Antipredator strategies increase the chances of survival of prey species but are subject to trade-offs and always come at a cost, one specific category being the "missed opportunity." Some animals that can modulate the timing of life-cycle events can also desynchronize this timing with the occurrence of a predator. In an unpredictable environment, such a modification may result in a mismatch with prevailing conditions, consequently leading to reproductive failure. In eastern Africa, temporary pools existing only during the rainy season are inhabited by annual fish of the genus Nothobranchius. We examined (i) the capability of multiple Nothobranchius populations and species to cease hatching when exposed to chemical cues from native fish predators and adult conspecifics and (ii) the ability of N. furzeri to modulate their growth rate in the presence of a gape-limited fish predator. As the tested Nothobranchius spp. originate from regions with extreme environmental fluctuations where the cost of a missed opportunity can be serious, we predicted an inability to cease hatching as well as lack of growth acceleration as both the predator's gape limitation and the environment select for the same adaptation. Our results showed no biologically relevant influence of kairomone on hatching and no influence on growth rate. This suggests that, in an unpredictable environment, the costs of a missed opportunity are substantial enough to prevent the evolution of some antipredator defense strategies.

Institute of Vertebrate Biology Brno Czech Republic

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Apfelbach, R. , Blanchard, C. D. , Blanchard, R. J. , Hayes, R. A. , & McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neuroscience & Biobehavioral Reviews, 29, 1123–1144. PubMed

Barry, M. J. (2014). The energetic cost of foraging explains growth anomalies in tadpoles exposed to predators. Physiological and Biochemical Zoology, 87, 829–836. PubMed

Benjamini, Y. , & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, 57, 289–300.

Bernot, R. J. , Dodds, W. K. , Quist, M. C. , & Guy, C. S. (2006). Temperature and kairomone induced life history plasticity in coexisting Daphnia. Aquatic Ecology, 40, 361–372.

Bjærke, O. , Andersen, T. , & Titelman, J. (2014). Predator chemical cues increase growth and alter development in nauplii of a marine copepod. Marine Ecology Progress Series, 510, 15–24.

Blažek, R. , Polačik, M. , & Reichard, M. (2013). Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo, 4, 1. PubMed PMC

Blažek, R. , Polačik, M. , Kačer, P. , Cellerino, A. , Řežucha, R. , Methling, C. , … Reichard, M. (2017). Repeated intra‐specific divergence in lifespan and ageing of African annual fishes along an aridity gradient. Evolution, 71, 386–402. PubMed

Bourdeau, P. E. , Bach, M. T. , & Peacor, S. D. (2016). Predator presence dramatically reduces copepod abundance through condition‐mediated non‐consumptive effects. Freshwater Biology, 61, 1020–1031.

Bourdeau, P. E. , & Johansson, F. (2012). Predator‐induced morphological defences as by‐products of prey behaviour: A review and prospectus. Oikos, 121, 1175–1190.

Brönmark, C. , Lakowitz, T. , Nilsson, P. A. , Ahlgren, J. , Lennartsdotter, C. , & Hollander, J. (2012). Costs of inducible defence along a resource gradient. PLoS One, 7, e30467. PubMed PMC

Bruton, M. (1979). The food and feeding behaviour of Clarias gariepinus (Pisces: Clariidae) in Lake Sibaya, South Africa, with emphasis on its role as a predator of cichlids. The Transactions of the Zoological Society of London, 35(1), 47–114.

Camargo, J. A. , Alonso, A. , & Salamanca, A. (2005). Nitrate toxicity to aquatic animals: A review with new data for freshwater invertebrates. Chemosphere, 58, 1255–1267. PubMed

Chandler, H. C. , Gorman, T. A. , & Haas, C. A. (2016). The Effects of crayfish predation and vegetation cover on tadpole growth, survival, and nonlethal injury. Journal of Herpetology, 50, 271–277.

Costa, Z. J. , & Kishida, O. (2015). Nonadditive impacts of temperature and basal resource availability on predator–prey interactions and phenotypes. Oecologia, 178, 1215–1225. PubMed

Dalesman, S. , Thomas, A. , & Rundle, S. D. (2015). Local adaptation and embryonic plasticity affect anti‐predator traits in hatchling pond snails. Freshwater Biology, 60, 663–672.

Dawidowicz, P. , & Wielanier, M. (2004). Costs of predator avoidance reduce competitive ability of Daphnia. Hydrobiologia, 526, 165–169.

Dayton, G. H. , & Fitzgerald, L. A. (2011). The advantage of no defense: Predation enhances cohort survival in a desert amphibian. Aquatic Ecology, 45, 325–333.

De Meester, L. (1996). Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, Daphnia magna . Evolution, 50, 1293–1298. PubMed

Frommen, J. G. , Herder, F. , Engqvist, L. , Mehlis, M. , Bakker, T. C. M. , Schwarzer, J. , & Thünken, T. (2011). Costly plastic morphological responses to predator specific odour cues in three‐spined sticklebacks (Gasterosteus aculeatus). Evolutionary Ecology, 25, 641–656.

Furness, A. I. , Lee, K. , & Reznick, D. N. (2015). Adaptation in a variable environment: Phenotypic plasticity and bet‐hedging during egg diapause and hatching in an annual killifish. Evolution, 69, 1461–1475. PubMed

Genade, T. (2005) Laboratory manual for culturing N. furzeri. Retrieved from https://www nothobranchius. info/pdfs/lab_protocols_1. pdf

Genade, T. , Benedetti, M. , Terzibasi, E. , Roncaglia, P. , Valenzano, D. R. , Cattaneo, A. , & Cellerino, A. (2005). Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell, 4, 223–233. PubMed

Gliwicz, Z. M. , & Maszczyk, P. (2007). Daphnia growth is hindered by chemical information on predation risk at high but not at low food levels. Oecologia, 150, 706–715. PubMed

Hall, A. E. , & Clark, T. D. (2016). Seeing is believing: Metabolism provides insight into threat perception for a prey species of coral reef fish. Animal Behaviour, 115, 117–126.

Hamisi, J. (2013) Study of rainfall trends and variability over tanzania. Doctoral dissertation. Retrieved from https://erepository.uonbi.ac.ke/bitstream/handle/11295/55844/Hamisi_Study%20Of%20Rainfall%20Trends%20And%20Variability%20Over%20Tanzania.pdf?sequence=3

Inglima, K. , Perlmutter, A. , & Markofsky, J. (1981). Reversible stage‐specific embryonic inhibition mediated by the presence of adults in the annual fish Nothobranchius guentheri. Journal of Experimental Zoology, 215, 23–33. PubMed

Jourdan, J. , Baier, J. , Riesch, R. , Klimpel, S. , Streit, B. , Müller, R. , & Plath, M. (2016). Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk. Aquatic Sciences, 78, 303–314.

Lass, S. , & Spaak, P. (2003). Chemically induced anti‐predator defences in plankton: A review. Hydrobiologia, 491, 221–239.

Lass, S. , Vos, M. , Wolinska, J. , & Spaak, P. (2005). Hatching with the enemy: Daphnia diapausing eggs hatch in the presence of fish kairomones. Chemoecology, 15, 7–12.

Lima, S. L. , & Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68, 619–640.

Magurran, A. E. (2005). Evolutionary ecology: The Trinidadian guppy. Oxford: UK, Oxford University Press.

Mazuze, F. M. (2007) Analysis of adoption of orange‐fleshed sweet potatoes: the case study of Gaza province in Mozambique. Retrieved from https://fsg.afre.msu.edu/mozambique/MAZUZE_MS.pdf

Miyakawa, H. , Sugimoto, N. , Kohyama, T. I. , Iguchi, T. , & Miura, T. (2015). Intra‐specific variations in reaction norms of predator‐induced polyphenism in the water flea Daphnia pulex . Ecological Research, 30, 705–713.

Mogali, S. , Saidapur, S. , & Shanbhag, B. (2016). Influence of desiccation, predatory cues, and density on metamorphic traits of the bronze frog Hylarana temporalis . Amphibia‐Reptilia, 37, 199–205.

Pietrzak, B. , Dawidowicz, P. , Prędki, P. , & Dańko, M. J. (2015). How perceived predation risk shapes patterns of aging in water fleas. Experimental Gerontology, 69, 1–8. PubMed

Pijanowska, J. , Dawidowicz, P. , Howe, A. , & Weider, L. J. (2006). Predator‐induced shifts in Daphnia life‐histories under different food regimes. Archiv fur Hydrobiologie, 167, 37–54.

Pinceel, T. , Vanschoenwinkel, B. , Deckers, P. , Grégoir, A. , Ver Eecke, T. , & Brendonck, L. (2015). Early and late developmental arrest as complementary embryonic bet‐hedging strategies in African killifish. Biological Journal of the Linnean Society, 114, 941–948.

Polačik, M. , Blažek, R. , & Reichard, M. (2016). Laboratory breeding of the short‐lived annual killifish Nothobranchius furzeri . Nature Protocols, 11, 1396–1413. PubMed

Polačik, M. , Blažek, R. , Řežucha, R. , Vrtílek, M. , Terzibasi Tozzini, E. , & Reichard, M. (2014). Alternative intrapopulation life‐history strategies and their trade‐offs in an African annual fish. Journal of Evolutionary Biology, 27, 854–865. PubMed

Polačik, M. , & Podrabsky, J. E. (2015). Temporary environments In Riesch R., Plath M., & Tobler M. (Eds.), Extremophile fishes ‐ ecology and evolution of teleosts in extreme environments (pp. 217–245). New Yoerk, NY: Springer International Publishing.

Prokešová, M. , Drozd, B. , Kouřil, J. , Stejskal, V. , & Matoušek, J. (2015). Effect of water temperature on early life history of African sharp‐tooth catfish, Clarias gariepinus (Burchell, 1822). Journal of Applied Ichthyology, 31, 18–29.

R Core Team . (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; Retrieved from https://www.R-project.org

Reaney, L. T. (2007). Foraging and mating opportunities influence refuge use in the fiddler crab, Uca mjoebergi . Animal Behaviour, 73, 711–716.

Reichard, M. (2010). Nothobranchius kadleci (Cyprinodontiformes: Nothobranchiidae), a new species of annual killifish from central Mozambique. Zootaxa, 2332, 49–60. PubMed

Reichard, M. (2015) The evolutionary ecology of African annual fishes In: Berois N., García G. & de Sá R. (Eds.), Annual Fishes: Life history strategy, diversity, and evolution. CRC Press: Boca Raton, FL, USA.

Reichard, M. , Polačik, M. , Blažek, R. , & Vrtílek, M. (2014). Female bias in the adult sex ratio of African annual fishes: Interspecific differences, seasonal trends and environmental predictors. Evolutionary Ecology, 28, 1105–1120.

Reichard, M. , Polačik, M. , & Sedláček, O. (2009). Distribution, colour polymorphism and habitat use of the African killifish, Nothobranchius furzeri, the vertebrate with the shortest lifespan. Journal of Fish Biology, 74, 198–212. PubMed

Rengefors, K. , Karlsson, I. , & Hansson, L. A. (1998). Algal cyst dormancy: A temporal escape from herbivory. Proceedings of the Royal Society of London B: Biological Sciences, 265, 1353–1358.

Rieder, J. P. , Newbold, T. S. , Sato, S. , Yasuda, H. , & Evans, E. W. (2008). Intra‐guild predation and variation in egg defence between sympatric and allopatric populations of two species of ladybird beetles. Ecological Entomology, 33, 53–58.

Rodd, F. H. , & Reznick, D. N. (1997). Variation in the demography of guppy populations: The importance of predation and life histories. Ecology, 78, 405–418.

Ruther, J. , Meiners, T. , & Steidle, J. L. (2002). Rich in phenomena‐lacking in terms. A classification of kairomones. Chemoecology, 12, 161–167.

Scherer, A. E. , Lunt, J. , Draper, A. M. , & Smee, D. L. (2016). Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey. Invertebrate Biology, 135, 97–107.

Smith, G. R. , Burgett, A. A. , Temple, K. G. , & Sparks, K. A. (2016). Differential effects of Bluegill Sunfish (Lepomis macrochirus) on two fish‐tolerant species of tadpoles (Anaxyrus americanus and Lithobates catesbeianus). Hydrobiologia, 773, 77–86.

Smith, L. A. , & Webster, M. M. (2015). Gammarus pulex show a grouping response to conspecific injury cues but not to predator kairomones. Behavioral Ecology, 26, 1188–1195.

Spencer, M. , & Blaustein, L. (2001). Hatching responses of temporary pool invertebrates to signals of environmental quality. Israel Journal of Zoology, 47, 397–418.

Terzibasi Tozzini, E. , Dorn, A. , Ng'oma, E. , Polačik, M. , Blažek, R. , Reichwald, K. , … Cellerino, A. (2013). Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evolutionary Biology, 13, 77. PubMed PMC

Touchon, J. C. , Gomez‐Mestre, I. , & Warkentin, K. M. (2006). Hatching plasticity in two temperate anurans: Responses to a pathogen and predation cues. Canadian Journal of Zoology, 84, 556–563.

Van Buskirk, J. (2000). The costs of an inducible defense in anuran larvae. Ecology, 81, 2813–2821.

Van Dam, A. R. , & Walton, W. E. (2008). The effect of predatory fish exudates on the ovipostional behaviour of three mosquito species: Culex quinquefasciatus, Aedes aegypti and Culex tarsalis . Medical and Veterinary Entomology, 22, 399–404. PubMed

Vanoverbeke, J. , & De Meester, L. (2009). Within season short‐term hatching delays suggest risk‐spreading behaviour in populations of the freshwater cladoceran Daphnia. Ecoscience, 16, 441–451.

Vrtílek, M. , & Reichard, M. (2016). Female fecundity traits in wild populations of African annual fish: The role of the aridity gradient. Ecology and Evolution, 6, 5921–5931. PubMed PMC

Walsh, M. R. , & Post, D. M. (2012). The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia ambigua . Journal of Evolutionary Biology, 25, 80–89. PubMed

Walton, W. E. , Van Dam, A. R. , & Popko, D. A. (2009). Ovipositional responses of two Culex (Diptera: Culicidae) species to larvivorous fish. Journal of Medical Entomology, 46, 1338–1343. PubMed

Waterkeyn, A. , Van Pottelbergh, N. , Vanoverbeke, J. , Vanschoenwinkel, B. , De Meester, L. , & Brendonck, L. (2013). Constitutive but no Triops‐induced differences in bet‐hedging strategies for hatching in Daphnia. Hydrobiologia, 715, 29–35.

Weber, A. (2003). More than one fish kairomone’? Perch and stickleback kairomones affect Daphnia life history traits differently. Hydrobiologia, 498, 143–150.

Weider, L. J. , & Pijanowska, J. (1993). Plasticity of Daphnia life histories in response to chemical cues from predators. Oikos, 67, 385–392.

Wildekamp, R. H . (2004). A world of killies: Atlas of the oviparous cyprinidontiform fishes of the world. Vol. IV: Elyria, OH, USA.

Wooton, R. J. , & Smith, C. (2015). Reproductive biology of teleost fishes. Chichester, UK: John Wiley & Sons.

Yin, M. , Laforsch, C. , Lohr, J. N. , & Wolinska, J. (2011). Predator‐induced defence makes Daphnia more vulnerable to parasites. Evolution, 65, 1482–1488. PubMed

Zengeya, T. A. , & Marshall, B. E. (2007). Trophic interrelationships amongst cichlid fishes in a tropical African reservoir (Lake Chivero, Zimbabwe). Hydrobiologia, 592, 175–182.

Phenotypic plasticity in specialists: How long-spined larval Sympetrum depressiusculum (Odonata: Libellulidae) responds to combined predator cues