Abstract
Organisms evolve to maintain fitness across generations, while short-term fitness in stochastic habitats such as temporary wetlands may be highly varied. As typical temporary wetland inhabitants, large branchiopods rely on bet hedging hatching that helps them survive throughout generations. An optimal hatching rate is predicted to be approximate to the successful reproduction probability (SRP). We tested the difference between hatching rate and SRP of large branchiopods Branchinella kugenumaensis and Eulimnadia braueriana in a temporary wetland in Taiwan, through field surveys and climatic records to evaluate their SRP. Comparisons were performed under two proposed scenarios, where a population’s hatching was bet hedged for a hydroperiod or for a wet season (with several hydroperiods), respectively. Population size fluctuations were simulated for these two scenarios under assumed egg mortalities and reproductive replenishments. Results showed that the hatching rates only fitted to SRP for E. braueriana under the scenario of bet hedging on a wet season, not for B. kugenumaensis, nor for both species under the scenario of bet hedging on a hydroperiod. Bet hedging on a wet season would have a smaller range of population size fluctuation and a lower rate of population size decrease. This implies that large branchiopods adopt a conservative hatching strategy, lowering the hatching fraction in each hydroperiod to reduce long-term egg bank size fluctuation. Bet hedging strategies could occur during other life cycle stages, coexist with other life history strategies, and lead to the diversified hatching fraction distribution rather than a single, optimal fraction throughout hydroperiods.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Beladjal L, Mertens J (2017) Risk reduction strategies in Branchipus schaefferi (Crustacea: Anostraca: Branchiopoda) as adaptation to a variable environment. Hydrobiologia 801:153–163. https://doi.org/10.1007/s10750-017-3156-9
Brendonck L, De Meester L (2003) Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84. https://doi.org/10.1023/A:1024454905119
Brendonck L, Riddoch BJ (2001) Hatching characteristics of the fairy shrimp Branchipodopsis wolfi in relation to the stochastic nature of its habitat, desert rock pools. Verh Intern Verein Limnol 27:3931–3935. https://doi.org/10.1080/03680770.1998.11901725
Brendonck L, Hamer ML, Riddoch BJ, Seaman MT (2000) Branchipodopsis species—specialists of ephemeral rock pools. Afr J Aquat Sci 25:98–104. https://doi.org/10.2989/160859100780177668
Brendonck L, Rogers DC, Olesen J, Weeks S, Hoeh R (2008) Global diversity of large branchiopods (Crustacea: Branchiopoda) in fresh water. Hydrobiologia 595:167–176. https://doi.org/10.1007/s10750-007-9119-9
Brown JS, Venable DL (1986) Evolutionary ecology of seed-bank annuals in temporally varying environments. Am Nat 127:31–47. https://doi.org/10.1086/284465
Bulmer MG (1984) Delayed germination of seeds: cohen’s model revisited. Theor Popul Biol 26:367–377. https://doi.org/10.1016/0040-5809(84)90040-6
Childs DZ, Metcalf CJE, Rees M (2010) Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proc R Soc Lond B Biol Sci 277:3055–3064. https://doi.org/10.1098/rspb.2010.0707
Clauss MJ, Venable DL (2000) Seed germination in desert annuals: an empirical test of adaptive bet hedging. Am Nat 155:168–186. https://doi.org/10.1086/303314
Cohen D (1966) Optimizing reproduction in a randomly varying environment. J Theor Biol 12:119–129. https://doi.org/10.1016/0022-5193(66)90188-3
Cohen D (1967) Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. J Theor Biol 16:1–14. https://doi.org/10.1016/0022-5193(67)90050-1
Cohen D (1968) A general model of optimal reproduction in a randomly varying environment. J Ecol 56:219–228. https://doi.org/10.2307/2258075
Cooper WS, Kaplan RH (1982) Adaptive “coin-flipping”: a decision-theoretic examination of natural selection for random individual variation. J Theor Biol 94:135–151. https://doi.org/10.1016/0022-5193(82)90336-8
Dumont HJ, Nandini S, Sarma SSS (2002) Cyst ornamentation in aquatic invertebrates: a defence against egg-predation. Hydrobiologia 486:161–167. https://doi.org/10.1023/A:1021346601235
Einum S, Fleming IA (2004) Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evol Ecol Res 6:443–455
Ellner S (1985) ESS germination strategies in randomly varying environments. II. Reciprocal yield-law models. Theor Popul Biol 28:80–116. https://doi.org/10.1016/0040-5809(85)90023-1
Evans MEK, Ferrière R, Kane MJ, Venable DL (2007) Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations. Am Nat 169:184–194. https://doi.org/10.1086/510599
Gremer JR, Venable DL (2014) Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecol Lett 17:380–387. https://doi.org/10.1111/ele.12241
Hairston NG Jr (1996) Zooplankton egg banks as biotic reservoirs in changing environments. Limnol Oceanogr 41:1087–1092. https://doi.org/10.4319/lo.1996.41.5.1087
Hann BJ, Lonsberry B (1991) Influence of temperature on hatching of eggs of Lepidurus couesii (Crustacea, Notostraca). Hydrobiologia 212:61–66. https://doi.org/10.1007/BF00025987
Hildrew AG (1985) A quantitative study of the life history of a fairy shrimp (Branchiopoda: Anostraca) in relation to the temporary nature of its habitat, a Kenyan rainpool. J Anim Ecol 54:99–110. https://doi.org/10.2307/4623
Huang S-L, Wang C-C, Huang W-P, Chou L-S (2010) Indeterminate growth of the fairy shrimp, Branchinella (Branchinellites) kugenumaensis (Branchiopoda: Anostraca) in an unpredictable ephemeral pool. J Crustac Biol 30:366–372. https://doi.org/10.1651/09-3235.1
Huang S-L, Wang C-C, Huang W-P, Chou L-S (2011) Reproductive potential of the fairy shrimp, Branchinella (Branchinellites) kugenumaensis, in an unpredictable ephemeral pool. J Crustac Biol 31:254–259. https://doi.org/10.1651/10-3318.1
Ishikawa C (1895) Phyllopod Crustacea of Japan. Zool Mag 7:1–154
Lin Y-S, Chou L-S (1991) Investigation of the ecology of fairy shrimp, Branchinella kugenumaensis. Yangmingshan National Park, The Construction and Planning Agency, Taiwan (in Chinese)
Maffei C, Vagaggini D, Zarattini P, Mura G (2005) The dormancy problem for Crustacea Anostraca: a rigorous model connecting hatching strategies and environmental conditions. Ecol Model 185:469–481. https://doi.org/10.1016/j.ecolmodel.2004.04.039
Menu F, Roebuck J-P, Viala M (2000) Bet-hedging diapause strategies in stochastic environments. Am Nat 155:724–734. https://doi.org/10.1086/303355
Molles MC Jr (2005) Life histories. In: Loewenberg KR (ed) Ecology: concepts and applications, 3rd edn. McGraw-Hill, New York, pp 298–321
O’Neill BJ (2016) Community disassembly in ephemeral ecosystems. Ecology 97:3285–3292. https://doi.org/10.1002/ecy.1604
Pake CE, Venable DL (1996) Seed banks in desert annuals: implications for persistence and coexistence in variable environments. Ecology 77:1427–1435. https://doi.org/10.2307/2265540
Philippi T (1993) Bet-hedging germination of desert annuals: beyond the first year. Am Nat 142:474–487. https://doi.org/10.1086/285550
Philippi T, Seger J (1989) Hedging one’s evolutionary bets, revisited. Trends Ecol Evol 4:41–44. https://doi.org/10.1016/0169-5347(89)90138-9
Philippi TE, Simovich MA, Bauder ET, Moorad JA (2001) Habitat ephemerality and hatching fractions of a diapausing anostracan (Crustacea: Branchiopoda). Israel J Zool 47:387–396
Pinceel T, Vanschoenwinkel B, Hawinkel W, Tuytens K, Brendonck L (2017) Aridity promotes bet hedging via delayed hatching: a case study with two temporary pond crustaceans along a latitudinal gradient. Oecologia 184:161–170. https://doi.org/10.1007/s00442-017-3858-8
Ricklefs RE, Miller GL (2000) Ecolution of life histories. In: Tenney S, Allen D, Maass D (eds) Ecology, 4th edn. W. H. Freeman and Company, New York, pp 658–675
Ripa J, Olofsson H, Jonzén N (2010) What is bet-hedging, really? Proc R Soc Lond B Biol Sci 277:1153–1154. https://doi.org/10.1098/rspb.2009.2023
Rogers DC (2014) Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). J Crustac Biol 34:135–143. https://doi.org/10.1163/1937240X-00002220
Rogers DC (2015a) A conceptual model for anostracan biogeography. J Crustac Biol 35:686–699. https://doi.org/10.1163/1937240X-00002369
Rogers DC (2015b) Hatching response to temperature along a latitudinal gradient by the fairy shrimp Branchinecta lindahli (Crustacea: Branchiopoda: Anostraca) in culture conditions. J Limnol 74:85–94. https://doi.org/10.4081/jlimnol.2014.1036
Sabnis NJ, Kulkarni MR, Padhye SM, Pai K (2017) Hatching phenology, life history and population dynamics of the oriental clam shrimp Eulimnadia indocylindrova Durga Prasad and Simhachalam with notes on phenology patterns in the Spinicaudata. J Nat Hist 51:1835–1849. https://doi.org/10.1080/00222933.2017.1355996
Saengphan N, Shiel RJ, Sanoamuang L-O (2005) The cyst hatching pattern of the thai fairy shrimp, Branchinella thailandensis Sanoamuang, Saengphan & Murugan, 2002 (Anostraca). Crustaceana 78:513–523. https://doi.org/10.1163/156854005774318123
Saiah H, Perrin N (1990) Autumnal vs spring hatching in the fairy shrimp Siphonophanes grubii (Dybowski) (Crustacea, Anostraca): diversified bet-hedging strategy? Funct Ecol 4:769–775. https://doi.org/10.2307/2389443
Schwartz SS, Jenkins DG (2000) Temporary aquatic habitats: constraints and opportunities. Aquat Ecol 34:3–8. https://doi.org/10.1023/A:1009944918152
Seger J, Brockmann HJ (1987) What is bet-hedging? Oxford Surv Evol Biol 4:182–211
Simons AM (2014) Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments. J Evol Biol 27:1047–1056. https://doi.org/10.1111/jeb.12378
Simovich MA, Hathaway SA (1997) Diversified bet-hedging as a reproductive strategy of some ephemeral pool anostracans (Branchiopoda). J Crustac Biol 17:38–44. https://doi.org/10.1163/193724097X00070
Slusarczyk M, Starzyński J, Bernatowicz P (2017) How long to rest in unpredictably changing habitats? PLoS One 12:e0175927. https://doi.org/10.1371/journal.pone.0175927
Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51:3–47. https://doi.org/10.1086/409052
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486. https://doi.org/10.1007/s001140050763
Su T, Mulla MS (2002) Factors affecting egg hatch of the tadpole shrimp Triops newberryi, a potential biological control agent of immature mosquitoes. Biol Control 23:18–26. https://doi.org/10.1006/bcon.2001.0982
Tuljapurkar S, Istock C (1993) Environmental uncertainty and variable diapause. Theor Popul Biol 43:251–280. https://doi.org/10.1006/tpbi.1993.1011
Vanschoenwinkel B, Seaman M, Brendonck L (2010) Hatching phenology, life history and egg bank size of fairy shrimp Branchipodopsis spp. (Branchiopoda, Crustacea) in relation to the ephemerality of their rock pool habitat. Aquat Ecol 44:771–780. https://doi.org/10.1007/s10452-010-9315-y
Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090. https://doi.org/10.1890/06-1495
Wang C-C, Chou L-S (2015) Terminating dormancy: hatching phenology of sympatric large branchiopods in Siangtian Pond, a temporary pool in Taiwan. J Crustac Biol 35:301–308. https://doi.org/10.1163/1937240X-00002322
Wang C-C, Huang S-L, Huang W-P, Chou L-S (2012) Spatial niche differentiation of sympatric Branchiopoda in a highly unpredictable ephemeral pool. J Crustac Biol 32:39–47. https://doi.org/10.1163/193724011X615316
Wang C-C, Liu J-Y, Chou L-S (2014) Egg bank spatial structure and functional size of three sympatric branchiopods (Branchiopoda) in Siangtian Pond, Taiwan. J Crustac Biol 34:412–421. https://doi.org/10.1163/1937240X-00002244
Wang C-C, Rogers DC, Liu J-Y (2018) Microhabitat preferences in three species of sympatric large branchiopods (Branchiopoda: Anostraca, Laevicaudata, Spinicaudata) in a continually changing environment in Taiwan. J Crustac Biol 38:140–146. https://doi.org/10.1093/jcbiol/rux108
Waterkeyn A, Vanoverbeke J, Pottelbergh NV, Brendonck L (2011) While they were sleeping: dormant egg predation by Triops. J Plankton Res 33:1617–1621. https://doi.org/10.1093/plankt/fbr048
Weeks SC, Marcus V, Alvarez S (1997) Notes on the life history of the clam shrimp, Eulimnadia texana. Hydrobiologia 359:191–197. https://doi.org/10.1023/A:1003106702451
Wiggins GB, Mackay RJ, Smith IM (1980) Evolutionary and ecological strategies of animals in annual temporary pools. Arch Hydrobiol 58:97–206
Williams WD (1985) Biotic adaptations in temporary lentic waters, with special reference to those in semi-arid and arid regions. Hydrobiologia 125:85–110. https://doi.org/10.1007/978-94-009-5522-6_7
Acknowledgements
We sincerely thank Dr. Jonathan Walter for providing statistical comments and Dr. Shiang-Lin Huang’s suggestions to the early draft. We are deeply grateful to two anonymous reviewers’ and the handling editor Dr. Nicole Phillips’ invaluable comments that have significantly broadened the scope and improved the quality of this study.
Author information
Authors and Affiliations
Contributions
CCW and DCR formulated the idea and wrote the draft. CCW developed the methodology and analyzed the data.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Nicole Phillips.
The datasets analyzed during the current study are available in the Google Drive (http://drive.google.com/open?id=1fi-4Clu46M4o-J7jqYlaJdWZQRJF9a-D). The climatic datasets analyzed during current study (i.e., precipitation and mean air temperature) are not publicly available due to the charge (only precipitation data available freely for the most recent ten years: http://www.cwb.gov.tw/V7/climate/dailyPrecipitation/dP.htm, Central Weather Bureau, Taiwan), but are available from the corresponding author on reasonable request.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, CC., Rogers, D.C. Bet hedging in stochastic habitats: an approach through large branchiopods in a temporary wetland. Oecologia 188, 1081–1093 (2018). https://doi.org/10.1007/s00442-018-4272-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4272-6