Round gobies are an important part of VHSV genotype IVb ecology in the St. Lawrence River and eastern Lake Ontario

Although viral hemorrhagic septicemia virus (VHSV) is known to affect at least 28 species of Great Lakes fish, round gobies (Neogobius melanostomus) appear to be particularly affected. The first report of VHSV in New York State waters occurred in round gobies and in subsequent surveillance efforts a disproportionately high proportion of round gobies were infected with VHSV compared with other species tested. In this study, we tested the experimental susceptibility of round gobies to infection with VHSV in the laboratory, using naïve and previously exposed fish. Naïve fish were significantly more susceptible than previously exposed fish, however previously exposed fish experienced a mortality of 35% over 45 days suggesting that previous exposure did not result in complete protection. Field studies at two sites showed a significant change in prevalence over 10 weeks in the spring based on non-lethal fin and gill samples, suggesting that great care must be taken when interpreting prevalence from single sampling efforts during VHSV surveillance. There was no difference in the observed diversity of sequence types of virus from fish that tested positive during times of low or high prevalence, or during a confinement-induced laboratory epidemic. These results show that round gobies are experimentally susceptible to VHSV and that the field prevalence of VHSV in this species can vary greatly within a short period of time; these results also provide a preliminary exploration of the role round gobies may be playing in the dynamics of VHSV in the eastern Great Lakes and St. Lawrence River.     

Occurrence and Food Habits of the Round Goby in the Profundal Zone of Southwestern Lake Ontario

Little is known about the ecology of round goby (Neogobius melanostomus), an invasive benthic fish, in the profundal zone of the Great Lakes. In April 2002–2005 we caught increasing numbers of round gobies with a bottom trawl in the 45–150 m depth range of southwestern Lake Ontario. In 2005, we examined gut contents of 30 round gobies from each of three depths, 55, 95, and 130 m, and qualitatively compared gut contents with density of benthic invertebrates determined by Ponar grabs. Round goby guts contained mostly Dreissena spp. and opposum shrimp, Mysis relicta (Mysis); the frequency of occurrence of dreissenids in guts decreased with depth, whereas the frequency of occurrence of Mysis in guts increased with depth. Abundance of these invertebrates in the environment followed the same pattern, although dreissenids of optimum edible size (3–12 mm) were still abundant (1,373/m²) at 130 m, where round gobies primarily consumed Mysis, suggesting that round gobies may switch from dreissenids to more profitable prey when it is available. Other food items were ostracods and fish, with ostracods generally eaten by smaller round gobies and fish eaten by larger round gobies. Occurrence and increasing abundance of round gobies in the profundal zone and predation on Mysis by round goby could have far-reaching consequences for the Lake Ontario fish community.     

Occurrence of Cyathocephalus truncatus (Cestoda) in Fishes of the Great Lakes with Emphasis on its Occurrence in Round Gobies (Neogobius melanostomus) from Lake Huron

Cyathocephalus truncatus is a pathogenic cestode that is common in many Laurentian Great Lakes fish species, but the depth distribution of this cestode has not been studied. Cyathocephalus truncatus has been reported from 21 fish species and one hybrid representing seven orders and nine families in Lakes Superior, Michigan, Huron, and Ontario. We examined the intestinal contents of six species of fish collected in Michigan waters of Lake Huron, from DeTour to Harbor Beach, in 2001 to 2003 for the presence of this cestode species. Cyathocephalus truncatus was found in five native fish species and the exotic round goby. Prevalence (52%) and mean intensity (4.6 cestodes per infected fish) were highest in bloaters. This is the first reported occurrence of this cestode in round gobies from the Great Lakes. None of the gobies trawled from Lake Huron at depths of 27 to 46 m were infected, but prevalence and intensity of infection in round gobies increased significantly with depth from 55 to 73 m. Our diet study of round gobies indicated that they preyed heavily on amphipods (Diporeia hoyi) at depths of 55 to 73 m. Cyathocephalus truncatus was found in eight of 605 D. hoyi obtained by Ponar grab sampling. This suggests that C. truncatus eggs may be released from infected gobies and sink to deep basins with silt bottoms where D. hoyi occur.     

Metazoan Parasites of Introduced Round and Tubenose Gobies in the Great Lakes: Support for the “Enemy Release Hypothesis”

Recent invasion theory has hypothesized that newly established exotic species may initially be free of their native parasites, augmenting their population success. Others have hypothesized that invaders may introduce exotic parasites to native species and/or may become hosts to native parasites in their new habitats. Our study analyzed the parasites of two exotic Eurasian gobies that were detected in the Great Lakes in 1990: the round goby Apollonia melanostoma and the tubenose goby Proterorhinus semilunaris. We compared our results from the central region of their introduced ranges in Lakes Huron, St. Clair, and Erie with other studies in the Great Lakes over the past decade, as well as Eurasian native and nonindigenous habitats. Results showed that goby-specific metazoan parasites were absent in the Great Lakes, and all but one species were represented only as larvae, suggesting that adult parasites presently are poorly-adapted to the new gobies as hosts. Seven parasitic species are known to infest the tubenose goby in the Great Lakes, including our new finding of the acanthocephalan Southwellina hispida, and all are rare. We provide the first findings of four parasite species in the round goby and clarified two others, totaling 22 in the Great Lakes—with most being rare. In contrast, 72 round goby parasites occur in the Black Sea region. Trematodes are the most common parasitic group of the round goby in the Great Lakes, as in their native Black Sea range and Baltic Sea introduction. Holarctic trematode Diplostomum spathaceum larvae, which are one of two widely distributed species shared with Eurasia, were found in round goby eyes from all Great Lakes localities except Lake Huron proper. Our study and others reveal no overall increases in parasitism of the invasive gobies over the past decade after their establishment in the Great Lakes. In conclusion, the parasite “load” on the invasive gobies appears relatively low in comparison with their native habitats, lending support to the “enemy release hypothesis.”     

Salinity tolerance of the invasive round goby: Experimental implications for seawater ballast exchange and spread to North American estuaries

The Eurasian round goby (Neogobius melanostomus) invaded the freshwater North American Great Lakes in ~ 1990 via accidental introduction from ballast water discharge. Its genotypes in the Great Lakes traced to estuaries in the northern Black Sea, where the round goby flourishes in a variety of salinities to 22 parts per thousand (ppt). To prevent further introductions, U.S. and Canadian Coast Guard regulations now require that vessels exchange ballast water at sea before entering the Great Lakes. Since salinity tolerance of the invasive round goby population is poorly understood, we tested 230 laboratory-acclimated fish in three experimental scenarios: (1) rapid salinity increases (0–40 ppt), simulating ballast water exchange, (2) step-wise salinity increases, as during estuarine tidal fluxes or migration from fresh to saltwater, and (3) long-term survivorship and growth (to 4 months) at acclimated salinities. Almost all gobies survived experiments at 0–20 ppt, whereas none survived ≥ 30 ppt, and at 25 ppt only 15% withstood rapid changes and 30% survived step-wise increases. Ventilation frequencies were lowest at 10–15 ppt in step-wise experiments, in conditions that were near isotonic with fish internal plasma concentrations, reflecting lower energy expenditure for osmoregulation. Growth rates appeared greatest at 5–10 ppt, congruent with the larger sizes reached by gobies in Eurasian brackish waters. Thus, we predict that the Great Lakes round goby would thrive in brackish water estuaries along North American coasts, if introduced. However, oceanic salinities appear fatal to the invasive round goby, which likely cannot withstand complete seawater ballast exchanges or oceanic habitats.     

Diel Vertical Migration of Round Goby Larvae in the Great Lakes

One hypothesis for the transcontinental and intra-Great Lakes basin transfer of round gobies (Neogobius melanostomus) has been that round gobies were pumped into the ballast water of ships. During June 2005 in Lake Erie, we obtained evidence of a vertical migration of round goby larvae, when we collected 167 round goby larvae in surface ichthyoplankton net tows at night and zero during day. These results complemented similar findings from the Muskegon River estuary of Lake Michigan during 2003 and 2004, documenting diel vertical migration for the first time in larval round gobies. We suggest vertical migration behavior may have allowed larval round gobies to be transported to and within the Great Lakes via ballast water and dispersed in the Great Lakes via advection of 6.5–8.5-mm long larvae at the surface. Based on our results, if ballast water was only taken on near the surface during daylight hours from May through September when larval round gobies were present, it would have mitigated the spread of round gobies throughout the Great Lakes.     

Impacts of predation by the Eurasian round goby (Neogobius melanostomus) on molluscs in the upper St. Lawrence River

An invasive Eurasian fish, the round goby Neogobius melanostomus, has recently spread from the Great Lakes into the St. Lawrence River. We quantified prey preferences of this benthivore and determined whether its predatory impacts on molluscs in the river are similar to those in the Great Lakes. We measured the size structure of gastropods and dreissenid mussels at 13 St. Lawrence River sites where round goby densities ranged from 0 to 6 m^− 2. For four of these sites, data were available for multiple years before and after invasion. Contrary to studies in the Great Lakes, there were no consistent effects of round goby density on the size structure of dreissenids, although there was an ontogenetic diet shift toward dreissenids. However, the abundance and richness of small gastropods (≤ 14 mm) was negatively correlated with round goby density across all sites, and declined over time at three of four sites sampled before and after invasion. Median gastropod size also declined across sites with increasing round goby density. Gastropods (as well as chironomid larvae, caddisfly larvae, and ostracods) were consistently among the most preferred prey items consumed by gobies, whereas dreissenids (as well as leeches and freshwater mites) were consistently avoided. These results indicate the major role of the round goby in structuring gastropod populations in the St. Lawrence River, and highlight large-scale spatial variation in its predatory impact on dreissenid populations.     

Effectiveness of Piscicides for Controlling Round Gobies (Neogobius melanostomus)

Round gobies (Neogobius melanostomus) were introduced to the Great Lakes presumably as a result of ballast water releases from seagoing freighters returning from European water bodies. These unwelcome fish have become established in the Great Lakes region and are expanding their range to suitable portions of other interior drainage basins including the Mississippi River traversing the central United States and the Trent-Severn waterway spanning south-central Ontario. If the invasion continues, use of chemical toxicants as a control measure may be necessary. Toxicity tests of the currently registered piscicides antimycin, rotenone, 3-trifluoromethyl-4-nitrophenol (TFM), and Bayluscide^® were conducted with three fish species native to the Great Lakes and round gobies collected from the Illinois Waterway. Tests indicated that round gobies are sensitive to all of the piscicides, however, the level of sensitivity is similar to that of the native fish species tested. Therefore, currently registered piscicides have limited potential to selectively remove round gobies. Bottom-release formulations of Bayluscide^® and antimycin were also evaluated as control agents for the normally bottom-dwelling round goby. Avoidance behavior tests demonstrated that the round goby did not react to the presence of either chemical. Therefore, the bottom-release formulations may have some application for the selective removal of round gobies, and may be one of the few tools presently available to fishery managers to help limit the range expansion of this invasive fish.     

Fish and Macroinvertebrate Communities in Tributary Streams of Eastern Lake Erie with and without Round Gobies (Neogobius melanostomus, Pallas 1814)

Round gobies have had significant impacts on benthic fish and invertebrate communities in nearshore habitats of the Great Lakes. As round gobies have become more abundant in lake habitats, there has been an expansion of their populations into tributary streams and rivers. We compared stream invertebrate and fish communities in New York tributaries to Lake Erie with round gobies present and absent. Four of six benthic invertebrate metrics differed between streams with and without round gobies. Streams with round gobies present had reduced Shannon diversity, EPT richness, and EPT/chironomid ratios, and increased macroinvertebrate density relative to streams without round gobies, but there was no difference in non-Diptera density, or total taxa richness. None of the four fish metrics examined differed between streams with and without round gobies. However, darters occurred in all streams lacking round gobies, but did not occur in any streams with round gobies. Comparisons with historical fish and macroinvertebrate distributional data support our suspicion of goby-induced community changes. In these New York streams, round gobies seem to have had significant impacts on invertebrate communities via their consumptive behavior, whereas the impacts on fish communities are less evident. If round gobies continue to expand their distribution inland, the resultant alterations in macroinvertebrate communities may impact the suitability of tributary streams as spawning and nursery habitat for several sport fish species and for energy dynamics in tributary streams.     

Trends in Diporeia populations across the Laurentian Great Lakes, 1997-2009

Benthic communities in the Laurentian Great Lakes have been in a state of flux since the arrival of dreissenid mussels, with the most dramatic changes occurring in population densities of the amphipod Diporeia. In response, the US EPA initiated an annual benthic macroinvertebrate monitoring program on all five Great Lakes in 1997. Although historically the dominant benthic invertebrate in all the lakes, no Diporeia have been found in Lake Erie during the first 13 years of our study, confirming that Diporeia is now effectively absent from that lake. Populations have almost entirely disappeared from our shallow (< 90 m) sites in lakes Ontario, Huron, and Michigan. In Lake Ontario, three of our four deep (> 90 m) sites still supported Diporeia populations in 2009, with densities at those sites ranging between 96 and 198/m². In Lake Michigan, populations were still found at six of our seven deep sites in 2009, with densities ranging from 57 to 1409/m². Densities of Diporeia in 2009 at the four deep sites in Lake Huron were somewhat lower than those in Lake Michigan, ranging from 191 to 720/m². Interannual changes in population size in Lake Huron and Lake Michigan have shown a degree of synchrony across most sites, with periods of rapid decline (1997-2000, 2003-2004) alternating with periods of little change or even increase (2001-2002, 2005-2009). There has been no evidence of directional trends at any sites in Lake Superior, although substantial interannual variability was seen.     

First occurrence of the mysid Hemimysis anomala in an inland lake in North America,Oneida Lake,NY

Hemimysis anomala (Crustacea, Mysidae) is a recent invader to North America that until now was reported only from the Laurentian Great Lakes and their immediate embayments, along with the St. Lawrence River. In August 2009, we identified Hemimysis in diets of white perch and yellow perch in Oneida Lake, NY. Night time vertical plankton net tows detected Hemimysis at four sites across the lake. Hemimysis in fish diets (5.5–8.6 mm) were larger than in net tows (2.2–7.0 mm) and reproduction is occurring as some females had brood sacs. This is the first documented introduction of Hemimysis to an inland lake in North America, outside the Great Lakes. Oneida Lake is located 53 river km upstream from Lake Ontario, the nearest known source of Hemimysis. No genetic differences were found between Hemimysis in Oneida Lake and Lake Ontario, indicating this is likely the source of introduction. Several large rapids, locks, and dams separate the two lakes, and as a result the most likely vector of introduction to Oneida Lake is pleasure boat or light commercial traffic via the canal system or overland transport. The presence of Hemimysis in Oneida Lake 3 years after it was first found in Lake Ontario suggests this species may spread rapidly throughout the basin. Despite an intensive monitoring program on Oneida Lake directed at fish, zooplankton, and limnology, Hemimysis was only detected in fish diets and night time zooplankton tows, indicating it may go undetected in lakes for some time using traditional daytime net tows.     

Diet shift of double-crested cormorants in eastern Lake Ontario associated with the expansion of the invasive round goby

The proliferation of the invasive round goby (Apollonia melanostoma) in the Great Lakes has caused shifts in the trophic ecology in some areas. We examined the diet of double-crested cormorants (Phalacrocorax auritas) prior to, and immediately after, round goby population expansion at two colonies, Pigeon and Snake Islands, in eastern Lake Ontario from 1999 to 2007. Cormorant diet was determined from the examination of 10,167 pellets collected over the nine-year period. By the second year round gobies were found in the diet (2002 at Snake Island and 2003 at Pigeon Island) they were the main species consumed by cormorants at each colony. The dominance of round goby in cormorant diets had a significant effect on both daily fish consumption and seasonal trends in fish consumption compared to the pre-goby years. Seasonal differences that were observed during the pre-goby years were lost once gobies became the main diet component of cormorants. The rapid switch to a benthic prey such as round goby, from a largely limnetic fish diet demonstrates the adaptive foraging ability of cormorants. Round goby may act as a buffer for yellow perch and smallmouth bass, two sport fish impacted by cormorant predation in eastern Lake Ontario.     

Significance of toxaphene in Great Lakes fish consumption advisories

Fish consumption advisories have been issued for the Great Lakes generally based on the most restrictive contaminant. For the Canadian waters of the Great Lakes, toxaphene causes minor restrictions only in Lake Superior, i.e., 3% of the total (restrictive + unrestrictive) advisories issued. However, the significance of the hazard posed by toxaphene in fish is not clear since more restrictive advisories due to other priority contaminants may be masking the less restrictive advisories. We simulated fish consumption advisories for the Toxaphene-only scenario by neglecting the presence of contaminants other than toxaphene, and compared with the issued advisories as well as with the published simulated Mercury-only scenario. Restrictive advisories under the Toxaphene-only scenario compared to the issued toxaphene related advisories would increase from 3% to 14%, < 1% to 4%, and 0% to 2% for Lakes Superior, Huron and Ontario, respectively, and remain at 0% for Lake Erie. For Lake Superior, most of the restrictive Toxaphene-only advisories would be for fatty fish. Overall, the Toxaphene-only advisories would be significantly less restrictive compared to the issued advisories, and also generally less restrictive compared to the Mercury-only scenario. These results suggest that toxaphene is less of a concern than PCBs (including dioxin-like PCBs), dioxins–furans and mercury from the perspective of health risk to humans consuming Great Lakes fish; elevated toxaphene is mainly a concern for human consumers of Lake Superior fatty fish. Our results suggest that the routine monitoring of toxaphene in other Canadian waters of the Great Lakes and Lake Superior lean/pan fish could be discontinued.     

Historical changes and current status of crayfish diversity and distribution in the Laurentian Great Lakes

Despite increasing recognition of the importance of invertebrates, and specifically crayfish, to nearshore food webs in the Laurentian Great Lakes, past and present ecological studies in the Great Lakes have predominantly focused on fishes. Using data from many sources, we provide a summary of crayfish diversity and distribution throughout the Great Lakes from 1882 to 2008 for 1456 locations where crayfish have been surveyed. Sampling effort was greatest in Lake Michigan, followed by lakes Huron, Erie, Superior, and Ontario. A total of 13 crayfish species occur in the lakes, with Lake Erie having the greatest diversity (n = 11) and Lake Superior having the least (n = 5). Five crayfish species are non-native to one or more lakes. Because Orconectes rusticus was the most widely distributed non-native species and is associated with known negative impacts, we assessed its spread throughout the Great Lakes. Although O. rusticus has been found for over 100 years in Lake Erie, its spread there has been relatively slow compared to that in lakes Michigan and Huron, where it has spread most rapidly since the 1990s and 2000, respectively. O. rusticus has been found in both lakes Superior and Ontario for 22 and 37 years, respectively, and has expanded little in either lake. Our broad spatial and temporal assessment of crayfish diversity and distribution provides a baseline for future nearshore ecological studies, and for future management efforts to restore native crayfish and limit non-native introductions and their impact on food web interactions.     

In vivo and in vitro phenotypic differences between Great Lakes VHSV genotype IVb isolates with sequence types vcG001 and vcG002

Viral hemorrhagic septicemia virus (VHSV) is an aquatic rhabdovirus first recognized in farmed rainbow trout in Denmark. In the past decade, a new genotype of this virus, IVb was discovered in the Laurentian Great Lakes basin and has caused several massive die-offs in some of the 28 species of susceptible North American freshwater fishes. Since its colonization of the Great Lakes, several closely related sequence types within genotype IVb have been reported, the two most common of which are vcG001 and vcG002. These sequence types have different spatial distributions in the Great Lakes. The aim of this study was to determine whether the genotypic differences between representative vcG001 (isolate MI03) and vcG002 (isolate 2010-030 #91) isolates correspond to phenotypic differences in terms of virulence using both in vitro and in vivo approaches. In vitro infection of epithelioma papulosum cyprini (EPC), bluegill fry (BF-2), and Chinook salmon embryo (CHSE) cells demonstrated some differences in onset and rate of growth in EPC and BF-2 cells, without any difference in the quantity of RNA produced. In vivo infection of round gobies (Neogobius melanostomus) via immersion exposure to different concentrations of vcG001 or vcG002 caused a significantly greater mortality in round gobies exposed to 10² plaque forming units ml^− 1 of vcG001. These experiments suggest that there are phenotypic differences between Great Lakes isolates of VHSV genotype IVb.     

Hydrology influences generalist–specialist bird-based indices of biotic integrity in Great Lakes coastal wetlands

Marsh bird habitats are influenced by water levels which may pose challenges for interpreting bird-based indices of wetland health. We determined how much fluctuating water levels and associated changes in emergent vegetation influence the Index of Marsh Bird Community Integrity (IMBCI) using data collected in Great Lakes coastal wetlands by participants in Bird Studies Canada's Great Lakes Marsh Monitoring Program. IMBCI scores for 90 wetlands in Lake Erie and 131 wetlands in Lake Ontario decreased with decreasing water levels due to decreasing number of marsh-dependent species in Lake Erie and perhaps also in Lake Ontario. The average magnitude of the decrease in scores between extremely high and low water periods for wetlands with sufficient data was 15% in Lake Erie where water dropped 0.9 m on average (n = 11 wetlands) and 18% in Lake Ontario where water dropped 0.5 m (n = 7). Scores in Lake Erie increased with increasing Typha due to increasing numbers of marsh-dependent species and decreased with increasing Phragmites due to increasing numbers of generalist species. The opposite was observed in Lake Ontario, perhaps due to denser Typha and sparser Phragmites. Scores were explained by the naturally fluctuating water levels of Lake Erie, which favored Phragmites expansion and the regulated water levels of Lake Ontario which promoted Typha expansion. Scores were influenced by fluctuating water levels and associated changes in emergent vegetation. Inter-annual water level fluctuations should be considered when interpreting any indicator of wetland health that is based on marsh-dependent bird species.     

Rapid response of the nearshore round goby population to temperature declines associated with upwelling events in Lake Ontario

Upwellings occur in all the Great Lakes in response to prolonged wind events. Several studies have modeled or measured changes in abiotic conditions associated with upwellings, but few direct observations of fish responses have been documented. Video-capture techniques were used in conjunction with moored temperature loggers to link the disappearance of benthic round gobies to temperature declines during upwelling events along the southern Lake Ontario nearshore in summer of 2019. Benthic water temperatures declined by as much as 18 °C within 18 h over as many as nine events. Round goby density estimates were as high as 50/m² prior to upwellings, but declined to as low as 0/m² during the events. Using just nine observation dates, ARMA trend analysis suggested a relationship between benthic temperature and round goby abundance (AIC = 78.7, t = 2.21, P = 0.063). Although the actual response of gobies to rapidly declining temperatures was unknown, this population was unobservable in our sample area during upwellings, yet returned to pre-upwelling densities within days. Understanding the magnitude and frequency of fish responses to these events can improve our understanding of the potential for this non-native benthic fish to affect the nearshore environment.     

Acoustic estimates of abundance and distribution of spawning lake trout on Sheboygan Reef in Lake Michigan

Efforts to restore self-sustaining lake trout (Salvelinus namaycush) populations in the Laurentian Great Lakes have had widespread success in Lake Superior; but in other Great Lakes, populations of lake trout are maintained by stocking. Recruitment bottlenecks may be present at a number of stages of the reproduction process. To study eggs and fry, it is necessary to identify spawning locations, which is difficult in deep water. Acoustic sampling can be used to rapidly locate aggregations of fish (like spawning lake trout), describe their distribution, and estimate their abundance. To assess these capabilities for application to lake trout, we conducted an acoustic survey covering 22 km² at Sheboygan Reef, a deep reef ( < 40 m summit) in southern Lake Michigan during fall 2005. Data collected with remotely operated vehicles (ROV) confirmed that fish were large lake trout, that lake trout were 1–2 m above bottom, and that spawning took place over specific habitat. Lake trout density exhibited a high degree of spatial structure (autocorrelation) up to a range of ∼ 190 m, and highest lake trout and egg densities occurred over rough substrates (rubble and cobble) at the shallowest depths sampled (36–42 m). Mean lake trout density in the area surveyed (∼ 2190 ha) was 5.8 fish/ha and the area surveyed contained an estimated 9500–16,000 large lake trout. Spatial aggregation in lake trout densities, similarity of depths and substrates at which high lake trout and egg densities occurred, and relatively low uncertainty in the lake trout density estimate indicate that acoustic sampling can be a useful complement to other sampling tools used in lake trout restoration research.