Resilience to heat waves in the aquatic snail Lymnaea stagnalis: Additive and interactive effects with micropollutants

Abstract

Multiple anthropogenic changes, such as climate change and chemical pollution, threaten the persistence of natural populations. Yet, their potential additive and interactive effects on organismal performance and fitness are poorly understood, thus limiting our ability to predict the effects of the global change. We conducted a laboratory experiment to study the singular and combined effects of experimental heat waves and micropollutants (i.e. low‐concentration toxicants; henceforth micropollutants [MPs]) on the freshwater snail, Lymnaea stagnalis. To comprehensively understand physiological and ecological consequences of stress, we studied a broad range of traits from respiration rate to feeding performance and growth. We also determined traits contributing to fitness and immune responses, as these are key traits in determining both organismal fitness and interspecific (e.g. host–parasite) interactions. We tested whether a constant exposure to MPs affects the ability of snails to tolerate heat waves (8 days of 23.5°C), and subsequently to recover from them, and whether the effects are immediate or delayed. We found strong immediate additive effects of both stressors on reproduction, while they synergistically increased respiration and antagonistically decreased food consumption. Moreover, these effects were transient. Although the heat wave increased metabolic rates, individuals did not increase their resource uptake. This caused an apparent imbalance in resource levels—a probable cause for the observed trade‐off between immune function and reproductive traits (i.e. phenoloxidase‐like activity decreased, while reproductive output increased). In addition, exposure to MPs led to a temporarily reduced reproductive output. Our results indicate that even short‐term heat waves and low concentrations of chemical pollution can have large, mainly additive impacts on organismal fitness (e.g. altering susceptibility to infections and reproductive output). This suggests that long‐term effects of existing stressors and heat waves need to be considered when assessing the resilience of natural populations.

Diurnal variation around an optimum and near‐critically high temperature does not alter the performance of an ectothermic aquatic grazer

“…L. stagnalis is a hermaphroditic pulmonate gastropod (thus, no gender‐based differences), with a wide distribution in stagnant or slowly flowing water bodies in the Northern Hemisphere. It is extensively used as a model organism to investigate the effects of warming (e.g., Leicht, Jokela, & Seppälä, ; Salo, Räsänen, Stamm, Burdon, & Seppälä, ; Salo, Stamm, Burdon, Räsänen, & Seppälä, ; Seppälä & Jokela, ) and pollutants (e.g., Coutellec & Lagadic, ; Nyman, Schirmer, & Ashauer, ; Salo et al, ; Salo et al, ) on organisms, as well as host‐parasite interactions (e.g., Karvonen, Savolainen, Seppälä, & Valtonen, ; Leicht & Seppälä, ) and immunology (e.g., Dikkeboom, Knaap, Meuleman, & Sminia, ; Seppälä & Leicht, ). In this species, exposure to high temperatures increases several organismal process rates (Salo et al, ), which leads to increased growth rate and reproductive output with a temporal threshold (1 week), after which the reproductive rate is reduced (Leicht et al, ).…”

“…In this species, exposure to high temperatures increases several organismal process rates (Salo et al, ), which leads to increased growth rate and reproductive output with a temporal threshold (1 week), after which the reproductive rate is reduced (Leicht et al, ). High temperatures also reduce snail immune defense (Leicht et al, ; Salo et al, ; Seppälä & Jokela, ), which increases their susceptibility to trematode parasites (Leicht & Seppälä, ). However, these earlier studies on the effects of warming have all used experimental treatments with constant temperatures.…”

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

“…We used structural equation modeling in IBM SPSS AMOS 23 (IBM, Armonk, NY, USA) to examine the effects of snail size, food consumption, respiration rate, and the examined immune parameters (PO‐like activity and antibacterial activity of hemolymph) as well as the causality of those effects on the snails' attractiveness to parasite cercariae and their susceptibility to infection. The original model was based on our estimates of the causality of possible impacts and included the following links between the variables: effects of snail size on food consumption (Salo, Stamm, Burdon, Räsänen, & Seppälä, ), respiration rate (Salo et al., ), attractiveness to parasites, immune function (both parameters (Salo et al., ; Seppälä & Jokela, )), and susceptibility to infection (Seppälä et al., ); effects of food consumption on attractiveness to parasites (Seppälä & Leicht, ), immune activity (both parameters (Langeloh et al., ; Seppälä & Jokela, )), and susceptibility to infection (Seppälä et al., ); effects of respiration rate on attractiveness to parasites and susceptibility to infection; effects of attractiveness to parasites and the level of immune parameters on susceptibility to infection. Additionally, the model included covariation between food consumption and respiration rate as well as between immune traits (Seppälä & Leicht, ).…”

“…We of snail size on food consumption (Salo, Stamm, Burdon, Räsänen, & Seppälä, 2017), respiration rate (Salo et al, 2017), attractiveness to parasites, immune function (both parameters (Salo et al, 2017;Seppälä & Jokela, 2010)), and susceptibility to infection (Seppälä et al, 2011); effects of food consumption on attractiveness to parasites (Seppälä & Leicht, 2015), immune activity (both parameters (Langeloh et al, 2017;Seppälä & Jokela, 2010)), and susceptibility to infection (Seppälä et al, 2011); effects of respiration rate on attractiveness to parasites and susceptibility to infection; effects of attractiveness to parasites and the level of immune parameters on susceptibility to infection. Additionally, the model included covariation between food consumption and respiration rate as well as between immune traits (Seppälä & Leicht, 2013).…”

Direct and transgenerational effects of an experimental heatwave on early life stages in a freshwater snail

“…The direct effect of high temperature on offspring survival may be due to temperature-induced changes in, for instance, protein structures and/or membrane fluidity (reviewed in Pörtner, Lucassen, & Storch, 2005), which can lead to body malfunctions and increased mortality. Iguchi & Ikeda, 2005;Salo, Stamm, Burdon, Räsänen, & Seppälä, 2017). Iguchi & Ikeda, 2005;Salo, Stamm, Burdon, Räsänen, & Seppälä, 2017).…”