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 foraging is well documented in arthropods (Cocroft and Rodríguez, 2005; Hill, 2009; Cocroft et al., 2014), especially arachnids (Barth et al., 1988; Brownell and Farley, 1979; Hill, 2009). However, vibration-cued foraging is insufficiently studied in terrestrial vertebrates (Hill, 2009). Herpetologically, it has only been tested in snakes (Young and Morain, 2002; Shine et al., 2004) and one lizard species (Hetherington, 1989). Amphibians are the terrestrial vertebrates most sensitive to vibrations (Hill, 2008), but the use of substrate-borne vibrational cues as a source of information has been reported in only a few species in limited contexts (Narins, 1990; Lewis et al., 2001; Hill, 2009; 2008; Cocroft et al., 2014). In predator-prey interactions, the use of vibrational cues is known from the escape-hatching behaviour of Agalychnis callidryas embryos. Vibrations produced 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.
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 0843-03092, Panamá, República de Panamá. * Corresponding author e-mail:
[email protected]
Atelopus laetissimus (Ruíz-Carranza et al., 1994) is an endemic harlequin frog from the wet montane forest of the Sierra Nevada de Santa Marta (SNSM), Colombia (Fig. 1). This species, like almost all harlequin frogs (Atelopus spp.), is threatened with extinction (La Marca et al., 2005; IUCN, 2015). Nonetheless, Atelopus laetissimus, A. nahumae and A. carrikeri populations in wet mountain forests and paramos of the SNSM survive with good conservation status (Rueda-Solano et al., 2016) (Fig. 1). Unlike most Atelopus, A. laetissimus is highly nocturnal, and A. nahumae is also active at night (Rueda-Solano et al., 2016). At night both species can be found perched on leaves along high-altitude mountain streams (Granda-Rodríguez et al., 2008; LARS pers. obs.), and both species use their nocturnal perch for foraging (Rueda Solano et al., in prep.) (Fig. 2). During the day, it is very rare to see Atelopus laetissimus, and
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Figure 1. Sierra Nevada de Santa Marta, north of Colombia, A. laetissimus locality (Δ); Atelopus nahumae locality (x); and A. carrikeri locality (•).
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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 such as leaf litter or rocks along streams. Thus, it appears that they climb onto plants only at night (LARS pers. obs.). In early May 2009, during the dry to rainy season transition at quebrada San Lorenzo (11° 06’ N 74° 03’ W, 2100 m, San Lorenzo Serrania, upper basin of Gaira river drainage; Fig. 1), the first author (LARS) observed the typical nocturnal foraging behavior of Atelopus laetissimus (Fig. 3A). Observations and video recordings were made using red light, at 20:00 h. The first focal A. laetissimus (male, 4.5 g, 4 cm SVL) was found perched on a Melastomataceae leaf about 0.5 m above the ground, immediately next to the stream. He had an active and alert body position with eyes open and limbs moderately separated (Fig. 3A), and there were several other male individuals with similar behaviour nearby. The initial focal individual was observed staying immobile for almost ten minutes without disturbance. After that, a simple behavioural assay was performed:
LARS used a small twig to touch the edge of the leaf on which the frog was perched, moving it against the leaf to generate a vibrational and visual stimulus (Fig. 3B). There were no insects visible on the twig or on the plant (Fig. 3B). The twig-leaf contact elicited the frog’s attention. It oriented towards the stimulus (Fig. 3C) and, within a few seconds, struck with its tongue at the twig-leaf contact point (Fig. 3D). The frog then resumed its alert position (Fig. 3E). LARS then repeated the stimulus on another leaf of the same plant, adjacent to the frog (Fig. 3F). Like the first time, this elicited orientation, movement towards the stimulus (Fig. 3G) and then an attack on the twig-leaf contact point (Fig. 3H). Following both attacks, the frog resumed its alert position (Fig. 3I). This trial was made with two individuals more along 50 m of the San Lorenzo stream with similar outcomes. In early May 2015, additional modified behavioural assays were performed with another, geographically distinct, Atelopus laetissimus population, in the middle basin of the Ancho River at 900 m (SNSM), La Guajira
Foraging behavior in Atelopus laetissimus
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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 light, at 20:00 h. Males in this population are smaller (about 3 cm SVL) than the San Lorenzo population. In addition, unlike the San Lorenzo frogs, which were entirely immobile when unstimulated, the La Guajira frogs moved repeatedly, assuming unusual body postures on the leaf during the initial observation periods (Fig. 4A). They stretched their fore- and hindlimbs while lifting up their chin (Fig. 4B). For the behavioural assays, we tested two frogs and used three variations of the stimulus: visual + vibrational (touching the leaf edge with a twig), visual only (moving twig near leaf edge, without touching it), and vibrational only (touching twig to the underside of the leaf, out of sight of the frog). We tested all stimuli systematically; first visual + vibrational stimulus; second was visual only; and last one was vibrational only. Each stimulus was presented for five minutes per trial, with a three-minute wait between stimuli. With the vibrational + visual stimulus, the frogs showed similar behavioural responses to the San Lorenzo population. They were attracted by the
stimulus, moving slowly over the leaf to the twig-leaf contact point. With the visual-only stimulus, the frogs showed no evident behavioural response; they just stayed immobile on the leaf with their limbs stretched and chin raised. With the vibration-only stimulus, the frogs showed head orientation towards the stimulus and slowly moved towards the twig-leaf contact point. In addition, they displayed toe-twitching behaviour, tapping on the leaf while the stimulus was presented and for a few seconds after it ended. The toe twitching was only displayed in response to the vibration-only stimulus, when the point of twig-leaf contact was under the leaf. We did not see this behaviour in other contexts. To date, Atelopus have only been reported to use nocturnal perches on vegetation for resting (Lindquist et al., 2007). Our observations reveal that A. laetissimus and A. nahume also use such perches for foraging. Moreover, our initial, simple behavioural assays of male Atelopus laetissimus suggest these frogs may use vibrational cues transmitted through plants for prey localization, as part
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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 not reject that other visual and/or auditory cues may also be used. Thus, a rigorous experimental test of the roles of vibration and other sensory modalities as foraging cues would be worthwhile. Most Atelopus species are diurnally active (Lötters, 1996), suggesting that A. laetissimus probably has relatively poor night vision. This could make the use of non-visual sensory modalities for foraging at night more useful. Moreover, most Atelopus lack a tympanum and middle ear structures, presumably reducing their sensitivity to airborne sound (Lindquist et al., 1998). It would be interesting to assess the impact of this morphology on vibrational sensitivity, if vibrational cues are important for foraging. Acknowledgments. We are grateful to the Conservation Leadership Program for the financial support of the Atelopus Project Colombia (Project ID: 02177014), and to the administrators of Parques Nacionales Naturales of Colombia Territorial Caribe and indigenous communities for their logistic support of our field trips. Thanks to A. Rocha, L. Mejia, L. Jimenez, J. Perez, J. Eguis, T. Mejia, J. Rueda, J.S. Mendoza and F. Vargas-Salinas for their field-work support in Ancho River. Magdalena University supported LARS’ scientific visit to the Smithsonian Tropical Research Institute, Gamboa, Panamá, in 2015, to work with KMW. KMW was supported by Boston University, the Smithsonian Tropical Research Institute, and the National Science Foundation (IOS-1354072).
Literature Cited Barth, F. G., Bleckmann, H., Bohnenberger, J., Seyfarth, E.A. (1988): Spiders of the genus Cupiennius Simon 1891 (Araneae, Ctenidae) - II. On the vibratory environment of a wandering spider. Oecologia 77(2): 194-201. Brownell, P., Farley, R.D. (1979): Prey-localizing behaviour of the nocturnal desert scorpion, Paruroctonus mesaensis: Orientation to substrate vibrations. Animal Behaviour 27: 185-193. Cocroft, R.B., Gogala, M., Hill, P.S.M., Wessel, A. (Eds.) (2014): Studying Vibrational Communication (Vol. 3). Heidelberg: Springer Cocroft, R.B., Rodríguez, R.L. (2005): The behavioral ecology of insect vibrational communication. BioScience 55(4): 323-334. Granda-Rodríguez, H.D., del Portillo-Mozo, A., Renjifo, J.M. (2008): Uso de hábitat en Atelopus laetissimus (Anura: Bufonidae) en una localidad de la Sierra Nevada de Santa Marta, Colombia. Herpetotropicos 4(2): 87-93. Hagman, M., Shine, R. (2008): Deceptive digits: the functional significance of toe waving by cannibalistic cane toads, Chaunus marinus. Animal Behaviour 75(1): 123-131. Hetherington, T.E. (1989): Use of vibratory cues for detection of insect prey by the sandswimming lizard Scincus scincus. Animal Behaviour 37: 290-297. Hill, P.S.M. (2008): Vibrational Communication in Animals. Cambridge, Massachusetts, London, England: Harvard University Press. Hill, P.S.M. (2009): How do animals use substrate-borne vibrations as an information source? Naturwissenschaften 96(12): 13551371. IUCN. (2016): The IUCN Red List of Threatened Species. Version 2016-1. Available at: http://www.iucnredlist.org. Last accessed on 11 April 2016.
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Foraging behavior in Atelopus laetissimus La Marca, E., Lips K.R., Lötters, S., Puschendorf, R., Ibáñez, R., Rueda-Almonacid, J.V., Schulte, R., Marty, C., Castro, F., Manzanilla-Puppo, J., García-Pérez, J.E., Toral, E., Bolaños, F., Chaves, G., Pounds, J.A., Young, B.E. (2005): Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190-201. Lewis, E.R., Narins, P.M., Cortopassi, K.A., Yamada, W.M., Poinar, E.H., Moore, S.W., Yu, X. (2001): Do Male White-Lipped Frogs Use Seismic Signals for Intraspecific Communication?. American Zoologist 41(5): 1185-1199. Lindquist, E.D., Hetherington, T.E., Volman, S.F. (1998): Biomechanical and neurophysiological studies on audition in eared and earless harlequin frogs (Atelopus). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 183(2): 265-271. Lindquist, E.D., Sapoznick, S.A., Rodriguez, E.J.G., Johantgen, P.B., Criswell, J.M. (2007): Nocturnal position in the Panamanian Golden Frog, Atelopus zeteki (Anura, Bufonidae), with notes on fluorescent pigment tracking. Phyllomedusa 6(1): 37-44. Lötters, S. (1996): The Neotropical Toad Genus Atelopus: Checklist - Biology - Distribution. Zülpicher Str. 79 Köln Germany: M.Vences & F. Claw Verlags GbR. Narins, P.M. (1990): Seismic Communication in Anuran Amphibians. BioScience 40(4): 268-274. Rueda-Solano, L.A., Flechas, S.V., Galvis-Aparicio, M., RochaUsuga, A.A., Rincón-Barón, E.J., Cuadrado-Peña, B., FrankeAnte, R. (2016): Epidemiological surveillance and amphibian assemblage status at the Estación Experimental de San Lorenzo, Sierra Nevada de Santa Marta, Colombia. Amphibian & Reptile Conservation 10(1) [General Section]: 7–19 (e114).
Ruíz-Carranza, P.M., Ardila-Robayo, M.C., Hernández-Camacho, J.I. (1994): Tres nuevas especies de Atelopus A.M.C. Duméril & Bibron 1841 (Amphibia: Bufonidae) de la Sierra Nevada de Santa Marta, Colombia. Revista de La Academia Colombiana de Ciencias Exactas, Físicas Y Naturales 19(72): 153-163 Shine, R., Brown, G.P., Elphick, M.J. (2004): Field experiments on foraging in free-ranging water snakes Enhydris polylepis (Homalopsinae). Animal Behaviour 68: 1313-1324. Sloggett, J.J., Zeilstra, I. (2008): Waving or tapping? Vibrational stimuli and the general function of toe twitching in frogs and toads (Amphibia: Anura). Animal Behaviour 76(5): 1-4. Warkentin, K.M. (2005): How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Animal Behaviour 70(1): 59-71. Young, B.A., Morain, M. (2002): The use of ground-borne vibrations for prey localization in the Saharan sand vipers (Cerastes). The Journal of Experimental Biology 205: 661-665.
Accepted by Iris Starnberger
