anguimorfo que se encuentra principalmente en China. Según los estudios de transectos se estima que en China existe una población salvaje total de aproximadamente 950 individuos. Ello constituye un espectacular descenso en comparación con los estudios anteriores. Actualmente sólo existen ocho áreas de distribución. Hace varios años que no se ha encontrado ningún lagarto cocodrilo chino en cuatro áreas que anteriormente estaban pobladas por esta especie. Las investigaciones han demostrado que la caza furtiva ha contribuido directamente a la disminución de las po blaciones. El segundo factor en importancia es la destrucción del hábitat, y particularmente las inundaciones. La minería, la construcción de pequeñas presas, y la pesca por envenenamiento o mediante la electricidad en los arroyos también contribuyen a que disminuyan las poblaciones. Por lo tanto, consideramos que serían tareas urgentes la educación de los nativos, la sanción de la caza furtiva y la intensificación de la investiga ción científica. Palabras clave: Lagarto cocodrilo chino (Shinisaurus crocodilurus), Estimas de población, Factores de ame naza, Estrategias de conservación. (Received: 29 IV 08; Conditional acceptance: 4 IX 08; Final acceptance: 6 X 08) C. M. Huang, China West Normal Univ., Nanchong 637000, P. R. China.– H. Yu, Z. J. Wu & Y. B. Li, Guangxi Normal Univ., Guilin 541004, P. R. China.– F. W. Wei, Key Laboratory of Animal Ecology and Conservation Biology, Inst. of Zoology, Chinese Academy of Science, Beijing 100081, P. R. China.–M. H. Gong, Inst. of Survey and Design, National Forestry Administration, Beijing 100081, P. R. China. Corresponding author: C. M. Huang. E–mail: cmhuang@ioz.ac.cn ISSN: 1578–665X

Huang et al.

Introduction Reptiles and amphibians are among the most sensitive animals to global and regional environmental change, and can be the indicator of such changes (Eriksson, 2003; Li et al., 2006). Shinisaurus crocodilurus, the Chinese crocodile lizard, inhabits the mountain ranges of Guangxi and Guangdong Provinces in China (Liu & Hu, 1962; Liu et al., 1989; Zhang, 1991; Li & Xiao, 2002). It has also recently been reported from Quang Ninh Province in Vietnam (Quyet & Ziegler, 2003). A comparative study of DAN, morphology, and ecology indicates that the Chinese crocodile lizard populations from China and Vietnam are not significantly different even though separated by at least 500 km (Ziegler et al., 2008). The species was first collected in 1928 (Ahl, 1930; Fan, 1931) and remains monotypic as the most re cently named lizard genus. Its rarity in captivity and in the wild has resulted in this lizard being poorly repre sented in museum collections and in the literature. Shinisaurus crocodilurus is a semi–aquatic predator and a strong swimmer, preying on fish, tadpoles, and aquatic insects and their larvae (Ahl, 1930; Shen & Li, 1982; Yu et al., 2006). It is viviparous (Shen & Li, 1982; Zhang & Tang, 1985; Mägdefrau, 1987; Zhao et al., 1999) and breeds in July and August in the wild (Zhang & Tang, 1985; Zhang, 1991) but at different times in captivity (Hofmann, 2000). The species was listed in CITES Appendix II in January 2007 and is a category I species under the Wild Animal Protection Law in China in view of its narrow distribution and small population (Mägde frau, 1987; Sprackland, 1989; Zhang, 2002).

Based on its many primitive characteristics, inclu ding the lacrimale, supratemporale, small teeth on pterygoideum, chromosome number 2n = 32, and other studies (Hu et al., 1984; Zhang, 1991; 2002; Zhang et al., 1996), it is considered to be a rem nant reptile from the Pleistocene. It thus has great scientific value not only for systematics, but also for understanding the origin, adaptation, radiation and evolution of reptiles. However, heavy pressure from human poaching for pets, food, medicine, and specimens, as well as local environmental changes, have forced the population into severe decline (Mo & Zou, 2000; Zhang, 2002; Zeng, 2003). Its habitat has also become both fragmented and deteriorated, further increasing concern among scientists and the forestry administration. Therefore, we conducted this study to clarify the present status of the total wild population of Chinese crocodile lizards in Chi na, and to investigate the factors which contribute to this population decline. Finally, we propose measures to be taken by local government and forestry administration personnel to protect this rare species. Material and methods Study area All areas in this survey were determined by references, previous reports and information from local forestry de partments. This included the counties of Jinxiu, Hexian, Zhaoping, Guiping, and Pingnan in Guangxi Province (23° 242'–24° 152' N and 109° 522'–111° 512' E) and

Table 1. Population density, hunting pressure and patch density in each distribution area: Da. Distribution area; Ppd. Population density (persons/km2); Ptd. Patch density (pieces/km2); Q. Questionaries; N. Never; O. Occasinally; F. Frequently; I. Index. (For other abbreviations see Method of survey in Material and methods.) Tabla 1. Densidad de la población humana, presión de caza y densidad de piezas cobradas en cada zona de distribución: Da. Área de distribución; Ppd. Densidad de población (personas/km2); Ptd. Densidad de las parcelas (piezas/km2); Q. Questionarios; N. Nunca; O. Ocasionalmente; F. Frecuentemente; I. Índice. (Para otras abreviaturas ver Método de reconocimiento en Material y métodos.) Da

Hunting pressure Ppd

Ptd

43.76

0.86

29.4

32.82

1.11

10.1

12.34

24.5

0.5

10.5

2.69

0.63

3.4

9.09

0.5

2.7

S&L

19.26

1.2

8.4

D&B

5.75

5.4

Total

Animal Biodiversity and Conservation 31.2 (2008)

Qujiang in Guangdong province (24° 362'–24° 39' N and 113° 132'–113° 222' E) (fig. 1) and Guposhan of Jianghua County (24° 332'–24° 352' N and 111° 322'–111° 372' E) in Hunan province. The survey was conducted between late April and early October 2004; this is the non–hibernation season for the Chinese crocodile lizard. The average temperature in this region is 18.7° (–5.6°–39.5°) with an annual precipitation of 2,113.9 mm. The area surveyed belongs to the headwaters of the Pear River system. Mountains are 500–1,200 m above sea level. Vegetative cover is secondary subtropical evergreen broadleaf forest or cultivated forest. The dominant secondary species include Liquidambar tawaniana, Alangium chinensis, Saplum discolor, Neolitsea levinei, Machilus thunbergi and Castanopsis eyrei, etc. Cunninghamia lanceolata, Illicium verum, Cinnamomum cassia have been planted for timber, fruit, and tea at lower levels of the mountain, the lizards’ main habitat. Method of survey Questionnaire We interviewed the local people to collect information about household economy, local human population, frequency of hunting the lizard, and the purposes for hunting (food, medicine, or sale) (table 1). We made random inquiries with a total of 75 local people in eight areas. Field survey All surveys were made in the daytime (Mo & Zou, 2000). We selected survey areas according to previ ous reports and information from the local forestry administration. We then determined the transect stream lines and marked them on the map (1:10,000). We surveyed a total of 199 transects, with 50 in Luoxiang (LX) in Jinxiu County, 54 in Jiulong (JL) in Zhaoping County, 19 in Daguishan (DG) and Lisong (LS) in Hexian County, 13 in Hema (HM) in Wuxuan County, seven in Guxiu (GX) in Mengshan County, 16 in Sanlian & Luoyi (S&L) and Datunxia & Bitan (D&B) in Guiping County, 15 in Guoan (GA) in Pingnan County in Guangxi province, and 25 in Luokeng (LK) in Qujiang County in Guangdong Province. The transect streams ranged in length from 570 m to 2,100 m. Guided by local villagers, we carefully searched for Chinese crocodile lizards along the stream transect at a speed of 1.5 km/hour. Once we found an animal, we established the location with GPS, and recorded habitat characteristics including land scapes of: broadleaf forest, conifer forest, conifer– broadleaf mixed forest, shrub, bare land or stone, built–up land, agricultural land, and water. All of the transect streams were surveyed once; we adopted an "invisible rate" index (i) to compensate for any individuals present but not seen in a one–time survey. In one area, we conducted three consecutive time surveys on each sample transect stream with one in daytime and two in the evening. We then calcu lated the "invisible rate" at this location (table 2).

We marked the captured animals in each survey in order to distinguish them from those captured later. The total crocodile lizard population was calculated by adding the observed numbers to the estimated "invisible" animals. Data analysis The total population was estimated using the follow ing formula: N=

S [n · (1 + i)]

where N is the total population, n is the number of observed individuals in a distribution area, and i is the invisible rate in a certain distribution area. The habitat area was calculated on a map with a scale 1:10,000 by GIS (Chen et al., 2006). We incorporated hunting pressure, a human interference index, and a habitat fragmentation index to evaluate habitat quality. Hunting pressure was obtained from the questionnaire given to local people living near the habitat, with: 0. Never hunting; 1. Occasional hunting; and 2. Frequent hunting. We used the averaged value to represent the hunting pressure on the habitat. The human population in the distribution area constituted the human interference index. On a satellite map (1:10,000), we calculated the patch density index (patches/km2) and used the index to represent the extent of habitat fragmentation. Data for habitat characteristics and landscape have already been published (Ning et al., 2006; Chen et al., 2006; Yu et al., 2006).

Table 2. The calculation of invisible rate in three sample transects on three consecutive days: T1. Transect 1 (550 m); T2. Transect 2 (810 m); T3. Transect 3 (580 m); * Newly observed lizards. Tabla 2. Cálculo de la tasa de invisibles en tres transectos de muestra, en tres días consecutivos: T1. Transecto 1 (550 m); T2. Transecto 2 (810 m); T3. Transecto 3 (580 m); * Lagartos observados recientemente. First daytime

2+1*

1+1*

2+1*

Third night–time

2+1*

Total individuals

Second night–time

Average invisibility rate (i)

[(3–2)+(3–1)+(3–2)] / (2+1+2) = 0.8

Total number First survey (2+1+2) + invisible (2+1+2) × 0.8 = 9

Huang et al.

China

Hunan

8 Vietnam

4 3

Guangdong 6

2 1

Distributing area

Guangxi

Province bound County bound 0

28,000

96,000

112,000 m

Fig. 1. Present distribution of the Chinese crocodile lizard (Shinisaurus crocodilurus) in China. Numbers indicate the eight areas of distribution: 1. D&B; 2. S&L; 3. LX; 4. GX; 5. JL; 6. DG; 7. LS; 8 LK. (For abbreviations see Method of survey in Material and methods.) Fig. 1. Distribución actual del lagarto cocodrilo chino (Shinisaurus crocodilurus) en China. Las cifras indican las ocho áreas de distribución: 1. D&B; 2. S&L; 3. LX; 4. GX; 5. JL; 6. DG; 7. LS; 8. LK. (Para las abreviaturas ver Método de reconocimiento en Material y métodos.)

Results Distribution The transect surveys indicated that there are eight areas of distribution for the Chinese crocodile lizard in five Counties in Guangxi Province and one county in Guangdong (fig. 1). Wuxuan and Pingnan Counties of Guangxi Province were surveyed without finding any Chinese crocodile lizards. No sightings of croco dile lizards over the last 10 years were reported in the questionnaire for the other previously–reported areas of Xiayi in Mengshan County, Beituo and Xi anhui in Zhaoping County in Guangxi Province and Guposhan in Jianghua County in Hunan Province (Zhang, 1991). The species might already be extinct in these regions. Among the eight areas of current distribution, seven are in Guangxi Province and one is in Qujiang County in Guangdong Province. All of these local ranges are separated from each other by a minimum distance of 10 km (from S&L to D&B). The total habi tat range of crocodile lizards in China is estimated as 456.45 km2 with the biggest in JL (335.19 km2) and the smallest in GX (2.2 km2) (table 3). The total surveyed population of crocodile lizards

in China is 950. Average density is 2.08 individuals/ km2. Site JL in Zhaoping County has the largest subpopulation of 350 individuals, while LK in Qujiang County has the second largest subpopulation (220 individuals) and GX in Mengshan County has the smallest subpopulation (only 10 individuals) (table 3). LS has the highest density of Chinese crocodile liz ards (10.29 individuals/km2), while JL has the lowest (1.04 individuals/km2) (table 3). Conservation status Among these eight habitat ranges, only three are in nature reserves: LK in Luokeng Nature Reserve, LX in Dayaoshan Nature Reserve, and GX in Guxiu Nature Reserve. Less than one third of the total population is therefore protected. In the nature reserves, the habitats were protected well, but the illegal hunting activities still occurred occasionally. In other areas, the habitats were seriously damaged and illegal hunting activities happened frequently (table 1). Human population densities in these eight ranges varied greatly (table 1). The human population densi ties of LX and JL were the highest, both of them were more than 30 persons/km2. The human interference

Animal Biodiversity and Conservation 31.2 (2008)

Table 3. Subpopulation and density in different areas: Q. Qujiang county; G. Guiping County; H. Hezhou County; J. Jinxiu County; Z. Zhaoping County; M. Mengshan County. Tabla 3. Subpoblación y densidad en distintas áreas: Q. Condado de Qujiang; G. Condado de Guiping; H. Condado de Hezhou; J. Condado de Jinxiu; Z. Condado de Zhaoping; M. Condado de Mengshan.

Guangdong

Guangxi

S&L

G D&B

Subtotal

220

100

Total

350

950

Area (km2)

55.6

5.71

10.43

28.8

4.86

13.7

335.19

2.2

Density (individuals/km2)

3.96

8.76

9.59

3.47

10.29

5.11

1.04

4.54

in these two areas was therefore much higher. The DG area was not inhabited. The densities of LK, D&B and GX were less than 10 persons/km2, suggesting human interferences in these four range areas was relatively low. Surveys among the 75 local people in the vil lages who filled out the questionnaires showed that 21 hunted the lizard "frequently" and 33 "occasion ally"; only 21 men "never did" (table 1). Among the 54 people who hunted the animal, only four hunted for food and four for medicine; all others hunted the lizards to sell them for money. The price for one Chinese crocodile lizard ranged from 10 to 200 RMB, and occasionally reached 1,000 RMB. A price of 200 RMB (about U.S. $27.40) equals two–month’s average wage for one person in these remote mountain areas. This helps explain why the local people hunt the lizard. Further investigation indicates that illegal collec tion, or poaching, is the most serious threat directly contributing to the population decline. Illegal collectors were from bigger cities nearby. They sell the lizards to urban residents for use as pets, food, or medicine. A small amount of the lizards are illegally exported, bringing double or triple the price. For this reason, Taiwan has a small population of as many as 30 in dividuals since the 1980’s (personal communication with Dr. Pei Jiaqi). In addition to illegal hunting, local villagers often use electro–fishing and poisonous chemicals to fish in the stream and this can kill all of the crocodile lizards in the water. Vegetation changes contribute directly to the de crease in aquatic resources in the streams. The ideal habitat for the crocodile lizards is broadleaf forest (Zhang, 1991) which maintains water flow in streams all year round. In most altered reserve habitats, natural broadleaf forest has been gradually cut down for sale and replaced with bush forest. Where more profitable trees such as Illicium verum and tea shrubs are planted, the ground vegetation is clear–cut and fertilized. In such cases, the vegetation that withholds water disappears.

Streams then flood in the rainy season and dry out in the non–rainy season, leaving a habitat that is no longer suitable for the crocodile lizard. Mining and small–scale dam constructions also influence the survival of the crocodile lizard. Min ing pollutes the stream water. Dam construction upstream changes water distribution and some streams dry up. At present, all of these eight areas have high habitat fragmentation (table 1, fig. 1). The patch densities of LX and LS were the highest (more than 20 pieces/km2). Although the patch densities of LK and GX were lowest, both of them were higher than 2 pieces/km2. The habitat qualities in LK and GX were the best among these eight range areas, since human population densities, hunting pressures, and habitat fragmentation were relatively low. Over time, this situation will restrict migration of individuals and reduce the gene flow. Discussion Method of survey Chinese crocodile lizard population surveys have been conducted six times in China since 1978. Some were conducted during the night and the researcher argued that the lizard slept deeply and couldn’t es cape during the night, so they were easy to count (Zhang, 2002; Zeng, 2003). Others have considered that night surveying is inconvenient and poses the risk that researchers could easily miss the animal, result ing in population underestimation. Furthermore, they state that researchers have better visibility surveying in the daytime (Mo & Zou, 2000; Ning et al., 2006). We adopted the daytime survey plus an invisibility index to estimate the population. This takes advan tage of better visibility in daytime and decreases the lower count due to the escape of animals. However, without doubt we could not observe every individual in the habitat.

Huang et al.

S&L Total D&B DG,LS

JL LX

1978

1986

1988

2002

2004

Fig. 2. Population decline in the Chinese crocodile lizard in China from 1978 to 2004: * Number of individuals in GX is too small to show. (For abbreviations see Method of survey in Material and methods.) Fig. 2. Descenso de la población del lagarto cocodrilo chino en China desde el año 1978 al 2004: * El número de individuos en GX es demasiado pequeño para ser representado. (Para las abreviaturas ver Método de reconocimiento en Material y métodos.)

The survey transects were based on previous reports and local information, and some streams with crocodile lizards may not have been surveyed. In such case, the total population would be underestimated. Total population of crocodile lizards in China This survey indicates that crocodile lizard popula tions and habitat have changed greatly. In LX, where the Chinese crocodile lizard was first discovered by Ren Guorong in 1928, the 700 to 800 individuals in 1978 (Zeng, 2003) had decreased to 70 individuals in this survey, a 90% decline in population. Another important area is JL, which had 1700 individuals in 1978 (Zeng, 2003) and declined to 350 individuals in this survey, an 80% decline in population. LS and DG in Hexian County and D&B in Guiping County also suffered 70% population declines respectively (fig. 2). The complete population has decreased from 6,000 individuals in 1978 (Zeng, 2003) to 950 individuals in this survey. And the population in 1978 did not include the populations in LK and GX which had not been surveyed before 2004.

Additional information also supports the decline of crocodile lizard population observed during this survey. In DG of Hexian County, villagers said they could easily see many crocodile lizards ten years ago, but it was difficult to find them in recent years. In LK, local people also said that one could catch more than 50 individuals a day to make money five years ago, but this has been difficult in the last two years. Measurements for conservation activities In China, overexploitation is the most pervasive threat to vertebrates (Li & Wilcove, 2005); it is the same with the Chinese crocodile lizard. Illegal collectors encourage local people to hunt the animal; this is the main threat to the Chinese crocodile lizard. There fore, punishing the illegal collection or "poaching" is an urgent need. If no one can illegally trade in the lizard, local people will not catch them. Educating lo cal people to protect the animal is also important. In addition, the Chinese government should enact and enforce laws to ban the following activities: eating the Chinese crocodile lizard, using the animal for Chinese

Animal Biodiversity and Conservation 31.2 (2008)

medicine, and illegally trading this animal. If laws ban these activities and are enforced, the illegal hunting would cease accordingly. More nature reserves should be set up in the habi tat range. Among the eight areas of distribution, only three areas are included in current nature reserves. In the other five areas, most habitats had been destroyed heavily by human activities, such as forest cutting and ground vegetation replacement. Accordingly, the lizards in these streams have died or migrated due to lack of enough water. If nature reserves were set up in these areas, the forest could be protected or gradually restored and the habitats of the Chinese crocodile lizard could recover. Based on the above conservation activities, Chi nese crocodile lizards could be bred artificially in nature reserves and released back into nature to restore the wild populations. The Chinese crocodile lizard is a viviparous animal, different from many other lizards. It has a pregnancy of about nine months and gives birth once a year with an average of four young per litter (Tang & Zhang, 1986; Zhang, 2002). The survival rate in the first year of life can exceed 80% in captivity (Zhang, 2002). Chinese crocodile lizards have been bred successfully in Luokeng Nature Reserve. In 2006, one female gave birth to seven babies and another gave birth to one, suggesting that artificially breeding the crocodile lizard and then releasing the young back into nature is a good way to recover wild populations. The Chinese crocodile lizard is classified as "vul nerable" (VU). However, this study indicates that the population size in LX, JL LS and DG and other habitats have all suffered more than 70% reduction. Accord ingly, its conservation status should be promoted to "endangered level" (EN) (IUCN, http://www.iucnredlist. org/info/categories), in order to draw wider attention to the importance of conservation. Furthermore, conservation efforts for the entire population of the Chinese crocodile lizard should include populations in both China and Vietnam. Acknowledgements This research was funded by National Natural Science Foundation of China (No. 30760039). In addition, the Projects of National Forestry Administration of China, the Creative Team Project of the Universities of Guangxi, the Projects from Institute of Survey and Design of the National Forestry Administration of China, and the Excellent Youth Program of the Education Ministry of China also financially supported this study. Thanks are given to people from the six counties where the crocodile lizard is distributed who helped us to conduct the survey. We especially thank Professor Zhang Yuxia who provided us important information based on more than 20 years of study of the crocodile lizard, Dr. Pipeng Li for his valuable suggestions as we wrote this article, and Dr. John Richard Schrock from Emporia State University in the U.S.A. and Ms. Charmalie from Kyoto University, Japan who polished the English.

References Ahl, E., 1930. Beitrage zur Lurch und Kriechtierfauna Kwangsi: Section 5, Eidechsen. Sitzungsberichte der Gesellschaftder Naturforschenden Freunde zu Berlin, 1930: 326–331. Chen, Z., Huang, C. M., Li, Y. B. & Yu, H., 2006. Research on Chinese crocodile lizard landscape classification in Daguishan of Guangxi Province. Journal of Guangxi Normal University, 24(1): 83–86. [In Chinese.] Eriksson, O., 2003. Dispersal: from Bacteria to Ver tebrates. Global Ecology, 12: 261–264 Fan, T. H., 1931. Preliminary report of reptiles from Yaoshan, Kwangsi, China. Bulletin of the Department of Biology, College of Science, Sun Yatsen University, 11: 19–24. Hofmann, E. G., 2000. The Chinese crocodile lizard (Shinisaurus crocodilurus): mysterious slumber of the Mogots. Reptiles Magazine, 8(4): 60, 62–71. Hu, Q. X., Jiang, Y. M. & Zhao, E. M., 1984. Research on the taxonomy of the crocodile lizard. Acta Herpetologica Sinica, 3(1): 1–7. [In Chinese.] Li, Y. M. & Wilcove, D. S., 2005. Threats to vertebrate species in China and the United States. Bioscience, 55(2): 147–153. Li, Y. M., Wu Z. J. & Richard, P. D., 2006. Why is lands are easier to invade: human influences on bullfrog invasion in the Zhoushan archipelago and neighboring mainland China. Oecologia, 148(1): 129–136. Li, Z. C. & Xiao, Z., 2002. Discovery of Shinisaurus crocodilurus in Guangdong Province. Journal of Zoology, 37(5): 76–77. [In Chinese.] Liu, C. C. & Hu, S. Q., 1962. Preliminary report on amphibians and reptiles in Guangxi. Acta Zoological Sinica, 14(suppl): 73–104. [In Chinese.] Liu, X. H., Zhou, F. & Pan, G. P., 1989. New record of distribution of Chinese crocodile lizard. Journal of Sichuan Zoology, 8(3): 32–33. [In Chinese.] Mägdefrau, H., 1987. Zur Situation der Chine sischen Krokodilschwanz–Hockerechse, Shinisaurus crocodilurus Ahl, 1930. Herpetofauna, 9(51): 6–11. Mo, Y. M. & Zou, Y., 2000. Present status and conservation of the crocodile lizard. Journal of Northeast Forestry University, 28(6): 121–122. [In Chinese.] Ning, J. J., Huang, C. M., Yu, H., Dai, D. L., Wu, Z. J. & Zhong, Y. M., 2006. Habitat characteristics of the Chinese crocodile lizard in Luoken Nature Reserve, Guangdong, China. Zoological Research, 27(4): 419–426. [In Chinese.] Quyet, L. K. & Ziegler, T., 2003. First record of the Chinese crocodile lizard from outside of China: report on a population of Shinisaurus crocodilurus Ahl, 1930 from northeastern Vietnam. Hamadryad, 27: 193–199. Shen, L. T. & Li, H. H., 1982. Notes on the distribution and habits of the lizard Shinisaurus crocodilurus Ahl. Acta Herpetologica Sinica, 1(1): 84–85. [In Chinese.]

Sprackland, R. G., 1989. An enigmatic dragon brought to light; the Chinese crocodile lizard in captivity. Shinisaurus crocodilurus. The Vivarium, 2(2): 12–24. Tang, Z. J. & Zhang, Y. X., 1986. Breeding and young est growth observations of the Chinese crocodile lizard in captivity. Journal of Zoology, 4: 10–12. [In Chinese.] Yu, H., Huang, C. M., Wu, Z. J., Ning, J. J. & Dai, D. L., 2006. Observations on the habits of the Chinese crocodilian lizard. Sichuan Journal of Zoology, 25(2): 364–366. [In Chinese.] Zeng, Z. F., 2003. Ecology, Status and Conservation of Shinisaurus crocodilurus Ahl. M. S. Thesis, Guangxi Normal University. [In Chinese.] Zhang, Y. X., 1991. The Crocodile Lizard of China. Chinese Forestry Publishing House, Beijing.

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– 2002. Biology of the Crocodilian Lizard. Guangxi Normal University Press, Guilin. [In Chinese.] Zhang, Y. X. & Tang, Z. J., 1985. The biology of Shinisaurus crocodilurus. Acta Herpetologica Sinica, 4: 337–340. [In Chinese.] Zhang, Y. X., Chen, Z. J. & Ban, R. X., 1996. Microstructure and Chromosome Studies of the Crocodile Lizard. Guangxi Normal University Press, Guilin. [In Chinese.] Zhao, E. M., Zhao, K. T. & Zhou, K. Y., 1999. Fauna Sinica, Reptilia Vol. 2: Squamata, Lacertilia. Sci ence Press, Beijing. [In Chinese.] Ziegler, T., Quyet, L. K., Thanh, T. N., Hendrix, R., Bohme, W., 2008. A comparative study of crocodile lizards (Shinisaurus crocodilurus AHL, 1930) from Vietnam and China. The Raffles Bulletin of Zoology, 56: 181–187.

Animal Biodiversity and Conservation 31.2 (2008)

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

Normes de publicació Els treballs s'enviaran preferentment de forma electrònica (abc@bcn.cat). El format preferit és un document Rich Text Format (RTF) o DOC que inclogui les figures i les taules. Les figures s'hauran d'enviar també en arxius apart en format TIFF, EPS o JPEG. 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 investigacions originals no publicades anteriorment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors. Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el progra ma utilitzat (preferiblement en Word). Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat. ISSN: 1578–665X

El primer autor rebrà 50 separates del treball 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 científics de gèneres i d’espècies i per als neologis mes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona. Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú. Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri. Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase. Les dates s’indicaran de la forma següent: 28 VI 99 (un únic dia); 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. Serà concís, però suficientment indicador del contingut. Els títols amb designacions de sèries numèriques (I, II, III, etc.) seran acceptats previ acord amb l'editor. Nom de l’autor o els autors. Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva. Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància. Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellanoparlants. Palabras clave en castellà. © 2008 Museu de Ciències Naturals

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

studies to conservation biology: a review. Anim. Biodivers. Conserv. La relació de referències bibliogràfiques d’un 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)...". Taules. Es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista. Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3, etc. i han de ser sempre ressen yades en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels au tors. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es reprodueixen bé. Peus de figura i capçaleres de taula. Seran clars, concisos i bilingües en la llengua de l’article i en anglès. Els títols dels apartats generals de l’article (Intro ducción, Material y métodos, Resultados, Discusión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols. Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules). Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una institució pública. Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

Animal Biodiversity and Conservation 31.2 (2008)

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

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

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preparado con un procesador de textos e indican do 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 pruebas de im prenta, introducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en for mato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos de ben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado. El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofrece, sin cargo ningu no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitándose siempre la primera persona. Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común. Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo. Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase. Las fechas se indicarán de la siguiente forma: 28 VI 99 (un único día); 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. Será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designacio nes 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 esen cia del manuscrito (introducción, material, métodos, resultados y discusión). Se evitarán las especula © 2008 Museu de Ciències Naturals

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

* Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. Las referencias se ordenarán alfabéticamente por autores, cronológicamente para un mismo autor y con las letras a, b, c,... para los trabajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospecciones realizadas (Begon et al., 1999)...". Tablas. Se numerarán 1, 2, 3, etc. y se reseñarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista. Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc. y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto. Deben evitarse las figuras tridimensionales. Tanto los mapas como los dibujos deben incluir la escala. Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien. Pies de figura y cabeceras de tabla. Serán claros, concisos y bilingües en castellano e inglés. Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Dis cusión, Agradecimientos y Referencias) no se nume rarán. 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 31.2 (2008)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal published by the Natural Science Museum of Barce lona since 1958. It includes empirical and theoretical research from around the world that examines any aspect of Zoology (Systematics, Taxonomy, Morphol ogy, Biogeography, Ecology, Ethology, Physiology and Genetics). It gives special emphasis to studies related to Conservation Biology. The journal does not publish bibliographic compilations, listings, catalogues or col lections of species, or isolated descriptions of a single specimens. Studies concerning rare or protected species will not be accepted unless the authors have been granted the relevant permits or authorisation. Each annual volume consists of two issues. Animal Biodiversity and Conservation is regis tered in all principal data bases and is freely available online at http://www.bcn.cat/ABC, assuring world–wide access to articles published therein. All manuscripts are screened by the Executive Edi tor, an Editor and two independent reviewers so as to guarantee the quality of the papers. The review process aims to be rapid and constructive. Once accepted, papers are published as soon as is practicable. This is 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 or cited without acknowledging the source of information.

Manuscripts must be presented in DIN A–4 format, 30 lines, 70 keystrokes per page. Maintain double spacing throughout. 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 Cata lan, though English is preferred. The journal provides linguistic revision by an author’s editor. Care must be taken to use correct wording and the text should be written concisely and clearly. Scientific names of gen era and species as well as untranslatable neologisms must be in italics. Quotations in whatever language used must be typed in ordinary print between quota tion marks. The name of the author following a taxon should also be written in lower case letters. When referring to a species for the first time in the text, both common and scientific names should be given when possible. Do not capitalize common names of species unless they proper nouns (e.g. Iberian rock lizard). Place names may appear ei ther in their original form or in the langua ge 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 within the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence. Specify dates as follows: 28 VI 99 (for a single day); 28, 30 VI 99 (referring to two days, e.g. 28th and 30th), 28–30 VI 99 (for more than two consecu tive days, e.g. 28th to 30th). Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (abc@bcn.cat). The preferred format is DOC or RTF. All figures must be readable by Word, embedded at the end of the manuscript and submitted together in a separate attachment in a TIFF, EPS or JPEG file. Tables should be placed at the end of the document. If a printed version is sent, four copies should be for warded to the Editorial Office, together with a copy on computer disc. A cover letter stating that the article reports original research that has not been published elsewhere and 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 specify that the authors follow current norms on the protec tion of animal species and that they have obtained all relevant permits and authorisations. Authors may suggest referees for their papers. Once an article has been accepted, authors should send a paper copy and an electronic copy of the final version. 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. Must be concise but as informative as possible. Numbering of parts (I, II, III, etc.) should be avoided and will be subject to the Editor’s consent. Name of author or authors. Abstract in English, no longer than 12 typewritten lines (840 spaces), covering the contents of the article (introduction, material, methods, results and discussion). Speculation and literature citation should be avoided. The 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 relevance. 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. Should include the historical back ground of the subject as well as the aims of the paper. © 2008 Museu de Ciències Naturals

Material and methods. This section should provide relevant information on the species studied, materi als, 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 re lated 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 bibliog raphy of the publications cited in the text. References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait variation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. References must be set out in alphabetical and

chronological order for each author, adding the letters a, b, c,... to papers of the same year. Bibliographic citations in the text must appear in the usual way: "... according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the prospections that have been carried out (Begon et al., 1999)..." Tables. Must be numbered in Arabic numerals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal. Figures. All illustrations (graphs, drawings, photo graphs) should be termed as figures, and numbered consecutively in Arabic numerals (1, 2, 3, etc.) with reference in the text. Glossy print photographs, if essential, may be included. The Journal will publish colour photographs but the author will be charged for the cost. Figures have a maximum size of 15.5 cm wide by 24 cm long. Figures should not be tridimen sional. Any maps or drawings should include a scale. Shadings should be kept to a minimum and preferably with black, white or bold hatching. Stippling should be avoided as it may be lost in reproduction. Legends of tables and figures. Legends of tables and figures should be clear, concise, and written both in English and Spanish. Main headings (Introduction, Material and methods, Results, Discussion, Acknowledgements and Refer ences) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages including figures and tables. If the article describes new taxa, type material must be deposited in a public institution. Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 31.2 (2008)

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Payment method International Cheque payable to Institut de Cultura de Barcelona and drawn against a Spanish bank. Send cheque by postal mail to: Lluïsa Arroyo Dept. of Scientific Publications Museu de Ciències Naturals de Barcelona Psg. Picasso s/n. 08003 Barcelona, Spain Bank Transfer to Caixa d’Estalvis i Pensions de Barcelona ("La Caixa") IBAN: ES03 2100 3000 1422 0170 1046 Swicht code / bic code: CAIX ES BB

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

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Animal Biodiversity and Conservation 31.2 (2008)

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http://www.bcn.cat/ABC

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

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Animal Biodiversity and Conservation 31.2 (2008)

Arxius de Miscel·lània Zoològica vol. 6 (2008) 2008 Museu de Ciències Naturals ISSN: 1698–0476

Índex/Índice/Contents Martínez–Ortí, A. & Uribe, F., 2008. Los ejemplares tipo de las colecciones malacológicas del Museu de Ciències Naturals de Barcelona y del Museu Valencià d'Història Natural. Arxius de Miscel·lània Zoològica, vol. 6: 1–156. Although the International Commission on Zoological Nomenclature has recommended publishing catalogues on biological type specimens, the main reason for publishing this catalogue in our case is the practical result of assuming responsibility for our museum collections. When the arduous work of so many past and present researchers results in their entrusting our museums with these type specimens, we cannot disregard the obligation to ensure the information on these types is published in the most practical way possible. Cadevall, J., Bros, V., Hernández, E., Nebot, J., Orozco, A. & Uribe, F., 2008. Fauna malacològica de les Planes de Son i la Mata de València (Alt Àneu, Pallars Sobirà, Pirineu Català): revisió bibliogràfica i noves dades. Arxius de Miscel·lània Zoològica, vol. 6: 157–233. Abstract Fauna of molluscs from Planes de Son and Mata de València (Alt Àneu, Pallars Sobirà, Catalan Pyrenees): bibliographic survey and new data.— The survey of bibliograpic information on the presence of molluscs at the Planes de Son and Mata de València (municipality of Alt Àneu, county of Pallars Sobirà, Catalan Pyrenees) has accounted for a list of 33 species of molluscs (seven of them are slugs) inhabiting historically this area. A current field survey (2006–2007) has detected 50 species of molluscs not slugs, two of these species are splitted in two subspecies. Detailed data from both faunistic inventories are provided. Key words: Pyrenees, Fauna, Mollusca. Arechavala–López, P., Bayle–Sempere, J. T., Sánchez–Jerez, P., Valle, C., Forcada, A., Fernández–Jover, D., Ojeda–Martínez, C., Vázquez–Luis, M. & Luna–Pérez, B., 2008. Biodiversity and structure of rocky reef fish assemblages in the Sierra Helada Natural Park (South–western Mediterranean Sea). Arxius de Miscel·lània Zoològica, vol. 6: 234–256. Abstract Biodiversity and structure of rocky reef fish assemblages in the Sierra Helada Natural Park (South–western Mediterranean Sea).— In the present study the fish assemblages in the rocky–bottom habitat of the Sierra Helada Natural Park (Alicante, Spain) were recorded to provide data for future evaluation of any changes induced by long-term management. Visual censuses were carried out along strip transects by Scuba diving on rocky bottoms at depths between 1 and 32 m. In the seven localities sampled, 44 species were recorded. Number of species, abundance, biomass and size structure values recorded did not show differences between high and low protection areas. Species composition was similar to other marine protected areas of the westernMediterranean. The main differences found between localities can be attributed to the high heterogeneity and complexity of the habitat at smaller spatial scales. Key words: Fish assemblages, Rocky bottom, Biodiversity, Distribution, Visual census, Mediterranean sea.

Web: http://www.bcn.cat/arxiusMZ

All works are licensed under a Creative Commons Attribution–NonCommercial 3.0 License

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

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

Índex / Índice / Contents Animal Biodiversity and Conservation 31.2 (2008) ISSN 1578–665X

1–9 J. D. Ruiz–Ramírez & L. H. Harris Branchiosyllis salazari sp. n. (Polychaeta, Syllidae) del Caribe noroccidental y comentarios sobre el material tipo de B. exilis (Gravier, 1900) 11–23 C. A. García–Alzate & C. Román–Valencia Hyphessobrycon ocasoensis sp. n. (Teleostei, Characidae) una nueva especie para el Alto Cauca, Colombia 25–35 R. Kautenburger & A. C. Sander Population genetic structure in natural and reintroduced beaver (Castor fiber) populations in Central Europe 37–43 S. Palazón, J. Ruiz–Olmo & J. Gosálbez Autumn–winter diet of three carnivores, European mink (Mustela lutreola), Eurasian otter (Lutra lutra) and small–spotted genet (Genetta genetta), in northern Spain

45–50 L. M. Carrascal, J. Seoane & D. Palomino Bias in density estimations using strip transects in dry open–country environments in the Canar y Islands 51–62 N. Clemann, J. Melville, N. B. Ananjeva, M. P. Scroggie, K. Milto & E. Kreuzberg Microhabitat occupation and functional morphology of four species of sympatric agamid lizards in the Kyzylkum Desert, central Uzbekistan 63–70 C. M. Huang, H. Yu, Z. J. Wu, Y. B. Li, F. W. Wei & M. H. Gong Population and conservation srategies for the Chinese crocodile lizard (Shinisaurus crocodilurus) in China