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DEATH FEIGNING BEHAVIOR IN THREE COLUBRID SPECIES OF TROPICAL ASIA

Russian Journal of Herpetology
Vol. 17, No. 1, 2010, pp. 15 – 21
Gernot Vogel(1) and Hans Kam Han-Yuen(2)
(1) Im Sand 3, D-69115 Heidelberg, Germany; E-mail: Questo indirizzo e-mail è protetto dallo spam bot. Abilita Javascript per vederlo.
(2) 07-67&68, 7th Floor, Berjaya Times Square, Jalan Imbi, 55100 Kuala Lumpur, Malaysia; E-mail: Questo indirizzo e-mail è protetto dallo spam bot. Abilita Javascript per vederlo.

 

Submited October 1, 2008.
Death feigning was reported for the first time for the species Coleognathus radiatus and Macrocalamus chanardi.
In Xenochrophis piscator this behavior is reported for the second time since 1947. These are the first reports on death feigning in snakes for the Indochinese and Malayan subregions.
Keywords: death feigning, Coelognathus radiatus, Macrocalamus chanardi, Xenochrophis piscator, Oriental region.

 

Death feigning, or thanatosis, is a form of defense behavior, in which an animal becomes immobile as if dead (McFarland, 1981). It is shared by mammals (e.g., Francq, 1969), birds (e.g., Sargeant and Eberhardt 1975), fishes (e.g., Howe, 1991), reptiles (e.g., Gehlbach, 1970), amphibians (e.g., Sazima, 1974; McCallum, 1999), mites (e.g., Ebermann, 1991), and insects (e.g., Fabre, 1900; Miyatake et al., 2008).

Death feigning is a behavior that has long been known in some snake species. Until now, it has been observed in the following genera:
Coluber (Lynch, 1978), Diadophis, Farancia, HemachatusHeterodon, Lampropeltis (Tryon and Guese, 1984), Leptomicrurus (L. dulcis and L. scutifrons only [Visser, 1966]), Lystrophis (Shaw and Campbell, 1974), Masticophis (Smith, 1975; Tucker, 1989; Pflanz and Powell, 1990), Micrurus (M. fulvius only), Naja (Naja haje [Dickinson, 1948], N. nigricollis [Ionides, 1952]), Natrix (e.g., Ushakov, 2007, Fig. 1) Rhabdophis (R. tigrinus [Mutoh, 1983]), Sonora, Storeria (Jordan, 1970; Liner, 1977), Virginia (Thomas and Hendricks, 1976), and Xenochrophis (MacDonald, 1947).

In some genera, only a sole species demonstrates this behavior, while in Diadophis punctatus, it is known only from some subspecies. Mori and Burghardt (2007) tested the anti-predator behavior of 27 species of natricine snakes, but death feigning was observed only in one of them.

There seems to be several different types of death feigning. Some species roll over before remaining rigid (Jordan, 1970; Thomas and Hendricks, 1976); some do not stay rigid at all and remain limp during the display (e.g., Tryon and Guese, 1984; Mutoh, 1983). A few species turn on their backs while playing dead (e.g., Doody et al., 1996), while others do not (e.g., Dickinson, 1948), and some open the mouth (e.g., Jordan, 1970; Mori and Burghardt, 2008), but other species keep the mouth shut (e.g., Mutoh, 1983; Doody et al., 1996). Some species show specific behavior while death feigning; for example, “neck bowing” in Rhabdophis tigrinus (Mutoh, 1983), which was observed in some localities in Japan.
However, death feigning was not noted in other species of the genus Rhabdophis, which occurs in the Indo-Malayan region.

MATERIAL AND METHODS

Observations were made on free-living snakes at five different localities by four different observers.
Specimens were collected for the purpose of being photographed, after which they were released. Notes on the behavior were made shortly after the events to ensure accurate descriptions of the circumstances and observations. In the case of Macrocalamus (case 4) no notes were made.

Death feigning by Natrix natrix
Fig. 1. Death feigning by Natrix natrix. Photograph by Petr Vlèek.

RESULTS

Case 1 (Fig. 2)

On the 18th of April 2007, an adult specimen of Coelognathus radiatus was collected 10 km N of Umphang, Tak Province, Thailand by Gernot Vogel. The snake was lying on the road, a short time after darkness at ~7.00 p.m.

It was placed in a bag — so that it could be photographed at a later stage. The next evening, the snake was removed to be photographed. At first, it displayed the normal behavior for this species; raising the forepart of the body, opening the mouth and making S-shaped curves with the body. In this manner, it was moving forward, while fiercely striking. The snake was held by itstail, and due to problems with the camera, the photo session lasted several minutes. Suddenly, the snake changed its behavior and laid down motionless on its back with the mouth slightly opened. At first, it gave the impression that it was dying due to stress or heatexhaustion. It was possible to move the snake in any way now and it stayed limp, even when we wanted to bring it back to a natural position to photograph it, it returned to a position with the ventral part turned upwards.

Death feigning by Coelognathus radiatus
Fig. 2. Death feigning by Coelognathus radiatus, Tak Province Thailand.

After photographing this position, the animal was left alone to see how long this behavior would last. The animal was obviously observing its surroundings by moving the head in a position to do so. When it noticed movements, the head went back to its previous position. After some time, the snake was placed back into its bag. Due to the problems with the camera, another photo session was held the next day, during which it was found that the snake was in perfect health. Interestingly, it showed exactly the same behavior again, and after several minutes of attacking and hissing, it feigned death in the same manner described earlier. After the second photographic session, the snake was released back into the wild.

Case 2

On the 18th of August 2007, an adult specimen of Coelognathus radiatus was collected from Grik (also called “Gerik”) in Perak State, Peninsular Malaysia, and was obtained from a local snake-catcher. Hence, the exact time of capture is unknown.

The specimen was kept in a bag to also be photographed at a later stage. When it was examined at ~11.30 a.m. the next day by Hans Kam Han-Yuen, the snake assumed a defensive S-shaped posture, along with hissing, when it was released from the bag, but was pinned down with a snake-hook at the base of the neck, and was then held with a firm grip behind the head. It was found that it was in the late stages of sloughing, and hence, manual removal of the dead skin was conducted by scrubbing and rinsing it under running water from a tap.

After the dead skin was removed, the specimen was brought to a table to be photographed, when it suddenly went limp in the author’s hands. Thinking that it had died from the stress of being handled, the specimen was placed on the table, where it remained in the same position, with the head turned sideways towards the ground with no movement and a “lifeless” appearance. While the author was preparing his camera, the specimen suddenly revived ~10 sec later, and began to move slowly across the table, with its tongue flickering.

The specimen was quickly restrained again by the author, with his hands, when the snake suddenly went limp again. The author then experimented with it, by placing it back on the table, and positioning it into various postures. All this time, the snake remained limp and devoid of any movement or flickering of the tongue despite the continuous handling. Each time, when positioned and left alone, the snake revived after 10 – 20 sec, raising its head from the sideways position into a normal position, flicker its tongue, and then move slowly off the table. The author remained relatively still while observing the snake each time in its “death” pose, acting only when the snake attempted to escape.

The experiment was conducted about eight times, during which the specimen never resumed its typical defense S-shaped posture, and instead attempted to play “dead” each time. It was then kept in a box, and taken out at ~8 p.m., where the author conducted the experiment again. However, the snake did not repeat this behavior anymore despite the author’s attempts to handle it considerably, and the snake remained in an aggressive posture throughout the session. The snake was released the next day.

Case 3 (Fig. 3)

On the 3rd of February 2008, an adult specimen Coelognathus radiatus was collected by Hans Kam Han-Yuen from a densely populated residential area in Kuala Lumpur at ~3.00 p.m.. Some snake species in Malaysia have adapted to an urban environment (due to the surrounding urban development encroaching on their former habitats) and can be found thriving in small or fragmented secondary forests, just a few hectares in size, within modern urban landscapes. In this case, the adult snake was caught by workers from a construction site in a housing estate that faced a small patch of secondary forest, and brought the snake to the author in a sealed bag. The author then released the snake in a garden to be photographed, where it displayed the same behavior observed in the C. radiatus specimen collected from Grik, approximately 300 km north from Kuala Lumpur. However, there was one slight difference in the death-feigning behavior of this individual; the snake demonstrated this behavior for a shorter period when handled roughly, before attempting to slither away. Otherwise, the snake continued to feign dead when touched or grabbed. After observing this behavior for several minutes, and recording it on camera, the snake was bagged and then released in a primary rainforest near Kuala Lumpur the next day.

Death feigning by Coelognathus radiatus
Fig. 3. Death feigning by Coelognathus radiatus, Grik, Perak State, Peninsular Malaysia.

Case 4 (Figs. 4 – 5)

An adult specimen of the species Macrocalamus chanardi was dug out of the soil of a garden in the Cameron Highlands, at an elevation of 1520 m. It was found about 15 cm deep below the loose soil. The temperature was between 18 and 22°C. It was feigning dead in making itself stiff and stopping all its movements. The exact circumstances were not noted, so it is not possible to say, if the belly was turned upside down.

The same behavior in this species was observed by one of the authors (HK), but again no notes were taken.

Death feigning by Macrocalamus chanardi
Fig. 4. Death feigning by Macrocalamus chanardi, Cameron Highlands, West-Malaysia, photograph by Allan Teo.

Macrocalamus chanardi
Fig. 5. Macrocalamus chanardi, same specimen, Cameron Highlands, West-Malaysia, photograph by Allan Teo.

Case 5 by Soham Mukherjee
(Team leader of “Snake Helpline Clubs, Orissa”)

On the 1st of May 2007, a call came in for a displaced snake from Sola crossing in Ahmedabad City, Gujarat Province, India. The snake was hiding under a pile of stones, and was identified as a Xenochrophis piscator with a total length of 140 cm. While we were returning to the rescue center, we were called back for more snakes. One by one, 13 hatchlings were caught. The clutch of hatched eggs was also discovered, and everything was collected from the same pile of stones. 75 eggs were counted, of which 5 were “failed” eggs, showing a high hatching success rate. It can be assumed that the female (it was later sexed in the rescue center) was the “mother” and was guarding the eggs. The hatchlings were a day old, as the eggs had not yet dried out fully. And we assume that as the hatchlings started to immerge, the mother must have also done so.

In the evening, the neonates and the mother were taken outside to be photographed. As soon as the female X. piscator was taken out of the bag, it was acting aggressive and snapped a couple of times. After about 2 min of struggling it started to ignore the handling and slowly was loosing grip. The muscle tone was going down and so were its reflexes. Then it was just hanging like a dead snake while still kept in the hands. It was still watching the handler as could see her eyes following the handler. The tongue was partially out and had stopped flickering. It was kept on the ground and stayed in the same position for a minute. It started tongue-flicking again and slowly started acting normal.

After handling again, it showed the same reaction for a second time. And after handling was continued for about one minute it turned its belly upside and the whole body was more or less in a “twisted” position with most of the belly exposed. Now the mouth was also partially open and the tongue was still sticking out. Lastly it released a very foul smelling odor from the anal opening. At this point of time there was no movement at all by the snake. Even the eyes had stopped following. The first movement after all this was after a gap of 5 – 6 min. It slowly started tongue-flicking, started looking around for any possible predators, and then slowly regained its normal body position. It stayed there for a minute and then started crawling away.

DISCUSSION

Most of the species that display death feigning are living in the Nearctic Realm: Coluber constrictorDiadophis punctatus, Farancia abacura, Heterodon sp., Lampropeltis alterna, Leptomicrurus dulcis, Masticophis flagellum, Micrurus fulvius, Sonora episcopa, Storeria occipitomaculata, and Virginia striatula. A few live in the Palearctic [Natrix natrix (Fig. 1), Rhabdophis tigrinus] or Afrotropical (Hemachatus haemachatusLeptomicrurus scutifrons, Naja haje, Naja nigricollis) regions. In our literature search, we only found one report of death feigning in the Neotropics (Lystrophis), one in Indo-Malayan snakes, and none in the Australasian region.

For the Indo-Malayan region, the only report of death feigning concerns Xenochrophis piscator (McDonald, 1947). In this old report, McDonald made the following notes on the behavior of several Xenochrophis piscator individuals after confronting them with a mongoose:
«This is done by the snake sometimes standing up and striking at the mongoose three or four times after which it sinks to the ground and in slow motion, turns over on to its back maintaining a slow muscular movement similar to a snake with its head beaten in. The mongoose as often as not will leave the snake without biting or harming it in any way. When danger seems past, the snake makes a hasty retreat only to repeat the “shamming” when the mongoose arrives. This is no exception but the rule in this species and need only be tried out for proof.»

Obviously these snakes all came from the vicinity of Mumbai, so the determination seems to be still correct (Vogel and David, 2006). However our observations are the first for the Indochinese and Malayian sub-regions and the first for the genera Coelognathus and Macrocalamus.

Most genera in which this behavior was observed are native to the Nearctics. Thus, the question arises whether this phenomenon is more widespread in reptiles than currently known. Therefore, the observations made especially in these areas were due to the fact that the snakes of these areas were simply better known.

Obviously, this behavior is commonly displayed only in three genera: Heterodon, Natrix, and Hemachatus. For Natrix natrix, it was recorded that 32 specimens out of 92 exhibited this behavior (Ushakov, 2007). In Virgulata striulata, only 2 out of 200 handled specimens showed death feigning (Thomas and Hendricks, 1976), in Masticophis flagellum, 6 out of 41, in Diadophis punctatus, 3 out of 21, and in Micrurus fulvius, 2 out of 6 exhibited this behavior (Gehlbach, 1970). From other genera, there are only a few observations and it is likely that these are rare actions from individuals.

It is remarkable then, that both authors observed this behavior independently for the species Coelognathus radiatus in individuals from different countries in three different cases. Furthermore, this behavior was repeated by one specimen, when the circumstances were replicated a day later. We have no explanation why there are no reports about death feigning in this species, as this species is commonly used in snake exhibits and among reptile keepers. However, it could be expected, since the circumstances in these shows are similar to those in the situations as follows. A possible explanation might be that this behavior is lost in captivity (Dickinson 1948; Tryon and Guese, 1984). Greene (1988) reports on the loss of this behavior in captivity among certain species of the same genus. In the same study, it was shown that the ease in which death feigning could be induced varies from specimen to specimen for Heterodon platirhinos. Doody et al (1996) also showed that it might be difficult to induce death feigning and for adult Farancia abacura, the stress level must be extremely high, much higher than that induced by handling by a human being. But this is not the only explanation, since for Heterodon platirhinos the opposite was shown: an increase of death feigning behavior during captivity (MacDonald, 1974). Clearly, to achieve a better understanding of the defensive strategies of Coelognathus radiatus, more empirical research about the behavior of this animal, as well as its natural enemies are required.

Macrocalamus chanardi is a species rarely encountered, so this might serve as an explanation for the fact that death feigning was not reported for this species before.

There is no explanation, that there is only one very old case reported for Xenochrophis piscator, as this is one of the most common snake species in India. Specimens from Thailand or Tamil Nadu (South India) did not show this behavior (personal observation). It might be coincidence, but both observations by (MacDonald [1947] and our own observation) were made in neighboring provinces of Western India.

CONCLUSION

Death feigning is a phenomenon in snakes that seems to be widely neglected in documentation. It is not really known which species show this behavior, and in which way. Nor have the different kind of death feigning “stages” been compared among species. It is our opinion, that there must surely be many more snake species that demonstrate death feigning behavior than what is presently known, and we encourage researchers to report such observations.

Acknowledgments. The authors wish to thank Patrick David and André Koch as well as Gerrut Norval for reviewing the manuscript. Also, to Allan Teo, Petr Vlèek, and Soham Mukherjee we would like to express our appreciation for their observation contributions and for making their photographs available to us.

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