Is salinity an obstacle for biological invasions?

Invasions of freshwater habitats by marine and brackish species have become more frequent in recent years with many of those species originating from the Ponto‐Caspian region. Populations of Ponto‐Caspian species have successfully established in the North and Baltic Seas and their adjoining rivers, as well as in the Great Lakes–St. Lawrence River region. To determine if Ponto‐Caspian taxa more readily acclimatize to and colonize diverse salinity habitats than taxa from other regions, we conducted laboratory experiments on 22 populations of eight gammarid species native to the Ponto‐Caspian, Northern European and Great Lakes–St. Lawrence River regions. In addition, we conducted a literature search to survey salinity ranges of these species worldwide. Finally, to explore evolutionary relationships among examined species and their populations, we sequenced the mitochondrial cytochrome c oxidase subunit I gene (COI) from individuals used for our experiments. Our study revealed that all tested populations tolerate wide ranges of salinity, however, different patterns arose among species from different regions. Ponto‐Caspian taxa showed lower mortality in fresh water, while Northern European taxa showed lower mortality in fully marine conditions. Genetic analyses showed evolutionary divergence among species from different regions. Due to the geological history of the two regions, as well as high tolerance of Ponto‐Caspian species to fresh water, whereas Northern European species are more tolerant of fully marine conditions, we suggest that species originating from the Ponto‐Caspian and Northern European regions may be adapted to freshwater and marine environments, respectively. Consequently, the perception that Ponto‐Caspian species are more successful colonizers might be biased by the fact that areas with highest introduction frequency of NIS (i.e., shipping ports) are environmentally variable habitats which often include freshwater conditions that cannot be tolerated by euryhaline taxa of marine origin.     

Domestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great Lakes

Ballast water moved by transoceanic vessels has been recognized globally as a predominant vector for the introduction of aquatic nonindigenous species (NIS). In contrast, domestic ships operating within confined geographic areas have been viewed as low risk for invasions, and are exempt from regulation in consequence. We examined if the St. Lawrence River could serve as a source of NIS for the Laurentian Great Lakes by surveying ballast water carried by domestic vessels and comparing biological composition in predominant St. Lawrence River—Great Lakes port-pairs in order to determine the likelihood that NIS could be transported to, and survive in, the Great Lakes. Thirteen potential invaders were sampled from ballast water, while 26 taxa sampled from St. Lawrence River ports are not reported from the Great Lakes. The majority of NIS recorded in samples are marine species with low potential for survival in the Great Lakes, however two euryhaline species (copepod Oithona similis, and amphipod Gammarus palustris) and two taxa reported from brackish waters (copepod Microsetella norvegica and decapod Cancer irroratus) may pose a risk for invasion. In addition, four marine NIS were collected in freshwater samples indicating that at least a subset of marine species have potential as new invaders to the Great Lakes. Based on results from this study, the ports of Montreal, Sorel, Tracy and Trois Rivières appear to pose the highest risk for new ballast-mediated NIS from the St. Lawrence River to the Great Lakes.     

Dispersal of the Ponto-Caspian amphipod Echinogammarus ischnus: invasion waves from the Pleistocene to the present

The geographical range of the amphipod crustacean Echinogammarus ischnus has expanded over the past century from the Ponto-Caspian region to Western Europe, the Baltic Sea, and the Great Lakes of North America. The present study explores the phylogeographic patterns of this amphipod across its current distribution, based on an examination of nucleotide diversity in the mitochondrial cytochrome c oxidase subunit I (COI) gene. Marked genetic divergence exists among populations of E. ischnus from the Black and Caspian Seas, as well as those from the drainage system of the Black Sea. This divergence suggests the prolonged geographic isolation of these native populations, reflecting the limited dispersal capability of E. ischnus. By contrast, invading populations are characterized by a lack of genetic variation; a single mitochondrial genotype of Black Sea origin has colonized sites from the Rhine River to North America. The dispersal pattern in E. ischnus is very similar to that in the Ponto-Caspian cladoceran Cercopagis pengoi. Despite their contrasting life history strategies, these invading species followed the same route of invasion from the northern Black Sea to the Baltic Sea region, and subsequently to North America.     

Recent mass invasion of the North American Great Lakes by Ponto-Caspian species

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'.     

Climate connectivity of the bobcat in the Great Lakes region

The Great Lakes and the St. Lawrence River are imposing barriers for wildlife, and the additive effect of urban and agricultural development that dominates the lower Great Lakes region likely further reduces functional connectivity for many terrestrial species. As the climate warms, species will need to track climate across these barriers. It is important therefore to investigate land cover and bioclimatic hypotheses that may explain the northward expansion of species through the Great Lakes. We investigated the functional connectivity of a vagile generalist, the bobcat, as a representative generalist forest species common to the region. We genotyped tissue samples collected across the region at 14 microsatellite loci and compared different landscape hypotheses that might explain the observed gene flow or functional connectivity. We found that the Great Lakes and the additive influence of forest stands with either low or high canopy cover and deep lake‐effect snow have disrupted gene flow, whereas intermediate forest cover has facilitated gene flow. Functional connectivity in southern Ontario is relatively low and was limited in part by the low amount of forest cover. Pathways across the Great Lakes were through the Niagara region and through the Lower Peninsula of Michigan over the Straits of Mackinac and the St. Marys River. These pathways are important routes for bobcat range expansion north of the Great Lakes and are also likely pathways that many other mobile habitat generalists must navigate to track the changing climate. The extent to which species can navigate these routes will be important for determining the future biodiversity of areas north of the Great Lakes.     

Ancient divisions, recent expansions: phylogeography and population genetics of the round goby Apollonia melanostoma

During the past two decades, the round goby Apollonia melanostoma (= Neogobius melanostomus ) has expanded its range via shipping transport and canals, extending north and west from the Ponto-Caspian region of Eurasia and to the North American Great Lakes. Exotic populations of the round goby have been very successful in the Baltic Sea and the Great Lakes regions, exerting significant ecological changes. Our study evaluates the population genetic and biogeographical structure of the round goby across its native and nonindigenous ranges, in light of geological history and its expansion pathways. We analyzed seven new nuclear microsatellite loci and mitochondrial DNA cytochrome b gene sequences from 432 individuals in 22 locations. Population structure was tested using F _ST-analogs, phylogenetic trees, clustering diagrams, Bayesian assignment tests and nested clade analyses. Results show that native populations in the Black vs. the Caspian Sea basins diverge by 1.4% and c. 350 000 years, corresponding to closure of their prior connections and supporting the taxonomic separation of the Black Sea A. m. melanostoma from the Caspian Sea A. m. affinis . Their within-basin populations diverge by ~0.4% and 100 000 years. Nonindigenous populations in the Baltic Sea and Danube and Dnieper Rivers trace to separate northern Black Sea origins, whereas the upper Volga River system houses mixed populations of A. m. melanostoma and A. m. affinis . Native populations average twice the genetic diversity of most exotic sites; however, sites in the Volga River system have high diversity due to mixing of the two taxa. Our results highlight how vicariance and anthropogenic disturbances have shaped a rapidly expanding species' genetic heritage.     

Straddling the divide: invasive aquatic species in Illinois and movement between the Great Lakes and Mississippi basins

The Laurentian Great Lakes and the Mississippi River are two of the largest freshwater ecosystems in North America, and each contains large numbers of non-native species. In 1900 the Great Lakes and Mississippi were permanently connected with the opening of the Chicago Sanitary and Ship Canal in the US state of Illinois. More recently, movement of trailered boats, bait, and other overland vectors have increased and further enabled movement of non-native aquatic species. To investigate the role of Illinois in continent-wide species spread we assembled a comprehensive database of recorded occurrences of aquatic non-native species in Illinois inland waters. For each species we determined vector, location, current stage in the invasion sequence (introduced or established), and ecological impacts. The arrival of non-native species has accelerated over time. Sixty species are now established, and a further 39 have been recorded. The Great Lakes have been a stronger source of species to Illinois and the Mississippi River basin than the reverse. Over the last two decades the most important vectors delivering non-native aquatic species have been unintentional release and shipping. Through a survey of Illinois aquatic ecologists we found that established species exhibit a continuous range of ecological impacts and that almost a third have high or very high ecological impacts. Local, national, and continental approaches will be required to mitigate the threat of further invasive species spreading into Illinois and between the Great Lakes and Mississippi basins.     

Distribution and habitat of Nitellopsis obtusa (Characeae) in the Laurentian Great Lakes

Nitellopsis obtusa, a macroalga (Characeae) native to Europe and Asia, was found in U.S. waters of the St. Clair-Detroit River system in 1983, thus extending the range of this taxon into the Laurentian Great Lakes about 850 km from the St. Lawrence River where it was first discovered in North America in 1978. Its occurrence only in water frequented by commercial shipping vessels suggests that it is distributed via this mechanism. In the St. Clair-Detroit River system, N. obtusa was collected with a Ponar grab at four locations, and with a grapnel at one additional location. It was the ninth most frequently found macrophyte and it was most abundant at Belle Isle in the Detroit River, where the mean dry-weight biomass in Ponar samples was 0 g m^-2 in June, 37 g m^-2 in August, and 32 g m⁻² in September. Maximum biomass of this taxon in one Ponar grab at this location was 289 g m^-2 in September. The alga occurred primarily in water of relatively low current velocity (11.3 cm s⁻¹) and in association with Vallisneria americana, Myriophyllum spicatum, Potamogeton richardsonii, Najas flexilis, and Elodea canadensis. Contribution 654, Great Lakes Fishery Laboratory, Ann Arbor, MI 48105, USA Contribution 654, Great Lakes Fishery Laboratory, Ann Arbor, MI 48105, USA     

A Review of the Biology and Ecology of the Quagga Mussel (Dreissena bugensis), a Second Species of Freshwater Dreissenid Introduced to North America

SYNOPSIS. North America's Great Lakes have recently been invadedby two genetically and morphologically distinct species of Dreissena.The zebra mussel (Dreissena polymorpha) became established inLake St. Clair of the Laurentian Great Lakes in 1986 and spreadthroughout eastern North America. The second dreissenid, termedthe quagga mussel, has been identified as Dreissena bugensisAndrusov, 1897. The quagga occurs in the Dnieper River drainageof Ukraine and now in the lower Great Lakes of North America.In the Dnieper River, populations of D. polymorpha have beenlargely replaced by D. bugensis; anecdotal evidence indicatesthat similar trends may be occurring in the lower LaurentianGreat Lakes. Dreissena bugensis occurs as deep as 130 m in theGreat Lakes, but in Ukraine is known from only 0–28 m.Dreissena bugensis is more abundant than D. polymorpha in deeperwaters in Dneiper River reservoirs. The conclusion that NorthAmerican quagga mussels have a lower thermal maximum than zebramussels is not supported by observations made of populationsin Ukraine. In the Dnieper River drainage, quagga mussels areless tolerant of salinity than zebra mussels, yet both dreissenidshave acclimated to salinities higher than North American populations;eventual colonization into estuarine and coastal areas of NorthAmerica cannot be ignored.     

Dynamics of biological invasions and pathways over time: a case study of a temperate coastal sea

Coastal and regional sea ecosystems suffer from several human-induced stressors, including human mediated bioinvasions. The Baltic Sea is generally considered to be susceptible to invasions by non-indigenous species (NIS). Out of the total of 132 NIS and cryptogenic species recorded, 59% are currently established in at least one country surrounding the Baltic Sea. On average, each country currently hosts 27 such species with 15% of the established species being found in at least 50% of the countries. Benthic macroinvertebrates dominate, both among those recorded (48%) and established (59%) species. Shipping, deliberate stocking and natural spread of NIS previously introduced to the North Sea are the main introduction pathways, with considerable dynamics over time. Amongst the pathways responsible for the currently established species, shipping and natural spread strongly dominate. Substantial uncertainty in the information on introduction pathways (except for deliberate releases) hampers detailed analyses and poses major challenges for management. Spatio-temporal variability in the invasion dynamics reflects both the spatial differences in the main hydrographic conditions of the Baltic Sea as well as the availability of introduction pathways. We conclude that the Baltic Sea cannot be considered as a uniform waterbody in terms of the established introduced species and at least two major regions with differing hydrographic conditions and introduction pathways can be clearly distinguished. Due to the importance of natural spread of NIS from the North Sea, regional cooperation in bioinvasion management should be enhanced in the future.     

Phylogeography and taxonomic status of trout and salmon from the Ponto‐Caspian drainages,with inferences on European Brown Trout evolution and taxonomy

Current taxonomy of western Eurasian trout leaves a number of questions open; it is not clear to what extent some species are distinct genetically and morphologically. The purpose of this paper was to explore phylogeography and species boundaries in freshwater and anadromous trout from the drainages of the Black and the Caspian Seas (Ponto‐Caspian). We studied morphology and mitochondrial phylogeny, combining samples from the western Caucasus within the potential range of five nominal species of trout that are thought to inhabit this region, and using the sequences available from GenBank. Our results suggest that the genetic diversity of trout in the Ponto‐Caspian region is best explained with the fragmentation of catchments. (1) All trout species from Ponto‐Caspian belong to the same mitochondrial clade, separated from the other trout since the Pleistocene; (2) the southeastern Black Sea area is the most likely place of diversification of this clade, which is closely related to the clades from Anatolia; (3) The species from the Black Sea and the Caspian Sea drainages are monophyletic; (4) except for the basal lineage of the Ponto‐Caspian clade, Salmo rizeensis, all the lineages produce anadromous forms; (5) genetic diversification within the Ponto‐Caspian clade is related to Pleistocene glacial waves; (6) the described morphological differences between the species are not fully diagnostic, and some earlier described differences depend on body size; the differences between freshwater and marine forms exceed those between the different lineages. We suggest a conservative taxonomic approach, using the names S. rizeensis and Salmo labrax for trout from the Black Sea basin and Salmo caspius and Salmo ciscaucasicus for the fish from the Caspian basin.     

Recent drastic changes in the gammarid fauna (Crustacea, Amphipoda) of the Vistula River deltaic system in Poland caused by alien invaders

During the last decade of 20th century, the nonindigenous gammarid species Gammarus tigrinus, Dikerogammarus haemobaphes, Pontogammarus robustoides and Obesogammarus crassus invaded the lower Vistula River and its deltaic, partly brackish regions. G. tigrinus, an oligohaline North‐American species, was introduced to western Europe in the 1950s; the remaining three species are oligohaline/freshwater Ponto‐Caspian species. All these species are now invading central and western Europe using the network of man‐made canals connecting different European river systems. In the Vistula River, the native European freshwater gammarid species Gammarus pulex and G. varsoviensis were replaced in the 1920s by the Ponto‐Caspian Chaetogammarus ischnus (syn. Echinogammarus ischnus), which in turn has been outnumbered by the more recent invasions of D. haemobaphes and P. robustoides. In brackish waters, the native Atlantic‐boreal species Gammarus zaddachi and Gammarus duebeni are replaced or at least outnumbered by G. tigrinus, P. robustoides and O. crassus. Possible invasion routes are discussed.     

Tracing recent invasions of the Ponto-Caspian mysid shrimp Hemimysis anomala across Europe and to North America with mitochondrial DNA

The mysid crustacean Hemimysis anomala ('bloody-red shrimp') is one of the most recent participants in the invasion of European inland waters by Ponto-Caspian species. Recently the species also became established in England and the Laurentian Great Lakes of North America. Using information from mitochondrial cytochrome oxidase I (COI) gene sequences, we traced the invasion pathways of H. anomala ; the inferences were enabled by the observed phylogeographical subdivision among the source area populations in the estuaries of the Ponto-Caspian basin. The data distinguish two routes to northern and western Europe used by distinct lineages. One route has been to and through the Baltic Sea and further to the Rhine delta, probably from a population intentionally introduced to a Lithuanian water reservoir from the lower Dnieper River (NW Black Sea area) in 1960. The other lineage is derived from the Danube delta and has spread across the continent up the Danube River and further through the Main–Danube canal down to the Rhine River delta. Only the Danube lineage was found in England and in North America. The two lineages appear to have met secondarily and are now found intermixed at several sites in NW Europe, including the Rhine and waters linked with the man-made Mittellandkanal that interconnects the Rhine and Baltic drainage systems.     

Historic speciation and recent colonization of Eurasian monkey gobies (Neogobius fluviatilis and N. pallasi) revealed by DNA sequences,microsatellites, and morphology

Aim Hidden diversity within an invasive ‘species’ can mask both invasion pathways and confound management goals. We assessed taxonomic status and population structure of the monkey goby Neogobius fluviatilis across Eurasia, comparing genetic variation across its native and invasive ranges. Location Native populations were analysed within the Black and Caspian Sea basins, including major river drainages (Dnieper, Dniester, Danube, Don and Volga rivers), along with introduced locations within the upper Danube and Vistula river systems. Methods DNA sequences and 10 nuclear microsatellite loci were analysed to test genetic diversity and divergence patterns of native and introduced populations; phylogenetic analysis of mtDNA cytochrome b and nuclear RAG‐1 sequences assessed taxonomic status of Black and Caspian Sea lineages. Multivariate analysis of morphology was used to corroborate phylogenetic patterns. Population genetic structure within each basin was evaluated with mtDNA and microsatellite data using F_ST analogues and Bayesian assignment tests. Results Phylogenetic analysis of mitochondrial and nuclear sequences discerned a pronounced genetic break between monkey gobies in the Black and Caspian Seas, indicating a long‐term species‐level separation dating to c. 3 million years. This pronounced separation further was confirmed from morphological and population genetic divergence. Bayesian inference showed congruent patterns of population structure within the Black Sea basin. Introduced populations in the Danube and Vistula River basins traced to north‐west Black Sea origins, a genetic expansion pattern matching that of other introduced Ponto‐Caspian gobiids. Main conclusions Both genetic and morphological data strongly supported two species of monkey gobies that were formerly identified as subspecies: N. fluviatilis in the Black Sea basin, Don and Volga Rivers, and the Kumo‐Manych Depression, and Neogobius pallasi in the Caspian Sea and Volga River delta. Genetic origins of introduced N. fluviatilis populations indicated a common invasion pathway shared with other introduced Ponto‐Caspian fishes and invertebrates.     

Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network

Aim Some nations, and the International Maritime Organization, are moving towards requirements for managing ballast water to reduce the number of alien species transported and released. These and other measures will be most efficient when targeted at ships posing the greatest risks. Here, we analyse world‐wide ship movements and port environmental conditions to explore how these risk components differ across arriving ships. Location Global, with a case study of the Laurentian Great Lakes. Methods We gathered salinity and temperature data for all global shipping ports, and data for all global ship movements during a 12 ‐month period. We applied these data to the Laurentian Great Lakes to determine which global ports may donate new species to the Great Lakes via ship traffic, and which are most environmentally similar to the Great Lakes. Results We show that ships regularly travel to the Great Lakes from all major coastal, and many inland, regions of the world. Most global ports, and thus the species in them, are separated from the Great Lakes by no more than two ship voyages. Combined with a measure of environmental similarity among global ports, we identify ship routes likely to transport species adapted for survival in the Great Lakes and global regions that may be the source of increasing future invasions. Main conclusions The Great Lakes account for a small fraction of global shipping yet are closely connected to all other ports, and the species in them, by the shipping network. Our methods and data allow risks from individual ships to be ranked so that management activities can be targeted at ships most likely to introduce new invaders. Because our data sets are global, they could be applied to ship arrivals at any global port.     

History of aquatic invertebrate invasions in the Caspian Sea

Incorporation of the fossil record and molecular markers into studies of biological invasions provides new historical perspectives on the incidence of natural and human-mediated invasions of nonindigenous species (NIS). Palaeontological, phylogeographic, and molecular evidence suggests that the natural, multiple colonizations of the Caspian basin via transient connections with the Black Sea and other basins played an important role in shaping the diversity of Caspian fauna. Geographically isolated, conspecific Ponto-Caspian lineages that currently inhabit fragmented habitats in the Ponto-Caspian region show limited genetic divergence, implying geologically recent episodes of gene flow between populations during the Pliocene to Pleistocene. Several molluscan lineages in the Caspian Sea may have descended from Lake Pannon stock before the Late Miocene isolation of the Caspian depression, about 5.8 million years ago. Anthropogenic activities during the 20th century were responsible for a 1800-fold increase in the rate of establishment of new aquatic species in the Caspian Sea compared to the preceding two million years of natural colonization. The observed success of NIS invasions during the 20th century was due primarily to human-mediated transport mechanisms, which were dominated by shipping activities (44%). Human-mediated species transfer has been strongly asymmetrical, toward the Volga Delta and Caspian Sea from or through Black and Azov Seas. Global and regional trade, particularly that mediated by commercial ships, provides dispersal opportunities for nonindigenous invertebrates, indicating that future invasions in the Caspian Sea are anticipated.     

The role of intraspecific competition in the dispersal of an invasive fish

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