Freshwater Isopod Asellus Aquaticus Research Articles

Island and Rensch’s rules do not apply to cave vs. surface populations of Asellus aquaticus

Body size is a trait of fundamental ecological and evolutionary importance that is often different between males and females (sexual size dimorphism; SSD). The island rule predicts that small-bodied species tend to evolve larger following a release from interspecific competition and predation in insular environments. According to Rensch’s rule, male body size relative to female body size increases with increasing mean body size. This allometric body size – SSD scaling is explained by male-driven body size evolution. These ecogeographical rules are rarely tested within species, and has not been addressed in a cave–surface context, even though caves represent insular environments (small and isolated with simple communities). By analyzing six cave and nine surface populations of the widespread, primarily surface-dwelling freshwater isopod Asellus aquaticus with male-biased SSD, we tested whether cave populations evolved larger and showed higher SSD than the surface populations. We found extensive between-population variation in body size (maximum divergence being 74%) and SSD (males being 15%–50% larger than females). However, habitat type did not explain the body size and SSD variation and we could not reject isometry in the male–female body size relationship. Hence, we found no support for the island or Rensch’s rules. We conclude that local selective forces stemming from environmental factors other than island vs. mainland or the general surface vs. cave characteristics are responsible for the reported population variation.

Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus).

Human activity is a major driver of ecological and evolutionary change in wild populations and can have diverse effects on eukaryotic organisms as well as on environmental and host-associated microbial communities. Although host-microbiome interactions can be a major determinant of host fitness, few studies consider the joint responses of hosts and their microbiomes to anthropogenic changes. In freshwater ecosystems, wastewater is a widespread anthropogenic stressor that represents a multifarious environmental perturbation. Here, we experimentally tested the impact of treated wastewater on a keystone host (the freshwater isopod Asellus aquaticus) and its gut microbiome. We used a semi-natural flume experiment, in combination with 16S rRNA amplicon sequencing, to assess how different concentrations (0%, 30%, and 80%) of nonfiltered wastewater (i.e. with chemical toxicants, nutrients, organic particles, and microbes) versus ultrafiltered wastewater (i.e. only dissolved pollutants and nutrients) affected host survival, growth, and food consumption as well as mid- and hindgut bacterial community composition and diversity. Our results show that while host survival was not affected by the treatments, host growth increased and host feeding rate decreased with nonfiltered wastewater - potentially indicating that A. aquaticus fed on organic matter and microbes available in nonfiltered wastewater. Furthermore, even though the midgut microbiome (diversity and composition) was not affected by any of our treatments, nonfiltered wastewater influenced bacterial composition (but not diversity) in the hindgut. Ultrafiltered wastewater, on the other hand, affected both community composition and bacterial diversity in the hindgut, an effect that in our system differed between sexes. While the functional consequences of microbiome changes and their sex specificity are yet to be tested, our results indicate that different components of multifactorial stressors (i.e. different constituents of wastewater) can affect hosts and their microbiome in distinct (even opposing) manners and have a substantial impact on eco-evolutionary responses to anthropogenic stressors.

Individual level microbial communities in the digestive system of the freshwater isopod Asellus aquaticus: Complex, robust and prospective.

The freshwater isopod Asellus aquaticus is an important decomposer of leaf detritus, and its diverse gut microbiome has been depicted as key contributors in lignocellulose degradation as of terrestrial isopods. However, it is not clear whether the individual-level microbiome profiles in the isopod digestive system across different habitats match the implied robust digestion function of the microbiome. Here, we described the bacterial diversity and abundance in the digestive system (hindgut and caeca) of multiple A. aquaticus individuals from two contrasting freshwater habitats. Individuals from a lake and a stream harboured distinct microbiomes, indicating a strong link between the host-associated microbiome and microbes inhabiting the environments. While faeces likely reflected the variations in environmental microbial communities included in the diet, the microbial communities also substantially differed in the hindgut and caeca. Microbes closely related to lignocellulose degradation are found consistently more enriched in the hindgut in each individual. Caeca often associated with taxa implicated in endosymbiotic/parasitic roles (Mycoplasmatales and Rickettsiales), highlighting a complex host-parasite-microbiome interaction. The results highlight the lability of the A. aquaticus microbiome supporting the different functions of the two digestive organs, which may confer particular advantages in freshwater environments characterized by seasonally fluctuating and spatially disparate resource availability.

Sex-dependent increase of movement activity in the freshwater isopod Asellus aquaticus following adaptation to a predator-free cave habitat.

Populations experiencing negligible predation pressure are expected to evolve higher behavioral activity. However, when sexes have different expected benefits from high activity, the adaptive shift is expected to be sex-specific. Here, we compared movement activity of one cave (lack of predation) and three adjacent surface (high and diverse predation) populations of Asellus aquaticus, a freshwater isopod known for its independent colonization of several caves across Europe. We predicted 1) higher activity in cave than in surface populations, with 2) the difference being more pronounced in males as they are known for active mate searching behavior, while females are not. Activity was assessed both in the presence and absence of light. Our results supported both predictions: movement activity was higher in the cave than in the surface populations, particularly in males. Relaxed predation pressure in the cave-adapted population is most likely the main selective factor behind increased behavioral activity, but we also showed that the extent of increase is sex-specific.

Building on 150 Years of Knowledge: The Freshwater Isopod Asellus aquaticus as an Integrative Eco-Evolutionary Model System

Interactions between organisms and their environments are central to how biological diversity arises and how natural populations and ecosystems respond to environmental change. These interactions involve processes by which phenotypes are affected by or respond to external conditions (e.g., via phenotypic plasticity or natural selection) as well as processes by which organisms reciprocally interact with the environment (e.g., via eco-evolutionary feedbacks). Organism-environment interactions can be highly dynamic and operate on different hierarchical levels, from genes and phenotypes to populations, communities, and ecosystems. Therefore, the study of organism-environment interactions requires integrative approaches and model systems that are suitable for studies across different hierarchical levels. Here, we introduce the freshwater isopodAsellus aquaticus, a keystone species and an emerging invertebrate model system, as a prime candidate to address fundamental questions in ecology and evolution, and the interfaces therein. We review relevant fields of research that have usedA. aquaticusand draft a set of specific scientific questions that can be answered using this species. Specifically, we propose that studies onA. aquaticuscan help understanding (i) the influence of host-microbiome interactions on organismal and ecosystem function, (ii) the relevance of biotic interactions in ecosystem processes, and (iii) how ecological conditions and evolutionary forces facilitate phenotypic diversification.

Higher mean and fluctuating temperatures jointly determine the impact of the pesticide chlorpyrifos on the growth rate and leaf consumption of a freshwater isopod

There is growing evidence that both increases in mean temperature and the widespread daily temperature fluctuations (DTF) may increase pesticide toxicity. Nevertheless, the likely more stressful, realistic combination of the two warming-related stressors has rarely been considered in ecotoxicology. Moreover, we have little knowledge on whether these stressor combinations could impair ecosystem functioning. We examined the effect of the pesticide chlorpyrifos under an increased mean temperature (+4 °C, from 18 °C to 22 °C) and in the presence of DTF (constant and 8 °C) on two life-history traits (mortality and growth rate) and one ecologically important behavioural trait (feeding rate) in the freshwater isopod Asellus aquaticus. The chlorpyrifos concentration used, 0.2 μg/L, did not cause mortality in any thermal condition, nor did it cause sublethal effects at the mean temperature of 18 °C. A key finding was that growth rate was strongly reduced by the pesticide only under the combination of both a higher mean temperature and DTF, highlighting the importance of testing toxicity under this realistic thermal scenario. The leaf consumption of chlorpyrifos-exposed isopods increased at the higher mean temperature when this was kept constant, however, it lowered again towards control levels when DTF was induced, thereby contributing to the growth reduction at this most stressful condition. These alterations of growth and leaf degradation rates may impact nutrient recycling, a key ecosystem function. Our results highlight the importance of integrating both increases in mean temperature and in DTF to improve current and future ecological risk assessment of pesticides.

Is foraging innovation lost following colonization of a less variable environment? A case study in surface- vs. cave-dwelling Asellus aquaticus.

Behavioral innovation is a key process for successful colonization of new habitat types. However, it is costly due to the necessary cognitive and neural demands and typically connected to ecological generalism. Therefore, loss of behavioral innovativeness is predicted following colonization of new, simple, and invariable environments. We tested this prediction by studying foraging innovativeness in the freshwater isopod Asellus aquaticus. We sampled its populations along the route of colonizing a thermokarstic water‐filled cave (simple, stable habitat with only bacterial mats as food) from surface habitats (variable environment, wide variety of food). The studied cave population separated from the surface populations at least 60,000 years ago. Animals were tested both with familiar and novel food types (cave food: bacterial mats; surface food: decaying leaves). Irrespective of food type, cave individuals were more likely to feed than surface individuals. Further, animals from all populations fed longer on leaves than on bacteria, even though leaves were novel for the cave animals. Our results support that cave A. aquaticus did not lose the ability to use the ancestral (surface) food type after adapting to a simple, stable, and highly specialized habitat.

No need to hide in caves: shelter-seeking behavior of surface and cave ecomorphs of Asellus aquaticus (Isopoda: Crustacea)

Shelter-seeking is a vital behavior for stress reduction and survival in a range of animals. It comes at the cost of reduced foraging, mate finding, dispersal and territoriality, and is expected to reflect the trade-off between fitness costs and benefits. One way to test this hypothesis is to compare shelter-seeking behavior in surface habitats and in caves where external threat factors are largely reduced. We did so using the freshwater isopod Asellus aquaticus from the Postojna-Planina Cave System and surrounding surface waters. Animals from two distinct, replicated pairs of surface and cave populations were individually offered a choice between shelter and open area. The thigmotatic sensation of a transparent plastic plate was the only stimulus that could trigger the sheltering behavior. Video recordings showed a clear reduction of shelter-seeking behavior in the cave ecomorph in one population pair (Pivka). There were no changes in the other population pair (Rak), where the behavioral response had a much higher variance. Our results were partly in agreement with the hypothesis that shelter-seeking behavior should be selected against in an environment with reduced external threats. It is nevertheless too early for generalizations as the results in the second population pair were inconclusive. Additionally, we showed that for benthic walkers like A. aquaticus the use of rough substrate is crucial to obtain unbiased behavioral responses. Results of some previous studies using smooth glass or plastic substratum could be affected by unnatural behavior of animals constantly trying to find firm contact with the ground.

The impact of temperature on metal mixture stress: Sublethal effects on the freshwater isopod Asellus aquaticus

Chemical and natural factors have been demonstrated to interact and potentially change the toxicity of the individual stressors. Yet, while there exists a multitude of papers studying the temperature-dependent toxicity of single chemicals, little research exists on the impact of temperature on chemical mixtures. This paper investigates the effect of temperature on environmentally-relevant mixtures of Cd, Cu and Pb. We linked the effects on respiration, growth, feeding rate and activity of Asellus aquaticus to the free ion activities, as a measure for the bioavailability of the metals, and the body concentrations. We observed interactions of temperature and metal body concentrations on all sublethal endpoints, except activity. Mixture effects on accumulation and feeding rate were observed as well and even an interaction between metal body burden, mixture and temperature treatment was revealed for the feeding rate of Pb exposed isopods. This research adds to a growing body of evidence that the current chemical-based monitoring is insufficient to estimate chemical toxicity in aquatic ecosystems and must, therefore, be complemented with effect-based tools.

Combined effects of metal mixtures and predator stress on the freshwater isopod Asellus aquaticus

Biotic stressors have been demonstrated to change the toxicity of pollutants. While the combined effects of predator cues and pesticides are well documented, the interaction of predator stress with metals is a topic that has remained largely unexplored. In this laboratory experiment, the freshwater isopod Asellus aquaticus is exposed to predator cues and metal mixtures of Cd, Cu and Pb. We examined the effects on growth, respiration and, as behavioral parameters, feeding rate and activity. These were linked to the free ion activities (FIAs) in the water and the metal body concentrations. The findings reveal that Cu accumulation significantly influenced the growth rate, the feeding rate and the activity of isopods exposed to predator stress. Furthermore, we found a concentration-dependent interaction of the Cd + Pb mixtures on the feeding rate and a lower feeding rate for Cd and Pb predator exposed asellids. As several interactions were found between metals and predator stress, it demonstrates the importance of investigating how organisms and whole ecosystems respond to multiple stressors. A better understanding of these interactions will undoubtedly improve risk assessment and management.

Reproduction in the freshwater crustacean Asellus aquaticus along a gradient of radionuclide contamination at Chernobyl

Nuclear accidents such as Chernobyl and Fukushima have led to contamination of the environment that will persist for many years. The consequences of chronic low-dose radiation exposure for non-human organisms inhabiting contaminated environments remain unclear. In radioecology, crustaceans are important model organisms for the development of environmental radioprotection. Previous laboratory studies have demonstrated deleterious effects of radiation exposure on crustacean reproduction. However, no studies have documented the effects of chronic radiation exposure on the reproduction of natural crustacean populations. Based on data from laboratory exposures, we hypothesised that populations of the freshwater isopod Asellus aquaticus exposed to radiation for thirty years at Chernobyl would display reduced reproductive output and altered timing of reproduction. To test this hypothesis, A. aquaticus was collected from six lakes at Chernobyl over two years with total dose rates ranging from 0.06–27.1μGy/h. No significant differences in the fecundity, mass of broods or proportion of reproducing female A. aquaticus were recorded. Significant differences in the body mass of gravid females were recorded suggesting different timings of reproduction, however this was not related to radiation contamination. No significant effect of a range of environmental parameters on A. aquaticus reproduction was recorded. Our data suggests current dose rates at Chernobyl are not causing discernible effects on the reproductive output of A. aquaticus. This study is the first to assess the effects of chronic low-dose radiation exposure on the reproductive output of an aquatic invertebrate at Chernobyl. These findings are consistent with proposed radiological protection benchmarks for the maintenance of wildlife populations and will assist in management of environments impacted by radiation.

How lethal concentration changes over time: Toxicity of cadmium, copper, and lead to the freshwater isopod Asellus aquaticus.

Metal pollution is a serious threat to environmental health. While the aquatic isopod Asellus aquaticus L. (Isopoda) is an important decomposer of freshwater ecosystems, very little research has reported its long-term or incipient lethal concentrations for metals. Moreover, the lethal concentrations at a certain percentage (LCxs) that can be found in the literature are often based on unmeasured concentrations, which could lead to a severe underestimation of the actual toxicity. In the present exploratory study, the 1-, 4-, 7-, and 14-d LC10, LC20, and LC50 values of copper, cadmium, and lead for adult A. aquaticus were determined. The LCx values were calculated using the nominal concentrations, the effective concentrations, and the free ion activities. Incipient lethal values were determined as well. In general, surprisingly lower lethal concentrations were found than in other studies. Furthermore, the present study shows that lethal concentrations based on free ion activities were generally much lower than nominal and effective concentrations. Although almost all LC values were higher than the environmental quality standards (EQS), the Cu 14-d LC10 and several (incipient) Pb LC10 and LC20 values, all calculated with free ion activities, were lower than the EQS. We conclude that lethal or effective concentrations based on free ion activities provide a more realistic view, which is vital for environmental policy making. Environ Toxicol Chem 2017;36:2849-2854. © 2017 SETAC.

Toxic and endocrine disrupting effects of wastewater treatment plant influents and effluents on a freshwater isopod Asellus aquaticus (Isopoda, Crustacea)

In the present study a biological “in vivo” assay, with freshwater isopod Asellus aquaticus, was used to define and evaluate the potential impact of the wastewater treatment plant (WWTP) wastewaters on local wildlife. Samples of both untreated and mechanically and biologically treated WWTP wastewater, were tested in the presence and absence of the formulated sediment for their lethal and sublethal effects. Chronic exposures to wastewater samples caused concentration dependent reduced locomotion, body pigmentation and molting frequency in exposed organisms. The observed effects indicate the overall toxicity and endocrine disruption of the wastewater samples. In contrast stimulations of the feeding rate and growth rate of the test organisms during the chronic exposure to sublethal levels of wastewater samples were observed, indicating an improvement in nutritional quality of the wastewater. The most sensitive exposure endpoint was molting frequency of tested organisms, which indicated the presence of estrogenically active endocrine disrupting compounds (EDCs). Raw wastewater caused up to 42% molting frequency reduction of exposed A. aquaticus when exposed to five times diluted untreated wastewater sample, while undiluted treated wastewater caused a 61% molting frequency reduction. The presence of estrogenically active compounds in the wastewater was confirmed with the yeast estrogen screen assay (YES test), which assigned the highest estrogenic activity to a mechanically and biologically treated wastewater sample, and lower estrogenic activity to all other tested samples. The importance of presence of the formulated sediment was determined, as it lessened the effects of all WWTP wastewater samples in all observed exposures.

Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment

Behavioural syndromes, that is correlated behaviours, may be a result from adaptive correlational selection, but in a new environmental setting, the trait correlation might act as an evolutionary constraint. However, knowledge about the quantitative genetic basis of behavioural syndromes, and the stability and evolvability of genetic correlations under different ecological conditions, is limited. We investigated the quantitative genetic basis of correlated behaviours in the freshwater isopod Asellus aquaticus. In some Swedish lakes, A. aquaticus has recently colonized a novel habitat and diverged into two ecotypes, presumably due to habitat-specific selection from predation. Using a common garden approach and animal model analyses, we estimated quantitative genetic parameters for behavioural traits and compared the genetic architecture between the ecotypes. We report that the genetic covariance structure of the behavioural traits has been altered in the novel ecotype, demonstrating divergence in behavioural correlations. Thus, our study confirms that genetic correlations behind behaviours can change rapidly in response to novel selective environments.

Evidence of Increased Anthropogenic Emissions of Platinum in Coastal Systems from Time-Series Analysis of Mussels Samples (1991-2011)

Evidence of Increased Anthropogenic Emissions of Platinum in Coastal Systems from Time-Series Analysis of Mussels Samples (1991-2011)

Predator faunas past and present: quantifying the influence of waterborne cues in divergent ecotypes of the isopod Asellus aquaticus

Waterborne chemical cues are an important source of information for many aquatic organisms, in particular when assessing the current risk of predation. The ability to use chemical cues to detect and respond to potential predators before an actual encounter can improve prey chances of survival. We investigated predator recognition and the impact of chemical cues on predator avoidance in the freshwater isopod Asellus aquaticus. This isopod has recently colonised a novel habitat and diverged into two distinct ecotypes, which encounter different predator communities. Using laboratory-based choice experiments, we have quantified behavioural responses to chemical cues from predators typical of the two predator communities (larval dragonflies in the ancestral habitat, perch in the newly colonised habitat) in wild-caught and lab-reared Asellus of the two ecotypes. Individuals with prior experience of predators showed strong predator avoidance to cues from both predator types. Both ecotypes showed similar antipredator responses, but sexes differed in terms of threat-sensitive responses with males avoiding areas containing predator cues to a larger extent than females. Overall, chemical cues from fish elicited stronger predator avoidance than cues from larval dragonflies. Our results indicate that in these isopods, prior exposure to predators is needed to develop antipredator behaviour based on waterborne cues. Furthermore, the results emphasise the need to analyse predator avoidance in relation to waterborne cues in a sex-specific context, because of potential differences between males and females in terms of vulnerability and life history strategies.

Changes in behavioural trait integration following rapid ecotype divergence in an aquatic isopod

Colonization of new habitats can relax selection pressures, and traits or trait combinations no longer selected for might become reduced or lost. We investigated behavioural differentiation and behavioural trait integration in the freshwater isopod Asellus aquaticus. This isopod has recently colonized a novel habitat and diverged into two ecotypes which encounter different predator faunas. We investigated sex-specific behavioural differences and phenotypic integration in three behavioural assays: (i) time to emerge (TE) from a shelter, (ii) activity and (iii) escape behaviour. General activity and escape behaviour differed between ecotypes. Furthermore, general activity and TE differed between sexes. Behavioural traits were more frequently correlated in the ancestral habitat, and phenotypic integration tended to be higher in this habitat as well. Our study suggests that different predator types, but also other ecological factors such as habitat matrices and population densities, might explain the differences in behavioural integration in these ecotypes.

Bacterial symbionts in the hepatopancreas of isopods: diversity and environmental transmission

The midgut glands (hepatopancreas) of terrestrial isopods contain bacterial symbionts. We analysed the phylogenetic diversity of hepatopancreatic bacteria in isopod species from various suborders colonizing marine, semiterrestrial, terrestrial and freshwater habitats. Hepatopancreatic bacteria were absent in the marine isopod Idotea balthica (Valvifera). The symbiotic bacteria present in the midgut glands of the freshwater isopod Asellus aquaticus (Asellota) were closely related to members of the proteobacterial genera Rhodobacter, Burkholderia, Aeromonas or Rickettsiella, but differed markedly between populations. By contrast, species of the suborder Oniscidea were consistently colonized by the same phylotypes of hepatopancreatic bacteria. While symbionts in the semiterrestrial isopod Ligia oceanica (Oniscidea) were close relatives of Pseudomonas sp. (Gammaproteobacteria), individuals of the terrestrial isopod Oniscus asellus (Oniscidea) harboured either 'Candidatus Hepatoplasma crinochetorum' (Mollicutes) or 'Candidatus Hepatincola porcellionum' (Rickettsiales), previously described as symbionts of another terrestrial isopod, Porcellio scaber. These two uncultivated bacterial taxa were consistently present in each population of six and three different species of terrestrial isopods, respectively, collected in different geographical locations. However, infection rates of individuals within a population ranged between 10% and 100%, rendering vertical transmission unlikely. Rather, feeding experiments suggest that 'Candidatus Hepatoplasma crinochetorum' is environmentally transmitted to the progeny.

Is size-assortative mating important for rapid pigment differentiation in a freshwater isopod?

Identifying mechanisms behind assortative mating is central to the understanding of ecological divergence and speciation. Recent studies show that populations of the freshwater isopod Asellus aquaticus can rapidly become locally differentiated when submerged Chara vegetation expands in lakes. In the novel Chara habitat, isopods have become lighter pigmented and smaller than in ancestral reed stands. In this study, we used a laboratory multiple-choice experiment to investigate assortative mating as a possible prezygotic reproductive barrier between Chara and reed isopods. Mating was assortative when Chara isopods were experimentally mixed with isopods from an adjacent reed site with large-size individuals, suggesting a partial prezygotic reproductive barrier. No deviation from random mating could, however, be detected when Chara isopods were mixed with smaller sized isopods from another reed site. In both experiments, assortative mating was apparently based on size, as Chara isopods were larger and reed isopods smaller in mixed pairs than in assortative pairs. Pigmentation did not have any clear influence on mating. We suggest that divergence in pigmentation evolved through natural selection in conjunction with size-assortative mating indirectly causing assortative mating between Chara and reed isopods. Size-assortative mating is likely a by-product of natural selection, but its importance may hypothetically be transient, if selection erodes the correlation between pigmentation and size over time.

Locally differentiated cryptic pigmentation in the freshwater isopod Asellus aquaticus

A repeated pattern of background colour matching in animals is an indication that pigmentation may be cryptic. Here, we examine the relationship between pigmentation of the freshwater isopod Asellus aquaticus and background darkness in 29 lakes, wetlands and ponds in Southern Sweden. The results show that Asellus pigmentation was correlated with substrate darkness across all localities. In seven localities, in which two contrasting substrate types were noted, Asellus populations were differentiated with respect to pigmentation. These findings thus provide phenomenological support for cryptic pigmentation in Asellus. Pigmentation generally increased with body size, but the relationship between pigmentation and size differed among localities, possibly as a result of differences in correlational selection on pigmentation and size. Selection thus appears to have resulted in local differentiation over a small spatial scale, even within lakes and wetlands. This differentiation is a likely cause behind elevated phenotype variation noted in localities with two substrate types, suggesting that habitat heterogeneity promotes genetic diversity.