Acta Chiropterologica, 18(1): 1–38, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.001

Higher level classification of phyllostomid with a summary of DNA synapomorphies

ROBERT J. BAKER1, SERGIO SOLARI2, ANDREA CIRRANELLO3, and NANCY B. SIMMONS4

1Department of Biological Sciences and Museum, Texas Tech University, Lubbock, TX 79409, USA 2Instituto de Biología, Universidad de Antioquia, Medellín, Colombia 3Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA 4Division of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA 5Corresponding author: E-mail: [email protected]

The family Phyllostomidae is recognized as representing the most extensive radiation known in any mammalian family. Creating a Linnaean classification for this clade has been difficult and controversial. In two companion papers, we here propose a revised classification drawing on the strengths of genetic and morphological data and reflecting current ideas regarding phylogenetic relationships within this monophyletic clade. We recognize 11 subfamilies (Macrotinae, Micronycterinae, Desmodontinae, , Glossophaginae, Lonchorhininae, Lonchophyllinae, Glyphonycterinae, , Rhinophyllinae, and ), 12 tribes (Diphyllini, Desmodontini, Macrophyllini, Phyllostomini, Vampyrini, Glossophagnini, Brachyphyllini, Choeronycterini, Lonchophyllini, Hsunycterini, Sturnirini, and Stenodermatini), and nine subtribes (Brachyphyllina, Phyllonycterina, Anourina, Choeronycterina, Vampyressina, Enchisthenina, Ectophyllina, Artibeina, and Stenodermatina). The proposed arrangement avoids non-monophyletic associations, only keeping those detected based on analyses of DNA sequence data. We propose that a classification based on the strengths of the most complete morphological and genetic data sets will provide the most robust classification for multiple uses by science and society.

Key words: Phyllostomidae, higher-level classification, DNA sequence data

INTRODUCTION Dávalos et al., 2014). Because this ecomorphologi- cal diversity has fascinated scientists for over a cen- The family Phyllostomidae (New World leaf- tury, Phyllostomidae is one of the best-known and nosed bats) comprises more than 200 species in 60 well-studied chiropteran groups (Jones et al., 2002). genera (see Solari and Martínez-Arias, 2014; Hur- Although comparative studies abound in the litera- tado and Pacheco, 2014), and is the second most ture, remarkably different systematic and phyloge- speciose chiropteran family (Simmons, 2005). The netic analyses have been proposed based on differ- family has undergone a radiation unparalleled in ent data sets and analysis methods (see reviews in other mammalian families in terms of ecological and Wetterer et al., 2000, and Baker et al., 2003). Until morphological diversity (Freeman, 2000; Dumont et recently, there has been little agreement regarding al., 2012). Phyllostomidae encompasses a range of the deep branching patterns and relationships in this dietary diversity larger than that seen in any other remarkable radiation, leading to considerable insta- monophyletic family, including omnivo- bility in classifications (Simmons, 2005; Baker et rous, insectivorous, carnivorous, nectarivorous, fru- al., 2012; Dávalos et al., 2012, 2014). Because of givorous and even hematophagous species (Gard- their diversity, abundance, and ubiquity across the ner, 1977a; Ferrarezzi and Gimenez, 1996; Dumont Neotropics, phyllostomid bats are the main focus of et al., 2012). Ecological variation in diets is associ- a number of research efforts; therefore, a well-sup- ated with extensive morphological diversity that ported and stable classification is highly desirable to involves skeletal, muscle, digestive, kidney, sensory communicate information among those studying systems, and behavior (Phillips, 2000; Wetterer et this family as well as those in other fields who ap- al., 2000; Dumont, 2004; Monteiro and Nogueira, preciate the biodiversity within this complex. The 2011; Baker et al., 2012; Dumont et al., 2012; categories of phyllostomid bats showing the least Acta Chiropterologica, 18(1): 39–71, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.002

Morphological diagnoses of higher-level phyllostomid taxa (Chiroptera: Phyllostomidae)

ANDREA CIRRANELLO1, 2, 5, NANCY B. SIMMONS1, SERGIO SOLARI3, and ROBERT J. BAKER4

1Division of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA 2Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA 3Instituto de Biología, Universidad de Antioquia, Medellín, Colombia 4Department of Biological Sciences and Museum, Texas Tech University, Lubbock, TX 79409, USA 5Corresponding author: E-mail: [email protected]

Phyllostomidae (New World leaf-nosed bats), the second most speciose chiropteran family, is one of the best-known and well- studied chiropteran groups. Due to the ecological and morphological diversity of this family, comparative studies of phyllostomids abound in the literature, and numerous systematic and phylogenetic analyses have been published. Unfortunately, many of these studies have reached different conclusions concerning phyllostomid relationships, and have proposed different classification schemes. This has led to confusion, and highlighted the need for a well-supported and stable classification of the family, particularly at the level of subfamilies and tribes, areas of the greatest controversy. The goal of this paper is to provide morphological diagnoses of higher-level taxa (subtribes, tribes, and subfamilies). Herein we provide morphological diagnoses for 11 subfamilies (Macrotinae, Micronycterinae, Desmodontinae, Lonchorhininae, Phyllostominae, Glyphonycterinae, Glossophaginae, Lonchophyllinae, Carollinae, Rhinophyllinae, and Stenodermatinae), 12 tribes (Desmodontini, Diphyllini, Macrophyllini, Phyllostomini, Vampyrini, Choeronycterini, Glossophagini, Brachyphyllini, Lonchophyllini, Hsunycterini, Sturnirini, and Stenodermatini), and nine subtribes (Anourina, Choeronycterina, Brachyphyllina, Phyllonycterina, Vampyressina, Enchisthenina, Ectophyllina, Artibeina, and Stenodermatina).

Key words: morphology, taxonomy, Phyllostomidae

INTRODUCTION I have founded the fourth great school of classifica- tion, the It-Doesn’t-Matter-Very-Much school.” Classification and taxonomy are often regarded Although we respect Felsenstein’s (2004) view as boring exercises in bookkeeping, but scientific that it is the phylogeny that matters, referencing names provide a critical framework for storage and nodes on a phylogeny by numbers or letters — or re- communication of scientific knowledge. Herein, we producing large phylogenies simply to be able to define taxonomy as the description, naming, and talk about them — is cumbersome and can hinder classification of organisms. At alpha taxonomic lev- effective scientific communication. To us, higher els (i.e., the level of the species), the importance of level taxonomy is important because it provides taxonomy is clear — it is difficult to imagine setting names, increasingly applied to clades that have been conservation priorities or conducting most field re- supported by data and tested through systematic re- search without first identifying study organisms to search. This shorthand approach to discussion of species. However, at higher taxonomic levels, this phylogenetic groups is both satisfying and neces- clarity of purpose may not be as obvious. To quote sary. Names of phylogenetic groups are used in Felsenstein (2004: 145): studies concerned with evolution (e.g., adaptive “A phylogenetic systematist and an evolutionary radiation, or biogeography), ecology (e.g., behav- systematist may make very different classifications, ioral ecology), and conservation biology (e.g., while inferring much the same phylogeny. If it is hotspot location, identification of unique lineages). the phylogeny that gets used by other biologists, We believe that having a well-supported and stable their differences about how to classify may not be classification for any group reduces confusion that important. I have consequently announced that among non-experts, enabling productive discussion, Acta Chiropterologica, 18(1): 73–90, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.003

The evolutionary history of the African fruit bats (Chiroptera: Pteropodidae)

FRANCISCA CUNHA ALMEIDA1, 3, 4, NORBERTO PEDRO GIANNINI1, 2, and NANCY B. SIMMONS1

1Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA 2Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET),Unidad Ejecutora Lillo, Miguel Lillo, 205, San Miguel de Tucumán, 4000, Argentina 3Current address: Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Intendente Güiraldes y Costanera Norte s/n, Pabellón II - Ciudad Universitaria, 1428, Capital Federal, Argentina 4Corresponding author: E-mail: [email protected]

Bats of the family Pteropodidae, also known as megabats or Old World fruit bats, are widely distributed in tropical areas of Africa, Asia, and Oceania. Of 45 genera in the family, 12 are endemic to the Afro-tropical region and two others have representative species on the African continent. African megabats inhabit wooded habitats and are nearly ubiquitous on the mainland and nearby islands with the exception of desert areas. Some species have been implicated as possible reservoirs of the Ebola Zaire virus. We studied the phylogenetic relationships of mainland African megabats using both mitochondrial and nuclear loci in separate and combined analyses. The phylogenetic trees obtained showed four main African clades: Eidolon, Scotonycterini (including two genera), African Rousettus (three species), and the previously identified ‘endemic African clade’ (nine genera). The latter three lineages form a clade that also includes the Asian species of Rousettus and the Asian genus Eonycteris; Eidolon does not show close relationships to other African genera, instead nesting elsewhere in the megabat tree. Although our results confirm many of the conclusions of previous studies, they challenge the taxonomic status and placement of Epomops dobsonii and Micropteropus, and provide evidence indicating that a new classification at subfamilial and tribal levels is highly desirable. The principal clades we detected represent four independent colonizations of Africa from most probably Asian ancestors. Estimates of divergence dates suggest that these events occurred in different periods and that although local diversification appears to have started in the late Miocene, the more extensive diversification that produced the modern fauna occurred much later, in the Pleistocene.

Key words: phylogenetic analysis, Africa, Epomophorinae, molecular systematics, molecular clock, pteropodids, Rousettus, classification

INTRODUCTION 11 genera almost exclusively found in continental Africa. Bergmans’ (1997) Epomophorinae included Megabats (Mammalia: Chiroptera: Pteropodi- species previously widely separated in the tradi- dae) represent a monophyletic group of mostly non- tional taxonomy, i.e., taxa included by Ander sen echolocating, phytophagous bats specialized for (1912) in the subfamilies Cynopterinae (Myo- consumption of fruit and flower products (nectar nycteris), Rousettinae (Lissonycteris) and Macro - and pollen — Kunz and Pierson, 1994). Pteropodids glossinae (Megaloglossus). Bergmans (1997) sub - are distributed along the Old World tropics from divided the epomophorines into four tribes: western Africa to eastern Polynesia (Kunz and Pie r - Epo mophorini (genera Epomophorus, Epomops, son, 1994), and within this range Sub-Saharan Afri - Hypsignathus, Micropteropus, and Nanonycteris), ca represents the largest land area where they occur. Myonycterini (Myonycteris, Lissonycteris, and The African megabat fauna includes species from Megaloglossus), Plerotini (with the monotypic several clades that may have arrived, or evolved, in- Plerotes), and Scotonycterini (Scotonycteris and dependently on the continent and adjacent islands. Ca si nycteris). Early molecular phylogenetic analy- Epomophorinae sensu Bergmans (1997) is the ses were in agreement with the existence of an en- largest group of African Pteropodidae, comprising demic African clade that included the former two Acta Chiropterologica, 18(1): 91–116, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.004

Evolutionary scenarios associated with the Pteronotus parnellii cryptic species-complex (Chiroptera: Mormoopidae)

RICARDO LÓPEZ-WILCHIS1, 6, MAYELA FLORES-ROMERO2, LUIS M. GUEVARA-CHUMACERO1, ALEJANDRA SERRATO-DÍAZ3, JHOANA DÍAZ-LARREA3, FERNANDO SALGADO-MEJIA2, CARLOS IBAÑEZ4, LEANDRO O. SALLES5, and JAVIER JUSTE4

1Departamento de Biología, Universidad Autónoma Metropolitana, Ciudad de México 09340, México 2Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Ciudad de México 09340, México 3Departamento de Hidrobiología, Universidad Autónoma Metropolitana, Ciudad de México 09340, México 4Estación Biológica de Doñana, C.S.I.C., Avda. Américo Vespucio s/n, 41092 Sevilla, Spain 5Museu Nacional/UFRJ, Departamento de Vertebrados.20940-040, Rio de Janeiro, RJ, Brazil 6Corresponding author: E-mail: [email protected]

One of the major challenges to understanding the evolution of Neotropical bats concerns our capacity to successfully scrutinize phylogenetic patterns associated with cases of cryptic species complexes. In this study Pteronotus parnellii is examined as a selected example of a known lineage of mormoopid that potentially contains several cryptic species. A samples of 452 individuals from 83 different localities, essentially covering its entire mainland distribution, was evaluated using two genetic markers: COI (mitochondrial) and DBY (nuclear) genes. The findings of this study strongly support the hypothesis of high genetic variability and identify at least six lineages within P. parnellii, some of which appear to be cryptic species.

Key words: bats, COI, DBY, Neotropical America, genetic diversity, biogeography, phylogeny, taxonomy

INTRODUCTION The family has only two genera, Mormoops Leach, 1821 and Pteronotus Gray, 1838; both com- The Neotropical region is home to the greatest prising insectivorous, gregarious, and strict cave- diversity of bats in the world, and it is well known dwelling bats, which are found in a wide variety of that this fauna awaits a number of basic lines of re- habitats, ranging from tropical rainforests to arid re- search, among which cryptic diversity stands as one gions, being particularly abundant in low dry forests of the most relevant. Thus, despite recent efforts to throughout the Neotropics. The genus Mormoops address the issue, not only in the Neotropics (Clare, has two species, Mormoops blainvillei Leach, 1821 2011; Clare et al., 2011; Pavan et al., 2011, 2013; which is distributed across the Greater Antilles and Hernández-Dávila et al., 2012; Larsen et al., 2012; small adjacent islands, and M. megalophylla (Peters, Velazco and Patterson, 2013; Parlos et al., 2014) but 1864), with an extant distribution extending from also in several other regions of the world (Mayer Mexico to northwestern South America, and the and von Helversen, 2001; Ibáñez et al., 2006; Fur - West Indies. Pteronotus consists of a diverse group man et al., 2010; Raghuram et al., 2014; Bogdano- of six currently recognized species: P. davyi Gray, wicz et al., 2015; Dammhahn et al., 2015; Has sanin 1838; P. gymnonotus Naterer, 1843; P. parnellii et al., 2015), cryptic species complexes have become (Gray, 1843) and P. personatus (Wagner, 1843), a top priority for a number of international agendas. which are all distributed from Mexico to Brazil, and Pteronotus parnellii is investigated here as a special P. macleayi (Gray, 1843) and P. quadridens (Gund - case in which to study cryptic species among Neo - lach, 1840), which are known from the Antilles and tropical bats, considering that due to its wide distri- the Bahamas (Simmons, 2005). bution and low morphological differentiation, the Pteronotus parnellii, as the most widely distrib- family Mormoopidae is an excellent subject for this uted species, is considered to be the basal branch kind of analysis. associated with the origin of the genus (Smith, 1972; Acta Chiropterologica, 18(1): 117–139, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.005

Hill forest dweller: a new cryptic species of Rhinolophus in the ‘pusillus group’ (Chiroptera: Rhinolophidae) from Thailand and Lao PDR

PIPAT SOISOOK1, 10, SUNATE KARAPAN2, MATTANA SRIKRACHANG3, ARIYA DEJTARADOL4, KWAN NUALCHAROEN4, SARA BUMRUNGSRI4, SAI SEIN LIN OO5, MOE MOE AUNG6, PAUL J. J. BATES7, MARGARITA HARUTYUNYAN8, MAGDALENA M. BUŚ9, and WIESŁAW BOGDANOWICZ9

1Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand 90110 2Halabala Wildlife Research Station, Wildlife Research Division, Wildlife Conservation Bureau, Department of National Parks, Wildlife and Plant Conservation, Wang, Narathiwat, Thailand 90160 3Wildlife Research Division, Wildlife Conservation Bureau, Department of National Parks, Wildlife and Plant Conservation, Phahonyothin Street, Jatuchak, Bangkok, Thailand 10900 4Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand 90110 5Department of Zoology, University of Mandalay, Mandalay, Myanmar 6Department of Zoology, University of Yangon, Yangon, Myanmar 7Harrison Institute, Centre for Systematics and Biodiversity Research, Bowerwood House, St. Botolph’s Road, Sevenoaks, Kent, TN13 3AQ, United Kingdom 8Bio-medical Department, Russian-Armenian (Slavonic) State University, 123 Hovsep Emin Street, 375051 Yerevan, Armenia 9Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warszawa, Poland 10Corresponding author: E-mail: [email protected]

A new species of Rhinolophus in the pusillus group is described from Ratchaburi, Kamphaeng Phet and Loei Provinces where it was found in evergreen forest at elevations ranging from 550 to 1,320 m a.s.l. It is distinguished from R. shortridgei and other similar species in the same group by its broad, parallel-sided sella, which is squared-off at the tip, relatively large body size with a forearm length of 42.2–44.1 mm, and bulbous rostral swellings. The echolocation frequency from hand-held individuals is 84.1–93.0 kHz. Bayesian analyses of a 654 bp of cytochrome oxidase subunit I (DNA barcode), and an 878 bp fragment of cytochrome b also support differences at the species level. Three specimens from Loaung Namtha, Lao PDR are referred to this new species based on DNA barcodes. Based on distinctive DNA barcodes and craniodental morphology, the taxon refulgens, is here regarded as a separate species from R. lepidus. Morphological comparisons between similar species are discussed and notes on ecology included.

Key words: new species, Rhinolophus, horseshoe bats, Thailand, evergreen forest, Southeast Asia

INTRODUCTION During a series of bat surveys in Thailand from 2006 through 2013, seven specimens of an unknown Horseshoe bats in the Rhinolophus pusillus Rhinolophus in the pusillus group were collected in group are characterised by a pointed connecting evergreen forest in three mountain ranges in Loei, process and high anterior median swellings (Csorba Ratchaburi and Kamphaeng Phet Provinces. Based et al., 2003). They are found in the Indian Sub - on forearm length and skull size and shape, these continent, throughout Southeast Asia, and eastwards specimens were provisionally identified as ‘R. cf. to Japan. Csorba et al. (2003) and Simmons (2005) shortridgei’. In addition, further specimens of listed 11 species belonging to this group. Recent R. shortridgei were recently collected from Myan- studies of the morphology and echolocation (Dejta - mar, which provide further data for the comparative radol, 2009) and genetics (Francis et al., 2010) of study. The morphology of the Thai specimens and the R. pusillus group in Southeast Asia suggest it is R. shortridgei, including the holotype from Myan- very complex and has high cryptic diversity. mar, with additional data on echolocation and Acta Chiropterologica, 18(1): 141–161, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.006

Geographical variation of Rhinolophus affinis (Chiroptera: Rhinolophidae) in the Sundaic subregion of Southeast Asia, including the Malay Peninsula, Borneo and Sumatra

SAVENG ITH1, 2, 3, 12, SARA BUMRUNGSRI2, NIKKY M. THOMAS4, PAUL J. J. BATES4, DEMIAN A. WILLETTE5, FAISAL ALI ANWARALI KHAN6, MONWADEE WONGLAPSUWAN7, PIPAT SOISOOK8, IBNU MARYANTO9, JOE CHUN-CHIA HUANG10, and NEIL M. FUREY3, 11

1Department of Biology, Faculty of Science, Royal University of Phnom Penh, Confederation of Russia Boulevard, Cambodia 2Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90112, Thailand 3Centre for Biodiversity Conservation, Room 415, Department of Biology, Faculty of Science, Royal University of Phnom Penh, Confederation of Russia Boulevard, Cambodia 4Harrison Institute, Bowerwood House, St Botolph’s Road, Sevenoaks, Kent, TN13 3AQ, United Kingdom 5Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, 90095, USA 6Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia 7Department of Molecular Biotechnology and Bioinformatics, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90112, Thailand 8Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90112, Thailand 9Museum Zoologicum Bogoriense, Research Center for Biology-Indonesian Institute of Science (LIPI), Widyasatwaloka Jl. Raya Cibinong KM 46, Cibinong, Bogor, Indonesia 10Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA 11Fauna & Flora International, Cambodia Programme, PO Box 1380, #19, Street 360, Boeng Keng Kong 1, Chamkarmon, Phnom Penh, Cambodia 12Corresponding author: E-mail: [email protected]

Rhinolophus affinis sensu lato is a widespread bat species in South and Southeast Asia which shows considerable geographical variation in its morphology, echolocation call frequencies and genetics. The taxonomic status of the taxon in the Sundaic subregion remains uncertain however as the limited studies to date have been largely based on morphology. The aim of the present study was to determine the taxonomic status of subspecific forms recognized in the subregion and to evaluate phylogeographic distinctiveness between those occurring in Borneo and the Malay Peninsula using genetic, morphological and acoustic datasets. Two forms were confirmed: R. a. nesites from Borneo and R. a. superans from the peninsula. The previous recognition of a population from southern- most Sumatra as R. a. superans was not supported, however, as this form is likely R. a. affinis. Genetic divergence between these three forms is rather deep and is estimated to have occurred during the arid climatic period of the Pleistocene when suitable habitats were reduced to isolated pockets. Our results support the phylogeographic distinctiveness hypothesis as R. affinis sensu lato shows discrete affinities between Borneo and the Malay Peninsula. Discovery of new forms of R. affinis is likely with greater sampling effort throughout the region. Our study also demonstrates the importance of employing multiple datasets in taxonomic evaluations, as the use of morphological and/or acoustic datasets alone could lead to erroneous conclusions.

Key words: echolocation, genetics, morphology, Rhinolophus affinis, subspecies, Sundaic subregion

INTRODUCTION China, mainland Southeast Asia, Borneo, and Java (Simmons, 2005; Francis, 2008). The taxon exhibits The intermediate horseshoe bat, Rhinolophus considerable morphological and acoustic variation affinis Horsfield, 1823 is a medium-sized rhinolo - across its range (Andersen, 1905; Csorba et al., 2003; phid (forearm length: 45–56 mm) distributed widely Kingsada et al., 2011; Ith et al., 2015). Nine sub- in South and Southeast Asia, ranging from northern species are traditionally recognized: R. affinis affinis In dia (including Andaman Islands), Nepal to southern Horsfield (type locality Java), R. a. an da man ensis Acta Chiropterologica, 18(1): 163–180, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.007

Cranial shape and diet variation in Myotis species (Chiroptera: Vespertilionidae): testing the relationship between form and function

SANDRA MILENA OSPINA-GARCÉS1, 5, EFRAÍN DE LUNA2, L. GERARDO HERRERA M.3, and JOSÉ JUAN FLORES-MARTÍNEZ4

1Posgrado en Ciencias Biológicas. Instituto de Biología, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, Distrito Federal, 04510, Mexico 2Instituto de Ecología A.C., Biodiversidad y Sistemática, Xalapa, Veracruz 91070, Mexico 3Estación de Biología de Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, A.P. 21, San Patricio, Jalisco, 48980, Mexico 4Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, Distrito Federal, 04510, Mexico 5Corresponding author: E-mail: [email protected]

The relationship between cranial morphology and diet has long been investigated in bats. Bats of the genus Myotis include insectivorous, facultatively piscivorous, and piscivorous species. We tested the hypothesis that facultatively piscivorous (five Myotis species) and piscivorous species (M. vivesi) present cranial morphological and functional changes with respect to insectivorous taxa (16 Myotis species). Cranial shapes in skull and mandible modules were described with four geometric landmark configurations in these dietary groups. Gape capacity was measured with the stretch factors for temporal and masseter muscles. Geometric configurations from two skull and two mandible shapes were analyzed to detect differences in cranial morphology in relation to diet. Differences in cranial morphology were found between piscivorous and insectivorous species involving the mandibular process where masticatory muscles are attached. Linear regression analysis of Procrustes distances and gape capacity showed that the shape of the mandibular process region was highly correlated with the stretch factor of the masseter muscle in piscivorous and facultatively piscivorous species. These results suggest differences in cranial morphology and performance among diets but the hypothesis of gradual changes in cranial shape among diets was only accepted for the mandible and not for the skull. Myotis vivesi appears to improve mechanical advantage of masticatory muscles at lower gapes, presumably allowing more efficient chewing of slippery prey.

Key words: Myotis, geometric morphometrics, piscivory, stretch factor, masticatory muscles

INTRODUCTION groups are noticeable in Phyllostomidae, a family that includes insectivorous, frugivorous, nectarivo- The relationship between cranial morphology rous, sanguinivorous, and carnivorous species and diet has long been investigated revealing that (Free man, 2000; Nogueira et al., 2005, 2009; Mon - bat species with different diets occupy different teiro and Nogueira, 2009; Dumont et al., 2012). regions of morphospace (Freeman, 1984, 2000; Even within dietary groups, cranial morphology No gueira et al., 2005, 2009; Dumont et al., 2009; varies in relation to food hardness; for example, in- Monteiro and Nogueira, 2009). Previous studies in sectivorous bats that feed on hard-shelled insects bats have also found that large cranial changes have short and thick-jawed skulls whereas those related to different types of prey are located in eating soft-shelled insects have long and delicate anatomic regions of biomechanical relevance, such jaws (Freeman, 1981). as the mandibles, the maxillae, and the processes of Changes in bat cranial morphology associated masticatory muscle insertion (Freeman, 2000; No- with vertebrate diets have been relatively less stud- gueira et al., 2005; Dumont et al., 2009). ied compared to other dietary transitions. Biome- Diet diversification in bats is linked to extensive ch anical data indicate that the skulls of carnivorous cranial shape divergence. For example, differences bats are larger and only modestly modified versions in cranial morphology and bite force among dietary of soft-insect specialists (Freeman, 1979; Giannini Acta Chiropterologica, 18(1): 181–191, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.008

Molecular dietary analysis of the endangered Ozark big-eared bat (Corynorhinus townsendii ingens)

RONALD A. VAN DEN BUSSCHE1, 6, DANA N. LEE1, 2, MEGAN E. JUDKINS1, JENNY E. DYER1, DENISE M. THOMPSON1, RICHARD C. STARK3, WILLIAM L. PUCKETTE4, and BRIAN FULLER5

1Department of Integrative Biology, Oklahoma State University, Stillwater, OK 74078, USA 2Current address: Department of Biology, McMurry University, Abilene, TX 79697, USA 3Ozark Plateau National Wildlife Refuge, United States Fish and Wildlife Service, Tulsa, OK 74129, USA 4Poteau Public School District, 100 Mockingbird Lane, Poteau, OK 74953, USA 5U.S. Fish and Wildlife Service, Oklahoma Ecological Services Field Office, Tulsa, OK 74129, USA 6Corresponding author: E-mail: [email protected]

Molecular techniques allow amplification of a mitochondrial barcoding gene, cytochrome c oxidase (COI), of prey DNA in bat fecal material that can be used to identify insect species. Most studies designed to use a molecular approach for dietary studies of bats suggest that fecal material should be collected within one week of deposit to prevent environmental degradation or contamination. However, Ozark big-eared bats (Corynorhinus townsendii ingens) are highly susceptible to human disturbance. The purpose of this study was to performing a molecular dietary analysis of Ozark big-eared bats. Our study detected 40 species representing two orders (Diptera and Lepidoptera) and 11 families of insects and thus, providing new information regarding dietary habits of Ozark big-eared bats.

Key words: molecular analysis, cytochrome c oxidase, diet, Ozark big-eared bat

INTRODUCTION technique. As an alternative to these methods, re- searchers moved to searching for remains of prey Understanding trophic relationships allows us to in fecal material or in roosts to analyze the diet of better understand how ecosystems function (Duffy several species of bats (Leslie and Clark, 2002; et al., 2007) whereas having precise information Gajdošik and Gaisler, 2004; Burles et al., 2008; Fu - regarding the diet of a species may allow for the kui et al., 2009) or to compare the selection of prey development of improved management or conser- relative to the abundance of prey species in the area vation plans (Marrero et al., 2004; Bradley et al., (Almenar et al., 2008; Salsamendi et al., 2008). 2007; Cristóbal-Azkarate and Arroyo-Rodríguez, Using these methods researchers obtained informa- 2007). Unfortunately, for most species of insectivo- tion regarding dietary preferences of several species rous bats direct observation of feeding is difficult of bats, however the list of prey items is likely resulting in a lack of understanding of trophic rela- incomplete as prey parts could have been missed tionships and precise knowledge of diet. To better due to mastication, digestion (Zeale et al., 2011), under stand the diets of insectivorous bats, re- or decay while resting on the cave floor (Dodd and searchers analyzed prey remains under feeding Lacki, 2007), thereby not providing diagnostic perches (e.g., Poulton, 1929). This approach pro- characters or limiting diagnosis to taxonomic levels vided insight into bat foraging ecology but was lim- above species. ited to the largest prey items and those species that Molecular methods offer an alternative approach utilized feeding perches (Alberdi et al., 2012). This for identifying prey items and can be used with was followed by the inspection of stomach contents DNA that has been degraded due to the diges- (Ross, 1967; Easterla and Whitaker, 1972), which tive process and found in fecal material (Deagle et is applicable to study the diet of any species of al., 2006; King et al., 2008). DNA sequences can bat but requires euthanasia, a no longer preferred serve as prey species-specific barcodes and have Acta Chiropterologica, 18(1): 193–198, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.009

A novel food preference in the greater short-nosed fruit bat, Cynopterus sphinx: mother-pup interaction a strategy for learning

AMBIGAPATHY GANESH1, 2, MURUGAN MUKILAN1, GANAPATHY MARIMUTHU3, and KOILMANI EMMANUVEL RAJAN1, 4

1Department of Science, School of Life Sciences, Bharathidasan University, Tiruchirappalli, 620 024, India 2Department of Basic Sciences, School of Medicine and Health Sciences, University of North Dakota, Grand Forks, ND 58203, USA 3Department of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625 021, India 4Corresponding author: E-mail: [email protected]

The greater short-nosed fruit bat Cynopterus sphinx relies on the diverse food resources available in its habitat, with individuals identifying and discriminating between food sources using their sense of smell, in relation to volatile compounds released from fruit, flowers and leaves. The work detailed in this article tested whether pups learn about novel food from interactions with their mothers during foraging and develop preferences. Mother-pup pairs or pups alone were trained during postnatal days (PND) 46–50 using Mangifera indica as a novel fruit. They were then tested during PND 61–65 for food preferences in relation to a known fruit (Achras sapota) and the novel fruit (M. indica). When the trained pups and untrained pups were tested for food preferences independently, those trained with the mother were found to exhibit significantly more marked preferences for the novel fruit as compared with either the pups trained without their mothers or the untrained pups. They made a greater number of feeding attempts and bouts in respect of the novel fruit. However, pups trained without their mothers and untrained pups also both showed a response to the novel fruit during the later period of testing. The results suggest that mother-pup interactions during the early foraging period may provide an opportunity for C. sphinx pups to learn about novel food sources thanks to their mother. Later they may learn independently on the basis of experience from mother’s milk and/or social interaction with conspecifics.

Key words: Cynopterus sphinx, mother-pup interaction, olfactory learning, food preference

INTRODUCTION locating of fruit under natural conditions (Oldfield et al., 1993). living in groups use different sources of Fruit- and nectar-feeding bats may use spatial information to locate their roosts or food sources. memory to locate previously experienced sources of Young animals in particular may learn about forag- food (Wilson and McNaughton, 1993; Fleming and ing techniques and (palatable/safe) food sources Eby, 2003; Thiele and Winter, 2005; Winter and from their mothers, from the behavior of con- Stich, 2005; Carter et al., 2010), as well as taking specifics, or via self-acquired information (Previde olfactory cues into account in assessing ripeness and and Poli, 1994; Terkel, 1996; Chiu et al., 2010; palatability on the basis of concentrations of volatile Wright et al., 2011; Brumm and Teschke, 2012; compounds originating from fruits and/or flowers Jones et al., 2013). The earlier influence of social (von Helversen et al., 2000; Luft et al., 2003; Sán - interactions on foraging behavior has been tested chez et al., 2006; Hodgkison et al., 2007). Laska for in laboratory conditions that drew on real-world (1990b) observed olfactory preferences in foraging problems (Page and Ryan, 2006), as spp. held in captivity, reporting that odor proved well as in free-ranging animals (Davis and Stamps, more important than the form or texture of fruit. 2004). Spatial memory and olfactory cues are Subsequent studies suggest that odor plays a critical seen to play a prominent role in the social lives of role in the detection and selection of ripe fruits (Luft bats (Voigt and von Helversen, 1999; Bouchard, et al., 2003; Sánchez et al., 2004, 2006). The greater 2001; Bloss et al., 2002; Safi and Kerth, 2003). short-nosed fruit bat, Cynopterus sphinx feeds upon Olfactory cues in particular are essential in the a variety of fruits, flowers and leaves (Bhat, 1994; Acta Chiropterologica, 18(1): 199–207, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.010

Daily and seasonal variation in non-acoustic communicative behaviors of male greater short-nosed fruit bats (Cynopterus sphinx)

D. PARAMANANTHA SWAMI DOSS1, 3, *, VENKATESH NAGARAJAN-RADHA2, *, and SRIPATHI KANDULA1

1School of Biological Sciences, Madurai Kamaraj University, Madurai 625021, India 2School of Biological Sciences, Monash University, Victoria 3800, Australia 3Corresponding author: E-mail: [email protected] *Authors equally contributing to this work

Monthly observations were made at a natural roosting site of Cynopterus sphinx, with a view to the behavior of males being observed over a period of one year. Here, we report seasonal, daily and inter-individual variation in three communicative behaviors engaged in by male bats. The frequency of male behaviors identified as scent-marking, vigorous wing-flapping and the making of an open- wing gesture were found to vary seasonally, depending on the reproductive status of conspecific females in the study colony. The duration of scent-marking was markedly high during mating seasons, in comparison with wing-flapping and wing-gesturing. In mating seasons, the pattern to the daily variation in behavior correlated strongly with the gender of the responder present in the diurnal roost and/or colony. For instance, scent-marking and vigorous wing-flapping were more frequent during late-evening and early-morning hours, mostly when females were absent from the day roost, while male-male encounters were possible. In contrast, wing-gesturing was more frequent during morning and early-evening hours, when females were present in the day roost. The results from our study suggest that male scent-marking and wing-flapping are directed towards competitor males in the colony, with a view to resource-defense behavior being manifested. Furthermore, male wing-gesturing is predicted to be directed towards co-roosting females, with the aim in this case being for some form of social information to be communicated, particularly during the mating season. However, marginal inter-individual variation in the frequency of occurrence of behaviors between seasons was apparent, suggesting that these communicative behaviors could be tied to male-male competition in this species.

Key words: communicative behavior, mate competition, resource defence, scent marking, sociality, wing gesturing

INTRODUCTION a few studies in bats have chosen to address the role of non-acoustic communication in transferring Communication within animal networks plays social information within groups. a crucial role in group formation, as the stability of Sexual selection for communicative behaviors a group depends on the beneficial information trans- has been observed across taxa. More explicitly, sex- ferred within the network of signalers and respon- ual selection acts on behaviors that are linked ders (Seyfarth and Cheney, 2003). Bats are highly closely with copulation and animals’ reproductive social and live in complex social systems fitness (Dixson, 1989). This is to say that commu- (Kerth, 2008). Within groups of bats, there are intri- nicative displays associated with copulatory behav- cate social interactions during which information iors, or in some way transmitting information as is transferred about the availability of roosts, food regarding interest in copulation on the part of sexu- and foraging strategies (Kerth and Reckardt, 2003; ally mature individuals in a group, incur selective Safi and Kerth, 2007). Intra-group communica- pressure at both the inter- and intra-sexual levels tion in bats is sophisticated, and occurs by means (Behr and von Helversen, 2004). This selective pres- of acoustic and non-acoustic signals (Bloss, 1999; sure is particularly strong where it leads to indi- Knörnschild et al., 2012). Acoustic communication viduals’ improved reproductive success (Dixson, has been identified as playing a crucial role in 1989). The suite of behaviors that have been de- driving sociality among echolocating bat species, scribed as subject to inter- and intra-sexual selection and many of the acoustic signals involved are used in bats include male-associated roost construction to communicate social information. However, only behavior, male-associated courtship vocalization, Acta Chiropterologica, 18(1): 209–213, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.011

Opportunistic use of banana flower bracts by soricina

MEGHAN MURPHY1, 5, ELIZABETH L. CLARE2, JENS RYDELL3, YOSSI YOVEL3, YINON BAR-ON3, PHILLIP OELBAUM4, and M. BROCK FENTON1

1Department of Biology, University of Western Ontario, 1151 Richmond Street, London N6A 3K7, Ontario, Canada 2School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, United Kingdom 3Department of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel 4Department of Biology, Dalhousie University, 6299 South Street, Halifax B3H 4R2, Nova Scotia, Canada 5Corresponding author: E-mail: [email protected]

The evolution of cue reception and cue production is well documented. The ability of species to use cues they did not evolve with is important in understanding flexibility in behaviour. We observed Neotropical nectar-feeding bats (Glossophaga soricina) feeding at Old World banana flowers (Musa acuminata) in a Belize garden. The flowers produce a rich source of nectar that is exposed as a bract lifts before dusk. We tested the hypothesis that the bracts serve as beacons to foraging bats and discuss this approach and the use of acoustic information by bats feeding at flowers. We ensonified a bract with cues like those of echolocating G. soricina, which revealed the production of strong echoes from the bract. Additionally, the removal of bracts from the flowers influenced the bats’ flower-visiting behaviour. We suggest that the bats use the echoes from the bract opportunistically as a cue to find the nectar source. Our findings provide an example of an interaction between a plant and flower visitor not reflecting a shared evolutionary past.

Key words: acoustic cues, echolocation, nectar-feeding

INTRODUCTION to the bat pollination syndrome (chiropterophily). This use of acoustic cues can involve beacons and Plant-pollinator systems often involve cues that co-adaptation. Strong echoes from structures on make flowers conspicuous to potential pollinators, flowers or leaves near flowers alert bats to available reducing search time and maximizing visits by de- nec tar and/or pollen. Acoustically conspicuous sirable pollinators. In some cases there is clear evi- structures can thus serve a clear functional role and dence of co-evolution between plants and pollina- make bats more efficient at detecting sources of nec- tors (e.g., Knaden and Hansson, 2013; Riffell et al., tar (e.g., von Helversen and von Helversen, 1999; 2014), but other interactions reflect opportunist- Simon et al., 2011), perhaps setting the stage for co- ic behaviour by pollinators (e.g., Heinrich, 2004). evolution. The bats benefit from nectar and/or pol - Exceptionally long tongues and deep corollas are len and pollinate the plants in the process. examples of co-evolution between bats and plants The Neotropical nectar-feeding bat Glossophaga (Muchala, 2006). In other cases, bats or other ani- soricina shows considerable behavioural flexibility mals can learn to find flowers based on features that in acquiring cues and targets by echolocation, per- did not develop for the purpose of attracting pollina- mitting individuals to change from eating nectar to tors. Rather, the interactions depend on behavioural insects (Clare et al., 2013). This requires flexibility flexibility and ecological fitting (Janzen, 1985). In in cue interpretation and feeding mechanisms, with this context, features may be evolutionary spandrels characteristics such as teeth and tongue morphology (sensu Gould and Lewontin, 1979) in their native and thumb manipulation of the food source. environment, or exaptations (sensu Gould and Vrba, Bananas (genus Musa) originated in South East 1982) when the species invade novel habitats. Asia and have been cultivated for over 6,000 years The discovery of ultrasonic nectar guides (von (Denham et al., 2003). The arrival of bananas in Helversen and von Helversen, 1999) and acoustic the Americas is debated in the literature, with the beacons (Simon et al., 2011) added a new dimension earliest estimated date around 200 BCE (Langdon, Acta Chiropterologica, 18(1): 215–222, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.012

Foraging strategy of Kuhl’s pipistrelle at the northern edge of the species distribution

EDITA MAXINOVÁ1, 6, MARINA KIPSON2, LADISLAV NAĎO3, PETRA HRADICKÁ4, and MARCEL UHRIN1, 5

1Department of Zoology, Institute of Biology and Ecology, Faculty of Science, Pavol Jozef Šafárik University in Košice, Moyzesova 11, 040 01 Košice, Slovakia 2Vertebrate Zoology Research Group, Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44 Praha, Czech Republic 3Department of Animal Ecology, Institute of Forest Ecology, Slovak Academy of Sciences, Štúrova 2, 960 53 Zvolen, Slovakia 4Department of Animal Physiology, Institute of Biology and Ecology, Faculty of Science, Pavol Jozef Šafárik University in Košice, Moyzesova 11, 040 01 Košice, Slovakia 5Department of Forest Protection and Wildlife Management, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Kamýcká 1176, 165 21 Praha 6, Czech Republic 6Corresponding author: E-mail: [email protected]

Rapid range expansion of Kuhl’s pipistrelle (Pipistrellus kuhlii) has been observed throughout Europe, and in addition to its natural habitats of temperate grasslands and agricultural areas, the species is common in city centres, where it roosts in human-made structures. It has been suggested that the flexibility of this species in regard to different human-induced changes, such as climate change and urbanization, is responsible for the apparent range shift. Although P. kuhlii exhibits one of the highest degrees of synanthropy among bat species in Europe, its ecology has thus far not been thoroughly studied. This study aims to describe its foraging and roosting selection in Central Europe (eastern Slovakia), where the northernmost maternity colony of P. kuhlii roosts in human settlements. Radio-tracking was conducted during the pre-parturition and post-lactation periods. We identified six artificial roosts within the study area that were interlinked, with bats switching between them. Ten individuals were used for modelling foraging-habitat utilization, which revealed that bats were highly selective. The only habitat type that bats clearly preferred, regardless of season, was an urban illuminated area close to a river. Only slight avoidance — of open areas — was observed during the pre-parturition period.

Key words: Chiroptera, urban, telemetry, prefabricated houses, foraging habitat

INTRODUCTION influence thermoregulation within roosts and con - sequently enhance energy savings and reproductive Urbanization is currently one of the most promi- phenology (e.g. birth dates) while also providing nent and increasing human-induced habitat alter- better anti-predator protection and/or enabling faster ations worldwide, acting as a homogenizing force juvenile development (Neuweiler, 2000; Lausen on the environment (McKinney, 2006). The loss of and Barclay, 2006). On the other hand, the higher structural variability has a huge impact on species level of traffic in towns may increase bat mortality persistence in such newly created landscapes (Sala in urban areas through collisions with vehicles et al., 2000). However, the impact of urbanization (Lodé, 2000). on biodiversity can be mixed, ranging from com- Among urban dwelling bat species, Kuhl’s pip- plete avoidance to exploitation (McKinney, 2008), istrelle (Pipistrellus kuhlii) exhibits one of the high- and is usually connected to life-history traits of indi- est degrees of synanthropy among Western Pale - vidual species (Kark et al., 2007). arctic bat species (Yom-Tov and Kadmon, 1998; It has been noted that certain bat species benefit Men delssohn and Yom-Tov, 1999; Bogdanowicz, from using artificial buildings as roosting sites 2004). It is a small vespertilionid that usually forms and adapt well to life in towns (Bihari, 2004; Neu - colonies of 20–100 females with their pups (Bogda - baum et al., 2007; Scales and Wilkins, 2007). The nowicz, 2004). Probably the main reason behind generally higher temperatures in cities in contrast the strong exploitation of urban habitats is that this to the surrounding landscape (Arnfield, 2003) could opportunistic aerial hawker largely benefits from Acta Chiropterologica, 18(1): 223–237, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.013

Activity patterns and use of night roosts by lesser horseshoe bats Rhinolophus hipposideros (Borkhausen, 1797)

NICK C. DOWNS1, 6, 7, WARREN J. CRESSWELL 1, PAOLA REASON1, GILES SUTTON2, DAVID WELLS3, LEYTON WILLIAMS4, and STEPHANIE WRAY5

1Arcadis, The Mill, Brimscombe Port, Stroud, Gloucestershire, GL5 2QG, United Kingdom 2GS Ecology, 119 Highgrove Street, Reading, Berks, RG1 5EJ, United Kingdom 3Collins Environmental Consultancy, Epsilom Dome, Cleve Mill Business Park, Newent, Gloucestershire, GL18 1EP, United Kingdom 4Jacobs, Churchill House, Churchill Way, Cardiff, Wales, CF10 2HH, United Kingdom 5Peter Brett Associates, 10 Queen Square, Bristol, BS1 4NT, United Kingdom 6University of Bristol, School of Biological Sciences, Woodland Road, Bristol, BS8 1UG, United Kingdom 7Corresponding author: E-mail: [email protected]

Close approach radio-tracking was used to investigate time and space use for both sexes of Rhinolophus hipposideros. Fifteen bats (nine males and six females, from three roosts) were radio-tracked (0 = 6.7 nights) within and around the National Trust Sherborne Park Estate, Gloucestershire (UK), between June and October 2003, at least seven of which (six males and one female) relocated to a different day roost after capture. The mean number of activity bouts per night was 3.5, each lasting for an average of 148 minutes. The mean distance travelled between fixes during each bout of activity was 3.8 km, and per night was 14.2 km. An average of 3.3 (SE = 1.8, range = 1–7, n = 12) night roosts were used per bat. Those individuals which continued roosting within the estate (n = 13) occupied a group foraging range covering approximately 1,175 ha with a 6.3 km range span (100% minimum convex polygon). The corresponding areas using the 95% Kernel isopleth and 95% Dirichlet tessellation enclosed approximately 539 ha and 1,553 ha, respectively. The maximum distance a bat was tracked from the roost of capture was 4.6 km, although the mean (n = 15) was much lower (2.2 km). A mean of 42% of the radio-tracking fixes from bats with at least one whole night of data were associated with night roosting, and of those, 56% were from the boiler room of a residential property within Sherborne village (used by 12 of the 15 bats). Therefore a range of suitable night roosts (i.e. sheltered locations adjacent to foraging areas) should be available throughout the foraging range (a minimum of 3 km from the roost) of a R. hipposideros colony. Night roosts on the edge of the home range, and warm night roosts are especially important.

Key words: range, time budget, minimum convex polygon, dirichlet tessellation, kernel analysis, night roost

INTRODUCTION Bat behaviour may be influenced by such factors as ambient light (Schofield, 2008; Stone et al., 2009, In order to ensure that effective conservation 2012), climatic conditions (Erkert, 1982), habitat strategies for bats can be implemented, a basic configuration (Russo et al., 2007; Schofield, 2008) knowledge of range size and use, and roost use, is and reproductive status (Knight, 2006; Alberdi et required. This is particularly important for species al., 2015). For example, differences in the emer- of conservation concern listed on both Annex II gence times of R. hipposideros relative to sunset and IV of the European Commission Council have been found in a number of studies (McAney Directive 92/43/EEC on the conservation of habi- and Fairley, 1988; Schofield, 1996; Williams, 2001; tats and of wild fauna and flora (the ‘Habitats Knight, 2006; Ramovš et al., 2010). Emergence is Directive’). Out of the 18 bat species known to be advanced by extensive cloud cover (i.e. determined present in the UK this includes both the lesser by ambient light levels) (Gaisler, 1963; McAney and (Rhinolophus hip posideros) and greater (Rhinolo - Fairley, 1988), a heavily shaded roost exit (Russo et phus ferrumequinum) horseshoe bats, as well as bar- al., 2007; Schofield, 2008) and lactation (Knight, bastelle (Barbastella barbastellus) and Bechstein’s 2006; possibly as a result of higher energy demands bat (Myotis bechsteinii). — Speakman and Racey, 1987), and inhibited by Acta Chiropterologica, 18(1): 239–247, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.014

Home range of Noack’s round-leaf bat (Hipposideros aff. ruber) in an agricultural landscape of central Ghana

EVANS E. NKRUMAH1, PETER VALLO2, 3, STEFAN M. KLOSE2, SIMON RIPPERGER2, EBENEZER K. BADU1, CHRISTIAN DROSTEN4, ELISABETH K. V. KALKO 2, 5, MARCO TSCHAPKA2, 5, and SAMUEL K. OPPONG1, 6

1Department of Wildlife and Range Management, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana 2Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany 3Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Květná 8, 603 65 Brno, Czech Republic 4Institute of Virology, University of Bonn Medical Centre, Bonn 53127, Germany 5Smithsonian Tropical Research Institute, Balboa, Panama 6Corresponding author: E-mail: [email protected]

Thirteen individuals of Noack’s round-leaf bat, Hipposideros aff. ruber, were radio-tracked for 38 nights in an agricultural landscape in Kwamang, Ashanti Region, Ghana. Local convex hulls were used to estimate home range sizes of the bats. Based on 1,192 fixes, the mean (± SD) home range size was 36 ha ± 35 ha. Individual home range size ranged from six to 95 ha and frequently overlapped among individuals. The foraging area covered 50% of the home range while the core area formed 2%. The mean maximum foraging distance was 1.1 km, with individual distances up to 2.6 km, suggesting Hipposideros aff. ruber is capable of covering relatively long distances. Male bats returned to the cave more often than females during the night. Although the cave was the main roost, each bat also had individual night roosts on trees.

Key words: core area, foraging area, local convex hull, maximum foraging distance, radio-tracking

INTRODUCTION these drivers and the animal’s cognitive map of its environment. Understanding the home range of animals is cen- On species level home range size may largely be tral in movement ecology and also important for determined by the respective body size and trophic developing effective management and conservation level of the animal (Harestad and Bunnell, 1979; strategies (Mitchell and Powell, 2003; Bonaccor- Lindstedt et al., 1986; Kelt and Van Vuren, 2001). so et al., 2005; Gschweng et al., 2012). The home Within-species variation, however, is only poorly range of an animal encompasses all areas where it understood (Campos et al., 2014). Individual home forages, mates and rears its offspring (Burt, 1943). ranges may respond to fluctuations in vegetation Home ranges thus represent cognitive maps (Nathan cover, food and water availability, thermal stress et al., 2008; Powell and Mitchell, 2012), that permit (Naidoo et al., 2012; Morellet et al., 2013) and par- the access to resources such as food, shelters, escape ticularly to food availability (Winkelmann et al., routes, as well as mating and breeding sites (Signer 2003; Elmore et al., 2005; Zeale et al., 2012). et al., 2015). These maps are regularly updated as Quantitative food requirements are primarily a func- the animal moves and interacts with its environment tion of body mass (Meer, 2006), which varies be- (Powell and Mitchell, 2012). Animal movements tween individuals, thus affecting individual home are characteristically affected by a multitude of range sizes (McNab, 1963; Lindstedt et al., 1986). drivers, acting at both spatial and temporal scales Energetic requirements tend to limit particularly the (Nathan et al., 2008). Such mechanistic drivers may home range size of pregnant and lactating animals be internal, motional, navigational and external fac- (Henry et al., 2002). Home range sizes within tors that are both biotic and abiotic components of species might also depend on colony size as individ- the environment (Nathan et al., 2008). The home uals living in larger colonies may have to travel range thus is a product of the interaction between over longer distances in order to establish exclusive Acta Chiropterologica, 18(1): 249–268, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.015

First record of Streblidae, Raymondia alulata Speiser, 1908 (Diptera: Streblidae), in Swaziland and a review of the genus Raymondia and their hosts in Africa

JULIE TERESA SHAPIRO1, 5, EDER BARBIER2, and ARA MONADJEM3, 4

1School of Natural Resources and Environment and Department of Wildlife Ecology and Conservation, University of Florida, Newins-Ziegler Hall, Gainesville, FL 32611, USA 2Programa de Pós-graduação em Biologia Animal, Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, Recife, Pernambuco 50670-901, Brazil 3Department of Biological Sciences, University of Swaziland, Private Bag 4, Kwaluseni, Swaziland 4Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Private Bag 20, Hatfield 0028, Pretoria, South Africa 5Corresponding author: E-mail: [email protected]

Species of the genus Raymondia (Diptera: Streblidae) are obligate ectoparasites of bats. They have a wide distribution across Africa and are associated with many different bat species. Here we present the first record of this family in Swaziland. The ectoparasites were of the species Raymondia alulata and were found parasitizing individuals of the species Nycteris thebaica. We review the status of Raymondia species known in Africa, including specimen records, hosts, and host distributions and provide an updated identification key for species in this genus.

Key words: distribution, Chiroptera, bat flies, ectoparasite, host-parasite relationships, parasitism

INTRODUCTION and richness of this family is greatest in tropical and subtropical regions of the world (Dick and Graciolli, Bats are known to host an exceptionally large 2008). The family comprises 33 known genera of number of ectoparasite species (Dick and Patterson, which 26 occur in the New World and seven in the 2006), with the highest ectoparasite diversity of any Old (Dick and Graciolli, 2008), with no common mammalian order (Dittmar et al., 2006). While in genera or subfamilies between the two regions. many cases ectoparasites appear to have very high However, recent research suggests that Streblidae host specificity (ter Hofstede et al., 2004), some spe- may be paraphyletic, with Old World Streblidae cies may parasitize multiple hosts (e.g., Marshall, forming a clade with Old World Nycteribiidae sepa- 1982; Dantas-Torres and Otranto, 2014). Si mi larly, rate from New World Streblidae (Dittmar et al., infested bats often host multiple ectoparasite spe- 2006). For this reason, we focus our study only on cies (Marshall, 1982). What factors deter mine the Old World Streblidae. species richness of ectoparasites for each host or the Of the Old World Streblidae, Raymondia specificity of ectoparasites is still debated, but in- Frauenfeld, 1855 is the second most diverse genus clude roost type, roost fidelity, group size, and indi- after Brachytarsina (Speiser, 1900) (31 spp.), with vidual body size of hosts (Bordes et al., 2008). Sex 21 known species. Raymondia alulata Speiser, 1908 and reproductive state also appear to play an impor- has a wide distribution over southern, central, and tant role in rates of infestation (Sundari et al., 2012). eastern Africa (Jobling, 1939; Maa, 1968; Theodor, Further, there is limited information about the extent 1968). It appears to be primarily associated with of occurrence and the possible overlap in distribu- Nyc teris thebaica E. Geoffroy, 1818 (Nycteridae) tions of many ectoparasite species. (Maa, 1968; Theodor, 1968), although it has also Streblidae (Hippoboscoidea: Diptera) is a family been recorded from Cloeotis percivali Thomas, of sanguivorous bat flies with a worldwide distribu- 1901, Hipposideros caffer (Sundevall, 1846), and tion that exclusively parasitize bats. The abundance Rhinolophus spp., which belong to the suborder Acta Chiropterologica, 18(1): 269–278, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.016

Records of the cave-dwelling bats (Mammalia: Chiroptera) of Hispaniola with an examination of seasonal variation in diversity

MIGUEL S. NÚÑEZ-NOVAS1, 2, 8, YOLANDA M. LEÓN3, 4, JEANNETTE MATEO5, 6, and LILIANA M. DÁVALOS7

1Museo Nacional de Historia Natural Profesor Eugenio De Jesús Marcano, Street César Nicolás Penson esq. Máximo Gómez, Plaza de la Cultura, Santo Domingo, Dominican Republic 2Universidad Iberoamericana, Área de Ciencia Ambiental y Biología, Av. Francia 129, Gazcue, Santo Domingo, Dominican Republic 3Instituto Tecnológico de Santo Domingo, Área de Ciencias Básicas y Ambientales, Ave. Los Próceres, Galá, Santo Domingo, Dominican Republic 4Grupo Jaragua, C/El Vergel 33, El Vergel, Santo Domingo, Dominican Republic 5Universidad Autónoma de Santo Domingo, Escuela de Biología, Edificio de Alta Tecnología, Ciudad Universitaria, Santo Domingo, Dominican Republic 6Consejo Dominicano de Pesca y Acuicultura, Edificio Ministerio de Agricultura, Los Jardines del Norte, Autopista Duarte Km. 6.5, Santo Domingo, Dominican Republic 7Department of Ecology and Evolution, and Consortium for Inter-Disciplinary Environmental Research, SUNY Stony Brook, 650 Life Sciences Building, Stony Brook, NY 11794, USA 8Corresponding author: E-mail: [email protected]

Despite a long history of scientific collection of bats, Hispaniola remains the least studied island of the Greater Antilles. Using standardized trapping methods during the wet and dry season at four major caves — Honda de Julián, La Chepa, Los Patos, and Pomier #4, we sampled a total of 1,472 individuals in four families, 11 genera and 12 species (of 18 recorded for the island). We report significantly fewer captures on the second night of sampling. We document seasonal variation in abundance of waterhousii, redmani, and jamaicensis, that results in 1–4 more species captured in the wet season. Additionally, singleton captures at all caves except for Honda de Julian produced wide confidence intervals in estimates of richness. Finally, we highlight the role of caves as major ecosystems for maintaining Hispaniolan mammal biodiversity. The high diversity recorded at La Chepa, together with possible declines at the historically very diverse Los Patos, highlight the conservation importance of all surveyed caves.

Key words: Chiroptera, harp trap, Natalidae, Phyllostomidae, wet and dry season

INTRODUCTION the bat fauna, as previously done for Jamaica (Geno- ways et al., 2005). That review found records for The Hispaniolan bat fauna is understudied com- 18 species in six families, comprising 90% of pared to the fauna of other Greater Antilles (Silva- the native extant mammals of the Dominican Re - Taboada, 1979; Gannon et al., 2005; Genoways public (Núñez-Novas and León, 2011). Of these, et al., 2005). Unlike Cuba or Puerto Rico, no long- 16 species, or 89% of the total recorded, use caves standing monitoring of bats has taken place to pro- as diurnal re fuges. Lacking any systematic sam- vide island-wide systematic records (Silva-Taboada, pling, however, the composition, richness and rela- 1979; Gannon et al., 2005). Most sampling on His- tive abundance of bat communities in Hispaniolan paniola has been opportunistic and instrumental caves remains unknown. to other goals such as sampling for phylogenetics To address the lack of systematic sampling at (Tejedor et al., 2005a, 2005b), molecular ecology in Hispaniolan caves, our goal was to survey the bat general (Corthals et al., 2015), or more recently fo- communities of four caves in the Dominican Re - cused on fossil communities (Velazco et al., 2013). public in a standardized manner for the first time. Only recently have extant records in museum col- Additionally, we compared the current species com- lections been harnessed to provide an overview of position with historical records for all caves using Acta Chiropterologica, 18(1): 279–299, 2016 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2016.18.1.017

Bat boxes — a review of their use and application, past, present and future

NIELS RUEEGGER1, 2, 3

1Australia School of Environment, Science and Engineering, Southern Cross University, Lismore, NSW 2480, Australia 2Present address: 43 Rutland Road, Medlow Bath, NSW 2780, Australia 3E-mail: [email protected]

Loss of tree cavities presents a threat to tree roosting echolocating bat populations. Bat boxes have been used for over a century to provide artificial cavities. The aims of this review were to provide a synthesis of bat box use in temperate parts of the world, to discuss the applications and effectiveness of bat boxes, to provide box deployment recommendations and to identify areas requiring further research. The 109 publications reviewed originated from four regions. The majority were from Europe (70%) followed by North America (16%), Australia (12%) and Asia (3%). Publications reported box use for research (n = 67), conservation management (n = 42) and public bat awareness (n = 1). The most commonly used bat box designs could be divided into five basic types, four originating from Europe and one from North America. Woodcement as a box material was frequently used in Europe and was practically absent elsewhere with timber boxes most commonly used overall. Seventy-one species of bats have been recorded using boxes, although only 18 were identified as using boxes commonly and 31 species were reported to have formed maternity roosts. The lack of maternity and overwintering roost records in boxes is a concern. There is a need to test current box types across geographical regions and to develop designs further. Where boxes are used as a conservation tool, consideration should be given to the long-term maintenance costs of a box program. Unless known to be unsuitable to target species, boxes should be made from durable materials, be unattractive to non-target species and be ‘self-cleaning’. Deploying a variety of box designs in clusters, time since box installation, non-target species box competition and target species-specific box design elements are likely influencing box uptake. The provision of boxes that comprise different microclimates and box aspects are likely best suited to meet the varying needs of a given tree roosting echolocating bat community. No conclusive evidence was found that box installation height is important for box uptake. There is concern that boxes may provide a competitive advantage for bat species commonly using boxes. Bat boxes should not be used as a justification for the removal of trees that comprise potential roost cavities.

Key words: bat box, bat house, artificial roost, tree cavity-roosting bats, conservation

INTRODUCTION The development of cavities occurs through either natural processes such as fungal decay, in- It is well documented that industries such as min- sects, fire and/or wind (Mackowski, 1984; Inions et ing and agriculture, as well as poor silvicultural prac- al., 1989; Adkins, 2006; Fox et al., 2009) or through tices and urban sprawl, negatively impact wild- the activity of wood-excavating birds (Jones et al., life habitat worldwide (Gibbons and Linden mayer, 1994; Newton, 1994; Jackson and Jackson, 2004). 2002; Lindenmayer and Franklin, 2002; Mick- Cavity development through natural processes is leburgh et al., 2002; Niemelä et al., 2005; Young et slow, with cavity-bearing tree recruitment likely to al., 2005). One aspect of habitat degradation is the take > 100 years (Gibbons et al., 2000; Kalcounis- loss of trees that comprise hollows, fissures or de - Rüppell et al., 2005; Cameron, 2006; Vesk et al., corticating bark which provide potential roost or 2008). As such, depletion of cavity-bearing trees and nest sites for various fauna species. This loss has the the many decades it takes for cavities to be recruited potential to impact on population size, abundance have invariably led to current and future scarcities of and diversity of cavity-using species (e.g., Linden - this resource in many environments. mayer et al., 1990; Holt and Martin, 1997; Evelyn Tree cavity abundance needs to be considered and Stiles, 2003; Marsden and Pilgrim, 2003; by local management authorities where cavity- Cockle et al., 2011), particularly species that are not dependant fauna are a conservation priority through able to excavate cavities (Newton, 1994). determining whether the present and predicted