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Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: Potential consequences

Authors:
Loic Bollache at University Bourgogne Franche-Comté
Loic Bollache
Simon Devin at University of Lorraine
Simon Devin
Remi Wattier at Université Bourgogne Europe
Remi Wattier
M. Chovet
M. Chovet
M. Chovet
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Abstract

Non-indigenous species are increasingly recognized as altering local communities in newly colonized areas. In some north European freshwater systems, the Ponto-Caspian invasive crustacean Dikerogammarus villosus (Amphipoda) is implicated to have such an effect, with general monitoring of its progress and general impact required. The present study contributes to this monitoring. D. villosus was observed in 2003 in all the major French rivers prospected (i.e. Rhine, Meuse, Moselle, Saône, Rhône, Seine, and Loire), a European region previously overlooked for its colonization. This species was also detected in some tributaries of the rivers Saône and Seine, and in Geneva Lake. The dynamics of this colonisation, inferred from samples made at different dates, show a rapid expansion westward, from its first appearance in the Saône in 1997. The colonised rivers are connected with the more important French harbours, which may facilitate future invasion of new countries. In two sites, D. villosus rapidly became the dominant crustacean species after its appearance. A comparison of the amphipod fauna between 2003 and ancient surveys also shows that some native species tend to disappear in the East of France. These data suggest an ongoing homogenisation process of amphipod assemblages.
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Arch. Hydrobiol. 160 1 57–66 Stuttgart, May 2004
Rapid range extension of the Ponto-Caspian
amphipod Dikerogammarus villosus in France:
potential consequences
L. Bollache1*, S. Devin2, R. Wattier1, M. Chovet3, J.-N. Beisel2,
J.-C. Moreteau2and T. Rigaud1
With 2 figures and 1 table
Abstract: Non-indigenous species are increasingly recognized as altering local com-
munities in newly colonized areas. In some north European freshwater systems, the
Ponto-Caspian invasive crustacean Dikerogammarus villosus (Amphipoda) is im-
plicated to have such an effect, with general monitoring of its progress and general im-
pact required. The present study contributes to this monitoring. D. villosus was ob-
served in 2003 in all the major French rivers prospected (i. e. Rhine, Meuse, Moselle,
Saône, Rhône, Seine, and Loire), a European region previously overlooked for its co-
lonization. This species was also detected in some tributaries of the rivers Saône and
Seine, and in Geneva Lake. The dynamics of this colonisation, inferred from samples
made at different dates, show a rapid expansion westward, from its first appearance in
the Saône in 1997. The colonised rivers are connected with the more important French
harbours, which may facilitate future invasion of new countries. In two sites, D. villo-
sus rapidly became the dominant crustacean species after its appearance. A comparison
of the amphipod fauna between 2003 and ancient surveys also shows that some native
species tend to disappear in the East of France. These data suggest an ongoing homo-
genisation process of amphipod assemblages.
Key words: invasions, Dikerogammarus villosus, gammarids, French hydrosystem.
1Authors’ addresses: Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéoscien-
ces, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France.
2Equipe de Démoécologie, UR LBFE, Université de Metz, Campus Bridoux, avenue
du Général Delestraint, 57070 Metz, France.
3DIREN Centre, Service de l’eau et des milieux aquatiques, 5 avenue Buffon, BP
6407, 45064 Orléans Cedex 2, France.
* Author for correspondence; E-mail: loic.bollache@u-bourgogne.fr
DOI: 10.1127/0003-9136/2004/0160-0057 0003-9136/04/0160-0057 $ 2.50
2004 E. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart
... Its displacement of native species (MacNeil et al., 2011;MacNeil & Platvoet, 2013) also facilitates the establishment of other invasive alien species (Bollache et al., 2004;Leuven et al., 2009). Notably, it is the only invasive amphipod with documented monetary costs . ...
... Our study was therefore limited by our focus on rivers and streams. Dikerogammarus villosus also occurs in lentic freshwaters including lakes, ponds, and brackish waters, and has marked impacts on these ecosystems (Bacela-Spychalska et al., 2013;Bollache et al., 2004;Minchin et al., 2019). Its occurrence in other countries could also be underestimated, resulting in relatively few time series, for example the Netherlands or Switzerland (Altermatt et al., 2014;Bij de Vaate & Klink, 1995). ...
Tracking a killer shrimp: Dikerogammarus villosus invasion dynamics across Europe
Article
Full-text available
Aim Invasive alien species are a growing problem worldwide due to their ecological, economic and human health impacts. The “killer shrimp” Dikerogammarus villosus is a notorious invasive alien amphipod from the Ponto‐Caspian region that has invaded many fresh and brackish waters across Europe. Understandings of large‐scale population dynamics of highly impactful invaders such as D. villosus are lacking, inhibiting predictions of impact and efficient timing of management strategies. Hence, our aim was to assess trends and dynamics of D. villosus as well as its impacts in freshwater rivers and streams. Location Europe. Methods We analysed 96 European time series between 1994 and 2019 and identified trends in the relative abundance (i.e. dominance %) of D. villosus in invaded time series, as well as a set of site‐specific characteristics to identify drivers and determinants of population changes and invasion dynamics using meta‐regression modelling. We also looked at the spread over space and time to estimate the invasion speed (km/year) of D. villosus in Europe. We investigated the impact of D. villosus abundance on recipient community metrics (i.e. abundance, taxa richness, temporal turnover, Shannon diversity and Pielou evenness) using generalized linear models. Results Population trends varied across the time series. Nevertheless, community dominance of D. villosus increased over time across all time series. The frequency of occurrences (used as a proxy for invader spread) was well described by a Pareto distribution, whereby we estimated a lag phase (i.e. the time between introduction and spatial expansion) of approximately 28 years, followed by a gradual increase before new occurrences declined rapidly in the long term. D. villosus population change was associated with decreased taxa richness, community turnover and Shannon diversity. Main Conclusion Our results show that D. villosus is well‐established in European waters and its abundance significantly alters ecological communities. However, the multidecadal lag phase prior to observed spatial expansion suggests that initial introductions by D. villosus are cryptic, thus signalling the need for more effective early detection methods.
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... Therefore, especially the invasion and a subsequent species turnover in Peracarida has the potential to change ecosystem functions, specifically leaf litter processing. One of the most successful Ponto-Caspian invaders of European aquatic ecosystems is the amphipod Dikerogammarus villosus (Sowinskyi, 1894) (Rewicz et al. 2014), which has not only been reported to change benthic invertebrate community composition, especially reducing native amphipod species (Bollache et al. 2004;Grabowski et al. 2007;Borza et al. 2015;Žganec et al. 2018;Boets et al. 2010) but which is also suspected to change ecosystem functions (Van Riel et al. 2006;Bollache et al. 2008;MacNeil et al. 2011). Most studies observed D. villosus to have lower rates of leaf litter processing compared to native amphipods, at least in laboratory settings (Boeker and Geist 2015;Jourdan et al. 2016;Kenna et al. 2017;Fincham et al. 2023;Pile et al. 2023). ...
Assessing the Complex Effects of the Invasive Amphipod Dikerogammarus villosus on Leaf Litter Breakdown in Rivers
Article
Full-text available
  • Feb 2025
  • FRESHWATER BIOL
1. Allochthonous organic matter is an essential resource of aquatic food webs, and freshwater amphipods, particularly species of the genus Gammarus, play a significant role in leaf litter decomposition. However, this important ecological function may be affected by the invasion of alien amphipods such as Dikerogammarus villosus, which has been reported to show lower leaf litter decay rates than native gammarids. The aim of this study was to determine whether the invasion of D. villosus would disrupt the ecological function of leaf litter breakdown under field conditions by comparing leaf litter decay rates at invaded and uninvaded river sites. 2. The experiment was conducted at six locations, four in Croatia and two in Germany, with one site upstream and one site downstream of an invasion front at each location. At each site, we placed preconditioned willow leaves in the river and sampled them three times to estimate leaf litter breakdown rates and invertebrate colonisation. 3. We hypothesized that leaf litter breakdown rates would be higher at the sites without D. villosus (upstream of the invasion front) compared to the invaded sites. Contrary to this hypothesis, the results indicated contrasting and obviously context dependent outcomes. This indicates a change but no general disruption of leaf litter processing by the invasion of the omniv-orous D. villosus, even when it displaces native shredders. 4. The outcome of the experiments most probably depended on the biomass of native shredders in the leaf bags. At three locations with low biomass of native shredders in the upstream leaf bags, the downstream sites with D. villosus presence showed higher breakdown rates than the upstream sites. At the three locations with high biomass of native shredders, the downstream sites with D. villosus had lower breakdown rates than the upstream sites. 5. These findings underscore the complex interactions between invasive and native species in freshwater ecosystems and their potential impact on ecosystem services.
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... material 1). Similar rapid invasion of C. ischnus and elimination of native species was observed in the Great Lakes in the USA (Dermott et al. 1998) and River Rhine in Europe ( Van der Velde et al. 2000), where rapid range extension of D. villosus was observed as well (Bollache et al. 2004). Chaetogammarus ischnus can disperse over great distances (Witt et al. 1997). ...
Recent invasion of Ponto-Caspian amphipods in the Masurian Lakeland associated with human leisure activities
Article
Full-text available
  • Jan 2024
Non-indigenous species (NIS) contribute to the decrease of native species' diversity on a local and global scale. One of Europe's most significant donors of freshwater invasions is the Ponto-Caspian Region. Following the construction of artificial canals connecting isolated waterbodies and the resulting heavy boat traffic, the Ponto-Caspian Amphipoda started to spread in Europe. Four amphipod species: Dikerogammarus haemobaphes, Dikerogammarus villosus, Pontogammarus robustoides and Chaetogammarus ischnus have invaded the Masurian Lakeland (North-eastern Poland). Based on literature and our data, we studied their distribution in 22 lakes in the region during the years 2001-2016. We analysed their distribution against several water quality parameters and levels of anthropogenic pressure. Our results also present the first records of two new invaders, D. villosus and C. ischnus, in the studied area. We show that the relative abundance and frequency of these two species rapidly increase and, simultaneously, the populations of the earlier invaders, i.e. D. haemobaphes and P. robustoides, decrease. The native species - Gammarus lacustris - seems to be negatively affected by NIS richness, as well as by the proximity of towns. The spread of NIS in the lakes appears to be facilitated by boating and the lower complexity of the shoreline. Our study shows how anthropogenic pressure, especially tourism, can facilitate bioinvasion, jeopardising native biodiversity unless appropriate regulations are implemented.
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... These particularities could be linked to the anthropic pressures that this aquatic ecosystem undergoes, as there was a strong presence of inhabitants in the study area. To this end, Malmqvist and Rundle (2002) and Bollache et al. (2004) concluded in their study that anthropogenic actions had negative consequences on the health of watercourses. They negatively influence not only the ecological quality of the hydro-system but also the biological communities in general. ...
Influence of Some Abiotic Factors on the Diatom Densities in the Mezam River (Bamenda, North-West Cameroon)
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Wetlands of the city of Bamenda are characterized by intense agricultural activities. The resulting consequences are aquatic pollution. The management of these wetlands requires the study of the animal and plant communities found there. Diatoms are known to be good markers of environmental change. The aim of the study was to determine the influence of some abiotic parameters on the diatom densities of the Mezam river. The study was conducted from January to December 2022. Some physicochemical parameters were measured in situ. Water samples were collected and transported to the laboratory for the measurement of nitrates, total phosphorus, carbon dioxide and biological oxygen demand. The diatoms were sampled and analyzed in the laboratory. Factorial axis 2 (0.47%) of correspondence factor analysis opposed the positive variables (conductivity, total dissolved solids and salinity) to the negative variables (water temperature, pH, nitrates, total phosphorus, oxidability, carbon dioxide and alkalinity). Study sites showed a mineralization gradient going from upstream (Site 1) to downstream (Site 3). Total species richness amounted to 4 classes divided in 18 families, 21 genera and 43 species. The most dominating family was Naviculaceae with 10 species. Multiple component analysis showed, in different study sites, the correlation between chemical parameters and density of different genera. The more the site was polluted, the more the density of Navicula, Tabellaria, Melosira and Coscinodiscus increased. On the contrary, the less the site was polluted, the more the density of Cyclotella, Gomphonema, Cocconeis, Gyrosigma, Synedra increased. These results showed that the distribution of diatoms in the different study sites was influenced by a set of conditions related to physicochemical parameters, but more on their densities.
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... As a result of their high predation ability, the species composition and diversity of invaded waters can change substantially (Arbačiauskas & Gumuliauskaitė, 2007;Dick & Platvoet, 2000). The native gammarid species used in our investigation, G. jazdzewskii and G. pulex, are widely distributed across Central Europe (Pinkster, 1972;Rudolph et al., 2018), but their displacement by larger and more predatory invasive gammarids has been documented previously (Boets et al., 2010;Bollache, 2004;MacNeil et al., 2011). ...
New species, new story: The impact of invasive non-host predators on host-trematode interactions
Article
  • Jul 2023
1. Predation is considered one of the key drivers shaping the relationships between animals. There is increasing evidence that non-host aquatic taxa use free-living parasite stages as prey, including motile cercariae of digenean trematodes. However, species-specific predator differences in cercarial consumption are poorly understood, especially when invasive consumers are involved. 2. We used experimental approaches to investigate the possible predator-induced reduction in trematode-host encounters in freshwater benthic communities. Four gammarid species, two native European (Gammarus jazdzewskii and G. pulex) and two invasive Ponto-Caspian (Dikerogammarus villosus and Pontogammarus robust-oides), were selected as predators of echinostomatid cercariae (Echinoparyphium aconiatum). 3. We hypothesised that (i) all predators will prey on cercariae, but the amount of prey consumed will vary, the invaders will be more voracious than native species, and (ii) the effect of predator-induced dilution of cercariae will depend on the environmental condition, i.e., the presence of the natural target host (the planorbid snail Planorbarius corneus) and alternative food resource; the exposure of predators to these two basic environmental factors will reduce their consumption rates of cercariae. 4. The extent of the dilution effect caused by gammarids was highly predator species-dependent and also varied depending on experimental conditions. Overall, all gammarids preyed on cercariae and reduced infection levels in the target snail host, but the invaders were more efficient than the native species. Furthermore, decreased consumption rates of cercarial prey were observed in the presence of both the target snail hosts and alternative food resources, except for invasive P. robustoides consuming more cercariae when a snail host was present. 5. The observed differences among predators in the consumption of cercariae may be a result of complex interaction traits of parasites, predators and target hosts, such as different predatory behaviour of invasive and native amphipods, change in parasite behaviour in response to the presence/chemical signals of the target host and a predator-induced “ecology of fear” interfering with the dilution effect of parasites. 6. We provided evidence that gammarids can cause a significant reduction in parasite- host encounters. The high consumption rates, especially in the presence of easily available alternative food resources, emphasise the importance of free- living cercariae as an energy resource in aquatic food webs. The observed preda-tor differences in the consumption of cercariae are further evidence of the higher competitive ability of invasive species. Simultaneously, our results indicate that the appearance of new predators in the environment may interfere with estab-lished host- parasite interactions.
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... However in the Gulf of Gdasnk, round gobies were found to migrate up to 40 km upstream in the Vistula River (Corkum et al. 2004). The secondary movements between sites has potentially been facilitated by abandoned eggs in nests deposited in crevices on ships on freight vessels dispersed by ships moving from port to port (Ray & Corkum 2001 Germany (Nesemann et al. 1995), France (Devin et al. 2004), Italy (Casellato et al. 2006), Belarus ) Poland (Grabowski et al. 2007) Ireland and England (Defra 2011 However, D. villosus is considered likely to continue to disperse in Great Britain, facilitated by its broad environmental tolerances, its climatic suitability to broad areas of GB, and the extensive connectivity, both natural and artificial, of the hydrological network (Gallardo et al. 2011). ...
Review of invasion pathways and provisional pathway management plan for non-native Ponto-Caspian species of potential invasion risk to Great Britain
Technical Report
Full-text available
  • Mar 2012
The potential (and in some cases actual) impact that each species would have in GB were also reviewed. • The list consisted of two species of molluscs, three fish, eight crustacea and one cnidaria of which five are recognised as currently being present in GB waters. • A literature review conducted on each of the species identified pathways and mechanisms of introduction and translocation most commonly associated with the species. • From this shipping was recognised as the most common pathway of introduction into GB, with ballast water being the most common mechanism and then (in descending order) inland boating (a secondary pathway of dispersal), hull fouling (a mechanism of the shipping pathway), unintentional stocking (secondary pathway), anglers gear (secondary pathway), air/land transport (primary pathways) and intentional release (secondary pathway). • The most common forms of dispersal (secondary pathway) were identified as natural dispersal and recreational activities (e.g. anglers, recreational boats and canoes), other secondary pathways identified were the ornamental trade, unintentional stocking and incidental transport. • The main drivers behind the predominant mechanisms/pathways were global trade/economic growth and recreation. • Species identified as being associated with more pathways and mechanisms are thus more likely to gain entry into GB and/or disperse within GB once introduced. It is therefore possible to rank the spread in order of 'threat' posed. • An outline of a provisional Pathway Management Action Plan (PAP) is provided outlining: o Stakeholders that should be involved in the further development of the PAP o Target areas of development to prevent further introductions o Actions to aid in preventing further spread o Recommendations on the development of biosecurity, control and/or eradication plans o The development of contingency plans for rapid response 3
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... Thus, to the extent of our knowledge, there are no high-resolution, up to date, modern distribution maps comprising the global ranges of APCAs. This is surprising given that numerous studies have provided such data at a regional scale (Jażdżewski and Konopacka 1988;Bollache et al. 2004;Grudule et al. 2007;Žganec et al. 2009;Arbačiauskas et al. 2011;Borza 2011;Borza et al. 2015;Meßner and Zettler 2018), and range expansions are routinely reported (Copilaș-Ciocianu and Arbačiauskas 2018; Moedt and Van Haaren 2018;Minchin et al. 2019;Lipinskaya et al. 2021;Copilaș-Ciocianu and Šidagyė-Copilas 2022). Even though the spatio-temporal dispersal patterns are relatively well known for many species (Bij de Vaate et al. 2002;Grigorovich et al. 2002;Cristescu et al. 2004;Rewicz et al. 2015;Jażdżewska et al. 2020), a lack of high resolution distribution data precludes efficient global monitoring and hampers predictions of future invasion pathways. ...
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Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes?
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Preditory impact of the freshwater invader Dikerogammarus vilosus (Crustacea: Amphipoda)
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To assess the increasing threats to aquatic ecosystems from invasive species, we need to elucidate the mechanisms of impacts of current and predicted future invaders. Dikerogammarus villosus, a Ponto-Caspian amphipod crustacean, is invading throughout Europe and predicted to invade the North American Great Lakes. European field studies show that populations of macroinvertebrates decline after D. villosus invasion. The mechanism of such impacts has not been addressed empirically; however, D. villosus is known to prey upon and replace other amphipods. Therefore, in this study, we used microcosm and mesocosm laboratory experiments, with both single and mixed prey species scenarios, to assess any predatory impact of D. villosus on a range of macroinvertebrate taxa, trophic groups, and body sizes. Dikerogammarus villosus predatory behaviour included shredding of prey and infliction of "bite" injuries on multiple victims. Dikerogammarus villosus killed significantly greater numbers of macroinvertebrates than did the native Gammarus duebeni, which is currently being replaced by D. villosus. This invader thus appears to impact on freshwater ecosystems through its exceptional predatory capabilities. We predict that future invasions by D. villosus will have serious direct and indirect effects on freshwaters, with its invasion facilitated in a larger "invasional meltdown" in regions like the North American Great Lakes.
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Range extensions of aquatic Ponto-Caspian macroinvertebrate species in Europe have mainly been facilitated by the interconnection of river basins through man-made canals and intentional introductions. Three inland migration corridors can be distinguished: (i) a northern corridor: Volga → Lake Beloye → Lake Onega → Lake Ladoga → Neva → Baltic Sea, (ii) a central corridor connecting the rivers Dnieper → Vistula → Oder → Elbe → Rhine, and (iii) a southern corridor connecting the Danube and Rhine rivers. Important trade harbours in Europe were connected via these corridors allowing further range extensions of macroinvertebrate species attached to a vessel's hull or in ballast water. The central corridor was the main migration route before 1992, after which the southern corridor became the most important migration route for the range expansions to the west because of the reopening of the Main-Danube Canal, connecting the Rhine and Danube basins. Especially the water level maintenance in the upper part of the canal, with water supply from the Danube basin, facilitated migration of mobile animals (e.g., crustaceans) from the Danube basin towards the Rhine basin; however, contribution of other transport mechanisms (e.g., shipping) is expected in the near future.
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Dikerogammarus villosus (Amphipoda : Gammaridae) : Another invasive species newly established in the Moselle River and French hydrosystems
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Based on field observations performed in 1999 and 2000, the exotic amphipod Dikerogammarus villosus is now well established throughout the navigable sector of the River Moselle in France. D. villosus co-occurs with Gammarus pulex, G. tigrinus and D. haemobaphes, another recent exotic species found in this tributary of the River Rhine. The maximal size of individuals of D. villosus collected (15.7 mm) is lower in the River Moselle than in other basins, where this species could reach up to 30 mm (Neseman et al. 1995). Nevertheless it represents the largest gammarids found in the French sector of the River Moselle. Other particular traits are its wide phenotypic plasticity, varying from a melanic to a striped form, and its predatory behavior. These particular traits may favour the establishment of this species on a recipient ecosystem. The occurrence of D. villosus was noted in the Alsace Canal and in the River Rhone, showing that its immigration across French hydrosystems is still in progress.
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Homogenization of Freshwater Faunas
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  • Annu Rev Ecol Systemat
Biotic homogenization is the increased similarity of biotas over time caused by the replacement of native species with nonindigenous species, usually as a result of introductions by humans. Homogenization is the outcome of three interacting processes: introductions of nonnative species, extirpation of native species, and habitat alterations that facilitate these two processes. A central aspect of the homogeniza-tion process is the ability of species to overcome natural biogeographic barriers either through intentional transport by humans or through colonization routes created by hu-man activities. Habitat homogenization through reservoir construction contributes to biotic homogenization as local riverine faunas are replaced with cosmopolitan lentic species. The homogenization process has generally increased biodiversity in most freshwater faunas, as the establishment of new species has outpaced the extinction of native species. There are important exceptions, however, where the establishment of nonindigenous species has had devastating impacts on endemic species. The ho-mogenization process appears likely to continue, although it could be slowed through reductions in the rate of invasions and extirpations and by rehabilitating aquatic habitats so as to favor native species.
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Recent mass invasion of the North American Great Lake by Ponto-Caspian species
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The North American Great Lakes have been invaded and dramatically altered by more than 145 alien species. Many invasions have occurred during the past few decades because of the release of Eurasian ballast water from transoceanic ships. Current regulations require ships to exchange foreign ballast with highly saline water before entering the Great Lakes; this procedure should prevent colonization by strictly freshwater species, but species with broad salinity tolerance might survive transport in exchanged water. A recent series of invasions by euryhaline organisms from the Black and Caspian Seas region signals a new phase in the transformation of the Great Lakes - one that supports the concept of an 'invasional meltdown'.
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Asymmetry in mutual predation: Possible reason for the replacement of native gammarids by invasives
Article
  • Jul 2003
  • Arch Hydrobiol
Mutual predation among two invasive gammarids (Dikerogammarus villosus and Echinogammarus ischnus) and two natives (Gammarus fossarum and Gammarus roeseli) was studied in laboratory experiments. Both invasives were much stronger predators than the two natives. Between 56-86% of the replicates resulted in the death of natives when the invasive species were the predators, while only 10-18% resulted in the death of invasives in reverse combinations. Predation by invasives on natives generally exceeded cannibalism within species by a factor of 2 to 4. Both invasive species preyed less heavily on each other than on natives. The results suggest that the observed asymmetry in strength of mutual predation can be a key factor in the displacement of native gammarids by invasives in parts of Central European rivers and that low predation between invasives may permit their coexistence. Thus, the results of this study support the opinion that intraguild predation can be an important reason for species replacement in the field.
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