Herpetology Notes, volume 9: 191-195 (2016) (published online on 05 September 2016) Foraging behavior with possible use of substrate-borne vibrational cues for prey localization in Atelopus laetissimus (Ruiz-Carranza, Ardila-Robayo and Hernández-Camacho, 1994) Luis Alberto Rueda Solano1,* and Karen M. Warkentin2,3 The use of substrate-borne vibrational cues during Atelopus laetissimus (Ruíz-Carranza et al., 1994) is an foraging is well documented in arthropods (Cocroft endemic harlequin frog from the wet montane forest of and Rodríguez, 2005; Hill, 2009; Cocroft et al., 2014), the Sierra Nevada de Santa Marta (SNSM), Colombia especially arachnids (Barth et al., 1988; Brownell and (Fig. 1). This species, like almost all harlequin frogs Farley, 1979; Hill, 2009). However, vibration-cued (Atelopus spp.), is threatened with extinction (La Marca foraging is insufficiently studied in terrestrial vertebrates et al., 2005; IUCN, 2015). Nonetheless, Atelopus (Hill, 2009). Herpetologically, it has only been tested in laetissimus, A. nahumae and A. carrikeri populations in snakes (Young and Morain, 2002; Shine et al., 2004) and wet mountain forests and paramos of the SNSM survive one lizard species (Hetherington, 1989). Amphibians are with good conservation status (Rueda-Solano et al., the terrestrial vertebrates most sensitive to vibrations 2016) (Fig. 1). Unlike most Atelopus, A. laetissimus is (Hill, 2008), but the use of substrate-borne vibrational highly nocturnal, and A. nahumae is also active at night cues as a source of information has been reported in only (Rueda-Solano et al., 2016). At night both species can be a few species in limited contexts (Narins, 1990; Lewis found perched on leaves along high-altitude mountain et al., 2001; Hill, 2009; 2008; Cocroft et al., 2014). streams (Granda-Rodríguez et al., 2008; LARS pers. In predator-prey interactions, the use of vibrational obs.), and both species use their nocturnal perch for cues is known from the escape-hatching behaviour of foraging (Rueda Solano et al., in prep.) (Fig. 2). During Agalychnis callidryas embryos. Vibrations produced the day, it is very rare to see Atelopus laetissimus, and during snake attacks on egg clutches induce embryo hatching (Warkentin, 2005). Toe twitching behaviour in frogs has been hypothesized to function in foraging by generating vibrations that elicit prey movement or by serving as a visual lure (Hagman and Shine, 2008; Sloggett and Zeilstra, 2008). Nevertheless, to our knowledge, there are no reports of the use of vibrational cues for prey detection or localization during foraging, in any amphibian species. 1 Facultad de Ciencias Básicas, Universidad del Magdalena, Carrera 32 No 22 - 08 C.P. No. 470004, Santa Marta D.T.C.H. - Colombia. 2 Department of Biology, Boston University, 5 Cummington Mall, Boston, MA, 02215, U.S.A. 3 Smithsonian Tropical Research Institute, Apartado Postal Figure 1. Sierra Nevada de Santa Marta, north of Colombia, 0843-03092, Panamá, República de Panamá. A. laetissimus locality (Δ); Atelopus nahumae locality (x); and * Corresponding author e-mail: [email protected] A. carrikeri locality (•). 192 Luis Alberto Rueda Solano & Karen M. Warkentin Figure 2. Individuals of Atelopus laetissimus (A. and B.) and Atelopus nahumae (C. and D.) perched on leaves in nocturnal foraging activity; Sierra Nevada de Santa Marta, Colombia. Photographs by Luis Alberto Rueda Solano. the few observations are all on terrestrial microhabitats LARS used a small twig to touch the edge of the leaf such as leaf litter or rocks along streams. Thus, it on which the frog was perched, moving it against the appears that they climb onto plants only at night (LARS leaf to generate a vibrational and visual stimulus (Fig. pers. obs.). 3B). There were no insects visible on the twig or on In early May 2009, during the dry to rainy season the plant (Fig. 3B). The twig-leaf contact elicited the transition at quebrada San Lorenzo (11° 06’ N 74° frog’s attention. It oriented towards the stimulus (Fig. 03’ W, 2100 m, San Lorenzo Serrania, upper basin of 3C) and, within a few seconds, struck with its tongue Gaira river drainage; Fig. 1), the first author (LARS) at the twig-leaf contact point (Fig. 3D). The frog then observed the typical nocturnal foraging behavior of resumed its alert position (Fig. 3E). LARS then repeated Atelopus laetissimus (Fig. 3A). Observations and video the stimulus on another leaf of the same plant, adjacent recordings were made using red light, at 20:00 h. The to the frog (Fig. 3F). Like the first time, this elicited first focal A. laetissimus (male, 4.5 g, 4 cm SVL) was orientation, movement towards the stimulus (Fig. found perched on a Melastomataceae leaf about 0.5 m 3G) and then an attack on the twig-leaf contact point above the ground, immediately next to the stream. He (Fig. 3H). Following both attacks, the frog resumed its had an active and alert body position with eyes open and alert position (Fig. 3I). This trial was made with two limbs moderately separated (Fig. 3A), and there were individuals more along 50 m of the San Lorenzo stream several other male individuals with similar behaviour with similar outcomes. nearby. In early May 2015, additional modified behavioural The initial focal individual was observed staying assays were performed with another, geographically immobile for almost ten minutes without disturbance. distinct, Atelopus laetissimus population, in the middle After that, a simple behavioural assay was performed: basin of the Ancho River at 900 m (SNSM), La Guajira Foraging behavior in Atelopus laetissimus 193 Figure 3. Video sequence showing possible use of vibrational cues for prey localization by foraging Atelopus laetissimus, San Lorenzo, Colombia. (A) Male Atelopus laetissimus on a leaf in nocturnal foraging position; (B, F) generating vibrational and visual stimulus by touching leaf with twig, white arrows indicates the twig-leaf contact point; (C, G) frog attention to stimulus (head orientation and movement toward it); (D, H) attacks on the exact position of the stimulus, yellow arrows indicate stimulus/ attack position; (E, I) active foraging posture following attacks. Still frames from video recorded by Luis Alberto Rueda Solano. Colombia. These observations were also made using red stimulus, moving slowly over the leaf to the twig-leaf light, at 20:00 h. Males in this population are smaller contact point. With the visual-only stimulus, the frogs (about 3 cm SVL) than the San Lorenzo population. showed no evident behavioural response; they just In addition, unlike the San Lorenzo frogs, which were stayed immobile on the leaf with their limbs stretched entirely immobile when unstimulated, the La Guajira and chin raised. With the vibration-only stimulus, the frogs moved repeatedly, assuming unusual body frogs showed head orientation towards the stimulus postures on the leaf during the initial observation periods and slowly moved towards the twig-leaf contact point. (Fig. 4A). They stretched their fore- and hindlimbs In addition, they displayed toe-twitching behaviour, while lifting up their chin (Fig. 4B). For the behavioural tapping on the leaf while the stimulus was presented assays, we tested two frogs and used three variations of and for a few seconds after it ended. The toe twitching the stimulus: visual + vibrational (touching the leaf edge was only displayed in response to the vibration-only with a twig), visual only (moving twig near leaf edge, stimulus, when the point of twig-leaf contact was without touching it), and vibrational only (touching under the leaf. We did not see this behaviour in other twig to the underside of the leaf, out of sight of the contexts. frog). We tested all stimuli systematically; first visual To date, Atelopus have only been reported to use + vibrational stimulus; second was visual only; and last nocturnal perches on vegetation for resting (Lindquist et one was vibrational only. Each stimulus was presented al., 2007). Our observations reveal that A. laetissimus and for five minutes per trial, with a three-minute wait A. nahume also use such perches for foraging. Moreover, between stimuli. With the vibrational + visual stimulus, our initial, simple behavioural assays of male Atelopus the frogs showed similar behavioural responses to the laetissimus suggest these frogs may use vibrational cues San Lorenzo population. They were attracted by the transmitted through plants for prey localization, as part 194 Luis Alberto Rueda Solano & Karen M. Warkentin Figure 4. Male Atelopus laetissimus in nocturnal foraging posture, La Guajira, Colombia. (A) Profile, showing raised chin and extended limbs. (B). Ventral view, showing lateral extension of forelimbs and raised chin. Still frames from video recorded by Luis Alberto Rueda Solano. of their nocturnal foraging behaviour. However, we do Literature Cited not reject that other visual and/or auditory cues may also Barth, F. G., Bleckmann, H., Bohnenberger, J., Seyfarth, E.A. be used. Thus, a rigorous experimental test of the roles (1988): Spiders of the genus Cupiennius Simon 1891 (Araneae, of vibration and other sensory modalities as foraging Ctenidae) - II. On the vibratory environment of a wandering cues would be worthwhile. Most Atelopus species are spider. Oecologia 77(2): 194-201. diurnally active (Lötters, 1996), suggesting that A. Brownell, P., Farley, R.D. (1979): Prey-localizing behaviour of the laetissimus probably has relatively poor night vision. nocturnal desert scorpion, Paruroctonus mesaensis: Orientation This could make the use of non-visual sensory modalities to substrate vibrations. Animal Behaviour 27: 185-193. Cocroft, R.B., Gogala, M., Hill, P.S.M., Wessel, A. (Eds.) (2014): for foraging at night more useful. Moreover, most Studying Vibrational Communication (Vol. 3). Heidelberg: Atelopus lack a tympanum and middle ear structures, Springer presumably reducing their sensitivity to airborne sound Cocroft, R.B., Rodríguez, R.L. (2005): The behavioral ecology of (Lindquist et al., 1998). It would be interesting to assess insect vibrational communication.