Behaviors guided by tactile cues

Tactile cues are important contributors to social and reproductive behaviors. Although chemical cues usually guide males to females, once the individuals meet, tactile information comes into play. If several males are simultaneously attracted to the same female, male combat is likely in some species. The winner is the male that eventually mates with the female. In some species, many males are present simultaneously, all competing for one female. This process is called "scramble competition" rather than male combat and leads to formation of the famous mating balls, which can contain dozens or even hundreds of males. Garter snakes (T. sirtalis) in some parts of their range form such balls.

Less chaotic mating arrangements are more common, a few males courting one female. In this circumstance, ritualized combat is likely to occur, as in some rattlesnake species. Two males engage each other in a pushing contest involving the anterior parts of their bodies, which usually are raised off the ground, each male pressing against the other. The winner is able to press his opponent down to the ground and hold

Adder snake sidewinding in the Namib Desert. (Photo by David Hughes. Bruce Coleman, Inc. Reproduced by permission.)

him there for a few seconds or longer. Losers of such contests typically retreat and are sexually refractory for days afterward. Although the contest requires effort, it seems most unlikely that physical exhaustion can be the explanation for the loser's withdrawal and refractoriness. Instead, a neuroendocrine mechanism must exist by which losing suppresses subsequent aggressive and sexual activities, at least temporarily. This mechanism may benefit both winner and loser in that the winner mates with no further distraction and the loser manages to avoid serious damage. An interesting characteristic of male combat among vipers is that males usually do not bite each other during the ritualized wrestling activity. Because the snakes are not immune to their venom, the vipers could inflict serious damage through fang punctures and venom injection. By replacing such actions with ritualized wrestling, both males benefit. By withdrawing after defeat, the loser spares himself further domination as well as, perhaps, a biting attack by the winner.

Species in which male combat occurs typically exhibit sexual dimorphism in body size, males being larger than females. The idea is that combat creates a selective pressure favoring large males, because size correlates with winning versus losing. On the other hand, females should generally be selected for large body size because this factor determines clutch size. Within the limits of opposing selective pressures, females should generally be large. Males also are large, even larger than females, if male combat is important for mating success. If male combat does not occur in a species, males are smaller than females. These generalizations appear to hold over a broad range of species.

Sexual dimorphism in size is relatively common among reptiles, as is sexual dichromatism. In dichromatic species, males usually are more brightly colored than are females, a fact that correlates with the males' need to defend and advertise territories and to attract females. There are some spectacular cases among the spiny lizards (genus Sceloporus) in which both males and females have brilliant (but different) color patterns. These cases are not well understood, but they constitute an extreme form of dichromatism in which both sexes may be sacrificing crypsis to communicate sexual identity. It is possible, however, that future research will reveal that one or both of these patterns, although perceived as brilliant and conspicuous to human observers of preserved specimens, are nevertheless cryptic in the natural habitat.

Because male combat is a form of tactile stimulation, (1) delivery of this stimulation has become highly ritualized in some snakes and lizards, (2) the "meaning" of the stimulation appears to depend on differential neuroendocrine events in winners and losers, (3) delivery of the stimulation appears to inhibit tissue-damaging bites, at least for a while (it is possible that escalated aggression, including bites, could occur if the loser fails to retire), and (4) this form of tactile stimulation has created a selective pressure favoring large body size and increased ability to deliver the tactile information. Females benefit when they mate with males who have won combat encounters and are, by this measure, superior males. Sons of such males are presumed to inherit the size and strength of their fathers. Daughters also may benefit from genes fa-

Bearded dragon lizard (Pogona barbata) secures a grasshopper for a meal in Queensland, Australia. (Photo by Jen and Des Bartlett. Bruce Coleman, Inc. Reproduced by permission.)

voring large size. Although females can benefit by doing nothing, that is, by simply letting males fight and then mate with the winner, it has been reported that females sometimes add an element of their own. Females of several pitviper species raise their heads above the ground when a male approaches. This is the same behavior that combating males use at the start of their contests. The female may be making an aggressive gesture that has the effect of differentiating dominant and subordinate males. Males that have recently lost in combat are intimidated by this action on the part of a female, whereas males who have recently won in combat are not intimidated and proceed with courtship. Females can easily discriminate these two types of males on the basis of the males' behavior immediately after the female presents a combat intention display. This is the hypothesis currently held by a number of herpetologists who study the reproductive behavior of vipers.

Courtship and copulation in nonvenomous species have been studied in detail, and a useful terminology has been developed. Precourtship behaviors are those by which the potentially large distances between male and female are reduced. These behaviors usually involve the following of female pheromone trails by males. In some species, males may also use a head-raised posture to search for visual cues arising from females. An important role of visual cues has been established for ratsnakes (genus Elaphe) and is believed to exist in other genera as well. Males are attracted by the visual cues, and when the male is relatively near the female, chemical cues become readily available regarding the female's specific and sexual identity and her state of sexual readiness.

On making contact with a receptive conspecific female, the male initiates a series of behaviors typically grouped into three phases: tactile-chase, tactile-alignment, and intromission and coitus. At first the male exhibits a high rate of tongue flicking, during which he is apparently confirming the information he has previously obtained during the trail-following period. Direct contact with sexual pheromone along the female's dorsal surface likely intensifies the male's sexual motivation, leading him to rub his chin in a linear series of jerky movements along the female's back. A female might flee at this point, and the male usually follows, sometimes attempting to mount the female. This tactile-chase phase continues until the female remains stationary and allows the male to mount along part or all of her dorsum. The most conspicuous act usually is chin rubbing by the male along the female's back, advancing toward her anterior, moving posterior, and starting forward again. In the family Boidae, in which males have vestigial pelvic structures in the form of spurs, the tactile-chase phase of courtship entails spurring, which is rapid, oscillating movements of the spurs against the female's body. In some species of rattlesnakes, the male curls his tail around the base of the female's tail and gently massages her by moving his curl over the female's vent and down the length of her tail while repeatedly rubbing his chin along her dorsal, anterior surface. These behaviors may be analogous to the titillation movements by which male pond turtles stroke the heads and necks of their mates with long fore claws.

The tactile-alignment phase contains all of the foregoing behaviors and the juxtaposition of cloacal apertures, a posture that eventually allows copulation. The male and female achieve this important posture entirely with tactile sensation; there is no visual guidance. (Although there is ample evidence of integumentary tactile receptors in snakes and other reptiles, the term "hedonic receptors" is rare or absent in the herpetolog-ical literature. This term and various synonyms occur commonly in the mammalian literature, especially the literature on human sexuality, and we suspect it is applicable to the receptors mediating these cloacal alignments during sexual encounters between squamates.) On attaining juxtaposition of the cloacal apertures, the female may exhibit cloacal gaping, and the male may evert one of his hemipenes. At this point, tail-search copulatory attempts occur in which the tails of the partners are engaging each other but the animals' heads are not (i.e., the eyes and other anterior sense organs are not involved). Male garter snakes have been observed to rub their chins on one female while aligning with the cloaca of another female.

Coupling is the eventual outcome of tail-search copula-tory attempts. In some colubrid genera, such as Elaphe, Lam-propeltis, and Pituophis, it is common for a male to obtain a mouth grip on a female's neck just before penetration and to maintain this grip during coitus. This is a regular feature of mating among lizards (most of the terminology developed by snake researchers can be applied to lizards). One of the most interesting aspects of snake reproduction has to do with the duration of coitus, which ranges from a few minutes in many species to well over 20 hours in others (e.g., vipers and pitvipers). In garter snakes of several species (T. sirtalis, T. sauritus, T. butleri, and probably others), coitus is relatively brief, but a mucoprotein plug forms thereafter in the cloaca of the female that blocks penetration of the female by other males. In vipers and pitvipers, the tendency of the male to remain coupled for extended periods accomplishes the same result as the copulatory plug in garter snakes. On the other hand, the male garter snake is free within 15-30 minutes to seek additional copulation, whereas male vipers and pitvipers are unable to do so for 20-30 hours. Such variation may be associated with several ecological factors, such as the availability of sexually receptive females nearby. If availability is high, it makes sense to uncouple quickly and for the male to initiate courtship with new females. If, however, females are widely spaced and it is likely that several males will be simultaneously attracted to each receptive female, a successful male may benefit more by guarding the inseminated female than by leaving her while he goes on an uncertain hunt for a new female. The density of predators that might take advantage of snakes in copula is another ecological factor that could influence the duration of coitus. A high density of predators leads to selection for brief copulations. These ecological factors have not yet been studied systematically by herpetologists.

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