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


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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  1. Alexander GJ (2007) Thermal biology of the southern African python (Python natalensis): does temperature limit its distribution. In: Henderson RW, Powell R (eds) Biology of the boas and pythons. Eagle Mountain Publishing, Eagle Mountain, pp. 50–75

    Google Scholar 

  2. Andrade DV, Marques OAV, Gavira RSB, Barbo FE, Zacariotti RL, Sazima I (2010) Tail luring by the golden lancehead (Bothrops insularis), an island endemic snake from south-eastern Brazil. South Am J Herpetol 5:175–180

    Article  Google Scholar 

  3. Barlow A, Baker K, Hendry CR, Peppin L, Phelps T, Tolley KA, Wűster CE, Wűster W (2013) Phylogeography of the widespread African puff adder (Bitis arietans) reveals multiple Pleistocene refugia in southern Africa. Mol Ecol 22:1134–1157

    Article  PubMed  Google Scholar 

  4. Cheney KL, Cotê IM (2005) Frequency-dependent success of aggressive mimics in a cleaning symbiosis. Proc R Soc Lond B 272:2635–2639

    Article  Google Scholar 

  5. Chiszar DD, Boyer D, Lee R, Murphy JB, Radcliffe CW (1990) Caudal luring in the southern death adder, Acanthophis antarcticus. J Herpetol 24:253–260

    Article  Google Scholar 

  6. Christy JH, Rittschof D (2011) Deception in visual and chemical communication in crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer Science and Business Media, New York, pp. 313–333

    Google Scholar 

  7. Clark RW (2006) The use of fixed videography in studying the predation behavior of ambush foraging snakes. Copeia 2006:181–187

    Article  Google Scholar 

  8. Clark RW, Dorr SW, Whitford MD, Freymiller GA, Putman BJ (2016) Activity cycles and foraging behaviors of free-ranging sidewinder rattlesnakes (Crotalus cerastes): the ontogeny of hunting in a precocial vertebrate. Zoology 119:196–206

    Article  PubMed  Google Scholar 

  9. Czaplicki JA, Porter RH (1974) Visual cues mediating the selection of goldfish (Carassius auratus) by two species of Natrix. J Herpetol 8:129–134

    Article  Google Scholar 

  10. Dalziell AH, Welbergen JA (2016) Mimicry for all modalities. Ecol Lett 19:609–619

    Article  PubMed  Google Scholar 

  11. Davies NB, Kilner RM, Noble DG (1998) Nestling cuckoos, Cuculus canorus, exploit hosts with begging calls that mimic a brood. Proc R Soc Lond B 265:673–678

    Article  Google Scholar 

  12. Driver A, Maze K, Rouget M et al. (2005) National spatial biodiversity assessment 2004: priorities for biodiversity conservation in South Africa. Strelitzia 17, Pretoria

  13. Drummond H, Gordon ER (1979) Luring in the neonate alligator snapping turtle (Macroclemys temminckii): description and experimental analysis. Z Tierpsychol 50:136–152

    Article  Google Scholar 

  14. du Preez L, Carruthers V (2009) A complete guide to the frogs of Southern Africa. Struik Nature, Cape Town

    Google Scholar 

  15. Edgehouse M, Brown CP (2014) Predatory luring behavior of odonates. J Insect Sci 14:2014

    Article  Google Scholar 

  16. Ewert JP (1970) Neural mechanisms of prey catching and avoidance behavior in the toad (Bufo bufo). Brain Behav Evolut 3:36–56

    CAS  Article  Google Scholar 

  17. Fathinia B, Rastegar-Pouyani N, Rastegar-Pouyani E, Todehdehghan F, Amiri F (2015) Avian deception using an elaborate caudal lure in Pseudocerastes urarachnoides (Serpentes: Viperidae). Amphibia-Reptilia 36:223–231

    Article  Google Scholar 

  18. FitzSimons VFM (1962) Snakes of Southern Africa. Purnell and Sons, Cape Town

    Google Scholar 

  19. Flower T (2011) Fork-tailed drongos use deceptive mimicked alarm calls to steal food. Proc R Soc Lond B 278:1548–1555

    Article  Google Scholar 

  20. Foster CD, Martin P (2008) Caudal movements in western fence lizards (Sceloporus occidentalis) prior to attempted prey capture. West N Am Naturalist 68:257–259

    Article  Google Scholar 

  21. Glaudas X (2004) Do cottonmouths (Agkistrodon piscivorus) habituate to human confrontations? Southeast Nat 3:129–138

    Article  Google Scholar 

  22. Goodman JD, Goodman JM (1976) Possible mimetic behavior of the twig snake, Thelotornis kirtlandi kirtlandi (Hallowell). Herpetologica 32:148–150

    Google Scholar 

  23. Greene HW (1973) Defensive tail display by snakes and amphisbaenians. J Herpetol 7:143–161

    Article  Google Scholar 

  24. Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, Alan R, vol 16. Liss, New York, pp. 1–152

    Google Scholar 

  25. Hagman M, Phillips BL, Shine R (2008) Tails of enticement: caudal luring by an ambush foraging snake (Acanthophis praelongus, Elapidae). Funct Ecol 22:1134–1139

    Article  Google Scholar 

  26. Hagman M, Phillips BL, Shine R (2009) Fatal attraction: adaptations to prey on native frogs imperil snakes after invasion of toxic toads. Proc R Soc Lond B 276:2813–2818

    Article  Google Scholar 

  27. Hagman M, Shine R (2008) Deceptive digits: the functional significance of toe waving by cannibalistic cane toads, Chaunus marinus. Anim Behav 75:123–131

    Article  Google Scholar 

  28. Hansknecht KA (2008) Lingual luring by mangrove saltmarsh snakes (Nerodia clarkii compressicauda). J Herpetol 42:9–15

    Article  Google Scholar 

  29. IBM Corp (2015) IBM SPSS statistics for Windows, Version 23.0., https://www.ibm.com/analytics/us/en/technology/spss/

  30. Ingle D (1968) Visual releasers of prey-catching behavior in frogs and toads. Brain Behav Evolut 1:500–518

    Article  Google Scholar 

  31. Jackson JF, Martin DL (1980) Caudal luring in the dusky pygmy rattlesnake, Sistrurus miliarius barbouri. Copeia 1980:926–927

    Article  Google Scholar 

  32. Jackson RR (1992) Eight-legged tricksters. Bioscience 42:590–598

    Article  Google Scholar 

  33. Jackson RR, Cross FR (2013) A cognitive perspective on aggressive mimicry. J Zool 290:161–171

    Article  Google Scholar 

  34. Jackson RR, Wilcox RS (1993) Spider flexibly chooses aggressive mimicry signals for different prey by trial and error. Behaviour 127:31–36

    Article  Google Scholar 

  35. Langmore NE, Maurer G, Adcock GJ, Kilner RM (2008) Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62:1689–1699

    Article  PubMed  Google Scholar 

  36. Langmore NE, Stevens M, Maurer G, Heinsohn R, Hall ML, Peters A, Kilner RM (2011) Visual mimicry of host nestlings by cuckoos. Proc R Soc Lond B 278:2455–2463

    Article  Google Scholar 

  37. Lillywhite HB, Henderson RW (1993) Behavioral and functional ecology of arboreal snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behavior. McGraw-Hill, New York, pp. 1–48

    Google Scholar 

  38. Master TL (1991) Use of tongue-flicking behavior by the snowy egret. J Field Ornithol 62:399–402

    Google Scholar 

  39. Mullin SJ (1999) Caudal distraction by rat snakes (Colubridae, Elaphe): a novel behavior used when capturing mammalian prey. Great Basin Nat 59:361–367

    Google Scholar 

  40. Murray BA, Bradshaw SD, Edward DH (1991) Feeding behavior and the occurrence of caudal luring in Burton’s pygopodid Lialis burtonis (Sauria: Pygopodidae). Copeia 1991:509–516

    Article  Google Scholar 

  41. Nelson XJ, Garnett DT, Evans CS (2010) Receiver psychology and the design of the deceptive caudal luring signal of the death adder. Anim Behav 79:555–561

    Article  Google Scholar 

  42. Pasteur G (1982) A classificatory review of mimicry systems. Annu Rev Ecol Syst 13:169–199

    Article  Google Scholar 

  43. Pernetta AP, Ross TN, Jones CG (2005) Leiolopisma telfairii (Telfair’s Skink): caudal luring. Herpetol Rev 36:320–321

    Google Scholar 

  44. Pough FH (1988) Mimicry of vertebrates: are the rules different? Am Nat 131:S67–S102

    Article  Google Scholar 

  45. Putman BJ, Clark RW (2015a) Habitat manipulation in hunting rattlesnakes. Southwest Nat 60:374–377

    Article  Google Scholar 

  46. Putman BJ, Clark RW (2015b) Crotalus oreganus (northern pacific rattlesnake): non-rattling tail display. Herpetol Rev 46:269–270

    Google Scholar 

  47. Rabatsky AM (2008) Caudal luring as a precursor in the evolution of the rattle: a test using an ancestral rattlesnake, Sistrurus miliarius barbouri. In: Hayes WK, Beaman KR, Cardwell MD, Bush SP (eds) The biology of rattlesnakes. Loma Linda University Press, Loma Linda, pp. 143–154

    Google Scholar 

  48. Randall JE (2005) A review of mimicry in marine fishes. Zool Stud 44:299–328

    Google Scholar 

  49. Reinert HK (1992) Radiotelemetric field studies of pitvipers: data acquisition and analysis. In: Campbell JA, Brodie Jr ED (eds) Biology of the pitvipers. Selva Press, Tyler, pp. 185–198

    Google Scholar 

  50. Reinert HK, Cundall D (1982) An improved surgical implantation method for radio-tracking snakes. Copeia 1982:702–705

    Article  Google Scholar 

  51. Reiserer RS (2002) Stimulus control of caudal luring and other feeding responses: a program for research on visual perception in vipers. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Eagle Mountain, pp. 361–383

    Google Scholar 

  52. Reiserer RS, Schuett GW (2008) Aggressive mimicry in neonates of the sidewinder rattlesnake, Crotalus cerastes (Serpentes: Viperidae): stimulus control and visual perception of prey luring. Biol J Linn Soc 95:81–91

    Article  Google Scholar 

  53. Sazima I (2002) Juvenile snooks (Centropomidae) as mimics of mojarras (Gerreidae), with a review of aggressive mimicry in fishes. Environ Biol Fish 65:37–45

    Article  Google Scholar 

  54. Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Franke W (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438

    CAS  Article  PubMed  Google Scholar 

  55. Schuett GW, Clark DL, Kraus F (1984) Feeding mimicry in the rattlesnake Sistrurus catenatus, with comments on the evolution of the rattle. Anim Behav 32:625–626

    Article  Google Scholar 

  56. Shulze RE (1997) South African atlas of agrohydrology and climatology. Water Research Commission, Pretoria

    Google Scholar 

  57. StatSoft Inc. (2014) STATISTICA (data analysis software system), version 12, www.statsoft.com

  58. Stoddard MC, Stevens M (2010) Pattern mimicry of host eggs by the common cuckoo, as seen through a bird’s eye. Proc R Soc Lond B 277:1387–1393

    Article  Google Scholar 

  59. Welsh HH Jr, Lind AJ (2000) Evidence of lingual-luring by an aquatic snake. J Herpetol 34:67–74

    Article  Google Scholar 

  60. Wickler W (1966) Mimicry in tropical fishes. Philos T Roy Soc B 251:473

    Article  Google Scholar 

  61. Wickler W (1968) Mimicry in plants and animals. Weidenfeld & Nicolson, London

    Google Scholar 

  62. Wignall AE, Taylor PW (2011) Assassin bug uses aggressive mimicry to lure spider prey. Proc R Soc Lond B 278:1427–1433

    Article  Google Scholar 

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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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Corresponding author

Correspondence to X. Glaudas.

Ethics declarations


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.

Informed consent

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

Additional information

Communicated by T. Madsen

Electronic supplementary material


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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