Bats of the Western Indian Ocean Islands

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Bats of the Western Indian Ocean Islands

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Bats of the Western Indian Ocean Islands
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O'Brien, John
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Chiroptera ( local )
Western Indian Ocean ( local )
Fruit Bats ( local )
Ecology ( local )
Conservation ( local )
serial ( sobekcm )


The natural colonisation of many remote oceanic islands by bats, including those of the western Indian Ocean, has been facilitated by their unique capability among mammals for powered flight. In the western Indian Ocean region, only the Malagasy islands of Madagascar and the Comoros archipelago have been naturally colonised by non-volant mammals. Despite their greater potential for inter-island dispersal, and thus gene transfer, endemicity of Chiroptera in the western Indian Ocean islands is high. Given their vulnerability to stochastic and anthropogenic disturbances, greater focus needs to be placed on investigating the demographic and ecological history of bats on Western Indian Ocean islands to safeguard not only their future, but also the ecosystem functioning on these islands, for which they are undoubtedly such an integral part. Here, I summarise the taxonomic and life history information available on bats from Western Indian Ocean islands and highlight knowledge gaps and conservation issues that threaten the continued persistence of some species.
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Animals, Vol. 1, no. 3 (2011-07-23).

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Animals 2011 , 1 , 259-290; doi:10.3390/ani1030259 animals ISSN 2076-2615 Review Bats of the Western Indian Ocean Islands John OÂ’Brien Department of Zoology, University College Dublin, Belfield, Dublin 4, Ireland; E-Mail: m; Tel.: +353-86-2310-395 Received: 23 July 2011; in revised form: 10 August 2011 / Accepted: 12 August 2011 / Published: 16 August 2011 Simple Summary: The purpose of this paper is to revi ew the literature pertaining to the bat faunas of the western Indian Ocean islands, pa rticularly in light of the identification of many new species on Madagasc ar and the taxonomic reassi gnment of others, and to summarise details of their general biology, feeding ecology, reproduction and conservation. Abstract: The natural colonisation of many remote oceanic islands by bats, including those of the western Indian Ocean, has been f acilitated by their unique capability among mammals for powered flight. In the wester n Indian Ocean region, only the Malagasy islands of Madagascar and the Comoros archipelago have been naturally colonised by non-volant mammals. Despite their greater potential for interisland dispersal, and thus gene transfer, endemicity of Chiroptera in th e western Indian Ocean islands is high. Given their vulnerability to stochastic and anthropog enic disturbances, greater focus needs to be placed on investigating the demographic and eco logical history of bats on Western Indian Ocean islands to safeguard not only their future, but also the ecosystem functioning on these islands, for which they are undoubtedly su ch an integral part. Here, I summarise the taxonomic and life history information availa ble on bats from Western Indian Ocean islands and highlight knowledge gaps and cons ervation issues that threaten the continued persistence of some species. Keywords: Chiroptera; Western Indian Ocean; fruit bats; ecology; conservation 1. Introduction The diversity of geological historie s for the western Indian Ocean is lands, make them a fascinating study of evolutionary history. The granitic Seychell es and Madagascar are c ontinental fragments, as OPEN ACCESS


Animals 2011 , 1 260 old as the major landmasses themselves. Isolated volcanic mounts, such as Réunion and Mauritius, have a diversity of ages ranging from 2.1 to 15 milli on years [1]. Coral atolls such as Aldabra and Mayotte, and archipelagos such as the Maldives ha ve undergone repeated inundations due to rising sea levels during the Holocene and so can be consider ed relatively young. Thus the evolutionary history of bats, and indeed the entire biota, on each island depends on whether the islands in question can be considered isolated ‘oceanic’ islands requiring long-distance aerial or ma rine dispersal, or have been at some stage attached to larger continental landmasse s, facilitating terrestrial dispersal of a vicariant fauna. While phylogeographic studies of this nature are of great intere st, there is a pressing need to initiate more in-depth investigations of the gene ral biology of island bats given their conservation concern. Islands are typically characterised by high e ndemism and reproductive isolation and it is these traits that render island fauna as th e most prone to extinction [2]. Here, I consider the Western Indian Ocean as being west of the southern tip of India (not including Sri Lanka) and east of the African coastline (including Ma dagascar, but not the Mozambique Channel). Typically, the vertebrate fauna of the western Indian Ocean islands is African-derived [3]. However, fluctuations in sea-level, such as during the Pleistocene which expos ed much greater land area along the Mid-Oceanic Ridge, certainly afforded easier di spersal opportunities from th e Orient [3]. Aerial dispersal from Australasia by means of the trade wi nds is also theoretically possible [3]. Thus, the extent to which bats have helped shape ecosystem development on these islands depends on the timing of their colonisation, either as an cient or recent dispersers. The la rge distances betw een Indian Ocean islands presents an even greater challenge to isla nd colonisation for smaller bats (see below), compared to their fruit bat counterparts. However, Rodrigues and the Maldives are the only islands inhabited by fruit bats that are not currently sympatrically occupi ed by a smaller representative of the Chiroptera. Bat diversity is greatest on Madagascar and, due to greater research efforts on this island in recent years, new species are being de scribed almost annually. Bats oc cur on most of the Seychelles archipelago with the exception of so me of the outlying islets (e.g., Deni s, Bird, Coetivy). Bats have not become established on Chagos, the Amirantes, the Farquhars or Agalega (a lthough occasional vagrants have been recorded), despite bats being present on Aldabra and Cosmoledo. The 18 families and over 1,000 species of the Order Chiroptera (which is considered to have diversified in the Miocene, about 50 million years ago [4]) have traditionally been divided into two sub-orders–the Megachiroptera (f ruit bats or flying foxes) and the Microchiroptera. However, molecular investigation has indi cated that the classic grouping of Microchiroptera is, in fact, paraphyletic with the super-fam ily Rhinolophoidea (Rhinolophidae, Hipposideridae, Megadermatidae and Rhinopomatidae) a sister group to the Megachiroptera, form ing a Yinpterochiroptera clade, and the remaining species forming the Yangochiroptera clade [4,5], but see [6], and it is this classification system that is followed here. 2. Yinpterochiroptera 2.1. Distribution, Taxonomy and Putative Origins Without doubt, Pteropus (Pteropodidae) has been the most successful genus in colonising the western Indian Ocean islands (see Appendix Table 1), just as it has been in dispersing throughout the


Animals 2011 , 1 261 western Pacific from its south-east Asian origins. Typically, a single representative species inhabits each island or archipelago. Only on the islands of Anjouan and Moheli (Comoros archipelago) are two species of Pteropus contemporaneously sympatric ( P. livingstonii and P. seychellensis comorensis ). However, there is historical evidence that Pteropus niger and Pteropus subniger (now extinct) were sympatric on both Mauritius and Ré union [7]; sub-fossil evidence that P. niger and Pteropus rodricensis were sympatric on Mauritius and Rodr igues [7]; and potential sympatry of Pteropus giganteus ariel and Pteropus hypomelanus maris (a species described based on a single type specimen and now probably extinct) in the southern Maldives. Pteropus bats are sympatric with representatives of other large yinpterochi ropteran genera including Eidolon, Rousettus and Epomophorus (all Pteropodidae) on the islands of Pe mba, Mafia, Madagascar and th e Comoro archipelago. Given, the proximity of the African coast to these islands (in some cases, less than 40 km) it is remarkable that the genus Pteropus appears to have never colonised the African mainland. A molecular study of extant Pteropus species [8] provides evidence of at least three colonisation events into the Indian Ocean: an initial colonisation into the westernmost part of the Indian Ocean (Pemba Island and the Comoro archipelago), another giving rise to P. rodricensis on Rodrigues, and a final, more recent event, resulting in colonisation of the Seychelles, Aldabr a, Madagascar, Mauritius and the Comoro archipelago. Given that Pemba was one of the first islands to be colonised by the genus, this initial colonisation to the westernmost edge of their distribution makes it all the more intriguing that Pteropus has not become established on the Afri can mainland itself. A subspecies of Pteropus seychellensis ( P. seychellensis comorensis ) occurs on Mafia Island south of Pemba, also within 40 km of the African coast. Monsoon winds that travel sout h along the African coast could have assisted bats in bridging the gap between Pakistan and India to Pemb a and the Comoro archipelago [9]. Dispersal from sub-continental India, utilising th e Maldive archipelago as stepping stones, to the Seychelles and beyond is an obvious alternative route of colonisati on, albeit difficult to confirm without fossil or sub-fossil evidence. Regrettably, this lack of reliabl y-dated fossil material for bats from the western Indian Ocean also precludes in ferences on the timing of divergence (and thus colonisation) events. However, the last complete inundation of Aldabra at oll is thought to have occurred approximately 125,000 years ago [10], so Pteropus aldabrensis and, most likely, its closelyrelated congeners on Madagascar, Seychelles, Maur itius and the Comoro ar chipelago can only have diverged after this time. The genetic differences between some species of Pteropus in the Western Indian Ocean are exceedingly small, particularly for ‘species’ arising from the most recent colonisation event. In fact, genetic divergence of less than 1.3% for cytochrome b gene sequences was reported between some purported species [8]. By way of co mparison, mean intra-specif ic sequence divergence for cytochrome b of 1.87% was described between individuals of Pteropus vampyrus from two sites in the Philippines [11]. Although genetic evidence suggest s that the taxonomic assignment of species for individual islands in the western Indian Ocean ma y be misleading, the phenoty pic differences between island species are suggestive of incipient speciation an d so island ‘speci es’ should be mana ged separately. Rousettus obliviosus has been recorded from three of the four islands in the Comoro archipelago (Gran Comore, Moheli and Anjouan), while Rousettus madagascariensis is endemic to Madagascar where it is widespread except in the south-west of the island. Both of these island endemics, which are sister taxa [12], are smaller in si ze and have different dentition to th e East African mainland species of Rousettus ( R. aegyptiacus leachii ) [13], which occurs on Pemba, Unguja (Zanzibar) and Mafia


Animals 2011 , 1 262 Island [14]. Rousettus is considered to have colonised Af rica via India or the Middle East through forested corridors [15-17] and arri val on these western Indian Ocean is lands is likely to have occurred secondarily to arrival on the African continent. Epomophorus wahlbergi is recorded only from Pemba and Unguja among the western Indian Ocean islands, but it occurs throughout eastern Africa. Epomophorus labiatus (minor) is recorded from Unguja and Mafia only, but is common and widespread in eastern and central Africa. The genus Eidolon is solely African, although this genus does not appear to be closely related to any other African fruit bat [15]. Eidolon helvum , a species recorded throughout Africa an d into the Near East, is also reco rded from Pemba and Unguja, with a congener, Eidolon dupreanum, endemic to Madagascar. Sub-fossil remains of Rousettus and Eidolon from a cave in north-western Madagascar have be en dated to approximately 80,000 years ago [18], but certainly this can only be considered a minimum tim e span for the presence of these genera on this island. In the western Indian Ocean, rhinolophid bats (Rhinolophidae) only occur on Socotra ( Rhinolophus clivosus) and the Tanzanian off-shore islands of Pemb a, Mafia and Unguja (see Appendix Table 1), where they are clearly associated with the faunal complement of mainland Tanzania (see Rhinolophus clivosus occurs on both the eastern Horn of Africa and the Arabian Peninsula, but it is not clear from whic h direction it colonised Socotra. Two other species of yi npterochiropteran bats have been described from Socotra Island; Rhinopoma cystops (hardwickii) (Rhinopomoatidae) and Asellia tridens (Hipposideridae) [19,20]. The genus Rhinopoma is thought to have extended its range from the Near East in the Early Miocene and genetic study indicates that colo nisation of Socotra occurred from this phylogeographic region [20]. There are seven species in the genus Triaenops (Hipposideridae); thr ee that are endemic to Madagascar ( T. auritus, T. furculus and T. menamena ); one that occurs only on Aldabra ( T. pauliani ); and three ( T. afer, T. parvus and T. persicus) that occur in an arc from Arabia through to East Africa [21]. Initial geneti c evidence supported two independent a nd unidirectional co lonisation events into Madagascar from Africa for Triaenops [22], but subsequent analysis indicate one East African colonisation giving rise to T. auritus and T. furculus and a separate Arabian-derived colonisation for T. menanmena [21] . In fact, the morphological/g enetic difference between T. menamena and the other Indian Ocean forms ( T. auritus, T. furculus and T. pauliani ) is so significant that it has been suggested that these latter species be placed in a new genus ( Paratriaenops ) [21]. There is some evidence of geographic partitioning of the sympatric species of Triaenops on Madagascar: T. auritus is restricted to the north and northwest, T. furculus is restricted to the central west and southwest, while T. menamena is widespread, but only in the dr y habitat of the island [23]. 2.2. Roosting and General Biology Most species of Pteropus fruit bat favour roosting in emergent trees, which are typically defoliated. Seychelles fruit bats ( P. seychellensis ) roost in tall trees (particularly Casuarina or Albizzia) , typically hanging from one foot with the other pressed against the ventrum; while P. aldabrensis also uses coconut palms, figs and Sideroxylon inerme [24]. Although roost sites tend to be in undisturbed forest areas, some species are tolerant of a range of habitat types, such as P. voeltzkowi whose roost sites vary from the centre of a village to primary forest and utilises a range of tree species [25], but unlike other


Animals 2011 , 1 263 species, uses heavily foliated trees. Eidolon helvum , the second largest fr uit bat on the African continent, typically roosts in emergent trees, but has also been reported to roost in caves [26]. In Kruger National Park in South Africa, E. wahlbergi roosts in relatively sm all groups of mixed sex among foliage in riverine forest [27], while in other parts of their range they favour forest edge habitat or may even be synantrophic (roosts in buildings) [28], but informati on on roosting behavior on islands appears to be lacking. Generally, roost sites are l ong-lived; although considerable monthly variation in bat abundance at known P. rufus roosting sites (ranges from 10 indi viduals to rarely 5,000 [29]) in Madagascar has been reported [30]. This ability to move between roosting sites could partially mitigate against anthropogenic thr eats such as hunting and forest clearance. Eidolon helvum is well known for its migratory behaviour and synchrony of roostin g behaviour at sites separated by hundreds of kilometres has been described from mainland Afri ca [31], although whether such synchrony occurs on western Indian Ocean islands is not clear. Rousettus bats tend to maintain close body contact when roosting in caves to reduce the ener getic costs of homeothermy [13]. Triaenops furculus and T. menamena primarily roost in caves and frequently co-habit (in fact in an ecomorphological study of variation among Malagasy bats, including four yinpt erochiropterans, these two species showed considerable morphol ogical overlap [32]. Large colonies of T. auritus have been recorded from a cave and a mining tunnel within its very restricted range [33]. Specimens of Hipposideros commersoni are considered to be smaller in the south of Madagascar and this species also shows pronounced sexual selec tion, with males being larger th an females [34]. This species primarily roosts in caves in larg e colonies, but single specimens have been found to roost in trees and in buildings and are possibly largel y inactive during the winter in Mada gascar [35]. At least in Egypt, R. cystops (hardwickii) typically roost singly in dry caves, underground tunne ls and buildings and tend to be active year-round, drawing on fat reserves that begin to appear in late July over the winter [36,37]. Wing clapping is a common behaviour observed among roosting bats and is considered a territorial display and a precursor to antagonistic interactions. Dominance of sympatric P. livingsonii over P. seychellensis comorensis in aggressive encounters when both species fed from Ceiba pentandra trees has been documented [38], but with little other ov erlap in feeding ecology or in reproductive behaviour between the two species. Rousettus obliviosus, which is also sympatric with P. livingstonii and P. seychellensis comorensis on some of the Comoros is lands, does not compete with Pteropus , at least for roost sites, since Pteropus is tree-roosting, while Rousettus roosts in large colonies in caves [39]. In addition, Rousettus is smaller and is unlikely to be ab le to compete aggressively with the much larger Pteropus species. Highly vocal, a range of vocalisations has been described in P. seychellensis and olfaction may mediate social contact in a ll pteropid bats through gla nds in the neck [24,40]. Male E. wahlbergi have air sacs on the neck that may ai d in amplifying vocalisations duri ng courtship, and conspicuous scent glands are present in both sexes at the base of the ear and the shoul der epaulets [41] . All species of fruit bat tend to spend large portions of their activity budget in grooming behaviour, particularly focussing on cleaning their wings and removing fruit residues from their fur. Body temperature in fruit bats may be regulated by hanging with the wings out stretched or by licking or urinating on the wings to aid evaporativ e cooling [42].


Animals 2011 , 1 264 2.3. Feeding Ecology Pteropus bats utilise fruits as their primary source of nutrition. Howeve r, this typically protein poor diet can be supplemented with pollen and leaves to o ffset these deficiencies. Fi gs are a consistent food item that arises in dietary analysis of practically a ll fruit bats in the Western Indian Ocean. Nectar and flowers are also regularly sought a nd in the process of securing them , bats pollinate tr ees such as C. pentandra , Pentadesma butyracea and Barringtonia sp. [43]. P. seychellensis are commonly observed flying with fruits of Anacardium occidentale [24], highlighting their prominent role in seed dispersal. Guettarda is an important food source for P. giganteus ariel on the Maldive Islands, even though this is quite a low growing plant, bats were obser ved feeding as low as 1.5m above ground. An unusual food preference in P. rufus from Berenty in SE Madagascar has been describe d where the vast majority of the diet consists of pollen from Agave sisalana [44]; a cultivated plant introduced only 60 years ago, thus demonstrating the ad aptability and opportunism of feeding behaviour in this genus. In fact, only 16% percentage o ccurrence of fruit has been reported in the diet of P. rufus, compared to 40% pollen and 22% leaf material [44]. Of concern is the preponderance of cultivated food pl ants in the diet of many fruit bats. An array of cultivated fruits have been described in the diet of P. giganteus ariel [43] including starfruit ( Averrhoa carambola ), papaya ( Carica papaya ), banana ( Musa sp. ), guava ( Psidium sp. ), betel nut ( Areca catechu ), among others, with bread fruit ( Atocarpus altilis ) and mango ( Mangifera indica ) causing greatest conflict with fruit growers on the islands. This conflict between fruit gr owers and fruit bats is repeated on other western Indian Ocean islands, incl uding Mauritius and Madaga scar [45]. Despite this reliance on cultivated fruits, in many cases fruit bats remain the most important seed dispersers and pollinators of native plants on these islands. Syzygium is a staple food of E. helvum on mainland Africa and they are al so said to be particularly fond of C. pentandra [46] and given the availability of thes e foods on the Tanzanian offshore islands, this is likely to be the case ther e also. This species may also chew on wood and bark [26]. In a study of E. dupreanum in eastern Madagascar, 30 plant species (including six introduced species) were recorded in a diet consisting mostly of fruit, but also Eucalyptus flowers [47]. Inte restingly, this species appeared to ignore plantations of guava ( Psidium sp. ) located close to their roost in favour of native Polyscias sp. located further away. Of greater impor tance, however, is the fact that E. dupreanum is most likely the main pollinator of the endangered endemic baobab Adansonia suarezensis [48]. Niche partitioning between genera of fruit bats sympatric on islands has not been extensively studied. Although dietary overlap ( Ficus sp., C. pentandra, Musa sp., C. papaya ) has been documented between Pteropus and Rousettus where they are sympatric, Rousettus is predominantly nocturnal in comparison to the more di urnal and crepuscular activity of the Pteropus species [39]. In addition, Rousettus is a more generalist feeder, foraging in a ll habitats and altitudi nal ranges [39]. In a study of the diets of Pteropus and Eidolon on Madagascar, of fifty plan t species recorded, 23 are consumed in common [49]. Foraging flights for E. wahlbergi are generally restricted to a ra nge of about 10 km, despite being a strong flier [50], while some species of Pteropus are reported to travel up to 40 km on nightly foraging flights [51]. Typica l foraging range for Eidolon sp. is up to 30 km from the roost site and often at higher altitudes than most other fr uit bats [26]. Gut rete ntion time of seeds could be up to 8 hours in


Animals 2011 , 1 265 Pteropus sp. [52]. Given these long foraging flights and the potential for s eed retention, the impact of fruit bats on pollination and seed dispersal ov er a wide area should not be underestimated. Rhinolophus hildebrandti is reported as venturing up to 2 km from its roost sites and its manoeuvrable wing morphology adapt it to foraging among the canopy [53]. In a study examining five sympatric species (including three yinpterochiropteran bats) fr om western Madagascar [54], H. commersoni was found to feed selectively on Coleoptera (particularly Ca rabidae and Scarabidae, [55]), while two species of Triaenops ( T. menamena and T. furculus ) appeared to have a preference for Lepidoptera. However, the authors al so indicated that there was some dietary overlap between species and considerable temporal va riation in diets. Activity of these five species of bat was greatest at forest edge habitat, coincident with th e greatest availability of prey. Asellia tridens , a species well suited to desert habitat and recorded only fr om Socotra among the Indian Ocean islands, are fast and agile fliers, with Lepidoptera and Coleoptera making up a large part of their diet in Israel [56], which is also likely to be the case on Socotra. Echolocation call paramete rs can suggest some elements of feeding biology; for example, Cloeotis percivali echolocates at frequencies exceeding 200 kHz, well beyond the hearing sensitivity of moths on which it predominantly preys [57]. 2.4. Reproductive Biology Due to the inherent difficulties in classical observa tional study of behaviour in bats (large colony size, nocturnal behaviour, and flig ht capabilities), social structures and reproductive biology are less well-defined as for other mammalian Orders (but s ee [58] for review). Th e propensity for multiple mating and post-copulatory delay mechanis ms compounds these difficulties. Most Pteropus fruit bats can be considered either strongly or moderately gregarious, although the extinct P. subniger was reported to inhabit tree hollows singly or in pairs [7]. Harem formation in wild and captive P. rodricensis has been reported and there is evid ence of resource defence polygyny in captive specimens of this species [59,60], whereby male s defend food or roost sites (or both), thereby monopolising reproductive access to females. Spermat ogenesis is thought to occur year-round in Pteropus bats [61]. Mating has been observed in March, June, October and November in P. aldabrensis , but females with young are only reported in December and January. Pteropus seychellensis typically copulates in June and July, but mating may be attempted year-round. Births peak in November and December but have also been recorded in September and October and, in one instance, in March [24]. Pteropus giganteus ariel has a paturition peak in April and May coinciding with the onset of the rainy season [62], as is also the case with P. giganteus on mainland India [63], although young of less than 3 months of age have been observed in November [43]. Pteropus rufus is considered to mate in April and Ma y with young appearing in October [36]. Female Pteropus fruit bats typically give birth to a single offspr ing (birth weight for P. seychellensis and P. giganteus = 31 g [24,64]). Juvenile bats are incapable of foraging until they can fly, and so are nutritionally depend ent for a longer period than terr estrial mammals of equivalent size [65]. Thus, despite faster juve nile growth rates compared to other mammals, the rate of population growth is low for mammals of thei r size due to substantial maternal investment in offspring. Following birth of P. seychellensis young in November and December, fam ily groups are the most common types of social groups in roosts, comprising of either a single adult male and female together with dependent


Animals 2011 , 1 266 young or adult groups of a single male with one or two adult females wit hout young [24]. However, by April, large juvenile amalgamati ons and single sex groups are mo re typical, which are maintained throughout the period of the south-ea st trade winds until females give birth and family groups become re-established. The timing of reproduction in R. obliviosus is unclear, with only incide ntal observations of roosting young in July, lactating and parous fe males in July and an embryo in October suggesting polyoestry or some form of preor post-copulato ry delay mechanism [39]. Mating of R. aegyptiacus may occur year-round and births occur, after approximately 4 months gestation, in East Africa in March and September [66], and this is likely to also be the case on the Tanzan ian off-shore islands. Mating occurs in E. helvum between April and June, and although em bryonic development takes four months, gestation periods can be as long as nine months due to delayed implantation [26]. Long distance migration by E. helvum into Zambia between October and Decem ber is considered to coincide with seasonal fruit abundances and is driven primarily by the energetic demands of pregnancy and lactation [31], and a lthough it is not known if E. helvum on the Tanzanian islands migrate, reproductive activity is also likely to be synchronised with food availability. Epomophorus wahlbergi has a lek-type mating system with males congrega ting at ‘arenas’, from wh ere they call to passing females with their shoulder epaulets prominently displayed [41]. Mating can occur twice a year and young are generally recorded around the end of Febr uary or from the beginning of October, with gestation lasting 5–6 months [41]. Pregnant females of R. hildebrandti have been encountered in September and October, with births occurring in November or December, coinciding with the warm and wet summer months [67,68]. There is evidence of a harem social system in Hipposideros caffer (which occurs on Pemba, Unguja and Mafia Island) in colonies studied in Zimbabwe [69] . Reproductive information for H. commersoni from Madagascar is lacking. 2.5. Conservation In general, Western Indian Ocean island fruit bats have few natural predators, so predation does not greatly impact on mortality levels in col onies. However, exceptionally high predation on R. madagascarensis by barn owls ( Tyto alba ) has been reported at one site in western Madagascar [70]. Fruit bats have been an important traditional food for many island peoples and continue to be utilised, with some species exploited on a commercial basis, such as P. seychellensis on the granitic Seychelles and P. rufus on Madagascar (360–480 bats taken loca lly each year, [71]). Unsustainable hunting pressure has been identifie d as a significant threat to the fruit bats on the Seychelles (J. Gerlach, pers. comm.) and it has been suggeste d that the IUCN methodology for assigning vulnerability status to bats has sign ificantly underestimated the degree of threat to P. seychellensis [72]. Hunting is thought to have been the causative factor in the extinction of P. niger on Réunion [73], and until recently, was a major concern on Rodrigues. A detail ed study is required of mortality, birth rates, hunting and inter-island movements to determine if a sustainable indus try can be established on these islands. Similarly, significant hu nting pressure by humans on H. commersoni in Madagascar occurs [74], coincident with periods of food s hortage. Undoubtedly, incidental captu re of other species (including yangochiropterans) also occurs when cap turing this species at roost sites.


Animals 2011 , 1 267 Conflict with fruit growers is a significant cont ributory factor to huntin g pressures; although the actual scale of damage done by fruit bats has been questioned [71]. Pteropus rufus can be legally hunted during a 4-month restricted s eason in Madagascar, but can also be killed at any time if found raiding crops. Although it is not yet a concern on Western Indian Ocean islands, th e potential for zoonotic disease transmission from fruit bats, may trigger culling programmes in the future. Already, antibodies against the human disease-causing Hendra, Ti oma and Nipah viruses have been reported from all three fruit bat species on Madagascar [75]. Currently, the greatest threat to bat populat ions is habitat alteration. Although some Pteropus species appear adaptable to secondary forest a nd anthropogenic landscapes, concomitant reductions in fruit bat populations generally follo w removal of primary forest habitat. The loss of the introduced tamarind tree ( Tamarindus indica ), the fruit of whic h is a favourite of P. rodricensis , has been proposed as a major factor in their decline [7], although this hypothesis has been questioned [76]. Habitat destruction associated with the extension of sugar cane plantations pr obably contributed to the extinction of P. subniger [73]. Thus, protected areas are a vita l component of conservation efforts for fruit bats on island habitats, and greater efforts mu st be made to safeguard current reserves and to establish, extend and enforce new ones wher e protection is deemed insufficient. The role that fruit bats play in pollination, seed di spersal and seed set on islands is unequivocal. In a germination study on Madagascar, plant germination was significantly higher fr om seeds taken from the faeces of either P. rufus or E. dupreanum in 80% of plants tested [71]. Thus, protecting bat roosting and foraging sites is likely to assist in forest regenerati on over even larger areas. On Réunion, all of the native frugivores including two Pteropus sp. ( P. niger and P. subniger ) have become extinct, except for a bulbul species that can only tackle small fruit. This may be the reason why new lava flows are not being colonised by trees th at produce fleshy fruits [73]. Environmental factors can also have a devastatin g effect on tree-roosting bat populations. Cyclonic storms that strip food and roost trees and sweep bats out to sea have signif icantly reduced populations of P. rodricensis [77]. Deforestation compounds the effects of these storms by reducing the forest buffer that protects bats from the full force of cyclonic winds. On Pemba, 94% of the P. voeltzkowi population is distributed between only 10 roost sites and larger colonies are associated with primary or secondary fo rest and in one case a gr aveyard activel y protected by locals [25]. Similarly, although P. giganteus ariel has been recorded on the majority of islands in the archipelago, group size is genera lly small (0.6–2.1 bats/hect are) and at least in some cases, visits are likely to be transitory [62] . Both highly localised and low popul ation densities render these bat populations vulnerable to stochastic or environmental factors. Cloeotis percivali appears to be particularly sensitiv e to disturbance, with large population fluctuations that may be responsible for the stocha stic extinctions described from colonies on mainland Africa [78]. The size of the colony of this sp ecies on Mafia Island is unknown and warrants further investigation. Recognising the combined impact that natural perturbations and anthropogenic effects could have on island populations of fruit bats, the IUCN lists one Western Indi an Ocean species of Pteropus as Critically Endangered (P. rodricensis) , two as Endangered (P. livingstonii, P. niger) and one Extinct (P. subniger) [79]. In October 1989, CITES member states approved the a ccession of seven species of


Animals 2011 , 1 268 Pteropus bats to Appendix I, and the remaining 53 speci es were given Appendix II status including all the western Indian Ocean species [80]. Based on th eir localised distribution and threats from cave disturbance, a revision of the IUCN Red Data List (2002) status of the Comoros endemic Rousettus obliviosus from Lower Rick: Near Threatened to Vu lnerable was recommended [33], and has since been enacted [79]. Rousettus madagascariensis is probably the most numer ous species of fruit bat on Madagascar, but still warrants its IUCN listing as Near Threatened due to continued hunting pressure [81]. An IUCN-sanctioned report from 1992 graded all species of Megachiropter a in relation to their conservation status and pr ioritised the need for conservation act ion [82]. Three western Indian Ocean Pteropus species ( P. livingstonii , P. rodricensis and P. voeltzkowi ) were given the highest priority rating, indicating that these species are in da nger of extinction. Since the report was published, numbers of P. voeltzkowi and P. rodricensis are growing [76,83,84]. The cap tive breeding programmes for P. voeltzkowi and P. livingstonii , recommended in the report, have not had the same success as that for P. rodricensis , with only one zoological institution holding an ex situ colony of P. voeltzkowi (currently only comprising three females) and only four institutions in the P. livingstonii breeding programme [85]. The IUCN report further suggested that efforts should be made to introduce P . rodricensis to suitable habitat in the Western Indian Ocean islands [82]; a proposal reiterated elsewhere [86]. A similar initiative could be considered for re-introducing P. niger onto Réunion in order to restore the large seed-dispe rsing frugivore fauna now absent fr om this island, bearing in mind that much of the suitable low-altitude habitat fa voured by this species is now gone. However, recent reports suggest that a small group of P. niger may, in fact, have already colonised and be breeding on Réunion naturally [87]. The need fo r national legislative protection, community-based protection and education projects has regularly been highlighted. The former has been enacted in Mauritius and to a lesser extent in Madagascar [71,88], the latter have proven highly successful in the Comoros, Rodrigues and Pemba [89]. Currently, among the non-fruit bat Yinpteropchir optera inhabiting the We stern Indian Ocean islands, only T. auritus is listed by the IUCN as Vulnerab le due to its rest ricted range; although populations are considered to be healthy [33]. Howe ver, some newly described species have yet to be annotated. 3. Yangochiroptera 3.1. Distribution, Taxonomy and Putative Origins The taxonomy of yangochiropteran bats is in a constant state of flux. Thus, the taxonomic names listed in Appendix Table 1 below are currently the most widely accepted, but may be revised in coming years. Only one species of Yangochiroptera has been recorded from the granitic Seychelle Islands ( Coleura seychellensis , Emballonuridae). There are only two species described in the genus Coleura (Emballonuridae): the widespread Coleura afra with a disjointed distri bution in low latitudes from southwestern Arabia to western Africa and Madaga scar; and the endemic Seychelles sheath-tailed bat ( Coleura seychellensis). These two species are differentiated mor phologically based on a distinctive lip


Animals 2011 , 1 269 groove in the Seychelles species. Until recently, C. seychellensis was probably present on all the larger granitic islands includin g Praslin and La Digue but can now only be confirmed for Silhouette and Mahé [90]. The genera Taphozous (Emballonuridae) and Chaerephon (Molossidae) are distributed from SE Asia and Australia westwards to Western Africa. The Mauritian tomb bat ( Taphozous mauritianus ) occurs on Aldabra, Madagascar, Maurit ius, Réunion and Unguja and is widespread throughout sub-Saharan Africa, this range correlating with areas of annual rainfall greater than 500 mm [91]. The species complex of Chaerephon pumilus ( leucogaster) is also broadly distributed south of the Sahara desert and on the Indian Ocean islands of Alda bra, Madagascar, Comoros, Pemba and Unguja. Recent and extensive studies of the Chaerephon pumilus (leucogaster) species complex have indicated that C. leucogaster is nested among lineages of C. pumilus [92-94]; although due to the morphological divergence of C. leucogaster the authors recommend that it retain its status as a separate species. The species previously referred to as C. pumilus occurring in Madagascar is sufficiently differentiated to be considered a separate species ( Chaerephon astinanana ) [94]. Chaerephon pumilus sensu lato occurring on the other western I ndian Ocean islands (Aldabra [95], the four islands of the Comoro archip elago [96], and possibly the Amirante Islands [97]) are ascribable to Chaerephon pusillus [94]. In Madagascar, C. leucogaster is restricted to the northern and eastern humid areas up to altitude s of 1,300 m [98], whereas the recently described C. atsinanana is common in the eastern areas up to 1,100 m [94]. Likewise, no distinguishing taxonomic differences were found in a comparison of the low-lying savannah species Mops midas (Molossidae) from Africa and Madagascar [99]. Indeed, a comp lete review of the genera Chaerephon/Tadarida/Mops is warranted, given the lack of a consistent taxonomy. Species diversity is greatest on Madagascar, as might be expected, w ith northern sites of sedimentary rock harbouring most species, although there is no evidence of a north-south cline [100]. Despite having a global distribution, the genus Eptesicus (Vespertilionidae) is only represented in the western Indian Ocean by one endemic species in Madagascar ( E. matroka ), although this species has also been assigned to the genus Neoromicia (Vespertilionidae) based on bacular morphology [101]. There are two species of the genus Emballonura (Emballonuridae) endemic to Madagascar ( E. atarata and E. tiavato ) [102]. Emballonura atarata is restricted to the moist eastern part of the island, while E. tiavato inhabits drier regions. Two other Emballonur id bats also have been documented on Madagascar; C. afra and T. mauritianus [102]. The Vespertilionida e are well represented on Madagascar with 15 described species (s ee Appendix Table 1). Four species of Scotophilus (Vespertilionidae) have been described from Madagascar ( S. robustus, S. barbonicus, S. leucogaster (viridis) and the recently described S. tandrefona ), of which three are ende mic [103]. Based on genetic data these Scotophilus species are not monophyletic, indicative of multiple colonisati on events [104]. Nine species of the genus Miniopterus (Miniopteridae) have been de scribed from Madagascar, two of which also occur on the Comoro archipelago, and in some areas of Madagascar, e.g. Namoroka, up to five cryptic species of Miniopterus are sympatric [105]. Further ta xonomic work may reveal greater cryptic diversity in certain lineag es. The enigmatic sucker-footed ba ts (Family Myzopodidae), endemic to Madagascar and until recently considered monotypic, are represented by two species ( Myzopoda aurita and Myzopoda schliemenni ); although M. aurita also occurred in East Africa during the Pleistocene [42]. Divergence of th ese two species has been estimated as occurring approximately 73,500 years ago [106]. Pipistrellus raceyi (Vespertilionidae) is known fr om only four low-elevation


Animals 2011 , 1 270 locations on Madagascar, two each on the east and we st sides of the island [101]. Intriguingly, it has been suggested that only the western populations of P. raceyi are forest dependent [107]. On the Mascarene islands (Mau ritius, Rodrigues and Réunion), T. mauritianus, Mormopterus acetabulosus (Molossidae) and S. borbonicus (leucogaster) have all been recorded from Mauritius and Réunion, although S. borbonicus (leucogaster) has not been observed on Réunion since 1867, and all are allied to counterparts on Madagas car or the African mainland [73]. Mormopterus acetabulosus is thought to be restricted to Mada gascar and the Mascarenes, but th ere are two possible records from South Africa and Ethiopia [108]. There are no recent or historical reports of yangochiropteran bats occurring on Rodrigues or the Maldive archipelago. Taphozous mauritianus has been recorded from the Comoro archipelago; although only as a single specimen from Mayotte [96]. The islands that lie close to th e African mainland (Pemba, Unguja an d Mafia Island) have subsets of the species complement of nearby Tanzania (see A ppendix Table 1), and these islands would benefit greatly from a complete survey focussing on bats. Species diversity appears to be lowest on Mafia Island and highest on Unguja, but with different species assemblages existing on each island [71,109] (see also es_Home.asp). An endemic species of the genus Mops ( M. bakarii ) has recently been described from Pemba Island [110]. These three islands could, therefore, provide a valuable study on ecological requirements and competitive exclusion for African bats (both yinpterochiropter an and yangochiropteran). Hypsugo (Pipistrellus) ariel (bodenheimeri) (Vespertilionidae) has been recorded from Socotra and thus is the only yangochiropteran representative of the restricted bat fauna here; there is some suggestion that the island population may even be a separate species to that of the mainland [111,112]. 3.2. Roosting and General Biology Coleura seychellensis typically roosts in groups in caves in boulder fields, either hanging by their hind limbs, or clinging with all four limbs and pressing their abdomen to the rock wall. Coleura seychellensis is most active in terms of flight at dawn and dusk and have a preference for coastal and low altitude habitat [113], although a potential high altitude roos t site (515 m) in a granite boulder field on Silhouette Island may also exist [114]. In a study of this species on Mahé , it was only encountered on the less well-develo ped west coast [90]. Chaerephon leucogaster (pumilus) , a largely synanthrophic species, roosts in large, stable colonies. Males a nd females roost together with high site fidelity throughout the year and the social system is suspected to be base d on female defence polygyny with some elements of resource defence, at least in western Africa [115]. Chaerephon leucogaster and C. pusillus are sympatric on the island of Mayotte of th e Comoro archipelago and have been captured at the same roost sites [95]. Taphozous mauritianus has been recorded from a variety of roost types throughout its range including cliff walls , trunks of large trees, the outer walls of buildings, often in the open but out of direct su nlight [91]. Typically, T. mauritianus roosts in small groups of up to 12, with individuals spaced 10–15 cm [116]. Roosting behaviour of yangochiropterans on Mada gascar ranges from synantrophy to cave and foliage-roosting and may be seasonal, particularly in the north [117], requiring more long-term studies of bat abundance and movements. Coleura afra preferentially roost close to areas of open water, quite


Animals 2011 , 1 271 often in large colonies, but with di stinct and stable clustering of i ndividuals in harems [118]. Both of the Emballonura species described from Madagascar are c onsidered forest depe ndent and typically roost in exposed rock outcrops or caves, although E. tiavato is also synantrophic. Myzopoda aurita roosts among the unfurled leaves of native Ravenala madagascariensis in groups of 9–51 individuals and changes roost site every 1–5 days [119,120]. However, despite a number of specimens of M. aurita having been captured, not one female specimen has been obtained and the roosting behaviour of females is unknown [120]. Its sister species, M. schliemanni, from the dry western parts of Madagascar has also been descri bed as roosting in Ravenala madagascariensis [121], and potentially also in caves [122]. Various cave roostin g species may often be found in close association such as Miniopterus spp. , Myotis goudoti , Emballonura spp. , and Triaenops auritus [117]; although there is a distinct paucity of investigation into inter-specific interactions between co-roosting species in terms of competition for roost space and territoriality. An investigation of the habitat us e of 10 species of sympatric bats in western Madagascar found that four were predominantly associated with intact humid forests ( Miniopterus manavi , Miniopterus majori , E. atrata and M. goudoti , the latter species being most strongly associated with this habitat type) [123]. An additional two species fa voured agricultural or cultivated land ( E. matroka and Neoromica melckorum ) and a further three were synantrophic ( Mormopterus jugularis , C. leucogaster and Mops lecuostigma ). Taxon richness was highest in the inta ct humid forest, but intriguingly bat activity was greatest on agricu ltural or cultivated land, indicating that this hab itat type may be a more important foraging resource for all bats. Du ring the austral winter , large numbers of Mormopterus francoismoutoui abandon the roost site of Trois Bassins, although it is not known where they move to [108]. Scent-related cues from the inte r-aural and muzzle glandular area s mediate sex discrimination and roost-mate recognition for two species of African bat ( Mops condylurus and C. leucogaster (pumilus) , both of which are genera that occur on Madagascar) [124], and individual-speci fic features of sweep calls by Otomops martiensseni allow this species to discriminate between individuals [125], which is probably also the case for Otomops madagascariensis . Gular sacs positioned alongside the lower jaw in T. mauritianus may function in sexual attraction or stimul ation of females [126] . Descriptions of courtship behaviour in yangochiro pterans are greatly lacking. 3.3. Feeding Biology All yangochiropteran bats on Western Indian O cean islands are insectivores. Wing morphology is an excellent predictor of feeding behaviour in bats and available inform ation on wing morphology for some of the yangochiropteran specie s (or closely-related mainland Afri can forms) from western Indian Ocean islands has been described [127]. For example, C. leucogaster (pumilus) is adapted for fast flight in uncluttered (open) te rrain and prey is consumed wh ile flying [128], while the more manoeuvrable wing morphology of Triaenops furculus is more suited to flying among the forest canopy [129]. Detailed studies of the diets of yangochi ropterans from the western Indian Ocean islands have only been carried out for C. seychellensis and for some species from Madagascar. Extrapolation of information from closely-related mainland bat sp ecies can be misleading si nce insect assemblages can be quite different on islands compared to the nearest mainland faunal complement. Coleura


Animals 2011 , 1 272 seychellensis forages alone using aerial capture and glean ing over a number of habitat types and, targets a diversity of arthropods, with Coleoptera and Lepidoptera from woodland and Diptera from marshland being the main prey items selected [90,130-132]. Together, these studies suggest some flexibility in foraging strategy, so changes in food availability are unlikely to have been the major contributing factor to populat ion decline in this critically endangered species. A study of the diets of 3 synantrophic bats ( M. leucostigma, M. jugularis and C. leucogaster (pumilus )) from eastern Madagascar f ound that Coleoptera, Hemiptera, Lepidoptera and Diptera were the most important insect groups [133]. Howe ver, although the proportions of Hemiptera and Lepidoptera in the diet were compar able across all th ree species, there were differences in Coleoptera and Diptera, with Diptera more frequent in the diet of M. leucostigma while Coleoptera were more prevalent in the diet of M. jugularis [133]. In a dietary study of sympatric bats in western Madagascar [54], M. goudoti favoured Hymenoptera, Neuroptera and Araneae, whereas M. manavi focussed on Hemiptera, and both concentrated fo raging effort at fore st edge habitat. Male M. aurita tend to forage for Lepidopt era and Coleoptera within 1.8 km of thei r roost site; primarily in coffee plantations, degraded humid fore st and wooded grasslands, suggesting this species may be less impacted by habitat change, at least in terms of availability of foraging habitat [119]. However, until the foraging behaviour of females of th is species is determined (a female specimen has yet to be captured), the impact of habitat cha nge on this species remains unclear. The obligate cave-dweller O. madagascariensis also favours Lepidoptera and Coleoptera, albeit with considerable site variation between the proportion s of these two prey items [134]. Taphozous mauritianus, generally only encountered flying alone and not higher than the tops of trees at night, is thought to feed primarily on mo ths found in close proximity to roosts [91]. In a comparative study of foraging behaviour of Molossid bats in South Africa M. midas, which also occurs on Madagascar, ventured at least 10 km from itsÂ’ roost sites and foraged in the open away from the forest canopy [53] and this is also li kely to be the case in Madagascar. Both Nycteris thebaica and Nycteris grandis have been reported as gene ralist feeders, consuming a broad range of invertebrate and ve rtebrate prey using a variety of hunting strategies [135,136]. In fact, N. grandis has been reported as preying on N. thebaica on mainland Africa [137], and these two species are also sympatric on Unguja where this predator-prey relationship may also exist. 3.4. Reproductive Biology Apart from investigations into C. seychellensis [24,132], the species of yangoc hiropteran bat in the western Indian Ocean of greatest conservation con cern, and on-going research in Madagascar, data on reproductive biology for other island species are la rgely incidental and an ecdotal. The reproductive biology of a range of African bats, including some yangochiroptera occurring on western Indian Ocean islands, has been summarised in a st udy of the evolution of reproductive patterns a nd delays [138]. It is likely that reproductive behaviour is not significantly different be tween island and African mainland forms, where such parapatry occurs. In general, bats of the Family Molossidae are pol yestrous in both tropical and temperate climates, with a decrease in the length of the reproductive season with increa sing latitude, although reproductive information on this group from west ern Indian Ocean islands is greatly lacking. Pregnant females of


Animals 2011 , 1 273 O. madagascariensis have been captured in October in west ern Madagascar and in November in the south [134]. The non-molossid bats display a tendency towards se asonal or aseasonal pol yoestry in tropical latitudes and seasonal monoestry in temperate zone s. This division appears to arise more from differences in adaptability to clim atic factors in terms of foraging and roosting behaviour as opposed to sexual selection per se . Reproductive delays are the excepti on rather than the norm in tropical latitudes, although reproductive delay at a latitude of 4°S, which is typical for non-molossids only at latitudes greater than 13°N and 15°S, has been described in C. afra [138]. Pregnant C. seychellensis have been recorded in November and flying young in December and January, suggesting that births oc cur at the start of the NW m onsoon, although mating has also been observed in May suggesting that C. seychellensis may be polyoestrus [132]. Coleura afra displays post-partum oestrus and highly synchronised parturition after a typica l gestation period of 114 days [118,139]. There are two reproductive seasons coinciding with the two rainy seasons in coastal Kenya (March to June and November to December), and although most female C. afra give birth during the early rains, a large proportion may not reproduce in the later rainy season [118], and this is probably also the case in the Tanzanian offs hore islands. Juveniles born in the later rainy season tend to develop more slowly, but have a higher su rvival rate than those born in the early rainy season [135]. Taphozous mauritianus reproduce throughout the year [138]. Nycteris grandis probably give birth in late November and early December [136] , at least in the eastern extent of their range, which includes Pemba and Unguja. Mating behaviour in N. thebaica involves rapid a nd erratic flight, together with in-flight head-buttin g and neck-biting [140]. Implantation occurs in the ri ght uterine horn 16 days after mating and the subsequent gestation period is 2.5–3 months in tropical zones [135]. There is little information on reproductive behavi our for the western Indian Ocean emballonurid bats, but pregnant females of E. tiavato have been recorded in mid-December and lactating females in February. Chaerephon leucogaster (pumilus) is reported to display y ear-round polyoestry, producing as many as three litters a year in an 8-month breeding season [115,141], and although the uterus is bicornuate, implantation almost invari ably occurs in the right horn [142]. Myzopoda aurita appear to segregate sexually, since all colonies described to date only contain male specimens [119]. Thus, the reproductive behaviour of this sp ecies from eastern Madagascar remains obscure. The breeding period of M. leucostigma on the islands of Anjouan a nd Moheli (Comoro archipelago) centers around late Novemb er-early December [96]. 3.5. Conservation In many cases data is deficient on yangochiropteran species of low de nsity or that are difficult to capture, so estimates of population size may not be accurate, thus making it difficult to assign conservation status and determine management priori ties. For example, originally considered rare, E. atarata is, in fact, widespread throughout its range [102]. For most yangochiropteran species, disturbance directly at roost site s and/or through habitat alteration is the greatest thr eat to island bats. For exam ple, the role that human disturbance, particularly in relation to tourist vi sits to caves, plays in bat abundance a nd distribution has been documented in


Animals 2011 , 1 274 Tsingy de Bemaraha National Park in Madagascar [35]. However, the rela tionship between habitat alteration and conservation status is not straight -forward. As described ea rlier, cultivated and agricultural lands act as an importa nt habitat type for foraging bats, and many species are synantrophic. Thus, it is important to effect a balance between providing native r oosting and foraging habitat for less adaptable species that may be more susceptible to anthropogenic-induced population declines with retaining the mosaic habitat that more opportunistic species may thrive in. In order to achieve this, much greater effort must be invested in determ ining the ecological parameters that influence bat populations. This also impacts on efforts to delin eate conservation areas. Only a few species of yangochiropteran have been described as being fo rest-dependent (5 of 27 species according to one study [100]) in the dry regi ons of western Madagascar. Thus, si mply protecting the last remaining undisturbed areas of forest in these regions will not be sufficient to adequately buffer non-forestdependent species from threats else where (e.g., hunting, cave disturbance, etc. ). However, given that forest edge habitat is clearly a favoured foraging habitat for ma ny bat species [35,54], efforts must continue to safeguard the integrity of forest habitats in Madagascar , not only for its chiropterans, but also its other flora and fauna. Coleura seychellensis is one of only 15 species of yangochir opteran currently lis ted as Critically Endangered by the IUCN [79]. The total population size of C. seychellensis is unlikely to exceed 100 individuals [90,131], with the greate st threats being human disturban ce, predation by introduced barn owls and habitat alteration. A reduc tion in human disturbance, coinci dent with vegetation management at one roost site, has contributed to an increase in the lo cal population size of C. seychellensis [131]. Thus, in order to secure the future of this species and, indeed, to restore self-sustaining populations on the islands it previously inhabited, major habitat restoration projects must be enacted. Such restoration must involve the partial replacement of non-native vegetation, the control of public access to roosting sites and probably more controversially, the control or eradication of non-native predators from at least some of the islands. Investigation of movement be tween islands would greatly facilitate a workable management plan for this high pr ofile and highly endangered species. Certain species are of concern because of thei r restricted distributions e.g., the cave dwelling Taphozous hildegardeae is found only on Pemba and Unguja and fewer than ten African coastal localities and is therefore susceptible to disturbance and local extirpation. Tadarida fulminans is considered a patchily distribut ed and uncommon species in Mada gascar, with records mostly originating from the central-s outh region of the island [143]. While conservation efforts for larg er Yinpterochiroptera have been effected throughout the western Indian Ocean, the less ‘charismatic’ Yangochiropter a have been largely ove r-looked. Many of the more recently described species from Madagascar have been recorded within established national parks [111], although this could be an artefact of sampling bias and in formation is limited on the status of bats outside of these areas. Gi ven that the biology of Yinpteroch iroptera and Yan gochiroptera are significantly different in many cases , conservation efforts for one group will not necessarily benefit the other. Clearly, greater efforts need to be focussed on protecti ng known cave roosting sites and synanthropic structures where they are important refuges for these smaller bats. Targeted education programmes, which have been so successful fo r fruit bats on islands such as Pemba and Rodrigues [89], need to be replicated for the yangochiro pteran bats that also pl ay an important role in


Animals 2011 , 1 275 ecosystem functioning. An update to the 2001 IUCN report ‘ Microchiropteran Bats: Global Status Survey and Conservation Status ’ is needed [144]. 4. Conclusions This work provides a synthesis of current data on bats from the islands in the western Indian Ocean. Clearly, not all available informati on is included, nor are all references cited. However, some obvious concerns are apparent: (1) greater efforts are requi red to enact legislative safeguards in many island nations to protect both yinpteroc hiropterand and yangochiropterans from excessive exploitation; (2) research into the fruit bat–fruit grower conflict must be unde rtaken urgently in terms of the likely economic costs of fruit bat foraging habits and po ssible mitigation strategies; (3) greater focus on the basic biology of yangochiropteran bats and, in particular, on fora ging and reproductive behaviour to better determine conservation requirements; (4) resour ces must continue to be dedicated to carrying out regular census surveys of bat populations throughout the region to elucidate population cycles and trends; and (5) expand community education programm es throughout the region to encompass all bats. Acknowledgments The author wishes to thank Justin Gerlach for pr oviding the initial impetus to produce this paper and the anonymous referees who provided valuable guidance on this and earlier versions of this manuscript. Conflict of Interest The author declares no conflict of interest. References 1. Alcover, J.A.; Sans, A.; Palmer, M. The exte nt of extinctions of mammals on islands. J. Biogeogr. 1998 , 25 , 913-918. 2. Warren, B.H.; Bermingham, E.; Bowie, R.C.K.; Prys-Jones, R.P.; Thébaud, C. Molecular phylogeography reveals island coloni zation history and diversificat ion of western Indian Ocean sunbirds ( Nectarinia : Nectariniidae). Mol. Phylogent. Evol . 2003 , 29 , 67-85. 3. Peake, J.F. The evolution of terrestri al faunas in the western Indian Ocean. Phil. Trans. Roy. Soc. Lond. B Biol. Sci. 1971 , 260 , 581-610. 4. Teeling, E.C.; Springer, M.S.; Madsen, O.; Bate s, P.; O’Brien, S.J.; Murphy, W.J. A molecular phylogeny for bats illuminates bi ogeography and the fossil record. Science 2005 , 307 , 580-584. 5. Jones, J.; Teeling, E.C. The evol ution of echoloc ation in bats. TREE 2006 , 21 , 149-156. 6. Hutcheon, J.M.; Kirsch, J.A.W. A movable face: Deconstructing the yangochiroptera and a new classification of extant bats. Acta Chiropterol. 2006 , 8 , 1-10. 7. Cheke, A.S.; Dahl, J.F. The status of bats on the western Indian Ocean islands, with special reference to Pteropus . Mammalia 1981 , 45 , 205-238.


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Animals 2011 , 1 284 142. Mutere, F.A. Reproduction in two species of equatorial free-taile d bats (Molossidae). Afr. J. Ecol. 1973 , 11 , 271-280. 143. Jenkins, R.K.B.; Kofoky, A.F.; Russ, J.M.; Fria fidison, A.; Siemers, B. M.; Randrianandrianina, F.H.; Mbohoahy, T.; Rahaingodrahety, V.N.; Racey, P.A. Ecology of bats in the southern Anosy region. In Biodiversity, Ecology and Conservation of Li ttoral Ecosystems in Southeastern Madagascar, Tolagnaro (Fort Dauphin) ; Ganzhorn, J.U., Goodman, S. M., Vincelette, M., Eds.; Smithsonian Institution: Wash ington, DC, USA, 2008; pp. 209-222. 144. Hutson, A.M.; Mickleburgh, S.P.; Racey, P.A. Micr ochiropteran Bats: Global Status Survey and Conservation Status. IUCN/SSC Chiroptera Specialist Grou p, IUCN: Gland, Switzerland, 2001; pp. 1-272. 145. Kock, D.; Stanley, W.T. Mammals of Mafia Island, Tanzania. Mammalia 2009 , 73 , 339-352. 146. Goodman, S.M.; Ranivo, J. A new species of Triaenops (Mammalia, Chiroptera, Hipposideridae) from Aldabra Atoll, Picard Island (Seychelles). Zoosystema 2008 , 30 , 681-693. 147. Rasolozaka, I.N. Les Microchiropteres. In Inventaire biologique Fore t de Zombitse. Recherches sur le development ; Serie Sciences biologiques; Goodm an, S.M., Legrand, O., Eds.; Centre dÂ’Information et de Documentation Scientifiq ue et Technique: No. Special. Antananarivo, Madagascar, 1994; pp. 64-67. 148. Goodman, S.M.; Ranivo, J. The geographica l origin of the type specimens of Triaenops rufus and T. humbloti (Chiroptera: Hipposiderida e) reputed to be from Madagascar and the description of a replacement species name. Mammalia 2009 , 73 , 47-55. 149. Goodman, S.M.; Maminirina, C.P.; Weyeneth, N. ; Bradman, H.M.; Christidis, L.; Ruedi, M.; Appleton, B. The use of molecular and morphol ogical characters to resolve the taxonomic identity of cryptic species: The case of Miniopterus manavi (Chiroptera: Miniopteridae). Zool. Scripta 2009 , 38 , 339-363. 150. Peterson, R.L.; Eger, J.L.; Mitchell, L. Faune de Madagascar. 84 Chiropteres ; Museum National d'Histoire Naturelle: Paris, France, 1995; pp. 1-204. 151. Goodman, S.M.; Bradman, H.M.; Maminirina, C.P.; Ryan, K.E.; Christidis, L.L.; Appleton, B. A new species of Miniopterus (Chiroptera: Miniopteridiae) from lowland southeastern Madagascar. Mammal. Biol. 2008 , 73 , 199-213. 152. Goodman, S.M.; Ryan, K.E.; Maminirina, C.P.; Fa hr, J.; Christidis, L.; Appleton, B. Specific status of populations on Madagascar referred to Miniopterus fraterculus (Chiroptera: Vespertilionidae), with description of a new species. J. Mammal. 2007 , 88 , 1216-1229. 153. Goodman, S.M.; Ranivo, J. The taxonomic status of Neoromicia somalicus malagasyensis . Mammal. Biol. 2004 , 6 , 434-438. 154. Goodman, S.M.; Jenkins, R.K.B.; Ratrimom anarivo, F.H. A review of the genus Scotophilus (Chiroptera: Vespertilionidae) on Madagascar , with the description of a new species. Zoosystema 2005 , 27 , 862-882.


Animals 2011 , 1 285 Appendix Table 1. Bats of the Western Indian Ocean islands. Seyc helles refers to granitic Seychelles (except a). * IUCN Risk data from 2010 IUCN Red List of Threatened Species http://www.iucn, Downloaded 05 January 2011. CR = Critical, DD = Data Deficient, EX = Ext inct, LC = Least Concern, LRlc = Low Risk least concern, LRnt = Low Ri sk near threatened, NT = Near Threatened, VU = Vulnerable. a Reported [145], but no voucher specimens taken. a Specifically, Picard Island—it has been suggested that references for T. furculus on Cosmoledo Atoll were in error [146]. b Presence questioned [109,110]. c Restricted to the island of Anjouan. dKnown only from a single specimen collected in 1868 at Sarodrano (may well be extinct). e Although this species is listed as DD by the IUCN, it has not been recorded on Réunion for almost 140 years, despite extensive survey work. f Reported in western Madagascar [ 147], but requires verification [101,100]. 1Some authors place T. furculus, T. auritus and T. paulani in a new genus Paratriaenops , while the other Malagasy species, T. menamena , remains in Triaenops [21]. IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra YINPTEROCHIROPTERA Pteropodidade E idolon dupreanum (Schlegel 1867) E idolon helvum (Kerr 1792) VU NT X X X X E pomophorus labiatus (minor) (Dobson 1880) E pomophorus wahlbergi (Sundevall 1846) LC LC X X X X X


Animals 2011 , 1 286 Table 1. Cont . IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra P teropus sp. P . aldabrensis (True 1893) P . giganteus ariel (Allen 1908) P . hypomelanus maris (Allen 1936) P . livingstonii (Gray 1866) P . nige r (Kerr 1792) P . rodricensis (Dobson 1878) P . rufus (Geoffroy 1803) P . seychellensis (Milne-Edwards 1877) P . subnige r (Kerr 1792) P . voeltzkowi (Matschie 1909) VU EX EN EN CR VU LC EX VU X X X X EX EX EX X X EX X X X EX X X R ousettus sp. R . aegypticus (Geoffroy 1810) R . madagascariensis (Grandidier 1928) R . obliviosus (Kock 1978) LC NT VU X X X X Rhinolophidae R hinolophus sp. R . clivosus (Cretzschmar 1828) R . deckenii (Peters 1867) R . eloquens (Andersen 1905) R . hildebrandti (Peters 1878) R . landeri (Martin 1838) R . swinnyi (Gough 1908) LC NT LC LC X X X X X X X X X


Animals 2011 , 1 287 Table 1. Cont . IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra Rhinopomatidae R hinopoma cystops (hardwickii) (Thomas 1913) LC X Hipposideridae A sellia tridens (Geoffroy 1813) LC X Cloeotis percivali (Thomas 1901) Xa H ipposideros caffer (Sundevall 1846) H ipposideros commersoni (Geoffroy 1813) H ipposideros vittatus (Peters 1852) LC NT X X X X X Triaenops sp1. T. auritus (Grandidier 1912) T. furculus (Trouessart 1906) T. menamena (rufus) [148] T. pauliani [146] VU LC LC X X X Xa YANGOCHIROPTERA Emballonuridae Coleura afra (Peters 1852) Coleura seychellensis (Peters 1868) LC CR X X X E mballonura atrata (Peters 1874) E mballonura tiavato [102] LC LC X X Taphozous mauritianus (Geoffroy 1818) Taphozous hildegardeae (Thomas 1909) LC VU X X X X X X X X


Animals 2011 , 1 288 Table 1. Cont . IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra Molossidae Chaerephon (Tadarida) sp. C. jobimena [98] C. leucogaster (pumilus) (Grandidier 1869) C. pusillus (Miller 1902) C. astinanana [94] LC X X X X X X X X X M ops (Tadarida) sp. M . bakarii [110] M . brachypterus (Peters 1852) M . leucostigma (Allen 1918) M . midas (Sundevall 1843) LC LC LC X X X X Xb X M ormopterus acetabulosus (Hermann 1804) M ormopterus francoismoutoui [108] M ormopterus jugularis (Peters 1865) VU LC X X X Otomops madagascariensis (Dorst 1953) LC X Tadarida fulminanas (Thomas 1903) LC X Myzopodidae M yzopoda aurita (Milne-Edwards & Grandidier 1878) LC X M yzopoda schliemanni [121] LC X


Animals 2011 , 1 289 Table 1. Cont . IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra Nycteridae N ycteris sp. N . grandis (Peters 1865) N . hispida (Schreber 1775) N . macrotis (luteola) (Dobson 1876) N . madagascariensis (Grandidier 1937) N . thebaica (Geoffroy 1818) LC LC LC DD LC X X X X X X X Vespertilionidae E ptesicus (Neoromicia) matroka (Thomas & Schwann 1905) LC X M iniopterus sp. M . aelleni [149] M . brachytragos [105] M . gleni [150] M . griveaudi (Harrison 1959) M . mahafaliensis [105] M . majori (Thomas 1906) M . manavi (Thomas 1906) M . minor (Peters 1867) M . petersoni [151] M . sororculus [152] LC LC LC DD LC X X X X X X X X X X X X


Animals 2011 , 1 290 Table 1. Cont . IUCNRisk*Madagascar Seychelles Aldabra Mauritius Rodrigues Réunion Comoros Maldives Pemba Unguja Mafia Socotra M yotis anjouanensis (Dorst 1960) M yotis goudoti (Smith 1834) DD LC X Xc N eoromicia sp . N . (Eptesicus) malagasyensis [153] N . (Pipistrellus) melckorum (Roberts 1919) EN DD X X P ipistrellus sp. P . grandidieri (capensis) (Dobson 1876) P . hesperidus (Temminck 1840) P . (Neoromica) nanus (Peters 1852) P . raceyi [101] P . rueppellii (Fischer 1829) LC LC DD LC X Xf X X X X X X X X H ypsugo (Pipistrellus) anchietae (Seabra 1900) H ypsugo (Pipistrellus) ariel (Thomas 1904) LC X X Scotophilus sp. S. cf. borbonicus (Geoffroy 1803) S. marovaza [103] S. robustus (Milne-Edwards 1881) S. tandrefana [154] S. viridis (Peters 1852) DD LC LC DD LC Xd X X X EXe X X © 2011 by the authors; licensee MDPI, Basel, Switzerland. This ar ticle is an open access article distributed under the terms an d conditions of the Creative Commons Attribution license (http://


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