The neglected role of environmental fluctuations as modulator of stress and driver of rapid evolution.
Final Report Abstract
The main goal of this project was to elucidate the role of natural environmental variability as amplifier or buffer of ecosystem changes in shallow marine habitats, and as a driver for rapid acclimation and/or adaptation. We characterized naturally occurring, yet often ignored, environmental fluctuations across temporal scales. Patterns of daily thermal variability, stochastic thermal variability over days to weeks, and seasonal cycles were highlighted, potentially representing a strong driver of ecosystem changes in a warming ocean. As particular phenomena, different extremes, namely marine heatwaves, hypoxic upwelling events and occurrences of sweater freshening, were identified, characterized, and we tested their relevance in shaping benthic populations and communities. This project demonstrates that environmental variability may act as both, amplifier or as buffer of ecosystem changes, strongly depending on the environmental context. Diurnal thermal variability may represent a burden to mytilid mussels under today’s thermal maxima. In contrast, in a future warming scenario, this same thermal variability, around an intensified baseline temperature, may represent a relief from stress as metabolic adjustments allow mussels to benefit from phases of stress recovery. Yet, we show that different outcomes may be seen if frequency in thermal cycles is matter of manipulation. Importantly, short-term temperature ramp assays may be used to predict the outcome from longer-term exposure of organisms to an environmental variability regime. This was shown in mytilid mussels and the concept may be applied to other organisms, particularly so to taxa capable of metabolic suppression. Environmental extremes are difficult, or impossible, to predict for an organism, and thus may have strong and long-lasting impacts on the ecosystem when thermal (or other) limits are exceeded in keystone species. In the current project we could demonstrate that not only the strength and duration of heatwave events may matter, but also their timing may play a role in the extent and direction of the impact. Marine heatwaves in spring may not be as dramatic, or even beneficial, as similar events observed in peak summer, when species’ thermal limits are more likely to be exceeded. Yet, winter marine heatwaves may have strong impacts as organisms have developed energy-saving strategies to cope with periods of low food availability under prevailing low temperatures. Similarly, upwelling events may represent a relieve from heat stress during early summer heatwaves, but their hypoxic nature may impose subsequent additional stress to marine ecosystems in late summer and early autumn. Most dramatic effects were observed when different environmental drivers, in this particular case heat stress and low salinity events, did act in synchrony. Here, starfish’s tolerance was affected most dramatically, with potential implications for mussel reefs, as starfish regulates mussel abundances in large parts of the Western Baltic Sea. Previous publications demonstrated that selection of a macrophyte under one stressor may enhance performance under another (testing ocean acidification, heat stress and eutrophication), but would simultaneously leave a population more susceptible to hypoxic stress. Our findings suggest that more heat-tolerant individuals of mussels may be selected by extremely warm seasons at their very early life-history stages, and that such stress tolerance can be mediated through their lower metabolic demands. Acclimation to heat stress seemed less pronounced in these mussels. This project aligns well with an earlier project looking into the apparent variability in carbonate chemistry of marine systems, that can be found from the very small spatial scale of µm (diffusive boundary layer of macrophyte surfaces) to larger-scale fluctuations found in macrophyte beds. Thus, as an important substrate for many organisms, macrophytes potentially play a crucial role in rendering organisms less susceptible to future changes. We clearly show that environmental variability may provide transiently extreme conditions for organisms but may also provide refuge from mid-term stress events or from shifts in ocean mean conditions as projected for the future ocean. Yet, the capability of organisms may depend on their metabolic portfolio (e.g., metabolic suppression, acclimation potential), likely leaving strong species-specific differences in an ecosystem with potential winners and losers, and therefore, community shifts. In next steps, we need to understand if (i) increases in stress tolerance due to directional selection in marine species can lead to rapid evolutionary adaptation of populations and (ii) identify the potentially manyfold refuges that environmental variability may provide in a changing ocean.
Publications
- (2018) Heat waves and their significance for a temperate benthic community: a near-natural experimental approach. Global Change Biology 24:4357-4367
Pansch C, Scotti M, Barbozza FR, Al-Janabi B, Briski E, Paiva F, Saha M, Sawall Y, Weinberger F, Yto M, Wahl M
(See online at https://doi.org/10.1111/gcb.14282) - (2019) A new mesocosm system to study the effects of environmental variability on marine species and communities. Limnology & Oceanography - Methods 17:145-162
Pansch C & Hiebenthal C
(See online at https://doi.org/10.1002/lom3.10306) - (2019) Response of foundation macrophytes to near-natural simulated marine heatwaves. Global Change Biology 26:417-430
Saha M, Barboza FR, Somerfield PJ, Al-Janabi B, Beck M, Brakel J, Ito M, Pansch C, Nascimento-Schulze JC, Jakobsson Thor SJ, Weinberger F, Sawall Y
(See online at https://doi.org/10.1111/gcb.14801) - (2020) Consistency of aquatic enclosed experiments: the importance of scale and ecological complexity. Diversity & Distributions 00:1-9
Paiva F, Brennecke D, Pansch C, Briski E
(See online at https://doi.org/10.1111/ddi.13213) - (2020) Warming and temperature variability determine the performance of two invertebrate predators. Scientific Reports 10:6780
Morón Lugo SC, Baumeister M, Mohamed Nour O, Wolf F, Stumpp M, Pansch C
(See online at https://doi.org/10.1038/s41598-020-63679-0) - (2021) Simultaneous recording of filtration and respiration in marine organisms in response to short-term environmental variability. Limnology & Oceanography - Methods 00:1-13
Vajedsamiei J, Melzner F, Raatz M, Kiko R, Khosravi M, Pansch C
(See online at https://doi.org/10.1002/lom3.10414)
