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Acknowledgments. — We would like to express our gratitude to Mathies, T. 2011. Reproductive cycles of tropical snakes. In R. D. Al-
Robert Meidinger of the World of Snakes, Alajuela, Costa Rica. We dridge, and D. M. Sever (eds.), Reproductive Biology and Phylog-
also thank Enrique La Marca and Daniel Lawson for their valuable eny of Snakes, pp. 511–550. CRC Press, Boca Raton, Florida.
contributions to the manuscript. Mole, R. R. 1924. The Trinidad snakes. Proc. Agr. Soc. Trinidad and
Tobago 14:363–369.
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ter (Lachesis muta stenophrys) and the blackheaded bushmaster
Alves, F. Q., A. J. S. Argolo, and G. C. Carvalho. 2014. Reproductive biol- (Lachesis muta melanocephala) for the first time in captivity. Bull.
ogy of the bushmaster Lachesis muta (Serpentes: Viperidae) in the Chicago Herpetol. Soc. 29:165–183.
Brazilian Atlantic Forest. Phyllomedusa 13:99–109. ———. 1999. Keys to understanding the bushmasters (genus Lache-
Amaral, A. 1926. On the oviparity of Lachesis muta Daudin, 1803. Co- sis Daudin 1803) Bull. Chicago Herpetol. Soc. 34:45–92.
peia 1925:93–94. ———. 2000. The bushmasters (genus Lachesis Daudin 1803): Mor-
Boyer, D. M., L. A. Mitchell, and J. B. Murphy. 1989. Reproduction and phology in evolution and behavior. CD-ROM. Ripa Ecologica,
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Zoo. Int. Zoo Ybk. 28:190–194. ———. 2001. The bushmasters (genus Lachesis Daudin 1803): Mor-
Campbell, J. A., and W. W. Lamar. 2004. The Venomous Reptiles of the phology in evolution and behavior. CD-ROM. Ripa Ecologica,
Western Hemisphere. Vol. I. Comstock Publishing Associates, Itha- Wilmington, North Carolina.
ca, New York. 976 pp. Rossi, J. V. 2006. General husbandry and management. In D. Mader
Corrales, G., R. Meidinger., S. Rodríguez., D. Chacón, and A. Gómez. (ed.), Reptile Medicine and Surgery (2nd ed.), pp. 25–41. Elsevier
2014. Reproduction in captivity of the Central American bush- Saunders, St. Louis, Missouri.
master (Lachesis stenophrys, Serpentes: Viperidae), in Costa Rica. Sánchez, D. 2000. Herpetofauna del cerro La Laguna, macizo del
Cuad. Herpetol. 28:137–139. Turimiquire, municipio Freites, estado Anzoátegui, Venezuela. Te-
Eisele, B.R. 2009. Propagation of the South American bushmaster sis de Licenciatura, Facultad de Agronomía, Universidad Central
(Lachesis muta muta) at the Jacksonville Zoo and Gardens. IRCF de Venezuela. 78 pp.
Reptil. Amphib.16:182–189. ———, L. De Sousa, L. Esqueda, and J. Manzanilla. 2004. Especie nueva
Fernandes, D. S., F. L. Franco, and R. Fernandes. 2004. Systematic re- de Atractus (Serpentes: Colubridae) del Macizo del Turimiquire,
vision of the genus Lachesis Daudin, 1803 (Serpentes, Viperidae). tramo oriental de la Cordillera de la Costa, Venezuela. Saber 16:89–
Herpetologica 60:245–260. 95.
Greene, H. W. 1997. Snakes: The Evolution of Mystery in Nature. Uni- Souza, R. 2007. Reproduction of the Atlantic bushmaster (Lachesis
versity of California Press, Berkeley, California. 351 pp. muta rhombeata) for the first time in captivity. Bull. Chicago Her-
———, and M. A. Santana. 1983. Field studies of hunting behavior by petol. Soc. 42:41–43.
bushmasters. Amer. Zool. 23:897. Turner, E., R. Carmichael, and R. Souza. 2008. Dialogues on the Tao of
Henao, A. M., and G. Corrales. 2015. First report of the reproduction in Lachesis. Bull. Chicago Herpetol. Soc. 43:157–164.
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1896). Herpetol. Notes 8:315–320. bushmaster, Lachesis muta, in Central America. Amer. Midl. Nat.
Lancini, V. A. 1986. Serpientes de Venezuela. 2nd ed. Talleres Graficas 78:182–187.
Armitano, Caracas. 262 pp.

HERPETOCULTURE NOTES
TESTUDINES — TURTLES a carapace covered with soft skin that lacks keratinized scutes.
The carapace can range from olive to black in coloration and
CARRETOCHELYS INSCULPTA (Fly River Turtle). CLEANING is counter shaded by a cream colored plastron. Carettochelys
MUTUALISM. Cleaning mutualism is a well-known symbiotic insculpta are fully aquatic and have four flipper-like limbs
relationship frequently observed in the wild. This interaction resembling the limbs of a sea turtle. They can also be identified
involves a cleaner, a host, and often times may take place at a by their long, snorkel-like snout (Cann 1998. Australian
cleaning station. A cleaning event typically involves the cleaner Freshwater Turtles. Beaumont Publishing, Singapore. 292 pp.)
species removing ectoparasites from a client species (Losey et al. A single male C. insculpta was observed over a period of
1994. Copeia. 1994:684–690). The cleaner may also feed on the skin four non-consecutive days in its enclosure at the Smithsonian
of the host to remove mucus or diseased skin (Floeter et al. 2007. National Zoo in Washington, District of Columbia, USA. The
J. Anim. Ecol. 76[1]:105–111). Cleaner species often linger around C. insculpta was housed with a Pterygoplichthys gibbiceps
an area known as the cleaning station, while clients approach (Leopard Pleco) during the observations. Carettochelys
such a place specifically to be cleaned. Cleaners may range from insculpta and P. gibbiceps do not occur naturally together in
specialized fish to birds (Losey 1972. Copeia. 1972:820–833; Poulin the wild; C. insculpta is endemic to parts of Australia and New
and Grutter 1996. Bioscience. 46[7]:512–517). Meanwhile clients Guinea, while P. gibbiceps naturally occurs in South America.
can include any species in need of ectoparasite removal, typically Nonetheless, a presumably symbiotic cleaning mutualism was
a species larger than the cleaner. Cleaning mutualisms occur regularly observed among these individuals.
among various species; however, most documented instances The C. insculpta was often seen posing during a cleaning
occur in marine environments (Floeter et al. 2007, op. cit.). event (Fig. 1A). Posing is a behavior common to clients in
Carettochelys insculpta is an omnivorous turtle found in cleaning mutualisms. During posing, the client species
freshwater streams and rivers in the Northern Territory of assumes a position in anticipation of a cleaning. This position
Australia and the southern part of Papua New Guinea. They have is only assumed during a cleaning interaction (Losey 1972, op.

Herpetological Review 47(4), 2016

Fig. 1. A) The Carettochelys insculpta seen posing during a cleaning event. B) The C. insculpta is seen with limbs stretched out and head lifted
upward. C & D) The C. insculpta can be observed lifting a portion of its plastron from the substrate as Pterygoplichthys gibbiceps moved in to
clean the area exposed underneath. E) The P. gibbiceps was observed resting on the carapace of the turtle.

cit.). The C. insculpta was observed posing for the fish five times event (Poulin and Grutter 1996, op. cit.), which was observed
out of seven cleaning events. As seen in Fig. 1B, the limbs of multiple times. Additionally, a possible cleaning station was
the C. insculpta were stretched out and the head lifted upward, identified in the enclosure. A single branch was frequented by
a pose that has been previously observed among clients. both individuals a large percentage of the observation time.
Similarly, clients often remain motionless during a cleaning Cleaning events were often observed at this site, indicating that

Herpetological Review 47(4), 2016

this branch may very well be a cleaning station in the enclosure. It is necessary to speculate why this cleaning mutualism
The use of this cleaning station was noted approximately occurred since C. insculpta and P. gibbiceps do not live together
seventy five times during the observations. in the wild. There are several species of fish that may fill the
A majority of the cleanings were instigated by the C. insculpta same niche as P. gibbiceps would that inhabit the Fly-Strickland
by nudging the fish to indicate the desire for a cleaning. The C. river system in New Guinea where C. insculpta is found (Roberts
insculpta was also observed shifting the direction of its body, 1978. Smithsonian Contrib. to Zoo. 281). However, there has not
moving limbs, or corralling the fish towards different parts of its yet been a documented cleaning mutualism between fish and C.
body. When the turtle would shift positions or move its limbs this inscuplta in the wild.
resulted in the fish cleaning those areas that were adjusted. In An alternate or additional explanation for this cleaning
Fig. 1C and Fig. 1D, the turtle can be observed lifting a portion of mutualism is simply the desire of this C. insculpta to be cleaned.
its plastron from the substrate and P. gibbiceps having moved in It is well known that C. insculpta is a host to ectoparasites found
to clean the area exposed underneath the turtle. The P. gibbiceps on its skin (Saumure and Doody 2000. Herpetol. Rev. 31[4]:237–
was observed cleaning the carapace, plastron, limbs, neck, chin, 238). It is possible that the turtle’s need to be cleaned stems
head, and around the cloaca during most cleaning events. from this natural tendency to get rid of these ectoparasites. This
Interestingly, the P. gibbiceps was observed on several may explain why the turtle initiated the majority of the cleaning
occasions simply resting on the turtle, either on a limb or the events.
shell (Fig. 1E). This resting behavior was observed a total of Because cleaning mutualisms have been known to occur
ten times throughout the observational periods; both during a among different species in captivity (Poulin and Grutter 1996,
cleaning event and when no cleaning event was in progress. The op. cit.), it is possible that a cleaning mutualism will also occur
reason for this behavior is unclear; this likely does not constitute with another individual of P. gibbiceps. Further study will be
cleaning behavior, but it is an interesting aspect of the possible needed to determine if the relationship observed between these
symbiotic relationship between these individuals. two individuals is specific to them or if the same relationship
The observation period ended when the P. gibbiceps was will result with a different fish. In the future P. gibbiceps or
found dead in the enclosure. It is unknown whether the C. another cleaner fish from within the same range of C. insculpta
insculpta decided to consume the P. gibbiceps or whether it died should be placed in the enclosure. The individuals should be
of another cause. It is well known that cheating clients exist in observed in the same manner as above. Initial interactions and
seemingly symbiotic relationships. A cheating client will take characteristics such as presence of a cleaning station and client
advantage of the cleaner by consuming it (Poulin and Grutter posing should be noted in the observations.
1996, op. cit.). The C. insculpta was not observed killing the P. ALESSANDRA CHIOTTI and MATT NEFF, Department of Herpetol-
gibbiceps, however the turtle was observed consuming parts of ogy, Smithsonian National Zoological Park, Washington, DC 20008, USA
the fish after it had died. The P. gibbiceps may have already died (e-mail: neffm@si.edu)
before consumption by the turtle. It is unclear what occurred.

Herpetological Review 47(4), 2016