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

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.

Parental exposures increase the vulnerability of copepod offspring to copper and a simulated marine heatwave.

Extreme temperatures from marine heatwaves (MHWs) and pollution are dominant stressors in tropical marine ecosystems. However, we know little about the role of transgenerational effects of metals and MHWs in shaping the offspring's vulnerability to these stressors. We addressed this fundamental knowledge gap by exposing the planktonic copepod Pseudodiaptomus incisus to copper (Cu: control, 15 and 60 µg L-1) under 2 temperatures (30 and a simulated marine heatwave at 34 °C) in the first generation (F1) and 16 treatments in F2: offspring from each of 4 F1 conditions (control or 15 µg Cu L-1 × 30 or 34 °C) was reared in 4 F2 conditions (control or 15 µg Cu L-1 × 30 or 34 °C). We assessed changes in copepod performance, particularly survival, adult size, grazing, and reproduction. In F1, Cu or marine heatwave (MHW) exposures reduced all fitness traits of F1; the effects were particularly strong when both stressors were present. Transgenerational effects of Cu or MHW also strongly reduced F2 performance. Direct Cu and MHW effects on the offspring were further strengthened by transgenerational effects, resulting in more substantial reductions in F2 performance when both generations were exposed to these stressors. As copepods are major food resources for corals, shrimps, or fish larvae and juveniles, strong transgenerational and direct effects of Cu and MHW can have a cascading effect on entire coastal food webs. These results highlight the importance of considering the interaction of transgenerational and direct effects of multiple stressors, particularly relevant for short-lived organisms in tropical marine ecosystems.

Development of metal adaptation in a tropical marine zooplankton.

Tropical marine ecosystems are highly vulnerable to pollution and climate change. It is relatively unknown how tropical species may develop an increased tolerance to these stressors and the cost of adaptations. We addressed these issues by exposing a keystone tropical marine copepod, Pseudodiaptomus annandalei, to copper (Cu) for 7 generations (F1-F7) during three treatments: control, Cu and pCu (the recovery treatment). In F7, we tested the "contaminant-induced climate change sensitivity" hypothesis (TICS) by exposing copepods to Cu and extreme temperature. We tracked fitness and productivity of all generations. In F1, Cu did not affect survival and grazing but decreased nauplii production. In F2-F4, male survival, grazing, and nauplii production were lower in Cu, but recovered in pCu, indicating transgenerational plasticity. Strikingly, in F5-F6 nauplii production of Cu-exposed females increased, and did not recover in pCu. The earlier result suggests an increased Cu tolerance while the latter result revealed its cost. In F7, extreme temperature resulted in more pronounced reductions in grazing, and nauplii production of Cu or pCu than in control, supporting TICS. The results suggest that widespread pollution in tropical regions may result in high vulnerability of species in these regions to climate change.