René Gergs

Effects of zebra mussels on a native amphipod and the invasive Dikerogammarus villosus: the influence of biodeposition and structural complexity

Abstract In the last decades, zebra mussels (Dreissena polymorpha) have invaded many freshwater systems with severe consequences for entire communities. Most benthic macroinvertebrates, especially amphipods and chironomids, increase in abundance in the presence of zebra mussels. Increased structural complexity and an unknown biotic factor lead to this effect. Dreissena-associated factors that might influence populations of the native Gammarus roeselii and the invader Dikerogammarus villosus in Lake Constance, Central Europe, were investigated in laboratory experiments. These factors were: 1) increased structural complexity related to mussel shells, 2) Dreissena biodeposition, 3) chironomids, the presence of which is increased by biodeposited matter, and 4) Dreissena kairomones. In habitat-choice experiments, the native and omnivorous amphipod G. roeselii showed a preference for mussel shells with biodeposited material and for mussel shells with biodeposited material with chironomids, whereas the invasive and predatory amphipod D. villosus showed a preference only for mussel shells with biodeposited material with chironomids. In a kairomone y-maze experiment, both amphipods avoided zebra-mussel-conditioned lake water. These results indicate that habitat complexity and food availability, mediated directly or indirectly through biodeposited material, are the factors by which amphipod abundances are increased in the presence of Dreissena. Thus, biodeposited material can form an important new food resource, translocated from the pelagic zone to the benthos by zebra mussel filtration, and this biodeposited material might support a new detritus-based food web in the benthos.

Temporal variation in zebra mussel (Dreissena polymorpha) density structure the benthic food web and community composition on hard substrates in Lake Constance, Germany

Invasive species often influence existing biocenoses by altering their environment or facilitating the ecology of other species. Here we combined stable isotope analysis with quantitative benthic community sampling to investigate temporal variation in the influence of biodeposition of organic material (biodeposits) by the zebra mussel (Dreissena polymorpha) on the benthic food web in hard substrate habitats of Lake Constance, Germany. The accumulation of organic material excreted by zebra mussels (faeces and pseudofaeces) is hypothesised to implement a biodeposition based food web. By means of stable isotope analyses, we found that the feeding strategy of amphipods was dependent on the availability of zebra mussel biodeposits. The proportion of pelagic resources contributing to the diet (by δ13C) and trophic position (by δ15N) of amphipods were significantly and positively correlated to the production of zebra mussel biodeposits. Also, the benthic community in Lower Lake Constance showed a shift towards higher densities of the mayfly Caenis spp., Chironominae, and the caddisfly Ecnomus tenellus, which might act as links to higher trophic levels when more zebra mussel biodeposits were available. These results demonstrate that temporal variation in zebra mussel density, and thus in organic biodeposition, have a strong impact on the benthic communities and food web structure associated with hard substrates to the extent that there may be dependence on zebra mussel occurrence in such habitats in Lake Constance.

Review on environmental alterations propagating from aquatic to terrestrial ecosystems.

Terrestrial inputs into freshwater ecosystems are a classical field of environmental science. Resource fluxes (subsidy) from aquatic to terrestrial systems have been less studied, although they are of high ecological relevance particularly for the receiving ecosystem. These fluxes may, however, be impacted by anthropogenically driven alterations modifying structure and functioning of aquatic ecosystems. In this context, we reviewed the peer-reviewed literature for studies addressing the subsidy of terrestrial by aquatic ecosystems with special emphasis on the role that anthropogenic alterations play in this water-land coupling. Our analysis revealed a continuously increasing interest in the coupling of aquatic to terrestrial ecosystems between 1990 and 2014 (total: 661 studies), while the research domains focusing on abiotic (502 studies) and biotic (159 studies) processes are strongly separated. Approximately 35% (abiotic) and 25% (biotic) of the studies focused on the propagation of anthropogenic alterations from the aquatic to the terrestrial system. Among these studies, hydromorphological and hydrological alterations were predominantly assessed, whereas water pollution and invasive species were less frequently investigated. Less than 5% of these studies considered indirect effects in the terrestrial system e.g. via food web responses, as a result of anthropogenic alterations in aquatic ecosystems. Nonetheless, these very few publications indicate far-reaching consequences in the receiving terrestrial ecosystem. For example, bottom-up mediated responses via soil quality can cascade over plant communities up to the level of herbivorous arthropods, while top-down mediated responses via predatory spiders can cascade down to herbivorous arthropods and even plants. Overall, the current state of knowledge calls for an integrated assessment on how these interactions within terrestrial ecosystems are affected by propagation of aquatic ecosystem alterations. To fill these gaps, we propose a scientific framework, which considers abiotic and biotic aspects based on an interdisciplinary approach.

Is Dikerogammarus villosus (Crustacea, Gammaridae) a 'killer shrimp' in the River Rhine system?

Communities and food web structures of aquatic ecosystems can be strongly affected by the establishment of alien macroinvertebrate species. In many European waters, the invasion of the Ponto-Caspian amphipod Dikerogammarus villosus has led to displacement of other macroinvertebrates. Predation by D. villosus is often assumed to be the key driver of the displacement based on results of laboratory studies, but this has not been verified in the field. Here, we report our investigation of the relevance of D. villosus predation in the River Rhine system using both stable isotope analyses of δ13C and δ15N, and molecular analyses of D. villosus gut contents with group-specific primers aiming at macroinvertebrate prey taxa. Stable isotope analyses of D. villosus from ten sites showed mean δ15N values comparable to those of primary consumers. Overall, only approximately 1% of all tested primer/gut content combinations revealed DNA of the respective taxa. Both indicate minor importance of predation by D. villosus as a driver of the observed macroinvertebrate displacement. Conceivably, competitive strength due to opportunistic feeding, indicated by different niche widths between and a strong intraspecific variation of δ13C values of D. villosus within sites of our study, is much more important for its invasion success.

Invasive species as driving factors for the structure of benthic communities in Lake Constance, Germany

The composition of benthic macroinvertebrate communities is influenced by a variety of factors, including the introduction of invasive species. However, only few analyses of factors influencing benthic community structure exist, especially those including invasive species. Our aim was to examine the importance of biotic factors on spatial and temporal variations in the benthic community within one system (Lake Constance, Germany). We examined the dependence of benthic community structure on invasive species by non-metric multidimensional scaling and distance-based redundancy analysis based on Bray–Curtis similarities. The three significant biotic factors explained 40% of the community variability. The mayfly Centroptilum luteolum and the snail Potamopyrgus antipodarum were positively associated with the amount of Chara, whereas some caddisfly taxa and Chironomidae were positively associated with the density of Dreissena polymorpha, which is a pattern most likely caused by their different habitat preferences. Several benthic taxa especially indigenous gammarids and Asellus aquaticus tended to decline with increased densities of the invasive amphipod Dikerogammarus villosus. Furthermore, density of D. villosus explained 26% of the benthic variability, demonstrating the strong impact of this species. Overall, our study demonstrates the large impact of invasive species on the composition of benthic macroinvertebrates.

Different ammonia tolerances may facilitate spatial coexistence of Gammarus roeselii and the strong invader Dikerogammarus villosus

The introduction of invasive species that can replace native species is one of the most critical threats to the biodiversity of aquatic systems. Here we investigated the potential contribution of one factor to the coexistence of the indigenous amphipod Gammarus roeselii and the invasive amphipod Dikerogammarus villosus in the same ecosystem (Lake Constance) within different microhabitats. We quantitatively studied the influence of ambient ammonia concentrations on the distributions of the two amphipod species. We also assessed the ammonia tolerance ranges of both species in laboratory experiments by measuring mortality rate, precopula disruption, egg mortality, and microhabitat choice. The proportion of G. roeselii among the two amphipod species was significantly positively related to the ammonia concentration in the water, which indicated that the distribution of the invasive D. villosus was limited at high ammonia concentrations. Although the mortality rates of the two species did not significantly differ, G. roeselii was more tolerant to ammonia with regard to precopula disruption, egg mortality, and microhabitat choice. The effective ammonia concentrations that led to a significantly reduced direct reproductive success in D. villosus were within the range of the highest field concentrations measured, where only G. roeselii occurred. D. villosus may have a smaller range than the indigenous G. roeselii partially because of its lower tolerance to higher ammonia concentrations, which lead to reduced reproductive success. Beside other habitat parameters differences on ammonia tolerance between the two amphipods might allow their coexistence along a gradient of microhabitats in Lake Constance.

Effects of leaf litter and its fungal colonization on the diet of Limnomysis benedeni (Crustacea: Mysida)

The strong invasive freshwater mysid Limnomysis benedeni, a detritivorous–herbivorous feeder, has a preference for small food particles, but also feeds on leaf litter. Here, we tested whether leaf litter consumption by L. benedeni depends on the tree species and leaf conditioning (two types of physical and biological leaf conditioning). At the physical leaf conditioning, L. benedeni was fed with shortly leached or extensively leached leaves of five tree species in laboratory food assays. The mysid consumed shortly leached leaves of Copper Beech, Lombardy Poplar, Common Oak, and especially White Willow, and did not feed on shortly leached Black Alder leaves. The consumption of extensively leached leaves by L. benedeni did not depend on the tree species. Overall, 74% of the variation of the leaf consumption by L. benedeni was explained by the significant interaction of the factors carbon content and polyphenol content of the leaves, caused the feeding strategy of L. benedeni. For the biological leaf conditioning, the mysids consumed to a high degree naturally conditioned leaves, followed by leaves colonized by one of three fungi, but oomycete-colonized leaf litter and autoclaved leaves were consumed at similar low levels. Our results indicate that L. benedeni feeds on different types of conditioned leaves to different extents, and therefore may affect leaf litter degradation in many invaded freshwaters.

Characterization of the first twelve microsatellite loci for the amphipod Gammarus roeselii (Crustacea: Amphipoda)

We characterised the first twelve microsatellites for the freshwater amphipod Gammarus roeselii. Overall 47 individuals from two populations were analyzed from the River Rhine system located in Southern and Middle Germany. Allele numbers range from 2 to 8 and observed heterozygosities vary between the values 0.08 and 0.86. From the two investigated populations, two loci were found to be significant departure from Hardy–Weinberg equilibrium, respectively. The reported microsatellite markers will facilitate investigations on the population genetic structure of G. roeselii, which is recently repressed by invasive amphipod species in the River Rhine system.

Establishment of group-specific PCR primers for the identification of freshwater macroinvertebrates

Analysis of the diversity of the species communities and food webs is essential for a better understanding of the ecosystem and PCR based methods are often used for taxonomic identifications. Here, we describe the development of 21 group-specific primers to amplify short sections of genes encoding nuclear ribosomal DNA from several freshwater invertebrate taxa as a potential approach to identify the prey of invertebrate predators, specified on 130 taxa of freshwater macroinvertebrates. Our primers cover a broad range of aquatic invertebrate taxa and may provide a useful tool for detecting target groups in mixed-DNA samples, making them also suitable for prey species identification in dietary samples.

Embryonic development time of the freshwater mysid Limnomysis benedeni Czerniavsky as a function of water temperature

The numbers of alien species in freshwater systems and their detrimental impacts on the stability of ecosystems and global species diversity are increasing. To predict and assess such impacts, a thorough knowledge of the autecology and life cycle of the alien species is required. Limnomysis benedeni is common and one of the most invasive mysids in Europe. Here we show a clear dependency of the development time of the brood of L. benedeni on water temperature. In laboratory experiments (one in spring 2008 and two in 2009, in spring and summer) under controlled conditions, we determined embryonic development times and the probability of survival of the females and juveniles at water temperatures ranging from 4 to 25°C. At 6.5 and 25°C, the probability of survival of both the females and the larvae was lower than at 10, 15, or 20°C. Since the development time is one of the key characteristics of the life cycle and is therefore necessary to calculate, for example, birth and mortality rates, we determined an equation for the development time as a function of the water temperature. This information will be useful to understand the distribution potential of this invasive species.