Animal Biodiversity and Conservation issue 26.2 (2003)

Formerly Miscel·lània Zoològica

2003

and

Animal Biodiversity Conservation 26.2

Mallarenga carbonera Parus major. Dibuix de Rafa Torralbo publicat al Butll. GCA, 17(2000) p 23 Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo–Roura Univ. Pompeu Fabra, Barcelona, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Vicente M. Ortuño Univ. de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Univ. de les Illes Balears, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA­–CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas–CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway Animal Biodiversity and Conservation 26.2, 2003 © 2003 Museu de Ciències Naturals (Zoologia), Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://bcn.cat/ABC

Animal Biodiversity and Conservation 26.2 (2003)

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A higher–taxon approach to rodent conservation priorities for the 21st century G. Amori & S. Gippoliti

Amori, G. & Gippoliti, S., 2003. A higher–taxon approach to rodent conservation priorities for the 21st century.

Animal Biodiversity and Conservation, 26.2: 1–18.

Abstract A higher–taxon approach to rodent conservation priorities for the 21st century.— Although rodents are not considered among the most threatened mammals, there is ample historical evidence concerning the vulnerability to extinction of several rodent phylogenetic lineages. Owing to the high number of species, poor taxonomy and the lack of detailed information on population status, the assessment of threat status according to IUCN criteria has still to be considered arbitrary in some cases. Public appreciation is scarce and tends to overlook the ecological role and conservation problems of an order representing about 41 percent of mammalian species.

We provide an overview of the most relevant information concerning the conservation status of rodents at the genus, subfamily, and family level. For species–poor taxa, the importance of distinct populations is highlighted and a splitter approach in taxonomy is adopted. Considering present constraints, strategies for the conservation of rodent diversity must rely mainly on higher taxon and hot–spot approaches. A clear understanding of phyletic relationships among difficult groups —such as Rattus, for instance— is an urgent goal. Even if rodent taxonomy is still unstable, high taxon approach is amply justified from a conservation standpoint as it offers a more subtle overview of the world terrestrial biodiversity than that offered by large mammals. Of the circa 451 living rodent genera, 126 (27,9 %), representing 168 living species, deserve conservation attention according to the present study. About 76 % of genera at risk are monotypic, confirming the danger of losing a considerable amount of phylogenetic distinctiveness.

Key words: Mammals, Rodents, Conservation priorities, Phylogenetic distance.

Resumen Aproximación a nivel de suprataxón de las prioridades de conservación de roedores en el siglo XXI.— Aunque los roedores no figuren entre los mamíferos con mayor amenaza de extinción, existen pruebas históricas que demuestran la vulnerabilidad de diversos linajes filogenéticos de roedores. Debido al gran número de especies existentes, la taxonomía deficiente y la falta de información detallada sobre el estado de las poblaciones, en determinados casos es arbitrario determinar hasta qué punto algunas especies se encuentran en peligro de extinción de acuerdo con los criterios de la UICN. Además, si a ello se une el escaso aprecio que el público en general siente por los roedores, la situación explica que se pase por alto tanto el papel ecológico como los problemas de conservación de un orden al que pertenecen aproximadamente el 40% de todas las especies de mamíferos. Se proporciona información exhaustiva y relevante sobre el estado de conservación de los roedores, a nivel de género, familia y subfamilia. Para aquellas especies cuya taxonomía sigue estando incompleta, se destaca la importancia de las distintas poblaciones y su taxonomía se analiza por separado. A causa de las limitaciones actuales, las diferentes estrategias para la conservación de la diversidad de roedores deben basarse fundamentalmente en un mayor análisis del taxón y de los lugares de mayor concentración de poblaciones.

Asimismo, una clara comprensión de las relaciones filéticas entre grupos difíciles (como por ejemplo Rattus) constituye un objetivo apremiante. Pese a que la taxonomía de los roedores no sea aún definitiva, desde un punto de vista conservacionista sigue siendo absolutamente justificable analizar el taxón con mayor detenimiento, ya que ofrece una visión general más precisa de la biodiversidad en zonas continentales que la que ofrecen los grandes mamíferos. De los aproximadamente 451 géneros de roedores existentes, 126 (el 27,9 %), que engloban a 168 especies, merecen una especial atención conservacionista según los datos de este estudio. Entre los ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

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Amori & Gippoliti

géneros que se encuentran en peligro de extinción, un 76 % son monotípicos, lo que confirma el peligro de perder una cantidad considerable de singularidades filogenéticas.

Palabras clave: Mamíferos, Roedores, Prioridades de conservación, Distancia filogenética.

(Received: 13 III 03; Conditinal acceptance: 27 III 03; Final acceptance: 29 VII 03)

Giovanni Amori & Spartaco Gippoliti, Istituto per lo Studio degli Ecosistemi CNR, Via Borelli 50, 00161 Rome (Italy) and IUCN/SSC Rodent Specialist Group. E–mail: giovanni.amori@uniroma1.it

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Animal Biodiversity and Conservation 26.2 (2003)

Introduction More than 10 years later, the papers collected

by LIDICKER (1989) after the 1985 meeting at the Third International Theriological Congress still provide the most recent global overview of rodent conservation status. Comprehensive synthesis and Action Plans are available for North America and Australia only (HAFNER et al., 1998; LEE, 1995), although more preliminary contributions at national or regional level have also been compiled (e.g. AMORI & ZIMA, 1994; HEANEY et al., 1998). National Red Lists are not included.

The high number of species and lack of experts, especially in relation to tropical faunas, impede significant progress with rodent conservation.

Current emphasis on biodiversity mapping and identification of conservation priorities which are not species–specific, highlight the importance of rodents (almost cosmopolitan in distribution, more than 2000 recognised species globally, more than 40 species and at least twelve new genera discovered since 1992 in the Neotropics alone (PATTERSON, 2000, MARES et al. 2000) as a biodiversity indicator group to use in setting world–wide conservation priorities. Furthermore, the vulnerability of this order is demonstrated by the fact that Rodent species represent 51– 52 % of mammalian extinctions in the last 500 years (CEBALLOS & BROWN, 1995; MACPHEE & FLEMMING, 1999). In Australia, native rodents suffer a 19 % extinction rate in contrast with 6.3 % of the total mammalian fauna (SMITH & QUIN, 1996). On the contrary, conservation initiatives will continue to be biased towards the most studied and attractive mammal groups and species (AMORI & GIPPOLITI, 2000) or on an opportunistic basis, despite increasing evidence of many rodent species sustaining ecosystems structures and functions. There are many examples of rodents performing critical and non–ecologically redundant roles in communities. Praire dogs Cynomys spp. are known to alter prairie land– scape in a way which is beneficial to a number of other species, providing foraging, shelter and nesting sites. Declining species such as the black– footed ferret Mustela nigripes, burrowing owl Athene cunicularia and ferruginous hawks Buteo regalis depend in some way on prairie dogs to hasten their population demise (KOTLIAR, 2000).

Other rodents suspected to have a key role in ecosystems include subterranean pocket gophers like Geomys bursarius and Thomomys bottae and the desert–adapted kangaroo rats Dipodomys spp. (POWER et al., 1996). The pocket gopher Tomomys bottae has been demonstrated to limit the establishment of the exotic and invasive barbed goatgrass Aegilops triuncialis through the control of a fungus (EVINER & CHAPIN, 2003). In general, pocket gophers have positive effects on ecosystems creating patterns of disturbance and promoting diversity (REICHMAN & SEABLOOM, 2002), a finding which could probably be gener-

alised to most subterranean rodents. Beavers Castor spp. are well known "ecosystem engineers", physically modifying river courses through the building of dams and creating the ideal habitats for a variety of species linked to wetlands (POLLOCK et al., 1995). Particular attention has also been attracted by the role of rodents in forest fragmentation dynamics (K OLLMANN & BUSCHOR, 2003; SANTOS & TELLERÍA, 1997). Finally, the importance of maintaining overall rodent species' diversity is illustrated by OSTFIELD & KEESING (2000). These authors found that exposure risk to Lyme disease in humans —a spirochetal disease transmitted by an ixodid tick— increases with reduction of small mammal species richness owing to dominance of a single common, most competent reservoir host, Peromyscus leucopus.

With the aim of providing governments, conservation organisations, and the captive–breeding community with some easy references to global rodent conservation priorities and to highlight the gaps in our understanding of rodent diversity, we undertook the task of reviewing, family by family, the conservation status of Rodentia, as it emerges from the most recently available Red List (IUCN, 2002) and other published information. In particular, given the size of the task —329 species and 61 subspecies are considered threatened to date (IUCN, 2002)— limited knowledge and interest, we feel it is appropriate to convey resources toward "higher" taxa (genus, subfamily or family) of conservation concern. However, we discuss conservation priorities at an intraspecific level in the case of species–poor lineages. Concentrating on threatened genera may result in a bias of interest towards those genera that have one or a few species as well as limited distribution, and which are probably locally rare (cf. SMITH & PATTON, 1993). However, these are clearly at greatest risk of disappearing (RUSSELL et al., 1998) and are most in need of urgent conservation measures. Furthermore, the presence of such relict taxa may underline areas of refuge and endemism for many other little–known organisms and provide an opportunity to detect and protect otherwise neglected habitats which lack more attractive vertebrates. M ACE & BALMFORD‘s (2000) analysis of Red List Mammals confirms the risk of losing a considerable amount of phylogenetic information because most species– poor orders and families are threatened.

Methods Systematic order follows WILSON & REEDER (1993) if not otherwise stated. This basic work has been updated using NOWAK (1999) as the main source together with other papers which appeared later.

Genera of conservation concern were divided into three categories. The first (threatened genera) in-

Amori & Gippoliti

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cludes all genera with all species included in the IUCN category of threat (Critically Endangered, Endangered and Vulnerable) or extinct (AMORI & GIPPOLITI, 2001). The second (potentially–threatened genera) includes those having all species in the threatened and near–threatened categories (i.e. Lower Risk: Conservation Dependent; Lower Risk: Near Threatened; Data Deficient). While based primarily on the 2002 IUCN Red list (IUCN, 2002), a few genera were also included as threatened even if they are not yet included in the IUCN Red List; these are Cansumys, Abditomys, Limnomys, Microhydromys, and Paulamys. Finally, a number of genera (genera of concern) are also briefly discussed as, owing to small ranges and ecological characteristics, they seem vulnerable to further habitat degradation in spite of the fact that they do not qualify for inclusion in the two above categories.

Systematic account Aplodontidae Monotypic primitive family restricted to the wet forest of north west United States, not threatened globally, but two subspecies, Aplodontia rufa nigra and A. rufa phaea, are considered vulnerable because of small geographic ranges (62 and 175 km2 respectively), habitat encroachment and predation from feral cats and dogs (STEELE, 1998).

Sciuridae All continents except Australia and Madagascar.

Threatened genera include Myosciurus – coastal central Africa including Bioko Island (GHARAIBEH & JONES , 1996); Eupetaurus – North–western Himalaya, where a population size of 1000– 3000 is estimated (ZAHLER & WOODS, 1997) and Yunnan, Hyosciurus (two species) – Sulawesi; Biswamoyopterus – North–eastern India and only known from the type specimen (C ORBET & HILL, 1992); Trogopterus – apparently widely distributed in mountain forests of Central and Southern China and Tibet between 1360– 2750 m a.s.l. but might be less threatened than thought given the wide use of this species’dung in traditional Chinese medicine (SUNG, 1998); the several taxa described by Thomas are all included in T. xanthipes (HOFFMANN et al., 1993).

If Allosciurus is accepted as a valid monotypic genus separated from Protoxerus, it may warrant inclusion here, as A. aubinni is rare and restricted to high forest from Liberia to Ghana (GRUBB et al., 1998; KINGDON , 1997). Several other genera are potentially threatened. These are Aeretes, only known from two isolated populations in Hebei / Gansu and Sichuan in China (SUNG , 1998); Belomys of South–eastern Asia; Epixerus of Central–western Africa, but

at least E. ebii could be only apparently rare owing to its extreme shyness (EMMONS, 1980); Euglacomys of North–western Himalaya – whose generic status has recently been confirmed (THORINGTON et al., 1996), although the only species, fimbriatus , appears to be common in various Pakistan habitats (ZAHLER & K ARIM, 1998); Pteromyscus of South–eastern Asia and Syntheosciurus , known only from four montane forest localities in Costa Rica and Panama (WELLS & GIACALONE, 1985). The Oriental Region, particularly the Sunda shelf, appears as the centre of endemism for Petauristini and Sciurini (MOORE & TATE, 1965), but deforestation and recent fires in the region may have negatively affected the status of an unknown number of taxa, especially endemics of small areas such as Hylopotes bartelsi from Western Java and Glyphotes simus and Dremomys everetti, both restricted to North–western Borneo. The maintenance of Sciuridae diversity is probably dependent on primary forest conservation (JOSHUA & J OHNSINGH, 1994) even though some species may take advantage of forest disturbance and fragmentation (U MAPATHY & K UMAR , 2000); these should benefit from programmes for primate habitat conservation. As the introduction of non–native squirrels may be a serious threat to native species (G URNELL & LURZ , 1997), trade in living squirrels should at least be carefully monitored.

Castoridae Holarctic, two species usually recognised (but see LAVROV, 1983), neither of which globally threatened. Castor fiber is being reintroduced in its former European range (NOLET & ROSELL, 1998), but several Asian subspecies – the Siberian, the Mongolian (STUBBE et al., 1991) and especially the Tuvinian subspecies Castor fiber tuvinicus, which was reduced to 40–50 individuals in the upper reaches of the Yenisei River (LAVROV, 1983), may be at serious risk and some of them have recently been added to the Red List (IUCN, 2002). Castor canadensis has been introduced in southern South America (EISENBERG, 1989), where it may constitute a severe ecological problem.

Geomyidae Canada to North–western Colombia. The monotypic Zygogeomys of Sierra Madre of Michoan (South–western Mexico) is threatened owing to competition with gophers of the genus Cratogeomys which penetrated into Zygogeomys range as the result of agricultural encroachment and deforestation (HAFNER & BARKLEY, 1984). Five threatened pocket gopher species are found in Mexico, and one in Costa Rica. Although locally common, most Central American species have restricted ranges which pose some conservation problems if agricultural encroachment continues.

Animal Biodiversity and Conservation 26.2 (2003)

Heteromyidae Mainly North America, but reaching North–western South America. No threatened genus but many declining taxa owing to restricted range (e.g.

Dipodomys elator), deforestation (ANDERSON & JARRÍN, 2002), and urban development in Southwestern United States, especially California, which represents the centre of endemism for the kangaroo–rat genus Dipodomys (PRICE & ENDO, 1989; BOLGER et al., 1997).

Dipodidae Desert and steppe of central Asia and North–western Africa except Sicistinae which occurs in Europe and Northern central Asia. Euchoreutes (subfamily Euchoreutinae) of North–west China and Mongolia is listed as endangered. The only member of the subfamily Cardiocraniinae, Cardiocranius paradoxus (China, Mongolia and Eastern Kazahhstan) is considered vulnerable. IUCN (2002) designates as vulnerable the monotypic Eozapus setchuanus, a species restricted to Central China and apparently poorly collected (SUNG, 1998). However, the species seems to adapt to secondary shrubland and was regularly collected inside its range (GIRAUDOUX et al., 1998).

Muridae Distributed world–wide in all terrestrial habitats.

Subfamily arrangement follow MUSSER & CARLETON (1993) and NOWAK (1999), but there is controversy about the taxonomic status and composition of many of them. CHALINE et al. (1977) argued for a different system, raising the following subfamilies to the family level: Sigmodontidae (called Cricetidae) and including Cricetinae, Spalacinae, Myospalacinae, Lophiomyinae and Platacanthomyinae; Nesomyidae including Otomyinae, Rhizomyidae, Gerbillidae, Arvicolidae, Dendromuridae including Petromyscinae, Cricetomyidae and Muridae including Hydromyinae. Although such an arrangement more properly highlights the affinities between the different taxa, and probably does more justice to the extreme diversity of "Muridae", for the sake of consistency the "classic" treatment proposed in the last compendiums on mammalian taxonomy is followed (WILSON & REEDER, 1993; NOWAK, 1999).

Sigmodontinae (93 genera, 7 threatened) New World.

Three threatened monotypic and little–known genera (Abrawayaomys, Phaenomys, Rhagamys) occur in the Atlantic Forest Region of Eastern Brazil and, possibly, in the Misiones Province of Argentina (for Abrawayaomys, MASSOIA et al., 1991); Kunsia in the Pantanal; Anotomys is only recorded in two regions of Northern Ecuador between 2890–4000 m (VOSS, 1988); and one genus —Nesoryzomys— is endemic of the Galapagos, where another genus, Megaoryzomys, is already extinct (DOWLER et al., 2000). Podomys floridanus,

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a Florida endemics, is threatened by loss of habitat to agriculture and urban development (KIRKLAND, 1998). The recently described Pearsonomys annectans (PATTERSON, 1992) as well as Geoxus, both of the Valdivian Chilean rainforest, may not be common and may warrant inclusion among the genera of concern owing to continued habitat fragmentation in the region (K ELT , 2000). The monotypic Podoxymys roraime is known from only six specimens, all originating from Mount Roraima at the border between Guyana, Venezuela and Brazil (PÉREZ–ZAPATA et al., 1992). Its habitat is safe for the time being (Aguilera, pers. com.).

Since the description of two new species (EMMONS, 1999b), the akodontine genus Juscelinomys appears less threatened even though its cerrado habitat in Brazil and Bolivia is undergoing rapid conversion and thus it deserves conservation attention. Water mice of the genus Rheomys and the Yucatan vesper mouse (Otonyctomys) may be particularly vulnerable to habitat degradation in Central America (REID, 1997).

Calomyscinae (1 genus) Middle and Central Asia.

A unique taxonomic entity formerly placed in Cricetinae (MICHAUX et al., 2001), six species of Calomyscus presently recognised by MUSSER & CARLETON (1993), three of which are classified lower risk/near threatened and one, C. hotsoni of South–western Pakistan, is listed as Endangered (IUCN, 2002).

Cricetinae (7 genera) Palearctic.

The recently re–evaluated monotypic Consumys canus of Gansu and Shaanxi Provinces (China) is only known from three specimens (NOWAK, 1999), and surely deserves inclusion among threatened taxa in need of immediate research.

Spalacinae (2 genera) Eastern Europe, Ukraine, Middle East, Asia Minor, North–eastern Africa.

No threatened genera (although Spalax may qualify for threatened status as only one of the five species, S. zemni, is not included in the Red List, perhaps due to an omission), but most of the recognised species are considered vulnerable owing to competition with human activities such as agriculture. To date, over 40 chromosomal forms have been described among Nannospalax, 30 of which in Turkey alone (SÖZEN et al., 1999). According to NEVO et al. (1995) all these forms should be treated as full species and an updated conservation assessment would thus be needed.

Myospalacinae (1 genus) Eastern Asia.

Possibly only a tribe of Cricetinae (MICHAUX & CATZEFLIS, 2000). Alpha–taxonomy is still unstable. Species of subgenus Eospalax from China

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(NOWAK, 1999); Myospalax fontanieri (including cansus and bailey which are considered distinct species by PANTELEYEV, 1998), M. smithi and M. rothschildi are considered of conservation concern, even if they may be locally common in cultivated fields (GIRAUDOUX et al., 1998).

Lophiomyinae (1 genus) East Africa and possibly Arabia.

A distinctive monotypic genus allied to Cricetinae. Lophiomys imhausi is not considered threatened at present (IUCN, 2002) but KINGDON (1997) considers it rare and perhaps declining.

Known distribution reviewed by KOCK & KÜNZEL (1999). In need of taxonomic revision, as several forms were lumped together by ELLERMAN (1940); some of them may be distinctive and of conservation concern.

Platacanthomyinae (2 genera) India and Indochina.

Formerly included among Gliridae, the two genera are not recognised as threatened, yet they deserve particular attention owing to their relict distribution and phyletic distinctiveness. One of the three recognised species, Typlomys chapensis, is considered Critically Endangered (IUCN, 2002).

Mystromyinae (1genus, threatened) South–eastern Africa.

The monotypic and distinctive Mystromys albicaudatus, formerly placed in the Cricetinae but now considered allied to Petromyscus (JANSA et al., 1999), is threatened by the overgrazing of the veld in South–eastern Africa (DEAN, 1978).

Nesomyinae (9 genera, 2 threatened) Madagascar.

A dubious monophyletic taxon (C ARLETON & MUSSER, 1984; JANSA et al., 1999). One monotypic genus, Hypogeomys antimena from western sandy forests, is considered threatened.

Hypogeomys status is of great concern owing to continued degradation of forests inside its small range in the Kirindy Forest and demographic susceptibility to small population size (G ANZHORN et al., 1996; S OMMER & H OMMEN , 2000; S OMMER et al., 2002). A captive population originating from five individuals collected

by Gerald Durrell in 1990 is managed by the Durrell Wildlife Conservation Trust through an international studbook (COWAN, 2000). The only member of Gymnuromys, G. roberti, although known from a few sites and classified as Vulnerable (IUCN, 2002), now appears more broadly distributed in the humid eastern forests and less threatened than previously believed (GOODMAN & CARLETON, 1998; Goodman pers. com.). Two genera discovered in recent years, Monticolomys and Voalavo , seem restricted to upper montane vegetation in Eastern Madagascar (GOODMAN et al., 1999) but do not appear immediately threatened.

Amori & Gippoliti

Otomyinae (2 genera) Africa.

A distinct taxonomic entity with unclear affinities (CARLETON & MUSSER, 1984), but likely to be included in Murinae (MICHAUX & CATZEFLIS, 2000).

Neither of the two genera threatened, but geographically isolated Otomys occidentalis of Mt. Oku in the Guinea highlands (DIETERLEN & VAN DER STRAETEN, 1992) is listed as Endangered (IUCN, 2002).

Rhizomyinae (3 genera) South–eastern Asia, Eastern Africa.

Alpha taxonomy still unstable. Many taxa of Tachyoryctes with restricted distribution in Eastern Africa are included in the IUCN Red List (IUCN, 2002), sometimes supporting charismatic species such as the Ethiopian wolf Canis simensis in the Bale region of Ethiopia (SILLERO–ZUBIRI et al., 1995).

Gerbillinae (14 genera, 1 threatened) Africa.

The monotypic threatened Ammodillus imbellis is restricted to the arid zone of Somalia and Eastern Ethiopia, while another monotypic potentially threatened genera, Microdillus peeli, occurs in the pre–desertic steppe of North–central Somalia where it is known from only three localities (ROCHE & PETTER, 1968).

Arvicolinae (27 genera) North America, Europe and Asia.

A very speciose clade with no threatened genus, although Chionomys of the Mediterranean region, Dinaromys of the Balkans, Myopus of Northern–eastern Palearctic and Proedromys of Southern China are considered potentially threatened following present IUCN designations (AMORI & GIPPOLITI, 2001). Some other genera have very restricted ranges, such as Prometheomys from the Caucasus, Hyperacrius from Pakistan and Blanfordimys from Afghanistan and Turkmenistan (NOWAK, 1999; PANTELEYEV, 1998).

Dendromurinae (8 genera, 2 threatened) Africa.

Dubiously monophyletic as here recognized (DENYS et al., 1995; MICHAUX & CATZEFLIS, 2000).

Megadendromus nikolausi is a little–known endemic of highlands in Eastern Ethiopia. It occurs in the Bale Mountains National Park (YALDEN et al., 1996). The monotypic Leimacomys buettneri is only known by two specimens collected in 1890 in Central Togo and is feared to be already extinct. SCHLITTER (1989) and MACPHEE & FLEMMING (1999) correctly include this species among extinct taxa adopting the 50–year rule of record absence, but several authorities pointed out that remaining forests of the region had not been properly sampled in recent decades (GRUBB et al., 1998). The two monotypic and very localised species Dendroprionomys rousseloti and Prionomys batesi of Central Africa deserve urgent research.

Animal Biodiversity and Conservation 26.2 (2003)

Petromyscinae (2 genera) Africa.

Two distinctive and monotypic genera (Petromyscus and Delanymys) with restricted range and unclear affinities. S CHLITTER (1989) and KINGDON (1997) consider Delanymys brooksi of the high–altitude marshes of the Albertine Rift threatened by habitat disruption.

Cricetomyinae (3 genera) Africa.

None of the three genera threatened, but Beamys of Eastern Africa is potentially threatened. Cricetomys emini cosensi of Zanzibar Island may warrant specific status and its conservation status deserves investigation (KINGDON, 1997).

Murinae (122 genera, 23 threatened) Most of the threatened murine genera are restricted to islands (AMORI & CLOUT, 2003). They are grouped here according to geographic criteria.

Philippines: Abditomys latidens is highly arboreal monotypic rat known from only two specimens collected in Northern and Southern Luzon (MUSSER & HEANEY, 1992). Anonymomys is known from only three specimens from North–eastern Mindoro Is. (HEANEY et al., 1998). The two species of Archboldomys are only known by the very few specimens collected on Mt. Isarog and Mt. Cetaceo in Luzon (RICKART et al., 1998). Four species of Crateromys are presently recognised, all are threatened by hunting and forest degradation and one, C. paulus of Ilin Is., is possibly already extinct (PRITCHARD, 1989). Monotypic Limnomys sibuanus is only known from seven specimens taken in Mindanao in mountain forest (MUSSER & HEANEY, 1992), even if it is not considered uncommon in high–elevation forest (HEANEY et al., 1998). The monotypic Tryphomys adustus is a little known species from three localities of Luzon (HEANEY et al., 1998).

Palawanomys, the single species P. furvus, is known from four specimens collected in 1962 on Mt. Mantalingajan, Palawan (MUSSER & NEWCOMB, 1983).

Sunda Islands: Nesoromys, monotypic endemic of Seram Is. Not recognised as a distinct genus by MUSSER & CARLETON (1993), apparently only known from the type specimen described by Thomas in 1922 (NOWAK, 1999).

Kadarsanomys, monotypic designated as lower risk/near threatened, but possibly threatened because no specimens has been collected since 1935. Only known from 1000 m high forest in the volcanic massif of Gunang Pangrango–Gede in Western Java (MUSSER, 1982).

Eropeplus, another monotypic genus, is known from only five specimens from mountain forests in Middle Sulawesi (MUSSER, 1970). The genus Tateomys, of which two species are known from very few specimens originating from Sulawesi, is sometimes placed in Melasmothrix (NOVAK, 1999).

Melasmothrix naso is restricted to cold and wet moss forests of Central Sulawesi (MUSSER, 1982).

7

A newly described genus and species, Sommeromys macrorhinos (MUSSER & DURDEN, 2002), from the mountains of Cerntral Sulawesi must be considered of conservation concern.

The monotypic Komodomys is currently known to occur on Rintja and Padar Islands, in the Lesser Sunda, but may possibly also live on other islands, such as Flores where it is known as sub–fossils (M USSER & C ARLETON , 1993). The monotypic Paulamys naso was described from sub–fossil material from Flores Is.: a living rat was trapped on Flores and assigned to this species even though KITCHENER et al. (1991) disputed its distinctiveness from Bunomys. The only extant species of Papagomys, P. armandvillei is presently known only from Flores Is. (MUSSER, 1981).

Nansei Shoto arcipelago: two species of Tokudaia usually recognised (CORBET & HILL, 1992) even though Japanese mammalogists treat them as subspecies (KAWAMICHI, 1997). A third species occurs on Tokun–oshima Is. but has not yet been described (MUSSER & CARLETON, 1993). Habitat degradation put the survival of endemic species on the Nansei Shoto Archipelago in great danger, with T. mueninki of Okinawa considered in a very critical conservation status (ITO et al., 2000).

South–east Asia: the genus Vernaya contain one or possibly two little–known species whose known range includes Northern Burma, Northern Sichuan and Yunnan (CORBETT & HILL, 1992; SUNG, 1998).

West–central Africa: the monotypic Lamottemys okuensis is only known by four specimens collected on Mt. Oku in South–western Cameroon, an area known as an important centre of endemism for rodents (VERHEYEN et al., 1997).

Ethiopian Highlands: Muriculus imberbis represent a monotypic genus endemic to the Ethiopian grassland plateaux, with two well–distinct subspecies, collected only rarely in recent years (YALDEN & LARGEN, 1992). The monotypic Nilopegamys plumbeus is known from only one specimen collected in 1927 near the source of the Little Abbai River in Ethiopia, later synonymised with Colomys but resurrected by KERBIS PETERHANS & PATTERSON (1995).

Australia: the two species of Leporillus were once widespread throughout much of the Southern arid and semi–arid zones of Australia. Leporillus conditor survive today only on the two small Franklin Islands of the Nuyts Archipelago, while L. apicalis is considered extinct. A captive breeding and translocation program to other off–shore islands is underway (LEE, 1995).

New Guinea: the two little–known species of Macruromys occur in the mountain forests of New Guinea where their appearance is both rare and localised (FLANNERY, 1995a). The genus Solomys contains more than five species endemic to the Solomons Archipelago, one of which (Solomys salamonis) is considered extinct by IUCN but extant by MACPHEE & FLEMMING (1999). All species are threatened by introduced predators and logging of forests (FLANNERY, 1995b).

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8

Hydromyinae (10 genera, 5 threatened) Australia, New Guinea.

Threatened genera among water rats include the monotypic Xeromys myoides, only known from a few specimens from scattered localities in Queensland and the Northern Territory of Australia, and Pseudohydromys (2 species), Neohydromys, and the distinctive Mayermys, all from New Guinea, mostly mountain forests. However, the paucity of available data on New Guinea rodents permit a preliminary conservation assessment only. For instance Neohydromys is not considered threatened at all by FLANNERY (1995a).

Both species of the genus Microhydromys (M. richardsoni and M. musseri), known from very few specimens (FLANNERY, 1995a), may warrant threatened status.

Anomaluridae Equatorial Africa, seven species in three genera (DIETERLEN, 1993), but a further genus — Anomalurops— and the existence of more species has been suggested (SCHUNKE & HUTTERER, 2000). No species currently considered threatened by IUCN, perhaps for the vast range of the few recognized species and high densities reported in optimal habitats (J ULLIOT et al., 1998). Monotypic Zenkerella insignis of the Western Equatorial forest block is potentially threatened as it is dependent on conservation of mature forest (KINGDON, 1997). The population recently reported from Bioko Island (VAL et al., 1995) may warrant subspecific status.

Glirulus of Japan, Myomimus (three or four species; OBUCH, 2001) of the Balkans and Middle East and Chaetocauda of Sichuan, for which we provisionally retain genus status (contra HOLDEN, 1993). Potentially threatened monotypic genera are Eliomys, Muscardinus and Glis, all with a wide but increasingly fragmented distribution in the Western Palearctic. Decline seems associated to intensive management of woodland and/ or to a reduction of hedgerows in agro–sylvo– pastoral landscapes (i.e. CAPIZZI et al., 2002).

Bathyergidae African fossorial family, 14 species recognised by NOWAK (1999), but number of valid species at least among Cryptomys in Zambia, is much larger (BURDA et al., 1999). Four species are included in the lower risk category. Heliophobius of East Africa is potentially threatened. The genus Bathyergus has a very limited range in coastal South–west Africa and is considered vulnerable by KINGDON (1997).

Hystricidae No threatened or potentially threatened genus for this Old World family. Only Hystrix brachyura is listed as Vulnerable (IUCN, 2002). No data are available about the current status of the Palawan endemic H. pumila (cf. HEANEY et al., 1998). Some species are of great economical importance as food source (i.e. Atherurus in Africa cf. JORI et al., 1998).

Petromuridae

Pedetidae Found in the arid areas of Southern and Eastern Africa. Pedetes is considered threatened (listed as vulnerable) because of eradication programs in agriculture areas and habitat loss due to overgrazing, although it may be locally abundant reaching a density of 10 springhares per hectare (BUTYNSKI, 1984). Cytogenetic and molecular data support the elevation of the eastern subspecies surdaster to full species status, thus supporting earlier taxonomic arrangements of this peculiar rodent genus (MATTHEE & ROBINSON, 1997).

Ctenodactylidae Rocky areas in arid regions of Sahara and Northern Afrotropical Region. The monotypic genus Felovia of Mali, Mauritania and Senegal is considered threatened by deforestation and desertification (SCHLITTER, 1989) but detailed data are lacking.

Gliridae Palearctic and African forests and dry–lands (HOLDEN, 1996; NOWAK, 1999). Threatened genera are Selevinia, endemic to Kazakhstan and sometimes considered to form its own family,

Monotypic, rocky outcrops of South–west Africa, not threatened at the moment but the status of Petromus typicus in Namibia need to be properly assessed (cf. GRIFFIN, 1998).

Thryonomyidae Cane rats are an important food source in SubSahara Africa (AMORI & GIPPOLITI, 2002; JORI et al., 1995).

Erethizontidae North and South American forests, still unstable alpha taxonomy (BONVICINO et al., 2002; EMMONS & F EER, 1997; NOWAK, 1999; V OSS & DA SILVA, 2001). No threatened or potentially threatened genus. Information is needed on the status of the Andean monotypic endemic Echinoprocta rufescens. Only Sphiggurus vestitus of Colombia and Venezuela is considered vulnerable. A number of restricted–range and disputed taxa may warrant urgent research, such as Coendou quichua of Ecuador Andes, Sphiggurus sneiderni of the Colombian western slopes of the Andes and the S. villosus complex of Brazilian Atlantic forest (EMMONS & FEER, 1997).

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Animal Biodiversity and Conservation 26.2 (2003)

Chinchillidae South America. Genus Chinchilla (two species) is threatened, although a domestic form is widespread in breeding farms around the world. Conservation status of these two species is very confusing, with the Vulnerable C. lanigera now considered more at risk than the Critically Endangered C. brevicaudata (COFRÉ & MARQUET, 1999) which was recently rediscovered in Northern Chile.

Dinomyidae Monotypic family found in isolated localities of the eastern foothills of the Andes from Colombia and Venezuela to Bolivia and the Amazon lowlands of W Brazil and Peru (EMMONS & FEER, 1997).

Dynomys branickii is hunted for food and considered endangered but it occurs at least in one protected areas, the Manu National Park, Perù (VOSS & EMMONS, 1996). A successful breeding program is presently being carried out at Calì Zoo (WHITE & ALBERICO, 1992).

Cavidae South America. Dolichotis (two species), found in scrub and grassland areas from Southern Bolivia to Southern Argentina, is considered potentially threatened, as it is hunted and competes with introduced Lepus europaeus (OJEDA & MARES, 1981). Dolichotis patagonum is commonly bred in zoos around the world.

Hydrochaeridae Panama, Northern and Central South America, not threatened. Capybara is harvested for meat and skin and can provide economic benefits to landowners while allowing habitat conservation in the seasonally flooded llanos (OJASTI, 1991).

Taxonomic and conservation status of the Capybaras West of the Andes, described as Hydrochaeris isthmius (MONES & OJASTI, 1986), should be assessed.

Dasyproctidae Central and South American forests. Although locally agoutis are extirpated by excessive hunting or owing to excessive habitat fragmentation (i.e. CHIARELLO, 1999) and some taxa may warrant conservation status, no genus appears threatened at this time. The whole genus is in need of taxonomic revision (VOSS & EMMONS, 1996).

Agoutidae Central and Southern America. Stictomys taczanowskii of the Andean region is listed as lower risk —near threatened by the IUCN (2002).

The other monotypic genus, Agouti paca, is the

most prized mammal of the Neotropics for its meat (EMMONS & FEER, 1997) and, although locally extirpated, is not yet considered globally threatened.

Ctenomyidae Extreme southern part of the Neotropical Region. One genus exhibiting high karyotypic diversity; 48 species recognised by NOWAK (1999), more than 60 according to GIMÉNEZ et al. (1999). Only Ctenomys magellanicus is considered threatened (IUCN, 2002).

Octodontidae Southern South America steppe. The monotypic Tympanoctomys barrerae is endemic of salt pansand dune habitats of Mendoza and La Pampa provinces of Argentina (OJEDA et al., 1999) and is considered vulnerable by IUCN (2002). The arid region of Northwest Argentina was found to contain two others recently discovered monotypic genera; Pipanacoctomys and Salinoctomys (MARES et al., 2000) whose conservation status has not yet been assessed.

Abrocomidae South-western Neotropics, 7 species (BRAUN & MARES, 2001). The status of the recently discovered Cuscomys ashaninka (EMMONS, 1999a) from the Northern Vilcabamba Mountains of Cusco, Peru, is undetermined at the moment as is the other species of the genus, C. oblativa, known only from remains in Inca tombs, still extant according to EMMONS (1999a).

Echimyidae New–world arboreal spiny–rats, taxonomy very unstable (NOWAK, 1999). The monotypic Chaetomys (formerly in Erethizontidae), endemic to the Atlantic Forest of South–east Brazil, is considered threatened although it has a more extensive range than once believed (OLIVER & SANTOS, 1991). Potentially threatened genera are Carterodon, Olallamys (2 species) and Isothrix (3 species; VIÉ et al., 1996). EMMONS & VUCETICH (1998) establish the new genus Callistomys for the little–known Echimys (Nelomys) pictus of Bahia, which is known from a very few individuals. The monotypic Kannabateomys amblonyx of South–eastern Brazil, Paraguay and Misiones (Argentina) is restricted to dense thickets especially near watersides and may deserve conservation attention (OLMOS et al., 1993). The arboreal spiny rat of the Atlantic region of Eastern Brazil is sometimes separated from Echimys and placed in its own genus Nelomys. Alpha taxonomy of this group is still unclear, and many taxa are considered threatened owing to small range size, deforestation and hunting pressure (cf. OLMOS, 1997). The terrestrial

Amori & Gippoliti

10

spiny rats are now known to be represented by two genera, the more wide–pread Proechimys and Trynomys (LARA & PATTON, 2000), essentially delimited to the Atlantic Forest domain and of conservation concern as not a single specimen was found even during a long–term study in the Rio Doce State Forestry Park (STALLINGS, 1989).

Proechimys is an important food source in regions were large game species have been extirpated (SUÁREZ et al., 1995).

Capromyidae Endemic to the West Indies, more than 30 recognised species in eight genera, at least 19 species and two genera extinct, probably following human settlement there (A LCOVER et al., 1998; CAMACHO et al., 1995; WOODS, 1989). Threatened genera are: Geocapromys (two species) from Jamaica and Bahamas, Mesocapromys (four species) from Cuba and the monotypic Plagiodontia from Hispaniola. The genus Mysateles of Cuba is potentially threatened. In Cuba, the four species of Mesocapromys are restricted to small islands or tiny ranges and two of them (M. nanus and M. sanfelipensis ) are possibly already extinct.

Isolobodon is here considered a threatened genus following IUCN (2002) classification of Isolobodon portoricensis of Hispaniola as CR although evidence of its survival is very weak (NOWAK, 1999).

Myocastoridae Freshwater habitats in Southern South America, monospecific, not considered threatened but declining owing to hunting for their pelt, at least in Argentina (OJEDA & MARES, 1981), introduced in many parts of Europe and North America and successfully eradicated in Great Britain (GOSLING & BAKER, 1989).

Discussion It should be emphasised that biological conservation depends upon and is closely tied to knowledge on the phylogenetic relationships and taxonomy of biological groups. Thus, what we identified as present priorities for rodent conservation should be regularly updated as systematic research refines our understanding of systematic affinities and diversity among rodents (AMORI & GIPPOLITI, 2003). For instance, extinction of two rodent species (Rattus macleari and R. nativitatis) on Christmas Island in the Indian Ocean at the beginning of the century, may be a negligible loss according to the most prevalent taxonomy, a major loss if the distinctiveness of the two species (M USSER & CARLETON, 1993) is taken into account and systematically formalised. Furthermore, the result of ecological research may show a brighter status for some endemic taxa which suffer less than thought from habitat disturbance (GIRAUDOUX et al., 1998).

Table 1. Number of living genera (Ng), species (N spp.) and threatened species (NT spp.; IUCN, 2002) of rodents by Family.

Tabla 1. Número de géneros vivos (Ng), de especies (N spp.) y de especies en peligro de extinción (NT spp.; IUCN, 2002) de roedores, agrupados por familias.

Family Aplodontidae Sciuridae Castoridae Geomyidae Heteromyidae Dipodidae Muridae Anomaluridae Pedetidae Ctenodactylidae Gliridae Bathyergidae Hystricidae Petromuridae Thrynomyidae Erethizontidae Chinchillidae Dinomyidae Cavidae Hydrochaeridae Dasyproctidae Agoutidae Ctenomyidae Octodontidae Abrocomidae Echimyidae Capromyidae Myocastoridae

Ng 1 51 1 6 6 17 300+ 3 1 4 10 5 3 1 1 4 3 1 5 1 2 2 1 6 2 16+ 6 1

N. spp. NT spp.

1 273 36 2 40 5 60+ 51 8 1,336+ 235 7 2 2 5 1 29 9 14+ 11 1 1 2 17 1 3 2 1 1 14 2 13 3 2 60+ 1 11 2 7 66+ 6 11 10 1

Of the 28 rodent families currently recognised, only two, Pedetidae and Dinomydae, are considered threatened at the present time (table 1).

Higher rates of endangerment at the generic level are found in the subfamily Euchoreutinae, Mystromyinae, Chaetomyinae, Plagiodontinae and Isolobodontinae —the latter possibly already extinct— all with 100 % of genera threatened, Hydromyinae and Capromyidae (50 %), Cardiocraniinae, Glirinae and Chinchillidae (33 %). According to the present study, 126 of the circa 451 living rodent genera (27,9 %), representing

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Animal Biodiversity and Conservation 26.2 (2003)

Table 2. A summary of rodent diversity and conservation status with a list of threatened, potentially threatened and of concern genera by Family and Subfamily. (In brackets, number of living species for each genus other than one.)

Tabla 2. Resumen de la diversidad de roedores y de su estado de conservación con una lista de géneros en peligro de extición, en peligro de extinción potencial y de interés, clasificados por familias y subfamilias. (Entre paréntesis, el número de especies existentes de cada género diferente del indicado.)

Family Subfamily Sciuridae Sciurinae Petauristinae

Geomyidae Dipodidae Cardiocraniinae Euchoreutinae Zapodinae Muridae Sigmodontinae

Cricetinae Spalacinae Lophiomyinae Mystromyinae Nesomyinae Gerbillinae Arvicolinae

Dendromurinae Petromyscinae Cricetomyinae Murinae

Threatened

Myosciurus Hyosciurus (2) Biswamoyopterus Eupetaurus Trogopterus

Potentially threatened

Of concern

Epixerus (2) Syntheosciurus Aeretes Belomys Euglacomys Pteromyscus

Allosciurus Gliphotes Petaurillus (2)

Chibchanomys Hodomys Lenoxus Podoxymys

Rheomys (4) Otonyctomys

Zygogeomys Cardiocranius Euchoreutes Eozaphus Abrawayaomys Anotomys Nesoryzomys (2) Podomys Rhagamys Kunsia (2) Phaenomys Cansumys

Spalax Lophiomys Mystromys Hypogeomys Gymnuromys Ammodillus

Brachyuromys

Leimacomys Megadendromus

Microdillus Chionomys (3) Dinaromys Myopus Proedromys Dendroprionomys Prionomys

Abditomys Anonymomys Archboldomys Crateromys (4) Tryphomys Limnomys Palawanomys

Beamys Kadarsanomys Stenocephalemys (2) Carpomys (2) Celaenomys Hapalomys (2) Srilankamys Xenuromys

Blanfordimys Hyperacrius Prometheomys

Delanymys Sommeromys

Amori & Gippoliti

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Tabla 2. (Cont.)

Family Subfamily

Hydromyinae

Anomaluridae Zenkerellinae Pedetidae Ctenodactylidae Gliridae Glirinae Leithiinae

Bathyergidae Erethizontidae Chinchillidae Dinomyidae Cavidae Dolichotinae Agoutidae Octodontidae Abrocomidae Echimyidae Chaetomyinae Dactylomyinae Echimyinae

Threatened Potentially–threatened Eropeplus Xenomys Tateomys (2) Diomys Melasmothrix Diplothrix Komodomys Leggadina (2) Papagomys Mesembriomys (2) Paulamys Rhabdomys Tokudaia Nesoromys Lamottemys Vernaya Muriculus Nilopegamys Leporillus Macruromys (2) Solomys (3) Xeromys Pseudohydromys (2) Neohydromys Mayermys

Isolobodontinae Plagiodontinae

Microhydromys (2)

Zenkerella Pedetes (2) Felovia Glirulus Myomimus (3) Selevinia Chaetocauda

Glis Muscardinus Eliomys (2)

Heliophobius

Bathyergus Echinoprocta

Chinchilla (2) Dinomys Dolichotis (2) Stictomys Tympanoctomys

Agouti Cuscomys

Chaetomys Olallamys (2) Isothrix (3) Carterodon

Eumysopinae Capromyidae Capromyinae

Of concern

Geocapromys (2) Mesocapromys (4) Isolobodon Plagiodontia

Mysateles (5)

Kannabateomys Nelomys Callistomys

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80 70

Percentages

60 50 40 30 20 10 0

R odent genera Rodent Monotypic genera

Threatened rodent genera Polytypic genera

Fig. 1. Percentage of monotypic and polyitypic genera in the Order Rodentia and in threatened or potentially threatened genera.

Fig. 1. Porcentaje de géneros monotípicos y politípicos del orden Rodentia y de los géneros en peligro o en peligro de extinción potencial.

168 species, deserve conservation attention (table 2). This is considerably more than the percentage of threat calculated at the species level (16 %) and seems to confirm previous findings on the possible loss of a disproportionate amount of phylogenetic diversity among mammals during the current extinction spasm (PURVIS et al., 2000).

There are some indications that there is a high probability that monotypic or species poor lineages are at risk (PURVIS et al., 2000). Of the 106 threatened and potentially threatened genera (thus considering only IUCN 2002 official data), only 25 (23,6 %) are not presently monotypic, while among the whole order Rodentia, polytipic genera represent 63 % circa of living genera (fig. 1). If we consider that even polytypic genera at risk are often represented by only two species, belong to non–speciose clade, and that genetic divergence among currently recognised genera in small mammals is higher than among genera of larger mammals (CASTRESANA, 2001), we may well suppose that there is a risk to lose a considerable amount of genetic diversity among rodents. However, it is unknown to what degree our results are influenced by the high level of threat observed among poor–species lineages restricted to islands.

Conservation of small mammal diversity is low in the environmental agenda (AMORI & GIPPOLITI, 2000; ENTWISTLE & DUNSTONE, 2000) despite increasing evidence of their role in supporting ecosystems and more "attractive" species. To change the popular view that “a rat is a rat” (CEBALLOS & BROWN, 1994) there is the need for refinement of rodent (and especially muroids) systematics

and an increase in educational activities focusing on small mammal diversity and ecological roles.

Conversely, strategies should be established and financial resources allocated for urgent conservation measures for the most threatened and unique rodent taxa at a global level. This study represents a step forward in the identification of a limited, affordable number of taxa to maintain diversity of the order.

Acknowledgements E. Capanna, T. M. Flannery, S. Goodman, B. Patterson, E. Van der Straeten, R. Wirth, D. Yalden, and J. Zima provided valuable advice in the preparation of this work. Thanks are due to all rodents experts who, with their sometimes obscure work in the field and in museums world–wide, made this review possible.

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Linking processes: effects of migratory routes on the distribution of abundance of wintering passerines A. Galarza & J. L. Tellería

Galarza, A. & Tellería, J. L., 2003. Linking processes: effects of migratory routes on the distribution of abundance of wintering passerines. Animal Biodiversity and Conservation, 26.2: 19–27.

Abstract Linking processes: effects of migratory routes on the distribution of abundance of wintering passerines.— Movements of migratory birds across the western Paleartic concentrate populations along Atlantic and Mediterranean coasts, thus producing flows of migrants that converge at both extremes of the Pyrenees. Here we analyse the effect of these corridors on the winter distribution of some passerines (F. Motacillidae, F. Turdidae and F. Fringillidae). The number of ring recoveries of migrants at the edges of the Pyrenees was higher than expected, a pattern that was also observed in the case of winter recoveries. In addition, there was a significant decrease in the abundance and species richness of the bird assemblages of the three families analysed wintering in the coastal farmlands of northern Iberian peninsula as their location was further away from the western corridor of the Pyrenees. These results suggest the existence of links between the routes of migratory passerines and their winter densities in northern Iberia.

Key words: Iberian peninsula, Migratory routes, Passerines, Wintering grounds.

Resumen Relacionando procesos: efectos de las vías migratorias sobre la distribución de la abundancia de pájaros invernantes.— Los movimientos de las aves migratorias en el Paleártico occidental producen concentraciones en las costas atlánticas y mediterráneas que convergen en ambos extremos de los Pirineos. En este estudio se analiza la relación entre esas vías de paso y la distribución invernal de ciertos pájaros (F. Motacillidae, F. Turdidae y F. Fringillidae). El número de recuperaciones de anillas de aves migratorias a ambos lados de los Pirineos fue mayor del esperado, una tendencia también observada en las recuperaciones invernales. Además, se observó una menor abundancia y diversidad de especies de las tres familias de aves analizadas en las campiñas costeras del norte de la península ibérica conforme aumentaba la distancia entre dichos lugares y el corredor occidental de los Pirineos. Estos resultados sugieren la existencia de una relación entre dichas vías de entrada y las densidades de pájaros invernantes en el norte de la península ibérica.

Palabras clave: Península ibérica, Rutas migratorias, Pájaros, Áreas de invernada.

(Received: 17 I 03; Conditional acceptance: 30 IV 03; Final acceptance: 23 VII 03) Aitor Galarza, Servicio de Conservación y Espacios Naturales Protegidos, Dept. de Agricultura, Diputación Foral de Bizkaia, E–48014 Bilbao, España (Spain). E–mail: agalarza@telefonica.net José Luis Tellería, Dept. de Biología Animal I (Zoología de Vertebrados), Fac. de Biología, Univ. Complutense, E–28040 Madrid, España (Spain). E–mail: telleria @bio.ucm.es

ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

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Galarza & Tellería

lntroduction Ecological barriers may produce variations in the direction of migratory birds, producing local concentrations of migrants along coastlands and mountain passes (ALERSTAM, 1990; BERTHOLD, 1993). Movements of migratory populations across the Western Paleartic may cause, for instance, concentrations of birds along Atlantic and Mediterranean coasts of South–western Europe that produce flows of migrants converging in both extremes of the Pyrenees (BERNIS, 1966–1971; FERRER et al., 1986; FORTIN et al., 1999; fig. 1). Several studies have shown the importance of these two corridors for the movements of large species and soaring birds (e.g. cranes, pigeons, raptors; FERNÁNDEZ CRUZ., 1981; PURROY, 1988; DE JUANA et al., 1988; MADROÑO et al., 1992).

However, there is a lack of comprehensive studies on their effect on the distribution of passerines (O. Passeriformes) passing through the north of the Iberian peninsula.

In addition to the effect of these corridors on the distribution of migrants, they could also play a role in the distribution of abundance of migratory passerines in wintering areas. This has been poorly studied to date, perhaps because it is commonly accepted that, at the end of the migratory period, other factors, such as weather or

food availability, are the main determinants of bird abundance (WIENS, 1989a for review). However, migratory passages might strongly affect the wintering distribution of birds in regions which receive huge numbers of migratory birds , such as the Iberian peninsula (TELLERÍA et al., 1988). Thus, it could be hypothesised that areas further from the main migratory routes will support fewer wintering individuals and species than those located closer to them.

This paper explores the relationship between the winter distribution of passerines in northern Iberia and the migratory corridors at the two edges of the Pyrenees (fig. 1). For this purpose, the distribution of birds belonging to the three most abundant families wintering in open habitats of northern Spain was studied (Motacillidae, Turdidae and Fringillidae) following two complementary approaches. First, the potential influence of corridors on the abundance of migratory passerines was evaluated by using ring recoveries.

Second, whether these migratory routes determine the winter distribution of bird abundance in northern Iberia was analysed. This latter point was assessed by means of two complementary analyses: i. The distribution of ring recoveries was studied during the winter; ii. Whether bird abundance and richness of the bird assemblages of the three

A

B Atlantic corridor

Mediterranean corridor Pyrenees

C

I

II III IV V VI VII VIII

IX

Fig. 1. A. Topographical features of the Iberian peninsula (areas of 500 m a.s.l. in grey and those of 1000 m a.s.l. in black) and location of the studied corridors. B. Distribution of the main mountain ranges in the Western Paleartic. C. Sectors delimited in this study.

Fig. 1. A. Rasgos topográficos de la península ibérica (en gris las áreas por encima de los 500 m s.n.m. y en negro las ubicadas por encima de los 1000 m s.n.m.). B. Distribución de las montañas más importantes en el Paleártico occidental. C. Sectores delimitados en este estudio.

21

Animal Biodiversity and Conservation 26.2 (2003)

studied families wintering in coastal farmlands of northern Iberia decrease from the Atlantic corridor westwards was evaluated.

Methods Ring–recovery data Ring–recoveries were used to evaluate the abundance of migratory birds. Trapped birds appear to be a proper index of migratory intensity (ZEHNDER & KARLSSON, 2001) even after accounting for the effects of biases related to variation in reporting rates (BAIRLEIN, 2001). Recoveries of birds ringed outside the Iberian peninsula and belonging to the three studied families were reviewed (BERNIS, 1966–1971; SANTOS, 1982; ASENSIO, 1983, 1985a, 1985b, 1985c, 1986, 1987; BUENO, 1990, 1991, 1992a, 1992b, 1998; PÉREZ–TRIS & ASENSIO, 1997a, 1997b; appendix 1). In order to analyse their distribution in northern Iberia, nine sectors were delimited following BERNIS (1966–1971; fig. 1). Recoveries were considered as belonging to either wintering or migratory birds according to the criterion used by each author consulted.

Postnuptial and prenuptial recoveries were not distinguished, as they were not differentiated in some of the studies reviewed in this paper. However, prenuptial recoveries represent only 13.4 % of those of small Turdidae during the migratory period in the Iberian peninsula (BUENO, 1990, 1991, 1992a, 1992b, 1998), 10.5 % of wagtails (G. Motacilla; PÉREZ–TRIS & ASENSIO, 1997a, 1997b) and 5,1 % of thrushes (G. Turdus; TELLERÍA & SANTOS, 1982).

Bird abundance during winter In order to explore the effect of the distance to the Atlantic corridor on the distribution of wintering birds, the abundance of the species considered in this study was quantified in the five sectors delimited along the Atlantic coastal belt (sectors I–V; fig. 1). Birds were counted by line– transects without census belt over units of 500 m long (appendix 2). Censuses were conducted during the last week in December 1997 and the first two weeks of January 1998. To prevent the effect of factors other than distance to the Atlantic corridor on the abundance of wintering birds, the potential effect of habitat structure and climate was controlled. To do this, all censuses were carried out in similar Atlantic farmlands dominated by meadows, scattered hedges and small woods. All these farmlands were located within 15 km from the shoreline and below 250 m a. s. l. to avoid the effects of weather (more extreme in inland areas and higher altitudes) on bird abundance. These coastal farmlands are in fact considered, the main wintering habitat of passerines in the north of the Iberian peninsula (TELLERÍA & GALARZA, 1990).

Data analysis Chi–square tests were used to analyse whether the observed distribution of recoveries in the corridors (sectors V, VI and IX) was higher than expected according to an even distribution of recoveries along the study region (all sectors). To do so, the expected number of recoveries in sectors with and without corridors was calculated by multiplying their area for the mean density of recoveries observed in the whole study area.

Spearman rank correlations were used to test for relationships between abundance and richness along the study sectors. Differences in the structure of wintering bird assemblages (abundance and species richness) along the Atlantic coast were tested by ANOVAs. Planned comparisons were used to test the hypothesis that the western sectors had lower densities and richness of wintering birds than the eastern sectors closer to the Atlantic corridor (contrast vectors: -2, -1, 0, 1 and 2 for sectors I, II, II, IV and V respectively). In these analyses, abundance and richness were log-transformed.

Results Distribution of migratory birds There was a significant difference in the distribution of the ring recoveries of migrants along northern Spain (fig. 2). As predicted, recoveries in both corridors of the Pyrenees (sector V, VI and IX) were higher than expected for the three studied families (Motacillidae: χ 2 = 54.65; Turdidae: χ 2 = 150.82, Fringillidae: χ 2 = 442.31; df = 1, P < 0.001). Furthermore, the number of recoveries in the Atlantic corridor were higher than the number recorded in the Mediterranean corridor (Motacillidae: χ 2 = 26.96; Turdidae: χ 2 = 84.72, Fringillidae: χ 2 = 31.20; df = 1, P < 0.001). Patterns in the richness of species moving across northern Iberia were related to the total number of recoveries (Motacillidae, rs = 0.94, P < 0.001; Turdidae, rs = 0.93, P < 0.001; Fringillidae, rs = 0.74, P = 0.022; fig. 2).

Distribution of wintering birds Recoveries of ringed birds The distribution of the total number of winter recoveries followed a pattern similat to that observed during the migratory period (rs = 0.75, P = 0.019, n = 9), and the corridors (sectors V, VI and IX) had many more records than expected for each family (Motacillidae: χ 2 = 52.80, Turdidae: χ 2 = 73.70, Fringillidae: χ 2 = 94.79; df = 1, P < 0.001). In winter, the number of recorded species showed a similar pattern to the total number of recoveries (Motacillidae: rs = 0.76, P = 0.018; Turdidae: rs = 0.83, P = 0.005; Fringillidae: rs = 0.85, P = 0.004; n = 9 in all cases; fig. 2).

22

Galarza & Tellería

Migratory period 16

Motacillidae Turdidae Fringillidae

200

12

160

10

120 80 40 0 I

II

III

IV

V

VI

160 120 80 40 I

II

III

IV V Sectors

6 4 2 I

Wintering period 10

Motacillidae Turdidae Fringillidae

200

8

0

VII VIII IX

Number of species

Number of recoveries

240

0

Motacillidae Turdidae Fringillidae

14

Number of species

Number of recoveries

240

VI

VII VIII IX

8

II

III

IV

V

VI

VII VIII IX

V

VI

VII VIII IX

Motacillidae Turdidae Fringillidae

6 4 2 0 I

II

III

IV

Sectors

Fig. 2. Number of ring recoveries and number of species recovered in the study sectors (see fig. 1) according to migratory and wintering periods.

Fig. 2. Número de recuperaciones y de especies recuperadas en los sectores estudiados (ver fig. 1) según periodos de migración o invernada.

Bird abundance and richness Despite strong inter–specific differences in the distribution of abundance (appendix 2), there was a significant decrease in abundance and species richness in the wintering bird assemblages of the three studied families as the location of farmlands was further away from the Atlantic corridor (fig. 3). Abundance and richness of farmland bird assemblages in these sectors suggested trends similar to those observed with ring recoveries (rs = 0.80, P = 0.109, n = 5) and species (rs = 0.95, P = 0.058, n = 5).

Discussion Effects of migratory routes on the distribution of passerines Results of this study corroborate the significant role of the Atlantic and Mediterranean extremes

of the Pyrenees as corridors for migratory passerines of the three studied families and illustrate how the Pyrennees act as a barrier for these small birds, despite their ability to cross mountain ranges (e.g. HILGERLOGH et al., 1992; BRUDERER, 1996) or wide tracts of sea (B ERNIS , 1963, HILGERLOGH et al., 1992). They also suggest that, given the observed differences in the number of recoveries, the Atlantic corridor is used by a larger number of migrants than the Mediterranean.

This pattern is possibly related to the size of the area from where migrants move to the Iberian peninsula. During the autumn migration, birds crossing the Atlantic corridor come from an area which extends from Northern Germany, the Netherlands, North–western France and the British Islands to Scandinavian and Baltic countries (fig. 1). This area is larger than the breeding quarters of the passerines crossing through the Mediterranean corridor, which come mainly from Switzerland, Southern Germany and Eastern

23

Animal Biodiversity and Conservation 26.2 (2003)

A

F 1,75 = 21,93 P < 0.001

303

60 40 105

20 0

22

I

103

3

II

III Sector

IV

8 Species / Km

Birds / Km

80

B 10

V

F 1,75 = 9,57 P < 0.01

15

12

6 8

4

3

2 0

15

I

II

III Sector

IV

V

Fig. 3. Mean number (± s.e.) of individuals (A) and species (B) counted per transect in the five sectors delimited in the Atlantic coast of the Iberian peninsula (fig. 1; black bars) and their relationships with the results obtained by using ring recoveries (white bars with the corresponding number of recoveries and species). Results of ANOVA planned comparisons testing for differences in abundance and richness of wintering birds between western sectors are also shown (see text for details).

Fig. 3. Número medio (± e.e.) de individuos (A) y especies (B) registrados por transecto en los cinco sectores de las costas atlánticas ibéricas (fig. 1; barras negras) y su relación con los resultados obtenidos de las recuperaciones de aves anilladas (barras blancas, con sus correspondientes valores). Se dan también los resultados de sendas ANOVA planificadas para ver las diferencias entre los valores obtenidos en los transectos de los diferentes sectores (ver texto).

France (BERNIS, 1966–71; SANTOS, 1982; ASENSIO, 1983, 1985a, 1985b, 1985c; 1986, 1987; BUENO, 1990, 1991, 1992a, 1992b).

Our results also show that the distribution of migrants in northern Iberia is a good predictor of their winter distribution, as suggested by the effect of the two corridors on the winter distribution of migrants (fig. 2). However, we agree, that the role of these corridors on the distribution of wintering individuals is likely blurred further south due to the increasing dispersion of individuals in the open valleys and plateaux of the Iberian peninsula and their active search for the best sectors to cope with winter restrictions related to climate, food availability, etc. Mountains and plateaux therefore seem to be avoided by many wintering passerines that will converge in the mildest sectors of the Iberian peninsula (Mediterranean and Atlantic coasts, and South–western Iberia) (TELLERÍA et al., 1988, 1999).

The westwards decreasing abundance of wintering birds along the belt between the Atlantic coastline and the mountains on northern Iberian peninsula could be interpreted as additional evidence of the role of corridors on the organisation of wintering bird assemblages (fig. 3). This interpretation was also supported by the similar pattern obtained from ring recoveries and censuses in the northern sectors. There are several hypotheses that could explain this effect. First of all, increasing winter densities in the eastern farm-

lands could be a mere "sampling effect" of migrants crossing the corridor from one side to another in relation to the almost permanent movement of many migratory birds throughout the winter in response to weather stress or food availability. Secondly, the use of Atlantic farmlands by wintering birds could be affected by a seasonal peninsula effect (BROWN & LOMOLINO 1998). In this case, western sectors are less likely to be occupied by wintering birds arriving at the Iberian peninsula through the Atlantic corridor than eastern sectors. Lastly, evolutionary adjustments, related to the advantages of wintering near the breeding grounds (e.g. early occupancy of the best breeding territories), could penalise the use of the western, farthest sectors (ALERSTAM & HEDENSTRÖM 1998 for review). However, there is an alternative hypothesis to the effect of the Atlantic corridor on the abundance distribution of wintering birds in Northern Spain: the bulk of European migratory populations are connected (see WEBSTER et al., 2002 for a review of this concept) to extensive wintering grounds in Southern Mediterranean areas of the Iberian peninsula and Morocco, and this connection could decrease the use of the North–western corner of Spain as wintering grounds. The geographical situation of North–western Spain, marginal to the main flux of the migratory population arriving at the Iberian peninsula (BERNIS, 1966–1971; TELLERÍA et al., 1999), could also affect the observed distribution

24

of ring recoveries during the migratory period.

Obviously, all these hypotheses need to be tested by more specific approaches.

Implications for the conservation of wintering birds It is commonly argued that studies carried out on different spatial and temporal scales are needed for a more complete understanding of which factors affect the numerical evolution of migratory bird populations (TERBORGH, 1989; BAILLIE & PEACH, 1992; SHERRY & HOLMES, 1996; ESLER, 2000).

Habitat quality is usually considered the main determinant of the abundance of migratory birds and, it is consequently accepted that their population levels will be strongly determined by changes in the availability and suitability of habitats in breeding and wintering grounds (DOLMAN & SUTHERLAND, 1994; SUTHERLAND & DOLMAN, 1994).

Local changes in habitat suitability due to depletion of key resources or landscape modifications will thus be related to concomitant changes in the regional size of bird populations. As a result, functional relationships between the local management of habitats and the regional evolution of populations are, as in other animal groups, at the basis of current strategies of bird conservation (VERNER et al., 1986; MORRISON et al., 1998).

An increasing body of theory and empirical evidence however, suggests that bird abundance and distribution are also affected by scale dependent, hierarchical processes that can affect their patterns of abundance (WIENS, 1989b).

Our results support this view since they suggest an effect of large scale, geographical processes related to migratory corridors on the regional abundance of migratory and wintering passerines. Further investigations are required to show the potential of this relationship between corridors and densities of migratory passerines in the design of proper management strategies directed to the conservation of these animals. Habitats in areas under the effect of flows of migrants must be of particular conservation concern as they contribute to maintaining the bulk of migratory populations during the passage and, in regions suitable for wintering (as the Iberian peninsula is), present the highest densities of many migratory species. This will probably affect any integrated approach to the management of migratory populations from a meta–population perspective (E SLER, 2000) given the reduced probability of occupation by migrants of habitat patches located at increasing distance of corridors.

Acknowledgements We thank Dr. Javier Pérez–Tris and Dr. Luis María Carrascal for constructive criticisms. This paper is a contribution to the project BOSS2000–0556 (Ministerio de Ciencia y Tecnología of Spain).

Galarza & Tellería

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Galarza & Tellería

Appendix 1. Number of recoveries of birds ringed outside the Iberian peninsula according to sectors and periods (migration vs. wintering).

Apéndice 1. Numero de recuperaciones de aves anilladas fuera de la península ibérica según sectores y períodos de captura (migración vs. invernada).

Sector I Km2

7900

II

III

IV

9800

10500

5300

V

VI

VII

VIII

IX

7200 10400 15600 12000 13600

Motacillidae

Motacilla alba Motacilla flava Motacilla cinerea Anthus pratensis Anthus trivialis

Migr.

1

0

4

1

17

5

0

1

5

Win.

5

1

2

0

4

2

0

0

2

Migr.

1

0

1

5

21

4

1

1

1

Migr.

2

0

1

3

10

0

2

0

4

Win.

1

0

1

2

6

0

1

0

1

Migr.

0

0

4

6

33

3

0

0

4

Win.

0

0

1

5

9

1

0

0

2

Migr.

0

0

0

0

5

1

0

1

0

Migr.

0

1

12

4

36

52

7

6

18

Win.

3

1

7

8

18

9

3

7

36

Migr.

0

0

0

0

2

1

1

0

0

Win.

0

0

0

0

0

0

0

0

1

Migr.

0

0

1

0

1

0

0

0

0

Turdidae

Erithacus rubecula Luscinia svecica Luscinia megarhy.

Phoenicurus phoenic.

Phoenicurus ochruros Oenanthe oenanthe Saxicola rubetra Saxicola torquata Turdus philomelos Turdus iliacus Turdus merula Turdus viscivorus Turdus pilaris Turdus torquatus

Migr.

0

0

0

0

12

37

10

12

3

Win.

0

0

0

1

1

1

0

0

1

Migr.

0

1

1

0

5

2

0

1

7

Win.

0

0

0

1

0

0

0

1

13

Migr.

0

0

0

1

6

6

0

1

1

Migr.

0

0

0

1

9

10

1

0

0

Migr.

0

0

0

2

5

2

0

1

2

Win.

0

0

0

1

0

0

0

0

4

Migr.

5

0

24

13

41

29

4

4

14

Win.

7

0

24

36

95

20

7

3

30

Migr.

1

1

12

7

27

8

1

1

2

Win.

0

0

35

10

38

3

-

2

4

Migr.

2

1

15

1

28

15

4

6

8

Win.

1

1

13

14

42

7

8

0

27

Migr.

0

0

2

0

1

3

5

0

1

Win.

0

0

1

0

2

0

0

0

1

Migr.

0

0

3

0

4

1

0

0

0

Win.

2

0

10

4

14

1

0

0

2

Migr.

0

0

0

0

3

2

0

0

0

Win.

0

0

0

0

0

0

0

0

0

Migr.

0

0

1

4

80

6

6

10

48

Win.

1

0

2

3

18

8

3

1

14

Migr.

0

0

0

1

13

4

3

2

8

Win.

0

0

1

1

6

0

2

2

7

Fringillidae

Carduelis cannabina Carduelis chloris

27

Animal Biodiversity and Conservation 26.2 (2003)

Appendix 1. (Cont.)

Sector I Km2

Carduelis spinus Carduelis carduelis Fringilla coelebs Serinus serinus

II

III

IV

V

10500 5300

VI

VII

VIII

IX

7900

9800

7200 10400 15600 12000 13600

Migr.

0

1

4

7

Win.

2

0

6

6

16

1

4

0

12

Migr.

1

0

0

5

105

81

8

3

29

Win.

0

0

0

4

19

18

6

1

10

Migr.

1

0

3

1

54

7

4

3

49

Win.

0

0

2

7

15

7

4

6

37

Migr.

0

0

0

0

5

0

0

Win.

0

0

0

0

0

1

73

13

6

1

2

26

1

14

0

13

Appendix 2. Mean abundance (number of individuals / km ± s.d.) of bird species censored in the five sectors of the Atlantic coast (fig. 1).

Apéndice 2. Abundancia media (número de individuos / km ± d.e.) de las especies de aves censadas en los cinco sectores de la costa atlántica (fig. 1).

Sector Transects (n)

I

II

III

IV

V

10

10

20

20

20

Motacillidae

Anthus pratensis

4.6±4.8

29.8±25.8

29.7±29.9

19.0±17.2

26.3±13.3

Motacilla alba

1.4±1.6

2.2±3.2

5.5±5.4

4.8±5.4

9.4±7.7

Saxicola torquata

1.6±2.8

3.4±2.8

1.4±2.6

0.6±1.5

2.8±1.9

Erithacus rubecula

6.2±3.2

2.2±1.7

4.4±2.8

4.6±3.9

7.3±3.9

0

0

0

0.1±0.4

0.2±0.6

Turdus merula

6.6±4.7

2.6±2.6

6.6±4.7

5.1±4.2

5.8±5.4

Turdus philomelos

3.0±6.9

2.2±3.3

4.7±6.6

4.4±5.4

5.8±5.2

Turdus iliacus

1.2±2.1

11.2±14.2

7.9±14.9

6.9±14.6

13.1±16.4

Turdus viscivorus

0

0

0

0

0.2±0.6

Turdus pilaris

0

0

0

0.1±0.4

0

Carduelis chloris

6.4±14.8

0

0.2±0.6

0

1.0±2.6

Carduelis spinus

0

0

1.9±6.7

0.6±2.7

2.2±7.2

1.8±2.2

1.9±3.11

5.6±8.3

9.5±18.1

11.7±12.3

0

1.0±2.5

0

0

0.1±0.4

6.0±5.2

5.0±3.2

12.0±12.0

30.3±44.4

40.4±55.3

Serinus serinus

0

0

0.2±0.9

0.4±1.2

2.6±4.4

Pyrrhula pyrrhula

0

0

0

0

0.1±0.5

Turdidae

Phoenicurus ochruros

Fringillidae

Carduelis carduelis Carduelis cannabina Fringilla coelebs

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 26.2 (2003)

29

Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) on the Alboran Island (Western Mediterranean) M. Paracuellos, J. C. Nevado, D. Moreno, A. Giménez & J. J. Alesina

Paracuellos, M., Nevado, J. C., Moreno, D., Giménez, A. & Alesina, J. J., 2003. Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) on the Alboran Island (Western Mediterranean). Animal Biodiversity and Conservation, 26.2: 29–37.

Abstract Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) on the Alboran Island (Western Mediterranean).— Due to the high risk of the global extinction in which Patella ferruginea Gmelin, 1791 is found, it is considered of great interest to describe and quantify its demographic characteristics in those sites where it still persists, as well as to evaluate the reasons which have led this limpet to be one of the most threatened marine species in the Mediterranean Sea. Over the study period (2000–2002), systematic census were made on the perimeter of the Alboran Island (Alboran Sea, westernmost area of the Mediterranean Sea) with the object to quantify the abundance of the species in the locality, as well as their external biometry and spatial distribution. As a result, the presence of a probable reproductive population of P. ferruginea was found on the island. The negative effect provoked by the continuous presence of man was proved, prejudicing the population in those zones which were more accessible for their harvesting. For this reason, it is necessary to regulate the use of the natural resources of the island to favour the conservation and spontaneous recolonisation of the zone by P. ferruginea.

Key words: Patella ferruginea, Alboran Island, Population, Conservation, Human influence, Western Mediterranean.

Resumen Estado de conservación y características demográficas de Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) en la Isla de Alborán (Mediterráneo occidental).— Dado el peligro de extinción global en el que actualmente se encuentra Patella ferruginea Gmelin, 1791, se considera de gran interés describir y cuantificar las características poblacionales de la especie en aquellas localidades donde aún persiste, así como evaluar las razones que han llevado a considerar a esta lapa como una de las especies marinas más amenazadas de extinción del Mediterráneo. Durante el período de estudio (2000–2002) fueron realizados muestreos sistemáticos en el perímetro de la Isla de Alborán (Mar de Alborán, extremo occidental del Mediterráneo) con objeto de cuantificar la abundancia de la especie en la localidad, así como su biometría externa y distribución espacial. Como resultado, se ha constatado la presencia en la isla de una población de P. ferruginea probablemente reproductora.

Se ha comprobado el efecto negativo provocado por la continua presencia humana en la isla, perjudicando a la población en aquellas zonas más accesibles para la recolección de ejemplares. Es por ello que se considera necesario regular el uso de los recursos naturales en la isla con objeto de favorecer la conservación y recolonización espontánea de la localidad por P. ferruginea.

Palabras clave: Patella ferruginea, Isla de Alborán, Población, Conservación, Influencia humana, Mediterráneo occidental.

(Received: 26 III 03; Final acceptance: 26 V 03) Mariano Paracuellos, Juan Carlos Nevado, Adela Giménez & Juan José Alesina, Dept. de Flora y Fauna, Consejería de Medio Ambiente, Junta de Andalucía, c/ Reyes Católicos 43, E–04071 Almería, España (Spain).

Diego Moreno, Aptdo. Arañas, Las dunas 2, E–04150 Cabo de Gata, Almería, España (Spain).

Corresponding author: Mariano Paracuellos. E–mail: mariano.paracuellos.ext@juntadeandalucia.es ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

Paracuellos et al.

30

Introduction

Patella ferruginea Gmelin, 1791 is an endemic species of the Western Mediterranean Sea. Although its distribution in this basin was widespread during the Pleistocene, in prehistorical and historical times has entered obvious regression owing to human predation and it is now considered in high risk of extinction (IMPERATORI, 1968; TEMPLADO, 2001). Given this situation, the species has been catalogued in Annex II of the Convention Relative to the Conservation of the Wildlife and Natural Environment in Europe (Bern Convention, European Council, 19 September 1979; Royal Decree of 13 May 1986; BOE, 235, 1 October 1986) as a strictly protected species, in Annex II of the Barcelona Convention (Monaco, 24 November 1996) as “endangered or threatened”, in Annex IV of the Directive 97/62/CE of the Council (Habitat Directive, of 27 October; DOCE, L 305, 8 November 1997) as communitarian interest requiring strict protection, as well as in the National Catalogue of Threatened Species (Order of 9 June 1999; BOE, 148, 22 June 1999) as “in risk of extinction”. One factor which likely accounts for the decline of the species is that the limpet usually lives on rocky substrates above sea level (upper mesolittoral) and is therefore easily detectable by man. As it reaches a considerable size when adult, it is well appreciated for human consumption and decoration. Other causes which may have influenced its present scarcity and decline could be the progressive deterioration of the coastal strip where the species inhabits, the low fecundity of individuals and their scarce dispersal ability (LABOREL–DEGUEN & LABOREL, 1991a, 1991b; TEMPLADO, 2001). Therefore, it is considered of great interest to describe and quantify its population structure in those areas where it still persists, as well as to evaluate the reasons that have made this limpet one of the marine species at highest risk of extinction in the Mediterranean Sea (PORCHEDDU & MILELLA, 1991; TEMPLADO, 1998).

However, although various authors have analysed diverse aspects of the distribution and biology of P. ferruginea (C URINI –GALLETTI , 1979; GRANDFILS, 1982; BIAGI & POLI, 1986; BOUDOURESQUE & L ABOREL –D EGUEN , 1986; L ABOREL –D EGUEN & LABOREL, 1990, 1991a, 1991c; PORCHEDDU & MILELLA, 1991; MORENO, 1992; LABOREL–DEGUEN et al., 1993; CRETELLA et al., 1994; APARICI–SEGUER et al., 1995), few studies to date have quantified the repercussions of the human factor as the cause of its spatial distribution and regression of the populations (however see, LABOREL–D EGUEN & LABOREL, 1991b).

The presence of P. ferruginea on the Alboran Island is described in various studies (i. e., GARCÍA RASO & SALAS, 1984; YUS & CABO, 1986; RUBIO, 2001). However, although some papers indicate the species is abundant in the area (SALAS & LUQUE, 1986), TEMPLADO (2001) observed a very low number of individuals (28 in 1996 and 13 in

1998) during the last census (“Fauna IV” and “Alboran 98”, respectively). This author emphasised the possibility that in those years the population was not viable as reproductive, due to the low number of specimens detected and the fact that they were some distance away from each other, making fecundation difficult.

In this study, the current diverse aspects related to P. ferruginea on the Alboran Island are described, paying special attention to its demographic characteristics, external biometry, spatial distribution and repercussion of the human factor on its presence and development.

Materials and methods Study area The Alboran Island (Almería; 35º 56’ N, 3º 02’ W) is situated in the centre of the Alboran Sea (westernmost area of the Mediterranean Sea), 46.5 miles from the Iberian coast and 30 from the Maghreb coast. It is a small remote promontory of 7.1 ha in size, 605 m in length, 265 m wide, with a maximum height of 14 m and a perimeter of about 2000 m of shoreline (fig. 1).

The lithological nature of the area is essentially volcanic, mainly made up of an andesite tufa substrate (HERNÁNDEZ–PACHECO & IBARROLA, 1970). Its surface is flat, with a contour of vertical cliffs or steep slopes 8–12 m in height along most of its perimeter (except for two small beaches / landing places). At the base of the border of the island, where the action of waves occurs, there is a horizontal platform which is uncovered at low tide, forming a surrounding stretch of 15–20 m in average width. Apart from the main island, there are some small inlets close to its shores, for example the Nube inlet or the inlet near to the Cuevas Viejas (fig. 1). Therefore, with the exception of the existent beaches, the rest of the contour is favourable for the colonisation of P. ferruginea.

Mankind has been present on the island throughout history, but mainly since the construction of a lighthouse and associated buildings in the 19th century (ARCHDUKE LUIS SALVADOR, 1898; RUBIO, 2001). Since 1997, a permanent military garrison composed of a normal complement of 12 members exists. In relation to man’s uses in the locality, an Integral Reserve within a Natural Reserve has been declared since 1997 on the surroundings of the island, this including therefore the interior limits inhabited by P ferruginea.

Therefore and since its protection, it is expressly forbidden to collect or fish the flora and fauna in this area (Order of 31 July 1997; BOE, 204, 26 August 1997; GUIRADO et al., 1999). At present, the global protection of the total area in and around the Alboran Island as a “Paraje Natural” and the official approval of the Development Plan of the Natural Resources of the Alboran Island are underway, both measures which should help to

31

Animal Biodiversity and Conservation 26.2 (2003)

Nube Inlet 10

15

2

5

Western Mediterranean

6

4

16

9 1

N

50 km

5

0

37º

10

N 36º

1

0

Alboran Island 0

35º N 6º

5º

4º

3º

2º

19

6

1

1º W

Western beach / landing place

0

Eastern beach / landing place 200 m

1

Fig. 1. The Alboran Island and its geographical location. Dotted lines delimit the distinct stretches of shore taken into account, showing the numbers of specimens of Patella ferruginea found at each in July 2002. Accessibility by land to each of the stretches is also shown: Dotted. High accessibility; Striped. Medium accessibility; In white. Null accessibility (see Field methods).

Fig. 1. La isla de Alborán y su ubicación geográfica. Mediante líneas discontinuas se delimitan los distintos tramos de orilla considerados, mostrando para cada uno de ellos el número de ejemplares de Patella ferruginea encontrados durante julio de 2002. También se señala la accesibilidad por tierra a cada tramo: Punteado. Accesibilidad alta; Rayado. Accesibilidad media; En blanco.

Accesibilidad nula (ver Field methods).

guarantee the future conservation of the species and its habitat on the island (Agreement of 20 December 1998, of the Council of the Government of the Junta de Andalucía; PINILLA, 2001; DIRECCIÓN GENERAL DE PLANIFICACIÓN, 2002).

Field methods The monitoring was undertaken from 2000 to 2002. A first survey was made in June 2000 to estimate and map the specimens, continuing with total and supplementary census in October 2001 and in July 2002 for the definitive collection of data. The samplings were always carried out during the day, taking advantage of the optimal environmental conditions (calm day at low tide).

In order to quantify the population and distribution of the species on Alboran, systematic census of the individuals was carried out around the entire island. The shoreline of the island and its inlets were divided into transects, and the mesolittoral level of the peripheral platform, and the close zones of the supra and infralittoral levels were surveyed. All transects were covered by 1–3 people, using a boat along the stretches where accessibility was difficult or impracticable.

The following data were taken in situ on each of the observed individuals: 1. Location (using car-

tography); 2. Length (widest diameter of the shell); 3. Width (narrowest diameter of the shell); 4. Height (elevation of the shell from the base to the apex) (also see GRANDFILS, 1982; PORCHEDDU & MILELLA, 1991; APARICI–SEGUER et al., 1995). The shells were measured with a vernier calliper, with a precision to a 0.1 mm. Full length digital photographs of all individuals located were taken.

Taking into account the historical presence of man on Alboran, accessibility to the potentially habitable zones for the species was evaluated, in order to analyse the pressure provoked by collection for human consumption on the population and distribution of P. ferruginea on the island.

The more accessible intervals of shoreline for man were expected to be more exposed to exploitation, presenting a fewer and smaller specimens (less appreciated) than in less accessible zones with a hypothetical higher number of specimens and larger sizes (more appreciated), taking into account the specimen’s length as a standard measure (see as well, LABOREL–DEGUEN & LABOREL, 1991b). To quantify the level of accessibility to shoreline, the perimeter was divided into 20 strips of similar extension according to the map. Depending on the cartography and estimates in the area, two variables directly associated to the human capability of access to the areas were taken

Paracuellos et al.

32

into account. On one hand, accessibility by land to each sectors was defined: i. Highly accessible strips of the shore zones which could be reached on foot from the interior of the island along their entire length; ii. Semi–accessible strips, which could be reached on foot from the interior of the island only partly; iii. Non–accessible strips, which were not accessible on foot from the interior of the island. On the other hand, the degree of access by sea to the different sectors was estimated, taking into account the distance by swimming or by boat from the nearest beach / landing place to the midpoint of the established sectors (the farther from the beaches / landing places, the more effort needed to collect and the less accessibility degree by sea).

The Analysis of Variance (ANOVA, applying the Duncan Test post hoc) as well as the Simple and Multiple Regression Analysis were used for statistical analysis (SOKAL & ROHLF, 1994). When needed and according to the nature of the data, certain variables were used after their trigonometrical transformation.

1 cm

3 cm 5 cm 7 cm 9 cm

Fig. 2. Specimen of Patella ferruginea found on the Alboran Island in July 2002.

Fig. 2. Espécimen de Patella ferruginea encontrado en la Isla de Alborán durante julio de 2002.

Results A total of 80 specimens of P. ferruginea were located on the Alboran Island during the first sampling in June 2000, as compared to 92 and 111 during the later systematic census in October 2001 and July 2002 respectively. The number of individuals found in each stretch of shore is shown in figure 1, and one of the specimens measured can be seen in figure 2. Length ranged between 21 and 96 mm and distribution was bimodal, with a maximum between 30 and 40 mm and another, of a bigger magnitude, between 70 and 80 (fig. 3A). The width of the individuals varied between 15 and 80 mm, the bimodal distribution being less apparent, with the greatest number between 60 and 70 (fig. 3B).

The height of the shells varied between 7 and 50 mm, the highest number being between 30 and 40 (fig. 3C). When the different biometrical measures were compared between them adjustments to the lineal relations explained a great percentage of variance with high regression coefficients (fig. 4).

The average density of the specimens encountered was 0.06 individuals/m over the entire rocky shoreline. The distribution of the limpets was not homogeneous throughout the total perimeter of the island; being the greatest part of the population concentrated in the northeastern sector (fig. 1).

Considering accessibility by land to the delimited strips of littoral, significative differences were observed in the density of the limpets according to the degree of access; having the areas more easily reached from the interior of the island fewer specimens / m of shore than the less accessible areas (fig. 5A), principally due to the existing contrasts between the intervals with high and

null accessibility (P = 0.004). Although limpets located in areas which were more inaccessible by land were in many cases bigger in size than those found in more accessible zones, there were no significative differences in the length of their shells (fig. 5B). When relating the distance by sea from the nearest beach / landing place to each of the strips with its average number of limpets / m of shore and with the average size of the encountered individuals, a direct and significative relationship could be observed between the variables. Stretches farther from the beaches or landing places usually had specimens of a higher density and a bigger size than closer ones (fig. 6). However, the maximum percentage of variance was explained when relating both variables of accessibility jointly, by land and sea, with the number of limpets / m of shore in each strip:

D = 0.07 – 0.04 arcsine (√(x)) + z (r2 = 0.53, F2,17 = 9.63, P = 0.002, N = 20) and with their average size in each strip:

S = 65.30 – 1.96 arcsine (√(x)) + 0.03z (r2 = 0.51, F2,13 = 6.80, P = 0.009, N = 16) where D represents the number of limpets / m of shore, S the average size of limpets, x the proportion of length of accessible strip by land according to the continuous values from 0 (totally inaccessible strips) to 1 (totally accessible strips), and z the distance to the nearest beach / landing place.

33

Animal Biodiversity and Conservation 26.2 (2003)

A Number of limpets

40

30

20

10

0 0 B

10 20 30 40 50 60 70 80 90 100 Length (mm)

Number of limpets

40

30

20

10

0

0

10 20 30 40 50 60 70 80 90 100 Width (mm)

0

10 20 30 40 50 60 70 80 90 100 Height (mm)

40 Number of limpets

C

30

20

10

0

Fig. 3. Frequency of distribution found for the length (A), the width (B) and the height (C) of the shells of Patella ferruginea in the population of the Alboran Island during October 2001.

Fig. 3. Frecuencia de distribución encontrada para la longitud (A), la anchura (B) y la altura (C) de la concha de Patella ferruginea en la población de la isla de Alborán durante octubre de 2001.

Discussion Results regarding the number of specimens of the population of P. ferruginea on the Alboran Island surpassed the number cited by TEMPLADO (2001) over eight–fold. Data provided by this

author show a very scarce population of species during 1996 and 1998, disperse and composed mainly of females (large specimens), aspects which probably made it non–reproductive. However, the characteristics of the population found during the present study (2000–2002) suggest it was po-

Paracuellos et al.

34

60

A

Height (mm)

50 40

y = -3.97 + 0.49 x r 2 = 0.71 y/x = 0.43 ! 0.08

30 20 10 0 10

B

Width (mm)

90 80 70 60 50

30

50 70 90 Length (mm)

110

y = -1.05 + 0.83 x r 2 = 0.93 y/x = 0.82 ! 0.05

40 30 20 10 0 10

30

C 60

Height (mm)

50 40

50 70 90 Length (mm)

110

y = -2.28 + 0.57 x r2 = 0.68 y/x = 0.52 ! 0.10

30 20 10 0 10

30

50 70 Width (mm)

90

Fig. 4. Statistical relationships (Simple Regression Analysis) between: height vs. length (A), width vs. length (B) and height vs. width (C) of shells of Patella ferruginea on the Alboran Island during October 2001. Average value ± SD is also expressed for each relationship (y / x).

Fig. 4. Relaciones estadísticas (Análisis de Regresión Lineal Simple) entre altura vs. longitud (A), anchura vs. longitud (B) y altura vs. anchura (C) de Patella ferruginea en la isla de Alborán durante octubre de 2001. También se expresa para cada relación (y / x) su valor medio ± DE

tentially fertile. This could possibly be due to the relative high number of individuals present, with the greatest numbers found in a reduced sector of shore (more than 90 % of specimens were observed in a sector of about 1000 m), permitting

the external fertilisation of the eggs. According to the measures obtained (some of the biggest observed for the species), nearly all the located individuals were possibly adults (GRANDFILS, 1982; L ABOREL –DEGUEN & LABOREL , 1991a; T EMPLADO,

35

Animal Biodiversity and Conservation 26.2 (2003)

A

F 2,17 = 7.76 P = 0.004

F 2,13 = 1.60 P = 0.24

100 Average length (mm)

0,2 Number of limpets / m

B

0,15

0,1

0,05

80 60 40 20 0

0 Null

Medium

High

Null

Medium

High

Fig. 5. Statistical differences (ANOVA) of the density (average number of limpets / m of shore ! SD) (A) and the size (average length of limpets ! SD) (B) of Patella ferruginea according to the degree of accessibility by land to the different delimited stretches on the Alboran Island during July 2002.

Fig. 5. Diferencias estadísticas (ANOVA) de la densidad (nº medio de lapas / m de orilla ! DE) (A) y el tamaño (longitud media de las lapas ! DE) (B) de Patella ferruginea según el grado de accesibilidad por tierra a los diferentes tramos delimitados en la isla de Alborán durante julio de 2002.

B

y = 0.01 + 0.0002 x r 2 = 0.32, F 1,18 = 8.66 P = 0.009

0,2

0,15

0,1

0,05

y = 62.69 + 0.03 x r 2 = 0.49, F 1,14 = 13.30 P = 0.003

90 Average length (mm)

Number of limpets / m

A

80 70 60

50 0

100 200 300 400 500 Distance to the nearest beach / landing place (m)

600

0

100 200 300 400 500 600 Distance to the nearest beach / landing place (m)

Fig. 6. Statistical relationships (Simple Regression Analysis) between the density (number of limpets / m of shore) (A) as well as the size (average length of limpets) (B) of Patella ferruginea in the different stretches delimited on the Alboran Island and accessibility to these areas by sea to the same (distance by sea from the nearest beach / landing place) during July 2002.

Fig. 6. Relaciones estadísticas (Análisis de Regresión Lineal Simple) entre la densidad (nº de lapas / m de orilla) (A) así como el tamaño (longitud media de las lapas) (B) de Patella ferruginea en los diferentes tramos delimitados de la isla de Alborán y la accesibilidad por mar a los mismos (distancia por mar desde la playa / embarcadero más cercana) durante julio de 2002.

Paracuellos et al.

36

2001). The distribution of sizes, with a maximum of specimens with a length between 70–80 mm and another between 30–40, could have indicated the mixed presence of adult females (bigger and around the former maximum) along with the reproductive males (smaller and around the latter maximum), also allowing cross fertilisation (see TEMPLADO, 2001). However, recruitment of new specimens of this population of the limpet should be investigated in the near future to evaluate its conservational status on the island over the following years.

The height vs. length ratio of the shell on Alboran Island was high when compared with those given for other populations in the Mediterranean (see data of GRANDFILS, 1982; PORCHEDDU & MILELLA, 1991). The conical profile of the shells in the study locality could be related to the level inhabited by the species with respect to the sea level. Limpets living in the higher parts of the mesolittoral normally required a greater hydric reserve and, therefore, presented higher shells (with a higher internal volume) than those others located in the lower part of the mesolittoral and exposed to greater hydrodynamism, with flatter shells (GRANDFILS, 1982; TEMPLADO, 2001). Although the level where individuals were found was not evaluated in this study, the proportionally high shells of specimens of Alboran probably indicated limpet location at a certain height with respect to the sea level, as on the Chafarinas Islands (GRANDFILS, 1982).

It could be deduced that the distribution and range sizes of P. ferruginea on the island during the study period was very affected by the human accessibility to its habitat, thus verifying the initial hypotheses and in spite of the fact that the species is still frequent in the locality.

Accordingly, zones which were more accessible on foot from the interior and closer to usual swimming places or landing areas, presented lower populations of Patella ferruginea than hard–to–reach zones by land or sea, where the main surviving population was concentrated and, in many cases, composed of older individuals.

Consequently, continued human presence on the island appears to lead to a probable decline of the limpet in some of its zones from harvesting, confirmed by the presence of shell remains of the species in rubbish tips in the island (pers. obs.). Another finding supporting the negative effect provoked by man on the species is related to the possible increase and recovery of its population in recent years, coinciding with the definitive installation of the military garrison and the declaration of the Integral Reserve on the island, as dissuasive factors of despoliation on the littoral perimeter of Alboran (on comparison of data on numbers of individuals from TEMPLADO, 2001 and present study). This confirms the need to regulate anthropic uses in the island, as it appears in the Development Plan of the Natural Resources of the Alboran Island

awaiting approval, with the object to favour the conservation and the future spontaneous recolonisation of P. ferruginea on the entire littoral perimeter of the island.

Acknowledgments We would like to thank Juan García and Antonio Rodríguez, the crew of the AMA VII (Junta de Andalucía), without whose ever available collaboration and help access to the island and the sampling of the limpets would not have been feasible. The authors also wish to thank José Templado (Museo Nacional de Ciencias Naturales, Madrid) for his comments as referee, José Carlos García–Gómez (Sevilla University) for contributing information and Philip Kramer for the translation to English.

References APARICI–SEGUER, V., GUALLART–FURIÓ, J. & VICENT– RUBERT, J. J., 1995. Patella ferruginea population in Chafarinas Islands (Alboran Sea, Western Mediterranean). In: Abstracts. Twelfth International Malacological Congress: 119–121 (A. Guerra, E. Rolán & F. Rocha, Eds.). Instituto de Investigaciones Marinas (CSIC), Vigo.

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CRETELLA, M., SCILLITANI, G., TOSCANO, F., TURELLA, P., PICARELLO, O. & CATAUDO, A., 1994. Relationships between Patella ferruginea Gmelin, 1791 and the other Tyrrhenian species of Patella (Gastropoda: Patellidae). Journal of Molluscan Studies, 60: 9–17.

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GARCÍA RASO, J. E. & SALAS, C., 1984. Aportaciones al conocimiento de la fauna y flora litoral de la Isla de Alborán (España). Jábega, 45: 76–80.

GRANDFILS, R., 1982. Contribución al conocimiento de Patella ferruginea (Gmelin, 1789). Iberus, 2: 57–69.

GUIRADO, J., RAMOS, A. A., SÁNCHEZ LIZASO, J. L., REY, J., PÉREZ–VÁZQUEZ, E., FERNÁNDEZ–SALAS, L. M. & D ÍAZ DE R ADA , C., 1999. Isla de Alborán:

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conservación y protección de su patrimonio natural. In: Conclusiones del Encuentro Medioambiental Almeriense. Recursos hídricos (J. Rivera, Ed.). CD–ROM. Consejería de Medio Ambiente (Junta de Andalucía), Instituto de Estudios Almerienses (Diputación Provincial de Almería), Universidad de Almería, Grupo Ecologista Mediterráneo, Almería.

HERNÁNDEZ–PACHECO, F. & IBARROLA, E., 1970. Nuevos datos sobre la petrología y geoquímica de las rocas volcánicas de la isla de Alborán (Mediterráneo occidental, Almería). Estudios Geológicos, 26: 99–103.

IMPERATORI, L., 1968. Vicisitudes de la Patella safiana en las costas españolas. Boletín de la Real Sociedad Española de Historia Natural (Biología), 66: 137–140.

LABOREL–DEGUEN, F. & LABOREL, J., 1990. Nouvelles donnés sur la patella géante Patella ferruginea Gmelin en Méditerranée. I. Statut, répartition et étude des populations. II. Ecologie, biologie, reproduction. Haliotis, 10: 41–62.

– 1991a. Statut de Patella ferruginea Gmelin en Méditerranée. In: Les espèces marines à protéger en Méditerranée: 91–103 (C. F. Boudouresque, M. Avon & V. Gravez, Eds.). GIS Posidonie Publishers, Marseille.

– 1991b. Nouvelles observations sur la population de Patella ferruginea Gmel. de Corse. In: Les espèces marines à protéger en Méditerranée: 105–117 (C. F. Boudouresque, M. Avon & V. Gravez, Eds.). GIS Posidonie Publishers, Marseille.

– 1991c. Une tentative de reproduction de Patella ferruginea Gmelin (Gastropode) dans le parc National de Port–Cros (Var, France). In: Les espèces marines à protéger en Méditerranée: 129–132 (C. F. Boudouresque, M. Avon & V. Gravez, Eds.). GIS Posidonie Publishers, Marseille.

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1993. Appauvrissement des populations de la patelle géante Patella ferruginea Gmelin (Mollusca, Gastropoda, Prosobranchiata) des côtes de la Réserve Marine de Scandola (Corse du Sud) et du Cap Corse (Haute Corse). Travaux Scientifiques du Parc Naturel Regional et des Reserves Naturelles de Corse, 41: 25–32.

MORENO, D., 1992. Presencia de Patella ferruginea Gmelin, 1791 en el Cabo de Gata (Almería, SE España). Cuadernos de Investigación Biológica, 17: 71.

PINILLA, R., 2001. Alborán, la isla desconocida.

Medio Ambiente, 36: 6–13.

PORCHEDDU, A. & MILELLA, I., 1991. Aperçu sur l’ecologie et sur la distribution de Patella ferruginea (L.) Gmelin, 1791 en mers italiennes.

In: Les espèces marines à protéger en Méditerranée: 11–128 (C. F. Boudouresque, M. Avon & V. Gravez, Eds.). GIS Posidonie Publishers, Marseille.

RUBIO, F. J., 2001. La pesca en la Isla de Alborán.

Textos y Ensayos, 17. Instituto de Estudios Almerienses (Diputación de Almería), Almería.

SALAS, C. & LUQUE, A. A., 1986. Contribución al conocimiento de los moluscos marinos de la Isla de Alborán. Iberus, 6: 29–37.

SOKAL, R. & ROHLF, F. J., 1994. Biometry. W. H. Freeman & Co., San Francisco.

TEMPLADO, J., 1998. Patella ferruginea (Gmelin, 1791). Naturalia Hispanica. http: //www.mma.es Ministerio de Medio Ambiente, Madrid.

– 2001. Patella ferruginea Gmelin, 1791. In: Los invertebrados no insectos de la Directiva Hábitats en España: 41–49 (M. A. Ramos, D. Bragado & J. Fernández, Eds.). Serie Técnica, Organismo Autónomo Parques Nacionales (Dirección General de Conservación de la Naturaleza, Ministerio de Medio Ambiente), Madrid.

YUS, R. & CABO, J. M., 1986. Guía de la naturaleza de la región de Melilla. Excmo. Ayuntamiento de Melilla, Melilla.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 26.2 (2003)

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Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia A. C. B. Pinto, C. Azevedo–Ramos & O. de Carvalho Jr.

Pinto, A. C. B., Azevedo–Ramos, C. & Carvalho Jr., O. de, 2003. Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia. Animal Biodiversity and Conservation, 26.2: 39–49.

Abstract Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia.— This work compared the activity patterns and diet of a group of Alouatta belzebul in areas of logged and unlogged forest in eastern Amazonia. An instantaneous scan sampling procedure was used for the behavioral study (9.3 ± 1.9 complete observation days/month) from February to November 2000. Fruit availability was estimated monthly. Activity budgets were not significantly different between sites. Rest was the predominant activity in both sites (53.6 % and 48.7 %, respectively). Average daily path length was 683.5 ± 215.1 m (n = 93), and the home range was 17.8 ha, including 7 ha in unlogged forest and 10.8 ha in the logged forest. Neither fruit availability nor diet varied significantly between sites. The diet was predominantly folivorous (43.4 % and 46.6 % in unlogged and logged forest, respectively) and frugivorous (43.9 % and 42.8 %). The spatial use by the group was positively related to fruit sources. This study documented the ability of a ranging group of A. belzebul to survive in a habitat influenced by reduced impact logging without dramatically influencing its activity patterns and diet.

Key words: Alouatta belzebul, Activity patterns, Diet, Reduced impact logging, Tropical rain forest, Amazonia.

Resumen Patrones de comportamiento y alimentación del mono aullador Alouatta belzebul en zonas de selva talada y sin talar del este de la Amazonia.— En este trabajo se comparan los patrones de comportamiento y alimentación de un grupo de Alouatta belzebul en zonas de selva deforestada y sin deforestar del este de la Amazonia. Para el estudio del comportamiento se utilizó un muestreo de barrido temporal instantáneo (observación completa durante 9,3 ± 1,9 meses/ días) entre los meses de febrero y noviembre de 2000. La disponibilidad de fruta se calculó mensualmente. Las actividades realizadas no fueron significativamente diferentes en ninguna de las dos ubicaciones. El descanso fue la actividad predominante en ambas, 53,6 % y 48.7 % respectivamente. La media de la longitud de los recorridos diarios era de 683,5 ± 215,1 m (n = 93) y el área de acción era de de 17,8 hectáreas, incluyendo 7 hectáreas de selva sin talar y 10,8 hectáreas de bosques talados. Ni la disponibilidad de fruta ni la dieta variaron significativamente entre las zonas. La dieta era eminentemente folívora (43,4 % y 46,6 % en las zonas de selva sin talar y deforestada, respectivamente) y frugívora (43,9 % y 42,8 %). El uso que el grupo hacía del espacio estaba relacionado de manera positiva con las fuentes de suministro de frutas. En este estudio se ha documentado la habilidad de un grupo de A. belzebul en libertad para sobrevivir en un hábitat afectado por una tala de impacto reducido sin que ello afectase dramáticamente a sus patrones de comportamiento y alimentación.

Palabras clave: Alouatta belzebul, Patrón de comportamiento, Alimentación, Tala de impacto reducido, Selva tropical, Amazonia.

(Received: 3 IV 02; Conditional acceptance: 3 X 02; Final acceptance: 12 V 03) Andréia C. B. Pinto & Claudia Azevedo–Ramos, Núcleo de Altos Estudos Amazônicos (NAEA), Univ. Federal do Pará (UFPA), CEP 66.075–900, Belém–PA, Brasil.

Claudia Azevedo–Ramos & Oswaldo de Carvalho Jr, Inst. de Pesquisa Ambiental da Amazônia (IPAM), Av. Nazaré 669, CEP 66.075–900, Belém–PA, Brasil.

ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

Pinto et al.

40

Introduction

Materials and methods

Brazilian Amazonia contains more than one third of the world’s forests and the richest Neotropical primate fauna. However, of the 123 primate taxa occurring in Amazonia (including species and subspecies), 18% are threatened (RYLANDS et al., 1997).

Deforestation and timber harvesting are the main disturbing factors affecting the region, especially in Eastern Amazonia. Selective logging invariably involves alterations in the physical structure of the vegetation and availability of food resources, which may have considerable impacts on primates (JOHNS, 1983; JOHNS & SKORUPA, 1987; GREISER JOHNS, 1997).

Despite these negative impacts, logged forests have a potential for conservation, as they contain a great share of native fauna, including primates.

However, a better understanding of primate adaptations to logged forests is urgently needed to allow the elaboration of more effective forest resource management and conservation strategies. It is reasonable to assume that behavioral flexibility would allow a better chance of surviving in altered habitats.

The howler monkeys (Allouatta) are known for their capacity to adapt in forest fragments (RYLANDS & KEUROGHLIAN, 1988; CHIARELLO, 1993; B ICCA –M ARQUES & C ALEGARO –M ARQUES , 1994; ESTRADA & COATES–ESTRADA, 1996; ESTRADA et al., 1999; JUAN et al., 2000; GÓMEZ–MARIN et al., 2001), which made us question how they would respond to logging activity. This study compares the activity patterns and diet of a group of Red– Handed howler monkeys, Alouatta belzebul, which lives in a mosaic of logged and unlogged forests in Eastern Brazilian Amazonia.

This species is endemic to Brazil and can be found in the Amazon and Atlantic forests (BONVICINO et al., 1989). The diet of the genus Alouatta can best be defined as folivorous–frugivorous (CROCKET & EISENBERG, 1987). Its diversified diet favors Alouatta’s occurrence under several environmental conditions (MILTON, 1980; NEVILLE et al., 1988; CROCKETT, 1998; HORWICH, 1998).

During periods of food shortage, howler monkeys may compensate for fruit scarcity by consuming leaves and decreasing physical activities to offset the low energetic return from leaves (MILTON, 1980; NEVILLE et al., 1988). Because selective logging may remove important tree species from the monkey’s frugivorous diet, the hypothesis of this work was that the abundance of fruits in the logged site would be lower, inducing howler monkeys to become more folivorous. As a consequence, the size of home range, as well as the time dedicated for locomotion should be smaller in the logged site. Changes in activity and diet may potentially modify the ecological services of this howler monkey group (e.g., from seed disperser to seed predator), a subtle effect of logging activities, which —if replicated in other animal groups— may affect long–term environmental sustentability.

The study was conducted in Cauaxi Ranch (3º 45’ 32” S; 48º 10’ 06” W), Paragominas Municipality, northeast of Para, Brazil. The area is covered by Terra Firme (up–land) rain forest, with total annual rainfall about 2,200 mm. This ranch has approximately 20,000 hectares, comprising a mosaic of logged and unlogged forests, and pasture areas. The logged site used for this study was harvested using reduced–impact techniques in 1996 (VERÍSSIMO et al., 1992; VIDAL et al., 1997).

The logging intensity was 25 m3/ha (~3 trees/ha).

The group of howler monkeys observed included six individuals (one adult male, two adult females, one sub–adult female, one young male, and an infant female). The group became accustomed to the observer for a period of 50 hours before data collection began. In order to quantify their home range, their localization in the area, and the resources that they utilized, a 50 x 50 m grid system was cleared in 80 ha (40 ha in a logged area and 40 in an unlogged area).

This area represents approximately 4 times the home range previously reported for this species (e.g. BONVICINO, 1989; SOUZA, 1999).

Activities of the Alouatta belzebul group were monitored using instantaneous scan samplings (ALTMANN, 1974) for ten days per month from 6.00 to 19.00 h, from February to November 2000. The observations totaled 1203.25 h, and were distributed in 105 observation days (93 complete and 12 incomplete days). During this period, a total of 5003 scans were conducted and 21300 behavioral records were obtained. Observations were made using binoculars, and a distance of at least 10 m was maintained between the observer and the monkeys at all times. The group's activities were recorded every 15 minutes (see QUEIROZ, 1995; JARDIM, 1997; PINA, 1999; SOUZA, 1999). In each scan and for each individual we recorded: (1) behavioral category, (2) age and sex and (3) location in the 50 x 50 m grid system.

Four behavioral categories were established based on previous studies (BONVICINO, 1989; JARDIM, 1997; PINA, 1999; SOUZA, 1999), and preliminary field observations: resting, moving, feeding and social interaction. When all individuals were out of sight during a scan, but their location was known, the record was attributed to the category of rest (PINA, 1999; SOUZA, 1999). During feeding events, the ingested item was categorized (fruit, leaf, flower, or termite’s nest), identified to species level whenever possible, and its source was plotted in the map area. When the ingested item was a fruit or leaf, the stage of maturity was also recorded.

The group’s home range was estimated by summing the visited grids. For this purpose we divided the larger 50 x 50 m grids into four 25 x 25 m2 when estimating their location. In order to determine the daily range, the route of the group was traced on the map containing the

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trail grid and then measured using a curvemeter, with its scale converted to meters.

A fruit abundance index for each area was calculated using an adaptation of Z HANG & WANG’s (1995) forest floor fruit counting methodology. In an area of 60 ha (30 ha for each site) a 1 ha sampling area (0.5 ha for each site) was selected at random each month and divided into 10 transects of 5 x 200 m. The fruit counting was conducted at the end of each month in both sites. All pre–existent fruits found on the floor were removed 10 days before each sample to avoid recording fruits whose availability did not correspond to that month. During the census, all fruits (mature, immature or fragmented) were counted along each transects. Fruits were identified to species level whenever possible or classified as morphospecies.

The differences in behavioral and feeding categories between logged and unlogged sites during the ten–month sampling were tested using the Wilcoxon non–parametric test for dependent samples (SIEGEL, 1979; AYERS et al., 2000). The difference between the fruit abundance index estimated for both sites was evaluated using the Mann–Whitney Test for independent samples. The Sorensen index was used to measure the similarity of fruit composition between the areas (KREBS, 1989).

Because the spatial use patterns of a group of primates may be influenced by food sources and the presence of other groups (MILTON, 1980; TERBORGH, 1983; JARDIM & OLIVEIRA, 1997), the spatial use of the habitat by these howler monkeys was evaluated using Pearson linear correlation relating the monthly home range with (1) the number of fruit sources used monthly by the group, (2) the number of fruits recorded through counting, and (3) inter–group encounters, based on the absolute number of encounters (visual or agonistic) between neighboring groups. The effect of the diet on howler monkey behavior was also tested by correlating the speed of locomotion with percentage of fruit ingestion.

Results The howler monkey group spent more time in the logged site (65.1 %) than in the unlogged site (34.9 %). Approximately half of the activity period of the howler monkeys in logged and unlogged sites was dedicated to rest (48.7 % and 53.6 %, respectively). The remaining time was divided among moving (28.7 % and 29.3 %), feeding (21.6 % and 15.9 %) and social interactions (0.8 % and 1.2 %). The howler monkey’s diet at both sites was characterized by the consumption of fruits (42.8 % and 43.9 % ) and leaves (46.6 % and 43.4 %), followed by a lower percentage of flowers (10.0 % and 12.5 %). Soil ingestion events (0.6 % and 0.2 %), representing the intake of nest termites, were more frequent in ad libitum records due to the rarity of this activity.

41

There was no significant difference in the time spent in each behavioral category between the sites within the 10 months of sampling (Wilcoxon Test, rest: Z = -1.784; P = 0.075; moving: Z = -0.051; P = 0.959; feeding: Z = -1.784; P = 0.075; social interactions: Z = -0.866; P = 0.386, n = 10 for all comparisons; fig. 1).

There were no significant differences within the same feeding category between sites: fruits (Wilcoxon Test, Z = -0.2801; n = 10; P = 0.779), young leaves (Z = -0.6625; P = 0.508), mature leaves (Z = -0.4146; P = 0.678) and flowers (Z = -0.5601; P = 0.575). In both sites, it was verified that the decrease in fruit consumption and the consequent higher intake of leaves and flowers was more accentuated during the beginning of the dry season (fig. 2).

The fruit abundance sample registered a total of 39 species / morphospecies, of which 19 (48.7 %) were exclusive to the unlogged site, 14 (35.9 %) were only present in the logged site, while six (15.4 %) were present in both. The similarity found between the sites was only 0.27 according to the Sorensen Index (values range from 0 to 1), indicating a strong difference in fruit composition. However, the absolute difference in fruit abundance between the logged and unlogged sites was not statistically significant (Mann– Whitney, U = 50; n = 10; P = 1.00). The temporal distribution of fruit species / morphospecies was very heterogeneous. Thirty (76.9 %) were recorded only once in ten months. The greatest abundance of fruits at both sites was in February which was also the richest month in the unlogged site (11 species, 5 for the logged site), followed

by March and November (5 species at each site).

Fifty six percent of the species (22 species) showed mature fruits (table 1).

The home range of the focal howler monkey group comprised 17.8 ha, including 7 ha of unlogged forests and 10.8 ha of logged forests was used by the howler monkeys (fig. 3). In the logged site, the howler monkeys did not avoid areas affected by harvesting trails and tree removals. The logging removed 23 trees within the group’s home range (fig. 3). However, when the logging intensity within the group’s home range (2.1 trees removed/ha) was compared to the logging intensity in the surrounding 16 ha (3 trees removed/ha; fig. 3), it was observed that the home range of the howler monkeys was confined to an area that was somewhat less impacted by tree removals.

During the study, 42 inter–group encounters were observed. Of these, 15 involved competition for food sources, two for sexual partners, two for sleeping sites and the other 23 had no direct cause identified, but were possibly for territorial defense. Twenty of the total encounters (47.6 %) were characterized by agonistic interaction, including violent chases between the males of rival groups, and reciprocal vocalizations. The other 22 encounters (52.4 %) were classified as

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Fig. 1. Variación mensual de la proporción de categorías de comportamiento principales de Alouatta belzebul en zonas sin talar (n = 7562 datos sobre comportamiento) y en zonas deforestadas (n = 13 738,35), entre los meses de febrero y noviembre de 2000, en Paragominas, Pará, Brasil: A. % en reposo; B. % en movimiento; C. % alimentándose; D. % social.

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O

N

Fig. 2. Monthly variation in the proportion of the main feeding categories of Alouatta belzebul in unlogged (n = 1261 feeding records) and logged forests (n = 2941), from February to November 2000, in Paragominas, Para, Brazil: A. % fruits; B. % young leaf; C. % madure leaf; D. % flowers.

Fig. 2. Variación mensual en el porcentaje de categorías de alimentos principales de Alouatta belzebul en zonas sin talar (n = 1261 datos de alimentación) y en zonas deforestadas (n = 2941), de febrero a noviembre de 2000 en Paragominas, Pará, Brasil: A. % frutos; B. % hojas jóvenes; C. % hojas maduras; D. % flores.

43

Animal Biodiversity and Conservation 26.2 (2003)

Table 1. Monthly fruit census in the unlogged and logged sites from February to November 2000 at the Cauaxi Ranch in Paragominas, Para, Brazil: N. Number of fruits; % Montly percentage; * Species utilized by Alouatta belzebul’s group as fruit resource.

Tabla 1. Censo mensual de frutas en las ubicaciones deforestadas y sin deforestar, entre los meses de febrero y noviembre de 2000 en el Rancho Cauaxi de Paragominas, Pará, Brasil: N. Número de frutos; % Porcentaje mensual; * Especies utilizadas por el grupo de Alouatta belzebul como fuente de suministro de frutas.

Family Species or morphospecies

Unlogged Forest

Logged Forest

Month

N

%

N

%

February

15

(4.4)

0

(0)

Sapotaceae

Manilkara amazonica*

March

01

(2.6)

0

(0)

Manilkara sp.*

September

0

(0)

01

(100.0)

Neoxythece elegans*

February

262

(76.2)

0

(0)

Pouteria bilocularis*

February

01

(0.2)

0

(0)

Pouteria laurifolia*

November

0

(0)

03

(3.8)

Pouteria sagotiana*

October

50

(96.2)

45

(93.8)

November

04

(14.8)

0

(0)

Morphospecie # 01

February

03

(0.9)

0

(0)

Morphospecie # 02

August

12

(17.4)

0

Morphospecie # 03

November

0

(0)

30

February

01

(0.3)

0

(0) (37.5)

Mimosaceae

Inga heterophylla*

(0)

July

0

(0)

12

Inga sp. 1*

February

06

(1.7)

0

(70.6) (0)

Inga sp. 2

November

0

(0)

05

(6.3)

Burseraceae

Protium guacayanum*

February

0

(0)

20

(14.1)

Protium sp.*

February

0

(0)

10

(7.0)

Lauraceae

Nectandra rubra*

Morphospecie # 04

February

0

(0)

01

(0.7)

March

01

(2.6)

0

(0)

August

0

(0)

01

November

02

(7.4)

0

(0)

July

30

(56.6)

0

(0)

February

14

(4.1)

0

(0)

November

0

(0)

02

(2.5)

February

02

(0.6)

0

(0)

July

20

(37.7)

0

(0)

March

01

(2.6)

0

(0)

(20.0)

Humiriaceae

Endopleura uchi *

Sacoglotis guianensis Moraceae

Brosimum amplicoma Helicostylis sp.

*

Asteraceae

Heteropsis jenmani*

Pinto et al.

44

Table 1. (Cont.)

Family

Month

Unlogged Forest

Logged Forest

N

%

N

%

February

01

(0.3)

0

(0)

March

0

(0)

87

October

01

(1.9)

0

(0)

February

0

(0)

01

(0.7)

July

02

(3.8)

0

(0)

October

0

(0)

02

(4.2)

November

10

(37.0)

40

(50.0)

February

01

(0.3)

0

August

0

(0)

01

February

38

(11.0)

0

(0)

March

28

(71.8)

0

(0)

Setember

12

(100.0)

0

(0)

November

10

(4.4)

0

(0)

Morphospecies # 05

February

0

(0)

110

(77.5)

Morphospecies # 06

March

0

(0)

06

(6.4)

Species or morphospecies Caryocaraceae

Caryocar glabrum Combretacae

Buchenavia sp.*

93.5

Chrysobalanaceae

Licania sp.* Lecythidaceae

Eschweillera odorata

Passifloraceae

Passiflora nitida*

(0) (20.0)

Polygalaceae

Moutabea guianensis* Tiliaceae

Luehea speciosa* Not identified

Morphospecies # 07

July

01

(1.9)

02

(11.8)

August

0

(0)

03

(60.0)

Morphospecies # 08

July

0

(0)

02

(11.8)

Morphospecies # 09

July

0

(0)

01

(5.9)

Morphospecies # 10

August

57

(82.6)

0

(0)

Morphospecies # 11

November

01

(3.7)

0

(0)

Morphospecies # 12

October

01

(1.9)

0

(0)

Morphospecies # 13

October

0

(0)

01

(2.1)

Morphospecies # 14

June

0

(0)

20

(100.0)

Morphospecies # 15

March

08

(6.4)

0

Total fruits

pacific, with only visual interactions, sometimes including few vocalizations with one of the groups leaving the area before any physical contact. The relationship between the size of the area used by the monkeys monthly and interâ&#x20AC;&#x201C;group encounters was positively significant in the unlogged

596

(0)

406

site (r = 0.652; P = 0.041), but not in logged site (r = 0.164; P = 0.651; fig. 4). In the later, the encounters took place manly in few areas with larger concentration of fruiting tree, without significant relationship to the exploration of new areas by the howler group. On the other hand, in

45

Animal Biodiversity and Conservation 26.2 (2003)

A

B

C

D

E

F

G

H

I

J

K

L

M

N

O

P

Q

1

200 m

3

150 m

4

100 m

5

50 m

6

Main road

7

0 m 50 m

8

100 m

N

10 11

300 m 250 m

2

9

R

Unlogged forest

12

Harvested trees

Intensity of use 0 – 1 % 1.1 – 2 % 2.1 – 3 % 3.1 – 4 % > 4 %

Log deck

150 m

Secondary road Primary skid trails Secondary skid trails Boundary home range

200 m 250 m 300 m

Fig. 3. Skid trails and harvested trees within / around the home range of the Alouatta belzebul, showing the intensity of spatial use (according to the number of scans in each 50 x 50 m2; n = 5003 scans), in Cauaxi farm, Paragominas, Para, Brazil.

Fig. 3. Senderos de arrastre y árboles talados dentro / alrededor del área de deambulación de Alouatta belzebul, que muestran la intensidad de uso del espacio (de acuerdo con el número de barridos cada 50 x 50 m2, n = 5003 barridos), en la granja Cauaxi, Paragominas, Pará, Brasil.

unlogged site, most of the encounters occurred along the west margin of the focal group’s home range, indicating an expansion of the home range to this direction. The expansion of the area used by the monkeys was motivated by the search for new fruit sources in logged and unlogged sites, as indicated by a linear correlation between the size of home range and the number of fruit sources used by the howler group (r = 0.787; P = 0.007; and r = 0.759; P = 0.011, respectively). Areas with low intensity use sometimes received visits exclusively focused on a specific fruit source. However, the relation between size of home range and number of fruits counted on the forest floor was not significant for either site, possibly due to low overlap between the counted species and the fruit species consumed by howlers (33.3 % in unlogged site and 23.3 % in logged sites).The daily range varied from 269 to 1300 m, with an average of 683.5 ± 215.1 m based on 93 days of complete observation. Direct comparisons of the daily path length between the sites was not possible, since the group used both sites almost on a daily basis and the locomotion behavior rarely took place exclusively in one of the sites alone. However, the relationship between the daily range and the time of permanence of the

howler monkey group in each site showed that there was no difference in the speed of locomotion between the unlogged (61.0 ± 22.04 m/h) and the logged sites (66.3 ± 28.32 m/h; Mann–Whitney, U = 45, n = 10, P = 0.706). However, there was a significant and positive correlation between speed of locomotion and frugivory (r = 0.660, P = 0.038).

Discussion The initial prediction that fruit availability would be lower in the logged site, and that this would press the monkeys towards a more folivorous diet, and consequently less activity in this area, was not confirmed. No significant alteration in the diet or in the behavioral pattern of the monkeys between areas was found.

Three factors may have contributed to the absence of behavioral modifications in the logged area. First, the low logging intensity (25 m3 / ha) and the reduced–impact operational model may not have altered the area considerably in terms of food resources availability, at least not to the point of provoking a change in the monkeys’ behavior. That was partially confirmed by the fruit

Pinto et al.

Unlogged forest Number of inter–group encounters

3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

Logged forest

6 5 4 3 2 1 0

1 2 3 4 5 Monthly size of home range (ha)

3

4 6 7 5 Monthly size of home range (ha)

Fig. 4. Relationship between the size of the area used monthly by the monkeys and inter–group encounters in the unlogged (r = 0.652; P = 0.041) and logged sites (r = 0.164; P = 0.651), from February to November 2000, in Paragominas, Para, Brazil.

Fig. 4. Relación entre las dimensiones del área que los monos utilizan mensualmente y los encuentros entre diferentes grupos en las zonas sin talar (r = 0,652; P = 0,041) y en las deforestadas (r = 0,164; P = 0,651), desde febrero a noviembre de 2000 en Paragominas, Pará, Brasil.

Unlogged forest

5

Monthly size of home range (ha)

Monthly size of home range (ha)

Number of inter–group encounters

46

4

3

2

1

0

5 10 Number of fruit sources

15

7

Logged forest

6

5

4

3 0

5 15 10 Number of fruit sources

20

Fig. 5. Relationship between the size of the area used monthly by the monkeys and the number of fruit sources used by the howler group in the unlogged (r = 0.759; P = 0.011) and logged sites (r = 0.787; P = 0.007), from February to November 2000, in Paragominas, Para, Brazil.

Fig. 5. Relación entre las dimensiones del área que los monos utilizan mensualmente y el número de fuentes de suministro de frutas utilizadas por el grupo de monos aulladores en las zonas sin talar (r = 0,759; P = 0,011) y en las deforestadas (r = 0,787; P = 0,007) desde febrero a noviembre de 2000 en Paragominas, Pará, Brasil.

47

Animal Biodiversity and Conservation 26.2 (2003)

census, which indicated similar fruit abundance between the sites, although the species composition was different. Second, the adjacent unlogged site possibly acted as a refuge for the monkeys, at least, minimizing possible harsh conditions due to logging activities, such as clime changes (e.g.

CHIARELLO, 1993; ESTRADA et al., 1999). Third, the time period between the harvesting and this study, approximately three years, could have been sufficiently long for the monkeys to reestablish their pre–harvesting behavior. Other studies (JOHNS, 1983; JOHNS & SKORUPA, 1987; GRIESER JOHNS, 1997) have shown a relatively short re-adaptation period for various animal species following logging and in the absence of subsequent anthropogenic pressures (e.g. hunting and/or agriculture). Likewise, leaves and flowers that show a decline in abundance immediately following logging, may show production peaks after logging (JOHNS, 1986, 1988, 1994). Additionally, some of Alouatta’s inherent characteristics, such as a recognized diet flexibility, and tolerance to disturbed habitats (MILTON, 1980; ESTRADA & COATES–ESTRADA, 1996; CROCKETT, 1998; HORWICH, 1998; SILVER et al., 1998; ESTRADA et al., 1999; GÓMEZ–MARIN et al., 2001) may help to explain how this group was able to persist in the logged area without significant changes in its behavioral patterns.

The lack of information on the behavior of A. belzebul in other logged forests makes it difficult to generalize from our results. However, the activity pattern and diet of our group were similar to those found for other groups of red–handed howler monkey in the Caxiuanã National Forest, in Pará, Brazil (PINA, 1999; SOUZA, 1999), an area of continuous rainforest with climatic similarities with our study site. In general, the behavioral budget of the focal group was typical for the Alouatta genus, with resting activities dominating other activities (BICCA–MARQUES & CALEGARO–MARQUES, 1994; SILVER et al., 1998; ESTRADA et al., 1999; JUAN et al., 2000). As to the home range, other studies on A. belzebul recorded a variation from 9.5 to 18.1 ha (BONVICINO, 1989; SOUZA, 1999, respectively); our group occupied an area at the high end of this range (17.8 ha). However, the average daily range of A. belzebul in this study was 50 % less than that recorded by JARDIM (1997) and SOUZA (1999), but similar to that reported by BONVICINO (1989) in an Atlantic Forest fragment.

As a general rule, the temporal and spatial distribution of food resources, the location of sleeping sites, and the degree of territoriality of the species, influence the spatial use pattern of primates (TERBORGH, 1983). For this study, fruit source distribution was a key element in explaining the howler monkeys’ spatial use patterns; the expansion of the home range was positively correlated with the search of new fruit sources. In general, the Amazonian species of Alouatta exhibits a pronounced frugivorous diet, as compared with howler species from others regions (e.g., JULLIOT & SABATIER, 1993; QUEIROZ, 1995;

JARDIM, 1997; PINTO, 2002), reinforcing the importance of this food source.

A close link between home range and food source availability has been demonstrated for howler monkeys. The study of STONER (1996) on habitat selection by Alouatta palliata in Costa Rica clearly showed that the density of the principal food resources was the most important factor driving habitat selection. The same species studied in forest fragments of different sizes in Mexico showed a higher index of frugivory and travelling activities among the groups living in larger fragments that also contained the highest number of food sources (JUAN et al., 2000). Additionally, CLARKE et al. (2002) observed a new arrangement in the home range of one group of A. palliata in Costa Rica. This group incorporated new stands of the fruit tree Muntingia calabura (Elaeocarpacaeae) when this source became available and was located close to their original home range.

As a consequence of their dietary preference for ripe fruits, the howlers monkeys have played an important role as seed dispersers (see ESTRADA & COATES–ESTRADA, 1984, 1986; JULLIOT, 1996, 1997; PINTO, 2001); and as a result of their feeding flexibility, the howlers present considerable ability to survive in altered areas. Thus, these monkeys may to persist under conditions of reduced–impact logging and contribute to regeneration of the logged area (through of the seed dispersal), since fruit sources not had been severely harvested. The intensity and type of logging (e.g. high–impact or reduced–impact logging) are certainly key factors for the maintenance of environmental conditions that will allow the permanence of primates species in logged forests (see JOHNS, 1983; JOHNS & SKORUPA, 1987; GREISER JOHNS, 1997). Therefore, this study suggests that forest management plans should foresee the maintenance of a temporal and spatial availability of fruits that allow a larger spatial use by the monkeys, and, therefore, improve the ecological services they might provide. Additionally, the maintenance of unlogged fragments next to logged forests may help as a faunal refuge and seed stock for forest regeneration. The control of indirect effects of logging, such as the increase in hunting due to the facilitated access to remote areas, is also important. This may represent the major threat to the survival of large primates after logging (see JOHNS, 1983; PERES, 1990, 1997).

Acknowledgements Paulo Moutinho and Stephen Ferrari reviewed an early draft of the manuscript. Yabanex Baptista and David Ray helped with English translation.

This study received logistic support from The Tropical Forest Foundation–Brazil and Cikel Brasil Verde, and was supported by a USAID grant and a scholarship to the first author from the Coordenação de Pessoal de Ensino Superior (Capes, Brazil).

48

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Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 26.2 (2003)

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Influence of forest and grassland management on the diversity and conservation of butterflies and burnet moths (Lepidoptera, Papilionoidea, Hesperiidae, Zygaenidae) T. Schmitt

Schmitt, T., 2003. Influence of forest and grassland management on the diversity and conservation of butterflies and burnet moths (Lepidoptera, Papilionoidea, Hesperiidae, Zygaenidae). Animal Biodiversity and Conservation, 26.2: 51–67.

Abstract Influence of forest and grassland management on the diversity and conservation of butterflies and burnet moths (Lepidoptera, Papilionoidea, Hesperiidae, Zygaenidae).— The distribution of butterflies and burnet moths was investigated at 38 patches in the Oettinger Forst (Bavaria, Germany) in 2001. Forty–two butterfly and four burnet moth species were recorded. They were unequally distributed over the study area. The diversity was significantly lower in the forests than in the non–forest patches. Windblows and meadows showed largely similar results but clearings had higher Shannon indices and Eveness and presented a trend to higher species numbers. The hay meadows had higher mean incidences of the 25 common species and exhibited a trend to higher numbers of individuals and species as well as higher mean Shannon indices than in the mulched meadows. The old quarries and sandpits harboured remarkable species, some of these occurring in high densities, thus underlining the conservation value of such structures in a non–target area for nature–conservation measurements.

Key words: Butterfly conservation, Meadows, Windblows, Clearings, Quarries, Sandpits.

Resumen Influencia de la gestión de los bosques y las zonas de pastos en la diversidad y conservación de las mariposas diurnas y zygenas (Lepidoptera, Papilionoidea, Hesperiidae, Zygaenidae).— Se ha estudiado la distribución de las mariposas diurnas y zygenas en 38 parcelas de Oettinger Forst (Baviera, Alemania) en el año 2001. En total, se contabilizaron 42 especies de mariposas diurnas y cuatro de mariposas zygenas, cuya distribución en la zona de estudio resultó bastante irregular. La diversidad fue considerablemente inferior en las zonas boscosas en comparación con las zonas de pastos. En general, no parece que los windblows (áreas de un bosque donde los árboles han sido abatidos por el viento) y los prados ejerzan influencia alguna sobre las concentraciones de especies, si bien los claros presentan unos índices de Shannon y Eveness más altos y una tendencia a contar con un mayor número de especies. Los campos de heno presentan la incidencia media más alta de las 25 especies comunes y muestran una tendencia general a contar con un número superior de especies y ejemplares, así como unos índices de Shannon más elevados que los prados cubiertos de mantillo. Las antiguas canteras y arenales albergan varias especies notables, algunas de ellas en grandes densidades, lo que pone de relieve el gran valor que este tipo de estructuras desempeñan en la conservación, pese a ser zonas que no suelen tenerse en cuenta al efectuarse mediciones sobre el estado de conservación de la naturaleza.

Palabras clave: Conservación de mariposas, Prados, Windblows, Claros, Canteras, Arenales.

(Received: 19 XII 02; Conditional acceptance: 27 III 03; Final acceptance: 16 V 03) Thomas Schmitt, Inst. für Biogeographie, Fachbereich VI, Wissenschaftspark Trier–Petrisberg, D–54286 Trier, Germany. E–mail: thsh@uni-trier.de

ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

Schmitt

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Introduction Different habitats offer a wide variety of diverse ecological niches. While many animal and plant species have rather limited ecological capacities, many species are restricted to one or a small set of habitats (WEIDEMANN, 1986; EBERT & RENNWALD, 1991; ELLENBERG, 1992; PRIMACK, 1993). Furthermore, many species tolerate only a limited level of human disturbances of their habitats (VAN SWAAY & WARREN, 1999; SWENGEL & SWENGEL, 1999; KITAHARA et al., 2000). This is of special relevance for Central European landscapes where human land–use for several hundreds or even thousands of years replaced the great majority of natural habitats.

However, many of the newly evolved Central European habitats that were extensively managed by men are even richer in species than the natural habitats such as calcareous grasslands (BOURN & THOMAS, 2002; POSCHLOD & WALLISDEVRIES, 2002; VAN SWAAY, 2002; WALLISDEVRIES et al., 2002). On the contrary, the intensively managed landscape evolving during the last few decades is rather impoverished in species if compared to extensively managed habitats (THOMAS 1983, 1984, 1991; ERHARDT, 1985a; KITAHARA & FUJII, 1994; THOMAS & MORRIS, 1994; KITAHARA et al., 2000; LÉON–CORTÉS et al., 1999, 2000; KITAHARA & SEI, 2001).

Butterflies and burnet moths (Lepidoptera: Papilionoidea, Hesperiidae, Zygaenidae) are an important umbrella species group for ecological evaluations on local, regional and interregional scales (e.g. THOMAS, 1984; POLLARD & YATES, 1993; LAUNER & MURPHY, 1994; THOMAS & MORRIS, 1994; SWENGEL & SWENGEL, 1999; WETTSTEIN & SCHMID, 1999; SMART et al., 2000). These insects are very sensitive bio–indicators due to their often highly complex life cycles (EBERT & RENNWALD, 1991; THOMAS, 1991; AKINO et al., 1999; BOUGHTON, 1999; VAN DYCK et al., 2000; HANSKI, 2001; THOMAS & ELMES, 2001; THOMAS et al., 2001). The distribution of many species is rather restricted (VAN SWAAY & WARREN, 1999; KUDRNA, 2002) and a lot of butterfly and burnet moth species are hardly found outside protected areas (e.g. nature reserves). Due to their higher attractiveness to researchers, these habitats are by far more intensively studied than the less species– rich majority of the landscape. Therefore, it is necessary to accumulate more data about non– target areas for nature–conservation measurements, and to analyse the ecological values and interactions between their different habitat types.

This is of enhanced importance because protected areas occupy only a very limited part of the earth’s surface. Therefore, understanding and management of the vast areas outside nature reserves is a key necessity for the conservation of biodiversity on a major scale.

In this study, the butterfly and burnet moth assemblages were analysed at 38 different habitat patches in the “Oettinger Forst” (Southern Germany) to address the following questions: (1)

Are butterflies unequally distributed in the study area? (2) Are the butterfly assemblages of the studied forests less diverse than of the wind blows, mulched meadows and fertilised hay meadows?

(3) Are man–made meadows significantly different from successional wind blows? (4) Are fertilised hay meadows less suitable for butterflies and burnet moths than unfertilised mulched meadows? (5) Are old quarries and sandpits important for the conservation of butterflies?

Material and methods The “Oettinger Forst” in western Bavaria (southern Germany) was selected as study area. This mostly forested area extends as a strip of circa ten kilometres length along a mountain ridge that is the northern boundary of the “Nördliner Ries”. As the altitude in the study area does not exceed 500 m the area has a hilly character. The northern part of the study area is part of the governmental unit of Mittelfranken, and the southern part belongs to Schwaben. The 49th latitude runs through the investigated area.

Forestry has a long tradition in the area and forests extend over more than 80 % of the surface. At least 50 % of these forests are spruce forests. Semi–natural deciduous forests of beech, oak and, at wet places, alder grow on less than 25 % of the surface. There are a lot of meadows: hay meadows, for agriculture and hunting; and mulched meadows (i.e. the grasses and herbs are cut into small pieces (but not removed afterwards) as hunting places —constituting less than 5 % within the forests, but abundant around the forested area. There are also some old quarries and sandpits whose surface may be 1 ‰ of the total area. The meadows were mowed once (partly twice) a year; mowing took place in early summer and, if twice a year, in late spring and late summer. Mulching took place in the second half of summer, mostly in the second half of July. As a result of the strong storms during the last decade, many large clearings in different successional stages exist throughout, maybe representing 10 % to 15 % of the study area. Small swamps often border the numerous traditionally–managed fishponds, but represent considerably less than 1% of the area.

Thirty–eight study plots representing the diversity of the different habitats present were equally distributed over the study area. They included planted coniferous, deciduous and mixed forests, clearings in early and medium successional stages, hay meadows and mulched meadows partly with small fields for game animals and small unmown areas, one swampy unmown maybe natural meadow, one quarry presently in use and two old quarries plus one old sandpit. An overview of the studied patches is given in Appendix 2.

All study patches were investigated during five different study periods during the year 2001 (22–

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24 V; 13–15 VI; 4–6 VII; 23–24 VII; 29–30 VIII).

Transect walks (slow walk, ca. two to three km per hour) were made for 20 minutes per patch per observation period; each butterfly and burnet moth seen within a radius of five meters was recorded. Hereby, a similarly large area (ca. 8,000 to 9,000 m2) of each surveyed patch was studied to achieve a maximum of comparability. Species which cannot be determined while flying were captured with a net and released again after determination. The number of observed individuals had to be estimated in the case of locally rather high densities (e.g. a great number of individuals at a small flowering thistle field). The recordings were performed when the weather was fine (temperature ≥ 18°C, little wind, sunny).

Observations were made between 10:00 and 17:00 hours (sometimes until 18:00 if atmospheric conditions permitted) so that daytime was neither too early nor too late for intensive butterfly activity.

The absolute numbers of observed individuals of butterflies and burnet moths are subject to several factors (e.g. butterfly activity is not constant for all species over the favoured daily flight period, even short cloudy periods have negative impacts on butterfly activity, traceability is not equal for all habitats (e.g. forests and meadows) and depends on vegetation height and density) (cf. POLLARD & YATES, 1993). Therefore, incidence (i.e. presence–absence data) was used for analyses of single species.

Diversity indices were calculated using BioDiversity Professional Beta (LAMBSHEAD et al., 1997). The Shannon indices HS were calculated on the basis of log10.

Eveness ES was based on these log10 Shannon indices. The dispersal ability of the species was rated using the classification of BINK (1992). Bink’s nine dispersal classes were concentrated into three groups: poor (class 1 to 3), medium (class 4 and 5), and good dispersers (class 6 to 9).

Cluster analyses were performed using the UPGMA method. Euclidean distances calculated on single linkage were used. Principal component analysis was done using the varimax factor rotation method. For these two latter analyses, the packet STATISTICA (Stat Soft inc., 1993) was used. As input data for these two analyses, the following data sets were applied (i) presence– absence data, (ii) the frequency of absolute incidences during the five investigation periods and (iii) the number of observed individuals per patch. The cluster analyses were performed (i) for all species observed and (ii) exclusively for the “common species” (i.e. at least 20 individuals observed during the whole observation period).

PCA was done for all observed species including (i) all studied patches, (ii) all studied patches apart from the forested habitats (iii) all wind blows and (iv) all meadows.

Differences between means of numbers of individuals and species, means of incidences and means of diversity and dispersal indices were

tested for significance by U–tests and KruskalWallis ANOVAs for two-tailed tests and by Wilcoxon–tests for pair-wise tests using STATISTICA (Stat Soft inc., 1993). Tests for differences between means of incidences were calculated on the base of the “common species” (i.e. at least 20 individuals observed); “rare species” (i.e. less than 20 individuals observed) were excluded.

The nomenclature of KARSHOLT & RAZOWSKI (1996) was used. In the field, it is not possible to distinguish between L. sinapis and L. reali or between Z. purpuralis and Z. minos. These two sibling species complexes were therefore treated as two morpho–species for the analysis.

Results A total of 42 butterfly and four burnet moth species were recorded for the 38 study patches, representing a total of around 5,000 individuals (see Appendix 1). Of these species, 13 were listed in the Red Data Book of Bavaria (GEYER & BÜCKER, 1992; WOLF, 1992) and 19 in the Red Data Book of Germany (PRETSCHER, 1998), but none in the European Red Data Book (VAN SWAAY & WARREN, 1999).

The butterflies were not equally distributed over the study patches. Focusing on the 25 “common species” (those with at least 20 individuals observed), only four species were more or less equally distributed (A. cardamines, G. rhamni, L. sinapis/reali, A. hyperantus), and occurred at any single patch at less than 10 % of the total number of individuals. On the other hand, seven species (P. brassicae, C. minimus, V. cardui, B. selene, M. galathea, P. aegeria, P. malvae) concentrated more than 20 % of all individuals observed at one single patch. The most extreme cases were B. selene and C. minimus with 63.3 % and 78.8 %, respectively, at their best patch. Furthermore, some of the “rare species” (with less than 20 individuals observed) appeared to occur accumulated (P. machaon 27.8 % of the 18 individuals at the best patch, A. urticae 29.4 % of the 17 individuals, B. dia 61.5 % of the 13 individuals, Z. viciae 23.5 % of the 17 individuals).

Poorly dispersing species were found on average in fewer patches than the medium dispersers, which were found in fewer patches than the good dispersers (10.3 ± 10.2 SD, 15.9 ± 12.5 SD, 20.8 ± 9.4 SD, respectively); however, these differences were only marginally significant (Kruskal–Wallis ANOVA: p = 0.10).

The Shannon indices HS ranged from 0.29 in the coniferous forest F1 to 1.25 in the wind blow C8 (mean: 0.92 ± 0.21 SD). The Eveness ES ranged from 0.60 in the deciduous forest F5 to 0.95 in the coniferous forest F1 (mean: 0.78 ± 0.08 SD).

The hypothesis of question 1 can therefore be accepted. The unequal distribution of butterflies and burnet moths in the study area is the necessary pre–requisite to address the other four questions.

Schmitt

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Forest versus non–forest The mean number of butterfly and burnet moth species was significantly lower in forest patches than in non–forest patches (6.7 ± 2.4 SD, 18.8 ± 4.6 SD, respectively, U–test: p = 0.0002). A similar result was obtained for the mean number of observed individuals (44 ± 23 SD, 178 ± 155 SD, respectively, U–test: p = 0.0015). Also the Shannon indices were significantly lower in the forest than in non-forest patches ( H S : 0.58 ± 0.18 SD, 0.99 ± 0.14 SD, respectively, U–test: p = 0.0002), but there was no significant difference between the means of the Eveness (ES: 0.76 ± 0.14 SD, 0.78 ± 0.07 SD, respectively, U–test: p = 0.66). The patch with the lowest number of individuals was the sole analysed spruce forest F1 where only eleven butterflies belonging to two species were observed during the five visits. In this patch, the lowest Shannon index (HS: 0.29) and the highest Eveness (E S: 0.95) were calculated. The mean incidences of the 25 common species differed significantly between forest and non–forest habitats (0.46 ± 0.83 SD, 1.11 ± 0.71 SD, respectively, Wilcoxon–test: p = 0.0002). A total of 14 of these species showed significant differences (U–tests: p < 0.05): 13 were more common in non–forest patches and only one was more common in forested patches (i.e. P. aegeria). The results for five of these species were significant after Bonferroni correction (L. sinapis / reali, A. levana, A. adippe, P. aegeria, O. sylvanus).

All cluster analyses performed yielded more or less similar results: the investigated forest patches clustered mostly closely together whereas all other patches showed considerably greater differentiations of their butterfly and burnet moths species assemblages, but no reliable differentiation between the different habitat types was found (fig. 1). Furthermore, all principal component analyses separated the forested habitats clearly from the other patches (fig. 2A).

Meadows versus successional patches The non–forest patches can be distinguished into meadows (mown or mulched, in some cases with small fields for game animals) and patches in the process of natural succession (forest clearings, fallow meadows, old and present quarries, old sandpits). The windblows —these clearings were by far the most common successional habitat type of the study area— had a rather similar mean number of individuals as the meadows (185 ± 245 SD, 187 ± 82 SD, respectively, U–test: p = 0.14). However, the mean Shannon indices and Eveness were significantly higher in the wind blows than in the meadows (HS: 1.04 ± 0.11 SD, 0.90 ± 0.15 SD, respectively, U–test: p = 0.027; ES: 0.82 ± 0.06, 0.73 ± 0.06, respectively, U–test: p = 0.0031). Furthermore, the mean number of species trended to be higher in clearings (19.4 ± 4.3 SD, 18.1 ± 5.7 SD, respectively, U–test:

p = 0.76). The mean incidences of the 25 common species did not show a distinct distribution pattern (1.06 ± 0.70 SD, 1.09 ± 0.78 SD, respectively, Wilcoxon–test: p = 0.89), but the incidences of three individual species differed in different habitat types: M. galathea was significantly more often observed in clearings (U–test: p = 0.031) whereas M. jurtina and P. c–album occurred more frequently in meadows (U–test: p = 0.026 and 0.0007, respectively). After Bonferroni correction, only the difference for the third species was significant.

Principal component analyses revealed that the windblows were much more alike than the meadows. With few exceptions, the windblows were nested within the variance breadth of the meadows (fig. 2B).

Within the windblows, the eight of early successional stages had a much broader intervariance than the four of later succession (fig. 2C).

Hay meadows versus mulched meadows In hay meadows, the mean numbers of observed individuals were about 49.7 % higher than in mulched meadows; nevertheless, this difference was not significant (214 ± 63 SD, 143 ± 88 SD, respectively, U–test: p = 0.17). The mean number of species also trended to be higher in hay meadows than in mulched meadows (19.8 ± 5.9 SD, 14.8 ± 5.8 SD, respectively, U–test: p = 0.22). The mean incidences of the 25 common species were significantly higher in the hay meadows (1.19 ± 0.96, 0.78 ± 0.68, respectively, Wilcoxon– test: p = 0.0069), and the incidence of two species differed significantly conforming to the meadow type: P. rapae and P. c–album had higher incidences in mowed meadows (U–test: p = 0.053 and 0.020, respectively), but these were not significant after Bonferroni correction. Principal component analyses supported a weak difference between mulched and fertilised hay meadows, as these were somewhat separated, but there was a great overlap of their variance components (fig. 2D). However, mean Shannon indices and Eveness were similar for the hay and mulched meadows (HS: 0.91 ± 0.18, 0.83 ± 0.09, respectively, U–test: p = 0.33; ES: 0.70 ± 0.07, 0.73 ± 0.06, respectively, U–test: p = 0.46).

Old quarries and sandpits The two old quarries and the old sandpit represent man–made successional habitats with intensive human disturbance in the past. They differ somewhat from all the other investigated habitats in the UPGMA analysis (fig. 1), but were nested within the variance breadth of the meadows in the principal component analyses (fig. 2B).

These three patches trended to a lower mean of observed individuals (150 ± 41 SD) than the non–anthropogenic successional habitats (i.e. windblows: 185 ± 245 SD); nevertheless, this difference was not significant (U–test: p = 0.39). On

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Fig. 1. UPGMA cluster diagram of the differentiation of the butterfly and burnet moth assemblages of the 38 patches using euclidean distances calculated from presence–absence data of all 46 recorded species.

Fig. 1. Diagrama de agrupamiento UPGMA referente a la diferenciación de las concentraciones de mariposas diurnas y zygenas en las 38 parcelas utilizando distancias euclidianas calculadas conforme a los datos de presencia / ausencia de las 46 especies identificadas.

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the contrary, the mean number of species trended to be higher in the two old quarries and the old sandpit than in the clearings (22.0 ± 0.0 SD, 19.3 ± 5.0 SD, respectively, U–test: p = 0.27). Focusing on the individual species, their mean incidences differed significantly between these two habitat types with higher mean incidences in the quarries and the sandpit than in the clearings (1.33 ± 0.88 SD, 1.09 ± 0.70 SD, respectively, Wilcoxon–test: p = 0.041). Four of the 25 common species (L. sinapis / reali, C. minimus, P. c– album, P. aegeria) trended to significantly higher incidences in the quarries and sandpits than in the clearings (U–tests: p < 0.05) , but this was not significant after Bonferroni correction; opposite results were not observed. Of these four species, C. minimus occurred exclusively in the two old quarries, where it was even common. The two single observed individuals of C. rubi and M. athalia were found in the old sandpit. Furthermore, the rare species Z. purpuralis / minos and Z. trifolii were not found in clearings. Mean Shannon indices and Eveness were marginally significantly higher in the old quarries and the sandpit than in the windblows (HS: 1.17 ± 0.04, 1.04 ± 0.11, respectively, U–test: p = 0.051; ES: 0.87 ± 0.03, 0.81 ± 0.06, respectively, U–test: p = 0.083).

Comparing the old quarries and the sandpit not only with the clearings but with all non– forest patches analysed, quite similar results were obtained, but the statistical support was stronger.

Thus, mean Shannon indices and Eveness were significantly higher even after Bonferroni correction in the old quarries and the sandpit than in all the other non-forest patches (HS: 1.17 ± 0.04, 0.97 ± 0.10, respectively, U–test: p = 0.012; ES: 0.87 ± 0.03, 0.77 ± 0.07, respectively, U–test: p = 0.016). In the comparison with all non–forest patches, the difference of mean incidences of C. minimus was significant even after Bonferroni correction (U–test: p < 0.0001).

Discussion Most butterflies and burnet moth species observed are unequally distributed in the “Oettinger Forst”.

This is a frequently observed phenomenon for butterflies (e.g. BOUGHTON, 1999; DENNIS & HARDY, 1999; COWLEY et al., 2000, 2001; GUTIÉRREZ et al., 2001). One important factor is the existence of rather different habitat types, each of which has a great variety of carrying capacities for individual species (i.e. one habitat can be an optimum habitat for one species and unsuitable for another species) (THOMAS et al., 2001). Thus, a landscape can harbour different metapopulation structures for different species and species groups (HANSKI, 1999). The resulting structure is strongly influenced by patch size (e.g. THOMAS et al., 1992; HANSKI, 1994; WETTSTEIN & SCHMID, 1999; SUMMERVILLE & CRIST, 2001), patch quality (e.g. LEÓN–CORTÉS et al., 1999; THOMAS et al., 2001) and connectivity of

patches (e.g. WETTSTEIN & SCHMID, 1999; HADDAD, 2000; THOMAS et al., 2001). Especially for the latter, the dispersal ability of the different species is of great importance. Consequently, good dispersing species had a wider distribution in our study area than the medium dispersers, and poor dispersing species had the most restricted distribution.

Fewer butterflies in forests The contrast between forest and non-forest patches was the most important factor for the unequal distribution of the species. This also answers question 2: the forests investigated were much poorer habitats for the great majority of butterfly species than the windblows and meadows: incidences, number of species and individuals as well as Shannon indices were significantly lower in forests than in non–forests. This might be largely due to a very reduced spectrum of flowers as nectar sources and due to strongly reduced insolation of potential larval habitats.

Similar results are known from other parts of the temperate zone of the northern hemisphere (e.g. ERHARDT, 1985b; KITAHARA & WATANABE, 2001).

Only one of the common species (i.e. P. aegeria) clearly preferred forests as habitat. The ecological demand of this species has been known for a long time and is well documented (WEIDEMANN, 1986; EBERT & RENNWALD, 1991; HILL et al., 1999; ASHER et al., 2001). The deciduous and mixed forests were generally richer in butterflies than the planted coniferous forest studied. This seems to be a more general feature as the same phenomenon has been observed elsewhere, such as in Japan (KITAHARA, 1999, 2000).

Windblows have higher butterfly diversity than meadows Windblows had higher Shannon indices than meadows and showed a trend for higher species numbers. Some species of the German Red Data Book (PRETSCHER, 1998) had strong populations exclusively in the clearings (i.e. B. dia, B. selene) whereas none of the Red Data Book species was frequent in the meadows. The two mentioned Boloria species are typical of sunny forest edges; especially B. dia is characteristic for thermophilous southern slopes in the process of succession (EBERT & RENNWALD, 1991; SETTELE et al., 1999).

This answers question 3: windblows and meadows differ considerably. This is further supported by the principal component analyses, which revealed some weak diversification between these two habitat types. The clearings seem to offer a sufficient amount of habitat necessary to support the survival of most of the species of the non-forest habitats observed in the study area.

The relatively high ecological value of these patches might be due to the relatively high

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0.1

0.3 0.5 Factor 1

0.7

0.9

Fig. 2. Principal Component Analyses of the species compositions (presence / absence data) of: A. All 38 studied patches (the first component explains 32.1 %, the second 19.6 % of the total variance); B. The 32 non–forest patches (the first component explains 30.8 %, the second 22.4 % of the total variance); C. The 13 windblows (the first component explains 36.9 %, the second 24.0 % of the total variance); D. The 15 meadows (the first component explains 31.6 %, the second 26.1 % of the total variance). Abbreviations: ! Forest; +. Windblow (in figure 2C: +. Early succession; %. Medium succession; +. Others); ). Meadow (in figure 2D: #. Hay meadow; ). Mulched meadow; (. Other meadows, sometimes fallow); ". Quarry; #.

Sand pit.

Fig. 2. Análisis de Componentes Principales de la composición de especies (datos de presencia / ausencia) de: A. Las 38 parcelas estudiadas (el primer factor es responsable del 32,1 % de la variación total y el segundo del 19,6 %); B. Las 32 parcelas sin masa forestal (el primer factor es responsable del 30,8 % de la variación total y el segundo del 22,4 %); C. Los 13 windblows (el primer factor es responsable del 36,9 % de la variación total y el segundo del 24,0 %); D. Los 15 prados (el primer factor es responsable del 31,6 % de la variación total y el segundo del 26,1 %). Abreviaturas: !.

Zonas boscosas; +. Windblows (en la figura 2C: +. Sucesión temprana; %. Sucesión media; +.

Otros); ). Prado (en la figura 2D: #. Prado de heno; ). Prado cubierto de paja; (. Otro tipo de prado, a veces tierras en barbecho); ". Cantera; #. Arenal.

Schmitt

58

amount of attractive nectar sources for butterflies and burnet moths such as thistle fields (especially composed of Cirsium arvense) and due to the fact that the flowering vegetation was not removed once or twice a year. Thus, human impact on these patches was less than on most of the meadows.

The other non–forest habitats of the study area maintained by agricultural and hunting activities seemed to be no stimulus for further increases of biodiversity of butterflies and burnet moths. This cannot be explained simply by a generally reduced biodiversity in managed grassland in comparison to successional patches (FRAZER, 1965; S OUTHWOOD & VAN EMDEN, 1967; DEMPSTER, 1971; ERHARDT, 1985a). It is more likely due to the manner and intensity of grassland management. The hay meadows were fertilised so that they were relatively rich in soil nutrients, especially nitrogen. The mulched meadows were also rich in nitrogen as the hay was not removed from these patches so that nitrogen could accumulate. In general, eutrophication changes the plant composition and decreases their species numbers (e.g. NEITZKE, 1991; KAHMEN et al., 2002). While the number of invertebrate species correlates to the number of plant species (cf. STEFFAN–DEWENTER & TSCHARNTKE, 2002), as was also demonstrated for butterflies (STEFFAN–DEWENTER & T SCHARNTKE, 2000), a great number of lepidopterans react negatively and rather sensitively to the eutrophication of their habitats (ERHARDT , 1985a; D ENNIS, 1992; SCHMITT , 1993; OOSTERMIJER & VAN SWAAY, 1998; VAN ES et al., 1998; FISCHER & FIEDLER, 2000). Thus, the enhanced soil-nitrogen values of the fertilised and mulched meadows might explain their relatively low attractiveness for butterflies and burnet moths.

Mowing or mulching?

The unfertilised mulched meadows were less suitable for butterflies and burnet moths than the fertilised hay meadows. The fertilised hay meadows trended to higher numbers of species and individuals, and the mean incidence of the 25 common species was higher, so that question 4, in general, has to be negated for the study area. Principal component analyses also revealed some weak diversification between these two types of meadows. This shows that mulching as performed in the study area in late summer is not enhancing lepidopteran biodiversity in comparison to traditionally managed hay meadows with fertilisation and one (sometimes two) cuts a year. However, there is evidence that mulching twice a year or early in summer reduces soil nitrogen (NEITZKE , 1991; KAHMEN et al., 2002; WALLISD EVRIES et al., 2002) so that in some special cases even this method might be an acceptable tool for conservation measures of meadows.

Of conservation interest: old quarries and sandpits The two old quarries and the old sandpit had significantly higher incidences of butterflies and burnet moth species than the other successional patches (i.e. windblows), and Shannon indices and Eveness were significantly higher than in the other non–forest patches.

Besides, the number of species trended to be higher in these patches, and three species of the German Red Data Book (P RETSCHER , 1998) (i.e. C. minimus , C. rubi , M. athalia ) were only observed in these patches. This positive answer to question 5 underlines the importance of such structures for the conservation of the local biodiversity in a non-target area. Furthermore, such habitats might play a role as stepping–stones in the regional gene flow, especially for poor dispersers like C. minimus (B AGUETTE et al., 2000; COWLEY et al., 2001).

This latter species depended completely on these two old quarries as its single larval foodplant Anthyllis vulneraria only grew in these two places in the study area.

The quarries and the sandpit had formerly been rather strongly modified by human activities. Since their human abandonment, barren flower–rich swards and thistle fields have developed on the exposed nutrient–poor soils.

There is thus the somewhat paradoxical situation that the patches with most intensive human disturbance in the past have now developed, since abandonment, a habitat type that is typical of low human disturbance. At present, these quarries and sandpits are definitively less disturbed by human activities than the mown and mulched meadows, so that these three patches might be functionally similar to unimproved grassland. If we accept this hypothesis, than we can postulate that the higher the degree of human disturbance, the lower the diversity of butterflies and burnet moths in non–forested habitats in the study area. This is a frequently observed phenomenon in a number of other investigations around the world (YAMAMOTO, 1977; RUSZCZYK & DEA RAUJO, 1992; KITAHARA & F UJII, 1994; HILL et al., 1995; KITAHARA et al., 2000; KITAHARA & SEI, 2001).

Acknowledgements I thank the Game Conservancy Deutsch–land and Fürst Oettingen–Spielberg (Oettingen, Germany) for the financial and logistical support that made this investigation possible. Thanks too to Andreas Erhardt (Basel, Switzerland), Masahiko Kitahara (Kenmarubi, Japan), Mechthild Neitzke (Trier, Germany), László Rákosy (Cluj, Romania), Zoltán Varga (Debrecen, Hungary) and two anonymous referees for useful comments on a draft version of this article and Desmond Kime (Linkebeek, Belgium) for the correction of my English.

Animal Biodiversity and Conservation 26.2 (2003)

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Appendix 1. Shannon index, Eveness and number of observed butterflies and burnet moth for all species and patches investigated in the “Oettinger Forst” (Bavaria, Germany) during the five investigation periods in 2001: RDB. Red Data Book [of Germany (G) (PRETSCHER, 1998); of Bavaria (BY) (GEYER & BÜCKER, 1992; WOLF, 1992); Endangered (3); Prewarning list (V)]; T. Total number of observed individuals; P. Total number of inhabited patches.

RDB G BY Shannon index HS Eveness ES Pyrgus malvae (L., 1758) Carterocephalus palaemon (Pall., 1771) Thymelicus lineola (O., 1808) Thymelicus sylvestris (Poda, 1771) Ochlodes sylvanus (Esp., [1778]) Papilio machaon L., 1758 Leptidea sinapis (L., 1758)/reali Reissinger 1989 Anthocharis cardamines (L., 1758) Pieris brassicae (L., 1758) Pieris rapae (L., 1758) Pieris napi (L., 1758) Colias hyale (L., 1758) Gonepteryx rhamni (L., 1758) Lycaena phlaeas (L., 1761) Callophrys rubi (L., 1758) Cupido minimus (Fuessly, 1775) Celastrina argiolus (L., 1758) Aricia agestis ([Den. & Schiff.], 1775) Polyommatus icarus (Rott., 1775) Argynnis paphia (L., 1758) Argynnis adippe ([Den. & Schiff.], 1775) Issoria lathonia (L., 1758) Brenthis ino (Rott., 1775) Boloria euphrosyne (L., 1758) Boloria selene ([Den. & Schiff.], 1775) Boloria dia (L., 1758) Vanessa atalanta (L., 1758) Vanessa cardui (L., 1758) Inachis io (L., 1758) Aglais urticae (L., 1758) Polygonia c-album (L., 1758) Araschnia levana (L., 1758) Melitaea athalia (Rott., 1775) Limenitis camilla (L., 1764) Apatura ilia ([Den. & Schiff.], 1775) Apatura iris (L., 1758) Pararge aegeria (L., 1758) Coenonympha arcania (L., 1761) Coenonympha pamphilus (L., 1758) Aphantopus hyperantus (L., 1758) Maniola jurtina (L., 1758) Melanargia galathea (L., 1758) Zygaena purpuralis (Brünn., 1763) /minos ([Den. & Schiff.], 1775) Zygaena viciae ([Den. & Schiff.], 1775) Zygaena filipendulae (L., 1758) Zygaena trifolii (Esp., 1783) Total

V

V V V

V

V V V V V

3

3

V 3 3 V V 3 V

3 3 V 3 3 V 3 V

3 V V 3

3

T

P

51 80 9 180 362 18 111 103 23 136 943 3 270 13 1 33 11 1 42 48 60 3 2 2 98 13 44 38 465 17 36 276 1 4 1 2 158 6 71 888 334 26

16 23 5 23 34 14 28 27 13 20 38 2 36 10 1 2 8 1 16 19 24 3 1 2 9 4 25 19 31 9 13 30 1 2 1 2 28 5 14 33 25 11

4 17 8 2 5014

2 8 4 2

Forests F1 F2 F3 F4 0.285 0.785 0.684 0.676 0.947 0.869 0.757 0.749 1 3 4 4 1 4 4 19 12 23 12 2 3 3 1 2 1 7 1 1 7 13 1 8 4 2 11

63

23

46

63

Animal Biodiversity and Conservation 26.2 (2003)

Apéndice 1. Índices de Shannon, Eveness y número total de mariposas diurnas y zygenas observado de la totalidad de las especies y parcelas estudiadas en “Oettinger Forst” (Baviera, Alemania) durante las cinco fases del estudio llevadas a cabo en 2001: RDB. Red Data Book [de Alemania (G) (PRETSCHER, 1998); de Baviera (BY) (GEYER & BÜCKER, 1992; WOLF, 1992); En peligro de extinción (3); Lista de preaviso (V)]; Total.

Número total de especímenes observados; Patch. Número total de parcelas con poblaciones de especies.

Forests F5 F6 C1 C2 C3 0.540 0.480 1.089 0.981 0.873 0.598 0.617 0.837 0.815 0.696 2 1 2 3 1 10 7 5 7 37 1 1 8 1 1 2 1 1 19 24 15 2 4 1 4 3 1 6 1 1 1 1 2 1 2 1 1 1 1 1 1 1 16 1 3 3 2 1 2 3 1 27 35 2 1 7 1 3 9 13 30 1 2 1 1 1 2 1 54

67

84

45

105

Windblows C4 C5 C6 C7 C8 C9 C10 C11 1.039 1.133 0.911 1.062 1.252 1.150 0.950 1.034 0.883 0.844 0.875 0.846 0.865 0.804 0.730 0.808 3 1 1 12 2 2 6 1 6 3 1 1 16 24 4 1 1 3 2 9 12 12 36 13 7 1 1 1 1 2 3 4 11 4 4 3 1 4 6 1 9 2 3 3 1 2 1 2 3 23 4 4 5 15 6 9 7 13 19 1 2 9 5 3 9 16 11 3 11 2 1 1 1 1 1 1 1 1 3 1 2 1 1 5 3 1 1 1 1 1 1 4 14 8 1 1 1 5 3 2 2 2 3 2 1 2 6 21 5 10 16 13 4 25 1 2 1 1 3 6 2 3 31 9 6 3 1 1 2 2 3 1 1 1 1 1 4 1 6 13 5 8 19 3 17 45 37 6 2 21 1 1 2 3 6 2 1 1 42

91

60

80

2 1 239

203

104

80

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64

Appendix 1. (Cont.)

Windblows Hay meadows C12 C13 M1 M2 M3 M4 Shannon index HS 1.011 1.025 0.985 1.117 0.979 0.802 Eveness ES 0.840 0.753 0.723 0.799 0.709 0.682 Pyrgus malvae (L., 1758) 1 1 Carterocephalus palaemon (Pall., 1771) 4 6 4 5 4 Thymelicus lineola (O., 1808) Thymelicus sylvestris (Poda, 1771) 2 4 1 7 3 Ochlodes sylvanus (Esp., [1778]) 3 19 8 17 4 3 Papilio machaon L., 1758 1 1 Leptidea sinapis (L., 1758)/reali Reissinger 1989 1 3 3 6 6 2 Anthocharis cardamines (L., 1758) 1 1 2 7 9 4 Pieris brassicae (L., 1758) 3 2 1 2 Pieris rapae (L., 1758) 5 4 2 15 Pieris napi (L., 1758) 4 34 45 48 89 124 Colias hyale (L., 1758) 1 Gonepteryx rhamni (L., 1758) 3 20 16 14 1 13 Lycaena phlaeas (L., 1761) 1 1 Callophrys rubi (L., 1758) Cupido minimus (Fuessly, 1775) Celastrina argiolus (L., 1758) 2 1 2 Aricia agestis ([Den. & Schiff.], 1775) Polyommatus icarus (Rott., 1775) 1 2 2 1 Argynnis paphia (L., 1758) 2 2 1 6 Argynnis adippe ([Den. & Schiff.], 1775) 8 1 2 1 1 Issoria lathonia (L., 1758) 1 Brenthis ino (Rott., 1775) 2 Boloria euphrosyne (L., 1758) Boloria selene ([Den. & Schiff.], 1775) 10 62 3 Boloria dia (L., 1758) 3 Vanessa atalanta (L., 1758) 1 1 1 7 Vanessa cardui (L., 1758) 1 3 2 1 Inachis io (L., 1758) 4 40 30 17 13 28 Aglais urticae (L., 1758) 1 1 Polygonia c-album (L., 1758) 4 1 5 7 Araschnia levana (L., 1758) 12 3 5 37 25 5 Melitaea athalia (Rott., 1775) Limenitis camilla (L., 1764) Apatura ilia ([Den. & Schiff.], 1775) Apatura iris (L., 1758) Pararge aegeria (L., 1758) 10 2 7 Coenonympha arcania (L., 1761) Coenonympha pamphilus (L., 1758) 6 1 Aphantopus hyperantus (L., 1758) 14 50 1 29 35 45 Maniola jurtina (L., 1758) 1 3 45 21 30 21 Melanargia galathea (L., 1758) 1 Zygaena purpuralis (Br端nn., 1763) 3 /minos ([Den. & Schiff.], 1775) Zygaena viciae ([Den. & Schiff.], 1775) 1 1 4 Zygaena filipendulae (L., 1758) Zygaena trifolii (Esp., 1783) 1 Total 63 276 188 237 258 272

M5 0.659 0.611 3 1 4 7 53 1 4 1 1 3 1 37 116

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Animal Biodiversity and Conservation 26.2 (2003)

Mulched meadows M6 M7 M8 M9 0.928 0.711 0.864 0.828 0.739 0.787 0.654 0.673 4 2 1 1 2 7 1 34 19 2 13 8 1 5 2 2 3 5 7 1 1 33 2 1 26 15 6 3 1 1 4 2 2 1 1 1 1 1 1 1 25 4 2 4 1 3 27 1 9 1 1 5 6 1 7 63 10 80 73 3 37 1 209

20

1 1 206

155

M10 0.964 0.754 2 4 15 3 10 1 2 55 3 1 1 5 3 1 15 2 13 6 39 181

Other meadows Quarries and sandpits M11 M12 M13 M14 M15 Q1 Q2 Q3 S1 0.954 1.083 0.799 0.943 1.034 0.973 1.150 1.145 1.208 0.760 0.795 0.741 0.751 0.841 0.827 0.857 0.853 0.900 1 1 3 9 2 3 4 9 3 5 1 2 1 13 5 14 23 2 3 10 6 19 12 8 11 20 11 1 1 1 1 1 8 2 4 5 5 10 4 1 9 2 3 2 3 2 1 2 22 21 2 1 5 9 3 20 68 52 14 24 11 14 20 9 3 7 18 15 7 5 3 5 13 2 2 1 26 7 2 8 1 6 2 7 3 8 4 2 1 2 4 6 2 5 1 2 3 1 1 2 1 3 1 1 2 1 4 1 1 8 1 1 27 15 50 5 40 11 10 1 5 4 1 3 6 23 4 7 8 5 6 9 1 3 2 2 2 5 1 2 1 2 7 7 7 35 35 30 68 15 5 13 37 13 46 4 7 8 20 18 1 7 1 119

295

140

1 220

100

112

3 3 1 143

4 3 194

113

Schmitt

66

Appendix 2. Description of the 38 habitat patches in the study area “Oettinger Forst” (Bavaria, Germany).

Apéndice 2. Descripción de las 38 parcelas del área de estudio "Oettinger Forst" (Baviera, Alemania).

N

Size (ha) Habitat description

F1

> 10

Coniferous forest of Picea abies trees mostly older than 50 years, few grassy patches with very few flowering plants

F2

> 10

Humid mixed forest mostly composed of Picea abies trees of all age classes but also some Fagus, Betula and Alnus trees; several small ponds and sunny patches, Molinia caerulea abundant

F3

> 10

Humid mixed forest mostly with Pinus sylvestris trees (> 50 years), some Betula trees of different ages; many sunny areas and abundant grassy patches often dominated by Molinia caerulea

F4

1–2

Humid deciduous forest composed of alder, beech and oak trees, more than 50, often more than 100 years old; some grassy patches and few flowering plants

F5

> 10

Deciduous forest composed of beech and oak trees, some few spruce trees, trees more than 50, often more than 100 years old; some sunny grassy patches with flowering plants and some blackberry shrubs; Lonicera and Lilium martagon common

F6

> 10

Beech forest with trees of 80 years and more; only few grassy patches and rather few flowering plants

C1

2–5

Small windblows in a humid mixed forest (F2) often with Agrostis stololifera and Digitalis purpurea, at wet patches Molinia caerulea; some of the clearings in rather early succession, but the majority with buckthorn bushes

C2

5–10

Windblow in early successional stage with Digitalis purpurea and Atropa bella–donna quite common; within the forest

C3

1–2

Wet windblow with many deep puddles, in early successional stage, Digitalis purpurea common, some Cirsium palustre; flanking a little lake; within the forest

C4

> 10

Windblow in early successional stage, Digitalis purpurea common; flanking a little lake; within the forest

C5

> 10

Windblow in early successional stage, Digitalis purpurea common, some blackberry shrubs especially along forest roads; flanking a little lake and a small water course; within the forest

C6

1–2

Windblow in early successional stage, Digitalis purpurea and Calamagrostis epigejos common; within the forest

C7

> 10

Windblow in early successional stage, some deep puddles and humid area, larger areas with bare ground, Digitalis purpurea common; at the forest edge

C8

> 10

Windblow in early successional stage, Digitalis purpurea common, some flower rich patches along a forest road with blackberry shrubs, some humid areas; at the forest edge

C9

> 10

Windblow in early successional stage, very diverse vegetation structure from patches with bare ground to high growing meadow like structures, on a warm southern slope; at the forest edge

C10

2–5

Windblow in medium successional stage with Calamagrostis epigejos, Rubus fruticosus agg, Digitalis purpurea and some Betula shrubs; within the forest

C11

1–2

Windblow in medium successional stage with abundantly growing little spruce trees, Digitalis purpurea and Calamagrostis epigejos common; within the forest

C12 5–10

Windblow in medium successional stage, many young spruce trees and blackberry shrubs, Calamagrostis epigejos abundant; within the forest

C13

Windblow in medium successional stage with abundant buckthorn bushes and large thistle field (mostly Cirsium arvense) on a warm southern slope; within the forest

2–5

Animal Biodiversity and Conservation 26.2 (2003)

Appendix 2. (Cont.)

N

Size (ha) Habitat description

M1

2–5

Fertilised hay meadow (mown once a year) with Arrhenatherum elatius as dominant grass and with a thistle field of Cirsium arvense which was mown only in late summer; small humid edge with Filipendula ulmaria; within the forest

M2

2–5

Fertilised hay meadow (mown once a year) with a greater variety of grass and herb species, one part mostly with Urtica dioica and Cirsium arvense; part with Iris sibirica not mown; within the forest

M3

> 10

Fertilised hay meadow, mostly mown once a year, partly twice, sectors mowed at different times; Holcus lanatus as dominant grass; at the forest edge

M4

2–5

Fertilised hay meadow (mown once a year); Arrhenatherum elatius as dominant grass; one small edge with several Cirsium species remained not mown; at the forest edge

M5

> 10

Fertilised hay meadow (mown twice a year), Arrhenatherum elatius dominant; at the forest edge

M6

1–2

Mulched meadow, rather eutrophic so that Urtica dioica was partly dominant, some flowering plants at the edges (e.g. Cirsium palustre); within the forest

M7

<1

Mulched meadow, mostly grassy vegetation (e.g. Calamagrostis epigejos, Agrostis stololifera); within the forest

M8

~1

Mulched meadow, partly fresh (e.g. Cirsium arvense common), partly humid (e. g.

Scirpus sylvaticus common); at the forest edge

M9

1–2

Mulched and partly unmown meadow, the latter with many plants of Urtica dioica and generally high growing vegetation; within the forest

M10 1–2

Complex of fresh mulched and unmown humid meadow (the latter rather high growing with Cirsium palustre, Urtica dioica, Phalaris arundinacea) as well as a small field for game animals (cultivation of Sinapis); within the forest

M11 1–2

Partly mown (once a year) fresh and partly not mown humid meadow (Equisetum sylvaticum, Phalaris arundinacea, Scirpus sylvaticus, Iris pseudacorus and Lysimachia thyrsiflora common) and a small field for game animals (cultivation of Sinapis); within the forest

M12 2–5

Hay meadow (mown once a year) with small field for game animals; within the forest

M13 1–2

Unfertilised hay meadow (mown once a year) with mostly barren vegetation and a small field for game animals; a little water course within the patch, joined by Cirsium palustre; within the forest

M14 2–5

Fallow meadow in medium successional stage with blackberry shrubs and some young spruce trees, Calamagrostis epigejos common; one larger thistle field (mainly Cirsium arvense); within the forest

M15 < 1

Not mown humid, high growing meadow; Phalaris arundinacea, Scirpus sylvaticus and Iris pseudacorus common; within the forest

Q1

2–5

Recent quarry with spontaneous vegetation (especially Cirsium arvense) and a lot of bare ground; within the forest

Q2

<1

Old quarry with barren flower–rich grassland; Anthyllis vulneraria was quite common in the grassland, some initial Betula shrubs; within the forest

Q3

<1

Old quarry with barren flower–rich grassland (comparable to Q2 but smaller and less barren), a thistle field (mainly Cirsium arvense) and Betula shrubs; within the forest

S1

~1

Old sandpit in medium successional stage but still large areas of uncovered ground, some rather humid areas and a pond, at some patches Cirsium arvense, C. vulgare, Digitalis purpurea and Cytisus scoparius abundant, some blackberry shrubs; within the forest

67

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 26.2 (2003)

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Dos nuevas especies y una subespecie de campodeidos cavernícolas de la cornisa cantábrica (Diplura, Campodeidae) A. Sendra, J. Mª Salgado & E. Monedero

Sendra, A., Salgado, J. Mª & Monedero E., 2003. Dos nuevas especies y una subespecie de campodeidos cavernícolas de la cornisa cantábrica (Diplura, Campodeidae). Animal Biodiversity and Conservation, 26.2: 69–80.

Abstract Two new species of cave–dwelling campodeids of the Cantabrian Cornice (Diplura, Campodeidae).— A total of 139 specimens of campodeid diplurans, collected from 27 caves of Cantabrian Cornice (Spain) are studied and two new species and one subspecies are described: Podocampa asturiana n. sp., Podocampa asturiana riberiensis n. ssp. and Litocampa zaldivarae n. sp. P. asturiana n. sp. differs from its most closely related species, P. group fragiloides (an endogean species) by troglomorphic characters; P. asturiana riberiensis n. ssp. is distinct from the type species by the number of trochanteral bacilliform sensilla; and L. zaldivarae n. sp. is easely recognized from Litocampa espanoli by the number of macrochaetae posterior lateral in IV urotergite. These new discoveries show the value and diversity of this family of apterygote insects in the Cantabrian subterranean environment.

Key words: Diplura, Campodeidae, Cantabrian Cornice, Spain, Taxonomy, Cave–dwelling.

Resumen Dos nuevas especies y una subespecie de campodeidos cavernícolas de la cornisa cantábrica (Diplura, Campodeidae).— Se han estudiado un total de 139 ejemplares de dipluros campodeidos, recolectados en 27 grutas de la cornisa cantábrica y se han descrito dos nuevas especies y una subespecie: Podocampa asturiana sp. n., Podocampa asturiana riberiensis ssp. n. y Litocampa zaldivarae sp. n. P. asturiana sp. n. difiere de la especie más próxima, Podocampa grupo fragiloides (una forma de hábitat endógeo), por características relacionadas con su facies cavernícola; P. asturiana riberiensis ssp. n. difiere de la especie tipo por el número de sensilos baciliformes trocanterales; y L. zaldivarae sp. n. es fácilmente distinguible de Litocampa espanoli por el número de macroquetas laterales posteriores del IV uroterguito. Estos nuevos hallazgos indican la riqueza y diversidad de esta familia de insectos apterigotos en el medio subterráneo cantábrico.

Palabras clave: Diplura, Campodeidae, Cornisa cantábrica, España, Taxonomía, Fauna cavernícola.

(Received: 31 VII 02; Conditional acceptance: 27 III 03; Final acceptance: 5 VI 03) Alberto Sendra & Emilio Monedero, Museu Valencià d’Història Natural (Fundación Entomológica Torres Sala), Paseo de la Pechina 15, 46008 Valencia, España (Spain). E–mail: Alberto.Sendra@uv.es J. Mª Salgado, Dept. de Biología Animal, Univ. de León, 24071 León, España (Spain). E–mail: dbajsc@unileon.es

ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

Sendra et al.

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Introducción La primera aportación al conocimiento taxonómico de los campodeidos cavernícolas de la cornisa cantábrica y de toda la península ibérica, se debe al Dr. B. CONDÉ (1949), con la descripción de Litocampa espanoli Condé, 1950, tras el estudio de una hembra capturada por los entomólogos españoles F. Español y R. Zariquiey en la cueva de Mañaria (Vizcaya). Seis años más tarde, en la que representa la obra más completa sobre la sistemática de los dipluros campodeidos, CONDÉ (1956) da a conocer otra nueva especie, Podocampa simonini Condé, 1956, descubierta en dos grutas bastante próximas, la cueva de Hernialde (localidad típica) y la cueva de Mendikute, ambas en la provincia de Guipúzcoa. Pasarán más de veinticinco años hasta que de nuevo CONDÉ (1982), fije su atención en los campodeidos cavernícolas de la cordillera cantábrica, en un trabajo en el que amplía el área de distribución de Litocampa espanoli, y describe un nuevo género y nueva especie, Oncinocampa falcifer Condé, 1982, de la cueva de la Marniosa (Santander), lo que va a otorgar un gran interés biogeográfico a esta región peninsular. Algunos años más tarde, en dos trabajos de SENDRA & CONDÉ (1988) y BARETH (1989), ambos publicados sin conocer sus autores el descubrimiento de sus colegas, se describen dos nuevas especies de Oncinocampa, O. asonensis Sendra & Condé, 1988, hallada en cinco cavidades cerca de la región de Asón, entre los valles de Miera y Soba, y O. genuitei Bareth, 1989, encontrada en la sima Trave, en el macizo central de los Picos de Europa.

En los últimos años, una laboriosa tarea de muestreo, en más de un centenar de cavidades de la cornisa cantábrica, ha permitido ampliar y conocer mejor la diversidad y vasta distribución de los dipluros campodeidos en el medio subterráneo. En el presente trabajo, se describen las tres novedades taxonómicas descubiertas: dos especies y una subespecie nuevas, dejando para un trabajo posterior la relación faunística de todas las formas conocidas, su variabilidad así como una discusión sobre la colonización de la península ibérica.

Material y métodos Los 139 ejemplares examinados han sido montados, tras un lavado con agua destilada, entre porta y cubre con Medio de Marc André II, para posteriormente ser conservados en una mezcla de agua destilada con propilen glicol–fenoxetol.

Su examen se realizó bajo un microscopio Leica DMLS, con contraste de fases y los dibujos realizados con la ayuda de un tubo de dibujo 1x.

Las medidas fueron tomadas con ayuda de un ocular micrométrico. Para la longitud corporal (LC) se midieron los ejemplares montados in toto desde los extremos del proceso frontal de la cabeza al de la válvula supranal del abdomen. Para evitar

los errores ocasionados por la contracción del cuerpo que sufren los ejemplares durante el proceso de montaje, se adoptó como estimador de la longitud total del cuerpo el LCT o sumatorio de las longitudes de cabeza, pronoto, mesonoto y metanoto (SENDRA, 1988). El LCT se mide de la siguiente forma: desde la base de la macroqueta distal del proceso frontal al final del borde posterior de la cápsula cefálica, para la cabeza, y desde la base de las macroquetas mediales anteriores hasta las bases de las sedas marginales posteriores, para cada uno de los notos torácicos.

Resultados

Podocampa asturiana sp. n.

Material típico Holotipo: cueva Campanas, Mestas de Con, T. M. de Cangas de Onís, Asturias, 30T UP 377002, 3 IX 1987, J. M. Salgado y D. Rodríguez leg. Macho de 8.9 mm, montado para su observación en el medio de Marc André II y conservado en fenoxietilen–glicol (nº 651), depositado en el Museu Valencià d´Historia Natural (Fundación Entomológica Torres Sala).

Paratipos: Principado de Asturias: cueva del Aspro, Aballe, Término Municipal de Cangas de Onís, Asturias, 30T UN 253991, 5{ 4} 1 juvenil.

20 IX 1997, J. M. Salgado leg.; cueva Campanas, Mestas de Con, T. M. de Cangas de Onís, Asturias, 30T UP 377002, 13{ 8}, 3 IX 1987, J. M. Salgado y D. Rodríguez leg.; cueva Les Canales, Veneros, T. M. de Caso, Asturias, 30T UN 113828, 1{, 3 X 1988, 1{, 1 VII 1989, J. M. Salgado y D. Rodríguez leg.; cueva Canellón, Collado de Andrín, T. M. Cangas de Onís, Asturias, 30T UN 266977, 1{, 4}, 12 V 1999, J. M. Salgado y D. Rodríguez leg.; cueva Cantiellu, Covadonga, T. M. de Cangas de Onís, Asturias, 30T UN 345975, 4{ 3}, 12 V 1997, J. M. Salgado y D. Rodríguez leg.; cueva Cardanoriu, Teleña, T. M. de Cangas de Onís, Asturias, 30T UN 341991, 1{ 1}, 26 IX 1998, J. M. Salgado y D. Rodríguez leg.; cueva La cueva, Lago, T. M. de Cangas de Onís, Asturias, 30T UP 236007, 2} 16 VII 1994, J. M. Salgado y D. Rodríguez leg.; cueva Cuevona, Labra, T. M. de Cangas de Onís, Asturias, 30T UP 339035, 2{ 1}, 9 V 1998, J. M. Salgado y D. Rodríguez leg.; cueva de La Curva, Coballes, T. M. de Caso, Asturias, 30T UN 067851, 2{ 4}, 20 V 1989, J. M. Salgado leg.; cueva del Foyu, Pando–Ribadesella, T. M. de Ribadesella, Asturias, 30T UP 289139, 3{ 1}, 9 IX 1995, J. M. Salgado y D. Rodríguez leg.; cueva de Mazaculos, La Franca, T. M. de Ribadedeva, Asturias, 30T UP 728049, 1{ 3}, 16 IX 1995, J. M. Salgado y D. Rodríguez leg.; cueva Pitufos o de la Carretera, Bodes, T. M. de Parres, Asturias, 30T UP 217089, 3}, 17 IX 1988, 1{ 1}, 13 V 1989, J. M. Salgado y D. Rodríguez leg.; cueva Pradón, Collia, T. M. de Parres, Asturias, 30T UP 222087, 1{, 23 V 1993, J. M. Salgado y D. Rodríguez leg; cue-

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va del Soto, Bodes, T. M. de Parres, Asturias, 30T UP 219095, 9{ 11}, 4 sexo?, 11 VII 1988, J. M. Salgado y D. Rodríguez leg.; cueva Les Xianes "A", La Piñera–Sevares, T. M. de Piloña, Asturias, 30T UP 154036, 1}, 29 VI 1996, J. M. Salgado y D. Rodríguez leg.; cueva del Xunes, Vis, T. M. de Amieva, Asturias, 30T UN 289951, 1{ 2}, 20 V 2000, J. M. Salgado y D. Rodríguez leg.; sumidero Linde–Bobia, Bobia, T. M. de Onís, Asturias, 30T UN 3999, 2{ 1}, 13 VIII 1978, O. Escolà leg.

Total: 103 ejemplares, 48{ 50} 1 juvenil y 4 ejemplares sin diferenciación de sexo, conservados entre porta y cubre con medio de Marc André II o en tubos de cristal con fenoxietilen– glicol, depositados en el Museu Valencià d’Historia Natural (Fundación Entomológica Torres Sala), Museu de Ciències Naturals de Barcelona, Museo Nacional de Ciencias Naturales de Madrid y Museo de Historia Natural de Ginebra (Departamento de Artrópodos e Insectos II).

Etimología El nombre específico hace referencia al Principado de Asturias, región muy rica en cavidades, donde han sido descritas numerosas especies exclusivas del medio hipógeo.

Longitudes Cuerpo de 5,1 a 8,9 mm (machos); 5,7 a 9,3 mm (hembras).

Tegumentos Epicutícula sin ornamentación. Las sedas de revestimiento de la cara tergal están desnudas o con 1 ó 2 bárbulas distales; las marginales posteriores son robustas y un poco barbadas.

Cabeza Antenas intactas con 35 a 43 antenómeros (tabla 1). El III antenómero es tan largo como ancho, con macroquetas casi completamente desnudas.

El sensilo del III antenómero (fig. 6 A) es grueso de aspecto bananiforme, con frecuencia engrosado en su mitad distal, y ocupa una posición laterotergal (entre las macroquetas b y c). Los antenómeros siguientes son más alargados, dos veces más largos que anchos. El antenómero apical es más de 2 veces tan largo como ancho; el órgano cupuliforme ocupa 1/6 de la longitud total del artejo y encierra 7 u 8 sensilos, cada uno con 2 a 3 collaretes. Los sensilos en gubia aumentan progresivamente desde 1 ó 2 unidades en el III antenómero, hasta los 18 sensilos, distribuidos en un solo verticilo, en los antenómeros distales.

Los palpos labiales son subovalares, con su sensilo latero–externo ligeramente bananiforme y con los 2 cortos pelos acompañantes; la parte anterior lleva de 8 a 16 sedas ordinarias; la media y posterior está cubierta por 140 a 180 sedas sensoriales. El sensilo del palpo maxilar es tan largo como el labial, pero más corto que el del III antenómero.

Tabla 1. Antenas completas, al parecer no regeneradas de Podocampa asturiana sp. n.: L. Localidades (CCp. Cueva Campanas; CA. Cueva Aspro; CCn. Cueva Cantiellu; CCv. Cueva Cuevona; CX. Cueva Les Xianes "A"); LC. Longitud corporal, en mm; LCT. Suma de las longitudes de la cabeza, pronoto, mesonoto y metanoto, en µ; A. Antena (D. Derecha; I. Izquierda); Ant. Antenómeros; LA. Longitud de las antenas, en mm; H. Holotipo.

Table 1. Complete antennae, not apparently regenerated from Podocampa asturiana n. sp.: L. Localities (CCp. Campanas cave; CA. Aspro cave; CCn. Cantiellu cave; CCv. Cuevona cave; CX. Les Xianes "A" cave); LC. Body length, in mm; LCT. Sum length head, pronotum, mesonotum and metanotum, in µ; A. Antenna (D. Right; I. Left); Ant. Antennomeres; LA. Antennae length, in mm; H. Holotype.

{ { {

L

LC

LCT

A

CCp

6,2

1705

CA CA

5,9 7,4

1810 1840

Ant

LA

D

37

5,0

I

36

4,3

D

43

6,7

I

40

7,7

D

38

7,8

}

CCn

7,6

1865

I

39

6,55

}

CCn

5,5

2010

I

38

5,6

}

CCp

8,4

2040

D

37

6,0

}

CCv

7,2

2050

I

40

7,0

D

38

7,3

}

CA

7,9

2050

D

42

7,8

I

41

7,9

{

CCp

7,4

2075

I

35

6,1

{

CA

7,8

2085

D

43

8,55

}

CCp

9,3

2120

D

37

6,05

I

35

6,1

D

38

7,4

H

CCp

8,9

2165

I

39

7,5

}

CA

7,5

2190

I

39

7,95

}

CX

7,1

2250

I

37

7,25

El proceso frontal lleva tres macroquetas, la anterior más larga que las dos posteriores (170 µ / 132 µ, hembra de 9,3 mm); la anterior revestida con unas pocas bárbulas sobre su 1/3 y las posteriores sobre la 1/2 distal. Las macroquetas que bordean la línea de inserción de las antenas están barba-

Sendra et al.

72

das sobre su 1/2 distal y las sedas x sobre su 1/3 distal (a = 132 µ, i = 158 µ, p = 118 µ, x = 102 µ; hembra de 9,3 mm).

Las macroquetas occipitales dorsales están poco diferenciadas, a excepción de las más próximas a la sutura ecdisial, que son un poco más largas, robustas (148 µ, hembra de 9,3 mm) y barbadas en su mitad distal.

Tórax Las macroquetas tergales son robustas y largas, en especial las laterales posteriores, y todas finamente barbadas sobre su 1/2 distal (tabla 2). Las sedas marginales más próximas a las macroquetas son largas, robustas y finamente barbadas sobre la 1/2 a los 2/3 distales.

La patas son largas; las metatorácicas llegan a alcanzar el extremo posterior del VII segmento. El fémur III lleva una macroqueta dorsal, de 385 µ en el holotipo, inserta a los 460 µ del extremo proximal del fémur (longitud del fémur = 1.040 µ, holotipo).

La macroqueta ventral es un poco más corta (370 µ) y está inserta a los 605 µ. Estas dos macroquetas están barbadas sobre su 1/2 distal. Las tibias I a III llevan 1, a veces 2, macroquetas ventrales, cortas y barbadas sobre la 1/2 distal; los calcares poseen

algunas bárbulas desde la base. El tarso lleva las dos hileras de sedas ventrales desnudas, como sucede con las tres sedas subapicales del extremo distal del tarso. Uñas subiguales simples (fig. 1), ligeramente y gradualmente curvadas, con los procesos laterales del telotarso sediformes o un poco laminados en su extremo distal y desnudos Abdomen Repartición de las macroquetas tergales (tabla 3, fig. 2).

Todas las macroquetas dorsales son robustas y barbadas sobre la 1/2 distal. Las macroquetas laterales anteriores (275–300 µ) son más cortas que las laterales posteriores (375–410 µ). Los pleuritos II a VII llevan una seda diferenciada y barbada en la mitad distal. El uroesternito I lleva 7+7 macroquetas bien diferenciadas, con largas bárbulas; los uroesternitos II a VII presentan 4 + 4 macroquetas con largas bárbulas y, el uroesternito VIII contiene 1 + 1 macroquetas.

La seda apical de los estilos posee 2 dentículos basilares y unas 4 a 6 bárbulas distales. La seda subapical posee 2 ó 3 bárbulas mediales y la mediana esternal es bifurcada, a veces, con alguna bárbula suplementaria.

Tabla 2. Repartición de las macroquetas y sus longitudes relativas en Podocampa asturiana sp. n.: L. Localidades (CA. Cueva Aspro; CF. Cueva Foyu; SLB. Sumidero Linde Bobia; CCp. Cueva Campanas; CP. Cueva Pitufos; CCn. Cueva Cantiellu); LC. Longitud corporal; LCT. Suma de las longitudes de la cabeza, pronoto, mesonoto y metanoto, ma. Macroqueta medial anterior; la. Macroqueta lateral anterior; lp. Macroqueta lateral posterior; sm. Longitud media de las tres sedas marginales más próximas a las macroquetas laterales posteriores; juv. Juvenil. (Todas las longitudes en µ a excepción de LC en mm) Table 2. Distribution of macrochaetae and their relative lengths in Podocampa asturiana n. sp.: L. Localities (CA. Aspro cave; CF. Foyu cave; SLB. Linde Bobia sink; CCp. Campanas cave; CP. Pitufos cave; CCn. Cantiellu cave); LC. Body length ; LCT. Sum length head, pronotum, mesonotum and metanotum; ma. Anterior medial macrochaeta; la. Anterior lateral macrochaeta; lp. Posterior lateral macrochaeta; sm. Mean length of the three marginal setae closest to the posterior lateral macrochaetae; juv. Juvenile. (All lengths in µ except LC in mm.)

Pronoto L

LC

LCT

ma

la

lp

Mesonoto sm

ma

la

lp

Metanoto sm

ma

lp

sm

-

87

juv. CA

3,55

980

165

140

280

102

175

200

290

107

195

{

CF

5,65

1650

300

245

425

197

300

330

425

215

330

410 145

{

CA

5,7

1750

300

255

425

193

280

310

-

198

300

410 145

}

SLB

5,8

1790

280

260

445

192

310

330

460

212

325

435 197

}

CCp

8,3

2060

325

265

420

212

335

325

425

218

345

}

CP

8,4

2130

350

270

450

220

360

350

450

233

365

440 192

}

CCp

7,9

2130

305

310

435

207

345

345

435

220

335

410 170

}

CCp

9,2

2190

320

275

440

220

327

345

450

235

395

440 183

}

CCn

6,9

2275

345

300

440

260

355

375

485

265

380

-

190

}

CCp

9,3

2340

345

275

450

227

345

365

450

240

-

-

-

-

177

73

Animal Biodiversity and Conservation 26.2 (2003)

sda III

sdp

sl

400 µ

ssa

IV

s

lp

100

µ

V

Fig. 1. Podocampa asturiana sp. n. Uñas y procesos laterales del telotarso del III par de patas de una hembra de 5,9 mm de la cueva Campanas (no figuran las sedas ordinarias ni las dos hileras de sedas esternales): sda.

Seda subapical dorsal anterior; sdp. Seda subapical dorsal posterior; sl. Seda subapical lateral; ssa. Seda subapical esternal.

Fig. 1. Podocampa asturiana n. sp. Claws and lateral setae of III pair of legs of a 5.9 mm female from Campanas cave (ordinary setae and two rows of sternal setae are not represented): sda. Dorsal anterior subapical seta; sdp . Posterior subapical seta; sl. Lateral subapical seta; ssa.

Sternal subapical seta.

Tabla 3. Repartición de las macroquetas urotergales de Podocampa asturiana sp. n: la.

Macroqueta lateral anterior; lp. Macroqueta lateral posterior; mp. Macroqueta medial posterior.

Table 3. Distribution of urotergal macrochaetae from Podocampa asturiana n. sp.: la. Lateral anterior macrochaeta; lp.

Lateral posterior macrochaeta; mp. Medial posterior macrochaeta.

Uroterguito III IV V–VII VIII IX

lp

la 0 0 1+1 0 0

lp mp 1+1 0 2+2 0 2+2 0 3+3 1+1 6+6 (total)

la

s

lp

s

lp

Fig. 2. Podocampa asturiana sp. n. Uroterguitos III a V de una hembra de 5,8 mm del sumidero Linde–Bobia: la. Macroqueta lateral anterior; lp. Macroqueta lateral posterior; s. Sensilo sediforme.

Fig. 2. Podocampa asturiana n. sp. III to V urotergites from a 5.8 mm female from Linde– Bobia sink: la. Anterior lateral macrochaeta; lp. Posterior lateral macrochaeta; s. Setaceous sensillum.

Cercos (fig. 3) Los cercos están incompletos en los adultos, sus fragmentos más largos corresponden al holotipo y una hembra de cueva Campanas (tabla 4). En éstos, los artejos proximales llevan 3 ó 4 verticilos de largas macroquetas barbadas en su mitad distal, acompañados por 1 ó 2 verticilos de finas sedas largas y desnudas. El número de verticilos aumenta progresivamente hacia los artejos distales, pasando a tener 5 ó 6 verticilos de macroquetas y 3 ó 5 verticilos de finas sedas largas. Cada uno de los artejos finaliza en un verticilo de cortas sedas desnudas.

Macho (fig. 4) El uroesternito I lleva sobre el margen posterior más de 200 sedas glandulares g1 sobre 5 a 6 hileras, precedidas por tres hileras de sedas cortas. Los apéndices son gruesos, de aspecto globoso a subtrapezoidal; en su borde posterior llevan más de 150 sedas a1, distribuidas en 3 a 6 hileras, precedidas por un campo glandular de más de un centenar de delgadas sedas a2.

Sendra et al.

74

Hembra (fig. 5) Los apéndices del uroesternito I son subcilíndricos, con un campo apical de unas cuarenta sedas glandulares a1, precedidas por una treintena de delgadas sedas a2.

Afinidades En la península ibérica el género Podocampa podría ser dividido en dos grupos de especies, unas que poseen macroquetas mediales anteriores urotergales, Podocampa con ma, y otras que no las presentan, Podocampa sin ma. Se conocen tres especies, habitantes del medio edáfico, del grupo de Podocampa sin ma: Podocampa grupo fragiloides, Podocampa moroderi Silvestri, 1932 y Podocampa cardini Silvestri, 1932; sin olvidar a Podocampa jorgei Wygodzinsky, 1944 y Podocampa seabrai Wygodzinsky, 1944 que deberían ser consideradas como simonías de P. grupo fragiloides (SENDRA, 1988). Este grupo de especies posee en común, por una parte, un tamaño corporal y número de antenómeros algo superior al de otras especies que viven en el suelo, y por otra, suelen hallarse en lugares permanentemente húmedos (laderas arcillosas cerca de fuentes, márgenes de los cursos de agua,...), características todas ellas que nos sugieren una cierta preadaptación al medio subterráneo, donde ocasionalmente han sido citadas (CONDÉ, 1956: 109; SENDRA, 1988: 235 y 236).

En 1956, CONDÉ describe por primera vez una forma cavernícola del grupo de Podocampa sin ma.

Se trata de Podocampa simonini Condé, 1956, hallada en dos grutas de los Montes Vascos. La distribución de las macroquetas laterales anteriores y posteriores de P. simonini es idéntica a la de P. moroderi, diferenciándose de esta última por el mayor tamaño de su cuerpo, el alargamiento de los apéndices, un número muy superior de antenómeros (hasta 64 en P. simonini y hasta 33 en P. moroderi) y un mayor número de sensilos en el órgano cupuliforme. Si se compara Podocampa asturiana sp. n. con P. grupo fragiloides se observa un caso similar al acabado de describir. P. asturiana sp. n. difiere de P. grupo fragiloides por poseer un mayor tamaño corporal (5,1 a 9,3 mm de P. asturiana sp. n., frente a 2,7 a 4,4 mm de P. grupo fragiloides), un número más elevado de antenómeros (36 a 39 antenómeros en P. asturiana sp. n. y un máximo de 30 en P. grupo fragiloides), mayor número de sensilos en el órgano cupuliforme (ocho o más en P. asturiana sp. n. pero sólo cuatro en Podocampa grupo fragiloides) y, por último, forma y tamaño de los cercos (éstos son más largos que la longitud total del cuerpo, con un recubrimiento de macroquetas y sedas largas en P. asturiana sp. n., bien distintos de los que posee la forma tipo de P. fragiloides).

Todas estas características diferenciales entre P. asturiana sp. n. y Podocampa grupo fragiloides pueden ser consideradas como apomorfías típicas de un campodeido de vida cavernícola y deberán ser objeto, en un futuro, de un estudio profundo en cuanto a su variabilidad y, por tanto, validez taxonómica.

Tabla 4. Cercos completos, al parecer no regenerados de Podocampa asturiana sp. n., ejemplar juvenil de cueva del Aspro, longitud total del cuerpo 3,55 mm: B. Base; Ci. Cerco izquierdo; Cd. Cerco derecho; LT. Longitud total de los cercos. (Todas las medidas en µ.)

Table 4. Complete cerci, not apparently regenerated from Podocampa asturiana n. sp., juvenile especimen of Aspro cave, total body length: 3.55 mm: B. Base; Ci. Left cercus; Cd. Right cercus; LT. Total cerci length.

(All measurements in µ.)

B

1º

2º

3º

4º

5º

6º

LT

Ci 700 325 440 560 725 775 780 4305 Cd 675 320 445 550 725 780 825 4320

Podocampa asturiana riberiensis ssp. n.

Material típico Holotipo: cueva de la Minona, Llandillena, T. M. de Ribera de Arriba, Asturias, 30T TN 686964, 18 VI 1988, J. M. Salgado y D. Rodríguez leg.

Hembra de 8,5 mm, montada para su observación en el medio de Marc André II y conservada en fenoxietilen–glicol (nº 551), depositada en el Museu Valencià d´Historia Natural (Fundación Entomológica Torres Sala).

Paratipos: Principado de Asturias: cueva La Cuevona, Llandillena, T. M. de Ribera de Arriba, Asturias, 30T TN 699976, 2{ 1}, 23 IV 1988, J. M. Salgado y D. Rodriguez leg.; cueva del Escobiu, Soto de Ribera, T. M. de Ribera de Arriba, Asturias, 30T TN 685983, 3{ 3}, 16 VII 1988, J. M. Salgado leg.; cueva de la Minona, Llandillena, T. M. de Ribera de Arriba, Asturias, 30T TN 686964, 1{ 2}, 18 VI 1988, J. M. Salgado y D. Rodriguez leg.

Total: 13 ejemplares 6{ y 7}, conservados entre porta y cubre con medio de Marc André II o en tubos de cristal con fenoxietilen–glicol, depositados en el Museu Valencià d’Història Natural (Fundación Entomológica Torres Sala), Museu de Ciències Naturals de Barcelona, Museo Nacional de Ciencias Naturales de Madrid y Museo de Historia Natural de Ginebra (Departamento de Artrópodos e Insectos II).

Etimología El nombre subespecífico hace referencia al término municipal de las tres cavidades donde se encuentra esta nueva subespecie.

Longitudes Cuerpo de 7,5 a 8,8 mm (machos); 7,8 a 9,6 mm (hembras).

75

Animal Biodiversity and Conservation 26.2 (2003)

A

base

1º

a1 2º

a2 g1

9º

B

200

µ

Fig. 4. Podocampa asturiana sp. n. Uroesternito I de un macho de 5,6 mm del sumidero Linde–Bobia.

10º

400

Fig. 4. Podocampa asturiana n. sp. First urosternite from a 5.6 mm male from Linde– Bobia sink.

µ

Fig. 3. Podocampa asturiana sp. n., holotipo: A. Primer artejo del cerco izquierdo, vista tergal; B. Décimo artejo del cerco izquierdo, vista tergal.

Fig. 3. Podocampa asturiana n. sp., holotype: A. First segment of the left cercus, tergal view; B. Tenth segment of the left cercus, tergal view.

a2

200

µ

a1

Cabeza Una sola antena, al parecer intacta, de 34 antenómeros (hembra de 9,6 mm, LCT: 438 µ). El III antenómero es un poco más largo que ancho, con un sensilo baciliforme (fig. 6B) en posición latero– esternal (entre la macroquetas d y e), y con las macroquetas desnudas. El proceso frontal no sobresale entre las bases de las antenas.

Fig. 5. Podocampa asturiana sp. n. Uroesternito I de una hembra de 5,8 mm del sumidero Linde–Bobia.

Fig. 5. Podocampa asturiana n. sp. First urosternite from a 5.8 mm female from Linde–Bobia sink.

76

Tórax Las macroquetas tergales son largas y robustas, con sedas marginales largas y barbadas. Todas las patas poseen al menos un sensilo trocanteral baciliforme, pero más frecuentemente 2, 3 ó incluso 4 sobre un mismo trocánter (fig. 6C).

Abdomen La repartición de las macroquetas urotergales es mostrada en la tabla 5.

Todas las macroquetas son robustas y barbadas sobre su tercio o mitad distal. Las macroquetas laterales anteriores (170–179 µ holotipo) son más cortas que las macroquetas laterales posteriores (255–276 µ, holotipo).

El uroesternito I de los machos lleva, sobre su margen posterior, hasta 280 sedas glandulares g1 distribuidas en 6 a 7 hileras, precedidas por 3 ó 4 hileras de sedas cortas. Los apéndices son gruesos, de forma subtrapezoidal y su borde posterior lleva unas 60 sedas glandulares a1, distribuidas en 2 ó 3 hileras, precedidas por una campo glandular de un centenar de delgadas sedas a2.

Los apéndices del uroesternito I de las hembras son subcilíndricos con un campo apical con hasta 38 sedas glandulares a1, precedidos por unas 40 sedas glandulares a2, más delgadas.

Afinidades El material estudiado procede de tres grutas, próximas entre sí, ubicadas en una misma región kárstica de Ribera de Arriba en la Cuenca Central Asturiana. La homogeneidad observada en los caracteres taxonómicos ha permitido proponer una nueva subespecie Podocampa asturiana riberiensis ssp. n., que difiere de la forma tipo por la presencia de macroquetas laterales anteriores en el uroterguito IV y la constante existencia, en cada artejo trocanteral de las patas, de 2 a 4 sensilos baciliformes.

Litocampa zaldivarae sp. n.

Material típico Holotipo: cueva Comparado, Cubillos del Rojo, T. M. de Soncillo, Burgos, 30T VN 4355, 6 XI 1983, A. Zubiaga, C. Prieto y P. Zaldivar leg. Hembra de 6,25 mm, montada para su observación en el medio de Marc André II y conservada en fenoxietilen– glicol (nº 540), depositada en el Museu Valencià d´Historia Natural (Fundación Entomológica Torres Sala).

Paratipos: Castilla y León: cueva de los Bloques, Urría, T. M. de Medina de Pomar, Burgos, 30T VN 6243, 2{ 2}, 22 VIII 1982, 1{ 5}, 30 VI 1985, A. Zubiaga, C. Prieto y P. Zaldívar leg.; cueva Comparado, Cubillos del Rojo, T. M. de Soncillo, Burgos, 30T VN 4355, 1} 2 juveniles, 6 XI 1983, A. Zubiaga, C. Prieto y P. Zaldivar leg.; sima Cova–Negra, Cubillos del Rojo, T. M. de. Soncillo, Burgos, 30T VN 4255, 1}, 15 III 1984, 1{ 1} 1 juvenil, 11 VIII 1985, P. Zaldivar leg.; cueva de Ojo Guareña o de San Bernabé,

Sendra et al.

Quisicedo, T. M. de Sotoscueva, Burgos, 30T VN 4665, 2}, 27 VIII 1968, M. Romero leg.; cueva Covarrubias, Aleje, T. M. de Crémenes, León, 30T UN 269474, 2}, 23 IX 1974, J. M. Salgado leg. Cantabria: cueva San Esteban, Pesquera, T. M. de Bárcena de Pie de Concha, 30T VN 1169, 1}, 3 VI 1989, J. M. Salgado leg.

País Vasco: cueva Mina de Zamundi, Baracaldo, Vizcaya, 30T VN 994886, 2}, 8 XII 1986, C. Prieto leg.

Total: 23 ejemplares 3{ 17} y 3 juveniles, conservados entre porta y cubre con medio de Marc André II o en tubos de cristal con fenoxietilen–glicol, depositados en el Museu Valencià d’Historia Natural (Fundación Entomológica Torres Sala), Museu de Ciències Naturals de Barcelona, Museo Nacional de Ciencias Naturales de Madrid y Museo de Historia Natural de Ginebra (Departamento de Artrópodos e Insectos II).

Etimología Se ha querido dedicar esta nueva especie a Pilar Zaldivar (Grupo Espeleológico Niphargus, Burgos), a modo de agradecimiento a su persona como a la de todos aquellos espeleólogos que con su desinteresado esfuerzo han contribuido al conocimiento de la fauna, en un entorno tan fascinante y a la vez arriesgado como son las cuevas y simas de la cornisa cantábrica.

Longitudes Cuerpo de 3,4 a 4,85 mm (machos); 2,8 a 6,8 mm (hembras); 2,8 mm (juvenil).

Tegumentos Epicutícula sin ornamentación. Sedas de revestimiento de la cara tergal desnudas; las sedas marginales son más largas y desnudas o barbadas sobre su 1/2 distal en el caso de las situadas en los márgenes de las más laterales.

Cabeza Antenas de 30 a 33 antenómeros (tabla 6). El III antenómero es un poco más largo que ancho, con un sensilo ligeramente claviforme (fig. 7A), en posición latero–esternal (entre d y e ), y macroquetas desnudas salvo las latero-internas, que llevan de 1 a 4 bárbulas. Los antenómeros siguientes son más alargados, casi dos veces más largos que anchos. El antenómero apical es más de dos veces más largo que ancho; el órgano cupuliforme encierra de 4 a 6 gruesos sensilos.

Los sensilos en gubia aparecen a partir del III antenómero, uno sólo y más corto que los restantes, y aumentan en número hasta una docena distribuidos en un verticilo distal.

Los palpos labiales son subovalares, con un sensilo latero–externo baciliforme, muy similar al sensilo del palpo maxilar (figs. 7B y 7C); la porción anterior lleva de 10 a 12 sedas ordinarias y la porción posterior está cubierta por 150 a 200 sedas sensoriales.

El proceso frontal es saliente pero corto y lleva las 3 macroquetas típicas, la anterior más larga que las posteriores con 1 a 3 bárbulas. Las macroquetas que bordean la línea de inserción de

77

Animal Biodiversity and Conservation 26.2 (2003)

C

A

100

B

µ

Fig. 6. A. Podocampa asturiana sp. n., sensilo del III antenómero de una hembra de cueva Campanas. B. Podocampa asturiana riberiensis ssp. n., sensilo del III antenómero de una hembra de cueva de la Minona. C. Podocampa asturiana riberiensis ssp. n., sensilos del trocanter de la pata III de una hembra de cueva de la Minona.

Fig. 6. A. Podocampa asturiana n. sp., sensillum from antennomere III from a female of Campanas cave. B. Podocampa asturiana riberiensis n. ssp., antennomere III sensillum of a female from Minona cave. C. Podocampa asturiana riberiensis n. ssp., trochanteral sensilla of leg III from a female of Minona cave.

Tabla 5. Repartición de las macroquetas urotergales de Podocampa asturiana riberiensis ssp. n.: la. Macroqueta lateral anterior; lp. Macroqueta lateral posterior, mp. Macroqueta medial posterior; * 1+0 en una hembra de cueva Cuevona.

Table 5. Distribution of urotergal macrochaetae of Podocampa asturiana riberiensis n. ssp.: la.

Anterior lateral macrochaeta; lp. Posterior lateral macrochaeta; mp. Posterior medial macrochaeta; * 1+0 in a femela from Cuevona cave.

Uroterguito III IV V–VII VIII IX

la 0 1+1* 1+1 0 0

lp mp 1+1 0 2+2 0 2+2 0 3+3 1+1 6 + 6 (total)

las antenas (a = 98 µ i = 138 µ, p = 111 µ) llevan de 2 a 7 bárbulas sobre su mitad distal; las sedas x son un poco más cortas y están desnudas o con sólo una bárbula apical. Todas las macroquetas occipitales se hallan poco diferenciadas, son desnudas o llevan de 1 a 5 bárbulas distales.

Tórax Las macroquetas son robustas y largas, barbuladas sobre su mitad distal, con distribución y tamaños mostrados en la tabla 7. Las sedas marginales son largas, desnudas o barbadas desde su mitad distal, y siempre diferenciadas de las sedas ordinarias.

Las macroquetas laterales posteriores metanotales son ligeramente más cortas que las mesonotales.

Las patas son largas y las metatorácicas llegan a alcanzar el extremo posterior del VII segmento. El fémur III lleva la macroqueta dorsal (195 µ, holotipo) inserta a los 302 µ del extremo proximal de la longitud total del fémur (611 µ, en el holotipo). La macroqueta ventral es un poco más corta (177 µ) y está inserta a los 340 µ del extremo proximal del fémur. Las dos macroquetas, dorsal y ventral, son largas y barbuladas sobre sus 2/3 distales. Las tibias I a III llevan 1 macroqueta ventral corta y bifurcada, o con 1 a 4 bárbulas distales (2 macroquetas ventrales en la hembra de mayor tamaño de la cueva San Esteban). Los calcares llevan largas bárbulas desde su base. El tarso posee dos hileras ventrales de sedas, con unas pocas bárbulas sobre su mitad proximal. Todas las sedas subapicales del extremo del tarso son desnudas.

Las uñas subiguales (fig. 7D) son acodadas y finamente estriadas transversalmente, con crestas laterales sin ornamentación tergal. Los procesos laterales del telotarso son sediformes y desnudos.

Abdomen La repartición de las macroquetas tergales del abdomen se muestran en la tabla 8.

Sendra et al.

78

D

siempre en cada artejo por 1 a 5 verticilos de sedas largas y desnudas, más el característico verticilo apical de sedas cortas. Este número de verticilos aumenta progresivamente desde los artejos proximales a los distales.

sdp sda

Afinidades Los ejemplares de Litocampa zaldivarae sp. n. se diferencian de la especie más afín, Litocampa espanoli, por el número de macroquetas laterales posteriores del IV uroterguito (2+2 lp en L. zaldivarae sp. n.; 1+1 lp en L. espanoli). Sin embargo, este carácter por sí solo no justificaría la A

B

C 50

µ

Fig. 7. Litocampa zaldivarae sp. n., holotipo: A. Sensilo del III antenómero; B. Sensilo del palpo labial; C. Sensilo del palpo maxilar; D. Uñas y procesos telotarsales del III par de patas. (Abreviaturas: sdp. Seda subapical dorsal posterior; sda. Seda subapical dorsal anterior.)

Fig. 7. Litocampa zaldivarae n. sp., holotype: A. Sensillum from antennomere III; B. Sensillum of labial palp; C. Sensillum of maxillar palp; D. Claws and telotarsal setae of III pair of legs.

(Abbreviations: sdp. Dorsal posterior subapical seta; sda. Anterodorsal subapical seta.)

Todas las macroquetas dorsales están bien desarrolladas, son largas y barbadas desde su 1/3 a 2/3 distales.

El uroesternito I lleva 7 + 7 macroquetas bien diferenciadas con largas bárbulas; los uroesternitos II a VII presentan 4 + 4 macroquetas, con largas bárbulas; el uroesternito VIII posee 1 + 1 macroquetas.

La seda apical de los estilos posee 2 dientes en la base y de 4 a 5 bárbulas distales; la seda subapical es casi desnuda, con sólo alguna minúscula bárbula en su mitad y la seda mediana esternal está bifurcada.

El uroesternito I de los machos alberga en su margen posterior un campo glandular de hasta unas 120 sedas g1, distribuidas en 2 ó 3 hileras; los apéndices están ensanchados en su extremo distal con hasta 20 sedas glandulares a1 y unas 20 a2. Las hembras presentan hasta 16 sedas glandulares a1 y 25 a2.

Cercos Se han examinado dos cercos completos de 7 y 10 artejos, el más corto es posiblemente regenerado (tabla 9). Revestimiento formado por macroquetas largas, barbadas desde su mitad a un tercio distal y ordenadas desde 5 a 8 verticilos, acompañadas

Tabla 6. Antenas completas, al parecer no regeneradas de Litocampa zaldivarae sp. n.: L. Localidades (CCv. Cueva Covanegra; CBl. Cueva Bloques; CMZ. Cueva mina Zamundi); LC. Longitud corporal, en mm (? No medible); LCT. Suma de las longitudes de la cabeza, pronoto, mesonoto y metanoto, en µ; A. Antena (I. Izquierda; D. Derecha); Ant. Antenómeros; LA. Longitud de la antena, en mm; juv. Juvenil.

Table 6. Complete antennae, not apparently regenerated from Litocampa zaldivarae n. sp.: L. Localities (CCv. Covanegra cave; CBl. Bloques cave; CMZ. Zamundi cave mine); LC. Body length, in mm (? Not measurable); LCT. Sum length head, pronotum, mesonotum and metanotum, in µ; A. Antenna (I. Left; D. Right); Ant. Antennomeres; LA. Antennae length, in mm; juv. Juvenile.

L }

LC

LCT

A

Ant

LA

CCv

3,0

765

I

32

2,35

juv. CCv

2,8

825

I

32

2,5

D

33

2,55

I

31

2,15

D

31

2,45

I

31

2,6

D

31

2,5

I

30

2,1

D

31

2,4

I

31

2,65

D

31

2,5

}

CCv

2,9

?

}

CBl

3,7

1040

}

CBl

3,6

1075

}

CBl

3,7

1180

} {

CMZ CBl

3,55 4,85

1215 1390

I

33

3,15

D

33

3,3

I

30

2,7

D

31

2,4

}

CBl

4,8

1410

I

31

2,7

{

CCv

4,2

1425

D

33

3,4

79

Animal Biodiversity and Conservation 26.2 (2003)

Tabla 7. Repartición de las macroquetas y sus longitudes relativas en Litocampa zaldivarae sp. n.: L. Localidades (CCv. Cueva Covanegra; CBl. Cueva Bloques); LC. Longitud corporal; LCT. Suma de las longitudes de la cabeza, pronoto, mesonoto y metanoto; ma. Macroqueta medial anterior; la.

Macroqueta lateral anterior; lp. Macroqueta lateral posterior; sm. Longitud media de las tres sedas marginales más próximas a las macroquetas laterales posteriores; juv. Juvenil. (Todas las longitudes en µ, a excepción de LC en mm.)

Table 7. Macrochaetae distribution and their relating lengths in Litocampa zaldivarae n. sp.: L. Localities (CCv. Covanegra cave; CBl. Bloques cave); LC. Body length; LCT. Sum length head, pronotum, mesonotum and metanotum; ma. Anterior medial macrochaeta; la. Anterior lateral macrochaeta; lp. Posterior lateral macrochaeta; sm. Mean length of three marginal setae closest to posterior lateral macrochaetae; juv. Juvenile. (All lengths in µ, except LC in mm.)

Pronoto juv } }

L CCv CBl CBl

LC 2,8 3,6 5,75

LCT 825 1075 1415

ma 88 142 123

la 95 145 150

lp 175 228 248

Mesonoto sm 78 133 135

Table 8. Urotergal macrochaeta distribution from Podocampa zaldivarae n. sp.: la.

Anterior lateral macrochaeta; lp. Posterior lateral macrochaeta; mp. Posterior medial macrochaeta. la 0 0 1+1 0 0

la 128 175 178

lp 182 238 248

sm 75 143 120

ma 85 118 128

lp sm 168 79 225 124 225 110

separación. A él se añaden otras diferencias significativas como son: el menor tamaño corporal, las macroquetas tergales desarrolladas pero no robustas, los apéndices más cortos, un menor número de antenómeros y un número muy reducido de sensilos en el órgano cupuliforme (tan sólo de 4 a 6 sensilos).

L. zaldivarae n. sp. solapa su área de distribución con L. espanoli, en la cueva mina Zamundi. Pero es probable que L. zaldivarae se extienda más allá de las grutas, a través del medio subterráneo superficial, por toda la mitad oriental de los montes cantábricos. Un argumento a favor de esta hipótesis radica en el paralelismo observado con otros Litocampa morfológicamente similares (número reducido de antenómeros, apéndices poco alargados y sólo cuatro sensilos en el órgano cupuliforme), como Litocampa vandeli Condé, 1947 y Litocampa cognata Condé, 1948, hallados en grutas y en el medio subterráneo superficial de la cordillera pirenaica (B ARETH, 1983).

Tabla 8. Repartición de la macroquetas urotergales de Podocampa zaldivarae sp. n.: la. Macroqueta lateral anterior; lp. Macroqueta lateral posterior; mp. Macroqueta medial posterior.

Uroterguito III IV V–VII VIII IX

ma 105 140 143

Metanoto

lp mp 1+1 0 2+2 0 2+2 0 3+3 1+1 6+6 (total)

Tabla 9. Cercos completos, al parecer no regenerados de Litocampa zaldivarae sp. n. } de 6,8 mm de longitud y LCT 1838 µ, procedente de la cueva San Esteban: B. Base; Cd. Cerco derecho; Ci. Cerco izquierdo; LT. Longitud total de los cercos. (Todas las medidas en µ.)

Table 9. Complete cerci, not seemingly regenerated in Litocampa zaldivarae n. sp. } of 6.8 mm length and 1838 µ LCT, from San Esteban cave: B. Base; Cd. Right cercus; Ci. Left cercus; LT. Total cerci length. (All measurements in µ.)

B

1

2

3

4

5

6

7

Cd

604

491

566

792

943

1245

1453

1717

Ci

943

321

498

574

623

705

830

876

8

9

10

LT 7811

906

981 1026

8283

Sendra et al.

80

Conclusión Las siete especies y una subespecie de campodeidos cavernícolas de la cornisa cantábrica pueden dividirse en dos grandes grupos monofiléticos (CONDÉ, 1982; SENDRA, 1988): Podocampoide y Taquicampoide.

Los Podocampoide comprenden un reducido número de especies de los géneros Podocampa y Litocampa (este último en sentido restringido, con sólo las especies que llevan una macroqueta tergal en el fémur), que en el área de estudio están representados por cuatro especies y una subespecie. En la cordillera cantábrica, los representantes del género Podocampa ocupan las grutas de la región asturiana hasta la sierra de Cuera (Podocampa asturiana sp. n. y Podocampa asturiana riberiensis ssp. n.), pero sin adentrarse en el área kárstica de los Picos de Europa. Es aquí donde pasa a ser sustituido por Litocampa, que ocupa la región cantábrica (L. espanoli y L. zaldivarae sp. n.). En los Montes Vascos vuelve a reaparecer Podocampa, pero con una especie bien distinta: P. simonini.

Los Taquicampoide, no examinados en el presente trabajo, están representados por el género Oncinocampa. Poseen una distribución más limitada, ocupando algunas cavidades del la franja central de la cordillera cantábrica, de una parte, en los Picos de Europa (O. falcifer y O. genuitei) y, de otra, en la región de Asón (O. asonensis).

Agradecimientos En primer lugar debemos agradecer la aportación de los siguientes entomólogos o espeleólogos, en esta labor de capturas de campodeidos en las grutas de la cornisa cantábrica, muy especialmente a D. Rodríguez que acompañó al Dr. Salgado en multitud de muestreos en busca de fauna cavernícola; de igual modo nuestro sincero agradecimiento al Dr. Prieto (Universidad

del País Vasco), P. Zaldivar, M. Romero, A. Subyaga, y a O. Escolà, y en su nombre al Museu de Ciències Naturals de Barcelona, que recolectaron y nos ofrecieron sus valiosos ejemplares.

En otros aspecto de nuestro trabajo, queremos igualmente hacer extensivo nuestro agradecimiento a la Dra. Planelles por sus precisas correcciones del manuscrito. Cabe por último mencionar el constante apoyo económico recibido de la Fundación Entomológica Torres Sala (Museu Valencià d’Història Natural), en éste y en anteriores trabajos.

Referencias BARETH, C., 1983. Diploures Campodéidés du milieu souterrain superficiel de la region Ariegeoise.

Mém. Bioespéologie, X: 67–71.

– 1989. Une nouvelle espece d’Oncinocampa recoltee dans une grotte des Picos de Europa (Nord de l’Espagne): Oncinocampa genuitei n.sp.

(Insecta, Apterygota, Campodeidae). Mém.

Biospéologie, XVI: 131–134.

CONDÉ, B., 1949. Description préliminaire d’un Campodéidé cavernicole du Pays basque espagnol. Bull. Mus. natn. Hist. nat., Paris, 2ª sér., 21(5): 569–573.

– 1956. Matériaux pour une Monographie des Diploures Campodéidés. Mém. Mus. natn. Hist. nat. Paris, s. A. Zool., 12: 1–202.

– 1982. Un extraordinaire Campodéidé troglobie des Picos de Europa (Santander), Espagne.

Revue suisse Zool., 88(3): 775–786.

SENDRA, A., 1988. Taxonomía, Filogenia y Biogeografía de la Fauna de campodeidos Ibérica, Balear y Canaria (Hexapoda, Diplura, Campodeidae). Tesis doctoral, Universidad de Valencia.

S ENDRA , A. & CONDÉ , B., 1988. Une nouvelle espèce d’ Oncinocampa Condé de grottes des Montes Cantábricos de Santander, Espagne (Insecta, Diplura). Revue suisse Zool ., 95(4): 1019–1026.

Animal Biodiversity and Conservation 26.2 (2003)

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Game species: extinction hidden by census numbers J. Carranza, J. G. Martínez, C. B. Sánchez–Prieto, J. L. Fernández–García, B. Sánchez–Fernández, R. Álvarez–Álvarez, J. Valencia & S. Alarcos

Carranza, J., Martínez, J. G., Sánchez–Prieto, C. B., Fernández–García, J. L., Sánchez–Fernández, B., Álvarez– Álvarez, R., Valencia, J. & Alarcos, S., 2003. Game species: extinction hidden by census numbers. Animal Biodiversity and Conservation, 26.2: 81–84.

Abstract Game species: extinction hidden by census numbers.— Management of game species may involve a risk of alteration of their genetic properties. Local adaptations may be disrupted if artificially selected individuals from farms or those belonging to distant geographical areas are introduced to increase population density or trophy “quality”. In Spain, red deer (Cervus elaphus) from different European subspecies have been introduced to increase the size of trophies (antlers) of local populations. Legislation against these introductions is not effective for various reasons, and once the individuals are in the Iberian peninsula it is virtually impossible to prevent their spreading throughout the whole territory without a genetic tool to distinguish between autochthonous and foreign specimens. We have developed such a genetic test and propose a strategy to dissuade land–owners from importing foreign deer. Since deer are bred mainly for their antlers, our strategy is based on an agreement with the National Trophy Body in Spain which rejects trophies from foreign populations. Rejection decreases the value of the trophy so that it becomes more profitable to produce autochthonous deer. Using such a strategy at some critical step in the production or commercialization process may be a good model to apply in protecting genetic properties of exploited species.

Key words: Game species, Red deer, Genetic variability, Hybridization, Conservation, Trophy.

Resumen Especies de caza: procesos de extinción ocultos tras elevados tamaños de censo.— La gestión de las especies de caza puede conllevar riesgos de alteración de sus propiedades genéticas. Las adaptaciones locales pueden deteriorarse si ejemplares producidos mediante selección artificial en granjas o procedentes de áreas geográficas distantes, son introducidos para aumentar la densidad poblacional o la "calidad" de los trofeos de caza. En España, se han introducido ejemplares de ciervo ibérico (Cervus elaphus) procedentes de distintas subespecies europeas para aumentar así el tamaño de las cuernas (trofeos de caza) de las poblaciones autóctonas. La legislación contra este tipo de introducciones no es eficaz por diversos motivos y, una vez introducidos los ejemplares en la península ibérica, es prácticamente imposible prevenir su dispersión por todo el territorio sin contar con herramientas genéticas que permitan diferenciar los ejemplares autóctonos de los foráneos. Nosotros hemos desarrollado un test genético para este fin, y hemos propuesto una estrategia para disuadir a los propietarios de llevar a cabo la importación de ejemplares foráneos. Puesto que los ciervos se crían fundamentalmente por su cornamenta como trofeo de caza, nuestra estrategia se ha basado en un acuerdo con la Junta Nacional de Homologación de Trofeos de Caza, para que ésta rechace los trofeos pertenecientes a ejemplares foráneos. Este rechazo reduce el valor de los ejemplares procedentes de otras poblaciones y favorece la producción de ciervo autóctono. Sugerimos que la utilización de estrategias de este tipo en puntos clave de procesos de producción o comercialización, puede ser un buen modelo a aplicar para proteger las propiedades genéticas de las especies sujetas a explotación por el hombre.

Palabras clave: Especies de caza, Ciervo ibérico, Variabilidad genética, Híbridos, Conservación, Trofeos cinegéticos.

(Recieved: 9 IV 03; Conditional acceptance: 10 VI 03; Final acceptance: 10 VII 03) ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

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Carranza et al.

J. Carranza, C. B. Sánchez–Prieto, B. Sánchez–Fernández, R. Álvarez–Álvarez, J. Valencia & S. Alarcos, Cátedra de Biología y Etología, Fac. de Veterinaria, Univ. de Extremadura, 10071 Cáceres, España (Spain).

J. G. Martínez, Dept. de Biología Animal y Ecología, Fac. de Ciencias, Univ. de Granada, 18071 Granada, España (Spain).

J. L. Fernández–García, Dept. de Zootecnia, Fac. de Veterinaria, Univ. de Extremadura, 10071 Cáceres, España (Spain).

Corresponding author: J. Carranza

Animal Biodiversity and Conservation 26.2 (2003)

In many natural areas, hunting is a traditional economic activity that may be fully compatible with conservation of autochthonous game if sustainable management practices are established.

However, in view of the fact that many game species have a wide distribution and large populations, it is often considered that hunting and other related management practices can be continued without the need to take ecological and genetic parameters into account. Indeed, the growing economic interest in hunting promotes practices that aim to increase census size as well as to improve (from a human point of view) some of the animal traits, but such measures may endanger the conservation of other natural features of the species or populations. A good example of this is the risk of hybridization after individuals are released into natural populations for hunting purposes.

In general, hybridization as the result of human release of farm–reared individuals or exotic species or subspecies is a serious conservation problem, particularly among exploited animal species. The generally negative consequences of hybridization have been widely acknowledged and reviewed (R HYMER & S IMBERLOFF , 1996; A LLENDORF et al., 2001), and are related to the reduction of fitness in hybrids, the distortion of the genetic structure of populations and the disruption of locally co–adapted gene complexes. Hatchery–reared fishes, such as the Iberian brown trout are a clear example. The introduction of hatchery trout is genetically homogenising the populations in the Iberian peninsula, distorting ancestral patterns of genetic variation (M ACHORDOM et al., 1999). Further examples can be seen in farm–reared game species. It is simple and frequent practice on farms to hybridise different subspecies, artificially selecting individuals with the desired phenotypes (see www.universalgamefarm.com or www.suwanneeriverranch.com). After their release, they may genetically contaminate the locally–adapted wild populations with foreign or artificially–selected genotypes. Farm deer, for instance, are selected for release into natural populations for hunting purposes according to antler size, as larger antlers represent more highly valued trophies. As a consequence of this practice, throughout Europe autochthonous deer are hybridising with released specimens which may be foreign or artificially–selected. This may account for the hybrid red deer subspecies, originally occurring in Central Europe, which clearly jeopardises the genetic integrity of each subspecies. Although it is important, this problem is more easily overlooked than the case of hybrids arising from the introduction of exotic species or their escape from farms or enclosures, as in the case of the introgression of sika deer ( Cervus nippon ) genes into the gene pool of native Scottish red deer ( Cervus

Forum – 83

elaphus; G OODMAN et al., 1999), or the hybridization between white–tailed deer ( Odocoileus virginianus ) and mule deer ( Odocoileous hemionus ), or between exotic red deer and elk ( Cervus canadensis ) in some areas of the United States (D ERR , 1991, O N TARIO F EDERATION OF A NGLERS AND H UNTERS , 1991).

The problem affecting European red deer has already reached the Iberian subspecies ( Cervus elaphus hispanicus ). Deer with larger antlers are more profitable for owners of hunting estates, which encourages them to introduce specimens from other European subspecies into their properties. The introduced individuals can reproduce and hybridise with local deer, and are permitted to be moved within Spain and Portugal. On some estates, nonautochthonous deer have intentionally been hybridised with Iberian species under controlled conditions, and hybrids may be purchased by other estates to “improve” the quality of the trophies in their populations. This practice represents a silent but true extinction risk for the Iberian red deer subspecies.

After hunting a big stag, the trophy class is determined from a rate table based mainly on antler size and width and number of tines. Trophies are ranked and given prizes (gold, silver and bronze medals). The ranking of trophies is controlled by the Spanish Trophy Measurement Body (Junta Nacional de Homologación, JNH), which depends on the Ministry of the Environment. In the present study, a strategy to preserve Iberian red deer genetic identity has been developed, with possible application to other similar cases. The specific objective of the present project was to provide the JNH with genetic markers to identify trophies belonging to foreign deer. Two types of genetic markers were developed. The first is a dominant multilocus marker, that is, presence/absence of bands depending on the subspecies studied (similar to DNA “fingerprinting” but by PCR amplification) and, the second is a variant of the RFLP–PCR assays (codominant marker) using different restriction enzymes. These two procedures show a range of different genotypes as a result of subspecific polymorphisms (Fernández–García et al., unpublished data). The JNH has decided to apply this test to trophies and those proving to come from introduced deer will be rejected from the Spanish ranking. Rejected trophies will lose their value and it is expected that owners will thus be dissuaded from importing foreign deer. Although the rejection of such trophies may represent a setback for the economic activity on some estates, it is considered that promoting the production of autochthonous, wild–reared red deer will be beneficial for big– game producers in general, since Iberian red deer could be promoted as an exclusive product to international hunters. Conservation of many natural areas in Spain depends on the adequate exploitation of natural resources, including hunt-

84 – Forum

ing. Increasing the value of natural products may contribute to conservation if their exploitation is more compatible with the preservation of biodiversity than alternative uses of the land, such as livestock or agriculture.

Other game species are equally threatened. Roe deer (Capreolus capreolus) is also being introduced from foreign populations. The wild boar (Sus scrofa) is being crossed with the domestic pig to increase the number of offspring per litter. It is produced under controlled conditions and the hybrids are released to the wild. Both cases are big–game species and the same strategy could be applied as there are trophies which are submitted to the JNH. Genetic markers for these are currently being developed. However, there are other well-known examples such as the red partridge (Alectoris rufa) which is hybridised on farms to provide thousands of individuals for the increasing demand for massive hunting. In these cases, the “trophy–rejection” strategy is not applicable, but some other type of control can surely be implemented.

Although the examples presented here refer to game species, similar guidelines may be used in other conservation tasks regarding exploited species all over the world. A key to the present project was to identify a bottleneck in the management process of a species or its products, and to design a strategy which in some way would determine the quality of the original product in agreement with competent authorities.

Acknowledgements The authors wish to thank JNH, the CIC delegation in Spain, and the many people who collabo-

Carranza et al.

rated by providing deer samples. Spanish Ministry of the Environment, "Fundación Biodiversidad" Government of Extremadura and project REN 2001–1524 from Ministerio de Ciencia y Tecnología contributed to financial support.

References

A LLENDORF , F. W., LEARY , R. F., S PRUELL, P. & W ENBURG , J. K., 2001. The problems with hybrids: setting conservation guidelines.

Tree , 16: 613–622.

D ERR , J. N., 1991. Genetic interactions between white–tailed and mule deer in the south– western United States. J. Wildl. Manage. , 55: 228–237.

G OODMAN , S. J., B ARTON , N. H., S WANSON , G., ABERNETHY , K. & PEMBERTON, J. M., 1999. Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (Genus Cervus ) in Argyll, Scotland. Genetics , 152: 355–371.

MACHORDOM, A., GARCÍA–MARÍN, J. L., SANZ, N., ALMODOVAR, A. & PLA, C., 1999. Allozyme diversity in brown trout (Salmo trutta) from Central Spain: genetic consequences of restocking.

Freshwater Biology, 41: 707–717.

O NTARIO F EDERATION OF ANGLERS AND HUNTERS , 1991. Report and recommendations on game farming and ranching of big game in Ontario: implications for native wildlife and conservation.

RHYMER, J. M. & SIMBERLOFF, D., 1996. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst., 27: 83–109.

Animal Biodiversity and Conservation 26.2 (2003)

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Conservation genetics in the recovery of endangered animal species: a review of US endangered species recovery plans (1977–1998) L. C. Moyle, J. R. Stinchcombe, B. R. Hudgens & W. F. Morris

Moyle, L. C., Stinchcombe, J. R., Hudgens, B. R. & Morris, W. F., 2003. Conservation genetics in the recovery of endangered animal species: a review of US endangered species recovery plans (1977–1998). Animal Biodiversity and Conservation, vol 26.2: 85–95.

Abstract Conservation genetics in the recovery of endangered animal species: a review of US endangered species recovery plans (1977–1998).— The utility of genetic data in conservation efforts, particularly in comparison to demographic information, is the subject of ongoing debate. Using a database of information surveyed from 181 US endangered and threatened species recovery plans, we addressed the following questions concerning the use of genetic information in animal recovery plans: I. What is the relative prominence of genetic vs. demographic data in recovery plan development? and, II. When are genetic factors viewed as a threat, and how do plans respond to genetic threats? In general, genetics appear to play a minor and relatively ill–defined part in the recovery planning process; demographic data are both more abundant and more requested in recovery plans, and tasks are more frequently assigned to the collection / monitoring of demographic rather than genetic information.

Nonetheless, genetic threats to species persistence and recovery are identified in a substantial minority (22 %) of recovery plans, although there is little uniform response to these perceived threats in the form of specific proposed recovery or management tasks. Results indicate that better guidelines are needed to identify how and when genetic information is most useful for species recovery; we highlight specific contexts in which genetics may provide unique management information, beyond that provided by other kinds of data.

Key words: Conservation genetics, Endangered species, Endangered species recovery plans.

Resumen Genética de la conservación para la recuperación de especies animales en peligro de extinción: revisión de los planes de recuperación de especies en peligro de extinción de Estados Unidos (1977–1998).— La utilidad de los datos genéticos en los esfuerzos conservacionistas, en particular en comparación con la información demográfica, es objeto de un continuo debate. Utilizando una base de datos con información sobre los 181 planes de recuperación de especies amenazadas y en peligro de extinción de Estados Unidos, hemos estudiado las siguientes cuestiones referentes al uso de la información genética en los planes de recuperación de especies animales: I ¿Cuál es la importancia relativa de los datos genéticos en comparación con los demográficos en el desarrollo de los planes de recuperación? y II ¿Cuándo se considera que los factores genéticos constituyen una amenaza, y cómo responden los planes a esas amenazas genéticas? En general, parece que la genética sólo desempeña un papel menor y relativamente mal definido en el proceso de planificación de la recuperación de especies; los datos demográficos son más abundantes y más solicitados para la elaboración de planes de recuperación, y las acciones que se llevan a cabo con frecuencia se enfocan más a las recopilación/observación de los datos demográficos que a la obtención de información genética. No obstante, las amenazas genéticas para la supervivencia y recuperación de especies se indican como un importante factor minoritario (22 %) en los planes de recuperación, si bien la respuesta a esas amenazas mediante medidas de gestión o recuperación específicas es poco uniforme. Los resultados apuntan a que se necesitan unas directrices más claras para determinar cómo y cuándo resulta más útil la información genética para la recuperación de especies; hemos resaltado contextos concretos en los que la genética puede proporcionar una valiosísima fuente de información para la gestión de esas cuestiones, superior a la que se pueda obtener a partir de otros datos.

ISSN: 1578–665X

© 2003 Museu de Ciències Naturals

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Palabras clave: Genética de la conservación, Especies en peligro de extinción, Planes de recuperación de especies en peligro de extinción.

(Received: 13 III 03; Final acceptance: 28 III 03) Leonie C. Moyle, Center for Population Biology, Univ. of California, Davis, CA–95616, USA. E–mail: lcmoyle@ucdavis.edu John R. Stinchcombe, Ecology and Evolutionary Biology Dept., Brown Univ., Box G–W, Providence, RI–02912, USA. E–mail: John_Stinchcombe@brown.edu Brian R. Hudgens & William F. Morris, Dept. of Biology, Box 90338, Duke Univ, Durham, NC 277080338, USA. Corresponding author: L. C. Moyle. E–mail: lcmoyle@ucdavis.edu

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Animal Biodiversity and Conservation 26.2 (2003)

Introduction Interest in the application of genetics to conservation biology has grown enormously in the last 20 years. With it has come vigorous debate both for and against the utility of genetic studies in practical conservation contexts. On one hand, it is acknowledged that genetic characteristics have the potential to influence a group’s ability to persist over both the short and long term (SCHONEWALD– COX et al., 1983; ELLSTRAND & ELAM, 1993; KELLER et al., 1994, FRANKHAM, 1995; PEAKALL & SYDES, 1996; HOGBIN & PEAKALL, 1999; SACCHERI et al., 1998; HEDRICK & KALINOWSKI, 2000). On the other hand, few direct links between extinction and genetics have been firmly established, leading some to argue that other more immediate concerns, such as demographic characteristics and population dynamics, should almost always have primacy over genetic considerations (L ANDE, 1988; CARO & LAURENSON, 1994; CAUGHLEY, 1994; SCHEMSKE et al., 1994). Resolving prioritization of recovery efforts is crucial in a continuing climate of limited funding for both conservation research and endangered species recovery efforts.

In the USA, the primary legal mechanism for protecting and subsequently managing endangered species is the Endangered Species Act of 1973 (ESA). One fundamental goal of the ESA is recovery of listed species, i.e. biological rehabilitation to a point where the threat of extinction no longer exists. To this end, the ESA provides for the development of a recovery plan for each listed species; each plan must identify explicit criteria for evaluating recovery, a set of specific management actions to achieve this recovery, and an outline of estimated time and costs of implementing these actions. Within this recovery process, genetics can play an important role by providing information relevant to the development of management and breeding strategies to promote species persistence, including conservation of genetic diversity and reduction of threats such as inbreeding and outbreeding depression (HEDRICK & K ALINOWSKI, 2000). In fact, a number of individual cases (in both Europe and the US) have clearly demonstrated the utility of genetic analysis and/or intervention in the management of endangered animal groups, especially in the alleviation of inbreeding depression via migration or translocation ( e.g.

WESTEMEIER et al., 1998; M ADSEN et al., 1999; VILA et al., 2003). Nonetheless, continuing disagreement over the general importance of genetic factors in species persistence, in combination with the relative difficulty of obtaining relevant genetic data, may negatively impact the use of genetic approaches in endangered species recovery planning. Indeed, the prevalence, importance, and overall utility of genetic information in the development of recovery plans in animal species is presently unknown.

In this paper we examine the use of genetic data in recovery plans for endangered and threatened animal species in the US, with the goal of providing a broad overview of genetics in the US recovery planning process. Our analysis makes use of a database on recovery plans compiled in conjunction with the National Center for Ecological Analysis and Synthesis (NCEAS), the Society for Conservation Biology (SCB), and the US Fish and Wildlife Service (FWS), as described

by BOERSMA et al. (2001), CLARK et al. (2002), and HOEKSTRA et al. (2002). The data were gathered using a survey developed jointly by SCB and USFWS; the database contains information on 181 endangered species complied from 136 recovery plans, drafted or revised during the period 1977 through 1998, and approved by the USFWS or the National Marine Fisheries Service (NMFS). For a description of the types of questions asked in the survey, see HOEKSTRA et al.

(2002). The entire database can be accessed at http://www.nceas.ucsb.edu/recovery/. From this sample of surveyed recovery plans, we focus on the presentation and use of genetic data for the conservation of animal species. Given the controversy over the relative utility of genetic versus demographic data, we begin by comparing the use and proposed collection of genetic and demographic data in recovery plans. We then determine how frequently and in what cases genetic factors are cited as threats to species persistence, and how plans respond to these perceived threats. Our goal is to assess the current status of genetics in US recovery plans, in order to better inform both managers and academics of the actual, and potential, uses of genetics in this fundamental conservation context. Although similar reviews of the role of genetics in the conservation of plant species in the USA and Australia can be found in SCHEMSKE et al. (1994) and PEAKALL & SYDES (1996), respectively, to our knowledge quantitative analyses of a large sample of recovery plans for species from a broad range of animal groups (mammals, birds, fish / reptiles / amphibians, invertebrates), are not presently available.

Methods Data preparation Eliminating data pertaining to plant species produced a reduced database containing information on 96 animal species from 90 endangered species recovery plans. To evaluate information presented in recovery plans, we identified survey questions in the database that specifically pertained to genetic and demographic data, and genetic threats, and coded these survey responses as binary data (variables of 0 and 1, reflecting yes or no for a given question in the plan under consideration), prior to analysis. In cases where

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multiple questions from the survey were relevant to a single analysis, we combined these questions and recoded data as a binary response of 1 if the survey indicated that, for any of the appropriate survey questions, the answer was yes, or 0 otherwise, for each plan under consideration.

Statistical analysis of the data consisted of likelihood ratio chi–square tests, performed using the PROC FREQ procedure of SAS (SAS Institute, 1997). The categories compared in analyses are described below (see also tables 2, 3, and 4 in results). Note that because recovery plans were of two types —multispecies plans (where multiple listed species are addressed in the same plan) and single–species plans— it can be difficult to determine the relevant unit of replication for statistical analysis. Accordingly, for questions related to whether species–specific data is presented or requested, or whether genetic threats such as inbreeding are associated with species characteristics (i.e., taxonomic group, range size), we analyzed data on the species level. Most of our analyses were at the species– level. However, for questions related to whether specific recovery tasks were proposed, we analyzed our data at the level of individual plans; this is because whether or not specific recovery tasks are assigned is not likely to be independent for two species in the same recovery plan. Thus for plan–level analyses, we reduced survey data from multi–species plans in the following conservative manner. If there was any positive response for any of the species included in a given multi–species recovery plan, we gave that plan a score of 1; for example, if the database indicated that a recovery task had been proposed for at least 1 species in a multi– species plan, we coded the entire recovery plan as having proposed that particular recovery task.

and invertebrates). Fish, reptiles, and amphibians were combined into a single general category to ensure sufficient sample sizes for statistical analysis. These analyses were performed on the species level.

Specific analyses

Results

What is the relative prominence of genetic vs. demographic data in recovery plan development?

What is the relative prominence of genetic vs. demographic data in recovery plan development?

To address this question, we determined what information was presented about each endangered species, and then compared the percentage of plans that included genetic or demographic information. We also examined whether the presented data were qualitative or quantitative in nature, whether there were explicit requests for additional data on genetic and demographic topics, and whether the use of, and specific responses to, this data differed for genetic versus demographic information. Finally, we evaluated whether inclusion of genetic or demographic data was associated with species taxonomic group by analyzing the frequency of plans that included or called for genetic or demographic data within 4 broad taxonomic groupings (mammals, birds, fish / reptiles / amphibians,

Recovery plans presented considerably more demographic than genetic data. Some form of demographic data was presented in 79 % of the recovery plans, whereas only 25 % presented genetic information (table 2). In plans in which data were presented, demographic data were more quantitative than genetic data (table 2).

Plans were also more likely to call for additional demographic data, in comparison to genetic data (table 2).

Species taxonomic group influenced the likelihood that plans presented demographic data but had no discernable influence on presentation of genetic data (table 3). For demographic information, this difference appears to be driven by the fact that 100 % of mammal plans presented some demographic data whereas these

When are genetic factors viewed as a threat, and how do plans respond to genetic threats?

We analyzed how frequently genetic inbreeding or bottlenecks were viewed as a threat to species persistence and whether citing genetics as a threat was associated with certain species characteristics. Specifically, we analyzed the frequency of plans that cited genetic factors as a threat for 4 broad taxonomic groupings (as outlined above), as well as for species range (i.e. restricted (< 1 km2) versus limited (< 100 km2) versus widespread (> 100 km2); as defined in the survey) and for number of extant populations (one population only vs. more than one population). The goal in the latter two analyses was to evaluate whether genetic threats are more likely to be identified when theory predicts species will be most vulnerable to processes of genetic erosion, i.e. where species range or number of populations is extremely restricted (e.g. ELLSTRAND & ELAM, 1993). Because these analyses sought to determine associations between genetic threats and species–specific characteristics, these analyses were also performed with species level data.

To examine plan responses to perceived genetic threats, we asked whether plans that cited genetic threats were more likely to call for more genetic information, or to propose the specific recovery tasks of captive breeding, translocation and/or reintroduction —all tasks that may alleviate such threats. These analyses were performed at the plan level.

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Animal Biodiversity and Conservation 26.2 (2003)

Table 1. Definitions of terms related to US Endangered Species recovery plans, as used in the text (adapted from STINCHCOMBE et al., 2002) Tabla 1. Definición de términos relacionados con planes de recuperación de especies en peligro de extinción de Estados Unidos, tal como se emplean en este documento (adaptadas de STINCHCOMBE et al., 2002).

Term

Definition

Data collection

The collection of any information on the population or species; in contrast to Monitoring

Monitoring

Taking direct measures of a population or species to determine if recovery is occurring; in contrast to data collection

Recovery criteria

Criteria or requirements that must be fulfilled to down–list or de–list the endangered species or population

Recovery task

A list of specific activities designed to promote recovery of the species. A list of recovery tasks is contained in the Implementation Schedule of every plan

Task priority

Implementation priority assigned to each recovery task. Recovery tasks are ranked on a scale of 1–3, with 1 being "high priority" in our usage

Table 2. Prominence of genetic versus demographic information in recovery plans: information presented for species. Degrees of freedom for likelihood ratio tests were 1 for each test.

Tabla 2. Importancia de la información genética en comparación con la demográfica en los planes de conservación: la información está organizada por especies. Los grados de libertad en el test del cociente de probabilidad fueron de 1 para cada test.

Were there differences between genetics and demography in terms of...

Answer χ2 p–value

...proportion of plans presenting this information?

Yes χ2 = 59.6 p < 0.0001

Presented Not presented

25 % 75 %

79 % 21 %

...the kind of information presented?

Yes χ2 = 17.94 p < 0.0001

Qualitative Quantitative

64 % 36 %

19 % 81 %

Yes Requested Did not request

41 % 59 %

60 % 40 %

...calls / requests for additional information?

χ2 = 5.96 p = 0.015

data were available in less than 60 % of invertebrate plans. In the case of every taxonomic group, however, the majority of plans presented demographic data but did not present genetic data (table 3). Assuming that all available information was presented in the recovery plan, results also suggest that birds, mammals, and invertebrates are particularly poorly described genetically (all with < 20 % of plans presenting genetic data), in comparison to reptiles/fish/amphibians where more than twice as many plans presented genetic data. (For con-

Category

Genetic Demographic information information

trast, plans drafted for endangered plants presented demographic and genetic data in 72 % and 31 % of plans respectively —Moyle, unpubl. data). Regardless, invertebrates appear to be poorly described for both genetic and demographic data.

With respect to assignment of specific recovery tasks, plans were more likely to assign tasks to monitor demographic than genetic parameters (table 4). The plans that assigned monitoring tasks were significantly more likely to indicate how

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Table 3. Prominence of genetic versus demographic data in plan development according to species taxonomic group.

Tabla 3. Importancia de los datos genéticos en comparación con los datos demográficos en el desarrollo de los planes según el grupo taxonómico de la especie.

Was taxon associated with availability / presentation of… …genetic data?

χ2

Answer No

χ2

= 6.08

p–value p = 0.11

…demographic data?

χ2

Answer Yes

χ2

p–value

= 13.97 p = 0.003

Freq. plans

Birds

16 %

84 %

with data

Herps / Ichs

41 %

78 %

Invertebrates

19 %

57 %

Mammals

17 %

100 %

Table 4. Tasks assigned to monitor genetic versus demographic data, and use of and responses to these data (Plan–level analyses).

Tabla 4. Estudios de análisis de los datos genéticos en comparación con los datos demográficos y su posterior uso y respuestas a estos datos (análisis a nivel de Plan de recuperación)

Were there differences between genetics and demography in terms of...

Answer χ2 p–value

...whether recovery tasks were assigned to monitor this kind of information?

Yes χ2 = 23.93 p < 0.0001

1+ tasks no tasks

20 % 80 %

56 % 44 %

...whether the use of monitored data was specified?

Yes χ2 = 9.35 p = 0.002

analysis specified no anal. spec.

13 % 87 %

32 % 68 %

...whether specific responses to monitored data were noted?

No χ2 = 0.74 p = 0.39

response noted no response

29 % 71 %

19 % 81 %

demographic data would be analyzed than genetic data (table 4); < 15 % of plans proposing to monitor genetic data specified how this data was to be analyzed (table 4). Interestingly, less than one third of plans that proposed monitoring of data in either category also indicated how this new data would change the recovery plan (table 4).

When are genetic factors viewed as a threat, and how do plans respond to genetic threats?

Of 96 species that had data available, 22 % of plans cited genetics (i.e. inbreeding depression or genetic bottlenecking) as a threat to species per-

Category

Genetic data

Demographic data

sistence. Of these, 65 % identified this threat as anticipated, while fewer plans (50 % of those with data available) identified the genetic threat as extant / current (as classified in the plan survey).

Identification of genetics threats did not differ statistically between taxonomic groups, although approximately one third of plans drafted for birds and mammals identified genetic factors as a threat, whereas approximately half as many plans for invertebrates and reptile / fish / amphibians did so (table 5). Estimated species range and number of populations did not influence whether genetic factors were cited as a threat (table 5), indicating that perceived genetics threats are not limited to those circumstances where theory suggests species

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Table 5. Associations between genetic threats to species persistence and species–level characteristics.

Tabla 5. Relación entre las amenazas genéticas para la supervivencia de una especie y las características de la misma.

Is citation of genetics as a threat associated with...

Answer χ2 p–value

Category

Frequency of plans citing genetic threats (n / N)

...taxonomic group?

No χ2 = 3.79 df = 3, p = 0.29

Birds Herps / Ichs Invertebrates Mammals Total

32 % 16 % 14 % 33 % 22 %

(7 / 22) (5 / 31) (3 / 21) (6 / 18) (21 / 92)

...species range?

No χ2 = 2.54 df = 2, p = 0.28

Restricted (< 1 km2) Intermediate (< 100 km2) Broad (> 100 km2) Total

15 % 11 % 28 % 22 %

(2 / 13) (2 / 17) (13 / 46) (17 / 76)

One population > one population Total

17 % (6 / 36) 25 % (10 / 40) 21 % (16 / 76)

...number of populations?

No χ2 = 0.545 p = 0.460

will be most vulnerable to processes of genetic erosion (i.e. single extant population and/or extremely restricted species range).

Plans that cited genetics as a threat were no more likely to call for more genetic information than plans that did not identify genetic threats, but were more likely to propose an explicit recovery task to monitor genetic information (table 6).

Nonetheless, citing genetics as a threat did not influence whether these recovery tasks were given highest (i.e. priority 1) versus secondary (priority 2 or 3) implementation priority (table 6); indeed, recovery tasks dealing with genetic threats were almost always assigned the highest priority (table 6) without regard to whether genetics was explicitly cited as a threat or not.

Finally, we found mixed evidence that plans that cited genetics as a threat proposed specific recovery tasks that can alleviate those threats, i.e. captive breeding, reintroduction, and/or translocation. Recovery tasks involving reintroduction into new or formerly occupied habitat were associated with identification of genetic threats, however tasks involving captive breeding and translocation of individuals were not (table 6).

Discussion In general, despite the prominence of genetic factors in the rescue and recovery of specific endangered animal groups (e.g. WESTEMEIER et al., 1998; MADSEN et al., 1999; VILA et al., 2003) genetics appears to have played a limited and ill-defined role in the US recovery planning process to

date, certainly one that appears incongruent with current academic interest in conservation genetics. First, our results indicate that demography is consistently better represented and emphasized than genetics in endangered species recovery plans.

This greater emphasis on demographic information agrees with the prescriptions of some conservation biologists (e.g. LANDE, 1988; CAUGHLEY, 1994) who maintain that, for critically endangered species, genetic data is unlikely to be as informative or valuable as demographic data in assessing biological status or determining appropriate management strategies. Our findings suggest that recovery plan managers do in fact rely more heavily on demographic parameters for these purposes.

Nonetheless, we also found that genetic factors are in fact cited as threats in a substantial minority (22 %) of recovery plans, but that individual plan responses to these perceived threats are neither uniform nor consistent. In addition, our results indicate that recovery plans often do not contain a clear articulation of how genetic data can be used effectively to address the recovery of endangered species; for example, less than one-third of plans that proposed monitoring genetic parameters indicated how new data would change the recovery plan. Overall, our results suggest that there is a limited understanding of how genetics can be used to aid in species recovery, even in cases where genetic factors are explicitly identified relevant to species persistence and recovery.

Our first major finding agrees qualitatively with prior surveys in plant species recovery plans that similarly found a discrepancy between demographic and genetic information. In particular,

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Table 6. Associations between perceived genetic threats to species persistence and recovery plan responses to genetic threats.

Tabla 6. Relación entre las supuestas amenazas genéticas para la supervivencia de una especie y las respuestas de los planes de recuperación a esas amenazas genéticas.

.

Cite genetics as a threat?

Does the recovery plan…

Significant association?

Yes (n / N)

No (n / N)

χ2 , p–value

...request further genetic information?

Yes No

27 % (6 / 22) 73 % (16 / 22)

17 % (11 / 64) 83 % (53 / 64)

No χ2 = 0.99, p = 0.32

...propose a matching recovery task?

Ye No

64 % (14 / 22) 36 % (8 / 22)

10 % (6 / 62) 90 % (56 / 62)

Yes χ2 = 23.95, p < 0.0001

...assign high priority to the proposed recovery task?

Highest priority

93 % (13 / 14)

83 % (5 / 6)

Secondary priority

No

χ2 7 % (1 / 14)

17 % (1 / 6)

= 0.39, p = 0.53

...propose a captive breeding task?

Yes No

67 % (14 / 21) 33 % (7 / 21)

47 % (30 / 64) 53 % (34 / 64)

No χ2 = 2.52, p = 0.11

...propose a translocation task?

Yes No

38 % (8 / 21) 62 % (13 / 21)

39 % (24 / 62) 61 % (38 / 62)

No χ2 = 0.002, p = 0.96

...propose reintroduction into former habitat?

Ye No

86 % (18 / 21) 14 % (3 / 21)

58 % (37 / 64) 42 % (27 / 64)

Yes χ2 = 5.99, p = 0.01

...propose reintroduction into new habitat?

Yes No

15 % (9 / 59) 85 % (50 / 59)

Yes χ2 = 3.75, p = 0.051

37 % (7 / 19) 63 % (12 / 19)

SCHEMSKE et al.’s (1994) survey of 98 USFWS plans for individual plant species (draft dates ranging from 1980 to 1992) found fewer than 8 % of plans presented detailed genetic information whereas detailed demographic data were presented in 33 % of all such plans. They also found that collection of additional demographic information was proposed for 84 % of plans, but only 26 % proposed additional genetic studies, similar to our findings for animal groups. By contrast, PEAKALL & SYDES (1996) reported that, for the Australian state of New South Wales, 57 % of all plant recovery plans they reviewed recommended inclusion of genetic studies in the recovery program. Quantitative discrepancies in the frequency of data presented between our analysis and the other US study may be due to divergent definitions of data (i.e. our plan survey did not require that presented data be detailed); however, the difference in historical coverage between the two studies is likely more important. In particular, SCHEMSKE et al.’s (1994) analysis —of plans from 1980 to 1992— captured fewer recent recovery plans than our survey. Elsewhere we have shown that more recently drafted US recovery plans (i.e. post–1995) are significantly more likely to assign monitoring, management, and recovery tasks to genetic

factors than older (pre–1995) plans (STINCHCOMBE et al., 2002), indicating that genetics receives more attention in more recently drafted, versus older, recovery plans. In comparison to SCHEMSKE et al. (1994), we found that more plans presented genetic data overall, which is consistent with this apparent trend to increased consideration of genetics in more recent plans. Conversely, note that the difference in taxonomic coverage (i.e., plants vs. animals) between the two analyses is unlikely to explain qualitative differences in the amount of genetic and demographic data presented, because plans written for plants in our database showed similar results to our findings for animal groups (Moyle unpubl. data).

The discrepancy between available data for genetics and demography was also observed within each of animal taxonomic group analyzed individually. Regardless, it is clear that —of all 4 taxonomic groupings— invertebrates are very poorly understood both genetically and demographically, suggesting a particular need for more basic biological research on endangered species within this animal group. Birds and mammals also appear to be poorly described genetically; although the reasons for this are unclear, it may be that for mammals and birds generally, other biological information (e.g. historical ranges /

Animal Biodiversity and Conservation 26.2 (2003)

abundances, demographic data) is frequently available such that information on genetics may less frequently (or consistently) be collected and / or included in recovery plans.

Our findings on the relative prominence and use of genetic versus demographic data are not altogether surprising. Given the relative ease with which some kinds of demographic data (e.g. birth and death rates for sessile organisms, or clutch / litter size / seed production) can be collected in comparison to data on genetic diversity, inbreeding depression or gene flow, one might expect demographic data to be more abundant. In addition, the relative youth of conservation genetics and confusion stemming from the controversial debate about its importance in the persistence and recovery of endangered and threatened species (e.g. LANDE, 1988; CAUGHLEY, 1994; FRANKHAM, 1995; PEAKALL & SYDES, 1996; HEDRICK & KALINOWSKI, 2000), might also be acting to limit the collection and application of genetic data in recovery plans.

Nonetheless, the second major finding of our analysis —that genetic factors are identified as threats to species persistence in a substantial minority of animal recovery plans— indicates that explicit consideration of genetic factors in species recovery planning is of more than purely academic interest. That genetic recovery tasks are almost always assigned highest priority underscores this recognition that genetic factors can be of real practical concern in the recovery of individual endangered species. Accordingly it is a genuine concern that, while there is good information available on the potential longer–term management and utility of genetic variation (e.g.

SCHONEWALD–COX et al., 1983; LANDWEBER & DOBSON, 1999), much of this work is failing to be translated into effective recovery strategies within the US recovery plan conservation process (see also STINCHCOMBE et al., 2002). Indeed, our findings generally support SCHEMSKE et al.’s (1994) suggestion that much genetic research that is proposed in recovery planning might be motivated by the hopeful search for limiting factors or ongoing threats to species, rather than by a clear vision of its utility in developing recovery objectives or facilitating recovery efforts. If genetics continues to increase in prominence in recovery plans (STINCHCOMBE et al., 2002), this failure will become an increasingly large liability in the recovery planning process.

Overall, our results suggest that the most pressing need of recovery managers with respect to conservation genetics is simple, concise and transparent guidelines as to contexts in which genetics can provide unique and useful information in the development and management of endangered species recovery. Fortunately, researchers have already begun to develop such guidelines. For example, in the case of plant species, PEAKALL & SYDES (1996) suggest that collection of genetic data will be most ap-

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propriate in four specific contexts. These are where: (i) it is not possible to conserve all available populations and/or reserve design is a management option; (ii) translocation or ex situ programs are prescribed; (iii) species may be extensively clonal or inbreeding; and, (iv) taxonomy is uncertain. In these cases, genetic data may offer unique insight into determining which units to preserve or use as source material, beyond that which is provided by other (e.g. demographic) types of data. For example, additional genetic data is more likely to provide unique management information where species occur in multiple extant populations that cannot all receive conservation attention; in contrast, for species limited to a single extant population genetic data may be less useful because demographic information already suggests that preserving individuals in the single remaining population is the highest recovery priority (PEAKALL & SYDES, 1996). Similarly, all other things being equal, species whose populations occur primarily on land that is already protected are less likely to benefit from additional genetic information than species for which land acquisition for protection remains a pressing issue. (We are not suggesting that taxa located primarily on protected lands are not in need of active management or additional research; merely that, on average, genetic data is likely to be more useful when there are decisions to be made about populations that are not yet formally protected.)

Given these wholly pragmatic considerations, we expect that in general genetic information will provide unique information in instances where the species occurs in more than one population, and/or where decisions must be made about which (currently unprotected) populations to preferentially preserve. Genetics can also play a unique role in determining which individuals most warrant protection, via genetic investigations of relatedness and/or taxonomic ambiguity (as well as, in the case of plants, potential clonality), in addition to making management decisions about intense manipulative conservation efforts ( e.g. captive breeding programs, reintroductions). In this way, rather than evaluating the utility of additional genetic data on the basis of predictions arising from genetic theory, genetics should be assigned a role in recovery planning based on whether it is likely to provide unique information on management strategies or options, beyond that provided by demographic and other data. As such, in the future it may be useful for recovery plans to integrate current guidelines as to the best use of genetic data (e.g. P EAKALL & S YDES, 1996) directly into the recovery planning process. Such rules of thumb will provide greater guidance as to the utility of collecting genetic data, particularly in the absence of any other relevant information, and would help clarify how such data is to be used to inform

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and modify recovery efforts. This would minimize resources wasted on uninformative research, while maximizing the utility of genetic data in contexts where it can provide unique insight into current and future management strategies. It should be clear that we are not advocating that less effort be put into the consideration of genetics of endangered species, but rather that more effort be devoted to considering how and when such information is most useful in urgent management situations, such as recovery efforts.

Finally, we believe this can best be achieved through further strengthening links between the academic and applied conservation communities.

In particular, the onus is on academic conservation biologists (particularly conservation geneticists) not just to develop more pragmatic guidelines as to the best practical use of genetics in conservation contexts, but also to be more directly involved in the recovery planning process itself, especially by serving on recovery planning teams. Recovery plans that do include at least one academic scientist as an author articulate a much clearer use of biological information in the design of monitoring strategies, and tend to show a clearer use of biological information in the selection of recovery criteria (GERBER & SCHULTZ, 2001), indicating that academic involvement in recovery planning can improve the utilization of biological information. Of all plans in the database analyzed here, however, only 5 % were authored by academic scientists, and only one third of recovery planning teams included academic scientists as members (Stinchcombe, unpubl. data). In addition, the participation of academic scientists as plan authors or in recovery planning teams did not increase in the period covered by the database (GERBER & SCHULTZ, 2001; Stinchcombe, unpubl. data), indicating there is considerable room for improvement in academic participation in the planning process. The USFWS has recently adopted new policy to formally encourage increased diversity within recovery planning teams (CLARK et al., 2002). It is now up to academic scientists to respond positively to this conservation need.

Acknowledgements This study was funded by Society for Conservation Biology, the US Fish and Wildlife Service, and the National Center for Ecological Analysis and Synthesis, a center funded by the National Science Center (Grant DEB 94–21535), the University of California–Santa Barbara, the California Resources Agency and the California Environmental Protection Agency. The Project director was Dee Boersma. Jeff Bradley, Debby Crouse, William Fagan, Jon Hoekstra, Peter Kareiva, Gordon Orians, and Jim Regetz all helped with parts of the project. A complete list of the more than 325 seminar and workshop participants can be

Moyle et al.

found at http://www.nceas.ucsb.edu/recovery/acknowledgments. In addition, Philip Bloch participated in preliminary discussions and data organization for analyses presented in this paper. Thanks to Diane Elam, Steve Chambers, Kelly Zamudio, and Peter Kareiva for helpful comments on an earlier draft of this paper.

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CARO, T. M. & LAURENSON, M. K., 1994. Ecological and genetic factors in conservation: a cautionary tale. Science, 263: 485–486.

CAUGHLEY, G., 1994. Directions in conservation biology. J. Animal Ecol., 63: 215–244.

CLARK, J. A., HOEKSTRA, J. M., BOERSMA, P. D. & KAREIVA, P., 2002. Improving US Endangered Species Act recovery plans: key findings and recommendations of the SCB Recovery Plan Project. Cons. Biol., 16: 1510–1519.

ELLSTRAND, N. C. & ELAM, D. R., 1993. Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics, 24: 217–242.

FRANKHAM, R., 1995. Inbreeding and extinction: a threshold effect. Cons. Biol., 13: 792–799.

GERBER, L. R. & SCHULTZ, C. B., 2001. Authorship and the use of biological information in endangered species recovery plans. Cons. Biol., 15: 1308–1314.

HEDRICK, P. W. & KALINOWSKI, S. T., 2000. Inbreeding depression in conservation biology. Ann. Rev. Ecol. Syst., 31: 139–162.

HOEKSTRA, J. M., CLARK, J. A., FAGAN, W. F. & BOERSMA, P. D., 2002. Comprehensive review of endangered species act recovery plans. Ecol.

Appl., 12: 630–640.

HOGBIN, P. M. & PEAKALL, R., 1999. Evaluation of the contribution of genetic research to the management of the endangered plant Zieria prostrata. Cons. Biol., 13: 514–522.

KELLER, L. F., ARCESE, P., SMITH, J. N. M., HOCHACHKA W. M. & STEARNS, S. C., 1994. Selection against inbred song sparrows during a natural population bottleneck. Nature, 372: 356–357.

LANDE, R., 1988. Genetics and demography in biological conservation. Science, 241: 1455–1460.

LANDWEBER, L. F. & DOBSON, A. P., 1999. Genetics and the extinction of species. Princeton University Press, Princeton, NJ. MADSEN, T., SHINE, R., OLSSON, M. & WITTZELL, H., 1999. Restoration of an inbred adder population. Nature, 402: 34–35.

PEAKALL, R. & SYDES, M. A., 1996. Defining priorities for achieving practical outcomes from the genetic studies of rare plants. In: Back from the Brink: refining the threatened species recovery process: 119–129 (S. Stephens & S. Maxwell, Eds.). Surrey Beatty and Sons, Sydney.

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SACCHERI, I., KUUSSAARI, M., KANKARE, M., VIKMAN, P., FORTELIUS, W. & HANSKI, I., 1998. Inbreeding and extinction in a butterfly metapopulation.

Nature, 392: 491–494.

SCHEMSKE, D. W., HUSBAND, B. C., RUCKELSHAUS, M. H., GOODWILLIE, C., PARKER, I. M. & BISHOP, J. G., 1994. Evaluating approaches to the conservation of rare and endangered plants. Ecology, 75: 584–606.

SCHONEWALD–COX, C. M. CHAMBERS, S. M., MACBRYDE, B. & THOMAS, W. L. (Eds). 1983. Genetics and conservation: a reference for managing wild animal and plant populations. Benjamin/ Cummings, Menlo Park, CA. STINCHCOMBE, J. R., MOYLE, L. C., HUDGENS, B. R., BLOCH, P. L., CHINNADURAI, S. & MORRIS, W. F.,

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W ESTEMEIER , R. L., B RAWN , J. D., S IMPSON, S. A., E SKER , T. L., J ANSEN , R. W., W ALK , J. W., K ERSHNER , E. L., B OUZAT , J. L. & P AIGE , K. N., 1998. Tracking the long–term decline and recovery of an isolated population. Science, 282: 1695–1698.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

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

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

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

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

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Animal Biodiversity and Conservation 26.2 (2003)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter­ disciplinària publicada, des de 1958, pel Museu de Zoologia de Barcelona. Inclou articles d'inves­tigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxo­nomia, morfo­logia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfa­ sis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica catàlegs, llistes d'espècies o cites puntuals. Els estudis realitzats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles.

Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a inter­ net a http://www.museuzoologia.bcn.es/servis/servis3. htm, de manera que permet una difusió mundial dels seus articles.

Tots els manuscrits són revisats per l'editor executiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció.

Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

Normes de publicació Els treballs s'enviaran preferentment de forma electrò­ nica (abc@mail.bcn.es). El format preferit és un do­ cument Rich Text Format (RTF) o DOC que inclogui les figures (TIF). Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció.

Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investi­ gacions originals no publicades anterior­ment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors.

Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el programa utilitzat (preferiblement en Word).

Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat.

El primer autor rebrà 50 separates del treball ISSN: 1578–665X

sense càrrec a més d'una separata electrònica en format PDF. Manuscrits Els treballs seran presentats en format DIN A­–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manus­crits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat.

El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona.

Els caràcters cursius s’empraran per als noms cien­ tífics de gèneres i d’espècies i per als neologismes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona.

Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú.

Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri.

Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase.

Les dates s’indicaran de la forma següent: 28 VI 99; 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30).

S’evitaran sempre les notes a peu de pàgina.

Format dels articles Títol. El títol serà concís, però suficientment indi­ cador del contingut. Els títols amb desig­nacions de sèries numèriques (I, II, III,...) seran acceptats previ acord amb l'editor.

Nom de l’autor o els autors.

Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva.

Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància.

Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellano­parlants.

Palabras clave en castellà.

Adreça postal de l’autor o autors. © 2003 Museu de Ciències Naturals

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(Títol, Nom, Abstract, Key words, Resumen, Palabras clave i Adreça postal, conformaran la primera pàgina.)

Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball.

Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mètodes d’estudi i d’anàlisi de les dades i zona d’estudi.

Resultados. En aquesta secció es presentaran úni­ cament les dades obtingudes que no hagin estat publicades prèviament.

Discusión. Es discutiran els resultats i es compa­ raran amb treballs relacionats. Els sug­geriments de recerques futures es podran incloure al final d’aquest apartat.

Agradecimientos (optatiu).

Referencias. Cada treball haurà d’anar acompanyat de les referències bibliogràfiques citades en el text. Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for con­ servation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

La relació de referències bibliogràfiques d’un tre­ ball serà establerta i s’ordenarà alfabè­ticament per

autors i cronològicament per a un mateix autor, afegint les lletres a, b, c..., als treballs del mateix any. En el text, s’indi­caran en la forma usual: “... segons Wemmer (1998) ... ”, “...ha estat definit per Robinson & Redford (1991)...”, “...les prospeccions realitzades (Begon et al., 1999)...” Quan en el text s’anomeni un autor de qui no es dóna referèn­cia bibliogràfica el nom anirà en rodo­na: “...un altre autor és Caughley...”

Taules. Les taules es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista.

Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3,... i han de ser sempre ressenya­ des en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels autors.

La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es repro­dueixen bé.

Peus de figura i capçaleres de taula. Els peus de figura i les capçaleres de taula seran clars, concisos i bilingües en la llengua de l’article i en anglès.

Els títols dels apartats generals de l’article (Intro­ ducción, Material y métodos, Resultados, Discu­ sión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols.

Els autors procuraran que els seus treballs origi­ nals no passin de 20 pàgines (incloent–hi figures i taules).

Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una insti­tució pública.

Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

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Animal Biodiversity and Conservation 26.2 (2003)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter­ disciplinar, publicada desde 1958 por el Museo de Zoología de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxo­nomía, morfolo­ gía, biogeografía, ecología, etología, fisiología y genética) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con especies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos.

Animal Biodiversity and Conservation está registrada en todas las bases de datos importan­ tes y además está disponible gratuitamente en internet en http://www.museuzoologia.bcn.es/servis/ servis3.htm, lo que permite una difusión mundial de sus artículos.

Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan­ tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siempre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo.

Una vez aceptado, el trabajo pasará a ser pro­ piedad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reproducida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@mail.bcn.es). El formato prefe­ rido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras (TIF). Si se opta por la versión impresa, deberán remitirse cuatro co­ pias juntamente con una copia en disquete a la Secretaría de Redacción. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre inves­tigaciones originales no publi­ cadas an­te­rior­mente y que se somete en exclusiva a Animal Biodiversity and Conservation. En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesarios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores.

Cuando el trabajo sea aceptado los autores deberán enviar a la Redacción una copia impresa de la versión final junto con un disquete del ma­ nuscrito preparado con un pro­cesador de textos e ISSN: 1578–665X

indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modificaciones sustanciales en las prue­ bas de im­pren­­ta, introducidas por los autores, irán a ­cargo de los mismos.

El primer autor recibirá 50 separatas del tra­ bajo sin cargo alguno y una copia electrónica en formato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espa­ cio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado.

El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofre­ce, sin cargo ninguno, un servicio de corrección por parte de una persona especializada en revistas científicas.

En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso.

La redacción del texto deberá ser impersonal, evitán­dose siempre la primera persona.

Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comi­ llas; el nombre del autor que sigue a un taxón se escribirá también en redonda.

Al citar por primera vez una especie en el tra­ bajo, deberá especificarse siempre que sea posible su nombre común.

Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo.

Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escri­ birán con cifras excepto al empezar una frase.

Las fechas se indicarán de la siguiente forma: 28 VI 99; 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30).

Se evitarán siempre las notas a pie de página.

Formato de los artículos Título. El título será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designaciones de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consentimiento del editor.

Nombre del autor o autores.

Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esencia del manuscrito (introducción, material, métodos, resultados y discusión). Se evitarán las © 2003 Museu de Ciències Naturals

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especulaciones y las citas bibliográficas. Irá enca­ bezado por el título del trabajo en cursiva.

Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia.

Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablan­tes.

Palabras clave en castellano.

Dirección postal del autor o autores.

(Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.)

Introducción. En ella se dará una idea de los antecedentes del tema tratado, así como de los objetivos del trabajo.

Material y métodos. Incluirá la información refe­ rente a las especies estudiadas, aparatos utilizados, metodología de estudio y análisis de los datos y zona de estudio.

Resultados. En esta sección se presentarán úni­ camente los datos obtenidos que no hayan sido publicados previamente.

Discusión. Se discutirán los resultados y se compara­ rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado.

Agradecimientos (optativo).

Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publica­ ciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773 * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for con­ servation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Tesis doctoral,

Uppsala University. * Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

Las referencias se ordenarán alfabética­men­te por autores, cronológicamen­te para un mismo autor y con las letras a, b, c,... para los tra­bajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospeccio­ nes realizadas (Begon et al., 1999)..." Cuando en el texto se mencione un autor no incluido en la bibliografía el nombre irá en redonda: "...otro autor es Caughley..."

Tablas. Las tablas se numerarán 1, 2, 3, etc. y se re­ señarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista.

Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc., y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto.

Deben evitarse las figuras tridimen­sionales. Tanto los mapas como los dibujos deben incluir la escala.

Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien.

Pies de figura y cabeceras de tabla. Los pies de figura y cabeceras de tabla serán claros, concisos y bilingües en castellano e inglés.

Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Discusión, Agradecimientos y Referencias) no se numerarán. No utilizar más de tres niveles de títulos.

Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas.

Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública.

Se recomienda a los autores la consulta de fascículos recientes de la revista para seguir sus directrices.

V

Animal Biodiversity and Conservation 26.2 (2003)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an inter­­dis­ci­pli­nary journal which has been published by the Zoolo­ gical Museum of Bar­celona since 1958. It includes empirical and theoretical research in all aspects of Zoology (Systematics, Taxo­nomy, Morphology, Bio­geography, Ecology, Etho­logy, Physio­logy and Genetics) from all over the world with special emphasis on studies that stress the relevance of the study of Conservation Biology. The journal does not publish catalogues, lists of species (with no other relevance) or punctual records. Studies about rare or protected species will not be accepted unless the authors have been granted all the relevant permits. Each annual volume consists of two issues.

Animal Biodiversity and Conservation is registered in all principal data bases and is freely available on­ line at http://www.museuzoologia.bcn.es/servis/ABCag. htm, thus assuring world–wide access to articles published therein.

All manuscripts are screened by the Executive Edi­ tor, an Editor and two independent reviewers in order to guarantee the quality of the papers. The process of review is rapid and constructive. Once accepted, papers are published as soon as practicable, usually within 12 months of initial submission.

Upon acceptance, manuscripts become the prop­ erty of the journal, which reserves copyright, and no published material may be reproduced without quoting its origin.

Manuscripts must be presented on A–4 format page (30 lines of 70 spaces each) with double spacing.

Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been accepted.

The text may be written in English, Spanish or Catalan. Authors are encouraged to send their con­ tributions in English. The journal provides a FREE service of correction by a professional translator specialized in scientific publications. Care should be taken in using correct wording and the text should be written concisely and clearly. Wording should be impersonal, avoiding the use of the first person.

Italics must be used for scientific names of genera and species as well as untrans­latable neologisms.

Quotations in whatever language used must be typed in ordinary print between quotation marks.

The name of the author following a taxon should also be written in small print.

The common name of the species should be written in capital letters. When referring to a spe­ cies for the first time in the text, both common and scientific names must be given when possible.

Place names may appear either in their origi­ nal form or in the language of the manuscript, but care should be taken to use the same criteria throughout the text.

Numbers one to nine should be written in full in the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence.

Dates must appear as follows: 28 VI 99, 28,30 VI 99 (days 28th and 30th), 28–30 VI 99 (days 28th to 30th).

Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (abc@ mail.bcn.es). The preferred format is a document Rich Text Format (RTF) or DOC, including figures (TIF). In the case of sending a printed version, four copies should be sent together with a copy on a computer disc to the Editorial Office. A cover letter stating that the article reports on original research not published elsewhere and that it has been submitted exclusively for consi­deration in Animal Biodiversity and Conservation is also necessary.

When animal manipulation has been necessary, the cover letter should also especify that the authors follow current norms on the protection of animal species and that they have obtained all relevant permissions. Authors may suggest referees for their papers.

Once an article has been accepted, authors should send a printed copy of the final version together with a disc. Please identify software (preferably Word). Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days. Expenses due to any substantial alterations of the proofs will be charged to the authors.

The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format.

ISSN: 1578–665X

Formatting of articles Title. The title must be concise but as infor­mative as possible. Part numbers (I, II, III,...) should be avoided and will be subject to the Editor’s consent.

Name of author or authors.

Abstract in English, no longer than 12 type­written lines (840 spaces), covering the con­tents of the article (introduction, material, methods, results and discussion). Speculation and literature citation must be avoided. Abstract should begin with the title in italics.

Key words in English (no more than six) should express the precise contents of the manuscript in order of importance.

Resumen in Spanish, translation of the Abstract.

Summaries of articles by non­–Spanish speaking au­ thors will be trans­lated by the journal on request.

Palabras clave in Spanish.

Address of the author or authors.

(Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.)

Introduction. The introduction should in­clude the historical background of the sub­ject as well as the © 2003 Museu de Ciències Naturals

VI

aims of the paper.

Material and methods. This section should provide relevant information on the species studied, ma­ terials, methods for collecting and analysing data and the study area.

Results. Report only previously unpublished results from the present study.

Discussion. The results and their comparison with related studies should be discussed. Sug­gestions for future research may be given at the end of this section.

Acknowledgements (optional).

References. All manuscripts must include a bi­ bliography of the publications cited in the text.

References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of species richness for conservation of biological diversity: conceptual and methodological issues.

Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abun­ dance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva­ tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.).

Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

References must be set out in alphabetical and chronological order for each author, add­

ing the letters a, b, c,... to papers of the same year. Biblio­graphic citations in the text must ap­ pear in the usual way: "...according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the pros­pec­tions that have been carried out (Begon et al., 1999)..." When an author is men­tioned in the text but no bibliographical re­ ference is given, the name must appear in ordinary print: "...another of these authors is Caughley..."

Tables. Tables must be numbered in Arabic nu­ merals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal.

Figures. All illustrations (graphs, drawings or photo­ graphs) must be termed as figures, numbered conse­ cutively in Arabic numerals and with re­ference in the text. Glossy print photographs, if essential, may be included. Colour photographs may be published but its publication will be charged to authors. Maximum size of figures is 15.5 cm width and 24 cm height.

Figures will not be tridimen­sional. Both maps and drawings must include scale. The preferred shadings are white, black and bold hatching. Avoid stippling, which does not reproduce well.

Legends of tables and figures. Legends of tables and figures must be clear, concise, and written both in English and Spanish.

Main headings (Introduction, Material and me­ thods, Results, Discussion, Acknowled­ge­ments and References) should not be number­ed. Do not use more than three levels of headings.

Manuscripts should not exceed 20 pages 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 26.2 (2003)

VII

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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, Current Primate References, Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 26.2 (2003) ISSN 1578–665X

1–18 Amori, G. & Gippoliti, S. A higher–taxon approach to rodent conserv­ation priorities for the 21st century 19–27 Galarza, A. & Tellería , J. L. Linking processes: effects of migratory routes on the distribution of abundance of wintering passerines 29–37 Paracuellos, M., Nevado, J. C. , Moreno, D., Giménez, A. & Alesina, J. J. Conservational status and demographic characteristics of Patella ferruginea Gmelin, 1791 (Mollusca, Gastropoda) on the Alborán Island (Western Mediterranean) 39–49 Pinto, A. C. B., Azevedo–Ramos, C. & Carvalho Jr., O. de Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in Eastern Amazonia 51–67 Schmitt, T. Influence of forest and grassland management on the diversity and conservation of butterflies and burnet moths (Lepidoptera, Papilionoidea, Hesperiidae, Zygaenidae) 69–80 Sendra, A., Salgado, J. Mª & Monedero, E. Dos nuevas especies y una subespecie de campodeidos cavernícolas de la cornisa cantábrica (Diplura, Campodeidae)

Fòrum 81–84 Carranza, J., Martínez, J. G., Sánchez–Prieto, C. B., Fernández–García, J. L., Sánchez–Fernández, B., Álvarez–Álvarez, R., Valencia, J. & Alarcos, S. Game species: extinction hidden by census numbers 85–95 Moyle, L. C. , Stinchcombe, J. R., Hudgens, B. R. & Morris, W. F. Conservation genetics in the recovery of endangered animal species: a review of US endangered species recovery plans (1977–1998)