8/2/2019 0022-1511%282007%2941%5B164%3ANOTBCM%5D2.0

1/4

SHORTER COMMUNICATIONS

Journal of Herpetology, Vol. 41, No. 1, pp. 164167, 2007Copyright 2007 Society for the Study of Amphibians and Reptiles

Nesting of the Black Caiman (Melanosuchus niger) in Northeastern Ecuador

FRANCISCO VILLAMARIN-JURADO1,2 AND ESTEBAN SUAREZ3

1Escuela de Ciencias Biologicas, Pontificia Universidad Catolica del Ecuador, Quito, Ecuador3Wildlife Conservation Society, Ecuador Program, Quito, Ecuador

ABSTRACT.Seven Black Caiman (Melanosuchus niger) nests were located and monitored at Limoncochaand Anangu lagoons (northeastern Ecuador), between October 2002 and March 2003. Melanosuchus nigernesting coincided with the annual low water level season in the Ecuadorian Amazon. Mean number of eggsper nest was 28 and 34 eggs at Limoncocha and Anangu, respectively. Egg chamber temperature wasmonitored in two nests during the incubation period and showed no relationship with external airtemperature, suggesting that the nests have their own heating sources. Mean hatching success was 42.4%, andflooding of the nests was identified as the main cause of egg mortality (29% of all the eggs).

Although knowledge about the natural history ofSouth American crocodilians has increased over the

last few decades, conservation of this group is stillhampered by the lack of information on their basicecology and habitat requirements in the broad di-versity of environmental conditions in which theylive. This is particularly true for species such as theBlack Caiman (Melanosuchus niger) in the northwest-ern limit of its distributional range, where animals areexposed to different environmental conditions thanthose found in countries where most previous studieshave been carried out, including Brazil (Brazaitis et al.,1996; Da Silveira et al., 1997; Da Silveira andMagnusson, 1999; Rebelo and Lugli, 2001) and Peru(Herron et al., 1990; Herron, 1991, 1994). Studies onBlack Caiman nesting biology have been carried out inCocha Cashu (Peruvian Amazon), where the nesting

behavior was thoroughly described for the first time(Herron et al., 1990). In the Mamiraua Reserve(Brazilian Amazon), one of the most extensive studieson Caiman crocodilus and Melanosuchus niger nesting

biology is being carried out (R. Da Silveira and J.Thorbjarnarson, unpubl. data).

In Ecuador, the nesting biology of this threatenedspecies is almost unknown, and we only haveanecdotal information provided by Medem (1983)and a partial description of two nests in the CuyabenoReserve (Asanza, 1985). According to the IUCNs RedList of Ecuadorian Reptiles, the Black Caiman is

considered VU A1bd (Endara and Villamarn-Jurado,2005). Based on population surveys in several areas ofthe Ecuadorian Amazon (T. Hines and K. Rice, AReport on an Initial Survey Effort to Assess the Statusof Black Caiman Melanosuchus niger in the Amazonregion of Ecuador, Unpubl., 1992; T. Hines and K.Rice, A Report on a Survey Effort to Assess the Statusof Black Caiman Melanosuchus niger in the AmazonRegion of Ecuador, Unpubl., 1994), Ecuadorian popu-lations were downlisted to CITES Appendix II in1995, subject to a ranching program with zero exportquota (UNEP-WCMC Species Database: CITES-ListedSpecies http://www.unep-wcmc.org/isdb/CITES/Taxonomy/index.cfmon the World Wide Web:

http://www.unep-wcmc.org/isdb/CITES/Taxonomy/tax-species-result.cfm?displaylanguage5eng&source5

animals&Species5%25niger%25&Genus5Melanosuchus&Country5,2006). In recent years, however, this pro-gram languished and failed (Villamarn-Jurado,2006).

We report on the monitoring of seven Black Caimannests studied between October 2002 and March 2003.Our main objective was to describe Black Caimannesting in the Limoncocha Biological Reserve (LBR)(76u3792.60W; 0u24912.20S) and Anangu Lagoon, inthe Yasun National Park (YNP) (76u26915.00W;0u31914.60S). Specifically, our goals were (1) tocharacterize the nests and nesting sites; (2) to recordaspects of parental care, predation, and nest flooding;and (3) to determine the hatching success of the eggs.

MATERIALS AND METHODS

Starting on October 2002, the margins of Limonco-cha and Anangu lagoons were searched for activeBlack Caiman nests. The vegetation at the study siteshas been classified as Lowland Evergreen Forestinundated by white water (Varzea, Limoncocha) and

black water rivers (Igapo, Limoncocha and Anangu)(Palacios et al., 1999). The shores of both lagoons aredominated by emergent vegetation where Montrichar-dia linifera (Araceae), Mauritiella aculeata (Arecaceae),and Poaceae and Cyperaceae grasses predominate.

Once a nest was found, its location was recorded

using a Garmin 12XL GPS, and the followingmeasurements were recorded: (1) nest dimensions;(2) length of the longest axis of the area of disturbedground around the nest; (3) distance between the nestand the closest water body; and (4) percentage ofcanopy cover above the nest. After measurement,a sample of four nests (two in each location) wascarefully opened, and the eggs were counted andmarked on their tops, avoiding turning the eggs alongtheir longitudinal axis. For each opened nest, thefollowing measurements were taken: egg chamberdimensions, and the number, linear dimensions, andmass of all the eggs found. Although the floatingvegetation mats in which the nests were found were

very solid, while accessing the nests, we took care toavoid stepping on weak areas that could collapse,increasing the possibility of flooding.

An Optic StowAwayH Data Logger was placedinside two egg chambers (Nests 1A and 4A) and

2 Corresponding Author. Present addres: PasajeKodaly D-52 y Luis de Beethoven, Quito, Ecuador;E-mail: franciscovillamarin@yahoo.com.ar

8/2/2019 0022-1511%282007%2941%5B164%3ANOTBCM%5D2.0

2/4

programmed to record the temperature every 15 min.Additionally, air temperature outside the nests wasrecorded every day at 0700, 1200, and 1800 h, usinga TaylorH Indoor/Outdoor Digital Thermometer,placed 1 m above the nests. Linear regressions wereused to analyze whether a relationship existed

between external air temperature (explanatory vari-able) and corresponding simultaneous measures oftemperature inside each nest (response variable).

Three camera traps (Cam TrakkerTM Watkinsville,GA) were set near two nests in Limoncocha and onenest in Anangu. Additionally, an observation platformwas built between the aerial roots of a tree, approx-imately 15 m from one nest in Limoncocha (Nest 4L).From this platform we carried out systematic ob-servations of the behavior of the adult femaleattending her nest over a two-month period.

At the end of the nesting season, we checked allnests to get a minimum estimate of hatching success(percentage of hatched eggs relative to the total

number of eggs). The minimum number of hatchedcaiman was determined by counting the number ofegg shells left near the nest. Because some of theeggshells of hatched neonates may be carried off bythe female and not left at the nest site, this representsonly a minimum number of successfully hatchedyoung. We also checked for deformed and rotten eggswhich were classified as nonviable eggs. Eggshellswere collected and deposited at the Museo deZoologa, Pontificia Universidad Catolica del Ecuador(QCAZ), Herpetology collection.

RESULTS

Seven Black Caiman nests were found around

Limoncocha (four) and Anangu (three) lagoonsbetween 15 October and 19 November 2002. The nestsare conical mounds constructed with leaf litter androots, with mean dimensions of 1.65 6 0.16 m (meansare given 6 standard deviation; N 5 7) 3 1.37 60.19 m (N5 7), and a mean height of 0.54 6 0.097 m(N 5 7). The mean of the maximum radius of thedisturbed area around the nests was 4.76 6 1.91 m (N5 7), and the mean canopy cover above the nests was80.2 6 5.79% and 85.3 6 5.87% in Limoncocha andAnangu, respectively. The nests remained shadedduring most of the day, but at certain times theyreceived direct solar radiation.

Six nests were located along the lagoons shoreline,on floating mats in permanently inundated areas,where Montrichardia linifera (Araceae) predominates.Only one nest was found in a seasonally inundatedforest (Igapo) area, along a creeks shoreline, where the

Mauritiella aculeata palm predominates.At the Limoncocha site, mean clutch size was 28.0 6

4.83 eggs per nest (range 5 2132), whereas egg lengthand mass averaged 87.87 6 3.66 mm (N5 49; range 585.9397.59 mm) and 142.356 6.09 g (N5 49; range 5130150 g), respectively. At Anangu Lagoon, corre-sponding values for clutch size were 34.0 6 2.00 eggsper nest (range 5 3236; N 5 3), whereas mean egglength and mass were 84.94 6 3.7 mm (N5 66; range5

81.2294.11 mm), and 125.4 6 13.24 g (N5

66;range 5 122.5147.5 g), respectively.

Temperature inside the egg chamber of nest 1Aremained relatively stable with a mean of 31.2 60.74uC. Nest 4A mean chamber temperature (31.2uC)

was very similar to that in nest 1A, but with a slightlygreater variation (6 1.08uC). Mean temperature withinthe egg chamber was more stable and consistentlyhigher than external air temperatures (mean 5 27.9 65.05uC; Fig. 1). Furthermore, linear regressionsshowed that the temperature inside the egg chamberswas not dependent on external air temperature (Nest1A: N5 54; r2 5 0.029; P 5 0.22; and Nest 4A: N5 87;r2 5 0.001; P 5 0.758).

Mean hatching success was 42.4 6 39.0% (range 5095.24%). Flooding of nests in both locations wasidentified as the main cause of egg mortality (29% ofall the eggs). Two nests (one in each location) floodedand, as a result, all the eggs failed to hatch (Nest 4L: N5 30, and Nest 3A: N5 32). Nonviability of eggs was

the second most important cause for hatching failure(22.9%). Additionally, only 0.47% of the eggs were lostto predation by an unidentified mouse (recorded bycamera trap pictures), and 7.94% to suffocation ofhatchlings that pipped from their eggs but could notcome out from the nest as the nesting female did notrelease them. Nests 1A and 4A were abandoned bythe nesting females. No signs of their presence wereregistered during the entire incubation period, noteven when the hatchlings emerged from their eggsand vocalized from inside the nest.

All the nests were found near a water pond. In fournests, the nesting female was observed inside thepond, hidden in the emergent vegetation such asPoaceae grasses and Montrichardia linifera (Araceae),taking care of their nests. Nests in Anangu were muchcloser to the lagoon edge (mean distance 5 17.1 67.2 m; N 5 3) than those in Limoncocha (meandistance5 58.5 6 15.81 m; N5 4).

The presence of the nesting female was detected, bydirect observations, looking for marks left by thefemale, or using cammera traps, in five nests (four inLimoncocha and one in Anangu). Two of the fournesting females in Limoncocha (total female lengthapproximately 2.9 m, estimated by comparing the sizeof the female in pictures to the size of other objects ofknown size) defended their nests by displaying

aggressive behavior (Nests 3L and 4L). On oneoccasion, upon observing the researchers, the femalein nest 3L came out of the water running andremained on the nest with her mouth open and tailraised. In one case, (nest 4L, in Limoncocha) the nest

FIG. 1. Records of temperature in egg chambers ofMelanosuchus niger (Nest 1A and Nest 4A) andexternal air temperatures.

SHORTER COMMUNICATIONS 165

8/2/2019 0022-1511%282007%2941%5B164%3ANOTBCM%5D2.0

3/4

flooded but the attending female remained at the nestfor approximately 15 days after it was inundated.

We obtained a direct record of the hatching processfrom camera trap photographs taken at nest 1L inLimoncocha. The pictures show that the processstarted on the night of 20 January 2003. The femalecame out of the water and lay on top of the nest. Thefollowing morning the female used its jaws and frontfeet to remove the material from the top of the nest,releasing the hatchlings and carrying them to thenearby water. The whole process lasted until noon on21 January.

DISCUSSION

In general terms, the characteristics described herefor the Black Caiman nests in northeastern Ecuador,coincide with the few other descriptions of BlackCaiman nesting (Herron et al., 1990; R. Da Silveira and

J. Thorbjarnarson, unpubl. data). In relation to eggmortality, however, our study found high levels of

mortality caused by flooding, but low levels ofpredation, which is unusual in the existing literatureregarding other crocodilians (e.g., Cintra, 1988; Cam-pos, 1993).

Reported values of clutch size and egg mass forBlack Caiman are very variable between populationsand between individuals within the same population.At Cocha Cashu, Herron et al. (1990) reported a clutchsize of 38 eggs and a mean egg mass of 141.7 g.Medem (1983) suggested that clutch size of BlackCaiman in Ecuador ranges between 40 and 60 eggs. Inthis sense, our results reflect the high variability ofprevious studies, as clutch size in our study sitesranged from 21 and 36 eggs per nest and egg mass

from 90155 g.There was no relationship between egg chamber

and external air temperatures, suggesting that BlackCaiman nests have their own heat sources; thisphenomenon has been previously reported for othercrocodilians for which vegetal material decomposi-tion, metabolic heat of embryos and the proximity totermite mounds (Magnusson et. al., 1985, 1990) werementioned as potential sources of heat for the nests.

Flooding was the most important factor affectingegg survival in our population of Black Caiman,a pattern that was also reported in species such as

Alligator mississippiensis (Kushlan and Jacobsen, 1990),

Caiman crocodilus (Allsteadt, 1994), and Caiman yacare(Cintra, 1988; Campos, 1993), among others. Non-viable eggs was the second most important cause forhatching failure; Allsteadt (1994) suggested that non-viable eggs could be the result of infertility, spoilingfrom extreme temperatures, desiccation, or fungalattack during incubation. A somewhat surprisingfinding was the low incidence of egg predation. Inother crocodilians, such as C. yacare, predation wasresponsible for up to 48.5% (Cintra, 1988) and 35%(Campos, 1993) of egg mortality. Allsteadt (1994) alsofound relatively low rates of eggs lost because ofpredation in A. mississippiensis nests (only four of 32nests were partially depredated). A possible explana-

tion for the low egg predation that we recorded couldbe the scarcity or absence of some of the species thathave been reported as important predators of caimaneggs, such as the jaguar (Pantera onca; R. Da Silveiraand J. Thorbjarnarson, unpubl. data). Jaguars and

other large terrestrial predators are becoming rare inour study area, especially in Limoncocha, which couldpartly explain the low egg predation that we reporthere. Lizards of the genus Tupinambis have also beenidentified as major nest predators (R. Da Silveira and

J. Thorbjarnarson, unpubl. data). Although we gota camera trap picture of a Tupinambis teguixin standing

on top of nest 1L, we did not find conclusive evidenceof this lizard preying on the eggs.

The nesting female in nest 3L showed a combinationof the attacking behavior defined by Cintra (1988) asleaving the water and staying on top of the nestwithout vocalization and swimming vigorously,passing near the nest to attack the investigators. Incontrast, in Anangu, one of the nests was quicklyabandoned by the female, even though it was visitedonly a few times during the incubation period and thedegree of disturbance on this nest was very lowcompared with the others. This nest showed thelowest hatching success of nests that did not flood

(14.7%

), suggesting that the probability of eggmortality increases if the female abandons the nest.Our finding of the importance of flooding as a cause

of hatching failure suggests that further research isneeded to understand the relationship between BlackCaiman recruitment and the unpredictable annualrainfall patterns in northwestern Amazon. This in-formation will become increasingly important as largeareas of lacustrine habitat are disturbed in this regionto allow development of human settlements for oilextraction, agriculture, and tourism infrastructure.

Acknowledgments.This project was funded by theWildlife Conservation Society Program in Ecuador. E.

Silva provided valuable help when planning theproject. We thank the Ministerio del Ambiente delEcuador and Byron Amaya for issuing our researchpermits and providing logistic support, the Universi-dad Catolica for its institutional support and the NapoWildlife Center for lodging and logistic support inAnangu. We are grateful to the Kichwa communitiesin Anangu and Limoncocha for all the knowledgeshared. Many thanks to J. Thorbjarnarson who pro-vided field training and advice during all the phasesof this study and to G. R. Smith and two anonymousreviewers who provided valuable comments onearlier version of this manuscript.

LITERATURE CITED

ALLSTEADT, J. 1994. Nesting ecology of Caiman crocodi-lus in Cano Negro, Costa Rica. Journal of Herpe-tology 28:1219.

ASANZA, E. 1985. Distribucion, biologa reproductiva yalimentacion de cuatro especies de Alligatoridae,especialmente Caiman crocodilus en la Amazonadel Ecuador. Unpubl. bachelors thesis. PontificiaUniversidad Catolica del Ecuador, Quito, Ecuador.

BRAZAITIS, P . , G . H . REBELO, C . YAMASHITA, E . A .ODIERNA, AND M. E. WATANABE. 1996. Threats toBrazilian crocodilian populations. Oryx 30:275

284.CAMPOS, Z. 1993. Effect of habitat on survival of eggs

and sex ratio of hatchlings of Caiman crocodilusyacare in the Pantanal, Brazil. Journal of Herpetol-ogy 27:127132.

166 SHORTER COMMUNICATIONS

8/2/2019 0022-1511%282007%2941%5B164%3ANOTBCM%5D2.0

4/4

CINTRA, R. 1988. Nesting ecology of the ParaguayanCaiman (Caiman yacare) in the Brazilian pantanal.

Journal of Herpetology 22:219222.DA SILVEIRA, R., AND W. E. MAGNUSSON. 1999. Diets of

Spectacled and Black Caiman in the Anavilhanasarchipelago, central Amazonia. Brazilian Journal ofHerpetology 33:181192.

DA SILVEIRA, R., W. E. MAGNUSSON, AND Z. CAMPOS. 1997.Monitoring the distribution, abundance and breed-ing areas of Caiman crocodilus crocodilus and

Melanosuchus niger in the Anavilhanas archipelago,central Amazonia, Brazil. Journal of Herpetology31:514520.

ENDARA, A., AND F. VILLAMARIN-JURADO. 2005. CaimanNegro (Melanosuchus niger). In E. Carrillo, S. Aldas,M. Altamirano, F. Ayala, D. Cisneros, A. Endara,C. Marquez, M. Morales, F. Nogales, P. Salvador,M. L. Torres, J. Valencia, F. Villamarn, M. Yanez,and P. Zarate (eds.), Lista Roja de Reptiles delEcuador, p. 20. Fundacion Novum Millenium,UICN-Sur, UICN-Comite Ecuatoriano, Ministeriode Educacion y Cultura. Serie Proyecto PEEPE,Quito, Ecuador.

HERRON, J. C. 1991. Growth rates of Black Caiman,Melanosuchus niger and Spectacled Caiman, Caimancrododilus, and the recruitment of breeders inhunted caiman populations. Biological Conserva-tion 55:103113.

. 1994. Body size, spatial distribution, andmicrohabitat use in the caimans, Melanosuchusniger and Caiman crododilus, in a Peruvian lake.

Journal of Herpetology 28:508513.HERRON, J. C., L. H. EMMONS, AND J. E. CADLE. 1990.

Observations on reproduction in the Black Cai-

man, Melanosuchus niger. Journal of Herpetology24:314316.

KUSHLAN, J. A., AND T. JACOBSEN. 1990. Environmentalvariability and the reproductive success of Ever-glades Alligators. Journal of Herpetology 24:176184.

MAGNUSSON, W. E., A. P. LIMA, AND R. M. SAMPAIO. 1985.Sources of heat for nests of Paleosuchus trigonatusand a review of crocodilian nest temperatures.

Journal of Herpetology 19:199207.MAGNUSSON, W. E., A. P. LIMA, J. M. HERO, M. SANAIOTTI,

AND M. YAMAKOSHI. 1990. Paleosuchus trigonatusnests: sources of heat and embryo sex ratios.

Journal of Herpetology 24:397400.MEDEM, F. 1983. Los Crocodylia de Sur America.

Venezuela, Trinidad-Tobago, Guyana, Suriname,Guyana Francesa, Ecuador, Peru, Bolivia, Brasil,Paraguay, Argentina, Uruguay. Volumen II. Uni-versidad Nacional de Colombia y Colciencias,Bogota, Colombia.

PALACIOS, W., C. CERON, R. VALENCIA, AND R. SIERRA.1999. Las formaciones naturales de la Amazonadel Ecuador. In R. Sierra (ed.), Propuesta Prelimi-nar de un Sistema de Clasificacion de Vegetacionpara el Ecuador Continental, pp. 109119. ProyectoINEFAN/GEF-BIRF y Ecociencia, Quito, Ecuador.

REBELO, G. H., AND L. LUGLI. 2001. Distribution andabundance of four caiman species (Crocodylia:Alligatoridae) in Jau National Park, Amazonas,Brazil. Revista de Biologa Tropical 49:10961109.

VILLAMARIN-JURADO, F. 2006. Anidacion y patrones deuso de habitat del Caiman Negro, Melanosuchusniger (Crocodylia: Alligatoridae), en dos locali-dades de la Amazona ecuatoriana. Unpubl.

bachelors thesis, Pontificia Universidad Catolicadel Ecuador, Quito, Ecuador.

Accepted: 12 October 2006.

SHORTER COMMUNICATIONS 167