HB vol. 9 no. 1 - Notas de História Natural & Distribuição Geográfica

Notas de História Natural & Distribuição Geográfica

BODY-BENDING BEHAVIOUR IN : NEW RECORDS OF A POORLY DOCUMENTED DEFENSIVE BEHAVIOUR

Daniella Pereira Fagundes de França1,2, Isabela Freitas Oliveira3, Daniela Gennari1,4, Bruno Rocha1, Paul Smith5,6, Gustavo José Scrocchi7, Paulo Roberto Machado-Filho1,2,*

1. Laboratório de Herpetologia, Museu de Zoologia da Universidade de São Paulo, 04218-970 São Paulo, São Paulo, Brazil. 2. Universidade Estadual Júlio de Mesquita Filho (UNESP), Campus Rio Claro, 13506-900 Rio Claro, São Paulo, Brazil. 3. Universidade Federal do Rio Grande do Norte (UFRN), 59064-74, Lagoa Nova, Natal, Rio Grande do Norte. 4. Instituto de Biociências, Universidade de São Paulo, 05508-900 São Paulo, São Paulo, Brazil. 5. FAUNA , Encarnación, Paraguay. 6. Para La Tierra, Centro IDEAL, Pilar, Paraguay. 7. Instituto de Herpetología. UEL (Fundación Miguel Lillo - CONICET), 4000 San Miguel de Tucumán, . *Corresponding author: [email protected]

nakes exhibit a broad array of de- Body-bending behaviour is a defensi- fensive tactics to avoid predators, ve strategy in which the contorts Sand detection avoidance is an im- the body into a zigzag, “horizontal la- portant component of many of them dder” position, resembling the shape (Martins, 1996). To avoid detection, of certain fallen vine stems (Marques snakes may use morphology, such as et al., 2006; Duarte, 2012). This beha- cryptic coloration; defensive behaviour, viour has been previously reported in a such as immobility, or a combination few Neotropical snake : Conio- of both strategies (Greene, 1988; Mar- phanes fissidens, viridis- tins, 1994). Body-bending, which acts sima, fuscus, C. monticola, to break up the body silhouette, is one Pantherophis obsoleta, Phrynonax of the more rarely-reported and poor- polylepis, Psomophis joberti, Spilo- ly understood defensive behaviours. tes pullatus, and S. sulphureus (Bee- 56 HB vol. 9 no. 1 - Notas de História Natural & Distribuição Geográfica

be, 1946; Abuys, 1986; Marques, et al., A specimen of Philodryas trilineata 2006; Doherty-Bone, 2009; Maddock (adult female, total length 1550 mm) col- et al., 2009; Duarte, 2012; Martins et lected 10 km south of the city of Andal- al., 2012). Here, we report records of galá (27º34’19.20”S, 66º18’14.40”W), this behaviour for five additional spe- Catamarca Province, Argentina, has cies of Neotropical and Dip- been kept in captivity at FML since 21 sadidae (Chironius exoletus, Erythro- October 2007. This individual someti- lamprus sagittifer, Philodryas baroni, mes exhibited body-bending behaviour P. chamissonis, P. psammophidea, P. during the cleaning of its terrarium (GS trilineata), as well as additional re- pers. obs.). ports for Chironius fuscus and Spilotes In October 2007 in an area of Chaco sulphureus. woodland, close to the headquarters In November 2002, a pregnant fema- of Parque Nacional Teniente Enciso le of Philodryas baroni was captured (21º04’48.00”S, 61º36’54.00”W), Bo- near the city of Tucumán, Tucuman querón Department, Paraguay, a pre- Province, Argentina (26º49’58.80”S, sumed juvenile of Philodryas psammo- 65º12’57.60”O) and sent to the Fun- phidea (Figure 1B) (approximately 35 dación Miguel Lillo laboratory (FML), cm total length), was encountered on where oviposition occurred overnight an exposed path approximately 2.5 m 14 to 15 December 2002. At the time wide through open-undergrowth woo- specimens were collected there were dland. As the observer approached, the no regulations concerning collection snake assumed a body-bending postu- of snakes in Argentina, so no permits re, and as the observer moved closer were issued. The eggs hatched on 28 to take photographs the individual be- February 2003 and photos of the ju- came aggressive, striking at the lens of veniles were taken on 4 April 2003. the camera from a distance of approxi- While being photographed, one indi- mately 30 cm. Following the aggressi- vidual (FML 13710; snout-vent length ve reaction of the snake, the observer 377 mm, tail length 116 mm) attempted withdrew and the snake moved rapidly to escape several times, requiring fre- into cover. quent handling (Figure 1A). Following At 11:30 a.m. on 2 November 2007, in an handling, it adopted a body-bending pos- area of the Distrito Chaqueño Occiden- ture, raising its head and the anterior third tal (Semi-arid or Dry Chaco), approxi- of the body off the ground to an angle of mately 1km from Rivadavia municipa- approximately 45°. The individual retai- lity (24º10’30.00”S, 62º52’33.60”W), ned this position for three or four minutes Salta Province, Argentina, an adult before attempting to escape again. individual of Erythrolamprus sagit-

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tifer modestus (Figure 1C) was obser- a bush and remaining approximately ved motionless on the ground in the 30cm above the ground. The observa- body-bending posture. The individual tion lasted a total of four minutes. had recently emerged from a nearby At 12:30 p.m. on 21 December 2013, water body and was on the dry shore. about 80 km west from the munici- The snake remained motionless du- pality of Comodoro (13º42’07.20”S, ring the observations, despite the close 60º26’09.60”W), Mato Grosso state, proximity of the observer. On 13 July Brazil, an individual of Spilotes sul- 2008, another adult individual of this phureus was observed in body-bending species (Figure 1D) was also observed posture on a dirt road in a seasonal body-bending in the same general area, semi-deciduous forest. Initially it was among fallen branches on the ground. mistaken for a liana stem (Figure 1G). On 2 March 2012, on Isla Negra The individual was removed from the (33º26’16.80”S, 71º39’43.20”W), Re- road after five minutes of observation gion V, Chile, an adult Philodryas cha- in the body-bending posture. missonis (Figure 1E) was observed in a At 15:38 p.m. on 14 May 2017 in restinga area on a moist rocky depres- the neighbourhood of Guapiruvu sion, with no vegetation cover, approxi- (24º18’57.60”S, 48º07’26.40”W), mu- mately 30m from the edge of the water. nicipality of Eldorado, southern São The individual retained a body-bending Paulo state, Brazil, an adult Chironius posture for more than eight minutes, fuscus (approximately 1.5 m total len- even when approached closely by the gth) was observed crossing a trail in observer. secondary Atlantic Forest (Figure 1H). On 15 December 2013 at 2:48 p.m., The snake stopped when the observer approximately 50 km south of the mu- approached, assuming the body-ben- nicipality of Parecis (12º15’14.40”S, ding posture and retaining it for five 61º12’07.20”W), Rondônia state, Bra- minutes. When the observer attemp- zil, an adult Chironius exoletus (appro- ted to catch the snake, it fled rapidly ximately 2 m total length) was observed towards the forest. in an Amazonian seasonal semi-deci- Liana vines occur in most of all sites in duous forest (Figure 1F). It lay motion- which these observations were made less in leaf litter on the forest floor in the and often litter the floor, offering a po- body-bending posture. At the approach tential defensive camouflage oppor- of the observer, the individual moved tunity for species that exhibit body- its head slightly, but made no other sig- -bending behaviour (Edmunds, 1974; nificant movements. On a closer second Marques et al., 2006). The abrupt tran- approach the specimen fled, climbing sition from a stretched to a body-ben- 58 HB vol. 9 no. 1 - Notas de História Natural & Distribuição Geográfica

ding posture could confuse a potential fuscus which assumed the posture predator with a search image for ani- on approach of the observer. On the mals with an elongated body shape. other hand, the individuals of Spilotes Body-bending behaviour has to date sulphureus had already adopted bo- been documented in two Neotropical dy-bending posture before they were families: Colubridae (genera Chiro- detected by the observer, who initially nius, Spilotes, Pantherophis, and Phry- mistook the snake for a fallen branch nonax) and Dipsadidae (genera Conio- and correctly identified it only at a close phanes, Erythrolamprus, Philodryas distance. The second individual of Ery- and Psomophis) (Zaher et al., 2019). throlamprus sagittifer modestus was Data is insufficient to confidently de- also observed body-bending at a dis- clare this behaviour as plesiomorphic tance among fallen branches. It seems in these groups, but our observations likely that individuals displayed the bo- corroborate previous suggestions that dy-bending behaviour in response to body-bending behaviour is an adap- the presence of the observer/predator, tive behaviour found in arboreal and and maintained that posture until they terrestrial snakes (Marques et al., were detected and the threat level in- 2006; Doherty-Bone, 2009; Martins creased. The data presented here is not et al., 2012). Chironius exoletus and consistent with the hypothesis that bo- Philodryas baroni present tendencies dy-bending is a physiological response towards arboreality; Philodryas cha- by snakes at non-optimal body tempe- missonis and P. trilineata are semi- rature (Marques et al., 2006), as some -arboreal; and Chironius fuscus, Ery- individuals either attacked or escaped throlamprus sagittifer modestus and rapidly, with no obvious limitations to Philodryas psammophidea are ter- their mobility. restrial species (Cei, 1993; Giraudo & Few reports of body-bending in wild Scrocchi, 2002; Machado-Filho & Mar- individuals exist, and we encourage the ques, 2020). publication of future observations to For several of the cases here it was not construct a more complete knowledge possible to record the length of time of the causal factors of behaviours. A that the individuals had been in bo- lack of reports of this behaviour in the dy-bending posture prior to their de- wild may be due to under-reporting or tection However, the captive juveniles because few taxa employ the defence. It of Philodryas baroni and P. trilineata could also be indicative of the efficiency both exhibited this behaviour imme- of this defensive technique against vi- diately following disturbance, as did sually-oriented predators. the free-living individual of Chironius 59 HB vol. 9 no. 1 - Notas de História Natural & Distribuição Geográfica

Acknowledgements

We are grateful to Carlos Frederico D. ling behaviour. Herpetology Notes, Rocha, Fausto E. Barbo, and Gabriela 5:303-304. Sobral for suggestions and their criti- Edmunds, M. 1974. Defense in ani- cal reviews of the manuscript. We are mals: a survey of anti-predator defen- also grateful to Gabriela Nuñez and to ces. Longman Group, Ltd., Essex. 357p. Ramón Hurtado Duarte for the photos and to CAPES for financial support. PS Giraudo, A. R. & G. J. Scrocchi. 2002. is grateful to the PRONII program of Argentinian snakes. An annotated che- CONACyT Paraguay. cklist. Smithsonian Herpetological In- formation Service, 132:1-53. Greene, H. W. 1988. Antipredator me- References chanisms in ; pp. 1-152. In: C. Gans, & R. B. Huey (eds.), Biology of Abuys, A. 1986. The snakes of Suri- the Reptilia. Vol. 16, Ecology B, Defen- nam, part XIII: Subfamily Xenodonti- se and Life History. Alan R. Liss, New nae (genera Pseudoeryx, Pseustes and York. Rhadinaea). Litteratura Serpentium, 6:19-30. Machado-Filho, P. R. & O. A. V. Mar- ques. 2020. Feeding habits and diet of Beebe, W. 1946. Field notes on the the snake genus Philodryas (Serpen- snakes of Kartabo, British Guiana and tes, Dipsadidae, Xenodontinae). Papéis Caripito, Venezuela. Zoologica, 31:11- Avulsos de Zoologia (in press). 52. Maddock, S., B. Tolhurst, M. Brown, Cei, J. M. 1993. Reptiles del noroeste, M. Peck, E. V. Pérez & J. N. Morales. nordeste y este de la Argentina: Her- 2011. Body bending behaviour: more petofauna de las selvas subtropicales. widespread than previously thought? Puna y Pampas. Monografia Museo New reports from two snake species of Regionale di Scienze Naturali Torino, Northwest Ecuador. Herpetology No- 16:1-949. tes, 4:79-81. Doherty-Bone, T. M. 2009. Elaphe ob- Marques, O. A. V., M. G. Rodrigues & I. soleta spilodes (Grey Rat Snake): bo- Sazima. 2006. Body bending: a cryptic dy-bending behaviour. Herpetological defensive behaviour in arboreal snakes. Bulletin, 109:38-39. Herpetological Bulletin, 97:2-4. Duarte, M. R. 2012. The intriguing Martins, M. 1996. Defensive tactics in “Liana-mimicry” or “body bending” lizards and snakes: the potential con- behaviour in snakes: cryptic or signa- tribution of Neotropical fauna; pp. 185- 60 HB vol. 9 no. 1 - Notas de História Natural & Distribuição Geográfica

199. In: K. Del Claro (ed.), Anais do XIV Encontro Anual de Etologia. Sociedade Brasileira de Etologia, Universidade Federal de Uberlândia, Brasil. Miranda, J.P., J. C. Lopes Costa & C. F. D. Rocha, 2012. Body-bending beha- viour: a new instance in a terrestrial snake from Brazil. Herpetological Bul- letin, 122: 35-37. Zaher, H., R. W. Murphy, J. C. Arre- dondo, R. Graboski, P. R. Machado-Fi- lho, K. Mahlow, G. C. Montingelli, A. B. Quadros, N. L. Orlov, M. Wilkinson, Y. P. Zhang & F. G. Grazziotin. 2019. Large-scale molecular phylogeny, mor- phology, divergence-time estimation, and the fossil record of advanced cae- nophidian snakes (: Serpen- tes). PloS one, 14:e0216148.

Editor: Henrique C. Costa

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Figure 1. New reports of body-bending behaviour in Neotropical snakes: (A) Philodryas psammophidea, (B-C) Erythrolamprus sagittifer modestus, (D)Philodryas baroni, (E) Chironius exoletus, (F) Philodryas chamissonis, (G) Spilotes sulphureus and (H) Chironius fuscus. 62