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

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

FRANCISCO VILLAMARIN-JURADO1,2
1

AND

ESTEBAN SUAREZ3

Escuela de Ciencias Biologicas, Pontificia Universidad Catolica del Ecuador, Quito, Ecuador 3 Wildlife Conservation Society, Ecuador Program, Quito, Ecuador

ABSTRACT.Seven Black Caiman (Melanosuchus niger) nests were located and monitored at Limoncocha and Anangu lagoons (northeastern Ecuador), between October 2002 and March 2003. Melanosuchus niger nesting coincided with the annual low water level season in the Ecuadorian Amazon. Mean number of eggs per nest was 28 and 34 eggs at Limoncocha and Anangu, respectively. Egg chamber temperature was monitored in two nests during the incubation period and showed no relationship with external air temperature, suggesting that the nests have their own heating sources. Mean hatching success was 42.4%, and flooding of the nests was identified as the main cause of egg mortality (29% of all the eggs). Although knowledge about the natural history of South American crocodilians has increased over the last few decades, conservation of this group is still hampered by the lack of information on their basic ecology and habitat requirements in the broad diversity of environmental conditions in which they live. This is particularly true for species such as the Black Caiman (Melanosuchus niger) in the northwestern limit of its distributional range, where animals are exposed to different environmental conditions than those found in countries where most previous studies have been carried out, including Brazil (Brazaitis et al., 1996; Da Silveira et al., 1997; Da Silveira and Magnusson, 1999; Rebelo and Lugli, 2001) and Peru (Herron et al., 1990; Herron, 1991, 1994). Studies on Black Caiman nesting biology have been carried out in Cocha 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 studies on 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 threatened species is almost unknown, and we only have anecdotal information provided by Medem (1983) and a partial description of two nests in the Cuyabeno Reserve (Asanza, 1985). According to the IUCNs Red List of Ecuadorian Reptiles, the Black Caiman is considered VU A1bd (Endara and Villamarn-Jurado, 2005). Based on population surveys in several areas of the Ecuadorian Amazon (T. Hines and K. Rice, A Report on an Initial Survey Effort to Assess the Status of Black Caiman Melanosuchus niger in the Amazon region of Ecuador, Unpubl., 1992; T. Hines and K. Rice, A Report on a Survey Effort to Assess the Status of Black Caiman Melanosuchus niger in the Amazon Region of Ecuador, Unpubl., 1994), Ecuadorian populations were downlisted to CITES Appendix II in 1995, subject to a ranching program with zero export quota (UNEP-WCMC Species Database: CITES-Listed Species http://www.unep-wcmc.org/isdb/CITES/ Taxonomy/index.cfmon the World Wide Web:
2 Corresponding Author. Present addres: Pasaje Kodaly D-52 y Luis de Beethoven, Quito, Ecuador; E-mail: franciscovillamarin@yahoo.com.ar

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 Caiman nests studied between October 2002 and March 2003. Our main objective was to describe Black Caiman nesting in the Limoncocha Biological Reserve (LBR) (76u3792.60W; 0u24912.20S) and Anangu Lagoon, in the Yasun National Park (YNP) (76u26915.00W; 0u31914.60S). Specifically, our goals were (1) to characterize the nests and nesting sites; (2) to record aspects 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 active Black Caiman nests. The vegetation at the study sites has been classified as Lowland Evergreen Forest inundated by white water (Varzea, Limoncocha) and black water rivers (Igapo, Limoncocha and Anangu) (Palacios et al., 1999). The shores of both lagoons are dominated by emergent vegetation where Montrichardia 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 following measurements were recorded: (1) nest dimensions; (2) length of the longest axis of the area of disturbed ground around the nest; (3) distance between the nest and the closest water body; and (4) percentage of canopy cover above the nest. After measurement, a sample of four nests (two in each location) was carefully opened, and the eggs were counted and marked on their tops, avoiding turning the eggs along their longitudinal axis. For each opened nest, the following measurements were taken: egg chamber dimensions, and the number, linear dimensions, and mass of all the eggs found. Although the floating vegetation mats in which the nests were found were very solid, while accessing the nests, we took care to avoid stepping on weak areas that could collapse, increasing the possibility of flooding. An Optic StowAwayH Data Logger was placed inside two egg chambers (Nests 1A and 4A) and

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programmed to record the temperature every 15 min. Additionally, air temperature outside the nests was recorded every day at 0700, 1200, and 1800 h, using a TaylorH Indoor/Outdoor Digital Thermometer, placed 1 m above the nests. Linear regressions were used to analyze whether a relationship existed between external air temperature (explanatory variable) and corresponding simultaneous measures of temperature inside each nest (response variable). Three camera traps (Cam TrakkerTM Watkinsville, GA) were set near two nests in Limoncocha and one nest in Anangu. Additionally, an observation platform was built between the aerial roots of a tree, approximately 15 m from one nest in Limoncocha (Nest 4L). From this platform we carried out systematic observations of the behavior of the adult female attending her nest over a two-month period. At the end of the nesting season, we checked all nests to get a minimum estimate of hatching success (percentage of hatched eggs relative to the total number of eggs). The minimum number of hatched caiman was determined by counting the number of egg shells left near the nest. Because some of the eggshells of hatched neonates may be carried off by the female and not left at the nest site, this represents only a minimum number of successfully hatched young. We also checked for deformed and rotten eggs which were classified as nonviable eggs. Eggshells were collected and deposited at the Museo de Zoologa, Pontificia Universidad Catolica del Ecuador (QCAZ), Herpetology collection. RESULTS Seven Black Caiman nests were found around Limoncocha (four) and Anangu (three) lagoons between 15 October and 19 November 2002. The nests are conical mounds constructed with leaf litter and roots, with mean dimensions of 1.65 6 0.16 m (means are given 6 standard deviation; N 5 7) 3 1.37 6 0.19 m (N 5 7), and a mean height of 0.54 6 0.097 m (N 5 7). The mean of the maximum radius of the disturbed area around the nests was 4.76 6 1.91 m (N 5 7), and the mean canopy cover above the nests was 80.2 6 5.79% and 85.3 6 5.87% in Limoncocha and Anangu, respectively. The nests remained shaded during most of the day, but at certain times they received 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 inundated forest (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 length and mass averaged 87.87 6 3.66 mm (N 5 49; range 5 85.9397.59 mm) and 142.35 6 6.09 g (N 5 49; range 5 130150 g), respectively. At Anangu Lagoon, corresponding values for clutch size were 34.0 6 2.00 eggs per nest (range 5 3236; N 5 3), whereas mean egg length and mass were 84.94 6 3.7 mm (N 5 66; range 5 81.2294.11 mm), and 125.4 6 13.24 g (N 5 66; range 5 122.5147.5 g), respectively. Temperature inside the egg chamber of nest 1A remained relatively stable with a mean of 31.2 6 0.74uC. Nest 4A mean chamber temperature (31.2uC)

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FIG. 1. Records of temperature in egg chambers of Melanosuchus niger (Nest 1A and Nest 4A) and external air temperatures. was very similar to that in nest 1A, but with a slightly greater variation (6 1.08uC). Mean temperature within the egg chamber was more stable and consistently higher than external air temperatures (mean 5 27.9 6 5.05uC; Fig. 1). Furthermore, linear regressions showed that the temperature inside the egg chambers was not dependent on external air temperature (Nest 1A: N 5 54; r2 5 0.029; P 5 0.22; and Nest 4A: N 5 87; r2 5 0.001; P 5 0.758). Mean hatching success was 42.4 6 39.0% (range 5 095.24%). Flooding of nests in both locations was identified as the main cause of egg mortality (29% of all the eggs). Two nests (one in each location) flooded and, as a result, all the eggs failed to hatch (Nest 4L: N 5 30, and Nest 3A: N 5 32). Nonviability of eggs was the second most important cause for hatching failure (22.9%). Additionally, only 0.47% of the eggs were lost to predation by an unidentified mouse (recorded by camera trap pictures), and 7.94% to suffocation of hatchlings that pipped from their eggs but could not come out from the nest as the nesting female did not release them. Nests 1A and 4A were abandoned by the nesting females. No signs of their presence were registered during the entire incubation period, not even when the hatchlings emerged from their eggs and vocalized from inside the nest. All the nests were found near a water pond. In four nests, the nesting female was observed inside the pond, hidden in the emergent vegetation such as Poaceae grasses and Montrichardia linifera (Araceae), taking care of their nests. Nests in Anangu were much closer to the lagoon edge (mean distance 5 17.1 6 7.2 m; N 5 3) than those in Limoncocha (mean distance5 58.5 6 15.81 m; N 5 4). The presence of the nesting female was detected, by direct observations, looking for marks left by the female, or using cammera traps, in five nests (four in Limoncocha and one in Anangu). Two of the four nesting females in Limoncocha (total female length approximately 2.9 m, estimated by comparing the size of the female in pictures to the size of other objects of known size) defended their nests by displaying aggressive behavior (Nests 3L and 4L). On one occasion, upon observing the researchers, the female in nest 3L came out of the water running and remained on the nest with her mouth open and tail raised. In one case, (nest 4L, in Limoncocha) the nest

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other large terrestrial predators are becoming rare in our study area, especially in Limoncocha, which could partly explain the low egg predation that we report here. Lizards of the genus Tupinambis have also been identified as major nest predators (R. Da Silveira and J. Thorbjarnarson, unpubl. data). Although we got a camera trap picture of a Tupinambis teguixin standing on top of nest 1L, we did not find conclusive evidence of this lizard preying on the eggs. The nesting female in nest 3L showed a combination of the attacking behavior defined by Cintra (1988) as leaving the water and staying on top of the nest without vocalization and swimming vigorously, passing near the nest to attack the investigators. In contrast, in Anangu, one of the nests was quickly abandoned by the female, even though it was visited only a few times during the incubation period and the degree of disturbance on this nest was very low compared with the others. This nest showed the lowest hatching success of nests that did not flood (14.7%), suggesting that the probability of egg mortality increases if the female abandons the nest. Our finding of the importance of flooding as a cause of hatching failure suggests that further research is needed to understand the relationship between Black Caiman recruitment and the unpredictable annual rainfall patterns in northwestern Amazon. This information will become increasingly important as large areas of lacustrine habitat are disturbed in this region to allow development of human settlements for oil extraction, agriculture, and tourism infrastructure. Acknowledgments.This project was funded by the Wildlife Conservation Society Program in Ecuador. E. Silva provided valuable help when planning the project. We thank the Ministerio del Ambiente del Ecuador and Byron Amaya for issuing our research permits and providing logistic support, the Universi dad Catolica for its institutional support and the Napo Wildlife Center for lodging and logistic support in Anangu. We are grateful to the Kichwa communities in Anangu and Limoncocha for all the knowledge shared. Many thanks to J. Thorbjarnarson who provided field training and advice during all the phases of this study and to G. R. Smith and two anonymous reviewers who provided valuable comments on earlier version of this manuscript. LITERATURE CITED ALLSTEADT, J. 1994. Nesting ecology of Caiman crocodi lus in Cano Negro, Costa Rica. Journal of Herpetology 28:1219. ASANZA, E. 1985. Distribucion, biologa reproductiva y alimentacion de cuatro especies de Alligatoridae, especialmente Caiman crocodilus en la Amazona del Ecuador. Unpubl. bachelors thesis. Pontificia Universidad Catolica del Ecuador, Quito, Ecuador. BRAZAITIS, P., G. H. REBELO, C. YAMASHITA, E. A. ODIERNA, AND M. E. WATANABE. 1996. Threats to Brazilian crocodilian populations. Oryx 30:275 284. CAMPOS, Z. 1993. Effect of habitat on survival of eggs and sex ratio of hatchlings of Caiman crocodilus yacare in the Pantanal, Brazil. Journal of Herpetology 27:127132.

flooded but the attending female remained at the nest for approximately 15 days after it was inundated. We obtained a direct record of the hatching process from camera trap photographs taken at nest 1L in Limoncocha. The pictures show that the process started on the night of 20 January 2003. The female came out of the water and lay on top of the nest. The following morning the female used its jaws and front feet to remove the material from the top of the nest, releasing the hatchlings and carrying them to the nearby water. The whole process lasted until noon on 21 January. DISCUSSION In general terms, the characteristics described here for the Black Caiman nests in northeastern Ecuador, coincide with the few other descriptions of Black Caiman nesting (Herron et al., 1990; R. Da Silveira and J. Thorbjarnarson, unpubl. data). In relation to egg mortality, however, our study found high levels of mortality caused by flooding, but low levels of predation, which is unusual in the existing literature regarding other crocodilians (e.g., Cintra, 1988; Campos, 1993). Reported values of clutch size and egg mass for Black Caiman are very variable between populations and between individuals within the same population. At Cocha Cashu, Herron et al. (1990) reported a clutch size of 38 eggs and a mean egg mass of 141.7 g. Medem (1983) suggested that clutch size of Black Caiman in Ecuador ranges between 40 and 60 eggs. In this sense, our results reflect the high variability of previous studies, as clutch size in our study sites ranged 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 Black Caiman nests have their own heat sources; this phenomenon has been previously reported for other crocodilians for which vegetal material decomposition, metabolic heat of embryos and the proximity to termite mounds (Magnusson et. al., 1985, 1990) were mentioned as potential sources of heat for the nests. Flooding was the most important factor affecting egg 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. Nonviable eggs was the second most important cause for hatching failure; Allsteadt (1994) suggested that nonviable eggs could be the result of infertility, spoiling from extreme temperatures, desiccation, or fungal attack during incubation. A somewhat surprising finding was the low incidence of egg predation. In other crocodilians, such as C. yacare, predation was responsible for up to 48.5% (Cintra, 1988) and 35% (Campos, 1993) of egg mortality. Allsteadt (1994) also found relatively low rates of eggs lost because of predation in A. mississippiensis nests (only four of 32 nests were partially depredated). A possible explanation for the low egg predation that we recorded could be the scarcity or absence of some of the species that have been reported as important predators of caiman eggs, such as the jaguar (Pantera onca; R. Da Silveira and J. Thorbjarnarson, unpubl. data). Jaguars and

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CINTRA, R. 1988. Nesting ecology of the Paraguayan Caiman (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 Anavilhanas archipelago, central Amazonia. Brazilian Journal of Herpetology 33:181192. DA SILVEIRA, R., W. E. MAGNUSSON, AND Z. CAMPOS. 1997. Monitoring the distribution, abundance and breeding areas of Caiman crocodilus crocodilus and Melanosuchus niger in the Anavilhanas archipelago, central Amazonia, Brazil. Journal of Herpetology 31:514520. ENDARA, A., AND F. VILLAMARIN-JURADO. 2005. Caiman Negro (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 del Ecuador, p. 20. Fundacion Novum Millenium, UICN-Sur, UICN-Comite Ecuatoriano, Ministerio de Educacion y Cultura. Serie Proyecto PEEPE, Quito, Ecuador. HERRON, J. C. 1991. Growth rates of Black Caiman, Melanosuchus niger and Spectacled Caiman, Caiman crododilus, and the recruitment of breeders in hunted caiman populations. Biological Conservation 55:103113. . 1994. Body size, spatial distribution, and microhabitat use in the caimans, Melanosuchus niger 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 Caiman, Melanosuchus niger. Journal of Herpetology 24:314316.

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KUSHLAN, J. A., AND T. JACOBSEN. 1990. Environmental variability and the reproductive success of Everglades Alligators. Journal of Herpetology 24:176 184. MAGNUSSON, W. E., A. P. LIMA, AND R. M. SAMPAIO. 1985. Sources of heat for nests of Paleosuchus trigonatus and 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 trigonatus nests: 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. Universidad Nacional de Colombia y Colciencias, Bogota, Colombia. PALACIOS, W., C. CERON, R. VALENCIA, AND R. SIERRA. 1999. Las formaciones naturales de la Amazona del Ecuador. In R. Sierra (ed.), Propuesta Prelimi nar de un Sistema de Clasificacion de Vegetacion para el Ecuador Continental, pp. 109119. Proyecto INEFAN/GEF-BIRF y Ecociencia, Quito, Ecuador. REBELO, G. H., AND L. LUGLI. 2001. Distribution and abundance 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 de uso de habitat del Caiman Negro, Melanosuchus niger (Crocodylia: Alligatoridae), en dos locali dades de la Amazon a ecuatoriana. Unpubl. bachelors thesis, Pontificia Universidad Catolica del Ecuador, Quito, Ecuador. Accepted: 12 October 2006.