A framework to understand the role of biological time in responses to fluctuating climate drivers

Understanding biological responses to environmental fluctuations (e.g. heatwaves) is a critical goal in ecology. Biological responses (e.g. survival) are usually measured with respect to different time reference frames, i.e. at specific chronological times (e.g. at specific dates) or biological times (e.g. at reproduction). Measuring responses on the biological frame is central to understand how environmental fluctuation modifies fitness and population persistence. We use a framework, based on partial differential equations (PDEs) to explore how responses to the time scale and magnitude of fluctuations in environmental variables (= drivers) depend on the choice of reference frame. The PDEs and simulations enabled us to identify different components, responsible for the phenological and eco-physiological effects of each driver on the response. The PDEs also highlight the conditions when the choice of reference frame affects the sensitivity of the response to a driver and the type of join effect of two drivers (additive or interactive) on the response. Experiments highlighted the importance of studying how environmental fluctuations affect biological time keeping mechanisms, to develop mechanistic models. Our main result, that the effect of the environmental fluctuations on the response depends on the scale used to measure time, applies to both field and laboratory conditions. In addition, our approach, applied to experimental conditions, can helps us quantify how biological time mediates the response of organisms to environmental fluctuations

A multiple baseline approach for marine heatwaves

Marine heatwaves and other extreme temperature events can drive biological responses, including mass mortality. However, their effects depend on how they are experienced by biological systems (including human societies). We applied two different baselines (fixed and shifting) to a time series of North Sea water temperature to explore how slowly vs. quickly adapting systems would experience extreme temperatures. We tested if the properties of marine heatwaves and the association with atmospheric heatwaves were robust to a change in baseline. A fixed baseline produced an increase in the frequency and duration of marine heatwaves, which would be experienced as the new normal by slowly adapting systems; 7 of the 10 most severe heatwaves occurred between 1990 and 2018. The shifting baseline removed the trend in the frequency but not duration of heatwaves; the 1990s appeared as a period of change in the frequency of strong and severe heatwaves as compared to the 1980s. There were also common patterns among baselines: marine heatwaves were more frequent in late summer when temperatures peak; temperature variability was characterized by low frequency, large amplitude fluctuations (i.e., as red noise), known to drive extinction events. In addition, marine heatwaves occurred during or just after atmospheric heatwaves. Our work highlights the importance of identifying properties of marine heatwaves that are robust or contingent on a change in baseline

A state-space approach to understand responses of organisms, populations and communities to multiple environmental drivers

Understanding the response of biotic systems to multiple environmental drivers is one of the major concerns in ecology. The most common approach in multiple driver research includes the classification of interactive responses into categories (antagonistic, synergistic). However, there are situations where the use of classification schemes limits our understanding or cannot be applied. Here, we introduce and explore an approach that allows us to better appreciate variability in responses to multiple drivers. We then apply it to a case, comparing effects of heatwaves on performance of a cold-adapted species and a warm-adapted competitor. The heatwaves had a negative effect on the native (but not on the exotic) species and the approach highlighted that the exotic species was less responsive to multivariate environmental variation than the native species. Overall, we show how the proposed approach can enhance our understanding of variation in responses due to different driver intensities, species, genotypes, ontogeny, life-phases or among spatial scales at any level of biological organization

On their way to the North: larval performance of Hemigrapsus sanguineus invasive to the European coast. A comparison with the native European population of Carcinus maenas

The Asian shore crab Hemigrapsus sanguineus has become invasive in North Europe and it co-occurs and competes with the native European shore crab Carcinus maenas. Both species develop through a feeding and dispersive larval phase characterised by several zoeal and a settling megalopa stage. Larvae of marine crabs are vulnerable to food limitation and warming has the potential to exacerbate the negative effects of food limitation on survival and growth. We quantified the combined effects of temperature and food limitation on larval performance (survival and growth) of H. sanguineus and we compared our results with those reported on performance of C. maenas larvae, under the same experimental design and methodology. Larvae from four females of H. sanguineus collected on Helgoland (North Sea) were experimentally reared from hatching to megalopa, at four temperatures (range 15–24 °C) and two food conditions (permanent vs. daily limited access to food). Larval survival of H. sanguineus was low at 15 °C and increased with temperature, in contrast to the high survival reported for C. maenas larvae in the range 15–24 °C. Food limitation reduced survival and body mass of H. sanguineus larvae at all temperatures, but without evidence of the exacerbating effect caused by high temperatures and reported for C. maenas. By contrast, high temperature (24 °C) mitigated the negative effect of food limitation on body mass on H. sanguineus larvae. Advantages of H. sanguineus over C. maenas appear especially under the increased temperatures expected from climate change

Quantifying the portfolio of larval responses to salinity and temperature in a coastal-marine invertebrate: a cross population study along the European coast

portfolio available for a species to cope with and mitigate effects of climate change. Here, we quantified variation in larval survival and physiological rates of Carcinus maenas among populations occurring in distant or contrasting habitats (Cádiz: Spain, Helgoland: North Sea, Kerteminde: Baltic Sea). During the reproductive season, we reared larvae of these populations, in the laboratory, under a combination of several temperatures (15–24 °C) and salinities (25 and 32.5 PSU). In survival, all three populations showed a mitigating effect of high temperatures at lower salinity, with the strongest pattern for Helgoland. However, Cádiz and Kerteminde differed from Helgoland in that a strong thermal mitigation did not occur for growth and developmental rates. For all populations, oxygen consumption rates were driven only by temperature; hence, these could not explain the growth rate depression found at lower salinity. Larvae from Cádiz, reared in seawater, showed increased survival at the highest temperature, which differs from Helgoland (no clear survival pattern), and especially Kerteminde (decreased survival at high temperature). These responses from the Cádiz population correspond with the larval and parental habitat (i.e., high salinity and temperature) and may reflect local adaptation. Overall, along the European coast, C. maenas larvae showed a diversity of responses, which may enable specific populations to tolerate warming and subsidise more vulnerable populations. In such case, C. maenas would be able to cope with climate change through a spatial portfolio effect

Methods to study organogenesis in decapod crustacean larvae. I. larval rearing, preparation, and fixation

Crustacean larvae have served as distinguished models in the field of Ecological Developmental Biology (“EcoDevo”) for many decades, a discipline that examines how developmental mechanisms and their resulting phenotype depend on the environmental context. A contemporary line of research in EcoDevo aims at gaining insights into the immediate tolerance of organisms and their evolutionary potential to adapt to the changing abiotic and biotic environmental conditions created by anthropogenic climate change. Thus, an EcoDevo perspective may be critical to understand and predict the future of organisms in a changing world. Many decapod crustaceans display a complex life cycle that includes pelagic larvae and, in many subgroups, benthic juvenile–adult stages so that a niche shift occurs during the transition from the larval to the juvenile phase. Already at hatching, the larvae possess a wealth of organ systems, many of which also characterise the adult animals, necessary for autonomously surviving and developing in the plankton and suited to respond adaptively to fluctuations of environmental drivers. They also display a rich behavioural repertoire that allows for responses to environmental key factors such as light, hydrostatic pressure, tidal currents, and temperature. Cells, tissues, and organs are at the basis of larval survival, and as the larvae develop, their organs continue to grow in size and complexity. To study organ development, researchers need a suite of state-of-the-art methods adapted to the usually very small size of the larvae. This review and the companion paper set out to provide an overview of methods to study organogenesis in decapod larvae. This first section focuses on larval rearing, preparation, and fixation, whereas the second describes methods to study cells, tissues, and organs