Herpetology Notes, volume 11: 857-861 (2018) (published online on 11 October 2018)

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

Manuel Iturriaga1,* and Álvaro Dugo-Cota2

Parental care has been defined as any behaviour type is reduced when jostling or turning eggs is done exhibited by a parent toward its offspring that increases during their early development by parents. On the other their chances of survival (Trivers, 1972). In amphibians, hand, parental care has also some potential costs, such this behaviour is a reproductive strategy where one as energetic losses and missed opportunities for mating or both parents provide an extensive look after to the in males (Pough et al., 2016). clutches of eggs or the hatchlings (Duellman and Trueb, The genus Eleutherodactylus is widely distributed 1986; Wells, 2007, Pough et al., 2016). In anurans, it in the West Indies (Henderson and Powell, 2009). It occurs in only 10-20% of all species (Pough et al., 2016). is characterized by terrestrial reproduction and direct Parental care may involve selection and preparation of development (Townsend and Stewart, 1985). Provision nest, burying of clutch during the oviposition, moistening of parental care to eggs and froglets in terrestrial and brooding the eggs, guarding and defending the nest sites is among the adaptive strategies exhibited clutches and/or the offspring, and transporting of by these frogs (Duellman and Trueb, 1994; Wells, froglets (Townsend, 1996). This behaviour also includes 2007). In Cuba, the parental care has been reported attendance of eggs (the most common form, but rare in in Eleutherodactylus albipes (Alonso et al., 2005), aquatic eggs), transport of eggs, attendance of tadpoles, E. atkinsi (Novo et al., 1987; Alfonso et al., 2017), transport of tadpoles, attendance of froglets (in direct- E. dimidiatus (Estrada, 1987) E. eileenae (Díaz and developing anurans), transport of froglets, and feeding Cádiz, 2008), E. guantanamera (Estrada, 1990), E. of tadpoles (only in dendrobatids). Parental care has at intermedius (Estrada, 1992), E. leberi (Rodríguez and least four functions according to McDiarmid (1978) Alonso, 2009), E. melacara (Díaz and Cádiz, 2008), E. and Wells, (1981, 2007): provision of an appropriate tetajulia (Estrada and Hedges, 1996a; Díaz and Cádiz, hydric regime for preventing desiccation of eggs in 2008), E. varleyi (Estrada, 1987), E. zeus (Alonso et al., terrestrial habitats, reduction of predation by insects, 2015) and E. zugi (Díaz and Cádiz, 2008). other frogs and conspecifics (heterocannibalism or filial The Greenhouse Frog E. planirostris is a ground- cannibalism), reduction of fungal infection because dweller broadly distributed in many West Indian islands fungi grow on dead eggs and they can spread and infest (Bahamas, Cayman Islands and Cuba) and introduced in the normal living eggs and reduction of developmental Jamaica, Florida (USA), Hawaii (Heinicke et al. 2011), abnormalities since the incidence of this abnormality 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 1 División de Colecciones Zoológicas, Instituto de Ecología y time and success, and duration of breeding season in Sistemática, carretera Varona 11835 e/ Oriente y Lindero, populations of Florida (Deckert, 1921; Skermer, 1939; Rpto Parajón, Boyeros, 11900, La Habana, Cuba. Carr, 1940; Goin, 1944), Cayman Islands (Grant, 1940) 2 Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avd Americo Vespucio and Cuba (Dunn, 1926). Historically, E. planirostris s/n, 41092 Seville, Spain. ([email protected]) have been classified as a species with no parental * Corresponding author. E-mail: [email protected] care (Goin, 1947; Schwartz and Henderson, 1991; 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. 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 reported by Deckert (1921). According to Goin (1947), case of parental care by E. planirostris. the number of eggs of this species is variable and can On September 14th 2014 the junior author (ADC) range from three to 26, and the number of eggs per found a clutch of E. planirostris inside a latticed brick clutch shows a seasonal variation, being the largest in the garden of a house in Vedado County (23.1304°N, clutches laid in mid-summer (July). In Cuba there are 82.3902°W), Plaza de la Revolución municipality, two extreme clutch sizes, with the tiniest species, E. Havana province, Cuba. The clutch consisted of 13 iberia and E. limbatus with only one egg (Noble, 1931; semiburied eggs in late developmental stage, partially Estrada and Hedges, 1996b) and the largest species, E. covered with mud (Fig.1A). The next day, the nest zeus with 72 eggs (Alonso et al., 2015). site was checked and a couple of frogs in axillary Goin (1947) found a clutch of fresh eggs close to a amplexus were found close to the clutch (Fig. 1B). On couple of E. planirostris still in amplexus. He disturbed September 16th in the morning, a female was spotted the nest and the frogs scurried away but 15 minutes later very close to the former clutch and a male was not far the author noted that one of the parents (presumably (Fig. 1C). The clutch was then totally covered with the female) had returned and covered the eggs. mud. In the afternoon, two adult males were observed Nonetheless, Goin considered that there was not any inside the latticed brick with, presumably, the former evidence of attendance and guarding of eggs, and they couple together (Fig. 1D). The female stayed close to were apparently abandoned shortly after oviposition. the clutch. At sunset, the two males were gone. The Consequently, E. planirostris was categorized by next day eight froglets were spotted inside the nest and Goin (1947) as a species with no parental care and this were accompanied by two adult males. During three classification was followed by some authors (Schwartz days, the nest site was checked and the offspring were and Henderson, 1991; Townsend, 1996). According always accompanied by these two males (Fig. 1E). to Townsend (1996) there are three valid evidences On September 20th, four scattered eggs were observed to consider a report as a reliable account of parental (Fig. 2A). They were partially covered with mud and care: repeated observations of adult brooding eggs, a two adult males were close to them. As a remarkable parent returning to nest if it is removed, and/or when comment, one of these males showed a defensive the parent refuses to abandon the eggs even when it behaviour towards the camera (Fig. 2B). Finally, on is disturbed. In Goin´s study, despite the fact that the September 21st, the nest was checked and there was an female returned to the nest and covered the eggs, the adult male. author considered that there was not any evidence of The clutch size of E. planirostris was similar to that moistening of eggs. However, the covering of eggs 860 Manuel Iturriaga & Álvaro Dugo-Cota

(egg-brooding behaviour), either partial (Estrada, 1987; Carr, A.F.Jr. (1940): A contribution to the herpetology of Florida. Joglar et al., 1996) or complete (Townsend et al., 1984; University of Florida Publications in Biology Science 3: 1-118. Estrada, 1992), is one way to keep the moisture during Deckert, R.F. (1921): Amphibian notes from Dade Co., Florida. Copeia 92: 20-23. the attendance of eggs (Townsend, 1996; Wells, 2007). Díaz, L.M., Cádiz, A. (2008): Guía taxonómica de los anfibios de In this report, no egg-brooding behaviour was Cuba. Bruxelas AbcTaxa. observed but there were other care types that point out Diesel, R., Bäurle, G., Vogel. P. (1995): Cave breeding and froglet that E. planirostris is a species with parental care. Two transport: A novel pattern of anuran brood care in the Jamaican adult males were spotted accompanied by eight froglets, frog, Eleutherodactylus cundalli. Copeia 1995: 354-360. and during three days these males guarded the froglets. Duellman, W., Trueb, L. (1986): Biology of Amphibians. Baltimore, The Johns Hopkins University Press. Therefore, the possibility that the first observation was Dunn, E.R. (1926): Notes on two Cuban frogs. Copeia 157: 154- a fortuitous case is ruled out. Attendance of froglets is 156. one of the care types reported for amphibians (Wells, Emerson, Y.S., Clifton, J.M., Diesmos, A.C. (2015): 2007). The defensive behaviour observed in one of the Eleutherodactylus planirostris (Greenhouse Frog). Philippines: two males of E. planirostris, is another evidence of Negros Island: Negros Occidental. Herpetological Review 46: parental care in this species. According to Townsend et 56. Estrada, A.R. (1987): Los nidos terrestres de dos especies de al. (1984), the aggressive behaviours by parental males anfibios cubanos del género Eleutherodactylus (Anura: during the nest defence included aggressive calling, Leptodactylidae). Poeyana 352: 1-9. biting, sustained biting, blocking and wrestling. In Estrada, A.R. (1990): Las puestas de Eleutherodactylus varians other species of Eleutherodactylus, aggressive calling (Gundlach y Peters). Revista Biologia 4: 163-167. has been reported in males that guard the clutch (Díaz Estrada, A.R. (1992): Comentarios sobre Eleutherodactylus and Cádiz, 2008; Rodríguez and Alonso, 2009) or the intermedius (Barbour et Shreve, 1937) de la región oriental de Cuba. Comunicaciones breves de Zoología, Editorial Academia: entrance of burrows (Estrada, 1992). Many forms of 12-14. male parental care evolved as a consequence of male Estrada, A.R., Hedges S.B. (1996a): A new frog of the genus territoriality in frogs (McDiarmid, 1978). Eleutherodactylus from eastern Cuba (Anura, Leptodactylidae). Herpetologica 52: 435-439. Acknowledgements. We thank Luis F. de Armas, from the Estrada, A.R., Hedges, S.B. (1996b): At the lower size limit in Institute of Ecology and Systematics, Havana, Cuba; Pedro P. tetrapods: A new diminutive frog from Cuba (Leptodactylidae: Herrera from Institute of Tropical Geography, Havana, Cuba Eleutherodactylus). Copeia 1996: 852-859. and Roberto Alonso Bosch from the Museum of Natural History Goin, C.J. (1944): Eleutherodactylus ricordii at Jacksonville, “Felipe Poey”, Faculty of Biology, Havana University, Cuba for Florida. Copeia 1944: 192. the critical review of the manuscript. A.D.C. was funded by a FPI Goin, C.J. (1947): Studies on the life history of Eleutherodactylus doctoral fellowship (BES-2011-050123) and a short research stay ricordii planirostris (Cope) in Florida. University of Florida (EEBB-I-14-08498) from the Spanish Government. Publications in Biology Science 4: 1-56. Grant, C. (1940): The herpetology of the Cayman Islands. Bulletin References of the Institute of Jamaica, Science Series 2: 1-65. Heinicke, M.P., Díaz, L.M., Hedges, S.B. (2011): Origin of invasive Alfonso, Y.U., Rodríguez-Gómez, Y., Charruau, P., Sanz- Florida frogs traced to Cuba. Biology Letters 1131: 1-4. Ochotorena, A., Krysko, K.L. (2017): Oviposition and Gonadal Henderson, R.W., Powell, R. (2009): Natural History of West Ultrastructure in the Cuban Groin-spot Frog, Eleutherodactylus Indian Reptiles and Amphibians. University of Florida Press, atkinsi Dunn, 1925 (Anura: Eleutherodactylidae). Copeia 105: Gainesville. 781-790. Joglar, R.L., Burrowes, P.A., Ríos, N. (1996): Biology of the Alonso, R.B., L.Y. García, S.D. del Castillo, and E.L.M. Torres. Puerto Rico cave-dwelling frog, Eleutherodactylus cooki, with 2015. Clutches, nest attendance, and hatching in a rock-cave some recommendations for its conservation. In: Contribution to dwelling frog, Eleutherodactylus (Syrrophus) zeus, from Cuba. West Indian Herpetology, p. 251-258. Powell, R., Henderson, Journal of Cave and Karst Studies 77: 83-86. Eds., Ithaca, New York Society for the Study of Amphibians Alonso, R., Rodríguez, A., Hernández, A. (2005): Eleutherodactylus and Reptiles. albipes (NCN). Reproduction. Herpetological Review 36: 433. McDiarmid, R.W. (1978): Evolution of parental care in frogs. In: Barquero, M.D., Araya, M.F. (2016): First record of the The development of behavior: comparative and evolutionary Greenhouse frog, Eleutherodactylus planirostris (Anura: aspect, p. 184-197. Burghardt, G.M., Bekoff, M. Eds., New Eleutherodactylidae), in Costa Rica. Herpetology Notes 9: 145- York, Garland STPM Press. 147. Noble, G.K. (1931): The biology of the amphibian. New York, Burrowes, P.A. (2000): Parental care and sexual selection in the McGraw-Hill. Puerto Rican cave-dwelling frog, Eleutherodactylus cooki. Novo, J., Estrada, A.R., Moreno, L.V. (1987): Apuntes sobre Herpetologica 56: 375-386. la reproducción de Eleutherodactylus atkinsi (Anura: Parental care in the Greenhouse Frog Eleutherodactylus planirostris from Cuba 861

Leptodactylidae). Miscelanea Zoológica, Academia de Ciencias Townsend, D.S., Stewart, M.M. (1985): Direct development in de Cuba 29: 2-3. Eleutherodactylus coqui (Anura: Leptodactylidae): A staging Pough, F.H., Andrews, R.M., Crump, M.L., Savitzky, A.H., Wells, table. Copeia 1985: 423-436. K.D., Brandley. M.C. (2016): Herpetology. Sunderland, Sinauer Townsend, D.S., Stewart, M.M. (1994): Reproductive ecology Associates, Inc. of the Puerto Rican frog Eleutherodactylus coqui. Journal of Rodríguez, A., Alonso, R. (2009): Eleutherodactylus leberi (NCN). Herpetology 28: 34-40. Clutch size and parental care. Herpetological Review 40: 204. Townsend, D.S., Stewart, M.M., Pough, F.H. (1984): Male parental Schwartz, A., Henderson, R.W. (1991): Amphibian and Reptiles care and its adaptive significance in a neotropical frog. Animal of the West Indies: Descriptions, Distributions, and Natural Behaviour 32: 421-431. History. Gainesville, University of Florida Press. Trivers, R.L. (1972): Parental investment and sexual selection. In: Skermer, G.H. (1939): A note on Eleutherodactylus ricordii. Sexual Selection and the Descent of Man, p. 136-179. Campbell Copeia 1939: 107-108. B.G. Eds., Chicago, Andine Press. Taigen, T.L., Pough, F.H., Stewart, M.M. (1984): Water balance of Wells, K.D. (1981): Parental behavior of male and female frogs. In: terrestrial anuran (Eleutherodactylus coqui) eggs: importance of Natural Selection and Social Behavior, p. 184-197. Alexander, parental care. Ecology 65: 248-255. R.D., Tinkle D.W. Eds. Incorporated, New York Chiron Press. Townsend, D.S. (1996): Patterns of parental care in frogs of Wells, K.D. (2007): The Ecology and Behavior of Amphibians. the genus Eleutherodactylus. In: Contribution to West India Chicago, The University of Chicago Press. Herpetology, pp. 229-239. Powell, R., Henderson R.W., Eds. New York Society for the Study of Amphibians and Reptiles, Ithaca.

Accepted by Gabriela Bittencourt-Silva