Barboza, Rafael Sá Leitão

Cunha, Fábio Andrew Gomes

Rebêlo, George Henrique

Repositório do INPA

The Spectacled Caiman (Caiman crocodilus [Linnaeus, 1758]) is a comparatively abundant species of the Crocodylia order and exhibits a high plasticity in habitat use (Brazaitis et al., 1996; Aguilera et al., 2008). With a wide distribution extending from the Amazon Basin northwards into Mexico (Ross, 1998), the Spectacled Caiman is able to live in a variety of different water bodies and often coexist with other crocodilian species (Rebêlo and Lugli, 2001). Such a wide range of habitats may also extend the knowledge on the reproductive ecology of the species. Knowledge on reproductive strategies is crucial to understand successful reproduction of a species (Whittier and Limpus, 1996). A behaviour not often found in crocodilians is communal nesting or communal oviposition, which can be described as non-accidental oviposition of eggs in a nest cavity shared by two or more individuals of the same species (Espinoza and Lobo, 1996). This behavior was described in Teiidae lizards (Kentropyx calcarata; Magnusson and Lima, 1984) and neotropical crocodilians, including Caiman latirostris in Argentina (Larriera, 2002) and Melanosuchus niger in Ecuador (Villamarín-Jurado and Suárez, 2007). Interspecific interactions in shared nest cavities were also reported between Crocodilus acutus and the neotropical lizard Iguana iguana (Dugan et al., 1981), and between Melanosuchus niger and Podocnemis unifilis (Maffei and Da Silveira, 2013). This behavior could occur because of a rareness of appropriate nesting areas (Rand, 1967), provoking sharing of or competition for the few available habitats. Communal nesting of crocodilians in the Amazon flooded Forest (várzea) has not yet been studied and published within the scientific literature. We herein report on communal nesting of females of Caiman crocodilus in the Lower Amazon River, in Pará State of Brazil (Figure 1).Nests of C. crocodilus were found along the banks of a small channel (six meters in width) in November 2012, during the dry season in the floodplain forest of the Amazon River, located near Santarém city, Pará state, Brazil. It is expected that females compete for nest sites in this habitat, where we observed a density of 8 nest/km in some parts of the channel. During the reproductive season 105 nests were found, among which two were located about five meters from each other and at seven meters from the channel (water body) that had completely dried out. The first nest contained no eggs, but two females were found close to it; the first female was recorded one meter away from the nest, with a snout vent length (SVL) of 66 cm and a weight of 6 kg, while the second female was recorded two meters from the nest, with a SVL of 78 cm and a weight of 10 kg. In the second nest we recorded 43 eggs (Figure 2c) with a third female found 1.5 m away, which measured 78 cm SVL and weighed 10 kg (Figure 2a, b). The female had an injury in the left lower lateral region nearly half way between the hind and fore limbs, with bite marks and abundant insect larvae (Figure 2d). All females were hidden under tree branches, supposedly to avoid predation (Da Silveira et al., 2010).Herpetology Notes, volume 9: 141-144 (2016) (published online on 09 June 2016)Communal nesting of Caiman crocodilus (Linneaus, 1758) (Crocodylia: Alligatoridae) in lower Amazon river floodplain, BrazilFábio Andrew Gomes Cunha1,*, Rafael Sá Leitão Barboza2 and George Henrique Rebêlo31 Instituto Nacional de Pesquisa da Amazônia INPA – Centro de Estudos de Quelônios da Amazônia. Av. André Araújo, 2.936 – Petrópolis – CEP: 69067-375 – Manaus, AM, Brasil.2 Instituto Chico Mendes de Conservação da Biodiversidade – ICMBIO. Rua coronel José Porfírio, 3455. Bairro Sao Sebastião. Cep 68372-040. Altamira, PA, Brasil.3 Instituto Nacional de Pesquisa da Amazônia INPA / Laboratório de Manejo de Fauna/LMF. Av. André Araújo, 2.936 – Petrópolis – CEP: 69067-375 – Manaus, AM, Brasil.* Corresponding autor e-mail: fabioagcunha@gmail.com Fábio Andrew Gomes Cunha et al.142The eggs of the second nest were organized in two incubation cavities arranged vertically above the same base. All the upper eggs were broken and of an advanced decomposed stage (N= 12), and were not measured. Because there were only 11 intact eggs in the lower cavity, it was not possible to determine if there was more than one group of eggs with different sizes or a separate egg-laying period. The average number of eggs for C. crocodilus varies from 22 to 28 eggs. The average number of eggs recorded in the study area in 2012 was 22 (unpublished data; Table 1). We believe that during the periodical absence of a large female the recorded third individual laid her eggs on top of the formed nest. The original female (owner of the first posture) then returned, provoked the injury to the new female and damaged the newly laid eggs. Figure 1. Localization of the communal nesting place of Caiman crocodilus in Água Preta community, Lower Amazon River, Brazil. 11Table 1. Average clutch size ± SD (range) of C. crocodilus in different neotropical areas 23Local, Year (N) Clutch size Source Cururu Lake, Amazon River. 2001 (N= 60) 25 ±5.6 (14-38) Campos, 2003 Literature review  24.4 Thorbjarnarson, 1996 Llanos, Venezuela. 1973, 1974     (N= 30) 28.6 ±0.91* (17-38) Staton and Dixon, 1977 Floodplain, Lower Amazon River. 2011, 2012 (N= 193) 22.12 ±6.19 (11-38) Unpublished data       SD = Standard Deviation; *SE = Standard Error 45Table 1. Average clutch size ± SD (range) of C. crocodilus in different neotropical areasEvidence of nest sharing by the females included: (a) the number of eggs (intact and broken) found in the nest was above the maximum clutch size recorded in nests of the same species in different habitats; (b) the presence of three females guarding the two nest sites; (c) two incubation cavities within a single nest. The presence of three females could be considered a coincidental phenomenon simply because one or two of the females could have been passing through the area. However, the high number of eggs in the nest renders this unlikely. The wounded female and the broken eggs represent a possible aggressive intraspecific interaction, suggesting that the nest sharing did not occur in a harmonic and consensual way, implying competition. A high density of nests was previously identified in crocodilians (Platt and Thorbjarnarson, 2000; Seijas and Chavez, 2002), yet the the occurrence of communal nesting may be caused by intraspecific competition for nesting sites as a result of limited nesting areas (Graves and Duvall, 1995). Another reason is the intraspecific brood care farming out – where a female exploits the parental effort of others when mixing the offspring with conspecifics, avoiding fitness reduction and mitigating the energetic costs of parental care when faced with inadequate conditions (Yanagisawa, 1985). Parental care can cause nutritional stress due to higher energy costs in females and increased susceptibility to predation (Da Silveira et al., 2010). In the Lower Amazon Várzea during the reproductive period, it is common to find females with low body mass close to their nests in areas where the water body is completely dried out. Communal nesting of Caiman crocodilus in lower Amazon river floodplain, Brazil 143Figure 2. A and B) C. crocodilus females in the area of the communal nest, under branches and thorns, exhibiting parental care, C) viable eggs from the communal nest, and D) injured female captured near the nest.Acknowledgements. We are grateful to Água Preta Community in Santarém/PA for all the lessons and comradeship, the students of the field course “Ecology, Management and Conservation of Aquatic Fauna of Floodplain: chelonians, caimans and pirarucus” in 2012 for their help, the Environmental Research Institute of Amazon – IPAM for the assistance.ReferencesAguilera, X., Coronel, J.S., Oberdorff, T., Van Damme, P.A. (2008): Distribution patterns, population status and conservation of Melanosuchus niger and Caiman yacare (Crocodylia, Alligatoridae) in oxbow lakes of the Ichilo river floodplain, Bolivia. Revista Biología Tropical 2: 909-929.Brazaitis, P., Rebêlo, G.H., Yamashita, C. (1996): The status of Caiman crocodilus crocodilus and Melanosuchus niger populations in the Amazonian regions of Brazil. Amphibia-Reptilia 17: 377-385.Campos, Z.M. da S. (2003): Observações sobre a biologia reprodutiva de três espécies de jacarés na Amazônia Central. Corumbá: Embrapa Pantanal. Boletim de Pesquisa e Desenvolvimento / Embrapa Pantanal 43: 1517-1981.Da Silveira, R., Ramalho, E.E., Thorbjarnarson, J., Magnusson, W.E. (2010): Depredation by jaguars on caimans and importance of reptiles in the diet of jaguar. Journal of Herpetology 44: 418-424.Dugan, A.B., Gordon, Rand, A.S., Burghardt, M., Bock, B.C. (1981): Interactions between nesting Crocodiles and Iguanas. Journal of Herpetology 15: 409-414.Espinoza, R.E., Lobo, F. (1996): Possible communal nesting in two species of Liolaemus lizards (Iguania: Tropiduridae) from northern Argentina. Herpetological Natural History 4: 65-68.Graves, B.M., Duvall, D. (1995): Aggregation of squamate reptiles associated with gestation, oviposition, and parturition. Herpetological Monographs 9: 102-119.Larriera, A. (2002): Caiman latirostris (Broad-snouted Caiman). Communal nesting. Herpetological Review 3: 33.Maffei, F.; Da Silveira, R. 2013. Primeiro relato de desovas múltiplas de tracajá (Podocnemis unifilis) em ninho de jacaré-açu (Melanosuchus niger) na Amazônia. Bol. Mus. Para. Emílio Goeldi. Cienc. Nat. 8: 3.Magnusson, W., Lima, A. (1984): Perennial communal nesting by Kentropyx calcaratus. Journal of Herpetology 18: 73-75.Platt, S., Thorbjarnarson, J. (2000): Nesting ecology of the American crocodile in the coastal zone of Belize. Copeia 3: 869-873. Rand, A.S. (1967): Communal eggs laying in anoline lizards. Herpetologica 23: 227-231.Rebêlo, G.H, Lugli, L. (2001): Distribution and abundance of four caiman species (Crocodylia: Alligatoridae) in Jaú National Park, Amazonas, Brazil. Revista Bioligía Tropical 49: 1019-1033. Ross, J.P. (1998): Crocodiles. Status Survey and Conservation Action Plan. 2 Ed. IUCN/SSC Specialist Crocodile Group. IUCN, Gland, Switzerland, and Cambridge, U.K.Seijas, A.E., Chávez, C.A. (2002): Reproductive status and nesting ecology of the Orinoco crocodile (Crocodylus intermedius) in the Cojedes River System, Venezuela. Vida Silvestre Neotropical 11(1-2): 23-32.Staton, M., Dixon, J. (1977): Breeding biology of the spectacled caiman, Caiman crocodilus crocodilus in the Venezuelan Llanos. Wildlife and Fisheries Sciences, Wildlife Research Report 5, Washington D.C.Thorbjarnarson, J.B. (1996): Reproductive characteristics of the order crocodylia. Herpetologia 52: 8-24.Villamarín-Jurado, F., Suàrez, E. (2007): Nesting of the Black Caiman (Melanosuchus niger) in Northeastern Ecuador. Journal of Herpetology 41: 164-167.Whittier, J.M., Limpus, D. (1996): Reproductive patterns of a biologically invasive species: The Brown tree snake (Boiga irregularis) in eastern Australia. Journal of Zoology 238: 591-597.Yanagisawa, Y. (1985): Parental strategy of the cichlid fish Perissodus microlepis, with particular reference to intraspecific brood ‘farming out’. Environmental Biology of Fishes 12: 211-249.Fábio Andrew Gomes Cunha et al.144Accepted by Maximilian Dehling

Communal nesting of Caiman crocodilus (Linneaus, 1758) (Crocodylia: Alligatoridae) in lower Amazon river floodplain, Brazil

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Communal nesting of Caiman crocodilus (Linneaus, 1758) (Crocodylia: Alligatoridae) in lower Amazon river floodplain, Brazil

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