Predator Deterrence in the Central Newt, Notophthalmus Viridescens Louisianensis (Wolterstorff) with Notes on Salamander Antipre

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1994 Predator Deterrence in the Central Newt, Notophthalmus viridescens louisianensis (Wolterstorff) with Notes on Salamander Antipredator Strategies Malcolm McCallum Eastern Illinois University This research is a product of the graduate program in Environmental Biology at Eastern Illinois University. Find out more about the program.

Recommended Citation McCallum, Malcolm, "Predator Deterrence in the Central Newt, Notophthalmus viridescens louisianensis (Wolterstorff) with Notes on Salamander Antipredator Strategies" (1994). Masters Theses. 2318. https://thekeep.eiu.edu/theses/2318

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Author Date Predator Deterrence in the central Newt, Noto~hthalmus viridescens louisianensis (Wolterstorff) with notes on salamander antipredator strategies.

BY Malcolm Mccallum

THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in Environmental Biology IN THE GRADUATE SCHOOL, EASTERN ILLINOIS UNIVERSITY CHARLESTON, ILLINOIS

I HEREBY RECOMMEND THIS THESIS BE ACCEPTED AS FULFILLING THIS PART OF THE GRADUATE DEGREE CITED ABOVE

9~/fftDATE

. ' . ' . 1

ABSTRACT

The effectiveness of the skin secretions of Notophthalmus viridescens as a predator deterrent has been well documented. Still, there have been documented cases of predation on this salamander. This study investigates the ability of a variety of herptiles to feed on N. viridescens louisianensis. In the first experiment, plethodonts and efts were fed on alternate weeks to snakes. Latency of response, anatomical location of predator attack, and behaviors displayed by predators and prey were recorded during each trial. In the second experiment, tongue flick frequency by I sirtalis to the essence of live N- viridescens louisianensis, Eurycea cirigerra, thawed larval Ambystoma tigrinum, and water was recorded. Tongue flicks to the four stimuli were compared at three satiation levels to determine if hunger might alter prey selection by snakes. Only Heterodon platyrhinos was found to accept efts as readily as controls. Chrysemys picta was found to accept efts and controls initially, but later refused all salamanders. I. sirtalis accepted efts and plethodonts with equal readiness. Plethodontidae displayed tail wrapping, thrashing, autotomy, and a new behavior called crawling. Efts displayed slow walking after an attack and unken reflex while in the grasp of a snake. Unken reflex was not observed predicating 2

an attack. Unken reflex, tail wrapping, and location of snake attack were found to increase swallowing times. As hunger increased, so did tongue flick rate. Stimulus type affected tongue flick rate. Satiation level did not significantly interact with prey preference. It appears that the skin secretions of N- viridescens louisianensis are a predation deterrent, but some predators can and will eat them. 3

ACDTOWLEDGMENTS

I would first like to sincerely thank my major professor, Dr. Michael A. Goodrich, for his patience in quiding me through this study and through my course work. I would also like to thank Dr. Edward o. Moll, Dr. Kipp c. Kruse and Dr. John Ebinger for their views and support. Special thanks are also given to Dr. R. A. Brandon at SIUC who took time out of his schedule to bring me to Mac Guires Orchard to collect newts. I would also like to thank him for his consultation on this project. Thanks also to Dr. Edmund D. Brodie, III at the University of Kentucky who discussed the importance of skin toxins with me. I would especially like to thank Tom Wilson and Doug Wood who spent four hours in a torrential downpour with me collecting plethodonts for this study. Many thanks to Dr. c. Costa for a "safe" place to store my animals and for his help relating to tetradotoxin resistance, to Dr. Bollinger, who took time out of his day to assist me with the Disc equation, and to Mr. L. Crofutt who helped with computer programs. I would like to thank the Illinois Department of conservation and the Indiana Department of Natural Resources for providing permits to collect specimens. 4

DEDICATION

This thesis is dedicated to my grandmother Catherine Zobel Mc Callum Danzero who died with Alzheimer's and Parkinson's diseases on September 15, 1993. May she rest in peace. 5

Table of Contents

Abstract ...... 1 Dedication ...... 2 Acknowledgment ...... 3 Introduction ...... 6 Materials and Methods ...... 14 Results ...... 20 Discussion ...... 27 Conclusions ...... 43 Literature Cited ...... 44 Tables ...... 50 Tab. 1 ...... 50 Tab. 2 ...... 51 Tab. 3 ...... 52 Tab. 4 ...... 53 Figures ...... 54 Fig. 1 ...... 54 Fig. 2 ...... 55 6

INTRODUCTION The central newt [Notophalmus viridescens louisianensis (Wolterstorff)] is a small salamander of the family Salamandridae. This animal has a distinctive life history. In the spring, females lay their eggs in thickets of submerged terrestrial or aquatic plants (Smith, 1978). Two to three months after hatching, the larvae emerge to feed on aquatic invertebrates (Brophy, 1980). In southern Illinois, larvae metamorphose into efts between July and October (Brandon, pers. comm.). After metamorphosing, efts spend between one and three years on land (Smith, 1978). After a heavy rain, efts crawl across the forest floor (Smith, 1961) where they are easily found. During drier conditions they are found under debris such as logs, rocks, boards, and sheet metal (Smith, 1961; Cochran, 1988) feeding on a variety of arthropods, worms, and other invertebrates (Burton, 1977). After as many as six years as an eft, newts return to the water where they permanently reside as adults (Hairston, 1987; Smith, 1961; Smith, 1978), feeding on a variety of aquatic invertebrates (Burton 1977). The adults undergo a complex mating ritual (Verrell, 1987) and the cycle is renewed. In some northern Illinois populations, adults become terrestrial during August and September and feed on snails (Cochran, 1988). There is also a southern Illinois population near Carbondale which displays neoteny (Brandon, Pers. Comm.). The dorsum of an adult central newt is peppered with black spots on an olive to yellowish-green background. A row 7 of up to nine red-orange spots may be present, extending from the cervical to the pelvic region, ventral to and on either side of the spinal column. The red spots may or may not be outlined with a black border. The venter is dark yellow and is sprinkled with black spots. Adults are 4-6 cm long and have a dorso-laterally compressed tail. The skin is smooth and vascularized to allow for aquatic respiration. During the breeding season, males develop greatly enlarged hind limbs with horny tubercles on the inner sides, the cloaca becomes enlarged, and a dorsal tail crest develops. Females have deep cornif ied ridges on the cloaca during the breeding season {Smith, 1961). Efts of the central newt are reddish-brown, unlike the eastern subspecies {H. viridescens viridescens Raf inesque) which are an aposomatic bright red-orange {Brown, Pers. Comm.; Goodrich, Pers. Comm.; Moll, Pers. Comm.). An eft's skin is thick and rough as in Taricha, to help prevent water loss {Brown, Pers. Comm.; Moll, Pers. Comm.). Newly emergent efts weigh between .3 and 1.0 grams. The sex of efts is difficult to determine {Smith, 1961). Larvae look like miniature adults with gills. They are smaller on average than emergent efts, but there is much variation in size at emergence. It is not uncommon to find larvae that are larger than average sized efts, or efts smaller than average sized larvae {Pers. Observ.). According to Smith {1961) the central newt was probably originally common throughout all but the western- 8 most portion of Illinois. Populations in central and eastern Illinois described by Hankinson (1917) and Garman (1892) appear now to be extinct. Today this species occurs only in the northern and the southern 1/4 of the state (Smith 1961). This range reduction may be caused by the draining of wetlands and deforestation for row-crop agriculture (Smith, 1961). Other causes may include increased use of pesticides and herbicides and the popularizing of this animal as an aquarium pet. Like many Amphibia, the central newt produces toxic skin secretions (Brodie, 1968; Brodie, Hensel, & Johnson, 1974; Hurlbert, 1970; Mosher & Fuhrman 1964) which may have medicinal uses (Pennisi, 1992). The evolutionary origin of these secretions as a defense against bacterial and fungal skin infections has been suggested by Habermehl (1981), because the skin of amphibians provides a perfect substrate for bacteria and fungi. Habermehl suggests that skin secretions of Amphibia may inhibit bacterial and fungal growth in concentrations as low as .001 moles/L to .00001 moles/L. He found that detoxified animals died of skin infections within a few days. Consequently, Habermehl believed that the primary purpose of skin toxins is not predator deterrence, but is antibiotic. Distasteful skin secretions in Amphibia have been described as an effective deterrence to many predators (Anderson, 1963; Barach, 1951; Brandon, Labanick, & Huheey, 1979a; 1979b; Brandon & Huheey, 1975; Brodie, 1968; Brodie & 9

Formanowicz, 1981; Brodie & Brodie, 1990; Dodd, Johnson, & Brodie, 1974; Cochran & Redmer, 1992; Estabrook & Dunham, 1976; Formanowicz & Brodie, 1982; Gawlik, 1980; Habermehl, 1981; Howard & Brodie, 1973; Huheey & Brandon, 1974; Hurlbert, 1970; Kruse & Francis, 1977; Kruse & Stone, 1984; Licht & Low, 1968; Orr, 1967; Pough, 1974; Tilley, Lundrigan & Brower, 1982; Webster, 1960). The bright colors of many Amphibia advertise this distastefulness. The central newt is one of these (Brandon & Huheey, 1975; Brandon, et al., 1979a; Brandon, et al., 1979b). The toxins produced by eastern newts (Notophthalmus viridescens viridescens) can kill a mouse injected with .01 cc of glandular extract in five minutes (Brodie, 1968). Consequently, many animals avoid newts because of their distastefulness (Brandon, et al., 1979a; Brandon, et al., 1979b; Brodie & Brodie, 1990; Brodie & Formanowicz, 1981; Howard & Brodie, 1973; Huheey & Brandon, 1974; Tilley, et al., 1982; Webster 1960). In fact the tetrodotoxin would be dangerous if ingested by humans (Brodie, 1982). Despite the apparent distastefulness and toxicity of eastern newts, Uhler, Cottam, & Clark (1936) recovered eastern newts from the stomach of a wild-caught eastern hognose snake (Heterodon platyrhinos). Wenzel (Pers. Comm.) fed adult newts to hognose snakes in captivity without any apparent problems. Brandon (Pers. Comm.) found central newts in the stomachs of Muskellunge (Esox masguinongy) . carpenter (1952) found Thamnophis sirtalis would eat li· viridescens in 10 the laboratory and in the field, but provided no quantitative data. He also found that four of six Thamnophis sauritis' stomach samples collected in 1950 contained eastern newts. Shure, Wilson, & Hochwender (1989) found a total of 58 efts (some still alive) in six southern Appalachian upland areas in North Carolina that were attacked by unknown predators. Signs of predation included evisceration, decapitation, midventral punctures, limb removal, and removal of the lower jaw. Predators apparently learned to exploit the less toxic parts of the newt (Shure, et al., 1989; Brodie, 1968), preying on an easily captured, slow-moving, and otherwise defenseless animal. Hurlbert (1970) fed eastern newts to single specimens of Lepomis gibbosus, Rana catesbeiena, Chelydra serpentina, Chrysemys picta, Charadrius vociferus, and Buteo jamaicensis. Although some of these individuals ate newts, these results may not be representative of their populations. He also tested two young and two older raccoons (Procyon lotor) and found that the young raccoons would not eat eastern newts. In contrast, older raccoons ate them after scrubbing the newts in water and rubbing them between their paws to remove the toxic materials. Hurlbert (1970) tested the ability of Thamnophis sirtalis to feed on the eastern newt. Only three post-larval migrant efts out of 49 offered were voluntarily eaten, while all of 34 plethodontid and ambystomid salamanders were accepted. He observed three seize newts, but then immediatly 11 reject them and mouth wipe on the substrate. In all three instances, rejection was immediate upon seizing the newt. He did, however, observe a forth ~. sirtalis voluntarily eat an eft. The snake spent 90 seconds handling the eft and then slowly swallowed it. When he force fed three snakes one newt each, the newts were retained by all three snakes and no ill effects were observed. Only 3 of 12 ~. sirtalis voluntarily accepted eastern newts as food in 49 attempts. It took five times longer for the snakes to swallow newts than to swallow other species of salamanders. ~. sirtalis showed no signs of distress when they ate newts voluntarily or when they were force fed (Hurlbert, 1970) . Brodie (1968) force fed adult eastern newts and efts to a single Rana catesbeiena and observed no ill effects. on one occasion the frog voluntarily accepted two adults and two efts in rapid succession but later regurgitated them. This frog later ate a two-year-old eft voluntarily without ill effects. Hurlbert {1970) fed a single B· catesbeiena for six months on a diet of eastern newts and an occasional crayfish. This frog experienced no ill effects. In contrast, Brown (Pers. comm.) described a B· catesbeiena that ate a newt and died, and later, the newt eventually crawled out of the frog's mouth unharmed! Brodie (1968) force fed eastern newts to Rana clamitans and Desmognathus quadromaculatus which regurgitated the eastern newts almost immediately, followed by mouth wiping. When he force fed eastern newts to a variety of herptiles, 12

including Ankistrodon contortrix, Eumeces fasciatus, Crotalus borridus, and two Diadophus punctatus the animals died: 75, 40, 300, 80 and 160 minutes, respectively, after force feeding. Brodie also force fed eastern newts to two Thamnophis proximus; and both died between 85 and 360 minutes after feeding. A third T· proximus ate a newt voluntarily without any ill effects. Brodie (1968) found efts quickly recovered when regurgitated as long as thirty minutes after being eaten by either toads or snakes. Webster (1960) observed a dead tiger trout (Salvelinus fontinalis x trutta) with no other signs of ill health, that contained a recently eaten eastern newt in its stomach. Webster & Little (1942) observed "a few specimens" of recently planted brown trout (Salmo trutta) with newts in their stomachs. Cooper (1942) reported three eastern newts among the stomach contents of 133 brook trout (Salvelinus fontinalis). Webster (1960) force fed eastern newts to three wild brook trout; two were dead in 90 minutes, and one became moribund but recovered. When Webster force fed newts to "smaller" brook trout they showed "acute convulsive distress and loss of equilibrium" within 5-10 minutes. He also found that hatchery trout (species not identified) seized eastern newts, but quickly spat them out. Hurlbert (1970) fed eastern newts to two Bufo americanus. "One always refused to eat newts, the other varied in its response". Rana clamitans (Brodie, 1968), Rana catesbeiena (Brodie, 1968; Hurlbert, 1970), and Lepomis 13 gibbosus (Hurlbert, 1970) all vary in their acceptance of eastern newts as a food item. As seen above, there is much variation in the published data with regard to the edibility of the eastern newt. Despite the extensive research to date on eastern populations of li· viridescens and its defenses against predators, there are only a few studies specifically involving the central newt. Cochran & Redmer (1992) found the central newt unpalatable to free-ranging raccoons. Brandon (Pers. comm.) states that the skin secretions of the central newt are similar, but not identical with those of the eastern subspecies. The central newt is believed distasteful (Brandon, et al., 1979a; 1979b) as is the eastern subspecies. Still, it may be susceptible to potential predators which have yet to be tested. This study investigates the ability of a variety of Illinois amphibians and reptiles to feed on the central newt. 14

MATERIALS AND METHODS

Larval central newts were collected at ponds in MacGuire's Orchard, about 11.3 Km. south of Carbondale, Jackson Co., Illinois. Larval newts were held at room temperature until they metamorphosed into efts. Upon metamorphosing, efts were moved into plastic shoeboxes containing landscaping bark as a substrate (approximately 25 efts per box). The substrate was misted with aged tap water daily and a petri dish of water was continuously present. Guidelines for maintenance of adult newts described by Verrel (1991) were followed. Three species of plethodont salamanders were used as controls in my feeding experiment: Plethodon cinereus, Plethodon dorsalis, and Eurycea cirrigera. Plethodonts were collected at Shades State Park in Indiana. Housing was the same as for efts. Efts and plethodonts were both maintained at 9 c. Both efts and plethodonts were given several hundred fruit flies per shoebox once a week.

Experiment 1: Response of Potential Predators of the Central Newt to Newts and Control Salamanders This experiment investigated the response of one species of salamander (Ambystoma tigrinum), two species of turtles (Terrepene carolina, Chrysemys picta), and five species of snakes (Diadophis punctatus, Heterodon platyrhinos, Lampropeltis calligaster, Nerodia sipedon, and Thamnophis sirtalis) to the central newt. These species were selected as

I_ 15

potential predators based on the published occurrence of salamanders and/or efts in their diets, and the availability of the predator species. All potential predators were housed and fed in captivity for at least one month prior to testing. Six Ambystoma tigrinum were housed individually in 39 oz. coffee cans with holes punched in the lids. Well washed sand was used as a substrate. Each container was misted daily to prevent desiccation. Each A· tigrinum was fed earthworms, mealworms, and a variety of insects biweekly prior to use in the study. Five Chrysemys picta were housed individually in 40 L aquaria containing 8 L of tap water. An incandescent lamp illuminated the tanks. They were fed earthworms, a variety of insects, and floating trout food pellets prior to use in the study. All five snake species were housed in 33 x 32 x 18 cm wood enclosures with glass fronts. These cages contained a 10 cm glass water bowl and a hiding place, with newspaper or artificial grass turf as a substrate. Lampropeltis calligaster were fed pinky mice while the other snakes were fed portions of thawed Ambystoma, thawed and live frogs, and/or live fish once a week. Six Terrepene carolina were housed communally in a square 80 L aquarium with a dish of water and wood bark as a substrate. Subjects were fed floating trout pellets soaked with water, a variety of greens and earthworms. Initially each individual of each species was offered a plethodontid 16

salamander to determine if the species ate salamanders. Salamanders were determined to be acceptable as a food item if a subject species completely refused to eat them after five trials. If a species was determined to be a salamander predator, it was entered into the experiment. Individuals were fed weekly alternating between a plethodont and an eft of the central newt until the end of the study. If the prey item was not eaten after fifteen minutes, it was replaced with the other prey type. The second prey type was also left in the cage for fifteen minutes. Prey items were placed in the center of the enclosure for each snake species and Ambystoma tigrinum, and quietly released into the enclosure for Chrysemys picta and Terrapene carolina. The following data were recorded for each potential predator: 1) eat or do not eat; 2) latency of response; 3) presence and duration of feeding response; 4) location of predator attack (for snakes); and 5) behaviors displayed by predators and prey during each trial and the chronology of their occurrence. The effectiveness of behaviors employed by predators in reducing handling time, and of behaviors employed by prey at increasing it and/or avoiding capture were also recorded. A subsequent experiment was conducted to determine if salamanders in the grasp of a snake predator escaped more frequently when the snake itself came under attack, as 17

compared with a snake that was not attacked. Four ~. sirtalis were offered one plethodont salamanders in each of seven trials (seven plethodonts total). Upon seizure of the prey by the snake, the snake was grasped by the lower body and lifted out of the cage. Escapes by salamanders were tabulated.

Experiment 2: The Effect of Hunger on Food Preference In this experiment Emlen's (1966) hypothesis that more hungry predators are less discriminating in prey choice was tested using garter snakes. Tongue flick frequency has been described as an indicator of food preference in several species of snakes including Thamnophis sirtalis (Arnold, 1978; Burghardt, 1966; 1967; 1968; 1970; 1971; 1974; Burghardt & Abeshaheen, 1971; Burghardt & Hess, 1968; Burghardt & Pruitt, 1975; Burghardt, Wilcoxon & Czaplicki, 1973). Forty-liter aquaria were divided with peg board into three 25 x 16 x 30 cm high compartments. Each compartment contained a rock, a water bowl, and was floored with artificial grass turf. one eft-eating garter snake from experiment one was housed in each compartment. Four garter snakes were used in this study. Satiation level for each garter snake was determined by feeding garter snakes 0.5 g portions of thawed Ambystoma tigrinum until the snake refused to eat. This was repeated once a week for five weeks and the mean satiation level calculated for each snake. Garter snakes were subsequently tested at 0%, 50%, and 100% satiation. Snakes were tested 18

using odoriferous cotton swabs following the procedures of Arnold (1978). The swabs were prepared by placing five live adult prey (Notophthalmus viridescens louisianensis, or Plethodon cinereus) or thawed pieces of Ambystoma tigrinum in beakers with a volume of tap water equal to that of the prey items. Tap water was used to prepare control swabs. Prey items and swabs were held in the water for 15 minutes prior to use. Swabs were swirled in the water to help pick up odor. Snakes were tested weekly on scheduled feeding days. During the first of three series of tests swabs were offered in the following order: two-lined salamander, central newt, tap water, and thawed Ambystoma. In each later run, the order was rot~ted so that each food type was offered in each time slot. A video recorder was used to record the snakes' responses for later review on a VCR to accurately count tongue flicks. The swab was held approximately one cm from the snakes' snout. If the snake failed to protrude its tongue, the swab was then touched to the snakes nose. Once the tongue had touched the swab a single time, the swab was held stationary for two minutes. If the snake struck at the swab it was quickly pulled away, then presented again. Tongue flicks were counted for two minutes, and averaged per minute for each item at each hunger level. Each snake was tested before feeding, two hours after feeding to 50% satiation, and two hours after feeding to 100% satiation. The time lapse between feeding and testing was 19

administered to prevent any sensory adaptation that might result during feeding from influencing tongue flick frequency. 20

RESULTS zsperiment 1: Response of Potential Predators of the central Newt to Newts and control Salamanders

Ambystoma tigrinum refused efts (Table 1). Upon seizing an eft, A· tigrinum shook it violently, then spat it out. A· tigrinum never refused an eft without first seizing it. Sometimes the eft was thrown across the container only to be grabbed again, if the eft moved quickly. Upon release by A· tigrinum, efts remained motionless for an unrecorded amount of time, then began "slow-walking". While slow-walking, the eft's body is held rigid with the tail extended, lifted off the ground. The eft moves without the usual serpentine movement, only the legs are used while slow-walking. Every step is taken very slowly and "deliberately". No eft was seized by A· tigrinum while slow-walking. In contrast, A· tigrinum accepted most (14/15) control salamanders (Table 1). However, there was a high mortality rate of A· tigrinum after ingesting controls. One died a few days after the first trial, 2 after the second trial, 2 after the third, and 1 after the fourth. Terrepene carolina refused to feed on newly metamorphosed A· texanum and control salamanders after having fed readily on a variety of other food types. This species was therefore not used further in the study. Chrysemys picta accepted both efts and controls as food through the first four trials. Individuals began refusing 21 both species after the second trial, and by the eighth trial these turtles refused both efts and the control (Table 1). In order to be certain that the turtles were refusing both prey types and weren't sick, the animals were offered some floating trout pellets in the last two runs on each turtle. In all cases the trout chow was eaten after rejecting both efts and plethodont. Earlier g. picta ate the yellow underside of efts but usually ignored the upper portions of the eft as described by Hurlbert (1970), and by Shure, et al. (1989). Eft remains from my study were retained and preserved. Two specimens of Diadophis punctatus fed readily on the control salamanders but rejected efts on the one occasion that they were offered (Table 1) . Diadophis punctatus was not further tested because of circumstances unrelated to the study. Six naive juvenile Lampropeltis calligaster refused to eat all salamanders so they were not further tested. Two juvenile Nerodia sipedon refused efts but accepted control salamanders (Table 1). Nerodia sipedon quickly seized efts in the first two trials. After holding an eft in its mouth for a moment, the snake released the animal, and ignored it for the duration of that sequence. Two juvenile Heterodon platyrhinos (1 known to be naive) accepted efts and control salamanders (Table 1) as food. No difference in fi. platyrhinos acceptance rates of efts and controls was found. 22

Five Thamnophis sirtalis accepted both efts and controls (Table 1). Efts and control salamanders appeared equally palatable to ~. sirtalis. No ill effects were observed in either fi. platyrhinos or

~. sirtalis as a result of eating either prey type. In fact, both snakes were often observed actively searching for more food 15 minutes after being fed either efts or control salamanders. Data for swallowing time was pooled from all snake species to compare overall time to swallow controls versus time to swallow efts. The log (time to swallow / weight of the salamander in grams / weight of the snake in grams) was calculated for controls and efts and then compared with an independent t-test. Time to swallow efts was significantly shorter (t = 3.4, df = 1, p<.05) than the time to swallow controls. Plethodonts performed three escape behaviors (tail autotomy, thrashing, and tail wrapping) reported by Feder & Arnold (1992). A fourth behavior, crawling, was not previously reported. Here the plethodont appeared to pull itself out of the snake's mouth by walking and pushing on the snake with its fore legs, as if trying to escape. This behavior was first observed near the end of the study so there was not enough data to adequetly quantify it. Tail autotomy was the most effective escape behavior used by plethodonts. Five of 10 plethodonts utilizing this behavior escaped predation. Autotomy was employed by 10 of 77 23 salamanders during a snake attack. Thrashing was employed by plethodonts when grabbed by a snake in 26 of 77 plethodont-snake interactions. This behavior resulted in five escapes. Tail wrapping was observed in 17 of 77 predatory interactions between control salamanders and snake predator species. Plethodonts never tail wrapped during an encounter with fi. platyrhinos (0/17 events). They tail wrapped in 7 of

15 encounters with H· sipedon, 7 of 34 encounters with ~. sirtalis, and 3 of 4 encounters with ~. punctatus. Tail wrapping was not observed in response to non-snake predators used in this study. The effect of both tail wrapping and the location where the snake seized the salamander's body on time to swallow was analyzed using a 2 X 5 Anova. Tail wrapping was found to significantly increase swallowing time (f=l0.17, df=l, p<.002) as did location of attack (f=2.50, df=4, p<.04). The interaction of tail wrapping and location of attack was significant (f=4.03, df=4, p<.004). It appears that tail wrapping, and the interaction between the two significantly reduce swallowing time. Figure 1 and Table 2 show the affect of tail wrapping and location of attack on time to swallow. The only location in which tail wrapping by plethodonts significantly increased time to swallow was the pelvic girdle. There was a large variance in the effectiveness of tail wrapping when seized by the pectoral girdle. swallowing time in midbody strikes was unaffected by tail wrapping. 24

Plethodonts tail wrapped less frequently when seized pelvicly than when seized in other areas (Table 3) however these results are not significantly different (Chi square = J.98, df = 4, p<.4077). When seized by the tail and occasionally when seized pelvically, plethodonts displayed a variation of tail wrapping. Here plethodonts wrapped their body over the top of the snake's head and released a sticky mucous. The affect of location of attack on swallowing time of efts was analyzed with a one-way anova. Location of attack was found to significantly affect swallowing time (f=3.16, df=4, p<.050) as shown in figure 1. A Student Newman-Keuls means comparisons test indicated that time to swallow is significantly higher when an eft was attacked at the midbody than when it was seized pectorally (Table 4). Unken reflex was performed by efts during 21 of 43 snake attacks. It was not observed except when in the mouth of the snake. While in unken, the eft presses its dorsum, especially the parotid and pelvic region against the teeth of the snake. The tail droops over the top of the snake's head and appears to grip it. A Mann-Whitney test was used to compare time to swallow efts performing unken versus efts that did not display this behavior. Efts in unken took significantly longer to swallow than efts that did not display this behavior (U = 19, p<.05). Unken did not significantly increase the probability of eft escape. The anatomical location of attack by snakes on control 25 salamanders was statistically analyzed with Chi square. snakes struck the pelvic region more often (Chi square = 15.09, df = 4, p<.005) than the head (table 3). There were no other significant differences in number of attacks between other regions. Four of seven control salamanders escaped when the T· §irtalis was seized and lifted out of the cage by the investigator. Previously, three of 34 salamanders escaped after being attacked by T· sirtalis that were not seized and lifted out of the cage.

Experiment 2: The Effect of Hunger on Food Preference The effect of hunger and food type on tongue flick frequency in T· sirtalis was statistically analyzed with a 3 X 4 Anova. Both satiation level (f=16.67, df=3, p<.0001) and food type (f=5.87, df=2, p<.0036) significanty influenced tongue flick frequency but the interaction between these two was not significant (f=l.79, df=6, p<.104). Garter snakes tongue flicked most frequently to two-lined salamander stimuli while 50% satiated and tongue flicked significantly more at 0% satiation than at 100% (fig. 2). Garter snakes that were 100% satiated showed a significantly higher tongue flick response to thawed Ambystoma tigrinum than to any of the other stimuli presented (fig. 2). There was no difference between tongue flick rates when presented with two-lined salamander, water, or efts at this level. When 50% satiated, water elicited a significantly 26 iower response than the other stimuli. Two-lined salamander, eft, and Ambystoma tigrinum did not elicit significantly different responses. Unsatiated garter snakes showed a significantly higher tongue flick frequency when presented with the essence of Ambystoma tigrinum than that of water, two-lined salamander, or efts. There were no other significant differences in tongue flick response by garter snakes when unsatiated. 27

DISCUSSION

B:xperiaent 1: Response of Potential Predators of the central Newt to newts and control Salamanders Efts were acceptable prey items to Heterodon platyrhinos and, to a lesser degree, to Thamnophis sirtalis. Chrysemys picta accepted efts initially, but they were later refused. Ainbystoma tigrinum, Nerodia sipedon, and Diadophis punctatus totally refused efts, but accepted other salamanders as food. It was surprising that Ambystoma tigrinum refused to eat efts because larval A· tigrinum have been found to depress larval Notophthalmus viridescens populations in natural ponds (Morin, 1983). Morin also found larval newts in the stomachs of some of these salamanders. The fact that tetrodotoxin (TTX) is produced by all stages, egg to adult (Fuhrman, 1967), and that larval A· tigrinum fed on newts, while my adults did not, may indicate either an age-biased resistance to TTX poisoning, or geographic variation in TTX resistance between Morin's population and the population in Henry county, Illinois. Having the ability to safely feed on newts as larvae would be highly adaptive where these two species utilize the same breeding ponds. Both larval and adult newts provide a "plentiful food source that could be exploited with little competition" (Shure, et al., 1989). As adults it might be adaptive for these salamanders to allocate resources elsewhere. Efts are rarely encountered, even where common in Illinois. Therefore adult A· tigrinum, unlike larvae, might 28

have little need for TTX resistance. Adults with and without such traits should be equally competitive. Adult A· tigrinum unable to tolerate a poison that is seldom encountered may experience a higher selection coefficient relative to TTX resistant adults. TTX resistance carries substantial costs to predators. They must process the chemical, requiring a more developed adrenal gland and other internal secretory tissues (Smith & White, 1955). There is also a substantial investment in repair of tissue damage resulting from both the TTX and the increased epinephrine levels needed for eating toxic prey (Edgren & Edgren, 1955). By partitioning resources (such as energy nutrients used in the production of epinephrines) in areas other than TTX resistance, adults could allocate these resources elsewhere, making such individuals more competitive. This is especially true if, as may be in the case of the study subjects, adults can recognize efts as poisonous prior to ingestion. Geographic variation may also explain the differential susceptability of efts to predation by A· tigrinum when comparing my study to that of Morin (1983). Brodie & Brodie

(1991) observed a similar situation in ~. sirtalis, where island populations ~- sirtalis were found to vary in their resistance to TTX. Geographic variation of TTX resistance in A· tigrinum is unreported. The "slow-walking" behavior displayed by efts was an effective "post-attack" strategy to avoid predation by A· tiqrinum. The smooth movement of the eft as it slowly creeps 29

away appears to be undetectable by A· tigrinum. "Slow-walking" was not utilized by efts until attacked, suggesting several possibile explanations. Efts may not recognize a predator until attacked. If they could recognize a predator, they could immediatly begin "slow-walking" and avoid the predation event altogether. Avoiding the predation event would decrease the susceptability of efts to injuries incurred in the attack. "Slow-walking" may have evolved in conjunction with or after the evolution of distasteful skin secretions of the newt. It is likely that a tactic as effective as "slow walking" would be perfomed more readily if it evolved independently of distastefulness. This trait may have evolved as a post-attack strategy independently of distastefulness if either of the following are true: 1) efts are more acceptable as a food source than previously assumed; or 2) predators can recognize slow-walking efts. A hypothetical, pre-eft that "slow-walked" as a pre-attack strategy would quickly be removed from the population by eft-eating predators. Slow walking efts are easily captured by virtue of their slow movements. This would leave only those individuals that "slow-walk" as a post-attack strategy. "Slow walking" could increase the fitness of efts because an eft that "slow walks" may avoid a second predatory event. The high mortality rate of A· tigrinum after eating control salamanders suggests that secretions of Eurycea cirrigera may be lethal to this species. Plethodon cinereus is known to be distasteful to shrews (Brodie, et al., 1979). 30

It is unknown whether the chemical causing this distastefulness is the cause of death of the A· tiqrinum in this study. The suseptability of A· tiqrinum to plethodont secretions has not been investigated. Shure, et al. (1989) described terrestrial predation on efts similar to the g. picta predation described by Hurlbert (1970). They suggested that a terrestrial turtle such as Terrepene carolina might feed on efts. It was surprising to find that this species refused to eat any salamanders, because this species is known to be omnivorous (Tyning, 1990) Salamanders are a nutritious food source, readily available in the areas where ~. carolina were collected. Hurlbert (1970) offered three live post-larval migrant efts to g. picta. The turtle ate two immediately, and ate the other after an initial rejection. My data suggest that either plethodonts are as distasteful to g. picta as efts, or this turtle is unable to tell these species apart. It is unfortunate that I was unable to test further Diadophis punctatus. Hamilton & Pollack (1956) reported salamanders as the principal diet of these snakes. In fact, Plethodon qlutinosus, believed to be an extremely noxious species, was frequently found in gut samples. If these snakes can eat ~. qlutinosus, they might have found efts edible as well. The data from this study, however, are too limited to make any conclusions. It is interesting that li· sipedon consistantly refused to eat efts. Brodie (1968) found that this species was 31

resistant to TTX. This would suggest that TTX resistance in H· sipedon could be a preadaptation to feeding on efts. Since these snakes refuse to eat efts, they must find them distasteful. Until an eft-liking phenotype evolves, the TTX resistance will not appreciably increase the fitness of H· sipedon. Eventually this trait would drop out of a population of aft-disliking phenotypes since individuals allocating resources to other areas would be at a selective advantage (Brodie & Brodie, 1990; 1991). Notophthalmus viridescens probably once occurred where my H· sipedon were collected (Smith, 1961). H· viridescens has not been reported in Coles County, Illinois for almost a century. This time span may be long enough to allow an eft-eating TTX resistant genome to drop out of the population especially if, as Brodie, III (Pers. Comm.) suggests, TTX resistance costs the snake a substantial amount of fitness in other areas. The reduction in trait expression has also been reported in association with the evolution of toxin resistance in bacteria, house flies, scale insects, and Drosophilla sp. (Grant, 1977). If a similar situation exists in H· sipedon, TTX resistance would be strongly selected against where large populations of prey containing TTX are not available. This supports the theory of geographical variation in TTX resistance in H· sipedon. It is also interesting that H· sipedon fed readily on newly metamorphosed toadlets but refused efts. The parotid secretions of toads (Bufonotoxin) are digitaloid poisons simmilar to TTX that can be harmful if ingested. Licht & Low 32

(1968) found that these secretions cause cardiac and muscular tetany and eventual death in snakes not specifically adapted to feeding on toads. It would have been surprising if H· platyrhinos had refused to eat efts because this species is an amphibian specialist well known for eating bufonids. There appeared to be no difference between the acceptance of efts and the control salamanders by H· platyrhinos. Except for the isolated field observation by Uhler, et al. (1936) this is the first recording of H· platyrhinos predation upon li· yiridescens. Thamnophis sirtalis did not readily accept efts at the onset of the study, but later accepted them at every trial. This suggests that either the snakes were unfamiliar with the prey and had to learn it was edible, or that the weekly feeding of a single salamander weighing between .5 and 1.5 grams was an insufficient volume of food, leading to more hungry snakes. This feeding level could have affected the snakes acceptance of efts (see experiment II). These garter snakes were believed naive to efts, because they were collected outside the newt's present range (Coles County, IL). The historical range of li· viridescens probably included the

collection site of these ~. sirtalis and a genetic predisposition for feeding on efts might remain in the population, although li· viridescens has been absent from this county for almost a century. This time period may have been to to small to remove an "eft-liking" phenotype from the 33

population of garter snakes. Geographic variation in food preferences in garter snakes has been reported by Brodie & Brodie (1991), Burghardt (1970) and by Dix (1968). Brodie & Brodie (1990; 1991) have shown geographical variation in garter snake TTX resistance. Hurlbert (1970) showed that garter snakes ate only three H· viridescens yiridescens out of 49 offered. The snakes in this study accepted H· viridescens louisianensis at a much higher rate. The rate of acceptance in my study may be an eft subspecies difference, garter snake geographical difference, or a factor of snake versus eft size. Brandon (Pers. Comm.) claims that the chemical composition of central newt skin secretions contain a lower concentration of TTX and an increased concentration of other substances. Snakes may be more sensitive to TTX than to these other products. Burghardt (1974) has shown that prey preference polymorphism may exist. If so, these polymorphisms may be unevenly distributed, explaining the differences among these studies. Garter snakes were larger than the other species of snakes I used in this study. It is possible that the volume of TTX produced by the salamanders was enough to deter small snakes, but too small to be effective against larger individuals. Garter snakes swallowed efts more quickly than did other snakes, therefore the eft to snake size ratio was much smaller for garter snakes than for other species. As eft to snake body size ratio increases, it might become more difficult for 34

snakes to handle efts. Compound this "size effect" with the effects of "escape manuevers" (that increase swallowing time) and the exposure to eft skin secretions could be greatly prolonged. Lengthened exposure to these secretions could increase their effectiveness, and the probability of escape for the eft. Furthermore, larger eft to snake size ratios could also increase the probability of abrasive action of the teeth, possibly stimulating the release of skin secretions. Hurlbert (1970) anecdotally observed that i. sirtalis took longer to swallow efts than to swallow either plethodont or ambystomid salamanders. In my study, I found the opposite to be true, but my results are confounded because the control salamanders performed various escape strategies that may slow the swallowing process. Of the four escape strategies employed by plethodontid salamanders, tail wrapping was the only one that occurred frequently enough to be analyzed. Because tailwrapping was employed against all snakes except li· platyrhinos it seems logical to conclude that H· platyrhinos in some way is able to prevent this behavior. A possible explanation may lie in the mild toxicity of the saliva of this species. McAlister (1963) found that injections of H· platyrhinos saliva were lethal to 15 of 17 individual anurans, while being harmless to mice. It is possible that the saliva of this snake is potent enough to prevent a tail wrapping response, but the effect of H· platyrhinos saliva on Amphibia needs more study. It is unknown what effect the saliva has on species of Urodella, or how effective it is at increasing H· 35

platyrhinos success in subduing and devouring amphibian prey. Plethodonts significantly increased snake swallowing time when tail wrapping was employed, but did not significantly increase escape rate. Snakes that attack plethodonts pelvically {where tail wrapping is least likely to occur) should have a competitive advantage over those which seize plethodonts at other locations. Increased swallowing time increases energy expenditure in handling prey. Feder & Arnold {1982) found that the level of anaerobic metabolism in garter snakes was positively correlated {r=0.57, p<.05) with handling time. As handling time increased, so did the lactate concentration, ie. anaerobic metabolism. It is beneficial to the snake to use as little energy as possible while handling prey, to avoid less efficient metabolic pathways. Increased swallowing time could also increase the exposure of the snake to predators. By tail wrapping the plethodont may increase the chances of the snake being attacked, resulting in the salamander's escape. A snake that is ingesting a prey item cannot defend itself with a full mouth. If the prey item is large and/or bulky, the snake's ability to escape may also be hampered. Upon attack by a predator, the value of the prey item might become outweighed by the value of escape {Stephens & Krebs, 1986). Under such conditions, salamanders should be more successful at escaping when the predator is under attack than when not under attack. My data from experiment 1 suggest that salamanders seized by snakes which are attacked do escape more frequently than those 36

captured by snakes that were not attacked. Snakes would experience increased fitness by attacking plethodonts pelvically. A pelvic trike reduces the chance of tail wrapping defense, resulting in a shorter swallowing time, therefore reducing the probability of being attacked while ingesting the prey. Conversely, salamanders would benefit from an increased swallowing time by the snake because this could increase the liklihood of the snake being attacked by a predator, thereby enhancing its probability of escape. Increased swallowing time by the snake decreases the number of prey items this predator can ingest as represented by the "disc equation" (Holling, 1959). The "disc equation" predicts the number of prey consumed per unit time as a function of prey density (Gross, et al., 1993; Spalinger & Hobbs, 1992). This consumption rate is decreased as prey handling (swallowing time) is increased as shown below: ADT N = number of prey captured N = A = predators searching efficiency ------l+AHD (square meters per minute) D = prey density (#/s9uare meter) T = duration of fora~ing (minutes) H = handling time (min./prey) If a hypothetical snake had an H = .5 min, T = 2 min, D = 2 prey/m, A= 2 m/min. then 2.67 prey would be captured.

(2) (2) (2) 8 N = ------= ------= 2.67 1+(2) (.5) (2) 3 If we increase the handling (swallowing) time (H) to one minute per prey, then prey captured would decrease to 1.60 prey while foraging: 37

(2) (2) (2) 8 N = ------= ------= 1.60 1+(2) (1) (2) 5 As seen above, the benefits of decreasing swallowing time for the snake can be dramatic. A doubled handling time in this hypothetical example resulted in a greater than 50% reduction in foraging success for the snake. This missed opportunity may be a strong selective force against snakes that do not attack salamanders pelvically. The loss of prey due to a tail wrap might have a more substantial effect than that of location of attack (a direct result of swallowing time differences). This might better explain why snakes attack the pelvic area more often than other areas. In order to substantiate this explanation it would be necessary to collect much more data on swallowing times for each anatomical location both with and without tail wrapping. In this way, the lost opportunity for each location could be accurately represented to better explain why snakes attack the pelvic region more often than other areas. Kin selection in plethodonts may play a role in tail wrapping to increase snake swallowing time as well. If, as suggested above, increased swallowing time does decrease the number of prey the snake can ingest, and siblings reside in the vicinity; then the plethodont increases its fitness by tail wrapping. By tail wrapping, the time for the snake to swallow is increased and the number of siblings and nearby relatives that can be ingested by the snake is decreased. This would increase the potential for the prey's genome that is shared with these related salamanders to be reproduced. The unken ref lex has previously been suggested as a warning of distastefulness to potential predators. Because efts in this study only displayed the unken while in the grasp of snakes, but never prior to an attack, this explanation seems unlikely. Ducey & Brodie (1983) failed to observe unken when efts were touched by garter snakes. They found that efts either walked away or "postured by elevating the body and flexing the head downward or by elevating the chin and forebody" when touched by the snakes tongue. They did not allow any snakes to attack salamanders. While perfoming the unken in the grasp of the snake, the dorsum of the eft is in maximum contact with the maxillary teeth of the snake. This would increase the stimulation of the skin on the dorsum and potentially expedite the release of distasteful secretions by the eft. These secretions, if unpalatable, may induce the snake to release the prey. This suggests that unken is not a warning behavior, as previously proposed, but is a defense strategy employed by this salamander to expedite release of distasteful skin secretions. If skin secretion is activated by abrasive stimulation, it may explain the results observed by Brodie (1968). Of the eight squamates Brodie force-fed efts, seven died. He also force fed efts to Rana catesbeiana, B· clamitans, and Desmognathus guadromacrolatus. Of these, only B· catesbeiana retained the efts. In force feeding these animals, it is 39 possible that efts were scraped against the teeth, stimulating the release of skin toxins. Rana catesbeiana, because of its large mouth, may have been easier to force feed than the other animals. Consequently, abrasive actions may have been reduced, precluding dermal exudate production. This might explain the retention of efts by this species and the death of the squamates observed by Brodie (1968). Geographical variation may explain the failure of efts of the central newt to show the unken response prior to an attack. Ducey & Brodie (1991) found that Bolitoglossa subpalmata showed geographical variation in its readiness to perform a tail display (a type of antipredator behavior) when touched by a snakes tongue. My results may be of a similar nature; it would be interesting to test the readiness of these efts to perform the unken reflex when contacted by a snake. The unken ref lex is similar to the tail wrapping behavior displayed by plethodonts. So much so, that at the onset of the study I undoubtedly recorded many unkens as tail wraps. Tail wraps were not observed in efts after I had identified the presence of the unken in the snakes grasp. Behaviors initially identified as tail wraps were reclassified as unken since the two behaviors are so simmilar in efts. At this time there is no clear difference between tail wrapping and the unken ref lex as displayed by the central newt. The simmilarity of the unken ref lex to tail wrapping suggests a common evolutionary origin. The family 40

Plethodontidae and the family Ambystomatidae utilize tail wrapping when attacked by snakes. Duellman & Trueb (1986) state that Plethodontidae and Ambystomatidae probably broke into separate groups at some time after their common ancestor separated from the predecessor of the Salamandridae. This suggests a possible phylogeny of the developement of tail wrapping. Apparently, tail wrapping was present in the common ancestor of both Ambystomatidae and Plethodontidae since both families have been observed to display this behavior. The common ancestor of Salamandridae either displayed tail wrapping and this behavior has now become modified into the unken reflex, or had a primitive behavior that later evolved into unken in Salamandridae and tail wrapping in the other two families. The fact that unken reflex does not appear to effectively grip the snake's head, althou9h the tail does drape over the head of the snake, suggests that the two behaviors are related. It would be interesting to survey the presence of tail wrapping behavior across Urodella to determine the phylogeny of this behavior.

Experiment 2: The Effect of Hunger on Food Preference It is possible that snakes in this study accepted efts because the period between feedings was too long. Emlen (1966) proposed that food preference should become less defined when an animal is hungry and more circumscribed when an animal is satiated. Chemical stimulation plays an important role in the feeding behavior of garter snakes. The 41 level of stimulation experienced by a snake can be detected usinq the snake's tonque flick frequency in response to a specific stimulus (Burqhardt, 1966). My data suqqest that food preference, as indicated by tonque flick frequency, is not chanqed by hunqer level. This is important in analyzinq this study and others like it. It is possible that more hunqry snakes are less selective in prey choice despite their innate preferences for prey. Hayes (1993) found that crotalus yiridis modified it feedinq behavior in response to hunqer level. As these snakes' hunqer level increased, their success rate at capturinq and handling prey decreased. My results suggest that garter snakes prefer thawed Ainbystoma tigrinum to the other food types and that more hunqry snakes respond more strongly than more satiated snakes to these stimuli. Since the portions of A· tigrinum were frozen and then thawed they may have produced a stronger smell. It is possible that tongue flick frequency in this study is not an indicator of preference, but a factor of stimulus strength. Tongue flicking may simply be a factor of the "excitement level" of the snake induced by the level of food stimuli, and not an indicator of preference. Arnold's (1978) using cotton swabs to carry chemical stimuli has potential for bias. An investigator could subconciously alter the tongue flick frequency of the snake because he knows which swabs carry which scent. snakes often began flicking if the swab was accidentally moved and sometimes the snakes would grab the swab. These are a few of 42 the problems with analyzing data obtained with this method. A better procedure might be to use cotton balls soaked in the desired stimulus. The cotton ball could be placed in a small screened box on the bottom of the cage and the response video recorded. This method would eliminate the problem of accidentally jiggling the swab and stimulating tongue flicking activity. 43

Conclusions There appears to be variation between predator species and their acceptance of efts as food. Ambystoma tigrinum, Chrysemys picta, and Nerodia sipedon refused efts as food, whereas Thamnophis sirtalis accepted efts as food but showed a significantly higher response to plethodonts. Heterodon platyrhinos fed on efts as readily as it fed on plethodont salamanders. Efts displayed two defensive behaviors: "slow-walking" and the unken reflex. Slow-walking was utilized exclusively as a post-attack strategy, possibly to avoid a second attack by the predator. The unken reflex was only displayed while in the mouth of a snake. This suggests that the unken reflex is not a warning behavior, but a defense mechanism to increase contact of the dorsal skin glands with the mouth of a predator. Swallowing time for snakes eating efts was significantly faster than when eating plethodont salamanders. This was probably due to the tail wrapping behavior plethodonts sometimes employ when attacked. Increasing time to swallow may augment fitness of the plethodont being attacked. The snake may experience increased fitness where swallowing times are abbreviated. 44

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Table 1. Acceptance rates of predators to Nothophthalmus viridescens lousianensis efts and plethodontid control salamanders. Predator Prey Eaten Offered

A· tigrinum eft o 6 control 14 15

Q. picta eft 12 40 (total} control 14 68

Q. picta {1st 4 eft 8 10 trials) control 11 12

Q. picta (last 6 eft 4 30 trials} control 3 56 Q. picta 1st vs. last 1st 19 22 last 7 86 .Q.. punctatus eft O 2 control 4 4

N. sipedon eft o 6 control 14 15

H_. platyrhinos eft 5 8 control 12 18

:r. sirtalis eft 18 27 control 31 34 51

Table 2. Time for snakes to swallow salamanders of the family Plethodontidae. The affect of anatomical location of attack (Anova f=2.50, df=4, p<.04), tail wrapping {Anova f=l0.17, df=l, p<.002) and the interaction between these {Anova f=4.03, df=4, p<.004) were found to significantly increase swallowing times of snakes.

Attack Tail Mean Time to Standard Location Wrap Swallow (minutes) Deviation Head n 0.62 .424 y 1.81 .777 Pectoral n 1.12 1. 79 y 2.90 2.21

Midbody n 1. 83 1. 72 y 2.39 2.87 Pelvic n 1.67 3.11 y 7.58 9.68 Tail n 1. 06 .338 y 0.45 0 52

Table J. The influence of anatomical location of attack by snakes on frequency of tail wraps by Plethodontidae with the frequency of snake attack at each location. Snakes attacked Plethodontidae more often at the Pelvic region than at the head {Chi square= 15.09, df = 4, p<.005). No significant difference in incidence of tail wraps at different anatomical locations by Plethodontidae was observed {Chi square = 3.98, df = 4, p<.4077).

Location of Number of Number of Attack Tail Wraps Attacks

Head 3 6

Pectoral 6 11

Midbody 3 7

Pelvic 4 22

Tail 1 9 53

Table 4. Time for snakes to swallow efts. Location of snake attack affects time to swallo (Anova f=3.15, df=3, p<.05). When snakes attack the midbody of an dft, it takes longer to swallow than when attacked pectorally (Student Neuman Kuels=. 4475, p<.05).

Attack Mean Time to Location Swallow (minutes) Standard Deviation Head 2.13 2.61 Pectoral 1. 36 .751 Midbody 5.74 5.47 Pelvic 2.32 1.93 54

Table 5. The amount of lost opportunity a snake incurs as a function of attack location or tail wrapping. potential Lost Probability Location ti prey Opportunity of tail wrap ------head 2.71 5.71 .5 pectoral 8.42 0.00 .72 midbody 3.09 5.33 .58 pelvic 2.80 5.62 .24 tail 5.10 3.32 .15

w/tail wrap .89 1. 34 NA w/o wrap 2.23 0.00 NA 54

Figure 1. The affect of tail wrapping and anatomical location of attack by snakes on time to swallow Plethodontidae. Tail wrapping (Anova f=l0.17, df=l, p<.002), attack location (Anova f=2.50, df=4, p>.04) and the interaction between these (Anova f=4.03, df=4, p<.004) significantly affected swallowing times by garter snakes (T. sirtalis) . 1.4 .µ tail wrap present ..c T bO N no tail wrap present •.-l Q) ~ - 1. 2 Q) ~ cu i:: Cl) -,,...... r:o .µ ..c bO •.-l o. 8 Q) ~ ,.., Q) "O ~ 0.6 s cu ,.....; cu Cl) ~ 0.4 I - I •.-l .µ ·1.I 0.2

·.. ·-..

bO - 0. 0 0 OJJJ ,.....; !

T N T N T N T N pectoral pelvic head tail mid body TAIL ..WRAP AND LO CATION 55

Figure 2. The influence of satiation and stimulus type on ton~ue flick response (Anova f=lS.67, df=3, p<.05). Satiation and ton~ue flick frequency are inversely related. As percent satiation increases, tongue flick rate is reduced (Anova f=5.87, df=2, p<.05). 60 -

Q) .l..J ·.. ;:l 50 i::: ·.-ls ,_. Q) p. 40 en ~ u •.-l .. ·,· ~ . 4-< 30 Q) ;:l ~ bD i::: 0 E-< 20

__.-· ,..-·· ··-•... __ ·_~ •. 10 - ---~

._b.•.• ·• I ~.l t . ·1

A B C ABC ABC ABC Water A. tigrinum E. cirrigera Newt STIMULUS TYPE AND SATIATION LEVEL A. 0% satiation B. 50% satiation C. 100% satiation