Anthropogenic noise does not strengthen multiple-predator effects in a freshwater invasive fish.

Anthropogenic noise has the potential to alter community dynamics by modifying the strength of nested ecological interactions such as predation. Direct effects of noise on per capita predation rates have received much attention but the context in which predation occurs is often oversimplified. For instance, many animals interact with conspecifics while foraging and these nontrophic interactions can positively or negatively influence per capita predation rates. These effects are often referred to as multiple-predator effects (MPEs). The extent to which noise can modulate MPEs and thereby indirectly alter per capita predation remains unknown. To address this question, we derived the relationship between per capita predation rate and prey density, namely the functional response (FR), of single and pairs of the invasive topmouth gudgeon Pseudorasbora parva when feeding on water fleas under two noise conditions: control ambient noise estimated at 95 dB re 1 µPa and ambient noise supplemented with motorboat sounds whose relative importance over ambient noise ranged from 4.81 to 27 dB. In addition, we used video recordings to track fish movements. To detect MPEs, we compared the observed group-level FRs to predicted group-level FRs inferred from the individual FRs and based on additive effects only. Regardless of the number of fish and the noise condition, the FR was always of type II, showing predation rate in a decelerating rise to an upper asymptote. Compared to the noiseless condition, the predation rate of single fish exposed to noise did not differ at high prey densities but was significantly lower at low prey densities, resulting in an FR with the same asymptote but a less steep initial slope. Noise also reduced fish mobility, which might explain the decrease in predation rate at low prey densities. Conspecific presence suppressed the individual response to noise, the FRs of two fish (observed group-level FRs) being perfectly similar between the two noise conditions. Although observed and predicted group-level FRs did not differ significantly, observed group-level FRs tended to fall in the low range of predicted group-level FRs, suggesting antagonism and a negative effect of nontrophic interactions on individual foraging performance. Interestingly, the difference between predicted and observed group-level FRs was not greater with noise, which means that noise did not strengthen MPEs. Our results show that when considering the social context of foraging, here through the presence of a conspecific, anthropogenic noise does not compromise foraging in the invasive P. parva.

Potential Benefits of Acanthocephalan Parasites for Chub Hosts in Polluted Environments.

Some parasites are expected to have beneficial impacts on wild populations in polluted environments because of their bioaccumulation potential of pollutants from their hosts. The fate of organic micropollutants in host-parasite systems and the combined effect of parasitism and pollution were investigated in chub Squalius cephalus, a freshwater fish, infected (n = 73) or uninfected (n = 45) by acanthocephalan parasites Pomphorhynchus sp. from differently contaminated riverine sites. Several ubiquitous pollutants (polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated diphenyl-ethers (PBDEs), polycyclic aromatic hydrocarbons (PAHs), phthalates, insecticides, pyrethroids, and N,N-diethyl-meta-toluamide (DEET)) and some of their metabolites were characterized for the first time in parasites and various fish matrices (muscle, liver, and stomach content). Most organic pollutants reached higher levels in parasites than in chub matrices. In contrast, metabolite levels were lower in parasite tissues compared to fish matrices. Infected and uninfected chub exhibited no significant differences in their pollutant load. Body condition, organo-somatic indices, and immunity were not affected by parasitism, and few correlations were found with chemical pollution. Interestingly, infected chub exhibited lower oxidative damage compared to uninfected fish, irrespective of their pollutant load. In light of these results, this correlative study supports the hypothesis that acanthocephalan parasites could bring benefits to their hosts to cope with organic pollution.

Parasitism effects on coexistence and stability within simple trophic modules.

Parasites are important components of food webs. Although their direct effects on hosts are well-studied, indirect impacts on trophic networks, thus on non-host species, remain unclear. In this study, we investigate the consequences of parasitism on coexistence and stability within a simple trophic module: one predator consuming two prey species in competition. We test how such effects depend on the infected species (prey or predator). We account for two effects of parasitism: the virulence effect (parasites affect the infected species intrinsic growth rate through direct effects on fecundity or mortality) and the interaction effect (increased vulnerability of infected prey or increased food intake of infected predators). Results show that coexistence is favored when effects have intermediate intensity. We link this result to modifications of direct and apparent competitions among prey species. Given a prey infection, accounting for susceptible-infected population structure highlights that coexistence may also be reduced due to predator-parasite competition. Parasites affect stability by modulating energy transfer from prey to predator. Predator infection therefore has a stabilizing effect due to increased energy fluxes and/or predator mortality. Our results suggest that parasites potentially increase species coexistence. Precise predictions however require an assessment of various parasite effects. We discuss the implications of our results for the functioning of trophic networks.

Behavioural response to boat noise weakens the strength of a trophic link in coral reefs.

In oceans, the noise generated by human activities has reached phenomenal proportions, with considerable harmful effects on marine life. Measuring this impact to achieve a sustainable balance for highly vulnerable marine ecosystems, such as coral reefs, is a critical environmental policy objective. Here, we demonstrate that anthropogenic noise alters the interactions of a coral reef fish with its environment and how this behavioural response to noise impairs foraging. In situ observations on the Moorea reef revealed that the damselfish Dascyllus emamo reacts to boat passage by moving closer to its coral bommie, considerably reducing the volume of water available to search for prey. Using boat noise playback experiments in microcosms, we studied D. emamo's behaviour and modeled its functional response (FR), which is the relationship between resource use and resource density, when feeding on juvenile shrimps. Similar to field observations, noise reduced D. emamo's spatial occupancy, accompanied by a lower FR, indicating a reduction in predation independent of prey density. Overall, noise-induced behavioural changes are likely to influence predator-prey interaction dynamics and ultimately the fitness of both protagonists. While there is an urgent need to assess the effect of anthropogenic noise on coral reefs, the ecological framework of the FR approach combined with behavioural metrics provides an essential tool for evaluating the cascading effects of noise on nested ecological interactions at the community level.

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.

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.

Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs.

Although trophically transmitted parasites are recognized to strongly influence food-web dynamics through their ability to manipulate host phenotype, our knowledge of their host spectrum is often imperfect. This is particularly true for the facultative paratenic hosts, which receive little interest. We investigated the occurrence and significance both in terms of ecology and evolution of paratenic hosts in the life cycle of the fish acanthocephalan Pomphorhynchus laevis. This freshwater parasite uses amphipods as intermediate hosts and cyprinids and salmonids as definitive hosts. Within a cohort of parasite larvae, usually reported in amphipod intermediate hosts, more than 90% were actually hosted by small-sized fish. We demonstrated experimentally, using one of these fish, that they get infected through the consumption of parasitized amphipods and contribute to the parasite's transmission to a definitive host, hence confirming their paratenic host status. A better knowledge of paratenic host spectrums could help us to understand the fine tuning of transmission strategies, to better estimate parasite biomass, and could improve our perception of parasite subwebs in terms of host-parasite and predator-parasite links.

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.

Field evidence for non-host predator avoidance in a manipulated amphipod.

Manipulative parasites are known to alter the spatial distribution of their intermediate hosts in a way that enables trophic transmission to definitive hosts. However, field data on the ecological implications of such changes are lacking. In particular, little is known about the spatial coexistence between infected prey and dead-end predators after a parasite-induced habitat shift. Here, we used an Amphipoda (Gammarus roeseli)-Acanthocephala (Polymorphus minutus) association to investigate how infection with a manipulative parasite affects the predation risk by non-hosts within the invertebrate community. First, we collected invertebrates by sampling various natural habitats and calculated the distribution amplitude of amphipods according to their infection status. Infection with P. minutus significantly reduced the habitat breadth in G. roeseli, parasitised individuals being mainly found in floating materials whereas uninfected ones were widespread throughout the sampled habitats. Second, to test if these changes also affect the risk for P. minutus to be ingested by non-hosts, we estimated the predation risk experienced by G. roeseli within the macro-invertebrate community. The habitat overlap between potential invertebrate predators and G. roeseli showed that the spatial probability of encounter was lower for P. minutus-infected amphipods than for uninfected conspecifics. For the first time, to our knowledge, a study used ecological tools to bring field evidence for the spatial avoidance of dead-end predators in a manipulated amphipod.

Host manipulation of a freshwater crustacean (Gammarus roeseli) by an acanthocephalan parasite (Polymorphus minutus) in a biological invasion context.

Several gammarid species serve as intermediate hosts for the acanthocephalan parasite Polymorphus minutus. This parasite influences gammarid behaviour in order to favour transmission to its ultimate host, generally a bird. We investigated this host manipulation in Gammarus roeseli, a gammarid species introduced in France 150 years ago which now coexists with several exotic species from different origins. In the field, vertical distribution of G. roeseli revealed a higher proportion of infected individuals close to the water's surface and the size distribution of infected gammarids revealed predation pressure on infected individuals. However, under laboratory conditions both infected and non-infected individuals remained benthic. The addition of a second gammarid, Dikerogammarus villosus, to the experimental device involved a vertical displacement of infected G. roeseli towards the water's surface. Dikerogammarus villosus, originating from the Ponto-Caspian basin, can be considered as an aggressive predator. The substitution of D. villosus with Atyaephyra desmarestii, a planktivore decapod, did not alter the gammarids' distribution, with both infected and uninfected G. roeseli staying benthic. Thus, biotic interactions between D. villosus and G. roeseli represent selective pressure encouraging the expression of manipulated behaviour in infected amphipods. Through manipulation, P. minutus was found to increase the survival of infected G. roeseli when faced with non-host predators and to make it more vulnerable to predation by the parasite's definitive host.

Non-specific manipulation of gammarid behaviour by P. minutus parasite enhances their predation by definitive bird hosts.

Trophically-transmitted parasites often change the phenotype of their intermediate hosts in ways that increase their vulnerability to definitive hosts, hence favouring transmission. As a "collateral damage", manipulated hosts can also become easy prey for non-host predators that are dead ends for the parasite, and which are supposed to play no role in transmission strategies. Interestingly, infection with the acanthocephalan parasite Polymorphus minutus has been shown to reduce the vulnerability of its gammarid intermediate hosts to non-host predators, whose presence triggered the behavioural alterations expected to favour trophic transmission to bird definitive hosts. Whilst the behavioural response of infected gammarids to the presence of definitive hosts remains to be investigated, this suggests that trophic transmission might be promoted by non-host predation risk. We conducted microcosm experiments to test whether the behaviour of P. minutus-infected gammarids was specific to the type of predator (i.e. mallard as definitive host and fish as non-host), and mesocosm experiments to test whether trophic transmission to bird hosts was influenced by non-host predation risk. Based on the behaviours we investigated (predator avoidance, activity, geotaxis, conspecific attraction), we found no evidence for a specific fine-tuned response in infected gammarids, which behaved similarly whatever the type of predator (mallard or fish). During predation tests, fish predation risk did not influence the differential predation of mallards that over-consumed infected gammarids compared to uninfected individuals. Overall, our results bring support for a less sophisticated scenario of manipulation than previously expected, combining chronic behavioural alterations with phasic behavioural alterations triggered by the chemical and physical cues coming from any type of predator. Given the wide dispersal range of waterbirds (the definitive hosts of P. minutus), such a manipulation whose efficiency does not depend on the biotic context is likely to facilitate its trophic transmission in a wide range of aquatic environments.

Parasite-induced suppression of aggregation under predation risk in a freshwater amphipod: sociality of infected amphipods.

Recent findings suggest that grouping with conspecifics is part of the behavioural defences developed by amphipod crustaceans to face predation risk by fish. Amphipods commonly serve as intermediate hosts for trophically transmitted parasites. These parasites are known for their ability to alter intermediate host phenotype in a way that promotes predation by definitive hosts, where they reproduce. If aggregation in amphipods dilutes the risk to be preyed on by fish, then it may dilute the probability of transmission for the parasite using fish as definitive hosts. Using experimental infections, we tested whether infection with the fish acanthocephalan Pomphorhynchus laevis alters attraction to conspecifics in the amphipod intermediate host Gammarus pulex. We also measured G. pulex's activity and reaction to light to detect potential links between changes in aggregation and changes in other behaviours. The attraction to conspecifics in the presence of predator cue, a behaviour found in uninfected gammarids, was cancelled by the infection, while phototaxis was reversed and activity unchanged. We found no correlation between the three behaviours in infected amphipods, while activity and aggregation were negatively correlated in uninfected individuals after the detection of predation cue. The physiological causes and the adaptive value of aggregation suppression are discussed in the context of a multidimensional manipulation.

Host-manipulation by parasites with complex life cycles: adaptive or not?

The effect of host manipulation by parasites on trophic transmission to final hosts remains unclear. The transmission benefits gained by manipulative parasites are difficult to assess, and evidence for a causal link between manipulation and trophic transmission is missing. In addition, infected intermediate hosts can also be more vulnerable to predation by nonhosts, whereas recent theoretical advances indicate that the evolution of host manipulation does not require increased specificity in trophic transmission. We propose that a deeper consideration of the evolution of complex life cycles in helminth parasites might provide a different perspective on the evolution of host manipulation by parasites.

Effect of gender on physiological and behavioural responses of Gammarus roeseli (Crustacea Amphipoda) to salinity and temperature.

The importance of potentially interacting factors in organisms responses to a stress are often ignored or underestimated in ecotoxicology. In laboratory experiments we investigated how gender, temperature and age influence the behaviour and the physiology of the freshwater amphipod Gammarus roeseli under salinity stress. Our results revealed a significant higher sensitivity of females in survival, ventilation and ionoregulation whereas no inter-age differences were reported. Water temperature also exerted a significant effect in survival and ventilation of G. roeseli. Some of those factors appeared to interact significantly. This study provides evidence that gender can affect organisms responses to a stressor and consequently has to be considered while assessing a stress impact. We discussed the potential relationships between biological and behavioural responses.