Parental care in the Greenhouse Frog Eleutherodactylus planirostris (Cope, 1862) from Cuba

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1 Herpetology Notes, volume 11: (2018) (published online on 11 October 2018) Parental care in the Greenhouse Frog Eleutherodactylus planirostris (Cope, 1862) from Cuba Manuel Iturriaga 1,* and Álvaro Dugo-Cota 2 Parental care has been defined as any behaviour exhibited by a parent toward its offspring that increases their chances of survival (Trivers, 1972). In amphibians, this behaviour is a reproductive strategy where one or both parents provide an extensive look after to the clutches of eggs or the hatchlings (Duellman and Trueb, 1986; Wells, 2007, Pough et al., 2016). In anurans, it occurs in only 10-20% of all species (Pough et al., 2016). Parental care may involve selection and preparation of nest, burying of clutch during the oviposition, moistening and brooding the eggs, guarding and defending the clutches and/or the offspring, and transporting of froglets (Townsend, 1996). This behaviour also includes attendance of eggs (the most common form, but rare in aquatic eggs), transport of eggs, attendance of tadpoles, transport of tadpoles, attendance of froglets (in directdeveloping anurans), transport of froglets, and feeding of tadpoles (only in dendrobatids). Parental care has at least four functions according to McDiarmid (1978) and Wells, (1981, 2007): provision of an appropriate hydric regime for preventing desiccation of eggs in terrestrial habitats, reduction of predation by insects, other frogs and conspecifics (heterocannibalism or filial cannibalism), reduction of fungal infection because fungi grow on dead eggs and they can spread and infest the normal living eggs and reduction of developmental abnormalities since the incidence of this abnormality 1 División de Colecciones Zoológicas, Instituto de Ecología y Sistemática, carretera Varona e/ Oriente y Lindero, Rpto Parajón, Boyeros, 11900, La Habana, Cuba. 2 Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avd Americo Vespucio s/n, Seville, Spain. (dugocota@gmail.com) * Corresponding author. manueliturriaga83@gmail.com type is reduced when jostling or turning eggs is done during their early development by parents. On the other hand, parental care has also some potential costs, such as energetic losses and missed opportunities for mating in males (Pough et al., 2016). The genus Eleutherodactylus is widely distributed in the West Indies (Henderson and Powell, 2009). It is characterized by terrestrial reproduction and direct development (Townsend and Stewart, 1985). Provision of parental care to eggs and froglets in terrestrial nest sites is among the adaptive strategies exhibited by these frogs (Duellman and Trueb, 1994; Wells, 2007). In Cuba, the parental care has been reported in Eleutherodactylus albipes (Alonso et al., 2005), E. atkinsi (Novo et al., 1987; Alfonso et al., 2017), E. dimidiatus (Estrada, 1987) E. eileenae (Díaz and Cádiz, 2008), E. guantanamera (Estrada, 1990), E. intermedius (Estrada, 1992), E. leberi (Rodríguez and Alonso, 2009), E. melacara (Díaz and Cádiz, 2008), E. tetajulia (Estrada and Hedges, 1996a; Díaz and Cádiz, 2008), E. varleyi (Estrada, 1987), E. zeus (Alonso et al., 2015) and E. zugi (Díaz and Cádiz, 2008). The Greenhouse Frog E. planirostris is a grounddweller broadly distributed in many West Indian islands (Bahamas, Cayman Islands and Cuba) and introduced in Jamaica, Florida (USA), Hawaii (Heinicke et al. 2011), Philippines (Emerson et al., 2015) and Costa Rica (Barquero and Araya, 2016). It is a species exceedingly adaptable that may thrive in a diversity of habitats, including anthropogenic areas (Henderson and Powell, 2009). The first data on its reproduction were concerned with the breeding habitats, characteristics of nest and oviposition sites, number and size of clutches, hatching time and success, and duration of breeding season in populations of Florida (Deckert, 1921; Skermer, 1939; Carr, 1940; Goin, 1944), Cayman Islands (Grant, 1940) and Cuba (Dunn, 1926). Historically, E. planirostris have been classified as a species with no parental care (Goin, 1947; Schwartz and Henderson, 1991;

2 858 Manuel Iturriaga & Álvaro Dugo-Cota Figure 1. Clutch size and parental care of Eleutherodactylus planirostris in Vedado, Plaza de la Revolución municipality, Havana A): clutch of 13 semi-buried eggs in late developmental stage, B): a couple in axillary amplexus, C): male and female close to the clutch of eggs, D): two males and a couple close to the nest, E): two males accompanying froglets. Photographs by the junior author.

3 Parental care in the Greenhouse Frog Eleutherodactylus planirostris from Cuba 859 Figure 2. Parental care provided by two males of Eleutherodactylus planirostris in Vedado, Plaza de la Revolución municipality, Havana A): two males guarding the clutch of four eggs, B): posture of defensive behaviour by one of two males confronting the approximation of the camera. Photographs by ADC. Townsend, 1996). Here we report for the first time a case of parental care by E. planirostris. On September 14 th 2014 the junior author (ADC) found a clutch of E. planirostris inside a latticed brick in the garden of a house in Vedado County ( N, W), Plaza de la Revolución municipality, Havana province, Cuba. The clutch consisted of 13 semiburied eggs in late developmental stage, partially covered with mud (Fig.1A). The next day, the nest site was checked and a couple of frogs in axillary amplexus were found close to the clutch (Fig. 1B). On September 16 th in the morning, a female was spotted very close to the former clutch and a male was not far (Fig. 1C). The clutch was then totally covered with mud. In the afternoon, two adult males were observed inside the latticed brick with, presumably, the former couple together (Fig. 1D). The female stayed close to the clutch. At sunset, the two males were gone. The next day eight froglets were spotted inside the nest and were accompanied by two adult males. During three days, the nest site was checked and the offspring were always accompanied by these two males (Fig. 1E). On September 20 th, four scattered eggs were observed (Fig. 2A). They were partially covered with mud and two adult males were close to them. As a remarkable comment, one of these males showed a defensive behaviour towards the camera (Fig. 2B). Finally, on September 21 st, the nest was checked and there was an adult male. The clutch size of E. planirostris was similar to that reported by Deckert (1921). According to Goin (1947), the number of eggs of this species is variable and can range from three to 26, and the number of eggs per clutch shows a seasonal variation, being the largest clutches laid in mid-summer (July). In Cuba there are two extreme clutch sizes, with the tiniest species, E. iberia and E. limbatus with only one egg (Noble, 1931; Estrada and Hedges, 1996b) and the largest species, E. zeus with 72 eggs (Alonso et al., 2015). Goin (1947) found a clutch of fresh eggs close to a couple of E. planirostris still in amplexus. He disturbed the nest and the frogs scurried away but 15 minutes later the author noted that one of the parents (presumably the female) had returned and covered the eggs. Nonetheless, Goin considered that there was not any evidence of attendance and guarding of eggs, and they were apparently abandoned shortly after oviposition. Consequently, E. planirostris was categorized by Goin (1947) as a species with no parental care and this classification was followed by some authors (Schwartz and Henderson, 1991; Townsend, 1996). According to Townsend (1996) there are three valid evidences to consider a report as a reliable account of parental care: repeated observations of adult brooding eggs, a parent returning to nest if it is removed, and/or when the parent refuses to abandon the eggs even when it is disturbed. In Goin s study, despite the fact that the female returned to the nest and covered the eggs, the author considered that there was not any evidence of moistening of eggs. However, the covering of eggs

4 860 (egg-brooding behaviour), either partial (Estrada, 1987; Joglar et al., 1996) or complete (Townsend et al., 1984; Estrada, 1992), is one way to keep the moisture during the attendance of eggs (Townsend, 1996; Wells, 2007). In this report, no egg-brooding behaviour was observed but there were other care types that point out that E. planirostris is a species with parental care. Two adult males were spotted accompanied by eight froglets, and during three days these males guarded the froglets. Therefore, the possibility that the first observation was a fortuitous case is ruled out. Attendance of froglets is one of the care types reported for amphibians (Wells, 2007). The defensive behaviour observed in one of the two males of E. planirostris, is another evidence of parental care in this species. According to Townsend et al. (1984), the aggressive behaviours by parental males during the nest defence included aggressive calling, biting, sustained biting, blocking and wrestling. In other species of Eleutherodactylus, aggressive calling has been reported in males that guard the clutch (Díaz and Cádiz, 2008; Rodríguez and Alonso, 2009) or the entrance of burrows (Estrada, 1992). Many forms of male parental care evolved as a consequence of male territoriality in frogs (McDiarmid, 1978). Acknowledgements. We thank Luis F. de Armas, from the Institute of Ecology and Systematics, Havana, Cuba; Pedro P. Herrera from Institute of Tropical Geography, Havana, Cuba and Roberto Alonso Bosch from the Museum of Natural History Felipe Poey, Faculty of Biology, Havana University, Cuba for the critical review of the manuscript. A.D.C. was funded by a FPI doctoral fellowship (BES ) and a short research stay (EEBB-I ) from the Spanish Government. References Alfonso, Y.U., Rodríguez-Gómez, Y., Charruau, P., Sanz- Ochotorena, A., Krysko, K.L. (2017): Oviposition and Gonadal Ultrastructure in the Cuban Groin-spot Frog, Eleutherodactylus atkinsi Dunn, 1925 (Anura: Eleutherodactylidae). Copeia 105: Alonso, R.B., L.Y. García, S.D. del Castillo, and E.L.M. Torres Clutches, nest attendance, and hatching in a rock-cave dwelling frog, Eleutherodactylus (Syrrophus) zeus, from Cuba. Journal of Cave and Karst Studies 77: Alonso, R., Rodríguez, A., Hernández, A. (2005): Eleutherodactylus albipes (NCN). Reproduction. Herpetological Review 36: 433. Barquero, M.D., Araya, M.F. (2016): First record of the Greenhouse frog, Eleutherodactylus planirostris (Anura: Eleutherodactylidae), in Costa Rica. Herpetology Notes 9: Burrowes, P.A. (2000): Parental care and sexual selection in the Puerto Rican cave-dwelling frog, Eleutherodactylus cooki. Herpetologica 56: Manuel Iturriaga & Álvaro Dugo-Cota Carr, A.F.Jr. (1940): A contribution to the herpetology of Florida. University of Florida Publications in Biology Science 3: Deckert, R.F. (1921): Amphibian notes from Dade Co., Florida. Copeia 92: Díaz, L.M., Cádiz, A. (2008): Guía taxonómica de los anfibios de Cuba. Bruxelas AbcTaxa. Diesel, R., Bäurle, G., Vogel. P. (1995): Cave breeding and froglet transport: A novel pattern of anuran brood care in the Jamaican frog, Eleutherodactylus cundalli. Copeia 1995: Duellman, W., Trueb, L. (1986): Biology of Amphibians. Baltimore, The Johns Hopkins University Press. Dunn, E.R. (1926): Notes on two Cuban frogs. Copeia 157: Emerson, Y.S., Clifton, J.M., Diesmos, A.C. (2015): Eleutherodactylus planirostris (Greenhouse Frog). Philippines: Negros Island: Negros Occidental. Herpetological Review 46: 56. Estrada, A.R. (1987): Los nidos terrestres de dos especies de anfibios cubanos del género Eleutherodactylus (Anura: Leptodactylidae). Poeyana 352: 1-9. Estrada, A.R. (1990): Las puestas de Eleutherodactylus varians (Gundlach y Peters). Revista Biologia 4: Estrada, A.R. (1992): Comentarios sobre Eleutherodactylus intermedius (Barbour et Shreve, 1937) de la región oriental de Cuba. Comunicaciones breves de Zoología, Editorial Academia: Estrada, A.R., Hedges S.B. (1996a): A new frog of the genus Eleutherodactylus from eastern Cuba (Anura, Leptodactylidae). Herpetologica 52: Estrada, A.R., Hedges, S.B. (1996b): At the lower size limit in tetrapods: A new diminutive frog from Cuba (Leptodactylidae: Eleutherodactylus). Copeia 1996: Goin, C.J. (1944): Eleutherodactylus ricordii at Jacksonville, Florida. Copeia 1944: 192. Goin, C.J. (1947): Studies on the life history of Eleutherodactylus ricordii planirostris (Cope) in Florida. University of Florida Publications in Biology Science 4: Grant, C. (1940): The herpetology of the Cayman Islands. Bulletin of the Institute of Jamaica, Science Series 2: Heinicke, M.P., Díaz, L.M., Hedges, S.B. (2011): Origin of invasive Florida frogs traced to Cuba. Biology Letters 1131: 1-4. Henderson, R.W., Powell, R. (2009): Natural History of West Indian Reptiles and Amphibians. University of Florida Press, Gainesville. Joglar, R.L., Burrowes, P.A., Ríos, N. (1996): Biology of the Puerto Rico cave-dwelling frog, Eleutherodactylus cooki, with some recommendations for its conservation. In: Contribution to West Indian Herpetology, p Powell, R., Henderson, Eds., Ithaca, New York Society for the Study of Amphibians and Reptiles. McDiarmid, R.W. (1978): Evolution of parental care in frogs. In: The development of behavior: comparative and evolutionary aspect, p Burghardt, G.M., Bekoff, M. Eds., New York, Garland STPM Press. Noble, G.K. (1931): The biology of the amphibian. New York, McGraw-Hill. Novo, J., Estrada, A.R., Moreno, L.V. (1987): Apuntes sobre la reproducción de Eleutherodactylus atkinsi (Anura:

5 Parental care in the Greenhouse Frog Eleutherodactylus planirostris from Cuba 861 Leptodactylidae). Miscelanea Zoológica, Academia de Ciencias de Cuba 29: 2-3. Pough, F.H., Andrews, R.M., Crump, M.L., Savitzky, A.H., Wells, K.D., Brandley. M.C. (2016): Herpetology. Sunderland, Sinauer Associates, Inc. Rodríguez, A., Alonso, R. (2009): Eleutherodactylus leberi (NCN). Clutch size and parental care. Herpetological Review 40: 204. Schwartz, A., Henderson, R.W. (1991): Amphibian and Reptiles of the West Indies: Descriptions, Distributions, and Natural History. Gainesville, University of Florida Press. Skermer, G.H. (1939): A note on Eleutherodactylus ricordii. Copeia 1939: Taigen, T.L., Pough, F.H., Stewart, M.M. (1984): Water balance of terrestrial anuran (Eleutherodactylus coqui) eggs: importance of parental care. Ecology 65: Townsend, D.S. (1996): Patterns of parental care in frogs of the genus Eleutherodactylus. In: Contribution to West India Herpetology, pp Powell, R., Henderson R.W., Eds. New York Society for the Study of Amphibians and Reptiles, Ithaca. Townsend, D.S., Stewart, M.M. (1985): Direct development in Eleutherodactylus coqui (Anura: Leptodactylidae): A staging table. Copeia 1985: Townsend, D.S., Stewart, M.M. (1994): Reproductive ecology of the Puerto Rican frog Eleutherodactylus coqui. Journal of Herpetology 28: Townsend, D.S., Stewart, M.M., Pough, F.H. (1984): Male parental care and its adaptive significance in a neotropical frog. Animal Behaviour 32: Trivers, R.L. (1972): Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, p Campbell B.G. Eds., Chicago, Andine Press. Wells, K.D. (1981): Parental behavior of male and female frogs. In: Natural Selection and Social Behavior, p Alexander, R.D., Tinkle D.W. Eds. Incorporated, New York Chiron Press. Wells, K.D. (2007): The Ecology and Behavior of Amphibians. Chicago, The University of Chicago Press. Accepted by Gabriela Bittencourt-Silva