A lure at both ends: aggressive visual mimicry signals and prey-specific luring behaviour in an ambush-foraging snake

Abstract

Aggressive mimic species use signals typically resembling an attractive or harmless model to deceive other organisms in order to increase foraging success. With the exception of a few brood parasitic birds that combine two signals, most known cases of aggressive mimicry involve only a single signal. Here, we used fixed videography, a technique which consisted in setting up continuously recording videocameras focused on ambushing animals, to describe—for the first time—the use of two clearly distinct aggressive visual mimicry signals in the same organism, the puff adder (Bitis arietans). Our observational data collected in South Africa revealed that puff adders extended their tongues (lingual luring) and waived their tails (caudal luring), presumably mimicking an invertebrate model, in order to lure prey within striking range. Lingual luring occurred only in the presence of amphibian prey, indicating discrimination between prey types. Our study reveals the diverse predatory strategies and complex decision-making process used by ‘sit-and-wait’ predators, such as ambush-foraging snakes, to catch prey, and indicates that snakes may have higher cognitive abilities than those usually afforded to them.

Significance statement

Predators exhibit various strategies to increase rates of prey capture. One strategy involves the use of luring behaviours, which are signals designed to attract prey within striking range. Using remote videocameras focused on ambush-hunting puff adders (Bitis arietans) in the field, we report—for the first time—the use of two clearly distinct luring behaviours in the same organism: puff adders extended their tongues and waived their tails, which presumably resemble invertebrate prey, to draw prey within striking range. Tongue-luring behaviour was solely used in the presence of amphibian prey, which indicates that puff adders distinguished between prey types. Our research underscores that the predatory decisions made by ambush-foraging snakes are diverse and context-dependent and further demonstrates that these predators possess higher cognitive abilities than first expected.

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Acknowledgments

We thank two anonymous reviewers for providing helpful comments on earlier drafts of this manuscript; K. Erlwanger, M.A. Costello and K. Thambu and the central animal service staff at the University of Witwatersrand for assisting with surgical procedures; G. Sauthier and H. Van Der Vyver for field assistance; and the landowners of the Dinokeng Game Reserve that granted us access to their properties to track snakes, specifically the Graf, Anderson, Engelbrecht, Keith, Leroux, Pretorius families, G. and T. Anderson and F. Erasmus. Last but not least, Gerd and Tienie Graf at iKhaya LamaDube Game Lodge greatly facilitated this study by providing free accommodation and good company for more than 3 years.

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Correspondence to X. Glaudas.

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Funding

This study was partly supported by a research grant from the Committee for Research and Exploration at the National Geographic Society (no. 9443-14) to XG and GJA and by postdoctoral fellowships from the Claude Leon Foundation and the University of the Witwatersrand’s research office to XG.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (University of the Witwatersrand, animal protocol no. 2012-42-04). Specimens were collected under scientific research permits CPF6-0167 and CPF6-0024, issued by the Gauteng Department of Agriculture and Rural Development.

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Informed consent was obtained from all individual participants included in the study.

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Communicated by T. Madsen

Electronic supplementary material

ESM A:

A male puff adder unsuccessfully lingual-luring at a red toad (Schismaderma carens). (MP4 12,128 kb)

ESM B:

A male puff adder unsuccessfully lingual-luring at a red toad (Schismaderma carens). (MP4 15,663 kb)

ESM C:

A female puff adder successfully lingual-luring a red toad (Schismaderma carens). (MP4 10,501 kb)

ESM D:

A male puff adder successfully lingual-luring an Amietophrynus toad. (MP4 68,585 kb)

ESM E:

A male puff adder successfully lingual-luring a red toad (Schismaderma carens). (MP4 24,365 kb)

ESM F:

A female puff adder unsuccessfully lingual-luring at a red toad (Schismaderma carens). (MP4 4522 kb)

ESM G:

A female puff adder unsuccessfully lingual-luring at an unknown prey. (MP4 13,421 kb)

ESM H:

A female puff adder successfully lingual-luring a bufonid toad. (MP4 24,935 kb)

ESM I:

A male puff adder unsuccessfully lingual-luring at an unknown prey. (MP4 5257 kb)

ESM J:

A male puff adder unsuccessfully lingual-luring at a bubbling kassina (Kassina senegalensis). (MP4 34,123 kb)

ESM K:

A male puff adder unsuccessfully lingual-luring at a red toad (Schismaderma carens). (MP4 9999 kb)

ESM L:

A female puff adder unsuccessfully caudal-luring at an unknown prey (video speed = ×16). (MP4 5987 kb)

ESM M:

A female puff adder unsuccessfully caudal-luring at an unknown prey (video speed = ×16). (MP4 5635 kb)

ESM N:

A male puff adder unsuccessfully caudal-luring at an unknown prey (video speed = ×16). (MP4 12,689 kb)

ESM O:

A male puff adder unsuccessfully caudal-luring at an unknown prey (video speed = ×16). (MP4 5329 kb)

ESM P:

A male puff adder unsuccessfully caudal-luring at an unknown prey (video speed = ×16). (MP4 27,146 kb)

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Glaudas, X., Alexander, G.J. A lure at both ends: aggressive visual mimicry signals and prey-specific luring behaviour in an ambush-foraging snake. Behav Ecol Sociobiol 71, 2 (2017). https://doi.org/10.1007/s00265-016-2244-6

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Keywords

  • Caudal luring
  • Coevolution
  • Lingual luring
  • Predator-prey relationship
  • Puff adder