Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat


Predators are often confronted with a broad diversity of potential prey. They rely on cues associated with prey quality and palatability to optimize their hunting success and to avoid consuming toxic prey. Here, we investigate a predator’s ability to assess prey cues during capture, handling, and consumption when confronted with conflicting information about prey quality. We used advertisement calls of a preferred prey item (the túngara frog) to attract fringe-lipped bats, Trachops cirrhosus, then offered palatable, poisonous, and chemically manipulated anurans as prey. Advertisement calls elicited an attack response, but as bats approached, they used additional sensory cues in a sequential manner to update their information about prey size and palatability. While both palatable and poisonous small anurans were readily captured, large poisonous toads were approached but not contacted suggesting the use of echolocation for assessment of prey size at close range. Once prey was captured, bats used chemical cues to make final, post-capture decisions about whether to consume the prey. Bats dropped small, poisonous toads as well as palatable frogs coated in toad toxins either immediately or shortly after capture. Our study suggests that echolocation and chemical cues obtained at close range supplement information obtained from acoustic cues at long range. Updating information about prey quality minimizes the occurrence of costly errors and may be advantageous in tracking temporal and spatial fluctuations of prey and exploiting novel food sources. These findings emphasize the sequential, complex nature of prey assessment that may allow exploratory and flexible hunting behaviors.

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  1. Barber JR, Conner WE (2007) Acoustic mimicry in a predator–prey interaction. Proc Natl Acad Sci U S A 104:9331–9334

    PubMed  Article  CAS  Google Scholar 

  2. Barclay RMR, Fenton MB, Tuttle MD, Ryan MJ (1981) Echolocation calls produced by Trachops cirrhosus (Chiroptera: Phyllostomatidae) while hunting for frogs. Can J Zool 59:750–753

    Article  Google Scholar 

  3. Bates DL, Fenton MB (1990) Aposematism or startle? Predators learn their responses to the defenses of prey. Can J Zool 68:49–52

    Article  Google Scholar 

  4. Chen KK, Kovarikova A (1967) Pharmacology and toxicology of toad venom. J Pharm Sci 56:1535–1541

    PubMed  Article  CAS  Google Scholar 

  5. Clark VC, Rakotomalala V, Ramilijaona O, Abrell L, Fisher BL (2006) Individual variation in alkaloid content of poison frogs of Madagascar (Mantella; Mantellidae). J Chem Ecol 32:2219–2233

    PubMed  Article  CAS  Google Scholar 

  6. Hanifin CT, Yotsu-Yamashita M, Yasumoto T, Brodie ED III, Brodie ED Jr (1999) Toxicity of dangerous prey: variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. J Chem Ecol 25:343–356

    Article  Google Scholar 

  7. Hristov NI, Conner WE (2005) Sound strategy: acoustic aposematism in the bat-tiger moth arms race. Naturwissenschaften 92:164–169

    PubMed  Article  CAS  Google Scholar 

  8. Ibáñez R, Rand AS, Jaramillo C (1999) The amphibians of Barro Colorado Nature Monument, Soberania National Park and adjacent areas. Mizrachi & Pujol, Panama

    Google Scholar 

  9. Kardong KV, Kiene TL, Johnson EK (1997) Proximate factors affecting the predatory behavior of the red spitting cobra, Naja mossambica pallida. J Herpetol 31:66–71

    Article  Google Scholar 

  10. Krebs J (1973) Behavioral aspects of predation. In: Bateson P, Klopfer P (eds) Perspectives in ethology. Plenum, New York, pp 73–111

    Chapter  Google Scholar 

  11. Marimuthu G, Neuweiler G (1987) The use of acoustical cues for prey detection by the Indian false vampire bat, Megaderma lyra. J Comp Physiol A 160:509–516

    Article  Google Scholar 

  12. Miller GS Jr (1907) The families and genera of bats. Bull US Natl Mus 57:1–282

    Google Scholar 

  13. Page RA, Ryan MJ (2005) Flexibility in assessment of prey cues: frog-eating bats and frog calls. Proc Roy Soc B 272:841–847

    Article  Google Scholar 

  14. Page RA, Ryan MJ (2006) Social transmission of novel foraging behavior in bats: frog calls and their referents. Curr Biol 16:1201–1205

    PubMed  Article  CAS  Google Scholar 

  15. Ratcliffe JM, Fullard JH (2005) The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach. J Exp Biol 208:4689–4698

    PubMed  Article  Google Scholar 

  16. Roberts JA, Taylor PW, Uetz GW (2007) Consequences of complex signaling: predator detection of multimodal cues. Behav Ecol 18:236–240

    Article  Google Scholar 

  17. Ryan MJ (1983) Frequency modulated calls and species recognition in a Neotropical frog. J Comp Physiol 150:217–221

    Article  Google Scholar 

  18. Saporito RA, Donnelly MA, Jain P, Garraffo HM, Spande TF, Daly JW (2007) Spatial and temporal patterns of alkaloid variation in the poison frog Oophaga pumilio in Costa Rica and Panama over 30 years. Toxicon 50:757–778

    PubMed  Article  CAS  Google Scholar 

  19. Surlykke A, Miller LA (1985) The influence of arctiid moth clicks on bat echolocation; jamming or warning? J Comp Physiol A 156:831–843

    Article  Google Scholar 

  20. Tandler B, Phillips CJ, Nagato T (1996) Histological convergent evolution of the accessory submandibular glands in four species of frog-eating bats. Eur J Morphol 34:163–168

    PubMed  Article  CAS  Google Scholar 

  21. Tandler B, Nagato T, Phillips CJ (1997) Ultrastructure of the unusual accessory submandibular gland in the fringe-lipped bat, Trachops cirrhosus. Anat Rec 248:164–175

    PubMed  Article  CAS  Google Scholar 

  22. Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol A 111:1–29

    Article  Google Scholar 

  23. Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214:677–678

    PubMed  Article  CAS  Google Scholar 

  24. von der Emde G, Bleckmann H (1998) Finding food: senses involved in foraging for insect larvae in the electric fish Gnathonemus petersii. J Exp Biol 201:969–980

    PubMed  Google Scholar 

  25. Winter Y, López J, Ov H (2003) Ultraviolet vision in a bat. Nature 425:612–614

    PubMed  Article  CAS  Google Scholar 

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We thank the Smithsonian Tropical Research Institute, especially the staff on Barro Colorado Island, for logistical support. For fieldwork assistance, we are grateful to L. Albrecht, A. Shah, R. Hodgkison, and S. Ghanem. We thank M. Guerra for the bat photograph (Supplemental Fig. 1), the staff at the Institute of Experimental Ecology at the University of Ulm for technical support, and Patricia Jones and three anonymous reviewers for their thoughtful comments on the manuscript. We dedicate this publication to Elisabeth Kalko, our dear friend and colleague, who passed away in September 2011.

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Correspondence to Rachel A. Page.

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Communicated by: Sven Thatje

Electronic supplementary material

Below is the link to the electronic supplementary material.

High-speed video sequence of a bat approaching, assessing, and rejecting a túngara frog coated in toad toxins (AVI 934 kb)

Fig. 1

Tubercles on the chin and lips of T. cirrhosus (photo by Marcos Guerra) (DOCX 84 kb)

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Page, R.A., Schnelle, T., Kalko, E.K.V. et al. Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat. Naturwissenschaften 99, 505–509 (2012).

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  • Multimodal cues
  • Foraging strategies
  • Prey palatability
  • Prey size
  • Predator flexibility
  • Trachops cirrhosus