Unmasking intraspecific variation in offspring responses to multiple environmental drivers

Abstract

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.

Maternal and cohort effects modulate offspring responses to multiple stressors

“…The most likely underpinning mechanism is an increase in osmoregulatory capacity at higher temperatures: thus, TMLS may be a consequence of this physiological plasticity. The TMLS is found in other coastal species and it is relevant in the light of climate change in that (moderate) warming may favour expansion towards coastal areas characterized by moderately low salinities [36]. However, the same study also found that responses vary among larvae from different females [36], which may be driven by variability in the maternal environment, for instance by the temperature and salinity experienced by females and embryos.…”

“…The TMLS is found in other coastal species and it is relevant in the light of climate change in that (moderate) warming may favour expansion towards coastal areas characterized by moderately low salinities [36]. However, the same study also found that responses vary among larvae from different females [36], which may be driven by variability in the maternal environment, for instance by the temperature and salinity experienced by females and embryos. Theoretically, salinity and temperature may alter embryonic developmental processes and hence modify larval performance in many possible ways.…”

“…Carcinus maenas is an euryhaline crab that is endemic to northern Europe [33][34][35] but considered a global invader. Larvae of C. maenas exhibit an antagonistic response to low salinity and increased temperature ('thermal mitigation of low salinity stress': TMLS; figure 1), whereby negative effects of low salinity on survival and developmental time are mitigated at high temperatures [36]. The most likely underpinning mechanism is an increase in osmoregulatory capacity at higher temperatures: thus, TMLS may be a consequence of this physiological plasticity.…”

Physiological basis of interactive responses to temperature and salinity in coastal marine invertebrate: Implications for responses to warming

“…Relevant examples to climate change are, for instance, synergistic effects of increased temperature combined with food limitation or elevated CO 2 (i.e., the combined effect of both stressors is larger than the sum of each separate effect: Giebelhausen & Lampert, 2001;Przeslawski et al, 2015;Schiffer et al, 2014;. By contrast, increased temperature and reduced salinity can operate antagonistically: That is, warming appears to mitigate the negative effects of low salinity (or other drivers) on the performance and fitness in some coastal marine organisms (Lange & Marshall, 2017;Spitzner et al, 2019;.…”

“…Second, we use our results and information from the literature to propose a testable hypothetical model linking osmoregulation, interactive effects of temperature and salinity on organismal performance, and future changes in species distributions across coastal-estuarine gradients in response to warming. We first focus on the antagonistic effect called thermal mitigation of low salinity stress (TMLS: Spitzner et al, 2019) which is common in coastal-estuarine organisms (Anger, 1991;González-Ortegón & Giménez, 2014;Janas & Spicer, 2008;Kinne, 1971). TMLS is defined as the mitigation of the negative effects of exposure to low salinity on performance or fitness (e.g., survival) by increased temperatures.…”