Tail vibration

Tail vibration is a common behavior in some snakes where the tail is vibrated rapidly as a defensive response to a potential predator. Tail vibration should not be confused with caudal luring, where the tail is twitched in order to attract prey. While rattlesnakes are perhaps the most famous group of snakes to exhibit tail vibration behavior, many other snake groups—particularly those in the Colubridae and Viperidae families—are known to vibrate their tails.

Description

Process

Tail vibration involves the rapid shaking of the tail in response to a predatory threat. The behavior is particularly widespread among New World species of Viperidae and Colubridae.[1][2] However, some Typhlopidae and Boidae species may also tail vibrate.[3][4] At least one species of lizard—Takydromus tachydromoides—has been shown to tail vibrate in response to a potential predator.[5]

Tail vibration behavior in rattlesnakes is somewhat different from tail vibration in other snakes because rattlesnakes hold their tails vertically when tail vibrating, whereas other snakes hold the tail horizontally. Presumably, this is because the rattlesnake rattle produces its own noise, which would be diminished by the exterior of the rattle contacting the ground, and, conversely, snakes without rattles must vibrate the tail against the ground or some other object in order to make noise.

Speed

The speed of tail vibration is directly correlated with temperature, at least for rattlesnakes. The warmer a rattlesnake, the faster it vibrates its tail.[6] Rattlesnakes tail-vibrate faster than other snakes, with some individuals nearing or exceeding 90 rattles per second.[7][8] This makes rattlesnake tail vibration one of the fastest sustained vertebrate movements—faster than the wingbeat of a hummingbird. The movement is possible thanks to specialized “shaker” muscles in the rattlesnake tail.

Snakes more closely related to rattlesnakes vibrate more quickly than do more distant rattlesnake relatives.[1] In one study that measured tail vibration in 155 snakes representing 56 species, vibratory speed ranged from 9 vibrations per second (Bothriopsis taeniata) to 91 rattles per second (Crotalus polystictus).[1] In the study, only two rattlesnakes (of 33 individuals filmed) had a maximum vibratory rate slower than the fastest non-rattlesnakes. The fastest non-rattlesnakes examined were species of Agkistrodon and New World Colubrids, both of which could sustain vibratory speeds up to about 50 rattles per second.

It is unknown what benefit a snake derives from such fast speeds of tail vibration. One study did find that ground squirrels, Spermophilus beecheyi, are able to ascertain the threat level posed by a rattlesnake based on its rattling speed.[9] Thus, it is possible that fast rattling speeds could be driven by predator-mediated selection, whereby snake predators avoid faster-vibrating individuals.

Function

It is also unknown what the specific function of tail vibration is. Many researchers[2][4][10] have posited that it is primarily an auditory aposematic warning signal— like the growling of a wolf or the sound associated with African whistling thorn acacia (Acacia drepanolobium).[11] Others have suggested it could serve as a distraction—particularly for nonvenomous species— meant to draw attention away from a snake’s head and towards its less vulnerable tail.[12]

It has also been suggested that tail-vibrating nonvenomous snakes sympatric with rattlesnakes may be Batesian mimics of rattlesnakes that gain protection from predators by mimicking the rattling sound produced by rattlesnakes (all of which are venomous). This hypothesis does not explain why Old World nonvenomous snakes also tail-vibrate, since rattlesnakes are solely a New World taxa.

Evolution

Tail vibration is widespread among Vipers and Colubrids, and the behavior may be deeply ancestral in both groups.

Tail vibration behavior in rattlesnakes may have evolved from tail vibration in rattle-less ancestors. In support of this hypothesis are studies that show the similarity in specialized tail morphology and rate and duration of tail vibration between rattlesnakes are their closest relatives.[1][13] The evolution of rattlesnake rattling from simple tail vibration behavior may, in fact, be an example of behavioral plasticity leading to the evolution of a novel phenotype.[1]

Other researchers have suggested that the rattle may have evolved originally to enhance caudal luring, and that caudal luring behavior therefore preceded defensive tail vibration in rattlesnakes.[14] In support of this hypothesis, researchers suggest that a “proto-rattle” would not have increased sound production since rattles require a certain threshold of complexity (at least two overlapping rings of keratin) in order to produce sound. Proponents of this hypothesis suggest that a proto-rattle may have enhanced caudal luring, a behavior common to rattlesnakes and their closest relatives,[1] because such a structure might have looked similar to an arthropod head.[14] Those in support of this hypothesis also point out that specialized keratinized structures have evolved in caudal luring species before, such as in the spider-tailed horned viper, Pseudocerastes urarachnoides.

Opponents of the "caudal luring hypothesis" point out the lack of parsimony in such a process, since it would require the behavior to evolve from an offensive to a defensive context (extant rattlesnakes only use the rattle in defensive contexts).[4][10][13] If rattlesnake rattling behavior evolved from tail vibration, it would require no such change in behavioral context. Additionally, some have suggested that a proto-rattle could have increased sound production if the modified tail tip increased noise production when vibrated against the substratum.[15]

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See also

References
  1. Allf, Bradley C., Paul AP Durst, and David W. Pfennig. "Behavioral Plasticity and the Origins of Novelty: The Evolution of the Rattlesnake Rattle." The American Naturalist 188.4 (2016): 475–483
  2. Young, Bruce A. "Snake bioacoustics: toward a richer understanding of the behavioral ecology of snakes." The Quarterly review of biology 78.3 (2003): 303–325
  3. Lazell, James D. “1988. “Typhlops braminus (Brahminy Blind Snake) rattling. Herpetological Review 19.4 (1988): 85
  4. Greene, Harry W. "Defensive tail display by snakes and amphisbaenians." Journal of Herpetology (1973): 143-161
  5. Mori, Akira. "Tail vibration of the Japanese grass lizard Takydromus tachydromoides as a tactic against a snake predator." Journal of Ethology 8.2 (1990): 81–88
  6. Martin, James H., and Roland M. Bagby. "Temperature-frequency relationship of the rattlesnake rattle." Copeia (1972): 482–485
  7. Allf BC, Durst PAP, Pfennig DW (2016) Data from: Behavioral plasticity and the origins of novelty: the evolution of the rattlesnake rattle. Dryad Digital Repository. https://dx.doi.org/10.5061/dryad.c36k6
  8. Schaeffer, P. J. K. E., K. Conley, and S. Lindstedt. "Structural correlates of speed and endurance in skeletal muscle: the rattlesnake tailshaker muscle." Journal of experimental Biology 199.2 (1996): 351–358
  9. Owings, Donald H., Matthew P. Rowe, and Aaron S. Rundus. "The rattling sound of rattlesnakes (Crotalus viridis) as a communicative resource for ground squirrels (Spermophilus beecheyi) and burrowing owls (Athene cunicularia)." Journal of Comparative Psychology 116.2 (2002): 197
  10. Klauber, Laurence M. Rattlesnakes. Vol. 1. Univ of California Press, 1956
  11. Lev-Yadun, Simcha. "Does the whistling thorn acacia (Acacia drepanolobium) use auditory aposematism to deter mammalian herbivores?." Plant Signaling & Behavior 11.8 (2016): e1207035
  12. Williams, George Christopher. Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, 2008
  13. Moon, Brad R. "Muscle Physiology and the Evolution of the Rattling System in Rattlesnakes." Journal of Herpetology (2001): 497–500. Web
  14. Schuett, Gordon W., David L. Clark, and Fred Kraus. "Feeding mimicry in the rattlesnake Sistrurus catenatus, with comments on the evolution of the rattle." Animal Behaviour 32.2 (1984): 625–626
  15. Tiebout, Harry M. "Caudal luring by a temperate colubrid snake, Elaphe obsoleta, and its implications for the evolution of the rattle among rattlesnakes." Journal of Herpetology 31.2 (1997): 290–292
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