Transgenerational exposure to marine heatwaves ameliorates the lethal effect on tropical copepods regardless of predation stress

Abstract

Marine heatwaves (MHWs) are emerging as a severe stressor in marine ecosystems. Extreme warm sea surface temperatures during MHWs often exceed the optimal thermal range for more than one generation of tropical coastal zooplankton. However, it is relatively unknown whether transgenerational plasticity (TGP) to MHWs may shape the offspring's fitness, particularly in an ecologically relevant context with biotic interactions such as predation stress. We addressed these novel research questions by determining the survival, reproductive success, and grazing rate of the copepod Pseudodiaptomus incisus exposed to MHW and fish predator cues (FPC) for two generations (F1 and F2). The experiment was designed in a full orthogonal manner with 4 treatments in F1 and 16 treatments in F2 generation. In both generations, MHW reduced P. incisus survival, reproductive parameters, and grazing by 10%–62% in MHW, but these parameters increased by 2%–15% with exposure to FPC, particularly at control temperature. F2 reproductive success and grazing rate as indicated by cumulative fecal pellets were reduced by 20%–30% in F1‐MHW, but increased by ~2% in F1‐FPC. Strikingly, MHW exposure reduced 17%–18% survival, but transgenerational exposure to MHWs fully ameliorated its lethal effect and this transgenerational effect was independent of FPC. Increased survival came with a cost of reduced reproductive success, constrained by reduced grazing. The rapid transgenerational MHW acclimation and its associated costs are likely widespread and crucial mechanisms underlying the resilience of coastal tropical zooplankton to MHWs in tropical coastal marine ecosystems.

Hot and hungry: A mechanistic approach to the direct and indirect effects of marine heatwaves on plankton communities

“…These environmental drivers can also mitigate or aggravate the signal of temperature effect through time. Additionally, even if our model design has complex ecosystem dynamics and higher functional diversity than most ecosystem models (Petrick et al, 2022), it does not consider phenotypic plasticity, evolution, or behavioral decisions like vertical migration and changes in foraging and predation avoidance that can maximize tness on an individual level and resilience on a community level (Matthew et al 2019;Truong et al 2020Truong et al , 2022Roncalli et al 2022;Sasaki et al 2023). These physiological and behavioral responses might allow species persistence that could dampen the impact of the heatwave and accelerate recovery periods.…”

Shifts in survival and reproduction after chronic warming enhance the potential of a marine copepod to persist under extreme heat events

“…growth and reproduction) can set narrower limits for the persistence of the species. It has long been recognized that energy investments in survival can be at the cost of reproductive efforts and vice versa ( Stearns, 1989 ; Truong et al ., 2022 ). In our study, P. grani reared under warm conditions could expand both survival and reproduction at extreme temperatures, providing further evidence of a strong coupling between both traits in this species under thermal stress ( Saiz et al ., 2015 ).…”

Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus

“…Transgenerational plasticity, which refers to modification of offspring phenotype induced by signals experienced by the parents, is well documented in marine taxa (Donelson et al, 2016;Zhao et al, 2020;Truong et al, 2022). In general, TGP has been studied extensively in marine invertebrates with mixed results depending on taxa and the context of the environmental factor in question (Byrne et al, 2020).…”