Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Lifetime eurythermy by seasonally matched thermal performance of developmental stages in an annual aquatic insect

  • 39 Accesses

Abstract

Organisms with annual life cycles are exposed to life stage specific thermal environments across seasons. Seasonal variation in thermal environments can vary across years and among sites. We investigated how organisms with annual life cycles respond to predictable seasonal changes in temperature and unpredictable thermal variation between habitats and years throughout their lives. Field surveys and historical records reveal that the spatially and temporally heterogeneous thermal environments inhabited by the annual mayfly Ephemerella maculata (Ephemerellidae) shift the date for transition to the next, life stage, so that the thermal phenotype of each life stage matches the thermal environment of the specific habitat and year. Laboratory studies of three distinct life stages of this mayfly reveal that life stage transitions are temperature dependent, facilitating timing shifts that are synchronized with the current season’s temperatures. Each life stage exhibited specific thermal sensitivity and performance phenotypes that matched the ambient temperature typically experienced during that life stage. Our study across the whole life cycle reveals mechanisms that allow organisms to achieve lifetime eurythermy in a dynamic seasonal environment, despite having narrower thermal ranges for growth and development in each life stage.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Allen RK (1968) New species and records of Ephemerella in western North America (Ephemeroptera: Ephemerellidae). J Kans Entomol Soc 1:557–567

  2. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

  3. Atkinson D (1994) Temperature and organism size: a biological law for ectotherms? Adv Ecol Res 25:1–58

  4. Bohle HW (1972) Die Temperaturabhängigkeit der Embryogenese und der embryonalen Diapause von Ephemerella ignita (Poda) (Insecta, Ephemeroptera). Oecologia 10:253–268

  5. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LE, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803

  6. Dallas HF, Ketley ZA (2011) Upper thermal limits of aquatic macroinvertebrates: comparing critical thermal maxima with 96-LT50 values. J Therm Biol 36:322–327

  7. Dallas HF, Rivers-Moore NA (2012) Critical thermal maxima of aquatic macroinvertebrates: towards identifying bioindicators of thermal alteration. Hydrobiologia 679:61–76

  8. Dallas HF, Ross-Gillespie V (2015) Sublethal effects of temperature on freshwater organisms, with special reference to aquatic insects. Water SA 12:712–726

  9. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122

  10. Elliott JM (1978) Effect of temperature on the hatching time of eggs of Ephemerella ignita (Poda) (Ephemeroptera: Ephemerellidae). Freshw Biol 8:51–58

  11. Gu L, Hanson PJ, Mac Post W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freeze: increased cold damage in a warming world? Bioscience 58:253–262

  12. Helmuth BS, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384

  13. Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159

  14. Kim KS, Chou H, Funk DH, Jackson JK, Sweeney BW, Buchwalter DB (2017) Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits. J Exp Biol 220:2598–2605

  15. Kingsolver JG, Woods HA, Buckley LB, Potter KA, MacLean HJ, Higgins JK (2011) Complex life cycles and the responses of insects to climate change. Integr Comp Biol 30:1–14

  16. Kristensen TN, Hoffmann AA, Overgaard J, Sørensen JG, Hallas R, Loeschcke V (2008) Costs and benefits of cold acclimation in field-released drosophila. Proc Natl Acad Sci 105:216–221

  17. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:6721

  18. Meyer MD, McCafferty WP (2008) Mayflies (Ephemeroptera) of the far western United States. Part 3: California. Trans Am Entomol Soc 134:337–430

  19. Miller NA, Paganini AW, Stillman JH (2013) Differential thermal tolerance and energetic trajectories during ontogeny in porcelain crabs, genus Petrolisthes. J Therm Biol 38:79–85

  20. Nielsen JL, Lisle TE, Ozaki V (1994) Thermally stratified pools and their use by steelhead in northern California streams. Trans Am Fish Soc 123:613–626

  21. Olden JD, Naiman RJ (2010) Incorporating thermal regimes into environmental flows assessments: modifying dam operations to restore freshwater ecosystem integrity. Freshw Biol 55:86–107

  22. Pincebourde S, Casas J (2015) Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits. Ecology 96:986–997

  23. Pritchard G, Harder LD, Mutch RA (1996) Development of aquatic insect eggs in relation to temperature and strategies for dealing with different thermal environments. Biol J Linn Soc 38:221–244

  24. Pruess KP (1983) Day-degree methods for pest management. Environ Entomol 12:613–619

  25. Radchuk V, Turlure C, Schtickzelle N (2013) Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J Anim Ecol 82:275–285

  26. Ragland GJ, Kingsolver JG (2008) Evolution of thermotolerance in seasonal environments: the effects of annual temperature variation and life-history timing in Wyeomyia smithii. Evolution 62:1345–1357

  27. Rivers-Moore NA, Dallas HF, Ross-Gillespie V (2013) Life history does matter in assessing potential ecological impacts of thermal changes on aquatic macroinvertebrates. River Res Appl 29:1100–1109

  28. Ross-Gillespie V (2014) Effects of water temperature on life-history traits of selected South African aquatic insects. Doctoral Dissertation, University of Cape Town

  29. Ross-Gillespie V, Picker MD, Dallas HF, Day JA (2018) The role of temperature in egg development of three aquatic insects Lestagella penicillate (Ephemeroptera), Aphanicercella scutata (Plecoptera), Chimarra ambulans (Trichoptera) from South Africa. J Therm Biol 71:158–170

  30. Sheldon KS, Dillon ME (2016) Beyond the mean: biological impacts of cryptic temperature change. Integr Comp Biol 56:110–119

  31. Somero G, Dahlhoff E, Lin J (1996) Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In: Johnston IA, Bennett AF (eds) Animals and temperature: phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge

  32. Stanford JA, Ward JV, Liss WJ, Frissell CA, Williams RN, Lichatowich JA, Coutant CC (1996) A general protocol for restoration of regulated rivers. US Department of Energy Publications, vol 1, pp 1–43

  33. Sweeney BW, Vannote RL (1978) Size variation and the distribution of hemimetabolous aquatic insects: two thermal equilibrium hypotheses. Science 200:4340

  34. Sweeney BW, Funk DH, Camp AA, Buchwalter DB (2018) Why adult mayflies of Cloeon dipterum (Ephemeroptera: Baetidae) become smaller as temperature warms. Freshw Sci 37:64–81

  35. Tauber MJ, Tauber CA (1976) Insect seasonality: diapause maintenance, termination, and postdiapause development. Annu Rev Entomol 21:81–107

  36. Uno H (2016) Stream thermal heterogeneity prolongs aquatic-terrestrial subsidy and enhances riparian spider growth. Ecology 97:2547–2553

  37. Uno H (2019) Migratory life cycle of Ephemerella maculata (Traver, 1934) (Ephemerellidae). Aquat Insects 40:123–136

  38. Uno H, Power ME (2015) Mainstem-tributary linkages by mayfly migration help sustain salmonids in a warming river network. Ecol Lett 18:1012–1020

  39. Van Buskirk J, Mulvihill RS, Leberman RC (2009) Variable shifts in spring and autumn migration phenology in North American songbirds associated with climate change. Glob Change Biol 15:760–771

  40. Verberk WCEP, Bilton DT, Calosi P, Spicer JI (2011) Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns. Ecology 92:1565–1672

  41. Willett CS (2010) Potential fitness trade-offs for thermal tolerance in the intertidal copepod Tigriopus californicus. Evolution 64:2521–2534

  42. Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90:214–235

  43. Wilson L, Barnett W (1983) Degree-days: an aid in crop and pest management. Calif Agric 37:4–7

Download references

Acknowledgements

We thank W.P. Sousa, M.R. Miller, S.M. O’Rourke, S.M. Carlson, S. Kupferberg, C. Williams, and E. Armstrong for comments on the manuscript; J. Khemani, J. Porzio, L. Walder, and S. Pneh for lab and field assistance; S. Fay for technical assistance; M.E. Power for discussion of study design. We thank P. Steel, the Steel and the Angelo families, and the University of California Nature Reserve system for providing research sites, and temperature and discharge data. We finally appreciate all the reviewers and editors who helped improving this manuscript toward publication. This study was conducted under CDFW permit SC-12223 issued to H. Uno. This work was supported by a Gordon and Betty Moore Foundation grant to the Berkeley Initiative for Global Change Biology, National Science Foundation for Doctoral Dissertation Improvement Grant to H. Uno (DEB-1501605) and Eel River Critical Zone Observatory (CZP EAR-1331940) as well as the graduate fellowships to H. Uno by Heiwa-Nakajima-Foundation and Japan Student Service Organization.

Author information

HU and JHS conceived the study; HU collected all data and performed the analysis. HU and JHS wrote the manuscript. All authors gave final approval for publication.

Correspondence to Hiromi Uno.

Additional information

Communicated by Jill Lancaster.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Uno, H., Stillman, J.H. Lifetime eurythermy by seasonally matched thermal performance of developmental stages in an annual aquatic insect. Oecologia (2020). https://doi.org/10.1007/s00442-020-04605-z

Download citation

Keywords

  • Aquatic insect
  • Temperature
  • Life cycle
  • Season
  • Stream