Unexplored Diversity and Conservation Potential of Neotropical Hot Caves

Unexplored Diversity and Conservation Potential of Neotropical Hot Caves

Essay Unexplored Diversity and Conservation Potential of Neotropical Hot Caves RICHARD J. LADLE,∗†JOAO˜ V. L. FIRMINO,∗ ANA C. M. MALHADO,∗§ AND ARMANDO RODR´IGUEZ-DURAN‡´ ∗Institute of Biological and Health Sciences, Federal University of Alagoas, Av. Lourival Melo Mota, s/n, Tabuleiro do Martins, Maceio,´ AL 57072-900, Brazil †School of Geography and the Environment, Oxford University, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, United Kingdom ‡Universidad Interamericana de Puerto Rico, 500 John W. Harris, Bayamon´ 00957, Puerto Rico Abstract: The term hot cave is used to describe some subterranean chambers in the Neotropics that are characterized by constantly high ambient temperatures generated by the body heat of high densities of certain bat species. Many of these species have limited geographic ranges, and some occur only in the hot-cave environment. In addition to the bats, the stable microclimate and abundant bat guano provides refuge and food for a high diversity of invertebrates. Hot caves have so far been described in the Caribbean and in a few isolated locations from Mexico to Brazil, although there is some evidence that similar caves may be present throughout the tropics. The existing literature suggests these poorly known ecosystems, with their unique combination of geomorphology and bat-generated microclimate, are particularly sensitive to disturbance and face multiple threats from urbanization, agricultural development, mining, and tourism. Keywords: arthropods, bats, Brazil, species discovery Diversidad No Explorada y Potencial de Conservacion´ de Cuevas Neotropicales Calientes Resumen: El t´ermino cueva caliente es utilizado para describir algunas camaras´ subterraneas´ en el Neotropico´ que se caracterizan por temperaturas ambientales elevadas generadas por el calor corporal de densidades altas de ciertas especies de murci´elagos. Muchas de estas especies tienen rangos de distribucion´ ge- ografica´ limitados, y algunas solo ocurren en el ambiente de cueva caliente. Adicionalmente a los murci´elagos, el microclima estable y la abundancia de guano de murci´elago proporcionan refugio y alimento a una alta diversidad de invertebrados. A la fecha, se han descrito cuevas calientes en el Caribe y en unas cuantas localidades aisladas entre M´exico y Brasil, aunque hay evidencia de que puede haber cuevas similares en los tropicos.´ La literatura existente sugiere que estos ecosistemas poco conocidos, con su combinacion´ unica´ de microclima generado por la geomorfolog´ıa y los murci´elagos, son particularmente sensibles a la perturbacion´ y enfrentan multiples´ amenazas por la urbanizacion,´ el desarrollo agr´ıcola, la miner´ıa y el turismo. Palabras Clave: Artropodos,´ Brasil, descubrimiento de especies, murcielagos´ Attributes of Hot Caves phenomenon, Dalquest and Hall (1949) describe a visit to a cave in the Tuxtla Mountains, Veracruz, Mexico, inhab- It has long been known that some chambers within ited by thousands of Wagner’s mustached bat (Pterono- caves in the Neotropics can reach very high temper- tus personatus) and Davy’s naked-backed bat (Pterono- atures (approximately 40 ◦C) due to the body heat tus davyi) (both Mormoopidae). They recount that “it emanating from high densities of certain bat species was impossible to remain long in the upper rooms be- (Juberthie 2000). In one of the first descriptions of this cause the temperature was high, probably more than §Address correspondence to Ana C. M. Malhado, email [email protected] Paper submitted September 18, 2011; revised manuscript accepted May 30, 2012. 1 Conservation Biology,Volume**,No.*,1–5 C 2012 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2012.01936.x 2 ConservationinHotCaves 95 ◦F[35◦ C], and the stench was almost unbearable” once existed as far south as the Brazilian state of Bahia (p. 426). (Czaplewski & Cartelle 1998) and as far north as Florida in Hot caves have distinct physical and biological char- the United States (Morgan 1987). However, the scattered acteristics. They usually have a single relatively small reports of hot caves in the scientific literature almost cer- entrance, low air circulation, a high (typically tens to tainly underestimate their frequency because, even when hundreds of thousands of individuals) density of bats, surveyed, they may not have been recognized, classified, constant year-round ambient temperatures of 28–40 ◦C, or labeled as such. and relative humidity >90% (Silva Taboada 1979; De La Although not referred to as hot caves, there is evi- Cruz 1992). There appears to be a lower size limit for dence that similar bat-generated microclimates may exist the formation of hot caves because the distinct microcli- in other parts of the tropics. Churchill (1991) describes mate depends on the maintenance of a sufficiently dense cave roosts of the orange horseshoe-bat (Rhinonycteris bat population (Rodr´ıguez-Dur´an 2009). More recently, aurantius) in tropical Australia of up to 25,000 individu- Rodr´ıguez-Dur´an (2009) categorized Caribbean hot caves als that maintain a constant cave temperature of 28–32 ◦C as “hot chamber foyers” (23–28 ◦C) or “hot main cham- and 85–100% relative humidity. However, it is not clear bers” (29–40 ◦C). This dichotomy is useful for classifica- to what extent, if any, this species contributes to the sta- tion, but is not absolute, and large cave systems may have bility of the microclimate, and the cave is occupied by chambers with a wide range of temperatures that create bats for only part of the year. Another likely location of opportunities for segregation of species on the basis of hot caves is the extensive karst landscapes of Southeast thermal associations (Rodr´ıguez-Dur´an & Soto-Centeno Asia, which occupy an area of approximately 400,000 2003; Rodr´ıguez-Dur´an 2009). km2 (Day & Urich 2000). A diverse and abundant bat Although caves are common geological features world- fauna inhabits these landscapes. Some cave systems in the wide, only a small proportion have the geomorphology Mulu karsts, Sarawak, contain more than a million individ- to become hot caves: medium to large fluviokarst caves, ual wrinkle-lipped bats (Chaerephon plicata) (Clements over 1 km in total length, a single small entrance, and et al. 2006). poorly ventilated chambers (Rodr´ıguez-Dur´an 2009). It has been estimated that as many as 8% (approximately 160) of caves in Puerto Rico could be classified as hot Fauna of Hot Caves caves and provide roosts for diverse bat communities (Rodr´ıguez-Dur´an 1998), although the proportion could The most prominent fauna of hot caves are the bat species be higher in other countries, where geomorphological that contribute to the characteristic microclimate. In the features facilitate the formation of caverns with poor air Neotropics, the family Mormoopidae is the main taxon as- flow (Mancina et al. 2007). sociated with hot caves, although they frequently share One of the key features of hot caves is that the high roosts with species in the families Phyllostomidae and temperatures are caused by heat radiating from the bod- Natalidae. All Antillean endemics in the family Mormoop- ies of the high densities of bats that occupy the chambers idae and most Natalidae are either restricted to hot caves and from decomposing guano (Peck et al. 1998). Thus, year round or during parturition. The same pattern exists they are qualitatively different from caves that are hotter for the range-restricted phylostomid genera Monophyl- than ambient due to the effects of geothermal heating lus, Erophylla,andPhyllonycteris (Silva Taboada 1979; (Bell et al. 1986) through the convection of hot air into Rodr´ıguez-Dur´an 1995; Gannon et al. 2005). Moreover, the cave (Rodr´ıguez-Dur´an 2009). Rather, hot caves rep- hot caves often have a limited number of characteristic resent a form of ecosystem engineering in which the ex- bat species assemblages (Rodr´ıguez-Dur´an 1998). ceedingly stable microclimate and the abundant guano One of the most notable differences between the bat strongly affect the space where other organisms (e.g., fauna of hot caves and other caves is in the density arthropods, gastropods, microbes) live (Hastings et al. of bats: the former are typically occupied by roosts of 2007). thousands or even hundreds of thousands of individu- Bat-engineered hot caves are best known from the als, whereas the latter typically have much lower abun- Caribbean, especially the islands of the Greater Antilles dances (Rodr´ıguez-Dur´an 2009). Rodriguez-Duran and (De La Cruz 1992). They have been most extensively stud- Lewis (1987) estimated that one cave in Puerto Rico con- ied in Cuba (Sampedro Marin et al. 1977; Tejedor et al. tained approximately 141,000 individuals of the sooty 2005; Mancina et al. 2007) and Puerto Rico (Rodr´ıguez- mustached bat (Pteronotus quadridens), a hot-cave Dur´an 1995, 1998; Rivera-Marchand & Rodr´ıguez-Dur´an specialist. 2001). Continental hot caves have been described in The stable microclimatic conditions and high humid- Mexico (Dalquest & Hall 1949), Venezuela (De La Cruz ity produced by the high density of bats also support 1992; Arends et al. 1995), and, most recently, northeast- a large number of other animals (Juberthie 2000), espe- ern Brazil (J.V.L.F., unpublished data). Fossil evidence cially arthropods that feed on the abundant bat guano from the Pleistocene suggests that hot caves may have and the decomposing remains of bats and other cave Conservation Biology Volume **, No. *, 2012 Ladle et al. 3 inhabitants (e.g., Vandel 1965; Barr 1968; Howarth 1983; thermoneutral temperature of bats on a daily basis in Trajano 2012). Most of these species are facultative cave- many locations (McNab 1969). These relatively low tem- inhabiting species as opposed to troglobites, which are peratures are not trivial for small bats, which respond generally found deeper in cave systems and are not typi- through behaviors such as clustering and roost modifi- cally associated with guano. In contrast to the relatively cation.

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