Abstract
For externally fertilizing animals, the early stages of development are often the most precarious. In the face of multiple abiotic and biotic stressors, parents must assess and select rearing sites that maximize the probability of offspring survival. This is particularly true for Neotropical poison frogs, many of which transport tadpoles to small pools of water called phytotelmata that serve as larval rearing sites. In these systems, pool choice can have a large effect on offspring growth and survival. Here, we studied the golden rocket frog (Anomaloglossus beebei, Aromobatidae), a territorial phytotelm-breeding frog that lives exclusively in giant tank bromeliads (Brocchinia micrantha), to examine phytotelm selection and reproductive resource defense. We first quantified the characteristics of phytotelmata and found that tadpoles were more likely to occur in pools with low levels of mucilage and in leaves at intermediate heights on the plant. We additionally found that low mucilage pools have significantly clearer water, have higher concentrations of dissolved oxygen, and are exposed to lower levels of photosynthetically active radiation. We then mapped the spatial distribution of pools with low levels of mucilage in relation to male territories and found that these “clear” pools are (1) more likely to be within male territories than outside of them, and (2) territory centroids are closer to clear pools than are random locations. Overall, our results show that male golden rocket frogs defend territories that include preferred tadpole deposition sites, suggesting a direct relationship between high-quality reproductive resources and territory defense.
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Data and code associated with this paper are archived on Dryad (https://doi.org/10.5061/dryad.66t1g1k74) and Zenodo (https://doi.org/10.5281/zenodo.8393752).
Change history
22 November 2023
A Correction to this paper has been published: https://doi.org/10.1007/s10682-023-10279-9
References
Ballego-Campos I, Paiva ÉAS (2018) Mucilage secretion in the inflorescences of Aechmea Blanchetiana: evidence of new functions of scales in Bromeliaceae. Flora: Morphology Distribution Functional Ecology of Plants 246–247:1–9. https://doi.org/10.1016/j.flora.2018.06.003
Benzing DH (2000) Bromeliaceae: profile of an adaptive radiation. Cambridge University Press, Cambridge, U.K
Benzing DH, Derr JA, Titus JE (1972) The water chemistry of microcosms associated with the bromeliad Aechmea bracteata. Am Midl Nat 87:60–70
Bivand R, Rundel C (2023) rgeos: Interface to geometry engine - open source (‘GEOS’). R package version 0.6-2. https://CRAN.R-project.org/package=rgeos
Bivand RS, Pebesma E, Gomez-Rubio V (2013) Applied spatial data analysis with R, Second edition. Springer, NY. https://asdar-book.org/
Bourne GR, Collins a C, Holder AM, McCarthy CL (2001) Vocal communication and reproductive behavior of the frog Colostethus beebei in Guyana. J Herpetol 35:272–281. https://doi.org/10.2307/1566118
Brooks M, Kristensen K, van Benthem KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized Linear mixed modeling. R J 9:378–400. https://doi.org/10.32614/RJ-2017-066
Brown JL, Morales V, Summers K (2008) Divergence in parental care, habitat selection and larval life history between two species of Peruvian Poison frogs: an experimental analysis. J Evol Biol 21:1534–1543. https://doi.org/10.1111/j.1420-9101.2008.01609.x
Brown JL, Morales V, Summers K (2009a) Tactical reproductive parasitism via larval cannibalism in Peruvian Poison frogs. Biol Lett 5:148–151. https://doi.org/10.1098/rsbl.2008.0591
Brown JL, Morales V, Summers K (2009b) Home range size and location in relation to reproductive resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Animal Behaviour 77:547–554. https://doi.org/10.1016/j.anbehav.2008.10.002
Buosi PRB, Cabral AF, Utz LRP et al (2015) Effects of Seasonality and Dispersal on the Ciliate Community Inhabiting Bromeliad Phytotelmata in Riparian Vegetation of a large Tropical River. J Eukaryot Microbiol 62:737–749. https://doi.org/10.1111/jeu.12232
Caldwell JP (1993) Brazil nut fruit capsules as phytotelmata: interactions among anuran and insect larvae. Can J Zool. https://doi.org/10.1139/z93-163
Caldwell JP, de Araujo MC (1998) Cannibalistic interactions resulting from indiscriminate predatory behavior in tadpoles of Poison frogs (Anura: Dendrobatidae). Biotropica 30:92–103. https://doi.org/10.1111/j.1744-7429.1998.tb00372.x
Caldwell JP, de Araújo MC (2004) Historical and ecological factors influence survivorship in two clades of phytotelm-breeding frogs (Anura: Bufonidae, Dendrobatidae). Miscellaneous Publications Museum of Zoology University of Michigan, pp 11–21
Caldwell JP, de Oliveira VRL (1999) Determinants of biparental care in the spotted Poison frog, Dendrobates vanzolinii (Anura: Dendrobatidae). Copeia 1999:565–575. https://doi.org/10.2307/1447590
Christy JH (1983) Female choice in the resource-defense mating system of the sand fiddler crab, Uca pugilator. Behav Ecol Sociobiol 12:169–180. https://doi.org/10.1007/BF00343209
Dendi D, Förster T, Chaboo CS (2023) Arthropod diversity in phytotelmata of Calathea capitata (Zingiberales; Marantaceae) host plants from Peru. Rev Peru Biol 30:e25654. https://doi.org/10.15381/rpb.v30i2.25654
Dodson GN (1997) Resource defense mating system in antlered flies, Phytalmia spp. (Diptera: Tephritidae). Ann Entomol Soc Am 90(4):496–504. https://doi.org/10.1093/aesa/90.4.496
Engelbrecht-Wiggans E, Tumulty JP (2019) Reverse sexual dichromatism in a neotropical frog. Ethology 125:957–964. https://doi.org/10.1111/eth.12942
Fincke OM (1992) Consequences of Larval Ecology for Territoriality and Reproductive Success of a neotropical damselfly. Ecology 73:449–462. https://doi.org/10.2307/1940752
Fincke OM (1999) Organization of predator assemblages in neotropical tree holes: effects of abiotic factors and priority. Ecol Entomol 24:13–23. https://doi.org/10.1046/j.1365-2311.1999.00166.x
Fouilloux CA, Serrano Rojas SJ, Carvajal-Castro JD et al (2021) Pool choice in a vertical landscape: Tadpole‐rearing site flexibility in phytotelm‐breeding frogs. Ecol Evol. https://doi.org/10.1002/ece3.7741. ece3.7741
Fouilloux CA, Yovanovich CAM, Rojas B (2022) Tadpole responses to environments with limited visibility: what we (don’t) know and perspectives for a sharper future. Front Ecol Evol 9:1–8. https://doi.org/10.3389/fevo.2021.766725
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. The American Naturalist, 124(4), 479–497.
Hartig F (2021) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.4.6.
Howard RD (1978) The influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecology 59(4):789–798. https://doi.org/10.2307/1938783
Jenkins DW, Carpenter SJ (1946) Ecology of the tree hole breeding mosquitoes of Nearctic North America. Ecol Monogr 16:31–47. https://doi.org/10.2307/1943573
Jocque M, Fiers F, Romero M, Martens K (2013) Crustacea in phytotelmata: a global overview. J Crustac Biol 33:451–460. https://doi.org/10.1163/1937240x-00002161
Kaufmann JH (1983) On the definitions and functions of Dominance and Territoriality. Biol Rev 58:1–20. https://doi.org/10.1111/j.1469-185X.1983.tb00379.x
Kitching RL (2000) Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press
Klug H, Bonsall MB (2014) What are the benefits of parental care? The importance of parental effects on developmental rate. Ecol Evol 4:2330–2351. https://doi.org/10.1002/ece3.1083
Lin Y-S, Lehtinen RM, Kam Y-C (2009) Time- and context-dependent oviposition site selection of a phytotelm-breeding frog in relation to habitat characteristics and conspecific cues. https://doi.org/10.1655/08-020r1.1. Herpetologica
Mageski MM, Ferreira RB, Beard KH et al (2016) Bromeliad selection by Phyllodytes luteolus (Anura, Hylidae): the influence of plant structure and water quality factors. J Herpetol 50:108–112. https://doi.org/10.1670/14-166
Miller TE, Horth L, Reeves RH (2002) Trophic interactions in the phytotelmata communities of the pitcher plant, Sarracenia purpurea. Community Ecol 3:109–116. https://doi.org/10.1556/ComEc.3.2002.1.13
Pašukonis A, Loretto M-C, Rojas B (2019) How far do tadpoles travel in the rainforest? Parent-assisted dispersal in Poison frogs. Evol Ecol. https://doi.org/10.1007/s10682-019-09994-z
Pettitt BA (2012) Paternal effort in relation to acoustically mediated mate choice in a neotropical frog. University of Minnesota, Minneapolis, MN. PhD Dissertation
Pettitt BA, Bourne GR, Bee MA (2018) Predictors and benefits of microhabitat selection for offspring deposition in golden rocket frogs. 50:919–928. https://doi.org/10.1111/btp.12609
Pettitt BA, Bourne GR, Bee MA (2020) Females prefer the calls of better fathers in a neotropical frog with biparental care. Behav Ecol 31:152–163. https://doi.org/10.1093/beheco/arz172
Poelman EH, Dicke M (2008) Space use of Amazonian poison frogs: testing the reproductive resource defense hypothesis. Journal of Herpetology, 42(2), 270–278. https://doi.org/10.1670/07-1031.1
Poelman EH, van Wijngaarden RPA, Raaijmakers CE (2013) Amazon Poison frogs (Ranitomeya amazonica) use different phytotelm characteristics to determine their suitability for egg and tadpole deposition. Evol Ecol 27:661–674. https://doi.org/10.1007/s10682-013-9633-3
Pröhl H (2005) Territorial behavior in Dendrobatid frogs. J Herpetol 39:354–365. https://doi.org/10.1670/162-04A.1
Pröhl H, Berke O (2001) Spatial distributions of male and female strawberry Poison frogs and their relation to female reproductive resources. Oecologia 129:534–542. https://doi.org/10.1007/s004420100751
Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Evol Syst 41:39–57. https://doi.org/10.1146/annurev-ecolsys-102209-144712
Rojas B (2014) Strange parental decisions: fathers of the dyeing Poison frog deposit their tadpoles in pools occupied by large cannibals. Behav Ecol Sociobiol 68:551–559. https://doi.org/10.1007/s00265-013-1670-y
Ruano-Fajardo G, Rovito SM, Ladle RJ (2014) Bromeliad selection by two salamander species in a harsh environment. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0098474
Rudolf VHW, Rödel MO (2004) Oviposition site selection in a complex and variable environment: the role of habitat quality and conspecific cues. Oecologia 142:316–325. https://doi.org/10.1007/s00442-004-1668-2
Salthe SN, Mecham JS (1974) Reproductive and courtship patterns. In: Lofts B (ed) Physiology of the Amphibia. Academic Press, Inc.
Sato T (1994) Active accumulation of spawning substrate: a determinant of extreme polygyny in a shell-brooding cichlid fish. Anim Behav 48:669–678. https://doi.org/10.1006/anbe.1994.1286
Schmidl J, Sulzer P, Kitching RL (2008) The insect assemblage in water filled tree-holes in a European temperate deciduous forest: community composition reflects structural, trophic and physicochemical factors. Hydrobiologia 598:285–303. https://doi.org/10.1007/s10750-007-9163-5
Schulte LM, Mayer M (2017) Poison frog tadpoles seek parental transportation to escape their cannibalistic siblings. J Zool 303:83–89. https://doi.org/10.1111/jzo.12472
Schulte LM, Yeager J, Schulte R et al (2011) The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian Poison frog. Anim Behav 81:1147–1154. https://doi.org/10.1016/j.anbehav.2011.02.019
Serrano-Rojas SJ, Pašukonis A (2021) Tadpole-transporting frogs use stagnant water odor to find pools in the rainforest. J Exp Biol 224. https://doi.org/10.1242/jeb.243122
Sowig P (1995) Habitat selection and offspring survival rate in three paracoprid dung beetles: the influence of soil type and soil moisture. Ecography 18:147–154. https://doi.org/10.1111/j.1600-0587.1995.tb00335.x
Stynoski JL, Noble VR (2012) To beg or to freeze: multimodal sensory integration directs behavior in a tadpole. Behav Ecol Sociobiol 66:191–199. https://doi.org/10.1007/s00265-011-1266-3
Summers K (1999) The effects of cannibalism on amazonian Poison frog egg and tadpole deposition and survivorship in Heliconia axil pools. Oecologia 119:557–564. https://doi.org/10.1007/s004420050819
Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in neotropical Poison frogs. Museum of Zoology, Univ Mich 192
Summers K, Tumulty J (2014) Parental care, sexual selection, and mating systems in Neotropical poison frogs. In: Macedo RH, Machado G (eds) Sexual Selection: Perspectives and Models from the Neotropics. Academic Press, Waltham, MA, pp 289–320
Summers K, Tumulty J (2013) Parental care, sexual selection, and mating systems in Neotropical poison frogs. In: Sexual Selection: Perspectives and Models from the Neotropics. pp 289–320. https://doi.org/10.1016/B978-0-12-416028-6.00011-6
Tumulty JP, Bee MA (2021) Ecological and social drivers of neighbor recognition and the dear enemy effect in a Poison frog. Behav Ecol 32:138–150. https://doi.org/10.1093/beheco/araa113
Tumulty JP, Fouilloux CA, Vallejos JG, Bee MA (2022a) Predicting and measuring decision rules for social recognition in a neotropical frog. Am Nat 200. https://doi.org/10.1086/720279
Tumulty JP, Lange ZK, Bee MA (2022b) Identity signaling, identity reception, and the evolution of social recognition in a neotropical frog. Evol (N Y) 76:158–170. https://doi.org/10.1111/evo.14400
Vaira M (2005) Annual variation of breeding patterns of the toad, Melanophryniscus rubriventris (Vellard, 1947). Amphibia Reptilia 26:193–199. https://doi.org/10.1163/1568538054253519
von May R, Medina-Mueller M, Donnelly MA, Summers K (2009) Breeding-site selection by the Poison frog Ranitomeya biolat in amazonian bamboo forests: an experimental approach. 463:453–463. https://doi.org/10.1139/Z09-026
Wassersug RJ, Feder ME (1983) The effects of aquatic oxygen concentration, body size and respiratory behaviour on the stamina of obligate aquatic (Bufo americanus) and facultative air-breathing (Xenopus laevis and Rana berlandieri) anuran larvae. J Exp Biol 105:173–190. https://doi.org/10.1242/jeb.105.1.173
Yanoviak SP (2001) Predation, resource availability, and community structure in neotropical water-filled tree holes. Oecologia 126:125–133. https://doi.org/10.1007/s004420000493
Acknowledgements
CAF would like to thank the Jyväskylä Journal Club for their helpful comments on earlier versions of this manuscript. We would like to thank James Cotner for help identifying components of the bromeliad mucilage and Mark Bee for feedback and mentoring. Finally, we thank two anonymous reviewers for comments which helped improve our paper.
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This research was funded by the Rosemary Grant Award from the Society for the Study of Evolution to JPT, the Lewis and Clark Fund grant from the American Philosophical Society to JPT, and a National Science Foundation Doctoral Dissertation Improvement Grant (no. 1601493) to JPT and Mark A. Bee.
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All authors conceived of the experiment and collected the data. CAF gave form to the initial manuscript; CAF and JPT prepared the figures; all authors conducted statistical analyses, reviewed and the text, and approved the final submission.
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Fouilloux, C.A., Goyes Vallejos, J. & Tumulty, J.P. Home is where the high-quality resources are: nursery characteristics and territory distribution suggest reproductive resource defense in golden rocket frogs. Evol Ecol (2023). https://doi.org/10.1007/s10682-023-10273-1
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DOI: https://doi.org/10.1007/s10682-023-10273-1