Evolutionary Biology

Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects

10.24072/pcjournal.176 - Peer Community Journal, Volume 2 (2022), article no. e57.

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When environmental conditions are unpredictable, expressing alternative phenotypes spreads the risk of failure, a mixed strategy called bet-hedging. In the southern part of its range, the Parsley Frog Pelodytes punctatus breeds both in autumn and in spring. Our aim was to study the breeding phenology and reproductive success associated with the use of those two seasonal niches to understand how this breeding strategy can be maintained. Field surveys revealed that breeding phenology was typically bimodal with a higher breeding effort in autumn. More importantly, in spring, the survival rate of offspring was severely reduced by the presence of autumn tadpoles, indicating a clear priority effect. However, the autumn cohort often failed to survive over winter, in which case spring cohorts were often successful. Based on those results, we constructed a model in which females can allocate a variable portion of eggs to each season and added a priority effect. We conclude that the existence of the two breeding seasons may indeed constitute a bet-hedging strategy.

Published online:
DOI: 10.24072/pcjournal.176
Jourdan-Pineau, Hélène 1; Crochet, Pierre-André 2; David, Patrice 2

1 ASTRE, Univ Montpellier, CIRAD, INRAE, F-34398 Montpellier, France
2 CEFE, UMR 5175 CNRS, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Jourdan-Pineau, Hélène; Crochet, Pierre-André; David, Patrice. Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects. Peer Community Journal, Volume 2 (2022), article  no. e57. doi : 10.24072/pcjournal.176. https://peercommunityjournal.org/articles/10.24072/pcjournal.176/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100147

[1] Alanärä, A.; Burns, M. D.; Metcalfe, N. B. Intraspecific resource partitioning in brown trout: the temporal distribution of foraging is determined by social rank, Journal of Animal Ecology, Volume 70 (2001) no. 6, pp. 980-986 | DOI

[2] Albrecht, M.; Gotelli, N. Spatial and temporal niche partitioning in grassland ants, Oecologia, Volume 126 (2001) no. 1, pp. 134-141 | DOI

[3] Altwegg, R.; Reyer, H.-U. Patterns of natural selection on size at metamorphosis in water frogs, Evolution, Volume 57 (2003) no. 4, pp. 872-882 | DOI

[4] Baker, G.; Beebee, T. J. Evidence for the induction of interference competition between anuran larvae in plastic pond cages, Amphibia-Reptilia, Volume 21 (2000) no. 1, pp. 25-37 | DOI

[5] Banks, B.; Beebee, T. J. C. Reproductive Success of Natterjack Toads Bufo calamita in Two Contrasting Habitats, The Journal of Animal Ecology, Volume 57 (1988) no. 2 | DOI

[6] Barandun, J.; Reyer, H.-U. Reproductive Ecology of Bombina variegata: Development of Eggs and Larvae, Journal of Herpetology, Volume 31 (1997) no. 1 | DOI

[7] Beaumont, H. J. E.; Gallie, J.; Kost, C.; Ferguson, G. C.; Rainey, P. B. Experimental evolution of bet hedging, Nature, Volume 462 (2009) no. 7269, pp. 90-93 | DOI

[8] Beebee, T. J. C.; Wong, A. L.-C. Prototheca-Mediated Interference Competition between Anuran Larvae Operates by Resource Diversion, Physiological Zoology, Volume 65 (1992) no. 4, pp. 815-831 | DOI

[9] Di Bitetti, M. S.; De Angelo, C. D.; Di Blanco, Y. E.; Paviolo, A. Niche partitioning and species coexistence in a Neotropical felid assemblage, Acta Oecologica, Volume 36 (2010) no. 4, pp. 403-412 | DOI

[10] Blaustein, L.; Margalit, J. Priority Effects in Temporary Pools: Nature and Outcome of Mosquito Larva-Toad Tadpole Interactions Depend on Order of Entrance, The Journal of Animal Ecology, Volume 65 (1996) no. 1 | DOI

[11] Brown, C. J.; O'Connor, M. I.; Poloczanska, E. S.; Schoeman, D. S.; Buckley, L. B.; Burrows, M. T.; Duarte, C. M.; Halpern, B. S.; Pandolfi, J. M.; Parmesan, C.; Richardson, A. J. Ecological and methodological drivers of species’ distribution and phenology responses to climate change, Global Change Biology, Volume 22 (2016) no. 4, pp. 1548-1560 | DOI

[12] Van Buskirk, J.; Arioli, M. Habitat specialization and adaptive phenotypic divergence of anuran populations, Journal of Evolutionary Biology, Volume 18 (2005) no. 3, pp. 596-608 | DOI

[13] Carothers, J. H.; Jaksić, F. M.; Jaksic, F. M. Time as a Niche Difference: The Role of Interference Competition, Oikos, Volume 42 (1984) no. 3 | DOI

[14] Cayuela, H.; Besnard, A.; Béchet, A.; Devictor, V.; Olivier, A. Reproductive dynamics of three amphibian species in Mediterranean wetlands: the role of local precipitation and hydrological regimes, Freshwater Biology, Volume 57 (2012) no. 12, pp. 2629-2640 | DOI

[15] Charmantier, A.; Gienapp, P. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes, Evolutionary Applications, Volume 7 (2014) no. 1, pp. 15-28 | DOI

[16] Cohen, D. Optimizing reproduction in a randomly varying environment, Journal of Theoretical Biology, Volume 12 (1966) no. 1, pp. 119-129 | DOI

[17] Cohen, D. A Theoretical Model for the Optimal Timing of Diapause, The American Naturalist, Volume 104 (1970) no. 938, pp. 389-400 | DOI

[18] Crochet, P.-A.; Chaline, O.; Cheylan, M.; Guillaume, C. P. No evidence of general decline in an amphibian community of Southern France, Biological Conservation, Volume 119 (2004) no. 3, pp. 297-304 | DOI

[19] Crump ML Choice of Oviposition Site and Egg Load Assessment by a Treefrog, Herpetologica, Volume 47 (1991), pp. 308-315

[20] Dayton, G. H.; Fitzgerald, L. A. Priority effects and desert anuran communities, Canadian Journal of Zoology, Volume 83 (2005) no. 8, pp. 1112-1116 | DOI

[21] Dayton, G. H.; Wapo, S. D. Cannibalistic Behavior in Scaphiopus couchii: More Evidence for Larval Anuran Oophagy, Journal of Herpetology, Volume 36 (2002) no. 3, pp. 531-532 | DOI

[22] Dempster, E. R. Maintenance of genetic heterogeneity, Cold Spring Harbor Symposia on Quantitative Biology, Volume 20 (1955), pp. 25-32 | DOI

[23] Eitam, A.; Blaustein, L.; Mangel, M. Density and intercohort priority effects on larval Salamandra salamandra in temporary pools, Oecologia, Volume 146 (2005) no. 1, pp. 36-42 | DOI

[24] Erich, M.; Ringler, M.; Hödl, W.; Ringler, E. Brood-partitioning behaviour in unpredictable environments: hedging the bets?, Behavioral Ecology and Sociobiology, Volume 69 (2015) no. 6, pp. 1011-1017 | DOI

[25] Esteban, M.; Sánchez-Herráiz, M. J.; Barbadillo, L. J.; Castanet, J. Age structure and growth in an isolated population of Pelodytes punctatus in northern Spain, Journal of Natural History, Volume 38 (2004) no. 21, pp. 2789-2801 | DOI

[26] Forrest, J. R. K.; Cross, R.; CaraDonna, P. J. Two-Year Bee, or Not Two-Year Bee? How Voltinism Is Affected by Temperature and Season Length in a High-Elevation Solitary Bee, The American Naturalist, Volume 193 (2019) no. 4, pp. 560-574 | DOI

[27] Frederiksen, M.; Harris, M. P.; Daunt, F.; Rothery, P.; Wanless, S. Scale-dependent climate signals drive breeding phenology of three seabird species, Global Change Biology, Volume 10 (2004) no. 7, pp. 1214-1221 | DOI

[28] García-Roger, E. M.; Carmona, M. J.; Serra, M. Modes, mechanisms and evidence of bet hedging in rotifer diapause traits, Hydrobiologia, Volume 796 (2017) no. 1, pp. 223-233 | DOI

[29] Gascon, C. Aquatic Predators and Tadpole Prey in Central Amazonia: Field Data and Experimental Manipulations, Ecology, Volume 73 (1992) no. 3, pp. 971-980 | DOI

[30] Guyétant, R.; Temmermans, W.; Avrillier, J. Phénologie de la reproduction chez Pelodytes punctatus Daudin, 1802 (Amphibia, Anura), Amphibia-Reptilia, Volume 20 (1999) no. 2, pp. 149-160 | DOI

[31] Gottsberger, B.; Gruber, E. Temporal partitioning of reproductive activity in a neotropical anuran community, Journal of Tropical Ecology, Volume 20 (2004) no. 3, pp. 271-280 | DOI

[32] Graham, J. K.; Smith, M. L.; Simons, A. M. Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1787 | DOI

[33] Gremer, J. R.; Kimball, S.; Venable, D. L. Within‐and among‐year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment, Ecology Letters, Volume 19 (2016) no. 10, pp. 1209-1218 | DOI

[34] Gremer, J. R.; Venable, D. L. Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment, Ecology Letters, Volume 17 (2014) no. 3, pp. 380-387 | DOI

[35] Haaland, T. R.; Wright, J.; Ratikainen, I. I. Individual reversible plasticity as a genotype‐level bet‐hedging strategy, Journal of Evolutionary Biology, Volume 34 (2021) no. 7, pp. 1022-1033 | DOI

[36] Halloy, M. Choice of oviposition site in Pleurodema borellii (Leptodactylidae): importance of conspecific tadpole size, South American Journal of Herpetology, Volume 1 (2006) no. 1, pp. 72-78 | DOI

[37] Halloy, M.; Fiaño, J. M. Oviposition Site Selection in Pleurodema borellii (Anura: Leptodactylidae) May Be Influenced by Tadpole Presence, Copeia, Volume 2000 (2000) no. 2, pp. 606-609 | DOI

[38] Hartel, T.; Nemes, S.; Mara, G. Breeding phenology and spatio-temporal dynamics of pond use by the yellow-bellied toad (Bombina variegata) population: the importance of pond availability and duration, Acta Zoologica Lituanica, Volume 17 (2007) no. 1, pp. 56-63 | DOI

[39] Jakob, C.; Poizat, G.; Veith, M.; Seitz, A.; Crivelli, A. J. Breeding phenology and larval distribution of amphibians in a Mediterranean pond network with unpredictable hydrology, Hydrobiologia, Volume 499 (2003) no. 1/3, pp. 51-61 | DOI

[40] Jourdan-Pineau, H.; David, P.; Crochet, P.-A. Phenotypic plasticity allows the Mediterranean parsley frog Pelodytes punctatus to exploit two temporal niches under continuous gene flow, Molecular Ecology, Volume 21 (2012) no. 4, pp. 876-886 | DOI

[41] Kivelä, S. M.; Välimäki, P.; Gotthard, K. Seasonality maintains alternative life-history phenotypes, Evolution, Volume 67 (2013) no. 11, pp. 3145-3160 | DOI

[42] Lardner, B.; Loman, J. Growth or reproduction? Resource allocation by female frogs Rana temporaria, Oecologia, Volume 137 (2003) no. 4, pp. 541-546 | DOI

[43] Lawler, S. P.; Morin, P. J. Temporal Overlap, Competition, and Priority Effects in Larval Anurans, Ecology, Volume 74 (1993) no. 1, pp. 174-182 | DOI

[44] Leimar, O. The Evolution of Phenotypic Polymorphism: Randomized Strategies versus Evolutionary Branching, The American Naturalist, Volume 165 (2005) no. 6, pp. 669-681 | DOI

[45] Lewontin, R. C.; Cohen, D. On population growth in a randomly varying environment, Proceedings of the National Academy of Sciences, Volume 62 (1969) no. 4, pp. 1056-1060 | DOI

[46] Licht, L. E. Survival of embryos, tadpoles, and adults of the frogs Rana aurora aurora and Rana pretiosa pretiosa sympatric in southwestern British Columbia, Canadian Journal of Zoology, Volume 52 (1974) no. 5, pp. 613-627 | DOI

[47] Maxwell, C. S.; Magwene, P. M. When sensing is gambling: An experimental system reveals how plasticity can generate tunable bet‐hedging strategies, Evolution, Volume 71 (2017) no. 4, pp. 859-871 | DOI

[48] Møller, A. P. Climate change and micro-geographic variation in laying date, Oecologia, Volume 155 (2008) no. 4, pp. 845-857 | DOI

[49] Morand, A.; Pierre, J. Habitat variability and space utilization by the amphibian communities of the French upper-rhone floodplain, Hydrobiologia, Volume 300-301 (1995) no. 1, pp. 249-257 | DOI

[50] Morin, P. J. Predation, Breeding Asynchrony, and the Outcome of Competition Among Treefrog Tadpoles, Ecology, Volume 68 (1987) no. 3, pp. 675-683 | DOI

[51] Morin, P. J.; Lawler, S. P.; Johnson, E. A. Ecology and Breeding Phenology of Larval Hyla Andersonii: The Disadvantages of Breeding Late, Ecology, Volume 71 (1990) no. 4, pp. 1590-1598 | DOI

[52] Murillo-Rincón, A. P.; Kolter, N. A.; Laurila, A.; Orizaola, G. Intraspecific priority effects modify compensatory responses to changes in hatching phenology in an amphibian, Journal of Animal Ecology, Volume 86 (2017) no. 1, pp. 128-135 | DOI

[53] Olofsson, H.; Ripa, J.; Jonzén, N. Bet-hedging as an evolutionary game: the trade-off between egg size and number, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1669, pp. 2963-2969 | DOI

[54] Philippi, T.; Seger, J. Hedging one's evolutionary bets, revisited, Trends in Ecology & Evolution, Volume 4 (1989) no. 2, pp. 41-44 | DOI

[55] Poethke, H. J.; Hovestadt, T.; Mitesser, O. The evolution of optimal emergence times: bet hedging and the quest for an ideal free temporal distribution of individuals, Oikos, Volume 125 (2016) no. 11, pp. 1647-1656 | DOI

[56] R Core Team R: A Language and Environment for Statistical Computing, 2018

[57] Rádai, Z. Cohort splitting from plastic bet-hedging: insights from empirical and theoretical investigations in a wolf spider, Theoretical Ecology, Volume 14 (2020) no. 1, pp. 9-21 | DOI

[58] Rand, W. M. A stochastic model of the temporal aspect of breeding strategies, Journal of Theoretical Biology, Volume 40 (1973) no. 2, pp. 337-351 | DOI

[59] Richter-Boix, A.; Llorente, G. A.; Montori, A. Breeding phenology of an amphibian community in a Mediterranean area, Amphibia-Reptilia, Volume 27 (2006) no. 4, pp. 549-559 | DOI

[60] Richter-Boix, A.; Llorente, G. A.; Montori, A. A comparative analysis of the adaptive developmental plasticity hypothesis in six Mediterranean anuran species along a pond permanency gradient, Evolutionary Ecology Research, Volume 8 (2006), pp. 1139-1154

[61] Richter-Boix, A.; Llorente, G. A.; Montori, A. A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient, Hydrobiologia, Volume 583 (2007) no. 1, pp. 43-56 | DOI

[62] Richter-Boix, A.; Llorente, G.; Montori, A. Hierarchical competition in pond-breeding anuran larvae in a Mediterranean area, Amphibia-Reptilia, Volume 28 (2007) no. 2, pp. 247-261 | DOI

[63] Richter-Boix, A.; Llorente, G. A.; Montori, A. Structure and dynamics of an amphibian metacommunity in two regions, Journal of Animal Ecology, Volume 76 (2007) no. 3, pp. 607-618 | DOI

[64] Ryan, T. J.; Plague, G. R. Hatching asynchrony, survival, and the fitness of alternative adult morphs in Ambystoma talpoideum, Oecologia, Volume 140 (2004) no. 1, pp. 46-51 | DOI

[65] Sadeh, A.; Mangel, M.; Blaustein, L. Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics, Ecology Letters, Volume 12 (2009) no. 11, pp. 1158-1164 | DOI

[66] Saiah, H.; Perrin, N. Autumnal vs Spring Hatching in the Fairy Shrimp Siphonophanes grubii (Dybowski) (Crustacea, Anostraca): Diversified Bet-Hedging Strategy?, Functional Ecology, Volume 4 (1990) no. 6 | DOI

[67] Salvador, A.; Paris, M. Anfibios Espanoles, 2001

[68] Salvidio, S.; Lamagni, L.; Bombi, P.; Bologna, M. A. Distribution, ecology and conservation of the parsley frog (Pelodytes punctatus) in Italy (Amphibia, Pelodytidae), Italian Journal of Zoology, Volume 71 (2004) no. sup1, pp. 73-81 | DOI

[69] Seger, J.; Brockman, H. What is bet-hedging?, Oxford Surv. Evol. Biol., Volume 4 (1987)

[70] Simons, A. M. Modes of response to environmental change and the elusive empirical evidence for bet hedging, Proceedings of the Royal Society B: Biological Sciences, Volume 278 (2011) no. 1712, pp. 1601-1609 | DOI

[71] Simovich, M.; Hathaway, S. Diversified bet-hedging as a reproductive strategy of some ephemeral pool anostracans (Branchiopoda), Journal of Crustacean Biology, Volume 17 (1997) no. 1, pp. 38-44 | DOI

[72] Slatkin, M. Hedging one's evolutionary bets, Nature, Volume 250 (1974) no. 5469, pp. 704-705 | DOI

[73] Smith, D. C. Adult Recruitment in Chorus Frogs: Effects of Size and Date at Metamorphosis, Ecology, Volume 68 (1987) no. 2, pp. 344-350 | DOI

[74] Summers, K. The effects of cannibalism on Amazonian poison frog egg and tadpole deposition and survivorship in Heliconia axil pools, Oecologia, Volume 119 (1999) no. 4, pp. 557-564 | DOI

[75] Székely, D.; Cogălniceanu, D.; Székely, P.; Armijos-Ojeda, D.; Espinosa-Mogrovejo, V.; Denoël, M. How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian, BMC Ecology, Volume 20 (2020) no. 1 | DOI

[76] Tarazona, E.; García-Roger, E. M.; Carmona, M. J. Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability, Oikos, Volume 126 (2017) no. 8, pp. 1162-1172 | DOI

[77] Tejedo, M. Effect of Predation by 2 Species of Sympatric Tadpoles on Embryo Survival in Natterjack Toads (Bufo-Calamita), Herpetologica, Volume 47 (1991), pp. 322-327

[78] Tejedo, M. Size-dependent vulnerability and behavioral responses of tadpoles of two anuran species to beetle larvae predators, Herpetologica, Volume 49 (1993), pp. 287-294

[79] Toxopeus, A.; Ohm, M.; Arntzen, J. Reproductive biology of the parsley frog, Pelodytes punctatus, at the northernmost part of its range, Amphibia-Reptilia, Volume 14 (1993) no. 2, pp. 131-147 | DOI

[80] Urban, M. C.; De Meester, L. Community monopolization: local adaptation enhances priority effects in an evolving metacommunity, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1676, pp. 4129-4138 | DOI

[81] Venable, D. L. Bet hedging in a guild of desert annuals, Ecology, Volume 88 (2007) no. 5, pp. 1086-1090 | DOI

[82] Wang, C.-C.; Rogers, D. C. Bet hedging in stochastic habitats: an approach through large branchiopods in a temporary wetland, Oecologia, Volume 188 (2018) no. 4, pp. 1081-1093 | DOI

[83] Wheeler, C. A.; Bettaso, J. B.; Ashton, D. T.; Welsh, H. H. Effects of Water Temperature on Breeding Phenology, Growth, and Metamorphosis of Foothill Yellow-Legged Frogs (Rana boylii): A Case Study of the Regulated Mainstem and Unregulated Tributaries of California's Trinity River, River Research and Applications, Volume 31 (2015) no. 10, pp. 1276-1286 | DOI

[84] Wolfram Research Inc. Mathematica, Version 11.3, 2018

[85] Yasui, Y.; Yoshimura, J. Bet-hedging against male-caused reproductive failures may explain ubiquitous cuckoldry in female birds, Journal of Theoretical Biology, Volume 437 (2018), pp. 214-221 | DOI

[86] Zeuss, D.; Brunzel, S.; Brandl, R. Environmental drivers of voltinism and body size in insect assemblages across Europe, Global Ecology and Biogeography, Volume 26 (2017) no. 2, pp. 154-165 | DOI

[87] Zuur, A. F.; Ieno, E. N.; Walker, N.; Saveliev, A. A.; Smith, G. M. Mixed effects models and extensions in ecology with R, Statistics for Biology and Health, Springer New York, New York, NY, 2009 | DOI

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