What constitutes the menu of Trachops cirrhosus ( Chiroptera ) ? A review of the species ’ diet

Few data are available on the predation of amphibians, reptiles, and mammals by the fringe-lipped bat Trachops cirrhosus (Chiroptera: Phyllostomidae: Phyllostominae), in particular in Brazil, where ecological studies of this species are still incipient. This study presents an overview of the data available in the literature on the composition of the diet of T. cirrhosus , including data from a semiarid region. The first records of the predation of the anurans Corythomanthis greeningi (Hylidae), Pleurodema diplolister (Leiuperidae), Proceratophrys cristiceps (Cycloramphidae), Dermatonotus muelleri (Microhylidae), Pipa carvalhoi (Pipidae), Leptodactylus sp. (Leptodactylidae), the lizards Vanzosaura rubricauda (Gymnophytalmidae), Hemidactylus mabouia (Gekknonidae), and a rodent of the family Cricetidae are reported. Insects (33%) constitute the principal component of the diet of T. cirrhosus , while anuran amphibians contributed 23% of the items recorded, followed by birds (14%), mammals (10%), lizards (8%), and invertebrates (8%). This diversity of prey is typical of a generalist predator, which is relatively unaffected by seasonal fluctuations in the availability of prey. This is especially important in the semi-arid Caatinga biome, which is subject to prolonged periods of drought that result in a shortage of feeding resources. Keywords: fringe-lipped bat, herpetofauna, prey-predator relationship, rodents, seasonally dry tropical forest.

Associated with environments in the vicinity of bodies of water, such as springs, streams, lakes, and reservoirs (Fleming et al., 1972), T. cirrhosus is often observed foraging near the ground (Kalko et al., 1999), and is commonly captured in the lower levels of mist nets.
The species is classified as "Least Concern" by the International Union for Conservation of Nature (IUCN) (Miller et al., 2015), and is not included in the Brazilian Red List of endangered fauna (Machado et al., 2008;IC-MBio, 2014).
Although the ability of this bat to prey on small amphibians in the wild is well documented, most of the data on the feeding behavior of the fringe-lipped bat are derived from the analysis of stomach contents or experimental provisioning with live prey in captivity, with few cases being observed directly in the field (Cramer et al., 2001).These bats are able to differentiate palatable species from toxic ones based on their vocalizations, as well as small-bodied individuals from those that are too large to be captured (Tuttle and Ryan, 1981).
Trachops cirrhosus ranges over relatively large areas (456 ha) and travels long distances (>1.5 km) between roosts and feeding areas (Bernard and Fenton, 2003), typically leaving the roost approximately 30 minutes after sunset (Kalko et al., 1999).As a predatory species, the fringe-lipped bat may require larger foraging areas than most other bats (Nogueira et al., 2007), which suggests that it may be a good indicator of habitat quality, due to the need for a healthy community of prey species to support a viable population.
The present study provides an overview of the composition of the diet of the genus Trachops, including new records on the predation of anuran, lacertilian, and rodent species in an area of the Brazilian Caatinga biome.
Fazenda Tamanduá is a private property located primarily in the municipality of Santa Terezinha, part of the Patos microregion, in the state of Paraíba,northeastern Brazil (7º01'31.23''S;37º23'31.04''W)(Lyra- Neves and Telino-Júnior, 2010;Passos Filho et al., 2015).This property covers a total area of 3073 hectares and includes the largest protected area (approximately 1000 ha) found in the Caatinga scrublands of the state of Paraíba, and one of the largest in northeastern Brazil.This area includes a legal reserve of 614 hectares and a Private Natural Heritage Reserve known as the RPPN Tamanduá (IBAMA-PB decree 110/98-N), with an area of 350 hectares.The site is located 18 km from the town of Patos (Neves et al., 1999;Lyra-Neves and Telino-Júnior, 2010;Passos Filho et al., 2015).
What constitutes the menu of Trachops cirrhosus (Chiroptera)?A review of the species' diet The local landscape is dominated by gallery forests and the presence of 18 natural ponds (Figure 1), five of which are permanent and 13 seasonal.These ponds provide feeding and breeding grounds for a unique faunal community (Lyra- Neves and Telino-Júnior, 2010;Passos Filho et al., 2015).
Mean annual rainfall, which has been recorded continuously by the local meteorological station since 1913, is 801.94 mm.This precipitation is concentrated within a relatively short rainy season, generally of two to four months' duration, which is followed by a prolonged dry season (Fazenda Tamanduá, 2011).
Regular field excursions were conducted to the Fazenda Tamanduá in 2011 and 2012, with two roosts being monitored, one within the area of the fazenda (roost A), and the other in an area outside the farm limits (roost B), in the municipality of Patos.Trachops cirrhosus was observed during these visits, and food debris was found regularly below the perches.A specimen of T. cirrhosus was captured at each site.One was captured at roost A with a hand net at 23h16 on March 15 th 2011 (Male; body   Neither specimen captured presented evidence of reproductive activity, and the epiphysis of the metacarpals and phalanges of the digits of the wings were ossified.No evidence of the presence of any other chiropterans was found at either roost, so it was assumed that all the debris found beneath the perches was derived from the foraging activities of T. cirrhosus.Guidelines for the handling of animals in research were followed as recommended by Sikes et al. (2011).
Records of prey items captured by T. cirrhosus were obtained from feeding perches at the two roosts during dry season (October-December).Roost A was located inside a toilet in a barn, denominated the Packing House (original name) here (7.017º S, 37.402º W, WGS 64, 287 m asl), near the VDB temporary pond.Roost B was approximately 13 km southeast of roost A (Figure 1), inside an abandoned house.This site is located in an area known as Cruz (7.096º S, 37.316º W, WGS 64, 254 m asl), an area of marshland, surrounded by grassland and shrubby scrub.The debris found beneath the feeding perches was collected for analysis in the laboratory, after first being processed in the field.Initial processing consisted of the identification and extraction of animal remains (carcasses and body parts) from the substrate.These remains were placed in labeled plastic bags for transportation to the Laboratory for Herpetological and Paleoherpetological Studies (LEHP) at the Federal Rural University of Pernambuco (UFRPE), in Recife.The identified specimens were deposited as vouchers in the Herpetological and Paleoherpetological Collection -CHP at UFRPE.
In order to update the list of prey items consumed by T. cirrhosus, an extensive literature search was conducted of the data available in published scientific papers and book chapters.The search was run in databases available online, including Scientific Electronic Library Online -SciELO (www.scielo.org/php/index.php),Web of Science -WoS (http://portal.isiknowledge.com), and Google Scholar (http://scholar.google.com.br).The search was based on different combination of the keywords "Chiroptera", "fringe-lipped bat", "Diet", "Trachops cirrhosus" and "Predation" (and their equivalents in Portuguese, where appropriate).
The published data on the composition of the diet of the Neotropical bat genus Trachops refer to the predation of 45 animal taxa (Table 1).The new items recorded in the present study bring this total to 54, which include six additional species of amphibians, two lizards, and one mammal (Table 2).Overall, the items consumed include arthropods (37%), amphibians (23%), mammals (16%), birds (14%), lizards (8%), and mollusks (2%) (Table 1).In Brazil, records are restricted to central Amazonia (northern Brazil), Pernambuco, in the northeast region of the country, and the state of Rio de Janeiro, in the southeast region.
In the Brazilian Caatinga, Silva (2007) obtained fecal samples from 19 specimens of T. cirrhosis captured over a one-year period, recording a relative frequency of 72.7% for insects, 50.0% for partially digested fruit pulp, and 9.1% each for fruit and small vertebrates (unidentified tissue and bone fragments).While Silva (2007) recorded 32 species of fruits during the rainy season, only one -Cecropia pachystachya Trec.(Cecropiaceae) -was exploited by T. cirrhosus.This indicates that this bat exploits the most available resource   opportunistically during periods of abundance, as observed in previous studies (Ruschi, 1953;Bonaccorso, 1979;Whitaker and Findley, 1980).
Overall, anuran amphibians, which have long been considered to be the principal prey of T. cirrhosus (Brosset, 1966;Wilson, 1973), contributed 24% of the items recorded in the present study (Figure 5), followed by mammals (17%), birds (13%), and lizards (7%).The most common item was insects, however, which contributed 32% of the samples, corroborating the findings of Silva (2007).We could conclude, then, that T. cirrhosus has a diet much more alike in comparison to other larger Phyllostominae than expected.
As T. cirrhosus is able to locate frogs through their vocalizations (Tuttle and Ryan, 1981), the consumption of amphibian prey might be expected to be restricted to the rainy season, when most species reproduce and their vocal activity peaks (Duellman and Trueb, 1994;Bernarde and Machado, 2000).The identification of three additional anuran species in the diet of T. cirrhosus, which were all recorded during the dry season, indicates that these bats may have located the anurans through alternative means, such as visual cues, as observed in previous studies (Peracchi et al., 1982).
The diversity of prey items recorded for T. cirrhosus, which include arboreal, terrestrial, and even aquatic animals, is typical of a generalist predator such as most of the larger Phyllostominae, which is relatively unaffected by seasonal fluctuations in the availability of prey (Mac-Arthur and Pianka, 1966).Fluctuations of this type are probably common in Caatinga habitats, where the prolonged dry season tends to result in a considerable reduction in the abundance of most anuran species (Navas et al., 2004).Data on the ecology and diet of T. cirrhosus in Brazil, in particular in the Caatinga scrublands, are still scarce, reinforcing the need for new records, such as those presented here.

Figure 2 .
Figure 2. The fringe-lipped bat, Trachops cirrhosus from two areas in Paraíba, northeastern Brazil, and its discarded prey items.A: an adult male T. cirrhosus, being handled at Fazenda Tamanduá, in Santa Terezinha; B: discarded prey items found under the feeding perch on the Fazenda Tamanduá; C: adult male T. cirrhosus from an area of marshland named Cruz, in Patos; D: discarded items under a feeding perch at Cruz.Photographs by Paulo B. Passos-Filho.

Figure 5 .
Figure 5. Relative contribution of different prey items to the diet of Trachops cirrhosus, based on published data and results of the present study.

Table 1 .
Vertebrate and invertebrate taxa known to be consumed by Trachops cirrhosus, including the records from the present study.In each case, the country or region in which the item was recorded is indicated.NI = not identified.What constitutes the menu of Trachops cirrhosus (Chiroptera)?A review of the species' diet