Animal Biodiversity and Conservation issue 36.2 (2013) by Museu Ciències Naturals de Barcelona MCNB

2013

and

Animal Biodiversity Conservation 36.2

Dibuix de la coberta: Calotriton asper, tritó pirirenc, tritón pirenaico, Pyrenean brook salamander (Jordi Domènech) Editor en cap / Editor responsable / Editor in Chief Joan Carles Senar Editors temàtics / Editores temáticos / Thematic Editors Ecologia / Ecología / Ecology: Mario Díaz (Asociación Española de Ecología Terrestre – AEET) Comportament / Comportamiento / Behaviour: Adolfo Cordero (Sociedad Española de Etología – SEE) Biologia Evolutiva / Biología Evolutiva / Evolutionary Biology: Santiago Merino (Sociedad Española de Biología Evolutiva – SESBE) Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Russell Alpizar–Jara Univ. of Évora, Évora, Portugal Xavier Bellés Inst. de Biología Evolutiva UPF–CSIC, Barcelona, 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 Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José A. Donazar Estación Biológica de Doñana–CSIC, Sevilla, Spain Jordi Figuerola 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 Jose Martin Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Santiago Merino Museo Nacional de Ciencias Naturales–CSIC, Madrid Juan J. 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 Javier Perez–Barberia The James Hutton Institute, Scotland, United Kingdom Oscar Ramírez Inst. de Biologia Evolutiva UPF–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Ignacio Ribera Inst. de Biología Evolutiva UPF–CSIC, Barcelona, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José L. Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Carles Vilà Estación Biológica de Doñana–CSIC, Sevilla, Spain Rafael Villafuerte Inst. de Investigación en Recursos Cinegéticos (IREC–CSIC–UCLM–JCCM), Ciudad Real, Spain Rafael Zardoya Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer Assistència Tècnica / Asistencia Técnica / Technical Assistance Eulàlia Garcia Anna Omedes Francesc Uribe

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

Assessorament lingüístic / Asesoramiento lingüístico / Linguistic advisers Carolyne Newey Pilar Nuñez

Animal Biodiversity and Conservation 36.2, 2013 © 2013 Museu de Ciències Naturals de Barcelona, Consorci format per l'Ajuntament de Barcelona i la Generalitat de Catalunya Autoedició: Montserrat Ferrer Fotomecànica i impressió: XXXXXXXXX ISSN: 1578–665 X eISSN: 2014–928 X Dipòsit legal: B. 5357–2013 Animal Biodiversity and Conservation es publica amb el suport de: l'Asociación Española de Ecología Terrestre, la Sociedad Española de Etología i la Sociedad Española de Biología Evolutiva The journal is freely available online at: www.abc.museucienciesjournals.cat

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Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 (Coleoptera, Carabidae, Trechini) una especie hipogea del sur de la península ibérica. Morfología, reubicación taxonómica, sistemática y biología

V. M. Ortuño & P. Barranco

Ortuño, V. M. & Barranco, P., 2013. Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 (Coleoptera, Carabidae, Trechini) una especie hipogea del sur de la península ibérica. Morfología, reubicación taxonómica, sistemática y biología. Animal Biodiversity and Conservation, 36.2: 141–152. Abstract Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 (Coleoptera, Carabidae, Trechini) a hypogean species from the south of the Iberian peninsula. Morphology, new taxonomic placement, systematics and biology.— Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 was discovered in two new localities in the municipal district of Siles (Jaen, Spain): Sima Curva del Espino and Sima de los 30 Años, approximately 10 and 17 km, respectively, away from the type locality. The study of several individuals through dissection and use of optic and electronic microscopic preparations has increased the knowledge of the anatomy of this species. Evagination of the internal sac allowed further study of the sclerotized structures and led to the proposal of a new placement for this species within the genus Trechus Clairville 1806: Trechus (Trechus) lencinai (Mateu & Ortuño, 2006) n. comb. Although it comprises characters of the T. fulvus group and the T. pyrenaeus group, the endophallus is more similar to several species of the T. quadristriatus group and the T. tingitanus group. It could not therefore be placed in any of the species groups proposed by Jeannel. Some data about its biology (temporal and spatial distribution) and accompanying arthropod fauna are given. Key words: Duvalius, Trechus, Hypogean fauna, Taxonomy, Biology, Iberian peninsula. Resumen Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 (Coleoptera, Carabidae, Trechini) una especie hipogea del sur de la península ibérica. Morfología, reubicación taxonómica, sistemática y biología.— Se ha descubierto Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 en dos nuevas localidades del término municipal de Siles (Jaén, España): la Sima Curva del Espino y la Sima de los 30 Años, a poco más de 10 y 17 km de la localidad típo, respectivamente. El estudio de numerosos ejemplares ha posibilitado realizar numerosas disecciones, preparaciones microscópicas y un estudio de microscopía electrónica, lo que ha ampliado el conocimiento anatómico de esta especie. La aplicación de técnicas de evaginación del endofalo, ha permitido estudiar con más detalle las piezas esclerotizadas, y proponer la reubicación de esta especie dentro del género Trechus Clairville 1806: Trechus (Trechus) lencinai (Mateu & Ortuño, 2006) n. comb. Aunque esta especie presenta caracteres de los grupos T. fulvus y T. pyrenaeus, el saco interno se asemeja más al de ciertas especies de los grupos T. quadristriatus y T. tingitanus. En este sentido, la especie no ha podido ser asignada a ningún grupo de especies de los propuestos por Jeannel. Se aportan algunos datos sobre su biología (distribución temporal y espacial) y la entomofauna acompañante. Palabras clave: Duvalius, Trechus, Fauna hipogea, Taxonomía, Biología, Península ibérica. Received: 17 IV 13; Conditional acceptance: 17 V 13; Final acceptance: 10 VI 13 Vicente M. Ortuño, Depto. de Ciencias de la Vida, Fac. de Biología, Ciencias Ambientales y Química, Univ. de Alcalá, E–28871 Alcalá de Henares, Madrid, España (Spain).– Pablo Barranco, Depto. de Biología y Geología, Cite II–B, Univ. de Almería, E–04120 Almería, España (Spain). Corresponding author: Vicente Ortuño. E–mail: vicente.ortuno@uah.es ISSN: 1578–665 X eISSN: 2014–928 X

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Introducción

revelado que se trata de la especie hipogea Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006, descubierta hace pocos años en la Cueva de El Farallón (Albacete), una vecina cavidad de la Sierra de Alcaraz (distante 10.300 m de la Sima Curva del Espino y 17.800 m de la Sima de los 30 años; la distancia entre estas dos últimas es de 8.600 m, fig. 1). El estudio ha puesto de relieve determinadas peculiaridades anatómicas que permiten mejorar la descripción de la especie y justificar una nueva ubicación taxonómica.

Con la publicación del último catálogo ibérico de Carabidae (Serrano, 2003) se compilaron 97 especies de Trechini y, desde entonces, se ha incrementado el conocimiento taxonómico de esta tribu de Carabidae, describiéndose 11 nuevas especies para el ámbito ibérico, todas ellas de vida subterránea (Salgado & Peláez, 2004; Ortuño & Arillo, 2005; Ortuño & Toribio, 2005; Mateu & Ortuño, 2006; Faille et al., 2010, 2012; Reboleira et al., 2009, 2010; Faille & Bourdeau, 2011; Ortuño & Jiménez–Valverde, 2011; Faille et al., 2012). A estas adendas taxonómicas también hay que sumar las propuestas de algunas sinonimias (Ortuño & Jiménez– Valverde, 2011; Coulon et al., 2011) y cambios de estatus (Ortuño & Arribas, 2010). Probablemente, estas novedades se incrementarán en los próximos años, debido a las numerosas exploraciones bioespeleológicas que se están desarrollando en diversos enclaves kársticos del ámbito íbero–balear. En este sentido, es pertinente mencionar que recientes prospecciones entomológicas en cuevas de Andalucía, están deparando interesantes hallazgos. El objetivo de este trabajo es poner de relieve la captura, por primera vez en la Sima Curva del Espino y la Sima de los 30 Años (Siles, Jaén, España), de un Trechini que exhibe evidentes rasgos de adaptación a la vida subterránea (despigmentación del tegumento, notable regresión ocular y cierta gracilidad corporal). El elevado número de capturas (más de medio centenar) ha facilitado un estudio anatómico detallado, el cual ha

Material y métodos Se colectó entomofauna en la Sima Curva del Espino mediante muestreos estacionales distribuidos en el tiempo, desde agosto de 2009 hasta mayo de 2010. Para ello se instalaron trampas de caída, distribuidas por toda la cavidad (fig. 2), enterradas a ras en el sustrato y rellenas, hasta la mitad de su capacidad, con solución de Turquin (1.000 ml de cerveza, 10 g de hidrato de cloral, 5 ml de ácido acético y 2 ml de formol) y cebadas con sobrasada. Las trampas permanecieron activas durante un mes en cada una de las estaciones del año. El material extraído de las trampas se conservó en etanol de 70º. La temperatura y humedad de la cueva fueron tomadas en la sala media (fig. 2): la temperatura osciló entre los 8ºC (en otoño) y los 11ºC (en invierno), y la humedad relativa (RH) entre el 72% (en verano) y el 100% (en otoño).

Villaverde de Guadalimar

Cueva de El Farallón

Cotillas

Campillo

Albacete Siles

Jaén

Sima Curva del Espino

Sima de los 30 Años

6 km

Fig. 1. Localización de las tres cuevas en donde se conoce la presencia de Duvalius (Duvalius) lencinai. Fig. 1. Location of the three caves where Duvalius (Duvalius) lencinai is found.

Animal Biodiversity and Conservation 36.2 (2013)

Los muestreos aunque también fueron sistemáticos en la Sima de los 30 Años, tan sólo permitieron capturar un espécimen de D. (D.) lencinai. Por esta razón, el estudio biológico de la especie se ha centrado exclusivamente en la población muestreada en la Sima Curva del Espino (fig. 1). Se han examinado 82 especímenes de D. (D.) lencinai colectados en la Sima Curva del Espino (07 IX 09, 16 I 10, 08 V 10, 09 VIII 10, GEV leg.), un espécimen de la Sima de los 30 años (09 VIII 10, GEV leg.) y dos especímenes (paratipos) de la Cueva de El Farallón. Como material de comparación se ha estudiado Trechus (Trechus) quadristriatus (Schrank, 1781): 10 especímenes de Laguna Grande de Beleña (Beleña, Guadalajara); T. (Trechus) fulvus Dejean, 1831: seis especímenes de Cueva PB4 (Peal de Becerro, Jaén); T. (Trechus) planipennis Rosenhauer, 1856: cinco especímenes de Corral del Veleta (Güejar Sierra, Granada). Los especímenes de D. (D.) lencinai que han servido para este estudio están depositados en la colección Vicente M. Ortuño, Universidad de Alcalá (Madrid, España), salvo dos especímenes que han sido depositados en el Museo Nacional de Ciencias Naturales (Madrid), dos en el Museu de Ciències Naturals de Barcelona y otros dos en la colección Paolo Magrini (Florencia, Italia). Las piezas diseccionadas, entre ellas el edeago (en posición dorsal y lateral) y la genitalia femenina, han sido preparadas en pequeñas láminas transparentes de acetato, utilizando una resina hidrosoluble (dimetil hidantoína formaldehido, DMHF). El complejo espermatecal se tiñó con Negro de Clorazol y posteriormente fue aclarado dos veces, la primera con una solución de KOH, y la segunda con solución de Scheerpeltz (60% etanol, 39,5% agua destilada, 0,5% ácido acético). Otras estructuras anatómicas han sido deshidratadas y se han metalizado con oro, para su observación, y fotografiado, a microscopía electrónica de barrido (SEM). Todas las mediciones de los especímenes se han realizado utilizando un estereomicroscopio con ocular calibrado. Resultados Anatomía Longitud (desde el ápice de las mandíbulas hasta el ápice de los élitros): 3,73–4,80 mm (ver tabla 1). Aunque en la descripción original de D. (D.) lencinai se hace referencia a ojos vestigiales (un pequeño resto de ojo visible con microscopía óptica), el estudio con microscopía electrónica muestra la superficie del área ocular sin cicatrices ni vestigios de omatidios (fig. 3E). Por lo tanto, la observación realizada con microscopía óptica quizá se corresponda con una estructura subcuticular y, por tanto, observable sólo por transparencia. El resto de la descripción original se completa con los detalles siguientes. Cabeza (figs. 4A, 4C) con las sienes provistas de microsetas dispersas (fig. 3E). Microescultura del disco cefálico con forma de malla poligonal isodiamétrica

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12 11

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Fig. 2. Topografía de la Sima Curva del Espino, (Siles, Jaén). Ubicación de los puntos de muestreo (numerados). Fig. 2. Topography of the Sima Curva del Espino, (Siles, Jaén). Location of the sampling points (numbered).

(fig. 3F). Escotadura del labio con un diente levemente bífido y dos setas sobre el área discal, las cuales están acompañadas por sendas foveolas multiperforadas (figs. 4A, 4B) de carácter sensorial. Área prebasilar provista de seis setas que jalonan toda la estructura (fig. 4A). Cuatro últimos antenómeros (VIII–XI) provistos de poros quimiorreceptores (figs. 3A, 3B, 3C, 3D) del tipo "sensilla ampullacea". Microescultura del disco pronotal de tipo transversal (fig. 5C). Alas extremadamente reducidas, constituyendo diminutos muñones (figs. 5A, 5B). Protibias visiblemente pilosas, tanto en la superficie dorsal como ventral (figs. 5D, 5E). Escotadura del órgano limpiador protibial provista de dos largas setas clip (fig. 5D). Mesotibia con la superficie externa muy pilosa y el órgano limpiador dispuestos en forma de peine (fig. 5F). Élitros con interestrías poco convexas, y todas las estrías marcadas, aunque como ya se apuntó en la descripción original, las estrías externas se muestran algo más tenues (fig. 6A). Disco elitral con microescultura transversa, tanto en machos como en

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Tabla 1. Valores de longitud (L, en mm) y anchura (A, en mm) máximas, utilizados en el análisis morfométrico de 47 especímenes de Duvalius (Duvalius) lencinai. Table 1. Maximum lengths (L, in mm) and widths (A, in mm) used in the morphometric analysis of 47 specimens of Duvalius (Duvalius) lencinai.

Machos L

Hembras

4,586

1,717

4,478

1,717

4,521

1,760

4,369

1,608

4,695

1,717

4,717

1,760

4,652

1,804

3,739

1,326

4,086

1,500

4,434

1,608

4,521

1,695

4,739

1,804

4,413

1,630

4,413

1,695

4,521

1,695

4,478

1,630

4,434

1,717

4,413

1,608

4,304

1,630

4,043

1,456

4,478

1,565

4,043

1,478

4,456

1,739

4,065

1,478

4,086

1,500

4,500

1,652

4,347

1,652

4,304

1,652

4,413

1,630

4,260

1,478

4,500

1,695

4,239

1,478

4,804

1,804

4,413

1,673

4,782

1,782

3,934

1,413

4,630

1,782

4,521

1,673

4,326

1,630

4,043

1,521

4,434

1,739

4,304

1,586

–

4,434

1,630

–

4,260

1,586

–

4,130

1,500

–

4,391

1,565

–

4,369

1,543

–

4,043

1,521

hembras (fig. 6B). Superficie ventral del élitro tapizada por formaciones cuticulares de aspecto cónico, no articuladas en la base, que podrían englobarse bajo la categoría de microtriquias (fig. 6C, 6D). La descripción original de la genitalia masculina indica lo siguiente: "la pieza del saco interno es alargada, subparalela, redondeada por delante y bífida por detrás; muestra una placa de escamas esclero-

tizadas y una nube de éstas en la parte anterior del saco" (Mateu & Ortuño, 2006). Sin embargo, ahora hemos observado que el endofalo contiene dos piezas esclerotizadas alargadas, laminares y subsimétricas que, tanto invaginadas como evaginadas, se disponen paralelas al plano sagital de simetría (figs. 7A, 7B, 7C). La parte membranosa del saco interno, una vez evaginada, constituye un tubo ancho que reúne las superficies escamosas (fig. 7C), las cuales se observan como áreas más o menos dispersas cuando el saco interno se halla invaginado (fig. 7A). Normalmente el dimorfismo sexual en los Trechini se manifiesta de forma evidente por la dilatación de los primeros tarsómeros de los protarsos masculinos, lo que sucede en D. (D.) lencinai. Menos frecuente es observar otros tipos de manifestaciones de dimorfismo sexual, como la mayor o menor curvatura de las tibias, la microescultura y micropunteaduras distintamente marcadas sobre el tegumento, o incluso la ausencia o presencia de pubescencia, según se trate de un sexo u otro (Ortuño & Novoa, 2011). Igual ocurre con la diferencia de tamaño corporal, como sucede en la especie ibérica Trechus jeannei Sciaky, 1998. En este sentido, se apuntó en la descripción original de D. (D.) lencinai, que "los machos estudiados muestran un mayor tamaño (4,65–4,75 mm) que las hembras (3,75–4,20 mm)". El elevado número de individuos que hemos estudiado ahora de D. (D.) lencinai indica que, si bien los especímenes más pequeños son hembras, su rango de variación se solapa ampliamente con el de los machos (tabla 1, fig. 8), lo que permite descartar que exista este tipo de dimorfismo sexual en D. lencinai. Biología Al final del periodo anual de muestreo en la Sima Curva del Espino se colectaron 2.481 especímenes de artrópodos (fig. 9), de los que el 53% fueron Diptera, mayoritariamente Phoridae y, en menor número, Sciaridae. Ello hace suponer que hay un aporte muy notable de nutrientes para la biocenosis de la cavidad. Los cadáveres de imagos y larvas que resultan de la eclosión de puestas realizadas sobre detritus, pueden formar parte de la dieta saprófaga–depredadora de este Trechini y de otros artrópodos con los que convive. La aparición de Hymenoptera es testimonial a nivel cuantitativo (cinco especímenes) y especialmente anecdótica, dado los hábitos parasitoides que ligan su aparición a la presencia de estos Diptera. El segundo grupo en importancia lo componen los Diplura Campodeidae con el 23%, representado por Plusiocampa lagari Sendra & Condé, 1987 (especie también presente en la Cueva del Farallón, localidad típica de D. lencinai) que, junto con los Collembola (10% de la fauna colectada), constituyen, posiblemente, la principal fuente de alimento de este Trechini hipogeo. Los Coleoptera Staphylinidae con un 7% y los Acari Gamasida con un 3%, dado su carácter depredador, suponen un notable factor de competencia para este Trechini, e incluso un riesgo de depredación al menos en los estadios preimaginales. Por último, los Orthoptera Gryllidae son muy escasos y representan menos del 1% con una sola especie, Petaloptila mogon Barranco, 2004.

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Fig. 3. Imágenes SEM de detalles de Duvalius (Duvalius) lencinai: A, B, C, D. Antenómeros XI, X, IX y VIII, respectivamente (se observan áreas porosas por la presencia de varias "sensilla ampullacea"); E. Área ocular, mejilla y sien; F. Microescultura del disco cefálico. Fig. 3. SEM images of details of Duvalius (Duvalius) lencinai: A, B, C, D. Antennomeres XI, X, IX and VIII respectively (porous areas due to the presence of several 'sensilla ampullacea' are observed); E. Ocular area, gena and temple; F. Microsculpture of the cephalic disk.

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Fig. 4. Imágenes SEM de detalles de Duvalius (Duvalius) lencinai: A. Labio, prebasilar, lígula y piezas de apéndices bucales; B. Foveola multiperforada de la superficie labial; C. Área anterior de la cabeza en vista dorsal. Fig. 4. SEM images of details of Duvalius (Duvalius) lencinai: A. Labium, prebasilar, ligula and oral appendages; B. Multiperforated foveola of the labial surface; C. Anterior area of the head in dorsal view.

La distribución espacial de D. lencinai en la Sima Curva del Espino es heterogénea en relación a los tres niveles o salas que presenta la cavidad (fig. 2). La mayor densidad de imagos se observó en la sala superior (–15 m), con más del doble de especímenes

capturados que los de la sala media (–30 m): 51 especímenes frente a 23. En la sala más profunda (–40 m) no se capturó ningún espécimen. La distribución temporal indica, de acuerdo con los muestreos estacionales, que hay un máximo pobla-

Animal Biodiversity and Conservation 36.2 (2013)

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Fig. 5. Imágenes SEM de detalles de Duvalius (Duvalius) lencinai: A. Región meso–metatorácica desprovista de los élitros; B. Ala vestigial (izquierda); C. Microescultura del disco pronotal; D. Extremo distal de la protibia en vista dorsal, a la altura del órgano limpiador protibial; E. Extremo distal de la protibia en vista ventral; F. Mesotibia con el órgano limpiador visible en el extremo distal. Fig. 5. SEM images of details of Duvalius (Duvalius) lencinai: A. Meso–metathoracic region without elytra; B. Vestigial wing (left); C. Microsculpture of the pronotal disk; D. Distal end of the protibia in dorsal view, at the level of the protibial cleaning organ; E. Distal end of the protibia in ventral view; F. Mesotibia with the cleaning organ at the distal end.

cional en otoño (fig. 10), tanto en la sala alta como en la media, con un promedio de cinco ejemplares/ trampa en la primera y de 2,02 en la segunda, y máximos de ocho y seis ejemplares/trampa, respec-

tivamente. La tónica general en la cavidad es que, no sólo D. lencinai sino también otros Arthropoda (por ejemplo Staphylinidae, Collembola y Acari), con excepción de Plusiocampa lagari, presentan máximos

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Fig. 6. Imágenes SEM de detalles de Duvalius (Duvalius) lencinai: A. Élitro en vista dorsal; B. Microescultura del disco elitral; C. Élitro en vista ventral; D. Microtriquias cónicas dispuestas sobre la superficie ventral de los élitros. Fig. 6. SEM images of details of Duvalius (Duvalius) lencinai: A. Elytron in dorsal view; B. Microsculpture of the elytral disk; C. Elytron in ventral view; D. Conical microtrichia arranged on the ventral surface of elytra.

poblacionales en otoño, los cuáles van decreciendo hasta la primavera–verano, cuando los efectivos son mínimos (fig. 10). Discusión El estudio con microscopía electrónica sin duda ha contribuido a revelar una serie de detalles anatómicos que amplían el conocimiento de Duvalius lencinai. El análisis del edeago evaginado ha aportado una información valiosa sobre la forma que tienen las piezas internas y de su orientación espacial. En este sentido, cabe destacar que en la descripción original se interpretó que eran piezas no del todo laminares y, por tanto, sujetas a mostrar cierto volumen y que, además, estaban dispuestas perpendicularmente al plano sagital (característica incompatible con su posible asignación al género Trechus). La nueva especie se

consideró además perteneciente al género Duvalius porque presenta, y en este trabajo se ha comprobado con microscopía electrónica, pilosidad en la mitad distal–dorsal de las protibias (fig. 5D), característica muy bien afianzada en el género y que, con frecuencia, ha sido utilizada para facilitar la discriminación entre éste y Trechus. Sin embargo, en Trechus, la expresión del carácter "tegumento pubescente" no es exclusivamente un rasgo cualitativo, sino también cuantitativo (Ortuño & Jiménez–Valverde, 2011), por lo que la presencia de pilosidad en las protibias no puede ser considerada como una característica totalmente ajena al mismo. En suma, si se atiende a la configuración detallada de las piezas del saco interno del edeago que hemos observado en este trabajo y a su disposición espacial, se justifica la reubicación de D. (D). lencinai en el género Trechus, ya que las dos piezas laminares son paralelas entre sí y, a su vez, paralelas al plano sagital (figs. 7B, 7C). Este modelo anatómico del

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Fig. 7. Edeagos de Duvalius (Duvalius) lencinai (A, B, C) y de Trechus (Trechus) quadristriatus (D, E, F): A, D. Con el saco interno invaginado; B, E. Con el saco interno evaginado; C, F. Detalle del saco interno evaginado. Fig. 7. Aedeagus of Duvalius (Duvalius) lencinai (A, B, C) and Trechus (Trechus) quadristriatus (D, E, F): A, D. With the internal sac invaginated; B, E. With the internal sac evaginated; C, F. Detail of the internal sac evaginated.

1,8

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● males; ○ females.

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Acari 82, 3% Hymenoptera Orthoptera 2, 0% Larvas Coleoptera 5, 0% 11, 1% Diplura 576, 23%

Coleoptera Staphylinidae 183, 7% Coleoptera Carabidae 74, 3% Collembola 241, 10%

Diptera 1.307, 53%

Fig. 9. Número de ejemplares y porcentaje de los grupos faunísticos recogidos en la Sima Curva del Espino, en cuatro muestreos estacionales realizados en 12 meses. Fig. 9. Number of specimens and percentage of faunal groups collected in the Sima Curva del Espino, with four seasonal samplings taken over 12 months.

saco interno es del mismo tipo que el que manifiesta Trechus quadristriatus (Schrank, 1781) (figs. 7D, 7E, 7F). Por ello, Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 debe ser reubicada sistemáticamente dentro del género Trechus, y nominarse del siguiente

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modo: Trechus (Trechus) lencinai (Mateu & Ortuño, 2006) (nov. comb.). Posicionar a T. (T.) lencinai en la sistemática de "grupos de especies" propuesta por Jeannel (1927) no resulta fácil. Obviando algunos caracteres del

Trechus lencinai n. comb. Plusiocampa lagari

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Fig. 10. Distribución temporal de Duvalius (Duvalius) lencinai en la Sima Curva del Espino, junto con otros grupos faunísticos. Fig. 10. Temporal distribution of Duvalius (Duvalius) lencinai in the Sima Curva del Espino, along with other faunal groups.

Animal Biodiversity and Conservation 36.2 (2013)

edeago, T. (T.) lencinai podría atribuirse al grupo de Trechus fulvus, cuyas especies presentan los siguientes caracteres: a) tibias anteriores netamente surcadas sobre la cara externa; b) pronoto con la base no surcada transversalmente y la superficie basal deprimida en torno a las fosetas, y los ángulos posteriores moderadamente obtusos con el vértice vivo (no redondeados); c) élitros con dos poros discales y todas las estrías marcadas, así como la estría apical recurrente prolongada ininterrumpidamente con el final de la 5ª estría; d) tarsos posteriores normalmente conformados; e) órgano copulador robusto, provisto de un gran alerón sagital y un saco interno armado con dos piezas esclerotizadas. Sin embargo, T. (T.) lencinai no encaja del todo en este grupo ya que presenta las estrías externas menos profundas que las internas, y lo que aún resulta más relevante, por la especial configuración de las dos piezas internas del edeago. Estas estructuras son laminares y subsimétricas, mientras que las típicas del citado grupo son cóncavas, a modo de valvas, siendo la derecha de una forma muy particular (más o menos triangular y afilada en punta saliente y recurvada). Otra posibilidad, quizá más verosímil que la ya expuesta, es que T. (T.) lencinai pertenezca al grupo de Trechus pyrenaeus, en el que también se halla otra especie geográficamente próxima, T. planipennis, que es orófila y endémica de Sierra Nevada (Granada–Almería). La ubicación de T. (T.) lencinai en este grupo vendría avalada por las características anteriormente mencionadas para el grupo de T. fulvus, a las que habría que añadir otras dos más: a) impresión más leve de las estrías externas de los élitros; b) margen basal de los élitros oblicuo. Sin embargo, al igual que en el supuesto anterior, las piezas del saco interno del edeago difieren notablemente de las del grupo de Trechus pyrenaeus, en el que de las dos piezas, la derecha es afilada y en su extremo apical se recurva dorsalmente. Por último, obviando cualquier característica de morfología externa, y atendiendo exclusivamente a similitudes en las características del saco interno, hay dos conjuntos de especies cuyos edeagos muestran ciertas similitudes. Por un lado está el grupo de Trechus quadristriatus (ver figs. 7D, 7E, 7F) y por otro el de Trechus tingitanus. No obstante, estas similitudes son parciales y, basándose únicamente en caracteres anatómicos, no es posible asignar esta especie a ninguno de los grupos propuestos por Jeannel (1927). Sin embargo, a pesar de todo lo expuesto, atendiendo a resultados moleculares aún inéditos, todo apunta a que T. (T.) lencinai pertenece al grupo de Trechus fulvus (Faille et al., com. pers.). Agradecimientos Deseamos expresar nuestro agradecimiento a Toni Pérez y a los integrantes del grupo espeleológico de Villacarrillo (GEV) quienes, siguiendo las directrices del contrato "Servicio para el estudio de los invertebrados cavernícolas de Andalucía", muestrearon la Sima Curva del Espino a lo largo de un año y nos facilitaron

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información topográfica de la cavidad. Igualmente, a Esmeralda Urea de la Unidad de Servicios Técnicos de la Universidad de Almería por la realización de las fotografías SEM, y a José D. Gilgado quien tuvo la amabilidad de realizar la fotografía de uno de los imagos que ahora ilustra este trabajo. A Paolo Magrini y a Achille Casale por la ayuda prestada en consultas de carácter taxonómico. Por último, a Arnaud Faille por proporcionarnos información inédita sobre biología molecular de esta especie. El proyecto de muestreo ha sido subvencionado con fondos FEADER y de la Consejería del Medio Ambiente de la Junta de Andalucía. Este trabajo también ha podido desarrollarse por la financiación obtenida a partir del programa I3 del Ministerio de Educación y Ciencia de España, para la “Incentivación de la Incorporación e Intensificación de la Actividad Investigadora”, del que es beneficiario V. M. Ortuño. Referencias Coulon, J., Pupier, R., Quéinnec, E., Ollivier, E. & Richoux, Ph., 2011. Coléoptères Carabiques, compléments et mise à jour. Volume 1. Fédération Française des Sociétés de Sciences Naturelles, Paris. Faille, A. & Bourdeau, C., 2011. Une nouvelle espèce de Trechinae troglobie du versant sud des Pyrénées (Coleoptera, Carabidae, Trechinae). Bulletin de la Société entomologique de France, 116(3): 261–267. Faille, A., Bourdeau, C. & Fresneda, J., 2010. A new species of blind Trechinae from the Pyrenees of Huesca, and its position within Aphaenops (sensu stricto) (Coleoptera: Carabidae: Trechini). Zootaxa, 2566: 49–56. – 2012. Molecular phylogeny of the Trechus brucki group, with description of two new species from the Pyreneo–Cantabrian area (France, Spain) (Coleoptera, Carabidae, Trechinae). ZooKeys, 217: 11–51. Jeannel, R., 1927. Monographie des Trechinae. Morphologie comparée et distribution géographique d’un groupe de Coléoptères. (Deuxième Livraison). L’Abeille, 33: 1–592. Mateu, J. & Ortuño, V. M., 2006. Descripción de un nuevo Duvalius Delarouzée, 1859 de la Península Ibérica (Coleoptera, Carabidae, Trechinae). Boletín de la Asociación española de Entomología, 30(1–2): 73–81. Ortuño, V. M. & Arillo, A., 2005 Description of a new hypogean species of the genus Trechus Clairville, 1806 from eastern Spain and comments on the Trechus martinezi–lineage (Coleoptera: Adephaga: Carabidae). Journal of Natural History, 39(40): 3483–3500. Ortuño V. M. & Arribas, O., 2010. Clarification of the status of Trechus comasi Hernando (Coleoptera: Carabidae: Trechini) from the Iberian Peninsula and its taxonomic position. The Coleopterists Bulletin, 64: 73–74. Ortuño, V. M. & Jiménez–Valverde, A., 2011. Taxonomic notes on Trechini and description of a new

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hypogean species from the Iberian Peninsula (Coleoptera: Carabidae: Trechinae). Annales de la Société Entomologique de France (n.s.), 47(1–2): 21–32. Ortuño, V. M. & Novoa, F., 2011. A New Species of Trechus from the Ethiopian Highlands (Coleoptera: Carabidae: Trechinae) and Key to the Trechus Species of Ethiopia. Annals of the Entomological Society of America, 104(2): 132–140. Ortuño, V. M. & Toribio, M., 2005. Descripción de un nuevo Trechus clairville, 1806 (Coleoptera, Carabidae, Trechini) de los Montes Cantábricos orientales (norte de España). Graellsia, 61(1): 115–121. Reboleira, A. S. P. S., Gonçalves, F. J. & Serrano, A. R. M., 2009. Two new species of cave dwelling Trechus Clairville, 1806 of the fulvus–group (Coleoptera,

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Carabidae, Trechinae) from Portugal. Deutsche Entomologische Zeitschrift, 56(1): 101–107. Reboleira, A. S. P. S., Ortuño, V. M., Gonçalves, F. & Oromí, P., 2010. A hypogean new species of Trechus Clairville, 1806 (Coleoptera, Carabidae) from Portugal and considerations about the T. fulvus species group. Zootaxa, 2689: 15–26. Salgado, J. M. & Peláez, M. C., 2004. Un nuevo tréquido cavernícola del carst asturiano: Apoduvalius (Apoduvalius) anseriformis n. sp. (Coleoptera: Carabidae). Fragmenta entomologica, 36(1): 33–41. Serrano, J., 2003. Catálogo de los Carabidae (Coleoptera) de la Península Ibérica. Monografías S.E.A., nº 9. Sociedad Entomológica Aragonesa. Zaragoza.

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Exotic tree plantations and avian conservation in northern Iberia: a view from a nest–box monitoring study I. de la Hera, J. Arizaga & A. Galarza

De la Hera, I., Arizaga, J. & Galarza, A., 2013. Exotic tree plantations and avian conservation in northern Iberia: a view from a nest–box monitoring study. Animal Biodiversity and Conservation, 36.2: 153–163. Abstract Exotic tree plantations and avian conservation in northern Iberia: a view from a nest–box monitoring study.— The spread of exotic tree plantations on the North Atlantic coast of the Iberian peninsula raises concern regarding the conservation of avian biodiversity as current trends suggest this region might become a monoculture of Australian Eucalyptus species. To shed more light on the factors promoting differences in avian communities between and within exotic tree (Monterey Pine Pinus radiata and Eucalyptus spp.) plantations and native forests in the Urdaibai area (northern Spain), this study aimed to explore (1) how the type of habitat and vegetation characteristics affect bird species richness and the settlement of some particular species during the breeding period, (2) if some reproductive parameters (i.e. egg–laying date and clutch size) vary among habitats in a generalist bird species (the Great Tit Parus major), and (3) the existence of differences among habitats in the abundance of a key food resource on which some insectivorous birds are expected to rely upon for breeding (i.e. caterpillars). Our results confirmed that Eucalyptus stands house the poorest bird communities, and identified understory development as an important determinant for the establishment of titmice species. Furthermore, we found that exotic trees showed lower caterpillar abundance than native Oak trees (Quercus robur), which might contribute to explain observed differences among habitats in bird abundance and richness in this region. However, we did not find differences among habitats in egg–laying date and clutch size for the Great Tit, suggesting that the potential costs of breeding in exotic tree plantations would occur in later stages of the reproductive period (e.g. number of nestlings fledged), a circumstance that will require further research. Key word: Bird diversity, Planted forests, Land–use changes, Linear mixed models, MAB Biosphere reserve, Iberian peninsula. Resumen Plantaciones de árboles exóticos y conservación de la avifauna en el norte de la península ibérica: perspectiva de un estudio de seguimiento de cajas nido.— La expansión de plantaciones de árboles exóticos en la costa can� tábrica de la península ibérica suscita preocupación por la conservación de la biodiversidad de aves, puesto que las tendencias actuales sugieren que esta región podría convertirse en un monocultivo de especies de eucalipto australiano. Para arrojar más luz sobre los factores que promueven las diferencias en las comunidades de aves entre y dentro de las plantaciones de árboles exóticos (pino de Monterrey Pinus radiata y Eucalyptus spp.) y los bosques nativos de la zona de Urdaibai (norte de España), el objetivo del presente estudio consistió en analizar (1) la forma en que el tipo de hábitat y las características de la vegetación afectan a la riqueza de especies de aves y el asentamiento de determinadas especies durante el período de cría; (2) si algunos parámetros reproductivos (p.ej. la fecha o el tamaño de puesta) varían entre los hábitats en una especie de ave generalista (el carbonero común, Parus major); y (3) la existencia de diferencias entre hábitats por lo que hace a la abundancia de una fuente clave de alimento de la que se prevé que las aves insectívoras dependan para la cría (las orugas). Nuestros resultados confirmaron que las poblaciones de eucalipto albergan las comunidades más pobres de aves y establecieron el desarrollo del sotobosque como un factor importante para el establecimiento de las especies de páridos. Asimismo, hallamos que los árboles exóticos presentaban una abundancia de orugas menor que la de los robles nativos (Quercus robur), lo que podría contribuir a explicar las diferencias observadas entre los hábitats en cuanto a la abundancia y la riqueza de aves de esta región. No obstante, no se hallaron diferencias entre los hábitats por lo que concierne a la fecha y el tamaño de puesta para el carbonero común, lo que sugiere que los posibles costes de criar en plantaciones de árboles exóticos se producirían en etapas posteriores del periodo reproductivo (p.ej. el número de pollos emplumados), una circunstancia que habrá que seguir investigando. ISSN: 1578–665 X eISSN: 2014–928 X

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Palabras clave: Diversidad de aves, Bosques plantados, Cambio del uso de la tierra, Modelos lineales mixtos, Reserva de la biosfera del MAB, Península ibérica. Received: 2 III 13; Conditional acceptance: 10 IV 13; Final acceptance: 19 VI 13 Iván de la Hera, Depto. de Zoología y Biología Celular Animal, Fac. de Farmacia, Univ. del País Vasco (UPV/ EHU), Paseo de la Universidad 7, 01006 Vitoria–Gasteiz, España (Spain).– Juan Arizaga, Urdaibai Bird Center. Sociedad de Ciencias Aranzadi, Orueta 7, 48314 Gautegiz–Arteaga, Bizkaia, España (Spain).– Aitor Galarza, Depto. de Agricultura, Diputación Foral de Bizkaia, 48014 Bilbao, España (Spain). Corresponding author: I. de la Hera. E–mail: idelahera@bio.ucm.es

Animal Biodiversity and Conservation 36.2 (2013)

Introduction Increasing human demands for wood and its by–pro� ducts (e.g. paper) in contemporary time (Ajani, 2011), and greater concern over the loss of natural forests, particularly in tropical regions (Gibson et al., 2011), have favoured commercial forest plantations as a main source of timber supply (Barlow et al., 2007; Brockerhoff et al., 2008). As a consequence of their profitability, forest plantations are replacing other land uses of decli� ning economic yield (such as pastures and agricultural lands; Sohngen et al., 1999). This shift in land use is dramatically changing the socio–economic context and the landscape of many regions, with potential effects on biodiversity worldwide (Foley et al., 2005; Bremer & Farley, 2010; Felton et al., 2010). Planted forests now cover more than 264 million hectares around the world (i.e. 7% of the global forest area), and they are expanding at a rate of five million hectares per year (FAO, 2010). In spite of the growing generalization of this land use, we still have a limited understanding of the consequences of plantations on biodiversity and other ecosystem services (Louzada et al., 2010). Such circumstances restrict our ability to design sustainable management policies to preserve native flora and fauna and improve habitat quality in these exploited areas (Hartley, 2002; Brockerhoff et al., 2008). The spread of stands of the non–native Monterey Pine (Pinus radiata, of North–American origin) and Eucalyptus species (mainly Eucalyptus globulus, native of Australia and Tasmania) have transformed the landscape of the Atlantic coast of Northern Iberia, where the original view just a century ago showed a mosaic of farmlands interspersed with hedges and coppices of natural vegetation (Lautensach, 1964). In recent decades, exotic tree plantations have progres� sively replaced pastures and farmlands (most of them devoted to hay production) that constitute a declining traditional activity (GV, 2005; Santos et al., in press). From the description of the bird communities of the different habitats present in Northern Iberia, several studies have raised concern about the proliferation of plantations, since they house fewer, and more generalist bird species than farmlands and natural forests (Bongiorno, 1982; Tellería & Galarza, 1990; Proença et al., 2010). Such circumstances suggest that the above–mentioned landscape modifications are impoverishing regional avifauna and probably the communities of other taxonomic groups (Proença et al., 2010; Calvino–Cancela et al., 2012). This situation may be aggravated even more as a consequence of the current drop in the prices of pine wood, since many foresters now prefer Eucalyptus plantations, which are by far the poorest habitat with regard to avian communities (Pina, 1989; Tellería & Galarza, 1990). Observed differences among habitats in avian ri� chness suggest that exotic tree plantations could set limits to the local distribution of some bird species. Understanding the mechanisms responsible for these patterns could help us to design recommendations to increase biodiversity in plantations (Hartley, 2002). For this purpose, it is necessary to explore how variation in some important characteristics of plantations, which are

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susceptible to be managed (e.g. vegetation structure), can affect avian communities, an issue that has barely been tackled in this region. At a more detailed scale, another issue that remains to be addressed is to know how generalist bird species perform in commercial plantations and are able to persist in these habitats. The study of the ecology of these widely–distributed species, and the comparison among habitats of some relevant parameters (e.g. breeding performance, body condition) might help to understand the observed variation in their abundance, as well as the potential causes that are constraining the occurrence in plan� tations of other more ecologically–demanding species (Carrascal & Tellería, 1990; Tellería & Galarza, 1990; Proença et al., 2010). In this study, we explored how habitat type and vegetation structure can affect species richness and the settlement of birds during reproduction in a study site located in northern Spain. We performed bird counts and monitored nest–boxes in seven localities representing the three main forest habitats of the area (natural Oak forests, and Pine and Eucalyptus plantations). We also analysed how some breeding parameters (egg–laying date and clutch size) varied in the Great Tit Parus major, a generalist species occurring at lower densities in plantations (Tellería & Galarza, 1990). Given that breeding success in the Great Tit and other species may depend on particular food resources (i.e. defoliating caterpillars; Visser et al., 2006; Wilkin et al., 2009), we also estimated cater� pillar abundance, which is expected to differ between natural forests and exotic tree plantations, because a number of native phytophagous arthropods might be unable to thrive in the latter (Kolb, 1996). With this approach, our goal was to go one step forward in this research topic and shed additional light on the mechanistic factors that might be promoting variation in bird abundance and composition in plantations and natural forests in Northern Iberia. Methods Study area and nest–box study design Fieldwork was carried out in the UNESCO–MAB Bios� phere Reserve of Urdaibai (Bizkaia province, Basque Country, Spain) and some surrounding municipalities (i.e. Bakio, Ereño and Ea). The study site is located within the North Atlantic coast of Iberia, an area where it is possible to find farmlands, Pine and Eucalyptus plantations, and a few remnants of natural Oak Quercus robur forest. This latter formation constitutes the climax forest ecosystem that would develop in many of the areas currently occupied by farmlands and exotic trees (Loidi et al., 2009). During mid–February 2012, we installed 212 nest–boxes in seven localities. These localities were not randomly selected but were previously identified as large enough to house at least 20 nest–boxes. Large patches of forest are rare in this region, which is characterized by the presence of a complex mosaic of small private plots that are normally devoted to

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different land–uses. Selected localities represented the three main wooded habitats of the region: three plots of Eucalyptus plantations in Jata (denoted as Euc–1 in the figures; 43º 24.855' N, 02º 51.778' W), Ea (Euc–2; 43º 22.063' N, 02º 35.649' W) and Mañu (Euc–3; 43º 24.744' N, 02º 47.041' W); three plots of Pine plantations in Arteaga (Pinus–1; 43º 21.595' N, 02º 39.633' W), Ereño (Pinus–2; 43º 20.739' N, 02º 36.783' W) and Matxitxako (Pin� us–3; 43º 26.434' N, 02º 44.888' W); and one Oak forest in Arratzu (Oak; 43º 17.767' N, 02º 38.236' W), the only forest in the area that was large enough to hold a reasonable number of nest–boxes. Within each locality, nest–boxes were hung from a nail hammered into the tree trunk at about 3.5 m height and separated approximately 50 m from each other. However, we finally considered a reduced subset of nest–boxes (n = 186), because 26 disappeared during the course of the study, with between 18 and 42 nest–boxes remaining per site (see fig. 2A). Nest–boxes were checked regularly (at least once per week) from early April to late June to determine the laying date of the first egg (assuming a production of one egg per day) and clutch size of the nest–boxes occupied by birds. Although we were particularly interested in obtaining measurements of chicks’ body condition, we failed in this purpose because anomalous bad weather con� ditions in May caused the death of recently hatched chicks or, less frequently, clutch desertion. In the end, only 32 chicks from eight Great Tit broods were able to fledge (from two to six fledglings per brood). Bird counts, vegetation structure and estimation of caterpillar abundance In mid–May, we also established 10 bird count stations in each of the seven localities. Each bird count station surveyed the proximity of a previously installed nest– box, all randomly selected from all the nest–boxes available within each locality. Surveys at bird count stations lasted five minutes and we annotated all the bird species that were detected (heard or seen) within a 25–m radius. All counts were conducted in the morning (between dawn and 11:00 h) and on non–rainy days without strong winds that could affect the reliability of our sampling protocol. Variation in the structure of avian communities and bird reproductive performance among wooded formations are likely to be the result of variation in vegetation structure among habitats. With the purpose of separating effects of habitat and vegetation structu� re, we also characterized the vegetation around each nest–box (25 m of radio) using nine variables: (1) general cover of shrubs (%), (2) cover of deciduous shrubs (%), (3) average shrub height (m), (4) tree cover in the canopy (%), (5) deciduous tree cover (%), (6) average tree height (m), (7) number of tree stems with a diameter higher than 40 cm, (8) average tree trunk diameter (cm), and (9) number of tree and shrub species. Given that some of these variables were expected to be strongly correlated with each other, we performed a principal component analysis (PCA) to obtain a smaller number of uncorrelated variables

De la Hera et al.

(the principal components, PCs), which were easier to interpret. For this purpose, we used the program STATISTICA 7.0 and a varimax rotation of factors. Such PCA yielded three independent components (table 1). PC1 values were associated with the age of the trees, PC2 was positively correlated with variables indicating a more developed shrub layer, and PC3 represented an index of tree cover development in the canopy (see factor loadings in table 1). As stated above, each tree species may hold a different invertebrate community, a circumstance that could affect avian richness and breeding performance (Kolb, 1996; Hartley et al., 2010). We used specific sampling methods to roughly estimate among–habitat relative abundance of the favourite invertebrate prey item used by some insectivorous birds (particularly by the Great Tit) to feed their chicks (i.e. caterpillars, order Lepidoptera; Visser et al., 2006; Wilkin et al., 2009). For this purpose, we placed one plastic washbasin (diameter of 42 cm) on the ground, near the trunk of 23 trees (seven Oaks, eight Eucalyptus and eight Pines). Washbasins were partly filled with water and were also covered with a metallic mesh to avoid other animals (e.g. large mammals) having access to the water and affecting our caterpillar es� timates. This method allowed us to collect drowned caterpillars which had descended from the canopy to the ground for pupation (see Zandt, 1994). Was� hbasins were checked approximately once per week between mid–April and late June, and the overall accumulated number of caterpillars found in each washbasin was used as a response variable in the statistical analyses. Statistical analyses First, we used linear mixed models (LMM) to ex� plore the existence of differences between habitats in vegetation characteristics (PCs). Next, we used generalized linear mixed models (GLMMs) with Pois� son errors to analyze whether bird species richness obtained from count stations varied among habitats, after controlling for vegetation characteristics (Zuur et al., 2009). A similar approach to the latter, but with a binomial error distribution, was performed to test habitat and vegetation effects on the probability of nest–boxes to be occupied (binary variable; empty nest–box = 0, occupied nest–box = 1). For the 25 first clutches detected for the Great Tit (see Results), we also tested for differences between habitats in egg–laying date (i.e. LMM) and clutch size (i.e. GLMM with Poisson errors). All these models were fitted in R using the package lme4 (Bates & Mae� chler, 2010). A Markov–Chain–Monte–Carlo sampling procedure (1 × 104 iterations) implemented in the package languageR was used to obtain the P–values for the fixed effects in the models analysing vegeta� tion characteristics and egg–laying dates (Baayen, 2008). All previous analyses included locality as a random factor. Furthermore, we explored whether the number of collected caterpillars per washbasin differed among tree species. For this purpose, we performed a Kruskal–Wallis test.

Animal Biodiversity and Conservation 36.2 (2013)

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Results Variation in vegetation structure among habitats Tree size or age (PC1) varied among habitats, with the Oak forest showing intermediate values of PC1 that did not differ significantly from the scores recorded in Pine (estimate = –1.148 ± 0.923, t [n = 99] = –1.25, P = 0.216) or Eucalyptus plantations (estimate = 0.601 ± 0.809, t [n = 117] = 0.74, P = 0.458), but PC1 was significantly higher in Pine than in Eucalyptus stands (estimate = 1.75 ± 0.572, t [n = 156] = 3.06, P = 0.003). Eucalyptus plantations did not differ sig� nificantly in shrub development (PC2) from the values recorded in Pine plantations (estimate = 0.064 ± 0.39, t [n = 156] = 0.17, P = 0.869). However, our Oak forest had a more developed understory than both types of exotic tree plantations, although this effect was only significant for the comparison with Pine plantations (Oak–Pine comparison: estimate = 0.845 ± 0.26, t [n = 99] = 3.26, P = 0.002; Oak–Eucalyptus com� parison: estimate = 0.909 ± 0.545, t [n = 117] = 1.67, P = 0.097). For PC3, Pine and Eucalyptus plantations showed similar values (estimate = 0.021 ± 0.218, t [n = 156] = 0.1, P = 0.923), these being significantly lower than those observed in the Oak forest (Oak– Pine comparison: estimate = 2.124 ± 0.15, t [n = 99] = 14.18, P = < 0.001; Oak–Eucalyptus comparison: estimate = 2.146 ± 0.303, t [n = 117] = 7.09, P < 0.001).

Table 1. Correlation coefficients (factor loadings) between the nine variables characterizing vegetation structure (VS) and the three principal components derived from the PCA. Eigenvalues and the percentage of variance explained by each component are also shown: 1. Overall shrub cover (in %); 2. Deciduous shrub cover (in %); 3. Average shrub height (in m); 4. Tree cover (in %); 5. Deciduous tree cover (in %); 6. Average tree height (in m); 7. Number of tree stems (d > 40 cm); 8. Average tree trunk diameter (in cm); 9. Number of tree and shrub species. Tabla 1. Coeficientes de correlación (cargas factoriales) entre las nueve variables que caracterizan la estructura de la vegetación (VS) y los tres componentes principales derivados del análisis de componentes principales (ACP). También se muestran las raíces latentes y el porcentaje de la varianza explicados por cada componente: 1. Cubierta arbustiva total (en %); 2. Cubierta de arbustos caducifolios (en %); 3. Altura media de los arbustos (en m); 4. Cubierta arbórea (en %); 5. Cubierta de árboles caducifolios (en %); 6. Altura media de los árboles (en m); 7. Número de árboles (d > 40 cm); 8. Diámetro medio del tronco de los árboles (en cm); 9. Número de especies arbóreas y arbustivas.

Bird species richness We recorded a total of 18 species (all passerines) after performing the 70 bird count station surveys (data are available from the authors upon request). Variation in bird species richness was better explained by habitat effects (see fig. 1) than by variation in vegetation structure (PC1 effect: estimate ± SE = 0.119 ± 0.109, Z [n = 70] = 1.09, P = 0.275; PC2 effect: estima� te ± SE = 0.147 ± 0.084, Z [n = 70] = 1.75, P = 0.081; PC3 effect: estimate ± SE = –0.033 ± 0.135, Z [n = 70] = –0.25, P = 0.807). Thus, Eucalyptus plantations were the poorest habitat and differed significantly in species richness when compared to Pine plantations (estimate = 0.773 ± 0.269, Z [n = 60] = 2.87, P = 0.004) or the Oak forest (estimate = 1.205 ± 0.422, Z [n = 40] = 2.86, P = 0.004). Pine plantations and the Oak forest showed similar values of species richness (estimate ± SE = 0.27 ± 0.505, Z [n = 40] = 0.534, P = 0.593; fig. 1). Nest–box occupancy rates Out of the 186 nest–boxes considered in the study, 43 were occupied by birds for reproduction. We considered occupied nest–boxes as those in which eggs were laid. The Great Tit was the most common breeding species (n = 31) and the only species occurring in the seven localities (fig. 2A). Less frequently, we detected Coal Tits Periparus ater (n = 6) and Blue Tits Cyanistes caeruleus (n = 6). We arbitrarily distinguished between Great Tits’ first and second clutches taking advantage of the fact that Coal Tits and Blue Tits are single–brooded

PC1

PC2

PC3

–0.22

0.80

0.27

–0.05

0.87

0.01

0.50

0.61

0.32

0.39

–0.11

0.76

–0.09

0.27

0.85

0.89

–0.01

0.10

0.88

–0.09

–0.06

0.93

0.08

0.17

0.11

0.80

–0.06

Eigenvalue

2.93

2.50

1.52

Explained variance

0.33

0.28

0.17

species (see appendix 1 for more details). Second clut� ches were only observed in six cases (their laying dates ranging from day 55 to day 68), all of them occurring in nest–boxes installed in Eucalyptus stands (fig. 2A), but they were not statistically more frequent in these plantations (results not shown). The overall percentage of occupied nest–boxes varied greatly among localities (ranging from four 4 to 40%; see fig. 2A). In our sta� tistical model, shrub development (PC2) was the only significant factor affecting the probability of a nest–box to be occupied (PC2 effect: estimate = 0.493 ± 0.213,

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Bird species richness

6 5 4 3 2 1 0

Oak

Pinus–1 Pinus–2 Pinus–3 Euc–1

Euc–2

Euc–3

Fig. 1. Variation among localities in the number of bird species detected (i.e. species richness; mean ± SE) during five minute bird counts at stations (10 random bird counts per locality). Fig. 1. Variación entre localidades en el número de especies de aves detectadas (riqueza de especies; media ± EE) durante recuentos de cinco minutos en las estaciones (10 recuentos aleatorios de aves por localidad).

Z [n = 186] = 2.32, P = 0.021; fig. 2B), while habitat type (post–hoc analysis Pine vs. Eucalyptus: estimate = 0.472 ± 0.67, Z [n = 156] = 0.71, P = 0.481; post–hoc analysis Oak vs. Eucalyptus: estimate = 1.421 ± 0.858, Z [n = 117] = 1.66, P = .098), PC1 (estimate = –0.163 ± 0.312, Z [n = 186] = –0.52, P = 0.602) and PC3 (estimate = –0.151 ± 0.312, Z [n = 186] = –0.48, P = 0.629) did not show significant effects. Egg–laying date and clutch size in the Great Tit For the 25 first clutches identified for the Great Tit, egg–laying date did not differ among Eucalyptus (mean date = 18 [18th of April] ± 5.3 d, n = 8), Pine (mean date = 24 [24th of April] ± 5 d, n = 9) and Oak stands (mean date = 21 [21st April] ± 5.3 d, n = 8; habitat effects: P > 0.05), but clutches were laid later in nest–boxes presenting older trees in their surroundings (PC1 effect: estimate = 10.17 ± 4.16, t [n = 25] = 2.45, P = 0.024). Great Tit clutch size ranged between five and eight eggs. Clutch size was not affected by habitat (post–hoc analysis Pine vs. Eucalyptus: estimate = –0.01 ± 0.212, Z [n = 17] = –0.05, P = 0.964; post–hoc analysis Oak vs. Eucalyptus: estimate = –0.108 ± 0.393, Z [n = 16] = –0.27, P = 0.784), or by vegetation structure effects (PC1, PC2 and PC3 effects: P > 0.05). Caterpillar abundance among habitats The total number of caterpillars collected per wash� basin differed among habitats (Kruskal–Wallis test: H2,13 = 10.4, P = 0.006; fig. 3), with washbasins located under Oak trees containing a higher accumulated number of caterpillars than both Pine and Eucalyptus trees, where caterpillars were nearly absent.

Discussion Our study confirms that the bird communities�� of Eu� calyptus stands are significantly impoverished, with species richness during the breeding period being lower in commercial plantations than in natural forests. We also identified understory development as a main factor affecting the nest–box occupancy rate of titmice species in the study area. Thus, a more developed shrub layer increased the chances of a nest–box being occupied for breeding. Likewise, a significant difference in caterpillar abundance was observed between exotic and native trees. Although observed variation among habitats in this food resource might affect some reproductive parameters in bird species relying upon caterpillars for breeding, we did not detect differences in the breeding performance of Great Tits during the earliest stages of their reproductive process (i.e. egg–laying date and clutch size). There is increasing concern about the burgeoning proliferation of exotic tree plantations around the world (Brockerhoff et al., 2008; Bremer & Farley, 2010; Putz & Redford, 2010), a trend that is also expected to have a pervasive impact in many areas of the Iberian Peninsula (Santos et al., 2006; Veiras & Soto, 2011). In coastal areas of northern Spain, the transformation of traditional land–uses (i.e. farmlands and pastures) into tree plantations seems to be an inexorable process that might imply the decline of many open–habitat bird species that normally would not occur in woodlands. Paradoxically, these open–habitat species were ori� ginally favoured by ancient human deforestation and farming (Tellería & Galarza, 1990; Williams, 2006). In order to maintain current regional avian biodiversity, conservation efforts should be channelled into pre�

Animal Biodiversity and Conservation 36.2 (2013)

A Nest–box occupancy (%)

Overall occupancy First broods Parus major Second broods Parus major

Oak Pinus–1 Pinus–2 Pinus–3 Euc–1 Euc–2 Euc–3 (n = 30) (n = 24) (n = 23) (n = 22) (n = 18) (n = 27) (n = 42)

2 Shrub development (PC2)

159

Empty nest–boxes Occupaied nest–boxes

–1

–2

Oak

Pinus–1 Pinus–2 Pinus–3

Euc–1

Euc–2

Euc–3

Fig. 2. A. Variation in the overall percentage of nest–boxes occupied by birds (black bars), and the percentage of Great Tit first (grey bars) and second clutches (open bars) among localities. Occupied nest–boxes were those in which eggs were laid. The number of available nest–boxes per locality is shown below the abscissa axis. B. Differences in understory development (mean ± SE of PC2) between empty and occupied nest–boxes for the seven study sites. Fig. 2. A. Variación en el porcentaje total de las cajas nido ocupadas por aves (barras negras) y el porcentaje de primeras (barras grises) y segundas (barras blancas) puestas del carbonero común entre localidades. Las cajas nido ocupadas eran aquellas en las que se habían puesto huevos. El número de cajas nido disponibles por localidad se muestra a continuación en el eje de las abscisas. B. Diferencias en el desarrollo del sotobosque (media ± EE de PC2) entre las cajas nido vacías y ocupadas de los siete lugares del estudio.

serving conventional farmlands, which hold a singular avian breeding community and are also an important wintering destination of many European migratory populations (Tellería et al., 2008; Santos et al., in press). On the other hand, the generalization of tree plantations can be considered an opportunity to recover the woodland species that had been confined to the remnants of natural forest scattered throughout this region (Quine & Humphrey, 2010; Navarro & Pereira,

2012). However, our results confirm that exotic tree plantations are not able to fulfil the role of natural forests (Bongiorno, 1982; Tellería & Galarza, 1990; Proença et al., 2010) because they lack some bird species with high demands for old forest stands, such as the European Nuthatch Sitta europaea (only present in the Oak forest) and the Short–toed Treecreeper Certhia brachydactyla (common in American Pine formations but completely absent from Eucalyptus stands).

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Nº of caterpillars

4 3

2 1 8 0

Oak

Pine

8 Eucalyptus

Fig. 3. Variation among Oak, Pine and Eucalyptus trees in the overall number of caterpillars collected. Graph shows means with standard errors and sample sizes. Fig. 3. Variación entre el roble, el pino y el eucalipto en cuanto al número total de orugas recogidas. En el gráfico se muestran las medias con los errores estándar y los tamaños muestrales.

The previously–described scenario raises the need to develop management practices that help commer� cial plantations diversify their bird communities. A conventional solution to achieve this purpose would consist of promoting a well–developed natural shrub layer (López & Moro, 1997; Santos et al., 2006). This measure should be weighed in relation to wildfire risk, but it could be feasible in our study area given that plantations have a less complex understory than natural forests. This is probably a consequence of the regular removal of native scrublands in exotic tree stands (Veiras & Soto, 2011), which would be depicted in the lower values of PC2 in exotic tree plantations compared to the Oak forest. However, our results showed no clear association between understory development and bird richness obtained from bird counts (P = 0.081; see Results). We did detect, nevertheless, that shrub development may benefit the settlement of some hole–nesting sedentary species (i.e. Titmice species) known to attract other breeding (migratory) species that use year–round residents as cues for habitat selection (Forsman et al., 2009). At this point, we should point out that we pro� vided birds with nest–boxes in all the study localities. Consequently, promoting a complex understory might be ineffective if nesting holes are a prerequisite for the settlement of birds during reproduction, because most exotic tree stands have very few natural cavities. This is particularly true for Eucalyptus plantations in the Basque Country, where trees are logged at a relatively early age (normally after 11 years of tree growth; Veiras & Soto, 2011), explaining the difficulty of finding Eucalyptus stands with high scores of PC1 in our study area.

In many European regions, Great Tits and other insectivorous forest bird species normally try to syn� chronize the hatching of their eggs with a short peak of tree defoliating caterpillars, which constitute an abundant and suitable food resource for feeding their chicks (Sanz et al., 2003; Visser et al., 2006). Although we used a very rough method based on washbasins to estimate caterpillar abundance (Zandt, 1994), our approach allowed us to corroborate that caterpillars are much rarer in exotic trees (both Pine and Eucalyptus) than in native Oaks. Such circumstance might affect the reproductive performance of Great Tits (Kolb, 1996). However, egg–laying date and clutch size did not differ among habitats, and only an effect of tree size/age (PC1) on egg–laying date emerged from our analyses, a finding that was difficult to interpret. Although our sample size was relatively small (n = 25) and limited to only one year, the lack of va� riation between habitats in egg–laying date and clutch size agrees with the results obtained by Kolb (1996), who detected that exotic trees only had a negative effect on later stages of the reproductive period. Un� fortunately, owing to bad meteorological conditions, we could not collect sufficient data from Great Tit chicks to explore this possibility. Kolb’s study was carried out using a more Northern European population of Great Tits, which seems to be more dependent on caterpillar availability (Kolb, 1996; Wilkin et al., 2009). Consequently, it remains to be tested whether similar patterns will be detected in our population for which caterpillar availability is actually very low according to the data obtained from the use of washbasins, and also whether this food resource in the diet of the chicks will tend to be replaced by other invertebrates (e.g. spiders; Pagani–Nuñez et al., 2011). In conclusion, our results further support the ne� gative consequences of exotic tree stands for birds at community level (i.e. bird species richness), with these penalties being stronger in Eucalyptus than in Pine plantations. The study went one step further and explored the possibility that differences in the composition of bird species composition be explained by vegetation structure. Also we tested the existence of variation among habitats in the reproductive per� formance of a generalist bird species (the Great Tit) and found a marked difference between exotic and native trees in caterpillar abundance, two aspects that had not been considered before in our study area. Although limited and preliminary as a consequence of the reduced sample size and the use of only one year of data, the patterns we observed establish the basis for future research into the observed variation among habitats in bird abundance and composition in the North Atlantic coast of Iberian peninsula. Our study also highlights the difficulty of uncoupling habitat from vegetation structure effects in the analyses, because management practices in this region (e.g. age at which trees are logged) differ notably depending on the exotic tree species considered (Eucalyptus vs. Pine). Together with the scarcity of Oak forests, these circumstances made it virtually impossible to find Eu� calyptus, Pine and Oak stands with similar vegetation characteristics, preventing a realistic separation of the

Animal Biodiversity and Conservation 36.2 (2013)

relative contribution of effects of habitat and vegeta� tion structure on our response variables. Clarifying this issue could therefore help us to assess whether the conservation value of planted forests in Northern Iberia is constrained by exotic trees themselves or by the management practices they undergo (Sax, 2002). Acknowledgements We are grateful to all those who helped us in the fieldwork, particularly Álvaro Asteinza. We also want to thank the staff at the Urdaibai Bird Center from Aranzadi Society of Sciences for their support and suggestions in the course of the study, and Eriz Guerra for revising the English. Nest–boxes were provided by the Spanish Government (Ministerio de Medio Ambiente y Medio Rural y Marino), and ringing permissions by the Diputación Foral de Bizkaia. I. de la Hera was funded by the Department of Education, Universities and Research of the Basque Government (fellowship BFI. 09–13). References Ajani, J., 2011. The global wood market, wood re� source productivity and price trends: an examina� tion with special attention to China. Environmental Conservation, 38: 53–63. Baayen, R. H., 2008. languageR: Data sets and functions with 'Analyzing linguistic data: a practical introduction to statistics'. R Package Version 0.953. http://CRAN.R–project.org/package=languageR. Barlow, J., Gardner, T. A., Araujo, I. S., Ávila–Pires, T. C., Bonaldo, A. B., Costa, J. E., Esposito, M. C., Ferreira, L. V., Hawes, J., Hernandez, M. I. M., Hoogmoed, M. S., Leite, R. N., Lo–Man–Hung, N. F., Malcolm, J. R., Martins, M. B., Mestre, L. A. M., Miranda–Santos, R., Nunes–Gutjahr, A. L., Overal, W. L., Parry, L., Peters, S. L., Ribeiro–Junior, M. A., da Silva, M. N. F., da Silva Motta, C. & Peres, C. A., 2007. Identifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences, 104: 18555–18560. Bates, D. & Maechler, M., 2010. lme4: Linear mixed– effects models using S4 classes. R package version 0.999375–33. http://CRAN.R–project.org/ package=lme4. Bongiorno, S. F., 1982. Land use and summer bird populations in Northwestern Galicia, Spain. Ibis, 124: 1–20. Bremer, L. L. & Farley, K. A., 2010. Does �� planta� tion forestry restore biodiversity or create green deserts? A synthesis of the effects of land–use transitions on plant species richness. Biodiversity & Conservation, 19: 3893–3915. Brockerhoff, E. G., Jactel, H., Parrotta, J. A., Quine, C. P. & Sayer, J., 2008. Plantation forests and biodiversity: oxymoron or opportunity? Biodiversity & Conservation, 17: 925–951. Calvino–Cancela, M., Rubido–Bara, M. & van Etten, E. J. B., 2012. Do eucalypt plantations provide

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Appendix 1. Identifying second clutches of Great Tit. Apéndice 1. Determinación de las segundas puestas de carbonero común. Great tits are facultative multiple breeders and some pairs can undertake a second breeding attempt. Second clutches contain fewer eggs than first clutches and may be more frequent in some habitats than in others, possibly affecting the reliability of our between–habitat comparisons. We used the laying dates of two species known to be single–brooded (i.e. Blue Tit Cyanistes caeruleus and Coal Tits Periparus ater) to show the existence of second clutches in the Great Tit. According to the range of egg–laying dates in Blue Tits and Coal Tits (i.e. from day 4 to day 39 considering the 1st of April as day 1; see fig. A), we considered that Great Tit clutches laid later after May 11th (day 41) were second clutches, and they were consequently, excluded from the statistical tests that analysed nest–box occupancy rate, laying date, and clutch size.

First clutches

Second clutches

Parus major

Periparus ater Cyanistes caeruleus –10 0 10 20

30 40 Laying date

Fig. A. Comparison between the laying dates of Great Tits Parus major and the laying dates of two single–brooded species (i.e. Coal Tit Periparus ater and Blue Tit Cyanistes caeruleus). Note that there are some overlapping data points. Fig. A. Comparación entre las fechas de puesta del carbonero común Parus major y las de dos especies de puesta única (carbonero garrapinos Periparus ater y herrerillo común Cyanistes caeruleus). Nótese que algunos datos se superponen.

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Forum 165

Trophy hunting, size, rarity and willingness to pay: inter–specific analyses of trophy prices require reliable specific data M. Sarasa

Sarasa, M., 2013. Trophy hunting, size, rarity and willingness to pay: inter–specific analyses of trophy prices require reliable specific data. Animal Biodiversity and Conservation, 36.2: 165–175. Abstract Trophy hunting, size, rarity and willingness to pay: inter–specific analyses of trophy prices require reliable specific data.— Awareness of the importance of the wildlife trade and human perception in animal conservation is growing. Recent studies carried out on a continental and world scale have analysed the associations between trophy score, rarity and prices. As a large range of ungulates are legally hunted throughout the world and numerous ungulate taxa are threatened, the relationship between rarity and trophy prices has been studied in several species. This article briefly reviews verifiable data on species and trophy prices and compares findings with data used in recent articles. The findings show that several elements of intra–specific data were inadequately addressed and that the trophy prices considered were not necessarily representative of real trophy prices. Furthermore, the body mass used for numer� ous taxa did not fit current knowledge of species, and several subspecies and rarity indexes that were considered disagreed with recognized subspecies or with the real conservation status of taxa. Thus, caution should be taken when considering some reported results. To improve our understanding of the associations between wildlife trade and wildlife conservation, further studies should take into account reliable specific data, such as that from government agencies, rather than publicity data. Key words: Ungulate, Recreational hunting, Trophy price, Game management, Wildlife trade. Resumen La caza de trofeos, el tamaño, la rareza y la disposición a pagar: los análisis interespecíficos de los precios de los trofeos requieren datos específicos fiables.— Cada día hay más conciencia de la importancia que tienen el comercio de fauna silvestre y la percepción de los animales por parte del hombre en la conservación de los mismos. En determinados estudios llevados a cabo recientemente a escala continental o mundial se han analizado las relaciones existentes entre la puntuación de los trofeos, la rareza y los precios. Numerosas especies de ungulados se cazan legalmente en todo el mundo y varias de ellas son especies amenazadas. Por este motivo, se ha estudiado la relación existente entre la rareza y los precios de los trofeos en varias especies. En el presente artículo se examinan brevemente los datos verificables relativos a las especies y los precios de los trofeos, y se comparan con los datos utilizados en algunos artículos recientes. Los resultados ponen de manifiesto que varios elementos de los datos intraespecíficos se trataron inadecuadamente y que los precios de los trofeos analizados no eran necesariamente representativos de los precios reales. Asimismo, el peso corporal utilizado para muchos ungulados no se ajustaba a los valores documentados para estas especies y varias de las subespecies así como algunos indicadores de rareza analizados no se correspondían con las subespe� cies reconocidas o con su estado real de conservación. Por consiguiente, los resultados documentados deberían ser considerados con cautela. Para comprender mejor las relaciones existentes entre el comercio y la conservación de la fauna silvestre, los futuros estudios deberían tener en cuenta información específica fiable, por ejemplo de organismos gubernamentales, en vez de información publicitaria. Palabras clave: Ungulados, Caza recreativa, Precio de trofeo, Gestión cinegética, Comercio de fauna silvestre. Received: 2 III 13; Conditional acceptance: 15 V 13; Final acceptance: 11 VII 13 M. Sarasa, Grupo Biología de las Especies Cinegéticas y Plagas (RNM–118), Sevilla, España (Spain). Current address: Mathieu Sarasa, Fédération Nationale des Chasseurs, 13, Rue du Général Leclerc, F–92136 Issy les Moulineaux Cedex (France). E–mail: mathieusar@hotmail.com; msarasa@chasseurdefrance.com ISSN: 1578–665 X eISSN: 2014–928 X

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Introduction

Misrepresented data

Public awareness of the wildlife trade is increasing and understanding the need for animal conserva� tion is growing (Johnson et al., 2010; Sarasa et al., 2012a). Human perception of species modulates wildlife conservation, and wildlife conservation policies affect human perception of species. Both international and local perception of wildlife may affect environmental policy and management prac� tices (Pusey et al., 2007; Li et al., 2010). However, the perceived rarity of species and even policy and legal frameworks that compile the conservation sta� tus of species and that regulate the trading of wild animals —such as the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and the International Union for the Conservation of Nature (IUCN)— may themselves increase trading activity because of a ‘Limited edi� tion’ effect on wildlife trade (Barnes, 1996; Slone et al., 1997; Raymakers, 2002; Stuart et al., 2006). The ‘limited edition’ effect might be defined as an increase in desire for goods because they are limited in number or supply. The ‘limited edition’ effect has been a key tool in marketing management for decades (Mazis et al., 1973; West, 1975; Worchel et al., 1975; Balachander & Stock, 2008) and in wildlife trade in recent years it has been called the anthropogenic Allee effect (Courchamp et al., 2006). The ‘limited edition’ concept carries a sense of immediacy and exclusivity of goods which will only be available for a short time and/or in limited numbers. The concept affects the perceived rarity; it favours stiff prices and benefits and it stimulates impulsive purchases and collector behaviours (Mazis et al., 1973; West, 1975; Worchel et al., 1975; Balachander & Stock, 2008). Exploited rare goods or species, might become even rarer and thus more valuable, sucking them into a vortex toward the extinction of populations or spe� cies. This phenomenon might affect, for instance, insects, bird eggs, hunting trophies, and even live animals (Slone et al., 1997; Kiff, 2005; Courchamp et al., 2006; Stuart et al., 2006). The ‘limited edi� tion’ effect in wildlife trade and conservation has received increasing interest over the last decade. As previously observed in collected insects (Slone et al., 1997), Johnson et al. (2010) highlighted the relationships between trophy score, rarity and prices of 159 taxa hunted in Africa. Palazy et al. (2012) later carried out a world scale analysis of these associations in trophy ungulates. Their compiled data were presented in an Appendix file that pro� vides the opportunity to verify the reliability of such analysis. In this article I briefly reviewed verifiable data on species and trophy prices to compare these to the data detailed in the Appendix file of Palazy et al. (2012). The operational sections of this review are mainly focused on the data set of Palazy et al. (2012), although other studies based on undetailed publicity data from commercial hunting companies (Courchamp et al., 2006; Johnson et al., 2010; Pa� lazy et al., 2011; Prescott et al., 2012) are probably affected by this issue to some extent.

Palazy et al. (2012) attempted to cover a larger range of taxa than previous studies, but several elements of intra–specific data noted thereafter were not ade� quately addressed. To compare trophy prices between species (see table 1 for detailed presentation of tro� phy price indexes), Palazy et al. (2012) used annual trophy prices from hunting companies, assuming that governments fix trophy fees and that trophy prices from hunting companies are representative of trophy fees and of the perceived value of trophies. However, this is not necessarily the case because, as detailed in table 1, trophy price is calculated using different formulas, and trophy fee is just one factor of the factors taken into account. Auction hammer prices, complementary prices and profits of hunting companies cause substantial differences between trophy fees and trophy prices. Moreover, in several countries, for instance in Spain, local hunters, national hunters and international hunt� ers may use different formulas to calculate trophy prices. For instance, Palazy et al. (2012) used a trophy price of USD 7,800 for both subspecies of the Iberian ibex Capra pyrenaica, Schinz 1838. Nevertheless, C. p. victoriae, Cabrera 1911, generally has longer and thicker horns than C. p. hispanica, Schimper 1848 (Granados et al., 2001) and so is often more appreciated by hunters and more expensive. Hunting permits for trophies are usually increased for auction (starting price in 2008: USD 6,635 at Riaño for C. p. victoriae; USD 3,650 in Andalucía for C. p. hispanica) and the perceived value of trophies, that is, their final sale price, consists of the hammer price plus a complementary price depending on the trophy score (Diario de León.es, 2008c; Junta de Andalucía, 2008) (tables 1, 2). The volatility of demand is hence a major factor in trophy prices. At Riaño, a record hammer price reached USD 39,870 in 2012, leading to a final price of USD 89,625 because of the score–based complementary price that reached USD 49,755 (Diario de León.es, 2012). According to table A1 of Palazy et al. (2012), only trophies of Markhor Capra falconeri, Wagner 1839, and of rhinoceros species would be more expensive than this trophy of Iberian ibex. How� ever, this suggests trophy prices are misrepresented in their data set. The Iberian ibex is not an isolated case and table 2 highlights that numerous other species are also affected by this issue. Mismatches between trophy prices used by Palazy et al. (2012) and true trophy prices were also recorded within and between other species (table 2). In 23 taxa with verifiable data, only two presented absolute mismatches lower than 10% (mean; min; max: 35%; –140%; 92%). For in� stance, the prices of Iberian ungulates were over– or under–estimated, and the reported price differences between species from Europe, Asia or Africa mismatch the true differences between trophy fees reported by several authors (table 2). Thus, the prices used by Palazy et al. (2012) —probably distorted by call prices and by exaggerated prices of hunting compa� nies (table 1)— are not representative of real trophy prices. Festa–Bianchet (2012) already suggested that

Animal Biodiversity and Conservation 36.2 (2013)

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Table 1. Definitions of trophy price indexes. Tabla 1. Definiciones de los índices de precios de los trofeos.

Trophy fees (TF)

Fixed amount of money paid to the management institution (e.g. governments or parks) for hunting one trophy individual.

Starting price for auction (SPA)

Initial amount of money expected by a management institution that sells by auction trophy hunting individuals.

Auction hammer price (AHP)

Final amount of money proposed by a purchaser to a management institution that sells by auction trophy hunting individuals. Auction hammer price is higher than the starting price for auction when the demand is greater that the supply.

Trophy score (TS)

Numerical value attributed to trophies according to measurements and appreciations (e.g. length, thickness, complexity, preferred shape, deformities, etc.) based on referenced hunters' aesthetic preferences.

Complementary price depending on the trophy score (CP)

Additional cost that can be fixed on the basis on the hunting trophy score of the individual hunted in the field. This additional cost is particularly common when the exact trophy value of individuals is estimable with difficulty from a distance or to apply penalties to mismatches between agreed hunting permits and observed hunting events.

Profit of hunting companies (PHC) Difference between the fees paid to management institutions by hunting companies and the fees paid by hunters to the latter for hunting trophy individuals. Call prices of hunting companies (CPHC)

Marketing tool of companies that can present underestimated trophy prices in their advertising to attract potential customers. Once obtained, the customer’s interest and confidence allows commercial profits to be derived from overblown complementary costs.

Exaggerated prices of hunting companies (EPHC)

Commercial tool that can be used by companies to increase their commercial profits by using overblown price of their hunting permits. EPHC are largely due to scarcity of information about sales of hunting permits and on management institutions' trophy fees.

Trophy price (TP) or final sale price

Amount of money paid by hunters for hunting one trophy individual. It reveals the perceived trophy values. When hunters directly pay management institutions that apply fixed trophy prices: TP = TF or TP = TF + CP When hunters directly pay management institutions that sell by auction trophy hunting individuals: TP = AHP or TP = AHP + CP When hunters pay for trophy hunting through hunting companies: TP = TF + PHC or TP = TF + CP + PHC or TP = AHP +PHC or TP = AHP + CP + PHC

marketing may have a stronger effect than rarity on the cost of a hunt with hunting operators, although the two concepts are sometimes linked to each other. Price mismatches could be a serious concern in Palazy et al.’s analyses and interpretations, particularly taking

into account that hunting companies just represent a variable, and often a minority part, of the total trophy hunting activity (Sharp & Wollscheid, 2009). This critical reappraisal was possible in Palazy et al.’s study because they presented a detailed data set.

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Table 2. Mismatches between available specific data and data used in Palazy et al. (2012) (*): 1 Starting price for auction. 2 Auction hammer price. 3 Fee paid to the management institution for one individual. 4 The distinction between West Siberian Moose A. a. pfizenmayeri and East Siberian moose A. a. buturlini has not been widely accepted; body mass presented for A. a. pfizenmayeri (Rodgers, 2001). 5 Alashan wapiti C. e. alashanicus and Gansu deer C. e. kansuensis are considered as synonyms by Dolan (1988) and Groves (2006) recommended that the recognition of these taxa should be left for further studies; body mass presented for C. e. kansuensis. 6 The valid name of this species is Damaliscus pygargus, not Damaliscus dorcas; the two well–differentiated subspecies are the Bontebok D. p. pygargus and the Blesbok D. p. phillipsi (Lloyd & David, 2008). 7 Unclear taxonomic position; S. c. brachyceros would include planiceros (Van Hooft et al., 2002). 8 It is still unclear whether C. caucasica and C. cylindricornis are two separate species or if they are a single species with geographically dependent variability (Weinberg, 2008); Mid–Caucasian tur is considered a potential hybrid of C. caucasica and C. cylindricornis (Kopaliani & Gurielidze, 2009). 9 The taxonomy of Capra sibirica subspecies is not yet resolved and C. s. hemalayanus is not a recognized subspecies (Reading & Shank, 2008). 10 Two subspecies are recognized: Defassa Waterbuck K. e. defassa and Ellipsen Waterbuck K. e. ellipsiprymnus; K. e. crawshayi is included in K. e. ellipsiprymnus and K. e. unctuosus is included K. e. defassa (IUCN SSC Antelope Specialist Group, 2008; Lorenzen et al., 2006). 11 Argali O. a. ammon and darwini could be considered a single ESU or subspecies (Tserenbataa et al., 2004). 12 Three subspecies are recognized and T. s. bea is included in T. s. strepsiceros (Kingdon, 1997; Nersting & Arctander, 2001). 13 Three subspecies are recognized and T. s. burlacei is T. s. cottoni (Nersting & Arctander, 2001). 14 The two last records of the table A1 in Palazy et al. (2012) referred to T. s. strepsiceros and can not be considered rigorously as different tax. Tabla 2. Diferencias entre los datos específicos disponibles y los datos utilizados en Palazy et al. (2012) (*): 1 Precio de salida para la subasta. 2 Precio de remate de la subasta. 3 Tasa pagada a la institución encargada de la gestión por un individuo. 4 La distinción entre el alce de Yakutia A. a. pfizenmayeri y el alce de Kamchatka A. a. buturlini aún no se ha aceptado ampliamente; peso corporal presentado para A. a. pfizenmayeri (Rodgers, 2001). 5 El uapití de Alashan C. e. alashanicus y el ciervo Gansu C. e. kansuensis se consideran sinónimos en Dolan (1988) y Groves (2006) recomendó que el reconocimiento de estos taxones se dejara para estudios posteriores; peso corporal presentado para C. e. kansuensis. 6 El nombre válido de esta especie es Damaliscus pygargus, no Damaliscus dorcas; las dos subespecies bien diferenciadas son el bontebok D. p. pygargus y el blesbok D. p. phillipsi (Lloyd & David, 2008). 7 Posición taxonómica poco clara; S. c. brachyceros incluiría a los búfalos del grupo S. c. planiceros (Van Hooft et al., 2002). 8 Aún no está claro si C. caucasica y C. cylindricornis son dos especies distintas o una sola con variabilidad geográfica (Weinberg, 2008); el tur del Cáucaso central se considera un posible híbrido de C. caucasica y C. cylindricornis (Kopaliani & Gurielidze, 2009). 9 La taxonomía de las subespecies de Capra sibirica aún no se ha resuelto y C. s. hemalayanus no es una subespecie reconocida (Reading & Shank, 2008). 10 Se reconocen dos subespecies: el antílope defasa K. e. defassa y el antílope acuático de Ellipsen K. e. ellipsiprymnus; K. e. crawshayi se incluye en K. e ellipsiprymnus y K. e. unctuosus se incluye en K. e. defassa (Grupo de especialistas sobre el antílope de la Comisión de Supervivencia de Especies de la Unión Internacional para la Conservación de la Naturaleza, 2008; Lorenzen et al., 2006). 11 Los muflones de Argal O. a. ammon y O. a darwini podrían considerarse una única UES o subespecie (Tserenbataa et al., 2004). 12 Se reconocen tres subespecies y T. s. bea se incluye en T. s. strepsiceros (Kingdon, 1997; Nersting & Arctander, 2001). 13 Se reconocen tres subespecies y T. s. burlacei se incluye en T. s. cottoni (Nersting & Arctander, 2001). 14 Los dos últimos registros de la tabla 1 en Palazy et al. (2012) hacen referencia a T. s. strepsiceros y no pueden considerarse rigurosamente como taxones distintos. Trophy price Species Subspecies (in table A1) (*)

Record Trophy price Trophy price (in table A1) (in USD) index (*) (*) (in USD)

Reference

Capra pyrenaica C. p. hispanica

34th

7,800

3,6501

C. p. victoriae

7,800

6,635

C. p. victoriae

7,800

17,120–20,300

(Diario de León.es, 2008b)

R. p. parva

168th

4,900

2,6541

(Diario de León.es, 2008c)

R. p. parva

168

4,900

4,378–4,436

(Diario de León.es, 2008a)

R. p. pyrenaica

169

4,900

4,237–4,767

(Heraldo.es, 2008)

th th

(Junta de Andalucía, 2008) (Diario de León.es, 2008c)

Rupicapra pyrenaica th th

2 2

Animal Biodiversity and Conservation 36.2 (2013)

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Table 2. (Cont.) Species

Subspecies (in table A1) (*)

Record Trophy price Trophy price (in table A1) (in USD) index (*) (*) (in USD)

Reference

Cervus elaphus C. e. hispanicus

58th

4,500

1,9901

(Diario de León.es, 2008c)

C. e. hispanicus

4,500

3,509

(Diario de León.es, 2008a)

2,216

1,327

(Diario de León.es, 2008c)

2,216

1,768

(Diario de León.es, 2008a)

32th

70,000

Capreolus capreolus

2 1 2

Capra falconeri C. f. falconeri

C. f. jerdoni

20,000–35,0003

(Frisina & Tareen, 2009)

6,500–11,0003

(Frisina & Tareen, 2009)

Ovis vignei 144th

O. v. cycloceros

Diceros bicornis

8,000

150,000 195,000–210,000 (Davies et al., 2009) 3

Syncerus caffer 176th

7408

6003

(Lamprey & Mugisha, 2009)

148th

632

1503

(Lamprey & Mugisha, 2009)

T. o. pattersonianus 182th

2125

5003

(Lamprey & Mugisha, 2009)

Hippopotamus amphibious 87

2328

500

(Lamprey & Mugisha, 2009)

3rd

663

2503

(Lamprey & Mugisha, 2009)

119

645

150

(Lamprey & Mugisha, 2009)

163th

605

2503

(Lamprey & Mugisha, 2009)

73th

910

3503

(Lamprey & Mugisha, 2009)

Phacochoerus aethiopicus 146

454

250

(Lamprey & Mugisha, 2009)

94th

676

5003

(Lamprey & Mugisha, 2009)

Male body mass

Reference

S. c. caffer Potamochoerus porcus Taurotragus oryx

Aepyceros melampus A. m. rendilis Ourebia ourebia

Redunca redunca R. r. wardi Damaliscus lunatus D. l. jimela

Kobus ellipsiprymnus K. e. defassa Body mass Species Subspecies (in table A1) (*)

Record Male (in table A1) body (*) mass (*)

Alces alces A. a. alces

9th

400

375–475

A. a. cameloides

12th

453.5

250–350

4 th

A. a. buturlini

453.5

A. a. andersoni

453.5

350–570

A. a. gigas

13th

453.5

400–700

340–6,554

(Bishop, 1988; Haigh et al., 1980; Rodgers, 2001; Wallin et al., 1996)

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Table 2. (Cont.) Species Subspecies (in table A1) (*)

Record Male (in table A1) body (*) mass (*)

Male body mass

Reference

Capra pyrenaica C. p. hispanica

34th

72.5

50.4–65

C. p. victoriae

72.5

61.9–90

C. s. cottoni

53th

2800

100–1,600

C. s. simum

54th

2800

2,000–2,400

C. e. alashanicus 5

56th

180.5

2405

http://www.scirecordbook.org/gansu–deer/

C. e. hippelaphus

180.5

160

(Geist & Bayer, 1988)

C. e. hispanicus

58th

180.5

80–160

C. e. kansuensis

180.5

2,405

C. e. nelsoni

180.5

350

(Geist & Bayer, 1988)

C. e. sibiricus

180.5

300

http://www.scirecordbook.org/altai–wapiti/

C. e. songaricus

62th

180.5

300

(Gao et al., 2011)

47.6

30–120

D. d. dorcas 6

71th

46.5

D. d. phillipsi 6

72th

52.5

(Couturier, 1962; Granados et al., 2001)

Ceratotherium simum (Groves et al., 2010)

Cervus elaphus

th th th

Cervus nippon

(Carranza, 2011) http://www.scirecordbook.org/gansu–deer/

(Groves, 2006)

Damaliscus dorcas 6

(Hayward et al., 2006)

Syncerus caffer S. c. aequinoctialis 174th

522

500–590

(Hayward et al., 2006; Solounias et al., 1994)

S. c. brachyceros 175th

522

400–500

http://www.scirecordbook.org/nile–buffalo/

S. c. caffer

176

522

432–754

http://www.scirecordbook.org/central–

S. c. nanus

177

522

265

S. c. planiceros 178

522

320–410

th th

african–savanna–buffalo/

http://www.scirecordbook.org/west– african–savanna–buffalo

Conservation status Species Subspecies (in table A1) (*)

Record (in table A1) (*)

Conservation status (*)

Proposed conservation status

Reference

Capra pyrenaica C. p. hispanica

34th

Least concern Least concern

C. p. victoriae Naemorhedus goral

35th 112th

Least concern

(Acevedo & Cassinello, 2009; Pérez et al., 2002)

Vulnerable

Near threatened Endangered

(CITES, 2011)

Ovis ammon O. a. hodgsoni

127th

Near threatened Endangered

(CITES, 2011)

O. a. polli

130th

Near threatened

(Schaller & Kang, 2008)

Vulnerable

Animal Biodiversity and Conservation 36.2 (2013)

171

Table 2. (Cont.)

Other unclear or unrecognized taxonomic distinctions Subspecies Species in table A1 (*)

Record in table A1 (*)

Capra cylindricornis 8

31th

Capra caucasica 8

29th

C. c. caucasica 8 C. c. dinniki 8

30th

Capra sibirica

C. s. hemalayanus

Kobus ellipsiprymnus

K. e. crawshayi

38th

93th

K. e. defassa 10

94th

K. e. ellipsiprymnus

K. e. unctuosus

95th 96th

Ovis ammon

O. a. ammon 11

123th

O. a. darwini

126th

Tragelaphus strepsiceros

T. s. bea

198th

T. s. burlacei

199th

T. s. chora

200th

T. s. strepsiceros

201th

T. s. strepsiceros

202th

However, other studies that used trophy prices from hunting companies (Courchamp et al., 2006; Johnson et al., 2010; Palazy et al., 2011) were exposed to this concern as well. The variability of trophy price setting systems between countries and taxa is a key factor of this question. Thus, to promote the reliability of results, a detailed presentation of trophy prices and of setting systems should be required for each record and taken into account. Further studies should consider trophy prices from governmental agencies rather than publicity data to improve the accuracy of row data, of results and of biological inferences. By separating sub–species, Palazy et al. (2012) were able to address a large range of taxa. Beyond unclear and unrecognized taxonomic distinctions (ta� ble 2), the ‘subspecies’ of 34 species (103 units in all) were considered as having a single mean body mass (BM) per species, but the subspecies of other taxa were considered to have different BM. Differences in BM were probably considered when found. However, in the Iberian ibex, C. p. hispanica is known to be smaller than C. p. victoriae (Couturier, 1962; Fandos & Vigal, 1988; Granados et al., 1997; Granados et al., 2001). Similarly, among other species, Alaska moose Alces alces gigas, Miller 1899, is the heaviest subspe� cies of moose (Flerov, 1952; Peterson, 1955; Bishop, 1988) and subspecies of Cervus elaphus, Linnaeus 1758, differ in size (Lowe & Gardiner, 1989; Haigh & Hudson, 1993; Novak, 1999), but this was not taken

into account (table 2). The data of Palazy et al. (2012) on BM are not representative of the 202 ungulate units used and as such their results would have been artificially smoothed. Of the 24 taxa with verifiable data, only five presented absolute mismatches lower than 10% (mean; min; max: –4%; –94%; 49%). These observed errors in BM cannot be due to consistent methodology because, as highlighted in the several examples (table 2), data on subspecies body mass are already available in the scientific literature in com� mon data bases on the Internet (http://wokinfo.com; http://scholar.google.com; etc.). Thus, further studies could detail the references for BM to encourage the use of reliable data. Hunting institution databases record the trophies that have been harvested over long periods of time (see, for instance, Monteith et al., 2013). However, trophy scores are estimated on the basis of the global biometry of the horns and the aesthetic preferences of hunters to compare trophies within a species. They do not therefore accurately take into account confounding factors such as the age of the animal. Trophy scores do not adequately reflect real horn size, at least in wild sheep (König & Hoefs, 1984), just as classical measurements of animal weapons are not necessarily representative of true horn growth (Sarasa et al., 2012b). Wild sheep represents 11% of the sample in Palazy et al. (2012) and most of their sample consists of horned ungulates. This is also a

172

major concern of the biological inferences derived from interspecific analysis of trophy score data. Courchamp et al. (2006) assumed that trophy scores allow interspecific comparisons but the reliability of this factor as a proxy for interspecific comparisons of trophy size is an issue that is still somewhat open. Confusion between trophy score and trophy size might not have affected the analyses per se. However, this questionable proxy favours confusion between two different concepts and it leads to an overblown per� ception of the biological reliability of trophy scores and of the inferences derived from these studies. Thus, the limitations of trophy scores as a proxy of trophy size should have been commented and mentions of trophy size should be avoided when referring to trophy score. Other studies that used trophy scores (Johnson et al., 2010; Palazy et al., 2011) were exposed to this concern as well. Palazy et al. (2012) used IUCN categories as a proxy of rarity. IUCN statuses are interesting proxies of the conservation status for a focal species at the temporal scale of decades. The long temporal scale of IUCN status is due to the definition of threatened status. It is often based on the restricted size of po� pulations and/or on population reductions over the last 10 years or three generations. As a result, IUCN status is a relative index of conservation status for each species, but not an absolute conservation index. IUCN categories may be intrinsically vague and are a problem for those trying to classify species (Regan et al., 2000). Thus, IUCN statuses are not an accurate source of information for inter–specific analyses. Assuming that IUCN statuses might be considered as accurate proxies of the human perception of the rarity of species, other problems remain. Palazy et al. (2012) considered subspecies to increase their sample size while conservation status of most subspecies is not detailed in the IUCN red list. Mismatches were also observed. Several mismatches in rarity values probably resulted from partial and incomplete updating of IUCN pages and of the overblown sample size in Palazy et al.’s study. For instance, both subspecies of Iberian ibex were considered to be of ‘Least Concern’ by Palazy et al. (2012). However, C. p. victoriae is classified as ‘Vulnerable’ since it only inhabits a few, small areas, while C. p. hispanica is of ‘Least Concern’ where its viability depends on ongoing conservation programmes (Pérez et al., 2002; Acevedo & Cassine� llo, 2009). Ovis ammon polii, Blyth 1841, is considered to be ‘Near Threatened’ by Palazy et al. (2012), but a status of ‘Vulnerable’ seems more accurate (Schaller & Kang, 2008). Thus, to remedy IUCN red list updating limits, specific scientific literature should be assessed in detail and researchers specialized in focal species should be contacted to avoid using incomplete and unrepresentative data. Specialists of focal species have updated knowledge of the conservation status and of the actual perceived rarity of species; well–in� formed dwellers/hunters sometimes forestall potential changes in conservation status by policy and legal frameworks (Rivalan et al., 2007). In Palazy et al. (2012), 81 subspecies of 25 species were considered to have a single conservation status per species and

Sarasa

the proxies of rarity are not necessarily representative of the real conservation status of the 202 considered records (table 1). Conclusion A critical question in inter–specific studies is that unre� liable data should be discarded as much as possible because it produces unreliable results. Study designs should be adjusted to ensure the best resolution in sampling while preserving the reliability of the data. In Palazy et al.’s study, taking into account that many data represent species but not subspecies, analysis of the 112 considered species rather than 202 questionable taxa may have been less overblown. The results of Palazy et al. (2012) are potentially interesting because they converge with those of Johnson et al. (2010). Nevertheless, as in other articles on the subject, in Palazy et al. (2012) several elements of intra–specific data were not properly addressed in at least 25–35% of the sample [25% if we only take into account mis� matches in trophy prices, body mass, IUCN status and unclear or unrecognized taxonomic distinctions; 35% if we also take into account that classical measurements of weapons and trophy scores misrepresent trophy size (König & Hoefs, 1984; Sarasa et al., 2012b)]. Thus, caution should be taken when considering the reported results. Moreover, while tourist/ foreign hun� ters spend far more per head than non–tourist/local hunters, international trophy hunting with commercial hunting operators is associated with a global total in spending that is much less than that of stay–at–home hunters (Sharp & Wollscheid, 2009). The economics of commercial hunting operators is a minor part of the total economics of hunting (Sharp & Wollscheid, 2009). This should be also taken into account to avoid overestimating the scientific importance of analysis of publicity data from commercial hunting companies compared to the total economics of hunting. To some extent, other studies that were based on undetailed publicity data from commercial hunting companies (Courchamp et al., 2006; Johnson et al., 2010; Pa� lazy et al., 2011; Prescott et al., 2012) are probably affected by this issue. Biological data and economic data should be adequately addressed in future studies. These should prefer representative lists of trophy prices from governmental agencies rather than publicity data; systematics, body mass, and rarity indexes should be properly represented when data are already available; trophy size should be properly characterized, avoiding aesthetic and incomplete proxies such as trophy score and horn length alone. A rigorous compilation of row data is required so that high quality studies may support the understanding of wildlife trade and the conservation of threatened species. Acknowledgements Thanks to Agnès Sarasa and Michael Lockwood for the English revision. This study received no specific financial support.

Animal Biodiversity and Conservation 36.2 (2013)

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European rabbit restocking: a critical review in accordance with IUCN (1998) guidelines for re–introduction J. Guerrero–Casado, J. Letty & F. S. Tortosa

Guerrero–Casado, J., Letty, J. & Tortosa, F. S., 2013. European rabbit restocking: a critical review in accord� ance with IUCN (1998) guidelines for re–introduction. Animal Biodiversity and Conservation, 36.2: 177–185. Abstract European rabbit restocking: a critical review in accordance with IUCN (1998) guidelines for re–introduction.— European rabbit restocking is one of the most frequent actions in hunting estates and conservation projects in Spain, France and Portugal where rabbit is a keystone species. The aim of this work was to review current knowledge regarding rabbit restocking in accordance with the IUCN (1998) guidelines for re–introduction in order to identify gaps in knowledge and highlight the techniques that improve the overall success rate. Eight of 17 items selected from these guidelines were identified as partly studied or unknown, including important items such as the management and release of captive–reared wild rabbits, the development of transport and monitoring pro� grams, the application of vaccine programs, and post–release long–term studies. Researchers should therefore concentrate their efforts on bridging these knowledge gaps, and wildlife managers should consider all the factors reviewed herein so as to establish accurate management guidelines for subsequent rabbit restocking programs. Key words: Lagomorphs, Hunting management, Oryctolagus cuniculus, Translocation, Wildlife management. Resumen Repoblaciones de conejo europeo: una revisión crítica según las directrices de la IUCN (1998) para las reintroducciones.— Las repoblaciones de conejo europeo son una de las medidas más empleadas en los cotos de caza y en los proyectos de conservación en España, Francia y Portugal, donde el conejo es una especie clave. El objetivo de este trabajo consiste en revisar el conocimiento actual sobre los factores que afectan al establecimiento de las poblaciones de conejo reintroducidas según las directrices de la IUCN (1998), a fin de determinar las lagunas de conocimiento en este ámbito y destacar las técnicas que mejoran los buenos resultados reales de las reintroduc� ciones. Ocho de los 17 puntos seleccionados de estas directrices se identificaron como desconocidos o parcial� mente estudiados, incluidos importantes aspectos como el manejo y la liberación de conejos salvajes criados en cautividad, la elaboración de planes de transporte y seguimiento, la aplicación de programas de vacunación y los estudios a largo plazo posteriores a la liberación. Por lo tanto, los investigadores deben concentrar sus esfuerzos en suprimir esta falta de conocimiento y los gestores deben analizar todos los factores que aquí revisamos, con el objetivo de establecer unas directrices precisas para las futuras repoblaciones de conejo. Palabras clave: Lagomorfos, Gestión cinegética, Oryctolagus cuniculus, Translocaciones, Gestión de fauna silvestre. Received: 19 II 13; Conditional acceptance: 20 V 13; Final acceptance: 9 VIII 13 José Guerrero–Casado & Francisco S. Tortosa, Dept of Zoology, Univ. of Córdoba, Campus de Rabanales, E–14071, Córdoba, España (Spain).– José Guerrero–Casado, Inst. for Terrestrial and Aquatic Wildlife Research, Univ. of Veterinary Medicine Hannover, Bischofsholer Damm 15, 30173 Hannover (Germany).– Jérôme Letty, Office National de la Chasse et de la Faune Sauvage, Direction des Etudes et de la Recherche, 147 route de Lodève, F–34990, Juvignac (France). Corresponding author: José Guerrero–Casado. E–mail: guerrero.casado@gmail.com

ISSN: 1578–665 X eISSN: 2014–928 X

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Introduction Translocation of animals for conservation manage� ment is increasing worldwide due to the alarming loss of biodiversity, but success is limited (Griffith et al., 1989, Armstrong & Seddon, 2008). As many reintroduction attempts have failed, the IUCN ed� ited guidelines for re–introductions (IUCN, 1998) to establish the knowledge needed to ensure that reintroductions meet their goal. Nevertheless, in many translocation programs, many questions remain unanswered (Armstrong & Seddon, 2008). This lack of knowledge includes data concerning the European rabbit (Oryctolagus cuniculus) in France, Portugal and Spain, where around half a million rabbits are translocated each year to promote the recovery of natural populations and to improve hunting stocks (Arthur, 1989; Calvete et al., 1997; Letty et al., 2008). Rabbits are an essential element in the Mediterra� nean ecosystem. They play a vital role as ecosystem engineers and are key prey for more than 30 species of predator (Delibes–Mateos et al., 2008a). What is more, rabbit hunting is an economically important activ� ity in Iberia and France (Delibes–Mateos et al., 2008a; Letty et al., 2008; Ferreira et al., 2010). The rabbit population declined drastically, however, in the 20th century, mainly as a consequence of optimal–habitat loss (Ward, 2005) and disease: recurrent outbreaks of the viral disease myxomatosis since 1952, and rabbit haemorrhagic disease (RHD) since the late 1980s (Vil� �� lafuerte et al., 1995; Marchandeau et al., 1998). This sharp decline is considered a major problem for the conservation of Iberian ecosystems and hunting activity (Marchandeau, 2000; Delibes–Mateos et al., 2009), and rabbit restocking has therefore increased significantly to recover populations (Delibes–Mateos et al., 2008b). The restocking success rate, however, has often been low in traditional restocking attempts. Failure has mainly been due to a low survival rate after the simultaneous release of a large number of rabbits and to a lack of other wildlife management measures (Calvete et al., 1997). Wildlife managers have consequently started to adopt management tools to improve rabbit survival. Some of these tools, such as soft–release or habitat management, have proven to be effective, whereas other strategies, such as vaccination or quarantining, are controversial. Ferreira & Delibes–Mateos (2010) suggested that recommendations made by researchers have not been fully implemented by wildlife managers or hunters, contributing to failure. A protocol for rabbit translocation is thus clearly needed. To establish the perspectives for future research we reviewed current knowledge on rabbit restocking in accordance with the IUCN guidelines for reintroductions. We highlight the techniques and the factors that improve translocation success, and discuss the issues yet to be solved. Data source We used the IUCN guidelines for re–introduction as a reference guide to review current knowledge of rabbit restocking because they establish the items and the

Guerrero–Casado et al.

steps that restocking programs should take. These guidelines define re–introduction as an attempt to establish a species in an area that was once part of its historical range, but from which it has been extirpated or become extinct; translocation as a deliberate and mediated movement of wild individuals or populations from one part of their range to another; and restocking as an addition of individuals to increase an existing population. Whatever the case, the IUCN establishes unique guidelines for re–introductions, restocking or reinforcement and translocations, and in accordance with the literature on rabbits and Armstrong & Seddon (2008), we hereafter use the terms restocking and translocation as synonyms. The IUCN guidelines are divided into three main sections: (1) pre–restocking activities, (2) planning, preparation and restocking phases, and (3) post–release activities. We have therefore analyzed the knowledge concerning rabbit restocking in accordance with these sections. In accordance with �� the suggestion of Arm� strong & Seddon (2008), this paper focuses mainly on the population level, particularly on the factors and management measures that affect the critical stage of establishing a reintroduced population. Therefore, for this study, we selected only items concerning the biological, ecological and practical monitoring aspects of restocking that scientific literature should document. Once established, the subsequent persistence of the population depends on general factors of ecology re� quirements and classical wildlife management. A total of 17 out of 52 items were eventually selected (table 1). An issue was deemed to be partly studied if the approach was only theoretical or not fully developed, or if there was no consensus about it. We reviewed papers that addressed rabbit restocking in the scientific literature using three main web engines: Google ScholarTM, ISI Web of Knowledge® and Scopus®. We searched the following words in the following combinations: 'rabbit' OR 'Oryctolagus' AND 'restocking' OR 'translocations'. To address each item involved in rabbit restocking (e.g. habitat management, vaccines, quarantine or stress) we performed additional searches following the same method. We also searched for data about these topics in Ph. D. Theses, books, and technical reports. Eight of the 17 items in the IUCN guidelines were identified as being poorly studied or unknown; they are summarized in table 1 and discussed in the following sections. Pre–restocking activities: biological knowledge The first step in a restocking program is to determine the source population from which the rabbits will be captured. This question is particularly relevant in the Iberian Peninsula, in which two rabbit subspecies coex� ist: Oryctolagus cuniculus algirus, and O. c. cuniculus (Branco et al., 2000). Nevertheless, Delibes–Mateos et al. (2008b) found algirus rabbits in localities within the cuniculus subspecies range, and vice–versa, as a consequence of past translocations, since in most cases rabbits are released regardless of their genetic lineage. These subspecies have differences in body

Animal Biodiversity and Conservation 36.2 (2013)

size, sexual maturation and litter size (Gonçalves et al., 2002; Ferreira, 2011), difference that could affect the success of rabbit translocations and have unknown ecological and demographic consequences. Wildlife managers should therefore avoid mixing subspecies by identifying the genetic lineage of the rabbits using DNA analysis, and both the donor and the receiving popula� tions must be located within the geographic range of the corresponding genetic lineage (Delibes–Mateos et al., 2008b). Furthermore, at the metapopulation level, although the impact of rabbit extraction on the donor population has not been empirically tested, it should also be considered because excessive captures of individuals may lead to the decline of the donor popula� tion (Cotilla & Villafuerte, 2007). Interest in captive rearing of wild rabbit for release purposes as an alternative to capturing wild individuals has increased over the last two decades (Arenas et al., 2006). The proportion of captive–reared rabbits released in Spain likely exceeds 50% of the total number of wild rabbits released (Sánchez–García et al., 2012). Nevertheless, the success of restocking operations using captive–reared rabbit remains un� tested, and genetic, epidemiological and behavioural problems could be expected when hybrids between wild and domestic lineages are reared in captive �� inten� sive systems, as occurs in some farms in France and Spain (Rogers et al., 1994; Piorno, 2006). Moreover, although Arenas et al. (2006) reported management techniques that improve the reproduction of wild rab� bits in captivity, training techniques to enhance rabbit restocking success in captive environments have not yet been developed. However, it seems possible to recreate wild–like environmental conditions �� (regard� ing food availability, soil type and aerial predator pressure) in breeding enclosures in situ that would enable appropriate rabbit behaviour for release pur� poses and greater ability to adapt to local conditions (Guerrero–Casado et al., 2013a). The sustainability of such captive–rearing populations and relevant fac� tors to consider for translocation success —such as body condition, behaviour and age of captive–reared individuals— should be further studied. With regard to habitat requirements, many types of habitat may be suitable for rabbits as they have a high phenotypic plasticity, however, release areas must include grazing areas, shelter to escape from predators and have soils that enable burrowing. Bu� rrows allow a rapid increase in both population size and viability, and they provide shelter from predators. Release into an optimal habitat is expected to increase rabbit survival and to limit dispersal movements (Cal� vete & Estrada, 2004; Moreno et al., 2004). On the other hand, if release and capture areas have similar ecological characteristics, rabbits can be expected to adapt better to the new environment, by means of pre–adaptations to landscape, soil, flora, or parasites type (Letty et al., 2008). It is therefore advisable that donor populations should be located as close to the target area as possible (Villafuerte & Castro, 2007). However, there is a gap in knowledge concerning the possible importance of adaptations to local ecological conditions in restocking success.

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Planning, preparation and restocking phases According to scientific literature, the crux of the translocation problem is the high mortality in the first weeks after release, and the interaction between the main factors affecting rabbit survival: predation, en� vironmental novelty and stress (Calvete et al., 1997; Moreno et al., 2004; Letty et al., 2008). Translocated animals may display high activity during the first days after release. When they are introduced into a novel habitat they are disorientated and they do not know where to feed, rest or seek refuge from predators. They may also explore the area in search of their usual landmarks or return to their previous home range �� (Letty et al., 2002b, 2008)�� . Stress is an inevi� table component of restocking programs, because the process of translocation involves multiple stressors: (1) capture and handling, (2) captivity or some form of prolonged restraint, (3) transport, and (4) release into an unfamiliar environment —likely the highest stressor (Letty et al., 2007; Teixeira et al., 2007; Dickens et al., 2010)�� . This succession of events could chroni� �� cally–stress translocated animals and may have a strong negative impact on their physiological condition (Cabezas et al., 2007)�� , thus�� increasing their vulner� ability to predation or diseases. Furthermore, eye damage, fractures, bites and wounds (Rouco, 2008) and even sporadic death (Letty et al., 2005) have been reported during the transport phase. Hence, in these phases, stress levels should be controlled by reducing handling and physical restraint (Letty et al., 2005), avoiding crowding, decreasing time between capture and release, and facilitating rapid access to high quality food (Calvete et al., 2005). Specific guidelines should specify all the points related to rabbit capture, transport and handling, with special emphasis on minimizing stress and ensuring animal welfare, since there is often little effort to reduce losses during these stages (Calvete et al., 1997). The effects of transport and handling stress, however, may be only induce temporary negative effects compared to those induced by the permanent change of area (Letty et al., 2003). Over the last decade, various release strategies have been developed to minimize the�� aforemen� tioned problems and improve rabbit survival, such as soft–release, habitat management, or predation exclusion. In the soft–release strategy, translocated rabbits are progressively acclimatised to the new environment in enclosures designed to prevent initial exploratory movements and predation mortality im� mediately after release, when the animals are more vulnerable. Such acclimatization highly increases the short–term rabbit survival (e.g. 82% Calvete & Estrada, 2004; 87% Rouco et al., 2010). As this gain in survival is not always clear and sometimes only temporary (Letty et al., 2000, 2008), a longer acclimatisation period is advised to increase early survival and to decrease dispersal, particularly in poor habitats �� (Calvete & Estrada, 2004)�� . This ap� proach is considered to increase initial breeding stock and overall restocking viability (Letty et al., 2008;

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Table 1. Selected items of IUCN guidelines for reintroduction programs, with the references that support the information and summary and/or observation in each case. Tabla 1. Puntos seleccionados de las directrices de la IUCN para los programas de repoblación, con las referencias que apoyan la información y el resumen y/o las observaciones en cada caso.

Pre–restocking activities Item

Knowledge Summary/Observations

References

Taxonomic Yes status

Avoid the mixing of the two subspecies and perform genetic analyses

Branco et al., 2000, Delibes–Mateos et al., 2008b

Status and Yes biology of wild population

Population crash after the Marchandeau et al., 2000; appearance of viral diseases. Delibes–Mateos et al., 2009; Many populations remain at low density Ferreira et al., 2010

Habitat Yes requirements

Positive effect of habitat quality. Moreno et al., 2004; No studies on the importance of local Villafuerte & Castro, 2007 ecological adaptations

Identification of Yes Mainly viral diseases and habitat loss previous causes of decline

Villafuerte et al., 1995; Delibes–Mateos et al., 2009

Wild population Partly management studied in captivity

No studies on training in captivity. Possible genetic, behavioural and ecological problems with hybrid domestic rabbits

Arenas et al., 2006; Piorno, 2006; Guerrero–Casado et al., 2013a

The release of Partly wild rabbit reared studied in captivity

No studies on restocking success. Genetic introgression of hybrid rabbits in wild populations

Piorno, 2006; Sánchez–García et al., 2012

How to minimize Yes the infection rate

Treat for external and internal parasites Cabezas & Moreno, 2007; before release Rouco et al., 2008

Planning, preparation and restocking phases Item

Knowledge Summary/Observations

References

Identification of No No suitable guidelines success indicators Design a monitoring program

Partly studied

No consensus about a standardised monitoring protocol

Fernández–de–Simón et al., 2011

Health of Yes release stock

Positive effect of body condition and negative impact of stress

Calvete et al., 2005; Cabezas et al., 2007

Vaccination Partly studied

Disagreements on its effectiveness. Calvete et al., 2004; Positive effect of animals released Guitton et al., 2008; with high natural antibody concentration Ferreira et al., 2009

Quarantine Yes

Negative effect on animals' physiological condition

Moreno et al., 2004; Calvete et al., 2005

Transport plan

No detailed guide. No demonstrated effect of crowding and long transports

Letty et al., 2003; Letty et al., 2005

Positive effect of soft–release, habitat management and predator exclusion

Calvete & Estrada, 2004; Rouco et al., 2008; Cabezas et al., 2011

Partly studied

Release strategy Yes

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Table 1. (Cont.)

Post–release activities Item

Knowledge Summary/Observations

References

Demographic, Partly ecological and studied behavioral studies

Restocked rabbit’s show the same behaviour in the long–term as wild individuals

Rouco et al., 2011b; Ruiz–Aizpurua et al., 2013

Long–term Partly adaptations studied

Low breeding contributions. No studies of the interactions with the resident congeners

Letty et al., 2002a

Investigation Yes of mortalities

Mainly predation, environmental novelty Calvete et al., 1997; and stress. Survival and dispersal after Letty et al., 2008; release in short–term are well documented Cabezas et al., 2011

Rouco et al., 2010). More recently, large in situ breed� ing enclosures have been widely used in predator conservation projects to enhance rabbit availability (Ward, 2005; Ferreira & Delibes–Mateos, 2010) and may be a highly effective way of establishing a new population. The role of fences is not only to reduce mortality due to terrestrial predators and dispersal movements but also to establish a captive in situ breeding stock so that young individuals will naturally disperse and settle in the surrounding areas (Letty et al., 2006; Rouco et al., 2008; Guerrero–Casado et al., 2013b). Furthermore, as rabbits translocated to a new environment are highly vulnerable to preda� tion in the short–term, soft–release or long–lasting acclimatization in predator–free enclosures should effectively minimise the impact of predation without concentrating efforts on removal of predators. The impact of predation can also be reduced by selecting areas with a high portion of natural shelter (Calvete & Estrada, 2004) or by increasing the shelter availability through habitat management (Cabezas et al., 2011). Habitat management is a highly effective and widespread practice in rabbit restocking (Catalán et al., 2008; Ferreira & Alves, 2009; Ferreira et al., 2013). If rabbits are released in a sub–optimal habitat, habitat management should occur prior to release so as to create feeding habitats and provide shelter through scrubland management and/or the construction of artificial warrens where refuge is scarce (Ferreira et al., 2013). Rabbit abundance and survival rate is significantly higher when the translocation is carried out in areas improved by the creation of pastureland and provision of artificial warrens (Cabezas & Moreno, 2007; Cabezas et al., 2011). Releasing rabbits into artificially constructed warrens is a common practice that also enhances the availability of shelter and breeding sites. Put simply, it is preferable to build many small warrens rather than a few large warrens (Rouco et al., 2011a). These smaller structures, preferentially built with tub�

ing, should be close enough to each other (Barrio et al., 2009) to allow a small population to settle, and they should be located in areas with adequate food and shelter (Fernández–Olalla et al., 2010). Detailed guidelines on how to conduct habitat management can be found in several technical documents (Ano� mynous, 2003; Ferreira & Alves, 2006; San–Miguel, 2006; Guil, 2009). The risk of disease is another threat that may jeop� ardize wild rabbit translocations. Many translocation therefore include the vaccination of rabbits against myxomatosis and RHD virus (Delibes–Mateos et al., 2008b) even though its effectiveness in the field is controversial. Despite some possible short–term negative effects, an overall positive effect of vac� cination has been recorded in free–ranging rabbit populations (Cabezas et al., 2006; Calvete, 2006; Guitton et al., 2008; Ferreira et al., 2009). Vaccina� tion in translocation may have some drawbacks: its short–term negative effect may negatively affect the physiological condition of rabbits and increase early mortality risks (Calvete et al., 2004); the immune response depends on body condition and may be decreased by the stress induced by translocation (Cabezas et al., 2006); the vaccine may cause an immunosuppressive effect in individuals with a poor physiological condition (Calvete et al., 2004); and its effectiveness may be reduced in immunized individu� als or, for RHD, in case of a significant evolution of the virus (Le Gall–Reculé et al., 2011). On the other hand, translocation is a rare case in which vaccina� tion may be relevant, and indeed, it could be crucial for population establishment in case of subsequent disease outbreak. The effectiveness of vaccination campaigns should be high since it is possible to vac� cinate the whole 'population' (released individuals). However, as a subsequent booster is not feasible, a long–lasting positive effect of a single vaccination and of the related immunity in wild rabbit seems question� able. The exact impact of vaccination on the fitness

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Guerrero–Casado et al.

Restocking portocol

Same sub–species

Crowding

Natural sex ratio

Long transport

Before breading season

Excessive release in a small area

Animal condition

Habitat factors

High antibody concentration

High habitat quality

Good physiological body condition

High shelter availability

Full–grown juveniles

Rabbit restocking success

Acclimatization period Predation exclusion

Vaccine

Quarentine

Desparasitation

Management actions

Artificial warrens

Food supplementation

Creating breeding Increase the habitats shelter availability

Fig. 1. Summary of the factors that affect wild rabbit restocking success. The symbols + and – indicate positive or negative relationships with the restocking success. Fig. 1. Resumen de los factores que afectan al éxito de las repoblaciones de conejo. Los símbolos + y – indican una relación positiva o negativa con los buenos resultados de las repoblaciones.

of translocated rabbits, and the related cost–benefit ratio for restocking success has therefore yet to be adequately and experimentally addressed. Given that long–term survival is positively cor� related with antibody concentrations before release (Cabezas et al., 2011)�� , Rouco (2008) proposed releas� ing rabbits with naturally high antibody concentrations as an alternative to vaccine. This might be feasible in the wild, since just after the annual outbreak of diseases, most individuals have natural antibodies in high density rabbit populations (Cotilla et al., 2010). Thus, vaccination is unnecessary when restocking with such individuals (Calvete, 2006), and vaccination protocols would only be necessary if donor popula� tions have low antibody prevalence (Cabezas et al., 2006). However, the precise monitoring of antibody prevalence in wild populations may not be easy to carry out in the field. In turn, in some restocking programs, rabbits are kept in quarantine for several days to ensure the effect of the vaccine and to make sure that animals do not incubate the viral diseases. Such captivity periods, nevertheless, induce stress, loss of body mass, abortion in pregnant females, and other pos� sible physiological disorders (Calvete et al., 2005). This management tool therefore controls diseased or injured animals (Calvete et al., 1997) but does not generally increase restocking success (Calvete & Estrada, 2004). Restocking operations have also been shown to be a potential means of introduc� ing pathogens into resident populations (Haz et

al., 2001; Reglero et al., 2007; Navarro–González et al., 2010). Hence, all rabbits should be treated for external and internal parasites before release in order to minimise the possibility of disease and parasite transmission. As regards the health of the stock released, selecting animals with a good body condition (those with a good index of fat, and free of traumatic injuries, cachexia, or high parasite levels) enhances the probability of survival (Calvete et al., 2005; Cabezas et al., 2006). Other factors suggested to affect restocking suc� cess are release timing, sex ratio, age, and the number of rabbits released. For demographical reasons, the release of rabbits before the breeding season could lead to higher population growth (Cotilla & Villafuerte, 2007), whereas releasing rabbits during the breeding season (when social stress is high) might increase agonistic behaviour and direct competition among rabbits �� (Moreno et al., 2004)�� .�� The timing of the re� lease could also affect the translocation success if, for instance, the impact of predation depends on the season (the availability of food and cover differs be� tween seasons). Regarding age, the model of Cotilla & Villafuerte (2007) indicated that success would be maximized by releasing only adult rabbits (at least 4 months old). However, the fitness of individuals to translocation may play a role; full–grown juveniles might be less affected by translocation than adults and better able to adapt to the new situation (Mauvy et al., 1991; Letty et al., 2008). It is therefore neces� sary to clarify the optimal age of release animals. As

Animal Biodiversity and Conservation 36.2 (2013)

a general rule, it is advisable to release rabbits in optimal numbers and in a natural sex ratio so at to attain viable population dynamics after release (e.g. 1:1 Moreno et al., 2004; Cabezas & Moreno, 2007). Post–release activities Little is known with regard to demographic, eco� logical and behavioral long–term adaptations in released populations. Some works, however, have suggested that restocked rabbits exhibit the same behavior in the long–term as wild individuals (Rouco et al., 2011b; Ruiz–Aizpurua et al., 2013). Indeed, social behavior can also affect restocking success (Ruiz–Aizpurua, 2013), although Letty et al. (2006, 2008) did not record a clear difference in the survival rate between individuals released in familiar groups (captured in the same warren) and unfamiliar groups, suggesting that the translocation process destabi� lizes previous social relationships. Earlier studies have also suggested a low breeding contribution of introduced individuals during the first months after release (Letty et al., 2002a). These points should thus be clarified in further research to understand the behavior of the rabbits released and their inte� ractions with the resident congeners. Finally, it is necessary to identify short– and long–term indicators to assess the outcome of the translocation in agreement with aims and objectives. Rabbit translocation often lacks careful monitoring (Cabezas & Moreno, 2007). A standardized monito� ring protocol is needed to acquire reliable data (rabbit abundance, special distribution, time scale,...) on restocking success. To correctly assess restocking effectiveness, wildlife managers could monitor rabbit abundance before and after release using indices based on transect counts or pellet counts (Fernán� dez–de–Simón et al., 2011). Conclusions Despite the relevance of rabbit restocking activities, eight of the items considered important in the IUCN re–introduction guidelines are only partly answered. Conservationists, hunters, wildlife managers and researchers should thus concentrate their efforts on bridging these knowledge gaps and implementing scientific recommendations to establishing accurate management guidelines for subsequent rabbit re� stocking. We suggest that the overall success rate would be improved by: (1) establishing a long period of acclimatization; (2) selecting a high quality habi� tat or enhancing its carrying capacity with artificial warrens, food supplementation or scrub manage� ment; (3) avoiding the mixing of two subspecies; (4) selecting animals with a good body condition and antibody concentration; (5) reducing predation risk and stress; (6) releasing full–grown rabbits in a natural sex ratio before the breeding season; and (7) avoiding the simultaneous release of an excessive number of animals in a small area (fig. 1).

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El viaje del Prof. Emil A. Rossmässler en 1853 por España y la localidad tipo de Iberus angustatus (Rossmässler, 1854) (Gastropoda, Helicidae) A. Martínez–Ortí & F. Robles

Martínez–Ortí, A. & Robles, F., 2013. El viaje del Prof. Emil A. Rossmässler en 1853 por España y la localidad tipo de Iberus angustatus (Rossmässler, 1854) (Gastropoda, Helicidae). Animal Biodiversity and Conservation, 36.2: 187–194. Abstract The journey of Prof. Emil A. Rossmässler in 1853 in Spain and the type locality of Iberus angustatus (Rossmässler, 1854) (Gastropoda, Helicidae).— We have identified the type locality of Helix Guiraoana var. angustata Rossmässler, 1854 as 'located in the heights surrounding the Venta del Molinillo near the Sierra de los Dientes de la Vieja, Diezma, Granada', from the description given by Rossmässler about his journey in the south east of Spain in 1853. The molecular analysis (COI and 16S) of a topotype collected live allowed us to confirm the identification of clade 4 of the genus Iberus proposed by Elejalde et al. (2008) with H. Guiraoana var. angustata, currently I. angustatus. Key words: Mollusca, Helicidae, Iberus angustatus, Type locality, Molecular phylogeny, COI, 16S. Resumen El viaje del Prof. Emil A. Rossmässler en 1853 por España y la localidad tipo de Iberus angustatus (Rossmässler, 1854) (Gastropoda, Helicidae).— Se identifica la localidad tipo de Helix Guiraoana var. angustata Rossmässler, 1854 como ''alturas situadas en los alrededores de la Venta del Molinillo cerca de la Sierra de los Dientes de la Vieja, Diezma, Granada'', a partir de la descripción realizada por Rossmässler de su viaje por el SE de España en 1853. El análisis molecular (COI y 16S) de un topotipo recogido vivo ha permitido confirmar la identificación del clado 4 del género Iberus, propuesta por Elejalde et al. (2008), con H. Guiraoana var. angustata, actualmente I. angustatus. Palabras clave: Mollusca, Helicidae, Iberus angustatus, Localidad tipo, Filogenia molecular, COI, 16S. Received: 18 III 13; Conditional acceptance: 10 IX 13: Final acceptance: 10 X 13 Alberto Martínez–Ortí, Museu Valencià d’Història Natural, L’Hort de Feliu–Alginet, Apdo. 8460, 46018 València, València, España (Spain).– Fernando Robles, Dept. de Geología, Fac. de Ciències Biològiques, Univ. de València, València, España (Spain). Correspondencia: A. Martínez–Ortí. E–mail: amorti@uv.es

ISSN: 1578–665 X eISSN: 2014–928 X

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Introducción Recientemente los autores (Martínez–Ortí & Robles, 2012) han publicado un trabajo en el que se revisaban algunos aspectos de las especies Helix alcarazana (Rossmässler, 1854), Helix Guiraoana (Rossmässler, 1854), Helix Guiraoana var. angustata (Rossmässler, 1854) y Helix Loxana (Rossmässler, 1854), descritas por Rossmässler (1854a) y atribuidas actualmente al género Iberus Montfort, 1810. En dicho trabajo se afirmaba que el material en que se basó dicho autor para describir estas especies había sido recogido por el naturalista murciano Ángel Guirao, basándose en una interpretación errónea del texto de Rossmässler, ya que solamente la muestra de H. Guiraoana fue recogida directamente por Guirao. Posteriormente los autores han tenido conocimiento de la existencia de una obra de este autor, ''Reise–Erinnerungen aus Spanien'' (Rossmässler, 1854b, 1857), recientemente traducida al castellano con el título ''Recuerdos de un viajero por España'' (Rossmässler, 2010), en la que se narra detalladamente el viaje realizado por el SE de España por el malacólogo alemán en 1853, en el que visitó las localidades tipo de H. alcarazanus, H. Guiraoana var. angustata y H. Loxana y recogió el material en que basó sus descripciones. Previamente a sus trabajos de 1854 Rossmässler publicó dos breves reseñas de su viaje en la revista Zeitschrift für Malakozoologie: en la primera, ''Briefe aus Spaniens'' (Cartas desde España) (Rossmässler, 1853a), se recogen dos cartas enviadas desde Murcia, el 4 de abril de 1853 y desde Granada, el 4 de mayo de 1853; en la segunda, ''Kurzer Bericht über meine malakozoologische Reise durch eine Theil des südöstlichen Spanien'' (Corto informe sobre mi viaje malacológico por una parte del sureste de España) (Rossmässler, 1853b), proporciona alguna información preliminar sobre sus muestreos. También Schmidt (1853) publicó una breve reseña en la misma revista, titulada ''Bermekungen zu dem vorstehenden Aufsatze des Herrn Prof. Rossmässler'' (Observaciones sobre el precedente informe del Sr. Prof. Rossmässler), con nueva información sobre el tema. Los datos contenidos en estas obras han permi� tido precisar la localidad típica de H. Guiraoana var. angustata (actualmente I. angustatus), recoger nuevo material de esta localidad y corroborar la identificación de esta especie realizada por Elejalde et al. (2008). Material y métodos Para la determinación de la localidad tipo de H. G. var. angustata se han revisado detalladamente las publicaciones originales, interpretándose las descrip� ciones que resultaban ambiguas tras la visita a los lugares mencionados en la bibliografía. Martínez–Ortí & Robles (2012) indican que muestrearon la Sierra de los Dientes de la Vieja sin encontrar ningún ejemplar de I. angustatus, aunque sí recogieron I. loxanus e I. alonensis like–02 sensu Elejalde et al. (2008). Con la nueva información disponible se visitó de nuevo la zona los días 7 y 8 de octubre de 2012 y se muestreó detalladamente el área situada entre la Sierra de los

Martínez–Ortí & Robles

Dientes de la Vieja y la antigua Venta del Molinillo, cuyas ruinas persisten en la actualidad. Los resulta� dos de estos muestreos en cuatro zonas se indican en la tabla 1. Todo el material recolectado se encuentra de� positado en el Museu Valencià de Historia Natural (MVHN). Para el análisis molecular, tras la extracción del ADN se ha procedido a la amplificación, mediante la técnica de la PCR (Polymerase Chain Reaction), de dos regiones de ADN de dos genes mitocondria� les, citocromo c oxidasa subunidad I (COI) y 16S rRNA, y a la secuenciación del ADN del topotipo de I. angustatus (ejemplar vivo de la muestra MVNH– 091012DS06), siguiendo la metodología utilizada por Elejalde et al. (2008). Los ''primers'' utilizados para ambos fragmentos son los diseñados por Palumbi et al. (1991) para el 16S rRNA y por Folmer et al. (1994) para el COI. Resultados Localidad tipo de Iberus angustatus (Rossmässler, 1854) La localidad tipo de Helix guiraoana var. angustata según Rossmässler (1854a: 11–12) es ''bajo los blo� ques de caliza no lejos de la Sierra de los Dientes de la Vieja, en la provincia de Granada''. Martínez– Ortí & Robles (2012: 102) indican que ''this place is very difficult to specify, because in the province of Granada and the rest of the Autonomous Community of Andalusia, there are several landforms that receive this designation. The author visited a place known as ‘Dientes de la Vieja’ located near of Diezma (Granada) which due to its proximity to area of I. angustatus sensu Elejalde et al. (2008) seems the most appropri� ate, but we did no find specimens of this species''. Debido a ello consideran que ''until new information is available on this matter, the situation of the type locality of I. angustatus remains doubtful''. Actualmente disponemos de nueva información que permite precisar la situación de la localidad típica citada por Rossmässler (1854a). Aunque las primeras reseñas de sus viajes publicadas por Rossmässler (1853a, 1853b) no proporcionan ningún dato al respecto, Schmidt (1853: 174) señala que los ejemplares de la variedad de H. Guiraoanus recibidos de Rossmässler tenían la indicación de ''raros en rocas calcáreas de la Sierra de los Dientes de la Vieja, entre Granada y Dierma (error por Diezma)'', lo que coincide con la localidad indicada por Martínez–Ortí & Robles (2012). Información mucho más detallada es proporcionada por el propio Rossmässler (1854b: 18–20, 2010: 266–267) en la descripción de su viaje por España: ''Una hora después de Diezma …nos encontramos con una profunda grieta por la cual… fluía el río Anchurón [= río Fardes] …El camino bajaba durante cerca de una hora junto al río Anchurón [= río Fardes] hacia la región de la Sierra del Molinillo o, como se llama también, Sierra de los Dientes de la Vieja …echaba miradas …hacia la izquierda, a las paredes empinadas de grandes alturas, que me prometían una vegetación de

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Tabla 1. Localidades y fecha de muestreo, coordenadas UTM, material recogido y número de muestra en la colección del Museu Valencià d’Història Natural: Loc. Localidad (1. Sierra de los Dientes de la Vieja; 2, 3. Paraje de los Dientes de la Vieja; 4. Venta del Molinillo, roquedo; 5. Finca La Ermita, junto a la Venta); v. Ejemplar vivo; c. Concha. Table 1. Areas and date of sampling, UTM coordinates, material collected and number of sample in the collection at the Museu Valencià d’Història Natural: Loc. Locality; v. Live sample; c. Shell. (For abbreviations of localities, see above.) Loc. 1

Fecha

UTM

7 X 2012

30SVG6027

I. angustatus

I. loxanus

60c MVHN–

1c MVHN–

091012DS03

091012DS04

1 XI 2005

30SVG6028

–

7 X 2012

30SVG6028

–

I. alonensis–02 –

2v+6c MVHN–1103 1v+3c MVHN–1104 1v + 60c MVHN–

1c MVHN–

291112JL01

291112JL02

1v+8c MVHN–

42c MVHN–

091012DS06

091012DS05

22c MVHN–

–

8 X 2012 8 X 2012

30SVG6228 30SVG6229

091012DS067

arbustos abundantes y entre numerosos bloques, una rica cosecha de caracoles. Pero por ninguna parte se nos ofrecía un paso sobre el torrente, aunque no me hubiese importado bajar con grandes dificultades hacia su lecho. Hacia el mediodía llegamos a una venta que se hallaba junto a un molino —quizás el molinillo que daba origen al nombre— abajo, a la orilla del arroyo… Una pequeña excursión hacia una de las alturas en los alrededores dio escasos resultados''. De las palabras de Rossmässler citadas se deduce que este viajero sólo pudo recolectar unas pocas mues� tras (como indica la observación ''con escasos resulta� dos'') en la excursión que realizó en los alrededores de la Venta del Molinillo. Esto concuerda con la localidad ''no lejos de la Sierra de los Dientes de la Vieja'' que señala Rossmässler (1854a) en la descripción original de Helix Guiraoana var. angustata y con la escasez de material (dos ejemplares) que componen la serie tipo de esta especie, depositada en el Senckenberg Museum de Frankfurt (SMF) (SMF 7911 y 7912), ejemplares que también menciona Schmidt (1853). El itinerario que siguió Rossmässler entre Murcia y Granada sigue el recorrido del antiguo ''camino carretero'' que, a mediados del siglo XIX, unía estas dos ciudades de acuerdo con las guías de viaje que pudo consultar este autor, como por ejemplo la de Mellado (1852), que era la más popular en la época. En la actualidad la carretera A–4004, que discurre junto a la autovía A–92, sigue el recorrido del antiguo camino carretero y permite acceder sin dificultad a los parajes visitados por Rossmässler (fig. 1). La descripción de la zona a que hace referencia Rossmässler necesita algunas aclaraciones. En primer lugar el topónimo ''Dientes de la Vieja'' se aplica a dos

– 2c MVHN– 091012DS01

lugares distintos: un paraje de pequeña extensión con una morfología característica de estratos verticales de caliza en los que la erosión ha labrado entalladuras que recuerdan una mandíbula deteriorada, que es atravesada por la A–4004. Este paraje (figs. 1, 2E, tabla 1: loc. 2), denominado puerto de Molinillo en la cartografía regional (SIGPAC, 2012), corresponde al puerto de los Dientes de la Vieja mencionado por Mellado (1852) y es conocido por este nombre por los habitantes de la zona. Fue visitado por los autores en 2005, quienes recogieron la muestra citada por Martínez–Ortí & Robles (2012), sin encontrar I. angustatus. Esa localidad ha vuelto a ser visitada también con resultado negativo. El topónimo Dientes de la Vieja se aplica también a una sierra (figs. 1, 2A, tabla 1: loc. 1) situada al sur del paraje citado, pasada la autovía A–92, de acuerdo con la cartografía SIGPAC. En ninguno de estos dos lugares recogió muestras Rossmässler, según su descripción del viaje. La localidad tipo de H. Guiraoana var. angustata corresponde, por consiguiente, a las alturas situadas en los alrededores de la Venta del Molinillo, donde realizó una excursión Rossmässler. Estas ''alturas'' corresponden a dos colinas de escasa altitud: la primera, que hemos denominado ''roquedo sobre la Venta'' (fig. 1, figs. 2B–2C, tabla 1: loc. 3) está situada unos 50 m al oeste de la venta; la segunda, que llamamos ''Finca la Ermita'' (figs. 1, 2D; tabla 1: loc. 4), está situada 150 m al noreste de la venta y es prolongación de la anterior, sólo separada de ella por el arroyo de Prado Negro. Ambas presentan una cota máxima de 1.311 m y presentan abundantes bloques de calizas en las laderas y en la base, lo que concuerda con las indicaciones de Rossmässler.

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Fig. 1. Mapa de distribución geográfica de Iberus angustatus. Fig. 1. Map of geographical distribution of Iberus angustatus.

En ambas localidades se han recogido ejemplares de esta especie, aunque no eran muy abundantes, lo que coincide con la observación de Rossmässler. Una tercera localidad, en las proximidades de la cima de la Sierra de los Dientes de la Vieja (entre 1.450 y 1.500 m de altitud) ha proporcionado material más abundante de I. angustatus (tabla 1). Sobre la identidad de Helix Guiraoana var. angustata Rossmässler, 1854 Elejalde et al. (2008), en su estudio taxonómico mediante filogenia molecular del género Iberus, iden� tificaron su clado 4 con H. Guiraoana var. angustata, proponiendo su validez específica con la designación de I. angustatus. El área de distribución de esta espe� cie abarcaría el sur de la provincia de Jaén, al oeste del río Guadiana Menor y el centro de la provincia de Granada, al norte del río Genil. El material utili� zado por estos autores procede de cinco localidades (Elejalde et al., 2008: fig. 2B, tabla 1), cuatro de ellas (I. angustatus–01, 02, 04 y 05) de Jaén y la quinta (I. angustatus–03), de Granada, se encuentra en la

cuadrícula UTM 30SVG52, contigua a la cuadrícula UTM 30SVG62 donde se sitúa la localidad tipo de H. G. var. angustata, según explicamos más arriba. Esta distribución geográfica parece confirmar la iden� tificación del clado 4, reconocido como una especie bien caracterizada mediante el estudio de la filogenia molecular, con el taxón I. angustatus (Rossmässler, 1854) como propusieron Elejalde et al. (2008). Para confirmar esta identificación se ha procedido al análisis molecular del ejemplar vivo recogido en la localidad tipo (tabla 1). Se han obtenido y publicado en el GenBank las secuencias de los dos genes mito� condriales, COI (KC693589) y 16S rRNA (KC493778), que han coincidido completamente con las obtenidas por Elejalde et al. (2008) para I. angustatus. Para la región COI corresponde al 100% de identidad (95% de cobertura de la secuencia y 0.0 de E valor) de la secuencia depositada en el GenBank I. angustatus–03 (EF440240.1) obtenido mediante BLAST contra la base de datos de nucleótidos, mientras que para la región 16S corresponde al 99% de identidad (94% de cobertura de la secuencia y 0.0 de E valor) de la secuencia depo� sitada en el GenBank I. angustatus–03 (EF440190.1).

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Fig. 2. A. Sierra de los Dientes de la Vieja. B–C. Roquedo sobre la Venta del Molinillo. D. Finca La Ermita. E. Paraje de los Dientes de la Vieja. Fig. 2. A. Sierra de los Dientes de la Vieja. B–C. Rock mountain above Venta del Molinillo. D. Finca La Ermita. E. Area of Dientes de la Vieja.

Sobre la variabilidad del área umbilical de la concha de I. angustatus Arrébola en Martínez–Ortí & Robles (2012) señala que ''I. angustatus sensu Elejalde et al. (2008) may not have an open umbilicus, but rather half–covered

or almost covered by the reflection of the peristome. There are areas where the specimens of I. angustatus show great variability in regard to the reflection of the peristome over the umbilicus, approaching the char� acteristics of I. guiraoanus''. Esta variabilidad había sido ya intuida por Schmidt (1853: 174) quien indicó

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Fig. 3. Concha de Iberus angustatus: A–B. Lectotipo (SMF 7111; 21,8 mm Ø; fotografía de S. Hof, Naturmuseum Senckenberg, Frankfurt, Alemania); C. Paralectotipo (SMF 7912; 22,2 mm Ø); D–E. Roquedo sobre la Venta del Molinillo (Diezma, Granada) (locus typicus) (23,1 mm Ø y 11,7 mm h); F. Roquedo sobre la Venta del Molinillo (Diezma, Granada) (19,8 mm Ø); G. Roquedo sobre la Venta del Molinillo (Diezma, Granada) (22,3 mm Ø); H. Finca La Ermita (locus typicus), junto a Venta del Molinillo (18,9 mm Ø); I. Finca La Ermita junto a Venta del Molinillo (18,7 mm Ø); J. Finca La Ermita, junto a Venta del Molinillo (19,5 mm Ø); K. Sierra de los Dientes de La Vieja (24,6 mm Ø). Fig. 3. Shell of Iberus angustatus: A–B. Lectotype (SMF 7111; 21.8 mm Ø; photographed by S. Hof, Naturmuseum Senckenberg, Frankfurt, Germany); C. Paralectotype (SMF 7912; 22.2 mm Ø); D–E. Rock mountain above Venta del Molinillo (Diezma, Granada) (locus typicus) (23.1 mm Ø and 11.7 mm h); F. Rock mountain above Venta del Molinillo (Diezma, Granada) (19.8 mm Ø); G. Rock mountain above Venta del Molinillo (Diezma, Granada) (22.3 mm Ø); H. Finca La Ermita (locus typicus), next to Venta del Molinillo (18.9 mm Ø); I. Finca La Ermita next to Venta del Molinillo (18.7 mm Ø); J. Finca La Ermita, next to Venta del Molinillo (19.5 mm Ø); K. Sierra de los Dientes de la Vieja (24.6 mm Ø).

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que ''En mi opinión existen solo dos ejemplares del mismo [caracol], es decir, como variedad descrita con la anotación ''raro'' sobre roca calcárea del S. de los Dientes de la Vieja, entre Granada y Dierma (error por Diezma)''. Si, debido a sus cinco bandas, no se identificase inicialmente como un Archelix [= Otala Schumacher] se podría caer en la tentación de tomarlo por un pariente de H. intermedia [= Chilostoma intermedius (Pfeiffer)], ya que tiene la misma morfología y su ombligo también es bastante ancho. Lo considero como la pareja española [en el sentido de estar em� parentado con] de H. niciensis [= Macularia niciensis (Férussac)]. Presupongo ahora que este H. Guiraorana [= Iberus guiraoanus (Rossmässler)] no solo tiene el ombligo medio cubierto, y algo más ancho, como los presentes ejemplares, sino que el ombligo también aparece completamente tapado y que las últimas for� mas podrían parecerse a H. hispanica [= Allognathus (Iberellus) hispanicus hispanicus (Rossmässler)] o H. loxana [= Iberus loxanus (Rossmässler)], como es el caso de estos últimos''. El elevado número de ejemplares de I. angustatus recogidos en la localidad tipo (Roquedo sobre la Venta del Molinillo y Finca la Ermita) y en sus al� rededores (cima de la Sierra de los Dientes de la Vieja) ha permitido analizar la variabilidad de este carácter. De acuerdo con nuestras observaciones la mayor parte de los especímenes presentan un ombligo completamente cubierto por la reflexión del borde columelar del peristoma o poseen una estre� cha fisura que deja entrever una mínima porción del interior del ombligo (figs. 3G, 3I–3J), aproximándose a la morfología de I. loxanus, como señaló Schmidt (1853). Mucho menos frecuentes son las conchas con la mitad del ombligo al descubierto (fig. 3F). En numerosos ejemplares la rotura de la parte externa de peristoma situada sobre el área umbilical produ� ce la falsa sensación de la existencia de un amplio ombligo abierto (figs. 3B, 3E, 3H, 3K). Solamente un ejemplar, el paratipo SMF 7912, presenta un ombligo completamente abierto comparable a los de I. guiraoanus (fig. 3C). Como puede observarse en las conchas figuradas, la mayor o menor cobertura del ombligo está directamente relacionada con el grado de reflexión del borde columelar del peristoma, poco reflejado cuando el área umbilical está abierta o semicerrada (figs. 3B–3C, 3E–3F) y muy reflejado cuando el ombligo aparece casi o completamente cubierto (figs. 3G, 3I–3J). Discusión Los resultados obtenidos muestran, una vez más, la necesidad de revisar exhaustivamente las fuentes originales, por difíciles de obtener que sean, para establecer la procedencia de las especies descritas por los autores clásicos, que muchas veces es difícil de precisar dificultando la actualización taxonómica. En el caso concreto de I. angustatus, la información que ha permitido localizar la localidad tipo no estaba contenida en una obra científica, sino en un libro de viajes en el que el autor de la especie refería sus

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vivencias y opiniones y que aparentemente presenta más interés para un sociólogo que para un investiga� dor en Zoología o Botánica. El conocimiento de esta localidad tipo ha permitido la recolección de topotipos y clarificar la posición taxonómica, dentro del género Iberus, de la especie Helix Guiraoana var. angustata. El análisis molecular de un ejemplar vivo recogido en la localidad tipo permite validar la identificación de H. Guiraoana var. angustata con el clado 4 del género Iberus de Elejalde et al. (2008) y la propuesta de estos autores de nombrar dicho clado 4 como I. angustatus. Precisamente el ejemplar con mayor coincidencia en el ADN con el topotipo estudiado por nosotros es I. angustatus–03, que fue recogido por Elejalde et al. (2008) en la provincia de Granada, en la cuadrícula U.T.M. contigua a la de la localidad tipo de H. Guiraoana var. angustata. El escaso material que compone la serie tipo de H. Guiraoana var. angustata (dos ejemplares en el SMF) había planteado dudas a los autores sobre la identificación de esta especie. El nuevo material recogido en la localidad tipo y en sus proximidades permite observar la extraordinaria variabilidad de su área umbilical. El morfotipo más frecuente, con el ombligo cerrado o con una estrecha fisura, no está representado en la serie tipo, compuesta por un ejemplar con el borde columelar roto y con el ombligo inicialmente semicubierto y otro ejemplar con el ombligo abierto. De acuerdo con nuestros datos, I angustatus presenta la máxima variabilidad en este carácter dentro de las especies del género Iberus. Conclusiones La localidad tipo de Helix Guiraoana var. angustata corresponde a las ''alturas situadas en los alrede� dores de la Venta del Molinillo cerca de los Dientes de la Vieja, Diezma, Granada'', de acuerdo con la descripción del viaje realizado por Rossmässler en 1853 por el SE de España. El análisis molecular permite confirmar la iden� tificación del clado 4 del estudio del género Iberus realizado por Elejalde et al. (2008) y validar la deno� minación de I. angustatus para esta especie. I. angustatus presenta una elevada variabilidad en la morfología del área umbilical, relacionada con el grado de reflexión del borde columelar del peristoma. Agradecimientos Al Dr. Ronald Janssen, conservador de Moluscos del Senckenberg Forschungsinstitut und Naturmuseum de Frankfurt am Main (Alemania) por la cesión del material tipo y a S. Hof, también del SFM, por la realización de algunas de las fotografías de dicho material. También a nuestro querido compañero de muestreo Antonio López Alabau por su gran e incansable ayuda. A nuestros amigos Patricia Pérez Rovira y Hubert Hanrath por su ayuda en la traducción del texto en alemán. Finalmente a los técnicos de la Sección de Genómica del SCSIE de la Universitat de

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València, donde se ha realizado el análisis molecular. Por úlimo agradecemos a los revisores anónimos su contribución a la mejora del manuscrito. Referencias Elejalde, M. A., Madeira, Mª J., Arrébola, J. R., Muñoz, B. & Gómez�� –Moliner, B. J., 2008. Molecular �� phy� logeny, taxonomy and evolution of the land snail genus Iberus (Pumonata: Helicidae). Journal of Zoological Systematics and Evolution Research, 46(3): 193–202. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijen� hoek R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3: 294–299. Martínez�� –�� Ortí, A. & Robles, F., 2012. On the taxo� nomical identity of some taxa of the Iberian en� demic genus Iberus Montfort, 1810 (Gastropoda, Helicidae). Animal Biodiversity and Conservation, 35(1): 99–106. (http://abc.museucienciesjournals. cat/files/ABC_35-1_pp_99-106.pdf) Mellado, F. de P., 1852. Guía del viagero (sic) en España. 5ª ed. VIII+514 pp. Establecimiento tipográfico de Mellado, Madrid. (http://books.google.es/books/ about/Gu%C3%ADa_del_viagero_en_Espa% C3%B1a.html?hl=es&id=cRhAAAAAIAAJ) Palumbi, S. R., Martin, A. P., Romano, S., McMillan, W. O., Stice, L. & Grabowski, G., 1991. The Simple Fool�� ’�� s Guide to PCR (Special Publication). Depart�

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ment of Zoology, University of Hawaii, Honolulu. Rossmässler, E. A., 1853a. Briefe aus Spanien. Zeitschrift für Malakozoologie, 10(7): 97–105. (http:// www.biodiversitylibrary.org/item/55066) –�� 1853b. Kurzer Bericht über meine malakozoolo� gische Reise durch einen Theil des südöstlichen Spanien. Zeitschrift für Malakozoologie, 10(11): 161– 171. (http://www.biodiversitylibrary.org/item/55066) – 1854a. Iconographie der Land-und SüsswasserMollusken Europa’s, mit vorzüglicher Berücksichtigung kritischer und noch nicht abgebildeten Arten, 3(1–2): 1–31. H Constenoble Ed., Leipzig. – 1854b. Reise-Erinnerungen aus Spaniens. Vol. 1: XVI+247 pp., vol. 2: 269 pp., 1 mapa. H. Costeno� ble Ed., Leipzig. (vol. 2: http://www.bsb-muenchendigital.de/~web/web1045/bsb10456591/images/ index.html) – 1857. Reise-Erinnerungen aus Spaniens. Zweite unveränderte Auflage. Vol. 1: XVI+247 pp., vol. 2: 269 pp., 1 mapa. H. Costenoble Ed., Leipzig (vol.1: https://ia700302.us.archive.org/19/items/reiseerin� nerung00rossgoog/reiseeri nnerung00rossgoog.pdf) – 2010. Recuerdos de un viajero por España. Trad. I. Prüfer Leske. CSIC. Ediciones Polifemo, Madrid. Schmidt, A., 1853. Bemekungen zu dem vorstehenden Aufsatze des Herrn Prof. Rossmässler. Zeitschrift für Malakozoologie, 10(11): 171–176. (http://www. biodiversitylibrary.org/item/55066) SIGPAC, 2012. Sistema de Identificación Geográfica de Parcelas Agrícolas. Ministerio de Agricultura, Alimentación y Medio Ambiente (http://sigpac. mapa.es/fega/visor/)

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Spatial distribution patterns of terrestrial bird assemblages on islands of the Sabana–Camagüey Archipelago, Cuba: evaluating nestedness and co–occurrence patterns C. A. Mancina, D. Rodríguez Batista & E. Ruiz Rojas Mancina, C. A., Rodríguez Batista, D. & Ruiz Rojas, E., 2013. Spatial distribution patterns of terrestrial bird assemblages on islands of the Sabana–Camagüey Archipelago, Cuba: evaluating nestedness and co–occurrence patterns. Animal Biodiversity and Conservation, 36.2: 195–207. Abstract Spatial distribution patterns of terrestrial bird assemblages on islands of the Sabana–Camagüey Archipelago, Cuba: evaluating nestedness and co–occurrence patterns.— Using distribution data of 131 terrestrial bird species on 17 islands of the Archipelago Sabana–Camagüey, Cuba, we tested for non–randomness in presence–absence matrices with respect to co–occurrence and nestedness. We conducted separate analyses for the whole assemblage and sub–matrices according to trophic levels and residence status (breeding and migratory). We also explored the influence of weighting factors such as island area and isolation. The C–occurrence analyses were susceptible to the species subsets and the weighting factors. Unweighted analyses revealed a significant negative co–occurrence pattern for the entire assemblage and for most sub–matrices. The area weighted analyses always indicated strong non–random structure. However, an analysis with intra–guild species pairs showed that most pairs were randomly assembled; very few pairs had a significant segregated pattern. Bird assemblages followed a nested subset structure across islands. Nestedness was strongly correlated with area and unrelated with island isolation. Overall, this study suggests that terrestrial bird assemblages were shaped by extinction processes mediated through area effects rather than interspecific trophic guild competition. Data suggest that conservation of largest islands will guarantee high terrestrial bird richness on the archipelago. Key words: Archipelago, Birds, Community ecology, Cuba, Macroecology, Null models. Resumen Patrones de distribución espacial de las agrupaciones de aves terrestres en las islas del archipiélago Sabana–Camagüey, Cuba: evaluación de los patrones de anidamiento y de coexistencia.— Se emplearon datos de distribución de 131 especies de aves terrestres en 17 islas del archipiélago Sabana–Camagüey para analizar la no aleatoriedad en las matrices de presencia y ausencia con respecto a la coexistencia y el anidamiento. Los análisis se realizaron para todo el conjunto y para submatrices por grupos tróficos y estados de residencia (especies migratorias y reproductivas). Además, se analizó la influencia de factores de ponderación, como el área y el aislamiento de las islas. El patrón de coexistencia fue sensible a los grupos de especies y los factores de ponderación. Los análisis no ponderados revelaron un patrón de coexistencia significativamente negativo para todo el conjunto y la mayoría de los grupos. Cuando se usó el área de las islas como factor siempre se observó una estructura no aleatoria de las agrupaciones. Sin embargo, dentro de los gremios tróficos la mayoría de los pares de especies mostraron un patrón aleatorio y muy pocos pares tuvieron un patrón significativamente segregado. La distribución de las aves terrestres sigue una estructura anidada. El anidamiento estuvo fuertemente correlacionado con el área y no presentó relación con el aislamiento de las islas. De manera general este estudio sugiere que las agrupaciones de aves terrestres en este archipiélago están más estructuradas por procesos de extinción selectiva relacionados con el área de las islas, que por la competición interespecífica dentro de gremios tróficos. Los datos sugieren que la conservación de las islas de mayor área podría garantizar una elevada riqueza de especies en el archipiélago. Palabras claves: Archipiélago, Aves, Ecología de comunidades, Macroecología, Modelos nulos. ISSN: 1578–665 X eISSN: 2014–928 X

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Received: 30 VII 12; Conditional acceptance: 11 I 13; Final acceptance: 24 X 13 Carlos A. Mancina & Daysi Rodríguez Batista, Inst. de Ecología y Sistemática, carretera de Varona km 3 ½ Capdevila, Boyeros, A. P. 8029, C. P. 10800, La Habana, Cuba; Edwin Ruiz Rojas, Centro de Estudios y Servicios Ambientales, Villa Clara (Cuba). Corresponding author: Carlos A. Mancina. E–mail: mancina@ecologia.cu

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Introduction Recognition of patterns in ecological communities and understanding the mechanisms that produce these patterns are fundamental goals of ecology and conservation biology. An essential question is whether communities are composed of random species assemblages or whether deterministic processes such as competition influence the composition of species within communities. Diamond (1975) expanded this approach with his analyses of the distribution of terrestrial bird species on islands of the Bismarck Archipelago. He found that interspecific interactions determine non– random co–occurrence patterns and proposed rules known as assembly rules, including the checkerboard distribution, forbidden species combinations, and so on. Diamond`s rules and other more recent community assembly rules (such as favored states, food–web structure, guild proportionality, and nested subset) are frequently examined in studies of metacommunities and community ecology (Fortuna et al., 2010; Beaudrot et al., 2013; Henriques–Silva et al., 2013). Many studies have relied on null models to test the community structure. Null models are randomization methods that exclude a target mechanism to determine whether a specific no–random pattern can be generated (Connor & Simberloff, 1979; Gotelli & Graves, 1996).Two of the most widely applied models are species co–occurrence (Gotelli, 2000) and nestedness (Patterson & Atmar, 1986). The co–occurrence patterns are attributed to competitive inter–specific interactions or environmental factors. Several co–occurrence indices are used to quantify patterns in presence–absence matrices, in many instances relating the observed patterns to Diamond`s assembly rules (Gotelli & McCabe, 2002; Collins et al., 2011; Wang et al., 2011). Nested species subsets are a common pattern of community assembly characteristic of many types of fragmented landscapes and insular systems. Nestedness is a condition in which species distributions occur hierarchically so that the fauna of species–poor islands comprise a perfect subset of the fauna on increasingly species–rich islands (Ulrich et al., 2009). In contract with co–occurrence models, nestedness is not directly related to competition events such as the structuring mechanism of communities. Rather, nested patterns could be related with differential colonization or extinction of species, passive sampling, and carrying capacities, distance or area effects (Patterson & Atmar, 1986; Wright et al., 1998; Ulrich et al., 2009). Many studies of avian communities on archipelagos or isolated habitats have shown more segregated patterns of co–occurrence than expected by chance, suggesting that interespecific interactions are an underlying mechanism in structuring of bird communities (Stone & Roberts, 1992; Gotelli & McCabe, 2002; Feeley, 2003). Besides, nested patterns of insular bird assemblages are common and have been related to extinction and colonization processes (Lomolino, 1996), habitat nestedness (Calmé & Desrochers, 1999; Wang et al., 2011) and passive sampling (Wright et al., 1998). The Sabana–Camagüey Archipelago (hereafter SCA) constitutes the largest system of islands or cays

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in the Caribbean region (Alcolado et al., 2007). Several studies have contributed to the knowledge of avian richness of some islands (e.g. Garrido, 1973; Sánchez et al., 1994; Wallace et al., 1996, 1999; Rodríguez, 2000; Sánchez & Rodríguez, 2001; González et al., 2008), and 241 bird species have been reported from this archipelago, representing 65% of the whole Cuban ornithofauna (Rodríguez et al., 2007). However, the distribution patterns and factors that determine the species richness on these islands remain unexplored. The high species richness of birds, their geographic position, and the high number of islands that differ in area and landscape characteristics make this archipelago an appropriate scenario to test hypotheses on assembly and structure of bird communities. In this study, we used null model analysis to test for patterns of species co–occurrence and nestedness with data on presence–absence of terrestrial birds from a set of 17 islands from SCA. We explored the potential role of extinction and colonization events as underlying mechanism in the structure of bird assemblages by analyzing correlations of nestedness and island traits, such as area and isolation. Material and methods Study area and avifauna data The Sabana–Camagüey Archipelago (SCA) is a chain of 2,515 islands or cays along 465 km of the north coast of Cuba; total area of the SCA is c. 3,414 km2. The islands range in area from < 0.1 km2 to 680 km2 Cayo Romano, the largest island of the SCA. The landscape heterogeneity and flora diversity tend to be higher on larger islands such as Sabinal, Coco, Romano and Guajaba (Priego–Santander et al., 2004). The vegetation is diverse and several plant communities have been described for the SCA. The mangrove forest is widespread along coasts and constitutes the main coverage on the smallest islands. The most extensive plant formations are the semi–deciduous and dry evergreen forests, xerophytic scrubs, and sandy coastal vegetation (Alcolado et al., 2007). Data of bird communities across SCA were gathered from an extensive review of literature and our field data. Although information is available about the bird fauna of 86 islands, we selected only 17 islands because these have more complete information about their avian communities (largest number of surveys across several years and seasons). The selected islands range in area from 0.27 to 680 km2 and are separated between 0.5 and 33 km from the main island of Cuba (table 1, fig. 1). These variables were obtained from digital maps using the software DIVA–GIS v 7.5 (Hijman et al., 2005). We selected only terrestrial species because their assemblages should depend on the islands as breeding or feeding sites. The data were organized as a presence–absence matrix in which each row represents a species and each column an island. To ensure that the results were not biased by the inclusion of species with very different strategies in the habitat use, we

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Table 1. Characteristics of the study islands in the Sabana–Camagüey Archipelago and number of terrestrial birds on each island: A. Area (in km2); I. Isolation (in km); N. Number of species. (Isolation is given as the nearest distance to the main island of Cuba.) Tabla 1. Características de las islas estudiadas del archipiélago Sabana–Camagüey y número de especies de aves por islas: A. Área (en km2); I. Aislamiento (en km); N. Número de especies. (El valor de aislamiento es la distancia más cercana a la isla de Cuba.) Island

A (km2)

I (km)

2.29

5.47

Coco

334.52

21.43

117

Cruz

26.14

29.95

Ensenachos

1.45

27.75

Fábrica

0.79

4.07

Francés

6.22

26.66

Guajaba

105.2

10.47

Guillermo

15.65

24.42

Las Brujas

7.23

24.79

Lucas

3.16

5.74

Mégano Grande

7.55

31.8

Aguada

Palma

0.27

0.49

Paredón Grande

10.71

32.99

Romano

680

14.16

Sabinal

338.3

2.16

Salinas

1.08

4.72

Santa María

21.9

28.69

generated presence–absence submatrices for two species subsets: 1) breeding vs. migratory species (including winter residents), and 2) four trophic guilds of breeding birds (omnivores, predators, insectivores and phytophagous) based on our field observations and published data (e.g. Kirkconnell et al., 1992). Vagrants, transients or very rare migrants in the Cuban archipelago were excluded from data analyses (Llanes et al., 2002; Garrido & Kirkconnell, 2010). Co–occurrence and nestedness analysis To estimate whether bird species co–occurred more or less than expected by chance, we used the checkerboard score (C–score) index (Stone & Roberts, 1990). C–score measures the average number of 'checkerboard units' among all possible pairs of species. This index measures the extent to which species

are segregated across islands but does not require perfect checkerboard distributions; the C–score should be significantly larger than expected by chance in communities structured by interspecific interactions (Gotelli, 2000). The C–score index was compared to those of 5,000 randomly assembled communities using the software EcoSim 7.0 (Gotelli & Entsminger, 2001). We used the sequential–swap algorithm to generate random null matrices (Manly, 1995). Simulated matrices were generated under two null models that differ in the way row and column totals are treated: 1) a fixed–fixed (FF) algorithm, where both the row and the column totals of the original matrix are fixed (the biological justification for this model is that it preserves in the null matrices the observed differences between sites in species richness —column totals— and observed differences among species in their frequency of occurrence or row totals, Gotelli, 2000); and 2) a fixed–weighted (FW) algorithm (Gotelli & Entsminger, 2001; Jenkins, 2006), where columns are weighted by factors that during randomization contribute to inter–island differences in community composition. We separately used two weighting factors: the island area (FWarea) and the distance (FWisolation) from the main island of Cuba (used as an isolation criterion). We calculated a standardized effect size (SES) as ([observed score–mean simulated score]/standard deviation of simulated score); SES indicates the number of standard deviations that the observed index is above or below the mean index of simulated matrices. Non–random matrices generally have SES for the C–score > |2| (Gotelli & McCabe, 2002). In addition, we used Bayes methods implemented by Gotelli & Ulrich (2010) to identify particular species pairs for each trophic guild that contributes to observed patterns, and to determine those random, segregated or aggregated species pairs. We used the criteria mean–based (Bayes M criterion) and conﬁdence interval (Bayes CL criterion) (Gotelli & Ulrich, 2010) calculated with the software 'Pairs' (Ulrich, 2008). For nestedness analysis, we used a metric–based on overlap and decreasing fill, NODF (Almeida–Neto et al., 2008). NODF calculates nestedness independently among rows and columns, evaluating nestedness only among islands (i.e. species richness) or only among species (i.e. species occupancy). NODF varies from 0 to 100 and higher values indicate more nested assemblage. The nestedness significance was estimated on 1,000 random matrices. We used a null model with a fixed–equiprobable algorithm, where the number species in an island is allowed to vary during randomization; this random model represents a scenario where the probability of colonization of all species is equal for all islands (Gotelli, 2000; Ulrich et al., 2009). Nestedness analyses and randomizations were conducted using the software 'NODF' (Almeida–Neto & Ulrich, 2011). To explore the role of extinction and colonization events upon nestedness we used Spearman rank correlations between island rank order in the maximally packed matrix, and island area and isolation, respectively (Patterson & Atmar, 2000). This method has

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199

N Las Brujas Francés

Aguada Lucas

Ensenachos Santa María Guillermo Coco

Fábrica

Paredón Grande

Palma

Mégano Grande

Salinas

Cruz Romano

Cuba Guajaba Sabinal 0

60 km

Fig. 1. Map of the Sabana–Camagüey Archipelago, Cuba; islands included in the study are named. Fig. 1. Mapa del archipiélago Sabana–Camagüey, Cuba; se indican las islas incluidas en el estudio.

proven useful for indicating the possible mechanisms involved in a nested pattern; for example, a significant correlation between isolation and maximal nestedness will be related with immigration or colonization events. However, correlation with the island area suggests that extinction processes should determine the nested pattern (Lomolino, 1996; Patterson & Atmar, 2000; Fernández–Juricic, 2002). Results A total of 131 terrestrial bird species were found to inhabit the islands considered in this study (appendix 1). There are similar numbers of breeding (67 species, 51.2%) and migrant (64 species, 48.8%) species; the species number ranges from 24 to 117 species across islands (table 1). Species richness on the islands is significantly correlated with island area (p < 0.001; both variables in logarithm) which explained 56% of the variance. Species richness is not correlated with the island isolation (p = 0.7). Co–occurrence patterns Our results were influenced by the type of null model algorithm used (table 2). The observed C–scores for most subsets, under the F–F model, were signiﬁcantly higher than expected by chance, suggesting segrega-

ted patterns of species co–occurrence. The C–score did not differ from null model figures only for phytophagous and predators, indicating random species co–occurrence. When the island area was used as a weighting factor (FWarea), all subsets were signiﬁcant (segregated patterns), being stronger (Z value > 10) for the whole assemblage, and for breeding and omnivorous species. On the other hand, when using isolation as the weighting factor (FWisolation) the null hypothesis was not rejected, suggesting random co–occurrence patterns. The C–score was found to be marginally significant only for the omnivorous species (observed score = 5.27, expected score = 3.92, p = 0.04), suggesting a weak pattern of interspecific segregation. Analysis of species pairs showed that most of them were randomly assembled. For each trophic guild, very few pairs had a significant segregated pattern. Neither species pairs showed an aggregated pattern. The highest percentage of species pairs occurred for omnivorous and insectivorous species; the Bayes conﬁdence interval criterion identified only 4.5% and 2.2% of segregated pairs, respectively. Table 3 shows the significantly segregated species pairs with highest values of C–Score; other species–pairs such as Gray Kingbird (Tyrannus dominicensis) – Oriente Warbler (Teretistris fornsi), Mangrove Cuckoo (Coccyzus minor) – Cuban Tody (Todus multicolor), and Smooth Billed Ani (Crotophaga ani) – Bahama Mockingbird (Mimus gundlachii), had values significantly

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Table 2. Results from the analysis of species co–occurrence of terrestrial bird assemblages inhabiting 17 islands of the Sabana–Camagüey Archipelago. The observed C–Score, the values expected by chance, and standardized effect size (in parentheses) are shown for each species subset. (Significant results in bold.) Tabla 2. Resultados de los análisis de coexistencia de las especies en las agrupaciones de aves terrestres que habitan en las islas del archipiélago Sabana–Camagüey. Para cada subgrupo de especies se muestran el valor del conteo C observado, los valores esperados por efecto del azar y el valor del tamaño del efecto estandarizado (entre paréntesis). (Los resultados significativos se indican con negritas.) Subset (# species)

Observed

Simulated C–scores

C–score

F–F

FWarea

FWisolation

All species (131)

3.41

3.18 (6.61)

1.02 (19.98)

3.98 (–2.65)

Migratory (64)

2.71

2.55 (2.65)

1.19 (7.62)

5.11 (–6.73)

Breeding (67)

2.83

2.61 (5.17)

0.85 (13.21)

3.04 (–0.74)

Phytophagous (16)

0.82

0.71 (1.27)

0.37 (2.36)

1.43 (–1.68)

Omnivorous (15)

5.27

4.86 (2.54)

1.02 (11.22)

3.92 (1.76)

Predators (10)

2.22

2.08 (0.72)

0.92 (2.63)

3.82 (–1.61)

Insectivorous (14)

2.84

2.60 (2.13)

0.93 (5.22)

2.33 (0.81)

(columns) was higher than the degree of nestedness in species occupancy (rows) for whole assemblage and for migratory and breeding subset separately (table 4). Spearman rank correlations between species order in the maximally nested matrix with island area and isolation indicate that area is the most important factor in nestedness (table 5). The analysis suggests that the distance to main island of Cuba has no influence on the degree of nestedness of avian assemblages from the Sabana–Camagüey Archipelago.

segregated but with low C–scores, suggesting weakly segregated patterns between these species pairs. Nestedness The entire community of terrestrial birds showed a significantly nested pattern (NODF = 78.41, p < 0.0001). The breeding subset of bird species showed higher degrees of nestedness than the migratory assemblage. The degree of nestedness of species richness among islands

Table 3. Species pairs with the highest and most significant figures of C–Score (Obs.) denoting segregated distribution patterns. The number of occurrences and the number of islands with joint occurrences (U) are shown in brackets. For each species pairs, the values expected by chance (Sim.) and standardized effect size (SES) are shown. Tabla 3. Parejas de especies con los índices de conteo C (Obs.) más elevados y significativos, indicando patrones significativamente segregados. Se muestran entre paréntesis el número de observaciones y la cantidad de islas donde coexisten (U). Para cada pareja de especies se muestra los valores esperados por efecto del azar (Sim.) y el valor del tamaño del efecto estandarizado (SES). Species 1

Species 2

Obs.

Sim. (SES)

Mimus gundlachii (8)

Dives atroviolaceus (5)

1.0

0.212 (5.42)

Mimus gundlachii (8)

Priotelus temnurus (4)

1.0

0.215 (4.88)

Icterus melanopsis (7)

Dives atroviolaceus (5)

0.68

0.227 (3.07)

Glaucidium siju (9)

Accipiter striatus (3)

0.59

0.082 (3.79)

Geotrygon chrysia (7)

Tiaris bicolor (3)

0.57

0.072 (4.31)

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Table 4. Results of nestedness analyses for the terrestrial bird assemblages on islands of the Sabana– Camagüe Archipelago. The table shows observed (NODFobs) and expected by chance (NODFsim) values, and also the degree of nestedness independently for columns and rows. (The standardized effect size is shown in brackets; all combinations were significantly nested, in bold.) Tabla 4. Resultados de los análisis de anidamiento de las agrupaciones de aves terrestres en las islas del archipiélago Sabana–Camagüey. Se muestran los valores del índice observado (NODFobs) y los valores esperados por efecto del azar (NODFsim), así como el grado de anidamiento para filas y columnas de forma independiente. (Entre paréntesis se muestra el valor del tamaño del efecto estandarizado; todas las combinaciones fueron significativamente anidadas, en negrita.)

Total NODFobs

Columns

NODFsim

NODFobs

Rows

NODFsim

NODFobs

NODFsim

All species

78.41

61.26 (72.75)

83.58

62.79 (11.62)

78.32

61.23 (73.2)

Migratory

78.15

51.36 (49.43)

80.47

53.12 (13.29)

78.00

51.24 (55.17)

Breeding

84.46

69.13 (31.37)

86.15

68.75 (6.88)

84.36

69.15 (37.64)

Discussion Our analyses show that terrestrial bird species co– occurred less frequently than expected by chance on islands from the Sabana–Camagüey Archipelago, suggesting that these avian communities are probably structured by negative interspecific interactions. However, similar to other studies (e.g. Meyer & Kalko, 2008), the results were susceptible to the species subsets and the weighting factors. When the fixed–fixed model was used we found random co–occurrence patterns for predators and phytophagous species. However, using area as weighting, all subsets showed significant segregated co–occurrence patterns. Contrarily, weighting analyses by island isolation showed random patterns for most species subsets. This result suggests that because of the short distance between the archipelago and the main island of Cuba, the differential dispersal abilities of the bird species would not be an important factor in the structure of the avian assemblages. On the other hand, island area and other attributes associated with of area, such as landscape diversity or the number of plant formations (see Priego–Santander et al., 2004), have a more important role structuring the bird communities of the Sabana–Camagüey Archipelago. Although the avifauna assemblages showed a wide segregated pattern, we found that species pairs, within each trophic guild, showed random patterns. This result suggests competitive exclusion could be rare in these bird assemblages. A similar result was obtained for other avifauna on archipelagos (Gotelli & Ulrich, 2010; Collins et al., 2011), and might reflect widespread, but weak species interactions or mechanisms of species segregation that are not related to direct species interactions but to historical events or resource abundance (Gotelli & McCabe, 2002; Gotelli & Ulrich, 2010).

The analyses indicate a strong nested structure in the entire assemblage and for breeding and migratory birds. Common and widespread species (e.g. Greater Antillean Grackle, Cuban Emerald, Yellow Warbler, etc.) tended to comprise the avifauna of islands with lesser species richness, while richer islands included these species in addition to other rare species or with restricted ranges. We found that island nested rank order was significantly correlated with the rank order of island area but not with island isolation. This result, together with the significant species–area relationship, suggests that the terrestrial bird assemblages at SCA are structured through

Table 5. Results of Spearman Rank correlations of island order in the maximally nested matrix with the values of area and isolation; p values were generated by 1,000 Monte Carlo simulations: A. Area; I. Isolation. Tabla 5. Resultados de la correlación por rangos de Spearman entre los valores ordinales que le corresponde a cada isla en la matriz de máximo anidamiento y sus valores de área y aislamiento; los valores p fueron generados por 1.000 simulaciones de Monte Carlo: A. Área; I. Aislamiento. Subset

A rs

I rs

All species –0.76

0.0003

0.078 0.76

Migratory

–0.74

0.0005

–0.24 0.34

Breeding

–0.73 0.00004

0.16 0.53

202

local extinction rather than through colonization or immigration processes from the main island of Cuba (Lomolino, 1996; Wright et al., 1998). The lower nested pattern observed in the migratory assemblages would be related to habitat generalists with high dispersal abilities (e.g. some wintering migrant passerines such as Black and White Warbler, Palm Warbler, American Redstart; Rappole, 1995; Wallace et al., 1996; Latta et al., 2003). The highest nested patterns of breeding birds would be related to the low habitat diversity or limited resource abundance on the small islands, although these would be limiting factors mainly for those breeding species with large area requirements or habitat specialists (e.g. Gundlach`s Hawk, Zapata Sparrow, Fernandina`s Flicker, Cuban Grassquit, etc.). Among the islands smaller than 15 km2, Cayo Paredón Grande had the highest species richness, with 84 bird species. This island has unusually high landscape heterogeneity and floristic diversity (Priego–Santander et al., 2004), supporting the idea that habitat diversity is an important factor in explaining the distribution and species richness on the archipelago. Ours results are consistent with several studies that show that nested avian assemblages on islands or fragmented habitat are apparently shaped by selective extinction processes through island or patch area and the habitat diversity effects rather than interspecific guild competition. (Fernández–Juricic, 2000; Feeley, 2003; Wang et al., 2011). The strong nested patterns and significant species–area relationships of the avian assemblages suggest, from a conservation perspective, that the protection of the largest islands with the most species rich assemblages (e.g. Romano, Sabinal, Coco, Guajaba and Santa María) will warrant high terrestrial bird richness. However, an adequate conservation strategy will be to conserve small and large islands with the purpose of maintaining a high heterogeneity in the environmental conditions on the Sabana–Camagüey Archipelago (Fischer & Lindenmayer, 2005). Acknowledgements We are grateful to Luis M. Carrascal, Eduardo E. Iñigo–Elias and Cayetano Casado for their reviews and constructive comments on drafts. References A.O.U. (American Ornithologist Union), 2011. Check– list of North American Birds. http://www.aou.org/ checklist Alcolado, P., García, E. E. & Arellano–Acosta, M., 2007. Ecosistema Sabana–Camagüey. Estado actual, avances y desafíos en la protección y uso sostenible de la biodiversidad. Editorial Academia. La Habana. Almeida–Neto, M., Guimaraes, P., Guimaraes, P. R., Loyola, R. D. & Ulrich, W., 2008. A consistent metric for nestedness analysis in ecological systems:

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las comunidades de aves en tres formaciones vegetales de Cayo Coco, Archipiélago de Sabana–Camagüey, Cuba. Ph D. Thesis, Instituto de Ecología y Sistemática, La Habana, Cuba. Rodríguez, D., Martínez, M., Arias, A., Ruiz E., Llanes, A., Pérez, E., Rodríguez, P., Socarrás, E., González, H., Parada, A., Barrios, O., Vilma, E., Chamizo, A. & Mancina, C. A., 2007. Vertebrados terrestres. In: Ecosistema Sabana–Camagüey: Estado actual, avances y desafíos en la protección y uso sostenible de la biodiversidad: 31–37 (P. M. Alcolado, E. E. García & M. Arellano–Acosta, Eds.). Editorial Academia, La Habana. Sánchez, B. & Rodríguez, D., 2001. Avifauna associated with the aquatic and coastal ecosystems of Cayo Coco, Cuba. Pitirre, 13: 68–75. Sánchez, B., Rodríguez, D. & Kirkconnell, A., 1994. Avifauna de los cayos Paredón Grande y Coco durante la migración otoñal de 1990 y 1991. Avicennia, 1:31–38. Simaiakis, S. M., Dretakis, M., Barboutis, C., Katritis, T., Portolou, D. & Xirouchakis, S., 2012. Breeding land birds across the Greek islands: a biogeographic study with emphasis on faunal similarity, species–area relationships and nestedness. Journal of Ornithology. DOI: 10.1007/ s10336–011–0803–1 Stone, L. & Roberts, A., 1990. The checkerboard score and species distributions. Oecologia, 85: 74–79. – 1992. Competitive exclusion or species aggregation? An aid in deciding. Oecologia, 91: 419–424. Ulrich, W., 2008. Pairs – a FORTRAN program for studying pair–wise species associations in ecological matrices. www.uni.torun.pl/~ulrichw Ulrich, W., Almeida–Neto, M. & Gotelli, N. J., 2009. A consumer’s guide to nestedness analysis. Oikos, 118: 3–17. Wallace G. E., González, H., McNicholl, M. K., Rodríguez, D., Oviedo, R., Llanes, A. & Sánchez, B., 1996. Winter surveys of forest–dwelling neotropicalmigrant birds and resident birds in three regions of Cuba. The Condor, 98: 745–768. Wallace, G. E., Wallace, E. A. H., Froehlich, D. R., Ealker, B., Kirkconnell, A. & Socarrás, E., 1999. Hermit Thrush and Black–throated Gray Warbler, new for Cuba, and other significant bird records from Cayo Coco and vicinity, Ciego de Avila province, Cuba, 1995–1997. Florida Field Naturalist, 27: 37–51. Wang, Y., Chen, S. & Ding, P., 2011. Testing multiple assembly rule models in avian communities on islands of an inundated lake, Zhejiang Province, China. Journal of Biogeography, 38: 1330–1344. Wright, D. H., Patterson, B. D., Mikkelson, G., Cutler, A. & Atmar, W., 1998. A comparative analysis of nested subset patterns in species composition. Oecologia, 113:1–20.

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Appendix 1. List of terrestrial bird species included in this study, ordering species according to the maximally nested matrix. Status (B. Breeding, M. Migratory). Trophic group (TG: O. Omnivores, P. Predators, I. Insectivores, Ph. Phytophagous). The last column shows the number of islands where each species was recorded. Nomenclature follows A.O.U. (2011). Apéndice 1. Listado de las especies de aves terrestres incluidas en este estudio, ordenadas acorde a su posición en la matriz de máximo anidamiento. Status (B. Reproductora, M. Migratoria). Grupo trófico (TG: O. Omnívora, P. Depredadora, I. Insectívora; Ph. Fitófaga). En la última columna se indica el numero de islas donde la especie han sido registrada. Taxonomía según la A.O.U. (2011). Common name

Scientific name

Status

Greater Antillean Grackle Turkey Vulture

Islands

Quiscalus niger

Cathartes aura

White Crowned Pigeon

Patagioenas leucocephala

Cuban Pewee

Contopus caribaeus

Cuban Emerald

Chlorostilbon ricordii

Commonm Ground Dove

Columbina passerina

Yellow Warbler

Setophaga petechia

Yellow–faced Grassquit

Tiaris olivaceus

American Kestrel

Falco sparverius

Black and White Warbler

Mniotilta varia

Northern Mockingbird

Mimus polyglottos

Palm Warbler

Setophaga palmarum

American Redstart

Setophaga ruticilla

Western Spindalis

Spindalis zena

La Sagra's Flycatcher

Myiarchus sagrae

Cuban Bullfinch

Melopyrrha nigra

Ovenbird

Seiurus aurocapilla

Cuban Green Woodpecker

Xiphidiopicus percussus

Gray Kingbird

Tyrannus dominicensis

White–winged Pigeon

Zenaida asiatica

Loggerhead Kingbird

Tyrannus caudifasciatus

Black–throated Blue Warbler

Setophaga caerulescens

Common Yellowthroat

Geothlypis trichas

Mourning Dove

Zenaida macroura

Killdeer

Charadrius vociferus

Great Lizard–Cuckoo

Coccyzus merlini

Gray Catbird

Dumetella carolinensis

Black–whiskered Vireo

Vireo altiloquus

Red–legge Thrush

Turdus plumbeus

Smooth Billed Ani

Crotophaga ani

Cuban Vireo

Vireo gundlachii

Yellow–bellied Sapsucker

Sphyrapicus varius

Zenaida Dove

Zenaida aurita

Northern Parula

Setophaga americana

Praire Warbler

Setophaga discolor

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Appendix 1. (Cont.) Common name

Scientific name

Status

Islands

Northern Waterthrush

Parkesia noveboracensis

Barn Owl

Tyto alba

Indigo Bunting

Passerina cyanea

West Indian Woodpecker

Melanerpes superciliaris

Yellow–throated Vireo

Vireo flavifrons

Yellow–throated Warbler

Setophaga dominica

Crested Caracara

Caracara cheriway

Merlin

Falco columbarius

Magnolia Warbler

Setophaga magnolia

Cape May Warbler

Setophaga tigrina

Red–tailed Hawk

Buteo jamaicensis

Mangrove Cuckoo

Coccyzus minor

Blue–gray Gnatcatcher

Polioptila caerulea

Peregrine Falcon

Falco peregrinus

Cuban Pygmy–Owl

Glaucidium siju

Cuban Tody

Todus multicolor

Blue Grosbeak

Passerina caerulea

Cave Swallow

Petrochelidon fulva

Painted Bunting

Passerina ciris

Antillean Nighthawk

Chordeiles gundlachii

Greater Antillean Nighthawk

Caprimulgus cubanensis

Bahama Mockingbird

Mimus gundlachii

Cuban Gnatcatcher

Polioptila lembeyei

Worm–eating Warbler

Helmitheros vermivorum

Northern Flicker

Colaptes auratus

White–eyed Vireo

Vireo griseus

Key West Quail–Dove

Geotrygon chrysia

Bobolink

Dolichonyx oryzivorus

Blackpoll Warbler

Setophaga striata

Yellow–billedCuckoo

Coccyzus americanus

Cuban Oriole

Icterus melanopsis

Oriente Warbler

Teretistris fornsi

Baltimore Oriole

Icterus galbula

Yellow–rumped Warbler

Setophaga coronata

Scarlet Tanager

Piranga olivacea

Chuck–will'swidow

Caprimulgus carolinensis

Rose–breasted Grosbeak

Pheucticus ludovicianus

Ruddy Quail–Dove

Geotrygon montana

Tawny–shouldered Blackbird

Agelaius humeralis

Cuban Blackbird

Dives atroviolaceus

Cuban Martin

Progne cryptoleuca

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Mancina et al.

Appendix 1. (Cont.) Common name

Scientific name

Status

Islands

Barn Swallow

Hirundo rustica

Tree Swallow

Tachycineta bicolor

Bay–breasted Warbler

Setophaga castanea

Bananaquit

Coereba flaveola

Prothonotary Warbler

Protonotaria citrea

Black–throated Green Warbler

Setophaga virens

Hooded Warbler

Setophaga citrina

Burrowing Owl

Athene cunicularia

Northern Harrier

Circus cyaneus

Cuban Crow

Corvus nasicus

Grasshopper Sparrow

Ammodramus savannarum

Eastern Meadowlark

Sturnella magna

Orchard Oriole

Icterus spurius

Blackburnian Warbler

Setophaga fusca

Swainson's Warbler

Limnothlypis swainsonii

Golden–winged Warbler

Vermivora chrysoptera

Bare–legged Owl

Gymnoglaux lawrencii

Summer Tanager

Piranga rubra

Cuban Trogon

Priotelus temnurus

Swainson`sThrush

Catharus ustulatus

Eastern Wood–Pewee

Contopus virens

Red–eyed Vireo

Vireo olivaceus

Scaly–naped Pigeon

Patagioenas squamosa

Gundlach's Hawk

Accipiter gundlachi

Broad–winged Hawk

Buteo platypterus

Black–faced Grassquit

Tiaris bicolor

Sharp–shinned Hawk

Accipiter striatus

Plain Pigeon

Patagioenas inornata

Savannah Sparrow

Passerculus sandwichensis

Chestnut–sided Warbler

Setophaga pensylvanica

Louisiana Waterthrush

Parkesia motacilla

Short–eared Owl

Asio flameus

Gray–cheeked Thrush

Catharus minimus

Kentucky Warbler

Geothlypis formosa

Orange–crowned Warbler

Oreothlypis celata

Tennessee Warbler

Oreothlypis peregrina

Nashville Warbler

Oreothlypis ruficapilla

Wilson's Warbler

Cardenilla pusilla

Stygian Owl

Asio stygius

Veery

Catharus fuscescens

Wood Thrush

Hylocichla mustelina

Animal Biodiversity and Conservation 36.2 (2013)

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Appendix 1. (Cont.) Common name

Scientific name

Status

Islands

Thick–billed Vireo

Vireo crassirostris

Philadelphia Vireo

Vireo philadelphicus

Cedar Waxwing

Bombycilla cedrorum

Cuban Grassquit

Tiaris canorus

Zapata Sparrow

Torreornis inexpectata

Clay–colored Sparrow

Spizella pallida

Northern Rough–winged Swallow

Stelgidopteryx serripennis

Shiny Cowbird

Molothrus bonariensis

Yellow–breasted Chat

Icteria virens

Northern Bobwhite

Colinus virginianus

Fernandina's Flicker

Colaptes fernandinae

Red–legged Honeycreeper

Cyanerpes cyaneus

Ruby–throated Hummingbird

Archilochus colubris

Sandhill Crane

Grus canadensis

110

Morelle et al.

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Pets becoming established in the wild: free–living Vietnamese potbellied pigs in Spain M. Delibes–Mateos & A. Delibes

Delibes–Mateos, M. & Delibes, A., 2013. Pets becoming established in the wild: free–living Vietnamese potbellied pigs in Spain. Animal Biodiversity and Conservation, 36.2: 209–215. Abstract Pets becoming established in the wild: free–living Vietnamese potbellied pigs in Spain.— Vietnamese potbellied (VPB) pigs (Sus scrofa) are a common pet in North America and Europe, but their recent decrease in popularity has increased their abandonment. Our main aim was to identify potential cases of free–living VPB pigs in Spain through an in–depth Google search. We identified 42 cases of free–living VPB pigs distributed throughout the country. The number of free–living VPB pigs reported increased by year but the species abundance still seems to be low. Signs of VPB pig reproduction and possible hybrids between VPB pigs and wild boar or feral pigs have been also reported. Free–living VPB pigs could erode the gene pool of the Spanish wild boar population and exacerbate the damage (e.g. crop damage or spread of diseases) already caused by wild board. Urgent evaluation and adequate management of wild VPB pig sightings is needed to prevent their establishment in natural habitats. Key words: Feral pig, Google search, Pet trade, Wild boar. Resumen Mascotas que se establecen en la naturaleza: cerdos vietnamitas que viven en libertad en España.— Los cerdos vietnamitas (Sus scrofa) son una mascota habitual en Norteamérica y Europa; sin embargo, su popularidad ha disminuido recientemente y esto ha provocado que se abandonen cada vez más. El objetivo principal de este trabajo es identificar casos de cerdos vietnamitas que viven en libertad en España a través de una búsqueda exhaustiva en Google. Se han identificado 42 casos de cerdos vietnamitas que viven en libertad distribuidos por todo el país. El número de casos aumenta cada año, aunque la abundancia de la especie aún parece ser baja. También se han observado indicios de que los cerdos vietnamitas se reproducen en libertad y de posibles híbridos de éstos con jabalíes o cerdos asilvestrados. El hecho de que los cerdos vietnamitas vivan en libertad podría reducir el patrimonio genético de la población española de jabalí, así como agravar los daños que este ya causa en España (como los daños a cultivos o los accidentes de tráfico). Con vistas a evitar que se establezcan en hábitats naturales, es urgente evaluar y gestionar debidamente las observaciones de cerdos vietnamitas salvajes. Palabras clave: Cerdo asilvestrado, Búsqueda en Google, Comercio de mascotas, Jabalí. Received: 1 VIII 13; Conditional acceptance: 11 X 13; Final acceptance: 26 X 13 Miguel Delibes–Mateos, Instituto de Investigación en Recursos Cinegéticos (IREC, CSIC–UCLM–JCCM), Ronda de Toledo s/n., 13071 Ciudad Real, España (Spain).– Adolfo Delibes, Junta de Castilla y León, c/ Rigoberto Cortejoso 14, 41014, Valladolid, España (Spain). Corresponding author: Miguel Delibes–Mateos. E–mail: mdelibesmateos@gmail.com

ISSN: 1578–665 X eISSN: 2014–928 X

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Introduction The deliberate or accidental release of pets has frequently resulted in the successful establishment of new wild populations (e.g. Bertolino & Lurz, 2013). Over the last years, Vietnamese potbellied pigs (Sus scrofa; hereafter VPB pigs; fig. 1) have become a popular pet species in many regions of the world (Braun & Casteel, 1993), including Spain (Jarandilla, 2011). However, their popularity has recently declined, leading to their frequent abandonment (Tynes, 1997). Given that this is a very opportunistic species, it could be expected that released or abandoned VPB pigs eventually establish free–living populations. Nevertheless, to our knowledge this has not yet been demonstrated. In this paper our main objective was to report, for the first time, the existence of free–living VPB pigs in Spain. In addition, we aimed to gather complementary information regarding these potential introductions, concerning the year, locality and habitat type in which they were observed (table 1). We also investigated whether pregnant VPB female pigs, piglets and/or hybrids between VPB pigs and wild boar (or feral pigs) were reported, as such sightings could indicate that VPB pigs are successfully establishing wild populations (see an example in Magalhaes & Jacobi, 2013). Finally, we briefly discuss the potential risks associated with the successful establishment of free–living VPB pigs. Material and methods We identified cases of free–living VPB pigs by means of a thorough Google search. We searched for terms that stemmed from the following words (in Spanish) in the following combinations: Vietnamese pig or Vietnamese boar, combined with wild boar or hybrid or wild or hunting or stalking or harvested or escaped or abandoned or abandonment (i.e. 9 * 2 = 18 combinations). We identified all the cases in which VPB pigs (or their reported hybrids with wild boar or feral pigs; see below) were unequivocally reported as roaming freely. We stopped the search for a word combination when 100 consecutive results did not identify any additional valid record, i.e., when we retrieved only repeated cases, results that did not exactly relate to free–living VPB pigs (e.g. web pages offering VPB pigs for sale), and/or cases in which it was impossible to unequivocally identify free–living VPB pigs (e.g. unclear observations, inconsistent rumours, etc.). Most valid cases were reported through searches in Internet forums (mainly in hunting websites) and in online newspapers and television channels. In total, more than 1,800 records were checked (18 word combinations and at least 100 records per search). All the searches were conducted between mid–February and mid–March 2013. When possible, we recorded the year, locality (and province), and number of individuals for each reported case (table 1). We differentiated between cases in urban and rural areas because the former would correspond to momentary VPB pig escapes

Delibes–Mateos & Delibes

or abandonments, whereas the latter would be more closely associated with individuals potentially becoming established in the wild. All the records from cities/towns, urban parks, highways close to the city/town, and so on were included in the urban area category, and those from natural environments (scrublands, woodlands, crops interspersed with natural vegetation, etc.) in the rural area category (table 1). We also recorded the presence of pregnant VPB pig females, piglets and/or potential VPB pig hybrids with wild boar or feral pig (table 1), as such sightings could indicate the establishment of viable free–living populations. Reported hybrids were described as individuals showing mixed morphological characteristics between VPB pigs and wild boar or feral pigs (fig. 1B). Furthermore, we differentiated between killed, captured or observed individuals, and we recorded the source of information: reported by hunters, reports in the news (online newspapers or televisions), and reports provided by forest rangers, hikers, bikers, and similar (table 1). Results We identified 42 cases of free–living VPB pigs (table 1, fig. 2). A very low percentage (< 1%) of the total records obtained through a Google search reported valid cases of free–living VPB pigs. Cases of free–living VPB pigs were relatively well distributed throughout Spain (fig. 2). Many occurred close to main cities, especially those identified near the coast (fig. 2). Free–living VPB pigs were firstly reported in Spain in 2007, and since then the number of cases has increased considerably. VPB pigs were recorded slightly more frequently in rural than in urban areas (57.15% vs 42.85%, n = 42). The first hybrid between VPB pig and wild board (or feral pig) was reported in 2010, and since then, the proportion of records of potential hybrids has increased substantially (table 1). Hybrids were reported in > 25% of the total cases (table 1). In addition, pregnant females or females taking care of piglets were also sporadically observed, captured or killed (table 1). Table 1 also shows that: 1) on most occasions, only one individual was observed, captured or killed (70%, n = 34), although some pairs and larger groups were also reported; 2) the number of records of observed, captured and killed individuals was similar; captured and killed animals were better sources for the identification of VBP pigs and hybrids (fig. 1); 3) most cases were reported either by hunters or in newspapers; and 4) nearly all the cases recorded in urban areas were reported in newspapers, and all the records provided by hunters came from rural landscapes. Discussion In this study we provide the first evidences of free– living VPB pigs in Spain, and, to the best of our knowledge, elsewhere in Europe, although they are also common pets in other countries. According to

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Fig. 1. A. A docile Vietnamese potbellied pig captured by a hunter in a wild environment within northern Spain (ID 3 in table 1 and fig. 2); B. Four potential hybrids between Vietnamese potbellied pigs and wild boar (on the left of the picture) killed during a hunting day in northern Spain (ID 1 in table 1 and fig. 2). The morphological aspect of reported hybrids differs notably to that of young wild boar (on the right of the picture). Fig. 1. A. Un cerdo vietnamita dócil capturado por un cazador en un entorno natural del norte de España (ID 3 en la tabla 1 y en la fig. 2); B. Cuatro posibles híbridos entre cerdos vietnamitas y jabalíes (a la izquierda de la imagen) cazados en el norte de España (ID 1 en la tabla 1 y en la fig. 2). El aspecto morfológico de los híbridos observados difiere notablemente del de los jabalíes jóvenes (a la derecha de la imagen).

our findings, free–living VPB pigs have been reported throughout the country. Although the number of cases identified was not high, it has increased in recent years. Importantly, our results indicate that VPB pigs might have successfully established wild populations because signs of VPB pig reproduction (i.e. pregnant females and females taking care of piglets, and/or hybrids of VPB pigs and wild boar or feral pigs) have been frequently observed in the wild. Reasons for the successful establishment, spread and adaptation

of VPB pigs to wild habitats are probably related to their highly adaptive and opportunistic behaviour, the scarcity of natural predators, and the favourable climatic conditions in Spain. Internet search engines are increasingly used in ecological studies (e.g. Maccallum & Bury, 2013), and in particular to monitor the escapes/releases of non–native pets into the wild (see Kikillus et al., 2012). From this perspective, Google searching could be an appropriate tool to monitor the presence of free–liv-

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Table 1. Cases of free–living Vietnamese potbellied pigs in Spain identified through an in–depth Google search (see Methods for details): ID. Locality numbers plotted in fig. 2; N. Number of pigs observed, captured or killed in each case; A. Area (R. Rural, U. Urban); H. Hybrid; P/N. Pregnant/nursing (* females that were taking care of piglets); T. Type (K. Killed, C. Captured, O. Observed); S. Source (H. Hunters, N. Newspaper, O. Others: O1 Forest rangers, O2 Conservationists). Tabla 1. Casos de cerdos vietnamitas que viven en libertad en España identificados mediante una búsqueda exhaustiva en Google (en el apartado Methods se ofrece información más detallada): ID. Números de las localidades indicadas en la fig. 2; N. Número de cerdos observados, capturados o cazados en cada caso; A. Área (R. Rural, U. Urbana); H. Híbrido; P/N. Embarazada/lactante (* hembras con crías); T. Tipo (K. Muerto, C. Capturado, O. Observado); S. Fuente (H. Cazadores, O. Otros: O1 Guardabosques, O2 Conservacionistas). ID Locality

Province

P/N

Year

1 Castillo de Onielo

Palencia

Yes

2013

2 Olivares de Duero

Valladolid

–

2013

3 Mucientes

Valladolid

2013

4 Maella

Zaragoza

–

2012

5 Unknown

Alicante

–

Yes

6 Mallorca

Baleares

Yes

2012

7 Puig de Santa

Baleares

Yes

2012

8 Cartagena

Murcia

–

2012

9 Elche

Alicante

2007

10 Santander

Cantabria

Yes

Yes*

2011

11 Argentona

Barcelona

2011

H/N

12 Pontons

Barcelona

2010

13 San Antonio

Baleares

2011

14 Olesa de Montserrat

Barcelona

Yes

2010

15 Valencia

Valencia

2008

16 András

Pontevedra

2008

17 Unknown

Huesca

–

2012

18 Unknown

Coruña

–

2012

19 Concejo de Siero

Asturias

2012

20 Murcia

Murcia

2012

21 Cuenca río Verdugo

Pontevedra

–

Yes

–

2012

22 Unknown

Valencia

Yes

2012

23 Unknown

Almería

–

2012

Magdalena de Inca

24 Retuerta del Bullaque/ Ciudad Real/

–

Los Yébenes

Toledo

25 Villaviciosa y Sariego

Asturias

–

2012

26 Valencia

Valencia

2012

27 Elda

Alicante

Yes*

2012

28 Parque Almijara

Málaga/

–

Yes

–

2011

Granada

29 La Seu de Urgell

Lleida

Yes

2013

30 Badajoz

Badajoz

2010

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Table 1. (Cont.) ID Locality

Province

P/N

Year

31 Baños de la Encina

Jaén

–

Yes

2012

32 Zaragoza

Zaragoza

2012

33 Vélez–Málaga

Málaga

2008

34 Rojales

Alicante

2011

35 Santiago de

Coruña

2010

36 Valencia

Valencia

2012

37 Zaragoza

Zaragoza

2007

38 Campo Lameira

Pontevedra

2010

39 La Solana

Ciudad Real

2012

40 Parque Natural

Alicante

2007

Alicante

2009

Alicante

–

Rural

2013

Compostela

del Montgó

41 San Vicente

del Raspeig

42 Southern Alicante

France 16

18 35 38 21

37 32

14 11

Spain 24

Portugal

26 15 2236

27 41 42 9 20 34 8

28 33

13 40

0 100 200 km

Fig. 2. Localities in which free–living Vietnamese potbellied pigs or reported hybrids between Vietnamese potbellied pigs and wild boar or feral pigs were observed, captured or killed. Dots generally represent approximate locations, as on most occasions we could not obtain the exact coordinates where free–living Vietnamese potbellied pigs were observed. Numbers correspond to the ID of each locality in table 1.

Fig. 2. Localidades en las que se observaron, capturaron o cazaron cerdos vietnamitas en libertad o híbridos entre cerdos vietnamitas y jabalíes o cerdos asilvestrados. Por lo general, los puntos representan las localidades aproximadas, puesto que en la mayoría de las ocasiones no fue posible obtener las coordenadas exactas en las que se observaron los cerdos vietnamitas en libertad. Los números son los que figuran en la columna ID de cada localidad en la tabla 1.

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ing VPB pigs in Spain. However, the use of Internet searches in scientific studies presents several limitations that must be taken into account. For example, in our study it was almost impossible to check the reliability of most of the observations of free–living VPB pigs; nevertheless, pictures of killed or captured VPB pigs were frequently shown on the websites returned from our searches. Similarly, identification of hybrids between VPB pigs and wild boar (or feral pigs) was not unequivocal through Google searching, and therefore genetic studies are needed to accurately confirm their presence in the wild. In addition, Google searching excludes communities that use Internet less frequently (Maccallum & Bury, 2013), such as older people, or residents in small villages (Proulx et al., in press). Such communities may be closer to wildlife, as these people frequently work in the field (e.g. farmers and gamekeepers); it could therefore be expected that their knowledge about the presence of free–living VPB pigs would be higher than that of other people. Taking this into consideration, we could have underestimated the number and distribution of wild VPB pigs. In contrast, given that striking news is especially highlighted in websites, the presence of free–living VPB pigs could also have been overestimated in our study. In any case, Internet search engines offer some advantages over conventional field–monitoring programs. For example, they permit cost–effective and rapid assessments to detect the recent introduction of invasive animals (Proulx et al., in press), such as the case addressed in the present manuscript. The introduction of VPB pigs into the wild is a result of their deliberate or accidental release, and seems to have been favoured by the huge development of the online pet–trade (Magalhaes & Jacobi, 2010). Thus, the number of Spanish websites advertising VPB pigs for sale estimated through a Google search increased from less than 10 in 2006 to more than 1,300 in 2012. As a result, the prize paid for VPB pigs in Spain has decreased drastically, dropping from several hundred euros to as little as 20 euros, a fact that facilitates their abandonment (Lord & Wittum, 1998). According to our results, VPB pigs observed were mostly solitary, suggesting that the number of individuals released per event was low. Nevertheless, as observed with other introduced pets (e.g. Alda et al., 2013), only a few founders may have been sufficient to establish free–living populations of VPB pigs across Spain. Furthermore, free–living VPB pigs were frequently documented in parks and gardens in urban areas, indicating these areas could play a key role in the establishment of free–living populations. This closely resembles the manner in which racoons were introduced (Procyon lotor) in central Spain (García et al., 2012). As VPB pigs have become established in wild ecosystems in Spain only recently, we can only speculate about the risk they may pose. Given the notable genetic divergence between European and Asian S. scrofa (Fernández et al., 2010), free–living VPB pigs could cause erosion of the gene pool of Spanish wild boar populations. In addition, they could

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create problems similar to those already caused by the wild boar in large areas of Spain (e.g. negative effects on crops and/or natural vegetation, Herrero et al., 2006; Gómez & Hódar, 2008). The fact that we found only a few cases of apparently successful establishment of VPB pigs in the wild suggests they are not yet abundant in our setting. However, previous experiences suggest that calls for early management action are required, because by the time released exotic animals are publicly recognised as a problem, it is often too late for effective action, due to logistic, economic, or scale factors (Bertolino & Genovesi, 2003). We therefore recommend the situation should be suitably managed before it runs out of control. An in–depth monitoring plan is needed to determine the current distribution and abundance of free–living VPB pigs in Spain, and to accurately assess the risk they may cause. To prevent further releases of exotic pets in the wild, we urgently need stricter trade regulations in Spain (see for a wider explanation on this topic Bertolino & Lurz, 2013). At the same time, we need to increase public awareness about the risks of free–living pets and the benefits of their prevention and mitigation for native biodiversity. Acknowledgements We are very grateful to Drs. M. Delibes, M. Díaz and P. White, and an anonymous reviewer for helpful comments on previous drafts, and to all the people who kindly provided information about free–living Vietnamese potbellied pigs in Spain. M. Delibes–Mateos was supported by a JAE–doc contract (Programa Junta para la Ampliación de Estudios), funded by CSIC and the European Social Fund. References Alda, F., Ruiz–López, M. J., García, F. J., Grompper, M. E., Eggert, L. S. & García, J. T., 2013. Genetic evidence for multiple introduction events of racoons (Procyon lotor) in Spain. Biological Invasions 15: 687–698. Bertolino, S. & Genovesi, P., 2003. Spread and attempted eradication of the grey squirrel (Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris) in Eurasia. Biological Conservation, 109: 351–358. Bertolino, S. & Lurz, P. W. W., 2013. Callosciurus squirrels: worldwide introductions, ecological impacts and recommendations to prevent the establishment of new invasive populations. Mammal Review, 43: 22–33. Braun, W. F. & Casteel, S. W., 1993. Potbellied pigs: miniature porcine pets. Veterinary Clinics of North America: Small Animal Practice, 23: 1149–1161. Fernández, A. I., Alves, E., Óvilo, C., Rodríguez, M. C. & Silió, L., 2010. Divergence time estimates of East Asian and European pigs based on multiple near complete mitochondrial DNA sequences.

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Animal Genetics, 42: 86–88. García, J. T., García, F. J., Alda, F., González, J. L., Aramburu, M. J., Cortés, Y., Prieto, B., Pliego, B., Pérez, M., Herrera, J. & García–Román, L., 2012. Recent invasion and status of the racoon (Procyon lotor) in Spain. Biological Invasions, 14: 1305–1310. Gómez, J. M. & Hódar, J. A., 2008. Wild boars (Sus scrofa) affect the recruitment rate and spatial distribution of holm oak (Quercus ilex). Forest Ecology and Management, 256: 1384–1389. Herrero, J., García–Serrano, A., Couto, S., Ortuño, V. M. & García–González, R., 2006. Diet of wild boar Sus scrofa L. and crop damage in an intensive agroecosystem. European Journal of Wildlife Research, 52: 245–250. Jarandilla, L., 2011. Cerdos vietnamitas. Editorial Hispano Europea, Barcelona. Kikillus, K. H., Hare, K. M. & Hartley, S., 2012. Online trading tools as a method of estimating propagule pressure via the pet–release pathway. Biological Invasions, 14: 2657–2664.

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Lord, L. & Wittum, T., 1998. Survey of humane organizations and slaughter plants regarding experiences with Vietnamese potbellied pigs. The Journal of the American Veterinary Medical Association, 211: 562–565. Magalhaes, A. L. B. & Jacobi, C. M., 2010. E–commerce of freshwater aquarium fishes: potential disseminator of exotic species in Brazil. Maringá, 32: 243–248. – 2013. Asian aquarium fishes in a Neotropical biodiversity hotspot: impeding establishment, spread and impacts. Biological Invasions, 15: 2157–2163. Mccallum, M. L. & Bury, G. W., 2013. Google search patterns suggest declining interest in the environment. Biodiversity and Conservation, 22: 1355–1367. Proulx, R., Massicotte, P. & Pépino, M., in press. Googling trends in conservation biology. Conservation Biology. Tynes, V. V., 1997. Potbellied pig husbandry and nutrition. Veterinary Clinics of North America: Exotic Animal Practice, 2: 193–208.

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Descripción de tres nuevas especies de tetigónidos de Costa Rica (Orthoptera, Tettigoniidae) P. Barranco Vega

Barranco Vega, P., 2013. Descripción de tres nuevas especies de tetigónidos de Costa Rica (Orthoptera, Tettigoniidae). Animal Biodiversity and Conservation, 36.2: 217–223. Abstract Description of three new species of katydids from Costa Rica (Orthoptera, Tettigoniidae).— Three new species of katydids from the Reserva Biológica Alberto Manuel Brenes (Alajuela) in Costa Rica (Central America) are described. The specimens were collected in the course of the Project INVARTRAB developed by the Central University of Costa Rica and the INIA de Madrid (España). The specimens were sampled by direct prospection on plants and light traps. The new species belong to the genera Phlugis, Scopiorinus and Viadana, respecti vely. Phlugis ramirezi n. sp. has little developed tegmens and wings, male tenth abdominal tergite ending in two spiniform processes, cerci curved with a basal spur, and four teeth in the apex. Scopiorinus estebani n. sp. shows male tenth abdominal tergite with a longer than broad expansion, subgenital plate depressed in the middle, and lateral spiniform processes at the end. Viadana rowelli n. sp. has rhomboidal tegmens and male cerci with an internal branch with serrulated apex inserted in the last third. Main characters are illustrated and compared in related species in each genus. Key words: New taxa, Phlugis, Scopiorinus, Viadana, Neotropical fauna. Resumen Descripción de tres nuevas especies de tetigónidos de Costa Rica (Orthoptera, Tettigonidae).— Se describen tres nuevas especies de tetigónidos procedentes de la Reserva Biológica Alberto Manuel Brenes (Alajuela) en Costa Rica (Centroamérica). El material se recolectó en virtud del proyecto INVARTRAB desarrollado con juntamente entre la Universidad Central de Costa Rica y el INIA de Madrid (España). Los ejemplares fueron capturados mediante muestreo directo sobre la vegetación y mediante trampas de luz. Las nuevas especies pertenecen a los géneros Phlugis, Scopiorinus y Viadana respectivamente. Phlugis ramirezi sp. n. se carac teriza por presentar tegminas y alas poco desarrolladas, décimo terguito abdominal del macho acabado en dos procesos espiniformes, y el cerco curvado con un espolón basal y el ápice dilatado con cuatro dientes. Scopiorinus estebani sp. n. presenta el décimo terguito abdominal del macho expandido en un proceso más largo que ancho y la placa subgenital escotada en el centro y con dos procesos espiniformes laterales en el ápice. Viadana rowelli sp. n. presenta tegminas romboidales y el cerco del macho con una ramificación con el ápice aserrado insertada en el último tercio. Se ilustran las estructuras que las caracterizan y se comparan con las especies afines dentro de cada género. Palabras clave: Nuevos taxones, Phlugis, Scopiorinus, Viadana, Fauna neotropical. Received: 4 X 13; Conditional acceptance: 13 XI 13; Final acceptance: 20 XI 13 Pablo Barranco Vega, Depto. Biología y Geología, CITE II–B. Univ. de Almería, ctra. Sacramento s/n., 04120 Almería, España (Spain). E–mail: pbvega@ual.es

ISSN: 1578–665 X eISSN: 2014–928 X

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Introducción En el transcurso del desarrollo el proyecto “Inventario de Artrópodos de la Reserva Biológica Alberto Ma nuel Brenes” (INVARTRAB), se realizó en 2006 una campaña entomológica para prospectar los siguientes grupos de insectos: coleópteros acuáticos, coleópte ros crisomélidos, lepidópteros nocturnos y ortópteros. Los muestreos se realizaron mediante prospec ciones directas sobre la vegetación a lo largo de transectos diurnos y nocturnos por los senderos de la Reserva y mediante trampas de luz. Estas últimas consistieron en un cebo luminoso fijo de alto rendi miento con una lámpara de llamada de 400 W de vapor de mercurio, dos de aproximación de 125 W también de vapor de mercurio y otras dos de aproxi mación de 100 W ultravioleta a sendos lados de una “manta” de tela blanca. El cebo luminoso permaneció activo de 18:30 a 5:30 h. El material ortopterológico fruto de esta campaña, junto con otro recolectado posteriormente por dife rentes entomólogos, ha sido estudiado y publicado en sendos trabajos, arrojando un total de 102 espe cies de ortópteros para la Reserva: 61 de Ensíferos (Anostostomidos y Tetigónidos) (Barranco, 2010a) y 41 de Celíferos (Barranco, 2010b). Entre estas espe cies se descubrieron cinco nuevas especies para la Ciencia, de las que tres se describen en este artículo. Subfamilia Meconematinae. Tribu Phlugidini Phlugis ramirezi sp. n. Holotipo: 1♂, Cascada río San Lorencito, Reser va Biológica Alberto Manuel Brenes, San Ramón, Alajuela, Costa Rica, 22 IX 2006, P. Barranco leg. Paratipo: 1♀, camino de acceso a la Estación Bioló gica, Reserva Biológica Alberto Manuel Brenes, San Ramón, Alajuela, Costa Rica, 18 IX 2006, P. Barranco leg. Ambos tipos depositados en el Museo de Insectos de la Universidad Central de Costa Rica, San José. Holotipo: macho (fig. 1). Coloración general en vivo, amarillenta pálida. Cabeza lisa. Ojos muy globosos y prominentes, oscuros, con el diámetro máximo en el eje axial. Cabeza prolongada a nivel de la inserción de las antenas, de modo que el vértex es bífido. Escapo globoso, antenas del mismo color que el cuerpo (incompletas). Palpos muy largos. Pronoto liso, tectiforme, sin quillas laterales, alar gado (0,31 x 0,2 mm) (figs. 2, 3). Prozona estrecha, mesozona un poco más dilatada y metazona abultada y elevada sobre la mesozona. Margen inferior de los paranotos convexo, con una escotadura a nivel del inicio de la metazona, rebordeado. Orificio timpánico descubierto, pequeño, circular. Prosterno inerme, lóbulos prosternales y metasternales no modifica dos; lóbulos mesosternales prominentes formando un tubérculo. Tegminas y alas poco desarrolladas (fig. 1), las primeras alcanzan en reposo el inicio del octavo terguito abdominal y las alas el del séptimo (en fresco). Fémures anterior y medio dilatados en la base. El primero con cuatro espinas en el margen

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interno y tres en el externo. Las internas de mayor longitud que las externas y en éstas, la proximal interna de mayor tamaño que se va reduciendo hasta la distal. Fémures medio y posterior inermes. Tibia anterior con cinco espinas tanto en su margen interno como externo. Tibia media con dos espinas externas. Tibia posterior con 29–31 espinas externas y 33–34 internas. Décimo terguito prolongado hacia atrás en dos procesos espiniformes, con una amplia escotadura cóncava entre ellos (fig. 4). Cercos muy desarrollados, curvados hacia adentro, con quilla basal que forma una espina externa a nivel de la inserción. Ápice ensanchado, con una parte superior formada por dos crestas muy esclerotizadas y otra parte inferior forma da por una fuerte espina negra; además externamente antes del ápice hay otra espina negra central (fig. 4). Placa subgenital muy grande, bilobulada y dilatada en la base, con dos largos estilos de dos veces y media de la porción basal (fig. 5). Los estilos contactan en la base, divergiendo posteriormente y arqueándose para volver a contactar en el ápice (fig. 5). En vista lateral, la placa subgenital es primero descendente adelgazándose y hacia la mitad se hace ascendente y se engrosa en el ápice (fig. 6). Hembra de aspecto general como el del macho, pero un poco más grande (fig. 7). Pronoto más corto y plano, metanoto no dilatado. Paranotos casi semicir culares (fig. 8). Tibia posterior con 29 espinas externas y 32 internas. Décimo terguito abdominal estrecho, convexo en el centro (fig. 9). Cercos delgados y lar gos y muy pilosos. Placa subgenital con el margen anterior cóncavo, el posterior emarginado y bilobulado (fig. 10). Oviscapto muy dilatado en la base, porción curva dos veces y media la basal (fig. 11). Medidas en cm (holotipo paratipo): longitud del pronoto: 0,35 0,32; anchura del pronoto: 0,22 0,20; longitud de la tegmina: 4,2 4,8; longitud del fémur posterior: 0,98 1,05; longitud total: 1,13 1,50; longitud oviscapto: 0,6. Longitud del ojo: 0,13 0,15; altura del ojo: 0,1 0,1; anchura del ojo: 0,07 0,07. Las especies neotropicales del género Phlugis ascienden a 45, incluyendo las listadas y descritas por Nickle (2003, 2005) y las descritas por Gorochov (2012). Si bien este último autor indica que tan sólo 10 de ellas pertenecen a este género y que el resto han de ser revisadas. Las especies costarricenses del género fueron revisadas por Nickle (2005) con la descripción de dos nuevas especies. Hasta la fecha existen siete especies en el país y su identi ficación es sencilla a partir de la clave dicotómica confeccionada por este autor. Esta nueva especie se encuadra en el grupo V de Nickle (2003) que se caracteriza por la presencia de tres y cuatro espinas en los márgenes externo e interno del fémur anterior, este grupo está integrado por diez especies, ocho del Perú y dos de Costa Rica. De estas especies, la única que presenta el décimo terguito abdominal del macho acabado en dos procesos espiniformes semejantes a Phlugis ramirezi sp. n. es Phlugis gigantea Nickle, 2003, pero tanto el cerco como la placa subgenital son completamente diferentes a los de la nueva especie, además de presentar tegminas

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Figs. 1–6. Phlugis ramirezi sp. n., holotipo, macho: 1. Aspecto general; 2. Pronoto en vista dorsal; 3. Pro noto en vista lateral; 4. Décimo terguito abdominal y cercos; 5. Placa subgenital en vista ventral; 6. Placa subgenital en vista lateral. (Escala 1 mm, salvo en la fig. 1 que es de 2 mm.) Figs. 1–6. Phlugis ramirezi n. sp., holotype, male: 1. General aspect; 2. Pronotum in dorsal view; 3. Pronotum in lateral view; 4. Tenth abdominal tergite and cerci; 5. Subgenital plate in ventral view; 6. Subgenital plate in lateral view. (Scale 1 mm, except in fig. 1 where it is 2 mm.)

y alas muy desarrolladas que superan la longitud del abdomen. La forma del cerco de Phlugis ramirezi sp. n. se asemeja al de Phlugis robertsi Nickle, 2005, pero es más aserrado y presenta una espina externa en la nueva especie. Además en P. robertsi el décimo tergui to es expandido y redondeado y también los dos pares de alas superan ampliamente el ápice del abdomen. Derivatio nominis: esta especie está dedicada al entomólogo costarricense, don Rolando Ramírez Campos por su inestimable ayuda en las prospec ciones de campo en la RBAMB. Subfamilia Pseudophyllinae. Tribu Pterophyllini Scopiorinus estebani sp. n. Holotipo: 1♂, Reserva Biológica Alberto Manuel Bre nes, San Ramón, Alajuela, Costa Rica, 17 IX 2006, P. Barranco leg. En tubos foliares de Heliconia. De positado en el Museo de Insectos de la Universidad Central de Costa Rica, San José. Aspecto como el del género. Color general en vivo verde. Cabeza alargada. Ojos pequeños pro minentes, globosos; diámetro del ojo la mitad de la altura de la gena subocular. Vértex muy estrecho, 0,4 mm, surcado, prolongado en pico entre las an

tenas. Tubérculo frontal pequeño, anguloso entre la base de las antenas. Frente inclinada 45°. Palpos delgados y pilosos, sobre todo el último artejo que es subcónico. Antenas muy largas, más de cinco veces la longitud del cuerpo, del mismo color que el cuerpo y pilosas. Escapo desarrollado, el doble de largo que ancho. Pronoto tectiforme, liso, con la quilla media patente en la pro y mesozona, y poco patente en la metazona, interrumpida únicamente por el surco típico un poco antes del medio. Quillas laterales poco conspicuas en la metazona. Margen posterior en ángulo obtuso. Paranotos trapezoidales, con el margen inferior recto y engrosado por un reborde. Tres pares de pequeñas manchas negras dorso laterales y una línea corta negra central en la intersección de la quilla media con el surco típico. Espinas prosternales anchas y cortas. Espinas mesosternales más desarrollodas, las metasternales forman una cresta. Abertura timpánica muy pequeña (0,6 x 0,2 mm) oval, con un pequeño repliegue en el margen anterior. Tegminas largas y estrechas, de color verde en vivo, con el ápice agudo, sobrepasando el ápice de los fémures posteriores extendidos. Margen costal casi recto, el anal ligeramente convexo. Espejo más largo que ancho, área estridular muy globosa. Alas posteriores hialinas y en reposo totalmente cubiertas por las tegminas llegando hasta el ápice de éstas.

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Figs. 7–11. Phlugis ramirezi sp. n., paratipo, hembra: 7. Aspecto general de la hembra; 8. Pronoto en vista lateral; 9. Décimo terguito abdominal; 10. Placa subgenital en vista ventral; 11. Oviscapto en vista lateral. (Escala 1 mm, salvo en la fig. 7 que es de 2 mm.) Figs. 7–11. Phlugis ramirezi n. sp., paratype, female: 7. General aspect of the female; 8. Pronotum in lateral view; 9. Tenth abdominal tergite; 10. Subgenital plate in ventral view; 11. Ovipositor in lateral view. (Scale 1 mm, except in fig. 7 where it is 2 mm.)

Espina procoxal dorsal presente y un diente ven tral. Mesocoxa con dos pequeños dientes ventrales, metacoxa con uno. Patas muy largas y finas en ge neral. Fémur anterior ornamentado con dos filas de puntos negros en la cara interna y una en la externa. Margen inferior interno provisto de cinco espinas ne gras en la mitad distal. Fémur medio inerme. Fémur posterior con una o dos espinas ventrales externas distales. Cóndilos exterior e interior de todos los fémures con una espina. Tibias con las siguientes espinas (inferior internas, inferior externas, superior internas, superior externas): anterior (12, 10, 0, 0), media (10–11 izquierda y derecha respectivamente, 10, 0, 0), posterior (13, 18, 31, 27). Décimo terguito muy desarrollado, prolongado hacia atrás en el centro en un tubérculo de igual longitud que la porción basal del terguito y con el ápice bifurcado (fig. 12), alcanzando el extremo de la placa subgenital. Cerco robusto, corto, piloso y curvado hacia dentro, con el ápice agudo terminado en una espina gruesa de color negro (figs. 13, 14). Titiladores dilatados en la porción proximal, porción distal cerciforme, más delgada y curvada hacia arriba con dentículos en el margen superior e interno en la inserción y a lo largo de toda su superficie en la mitad distal que acaba también en una fuerte espina negra (fig. 14). Placa subgenital prolongada hacia atrás, ensanchada en el ápice, con el borde posterior levemente escotado en el centro, sinuoso y los extremos sin estilos, acabados

en pequeños procesos espiniformes negros (fig. 15); en vista lateral ligeramente curvada hacia arriba (fig. 16), tan larga como la prolongación del décimo terguito. Margen basal cóncavo, bordes laterales convergentes hacia la mitad de la prolongación posterior. Quilla central muy patente en la porción basal. Medidas en cm: longitud del pronoto: 0,51; tegmi na: 2,94; fémur anterior: 1,29; fémur posterior: 2,34; longitud cuerpo: 2,79. Derivatio nominis: especie dedicada al entomólo go Dr. José Esteban Durán del INIA de Madrid, en reconocimiento a su dedicación a la entomología aplicada y coleopterología tropical. El género Scopiorinus Beier, 1960 se diferencia de otros géneros afines de la tribu por la ausencia de estilos en la placa subgenital del macho (Beier, 1960, 1962). Piza (1980a) describe S. turrialbae de Costa Rica que relaciona a S. mucronatus (Saussure & Pictet, 1898) diferenciándola por la espina de los lóbulos geniculares y por la forma de la placa sub genital de ambos sexos. Posteriormente, Morris & Beier (1982) adscribieron a este género también S. carinulatus (Saussure & Pictet, 1898), pues la placa subgenital del macho carece de estilos. De estas seis especies que integran el género, S. turrialbae, S. mucronatus y S. impressopunctatus Beier, 1960 han sido descritas de Costa Rica. Las otras tres especies S. nigridens (Stål, 1875), S. fragilis (Hebard, 1927) y S. similis Beier, 1960 han sido descritas de Panamá,

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Figs. 12–16. Scopiorinus estebani sp. n., holotipo, macho: 12. Décimo terguito abdominal; 13. Cerco de recho en vista dorsal; 14. Titilador derecho y cerco en vista lateral; 15. Placa subgenital en vista ventral; 16. Placa subgenital en vista lateral. (Escala 1 mm.) Figs. 12–16. Scopiorinus estebani n. sp., holotype, male: 12. Tenth abdominal tergite; 13. Right cercus in dorsal view; 14. Right titillator and cercus in lateral view; 15. Subgenital plate in ventral view; 16. Subgenital plate in lateral view. (Scale 1 mm.)

si bien la primera de ellas también ha sido citada en el país anterior. Los machos del género Scopio rinus presentan modificaciones del décimo terguito abdominal y la placa subgenital muy características, de modo que estas estructuras permiten diferenciar claramente unas especies de otras. Scopiorinus estebani sp. n. se asemeja tanto por la forma del 10º terguito abdominal como por la placa subgenital a Scopiorinus fragilis (Hebard, 1927), si bien la nueva especie presenta la prolongación del 10º terguito más larga que la anchura del mismo y el ápice de ésta más escotado. El borde distal de la placa subgenital también difiere, pues la depresión es sólo central en la nueva especie y con procesos espiniformes en sendos extremos, mientras que S. fragilis presenta el borde posterior ampliamente convexo y sin procesos espiniformes. Subfamilia Phaneropterinae. Tribu Viadanini Viadana rowelli sp. n. Holotipo: 1♂, Reserva Biológica Alberto Manuel Brenes, San Ramón, Alajuela, Costa Rica, a la luz, 22 IX 2006, P. Barranco leg. Paratipo: 1♂, Reserva Biológica Alberto Manuel Brenes, San Ramón, Alajue la, Costa Rica, a la luz, 23 IX 2006, P. Barranco leg. Ambos depositados en el Museo de Insectos de la Universidad Central de Costa Rica, San José. Coloración general en vivo del cuerpo, alas y apéndices verde claro amarillento. Cuerpo y apéndices

cubiertos de una pilosidad dispersa blanca. Cabeza pequeña, casi ortognata. Inserción de las antenas con un reborde cefálico en la parte superior. Fastigio muy agudo, sin superar el reborde de las antenas. Ojos glo bosos, tan anchos como altos. Tubérculo frontal nada marcado y en contacto con la base del vértex. Escapo algo más del doble de largo que ancho. Palpos muy delgados y largos y del mismo color que la cabeza. Pronoto plano dorsalmente, liso, margen anterior cóncavo, el posterior convexo. Disco pronotal con los bordes paralelos, de modo que la anchura es constante en la prozona y en la metazona. Surco típico, poco marcado, en el último tercio. Paranotos planos, con un fino reborde, el margen anterior un poco anguloso, el inferior y posterior redondeado. Prosterno no modificado, meso y metasterno con los lóbulos laterales prominentes formando una especie de quilla que contactan en el extremo distal. Abertura timpánica muy amplia, tapada por los paranotos. Tegmina verde, romboidal, con el borde anal muy convexo y el costal casi recto (fig. 17). Fila estridu ladora constituida por 43 dentículos. Alas hialinas con el ápice verde y agudo que sobresale de las tegminas. Fémur anterior cilíndrico, margen inferior interno armado de una a tres pequeñas espinas en la mitad distal. Fémur medio con una o ninguna espina inferior interna distales. Fémur posterior con una o dos espinas inferiores internas distales. Cóndilos posteriores con una pequeña espina. Tibias con las siguientes espinas (inferior internas, inferior externas, superior internas, superior externas): anterior (7–8, 5, 0, 0), media (7, 10, 0, 0), posterior (10, 19, 27, 21–22).

222

Barranco Vega

17 18

Figs. 17–22. Viadana rowelli sp. n., holotipo, macho: 17. Tegmina izquierda; 18. Décimo terguito abdominal y cerco izquierdo; 19. Detalle del diente interno del cerco; 20. Cerco derecho en vista lateral; 21. Titilador izquierdo; 22. Placa subgenital en vista ventral. (Escala 1 mm, salvo en la fig. 17 que es de 5 mm.) Figs. 17–22. Viadana rowelli n. sp., holotype, male: 17. Left tegmen; 18. Tenth abdominal tergite and left cercus; 19. Detail of inner tooth of cercus; 20. Right cercus in lateral view; 21. Left titillator; 22. Subgenital plate in ventral view. (Scale 1 mm, except in fig. 17 where it is 5 mm.)

Décimo terguito abdominal ampliamente cóncavo en el margen anterior y levemente cóncavo en el posterior (fig. 18). Epiprocto largo, tanto como el 10º terguito y bilobulado en el ápice. Cercos largos y ramificados en el tercio apical (figs. 18, 20). Diente interno muy desarrollado, ensanchado en la base y aserrado en el ápice que es negro (fig. 19). Extremo distal del cerco aplanado y sin diente. Titiladores muy desarrollados, con el margen interno del brazo distal profusamente dentado desde la base hasta el ápice (fig. 21); porción membranosa proximal formando una uña lateral muy esclerotizada de color negro (fig. 21). Placa subgenital con el margen anterior cóncavo, re dondeado; el distal prolongado en el centro con dos salientes agudos en los extremos y cóncavo entre ellos; carente de estilos (fig. 22). Medidas en cm (holotipo paratipo): longitud del pronoto: 0,37 0,38: longitud de la tegmina: 2,80 3,23; anchura máxima de la tegmina: 1,00 1,10; longitud del ala: 3,12 3,55; longitud del fémur anterior: 0,43 0,54; longitud del fémur posterior: 1,59 1,50; longitud de la tibia posterior: 1,82 1,81. Derivatio nominis: Esta especie está dedicada al Dr. C. H. F. Rowell por su contribución al estudio de la acridofauna neotrópical, en especial la de Costa Rica.

El género Viadana Walker, 1869 se diferencia de otros afines de la tribu por presentar los márgenes costal y anal de las tegminas no paralelos, el primero más amplio y expandido, reticuladas y el fastigio del vértex más corto que los escapos (Cadena–Casta ñeda, 2012). Brunner von Wattenwyl (1878, 1891) separa las especies del género Viadana (entonces Ctenophlebia Stål, 1873) en dos grupos según la for ma de las tegminas: forma oblongo ovalada y forma romboidea. En la actualidad este género agrupa a 25 especies (Eades et al., 2013) de las que atendiendo al criterio anterior, 11 poseen tegminas romboidales, las otras 14 las presentan oblongo ovaladas. La gran mayoría de los machos de las especies del género Viadana poseen el cerco simple sin ninguna ramificación o modificación; tan sólo tres especies junto a la que aquí se describe, presentan el cerco ramificado: Viadana curvicercata (Brunner von Wat tenwyl, 1878), Viadana septemtrionalis (Piza, 1980) y Viadana zetterstedti (Stål, 1861). De ellas, las dos primeras poseen tegminas oblongo ovaladas, y tan sólo la última posee tegminas romboidales, como la nueva especie que nos ocupa. El cerco de V. septe mtrionalis es curvo, con el ápice agudo y presenta un diente triangular muy agudo cerca del extremo (Piza,

Animal Biodiversity and Conservation 36.2 (2013)

1980b). Los cercos de V. rowelli sp. n. presentan una ramificación y una conformación característica que se relaciona con la de V. zetterstedti, pero la bifurcación del cerco en V. zetterstedti es subapical y en V. rowelli sp. n. está en la base del último tercio. En esta nueva especie, tanto la rama distal como la proximal, son de mayor longitud, de modo que el diente interno se despega ampliamente de la rama principal. Además de estas nuevas especies, se aporta la primera cita para el país de Ceraia intermedia (Márquez, 1957) a partir de los ejemplares citados como Ceraia sp. en Barranco (2010a). Después de un profundo estudio y comparación con las especies conocidas del género (Grant, 1964; Emsley & Nickle, 1969) se asignan esos ejemplares a esta especie en la que se aprecian ciertas diferencias referentes a la mayor prolongación del décimo terguito y sus estructuras membranosas, el esclerito más grande y arqueado y diente distal del cerco más desarrollado. Si bien éstas pueden ajustarse a las variaciones indicadas por Grant (1964). Agradecimientos Queremos expresar aquí nuestro agradecimiento a todas las personas que posibilitaron las jornadas de prospección en la Reserva Biológica Alberto Manuel Brenes. En primer lugar a don Alberto Hamer Salazar Rodríguez, director de la Reserva durante el periodo de prospecciones en 2006 y responsable costarri cense del proyecto INVARTAB. A don José Rafael Esteban Durán, investigador del INIA de Madrid y principal artífice para el desarrollo de las jornadas entomológicas desarrolladas por españoles en la RBAMB y corresponsable del proyecto INVARTAB en España. A los entomólogos don Marco Antonio Zumbado Echevarría de la Universidad de Costa Rica y Rolando Ramírez Campos por su inestimable ayuda en las prospecciones de campo durante la estancia y el envío posterior de material para su estudio. A don Hugo Pérez, por su afable trato, organización en la intendencia y predisposición para la ubicación y colocación de trampas de luz móviles. A las entidades que sufragaron la estancia en la RBAMB: Universidad de Almería que mediante el Plan propio concedió una subvención y a la Consejería de Innovación, Ciencia y Empresa de la Junta de Andalucía que concedió un incentivo de actividades de carácter científico y técnico, en la modalidad de estancia. Referencias Barranco, P., 2010a. Ortópteros de la Reserva Biológica Alberto Manuel Brenes (San Ramón, Costa Rica). I. Anostostomatidae y Tettigoniidae (Orthoptera: Ensifera). Boletín de la Sociedad Entomológica Aragonesa, 46: 509–517.

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– 2010b. Ortópteros de la Reserva Biológica Al berto Manuel Brenes (San Ramón, Costa Rica). II. Orthoptera: Caelifera. Boletín de la Sociedad Entomológica Aragonesa, 47: 21–32. Beier, M., 1960. Orthoptera, Tettigoniidae, Pseudo phyllinae II. Das Tierreich, 74: 1–396. – 1962. Orthoptera, Tettigoniidae, Pseudophyllinae I. Das Tierreich, 73: 1–468. Brunner von Wattenwyl, C., 1878. Monographie der Phaneropteriden. Verhandlungen der Kaiserlich– Königlichen Zoologisch–Botanischen Gesellsa chaft in Wien, 28: 1–401. – 1891. Additamenta zur Monographie der Phaneropteriden. Verhandlungen der Kaiserlich– Königlichen Zoologisch–Botanischen Gesellsa chaft in Wien, 41: 1–196. Cadena–Castañeda, O., 2012. La tribu Viadaniini n. trib. (Orthoptera: Tettigoniidae): primer aporte a la organización supra–genérica de los faneropterinos neotropicales. Journal of Orthoptera Research, 21(1): 25–43. Eades, D. C., Otte, D., Cigliano, M. M. & Braun, H., 2013. Orthoptera Species File Online. Version 2.0/4.1. [22/08/2013]. http://Orthoptera.SpecieFile.org Emsley, M. G. & Nickle, D. A., 1969. The systematics of Ceraia (Orthoptera: Tettigoniidae: Phaneropte rinae). Proceedings of the Academy of Natural Sciences, Philadelphia, 121: 25–78. Grant Jr., H. J., 1964. A revision of the genus Ceraia and Euceraia, with notes on their relationship to Scudderia (Orthoptera: Tettigoniidae: Phanerop terinae). Proceedings of the Academy of Natural Sciences, Philadelphia, 116(2): 29–147. Gorochov, A., 2012. Systematics of the American katydids (Orthoptera: Tettigoniidae). Communica tion 2. Trudy Zoologicheskogo Instituta, 316(4): 285–306. Nickle, D. A., 2003. New neotropical species of the genus Phlugis (Orthoptera: Tettigoniidae: Meco nematinae). Journal of Orthoptera Research, 12: 37–56. – 2005. Additional notes on the genus Phlugis (Or thoptera: Tettigoniidae: Meconematinae) with the descriptions of two new arboreal species from Costa Rica. Journal of Orthoptera Research, 14: 57–62. Morris, G. K. & Beier, M., 1982. Song structure and description of some Costa Rican katydids. Tran sactions of the American Entomological Society, 108: 287–314. Piza, S. T. Jr., 1980a. Espécies novas de Pseudo phyllinae especialmente do Brasil (Orthoptera, Tettigoniidae). Anais da Escola Superior de Agri cultura “Luiz de Queiroz” (Universidade de São Paulo), 37(1): 209–222. – 1980b. Oito novos gêneros de Phaneropterinae do Brasil (Orthoptera – Tettigoniidae). Revista de Agricultura (Piracicaba), 55(4): 221–230.

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Analysis of the effect of atmospheric oscillations on physical condition of pre–reproductive bluefin tuna from the Strait of Gibraltar J. C. Báez, D. Macías, M. de Castro, M. Gómez–Gesteira, L. Gimeno & R. Real Báez, J. C., Macías, D., De Castro, M., Gómez–Gesteira, M., Gimeno, L. & Real, R., 2013. Analysis of the effect of atmospheric oscillations on physical condition of pre–reproductive bluefin tuna from the Strait of Gibraltar. Animal Biodiversity and Conservation, 36.2: 225–233. Abstract Analysis of the effect of atmospheric oscillations on physical condition of pre–reproductive bluefin tuna from the Strait of Gibraltar.— The aim of this study was to explore the possible effects of atmospheric oscillations: North Atlantic Oscillation (NAO) and Arctic Oscillation (AO), on the physical condition of bluefin tuna (Thunnus thynnus). We estimated a fitness ratio from 3,501 pairs of length–weight data based on bluefin tuna caught in bait–boat fisheries before the spawning season (January, February and March), for each length class and year. In order to obtain a single fitness ratio (K–mean) per year we determined the average for all length classes. We also evaluated Le Cren’s condition index (KLC). We observed significant positive correlations between the atmospheric oscillations and both physical condition indexes. In the case of K–mean, the AO explained 75% of the observed variability. Regarding KLC, the NAO explained approximately 73% of the observed variability, while the AO explained 70% of the observed variability. The increase in physical conditions of bluefin tuna in association with positive atmospheric oscillations could be mediated by the increase in the prevalence of strong trade winds. We concluded that the increase in the prevalence of strong westerly winds, mediated by a positive AO or NAO, favours the trip from the Atlantic to the Mediterranean by reducing energy costs due to migration and by increasing the supply of nutrients at the surface by the mixing of deep water and surface water in local areas such as the Strait of Gibraltar. Key words: Arctic Oscillation, Atmospheric Oscillations, Clime, North Atlantic Oscillation, Fisheries, Tuna. Resumen Análisis del efecto de las oscilaciones atmosféricas en la condición física del atún rojo del estrecho de Gibraltar antes de su reproducción.— El objetivo de este estudio fue explorar los posibles efectos de las oscilaciones atmosféricas, la oscilación del Atlántico Norte (NAO) y la oscilación del Ártico (AO), en la condición física del atún rojo (Thunnus thynnus). Para ello, estimamos un índice de condición física para cada clase de talla y año a partir de 3.501 pares de datos de talla–peso de atunes capturados en la pesca de cebo vivo antes de la temporada de desove (enero, febrero y marzo). Con el fin de obtener un valor único del índice de condición física (K–mean) por año calculamos el promedio de todas las clases de talla. Además, calculamos el índice de condición física de Le Cren (KLC). Observamos correlaciones positivas significativas entre las oscilaciones atmosféricas y los dos índices decondición física. En el caso del K–mean, la AO explicó un 75% de la variabilidad observada. En relación con el KLC, la NAO explicó aproximadamente un 73% de la variabilidad observada, mientras que la AO explicó un 70% de la variabilidad observada. El aumento de la prevalencia de fuertes vientos de componente oeste podría intervenir en la mejora de la condición física del atún rojo asociada con una fase positiva de las oscilaciones atmosféricas. Llegamos a la conclusión de que el aumento de la prevalencia de fuertes vientos de componente oeste, ya sea por una AO o una NAO positiva, favorece el viaje de los atunes que llegan desde el Atlántico hasta el Mediterráneo porque, por un lado, reduce los costes energéticos de la migración y, por otro, aumenta la cantidad de nutrientes en superficie al mezclar las capas de agua profundas y superficiales en zonas locales como el estrecho de Gibraltar. Palabras clave: Oscilación ártica, Oscilaciones atmosféricas, Clima, Oscilación del Atlántico Norte, Pesca, Atún. ISSN: 1578–665 X eISSN: 2014–928 X

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Received: 26 VI 13; Conditional acceptance: 22 X 13; Final acceptance 22 XI 13 José C. Báez, David Macías & Raimundo Real, Depto. de Biología Animal, Fac. de Ciencias, Univ. de Málaga, E–29071 Málaga, España (Spain).– Maite De Castro, Moncho Gómez–Gesteira & Luis Gimeno, EphysLab, Univ. de Vigo, Fac. de Ciencias de Ourense, Ourense, España (Spain). Corresponding author: J. C. Báez, Inst. Español de Oceanografia (IEO), Centro Oceanográfico de Málaga, Puerto pesquero de Fuengirola s/n., 29640 Málaga, Spain. E–mail: jcarlos.baez@ma.ieo.es

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Introduction Many studies have described the response of tuna regarding factors such as distribution and recruitment to climatic variability (Fromentin et al., 2000; Fromentin, 2001, 2002a, 2002b, 2002c, 2003, 2009; Ravier–Mailly, 2003; Ravier & Fromentin, 2001a, 2001b, 2001c, 2002, 2003, 2004; Borja & Santiago, 2002; Mejuto, 2003; Caballero–Alfonso et al., 2012; Di Natale & Idrissi, 2012) and the cumulative influence of climate variability during the life history of fish (Báez et al., 2011b). Studies on the effect of climatic variability on the physical condition of tuna, however, are scarce (Golet et al., 2007; Báez et al., 2011b). The bluefin tuna (Thunnus thynnus), an economically important fish, is a highly pelagic migratory species and the largest member of the Scombridae family. According to the International Commission for the Conservation of Atlantic Tunas, this species is managed considering two stocks in the Atlantic Ocean: one that spawns in the Gulf of Mexico, and the other that spawns in the Mediterranean Sea. In the Mediterranean Sea, bluefin tuna are currently commercially caught mainly by purse seiners and tuna traps; catches by other gears are minor. Most catches occur just before, during and just after the spawning season —mainly from March to August, with a peak in June—, taking advantage of the massive influx of bluefin tuna from the Atlantic through the Strait of Gi-

braltar to the spawning grounds in the Mediterranean. In addition, some small–scale fishery is carried out by bait–boat and hand lines in the Strait of Gibraltar throughout the year (fig. 1). Commercial bait–boats in this area mainly target adult bluefin tunas. The North Atlantic Oscillation (NAO) is a dominant pattern of coupled ocean–climate variability in the North Atlantic and Mediterranean basin (Hurrell, 1995). However, this atmospheric oscillation is closely correlated with Arctic Oscillation (AO). Nevertheless, the dominant mode of atmospheric circulation variability in the Northern Hemisphere is determined by the Arctic Oscillation (AO). The AO is characterized by a meridional dipole in atmospheric sea level pressure between the northern polar regions and mid–latitudes (Thompson & Wallace, 1998). The AO has been attributed to stratosphere–troposphere coupling. According to Thompson et al. (2000), this includes the NAO, which may be considered a different view of the same phenomenon. Thus, the AO and the NAO both tend to be in a positive phase during winters when the stratospheric vortex is strong (Douville, 2009). Few studies have analyzed the possible effect of the AO on fish ecology; for example, Yatsu et al. (2005) studied this effect in the Pacific Ocean, and Gancedo (2005) in the Atlantic Ocean. The aim of this study was to explore the possible effects of the NAO and AO on the physical condition of bluefin tuna.

–6º 20'

–6º 00'

–5º 40'

–5º 20'

–5º 00'

–4º 40' 36º 40'

36º 20'

Gulf of Cadiz Strait of Gibraltar

36º 00'

Alboran Sea

35º 40'

35º 20'

GMT 2011 Oct 18 04:18:39

Seaturtle.org/maptool Projection: Mercator

Fig. 1. The study area was centred on the Strait of Gibraltar. The Strait of Gibraltar separates two regions: the Gulf of Cadiz (in the Atlantic Ocean) and the Alboran Sea (within the Mediterranean Sea). Fig. 1. La zona del estudio tiene en su centro el estrecho de Gibraltar. El estrecho de Gibraltar separa dos regiones: el golfo de Cádiz (en el océano Atlántico) y el mar de Alborán (en el mar Mediterráneo).

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Table 1. Length–weight relationship parameters per year for the bluefin tuna (Thunnus thynnus) longer than 130 cm FL, and caught in bait–boat between January and March in the Strait of Gibraltar: Year. Year of harvest; n. Number of tunas sampled per year; R2. Regression coefficient from each adjust the length–weight relationships, according to the function: W = a·FLb (i), where W is the weight and FL is fork length; P. Significance observed per function; a. Constant parameter of the function; b. Power parameter of the function. Tabla 1. Parámetros que relacionan la talla y el peso por año para los ejemplares de atún rojo (Thunnus thynnus) cuya longitud furcal supere los 130 cm y se hayan capturado en la pesca de cebo vivo entre enero y marzo en el estrecho de Gibraltar: Year. Año de la captura; n. Número de atunes muestreados por año; R2. Coeficiente de regresión de cada ajuste de las relaciones talla–peso, de acuerdo con la función: W = a·FLb (i), donde W es el peso y FL es la longitud furcal; P. Significancia observada por función; a. Parámetro constante de la función; b. Potencia de la función. Year

2001

681

2002

R 2

0.969

< 0.001

20888.4

0.0485

2.808

482

0.977

< 0.001

20298.9

0.0332

2.8894

2003

683

0.969

< 0.001

18868.9

0.0892

2.6961

2004

170

0.956

< 0.001

3691.77

0.0476

2.8221

2005

401

0.95

< 0.001

7608.74

0.0581

2.7841

2006

139

0.981

< 0.001

7089.96

0.0338

2.885

2007

582

0.95

< 0.001

11087

0.0608

2.772

2008

308

0.931

< 0.001

4109.96

0.1155

2.6539

2009

0.886

< 0.001

256.58

0.0249

2.949

2010

0.951

< 0.001

348.38

0.1625

2.5771

Material and methods The study area coincides with the the fishing ground located in Spanish waters of the Strait of Gibraltar between the Rock of Gibraltar and Cape Trafalgar (fig. 1). We hypothesized that the physical condition of bluefin tuna before the spawning season could be associated with atmospheric oscillations. Under this hypothesis, the accumulation of fat by adult bluefin tuna during the pre–spawning period could have reproductive benefits during the spawning season and be a crucial factor in spawning success. The length–weight relationship (LWR) in fishes is a widely used tool in fisheries biology and has several applications in population dynamics and stock assessment. Moreover, the LWR in fishes from a specific geographic region during a specific season could be useful to estimate their physical condition. We used 3501 pairs of length–weight data based on bluefin tuna caught in bait–boat fisheries before the spawning season (January, February and March) from 2001 to 2010 (see Macías et al., 2011) (table 1). To adjust the length–weight relationships, a power curve regression was used according to the function: W = a·FLb

(i)

where W is the weight, FL is fork length, and a and b are parameters of the function. According to Froese (2006), based on the length–weight relationship, it is possible to estimate a fitness ratio or K–mean for each length class and year: K–mean= a·FL(b-3) to obtain a single value of K–mean per year we obtained the average for all length classes, b�� ecause K–mean could be affected by changes in length (Le Cren, 1951; Nath Saha et al., 2009). According to Le Cren (1951), the effect of length could be eliminated using Le Cren’s condition index (KLC, hereafter): Wo/We; where Wo is the weight observed per fish, and We is the weight estimated from the formula (i). Atmospheric data Monthly values of the NAO index and AO index during the study period were taken from the website (from 2000 to 2010) of the National Oceanic and Atmospheric Administration: http://www.cpc.noaa. gov/products/precip/CWlink/pna/nao_index.html and http://www.esrl.noaa.gov/psd/data/correlation/ao.data, respectively.

Animal Biodiversity and Conservation 36.2 (2013)

Table 2. The physical condition indexes (K– means and KLC) obtained per year according to Froese (2006) and Le Cren (1951), respectively: NAOsm. Average of the monthly North Atlantic Oscillation index between September of the year prior to capture, to March; AOsm. Average of the monthly Arctic Oscillation index between September of the year prior to capture, to March (AOsm). Tabla 2. Los índices de condición física (K– means y KLC) obtenidos por año según Froese (2006) y Le Cren (1951), respectivamente: NAOsm. Promedio del índice mensual de la oscilación del Atlántico Norte entre septiembre del año anterior a la captura y marzo; AOsm. Promedio del índice mensual de la oscilación ártica entre septiembre del año anterior a la captura y marzo (AOsm). Year

NAOsm

AOsm

K–mean

2001

–0.1929

–0.927

1.797

2002

0.1629

0.4406

1.8805 1.00486

2003

–0.429

–0.5657

1.813

2004

0.12

–0.3131

KLC

229

Table 3. Pearson´s correlation obtained between the physical condition indexes (K– means and K LC), obtained per each year according to Froese (2006) and Le Cren (1951), respectively, and the average of the monthly North Atlantic Oscillation index between September of the year prior to capture, to March (NAOsm); and the average of the monthly Arctic Oscillation index between September of the year prior to capture, to March (AOsm). Tabla 3. Correlación de Pearson entre los índices de condición física (K–means y KLC) obtenidos por año según Froese (2006) y Le Cren (1951) respectivamente, el promedio del índice mensual de oscilación del Atlántico Norte entre septiembre del año anterior a la captura y marzo (NAOsm) y el promedio del índice mensual de la oscilación ártica entre septiembre del año anterior a la captura y marzo (AOsm).

0.967 0.989

Atmospherics oscillations AO

1.866

1.0249

2005

0.1214 –0.00214 1.844

1.0239

2006

–0.2314

–0.425

1.893

0.991

2007

–0.1271

0.613

1.943 1.00956

2008

0.5414

0.458

1.913

2009

0.1429

0.334

1.9044 1.0487

2010

–0.7771

–1.558

1.839

NAO

K–mean

KLC

R2 = 0.752

R2 = 0.695

p = 0.012

p = 0.026

Not significant

R2 = 0.728

p = 0.017

1.0365 0.986

We expected a delay between the atmospheric fluctuation and the capture and physical condition of bluefin tuna. Since the catches of bluefin tuna in bait–boat occur from January to March, and the feeding season extends from September (end of post–reproductive migration) to March (beginning of reproductive migration), we used the average of the monthly AO and NAO indexes from September of the year prior to capture to March (AOsm and NAOsm, respectively, hereafter). Data analysis We initially obtained ten length/weight relationships, one for every year studied. Length �� and weight frequencies by year can be seen in Macias et al. (2011). The different K–mean and KLC per year (table 2) were estimated from these parameters. We correlated both parametric variables using Pearson correlations. Normality of the data was tested by means of the Kolmogorov–Smirnov test (Sokal & Rohlf, 1995).

Results and discussion We observed positive significant correlations between the atmospheric oscillations and the two physical condition indexes (table 3). In the case of K–mean, the AO explained 75% of the observed variability, while the relationship with NAOsm was not significant (fig. 2). Regarding KLC, the NAO explained approximately 73% of the observed variability, while the AO explained 70% of the observed variability (fig. 3). Our results indicate that the physical condition indexes (K–mean and KLC) of bluefin tuna caught from the Strait of Gibraltar are associated with the atmospheric oscillations. The present paper is the first reference about the effect of AO on fisheries located that southerly. Positive AO phase is characterized by a strong polar vortex (from the surface to the lower stratosphere). In this situation, storms increase in the North Atlantic and drought prevails in the Mediterranean basin. When the AO is in a negative phase, the continental cold air sinks into the Midwestern United States and Western Europe, while storms bring rain to the Mediterranean region (Ambaum et al., 2001; Báez et al., 2013).

230

Báez et al.

1.96

1.94 1.92

R2 = 0.2324

K–mean

1.9 1.88 1.86 1.84 1.82 1.8 –1

–0.8

–0.6

–0.4

1.78 –0.2 0

0.2

0.4

0.6

0.8

KCL

–1

–0.8

–0.6

–0.4

1.06 1.05 1.04 1.03 1.02 1.01 1 0.99 0.98 0.97 0.96 –0.2 0 NAOsm

R2 = 0.5348

0.2

0.4

0.6

0.8

Fig. 2. Plots showing the correlation between the bluefin tuna physical condition indexes and the average of NAO for the period from September (previous year of the capture) to March (NAOsm): A. Relationship between K–mean vs. NAOsm; B. Relationship between KCL vs. NAOsm. The linear regression coefficient (R2) is shown in both plots. Fig. 2. Gráficos en los que se muestra la correlación existente entre los índices de condición física del atún rojo y el promedio de la NAO en el período comprendido entre septiembre (año anterior a la captura) y marzo (NAOsm): A. Relación entre el K-mean y el NAOsm; B. Relación entre el KLC y el NAOsm. En ambos gráficos se muestra el coeficiente de regresión lineal (R2).

As Visbeck et al. (2001) reported, a positive NAO phase results in stronger–than–average westerly winds across northern mid–latitudes, which affect both marine and terrestrial ecosystems. Therefore, the increase in bluefin tuna physical condition in association with a positive AO or NAO could be mediated by the increase in the prevalence of strong westerly winds, in the geographical area delimited between the parallels 40 N and 60 N (�� Greatbatch, 2000)�� . Strong winds agitate the water, favouring the mixing of deep water and surface water, and thus increasing the supply of nutrients at the surface. Studies from the stomach contents of 595 specimens of bluefin tuna caught from Gibraltar area indicated the opportunistic character of this species in terms of feeding strategy (Serna et al., 2012). Changes in the

nutrient concentration in the local area could therefore affect the bluefin tuna in the short term. Golet et al. (2007) observed a significant decline in the fat and oil content and shape of northern bluefin tuna landed in the Gulf of Maine over a period of 14 years. They suggested this decline was due to an increase in the number of bluefin tuna migrating to the Gulf of Maine from the eastern Atlantic. Thus, according to Golet et al. (2007) both increases in bluefin tuna migration distance and travel through unproductive waters imply a major cost in stored energy. Similarly, in the case of migrant loggerhead sea turtles, Báez et al. (2011a) observed that prevailing westerly winds during positive NAO phases and the subsequent delayed decrease in SST may lead to

Animal Biodiversity and Conservation 36.2 (2013)

231

1.96

1.94 1.92

R2 = 0.5668

K–mean

1.9 1.88 1.86 1.84 1.82 1.8

–2

–1.5

–1

–0.5

1.78

0.5

KCL

–2

–1.5

–1

–0.5 AOsm

1.06 1.05 1.04 1.03 1.02 1.01 1 0.99 0.98 0.97 0.96

R2 = 0.4839

0.5

Fig. 3. Plots showing the correlation between the bluefin tuna physical condition indexes and the average of AO from September (previous year of the capture) to March (AOsm): A. The relationship between K–mean vs. AOsm; B. The relationship between KCL vs. AOsm. The linear regression coefficient (R2) is shown in both plots. Fig. 3. Gráficos en los que se muestra la correlación existente entre los índices de condición física del atún rojo y el promedio de la AO entre septiembre (año anterior a la captura) y marzo (AOsm): A. Relación entre el K–mean y el AOsm; B. Relación entre el KCL y el AOsm. En ambos gráficos se muestra el coeficiente de regresión lineal (R2).

turtles from the West Atlantic accumulating in the Gulf of Cadiz and Mediterranean Sea. We concluded that the increase in the prevalence of strong trade winds, mediated by a positive AO or NAO, can improve the physical condition of bluefin tuna in their journey from the Atlantic to the Mediterranean. These strong winds reduce energy costs due to migration and increase the supply of nutrients at the surface by mixing deep water and surface water in local areas such as the Strait of Gibraltar. Our results indicate that the positive phases of the main atmospheric oscillation in the North Atlantic Ocean (AO and NAO) could favour good physical condition pre–spawning individuals being in. This better physical condition could improve the spawning season (the spawners may lay more and

better–quality eggs, and the spawning season could last longer). The better quality of eggs could produce offspring that have higher survival and growth rates, having an effect on subsequent recruitment (Berkeley et al., 2004a, 2004b; Birkeland & Dayton, 2005). In addition, a longer spawning season could improve the survival rate of larvae (Cushing, 1995). More studies are needed to determine further possible relationships between atmospheric oscillations and bluefin tuna recruitment. Acknowledgements This work was partially supported by projects from the IEO based in Malaga, GPM–4 programs (IEO)

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and PNDB (EU–IEO), project CGL 2009–11316/ BOS from the Spanish Government and FEDER, and from the Xunta de Galicia under Programa de Consolidación e Estruturación de Unidades de Investigación (Grupos de Referencia Competitiva) funded by FEDER. We would also like to thank Andrew Paterson for style corrections. References Ambaum, M. H. P., Hoskins, B. J. & Stephenson, D. B., 2001. Arctic Oscillation or North Atlantic Oscillation?. Journal of Climate, 14: 3495–3507. Báez, J. C., Gimeno, L., Gómez–Gesteira, M., Ferri– Yáñez, F. & Real, R., 2013. Combined effects of the Arctic Oscillation and the North Atlantic Oscillation on Sea Surface Temperature in the Alborán Sea. PlosOne, 8(4): e62201. DOI:10.1371/journal. pone.0062201 Báez, J. C., Bellido, J. J., Ferri–Yáñez, F., Castillo, J. J., Martín, J. J., Mons, J. L., Romero, D. & Real, R., 2011a. The North Atlantic Oscillation and sea surface temperature affect loggerhead abundance around the Strait of Gibraltar. Scientia Marina, 75(3): 571–575. Báez, J. C., Ortiz De Urbina, J. M., Real, R. & Macías, D., 2011b. Cumulative effect of the north Atlantic oscillation on age–class abundance of albacore (Thunnus alalunga). Journal of Applied Ichthyology, 27: 1356–1359. Berkeley, S. A., Chapman, C. & Sogard, S. M., 2004a. Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology, 85: 1258–1264. Berkeley, S. A., Hixon, M. A., Larson, R. J. & Love, M. S., 2004b. Fisheries Sustainability via protection of age structure and spatial distribution of fish populations. Fisheries, 29: 23–32. Birkeland, C. & Dayton, P. K., 2005. The importance in fishery management of leaving the big ones. Trends in Ecology and Evolution, 20: 356–358. Borja, A. & Santiago, J., 2002. Does the North Atlantic Oscillation control some processes influencing recruitment of temperate tunes? ICCAT Collective Volume, Scientific Papers, 54: 964–984. Caballero–Alfonso, A. M., Ganzedo, U., Zorita, E., Ibarra–Berastegi, G., Sáenz, J., Ezcurra, A., Trujillo– Santana, A., Santana del Pino, A. & Castro–Hernández, J. J., 2011. Climate and historic fluctuations in the Gibraltar Strait and western Mediterranean. Presented at the ICCAT–GBYP Symposium on Trap Fishery for Bluefin Tuna, Tangier. Cushing, D., 1995. Population production and regulation in the sea: a fisheries perspective. Ed. Cambridge University Press, Cambridge, U.K. Di Natale, A. & Idrissi, M., 2012. Factors to be taken into account for a correct reading of tuna trap catch series. Collect. Vol. Sc. Pap. ICCAT, 67(1): 242–261. Douville, H., 2009. Stratospheric polar vortex influence on Northern Hemisphere winter climate variability. Geophysical Research Letters, 36: 1–5. Froese, R., 2006. Cube law, condition factor and

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Animal Biodiversity and Conservation 36.2 (2013)

Animal Biodiversity and Conservation

Manuscrits

Animal Biodiversity and Conservation és una revista interdisciplinària publicada, des de 1958, pel Museu de Ciències Naturals de Barcelona. Inclou articles d'inves tigació empírica i teòrica en totes les àrees de la zoo logia (sistemàtica, taxonomia, morfologia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfasis als estudis que permetin compendre, desde un punt de vista pluridisciplinar i integrat, els patrons d'evolució de la biodiversitat en el seu sentit més ampli. La revista no publica compilacions bibliogràfiques, catàlegs, llistes d'espècies o cites puntuals. Els estudis realitzats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles. Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a internet a www.abc.museucienciesjournals.cat, 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.

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Animal Biodiversity and Conservation 36.2 (2013)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation es una revista interdisciplinar, 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, morfología, biogeografía, ecología, etología, fisiología y genéti ca) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que permitan comprender, desde un punto de vista pluridisciplinar e integrado, los patrones de evolución de la biodi versidad en su sentido más amplio. La revista no publica compilaciones 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 www.abc.museucienciesjournals.cat, lo que permite una difusión mundial de sus artículos. Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siempre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo. Una vez aceptado, el trabajo pasará a ser 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.

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ISSN: 1578–665X eISSN: 2014–928X

III

remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modifica ciones sustanciales en las pruebas de imprenta, intro ducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en formato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 lí neas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado. El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofrece, sin cargo ningu no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitándose siempre la primera persona. Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común. Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo. Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase. Las fechas se indicarán de la siguiente forma: 28 VI 99 (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 especulacio nes 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. Animal Biodiversity and Conservation. 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 36.2 (2013)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation is an inter disciplinary journal published by the Natural Science Museum of Barcelona since 1958. It includes empiri cal and theoretical research from around the world that examines any aspect of Zoology (Systematics, Taxonomy, Morphology, Biogeography, Ecology, Ethol ogy, Physiology and Genetics). Special emphasis is given to integrative and multidisciplinary studies that help to understand the evolutionary patterns in biodiversity in the widest sense. The journal does not publish bibliographic compilations, listings, catalogues or collections of species, or isolated descriptions of a single specimen. 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 registered in all principal data bases and is freely available online at www.abc.museucienciesjour nals.cat assuring world–wide access to articles published therein. All manuscripts are screened by the Executive Editor, 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 ac cepted, papers are published as soon as is practicable. This is usually within 12 months of initial submission. Upon acceptance, manuscripts become the pro perty 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 Catalan, 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 genera and species as well as untrans latable neologisms must be in italics. Quotations in whatever language used must be typed in ordinary print between quotation marks. The name of the author following a taxon should also be written in 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 are proper nouns (e.g. Iberian rock lizard). Place names may appear either in their original form or in the language of the manuscript, but care should be taken to use the same criteria throughout the text. Numbers one to nine should be written in full 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. A cover letter stating that the article reports original research that has not been published elsewhere and has been submitted exclusively for considera tion 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 protection 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 eISSN: 2014–928X

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 authors will be translated by the journal on request. Palabras clave in Spanish. Address of the author or authors. (Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.) Introduction. Should include the historical back ground of the subject as well as the aims of the paper. © 2013 Museu de Ciències Naturals de Barcelona

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. Animal Biodiversity and Conservation. References must be set out in alphabetical and chrono

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

Animal Biodiversity and Conservation 36.2 (2013)

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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, BIOSIS Previews, CiteFactor, Current Primate References, Current Contents/Agriculture, Biology & Environmental Sciences, DIALNET, DOAJ, DULCINEA, e–revist@s, 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, Latindex, Marine Sciences Contents Tables, Oceanic Abstracts, RACO, Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Science Citation Index Expanded, Scientific Commons, SCImago, SCOPUS, Serials Directory, SHERPA/ RoMEO, Ulrich’s International Periodical Directory, Zoological Records.

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Índex / Índice / Contents Animal Biodiversity and Conservation 36.2 (2013) ISSN 1578–665X eISSN 2014–928X

141–152 V. M. Ortuño & P. Barranco Duvalius (Duvalius) lencinai Mateu & Ortuño, 2006 (Coleoptera, Carabidae, Trechini) una especie hipogea del sur de la península ibérica. Morfología, reubicación taxonómica, sistemática y biología 153–163 I. de la Hera, J. Arizaga & A. Galarza Exotic tree plantations and avian conservation in northern Iberia: a view from a nest–box monitoring study 165–175 M. Sarasa Trophy hunting, size, rarity and willingness to pay: inter–specific analyses of trophy prices require reliable specific data 177–185 J. Guerrero–Casado, J. Letty & F. S. Tortosa European rabbit restocking: a critical review in accordance with IUCN (1998) guidelines for re–introduction 187–194 A. Martínez–Ortí & F. Robles El viaje del Prof. Emil A. Rossmässler en 1853 por España y la localidad tipo de Iberus angustatus (Rossmässler, 1854) (Gastropoda, Helicidae)

Amb el suport de / Con el apoyo de / With the support of:

195–207 C. A. Mancina, D. Rodríguez Batista & E. Ruiz Rojas Spatial distribution patterns of terrestrial bird assemblages on islands of the Sabana– Camagüey Archipelago, Cuba: evaluating nestedness and co–occurrence patterns 209–215 M. Delibes–Mateos & A. Delibes Pets becoming established in the wild: free– living Vietnamese potbellied pigs in Spain 217–223 P. Barranco Vega Descripción de tres nuevas especies de tetigónidos de Costa Rica (Orthoptera, Tettigoniidae) 225–233 J. C. Báez, D. Macías, M. de Castro, M. Gómez– Gesteira, L. Gimeno & R. Real Analysis of the effect of atmospheric oscillations on physical condition of pre–reproductive bluefin tuna from the Strait of Gibraltar