The introduction of invasive species, which often differ functionally from the components of the recipient community, generates ecological impacts that propagate along the food web. This review aims to determine how consistent the impacts of aquatic invasions are across taxa and habitats. To that end, we present a global meta-analysis from 151 publications (733 cases), covering a wide range of invaders (primary producers, filter collectors, omnivores and predators), resident aquatic community components (macrophytes, phytoplankton, zooplankton, benthic invertebrates and fish) and habitats (rivers, lakes and estuaries). Our synthesis suggests a strong negative influence of invasive species on the abundance of aquatic communities, particularly macrophytes, zooplankton and fish. In contrast, there was no general evidence for a decrease in species diversity in invaded habitats, suggesting a time lag between rapid abundance changes and local extinctions. Invaded habitats showed increased water turbidity, nitrogen and organic matter concentration, which are related to the capacity of invaders to transform habitats and increase eutrophication. The expansion of invasive macrophytes caused the largest decrease in fish abundance, the filtering activity of filter collectors depleted planktonic communities, omnivores (including both facultative and obligate herbivores) were responsible for the greatest decline in macrophyte abundance, and benthic invertebrates were most negatively affected by the introduction of new predators. These impacts were relatively consistent across habitats and experimental approaches. Based on our results, we propose a framework of positive and negative links between invasive species at four trophic positions and the five different components of recipient communities. This framework incorporates both direct biotic interactions (predation, competition, grazing) and indirect changes to the water physicochemical conditions mediated by invaders (habitat alteration). Considering the strong trophic links that characterize aquatic ecosystems, this framework is relevant to anticipate the far-reaching consequences of biological invasions on the structure and functionality of aquatic ecosystems.
North American brine shrimp Artemia franciscana have been exported worldwide since the 1950s for use in aquarium trade and fish farming. Aquaculture is expanding along the Mediterranean coast, leading to the release of A. franciscana into native Artemia populations. A. franciscana was first detected in 1981 in Portugal and has since spread to saltworks along the East Atlantic flyway used by shorebirds. Once A. franciscana becomes established in a locality, native Artemia tend to disappear. To test whether migratory shorebirds can disperse invasive and native Artemia between wetlands, we extracted Artemia cysts from feces and pellets collected at Castro Marim (Portugal) and Cadiz Bay (Spain) during southward migration. We found that large numbers of viable eggs of A. franciscana and native Artemia parthenogenetica were dispersed by Redshank Tringa totanus, Blacktailed Godwit Limosa limosa, and other shorebirds migrating through the Iberian Peninsula. This is the most extensive field demonstration to date that invertebrates can disperse readily via gut passage through birds.
Understanding how introduced species succeed and become widely distributed within non‐native areas is critical to reduce the threats posed by them. Our goal was to reconstruct the main invasion routes and invasion dynamics of a global freshwater invader, the red swamp crayfish, Procambarus clarkii, through the analysis of its genetic variability in both native and invasive ranges. We inferred invasion routes and population structure from the analysis of a fragment (608 base pairs) of the mitochondrial marker cytochrome c oxidase subunit I from 1,062 individuals of P. clarkii in addition to 354 GenBank sequences, for a total of 122 populations (22 natives and 100 invaded). Genetic structure was assessed using analysis of molecular variance and non‐metric multidimensional scaling analyses. We analysed haplotype frequencies for the genetic variability in each locality and region. The haplotype network was depicted by using PopART software. A high haplotype diversity was found in the native range (haplotype diversity [Hd]: 0.90), but also in some non‐native areas, such as western U.S.A. (Hd: 0.80), areas of Mexico (Hd: 0.78), and some hotspots in Europe (e.g. southern Spain or Italy), suggesting a complex pattern of multiple introductions. We grouped all localities in five differentiated groups according to biogeographic origin: the native area, west Americas, east U.S.A., Asia, and Europe. Additionally, the identification of 15 haplotypes shared between at least two localities, the phylogenetic network estimation and indices of genetic differentiation among localities allowed us to identify a large genetic admixture in the native range; the two independent invasion routes (i.e. westwards and eastwards) in U.S.A. from the native range (Louisiana and Texas) with translocations within each area; a stepping‐stone introduction from U.S.A. to Japan (involving few individuals) themselves introduced to China afterwards; the entry of P. clarkii from Louisiana (U.S.A.) into southern Spain and their multiple secondary introductions over Europe as well as other possible introductions in central Europe. Our study emphasises the need for unravelling the global invasion routes and the demographic processes underlying the introduction of exotic species (i.e. admixture, bridgehead invasion effect, and propagule pressure) to control the spread of invasive species. Our findings highlight the value of genetic analyses to identify the geographic origin of source populations as well as the variability of invaded areas in order to reconstruct invasion dynamics and facilitate management of invasive species (e.g. through environmental DNA monitoring).
The hypersaline environments and salterns present in the western Mediterranean region (including Italy, southern France, the Iberian Peninsula and Morocco) contain autochthonous forms of the brine shrimp Artemia, with parthenogenetic diploid and tetraploid strains coexisting with the bisexual species A. salina. Introduced populations of the American brine shrimp A. franciscana have also been recorded in these Mediterranean environments since the 1980s. Based on brine shrimp cyst samples collected in these countries from 1980 until 2002, we were able to establish the present distribution of autochthonous brine shrimps and of A. franciscana, which is shown to be an expanding invasive species. The results obtained show that A. franciscana is now the dominant Artemia species in Portuguese salterns, along the French Mediterranean coast and in Cadiz bay (Spain). Co-occurrence of autochthonous (parthenogenetic) and American brine shrimp populations was observed in Morocco (Mar Chica) and France (Aigues Mortes), whereas A. franciscana was not found in Italian cyst samples. The results suggest these exotic A. franciscana populations originate as intentional or non-intentional inoculations through aquacultural (hatchery effluents) or pet market activities, and suggest that the native species can be rapidly replaced by the exotic species.
The hypersaline environments and salterns present in the western Mediterranean region (including Italy, southern France, the Iberian Peninsula and Morocco) contain autochthonous forms of the brine shrimp Artemia, with parthenogenetic diploid and tetraploid strains coexisting with the bisexual species A. salina. Introduced populations of the American brine shrimp A. franciscana have also been recorded in these Mediterranean environments since the 1980s. Based on brine shrimp cyst samples collected in these countries from 1980 until 2002, we were able to establish the present distribution of autochthonous brine shrimps and of A. franciscana, which is shown to be an expanding invasive species. The results obtained show that A. franciscana is now the dominant Artemia species in Portuguese salterns, along the French Mediterranean coast and in Cadiz bay (Spain). Co-occurrence of autochthonous (parthenogenetic) and American brine shrimp populations was observed in Morocco (Mar Chica) and France (Aigues Mortes), whereas A. franciscana was not found in Italian cyst samples. The results suggest these exotic A. franciscana populations originate as intentional or non-intentional inoculations through aquacultural (hatchery effluents) or pet market activities, and suggest that the native species can be rapidly replaced by the exotic species.
The red swamp crayfish (Procambarus clarkii), originally from North America, is one of the world's worst aquatic invaders. It is a favoured prey item for waterbirds, but the influence of this novel predator–prey relationship on dispersal of other organisms has not previously been considered. We investigated the potential for dispersal of plants and invertebrates by migratory waterbirds feeding on alien P. clarkii in European ricefields at harvest time. In November–December of 2014–2015, we collected propagules from the outside of 13 crayfish captured as they moved out of ricefields during harvest in Doñana, south‐west Spain. We also collected excreta (N = 76 faeces, 14 pellets) of lesser‐black backed gull (Larus fuscus). We recorded diaspores from at least 11 plant species (161 seeds from 10 angiosperm taxa, and 14 charophyte oogonia) on the outside of crayfish, together with 54 eggs from eight aquatic invertebrate taxa. Adults and juveniles of at least nine microcrustaceans, including the alien ostracods Hemicypris reticulata and Ankylocythere sinuosa, were also recovered from crayfish. No intact propagules were present in the digestive system of the crayfish. Contents of regurgitated pellets confirmed P. clarkii as the main food item for gulls. Diaspores from at least 12 plant species (154 seeds from 11 angiosperm taxa, and 17 charophyte oogonia) were recovered from gull excreta, together with 129 eggs of 12 aquatic invertebrate taxa. A statoblast of the alien bryozoan Plumatella vaihiriae was found in gull faeces. Seven of the plant species are important agricultural weeds, and two are alien to Spain. Diaspores from six plant taxa were germinated, confirming viability. These propagules were from a similar set of plants and invertebrates to those found on the outside of crayfish, suggesting that propagules in gull excreta were ingested inadvertently with their crayfish prey. Ricefields constitute a major artificial aquatic habitat covering an increasing proportion of the world's land surface and typically support native or alien crayfish. Crayfish invasion can lead to novel secondary dispersal pathways for plants and invertebrates through interactions with their predators, promoting the expansion of alien and native species (including weeds) through long‐distance dispersal via migratory waterbirds and increasing connectivity of organisms between artificial and natural ecosystems. This represents a previously overlooked impact of crayfish invasion on ecosystem services.
Shorebirds (Charadriiformes) undergo rapid migrations with potential for long‐distance dispersal (LDD) of plants. We studied the frequency of endozoochory by shorebirds in different parts of Europe covering a broad latitudinal range and different seasons. We assessed whether plants dispersed conformed to morphological dispersal syndromes. A total of 409 excreta samples (271 faeces and 138 pellets) were collected from redshank Tringa totanus, black‐winged stilt Himantopus himantopus, pied avocet Recurvirostra avosetta, northern lapwing Vanellus vanellus, Eurasian curlew Numenius arquata and black‐tailed godwit Limosa limosa in south‐west Spain, north‐west England, southern Ireland and Iceland in 2005 and 2016, and intact seeds were extracted and identified. Godwits were sampled just before or after migratory movements between England and Iceland. The germinability of seeds was tested. Intact diaspores were recovered from all bird species and study areas, and were present in 13% of samples overall. Thirteen plant families were represented, including Charophyceae and 26 angiosperm taxa. Only four species had an ‘endozoochory syndrome’. Four alien species were recorded. Ellenberg values classified three species as aquatic and 20 as terrestrial. Overall, 89% of seeds were from terrestrial plants, and 11% from aquatic plants. Average seed length was higher in redshank pellets than in their faeces. Six species were germinated, none of which had an endozoochory syndrome. Seeds were recorded during spring and autumn migration. Plant species recorded have broad latitudinal ranges consistent with LDD via shorebirds. Crucially, morphological syndromes do not adequately predict LDD potential, and more empirical work is required to identify which plants are dispersed by shorebirds. Incorporating endozoochory by shorebirds and other migratory waterbirds into plant distribution models would allow us to better understand the natural processes that facilitated colonization of oceanic islands, or to improve predictions of how plants will respond to climate change, or how alien species spread.
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