Chelonian Predation by Jaguars (Panthera onca)

Abstract

We present a new record of freshwater turtle predation by the jaguar, Panthera onca, in addition to a current review of chelonian predation by this feline. In total, 16 species of chelonians were predated by jaguars: 3 were terrestrial, 8 freshwater, and 5 marine. Our review revealed that jaguars prey on a large number of chelonians, including heavily armored species, such as the Chelonoidis tortoises, and also small freshwater species.

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NOTES AND FIELD REPORTS
Chelonian Conservation and Biology, 2018, 17(2): 280–283
Ó2018 Chelonian Research Foundation
Chelonian Predation by Jaguars
(Panthera onca)
ELIZA
ˆNGELA SILVA BRITO
1,*
,
EVERTON MIRANDA
2,3
,AND
FERNANDO RODRIGO TORTATO
3,4
1
Herpetology Laboratory, Biodiversity Centre, Institute of
Biosciences, Federal University of Mato Grosso, Av. Fernando
Correa da Costa, 2367, 78060-900, Cuiab ´
a, Mato Grosso, Brazil
[eliz.chelidae@gmail.com];
2
IUCN/SSC Boa and Python Specialist Group, Buenos Aires,
Argentina;
3
Postgraduate Program in Ecology and Biodiversity Conservation,
Federal University of Mato Grosso, Av. Fernando Correa da Costa,
2367, 78060-900, Cuiab ´
a, Mato Grosso, Brazil
[mirandaebp@gmail.com];
4
Panthera, 8 West 40th Street, 18th Floor, New York, New York
10018 USA [ftortato@panthera.org]
*Corresponding author
ABSTRACT. – We present a new record of freshwater
turtle predation by the jaguar, Panthera onca,in
addition to a current review of chelonian predation by
this feline. In total, 16 species of chelonians were
predated by jaguars: 3 were terrestrial, 8 freshwater,
and 5 marine. Our review revealed that jaguars prey
on a large number of chelonians, including heavily
armored species, such as the Chelonoidis tortoises, and
also small freshwater species.
Predation is acknowledged as one of the main forces
of natural selection. It is involved in the regulation of a
diverse range of evolutionary and ecological processes,
including Cambrian diversity explosion (Bengtson 2002),
top-down population regulation (Orihuela et al. 2014),
landscape-level soil nutrient distribution (Bump et al.
2009), habitat use of a variety of prey species (Preisser et
al. 2005), and natural selection itself (Genovart et al.
2010). Being such a strong selective force, predation has
been responsible for a variety of adaptations in prey
species. A large and continually growing body of research
has focused on this subject (Greene 1988; Caro 2005), and
a general classification of antipredator defenses separates
prey strategies into 2 main classes (Brodie et al. 1991):
predation avoidance by flight, being constantly vigilant
and morphologically adapted to escape via speed (passer-
ines, most monkeys, iguanids), and prey that is able to
confront (peccaries, boars, skunks) or physically resist
predators (armadillos, tortoises).
Among the most remarkable adaptations of physical
resistance to predation are the shells developed by
chelonians. Formed by the fusion of vertebras, ribs, and
sternal bones, this unique development has been the basis
of the group’s evolutionary success. Living chelonians can
be found in nearly every major ecosystem on Earth, except
those of the polar regions (Ernst and Barbour 1989). The
shell is often complemented by spiny scutes on the legs
and has the ability to house the retracted legs and head.
Predators have developed a variety of strategies to
overcome this suite of defensive measures, including
member amputation (Heithaus et al. 2008), dropping
animals from the air or cliffs (Watson 2010), and direct
shell destruction (Salera-Junior et al. 2009). Despite this,
adults of most chelonian species suffer low mortality
(Iverson 1991). However, Panthera onca (jaguar) is well
known for preying on chelonia (Da Silveira et al. 2010).
Their heads show several characteristics relating to
durophagy, including thick canines and large masseter
and temporal muscles (Seymour 1989) and one of the
strongest bites relative to body size in the genus Panthera
(Christiansen and Adolfssen 2005).
Here we review chelonian species preyed on by
jaguars in order to provide to other researchers authors
with a current, single-source review of chelonian predation
by jaguars. We also synthesize information on body size
and reproductive condition of chelonia that are preyed on
by jaguars. In addition, we report the first record of
predation on Acanthochelys macrocephala by jaguar.
A search of the literature concerning interactions
between jaguars and turtles was performed using Google
Scholar. We used the key words jaguar, P. onca, and on¸ca-
pintada combined with diet, feeding habits, food habits,
h´
abitos alimentarios, and dieta. This allowed us to find
published and unpublished information in English,
Portuguese, and Spanish.
In September 2014, we found a dead adult individual
of A. macrocephala on the Transpantaneira Park Road (lat
17816047 00 S, long 56852016 00 W, WGS84), located within
the Brazilian Pantanal wetlands of the Paraguay River
basin. Acanthochelys macrocephala is a medium-sized
freshwater turtle that lives in marshes, wetland areas,
shallow bays, and brackish lagoons (Rhodin et al. 2009).
The individual was found on dry land, with visible bite
marks on the carapace, and jaguar tracks were found at the
site. The distance between canines (.70 mm) marked on
the carapace was consistent with that of a jaguar bite
(Hoogesteijn and Hoogesteijn 2005), confirming the
predator’s identity.
In addition, our search revealed records of jaguar
predation on 15 species of chelonia, totaling 16 with the
addition of A. macrocephala (Table 1). Of these, 3 species
were terrestrial, 8 freshwater, and 5 marine. The latter were
killed during nesting times, as were the large freshwater
species, which usually nest in large numbers on beaches.
Small chelonia, such as A. macrocephala, can be
considered a rare prey of jaguars because this turtle
occasionally moves onto dry land to migrate to other water
bodies, as these bodies of water are not always connected

(Junk et al. 2011). This kind of terrestrial movement is
common in small and midsized freshwater turtles living in
seasonal environments (Bodie and Semlitsch 2000).
Chelonia predation by jaguars has been recorded since
the early days of Neotropical natural history (e.g.,
Humboldt 1877). Topic of durophagy, however, is the
subject of little research (Miranda et al. 2016). Here we
have shown that the jaguar preys on chelonians, including
such heavily armored species as the Chelonoidis tortoises,
and also small species. The study also extends knowledge
of such predation to marine turtles, which are extensively
preyed on during the nesting time. Predation events are
usually higher during peak nesting season and increase as
nesting populations increase (Arroyo-Arce and Salom-
P´
erez 2015). Predation of nesting marine turtle has been
the subject of intense discussion because of the conserva-
tion concern for the species being preyed on (especially as
they are all reproductive females) (Ver´
ıssimo et al. 2012;
Arroyo-Arce and Salom-P´
erez 2015). This behavior is
unique in large Panthera cats, with no other species known
to prey on chelonia to such an extent.
Although chelonians have evolved formidable mor-
phological adaptations to avoid predation, the jaguar’s
mandibular adaptions for durophagy appear to have
surpassed them. Jaguars possess the potential capacity to
kill adults of virtually all chelonian species within their
distribution, and our data indicate that they prey on at least
16 species, including A. macrocephala. They can take
advantage of mass nesting events to transform large
aquatic chelonians into staple food items as well as of
opportunistic predation. Predation on nesting females can
lead to conservation conflicts when the prey species is
considered threatened. We suggest that further research on
jaguars preying on chelonia approach the subject from the
foraging theory point of view (Stephens et al. 2007),
comparing predation with prey abundance.
Acknowledgments. — We would like to thank
Conselho Nacional de Desenvolvimento Cient´
ıfico e
Tecnol´
ogico (CNPq) for grant 130873/2014-4 (E.M.),
Coordena¸c˜
ao de Aperfei¸coamento de Pessoal de N´
ıvel
Superior (CAPES) for the PNPD grant (E.S.B.), and
Panthera Brasil for logistic support. We further thank
Marina Secco, Sˆ
onia Helena Santesso Teixeira de
Mendon¸ca, Rodrigo de Oliveira Lula Salles, Adriano
Lima Silveira, and Vera L ´
ucia Ferreira Luz, who kindly
offered us the data on Acanthochelys radiolata mass.
LITERATURE CITED
ALFARO, L.D., MONTALVO, V., GUIMARAES, F., SAENZ, C., CRUZ, J.,
MORAZAN, F., AND CARRILO, E. 2016. Characterization of attack
events on sea turtles (Chelonia mydas and Lepudochelys
oliv ´
acea) by Jaguar (Panthera onca) in Naranjo Sector, Santa
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) Ch´
avez-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 Fach´
ın-Ter´
an 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 Tro¨
eng (2000); Carrillo et al. (2009);
Ver´
ıssimo et al. (2012); Arroyo-Arce
and Salom-P´
erez (2015); Alfaro et al.
(2016)
Eretmochelys imbricata 82,000 Rueda Almonacid et al. (2007) X Ver´
ıssimo et al. (2012); Arroyo-Arce
and Salom-P´
erez (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 Tro¨
eng (2000); Ver´
ıssimo et al. (2012);
Arroyo-Arce and Salom-P´
erez (2015)
NOTES AND FIELD REPORTS 281

Rosa, National Park, Costa Rica. International Journal of
Conservation Science 7:101–108.
ARROYO-ARCE,S.AND SALOM-PE
´REZ, R. 2015. Impacto of jaguar
Panthera onca (Carnivora: Felidae) predation on marine turtle
populations in Tortuguero, Caribbean coast of Costa Rica.
Revista de Biolog´
ıa Tropical 63:815–825.
ARROYO-ARCE, S., THOMSON, I., HARRISON, E., WILMOTT, S., AND
BAKER, G. 2017. First record of jaguar (Panthera onca)
predation on a loggerhead sea turtle (Caretta caretta)in
Tortuguero National Park, Costa Rica. Herpetology Notes 10:
17–18.
BENGTSON, S. 2002. Origins and early evolution of predation.
Paleontological Society Papers 8:289–318.
BODIE, J.R. AND SEMLITSCH, R.D. 2000. Spatial and temporal use
of floodplain habitats by lentic and lotic species of aquatic
turtles. Oecologia 122:138–146.
BRODIE, E.D., JR., FORMANOWICZ, D.R., JR., AND BRODIE, E.D., III.
1991. Predator avoidance and antipredator mechanisms:
distinct pathways to survival. Ethology Ecology and Evolution
3:73–77.
BUMP, J.K., PETERSON, R.O., AND VUCETICH, J.A. 2009. Wolves
modulate soil nutrient heterogeneity and foliar nitrogen by
configuring the distribution of ungulate carcasses. Ecology 90:
3159–3167.
CARO, T. 2005. Antipredator Defenses in Birds and Mammals.
Chicago: University of Chicago Press, 592 pp.
CARRILLO, E., FULLER, T.K., AND SAENZ, J.C. 2009. Jaguar
Panthera onca hunting activity: effects of prey distribution
and availability. Journal of Tropical Ecology 25:563–567.
CARVALHO, E.A.R., JR., CARVALHO-NETO, C.S., AND PASCHOALINI,
E.L. 2008. Diet of Kinosternon scorpioides in Serra dos Caraj´
as,
Eastern Amazonia. Herpetological Review 39:283–285.
CHA
´VEZ-TOVAR, J. 2010. Ecolog´
ıa y conservaci´
on del jaguar
Panthera onca y puma Puma concolor en la regi´
on de
Calakmul y sus implicaciones para la conservaci ´
on. PhD
Thesis, Universidad Nacional Aut´
onoma de M´
exico, M´
exico
City, M´
exico.
CHRISTIANSEN,P.AND ADOLFSSEN, J.S. 2005. Bite forces, canine
strength and skull allometry in carnivores Mammalia,
Carnivora. Journal of Zoology 266:133–151.
DASILVEIRA, R., RAMALHO, E.E., THORBJARNARSON, J.B., AND
MAGNUSSON, W.E. 2010. Depredation by jaguars on caimans
and importance of reptiles in the diet of jaguar. Journal of
Herpetology 44:418–424.
EMMONS, L. 1989. Jaguar predation on chelonians. Journal of
Herpetology 23:311–314.
ERNST, C.H. AND BARBOUR, R.W. 1989. Turtles of the World.
Washington, DC: Smithsonian Institution Press, 313 pp.
FACHI
´N-TERA
´N,A.AND VOGT, R. 2004. Estrutura populacional,
tamanho e raz˜
ao sexual de Podocnemis unifilis (Testudines,
Podocnemididae) no rio Guapor ´
e RO, norte do Brasil.
Phyllomedusa 3:29–42.
GARLA, R.C., SETZ, E.Z.F., AND GOBBI, N. 2001. Jaguar Panthera
onca food habits in Atlantic rain forest of southeastern Brazil.
Biotropica 33:691–696.
GENOVART, M., NEGRE, N., TAVECCHIA, G., BISTUER, A., PARPAL,
L., AND ORO, D. 2010. The young, the weak and the sick:
evidence of natural selection by predation. PLoS One 5:e9774.
GEORGES, J.Y. AND FOSSETTE, S. 2006. Estimating body mass in
the leatherback turtle Dermochelys coriacea. Marine Ecology
Progress Series 318:255–262.
GREENE, H. 1988. Antipredator mechanisms in reptiles. In: Gans,
C. and Huey, R.B. (Eds.). Biology of the Reptilia. New York:
Alan R. Liss, pp. 11–113.
HAYS, G.C., BRODERICK, A.C., GLEN, F., AND GODLEY, B.J. 2002.
Change in body mass associated with long-term fasting in a
marine reptile: the case of green turtles Chelonia mydas at
Ascension Island. Canadian Journal of Zoology 80:1299–
1302.
HEITHAUS, M.R., WIRSING, A.J., THOMSON, J.A., AND BURKHOLDER,
D.A. 2008. A review of lethal and non-lethal effects of
predators on adult marine turtles. Journal of Experimental
Marine Biology and Ecology 356:43–51.
HERREL,A.,O’REILLY, J.C., AND RICHMOND,A.M.2002.
Evolution of bite performance in turtles. Journal of Evolu-
tionary Biology 15:1083–1094.
HOOGESTEIJN,R.AND HOOGESTEIJN, A. 2005. Manual sobre
problemas de depredaci´
aon causadas por grandes felinos en
hatos ganaderos. Programa de Extensi ´
on para Ganaderos.
Programa de Conservaci´
on del Jaguar. Campo Grande:
Wildlife Conservation Society, 48 pp.
HUMBOLDT, A. 1877. Personal Narrative of Travels to the
Equinoctial Regions of the New Continent During the Years
1799–1804. New York: AMS Press, 505 pp.
IVERSON, J.B. 1991. Patterns of survivorship in turtles order
Testudines. Canadian Journal of Zoology 69:385–391.
JUNK, W.J., NUNES DA CUNHA C., AND DA SILVA, C.J. 2011. The
Pantanal: a large American wetland and its position in
limnological theory. In: Junk, W.J., Silva, C.J., Nunes da
Cunha, C., and Wantzen, K.M. (Eds.). The Pantanal: Ecology,
Biodiversity and Sustainable Management of a Large
Neotropical Seasonal Wetland. Sofia: Pensoft Publishers, pp.
127–141.
MCBRIDE, R., GIORDANO, A., AND BALLARD, W. 2010. Note on the
winter diet of jaguars Panthera onca in the Paraguayan
Transitional Chaco. Bellbird 4:1–12.
MIRANDA, E.B.P., MENEZES, J.F.S., AND RHEINGANTZ, M.L. 2016.
Reptiles as principal prey? Adaptations for durophagy and
prey selection by jaguar (Panthera onca). Journal of Natural
History 50:2021–2035.
MONTALVO, V.H., ALFARO, L.D., SA
´ENZ, C., AND CARRILO,E.
2014. The jaguar as a potential predator of Kinosternon
scorpioides (Linnaeus, 1766). Herpetozoa 27:205–207.
MOSKOVITS, D. 1988. Sexual dimorphism and population
estimates of the two Amazonian tortoises Geochelone
carbonaria and G denticulata in northwestern Brazil.
Herpetologica 44:209–217.
ORIHUELA, G., TERBORGH, J., CEBALLOS, N., AND GLANDER,K.
2014. When top-down becomes bottom up: behaviour of
hyperdense howler monkeys Alouatta seniculus trapped on a
06 ha island. PLoS One 9:e82197.
PORTELINHA, T., MALVASIO, A., PIN
˜A, C., AND BERTOLUCI, J. 2014.
Population structure of Podocnemis expansa (Testudines:
Podocnemididae) in southern Brazilian Amazon. Copeia 4:
707–715.
PRADO, H.A. 1969. Contribuci ´
on al conocimiento de la
morfolog´
ıa, ecolog´
ıa, comportamiento and distribuci´
on geo-
gr´
afica de Podocnemis vogli (Testudinata). Revista de la
Academia Colombiana 13:303–329.
PREISSER, E.L., BOLNICK, D.I., AND BENARD, M.F. 2005. Scared to
death? The effects of intimidation and consumption in
predator-prey interactions. Ecology 86:501–509.
RHODIN, A.G.J., ME
´TRAILER, S., VINKE, T., VINKE, S., ARTNER, H.,
AND MITTERMEIER, R.A. 2009. Acanthochelys macrocephala
(Rhodin, Mittermeier, and McMorris 1984—big-headed
Pantanal swamp turtle, Pantanal swamp turtle. In: Rhodin,
A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A.,
Buhlmann, K.A., Iverson, J.B., and Mittermeier, R.A. (Eds.).
Conservation Biology of Freshwater Turtles and Tortoises: A
282 CHELONIAN CONSERVATION AND BIOLOGY,Volume 17, Number 2 – 2018

Compilation Project of the IUCN/SSC Tortoise and Freshwa-
ter Turtle Specialist Group. Chelonian Research Monographs
5:040.1–040.8.
RUEDA-ALMONACID, J.V., CARR, J.L., MITTERMEIER, R.A., RODRI
´-
GUEZ-MAHECHA, J.V., MAST, R.B., VOGT, R.C., RHODIN, A.G.J.,
OSSA-VELA
´SQUEZ, J., RUEDA, J.N., AND MITTERMEIER, C.G.
2007. Las tortugas y los cocodrilianos de los pa´
ıses andinos
del Tr´
opico. Bogot´
a: Conservati´
on Internacional, 537 pp.
SALERA-JUNIOR, G., MALVASIO, A., AND PORTELINHA, T.C.G. 2009.
Avalia¸c˜
ao da preda¸c˜
ao de Podocnemis expansa ePodocnemis
unifilis Testudines, Podocnemididae no rio Java´
es, Tocantins.
Acta Amazonica 39:207–213.
SCHULZ, J.P. 1975. Sea turtles nesting in surinam. Zoologische
Verhandelingen 143:1–143.
SCOGNAMILLO, D., MAXIT, I.E., SUNQUIST, M., AND POLISAR,J.
2003. Coexistence of jaguar Panthera onca and puma Puma
concolor in a mosaic landscape in the Venezuelan llanos.
Journal of Zoology 259:269–279.
SEYMOUR, K. 1989. Panthera onca. Mammalian Species 340:1–9.
STEPHENS, D., BROWN, J., AND YDENBERG., R. 2007. Foraging:
Behavior and Ecology. Chicago: University of Chicago Press,
608 pp.
TABER, A.B., NOVARO, A.J., NERIS, N., AND COLMAN, F.H. 1997.
The food habits of sympatric jaguar and puma in the
Paraguayan Chaco. Biotropica 29:204–213.
TROE
¨NG, S. 2000. Pr´
edation of green Chelonia mydas and
leatherback Dermochelys coriacea turtles. Chelonian Conser-
vation and Biology 3:751–753.
VERI
´SSIMO, D., JONES, D., CHAVERRI, R., AND MEYER, S. 2012.
Jaguar Panthera onca predation of marine turtles: conflict
between flagship species in Tortuguero, Costa Rica. Oryx 46:
340–347.
WALLER, T., MICUCCI, P., AND RICHARD, E. 1989. Preliminary
Results of the Research on Biology, Ecology and Conserva-
tion of the Chelonoidis chilensis (Sensu Lato) Gray, 1870
Tortoise in Argentina. Buenos Aires: Proyecto Tortuga,
Fundaci´
on Vida Silvestre Argentina, 43 pp.
WANG, E., DONATTI,C.I.,FERREIRA,V.L.,RAIZER,J.,AND
HIMMELSTEIN, J. 2011. Food habits and notes on the biology
of Chelonoidis carbonaria Spix 1824 Testudinidae, Chelonia
in the southern Pantanal, Brazil. South American Journal of
Herpetology 6:11–19.
WATSON, J. 2010. The Golden Eagle. Poyser: Bloomsbury
Publishing, 320 pp.
Received: 24 April 2018
Revised and Accepted: 5 July 2018
Published Online: 18 December 2018
Handling Editor: Jeffrey A. Seminoff
NOTES AND FIELD REPORTS 283