Table Of ContentTropical Natural History 20(1): 95-103, April 2020
2020 by Chulalongkorn University
Short Note
Social Behavior Displayed by the Green Pit Viper Trimeresurus
(Cryptelytrops) macrops
CURT H. BARNES1*, WILLIAM FARREN2, COLIN T. STRINE1 AND
PONGTHEP SUWANWAREE1
1Suranaree University of Technology, Nakhon Ratchasima, THAILAND
2Sakaerat Conservation and Snake Education Team, Sakaerat Environmental Research Station, Nakhon
Ratchasima, THAILAND
* Corresponding Author: Curt H. Barnes ([email protected])
Received: 18 March 2019; Accepted: 11 November 2019
Study of behavior and sociality has sidewinder (C. cerastes) rattlesnakes to
historically been well-represented in non- evaluate social behavior (summarized5,10).
squamate amniotic organisms1-3. Such study Investigation of viper behavior in the tropics
with squamates (lizards, snakes, and has progressed little past spatial ecology.
amphisbaenians) is still in the infancy stage Arboreal vipers are among the least studied
however, especially regarding snakes4,5. snakes because of limiting factors such as
While more complex and visible social body size and challenging habitats11. Recent
systems may be observed for mammals and study of green pit vipers (Trimeresurus
birds, understanding of seemingly simpler spp.) suggests moderate home range overlap
behavior and sociality displayed by snakes between conspecific females, as well as
may provide valuable insight from which interspecies overlap in males12.
complexity may be derived5. Behaviors related to sexual activity, such
Reliable and comprehensive knowledge as male combat, courtship, and mating, are
is essential if behavioral ecology is to serve considered as evidence of social systems13.
as an effective conservation tool6. Snakes also interact and aggregate with
Contesting the traditional perception that the conspecifics for reasons other than
snake clade completely lacks complex and procreation-even before they are born-
noteworthy social behavior has been a aggregations of gravid females in several
considerable challenge7,8. Viper home rattlesnake species, a form of parental care
ranges in temperate regions frequently (> 50 species of > 30 genera), and
overlap with conspecifics and limited cooperative hunting in sea snakes, all
interactions between species were evidence snakes are an overlooked source of
infrequently reported until fairly recently9. social behavior8.
To date, most behavioral and social study of We present observations of social
wild snakes has been conducted with interactions of wild adult big-eyed pit vipers
temperate climate vipers, particularly (Trimeresurus (Cryptelytrops) macrops14) at
rattlesnakes. Camera technology has ambush sites within the Sakaerat Biosphere
recently been utilized with considerable Reserve (SBR) in northeast Thailand. Like
success on red diamond (Crotalus ruber), most other green pit vipers, T. macrops
northern pacific (C. oreganus), timber (C. exhibits profound sexual dimorphism both
horridus), Arizona black (C. cerberus), and in size and coloration15. Male T. macrops
TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 96
display a vibrant white “racing stripe” male (SVL = 424 mm, mass = 24.2 g, Table
(postocular stripe) above each eye, which 1) at the transition zone study site in our
females lack, and could play a role in investigation.
signaling of body condition. Females are Field videography: We set Bushnell trail
significantly larger morphologically, not cameras Model X-8 (model #119327, f/3,
only in body mass and snout-vent length but exposure time 1/20 sec, ISO 100, 35mm
also in head width and length. focal length, infrared night capability) and
Study site and animals: Our observations Trophy Cam (model #119636C, f/2.8,
were part of a larger project looking at green exposure time 1/20 sec, ISO 100, 35mm
pit viper behavior, spatial ecology, and focal length, infrared night capability)
habitat selection within the Sakaerat approximately 1-3 m from focal adult green
Biosphere Reserve in northeast Thailand. At pit vipers after a minimum 2 week recovery
our sites, we opportunistically captured period from latest capture (Fig. 1). The
vipers during visual searches after dark and camera interval was one minute with one or
then recorded morphometrics (snout-vent three consecutive photographs taken each
length [SVL] and body mass) the following minute. Care was taken when placing
day with an acrylic tube and isoflurane cameras not to disturb vipers or
anesthesia described by Wilkinson (2014)16. considerably alter natural behavior and
We sexed each individual under anesthesia. habitat, and we did not use recordings in
We gently palpated for the presence of which vipers abandoned ambush or resting
vitellogenic follicles and embryos under sites within an hour of setting cameras for
anesthesia, if present we considered them to analyses.
be “gravid” and if not then “not gravid.” Ethology: We specifically looked at
Radio transmitters (1.8 g, Holohil BD-2T interactions between focal T. macrops and
and BD2-THX) were implanted in adult pit conspecifics which occurred on the cameras
vipers deemed large enough and in good while pit vipers were ambushing. We
condition (transmitter < 5% of body mass) defined ambush behavior as stationary
following 17,18. foraging, coiled with the head set in a ready-
We radiotracked one adult female T. to- strike position19. We defined interactions
macrops in the core zone of SBR and two as direct if a viper came within half of a
adult females in the transitional zone. All body length (or closer) to another viper, and
three females were gravid during transmitter indirect if further but still visible on camera.
implantation (n = 3, median SVL = 580 mm, Outcome of interactions were defined as
range = 514 - 612; mass = 91.3 g, range = neutral, distracting, or agonistic. We classed
52.5 - 109, Table 1). Big- eyed pit vipers interactions as neutral when the focal viper
exhibit profound sexual dimorphism did not appear to be aware of or did not
(females being larger than males), with adult acknowledge a conspecific. The interaction
males in our study area at mean mass was distracting when the focal viper
precariously close to the 5% body mass appeared aware of or acknowledged a
cutoff for transmitter implantation (they are conspecific, but no subsequent responses
too small to ethically implant)15. To safely were evident. Agonistic outcomes included
observe sex differences without unethically active responses, requiring subsequent
implanting adult male vipers which were too movement, of a focal viper to a conspecific.
small, we included an adult non-tracked
97 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER
FIGURE 1. Bushnell trail camera set to observe an ambushing big-eyed pit viper (Trimeresurus
(Cryptelytrops) macrops).
We report median values for duration and minutes, for a median number of 2 bouts per
occurrence of interactions. individual (Table 1). All interactions
This research found that, in total, we occurred between early evening and early
opportunistically set cameras (mean 8556.5 morning time (19:20 - 05:21) from late
minutes per individual, n = 4, Table 1) on November to early May.
and observed nine interactions between Females (n = 3) were observed interacting
focal T. macrops and conspecifics for a total with other vipers for a total of 248 min for a
of 272 minutes from May 2015- January median of 74 min per viper. All female
2017 (see at Movie Archives of Animal interactions were at the low ground height
Behavior (http://movspec.mus-nh.city.osaka. level (>0 - 0.5 m) except for one which was
jp/ethol/title-e.php) and https://www.youtube. at groundstory height (0.5 - 1 m). Two of
com/channel/UCdRlzXz9YbUR2eWyEAEG the three female T. macrops, one in the
U4g). Median duration of each bout was 14 transition (TRMA220) and one in the core
TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 98
TABLE 1. Summary of focal big- eyed pit viper (Trimeresurus (Cryptelytrops) macrops) biometrics (snout-
vent length [SVL] in mm and mass in g), time observed on camera (in min), and number and duration (in min)
of interactions observed. Locations are the same as Strine et al. (2018, “upper dam pond, shortened to “pond”)
and Barnes et al. (2017, “canal”).
Biometrics Interactions
Viper ID Location Sex SVL Mass Time observed Number Duration
TRMA220 Canal Female 580 91.3 16307 4 28
TRMA226 Canal Male 424 24.2 7735 1 24
TRMA232 Canal Female 612 109.0 2254 1 74
TRMA271 Pond Female 514 52.5 7930 3 146
area (TRMA271), in this study interacted the day following the interaction. The male
with conspecifics on multiple occasions returned to the same ambush site on the
(median 3.5 interactions, median 7 min per night immediately following the agonistic
interaction) within a short time frame for a interaction after the conspecific
median of 70 min between interactions. The (presumably the same which disturbed him)
single male (TRMA226) had a single had left its shelter and moved elsewhere
observable interaction, for a total of 24 min, (not visible on camera). A conspecific
at low ground level height (>0 - 0.5 m). appeared to chase a focal female off an
Interactions of focal female vipers were ambush site in the core area (TRMA271)
primarily indirect (6 bouts) rather than during an agonistic interaction. The focal
direct (2 bouts). The most frequently viper completely abandoned the site (did not
observed outcome of interactions with focal return, moved >5 m lateral distance to a
female vipers was neutral (4 bouts), with new foraging site), while the conspecific
distracting (2 bouts) and agonistic (2 bouts) immediately proceeded to forage at the
outcomes infrequent. One female bout was ambush site previously occupied after the
direct and agonistic in the transition area of focal female was out of sight on camera.
SBR (TRMA220), and one was direct and In conclusion, novel findings of our
agonistic in the core area of the reserve investigation include clear agonistic
(TRMA271). The single focal male behavior between conspecifics which has
(TRMA226) interaction was direct and not yet been recorded outside of a sexual
agonistic. context (male combat) for green pit vipers
Agonistic interactions (Fig. 2) varied in and insight into more frequently observed
behavior following the encounters. One apathetic interactions.
female in the transition area (TRMA220) Direct social interaction of green pit
and the male (TRMA226) continued to vipers may be reduced due to largely
ambush at the same sites following sedentary lifestyle. Green pit vipers are
agonistic interactions for at least one night extremely sedentary and only the smallest
afterwards. The viper which disturbed the viper in the world, the Namaqua dwarf
male (TRMA226) appeared to shelter adder (Bitis schneideri), displays smaller
within close proximity (<0.5 m, observed known home range sizes among all
entering and exiting on camera) of it during snakes12,19,20. How limited movement
99 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER
FIGURE 2. Agonistic interactions of three focal big-eyed pit vipers (Trimeresurus (Cryptelytrops) macrops)
including female TRMA220 (A), male TRMA226 (B), and female TRMA271 (C) recorded on Bushnell trail
cameras. Interacting vipers are circled in yellow for reference.
translates into social behavior remains behavior and reducing direct competition.
largely unknown. Understanding of Sexual dimorphism, both in coloration and
behavior and communication within in size, likely reduces competition and
subpopulations is worth investigating with agonistic interactions15,21. Additionally,
green pit vipers due to their small home several studies suggest niche partitioning
ranges. Subpopulations which are naturally and vertical stratification among green pit
or anthropogenically isolated from others vipers, including T. macrops15,21,22. These
may show different behaviors or degrees of factors may explain the higher number of
sociality. neutral interaction outcomes compared to
Previous observations of big-eyed pit agonistic, and perhaps why we observed so
viper morphology and natural history have few interactions overall.
suggested unique adaptations for social
TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 100
Big-eyed pit vipers have been previously suggest they may display similar agonistic
documented and suggested to breed characteristics at least occasionally (3 out of
primarily between September and 9 interactions in our study) outside of the
November, which corresponds to the end of breeding season.
the rainy season in Thailand24,25. This We cautiously suggest limited resources
species is unique among vipers in that biting and sub-optimal seasonal conditions may be
has been directly observed in the wild driving factors behind the interactions we
during male combat during the breeding witnessed on camera. Pit vipers in our study
season, which has been suggested to be a interacted during the cold and hot dry
period of increased agonistic behavior25. seasons, which were not optimal foraging
Our observations (late November to early periods for anuran prey. Frogs likely
May) occurred outside of previously comprise a significant portion of T. macrops
reported mating season for the species. We diet24,33. Presence and utilization of quality
describe the first evidence of social foraging sites may also be a premium during
interactions in conspecific green pit vipers. these time periods (cold and hot dry
Interactions primarily resulted in what seasons). Lateral distance between ambush
appeared to be neutral outcomes, however, and shelter sites is negligible12,19, and the
several interactions were clearly agonistic two are likely not independently related.
which is novel for the green pit viper taxon Thus, site selection (and social behavior,
outside of breeding activities. subsequently) is likely influenced by the
Resource defense and territorial behavior balance of thermoregulation and energy
likely evolved or occurs when the benefits expenditure to obtain additional nutrients.
gained by defending a particular area that Shelter, resting, and ambush sites with
contains required resources exceed the costs adequate prey abundance may be scarce in
of defending it26,27,28. It is frequently rural communities and other highly
observed in terrestrial vertebrate groups, disturbed areas, additionally increasing
including birds, mammals, lizards, frogs, opportunities for interactions and
and salamanders29,30; although evidence is competition. Decreased prey and increased
scarce for snakes. Only two insular habitat homogeneity were observed for
colubrids (Oligodon formosanus and timber rattlesnakes (C. horridus) in a rural
Dinodon semicarinatum) defending sea landscape in North America, which
turtle nests (food resource) against subsequently altered foraging behavior34.
conspecifics have conclusively been Further investigation of ambush site
suggested to display resource defense and selection, chemical cues, and prey
territoriality among all known snake availability would greatly augment
species31,32. Infrequent feeding and the behavioral inferences. Whether social
unpredictability of exact time and place of interaction prevalence is related to ambush
available prey were factors suggested by32 site availability or quality would be a
as to why snakes generally do not defend beneficial testable hypothesis for future
food resources. Not enough evidence was study.
provided in our work to definitively From our camera observations, the
characterize T. macrops as territorial by sex, conspecifics interacting with our focal
season, or with increased human vipers appeared to be female T. macrops on
disturbance; however, our observations the basis of size and general morphology,
101 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER
however, recording quality of the cameras subsequent communication and resulting
was not sufficient to positively confirm behavior are crucial for ecological study and
species, sex, or fecundity. Similarly, low conservation.
recording rate (1-3 frames per minute) may
indicate missed or misinterpreted behaviors.
ACKNOWLEDGEMENTS
Thus, we were conservative with our
characterizations of behaviors and outcomes
We thank Suranaree University of
of interactions, as we believe acknowledging
Technology (SUT) for supporting this
the limitations of camera technology is
project. All methods were carried out under
essential for reducing potential misinter-
the guidelines and approval of the SUT
pretation and overstating our results.
animal use and ethics committee. The
Similarly, we believe it is essential to not
National Research Council of Thailand
over-extrapolate our results due to our
(NRCT), Thailand Institute of Scientific and
limited sample size and having a single
Technological Research (TISTR), and
study area in northeast Thailand.
Sakaerat Environmental Research Station
While certainly a time intensive method,
(SERS) provided funding, site permission,
we encourage further study with fixed
and logistical and technical support
cameras to better understand the
throughout the project.
consequences of intra and interspecific
interactions of animals employing ambush
foraging strategies. Green pit vipers employ LITERATURE CITED
ambush strategies and sedentary lifestyles
1. Brattstrom, B.H. 1974. The evolution of
which make them ideal for investigating
reptilian social behavior. American Journal of
behavioral interactions with fixed cameras.
Zoology, 14: 35-49.
As a result we propose the group as a model 2. Bonnet, X., Shine, R., and Lourdais, O. 2002.
species for behavior and social interaction Taxonomic chauvinism. Trends in Ecology and
study of ambush foraging predators. Evolution, 17: 1-3.
3. Pawar, S. 2003. Taxonomic chauvinism and the
To conclude, even broadly trained
methodological challenged. Bioscience, 53: 861-
scientists are frequently ignorant of basic
864.
information about snakes, including social 4. Ford, N. 1995. Experimental design in studies of
behavior30,35-36. Lin et al. (2007)37 provided snake behavior. Herpetological Monographs, 9:
130-139.
personal observation that green pit vipers
5. Schuett, G.W., Clark, R.W., Repp, R.A.,
“tend not to interact in an antagonistic or
Amarello, M., Smith, C.F., and Greene, H.W.
repellent manner; in fact they generally 2017. Social behavior of rattlesnakes: a shifting
ignore each other’s presence even when paradigm. In: Schuett, G.W., Feldner, M.J.,
they are in physical contact or in ambush Smith, C.F., and Reiserer, R.S. (eds.).
Rattlesnakes of Arizona, vol. 2. Eco Publishing,
positions on the same or adjacent sites in the
Rodeo, NM, USA. p. 161-244.
field or laboratory,” and fashioned their
6. Caro, T. 1999. The behavior-conservation
retreat site selection study design interface. Trends in Ecology and Evolution,
accordingly. While social interaction 14(9): 366-369.
7. Burghardt, G. M., Chiszar, D., Murphy, J.B.,
between green pit vipers may be rare (272
Romano Jr., J., Walsh, T., and Manrod, J. 2002.
minutes of 34, 226 minutes for the T.
Behavioral complexity, behavioral development
macrops observed in our study), consequences and play. In: Murphy, J.B, Ciofi, C., de La
of such contact and knowledge of Panouse, C., and Walsh, T. (eds.). Komodo
TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 102
Dragons: Biology and Conservation. macrops Kramer, 1977, in Northeast Thailand.
Smithsonian Institution Press, Washington, D. Amphibia- Reptilia, 39: 335-345.
C., USA. p. 78-117. 20. Maritz, B., and Alexander, G.J. 2012. Dwarfs on
8. Doody, J.S., Burghardt, G.M., and Dinets, V. the move: spatial ecology of the world's smallest
2013. Breaking the social–non-social viper, Bitis schneideri. Copeia, 1: 115-120.
dichotomy: a role for reptiles in vertebrate 21. Sawant, Nitin S. and Jadhav, T.D. 2012. Factors
social behavior research? Ethology, 199:1-9. influencing habitat selection by arboreal pit
9. Nowak, E.M., Theimer, T.C., and Schuett, G.W. vipers. Zoological Science, 30: 21-26.
2008. Functional and numerical responses of 22. Reza, Fachrul. 2018. Keanekaragaman ular
predators: where do vipers fit in the traditional pitviper Sumatera (Serpentes: Viperidae:
paradigms? Biological Review, 83: 601-620. Crotalinae) berdasarkan ketinggian di Sumatera
10. Clark, R.W. 2016. The hunting and feeding barat. Journal of Tropical Biodiversity and
behavior of wild rattlesnakes. In: Schuett, G.W., Biotechnology, 3: 49-56.
Feldner, M.J., and Smith, C.F. (eds.). The 23. Cox, R.M., Butler, M.A., and John-Alder, H.B.
Rattlesnakes of Arizona. Eco Publishing, 2007. The evolution of sexual size dimorphism
Rodeo, NM, USA. p. 91-118. in reptiles. In: Sex, Size and Gender Roles:
11. Dorcas, M.E., and Willson, J.D. 2009. Evolutionary Studies of Sexual Size
Innovative methods for studies of snake ecology Dimorphism, p. 38-49. Fairbairn, D.J.,
and conservation. Snakes: ecology and Blanckenhorn, W.U., and Szekely, T., Eds,
conservation, p. 5-37. Oxford University Press, London.
12. Barnes, C.H., Strine, C.T., Suwanwaree, P., and 24. Chanhome, L., Cox, M. J. Vararuchapong, T.
Hill III, Jacques. 2017. Movement and home Chaiyabutr, N. and Sitprija, V. 2011.
range of green pit vipers (Trimeresurus spp.) in Characterization of venomous snakes of
a rural landscape in Northeast Thailand. Thailand. Asian Biomedicine, 5: 311-328.
Herpetological Bulletin, 142: 19-28. 25. Strine, C., Brown, A., Barnes, C.H., Major, T.,
13. Gillingham, J.C. 1987. Social behavior. In: Artchawakom, T., Hill III, J.G., and
Seigel, R.A., Collins, J.T., and Novak, S.S. Suwanwaree, P. 2018. The first record of
(eds.). Snakes: Ecology and Evolutionary arboreal male to male combat of free ranging
Biology. MacMillan Publishing Company, New big-eyed green pit vipers (Trimeresurus
York, USA. p. 184-209. macrops) in Northeast Thailand. Current
14. Kramer, E. 1977. Zur Schlangenfauna Nepals. Herpetology, 37(1): 81-87.
Revue suisse Zoologie, 84: 721-761. 26. Schoener, T.W. 1983. Simple models of optimal
15. Strine, C., Silva, I., Nadolski, B., Crane, M., feeding- territory size: A reconciliation. The
Barnes, C., Artchawakom, T., Hill, J., and American Naturalist, 121: 608-629.
Suwanwaree, P. 2015. Sexual dimorphism of 27. Grant, J.W.A. 1993. Whether or not to defend?
tropical Green Pit Viper Trimeresurus The influence of resource distribution. Marine
(Cryptelytrops) macrops in Northeast Thailand. Behaviour and Physiology, 23: 137-153.
Amphibia-Reptilia, 36: 1-12. 28. Dubois, F., and L.A. Giraldeau. 2005. Fighting
16. Wilkinson, S.L. 2014. Guide to venomous for resources: The economics of defense and
reptiles in veterinary practice. Journal of Exotic appropriation. Ecology, 86: 3-11.
Pet Medicine, 23: 337-346. 29. Brown, J.L., and G.H. Orians. 1970. Spacing
17. Reinert, H.K., and Cundall, D. 1982. An patterns in mobile animals. Annual Review of
improved surgical implantation method for Ecology and Systematics, 1: 239-262.
radio-tracking snakes. Copeia, 1982: 702-705. 30. Greene, H.W. 1997. Snakes: The evolution of
18. Hardy, D.L. and Greene, H.W. 2000. Inhalation mystery in nature. Berkeley, CA: University of
of anesthesia of rattlesnakes in the field for California Press.
processing and transmitter implantation. 31. Huang, W.S., H.W. Greene, T.J. Chang, and
Sonoran Herpetology, 13: 109-113. Shine, R. 2011. Territorial behavior in
19. Strine, C., Silva, I., Barnes, C.H., Marshall, Taiwanese kukrisnakes (Oligodon formosanus).
B.M., Artchawakom, T., Hill III, J., and Proceedings of National Academy of Sciences,
Suwanwaree, P. 2018. Spatial ecology of a 108: 7455-7459.
small arboreal ambush predator, Trimeresurus 32. Mori, A., Ota, H., and Hirate, K. 2019.
Defending resources on isolated islands. p. 288-
103 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER
309. In: H. B. Lillywhite and M. Martins. 35. Greene, H.W. 2013. Tracks and Shadows. Field
Islands and Snakes. Isolation and Adaptive Biology as Art. University of California Press,
Evolution. Oxford University Press, New York. Berkeley and Los Angeles, USA.
33. Orlov, N., Ananjeva, N., and Khalikov, R. 2002. 36. Lillywhite, H.B. 2014. How Snakes Work.
Natural history of pitvipers in Eastern and Structure, Function and Behavior of the World’s
Southeastern Asia. In: Schuett, G., Hoggren, Snakes. Oxford University Press, New York,
W.M., Douglas, M.E., and Green, H.W. (eds.). USA.
Biology of the Vipers. Eagle Mountain 37. Lin, H.C., Hung, H.Y., Lue, K.Y., and Tu, M.C.
Publishing, Eagle Mountain, Utah, USA. p. 345- 2007. Diurnal retreat site selection by the
361. arboreal Chinese green tree viper (Trimeresurus
34. Wittenberg, R.D. 2012. Foraging ecology of the s. stejnegeri) as influenced by temperature.
timber rattlesnake (Crotalus horridus) in a Zoological Studies, 46: 216-2.
fragmented landscape. Herpetological Conservation
and Biology, 7: 449-461.
