Introduction: Reproduction in Crocodilians

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Introduction: Reproduction in Crocodilians
Author(s): Carlos I. Piña Mark E. Merchant and Luciano M. Verdade
Source: South American Journal of Herpetology, 10(1):1-3.
Published By: Brazilian Society of Herpetology
DOI: http://dx.doi.org/10.2994/SAJH-D-15-00006.1
URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-15-00006.1
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Introduction: Reproduction in Crocodilians
Carlos I. Piña1,2,3,*, Mark E. Merchant4, Luciano M. Verdade5
1 Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción, Consejo Nacional de Investigaciones Científicas y Técnicas.
Matteri y España s/n, CP E3105BWA, Diamante, ER, A rgentina.
2 Proyecto Yacaré, Laboratorio de Zoología Aplicada: Anexo Vertebrados (Facultad de Humanidades y Ciencias–Universidad Nacional del Litoral/
Ministerio de Aguas, Ser vicios Públicos y Medio Ambiente), A. del Valle 8700, CP3000, Santa Fe, Argentina.
3 Facultad de Ciencias y Tecnología, Universidad Autónoma de Entre Ríos, Diamante, ER, Argentina.
4 Department of Chemistry, McNeese State University, Box 90455, Lake Charles, LA 70609, USA.
5 Laboratório de Ecologia Isotópica, Centro de Energia Nuclear na A gricultura, Universidade de São Paulo. Avenida Centenário, 303, Caixa Postal 96,
CEP 13400–970, Piracicaba, SP, Brazil.
* Corresponding author. Email: cidcarlos@infoaire.com.ar
etal., 2013), and multiple paternity appears to be com-
mon, although reproduction tends to be limited to a few
dominant males (Zucoloto et al., 2006, 2009; Amavet
etal., 2008; McVay etal., 2008; Lance etal., 2009b; Budd
etal., 2015). So far, all extant crocodilian species studied
exhibit temperature-dependent sex determination (Piña
etal., 2003, 2007b; Deeming, 2004). We have also learned
that weather conditions appear to influence the repro-
ductive efforts of females (Lance etal., 2009a; Simoncini
etal., 2011), and that a great portion of the reproductive
energy is usually lost due to nest predation or hatchling
mortality during the first year of life (Larriera and Piña,
2000; Platt etal., 2008; Somaweera etal., 2013; Mazzotti
etal., 2014; Parachú-Marcó etal., 2015a).
This issue of the South American Journal of Herpetol-
ogy is dedicated to crocodilian reproduction and is derived
from a series of papers presented at the 23rd Working
Meeting of the Crocodile Specialist Group, held in Lake
Charles, Louisiana, USA, in May 2014. These papers in-
clude studies on diverse crocodilian species and topics, all
of them related to reproduction.
Two studies (Parachú Marcó etal., 2015b; Iungman
etal., 2015) are related to stress hormones (or their syn-
thetic homologues) and their possible effects on develop-
ment and sexual determination. Stress hormones do not
appear to affect sexual determination (at least at the stud-
ied dosage and time of application), but the synthetic ho-
mologues increased the body size of hatchlings. Such re-
sults can be relevant in ranching and farming operations.
Two other papers provide novel information on the
reproduction of crocodiles on oceanic islands, where they
present a high mortality rate of hatchlings (Balaguera
Reina etal., 2015). Budd etal. (2015) report that mate fi-
delity and high relatedness values could be a consequence
of the smaller number of adult crocodiles in those popula-
tions or an indication of a small local number of dominant
males.
Moore and Kelly (2015) describe the histological
structure and functionality of the American alligator phal-
lus. This study reveals that the crocodilian penis contains
rigid structures in order to facilitate cloacal intromission
Crocodilians were used for medicinal and religious
purposes by the Aztecs and the Mayas in the Americas
and the Egyptians in Africa. Romans printed figures of
crocodiles on their coins, and images of crocodiles appear
in stone on the temples of Angkor Wat in Cambodia. More
recent cultures have overhunted crocodiles for their skin.
As a result, by the 1970s all crocodilian species had been
included in AppendixI of the Convention on Internation-
al Trade in Endangered Species, with consequent banning
of their international trade.
Currently, most populations have recovered and are
being exploited under regulated sustainable programs. It
is known that populations can be subjected to manage-
ment if the number of reproductive females is not reduced
(Abercrombie and Verdade, 1995), both in ranching pro-
grams based on the collection of eggs or hatchlings from
wild populations of Alligator mississippiensis (Daudin,
1802) in the USA (Elsey etal., 2001; Elsey and Woodward,
2010), Caiman latirostris (Daudin, 1802) and Caiman ya-
care (Daudin, 1802) in Argentina (Larriera et al., 2008),
Crocodylus porosus Schneider, 1801 in Australia (Webb
et al., 2010), and Crocodylus niloticus Laurenti, 1768 in
many African countries (Fergusson, 2010), and hunting
programs of Alligator missippiensis in the USA (Elsey and
Woodward, 2010), Caiman crocodilus (Linneaus, 1758) in
Venezuela (Velasco and Ayarzagüena, 2010), Caiman ya-
care in Bolivia (Campos etal., 2010), and Crocodylus niloti-
cus in many African countries (Fergusson, 2010). Farming
operations (i.e., closed production cycle) are also carried
out with crocodilians in many countries (e.g., Verdade,
2001a). In these three types of management systems
(ranching, hunting, and farming) it is necessary to main-
tain sustainable levels of reproduction.
Since the 1970s, our understanding of reproduction
in crocodilians has increased considerably. We now know
that both males and females take a relatively long time to
reach sexual maturity (Verdade etal., 2003, Larriera etal.,
2006; Platt et al., 2008; Lance et al., 2015)—although
they have significant sexual dimorphism (Verdade 2001b;
Verdade, 2003; Piña etal., 2007a)—females guard nests
and hatchlings (Charruau and Hénaut, 2012; Somaweera
South American Journal of Herpetology, 10(1), 2015, 1–3
© 2015 Brazilian Society of Herpetology
Submitted: 14 April 2015
Accepted: 21 April 2015
Handling Editor: Taran Grant
doi: 10.2994/SAJH-D-15-00006.1
10(1), 2015, 1
14 April 2015
21 April 2015
Taran Grant
10.2994/SAJH-D-15-00006.1

latirostris in Santa Fe, Argentina. Journal of Experimental Zoolog y Part
A: Ecological Genetics and Physiology 309:637–642. doi:10.1002/jez .496
Balaguera-Reina S.A., Venegas-Anaya M., Sanjur O.I., Lessios
H.A., Densmore L.D. III. 2015. Reproductive ecology and
hatchlings’ growth rates of American Crocodile (Crocodylus acutus)
on Coiba Island, Panama. South American Journal of Herpetology
10:10–22. doi:10.2994/SAJH-D-14-00024.1
Budd K.M., Spotila J.R., Mauger L.A. 2015. Preliminary mating
analysis of American Crocodiles, Crocodylus acutus, in Las Baulas,
Santa Rosa, and Palo Verde National Parks, Guanacaste, Costa
Rica. South American Journal of Herpetology 10:4–9. doi:10.2994/
SAJH-D-14-00022.1
Campos Z., Llobet A., Piña C.I. Magnusson W.E. 2010. Yacare
Caiman Caiman yacare. Pp. 23–28, in Manolis S.C., Stevenson C.
(Eds.), Crocodiles. Status Survey and Conservation Action Plan.
Third Edition, Crocodile Specialist Group: Darwin.
Charruau P., Hénaut Y. 2012. Nest attendance and hatchling care
in wild American crocodiles (Crocodylus acutus) in Quintana Roo,
Mexico. Animal Biology 62:29–51. doi:10.1163/157075511X597629
Daudin F.M. 1802. Histoire Naturelle, Générale et Particulière des
Reptiles; ouvrage faisant suit à l’Histoire naturell générale et
particulière, composée par Leclerc de Buffon; et rédigee par C.S.
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Paris.
Deeming D.C. 2004. Prevalence of TSD in crocodilians. Pp. 33–41,
in Valenzuela N., Lance V.A. (Eds.), Temperature Dependent Sex
Determination in Vertebrates. Smithsonian Books, Washington.
Elsey R.M., McNease L., Joanen T. 2001. Louisiana’s alligator
ranching programme: a review and analysis of releases of captive-
raised juveniles. Pp.426–441, in Grigg G.C., Seebacher F., Franklin
C.E. (Eds.), Crocodilian Biology and Evolution. Surrey Beatty &
Sons, Chipping Norton.
Elsey R.M., Woodward A.R. 2010. American alligator Alligator
mississippiensis. Pp. 1–4, in Manolis S.C., Stevenson C. (Eds.),
Crocodiles. Status Survey and Conservation Action Plan. Third
Edition, Crocodile Specialist Group: Darwin.
Fergusson R.A. 2010. Nile crocodile Crocodylus niloticus. Pp. 84–89,
in Manolis S.C., Stevenson C. (Eds.), Crocodiles. Status Survey
and Conservation Action Plan. Third Edition, Crocodile Specialist
Group: Darwin.
Iungman J.L., Somoza G.M., Piña C.I. 2015. Are stress-
related hormones involved in the temperature-dependent sex
determination of the Broad-Snouted Caiman? South Amarican
Journal of Herpetology 10:41–49. doi:10.2994/SAJH-D-14-00027.1
Lance V.A., Rostal, D.C., Elsey, R.M., Trosclair P.L. III. 2009a.
Ultrasonography of reproductive structures and hormonal correlates
of follicular development in female American alligators, Alligator
mississippiensis, in southwest Louisiana. General and Comparative
Endocrinology 162:251–256. doi:10.1016/j.ygcen.2009.03.021
Lance S.L., Tuberville T.D., Dueck L., Holz-Schietinger C.,
Trosclair P.L. III, Elsey R.M., Glenn T.C. 2009b. Multiyear
multiple paternity and mate fidelity in the American alligator,
Alligator mississippiensis. Molecular Ecology 18:4508–4520.
doi:10.1111/j.1365-294X.2009.04373.x.
Lance V.A., Elsey R.M., Trosclair P.L. III. 2015. Sexual maturity in
male alligator in southwest Louisiana. South American Journal of
Herpetolog y 10:58–63. doi:10.2994/SAJH-D-15-00005.1.
Larriera A., Piña, C.I. 2000. Caiman latirostris (broad-snouted
caiman) nest predation: does low rainfall facilitate predator access?
Herpetological Natural History 7:73–77.
Larriera A., Imhof A., Siroski P. 2008. Estado actual de los programas
de conservación y manejo del género Caiman en Argentina. Pp.143–
179, in Castroviejo J., Ayarzaguena J., Velasco A. (Eds.), Contribución
al Conocimiento de los Caimanes del Género Caiman de Suramérica.
Publicaciones de la Asociación Amigos de Doñana 18, Seville.
Larriera A., Siroski P., Piña C.I., Imhof A. 2006. Sexual maturity
of farm-released Caiman latirostris (Crocodylia: Alligatoridae) in the
wild. Herpetological Review 37:26–28.
and that the sulcus spermaticus (i.e., the open groove
that runs along the ventral aspect of the phallic shaft) is
a spatially heterogeneous reproductive structure contain-
ing a complex architecture of multiple tissue types, and
its morphology changes from its proximal origin between
the crurae to its distal exit from the phallus tip.
Studies of reproduction in the wild are usually diffi-
cult to conduct, but new technologies can now help us un-
derstand many aspects of crocodilian reproduction that
have been obscure until recently. Portelinha etal. (2015)
used radio transmitters to follow reintroduced females
and compared their behavior to wild females. These au-
thors also used echographic images and hormone profiles
to understand egg development. Their results show that
wild and reintroduced females seem to have similar be-
havior, with 35–50% of females reproducing per year on
average and ovulation occurring one or two months be-
fore nesting. Lance etal. (2015) describe the onset of sex-
ual maturation of male American alligators, with males
presenting a clear cycle of testosterone levels, peaking in
breeding season, but varying ontogenetically.
Crocodilians comprise a group of amazing species
that have faced profound environmental changes over
the course of their long evolutionary history, from the ef-
fects of asteroids to the devastating impact of humans.
Their reproductive biology has shown an incredibly ro-
bust adaptive capacity. Crocodilians are still used as nat-
ural resources in many regions of the world, and, thus,
understanding their reproductive biology is paramount
for maintaining their sustainable use. We hope this the-
matic issue of the South American Journal of Herpetology
on crocodilian reproductive biology can help improve our
knowledge on such an intriguing subject.
ACKNOWLEDGMENTS
We would like to thank all the people involved in
the production of this thematic issue on the reproduction
of crocodilians. In special, we would like to express our
appreciation for the anonymous reviewers and the chief
editor of the journal for their enthusiasm and support.
Last but not least, we would like to thank the Crocodile
Specialist Group for their support during the whole edit-
ing process of this thematic issue of the South American
Journal of Herpetology.
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Introduction: Reproduction in Crocodilians
Carlos I. Piña, Mark E. Merchant, Luciano M. Verdade 3
South American Journal of Herpetology, 10(1), 2015, 1–3