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.”     

Round Goby and Mottled Sculpin Predation on Lake Trout Eggs and Fry: Field Predictions from Laboratory Experiments

The accidental introduction of round gobies (Neogobius melanostomus) into the North American Great Lakes has raised concerns about their potential impacts on local fauna. Gobies have similar habitat and spawning requirements to mottled sculpins (Cottus bairdi) and slimy sculpins (C. cognatus), and may already be displacing sculpins where the ranges of the species overlap. Like sculpins, gobies are capable of penetrating interstitial spaces to acquire food, and therefore may become predators of interstitially incubating lake trout eggs. Laboratory experiments were conducted to compare egg consumption rates and critical size (the minimum size at which a fish was capable of ingesting an egg) between round gobies and mottled sculpins. Predation by both species on lake trout eggs and fry was also examined in two grades of substrate (cobble and gravel). Mottled sculpins consumed larger numbers of eggs than round gobies of similar size, and were capable of ingesting eggs at smaller sizes than gobies. Both gobies and sculpins had lower foraging success on smaller substrates (gravel) than on cobble. Gobies are currently present at higher densities than sculpins in areas where they are established in the Great Lakes. The similar predation of lake trout eggs by round gobies and mottled sculpin and high densities the goby has achieved at some Great Lakes sites leads to the prediction that the round goby may negatively affect lake trout reproduction and therefore rehabilitation.     

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.     

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.     

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.     

Factors governing the distribution and fish-community associations of the round goby in Michigan tributaries of the Laurentian Great Lakes

The round goby (Neogobius melanostomus) is increasingly being reported in tributaries of the Laurentian Great Lakes where these fish have been shown to adversely impact native stream biota. Determining the characteristics and distribution of invaded streams are the first steps toward effective round goby management. We sampled 30 tributaries in the Great Lakes basin and characterized each in terms of nine physical reach-scale attributes. Round goby were detected in 14 streams where abundances ranged from 4% to 53% of the fish sampled in each stream. Round goby was the single most abundant fish species sampled, constituting 14% of all fish encountered across all sites, and 30% of individuals in round goby-present sites. Round goby-present sites were larger, had lower channel slopes, less large wood, and less canopy cover than round goby-absent sites, suggesting that these attributes may promote round goby establishment. Mottled sculpin, cyprinids, brook stickleback, white sucker and rainbow trout were associated with goby absence while centrarchids, percids, yellow bullhead, and mud minnow were associated round goby presence. Collectively these results demonstrate that round goby are widespread in eastern Michigan tributaries to the Great Lakes, present in streams with a range of physical habitat characteristics, and that round goby presence is associated with certain fish species.     

Comparison of thermal tolerance and standard metabolic rate of two Great Lakes invasive fish species

Round goby (Neogobius melanostomus) and western tubenose goby (Proterorhinus semilunaris) invaded the Laurentian Great Lakes at approximately the same time and area yet have shown substantial differences in their post-invasion success with more rapid establishment and development of much larger abundances of round goby populations throughout the invaded habitat. In this study, we compared differences in physiological performance (thermal tolerance and standard metabolic rate) between round and tubenose goby collected from the Huron-Erie corridor. Tubenose goby were observed to have lower thermal tolerance but exhibited similar standard metabolic rate across environmental temperatures compared to round goby. At temperatures exceeding 31 °C, tubenose goby demonstrated significantly higher mortalities and shorter times to death relative to round goby. The observed differences in thermal tolerance were consistent with differences in the native geographic ranges observed for each species at their southern ranges. The observed differences in physiological performance combined with species differences in other life history traits such body size, reproduction, feeding ecology and habitat affiliation may also explain differences in the invasiveness experienced by these two Great Lakes invasive fish including a greater ability of round gobies to occupy extreme habitats with large water temperature fluctuations.     

Size preferences and behaviors of native yellow perch foraging on invasive round gobies

Predation is one of the primary mechanisms that shape aquatic food webs and predator–prey interactions are typically highly dependent on sizes of both forager and its prey. Round goby Neogobius melanostomus is a recent invader to the Great Lakes and can be an important prey item for native predators. However, predation patterns on round gobies have received limited attention. We assessed size-specific predator–prey interactions between invasive round gobies and native yellow perch Perca flavescens by comparing prey preferences for three size classes of adult yellow perch foraging on six size classes of round gobies. Small yellow perch preferred the smallest round gobies available, medium sized yellow perch increased the range of round goby sizes consumed but still preferred smaller prey, whereas large yellow perch consumed larger round gobies and excluded the smallest prey size. Yellow perch foraging behaviors indicated that intermediate sizes of round gobies were struck at most frequently and that pursuit and handling time increased whereas capture efficiency and prey profitability decreased with round goby size. Our results indicate that predator–prey interactions between yellow perch and round gobies may be size dependent and heavily influenced by capture efficiency and prey profitability.     

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.     

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.     

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.     

Genetic and Biogeographic Relationships of the Invasive Round (Neogobius melanostomus) and Tubenose (Proterorhinus marmoratus) Gobies in the Great Lakes Versus Eurasian Populations

Population genetic structure and systematic relationships were investigated for two exotic fishes introduced to the Great Lakes in 1990, the round goby Neogobius melanostomus and the tubenose goby Proterorhinus marmoratus, using DNA sequences from the left domain of the mitochondrial DNA control region. Samples of round gobies were compared from different sites in the Great Lakes, an introduced population from the Gulf of Gdansk in Poland, and a native population from the northern Black Sea. The round goby was characterized by relatively high genetic variability, and 17 haplotypes were identified from 64 individuals. Levels of genetic variation for the round goby were similar in the invasive and native sampling sites, suggesting relatively large founding populations and lack of bottlenecks. The northern Black Sea was eliminated as a probable founding source for both the Great Lakes and the exotic population in Poland. Substitutions in the left domain of the control region revealed significant differences among samples from the Great Lakes and Eurasia, and between Lakes Erie and St. Clair, suggesting non-random mating. No variation was detected in the tubenose goby population in the Great Lakes, which has been less successful in terms of spread and population growth. A molecular clock calibration suggested that the genera Neogobius and Proterorhinus diverged about 5.2 ± 1.0 million years ago, apparently separating from a common ancestor shared with Gobius during the isolation of the Paratethys basin from the Mediterranean Tethys Sea.     

Comparison of Methods Needed to Estimate Population Size of Round Gobies (Neogobius melanostomus) in Western Lake Erie

The round goby (Neogobius melanostomus) is a small, demersal fish that was introduced into the Great Lakes basin in 1990. Since their arrival, the round goby has been implicated in many ecological changes—most notably changes in the flow of energy from the benthic to the pelagic food web through their consumption of dreissenid mussels. However, methods for evaluating the density and size of round gobies across different substrates are lacking, preventing the true quantification of the effects of round gobies on invaded ecosystems. In our study, we evaluated catch efficiency of numerous passive and active sampling methods for capturing round gobies. We then applied the best techniques to estimate the distribution, density, and biomass of round gobies in western Lake Erie. Visual census (underwater video transects) proved the best technique for assessing round goby size and density across a wide range of substrates. A combination of angling and bottom trawling proved most effective for obtaining biological samples. We estimated 9.9 billion round gobies in western Lake Erie in 2002. Continued efforts to describe abundance and demographics of round gobies in invaded ecosystems will enable scientists and managers to fully understand the impacts of this invading species.     

Use of wetland versus open habitats by round gobies in lakes Michigan and Huron: Patterns of CPUE,length, and maturity

It has been suggested that some Great Lakes coastal wetlands may be resistant to invasion by several non-indigenous species including round goby, Neogobius melanostomus. However, there is inconclusive evidence regarding how susceptible exposed fringing coastal wetlands, in particular, are to round goby invasion. Therefore, we quantified round goby catch per unit effort (CPUE) using fyke nets in the Beaver Archipelago of Lake Michigan, and the Les Cheneaux islands and Saginaw Bay regions of Lake Huron. In addition, we examined the influence of body size and maturity on round goby habitat use. Catch per unit effort from fyke nets was highest in the Beaver Archipelago, where wetlands were dominated by small, immature round gobies and open water habitats were dominated by large adults. Fyke net catches within Les Cheneaux sites were similar between habitats and differences in size and maturity were not observed. Conversely, very few round goby were captured in wetlands of Saginaw Bay where CPUE was moderate in open water. This indicates that some exposed fringing wetlands in the Great Lakes, specifically those with high productivity, could have a higher degree of resistance to round goby invasion.     

Diet,trophic position of upper St. Lawrence River round goby giants reveals greater dependence on dreissenids with increasing body size

Round gobies (Neogobius melanostomus) from the upper St. Lawrence River (USLR) have an abundance of some of the largest individuals recorded from the Great Lakes (>230-mm total-length). We found a distinct separation in diet and isotopic signatures (δ¹⁵N and δ¹³C) between round goby classified as small (≤130-mm; n = 63) and large (>130-mm total-length; n = 75) from USLR coastal bays. At small sizes, round gobies had variable diets indicative of generalist and opportunistic feeding on native and non-indigenous benthic prey. Between 100 and 130-mm total-length, signatures of assimilated carbon (δ¹³C) indicated a directed shift towards a dreissenid-centric diet and once larger than 130-mm total-length, round gobies appeared to feed proportionally more on dreissenid mussels. We also found that large round gobies fed proportionally more on Hydrobiidae than small round gobies. A weak negative relationship between δ¹⁵N (indicative of trophic position) and round gobies total length resulted where smaller round gobies had slightly higher δ¹⁵N values than larger conspecifics. Round gobies larger than 180-mm total-length were common in nearshore habitats (≤2-m) during the spring, and dreissenid mussels and Hydrobiidae were the most frequently encountered prey. Our results demonstrate elevated reliance on dreissenids as round goby increased body size, but the diversity of prey suggest more complex trophodynamic pathways associated with coastal bay habitats.     

Dietary niche and growth rate of the nonnative tubenose goby (Proterorhinus semilunaris) in the Lake Superior basin

The tubenose goby (Proterorhinus semilunaris) entered the Great Lakes in the 1990s via ballast water, but remains poorly studied within North America, making it difficult to predict its effects on native ecosystems. Dietary breadth and somatic growth rate have important ramifications for survival, competitiveness, and dispersal ability of a fish species, and thereby its ecological impact. We studied diet and growth of age-0 tubenose goby within the St. Louis River, a tributary to Lake Superior that contains the largest population within the Lake Superior basin. We sampled tubenose gobies from shallow, vegetated habitats during summer and fall. Stomach contents were identified and weighed to measure fullness and dietary breadth between seasons and several locations. We aged fish based on otolith daily increments to model somatic growth. Diet was dominated by isopods and amphipods, and dietary breadth was low and not significantly different between locations and seasons. Tubenose goby diet strongly overlapped with that of tadpole madtom (Noturus gyrinus), a native, demersal species. We tested several candidate growth models; the Gompertz growth function was the most parsimonious model among those examined. The model demonstrates that tubenose goby obtains a small maximum size and is short-lived. We conclude that tubenose goby presents a unique risk to the Great Lakes and other freshwater bodies because their life history is typical of invasive species, their diet overlaps with native fish, and because they occupy shallow, vegetated habitat which functions as both nursery and foraging habitat for many native fishes.     

Fish Assemblages and Environmental Variables Associated with Gobiids in Nearshore Areas of the Lower Great Lakes

We investigated which fish species and environmental variables were associated with the invasive round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus marmoratus) in nearshore Canadian waters of the Huron-Erie corridor of the lower Great Lakes. We measured a suite of environmental variables and used triplicate beach seine samples to collect fishes in summer 2006. Thirty sites were sampled in the day and a subset (n = 14) at night. Of 1,955 individuals caught in daytime samples, round goby (21.0 %), spottail shiner (17.3%) and emerald shiner (14.2%) were most abundant. Of 1,521 individuals collected at night, the most abundant species were round goby (42.3%) and emerald shiner (24.1%). Tubenose gobies represented 1% and 1.7% of all individuals caught in the day and night, respectively. Rarefaction analysis showed that overall species richness was greater in the day than night. Significantly more emerald shiner (P = 0.017), rock bass (P = 0.046) and round goby (P = 0.035) were caught at night than in the day; more logperch were caught in the day than at night (P = 0.042). Round gobies were positively associated with water temperatures up to 24°, but there was no relationship between round goby abundance and warmer temperatures. There were too few tubenose goby captured to determine their statistical association with environmental factors; however, tubenose gobies were found only where round gobies were collected. Round goby and tubenose goby were associated with yellow perch and rock bass. The benthic round goby was the most abundant species, whereas other abundant species were pelagic, schooling fishes that occupied a habitat distinct from round goby.     

Habitat and Site Affinity of the Round Goby

A study was conducted in 1996 to compare densities of the round goby (Neogobius melanostomus) in rock and sand habitats in day and night at three sites (Sarnia, St. Clair River; town of Belle River, Lake St. Clair; Peche Island, Detroit River). The sites represent an expansion in round goby distribution from Sarnia where gobies were first reported in 1990 downstream to Peche Island where gobies appeared in 1993. Site affinity at Peche Island was estimated using mark-recapture and observations of individual fish. Mean density of round gobies differed among sites (p < 0.001), light regime (p < 0.001), habitat (p < 0.001), and the interaction of light regime and site (p = 0.007). Mean densities of the round goby were 0.3 to 3 fish/m² (Peche Island), 0.5 to 3 fish/m² (town of Belle River), and 5 to 9 fish/m² (Sarnia). Overall, highest densities of the round goby occurred in the day and on rocks. Small (≤5 cm) round gobies were most common at Peche Island, the most recently colonized site, indicating that juveniles may disperse more rapidly than adults. Of 200 fish that were marked, 58% were recaptured, indicating high site fidelity among round gobies. The estimated mean (± SE) home range of the round goby determined using SCUBA (5 ± 1.2 m²) was likely underestimated because few fish were observed. Larger round gobies may induce smaller fish to leave preferred rock habitats and move to sand habitats from which they disperse.     

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.