2001/09/01 by Brad R. Moon · 3 citations
Environmental Science · Agricultural and Biological Sciences · #Amphibian and Reptile Biology #Animal Behavior and Reproduction #Turtle Biology and Conservation #Biology #Zoology #Evolutionary biology #Anatomy
paper · doi:10.2307/1565969
openalex publication_date 2001/09/01 · openalex created_date 2025/10/10 · openalex updated_date 2026/03/13
The rattle appears to have a been a key innovation in the adaptive radiation of rattlesnakes (Greene, 1988, 1992). However, despite the importance of the rattle to the biology of rattlesnakes, the evolution of the rattle remains poorly known. The rattle is associated with a suite of anatomical, physiological, and behavioral specializations (e.g., Greene, 1992; Rome et al., 1996; Schaeffer et al., 1996) that together represent an integrated system. Several of these specializations appear to vary among pitvipers and, therefore, have great potential for helping to resolve the evolution of the rattling system. The physiological specializations associated with tail vibration and rattling can help distinguish among possible ancestral states in the evolution of the rattling system. Currently, only limited behavioral and morphological data are available for studying rattle evolution. Nevertheless, several recent morphological and behavioral studies, discussed below, have highlighted recent progress, as well as major gaps, in our knowledge of rattle evolution. Some of these gaps may be filled by combining physiological data with the morphological and behavioral results. Here I discuss the potential bearing of some morphological, physiological, and behavioral features on the evolution of the rattling system. Anatomy and Mechanics of the Rattle.-Although the structure of the rattle in its current state is well known (Zimmerman and Pope, 1948; Klauber, 1972), the form of the rattle early in its evolution remains unknown. The starting condition for the origin of the rattle may be reflected in the cornified tail tips of several extant species of pitvipers (Garman, 1888; Greene, 1992). However, the particular type of cornified tail tip that may have been ancestral to the rattle is unresolved because none of the cornified tail tips in extant pitvipers approaches the complexity of the rattle (Klauber, 1972; Greene, 1988) and because the relationships between rattlesnakes and other pitvipers remain unresolved. Slow vibrations of a two-lobed tail cap, similar to a rattle button, probably did not enhance sound production in early rattlesnakes (Sisk and Jackson, 1997). However, the louder sounds produced by faster rattling (Rowe and Owings, 1996) suggest that high frequencies of vibration were at least as important to sound production as the structure of the incipient rattle. This inference in turn suggests that early tail vibration behaviors involved high twitch frequencies. However, few studies have addressed the relationship between tail vibration behaviors and vibration frequencies. The Origin of Rattling Behavior.-Two behavioral contexts have been hypothesized for the origin of the rattling system. The traditional hypothesis for the origin of the rattle is that it evolved as a warning device against predators or other potentially dangerous animals, such as large grazing mammals that could trample the snakes (Hay, 1887; Barbour, 1922, 1926). Use of the rattle only as a warning device in all living rattlesnakes supports this hypothesis (Klauber, 1972; Greene, 1988). The quiet sounds of small rattles (e.g., Sistrurus species; Cook et al., 1994) provide evidence against the warning hypothesis for the origin of the rattle (Schuett et al., 1984). In early rattlesnakes, small or structurally simple rattles may have been completely inaudible to large predators or grazing mammals. Instead, Schuett et al. (1984) argued that the rattle may have evolved as a device to enhance the visual attractiveness of caudal luring, in which the tip of the tail is held off the ground and twitched slowly to attract prey. However, Tiebout (1997) noted that three lines of evidence refute the caudal luring hypothesis for origin of the rattle. First, no incipient rattle-like structures are known in other snakes, including nonrattlesnake pitvipers and other snakes that use caudal luring to attract prey. Second, rattles larger than the (silent) button appear not to be used in caudal luring. Third, sound production by a small or simple rattle may have been enhanced by tail vibration against the substratum rather than in a tail held off the ground. Fast, audible tail vibration against the ground is used as a defensive behavior in many snakes, including nonrattlesnake pitvipers, diverse colubrids, and some basal snakes (Greene, 1988, 1992). In terms of character state changes, the origin of the rattle as a caudal luring device and its subsequent shift to a warning device would require at least two evolutionary steps in the use of the rattle. In contrast, inferring that the rattle originated as a warning device would require only one evolutionary step, which better fits the available data on rattle use only as a warning device in extant rattlesnakes. The phylogenetic and behavioral evidence indicating that rattling evolved from defensive tail vibration would be strengthened by mechanistic evidence that links tail vibration, rather than caudal luring, to rattling. The Bearing of Muscle Physiology on Rattle Evolution.Both caudal luring and antipredator tail vibration occur in diverse snakes and appear to be ancestral features in rattlesnakes (Greene, 1988, 1992). Which of these behaviors was associated with the evolution of the rattling system? Physiological evidence can be used to distinguish between caudal luring versus defensive tail vibration as the ancestral behavior to rattling. Extant rattlesnakes have tailshaker muscles that are highly specialized for sustaining fast contractions of 20-95 Hz for minutes to hours (Conley and Lindstedt, 1996; Rome et al., 1996; Schaeffer et al., 1996). Hoyvever, typical reptilian muscle can sustain only slow movements and fatigues quickly during fast contractions (Bennett, 1978, 1982; Lillywhite, 1987). Caudal luring involves slow, intermittent twitches (Greene, 1988). Therefore, caudal luring should not require any physiological specializations of the tail musculature. In contrast, antipredator tail vibrations and rattling are fast and often sustained for long periods. Further497