Herpetological Review, 2002, 33(x), xxxx.

2002 by Society for the Study of Amphibians and Reptiles

Scavenging Behaviors of Cottonmouth Snakes at Island Bird Rookeries

HARVEY B. LILLYWHITE * COLEMAN M. SHEEHY III and MARSHALL D. MCCUE Seahorse Key Marine Laboratory, Department of Zoology The University of Florida, Gainesville, Florida 32611-8525, USA e-mail [HBL]: hbl@zoo.ufl.edu
*

To whom correspondence should be sent concerning this manuscript.

Cottonmouth snakes, Agkistrodon piscivorus, are well known as generalist and opportunistic feeders consuming fish, amphibians, rodents, birds, various reptiles including snakes and conspecifics, and carrion (Gloyd and Conant 1990; Savitzky 1992). The Florida cottonmouth, A. p. conanti, is an abundant snake throughout much of Florida, with well-established populations on some of the offshore islands. The success of this species in varied habitats is related, in part, to the wide range of prey items that provide a potential energy base for populations (see also Fritts 1988). Insular populations of cottonmouths inhabiting the Cedar Keys of Florida have been studied by Wharton (1966, 1969) who focused his investigations on an unusually dense population of snakes inhabiting Seahorse Key. This island is approximately 64 ha in size and was estimated to support 600 cottonmouths during the period when Wharton conducted his studies. The island has no permanent fresh water, and the cottonmouths inhabit a mixed hardwood forest where they are entirely terrestrial. These snakes subsist largely or entirely on fish that are dropped or regurgitated by colonial wading birds that nest on the island in large numbers from March through September or October. At present, the colonial nesting birds are largely represented by Brown Pelicans (Pelecanus occidentaliscarolinensis ), Double-crested Cormorants (Phalacrocorax auritus), White Ibis (Eudocimus albus), and several species of herons and egrets. One of us (HL) has confirmed and extended the observations of cottonmouth behaviors recorded by Wharton. At Seahorse Key these snakes characteristically forage at night on substrate directly beneath bird rookeries where avian excreta alter the vegetation and humus layers of soil. Foraging snakes methodically investigate these environments where numerous objects become splattered with fluids that are regurgitated or excreted by birds and presumably contain fish odors. The snakes largely consume fish, although occasional young birds fallen from nests might also be ingested. It is not clear, however, whether birds are eaten for their own sake or because they bear fish odors. Dead birds that are ignored by snakes are frequently found in or near the rookeries. Both their shape and size appear to render them too difficult to swallow. Foraging snakes are generally quite placid and can be approached and observed at close distances. They readily eat fish when these are presented to, or thrown near, a foraging snake. Snakes are also observed to investigate and grasp objects such as plant materials, bones, or bird feathers that have contacted avian excreta or fish fluids. These are usually released following contact with the internal tissues of the mouth.

Recently we observed some unusual scavenging behaviors in a foraging female cottonmouth estimated to be about 110 cm in total body length. The snake was first seen at 1810 h EDST and was observed for 20 min while it foraged in an open area beneath a Brown Pelican rookery at Seahorse Key, 2 June 2001. The substrate was comprised of sandy soil covered with many fallen twigs, dried leaves, and other scattered debris. Most of these objects were white or mottled due to urates that were excreted by the pelicans nesting overhead. The area was in full sun, and the ambient temperature and humidity at the time of observation were 31.4C and 61%, respectively. The snake appeared to be in good health and was somewhat distended posteriorad, suggesting possible pregnancy. The snake crawled very slowly and deliberately over the substrate while investigating various objects with frequent tongue flicks. We first observed the animal through binoculars from a distance of about 8 m. Eventually, we advanced closer to the snake, which continued to forage and eventually approached us within 0.5 m distance. Although the snake appeared to be aware of our presence at this point, it continued to forage as described. Soon after we first saw the snake, it investigated the ground intensely at one location and positioned its head nearly vertically with the mouth directed downward as it grasped a dark object. When the snake lifted its head, the grasped item was seen to be soil as half of it broke away from that being held in the mouth and fell to the ground. The snake then lifted its head upward at an angle of about 30 and swallowed the soil, which was seen to be damp and loosely held together with moisture. Later inspection of the ground on which the snake foraged revealed several locations where the soil was wetted, due either to excreta or regurgitated fluids from birds overhead. Following this act, the snake continued to investigate objects that were on the ground. Next it investigated the blunt end of a wooden branch about 1 cm in diameter and bearing several stains of bird excreta. The snake grasped this branch and attempted to advance the jaws over it, but the object was soon dropped and the effort abandoned. The snake continued to crawl slowly over the substrate using rectilinear locomotion while investigating objects with searching movements of the head and tongue. Finally, the snake stopped to investigate an object roughly 4 x 4 x 1.5 cm in overall size and comprised of a partial fish skull with other bones, debris and several dry leaves adhering to it. The snake grasped this object and advanced its jaws to hold the bulk of the item firmly within its mouth (Fig. 1). Then it elevated its head further off the ground, crawled forward about 3 m and stopped with the head elevated. We believe the item would have been swallowed, but we disturbed the snake while advancing to take photographs. The snake crawled forward and disappeared within the forest edge that bordered the rookery site. These and other observations of cottonmouth foraging behaviors at Seahorse Key suggest that numerous, diverse objects of appropriate size, shape, and odor might be ingested by foraging snakes. Thus, feces that are defecated by wild-caught snakes sometimes contain leaves that are ingested inadvertently as adhering parts of carrion. In general, Agkistrodon species appear to rely more on chemosensory information during foraging than do other crotalines (Chiszar et al. 1979; Cock Buning et al. 1981). It has been suggested that evolutionary reliance on an envenomation

Wikelski and Trillmich 1997).

Acknowledgments.We owe special thanks to Kenneth Litzenberger of the Lower Suwannee and Cedar Keys National Wildlife Refuge management office for a special use permit to study cottonmouth snakes at Seahorse Key. Logistical support was provided by the University of Florida Seahorse Key Marine Laboratory. LITERATURE CITED ADLER, G. H., AND R. LEVINS.1994. The island syndrome in rodent populations. Quart. Rev. Biol. 69:473487. CHISZAR, D., L. SIMONSEN, C. W. RADCLIFFE, AND H. M. SMITH.1979. Rate of tongue flicking by cottonmouths (Agkistrodon piscivorus) during prolonged exposure to various food odors, and strike-induced chemosensory searching by the cantil (Agkistrodon bilineatus). Trans. Kansas Acad. Sci. 82:4954. COCK BUNING, T. DE, R. C. GORIS, AND S. TERASHIMA.1981.The role of thermosensitivity in the feeding behavior of the pit vipers Agkistrodon blomhoffii brevicaudatus. Jap. J. Herpetol. 9:727. FRITTS, T. H. 1988. The brown tree snake, Boiga irregularis, a threat to Pacific islands. U.S. Fish Wildl. Serv., Biol. Rep. 88(31). 36 pp. GLOYD, H. K., AND R. CONANT. 1990. Snakes of the Agkistrodon complex. A Monographic Review. Society for the Study of Amphibians and Reptiles. MCNAB, B. K.1994. Resource use and the survival of land and freshwater vertebrates on oceanic islands. Amer. Nat. 144:643660. SAVITZKY, B. A. C. 1992. Laboratory studies on piscivory in an opportunistic pit viper, the cottonmouth, Agkistrodon piscivorus. In J. A. Campbell, and E.D. Brodie, Jr. (eds.), Biology of the Pitvipers, pp. 347368. Selva, Tyler, Texas. WHARTON, C. H. 1966. Reproduction and growth in the cottonmouth Agkistrodon piscivorus Lacpde, of Cedar Keys, Florida. Copeia 1966:149-161. ______. 1969. The cottonmouth moccasin on Sea Horse Key, Florida. Bull. Florida State Mus., Biol. Sci. 14:227272. WIKELSKI, M., AND F. TRILLMICH. 1997. Body size and sexual size dimorphism in marine iguanas fluctuate as a result of opposing natural and sexual selection: an island comparison. Evolution 51:922936.

FIG. 1. A female Florida cottonmouth, Agkistrodon piscivorus conanti, ingesting a dry mass of fish skull with adhering bones, dry leaves, sticks, and soil debris at a pelican rookery on Seahorse Key. Note the generally white appearance of the ground and numerous white spots on the leaves and other objects, including the snake. These are dried urates excreted by pelicans from the overhead tree canopy.

feeding system and use of a strongly proteolytic venom, coupled with predominance of chemosensory information during foraging, have likely conferred a predilection for carrion in the cottonmouth (Savitzky 1992). However, the significance of such behavior in energetic contexts has not previously been emphasized. At Seahorse Key, fish dropped by nesting birds can be a boom or bust situation. In the 1970s, as many as 200,000 colonial birds occupied the Cedar Keys, and 95% of all nesting occurred on Seahorse Key (U.S. Fish & Wildlife Service, unpublished records). Such numbers produce abundant and concentrated energy resources for cottonmouths, which literally gorge themselves during periods lasting from April/May to October/November (late fall nesting attributable to pelicans; HBL, unpublished observations). In recent years, however, drought has severely impacted wetlands on which many of the nesting birds depend for feeding their chicks. Consequently, the number of nesting birds has diminished greatly. Recent counts have been as low as 10,000 or fewer nesting birds. During the severe 2000 drought in Florida (especially at Seahorse Key), avian nesting was greatly curtailed at Seahorse Key, and the snake foraging period was shortened to JulyOctober. Moreover, cottonmouths do not forage during drought, even though dropped fish might be available at the rookeries (unpublished observations). Consequently, foraging success can vary greatly from year to year. It seems reasonable to infer that carrion degraded by age or adherence of indigestible materials might be significant resources when snakes employ foraging behaviors that maximize the intake of available energy. Snakes at Seahorse Key remain beneath or very near the rookeries, and they do not usually move extensive distances unless the locations of food resources change (Wharton 1969). Thus, the scavenging of diverse objects that yield potentially useful energy during foraging might have significant selective advantages in island environments where alternative prey items are scarce or limited. The intensive scavenging behaviors of cottonmouth snakes at Seahorse Key perhaps have become incorporated to be part of an island syndrome of behavioral and physiological modifications that have evolved in response to resource limitations on islands (Adler and Levins 1994; McNab 1994;