First Record of Male Combat in a Wild Malayan Pit Viper（Calloselasma rhodostoma）

Colin T. STRINE， Curt BARNES， Inês SILVA， Bartosz NADOLSKI， Taksin ARTCHAWAKOM， Jacques G. HILLand Pongthep SUWANWAREE*

1Suranaree University of Technology， Nakhon Ratchasima， Thailand

2Sakaerat Environmental Research Station， Nakhon Ratchasima， Thailand

3Department of Biological Science， University of Arkansas， Fayetteville， AR， USA

First Record of Male Combat in a Wild Malayan Pit Viper（Calloselasma rhodostoma）

Colin T. STRINE1， Curt BARNES1， Inês SILVA2， Bartosz NADOLSKI1， Taksin ARTCHAWAKOM2， Jacques G. HILL3and Pongthep SUWANWAREE1*

1Suranaree University of Technology， Nakhon Ratchasima， Thailand

2Sakaerat Environmental Research Station， Nakhon Ratchasima， Thailand

3Department of Biological Science， University of Arkansas， Fayetteville， AR， USA

Thefi rst record of ritualized combat behavior between two male Calloselasma rhodostoma （Malayan Pit Viper） was observed in Sakaerat Biosphere Reserve， Nakhon Ratchasima， Thailand. Although most of the behavior of C. rhodostoma was similar to that recorded for other viperids， an instance of submissive behavior， which to our knowledge， has not been recorded in any snake species. Additional fi eld observations are required to better understand the structure and function of combat behavior in C. rhodostoma.

Calloselasma rhodostoma， Ritualized combat， Sakaerat， Southeast Asia

Our observation occurred at the Sakaerat Environmental Research Station （SERS）， Nakhon Ratchasima Province， Thailand （14.4933°S， 101.9219°W，datum： WGS84， elev. = 470 m）. The protected area is approximately 82 km2， ranges in elevation from 250-762 m， and is characterized by a patchy network of two main forest types： Dry Dipterocarp Forest （DDF； 18%） and Dry Evergreen Forest （DEF； ＞ 60%）. All the remaining area consists of Bamboo fragments and sparse grasslands except for the 1% of the area consisting of the station headquarters， which contain staff offices and student dormitories. We got research permission from SERS and this study was approved by Suranaree University of Technology Ethics committee.

We discovered two male C. rhodostoma intertwined and combating on 14 May 2014 at 1945 h， and we observed the interaction for several minutes. An adult femaleC. rhodostoma was approximately 0.25 m away from the combating snakes， but we did not see the femaleafter the two males separated. The combat occurred near the station headquarters in a mixed deciduous forest edge habitat. Dense ground cover at the site was composed of leaf litter and low-lying mixed vegetation ＜ 15 cm high. We observed and photographed the event from a distance of 3-4 m， to avoid disturbing the snakes. During the observation， cloud cover was 60% and the moon was full.

At the start of the combat， both males raised the midanterior portions of their bodies， then intertwined or remained parallel to one another. The snakes rapidly extended their anterior bodies， aligned their heads parallel to each other （Figure 1）， and twisted their bodies so that their heads were facing in opposite directions. Periods between elevated physical contact were characterized by the two males moving along the ground parallel to one another， while in close or direct contact. We also observed head pinning behavior several times （Figure 2）. The snakes rose over 30% of the anterior body on several occasions， with each male attempting to gain a higher position of control than the other

We observed a “slamming behavior” characterized by both snakes raising their heads several centimeters above the ground， followed by thrusting their heads downward in an effort to push down the opposing male. The snakes then quickly raised the first 10 cm of their bodies. The interaction ended with both snakes twisting and thrashing through the low vegetation.

We observed no bites during the ritual， and both individuals seemed oblivious to human observers and their surroundings. The combatants wrestled through the vegetation and briefly over a small metal pipe. The combat behaviors we observed were similar to other viperid species and consistent with male-male combat observed in captive C. rhodostoma （York， 1984）. However， after the combat ritual concluded， but before the two individuals separated， we observed one male exposing his ventral scales in what appeared to be a submissive posture （Figure 3）. We were unable to identify which of the two snakes lost the bout， because their patterning was nearly identical.

We captured the two snakes after completion of combat at 2015 h. While attempting to capture the first male， we discovered the large adult female 0.25 m away beneath the leaf litter. We had previously marked and captured the female on 23 April 2013 at 2130 h， while copulating with another male， and within 10 m of our combat observation. When fi rst captured， the female was 510 mm snout-to-vent length （SVL）， and her mass was 79.4 g. The two males involved in the combat ritual （SVL = 534 mm， mass = 81.8 g； SVL = 474 mm， mass = 120 g）were similar in body size to the male found copulating with the female in 2013 （SVL = 492 mm， mass = 86.1 g）. However， the competing males differed in size； the second male was 60 mm shorter， and 38.4 g heavier than the first， indicating that body size may have influenced the outcome of the combat. Although there was a clear winner of the interaction， we were unable to identify which individual was the victor due to the similarity in patterning.

On the second capture， the female had a bolus running through the fore， mid， and hind-gut， and she voluntarily expelled a large fecal sample with mammal hairs present. We also noted an increase of 154 mm SVL and 207.6 g since the previous year， for a total of 674 mm SVL and 287 g. We palpated the female during processing， and we detected enlarged ova， indicating that she may have been ovulating. The female was likely receptive to mating，which may have induced the male combat we observed. Although our observations suggest the possibility of a female mating with multiple males， there are no records of multiple mating in wild or captive individuals of this species.

Our data indicate that mating in C. rhodostoma at SERS occurs in May， which coincides with the beginning of the first rainy season. Hill et al. （2006） observed nesting behavior of a single female Malayan Pitviper at SERS and reported that oviposition occurred in mid-August. The timing of the combat ritual observed in this study fits the timing of the nesting behavior observed by Hill et al. （2006）. If mating occurs in May， then that would allow several months for development of eggs to occur before ovipostion in August. Previous captive studies support our observations that the breeding season occurs in May （Chanhome et al.， 2011； York，1984） ，however extrapolating captive studies to wild populations should be cautioned. Thus we suggest here，thatC.rhodostoma in Thailand mate and compete in May，although further observation is needed to confirm the timing of reproductive behavior across the range.

Thefi nal stage of combat recorded in our observation，ventral body presentation by one of the males， has not been recorded in C. rhodostoma， or other vipers， and requires further investigation. To our knowledge， no other snake species displays similar submissive behavior upon losing a combat bout.

Observations of combat from other parts of the range ofC. rhodostoma would also improve our understanding of this behavior， particularly to confirm whether or not combat behavior occurs with the same time frame across the species range. In addition， genetic data， paired with behavioral observations during mating， would better clarify the role of male combat in the context of sexual selection in wild C. rhodostoma.

Chanhome L.， Cox M. J.， Vasaruchapong T.， Chaiyabutr N.，Sitprija V. 2011. Characterization of venomous snakes of Thailand. Asian Biomed， 5： 311-328

Hill J. G.， Chanhome L.， Artchawakom T.， Thirakhupt K.， Voris H. K. 2006. Nest attendance by a female Malayan pit viper（Calloselasma rhodostoma） in northeast Thailand. Nat His J Chula Uni， 6（2）： 57-66

Shine R. G. 1994. Sexual size dimorphism in snakes revisited. Copeia， 1994： 326-346

York D. S. 1984. The combat ritual of the Malayan Pit Viper（Calloselasma rhodostoma）. Copeia， 1984： 770-772

Dr. Pongthep SUWANWAREE， from Suranaree University of Technology， Nakhon Ratchasima， Thailand， with his research focusing on environmental quality， invasive species and wildlife ecology in Lao and Thailand.

E-mail： pongthep@sut.ac.th

6 July 2014 Accepted： 25 November 2014 responsible for the greatest number of snakebites in Thailand. Nevertheless， studies of wild C. rhodostoma are few， and little is known about the species' ecology and breeding biology. Male-male combat has only been described in captive C. rhodostoma （York， 1984）. Here，we record the first observation of male-male combat behavior in wild C. rhodostoma.

Male-male combat behavior occurs in over 120 snake species from four families （Boidae， Colubridae， Elapidae and Viperidae； Shine， 1994）. Reproductive success presumably depends on the males' combat ability because they are competing for access to females； this correlation is has been understudied in tropical snake species. Although ritualized male combat is well-documented in pit viper species where males reach larger body sizes than females， combat has rarely been reported for species in which the female is generally larger （Shine， 1994）， as is the case with C. rhodostoma （Malayan Pit Viper）.

Calloselasma rhodostoma is en demic to Southeast Asia and is one of the few pit vipers that exhibit femalebiased sexual size dimorphism （Chanhome et al.， 2011）. In Sakaerat， C.rhodostoma exhibit nest attendance and defend their clutch by coiling around the eggs through gestation （Hill et al.， 2006）. The distribution of C. rhodostoma includes much of Indochina （Thailand，Malaysia， Lao， Cambodia， Vietnam， Singapore） and Indonesia （Chanhome et al.， 2011）， and is the species