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40-60 days per year (Dinh K.V., Doan X.N and Pham Q.H., unpublished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.