Communication and Displays of Snakes

AMER. ZOOL.. 17:217-223(1977). Communication and Displays of Snakes CHARLES C. CARPENTER Department of Zoology, University of Oklahoma, Norman, Oklahoma 73069 SYNOPSIS With limitations imposed by the lack of appendages and elongate morphology, snakes exhibit a variety of unique ritualistic behaviors in the contexts of agonistic encounters and courtship and mating. During male combat rituals, actions involve high vertical display stances (crotaline) to horizontal stances (colubrid) with either male attempting to force the other's head down. Superior position appears to be important during these encounters. Dominant and subordinate actions and postures are recognized. Courting snakes exhibit a variety of positions and movements, performed primarily by the male, which appear to passify the female and induce her receptivity. Actions involved may be chin rubbing, body jerks or caudocephalic waves, cephalocaudal waves, tail searching, pushing, nudging, biting, and tail raising. Sequences and phases of the actions used vary with the species. Significant features of these behaviors are the different actions taking place separately or simultaneously along the elongate cylindrical snake. Visual, tactile, and olfactory communication each play a role. INTRODUCTION The prevailing theory on the origin of snakes from ancient fossorial forms closely related to the platynotid lizards is reviewed by Bellairs and Underwood (1951). Subsequent adaptive radiation has produced a wide variety of species with modifications for arboreal, scansorial, ground dwelling, fossorial, amphibious and aquatic modes of living. These modifications have been imposed upon a unique (except for some lizards) body form which is very elongate and tubular, has extreme reduction or loss of limbs, a spectacle scale over the eye (no eyelids), absence of a tympanic membrane and middle ear cavity, and a great development of the vomeronasal apparatus. These modifications limit the development of certain behaviors {i.e., lack of limbs) and at the same time prescribe unique behaviors evolved to use the structures at hand. Our present knowledge indicates that snakes lack overt group social structure manifested in some lizards, and in many birds and mammals. I shall examine this lack in its relationship to its dependence upon communication systems. Various types of aggregations are noted for snakes, i.e., hibernating dens (Aleksuik, 1975; Carpenter, 1953; Parker and Brown, 1973; Woodbury, 1951), cover aggregations (Dundee and Miller, 1968) breeding aggregations (Aleksuik, 1975; Kropach, 1971), but no organized social structure has been reported for these groupings. Aggressive behavior has been noted for pairs of snakes in nest areas (Smith, 1939) and an incident of territoriality has been suggested for Masticophis fiagellum (Kennedy, 1965) but this phenomenon is very poorly developed, or very poorly understood in snakes. DO SNAKES COMMUNICATE? Social behaviors in contexts not relating to groups or aggregations are known and can be separated as agonistic behaviors, courtship and mating behavior and behavior associated with parental care. It is here perhaps that one should look for the presence of communication systems in snakes. What constitutes communication in snakes? If we accept communication as the transfer of information from one individual to another, whether intraspecific or interspecific, we can then first list the potential channels used by snakes over which communication signals may travel. The apparent communication channels availa- 217

218 CHARLES C. CARPENTER ble to snakes include the visual, olfactory (vomeronasal), tactile and acoustical. There is little evidence to suggest that snakes use acoustical communication and the lack of tympanum and middle ear support this. The other channels however, do play a part in snake interactions and a variety of signals are apparent which, interpreted in the context of their presentation, presumably communicate information between individuals. Smith (1969) states: "Animals possess in their behavior repertoires acts that have become specialized in the course of evolution to convey information and are called 'displays'; these acts include postures, movements, vocalizations and other sounds, the release of volitile chemicals, and so on." When a snake produces a signal(s), which we suppose has the potential for transferring information to a conspecific (or heterospecific), does this signal constitute a display? With respect to visual and tactile signals my interpretation is yes, the snake is displaying. This is probably true also for chemical signals, but more difficult to determine. THE POTENTIAL OF SNAKE MORPHOLOGY In approaching an analysis of communication displays of snakes I have first considered the potential acts and act systems (Russel, et al., 1954) available to snakes with their particular morphology. In doing so I have divided the hypothetical snake into regions and examined the actions for each region: the head (with its moveable tongue, jaws and cranium); neck (a region difficult to delimit in a snake, referring to that area just behind the head and extending to meet the anterior trunk region); trunk (extending from the neck to the vent and generally considered as anterior and posterior trunk regions); cloacal region (circumscribing the vent); and tail. As I will demonstrate, each of these regions is capable of separate or independent postures and/or actions which may serve as a potential signaling device in a display, or may be involved in dependent postures or actions, that is, because of the action of one region, another region is also part of a signal (raising the neck and anterior trunk raises the head). Thus for each region, set of regions, or the entire snake, there may be potential postures, movements (visual), and contacts (tactile) which function as signals and these in turn can potentially be combined in synchrony and/or presented in a sequential manner (irregular or stereotyped) through time (temporal aspects). Each action or series of actions has imposed upon it the context in which it is presented (agonistic, courtship and mating, parental care). Agonistic contexts include aggression (threat, aposematic), combat rituals, dominance and submission, letisimulation and body bridging (defense) and luring. Courtship and mating contexts involve those behaviors facilitating the bringing together of male and female and leading to successful intromission and copulation. I will confine the remainder of my remarks to displays during combat rituals, courtship and mating, and examine examples I have studied in relationship to communication. According to my estimates from the published records and my own observations, combat ritualistic behavior has been noted for only 5.5% of the genera and just under 2% of the known species of snakes, and courtship and mating behavior for 8% and 3% respectively. RITUALIZED BEHAVIORS IN SNAKES Combat rituals A combat ritual involves interaction sequences between two male snakes which appear to be a contest for superiority or dominance. Behaviors fitting the context of combat rituals have been recorded for four groups of snakes: colubrids, elapids, viperines and crotalines. To the unfamiliar observer, such combats may not have the appearance or characteristics of ritualism. On close observation and analysis such interactions exhibit repeated actions which are generally similar for all species so far

COMMUNICATION AND DISPLAYS OF SNAKES 219 observed, but also demonstrate (and will do so more as additional studies are recorded) generic and species characteristics. The general characteristics of snake combat rituals include body contact, during some phase of the contest, with the opponents exerting pressures through pushing, flipping or entwining, which appear to be attempts to physically subdue one another. The general pattern for elapids (Demansia, Pseudechis (Fleay, 1951), Dendroaspis (Grant, 1956)) involves tight entwining and twisting of the mid to posterior trunk regions and tails, the anterior trunk, neck and head regions arising obliquely or vertically with swaying back and forth as each attempts to entwine anteriorly and force his opponent down. During these actions they may move forward, separate and repeat the above actions many times. Colubrids, during combat rituals, tend to assume horizontal alignment with the trunk and tail regions entwined or lying over one another, with some oblique or slight vertical raising of the head and neck regions. High vertical stance of the head, neck and anterior trunk has been described for certain Old World colubrids (Elaphe longissima and Ptyas mucosa (Shaw, 1951). These forms also maneuver to get their head and neck over the opponent (hovering) (Fig. 1) and attempt to force him down. High vertical stance of the head, neck and anterior trunk region during combat ritual is characteristic of the Viperidae, both viperine (Fig. 2) and crotaline (Fig. 3) forms, while the posterior trunk and tail regions are usually in contact with these regions lying over one another or partially entwined. The raised regions sway back FIG. 2. Typical posture during combat ritual between two male Vipera ammodytes. Note high oblique stance with entwining - both visual and tactile communication (Thomas, 1971). and forth (Fig. 4) with one male untimately looping about the vertical column of the other and quickly attempting to push him down (topping) (Figs. 5, 6). One viperine form (Bitis arietans) does not rise to a vertical stance but performs a dorsal crawl with hovering (Thomas, 1972) (Fig. 7). An attribute during the sequence of a combat ritual is a visual display by one or both parties. Such displaying is most apparent in those forms with a high raised vertical stance. The displayer appears to try to entice his opponent by holding his raised posture (Fig. 8) and swaying back and forth (Fig. 4). Such enticing appears to also stimulate the adversary to respond and reciprocate by rising to a similar stance (Fig. 3). While both are thus displaying FIG. 1. Hovering position of one male over another during combat ritual in Lampropeltis getulus holbrooki. Sketched from videotape. FIG. 3. Mutual display during combat ritual between two male Crotalns atrox. Note high vertical stance, neck flexion and posterior trunk contact both visual and tactile communication. From motion picture frame.

220 CHARLES C. CARPENTER FIG. 6. Topping attempt during combat ritual between two male Sistrurus milianus (S. m. barbouri FIG. 4. Swaying.during mutual display between superior, S. m. streckeri inferior). Topping attempt two male Crotalus lepidus klauberi, as visual communication. From motion picture frames. tion for dominance. From motion picture is from a high oblique display stance communica- frame. they eventually proceed to a topping attempt which ends with tumbling from their high stance, only to have one immediately rise again to display with the other following suit. The displayer, in his rasied stance, conveys his "readiness" to do combat with his opponent. The displayer may move away from his opponent but then comes back towards him indicating an attracting force to his opponent. The opponent, free to retreat or avoid combat, responds by staying with the displayer, orienting towards him (Figs. 8, 9) and responding with his display. Courtship and mating Courtship and mating in snakes involves those actions performed by the male and the female which bring them together in proper alignment and behavioral state to effect intromission and complete copulation. It is the male that performs most of the actions during courtship. He seeks out the female, attempts to passify her, while aligning his body to bring the cloacae into juxtaposition. Such actions often appear very erratic and disordered. Critical observation and analysis indicates their ritualistic nature and implicates the importance of tactile communication. Courtship and mating have been noted in five groups of snakes: boids, colubrids, elapids, viperines and crotalines. The characteristic actions of the courting male boid while lying over the female is the use of the spurs or hooks (vestigial hind appendages) to stroke, scratch, or vibrate against the female in her cloacal region to passify her and induce her to twist her cloaca lateral and gape it so the male can effect intromission. The colubrid courtship appears to be more complex, but this may reflect the greater amount of information available on these forms. Characteristics of courtship (primarily by the male) for colubrids FIG. 5. Topping behavior during combat ritual between two male Crotalus lepidus klauben. Note one male attempting to force his opponent down tactile communication for dominance. From motion picture frame. FIG. 7. Dorsal crawl during combat ritual between two male Bitis anetans in attempt to dominate by the superior male. Lower male will rise rapidly flipping the superior male off (Thomas, 1972). Tactile communication.

COMMUNICATION AND DISPLAYS OK SNAKES 221 FIG. 8. Combat ritual between two male Crotalus vindis. Note one male displaying, the other orienting (orientor) on the displayer. Note the high vertical stance (visual communication) of the displayer and the trunk contact (tactile communication). From motion picture frame. which appear to varying degrees in the species observed are: following or chasing, dorsal mount with parallel alignment (Fig. 10) (sometimes entwining), lateral trunk loops which move along dorsally over the female (cephalocaudal waves), movement of the adpressed chin (chin rubbing) (Figs. 10, 11) along the dorsum of the female, lateral or ventrolateral jerks or rippling movements of the trunk wall which generally move anterior (caudocephalic waves), tail looping (tail search) (Fig. 12) movements which move anterior, and biting (in some a bite hold). Certain similar actions (from scant literature) characterize elapid courtship: follow or chase, dorsal mount with alignment, moving lateral trunk loops, chin rubbing, caudocephalic waves and biting. The viperine male raises his anterior trunk when approaching or chasing the female, entwines with her and uses tail search movements. In the crotalines the dorsally mounted male performs jerking movements in the head and neck region, sometimes in the trunk region, and may prod the female with his snout. VISUAL AND TACTILE COMMUNICATION The actions of snakes during the combat ritual imply some visual communication by postural displaying, while during both combat ritual and courtship and mating, tactile communication must play a highly significant role. The chemical aspects (pheromones) of communication in snakes is undoubtedly also significant, especially in the initial species and sex recognition and is an area which needs to have much more exploration. The starting of a combat ritual, after species and sex recognition are made, appears to be visual, especially in crotaline and viperine forms, whence the rising anterior column of the displayer entices similar actions by the other male (Figs. 3, 8). I have observed this response intergenerically between crotalines (Fig. 9). When contact is lost, they visually respond to one another by coming back together to continue the ritual. During the ritual in crotalines the two males, their vertical stances swaying back and forth (Fig. 4) visually communicate each other's presence and the context of combat readiness allowing orientation so one or both can approach for the topping bout (Fig. 5). The displayer appears to attempt to keep his head higher than that of his opponent, which may function as a challenge stimulus to his opponent. The hovering of combating colubrid males may be homologous to and serve as a display signal as does the FIG. 9. Intergeneric combat ritual interaction between a male Crotalus vindis (displayer in high vertical stance) enticing a male Agkistrodon piscworus to respond by also rising to display (visual communication). Note trunk contact (tactile communication). From motion picture frame.

222 CHARLES C. CARPENTER FIG. 10. Dorsal crawl with chin rubbing during courtship in Thamnophis metanogaster. Male is superior. Tactile communication with head (chin rub) and dorsal crawl as the male's trunk loops and chin move along the dorsum of the female. From motion picture frame. high vertical stance of the cortaline male. The contact established by crawling over, lying on or entwining may serve as tactile communication for maintaining alignment as well as a dominance signal when in a superior position. Communication during courtship in snakes appears to be primarily tactile, once species and sex identification have been made. Chin rubbing and dorsal crawling with cephalocaudal waves by the male help to acheive parallel alignment while at the same time supposedly serving to passify the female and maintain this alignment. The body jerks or rippling muscle actions in the form of caudocephalic waves by the male in contact with the female posteriorly may contribute to keeping the female quiet and also stimulate her to be receptive to the tail actions. The searching or pushing movements by the tail of the male, usually starting posterior and moving anteriorly in contact with the tail and cloacal region of the female appear to function to induce the female to raise her tail and gape her cloacal opening (Fig. 13), and at the same time bring the erect hemipenis into position for intromission. The synchronization of the cloacal gaping and intromission is paramount to successful coupling and thus must depend upon precisely timed tactile communication signals. Once intromission is effected, the engorged hemipenis probably serves to "lock" the two snakes together during copulation. As copulation proceeds the male usually maintains his position lying on top of the female with little additional action except for intermittant slow tail movements or caudocephalic waves just anterior to his cloacal region. All of the above actions appear to be tactile, i.e., tactile communication, taking place in the different regions along the length of the male snake. In analyzing the sequences of actions during courtship and copulation three phases emerge (Gillingham, et ah, 1977) tactile-chase, tactile-alignment and intromission and coitus. Each of these phases involves tactile signals as mentioned above. The species characteristics or species-specific nature of these phases and the signals involved are not yet fully determined or understood. It is known that certain species have long courtship times (Thamnophis), others short (Elaphe) (Gillingham, 1976). There may be significant differences in the temporal aspects of chin rubbing with dorsal crawling, cephalocaudal waves, caudocephalic waves and tail searching between species where the sequencing of, and synchronization of the actions may produce the proper species-specific signals (code) and message FIG. 11. Chin rubbing posture by male Helerodon platyrhtnos as he moves both anterior and posterior along the dorsum of the female tactile communication. From motion picture frame. FIG. 12. Tail searching behavior by a male Thamnophis melanogaster courting a female. Note his tail looped both under and over the female's tail which he forms posterior and slides anterior. Note he also lies dorsal to the female as he adpresses his chin to the female dorsum. Tactile communication by the head, trunk, and tail simultaneously. From motion picture frame.

COMMUNICATION AND DISPLAYS OF SNAKES 223 FIG. 13. Cloacal gaping by a female Thamnophis melanogaster in response to tail searching actions by a male during courtship a response to tactile communication signals. From motion picture frame. for inducing the proper responses by the female. The fascinating aspect of the communication between snakes, to me, lies in the unique behaviors evolved within the restricted morphological parameters of the elongate snake, with the different regions providing different acts and act systems which in sequence or in simultaneous synchrony adapt these animals to their own modes of operation. To answer the questions presented above. Yes snakes do display, visual displays and tactile displays which appear to be ritualized. Yes snakes do communicate using these display. Yes dominance is implicated as a function of the combat ritual, though territoriality in snakes needs to be more fully demonstrated, as does any type of significant group social organization for snakes. REFERENCES Aleksuik, M. 1975. Manitoba's fantastic snake pits. Nat. Geog. 14:714-723. Bellairs, A. d'a. and G. Underwood. 1951. The origin of snakes. Biol. Rev. 26:193-237. Carpenter, C. C. 1953. A study of hibernacula and hibernating associations of snakes and amphibians in Michigan. Ecology 34:74-80. Dundee, H. A. and M. C. Miller III. 1968. Aggregative behavior and habitat conditioning by the prairie ringneck snake, Diadophis punctatus arnyi. Tulane Stud. Zool. Bot. 15:41-58. Fleay, D. 1951. Savage battles between snakes. Walkabout 17:10-13. Gillingham, J. C. 1976. Comparative reproductive behavior of the ratsnakes of Eastern North America, genus Elaphe. Ph.D. Diss., University of Oklahoma. Gillingham, J. C, C. C. Carpenter, B. J. Brecke, and J. B. Murphy. 1977. Courtship and copulatory behavior of the Mexican milk snake, Lampropeltis tnangulum sinaloae (Colubridae). Southwest Natur. (In Press) Grant, G. A. 1956. The mating of black mambas. Afr. Wildlife 10:111-113. Kennedy, J. P. 1965. Territorial behavior in the eastern coachwhip, Masticophisjtagellum. Anat. Rec. 151:499(abst) Kropach, C. 1971. Sea snake (Pelamis platurus) aggregations on slicks in Panama. Herpetologica 27:131-135. Parker, W. S. and W. S. Brown. 1973. Species composition and population changes in two complexes of snake hibernacula in Northern Utah. Herpetologica 29:319-326. Russell, W. A., A. P. Meade and J. S. Hayes. 1954. A basis for the quantitative study of the structure of behavior. Behaviour 6:153-205. Shaw, C. E. 1951. Male combat in American colubrid snakes with remarks on the combat in other colubrid and elapid snakes. Herpetologica 7:149-168. Smith, M. A. 1939. The fauna of British India, Ceylon and Burma. Reptiha and Amphibia. Vol. 3, Serpentes. Taylor and Francis, London. Smith, W. J. 1969. Messages of vertebrate communication. Science 165:145-150. Thomas, E. 1971. Vipera ammodyles monlandoni (Viperidae). Kommentkampf der Mannchen. Publ. Wiss. FilSekt. Biol. 4:178-188. Thomas, E. 1972. Bilk anetans (Viperidae). Kommentkampf der Mannchen. Publ. Wiss. Film Sekt. Biol. 5:291-299. Woodbury, A. M. 1951. A snake den in Tooele County, Utah. Herpetologica 7:1-14.