Unmasking intraspecific variation in offspring responses to multiple environmental drivers
Understanding organismal responses to environmental drivers is relevant to predict species capacities to respond to climate change. However, the scarce information available on intraspecific variation in the responses oversimplifies our view of the actual species capacities. We studied intraspecific variation in survival and larval development of a marine coastal invertebrate (shore crab Carcinus maenas) in response to two key environmental drivers (temperature and salinity) characterising coastal habitats. On average, survival of early larval stages (up to zoea IV) exhibited an antagonistic response by which negative effects of low salinity were mitigated at increased temperatures. Such response would be adaptive for species inhabiting coastal regions of freshwater influence under summer conditions and moderate warming. Average responses of developmental time were also antagonistic and may be categorised as a form of thermal mitigation of osmotic stress. The capacity for thermal mitigation of low-salinity stress varied among larvae produced by different females. For survival in particular, deviations did not only consist of variations in the magnitude of the mitigation effect; instead, the range of responses varied from strong effects to no effects of salinity across the thermal range tested. Quantifying intraspecific variation of such capacity is a critical step in understanding responses to climate change: it points towards either an important potential for selection or a critical role of environmental change, operating in the parental environment and leading to stress responses in larvae.
We are grateful to Julia Brinkmann, Stefan Eiler, Wladimir Escalante Alvarado, Michael Exton and Simon Wolf for their assistance in animal husbandry. We thank the students of the “Schülerlabor” (Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Helgoland, Germany) for their help in collecting the berried females at the Helgoland intertidal. We acknowledge A. Sombke for conceptual discussion and assistance during the initial phase of this project.
LG, SH and GT conceived the experiments. FS, RM and GT performed the experiments. FS and LG analysed the data. FS wrote the first draft as part of her doctoral dissertation. LG and GT wrote the final manuscript. All the authors improved the final manuscript. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
This work was funded by the Deutsche Forschungsgemeinschaft (DFG, Research Training Group 2010: RESPONSE programme, work-package B3) and involved a collaboration between the working groups of S. Harzsch (Greifswald University, Germany), G. Torres (AWI-Helgoland, Germany) and L. Giménez (Bangor University, UK and AWI-Helgoland, Germany). The funding body did not influence the design of the study and collection, analysis, and interpretation of data nor the writing of the manuscript.
Compliance with ethical standards
Conflicts of interest
The authors declare that they have no conflicts of interests.
The research presented in this paper complies with the guidelines from the directives 2010/63/EU of the European parliament and of the Council of 22nd September 2010 on the protection of animals used for scientific purposes.
- Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso J-P, Havenhand J, Hutchins DA, Riebesell U, Rintoul MS, Vichi M, Biswas H, Ciotti A, Gao K, Gehlen M, Hurd CL, Kurihara H, McGraw CM, Navarro JM, Nilsson GE, Passow U, Pörtner H-O (2018) Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob Change Biol 24:2239–2261CrossRefGoogle Scholar
- Flügel H (1963) Elektrolytregulation und Temperatur bei Crangon crangon L. und Carcinus maenas L. Kiel Meeresforsch 19:189–195Google Scholar
- Fregly MJ (2011) Adaptations: some general characteristics. Comp Physiol 14:3–15Google Scholar
- Gattuso JP, Hansson L (2009) Ocean Acidification. Oxford University Press, OxfordGoogle Scholar
- IPCC (2014) Climate change 2014: synthesis report. In: Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change [Core writing team, Pachauri RK, Meyer LA (eds)] IPCC, Geneva, Switzerland, p 151Google Scholar
- Kinne O (1971) Salinity. Marine ecology. A comprehensive, integrated treatise on life in oceans and coastal waters. Wiley, LondonGoogle Scholar
- Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. Oceanogr Mar Biol Annu Rev 46:203–262Google Scholar
- Nagaraj M (1993) Combined effects of temperature and salinity on the zoeal development of the green crab, Carcinus maenas (Linnaeus, 1758) (Decapoda, Portunidae). Sci Mar 57(1):1–8Google Scholar
- Pechenik JA (1987) Environmental influences on larval survival and growth. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 9. Blackwell Scientific, New York, pp 551–608Google Scholar
- Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018). nlme: linear and nonlinear mixed effects models. R package version 3.1–137. https://CRAN.R-project.org/package=nlme. Accessed 11 Dec 2018
- RStudio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com/
- Torres G, Spitzner F, Harzsch S, Giménez L (2019) Ecological developmental biology and global ocean change: brachyuran crustacean larvae as models. In: Fusco G (ed) Perspectives in evolutionary and developmental biology. Padova University Press, PadovaGoogle Scholar