LAGOMORPHS

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LagomorphsPikas, Rabbits, and Hares of the World

edited by Andrew T. Smith Charlotte H. Johnston Paulo C. Alves Klaus Hackländer

J O H N S H O P K I N S U N I V E R S I T Y P R E S S | b a l t i m o r e

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© 2018 Johns Hopkins University PressAll rights reserved. Published 2018Printed in China on acid- free paper9 8 7 6 5 4 3 2 1

Johns Hopkins University Press2715 North Charles StreetBaltimore, Maryland 21218-4363www .press .jhu .edu

Library of Congress Cataloging-in-Publication Data

Names: Smith, Andrew T., 1946–, editor.Title: Lagomorphs : pikas, rabbits, and hares of the world / edited by Andrew T. Smith, Charlotte H. Johnston, Paulo C. Alves, Klaus Hackländer.Description: Baltimore : Johns Hopkins University Press, 2018. | Includes bibliographical references and index.Identifiers: LCCN 2017004268| ISBN 9781421423401 (hardcover) | ISBN 1421423405 (hardcover) | ISBN 9781421423418 (electronic) | ISBN 1421423413 (electronic)Subjects: LCSH: Lagomorpha. | BISAC: SCIENCE / Life Sciences / Biology / General. | SCIENCE / Life Sciences / Zoology / Mammals. | SCIENCE / Reference.Classification: LCC QL737.L3 L35 2018 | DDC 599.32—dc23 LC record available at https://lccn.loc.gov/2017004268

A catalog record for this book is available from the British Library.

Frontispiece, top to bottom: courtesy Behzad Farahanchi, courtesy David E. Brown, and © Alessandro Calabrese.

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Ochotona macrotis, Large- eared Pika 58 Ochotona mantchurica, Manchurian Pika 60 Ochotona nubrica, Nubra Pika 61 Ochotona opaca, Kazakh Pika 62 Ochotona pallasii, Pallas’s Pika 65 Ochotona princeps, American Pika 67 Ochotona pusilla, Steppe Pika 72 Ochotona roylei, Royle’s Pika 75 Ochotona rufescens, Afghan Pika 77 Ochotona rutila, Turkestan Red Pika 79 Ochotona syrinx, Qinling Pika 82 Ochotona thibetana, Moupin Pika 83 Ochotona thomasi, Thomas’s Pika 84 Ochotona turuchanensis, Turuchan Pika 85

Family Leporidae 87The Rabbits 87 Brachylagus idahoensis, Pygmy Rabbit 87 Bunolagus monticularis, Riverine Rabbit 90 Caprolagus hispidus, Hispid Hare 93 Nesolagus netscheri, Sumatran Striped Rabbit 95 Nesolagus timminsi, Annamite Striped Rabbit 97 Oryctolagus cuniculus, European Rabbit 99 Pentalagus furnessi, Amami Rabbit 104 Poelagus marjorita, Bunyoro Rabbit 107 Pronolagus crassicaudatus, Natal Red Rock Hare 108 Pronolagus randensis, Jameson’s Red Rock Hare 110 Pronolagus rupestris, Smith’s Red Rock Hare 111 Pronolagus saundersiae, Hewitt’s Red Rock Hare 113 Romerolagus diazi, Volcano Rabbit 114

Preface vii

Contributors ix

1 Introduction 12 Evolution of Lagomorphs 43 Systematics of Lagomorphs 94 Introduced Lagomorphs 135 Diseases of Lagomorphs 186 Conservation of Lagomorphs 22

SPECIES ACCOUNTS

Order Lagomorpha 29

Family Ochotonidae 31 Ochotona alpina, Alpine Pika 31 Ochotona argentata, Helan Shan Pika 33 Ochotona cansus, Gansu Pika 34 Ochotona collaris, Collared Pika 36 Ochotona coreana, Korean Pika 39 Ochotona curzoniae, Plateau Pika 40 Ochotona dauurica, Daurian Pika 43 Ochotona erythrotis, Chinese Red Pika 46 Ochotona forresti, Forrest’s Pika 47 Ochotona gloveri, Glover’s Pika 48 Ochotona hoffmanni, Hoffmann’s Pika 49 Ochotona hyperborea, Northern Pika 51 Ochotona iliensis, Ili Pika 53 Ochotona koslowi, Koslov’s Pika 55 Ochotona ladacensis, Ladak Pika 57

CONTENTS

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vi Contents

Sylvilagus 117 Sylvilagus aquaticus, Swamp Rabbit 117 Sylvilagus audubonii, Desert Cottontail 120 Sylvilagus bachmani, Brush Rabbit 122 Sylvilagus brasiliensis sensu stricto, Tapetí, Andean

Cottontail, Rio de Janeiro Dwarf Cottontail 125 Sylvilagus cognatus, Manzano Mountain

Cottontail 130 Sylvilagus cunicularius, Mexican Cottontail 131 Sylvilagus dicei, Dice’s Cottontail 135 Sylvilagus floridanus, Eastern Cottontail 137 Sylvilagus gabbi, Gabb’s Cottontail 140 Sylvilagus graysoni, Tres Marías Cottontail 142 Sylvilagus insonus, Omiltemi Rabbit 144 Sylvilagus mansuetus, San José Brush Rabbit 145 Sylvilagus nuttallii, Mountain Cottontail 147 Sylvilagus obscurus, Appalachian Cottontail 149 Sylvilagus palustris, Marsh Rabbit 152 Sylvilagus robustus, Davis Mountains Cottontail 154 Sylvilagus transitionalis, New England Cottontail 156 Sylvilagus varynaensis, Venezuelan Lowland

Rabbit 157Lepus 159 Lepus alleni, Antelope Jackrabbit 159 Lepus americanus, Snowshoe Hare 163 Lepus arcticus, Arctic Hare 165 Lepus brachyurus, Japanese Hare 168 Lepus californicus, Black- tailed Jackrabbit 170 Lepus callotis, White- sided Jackrabbit 173

Lepus capensis, Cape Hare 176 Lepus castroviejoi, Broom Hare 179 Lepus comus, Yunnan Hare 181 Lepus coreanus, Korean Hare 182 Lepus corsicanus, Corsican Hare 184 Lepus europaeus, European Hare 187 Lepus fagani, Ethiopian Hare 190 Lepus flavigularis, Tehuantepec Jackrabbit 191 Lepus granatensis, Iberian Hare 193 Lepus habessinicus, Abyssinian Hare 195 Lepus hainanus, Hainan Hare 196 Lepus insularis, Black Jackrabbit 198 Lepus mandshuricus, Manchurian Hare 200 Lepus nigricollis, Indian Hare 201 Lepus oiostolus, Woolly Hare 202 Lepus othus, Alaskan Hare 204 Lepus peguensis, Burmese Hare 205 Lepus saxatilis, Cape Scrub Hare 206 Lepus sinensis, Chinese Hare 208 Lepus starcki, Ethiopian Highland Hare 209 Lepus tibetanus, Desert Hare 211 Lepus timidus, Mountain Hare 212 Lepus tolai, Tolai Hare 216 Lepus townsendii, White- tailed Jackrabbit 218 Lepus victoriae, African Savanna Hare 220 Lepus yarkandensis, Yarkand Hare 222

References 225

Index 259

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of topics of broad interest across all lagomorph species: evolution, systematics, lagomorph diseases, introduced lagomorphs, and conservation and management. Despite several ongoing controversies in lagomorph taxonomy, we have maintained a conservative systematic approach. Nevertheless, we highlight relevant taxonomic issues that require attention. This work has been a team effort, with 82 specialists contributing to species accounts. We especially thank Rachel Fadlovich for her work on the references, and Aryn Musgrave for constructing all the species range maps. ATS thanks Harriet Smith for her insightful editorial work on his chapters. We are grateful to all the photographers who provided their work for free. We appreciate the meticulous copy editing by Maria E. denBoer. Finally, the collabora-tion with our editorial team from Johns Hopkins Univer-sity Press, Vincent Burke, Tiffany Gasbarrini, Debby Bors, and Meagan M. Szekely, is highly appreciated.

The IUCN Species Survival Commission Lagomorph Specialist Group (LSG) and the World Lagomorph Society (WLS) are pleased to present this compre-

hensive compendium of all the lagomorphs in the world. This work is designed to expand coverage of the world’s lagomorphs and update the 1990 LSG Lagomorph Action Plan (Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan, compiled and edited by Joseph A. Chapman and John E. C. Flux). The Action Plan has served as the most thorough single source of informa-tion on lagomorphs for biologists, but it was never widely available to the public and it has become outdated. In this book we present updated range maps of all lagomorph species, high- quality images of most species, as well as current information on identification, systematics, ecol-ogy, behavior, reproduction, genetics, physiology, and con-servation and management of the pikas, rabbits, and hares of the world. The book also summarizes key components

PREFACE

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Fernando BallesterosSistemas Naturalesc/ Santa Susana 15 3° COviedo, Spain

Ron BarryP. O. Box 471Lewiston, Maine, United States

Amando BautistaCentro Tlaxcala de Biología de la ConductaUniversidad Autónoma de TlaxcalaTlaxcala, Mexico

Penny A. BeckerWashington Department of Fish and WildlifeOlympia, Washington, United States

Erik A. BeeverU.S. Geological SurveyNorthern Rocky Mountain Science CenterBozeman, Montana, United States

Hichem Ben SlimenHigh Institute of Biotechnology of BéjaBéja, Tunisia

Joel BergerDepartment of Fish, Wildlife and Conservation BiologyColorado State UniversityFort Collins, Colorado, United States

Pelayo AcevedoInstituto de Investigación en Recursos CinegéticosCiudad Real, Spain

Maria AltemusSchool of Natural Resources and the EnvironmentUniversity of ArizonaTucson, Arizona, United States

Sergio Ticul Álvarez- CastañedaCentro de Investigaciones Biológicas del NoroesteLa Paz, Baja California Sur, Mexico

Paulo C. AlvesFaculdade de Ciências & CIBIOUniversidade do Porto, Campus de VairãoVairão, Vila do Conde, Portugal

Nguyen The Truong AnLeibniz Institute for Zoo and Wildlife ResearchBerlin, Germany

Anders AngerbjörnDepartment of ZoologyStockholm UniversityStockholm, Sweden

Asma AwadiFaculty of Sciences of TunisUniversity El ManarTunis, Tunisia

CONTRIBUTORS

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x Contributors

Leah K. BerkmanCooperative Wildlife Research LaboratorySouthern Illinois UniversityCarbondale, Illinois, United States

Sabuj BhattacharyyaMolecular Ecology LaboratoryCentre for Ecological SciencesIndian Institute of ScienceBangalore, Karnataka, India

Jorge BolañosEl Colegio de la Frontera SurDepartamento de Conservación de la BiodiversidadSan Cristóbal de Las Casas, Chiapas, Mexico

Never BoninoInstituto Nacional de Tecnologica AgropecuariaBariloche, Argentina

Christy J. BraggDrylands Conservation ProgrammeThe Endangered Wildlife TrustSouth Africa

David E. BrownSchool of Life SciencesArizona State UniversityTempe, Arizona, United States

Arturo Carrillo- ReyesOikos: Conservación y Desarrollo SustentableSan Cristóbal de Las Casas, Chiapas, Mexico

Fernando A. CervantesInstituto de Biología, UNAMColección Nacional de MamíferosDistrito Federal, Mexico

Kai CollinsMammal Research InstituteDepartment of Zoology & EntomologyUniversity of PretoriaPretoria, South Africa

Brian D. CookeInstitute for Applied EcologyUniversity of CanberraCanberra, Australia

Mayra de la PazCentro de Investigaciones Biológicas del NoroesteLa Paz, Baja California Sur, Mexico

Miguel Delibes- MateosCIBIO, Universidade do PortoCampus Agrario de VairãoVairão, Vila do Conde, Portugal

Robert C. DowlerDepartment of Biology, Angelo State UniversitySan Angelo, Texas, United States

Ricardo Farrera- MuroInstituto Tecnológico de Estudios Superiores de

MonterreyCampus Puebla, Puebla, Mexico

Craig FaulhaberFlorida Fish and Wildlife Conservation CommissionOcala, Florida, United States

John E. C. Flux23 Hardy Street, WaterlooLower Hutt, Wellington, New Zealand

Johnnie FrenchDepartment of BiologyPortland State UniversityPortland, Oregon, United States

Antonio García- MéndezEl Colegio de la Frontera SurDepartamento de Conservación de la BiodiversidadSan Cristóbal de Las Casas, Chiapas, Mexico

Fernando Gopar- MerinoCentro de Investigaciones en Geografia AmbientalUniversidad Nacional Autonoma de MexicoMorelia, Michoacán, Mexico

Thomas GrayWWF—Greater MekongPhnom Penh, Cambodia

Klaus HackländerUniversity of Natural Resources and Life Sciences ViennaInstitute of Wildlife Biology and Game ManagementVienna, Austria

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Contributors xi

David C. D. HappoldResearch School of BiologyAustralian National UniversityCanberra, A.C.T., Australia

Jeremy HoldenFlora and Fauna InternationalCambridge, United Kingdom

Yeong- Seok JoDivision of Animal ResearchNational Institute of Biological ResourcesIncheon, South Korea

Charlotte H. JohnstonSchool of Life SciencesArizona State UniversityTempe, Arizona, United States

Patrick A. KellyDepartment of Biological SciencesCalifornia State University, StanislausTurlock, California, United States

Howard Kilpatrick391 Rt. 32North Franklin, Connecticut, United States

Adrienne KovachUniversity of New HampshireDurham, New Hampshire, United States

Charles J. KrebsDepartment of ZoologyUniversity of British ColumbiaVancouver, British Columbia, Canada

Hayley C. LanierDepartment of Zoology and PhysiologyUniversity of WyomingCasper, Wyoming, United States

John W. LaundréJames San Jacinto Mountains Natural ReserveIdyllwild, California, United States

Antonio LavazzaVirology Department, IZSLERBrescia, Italy

Weidong LiNatural Ecological Protection StudioÜrümqi, Xinjiang, China

Andrey LissovskyZoological Museum, Moscow State UniversityMoscow, Russia

John A. LitvaitisDepartment of Natural Resources and the EnvironmentUniversity of New HampshireDurham, New Hampshire, United States

Marian LitvaitisDepartment of Natural Resources and the EnvironmentUniversity of New HampshireDurham, New Hampshire, United States

Shaoying LiuSichuan Academy of ForestryChengdu, Sichuan, China

Consuelo LorenzoEl Colegio de la Frontera SurDepartamento Conservación de la BiodiversidadSan Cristóbal de Las Casas, Chiapas, Mexico

Debbie MartyrFauna & Flora International- Indonesia ProgrammeRagunan, Jakarta, Indonesia

Conrad A. MattheeDepartment of Botany and ZoologyStellenbosch UniversityStellenbosch, South Africa

Jennifer L. McCarthyUniversity of Delaware, Associate of Arts ProgramWilmington, Delaware, United States

Robert McCleeryDepartment of Wildlife Ecology and ConservationUniversity of FloridaGainesville, Florida, United States

José Melo- FerreiraCIBIO, Centro de Investigação em Biodiversidade e

Recursos GenéticosInBIO Laboratório Associado & Faculdade de CiênciasUniversidade do PortoPorto, Portugal

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xii Contributors

José M. MoraInstituto Internacional en Conservación y Manejo de Vida

SilvestreUniversidad NacionalHeredia, Costa Rica

Sanjay MolurZoo Outreach OrganizationCoimbatore, Tamil Nadu, India

Dennis L. MurrayDepartment of BiologyTrent UniversityPeterborough, Ontario, Canada

P. O. NameerCentre for Wildlife StudiesKerala Agricultural University Thrissur City, Kerala, India

Clayton K. NielsenCooperative Wildlife Research Laboratory and

Department of ForestrySouthern Illinois UniversityCarbondale, Illinois, United States

Janet L. RachlowDepartment of Fish and Wildlife SciencesUniversity of IdahoMoscow, Idaho, United States

Juan Pablo Ramírez- SilvaPrograma Académico de BiologíaUnidad Académica de AgriculturaUniversidad Autónoma de NayaritXalisco, Nayarit, Mexico

Chris RayInstitute for Arctic and Alpine ResearchUniversity of ColoradoBoulder, Colorado, United States

Tamara Rioja- ParadelaSustentabilidad y Ecología AplicadaUniversidad de Ciencias y Artes de ChiapasTuxtla Gutiérrez, Chiapas, Mexico

Terry J. RobinsonDepartment of Botany and ZoologyStellenbosch UniversityMatieland, South Africa

Luisa Rodríguez- Martínez Centro Tlaxcala de Biología de la ConductaUniversidad Autónoma de TlaxcalaTlaxcala, Mexico

Luis A. RuedasDepartment of BiologyPortland State UniversityPortland, Oregon, United States

Eugenia C. Sántiz- LópezEl Colegio de la Frontera SurDepartamento de Conservación de la BiodiversidadSan Cristóbal de Las Casas, Chiapas, Mexico

Stéphanie Schai- BraunUniversity of Natural Resources and Life Sciences ViennaInstitute of Wildlife Biology and Game ManagementVienna, Austria

Lisa A. ShipleySchool of the EnvironmentWashington State UniversityPullman, Washington, United States

Andrew T. SmithSchool of Life SciencesArizona State UniversityTempe, Arizona, United States

Adia SovieDepartment of Wildlife Ecology and ConservationUniversity of FloridaGainesville, Florida, United States

Andrew TilkerLeibniz Institute for Zoo and Wildlife ResearchBerlin, Germany, andGlobal Wildlife ConservationAustin, Texas, United States

Zelalem Gebremariam TolesaDepartment of BiologyHawassa UniversityHawassa, Ethiopia

Myles B. TraphagenWestland Resources, Inc.Tucson, Arizona, United States

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Contributors xiii

Julieta VargasInstituto de Biología, UNAMColección Nacional de MamíferosDistrito Federal, Mexico

Jorge VázquezCentro Tlaxcala de Biología de la ConductaUniversidad Autónoma de TlaxcalaTlaxcala, Mexico

Alejandro Velázquez Centro de Investigaciones en Geografia AmbientalUniversidad Nacional Autonoma de MexicoMorelia, Michoacán, Mexico

Rafael VillafuerteIESA- CSICCampo Santo de los Mártires 7Códoba, Spain

Fumio YamadaDepartment of Wildlife BiologyForestry and Forest Products Research InstituteMatsunosato 1, Tsukuba, Ibaraki, Japan

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144 Sylvilagus insonus

gramme (MAB- ICC) added the Tres Marías Islands to the UNESCO’s World Network of Biosphere Reserves, with the aim of integrating conservation of biodiversity and management of natural resources.

account authors: Consuelo Lorenzo, Juan Pablo Ramírez- Silva, Fernando A. Cervantes, and Ricardo Farrera- Muro

Key References: Acevedo 1995; Ceballos and Navarro 1991; Cer-vantes 1997; Chapman and Ceballos 1990; Chapman et al. 1990; Diersing and Wilson 1980; Dooley 1988; Hall 1981; Lorenzo et al. 1993; Nelson 1899; SEMARNAT 2010; Wilson 1991.

Sylvilagus insonus (Nelson, 1904)

Omiltemi Rabbit

OTHER COMMON NAMES: Omiltemi cottontail; Conejo de Omiltemi, Conejo (Spanish)DESCRIPTION: The Omiltemi rabbit is a medium- sized cottontail that has a short tail, medium- sized hind feet, and medium- sized ears. The dorsal and nape pelage is rufous black. The ears are black- brown, the sides are grayish black, and the tail is reddish black on the dorsal surface and dingy buffy on the ventral surface. The sides of the nose and the orbital area have dingy buffy grayish coloration. The ventral surface of the cottontail rabbit is

buffy brown. There is a significant amount of white on the dorsal surface of the hind feet. The skull is medium- sized with a long palate; it has a broad braincase, a narrow breadth across the nasals, large maxillary and mandibular tooth rows, short incisive foramina, a short diastema, a narrow basioccipital, and medium- sized auditory bullae, and is broad across the carotid foramina with a narrow breadth across the infra-orbital canals. The shield- bulla depth is shallow as well as the skull depth. The supraoccipital shield is squared, and the posterior section of the supraorbital process is slender and flat.SIZE: Head and body 398–440 mm; Tail 40–45 mm; Hind foot 89–104 mm; Ear 60–76 mm; Greatest length of skull 77–78 mmCURRENT DISTRIBUTION: The Omiltemi rabbit has a very restricted distribution, less than 500 km² within the Sierra Madre del Sur, Guerrero, Mexico. This rabbit lives in a highly fragmented area within a natural reserve, the Omiltemi State Park (Parque Ecológico Estatal Omiltemi) in the Sierra Madre del Sur. It occurs at elevations be-tween 2,133 and 3,505 m.TAXONOMY AND GEOGRAPHIC VARIATION: No sub-species. The phylogenetic relationship of S. insonus with other species of Sylvilagus is unclear. Morphological comparisons between the tapetí (S. brasiliensis), Dice’s cottontail (S. dicei), and the Omiltemi rabbit indicate that the tapetí and Dice’s cottontail are more closely related to each other than either is to the Omiltemi rabbit. The Omiltemi rabbit is one of the most poorly known of all mammals; it is represented by only five museum speci-mens, four complete and one with only a skin.ECOLOGY: Very little is known about the natural history of the Omiltemi rabbit. It is sympatric with the Mexican cottontail (S. cunicularius). It creates runways within the dense undergrowth, and occupies burrows under rocks or other similar shelters.HABITAT AND DIET: The preferred habitat of the Omiltemi rabbit is dense cloud forest, where pines (Pinus), oaks (Quercus), and alders (Alnus) are abundant.BEHAVIOR: The Omiltemi rabbit is mainly a nocturnal species.PHYSIOLOGY AND GENETICS: Comparative phylogenetic analysis based on partial sequences (560 bp) of the gene 16S between eight species of Sylvilagus showed that the Omiltemi rabbit is most closely related to the desert cot-tontail (S. audubonii) and the Mexican cottontail instead of the tapetí as had been proposed previously. The sym-patric distribution between the Omiltemi rabbit and the

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Sylvilagus mansuetus 145

Mexican cottontail (in Guerrero, Mexico) seems to sup-port the close relationship between these species. Genetic analysis using partial sequences of cytochrome b gene revealed an average genetic divergence of 15% between the Omiltemi rabbit and the Mexican cottontail.CONSERVATION STATUS: IUCN Red List Classification: Endangered (EN)—B2ab(ii,iii) National- level Assessments: Mexico (Endangered Offi-cial Norm NOM-059-ECOL-2010 (SEMARNAT))MANAGEMENT: Scientists consider the Omiltemi rabbit to be one of the most endangered mammals in the world. Deforestation is a serious threat to the Omiltemi rabbit, as the forests within its known range have been exten-sively logged, resulting in habitat fragmentation. Cattle grazing accompanies the deforestation and intensifies the threat. Hunting of the Omiltemi rabbit remains a concern even though most of the known range has been incorporated into a natural reserve area. The type local-ity of the Omiltemi rabbit is located within the Omiltemi State Ecological Park, which has been declared a natural reserve area (~ 3,613 ha). Intensive studies are necessary to determine whether the Omiltemi rabbit still exists and to confirm its current local distribution. Research and a risk assessment analysis should focus on habitat require-ments and the survival of this threatened species. Until such information is available, a comprehensive conser-vation strategy for this species and its habitat cannot be developed.

account authors: Consuelo Lorenzo, Fernando A. Cervantes, Julieta Vargas, and Ricardo Farrera- Muro

Key References: AMCELA 2008c; Cervantes and Lorenzo 1997a; Cervantes et al. 2004; Chapman and Ceballos 1990; Diersing 1981; González- Cózatl et al. 2007; Hall 1981; Jiménez- Almaraz et al. 1993; Lorenzo et al. 2015; Nelson 1904, 1909; SEMARNAT 2010.

Sylvilagus mansuetus Nelson, 1907

San José Brush Rabbit

OTHER COMMON NAMES: Conejo de la Isla San José (Spanish)DESCRIPTION: The San José brush rabbit is a medium- sized rabbit. The dorsal part is pale brown mixed with yellowish gray at the top of the back and head, slightly

obscured by the black tip of each hair. The sides of the body are paler gray than the back. The ears are brown to pale mixed with gray and have whitish hairs on the inside. The sides of the neck are paler than the sides of the body, and the throat is gray mixed with white. The front legs are ochre- colored clay, and the hind legs are yellowish white. The ventral part of the body is white mixed with gray, and the ventral part of the tail is pale white. Proportionally, the skull of the San José brush rabbit is longer and narrower than that of the closely related brush

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Sylvilagus mansuetus. Photo courtesy Arturo Carrillo- Reyes

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