Gordon M. Burghardt

A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles.

In studies of squamate responses to prey chemicals presented on cotton-tipped applicators, investigators typically record several responses, each of which gives only part of the overall picture. The tongue-flick/attack score (TFAS) is a widely used composite measure of response strength that accounts for attack, its latency, and number of tongue-flicks. We present data and analyses on these variables and investigate the utility of several other possible response variables. It is concluded, for both practical and theoretical reasons, that TFAS and two modifications of it are the best measures of response strength. Uses and statistical analyses of TFAS and variables derived from it are discussed. It is recommended that information on tongue-flick rate, number of individuals attacking, and latency to attack be presented.

Comparative Prey-Attack Studies in Newborn Snakes of the Genus Thamnophis

Garter snakes (Thamnophis) from five species (including three subspecies of one form) were tested several days after birth with water extracts of at least 12 small animals (1.5 g animal to 10 ccm warm distilled water). The 12 prey animals included three species of earthworms and three of fish, a salamander and its larva, a frog, a leech, a slug and a baby mouse. A distilled water swab elicited tongue flicking only, while certain extract swabs resulted in actual prey-attack behavior after at least one tongue flick. A score was given to each extract test using a simple formula based upon tongue flick frequency and attack latency. Differences and similarities between the species were found and are discussed in relation to the actual feeding preferences in nature and captivity. For example, the aquatic Thamnophis elegans aquaticus attacked only the extracts made from the salamander larva, the frog, and the three fish; Thamnophis sirtalis also attacked the leech and the three earthworm extracts. It is suggested that the perceptual selectivity shown by naive snakes is an evolutionary response to present and past ecological conditions. The ability of newborn snakes to rapidly acquire a food avoidance response was also demonstrated.

Chemical-Cue Preferences of Inexperienced Snakes: Comparative Aspects

Different species of new-born, previously unfed snakes will respond with tongue flicking and prey-attack behavior to water extracts of the skin substances of various small animals. However, there are clear species differences in the type of extract responded to by previously unfed snakes, even within the same genus. These differences correspond to the normal feeding preferences shown by the various species.

Synthetic ethology and the evolution of cooperative communication

Synthetic ethology is proposed as a means of conducting controlled experiments investigating the mechanisms and evolution of communication. After a discussion of the goals and methods of synthetic ethology, two series of experiments are described based on at least 5000 breeding cycles. The first demonstrates the evolution of cooperative communication in a population of simple machines. The average fitness of the population and the organization of its use of signals are compared under three conditions: communication suppressed, communication permitted, and communication permitted in the presence of learning. Where communication is permitted, the fitness increases approximately 26 times faster than when communication is suppressed; with communication and learning, the rate of fitness increase is nearly 100-fold The second series of experiments illustrates the evolution of a syntactically simple language, in which a pair of signals is required for effective communication.

Food imprinting in the snapping turtle, Chelydra serpentina.

Three groups of hatchling snapping turtles, totaling 20, were fed either meat, fish, or worms. When they were tested for preference after 12 daily feedings, each preferred the diet to which it was accustomed. After 12 more days of eating a different food, each still preferred its original diet. A form of imprinting may be operative in the feeding behavior of this species.

CURRENT PERSPECTIVES ON THE BIOLOGICAL STUDY OF PLAY: SIGNS OF PROGRESS

There has been a recent resurgence of interest in the study of play behavior, marked by much empirical research and theoretical review. These efforts suggest that play may be of greater biological significance than most scientists realize. Here we present a brief synopsis of current play research covering issues of adaptive function, phylogeny, causal mechanisms, and development. Our goal is to selectively highlight contemporary areas of research in which the underlying processes and consequences of play should not be ignored. We elucidate some of the new and burgeoning areas of play research and interpret them from an integrative biological theoretical perspective that highlights areas in need of further experimental, comparative, and field research.

Behavioral and Stimulus Correlates of Vomeronasal Functioning in Reptiles: Feeding, Grouping, Sex, and Tongue Use

Whatever the reason for the general neglect, until recently, of the vomeronasal organ (VNO), its associated structures, and the behavioral significance of the system, we are now beginning to understand its widespread function in reptiles. Studies of the system are hindered, however, by a lack of anatomical, neurological, and neurophysiological information. But a start has been made and the primary purpose of this paper will be to review recent advances in our knowledge of the function of the reptilian vomeronasal system and to present some new data and speculation. Rather complete reviews are available (Burghardt, 1970a; Madison, 1977) that cover early experimental studies on the role of the chemical senses in reptile behavior.

Vomerolfaction and vomodor.

The major chemical senses of vertebrates are gustation, olfaction, and the sense supported by the vomeronasal system. The vomeronasal system is widespread in the tetrapods, being absent or vestigial only in crocodilians, some arboreal lizards, some aquatic turtles, birds, and adults of aquatic mammals and higher primates (Bertmar, 1981). Oddly, there is no term to denote chemical perception by the vomeronasal sense. At present, one must resort to vomeronasal sense, vomeronasal olfaction, or similar phrases. To distinguish it from the vomeronasal sense, olfaction is sometimes called nasal olfaction. Such terms do not pose a great problem for occasional use, but with the steadily increasing volume of papers on the structure, function, and behavioral roles of the vomeronasal system, especially in mammals and squamate reptiles (see Duvall et al., 1986), a term distinguishing the chemical sense supported by the vomeronasal system from that supported by the olfactory and gustatory systems is needed. Similarly, a term equivalent to odor for the stimuli sensed by the vomeronasal system would be useful. The vomeronasal sense is similar to olfaction, but its anatomical substrates and sensitivities are distinct (Parsons, 1970, Halpern, 1983). Briefly, the vomeronasal organ has a sensory epithelium that is histologically quite similar to the olfactory epithelium, although there are differences in numbers of bipolar cells, cellular structure (including lack of cilia in bipolar neurons of the vomeronasal epithelium), and binding of cells to monoclonal antibodies against lactoseries carbohydrates (Halpern, 1983; Wang and Halperu, 1980; Mori, 1987). The neural connections also differ. Whereas the olfactory nerves terminate in the primary olfactory bulbs, the vomeronasal nerves terminate in the accessory olfactory bulbs. A further distinction is that the vomeronasal and olfactory systems are most sensitive to substances having different molecular weights and appear to have different behavioral roles (e.g., Cowles and Phelan, 1958; Stoddart, 1980). At least in squamate reptiles, the vomeronasat system can detect volatile substances (Burghardt, 1980), but unlike the primary olfactory organ, it is quite sensitive to compounds of very high molecular weight (Stoddart, 1980, Burghardt et al., 1988). In squamate reptiles, the vomeronasal system detects molecules of high molecular weight, often sampled from substrates; the olfactory system detects mainly volatile airborne substances (Halpern, 1983).

Stimulus control of the prey attack response in naive garter snakes

Newborn garter snakes without prior feeding experience were found to selectively respond with attack behavior to water extracts of organisms normally eaten in captivity and not to respond to extracts of other organisms and controls. Differences were noted in the frequency and latency of responding to the effective stimuli. This response to chemical stimulation did not easily habituate. Visual stimuli may cause the S to orient toward and “explore” a potential food object, particularly if moving; but it is concluded that the basic somatic movements involved in the attack of prey are present at birth and that this behavior can only be elicited by certain chemical stimuli in naive Ss.

The comparative imperative: genetics and ontogeny of chemoreceptive prey responses in natricine snakes

Reptiles offer a rich diversity for the study of chemoreception, and snakes are a particularly appropriate group for comparative, evolutionary, genetic, developmental, and mechanistic studies. A long-term program of research is described that attempts to integrate these approaches, focusing on the widespread North American genus Thamnophis (Natricinae). Prior to their first meal, neonatal snakes respond to aqueous surface substances from species-typical prey with increased tongue-flicking and open-mouth attacks; these responses are mediated by the vomeronasal organ. Such responses predict what prey snakes will eat and can also predict relative prey preference. Species, population, litter, and individual differences exists and are important at different levels of analysis. Chemoreceptive responses are heritable, although they may show different developmental trends. Some species respond to prey types they do not eat in nature. In the earthworm specialist, T. butleri, response to fish chemicals can be interpreted as a chemoreceptive response inertially inherited from ancestral species, decoupled from prey capture techniques, and in the process of being lost. Ontogeny and experience can modify behavior of the neonate in various ways. Feeding experience can alter response to some prey more than others, and ambient prey odor may shift prey preference. Psychophysical studies show that prey preference and threshold sensitivity to prey chemicals can be independent and differ between closely related species, indicating that neural tissue is devoted to recognition of specific types of prey. In site choice tests, garter snakes can also discriminate between feces derived from conspecific snakes fed similar or different diets.(ABSTRACT TRUNCATED AT 250 WORDS)