From behaviour to complex communities: Resilience to anthropogenic noise in a fish-induced trophic cascade.

Sound emissions from human activities represent a pervasive environmental stressor. Individual responses in terms of behaviour, physiology or anatomy are well documented but whether they propagate through nested ecological interactions to alter complex communities needs to be better understood. This is even more relevant for freshwater ecosystems that harbour a disproportionate fraction of biodiversity but receive less attention than marine and terrestrial systems. We conducted a mesocosm investigation to study the effect of chronic exposure to motorboat noise on the dynamics of a freshwater community including phytoplankton, zooplankton, and roach as a planktivorous fish. In addition, we performed a microcosm investigation to test whether roach's feeding behaviour was influenced by the noise condition they experienced in the mesocosms. Indeed, compared to other freshwater fish, the response of roach to motorboat noise apparently does not weaken with repeated exposure, suggesting the absence of habituation. As expected under the trophic cascade hypothesis, predation by roach induced structural changes in the planktonic communities with a decrease in the main grazing zooplankton that slightly benefited green algae. Surprisingly, although the microcosm investigation revealed persistent alterations in the feeding behaviour of the roach exposed to chronic noise, the dynamics of the roach-dominated planktonic communities did not differ between the noisy and noiseless mesocosms. It might be that roach's individual response to noise was not strong enough to cascade or that the biological cues coming from the conspecifics and the many planktonic organisms have diverted each fish's attention from noise. Our work suggests that the top-down structuring influence of roach on planktonic communities might be resilient to noise and highlights how extrapolating impacts from individual responses to complex communities can be tricky.

The "parasite detoxification hypothesis": lead exposure potentially changes the ecological interaction from parasitism to mutualism.

In urban areas, organisms are exposed to high pollutant levels, especially element trace metals that may impact host-parasite interactions. Indeed, parasites have been reported to reduce the negative effects of pollutants on their hosts. The fitness of parasitized organisms in polluted environments may therefore be greater than that of unparasitized organisms. In our study, we used an experimental approach to test this hypothesis on feral pigeons (Columba livia), which are endemically parasitized by nematodes and exposed to high levels of lead in urban areas. We tested the combined effects of lead exposure and helminth parasitism on different pigeon fitness components: preening, immunocompetence, abundance of lice (Columbicola columbae) and haemosporidian parasites (Heamoproteus spp., Plasmodium spp.), reproduction investment, and oxidative stress. Our results show that among pigeons exposed to lead treatment, individuals harboring nematode parasites exhibit more preening activity and have fewer ectoparasites lice than nematode-free individuals. Benefits for nematode-parasitized individuals exposed to lead were not detected for other fitness parameters. Further studies are required to confirm the "parasite detoxification hypothesis" in pigeons and to identify the mechanisms by which this detoxification occurs.

Dysbiosis of fish gut microbiota is associated with helminths parasitism rather than exposure to PAHs at environmentally relevant concentrations.

Although parasite infection and pollution are common threats facing wild populations, the response of the gut microbiota to the joint impact of these stressors remains largely understudied. Here, we experimentally investigated the effects of exposure to Polycyclic Aromatic Hydrocarbons (PAHs) and infection by a common acanthocephalan intestinal parasite (Pomphorhynchus sp.) on the gut microbial flora of a freshwater fish, the European chub (Squalius cephalus). Naturally infected or uninfected individuals were exposed to PAHs at environmentally realistic concentrations over a five-week period. Characterization of the gut bacterial community through 16S rRNA gene amplicon sequencing revealed that parasitic infection was a more structuring factor of bacterial diversity and composition than PAH exposure. Specifically, chub infected by Pomphorhynchus sp. harbored significantly less evenly represented gut bacterial communities than the uninfected ones. In addition, substantial changes in sequence abundance were observed within the main bacterial phyla, including the Firmicutes, Fusobacteriota, Actinobacteriota, and Proteobacteria. Again, these compositional changes correlated with host infection with Pomphorhynchus sp., confirming its pivotal role in gut microbial assemblage. Overall, these results highlight the importance of defining the parasitic status of individuals when conducting microbial ecotoxicological analyses at the digestive tract level, as this should lead to better understanding of microbiota modulations and help to identify microbial markers specifically associated with chemicals.

Parasitism reduces oxidative stress of fish host experimentally exposed to PAHs.

Some parasites are known to bioaccumulate some environmental pollutants within their host. We hypothesized that these parasites may be beneficial for their hosts in polluted environments. We experimentally increased long-term (five weeks) exposure to polycyclic aromatic hydrocarbons (PAHs, three levels: 0.1X, 1X, 10X environmental exposure) in European chubs (Squalius cephalus) that were naturally infected or uninfected with acanthocephalan parasites. We monitored PAHs levels in fish tissues, as well as oxidative stress, telomere length and condition indices. Although parasite infection did not significantly reduce the levels of PAHs and PAH metabolites in host tissues, host oxidative status was explained by parasitism and pollution levels. Oxidative damage increased with parasitism in fish exposed to low PAH levels (0.1X) but decreased in infected fish at higher PAH exposure (10X), thus corroborating our hypothesis. Meanwhile, antioxidant capacity did not differ in response to parasite infection nor PAHs exposure. Despite this imbalance in oxidative status, experimental increase in PAH levels did not compromise telomere length, body condition, or survival in infected and uninfected fish. This study provides the first experimental evidence that the outcome of host-parasite interactions can shift from negative to positive as pollutant exposure increases.

Density-dependent natural selection mediates harvest-induced trait changes.

Rapid life-history changes caused by size-selective harvesting are often interpreted as a response to direct harvest selection against a large body size. However, similar trait changes may result from a harvest-induced relaxation of natural selection for a large body size via density-dependent selection. Here, we show evidence of such density-dependent selection favouring large-bodied individuals at high population densities, in replicated pond populations of medaka fish. Harvesting, in contrast, selected medaka directly against a large body size and, in parallel, decreased medaka population densities. Five years of harvesting were enough for harvested and unharvested medaka populations to inherit the classically predicted trait differences, whereby harvested medaka grew slower and matured earlier than unharvested medaka. We show that this life-history divergence was not driven by direct harvest selection for a smaller body size in harvested populations, but by density-dependent natural selection for a larger body size in unharvested populations.

Unidirectional response to bidirectional selection on body size II. Quantitative genetics.

Anticipating the genetic and phenotypic changes induced by natural or artificial selection requires reliable estimates of trait evolvabilities (genetic variances and covariances). However, whether or not multivariate quantitative genetics models are able to predict precisely the evolution of traits of interest, especially fitness-related, life history traits, remains an open empirical question. Here, we assessed to what extent the response to bivariate artificial selection on both body size and maturity in the medaka Oryzias latipes, a model fish species, fits the theoretical predictions. Three lines (Large, Small, and Control lines) were differentially selected for body length at 75 days of age, conditional on maturity. As maturity and body size were phenotypically correlated, this selection procedure generated a bi-dimensional selection pattern on two life history traits. After removal of nonheritable trends and noise with a random effect ("animal") model, the observed selection response did not match the expected bidirectional response. For body size, Large and Control lines responded along selection gradients (larger body size and stasis, respectively), but, surprisingly, the Small did not evolve a smaller body length and remained identical to the Control line throughout the experiment. The magnitude of the empirical response was smaller than the theoretical prediction in both selected directions. For maturity, the response was opposite to the expectation (the Large line evolved late maturity compared to the Control line, while the Small line evolved early maturity, while the opposite pattern was predicted due to the strong positive genetic correlation between both traits). The mismatch between predicted and observed response was substantial and could not be explained by usual sources of uncertainties (including sampling effects, genetic drift, and error in G matrix estimates).

Unidirectional response to bidirectional selection on body size. I. Phenotypic, life-history, and endocrine responses.

Anthropogenic perturbations such as harvesting often select against a large body size and are predicted to induce rapid evolution toward smaller body sizes and earlier maturation. However, body-size evolvability and, hence, adaptability to anthropogenic perturbations remain seldom evaluated in wild populations. Here, we use a laboratory experiment over 6 generations to measure the ability of wild-caught medaka fish (Oryzias latipes) to evolve in response to bidirectional size-dependent selection mimicking opposite harvest regimes. Specifically, we imposed selection against a small body size (Large line), against a large body size (Small line) or random selection (Control line), and measured correlated responses across multiple phenotypic, life-history, and endocrine traits. As expected, the Large line evolved faster somatic growth and delayed maturation, but also evolved smaller body sizes at hatch, with no change in average levels of pituitary gene expressions of luteinizing, follicle-stimulating, or growth hormones (GH). In contrast, the Small medaka line was unable to evolve smaller body sizes or earlier maturation, but evolved smaller body sizes at hatch and showed marginally significant signs of increased reproductive investment, including larger egg sizes and elevated pituitary GH production. Natural selection on medaka body size was too weak to significantly hinder the effect of artificial selection, indicating that the asymmetric body-size response to size-dependent selection reflected an asymmetry in body-size evolvability. Our results show that trait evolvability may be contingent upon the direction of selection and that a detailed knowledge of trait evolutionary potential is needed to forecast population response to anthropogenic change.

Short-term change in water availability influences thermoregulation behaviours in a dry-skinned ectotherm.

Mechanistic models of terrestrial ectotherms predict that climate warming will induce activity restriction due to heat stress and loss of shade, leading to the extinction of numerous populations. Such models rely on the assumption that activity patterns are dictated by simple temperature thresholds independent of changes in water availability. However, changes in water availability may further influence thermoregulation behaviour of ectotherms through dehydration risk perception, changes in water balance or changes in microclimatic conditions. Here, we experimentally assess the interactive effects of thermal conditions and water availability on activity patterns, shade selection and thermoregulation efficiency in a model ectothermic species. Thermoregulation behaviour of adult common lizards Zootoca vivipara was monitored in outdoor mesocosms as we manipulated water availability, providing water as mist in the morning and free-standing water during the daytime. We recorded operative temperatures and micro-meteorological conditions to infer thermal constraints and dehydration risk. Activity and shade selection were better predicted by continuous changes in thermal conditions and dehydration risk, respectively, than by threshold functions. In addition, water supplementation increased activity in males and reduced shade selection in both sexes, most probably as a behavioural response to the perception of a stronger dehydration risk. Water supplementation also influenced the thermal quality of the environment, which in turn altered daily activity patterns and thermoregulation statistics. This demonstrates that dual effects of heat and water stress on activity patterns may lead to stronger activity restriction as a result of climate change than currently predicted.

Chronic water restriction triggers sex-specific oxidative stress and telomere shortening in lizards.

Animals use a variety of strategies to avoid acute dehydration and death. Yet, how chronic exposure to sub-lethal dehydration may entail physiological and fitness costs remains elusive. In this study, we experimentally tested if water restriction causes increased oxidative stress (OS) and telomere length (TL) shortening, two well-described mediators of environment-fitness relationships. We exposed 100 yearling female and male common lizards (Zootoca vivipara) either to a 51-day period of water restriction or to water ad libitum, followed by 45 days in common garden outdoor conditions. We measured the kinetic changes in OS and TL and found that water-restricted males had enhanced antioxidant defences and decreased oxidative damage at day 36, whereas females did not immediately respond. A month and a half after water restriction, both sexes experienced a drop in antioxidant capacity but only males exhibited significant TL shortening. In the following 3 years, we found that lizards with longer initial TL and those who maintained stronger antioxidant defences experienced higher longevity, irrespective of sex and water restriction. Together, these results unravelled sex-specific responses to water restriction, with potential applications in better understanding the physiological costs of increasing summer droughts as a result of global climate change.

Acclimation to Water Restriction Implies Different Paces for Behavioral and Physiological Responses in a Lizard Species.

Chronic changes in climate conditions may select for acclimation responses in terrestrial animals living in fluctuating environments, and beneficial acclimation responses may be key to the resilience of these species to global changes. Despite evidence that climate warming induces changes in water availability, acclimation responses to water restriction are understudied compared with thermal acclimation. In addition, acclimation responses may involve different modes, paces, and trade-offs between physiological and behavioral traits. Here, we tested the dynamical acclimation responses of a dry-skinned terrestrial ectotherm to chronic water restriction. Yearling common lizards (Zootoca vivipara) were exposed to sublethal water restriction during 2 mo of the summer season in laboratory conditions, then released in outdoor conditions for 10 additional months. Candidate behavioral (exploration, basking, and thermal preferences) and physiological (metabolism at rest and standard water loss rate) traits potentially involved in the acclimation response were measured repeatedly during and after water restriction. We observed a sequential acclimation response in water-restricted animals (yearlings spent less time basking during the first weeks of water deprivation) that was followed by delayed sex-specific physiological consequences of the water restriction during the following months (thermal depression in males and lower standard evaporative water loss rates in females). Despite short-term negative effects of water restriction on body growth, annual growth, survival, and reproduction were not significantly different between water-restricted and control yearlings. This demonstrates that beneficial acclimation responses to water restriction involve both short-term flexible behavioral responses and delayed changes in thermal and water biology traits.

Chronic elevation of glucorticoids late in life generates long lasting changes in physiological state without a life history switch.

Chronic stressors have profound impacts on phenotypes and life history strategies on the short term, but delayed effects of stress experienced late in life remain poorly investigated in wild populations. Here, we used a combined laboratory and field experiment to test if chronic stress late in life has immediate and delayed effects on physiological and demographic traits in the common lizard, Zootoca vivipara. We increased plasma corticosterone levels in adults and yearlings during three weeks of the post-reproductive season. We quantified immediate responses in the laboratory, delayed intra-generational effects in field enclosures one month and one year later during the next reproductive season, and delayed inter-generational effects in the first generation of offspring. Our phenotypic assays included metabolism, immune capacities, lipid metabolism and oxidative stress. Relative to placebos, lizards treated with corticosterone had higher body condition and lower oxidative damages but an increased skin swelling response directly after the manipulation. Delayed responses in field enclosures were of three types. First, we found catch-up growth for body mass such the placebos had similar body conditions one month after the laboratory manipulation. Second, we found persistent differences in oxidative damages during one month but not one year later. Third, during the next reproductive season, corticosterone-treated females had higher levels of plasma triglycerides, whereas corticosterone-treated individuals had a higher skin swelling response. We found no delayed inter-generational effects on demographic traits of offspring. Our study demonstrates the potential for long-lasting physiological consequences of chronic corticosterone enhancement despite no obvious changes in life history.

Some like it dry: Water restriction overrides heterogametic sex determination in two reptiles.

ABSTRACT: The evolution of sex determination is complex and yet crucial in our understanding of population stability. In ectotherms, sex determination involves a variety of mechanisms including genetic determination (GSD), environment determination (ESD), but also interactions between the two via sex reversal. In this study, we investigated whether water deprivation during pregnancy could override GSD in two heterogametic squamate reptiles. We demonstrated that water restriction in early gestation induced a male-biased secondary sex ratio in both species, which could be explained by water sex reversal as the more likely mechanism. We further monitored some long-term fitness estimates of offspring, which suggested that water sex determination (WSD) represented a compensatory strategy producing the rarest sex according to Fisher's assumptions of frequency-dependent selection models. This study provides new insights into sex determination modes and calls for a general investigation of mechanisms behind WSD and to examine the evolutionary implications. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.mv06pv1.

Experimental increase in temperature affects eggshell thickness, and not egg mass, eggshell spottiness or egg composition in the great tit (Parus major).

Phenotypic effects of global warming have been documented in many different taxa. However, the importance of transgenerational phenotypic plasticity in these adaptations are seldom studied. In birds, temperature could affect egg characteristics. Higher temperatures during egg-laying may reduce maintenance costs for females and allow a higher investment in reproduction. Yet, females may also use temperatures as a cue for the risk of mismatch latter in the season. Thus, higher temperatures may be correlated to an acceleration of embryonic development (e.g. via hormonal manipulation). We performed an experiment in which night-time temperature was increased in the nestbox by approximately 1 °C throughout the entire laying period in great tits (Parus major). We collected one pre-treatment egg (beginning of the laying sequence) and one post-treatment egg (end of the laying sequence). Egg content (yolk androgens and lysozymes in the albumen), eggshell coloration, eggshell mass, egg mass, and shape were not affected by the treatment. However, last-laid eggs in clutches from control nestboxes had a thicker eggshell than last-laid eggs from heated nestboxes, suggesting a putative slight decrease of maternal investment with the experimental increase of temperature. We also observed effects of the laying sequence on egg characteristics. Eggs that were laid late in the laying sequence were heavier, larger, had larger spots and higher yolk androgens than eggs laid earlier. Lysozyme concentration decrease with the laying sequence in late clutches only. Thus, effects of temperature may also change with the laying sequence and it would be interesting in the future to tests the effects on first-laid eggs.

Habitat degradation increases stress-hormone levels during the breeding season, and decreases survival and reproduction in adult common lizards.

The allostatic load model describes how individuals maintain homeostasis in challenging environment and posits that costs induced by a chronic perturbation (i.e., allostatic load) are correlated to the secretion of glucocorticoids, such as corticosterone. Habitat perturbations from anthropogenic activities are multiple and functional responses to those are still unclear. Here, we manipulated the habitat quality in 24 semi-natural populations of the common lizard during 1 year. We tested the predictions of the allostatic load model that habitat degradation should increase baseline corticosterone levels, and should induce concomitant physiological changes, such as lipid mobilization and lower immunocompetence, and demographic changes, such as lower body growth, survival and/or reproductive performances. Our results highlight stage-dependent effects of habitat degradation on physiological traits during the breeding season: adult lizards had higher baseline corticosterone levels and yearling lizards had a lower inflammatory response than adults, whereas juveniles had higher circulating lipid levels than yearlings and adults without concomitant change in corticosterone levels. In addition, habitat degradation reduced the performances of adults but not of juveniles: in low habitat quality populations, adult males had a lower survival and females had a smaller fecundity. These results are in accordance with the allostatic load model given that allostatic load was detected only during the season and in life stages of maximal energy expenditure. This underlines the importance to account for individual energy requirements to better understand demographic responses to habitat perturbation.