Alien Gammarid Research Articles

Resilient amphipods: Gammarid predatory behaviour is unaffected by microplastic exposure and deoxygenation

Microplastics are a ubiquitous and persistent form of pollution globally, with impacts cascading from the cellular to ecosystem level. However, there is a paucity in understanding interactions between microplastic pollution with other environmental stressors, and how these could affect ecological functions and services. Freshwater ecosystems are subject to microplastic input from anthropogenic activities (eg. wastewater), but are also simultaneously exposed to many other stressors, particularly reduced dissolved oxygen availability associated with climatic warming and pollutants, as well as biological invasions. Here, we employ the comparative functional response method (CFR; quantifying and comparing organism resource use as a function of resource density) to investigate the relative impact of different microplastic concentrations and oxygen regimes on predatory trophic interactions of a native and an invasive alien gammarid (Gammarus duebeni and Gammarus pulex). No significant effect on trophic interaction strengths was found from very high concentrations of microplastics (200 mp/L and 200,000 mp/L) or low oxygen (40 %) stressors on either species. Additionally, both gammarid species exhibited significant Type II functional responses, with attack rates and handling times not significantly affected by microplastics, oxygen or gammarid invasion status. Thus, both species showed resistance to the simultaneous effects of microplastics and deoxygenation in terms of feeding behaviour. Based on these findings, we suggest that the trophic function, in terms of predation rate, of Gammarus spp. may be sustained under acute bouts of microplastic pollution even in poorly‑oxygenated waters. This is the first study to investigate microplastic and deoxygenation interactions and to find no evidence for an interaction on a key invertebrate ecosystem service. We argue that our CFR methods can help understand and predict the future ecological ramifications of microplastics and other stressors across taxa and habitats.

Salinity tolerance and geographical origin predict global alien amphipod invasions

Invasive alien species are driving global biodiversity loss, compromising ecosystem function and service provision, and human, animal and plant health. Habitat characteristics and geographical origin may predict invasion success, and in aquatic environments could be mediated principally by salinity tolerance. Crustacean invaders are causing global problems and we urgently require better predictive power of their invasiveness. Here, we compiled global aquatic gammarid (Crustacea: Amphipoda: Gammaroidea) diversity and examined their salinity tolerances and regions of origin to test whether these factors predict invasion success. Across 918 aquatic species within this superfamily, relatively few gammarids (n = 27, 3%) were reported as aliens, despite extensive invasion opportunities and high numbers of published studies on amphipod invasions. However, reported alien species were disproportionately salt-tolerant (i.e. 32% of brackish-water species), with significantly lower proportions of aliens originating from freshwater and marine environments (both 1%). Alien gammarids also significantly disproportionally originated from the Ponto-Caspian (20% of these taxa) when compared with all ‘other' grouped regions (1%), and principally invaded Eurasian waters, with translocations of salt-tolerant taxa to freshwaters being pervasive. This suggests habitat characteristics, alongside regional contexts, help predict invasibility. In particular, broad environmental tolerances to harsh environments and associated evolutionary history probably promote success of aliens globally.

Isolation and characterization of eleven novel microsatellite markers for fine-scale population genetic analyses of Gammarus pulex (Crustacea: Amphipoda).

The freshwater amphipod species Gammarus pulex (Linnaeus, 1758) is widespread across Europe and Asia and is able to live in a broad range of environmental conditions. Yet, it is of great interest to which degree it is able to tolerate and adapt to the current rapid anthropogenic environmental changes affecting its habitat, such as pollution, changes in river morphology, and invasions of alien gammarid species. Microsatellite primers for genetic population studies with G. pulex have been developed but due to the existence of several genetically different lineages within the species, the application of these primers is not always successful. In order to investigate the impacts of anthropogenic environmental changes on the spatio-genetic patterns of G. pulex lineage E in streams in the Saale river catchment in Germany, we designed eleven novel polymorphic microsatellites for this lineage using a high-throughput sequencing approach. These microsatellites enabled highly specific characterization of three closely related populations. The results show genetically distinct populations reflected by both a principal coordinates analysis and an analysis of molecular variance. Several of the newly designed microsatellite primers also enabled successful cross-amplification of the respective microsatellites in specimens of G. pulex lineage C, while only two microsatellites were amplified successfully and showed polymorphisms for all of the analyzed specimens of G. fossarum Koch, 1836. The microsatellites identified here are suitable for future assessments of micro-evolutionary dynamics of G. pulex from central Germany.

Size structure and body condition of Ponto-Caspian gammarids in the Vistula estuary (Poland)

Abstract Over the past few decades, Ponto-Caspian gammarids Pontogammarus robustoides, Obesogammarus crassus and Dikerogammarus haemobaphes have colonized the European inland and coastal brackish waters. Previous experimental studies of P. robustoides, O. crassus and D. haemobaphes indicated that the salinity optimum for the species is about 7 PSU. We examined whether salinities below 5 PSU in the Vistula estuary – the Vistula Lagoon and the Vistula Delta, create a favorable environment and have a positive effect on Ponto-Caspian gammarids. The objective of this work was to determine the population parameters (size structure) and biological indicators (condition) of the studied gammarid species at a low salinity level. Length–weight relationships can be considered as their body condition in the environment. These relationships were calculated for each gammarid species according to the exponential equation y = axb, where: y – wet weight, x – total length, a – intercept, b – slope. The results clearly show responses of Ponto-Caspian gammarids to the low salinity habitat and indicate that such environment provides excellent conditions. The results of analysis show that the condition of gammarids is good. The optimal strategy of the examined alien gammarids may help them to maintain a strong competitive position in the environment and affect the colonization process in non-native waters with low salinity.

Competition for shelter sites: Testing a possible mechanism for gammarid species displacements

Invasions of alien gammarid species have led to reduced abundance of many native gammarid species and earlier gammarid invaders. Intra-guild predation (IGP) has been suggested as the main mechanism causing such species displacements. This study elucidates a mechanism for species displacement that is based on competition for shelter, viz. species excluding each other from a shelter place. Preferences of Dikerogammarus villosus and Gammarus roeselii for shelter space were studied in laboratory experiments. In contrast with night conditions both species showed a strong preference for shelter sites under daytime conditions so that all experiments were carried out under permanent light conditions. Single individuals of D. villosus sheltered more than those of G. roeselii. Intraspecific competition experiments with different size classes and sexes showed that in contrast with D. villosus, the size class had a significant effect on the mean sheltering proportion of individuals of G. roeselii. When both species were brought together in a basin with a shelter site to test interspecific competition, individuals of G. roeselii were actively pushed out of their shelters within 24h, while D. villosus showed no change in shelter. This led to a significantly increased predation risk for G. roeselii, which was confirmed in an experiment in which a benthic fish was added. IGP only manifested itself after 48h, indicating that competition for shelter preceded IGP. When shelter opportunities are in short supply, shelter exclusion may be one of the initial mechanisms for gammarid species displacements.

Fate of Lamprodrilus isoporus (Oligochaeta: Lumbriculidae) in eutrophic lakes

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Evaluation and comparison of data-driven and knowledge-supported Bayesian Belief Networks to assess the habitat suitability for alien macroinvertebrates

Defining habitats vulnerable to invasion is important to support the management of invasive alien species (IAS). We developed and applied data-driven and knowledge-supported data-driven Bayesian Belief Networks (BBNs) to assess the habitat suitability for alien gammarids. Data-driven model development using a Naive Bayes classifier and equal width discretization resulted in a habitat suitability model with a moderate technical performance (CCI = 68% K = 0.33). Although the structure of the knowledge-supported model yielded important ecological insight between environmental and biotic variables and the occurrence of alien gammarids, the performance was lower (CCI = 60% K = 0.19) compared to the purely data-driven model. The lower predictive performance of the knowledge-supported model may be attributed to its higher model complexity. Our study shows that BBNs can support the management of IAS as they are visually appealing, transparent models that facilitate integration of monitoring data and expert knowledge.

Trophic interactions between native and alien palaemonid prawns and an alien gammarid in a brackish water ecosystem

Macroalgae are an important habitat for small mobile invertebrates such as gammarid amphipods and palaemonid prawns. Gammarid amphipods are important grazers of micro- and macroalgae whereas palaemonid prawns are feeding on macroalgae and small aquatic invertebrates including gammarids. Recently the invasive palaemonid prawn Palaemon elegans established in the Baltic Sea. As P. elegans occurs within the same habitats as the native Palaemon adspersus, it is expected that this invasion modifies the existing trophic interactions. To address this question, we experimentally investigated the feeding of the native P. adspersus and the invasive P. elegans on the benthic macroalga Cladophora glomerata and on the invasive gammarid amphipod Gammarus tigrinus. In the course of the experiment neither G. tigrinus nor Palaemon spp. had effects on filamentous macroalgae. The presence of prawns drastically increased the mortality of amphipods with no difference in the feeding efficiency between the two prawn species. To conclude, the alien prawn does not add an extra function to the trophic system of the coastal ecosystem of the Baltic Sea. Nevertheless, due to its progressively increasing densities and wide habitat range, P. elegans is expected to exert stronger predation pressure on gammarid amphipods as compared to P. adspersus alone.

Expansion of alien gammarids in the Vistula Lagoon and the Vistula Delta (Poland)

Amphipod crustaceans belong to the most successful invaders of aquatic environments. The work provides information concerning the spatial and temporal scales of expansion of four alien gammarid amphipods (three of them of Ponto-Caspian and one of North American origin): Pontogammarus robustoides (G.O. Sars, 1894), Obesogammarus crassus (G.O. Sars, 1894), Dikerogammarus haemobaphes (Eichwald, 1841), and Gammarus tigrinus Sexton, 1939 in the Vistula Lagoon (VL) and the Vistula Delta (VD) in 2008-2010. The mean abundance of these gammarids in nearshore zones was 382 ind m(-2) in VL and 89 ind m(-2) in VD. Their mean biomasses were likewise greater in VL (0.91 g m(-2)) than in VD (0.49 g m(-2)). G. tigrinus was the most dominant species in both nearshore zones of VL and VD and attained the highest frequency in these areas. The study gives evidence of total extinction of native gammarid species.

The impact of zebra mussel (Dreissena polymorpha) periostracum and biofilm cues on habitat selection by a Ponto-Caspian amphipod Dikerogammarus haemobaphes

Dikerogammarus haemobaphes is one of several Ponto-Caspian gammarids invading Europe in recent decades. Previously, it exhibited active preferences for habitats associated with another Ponto-Caspian alien, zebra mussel. Now we tested gammarid preferences for living mussels and their empty shells with biofilm and/or periostracum present or absent, to find the exact cues driving gammarid responses. We observed a strong prefer- ence of gammarids for biofilmed shells, even if the biofilm was relatively young (2-day old). However, the biofilm quality, related to the substratum on which it had developed (shells with or without the periostracum, or coated with nail varnish) did not affect their behaviour. In the absence of biofilm, gammarids positively responded to the shell perios- tracum. Furthermore, they clearly preferred living zebra mussels over old empty shells, independent of the presence or absence of biofilm, confirming the importance of a periostracum-associated cue in their substratum recognition. On the other hand, shells obtained shortly after mussels' death were preferred over living bivalves. Thus, the attractant is associ- ated with fresh mussel shells, rather than with living mussels themselves. The ability of alien gammarids to locate sites inhabited by zebra mussels may contribute to their invasion success in novel areas inhabited by this habitat-forming bivalve.

A comparison of the short-term toxicity of cadmium to indigenous and alien gammarid species

Amphipods play an important role in many aquatic ecosystems and are commonly used in ecotoxicology and ecosystem health assessment. Several alien gammarids have been introduced in many regions of the world during the last decades. In this study, we investigated if differences in cadmium sensitivity occurred between (1) different species belonging to the family Gammaridae and (2) different populations of the same species originating from a polluted or a non-polluted site. The acute cadmium toxicity to two indigenous (Gammarus pulex and Gammarus fossarum) and four alien (Dikerogammarus villosus, Echinogammarus berilloni, Gammarus roeseli and Gammarus tigrinus) gammarids occurring in Belgium was tested. Significant differences (P < 0.05) in median lethal concentrations (LC(50)) were found between the different species, with 72 h-LC50s ranging from 6.3 to 268 μg/l and 96 h-LC50s from 4.7 to 88.9 μg/l. No clear trend in Cd sensitivity was found when comparing indigenous and alien gammarids. D. villosus, an alien invasive species, was the most sensitive to Cd toxicity and E. berilloni, another alien species, the least sensitive. In addition, larger Gammarid species were more sensitive to Cd toxicity than smaller ones. No significant differences were found between populations of the same species originating from metal polluted sites or non-polluted sites. Overall, our results showed that considerable differences in Cd sensitivity exist between gammarid species, which should be taken into consideration in environmental risk assessment and water quality standard setting. Finally, our data suggest that alien gammarids would not have an advantage over indigenous gammarids in Cd contaminated environments.

Cryptic invasion of Baltic lowlands by freshwater amphipod of Pontic origin

Gammarus varsoviensis is morphologically close to G. lacustris, with which it is often misidentified. Geographic range of G. varsoviensis includes Germany, Poland, Lithuania, Latvia, Belarus and Ukraine. Such a distribution pattern led us to the assumption that the species might have originated in the Black Sea drainage area. From there, as early as the nineteenth century, it could possibly have migrated to the Baltic basin through the Pripyat-Bug canal. Thus, the goals of this study are: (1) to indicate the level of genetic divergence of G. varsoviensis from the morphologically closest species – G. lacustris and (2) to investigate the possibility of the Pontic origin of G. varsoviensis and its range expansion across the Black Sea/Baltic Sea watershed to Central Europe through the artificial canal network. Altogether 128 partial 16S rDNA sequences of Gammarus varsoviensis from 19 localities were gained. They were analysed in conjunction with a sequence of G. lacustris obtained in this study from the Dnieper system and sequences of G. lacustris, G. pulex and G. fossarum available in GenBank in order to estimate the relationships among the species. GenBank accession numbers for all the haplotypes defined within this study are: G. varsoviensis – from JN641868 to JN641875; G. lacustris – JN641876. The genetic distance within and between the species was calculated, as well as phylogenetic relationships among haplotypes, which were inferred with Neighbor-Joining method. The haplotype relationships were analysed with the Minimum Spanning Network. Also mismatch distribution of the haplotypes were tested under sudden expansion model and sequence deviations from selective neutrality. Neighbor-Joining analysis revealed that G. varsoviensis and G. lacustris haplotypes formed separate well defined clades. Mean genetic diversity between the two species was ca. 15× higher than the intraspecific distance and similar to the value obtained for G. fossarum/G. pulex species pair. Therefore, G. varsoviensis can be definitely considered as a distinct species from G. lacustris. Among 128 sequences obtained from G. varsoviensis, 8 haplotypes were identified and grouped into two clades: one found only in the lower Dnieper (two haplotypes) and the second one encompassing the rest of haplotypes observed in the upper Dnieper and Baltic Sea basin. Only one haplotype was found in the Baltic Sea drainage area. A mismatch distribution curve as well as selective neutrality tests demonstrated sudden expansion model. Our findings suggest that G. varsoviensis is an alien gammarid that originated in the Pontic area. Its expansion in Central Europe apparently started soon after the opening of the artificial waterways joining the Black and the Baltic Sea drainage basins.

Seasonal variability in the grazing potential of the invasive amphipod Gammarus tigrinus and the native amphipod Gammarus salinus (Amphipoda: Crustacea) in the northern Baltic Sea

Mesograzers are known to reduce the biomass of their host plant and modify the structure of the whole macrophyte community in many ecosystems. Thus, the introduction of an efficient mesograzer may destabilize macrophyte community and also affect the native grazers. We estimated how large proportion of macrophyte production are consumed by the alien gammarid G. tigrinus and the native gammarid G. salinus in the species poor ecosystem of the northern Baltic Sea. We analysed whether G. tigrinus consumes different diet as the native G. salinus and whether the effect of G. tigrinus on the survival of the native G. salinus is macrophyte species specific. Grazing experiments showed that there was a clear difference in the grazing rates of gammarids among the studied macrophyte species in summer and autumn but not in spring. The grazing rates were significantly higher in the prevailing macrophyte Pilayella littoralis as compared to other macrophytes. The grazing was inversely related to the diurnal net photosynthetic values of macrophytes. The gammarid amphipods potentially removed only a minor part of plant primary production except for summer and autumn when grazing of a few perennial species exceeded macrophyte production. Macrophyte species and presence of G. salinus had no effect on the survival of G. tigrinus. The presence of G. tigrinus, however, reduced the survival of the native gammarids within P. littoralis in summer. To conclude it is likely that both native and alien gammarid amphipods do not exert significant pressure on the macroalgal communities in the northern Baltic Sea. Competitive interactions between G. tigrinus and G. salinus within the prevailing macrophyte P. littoralis is the likely explanation of the decline of the native gammarid amphipods after the establishment of G. tigrinus in the northern Baltic Sea.

Invasions of alien gammarid species and retreat of natives in the Vistula Lagoon (Baltic Sea, Poland)

During the last decades of the twentieth century, the alien gammarid species Gammarus tigrinus, Dikerogammarus haemobaphes, Pontogammarus robustoides and Obesogammarus crassus invaded the lower Vistula River and its deltaic, partly brackish regions. In brackish waters of the Vistula Lagoon the native Atlantic-boreal species Gammarus zaddachi and Gammarus duebeni have been replaced or at least outnumbered by the aliens. As compared to our earlier studies, through the years 1998–2004 we could observe nearly total decline of the native gammarid populations along the coasts of the Lagoon, and overdomination of the North-American G. tigrinus in most places. Possible reasons for the observed phenomena are e.g. increasing pollution and eutrophication of the Lagoon accompanied by competition between the native and the alien species.

Population dynamics of alien gammarid species in the River Odra estuary

During the period of 1988–2000, three alien gammarid species, i.e. Gammarus tigrinus Sexton, 1939, Pontogammarus robustoides G. O. Sars, 1894, and Dikerogammarus haemobaphes (Eichwald, 1841) were recorded in the Odra estuary. This study, the first record of G. tigrinus and P. robustoides in Poland, focuses on the distribution, abundance, and biomass as well as on population structure of the three new species found in the coastal zone of the estuary. G. tigrinus and P. robustoides were first sampled in the Szczecin Lagoon (mid-part of the estuary) in 1988. The densities of both species were high from the time they were first recorded and exceeded 10 000 ind. m−2, while the biomass was 25 and 140 g m−2, respectively. G.␣tigrinus occurred at higher densities in northern and eastern parts of the Lagoon, while P. robustoides was particularly abundant in the south-eastern part, most heavily affected by River Odra discharge. In 1999, the third gammarid, D. haemobaphes, was recorded in the southern part of the estuary. Both in 1999 and 2000, the species was found in qualitative samples (dredge collections of Dreissena polymorpha) taken from the western branch of the river. As estimated from quantitative samples, densities and biomass in the eastern branch were rather low and did not exceed 150 ind. m−2 and 2.7 g m−2, respectively. The Szczecin Lagoon population of G. tigrinus produces at least two generations within a year: a summer one and an overwintering one. The latter is dominated by older and larger specimens. The species may reproduce in the Lagoon from April until November.

Obesogammarus crassus (G.O. Sars, 1894) – one more Ponto-Caspian gammarid species in Polish waters

Obesogammarus crassus, a new Ponto-Caspian gammarid species has been recorded in Poland in the deltaic Vistula system. Notes on its origin, places of acclimatization in Europe, as well as probable ways of invasion are presented. Since the majority of alien gammarid species is still poorly recognized, the authors include a simple key and figures allowing the identification of all Ponto-Caspian gammarid crustaceans recently appearing in Polish waters.