Animals often face opposing selection forces. To pass on their genes to the next generation, they must attract mates. But to survive, they must evade detection by eavesdropping predators. This classic conundrum, the tug between reproduction on the one hand and predation on the other, shadows and shapes much of the animal world.
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Research Focus
In our lab, we investigate sensory and cognitive mechanisms underlying animal behavior. Animals use a wide array of cues and signals to glean information about their environment. An animal’s sensory and perceptual systems filter incoming stimuli and define an animal’s Umwelt, or the specific way it perceives the world. Bats are a highly diverse ecological group, and variation in their use of sensory modalities, foraging strategies, and social information makes them excellent candidates for in depth studies of sensory and cognitive ecology.
One of the great joys of being positioned in Panamá is having our field sites right outside our laboratory doors, allowing us the opportunity to dive deeply into natural history. By closely observing animals in nature, and then designing hypothesis-driven tests that we can conduct outdoor flight chambers, we shed light on the sensory and cognitive tools animals use to make sense of the world around them.
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Research Overview
How do predators shape their prey, and how, in turn, do prey shape their predators?
Focusing on Neotropical bats, katydids and frogs, we study the dynamics that shape predator-prey interactions. We investigate the mechanisms that enable predators to find their prey, and those that help their prey avoid them. Our investigations include eavesdropping, learning, memory, signal evolution, and the exploitation of multimodal communication courtship displays.
What are the costs and benefits of multimodal courtship display?
The male túngara frog competes for mates using multimodal advertisement signals. Males gather in shallow bodies of water in the forest at night, producing loud mating calls which increase in complexity when acoustically competing with other males. To produce their calls, males shuttle air back and forth across their vocal folds, between the body cavity and a large, visually conspicuous vocal sac. Both female frogs and eavesdropping bats attend to the sound of the mating call as well as to the movement of the dynamically inflating and deflating vocal sac, female frogs using vision, bats using echolocation. Vocal sac inflation, in turn, generates ripples on the water surface that influences calling in nearby males, and increases attractiveness to predatory bats. This trimodal communication system (acoustic, visual/echolocation, seismic), exploited by both intended and unintended receivers, provides fertile ground for experiments investigating the costs and benefits of multimodal courtship display.
How do learning and memory shape foraging success?
The acquisition, retention, and retrieval of information is critical to successful foraging. Through studies both in the lab and in the field, our group is investigating flexibility, learning, and memory in predator foraging behavior. Frog-eating bats use prey mating calls to detect, locate and assess their prey. Based on the frog mating call alone, bats can distinguish between palatable and poisonous prey. We have shown that bats can rapidly alter their prey-cue/prey-quality associations in response to variation in foraging success, and that forging information can be quickly spread from bat to bat via social learning. We are currently investigating the role of long-term memory in foraging success, and how social learning affects foraging dynamics in the wild.
How do animals process, represent and use multimodal sensory information in the natural world?
New technology is allowing us to address questions in ways that were not possible just a few years ago. We are attaching GPS loggers, proximity sensors, and miniature ultrasonic microphones on free-flying bats in nature. These technologies are allowing us an unprecedented view into predators’ sensory worlds.
Education
B.A., Columbia University, 1996.
Ph.D., University of Texas at Austin, 2008.
Selected Publications
Dixon MM, Jones PL, Ryan MJ, Carter GG, Page RA. 2022. Long-term memory in frog-eating bats. Current Biology. 32, R557-R558. doi: 10.1016/j.cub.2022.05.031.
Bernal XE, Page RA. 2022. Tactics of evasion: strategies used by signallers to deter eavesdropping enemies from exploiting communication systems. Biological Reviews. doi: 10.1111/brv.12904.
Page RA, ter Hofstede HM. 2021. Sensory and cognitive ecology of bats. Annual Review of Ecology, Evolution, and Systematics. 52: 541-562. doi: 10.1146/annurev-ecolsys-012921-052635.
Geipel I, Lattenkamp EZ, Dixon MM, Wiegrebe L, Page RA. 2021. Hearing sensitivity: an underlying mechanism for niche differentiation in gleaning bats. Proceedings of the National Academy of Sciences. 118: e2024943118.
Muñoz-Romo M, Page RA, Kunz TH. Redefining the study of sexual dimorphism in bats: following the odor trail. Mammal Review. doi: 10.1007/s00265-020-02914-0.
Page RA, Bernal XE. 2020. The challenge of detecting prey: Private and social information use in predatory bats. Functional Ecology. 34: 344-363. doi: 10.1111/1365-2435.13439.
Page, RA, Jones, PL. 2017. Overcoming sensory uncertainty: factors affecting foraging decisions in frog-eating bats. In: Perception and Cognition in Animal Communication (volume editors, MA Bee and CT Miller), in the book series Animal Signals and Communication (series editors: P.K. McGregor and V.M. Janik). Springer. pp 285-312.
Gomes, DGE, Page, RA, Geipel, I, Taylor, RC, Ryan, MJ, Halfwerk W. 2016. Bats perceptually weight prey cues across sensory systems when hunting in noise. Science. 353: 1277-1280. DOI 10.1126/science.aaf7934.
Jones, PL, Page, RA, Ratcliffe, JM. 2016. To scream or to listen? Prey detection and discrimination in animal-eating bats. In: Bat Bioacoustics (volume editors: B. Fenton and A. Grinnell; series editor: A. Popper). Springer. pp. 93-116.
Ramakers JJC, Dechmann DKN, Page RA, O’Mara MT. 2016. Frugivorous bats prefer information from novel social partners. Animal Behaviour. 116: 83-87.
Falk, JJ, ter Hofstede, HM, Jones, PL, Dixon, MM, Faure, PA, Kalko, EKV, Page, RA. 2015. Sensory-based niche partitioning in a multiple predator-multiple prey community. Proceedings of the Royal Society Series B. 282: 20150520. http://dx.doi.org/10.1098/rspb.2015.0520.
Fugère, V, O'Mara, MT, Page, RA. 2015. Perceptual bias does not explain preference for prey call adornment in the frog-eating bat. Behavioral Ecology and Sociobiology. DOI 10.1007/s00265-015-1949-2.
Rhebergen, F, Taylor, RC, Ryan, MJ, Page, RA, Halfwerk, W. 2015. Multimodal cues improve prey localisation under complex environmental conditions. Proceedings of the Royal Society Series B. 282: 20151403. http://dx.doi.org/10.1098/rspb.2015.1403.
Jones, PL, Ryan, MJ, Page, RA. 2014. Population and seasonal variation in response to prey calls by an eavesdropping bat. Behavioral Ecology and Sociobiology. DOI 10.1007/s00265-013-1675-6.
Clarin, TMA, Borissov, I, Page, RA, Ratcliffe, JM, Siemers, BM. 2014. Social learning within and across species: information transfer in mouse-eared bats. Canadian Journal of Zoology. 129-139. DOI 10.1139/cjz-2013-0211.
Halfwerk, W, Jones, PL, Taylor, RC, Ryan, MJ, Page, RA. 2014. Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display. Science. 342: 413-416, DOI 10.1126/science.1244812.
Page, RA, Ryan, MJ, Bernal, XE. 2014. Be loved, be prey, be eaten. In: Animal Behavior, vol 3. Case Studies: Integration and Application of Animal Behavior (ed., K. Yasukawa), New York: Praeger. pp. 123-154.
Jones, PL, Ryan, MJ, Page, RA. 2013. When to approach novel prey cues? Social learning strategies in frog-eating bats. Proceedings of the Royal Society Series B. 280.
Page, RA, Schnelle, T, Kalko, EKV, Bunge, T, Bernal, X.E. 2012. Reassessment of prey through sequential use of multiple sensory cues by an eavesdropping bat. Naturwissenschaften 99: 505-509.
Akre, KL, Farris, HE, Lea, AM, Page, RA, Ryan, MJ. 2011. Signal perception in frogs and bats and the evolution of mating signals. Science 333: 751-752.
Page, RA, Ryan, MJ. 2008. The effect of signal complexity on localization performance in bats that localize frog calls. Animal Behaviour 76: 761-769.
Page, RA, Ryan, MJ. 2006. Social transmission of novel foraging behavior in bats: frog calls and their referents. Current Biology 16: 1201-1205.