Sensory ecology of the frog-eating bat, Trachops cirrhosus, from DNA metabarcoding and behavior

Abstract

Metabarcoding of prey DNA from fecal samples can be used to design behavioral experiments to study the foraging behavior and sensory ecology of predators. The frog-eating bat, Trachops cirrhosus, eavesdrops on the mating calls of its anuran prey. We captured wild T. cirrhosus and identified prey remains in the bats’ fecal samples using DNA metabarcoding of two gene regions (CO1 and 16S). Bats were preying on frogs previously unknown in their diet, such as species in the genus Pristimantis, which occurred in 29% of T. cirrhosus samples. Twenty-three percent of samples also contained DNA of Anolis lizards. We additionally report apparently rare predation events on hummingbirds and heterospecific bats. We used results from metabarcoding to design acoustic and 3D model stimuli to present to bats in behavioral experiments. We show predatory responses by T. cirrhosus to the calls of the frog Pristimantis taeniatus and to the rustling sounds of anoles moving through leaf-litter, as well as attacks on a stuffed hummingbird and a plastic anole model. The combination of species-specific dietary information from metabarcoding analyses with behavioral responses to prey cues provides a unique window into the foraging ecology of predators that are difficult to observe in the wild.

We eat meat: a review of carnivory in bats

“…Douglas 1967, Vehrencamp et al 1977, Medellín 1988) are decades old and based on the identification of prey remains; there is a bias towards vertebrates, and arthropods are often reported only as orders. Recent studies using DNA barcoding (Ibáñez et al 2016, Arteaga Claramunt et al 2018, Jones et al 2020) have revealed new, taxonomically diverse prey with interesting ecological implications (Appendix ). While all the bat species have at least one account of predation of vertebrates, some species’ diets are much more reliant on them, so that vertebrates account for most taxa (Fig.…”

“…Not enough data were found to include Mimon crenulatum, Nyctalus aviator, and Tonatia saurophila . Averages obtained from data by Ross (1961), Fleming et al (1972), O’Shea and Vaughan (1977), Vehrencamp et al (1977), Fenton et al (1981), Bell (1982), Schulz (1986), dos Reis and Peracchi (1987), Medellín (1988), Aldridge et al (1990), Fenton et al (1992), Martuscelli (1995), Fenton et al (2001), Bonato et al (2004), Ramanujam and Verzhutskii (2004), Lenhart et al (2010), Witt and Fabián (2010), Felix et al (2013), Kaliraj (2014), Ibáñez et al (2016), Barbosa Leal et al (2018), Czaplewski et al (2018), Jones et al (2020) and Carvalho et al (2020). Largest prey from data by Ruschi (1953), Prakash (1959), Vaughan (1976), Schulz (1986), Medellín (1988), Fenton et al (1990, 1992), Martuscelli (1995), Kalko et al (1996), Arias et al (1999), Ramanujam and Verzhutskii (2004), Thabah et al (2007), Ibáñez et al (2016), Czaplewski et al (2018) and Molina‐Moreira and Alava (2019).…”

“…For example, Vampyrum spectrum , arguably the most carnivorous bat, has been seen eating mainly birds in Panama (Vehrencamp et al 1977), but bats, rodents, small amounts of insects, and fruit have been found in this species’ diet in Costa Rica, Brazil, and Mexico (Goodwin 1946, Howell & Burch 1973, Navarro 1979, Bonato et al 2004). Trachops cirrhosus , the frog‐eating bat, actually eats a substantial number of frogs in parts of Brazil, Panama, and Ecuador, but appears to rely heavily on lizards in Costa Rica and Panama (Whitaker & Findley 1980), on birds in north‐eastern Brazil (Rodrigues et al 2004), and even to be highly insectivorous in other parts of these countries (Fleming et al 1972, Bonaccorso 1975, Humphrey et al 1983, Kalko et al 1996, Bonato & Facure 2000); it also shows geographic variation in its response to frog acoustic cues (Jones et al 2014) and limited seasonal variation (Jones et al 2020). Vertebrates, especially birds, rodents and bats (Medellín 1988, Bonato et al 2004), constitute most of the diet of Chrotopterus auritus in Mexico and Brazil, but in Brazil reports of fruit consumption are somewhat frequent (Bonato et al 2004, Uieda et al 2007, Witt & Fabián 2010) and insect consumption increases during the rainy season (Bonato et al 2004).…”

“…, Witt & Fabián 2010, Vernier & Vedovato 2011, Fukui et al 2013, Jones et al 2013, Smirnov & Vekhnik 2013, Surlykke et al 2013, Halfwerk et al 2014, Kaliraj 2014, Smarsh & Smotherman 2015, Ibáñez et al 2016, Ripperger et al 2016, Jones et al 2017, Smarsh & Smotherman 2017, Brewton et al 2018, Czaplewski et al 2018, Vargas-Mena et al 2018, Vleut et al 2019, Carvalho et al 2020, Jones et al 2020, Page & Bernal 2020, Perrella et al 2020 …”

No need for artificial light: nocturnal activity by a diurnal reptile under lunar light

“…While nocturnal activity may facilitate diurnal predator avoidance, it may also expose anoles to novel nocturnal predators. This could partially explain high anole predation by owls on Dominica [21] as well as predation by bats, besides their apparent ability to locate sleeping anoles [22]. From an invasive perspective, we note that the artificial night-light niche is utilized by many anole species with invasive populations [6,23,24].…”