Igor A. Grigorovich

Propagule Pressure: A Null Model for Biological Invasions

Invasion ecology has been criticised for its lack of general principles. To explore this criticism, we conducted a meta-analysis that examined characteristics of invasiveness (i.e. the ability of species to establish in, spread to, or become abundant in novel communities) and invasibility (i.e. the susceptibility of habitats to the establishment or proliferation of invaders). There were few consistencies among invasiveness characteristics (3 of 13): established and abundant invaders generally occupy similar habitats as native species, while abundant species tend to be less affected by enemies; germination success and reproductive output were significantly positively associated with invasiveness when results from both stages (establishment/spread and abundance/impact) were combined. Two of six invasibility characteristics were also significant: communities experiencing more disturbance and with higher resource availability sustained greater establishment and proliferation of invaders. We also found that even though ‘propagule pressure’ was considered in only ~29% of studies, it was a significant predictor of both invasiveness and invasibility (55 of 64 total cases). Given that nonindigenous species are likely introduced non-randomly, we contend that ‘propagule biases’ may confound current paradigms in invasion ecology. Examples of patterns that could be confounded by propagule biases include characteristics of good invaders and susceptible habitats, release from enemies, evolution of ‘invasiveness’, and invasional meltdown. We conclude that propagule pressure should serve as the basis of a null model for studies of biological invasions when inferring process from patterns of invasion.Invasion ecology has been criticised for its lack of general principles. To explore this criticism, we conducted a meta-analysis that examined characteristics of invasiveness (i.e. the ability of species to establish in, spread to, or become abundant in novel communities) and invasibility (i.e. the susceptibility of habitats to the establishment or proliferation of invaders). There were few consistencies among invasiveness characteristics (3 of 13): established and abundant invaders generally occupy similar habitats as native species, while abundant species tend to be less affected by enemies; germination success and reproductive output were significantly positively associated with invasiveness when results from both stages (establishment/spread and abundance/impact) were combined. Two of six invasibility characteristics were also significant: communities experiencing more disturbance and with higher resource availability sustained greater establishment and proliferation of invaders. We also found that even though ‘propagule pressure’ was considered in only ~29% of studies, it was a significant predictor of both invasiveness and invasibility (55 of 64 total cases). Given that nonindigenous species are likely introduced non-randomly, we contend that ‘propagule biases’ may confound current paradigms in invasion ecology. Examples of patterns that could be confounded by propagule biases include characteristics of good invaders and susceptible habitats, release from enemies, evolution of ‘invasiveness’, and invasional meltdown. We conclude that propagule pressure should serve as the basis of a null model for studies of biological invasions when inferring process from patterns of invasion.

Lake Superior: An invasion coldspot?

Lake Superior receives a disproportionate number of ballast water discharges from transoceanic ships operating on the Laurentian Great Lakes. Although this provides dispersal opportunities for nonindigenous species (NIS), relatively few NIS were initially discovered in this lake prior to being recorded elsewhere in the basin. A lack of NIS records from this lake may be an artefact of sampling bias. We tested this hypothesis by sampling benthos and plankton from littoral and deepwater habitats around the perimeter of Lake Superior during June and August 2001. Using morphological analysis techniques, we identified a total of 230 invertebrate taxa representing planktonic, benthic and nektonic lifestyles. Five species with invasion histories in the lower Great Lakes, the bivalves Sphaerium corneum, Pisidium amnicum and P. moitessierianum, gastropod Potamopyrgus antipodarum and amphipod Echinogammarus ischnus, were identified for the first time in Lake Superior. In addition, records of expanded distributions within this lake are presented for the amphipod Gammarus fasciatus and oligochaetes Ripistes parasita and Vejdovskyella intermedia. Recently introduced NIS in Lake Superior were found near international ports, implicating shipping as the vector of their introduction. Intrinsic physical-chemical aspects of Lake Superior may account for the scarcity of NIS in this lake as compared to the lower Great Lakes.

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.

Introduction of the Ponto-Caspian Bloody-red Mysid Hemimysis anomala into the Lake Michigan Basin

ABSTRACT Hemimysis anomala G.O. Sars, 1907, a mysid species native to the Ponto-Caspian region, was discovered during fall 2006 in the Lake Michigan basin. Large numbers of individuals formed aggregations (averaging 1,540 ± 333 individuals/m2) in a shallow docking basin connected to the channel linking Lake Michigan and Muskegon Lake. The population included females (63%), males (35%), and juveniles (2%). The global invasion pattern in H. anomala is similar to that in another Ponto-Caspian peracarid crustacean, Echinogammarus ischnus. As with E. ischnus, the expansion of H. anomala in North America is anticipated.

Distribution, Fecundity, and Genetics of Cercopagis pengoi (Ostroumov) (Crustacea, Cladocera) in Lake Ontario

Two distinctive forms of cercopagids, first detected in 1998 and identified as Cercopagis pengoi and C. ossiani using taxonomic keys, were observed to co-occur in Lake Ontario. C. ossiani was the predominant form in western Lake Ontario in mid-June 1999 but was then replaced by C. pengoi-like animals over the rest of the season. Mitochondrial DNA analyses revealed that these forms were genetically identical at the ND5 gene and that they are morphologically distinctive forms of C. pengoi. In 1999, Cercopagis reached a maximum abundance of 1,759 individuals/m3 (average abundance = 281 individuals/ m3, average biomass = 5.2 mg/m3). In August, Cercopagis biomass was lowest at nearshore and embayment sites and highest at offshore sites. Body length of parthenogenetic females was lower at nearshore (1.16 mm) and embayment (1.19 mm) sites relative to offshore (1.32 mm) ones. Maximal clutch size of parthenogenetic females was 24 embryos per individual. Cercopagis has already spread to Lake Michigan and five Finger Lakes. Although waterfowl may disperse Cercopagis, these invasions likely resulted from human activities.

Filtering Impacts of an Introduced Bivalve (Dreissena polymorpha) in a Shallow Lake: Application of a Hydrodynamic Model

ABSTRACT Nonindigenous species may exert strong effects on ecosystem structure and function. The zebra mussel (Dreissena polymorpha) has been attributed with profound changes in invaded ecosystems across eastern North America. We explored vertical profiles of water flow velocity and chlorophyll a concentration in western Lake Erie, over rocky substrates encrusted with Dreissena, to assess the extent to which mussels influence coupling between benthic and pelagic regions of the lake. Flow velocity was always low at surveyed sites (less than or equal to 2.9 cm s-1) and declined in direct proximity to the lakebed. Mean chlorophyll a concentration was also low (less than 5μg L-1) at all sites and depths. Chlorophyll a concentration was positively correlated with distance above lakebed and was lowest (0.3μg L-1) directly adjacent to the lakebed. Spatial patterns of zooplankton grazers could not explain observed vertical gradients in chlorophyll concentration. Hydrodynamic modeling revealed that filtering effects of Dreissena in a nonstratified, shallow basin depend mainly on upstream chlorophyll concentration, intensity of turbulent diffusion, feeding efficiency of the mussel colony, and the distance downstream from the leading edge of the mussel colony. In contrast to widespread perceptions that molluscs reduce phytoplankton concentration only adjacent to the lakebed, modeling scenarios indicated that depletion occurs throughout the water column. Depletion was, however, inversely proportional to distance above the lakebed. Simulation results are consistent with field-based observations made in shallow water habitats populated by large Dreissena populations in the Great Lakes and elsewhere. Results from this study indicate that zebra mussels strongly enhance coupling between pelagic and benthic regions in shallow lakes. Enhanced coupling between these regions explains, in part, high population densities of Dreissena and of many benthic invertebrates in ecosystems invaded by zebra mussels.

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.

The Quagga Mussel Invades the Lake Superior Basin

ABSTRACT Prior studies recognized the presence of a single dreissenid species in Lake Superior—the zebra mussel Dreissena polymorpha. However, taxonomic keys based on traditional shell morphology are not always able to differentiate dreissenid species with confidence. We thus employed genetic and morphological analyses to identify dreissenids in a major river-embayment of Lake Superior—the lower St. Louis River/Duluth-Superior Harbor—during 2005–2006. Our results revealed the presence of a second dreissenid species—the quagga mussel D. bugensis (alternatively known as D. rostriformis bugensis). Both species occurred in mixed clusters, in which zebra mussels outnumbered quagga mussels (20–160:1). The largest quagga mussel collected in 2005 was 26.5 mm long and estimated to be two years old, suggesting that the initial introduction occurred no later than 2003. Further monitoring is necessary to determine whether the quagga mussel will colonize Lake Superior. Our results indicate that the coupling of conventional morphological and molecular approaches is essential for monitoring dreissenid species.

Range Expansion of the Exotic Zooplankter Cercopagis pengoi (Ostroumov) into Western Lake Erie and Muskegon Lake

Previously reported from Lakes Ontario and Michigan, the nonindigenous zooplankter Cercopagis pengoi was found for the first time in western Lake Erie, the Detroit River, and Muskegon Lake, Michigan, during summer 2001. A native of the Ponto-Caspian region, C. pengoi is currently expanding its range in North America. Analysis of mitochondrial gene ND5 sequences confirmed that the Lake Erie haplotype is identical to that reported previously from Lakes Ontario and Michigan and the Finger Lakes, New York. These findings support the hypothesis that C. pengois range expansion in the Great Lakes likely resulted from inter-lake transfer of ballast water, rather than from additional introductions from European locations. Pleasure-craft traffic operating between Lake Michigan and Muskegon Lake is likely responsible for this inland transfer of Cercopagis, a trend that likely will increase due to human activities.

Status of Non-Indigenous Benthic Invertebrates in the Duluth-Superior Harbor and the Role of Sampling Methods in Their Detection

ABSTRACT As part of a study to develop recommendations for non-indigenous species (NIS) monitoring in Great Lakes areas at risk of invasion, we conducted intensive sampling in the Duluth-Superior Harbor and lower St. Louis River in 2005 and 2006. Of the ∼240 benthic invertebrate taxa identified, 19 were non-indigenous, including 8 first detection records for this system: New Zealand mud snail Potamopyrgus antipodarum; African/Asianorigin cladoceran Daphnia lumholtzi; Eurasian-origin amphipod Echinogammarus ischnus; Eurasian-origin bivalves Dreissena bugensis, Pisidium henslowanum and Pisidium supinum; and possibly range expanding oligochaetes Paranais frici and Pristina acuminata. Dreissenids were by far the most abundant NIS. Several other NIS were also common, but others were detected in only a few of the >200 samples taken. Non-indigenous amphipods and Dreissena were most frequently detected in sweep net and colonization plate samples of littoral vegetation, while NIS oligochaetes, gastropods, and non-dreissenid bivalves were most frequently detected in ponar and bottom sled samples of sediments. Our findings confirm that this major shipping port remains a NIS “hotspot” and emphasize that regular surveys covering a range of habitats with multiple sampling gears and thorough taxonomic effort are needed to detect and monitor non-indigenous species.