The Vulnerable Fish-Eating Bat Myotis Vivesi

Geographical distribution and conservation status of an endemic insular mammal: the Vulnerable fish-eating bat Myotis vivesi

L. GERARDO H ERRERA M., JOSÉ J UAN F LORES-MARTÍNEZ and V ÍCTOR S ÁNCHEZ-CORDERO

Abstract Endemic insular species are particularly vulner- and vulnerability to a variety of threats (Courchamp et al., able to anthropogenic threats. The fish-eating bat Myotis ). Mexico is an important region for biodiversity con- vivesi is restricted mainly to the islands of the Gulf of servation, given its high number of species, many of California in Mexico and although several aspects of its biol- which are endemic (Martínez-Meyer et al., ). A high ogy have been studied there are no recent accounts of its proportion of Mexican mammal species are endemic current distribution. We conducted several expeditions dur- (%), of which % are found only on islands (Ceballos ing – to verify the current geographical distribution & Rodríguez, ). Endemic insular mammal species are of this bat, and to record the presence of introduced preda- particularly vulnerable; for example, % of extinctions of tors. We identified the localities in which maternity colonies endemic Mexican mammals have occurred on islands occur, estimated the size of the bat population on Partida (Ceballos & Navarro, ; Mellink, ; Tershy et al., Norte Island in , and monitored bat presence on this ). island during –. We found fish-eating bats on  A prominent example of an insular threatened Mexican islands and maternity colonies on  islands. Introduced mammal is the fish-eating bat Myotis vivesi (Vespertillionidae; rats Rattus rattus or cats Felis catus were captured on Herrera & Flores-Martínez, ). The bat is endemic to seven islands where the bats were present, and on five is- islands of the Gulf of California, with a few reports of its lands where they were absent. We estimated a population presence on the Gulf and Pacific coastlines (Blood & of c. , fish-eating bats in May  and we confirmed Clark, ), and is categorized as Vulnerable on the the species’ presence on Partida Norte Island during – IUCN Red List (Arroyo-Cabrales & Ospina-Garces, ) . Based on the information compiled from our surveys and Endangered, with risk of extinction, by Mexican au- and previous studies, we discuss the adequacy of the species’ thorities (SEMARNAT, ). The fish-eating bat generally current categorization as Vulnerable on the IUCN Red List, roosts within rock crevices on talus slopes, making it easy and its conservation status conferred by Mexican conserva- prey for introduced domestic cats Felis catus and black tion authorities. Rattus rattus and brown rats Rattus norvegicus. The bat forms maternity colonies during spring–summer (Flores- Keywords Bat maternity colonies, endemic species, Gulf of Martínez et al., ) and, unlike other bat species, it California, introduced fauna, islands, Mexico, Partida Norte feeds mainly on marine fish and crustaceans (Otálora- Island, risk of extinction Ardila et al., ). Supplementary material for this article is available at The fish-eating bat has been reported historically from https://doi.org/./S almost  localities (McLellan, ; Miller & Allen, ; Burt, ; Walker, ; Reeder & Norris, ; Cockrum & Bradshaw, ; Maya, ; Patten & Findley, ; Villa, ; Blood & Clark, ) but there is no recent Introduction account of its distribution. Here we present the results of ceanic islands have captured the attention of conserva- several expeditions conducted to verify the current geo- tion biologists because of the high species endemism graphical distribution of the fish-eating bat. We identified O the localities in which maternity colonies are formed, estimated the population size of the Partida Norte colony in L. GERARDO HERRERA M. (Corresponding author) Estación de Biología de , and monitored the presence of bats on Partida Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, – Apartado Postal 21, San Patricio, Jalisco 48980, México Norte Island during . We also recorded the pres- E-mail [email protected] ence of introduced domestic cats and rats (Villa, ). JOSÉ JUAN FLORES-MARTÍNEZ (Corresponding author) and VÍCTOR SÁNCHEZ- Based on the information derived in our surveys along CORDERO, Laboratorio de Sistemas de Información Geográfica, Departamento with published information on the biology of the fish- de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Cd. de México, México. E-mail [email protected] eating bat, we discuss the adequacy of its conservation status Received  January . Revision requested  February . on the IUCN Red List and that established by Mexican Accepted  May . First published online  September . authorities.

Oryx, 2019, 53(2), 388–393 © 2017 Fauna & Flora International doi:10.1017/S0030605317000874 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 27 Sep 2021 at 16:31:10, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605317000874 The fish-eating bat 389

Methods We extracted fish-eating bats from – quadrats ( ×  m) in each sampling period, and returned them to their roosts   We visited sites ( islands and eight mainland sites) in following processing. Therefore, our sampling protocol did     the Gulf of California ( , km ; Case et al., )in not use a standard methodology to produce estimates of – north-west Mexico during expeditions in , population size or to establish patterns in sex ratio; rather it –   – , , and (Supplementary was conducted opportunistically while monitoring the long-  Table S ). Sites were selected based on historical records of term temporal presence of fish-eating bats on the island. the presence of fish-eating bats, but we also included sites where their presence was not reported previously. Most sites visited were islands; only eight were on the mainland. Results We opened – mist nets (× m) during – nights at each   site visited; nets were open from sunset to . and they We captured or observed fish-eating bats on islands, of  were checked every – minutes. Captured bats were which were new reports (Supplementary Table S ). We re-   sexed and their reproductive condition determined based corded absence of the bats at sites, of which had been  on external morphological evidence. To determine the reported previously (Supplementary Table S ). Maternity  presence of introduced domestic cats and rodents on each colonies of the fish-eating bat were found on islands  island, we set – Tomahawk (Hazelhurst, USA) and – (Supplementary Table S ). We captured black rats on five is-  Sherman (Tallahassee, USA) traps during – nights; lands where the bat was present and on one island where the we also surveyed the area for the presence of cat scats. bat was absent; we captured mice Mus musculus on one island Some islands were surveyed for bats and introduced fauna where the bat was present, and black rats and mice on one on more than one occasion. We used ArcGIS . (ESRI, island with and one island without bats (Supplementary  Redlands, USA) to estimate the extent of occurrence (‘the Table S ). We captured no cats but we found their scats on area contained within the shortest continuous imaginary one island where the bat was present and on three islands  boundary which can be drawn to encompass all the where the bat was absent (Supplementary Table S ). The    known, inferred or projected sites of present occurrence of extent of occurrence estimated for the bat was , km . a taxon’; IUCN, ) based on the sites where we found the The sum of the areas of the islands on which fish-eating    bat. We estimated the area of each island surveyed using bats were found was . km , and the sum of the areas of    ArcGIS .. the islands on which the bat was absent was . km  We estimated the size of the adult population in the bat (Supplementary Table S ).   colony on Partida Norte Island in May  using the We estimated a population size of , adult fish-eating   method used by Flores-Martínez et al. (). The popula- bats in May on Partida Norte Island, of which c. %    tion size of this colony had been estimated in May  were females (Table ). We estimated the presence of ,   using quadrats located at two sites used as roosts by bats young, with a slightly higher proportion of males ( . %)    (sites  and  in Flores-Martínez et al., ). Fish-eating than females ( . %; Table ). We captured fish-eating  bats also roost on cliffs but surveying these areas was not bats in all years in which we visited Partida Norte   possible. We recorded presence of fish-eating bats in – Island (Supplementary Table S ; Table ). quadrats ( ×  m) placed randomly in seven roosting areas  (Table ). We measured the area covered by each roosting Discussion site using a metric tape and extrapolated the number of bats present using the mean number of bats per quadrat at Given the high levels of endemism on its .  islands, the each site. We considered the total adult population size to be Gulf of California is a biodiversity hotspot for conservation the sum of the number of bats estimated for each roosting (Case et al., ; Tershy et al., ). The uniqueness of the area. We recorded the presence of young and estimated biology of the fish-eating bat makes it a particularly threa- their total number similarly. We conducted our sampling tened species. Our expeditions found that this bat is wide- in the southern portion of the island, including sites ,  spread in the Gulf of California, although we failed to find and  from Flores-Martínez et al. () and four additional evidence of its presence at some sites where it was recorded sites. We did not sample the northern part of the island historically. At some sites (San Carlos Bay and San Sebastián (sites ,  and  from Flores-Martínez et al., ). We Vizcaíno) the absence is probably temporary; for example, also monitored the presence of the bat on Partida Norte records from the mainland probably reflect temporary Island in – periods during – and –. roosting when foraging (Maya, ). Similarly, some of We did not attempt to repeat the extensive surveying con- the islands where we did not observe fish-eating bats are ducted in  and , to avoid disturbing the roosts. probably used occasionally at night; for example, there is a Instead, we conducted low-intensity, non-systematic sam- historical record of the presence of fresh guano on Carmen pling as part of other projects to study the bat’s ecology. (Maya, ), and it seems the bats use Rasa to perch while

TABLE 1 Population estimates for the fish-eating bat Myotis vivesi at seven roosting sites at the southern end of Partida Norte Island in May  (site , Fig. ), with the site area, number of  ×  m quadrats, and numbers of adult and young males and females.

No. of adults No. of young Males per Females per Males per Females per Area No. of quadrat Total quadrat Total quadrat Total quadrat Total Site (m2) quadrats (mean ± SE) males (mean ± SE) females (mean ± SE) males (mean ± SE) females 1 941 8 0 0 3.25 ± 0.31 3,058 0.75 ± 0.12 706 2.12 ± 0.29 1,995 2 2,622 15 0.13 ± 0.04 341 2.73 ± 0.34 7,158 1.40 ± 0.16 3,670 0.92 ± 0.11 2,412 3 3,405 15 0.06 ± 0.04 204 1.20 ± 0.37 4,086 0.53 ± 0.17 1,805 0.46 ± 0.17 1,566 4 1,352 9 0 0 2.77 ± 0.25 3,745 1.44 ± 0.16 1,947 0.88 ± 0.13 1,190 5 500 13 0.07 ± 0.04 35 1.42 ± 0.36 710 0.75 ± 0.14 375 0.57 ± 0.18 285 6 673 16 0.07 ± 0.02 47 1.25 ± 0.27 845 0.66 ± 0.15 444 0.50 ± 0.18 337 7 5,814 14 0.14 ± 0.05 813 1.64 ± 0.23 9,534 0.71 ± 0.17 4,125 0.71 ± 0.12 4,125 Total 1,440 29,136 13,072 11,910

foraging, as we found fresh guano there during our visit. In we found only rats in  and . It is probable that the contrast to most historical accounts of the bat’s distribution, bats use the island transiently while foraging, and that their we are certain that the sites where we recorded presence of permanent presence is prevented by the presence of rats. Rat the fish-eating bat represent established colonies on islands eradication actions were conducted on Mejía in  (J.J. used as daytime roosts (but see below for Mejía Island). The Flores-Martínez, pers. comm.) but eradication was not con- absence of fish-eating bats on some islands may simply in- firmed afterwards. In our surveys in  and  we cap- dicate that their use of islands is temporary, and that some tured no rats on Mejía but nor did we capture any bats. We islands are abandoned when new sites are colonized; for ex- did not observe fish-eating bats on San Pedro Mártir () ample, although Partida Norte and Cardonosa Islands are or Rasa Islands after eradications, although these islands are occupied by an equal number of males and females during probably used as nocturnal perches. autumn and winter, most adult males abandon these islands The fish-eating bat is categorized as Vulnerable on the during spring–summer, with the remaining bats comprising IUCN Red List (Arroyo-Cabrales & Ospina-Garces, ) mostly pregnant and lactating females with young (Maya, based on a . % population decline over the last three gen-  ; Flores-Martínez et al., ). It is possible that males erations, an area of occurrence of , km with a severe- use different islands at different times of the year, and there- ly fragmented distribution, a declining area of occupancy fore the timing of surveys is critical for their detection at a (‘the area within its extent of occurrence which is occupied particular site. In most cases we are not certain if the sites by a taxon’; IUCN, ), and a low rate of recolonization of where we found maternity colonies have similar presence– restored habitat because of a strong female philopatry. We absence temporality to Partida Norte and Cardonosa consider this categorization to be appropriate but we dis- Islands, as they were visited mostly during spring–summer. agree in part with some of the reasoning. There is no Most islands where fish-eating bats were observed published evidence that the population size (‘total number seemed to offer adequate conditions for their survival, as of individuals of the taxon’; IUCN, ) has decreased by no introduced domestic cats or rats were found. However, . %. The only colony in which the population size has these introduced species are predators of the fish-eating been estimated is on Partida Norte Island, where there bat (Villa, ; Vázquez-Domínguez et al., ) and are were estimated to be ,–, adults in June–July probably one of the main threats to its survival (Ceballos  (Maya, ), c. , adults in May  (Flores- & Navarro, ). Invasive mammals are responsible for Martínez et al., ), and , adults in May  (this most extinctions and extirpations in north-west Mexico study). These estimates indicate that the size of the colony (Tershy et al., ) and we found cats and rats on several did not decrease in the -year period in which the surveys islands where fish-eating bats were present. Cats have been were conducted. Additionally, we have recorded a continu- eradicated from Mejía (–), Danzante () and ous presence of fish-eating bats on Partida Norte Island Estanque Islands (), and rats have been eradicated since , with no obvious declining trend. Our estimate  from Rasa (–), San Pedro Mártir () and San of the area of occurrence (, km ) is less than half Jorge Islands (–) (Ceballos & Ramírez, ; that estimated by IUCN, which is partly explained by the Aguirre-Muñoz et al., , ). We found fish-eating fact that we did not record the presence of bats at mainland bats on Danzante, Estanque and San Jorge Islands after sites, which are probably used only as resting sites. Although these predators had been eradicated. We found both fish- the area of occurrence of fish-eating bats is highly fragmen- eating bats and rats on Mejía Island in  and , but ted, with daytime roost sites separated by large expanses of

The fish-eating bat is listed as an Endangered species by Mexican conservation authorities, based on its geographical distribution in Mexico, the quality of the habitat in relation to the requirements of the species, its intrinsic biological vulnerability, and the impact of human activity (Sánchez et al., ). We consider this categorization to be appropriate, as the species’ extent of occurrence is , % of Mexico’s total land area. The species is intrinsically vulnerable because its roosting habits expose it to a large range of terrestrial predators and it aggregates in large numbers (thousands of individuals) in relatively small areas. The bat is susceptible to the effects of human activities because the islands are used regularly by local fishers to camp, and to the presence of cats and rats (which are also vectors of emerging diseases). The Gulf of California is exposed to the effects of inter- annual climate events, industrialized, sport and artisanal fisheries, and coastal zone usage that can have profound effects on biota (Lluch-Cota et al., ). Several of the islands on which we recorded fish-eating bats are considered to be of high priority for biodiversity conservation in this area FIG. 1 Sites in the Gulf of California surveyed for the presence (WWF, ). Management strategies for the conservation of the fish-eating bat Myotis vivesi during – (see of this species are similar to currently established policies for Supplementary Table S for details). Numbers in black represent other threatened vertebrates inhabiting these islands; for sites where the bat was found; numbers in red represent sites example, monitoring of the presence of introduced verte- where the bat was absent. brates, and implementation of eradication programmes where necessary; restriction of human activities on the is- open water, nuclear DNA analysis has indicated high rates lands; monitoring of the population size of selected colonies of gene flow among colonies (Floyd et al., ). The area of (especially maternity colonies); periodic surveys of the geo- occupancy of the species has probably declined over time, as graphical distribution of the species; examination of bat tis- indicated by the IUCN assessment and the fact that we did sues for the presence of anthropogenic contaminants (e.g. not find bats in some locations where they had been re- heavy metals; Méndez & Alvarez-Castañeda, ); and as- corded previously. The area of occupancy of fish-eating sessment of the effects of fisheries on food resource avail- bats includes both terrestrial and oceanic habitats, which ability. Given its feeding habits, the conservation of the play different roles and have different properties. The fish-eating bat is relevant for the nutritional and energy oceanic part of the area of occupancy is used for foraging, budget of terrestrial ecosystems where it roosts, because it and preliminary global positioning system tracking of bats transports marine-derived nutrients and energy (Otálora- from Partida Norte Island revealed that foraging is consist- Ardila et al., ). Protecting the species involves the con-  ently restricted to an area of c. , km (E. Hurme, servation of a unique adaptation to marine environments Y. Yovel & L. G. Herrera M., unpubl. data). The terrestrial not present in any other bat species. component of the area of occupancy is represented by the suitable portion of the islands used as roosting habitat. The total area of all islands where we found bat roosts was  Acknowledgements . km but the sum of the actual areas used as roost by bats on each island may be smaller; for example, on This study was funded by grants to LGHM and JJFM from Partida Norte Island areas with rock slides that are suitable Bat Conservation International and Programa para la for establishing roosting sites comprise , % of the total Conservación de los Murciélagos de México, by a grant to surface of the island. Therefore, the area of occupancy for JJFM from Consejo Nacional de Ciencia y Tecnología the oceanic and terrestrial habitats may be only a small por- (#), and by grants to LGHM from Dirección de tion of the habitat available for the fish-eating bat within its Asuntos del Personal Académico (IN,IN), extent of occurrence. We agree that strong female philopatry Fondo Sectorial de Investigación Ambiental (#C-), could reduce the probability of fish-eating bats recolonizing Comisión Nacional Para el Uso y Conocimiento de la restored habitats (Floyd et al., ), although we know of Biodiversidad (#HK), and Consejo Nacional de no attempts to evaluate this. Ciencia y Tecnología (#). The study was conducted

with permits from Secretaría de Medio Ambiente y Recursos COURCHAMP, F., HOFFMANN, B.D., RUSSELL, J.C., LECLERC,C.& Naturales. Ulalume Hernández A., Valeria B. Salinas R., BELLARD,C.() Climate change, sea-level rise, and conservation:  Aída Otálora A. and Marcia Carmona M. participated in keeping island biodiversity afloat. Trends in Ecology & Evolution, , –. the projects from which the long-term monitoring of the FLORES-MARTÍNEZ, J.J., FLOYD, C.H., HERRERA, L.G. & MAY,B. bat colony on Partida Norte Island was derived. () Genetic variation and population size of the fishing bat, Transportation was generously provided by Secretaría de Myotis vivesi, in Isla Partida. In Homenaje a Bernardo Villa (eds Marina-Armada de México. Alfredo Zavala, Carlos R. Medellín & V. Sánchez-Cordero), pp. –. Universidad Godínez, Juan Pablo Gallo, Tad Pfister, Lorayne Meltzer, Nacional Autónoma de México, Mexico City, Mexico. FLOYD, C.H., FLORES-MARTÍNEZ, J.J., HERRERA M., L.G., MEJÍA,O. the Prescott College Kino Bay Center and personnel from &MAY,B.() Conserving the endangered Mexican fishing bat the Área de Protección de Flora y Fauna Islas del Golfo de (Myotis vivesi): genetic variation indicates extensive gene flow California-Baja California provided invaluable logistic sup- among islands in the Gulf of California. Conservation Genetics, , port. We thank Leonel Moreno M. and Vaporub for making –.  the expeditions safer and more enjoyable. HERRERA, L.G. & FLORES-MARTÍNEZ, J.J. ( ) Conserving fishing bats in the Sea of Cortez. Bats, , –. IUCN () IUCN Red List Categories and Criteria: Version .. Second edition. IUCN, Gland, Switzerland, and Cambridge, UK. Author contributions LLUCH-COTA, S.E., ARAGÓN-NORIEGA, E.A., ARREGUÍN-SÁNCHEZ, F., A URIOLES-GAMBOA, D., BAUTISTA-ROMERO, J.J., BRUSCA, R.C. LGHM and JJFM designed the study and collected data. et al. 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conservation model integrating research, education and exotic WWF () Estableciendo prioridades de conservación en islas del mammal eradication. In Turning the Tide: The Eradication of Golfo de California: un ejercicio con criterios múltiples. Http:// Invasive Species (eds C.R. Veitch & M.N. Clout), pp. –. IUCN awsassets.panda.org/downloads/rep_prioridadesconservacionislas_ SSC Invasive Species Specialist Group. IUCN, Gland, Switzerland, .pdf [accessed  June ]. and Cambridge, UK. VÁZQUEZ-DOMÍNGUEZ, E., CEBALLOS,G.&CRUZADO,J.() Extirpation of an insular subspecies by a single introduced cat: the Biographical sketches case of the endemic deer mouse Peromyscus guardia on Estanque Island, Mexico. Oryx, , –. L. GERARDO H ERRERA and J. J UAN F LORES-MARTÍNEZ have led VILLA,B.() Algunas aves y la rata noruega Rattus norvegicus several projects on the biology and conservation of the fish-eating bat ‘versus’ el murciélago insulano Pizonyx vivesi en las islas del Mar de during the last  years. Herrera conducts research in bat ecology, Cortés, México. Anales del Instituto de Biología, Universidad physiology and conservation. Flores-Martínez is carrying out research Nacional Autónoma México, Serie Zoología, , –. on mammal biology, and supervises projects for the eradication of in- WALKER, L.W. () The fish bats of Pescador. Audubon, , troduced fauna. VÍCTOR SÁNCHEZ-CORDERO conducts research in –. natural protected areas.