Preliminary Observations on Chemical Preference, Antipredator Responses, and Prey-Handling Behavior of Juvenile Leioheterodon Madagascariensis (Colubridae)

Preliminary Observations on Chemical Preference, Antipredator Responses, and Prey-Handling Behavior of Juvenile Leioheterodon madagascariensis (Colubridae)

AKIRA MORI* AND KOJI TANAKA

Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto, 606- 8502 JAPAN

Abstract: Innate responses to prey chemicals, antipredator responses, and prey-handling behavior of a Madagascan colubrid snake, Leioheterodon madagascariensis, were experimentally examined. In a chemical test, ingestively naive hatchlings flicked their tongues frequently to the chemicals prepared from the animal taxa included in their natural diets, suggesting the presence of innate chemical prey preference. In a second test, three different types of stimuli were presented to elicit antipredator responses of the hatchlings. In a nonmoving stimulus session, only a single snake struck and exhibited characteristic displays such as body flattening, neck flattening, head elevation, and jerk. In a moving stimulus session, either no specific responses or a simple flight response was exhibited. In a tactile stimulus session, the above characteristic displays were frequently exhibited. Among these, lateral neck tilting posture accompanying head elevation and neck flattening was unique to L. madagascariensis. In a third test, five types of prey animals were offered to juveniles to examine the effects of prey size and type on prey-handling behavior, but no such effects were detected. Direction of ingestion seemed to depend on initial bite position. Con- stricting behavior was observed only in a single trial. All but one prey were swallowed alive. This inflexibility of prey-handling methods in the juvenile snakes may reflect the characteristics of generalist feeders, which require ontogenetic experiences to handle prey efficiently. Although L. madagascariensis is considered to have well-developed Duvernoy's glands with enlarged, posterior maxillary teeth, the gland secretion did not seem to cause rapid death of prey.

Key words: Madagascar; Leioheterodon madagascariensis; Chemical preference; Antipredator behavior; Prey-handling behavior

INTRODUCTION Madagascar is a biologically unique island * Corresponding author. Tel: +81-75-753-4075; characterized by an abundance of endemic Fax: +81-75-753-4113 taxa. Currently, 17 genera of colubrid snakes E-mail address: [email protected] are known from Madagascar, all of which are (A. Mori) endemic to this island and adjacent islets 40 Current Herpetol. 20(1) 2001

(Randriamahazo, 1999). Because of this pecu- TABLE 1. Measurements of eggs of Leioheterodon liarity, most previous studies on these snakes madagascariensis. The shells of the lower five eggs have focused on their taxonomy and biogeogra- were soft and yellowish. These eggs were preserved phy, and little is yet known of behavioral and in formalin within five days after oviposition. ecological aspects of the Madagascan snakes. Maternal body mass after oviposition was 685g. Leioheterodon madagascariensis is a rela- tively large (SVL>100cm), common colubrid distributed throughout Madagascar (Glaw and Vences,1994). Available information suggests that this species is a generalist predator feeding on a variety of vertebrates (Conant,1938; Campbell and Murphy, 1977; Groves and Groves, 1978; Preston-Mafham, 1991; von Dathe and Dedekind, 1996; Mori and Ran- driamahazo, in press). It is also reported that L. madagascariensis is quite aggressive (Bry- goo, 1982; von Dathe and Dedekind, 1996) and is potentially capable of envenomation through enlarged, posterior, maxillary teeth equipped with distinct Duvernoy's glands sured immediately (Table 1). Except for (Domergue and Richaud, 1971; Domergue, three soft yellowish eggs, which were appar- 1989; Mori, 2000). However, no systematic ently abnormal and thus were preserved in for- behavioral observations have been conducted malin immediately, the eggs were kept in a for this species. plastic box filled with wet sand at natural We experimentally examined three behav- temperatures in Ampijoroa. On 4 November ioral features of the juvenile L. madagascar- two more eggs turned yellowish and started iensis: innate responses to prey chemicals, to smell, and were preserved in formalin. The antipredator responses, and prey-handling remaining five eggs were transported to our behavior. These behavioral features have been laboratory in Japan on 13 November, where well studied in many other colubrid species, but they were kept in an environmental chamber at no comparable studies have been made for approximately 30℃. Malagasy snakes. Innate chemical preference The eggs hatched from 26 to 29 January to various animal taxa was examined using 2000. The hatchlings were measured (Table ingestively naive hatchlings. Characteristics 2) and individually housed in a plastic cage of antipredator responses and prey-handling (295×185×165mm) provided with a paper behavior are described, and the effects of stimu- floor covering, shelter, and water dish at room lus and prey types on these behaviors were temperature between 25 and 30℃. investigated. Basic information on reproductive traits is also provided. TABLE 2. Measurements of hatchlings of Leioheterodon madagascariensis. SVL: snout-vent length, TL: tail length, BM: body mass. ANIMALS AND GENERAL METHODS A female L. madagascariensis (SVL=1293 mm, body mass=975g), collected in the dry for- est at the Jardin Botanique A of Ampijoroa, northwestern Madagascar on 21 October 1999, laid ten eggs in a snake bag on 1 November. The eggs were removed from the bag and mea- MORI & TANAKA-BEHAVIOR OF SNAKES 41

Chemical and antipredator response tests were to examine the chemical responses (see Coo- conducted on 18 and 20 February, respec- per et al., 2000), unavailability of appropriate tively. No foods were offered before these animals obliged us to use allopatric species. experiments. From 22 February, small mice Nonetheless, our aim was to examine the (Mus musculus, 1.5-5.6g) were provided basi- responses of the snake to a given major taxon, cally twice a week. The prey-handling test was not to a specific animal, and we believe that the conducted from 20 July 2000. The snakes were above treatment did not substantially affect fasted for a week before the prey-handling test. the results at that level. Distilled water and Because of the small sample size, no statistical cologne (Fresh Floral, Mandam Co. Ltd, tests were conducted. diluted to ca. 33%) were used as controls for the experimental procedure and for detectable but biologically irrelevant odors, respectively. CHMICAL TEST Before the experiment, the cages of the It has been reported that in many colubrids snakes were moved onto the testing table, and ingestively naive snakes respond to chemical water bowls, shelters, and paper floor cover- cues from species-typical prey with increased ings were removed. After more than 10min, tongue flicking, indicating the presence of the tip of a cotton swab, which was either rolled innate chemical prey preference (see Ford and over the external surface of the animals or Burghardt, 1993 for review). The first test dipped into the control fluids just before each was conducted to investigate responses of test, was presented 1-2cm in front of the snout newly hatched, ingestively naive L. madagas- of the snake. The number of tongue flicks cariensis to chemicals from various groups of directed to the swab was counted for 60sec potential prey and to examine the occurrence of after the first tongue flick was observed. If no innate chemical prey preference in this species. tongue flicks were made 30sec after the presentation of the swab, the tip of the swab was Methods gently touched to the snout of the snakes. If the Preparation and presentation of chemical snake did not flick its tongue for 60sec, the stimuli followed a well-established procedure trial was terminated. A new stimulus was used employed for testing chemical discrimination by for each snake. the vomeronasal organ in Squamata (Burghardt, The order of the presentation of the stimuli 1970; Cooper, 1998). Cotton swabs bearing was randomized and counterbalanced. To the chemical stimuli were presented to the make the blind test, the second author pre- snakes. The animals used for chemical stim- sented swabs to each snake without being uli represented a variety of taxa. They informed of the source of the chemicals on included earthworms (Oposthopora), slugs each swab. (Stylommatophora), fish (Cyprinidae, Caras- sius auratus; Adrianichthyidae, Oryzias lati- Results pes), frogs (Rhacophoridae, Rhacophorus v. There was considerable individual variation viridis; Ranidae, Rana narina), newts (Sala- in the responses to the chemicals: one snake mandridae, Cynops ensicauda), lizards (Oplu- flicked its tongue at least once for all chemi- ridae, Oplurus c. cuvieri; Scincidae, Eumeces cal stimuli, whereas another snake flicked its elegans), snakes (Colubridae, Elaphe quadriv- tongue to only three stimuli (two frog species irgata, Rhabdophis tigrinus), birds (Ploceidae, and Oplurus chemicals). However, the mean Lonchura striata), and mammals (Muridae, numbers of tongue flicks showed a variation baby and adult Mus musculus). All of these among the stimuli (Fig. 1). Snakes flicked animals except for O. c, cuvieri and M muscu- their tongues frequently to the chemicals of lus are not sympatric with L. madagascarien- frogs and reptiles and moderately to those of sis. Although it is ideal to use sympatric species birds and mammals. Only a few tongue flicks 42 Current Herpetol. 20(1) 2001

Chemical cues FIG, 1. Mean number of tongue flicks made by hatching Leioheterodon madagascariensis to cotton swabs bearing various chemical cues. Bars indicate 1SE. were observed to the chemicals of cologne, means, the food items utilized by this species in invertebrates, fish, and newts. The mean of nature. In several species of snakes, newborns tongue flicks to the distilled water was moder- are known to respond to prey chemicals not ately high (8.8), but this was apparently due to only with increased tongue flicking but also by a high response of one individual; if this indi- open-mouthed attack on the swab (Ford and vidual was excluded from the calculation, the Burghardt, 1993). The absence of attack in L. mean tongue flick to the distilled water dropped madagascariensis suggests that other stimuli, to 3.5. No snakes attacked the stimuli. such as visual ones, may be indispensable to elicit prey attack in this species (Ford and Discussion Burghardt, 1993). Available information on natural diets of L. madagascariensis suggests that this species is a ANTIPREDATOR RESPONSE TEST generalist feeder, eating frogs, lizards, birds, and mammals (Preston-Mafham, 1991; Mori and The aim of this experiment was to examine Randriamahazo, in press). Chemicals from antipredator responses of neonate L. madagas- these animals elicited moderate to high tongue cariensis to various threatening stimuli and flick responses. It is suggested, therefore, that characterize the antipredator behaviors of this naive hatchlings can recognize, by chemical species. MORI & TANAKA-BEHAVIOR OF SNAKES 43

Methods every three sec for a total of 20 times, with a To elicit antipredator responses of the snakes, long metal snake hook. On the tip of the we used standardized methods developed for hook, a 50×15mm polyproplylene plate was assessing levels of antipredator reactions of attached so that the snake was pinned down snakes (for non-tactile stimulus, Herzog and by the plate. Burghardt [1986] and Herzog et al. [1989]; for In the first two sessions, we recorded the tactile stimulus, Mori et al. [1996] and Mori occurrences of "strike", "bite", and "flight", and Burghardt [2000]). A snake was gently which are the main behavioral variables previ- removed from its home cage and introduced ously used in comparable studies. When the "strike" occurred into an arena (44×29×30cm) at an ambient tem- , its frequency was recorded as perature of 24-25℃. After leaving the snake well. Other characteristic behaviors observed, undisturbed for five minutes, the experimenter such as "body flattening" and "neck flattening" slowly brought a forefinger to within 1 to 2cm were also recorded. In the tactile stimulus ses- of the snake's snout and held it stationary for sion, behavior of the snake in response to each 60sec. This is referred to as a nonmoving stimulus was observed and recorded. All ses- stimulus session. If the snake crawled away sions were videotaped, and videotape analysis during the test, the experimenter followed it, was done to record the above variables. keeping the extended finger in front of the snake. Then the snake was left undisturbed for Results 60sec. The moving stimulus session began Only a single snake struck the nonmoving when the experimenter again extended the fore- stimulus (twice) and exhibited characteristic dis- finger to within 1 to 2cm of the snake's snout. plays such as body flattening, neck flattening, This time he moved the finger back and forth at head elevation, and jerk (see below). Other the rate of approximately three to four oscilla- snakes in the nonmoving stimulus session either tions per second throughout the 60sec period. showed no specific responses or simply fled As with the nonmoving stimulus session, the (two snakes each). Toward the moving stimu- experimenter kept the finger in front of the lus, two snakes exhibited no specific responses, snake. The snake was then given another 60sec and the other three showed a simple flight undisturbed period. Following this period, the response. tactile stimulus session, which lasted 60sec, In response to the tactile stimulus, one began. During this session the snake's body snake simply fled in response to all 20 stimuli. (excluding head and tail) was gently pinned The other four snakes exhibited dorsoventral

FIG. 2. Hatchling Leioheterodon madagascariensis exhibiting characteristic displays against artificial threatening stimuli. (a) Neck flattening accompanying slight head elevation and body flattening. (b) Neck flattening with prominent elevation and tilting of the anterior body so that the dorsal surface of the neck is directed toward the source of the stimulus. 44 Current Herpetol. 20(1) 2001 flattening of the neck (neck flattening) and/or prey-handling behavior according to prey size flattening of the body posterior to the neck (body and type: larger prey animals tend to be con- flattening; Fig. 2a), occasionally accompanied stricted to death, and then swallowed head first by lifting the head and neck region high above more frequently (Loop and Bailey, 1972; Mori, the substrate (head elevation). During head ele- 1991); mammalian prey tends to be constricted vation, the snake often tilted the neck so that its to death prior to swallowing more frequently dorsal surface was directed to the source of stim- than ectothermic animals such as frogs (Gregory ulus (Fig. 2b). From this posture, the snake fre- et al., 1980; Mori 1991); and certain prey ani- quently showed strikes with its mouth open in mals are always swallowed head first regardless response to the stimulus (strike), but actual bit- of their size (Voris et al., 1978; Mori 1998). The ing rarely occurred. In some cases, the snake degree of such behavioral flexibility is, to some irregularly formed circular or S-shaped loops extent, species-specific (Halloy and Burghardt, with its neck and body flattened, and wriggled 1990; Mori, 1996, 1997, 1998), and it has been violently and intermittently in response to the suggested that dietary specialists change their physical contact of the stimulus (jerk). Average behavior more efficiently than dietary general- frequencies of these responses for the four ists, especially when they are young (Drum- snakes were 18.25 (neck flattening), 16.75 (body mond,1983; Halloy and Burghardt, 1990; Mori, flattening), 9.0 (head elevation), 10.5 (strike), 1993, 1994, 1995, 1996). 3.75 (jerk), and 0.75 (flee). The third test was conducted to examine the effects of prey size and type on prey-handling Discussion behavior of the juvenile L. madagascariensis Body flattening and head elevation accompa- that had been fed only one type of prey. Possible nying neck flattening are both common anti- roles of Duvernoy's gland secretion in feeding predator displays in snakes (Greene, 1988). were also examined. Neck tilting during head elevation seems to be a characteristic display of L. madagascariensis. Methods Antipredator responses similar to jerk of L. Five types of prey animals were used: small madagascariensis are known in other colubrids mice (baby Mus musculus one to three days after (e.g., Rhabdophis tigrinus, Mori et al., 1996) and birth, 1.7-2.0g), large mice (juvenile M. muscu- members of other ophidian families such as the lus, 9.5-12.2g), small frogs (metamorphosed Elapidae (e.g., Maticora intestinalis, Mori and Hyla japonica, 0.3-0.6g), medium frogs (juve- Hikida, 1991). nile Rana nigromaculata, 1.8-2.3g), and large A suite of antipredator displays (neck flatten- frogs (adult R. nigromaculata, 12.0-18.9g). ing, head elevation, body flattening, and strike) Approximately one hour prior to the experiment, were apparently more easily elicited by physical water bowls, shelters, and paper floor coverings contact than by non-contact threatening stimuli. were removed from the cages, and the ceiling Similar results were observed in an Asian colu- was replaced with a transparent acrylic board. brid, Rhabdophis tigrinus (Mori et al., 1996). Each trial began by gently introducing a prey However, in the present test possible contribu- into the cage. Feeding behavior of the snakes tion of presentation order to the results can not was recorded with an 8mm video camera- be precluded because the tactile stimulus session recorder until the prey was completely swal- was always conducted after non-tactile stimulus lowed. If the snakes did not attack the prey sessions. within 20min, the trial was terminated. For the index of prey size, we used relative

PREY-HANDLING TEST prey width (i.e., prey head width/snake head width), because width is generally considered It has been demonstrated that as a conse- a better indicator of the prey size than length quence of behavioral adaptation, snakes change or mass when evaluating the prey-handling MORI & TANAKA-BEHAVIOR OF SNAKES 45 efficiency of gape-limited predators (Pough TABLE3. Relationships between the initial bite and Groves, 1983; Mori, 1998). The following position and the direction of prey ingestion by variables were recorded for each trial by ana- juvenile Leioheterodon madagascariensis. Numerals lyzing the videotapes. Bite position: the site indicate the numbers of prey animals. where the snake first seized the prey. Direction of prey ingestion: the prey was eventually swallowed "head first" or "hind legs (rump) first". Holding duration: time in sec from the initial seizure of the prey to the first "lateral jaw walking movements" by the snake in any direction. Manipulating duration: time in sec from the first lateral jaw walking movements to the commencement of swallowing. The 3). No apparent tendency for head first inges- commencement of swallowing was defined as tion was recognized even for large mice and the first jaw walking movements over the body frogs. In trials with small and medium sized of the prey in the direction in which the prey prey seven out of 14 were swallowed head first, was subsequently swallowed. Swallowing and three out of eight large prey were swal- duration: time in sec from the commencement lowed head first. Except for one large frog, all of swallowing to the moment at which the prey prey animals were swallowed alive. was no longer visible externally. Condition of Constricting behavior was observed only in prey at swallowing: prey that made any move- a single trial with a large mouse. Two seconds ments, including breathing, during swallowing after a snake seized the rump of a mouse, were considered "alive", otherwise "dead". Pat- inducing a vigorous struggling by the prey, the tern of constricting or coiling behavior during snake attempted to coil around the prey by typ- prey-handling was also recorded, whenever ical wrapping and winding movements (Green- observed. wald, 1978). However, the configuration of the coil was irregular and unstable, and the snake Results was not able to successfully coil around the One individual did not attempt to eat small prey. The prey continued to struggle, and the and large mice, and another did not eat a snake then tried to reconstrict the prey two large mouse. All individuals readily struck more times, eventually holding three neat coils and attempted to swallow the frogs regardless around the prey. However, the prey was not of their size. In all cases, snakes struck the killed by constriction and was swallowed alive prey immediately after the prey showed some and rump first. Large mice and frogs in the kind of movement (locomotion, head turn, other trials also struggled vigorously during the body adjustment, etc). Attempts were made to holding phase, but the snakes never attempted swallow two large frogs, but they were eventu- to constrict them. ally regurgitated probably because the snakes Holding duration was quite short, and were unable to engulf them completely due to snakes began lateral jaw walking movements their gape limitation (see below). soon after the initial seizure (holding dura- Irrespective of prey type, the direction of tion, x=2sec, range=0 to 9). In all but one trial ingestion seemed to depend on the initial bite with small and medium sized frogs snakes position: prey animals were swallowed head began to swallow without manipulation phase. first when the bite position was located on the Manipulating duration was also short for small anterior part of the body including the head, mice (x=8.3sec, range=2 to 23) and varied and they were swallowed hind legs first when from 0 to 492sec for large frogs and mice the bite position was located on the posterior (x=147sec). Swallowing duration considerably part of the body including the hind legs (Table increased when relative prey width exceeded 0.8 46 Current Herpetol. 20(1) 2001

Relative prey width FIG. 3. Relationship between relative prey width (prey head width/snake head width) and swallowing duration in feeding trials of juvenile Leioheterodon madagascariensis. Direction of prey ingestion (head first or hind leg [or rump] first) is also shown.

(Fig. 3). For prey animals with relative prey gitation, flicked their tongues toward the frogs width<0.8, direction of ingestion did not seem frequently, but they never tried to swallow the to affect the swallowing duration. For larger regurgitated frogs (one dead and one alive) prey (relative prey width>0.8), however, head again. The live frog eventually died approxi- first ingestion was likely to enable the snakes mately 4 hours after regurgitation. Extensive to swallow prey quicker than hind leg first bleeding during the swallowing phase was ingestion. In fact, two snakes that tried to observed in three trials with large frogs. swallow large frogs (relative prey width=1.33 and 1.30) hind leg first eventually abandoned Discussion the swallowing attempts after 42.4-min and Virtually no effects of prey size and type on 79.3-min, respectively: the snakes engulfed the prey-handling behavior were detected in the frogs over their pectoral girdles but not their juvenile L, madagascariensis. Adaptive func- forelegs, and voluntarily regurgitated the frogs. tion of head first ingestion of (large) prey has In both cases the snakes initially began to swal- been considered to reduce swallowing dura- low the frog from one of the hind legs letting tion by minimizing the resistance caused by the other stretch far anteriorly so that the tip the prey's appendages (Diefenbach and Emslie, of the latter leg reached anterior to the snout 1971; Mori, 1991). Direction of prey inges- of the frog while swallowing. The snakes, left tion in L. madagascariensis seems to basi- undisturbed for additional 10min after regur- cally depend on initial bite position. As a MORI & TANAKA-BEHAVIOR OF SNAKES 47

result, swallowing duration was prolonged basis of our definition, it is highly likely that when large prey was ingested hind leg first, the frog was still alive when the swallowing and in the extreme cases, prey animals were process was initiated because its body did not eventually regurgitated after a prolonged swal- seem to lose tension throughout the process. lowing attempt. Thus, virtually no prey would have been Selective advantage of constriction has been killed before the swallowing phase. How- considered to prevent prey from retaliating or ever, the eventual death of the regurgitated to reduce total feeding duration by killing or frogs suggests that Duvernoy's secretion was restraining the prey (Loop and Bailey, 1972; delivered during prey-handling. These de Queiroz, 1984; Mori, 1991). In the present results suggest that Duvernoy's secretion of observations, except for a single large mouse, L. madagascariensis is insufficient to bring all prey were simply swallowed without any about rapid death of prey, but may be effec- constricting attempt even though most of the tive to incapacitate large prey when feeding large frogs and mice struggled vigorously dur- duration is prolonged. Obviously L, mada- ing the handling phase. The single case of gascariensis offers an additional example of neat coiling indicates that L. madagascarien- snakes with both well-developed Duver- sis is potentially capable of constriction from noy's glands and potential for prey constric- the viewpoint of morphological body plan, tion during feeding (Shine, 1985; Rochelle either to kill or simply restrain the prey. The and Kardong, 1993; Mori, 1998). ability of efficient constriction in L, madagascariensis may develop ontogenetically as CONCLUSION in other generalist semi-constrictors such as Elaphe quadrivirgata (Mori, 1994, 1996). Our results showed that L. madagascarien- The functional roles of Duvernoy's glands sis is an ideal species for studies on various during feeding have been disputed and tested aspects of snake behavior. This snake is a in several colubrid snakes (Kardong, 1982; dietary generalist, responds to chemical stim- Hayes et al., 1993; Rodriguez-Robles, 1994). uli from various types of natural prey, has a After the initial seizure of prey, some snakes rich repertoire of distinct antipredator dis- hold it with the jaws for a while presumably plays, and possesses two representative prey until the glands' secretion takes effect (Broad- subduing mechanisms of snakes (i. e., con- ley, 1983; Jayne et al., 1988; Mori, 1998), and striction and venom injection). Apparently other snakes repeatedly open and close the jaws inefficient prey-handling by the juvenile without shifting the position of bite (forceful snakes suggests that this species is a good chewing) probably to inject more secretion subject to study the ontogenetic development (Jansen and Foehring,1983; Rodriguez-Robles, of prey-handling behavior as a representative 1992; Thomas and Leal, 1993). In some cases, of generalist feeders (see Mori, 1996). Fur- prey animals are killed during handling (Jayne ther examination of these behavioral proper- et al., 1988; Mori, 1997), whereas in other ties with greater sample size, coupled with cases they are only weakened and incapaci- comparisons involving snakes from other tated (Mori, 1998). Some prey animals are regions of the world, might shed light on the swallowed alive without any sign of envenom- unique features of the behavioral evolution in ation (Mori, 1997) or killed by constriction Malagasy snakes, as well as on the ubiqui- without any apparent assistance of the secre- tous behavioral patterns in snakes. tion (Rochelle and Kardong, 1993). In L. madagascariensis initial holding dura- ACKNOWLEDGMENTS tion was quite short, and no chewing-like behavior was observed. Although a single We thank S. Yamagishi for giving us an frog was recorded as "swallowed dead" on the opportunity to conduct this study and the 48 Current Herpetol. 20(1) 2001 staff of Parc Botanique et Zoologique de par Madagascarophis (Colubridae opisthoglyphe). Tsimbazaza for their assistance with the field Arch. Inst. Pasteur Madagascar, 56(1): 299-311. study. M. Toda, R. Yamamoto, J. Motokawa, DOMERGUE,C. A. ANDJ. RICHAUD.1971. Activite hemolytique des secretions des glandes de Duver- H. 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