When worlds collide: Invader-driven benthic habitat complexity alters predatory impacts of invasive and native predatory fishes.

Interactions between multiple invasive alien species (IAS) might increase their ecological impacts, yet relatively few studies have attempted to quantify the effects of facilitative interactions on the success and impact of aquatic IAS. Further, the effect of abiotic factors, such as habitat structure, have lacked consideration in ecological impact prediction for many high-profile IAS, with most data acquired through simplified assessments that do not account for real environmental complexities. In the present study, we assessed a potential facilitative interaction between a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), and an invasive bivalve, the Asian clam (Corbicula fluminea). We compared N. melanostomus functional responses (feeding-rates under different prey densities) to a co-occurring endangered European native analogue fish, the bullhead (Cottus gobio), in the presence of increased levels of habitat complexity driven by the accumulation of dead C. fluminea biomass that persists within the environment (i.e. 0, 10, 20 empty bivalve shells). Habitat complexity significantly influenced predation, with consumption in the absence of shells being greater than where 10 or 20 shells were present. However, at the highest shell density, invasive N. melanostomus maximum feeding-rates and functional response ratios were substantially higher than those of native C. gobio. Further, the Relative Impact Potential metric, by combining per capita effects and population abundances, indicated that higher shell densities exacerbate the relative impact of the invader. It therefore appears that N. melanostomus can better tolerate higher IAS shell abundances when foraging at high prey densities, suggesting the occurrence of an important facilitative interaction. Our data are thus fully congruent with field data that link establishment success of N. melanostomus with the presence of C. fluminea. Overall, we show that invader-driven benthic habitat complexity can alter the feeding-rates and thus impacts of predatory fishes, and highlight the importance of inclusion of abiotic factors in impact prediction assessments for IAS.

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.

Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages.

The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species' impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10530-021-02542-3.

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.

Author Correction: Metabolic changes in Medaka fish induced by cyanobacterial exposures in mesocosms: an integrative approach combining proteomic and metabolomic analyses.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

Metabolic changes in Medaka fish induced by cyanobacterial exposures in mesocosms: an integrative approach combining proteomic and metabolomic analyses.

Cyanobacterial blooms pose serious threats to aquatic organisms and strongly impact the functioning of aquatic ecosystems. Due to their ability to produce a wide range of potentially bioactive secondary metabolites, so called cyanotoxins, cyanobacteria have been extensively studied in the past decades. Proteomic and metabolomic analyses provide a unique opportunity to evaluate the global response of hundreds of proteins and metabolites at a glance. In this study, we provide the first combined utilization of these methods targeted to identify the response of fish to bloom-forming cyanobacteria. Medaka fish (Oryzias latipes) were exposed for 96 hours either to a MC-producing or to a non-MC-producing strain of Microcystis aeruginosa and cellular, proteome and metabolome changes following exposure to cyanobacteria were characterized in the fish livers. The results suggest that a short-term exposure to cyanobacteria, producing or not MCs, induces sex-dependent molecular changes in medaka fish, without causing any cellular alterations. Globally, molecular entities involved in stress response, lipid metabolism and developmental processes exhibit the most contrasted changes following a cyanobacterial exposure. Moreover, it appears that proteomic and metabolomic analyses are useful tools to verify previous information and to additionally bring new horizons concerning molecular effects of cyanobacteria on fish.

Global metabolome changes induced by cyanobacterial blooms in three representative fish species.

Cyanobacterial blooms induce important ecological constraints for aquatic organisms and strongly impact the functioning of aquatic ecosystems. In the past decades, the effects of the cyanobacterial secondary metabolites, so called cyanotoxins, have been extensively studied in fish. However, many of these studies have used targeted approaches on specific molecules, which are thought to react to the presence of these specific cyanobacterial compounds. Since a few years, untargeted metabolomic approaches provide a unique opportunity to evaluate the global response of hundreds of metabolites at a glance. In this way, our study provides the first utilization of metabolomic analyses in order to identify the response of fish exposed to bloom-forming cyanobacteria. Three relevant fish species of peri-urban lakes of the European temperate regions were exposed for 96h either to a microcystin (MC)-producing or to a non-MC-producing strain of Microcystis aeruginosa and metabolome changes were characterized in the liver of fish. The results suggest that a short-term exposure to those cyanobacterial biomasses induces metabolome changes without any response specificity linked to the fish species considered. Candidate metabolites are involved in energy metabolism and antioxidative response, which could potentially traduce a stress response of fish submitted to cyanobacteria. These results are in agreement with the already known information and could additionally bring new insights about the molecular interactions between cyanobacteria and fish.