Introduction
Marine heatwaves (MHWs) are discrete events of abnormally high temperature periods (≥ 5 days) above the 90th percentile of 30-years sea surface temperatures measured at the locality (Hobday et al., 2016; Oliver et al., 2018). In the last decade, MHWs have emerged as one of the greatest drivers reshaping the marine biodiversity, including the tropicalisation of the temperate coastal ecosystems, mass coral bleaching worldwide, mass mortality of coastal invertebrates (Garrabou et al., 2009; 2019; Hughes et al., 2017; Smale et al., 2019). The effects of MHWs on marine ecosystems and biota are becoming more severe under ongoing climate change (Smale et al., 2019). In the Southeast Asian region, coastal marine organisms are also increasingly being exposed to episodes of MHWs (Feng et al., 2022; Yao, Wang, Yin, & Zou, 2020). In 1982 – 2018, the duration of MHWs in the Southeast Asian Seas had increased from 5 to 9 days per decade (Yao et al., 2020), and the number of days that the sea surface temperature exceeded 34°C is about 40-60 days per year (Dinh K.V., Doan X.N and Pham Q.H., unpublished data), which are often beyond one generation of tropical coastal invertebrates. A few studies have investigated the effects of MHWs on marine organisms such as copepods and fish in the Southeast Asian region (e.g., Doan et al., 2019; Le, Dinh, Nguyen, & Rønnestad, 2020; Nguyen et al., 2020), yet, most of these studies have limited the MHW effects on one generation. It remains to explore how transgenerational acclimation to MHWs may ameliorate the effects of warming on offspring generation (see, e.g., in coral fish, Donelson, Munday, McCormick, & Pitcher, 2012).
Recent advancements in eco-evolutionary studies on adaptations of organisms to warming, ocean acidification, and contaminants have revealed the critical role of transgenerational plasticity that the environment experienced by parental generation may improve the offspring performance in the same environment (Donelson et al., 2012; Donelson, Salinas, Munday, & Shama, 2018; Fox, Donelson, Schunter, Ravasi, & Gaitán-Espitia, 2019; Guillaume, Monro, & Marshall, 2016; Krause, Dinh, & Nielsen, 2017; Munday, 2014; Thor & Dupont, 2015). For example, transgenerational exposure to ocean acidification may alleviate the fecundity loss in marine copepod Pseudocalanus acuspes (Thor & Dupont, 2015). Parental exposure to pyrene also resulted in higher performance of copepod Acartia tonsa at 100 nM pyrene (Krause et al., 2017). The transgenerational effect may occur through maternal provisioning, phenotypic plasticity, epigenetic changes, and genetic selections (Dinh, Dinh, Pham, Selck, & Truong, 2020; Donelson et al., 2012; Ryu, Veilleux, Donelson, Munday, & Ravasi, 2018).
In the shallow tropical coastal ecosystems such as seagrasses, mangroves, and coral reefs, the predation stress is typically high as these ecosystems are the spawning and nursery ground of marine species. To survive, prey species such as zooplankton will have to adjust their physiology to cope with thermal stress during MHW and the stress caused by natural predators such as voracious fish larvae and juveniles. Predators can significantly influence their prey’s morphology, behaviour, physiology, growth, and reproduction (e.g., Bjærke, Andersen, & Titelman, 2014; Lasley-Rasher & Yen, 2012; Truong et al., 2020). Investigations of the transgenerational effect of MHWs in an ecologically relevant context, such as the presence of fish predator cues (FPC) on key zooplankton species such as copepods are relevant and timely because these species have to cope with both stressors from one to another generation. The vulnerability or resilience of copepods to MHWs in an ecologically relevant context such as predation stress is a key pathway for the transfer of energy and resources from photosynthesis organisms to higher trophic levels, hence the productivity of the coastal ecosystems (Chew, Chong, Tanaka, & Sasekumar, 2012). However, the combined effects of heatwaves and non-consumptive predation risk on the prey are still a major knowledge gap in current ecology, especially across generations.
Our previous study shows that fish predator cues induced a higher individual performance of the calanoid copepod Pseudodiaptomus incisus under control temperature, but it magnified the impacts of MHW on grazing and reproductive success (Truong et al., 2020). In this study, we fundamentally increase the realism in the experiment by investigating the role of transgenerational exposure to MHW and/or fish predator cues in shaping the fitness of the offspring generation. We tested the susceptibility of P. incisus to MHW and FPC by following four hypotheses:
(1) FPC strengthens the MHW effect on P. incisus (see Truong et al., 2020). (2) Parental MHW exposure increases the MHW tolerance of P. incisus offspring (see Donelson et al., 2012). (3) Parental FPC exposure increases the FPC performance of P. incisus offspring (see Sentis et al., 2018). (4) Transgenerational FPC effect strengthens the transgenerational MHW effect.