See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/330162923

Chelonian Predation by Jaguars (Panthera onca)

Article  in  Chelonian Conservation and Biology · December 2018

DOI: 10.2744/CCB-1325.1

CITATIONS READS
0 735

3 authors:

Elizangela Brito Everton Miranda

42 PUBLICATIONS   148 CITATIONS   
The Peregrine Fund
30 PUBLICATIONS   228 CITATIONS   
SEE PROFILE
SEE PROFILE

Fernando Rodrigo Tortato

Panthera
82 PUBLICATIONS   574 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Dinâmica de populações e metapopulações de Mesoclemmys vanderhaegei (Testudines: Chelidae) na bacia do Paraguai, Brasil View project

Pantanal Jaguar Project - Panthera Brasil View project

All content following this page was uploaded by Elizangela Brito on 25 February 2019.

The user has requested enhancement of the downloaded file.

 NOTES AND FIELD REPORTS
Chelonian Conservation and Biology, 2018, 17(2): 280–283 of the group’s evolutionary success. Living chelonians can
Ó 2018 Chelonian Research Foundation
be found in nearly every major ecosystem on Earth, except
those of the polar regions (Ernst and Barbour 1989). The
Chelonian Predation by Jaguars shell is often complemented by spiny scutes on the legs
(Panthera onca) and has the ability to house the retracted legs and head.
Predators have developed a variety of strategies to
ELIZÂNGELA SILVA BRITO1,*, overcome this suite of defensive measures, including
EVERTON MIRANDA2,3, AND member amputation (Heithaus et al. 2008), dropping
FERNANDO RODRIGO TORTATO3,4 animals from the air or cliffs (Watson 2010), and direct
shell destruction (Salera-Junior et al. 2009). Despite this,
1
Herpetology Laboratory, Biodiversity Centre, Institute of adults of most chelonian species suffer low mortality
Biosciences, Federal University of Mato Grosso, Av. Fernando (Iverson 1991). However, Panthera onca (jaguar) is well
Correa da Costa, 2367, 78060-900, Cuiabá, Mato Grosso, Brazil known for preying on chelonia (Da Silveira et al. 2010).
[[email protected]]; Their heads show several characteristics relating to
2
IUCN/SSC Boa and Python Specialist Group, Buenos Aires,
durophagy, including thick canines and large masseter
Argentina;
3
Postgraduate Program in Ecology and Biodiversity Conservation, and temporal muscles (Seymour 1989) and one of the
Federal University of Mato Grosso, Av. Fernando Correa da Costa, strongest bites relative to body size in the genus Panthera
2367, 78060-900, Cuiabá, Mato Grosso, Brazil (Christiansen and Adolfssen 2005).
[[email protected]]; Here we review chelonian species preyed on by
4
Panthera, 8 West 40th Street, 18th Floor, New York, New York jaguars in order to provide to other researchers authors
10018 USA [[email protected]]
with a current, single-source review of chelonian predation
*Corresponding author
by jaguars. We also synthesize information on body size
ABSTRACT. – We present a new record of freshwater and reproductive condition of chelonia that are preyed on
turtle predation by the jaguar, Panthera onca, in by jaguars. In addition, we report the first record of
addition to a current review of chelonian predation by predation on Acanthochelys macrocephala by jaguar.
this feline. In total, 16 species of chelonians were A search of the literature concerning interactions
predated by jaguars: 3 were terrestrial, 8 freshwater, between jaguars and turtles was performed using Google
and 5 marine. Our review revealed that jaguars prey Scholar. We used the key words jaguar, P. onca, and onça-
on a large number of chelonians, including heavily pintada combined with diet, feeding habits, food habits,
armored species, such as the Chelonoidis tortoises, and hábitos alimentarios, and dieta. This allowed us to find
also small freshwater species. published and unpublished information in English,
Portuguese, and Spanish.
Predation is acknowledged as one of the main forces In September 2014, we found a dead adult individual
of natural selection. It is involved in the regulation of a of A. macrocephala on the Transpantaneira Park Road (lat
diverse range of evolutionary and ecological processes, 17816 0 47 00 S, long 56852 0 16 00 W, WGS84), located within
including Cambrian diversity explosion (Bengtson 2002), the Brazilian Pantanal wetlands of the Paraguay River
top-down population regulation (Orihuela et al. 2014), basin. Acanthochelys macrocephala is a medium-sized
landscape-level soil nutrient distribution (Bump et al. freshwater turtle that lives in marshes, wetland areas,
2009), habitat use of a variety of prey species (Preisser et shallow bays, and brackish lagoons (Rhodin et al. 2009).
al. 2005), and natural selection itself (Genovart et al. The individual was found on dry land, with visible bite
2010). Being such a strong selective force, predation has marks on the carapace, and jaguar tracks were found at the
been responsible for a variety of adaptations in prey site. The distance between canines (. 70 mm) marked on
species. A large and continually growing body of research the carapace was consistent with that of a jaguar bite
has focused on this subject (Greene 1988; Caro 2005), and (Hoogesteijn and Hoogesteijn 2005), confirming the
a general classification of antipredator defenses separates predator’s identity.
prey strategies into 2 main classes (Brodie et al. 1991): In addition, our search revealed records of jaguar
predation avoidance by flight, being constantly vigilant predation on 15 species of chelonia, totaling 16 with the
and morphologically adapted to escape via speed (passer- addition of A. macrocephala (Table 1). Of these, 3 species
ines, most monkeys, iguanids), and prey that is able to were terrestrial, 8 freshwater, and 5 marine. The latter were
confront (peccaries, boars, skunks) or physically resist killed during nesting times, as were the large freshwater
predators (armadillos, tortoises). species, which usually nest in large numbers on beaches.
Among the most remarkable adaptations of physical Small chelonia, such as A. macrocephala, can be
resistance to predation are the shells developed by considered a rare prey of jaguars because this turtle
chelonians. Formed by the fusion of vertebras, ribs, and occasionally moves onto dry land to migrate to other water
sternal bones, this unique development has been the basis bodies, as these bodies of water are not always connected
 NOTES AND FIELD REPORTS 281

Table 1. Chelonian species preyed on by the jaguar, including the average mass of each species. An ‘‘X’’ indicates that the predation
event occurred during nesting.

Species Mass (g) Source Nesting Predation source

Freshwater turtles
Chelidae
Acanthochelys macrocephala 1761 E. Brito (unpubl. data) This work
Acanthochelys radiolata 422 M. Secco et al. ( pers. comm.) Garla et al. (2001)
Platemys platycephala 245 Herrel et al. (2002) Emmons (1989)
Geoemydidae
Rhinoclemmys punctularia 810 E. Brito (unpubl. data) Chávez-Tovar (2010)
Kinosternidae
Kinosternon scorpioides 284 Carvalho et al. (2008) Montalvo et al. (2014)
Podocnemididae
Podocnemis expansa 24,700 Portelinha et al. (2014) X Salera-Junior et al. (2009)
Podocnemis unifilis 5760 Fachı́n-Terán and Vogt (2004) X Emmons (1989); Salera-Junior et al.
(2009)
Podocnemis vogli 945 Prado (1969) Scognamillo et al. (2003)
Terrestrial turtles
Testudinidae
Chelonoidis carbonarius 6684 Wang et al. (2011) McBride et al. (2010)
Chelonoidis chilensis 1426 Waller et al. (1989) Taber et al. (1997)
Chelonoidis denticulatus 6430 Moskovits (1988) Emmons (1989); Garla et al. (2001)
Marine turtles
Cheloniidae
Caretta caretta 116,000 Rueda-Almonacid et al. (2007) X Arroyo-Arce et al. (2017)
Chelonia mydas 166,300 Hays et al. (2002) X Troëng (2000); Carrillo et al. (2009);
Verı́ssimo et al. (2012); Arroyo-Arce
and Salom-Pérez (2015); Alfaro et al.
(2016)
Eretmochelys imbricata 82,000 Rueda Almonacid et al. (2007) X Verı́ssimo et al. (2012); Arroyo-Arce
and Salom-Pérez (2015)
Lepidochelys olivacea 35,000 Schulz (1975) X Carrillo et al. (2009); Alfaro et al. (2016)
Dermochelyidae
Dermochelys coriacea 408,100 Georges and Fossette (2006) X Troëng (2000); Verı́ssimo et al. (2012);
Arroyo-Arce and Salom-Pérez (2015)

(Junk et al. 2011). This kind of terrestrial movement is 16 species, including A. macrocephala. They can take
common in small and midsized freshwater turtles living in advantage of mass nesting events to transform large
seasonal environments (Bodie and Semlitsch 2000). aquatic chelonians into staple food items as well as of
Chelonia predation by jaguars has been recorded since opportunistic predation. Predation on nesting females can
the early days of Neotropical natural history (e.g., lead to conservation conflicts when the prey species is
Humboldt 1877). Topic of durophagy, however, is the considered threatened. We suggest that further research on
subject of little research (Miranda et al. 2016). Here we jaguars preying on chelonia approach the subject from the
have shown that the jaguar preys on chelonians, including foraging theory point of view (Stephens et al. 2007),
such heavily armored species as the Chelonoidis tortoises, comparing predation with prey abundance.
and also small species. The study also extends knowledge
of such predation to marine turtles, which are extensively Acknowledgments. — We would like to thank
preyed on during the nesting time. Predation events are
Conselho Nacional de Desenvolvimento Cientı́fico e
usually higher during peak nesting season and increase as
Tecnológico (CNPq) for grant 130873/2014-4 (E.M.),
nesting populations increase (Arroyo-Arce and Salom-
Coordenação de Aperfeiçoamento de Pessoal de Nı́vel
Pérez 2015). Predation of nesting marine turtle has been
Superior (CAPES) for the PNPD grant (E.S.B.), and
the subject of intense discussion because of the conserva-
tion concern for the species being preyed on (especially as Panthera Brasil for logistic support. We further thank
they are all reproductive females) (Verı́ssimo et al. 2012; Marina Secco, Sônia Helena Santesso Teixeira de
Arroyo-Arce and Salom-Pérez 2015). This behavior is Mendonça, Rodrigo de Oliveira Lula Salles, Adriano
unique in large Panthera cats, with no other species known Lima Silveira, and Vera Lúcia Ferreira Luz, who kindly
to prey on chelonia to such an extent. offered us the data on Acanthochelys radiolata mass.
Although chelonians have evolved formidable mor-
phological adaptations to avoid predation, the jaguar’s LITERATURE CITED
mandibular adaptions for durophagy appear to have ALFARO, L.D., MONTALVO, V., GUIMARAES, F., SAENZ, C., CRUZ, J.,
surpassed them. Jaguars possess the potential capacity to MORAZAN, F., AND CARRILO, E. 2016. Characterization of attack
kill adults of virtually all chelonian species within their events on sea turtles (Chelonia mydas and Lepudochelys
distribution, and our data indicate that they prey on at least olivácea) by Jaguar (Panthera onca) in Naranjo Sector, Santa
282 CHELONIAN CONSERVATION AND BIOLOGY, Volume 17, Number 2 – 2018

Rosa, National Park, Costa Rica. International Journal of HAYS, G.C., BRODERICK, A.C., GLEN, F., AND GODLEY, B.J. 2002.
Conservation Science 7:101–108. Change in body mass associated with long-term fasting in a
ARROYO-ARCE, S. AND SALOM-PÉREZ, R. 2015. Impacto of jaguar marine reptile: the case of green turtles Chelonia mydas at
Panthera onca (Carnivora: Felidae) predation on marine turtle Ascension Island. Canadian Journal of Zoology 80:1299–
populations in Tortuguero, Caribbean coast of Costa Rica. 1302.
Revista de Biologı́a Tropical 63:815–825. HEITHAUS, M.R., WIRSING, A.J., THOMSON, J.A., AND BURKHOLDER,
ARROYO-ARCE, S., THOMSON, I., HARRISON, E., WILMOTT, S., AND D.A. 2008. A review of lethal and non-lethal effects of
BAKER, G. 2017. First record of jaguar (Panthera onca) predators on adult marine turtles. Journal of Experimental
predation on a loggerhead sea turtle (Caretta caretta) in Marine Biology and Ecology 356:43–51.
Tortuguero National Park, Costa Rica. Herpetology Notes 10: HERREL, A., O’REILLY, J.C., AND RICHMOND, A.M. 2002.
17–18. Evolution of bite performance in turtles. Journal of Evolu-
BENGTSON, S. 2002. Origins and early evolution of predation. tionary Biology 15:1083–1094.
Paleontological Society Papers 8:289–318. HOOGESTEIJN, R. AND HOOGESTEIJN, A. 2005. Manual sobre
BODIE, J.R. AND SEMLITSCH, R.D. 2000. Spatial and temporal use problemas de depredaciáon causadas por grandes felinos en
of floodplain habitats by lentic and lotic species of aquatic hatos ganaderos. Programa de Extensión para Ganaderos.
turtles. Oecologia 122:138–146. Programa de Conservación del Jaguar. Campo Grande:
BRODIE, E.D., JR., FORMANOWICZ, D.R., JR., AND BRODIE, E.D., III. Wildlife Conservation Society, 48 pp.
1991. Predator avoidance and antipredator mechanisms: HUMBOLDT, A. 1877. Personal Narrative of Travels to the
distinct pathways to survival. Ethology Ecology and Evolution Equinoctial Regions of the New Continent During the Years
3:73–77. 1799–1804. New York: AMS Press, 505 pp.
BUMP, J.K., PETERSON, R.O., AND VUCETICH, J.A. 2009. Wolves IVERSON, J.B. 1991. Patterns of survivorship in turtles order
modulate soil nutrient heterogeneity and foliar nitrogen by Testudines. Canadian Journal of Zoology 69:385–391.
configuring the distribution of ungulate carcasses. Ecology 90: JUNK, W.J., NUNES DA CUNHA C., AND DA SILVA, C.J. 2011. The
3159–3167. Pantanal: a large American wetland and its position in
CARO, T. 2005. Antipredator Defenses in Birds and Mammals. limnological theory. In: Junk, W.J., Silva, C.J., Nunes da
Chicago: University of Chicago Press, 592 pp. Cunha, C., and Wantzen, K.M. (Eds.). The Pantanal: Ecology,
CARRILLO, E., FULLER, T.K., AND SAENZ, J.C. 2009. Jaguar Biodiversity and Sustainable Management of a Large
Neotropical Seasonal Wetland. Sofia: Pensoft Publishers, pp.
Panthera onca hunting activity: effects of prey distribution
127–141.
and availability. Journal of Tropical Ecology 25:563–567.
MCBRIDE, R., GIORDANO, A., AND BALLARD, W. 2010. Note on the
CARVALHO, E.A.R., JR., CARVALHO-NETO, C.S., AND PASCHOALINI,
winter diet of jaguars Panthera onca in the Paraguayan
E.L. 2008. Diet of Kinosternon scorpioides in Serra dos Carajás,
Transitional Chaco. Bellbird 4:1–12.
Eastern Amazonia. Herpetological Review 39:283–285.
MIRANDA, E.B.P., MENEZES, J.F.S., AND RHEINGANTZ, M.L. 2016.
CHÁVEZ-TOVAR, J. 2010. Ecologı́a y conservación del jaguar
Reptiles as principal prey? Adaptations for durophagy and
Panthera onca y puma Puma concolor en la región de
prey selection by jaguar (Panthera onca). Journal of Natural
Calakmul y sus implicaciones para la conservación. PhD
History 50:2021–2035.
Thesis, Universidad Nacional Autónoma de México, México
MONTALVO, V.H., ALFARO, L.D., SÁENZ, C., AND CARRILO, E.
City, México.
2014. The jaguar as a potential predator of Kinosternon
CHRISTIANSEN, P. AND ADOLFSSEN, J.S. 2005. Bite forces, canine scorpioides (Linnaeus, 1766). Herpetozoa 27:205–207.
strength and skull allometry in carnivores Mammalia, MOSKOVITS, D. 1988. Sexual dimorphism and population
Carnivora. Journal of Zoology 266:133–151. estimates of the two Amazonian tortoises Geochelone
DA SILVEIRA, R., RAMALHO, E.E., THORBJARNARSON, J.B., AND carbonaria and G denticulata in northwestern Brazil.
MAGNUSSON, W.E. 2010. Depredation by jaguars on caimans Herpetologica 44:209–217.
and importance of reptiles in the diet of jaguar. Journal of ORIHUELA, G., TERBORGH, J., CEBALLOS, N., AND GLANDER, K.
Herpetology 44:418–424. 2014. When top-down becomes bottom up: behaviour of
EMMONS, L. 1989. Jaguar predation on chelonians. Journal of hyperdense howler monkeys Alouatta seniculus trapped on a
Herpetology 23:311–314. 06 ha island. PLoS One 9:e82197.
ERNST, C.H. AND BARBOUR, R.W. 1989. Turtles of the World. PORTELINHA, T., MALVASIO, A., PIÑA, C., AND BERTOLUCI, J. 2014.
Washington, DC: Smithsonian Institution Press, 313 pp. Population structure of Podocnemis expansa (Testudines:
FACHÍN-TERÁN, A. AND VOGT, R. 2004. Estrutura populacional, Podocnemididae) in southern Brazilian Amazon. Copeia 4:
tamanho e razão sexual de Podocnemis unifilis (Testudines, 707–715.
Podocnemididae) no rio Guaporé RO, norte do Brasil. PRADO, H.A. 1969. Contribución al conocimiento de la
Phyllomedusa 3:29–42. morfologı́a, ecologı́a, comportamiento and distribución geo-
GARLA, R.C., SETZ, E.Z.F., AND GOBBI, N. 2001. Jaguar Panthera gráfica de Podocnemis vogli (Testudinata). Revista de la
onca food habits in Atlantic rain forest of southeastern Brazil. Academia Colombiana 13:303–329.
Biotropica 33:691–696. PREISSER, E.L., BOLNICK, D.I., AND BENARD, M.F. 2005. Scared to
GENOVART, M., NEGRE, N., TAVECCHIA, G., BISTUER, A., PARPAL, death? The effects of intimidation and consumption in
L., AND ORO, D. 2010. The young, the weak and the sick: predator-prey interactions. Ecology 86:501–509.
evidence of natural selection by predation. PLoS One 5:e9774. RHODIN, A.G.J., MÉTRAILER, S., VINKE, T., VINKE, S., ARTNER, H.,
GEORGES, J.Y. AND FOSSETTE, S. 2006. Estimating body mass in AND MITTERMEIER, R.A. 2009. Acanthochelys macrocephala
the leatherback turtle Dermochelys coriacea. Marine Ecology (Rhodin, Mittermeier, and McMorris 1984—big-headed
Progress Series 318:255–262. Pantanal swamp turtle, Pantanal swamp turtle. In: Rhodin,
GREENE, H. 1988. Antipredator mechanisms in reptiles. In: Gans, A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A.,
C. and Huey, R.B. (Eds.). Biology of the Reptilia. New York: Buhlmann, K.A., Iverson, J.B., and Mittermeier, R.A. (Eds.).
Alan R. Liss, pp. 11–113. Conservation Biology of Freshwater Turtles and Tortoises: A
 NOTES AND FIELD REPORTS 283

Compilation Project of the IUCN/SSC Tortoise and Freshwa- TROËNG, S. 2000. Prédation of green Chelonia mydas and
ter Turtle Specialist Group. Chelonian Research Monographs leatherback Dermochelys coriacea turtles. Chelonian Conser-
5:040.1–040.8. vation and Biology 3:751–753.
RUEDA-ALMONACID, J.V., CARR, J.L., MITTERMEIER, R.A., RODRÍ- VERÍSSIMO, D., JONES, D., CHAVERRI, R., AND MEYER, S. 2012.
GUEZ-MAHECHA, J.V., MAST, R.B., VOGT, R.C., RHODIN, A.G.J., Jaguar Panthera onca predation of marine turtles: conflict
OSSA-VELÁSQUEZ, J., RUEDA, J.N., AND MITTERMEIER, C.G. between flagship species in Tortuguero, Costa Rica. Oryx 46:
2007. Las tortugas y los cocodrilianos de los paı́ses andinos 340–347.
del Trópico. Bogotá: Conservatión Internacional, 537 pp. WALLER, T., MICUCCI, P., AND RICHARD, E. 1989. Preliminary
SALERA-JUNIOR, G., MALVASIO, A., AND PORTELINHA, T.C.G. 2009. Results of the Research on Biology, Ecology and Conserva-
Avaliação da predação de Podocnemis expansa e Podocnemis tion of the Chelonoidis chilensis (Sensu Lato) Gray, 1870
unifilis Testudines, Podocnemididae no rio Javaés, Tocantins. Tortoise in Argentina. Buenos Aires: Proyecto Tortuga,
Acta Amazonica 39:207–213. Fundación Vida Silvestre Argentina, 43 pp.
SCHULZ, J.P. 1975. Sea turtles nesting in surinam. Zoologische WANG, E., DONATTI, C.I., FERREIRA, V.L., RAIZER, J., AND
Verhandelingen 143:1–143. HIMMELSTEIN, J. 2011. Food habits and notes on the biology
SCOGNAMILLO, D., MAXIT, I.E., SUNQUIST, M., AND POLISAR, J. of Chelonoidis carbonaria Spix 1824 Testudinidae, Chelonia
2003. Coexistence of jaguar Panthera onca and puma Puma in the southern Pantanal, Brazil. South American Journal of
concolor in a mosaic landscape in the Venezuelan llanos. Herpetology 6:11–19.
Journal of Zoology 259:269–279. WATSON, J. 2010. The Golden Eagle. Poyser: Bloomsbury
SEYMOUR, K. 1989. Panthera onca. Mammalian Species 340:1–9. Publishing, 320 pp.
STEPHENS, D., BROWN, J., AND YDENBERG., R. 2007. Foraging:
Behavior and Ecology. Chicago: University of Chicago Press,
Received: 24 April 2018
608 pp.
TABER, A.B., NOVARO, A.J., NERIS, N., AND COLMAN, F.H. 1997. Revised and Accepted: 5 July 2018
The food habits of sympatric jaguar and puma in the Published Online: 18 December 2018
Paraguayan Chaco. Biotropica 29:204–213. Handling Editor: Jeffrey A. Seminoff

View publication stats