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.     

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.     

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.     

Morphology,Feeding, and Reproduction of the Round Goby,Neogobius melanostomus (Pallas), in the Danube River Basin,Yugoslavia

The round goby Neogobius melanostomus was the last Ponto-Caspian goby species to enter in the Danube River bordered by Serbia and Yugoslavia. There are five Ponto-Caspian goby species in the waters of Serbia including the sand goby Neogobius fluviatilis, the round goby Neogobius melanostomus, the racer goby Neogobius gymnotrachelus, the bighead goby Neogobius kessleri, and the tubenose goby Proterorhinus marmoratus. The sand, bighead, and tubenose gobies occur along the Yugoslav Danube and in the lower reach of the Danube's tributaries; the racer goby is found both upstream and downstream of the Djerdap II dam; and, the round goby has been collected only downstream of the Djerdap II dam. Investigations on the continuous morphological characters of the round goby revealed neither sexual dimorphism, nor significant differences in adult size-classes, although some suggestions of sexual dimorphism were found in cranial skeletal analyses. Analysis of external continuous characters revealed a west-east cline along the distribution range of the round goby in the Black Sea basin. Molluscivory for the round goby was corroborated along the Danube. Standard length of each age class for the round goby in the Danube was less than populations in the Caspian and Azov seas.     

The effects of riprap in enhancing the abundance and coexistence of Gobiidae along the southern Caspian Sea coast

Many natural coastal habitats around the world are being replaced by hard coastal defense structures as a result of rising sea levels and increasing intensity of storms. To examine the potential effects of riprap on gobies in the nearshore zone of the southern Caspian Sea, we used angling to compare their abundance and diversity in 13 riprap and natural habitats (sandy and gravel shores) from April 2012 through April 2013. In total, 819 gobies of three species, Caspian sand goby Neogobius pallasi (N?=?433), round goby Neogobius melanostomus (N?=?206), and Caspian goby Neogobius caspius (N?=?180) were collected. No round gobies were caught from sandy shores and only two Caspian gobies were caught from gravel habitats, while all three species were abundant in riprap shores. A significant difference was observed in CPUE of all three goby species among shore types, with riprap sites having the highest abundance. PERMANOVA and nMDS demonstrated differences in goby assemblages among all three habitats. There were significant differences in round goby and Caspian goby sizes among riprap and natural habitats, while there were no significant differences in Caspian sand goby size among habitat types. In general deployment of riprap, especially in an area characterized as having natural shores with low structural complexity, could enhance the abundance and coexistence of nearshore gobies and act as a dispersal vector.     

Distribution,Abundance, and Range of the Round Goby,Apollina melanostoma,in the Duluth-Superior Harbor and St. Louis River Estuary, 1998–2004

Round gobies were first discovered in the Duluth-Superior Harbor, Lake Superior, in 1995. Anecdotal sightings by anglers and others suggested that the infestation was growing and expanding; however, direct evidence of the distribution and expansion rate in the harbor was largely unknown. Distribution and range of the round goby, Apollonia melanostoma, (formerly Neogobius melanostomus) was assessed using bottom trawl sampling throughout the Duluth-Superior Harbor, and portions of the lower St. Louis River from 1998 to 2004. Previous to 1998, round gobies only were reported to occupy the harbor between the two shipping entries (river kilometer 1 to 7). By 2004, they expanded throughout the harbor and upstream to river kilometer 13, but remained absent in western Lake Superior. The number of round gobies captured per 5 minutes of trawling (catch per unit effort, CPUE) increased from less than 1 fish in 1998 to an average 5.4 ± 1.2 SE fish in 2004, indicating a large increase in the population. The median yearly fish total length varied from 56.0 to 81.5 mm and wet weight varied from 2.3 to 7.0 g. As nest guarding male round gobies were located in rocky habitats inaccessible to trawling, the initial years were dominated by female round gobies with a 16:1 female to male ratio, but by 2002 the maximum ratio was 2:1. The ratio change may be indicative of the increasing population forcing males from their preferred rocky habitat onto open substrates that were more accessible to trawling.     

Density and habitat use by the round goby (Apollonia melanostoma) in the Bay of Quinte,Lake Ontario

We assessed round goby (Apollonia melanostoma) density and size structure in two sections of the Bay of Quinte (Lake Ontario) that had been invaded by this species two years apart. Round goby density was assessed with 50 m linear transects, recorded with an underwater video recording apparatus developed for this study that included a depth sounder for maintaining a fixed distance above the substrate. The highest mean round goby densities were observed in the shallowest depth zone (1.5–3 m) at both sites, but there were differences between the sites in the habitat types where the highest densities occurred and there were no significant density differences among habitat types at either site (rock with sparse vegetation, mud with sparse vegetation, sand/mud with moderate vegetation cover). In the upper bay, mean body length of round gobies declined with depth, whereas in the lower bay, mean round goby length was greatest in the deepest zone. Mean body length of round gobies did not differ significantly by habitat type in either section of the bay.     

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.     

Activity,Aggression, and Habitat Use of Ruffe (Gymnocephalus cernuus) and Round Goby (Apollonia melanostoma) under Laboratory Conditions

Potential negative ecological interactions between ruffe Gymnocephalus cernuus and round goby Apollonia melanostoma (formerly Neogobius melanostomus) might affect the colonization dynamics of these invasive species where they are sympatric in the Great Lakes. In order to determine the potential for ecological interactions between these species, we examined the activity, aggression, and habitat use of round gobies and ruffe in single species and mixed species laboratory experiments. Trials included conditions in which food was concentrated (in light or darkness) or scattered. Results showed that ruffe were more active than gobies, particularly when food was scattered. Activity of both species was significantly lower during darkness. Round gobies were significantly more aggressive than ruffe, and total aggression was lower in mixed species trials. Habitat use by ruffe and round gobies overlapped considerably, but we observed significant differences between species in their use of specific habitats that depended on experimental conditions. Overall, ruffe used open habitats more often than did round gobies, primarily when food was scattered. Round gobies used rocks significantly more frequently than did ruffe, but their use of rock habitat decreased during dark conditions. Ruffe were found more often in plant habitats and less often near the wall of the pool in trials during daylight with concentrated food. Activity and habitat use of ruffe and round goby did not significantly differ between single and mixed species trials. Overall, we found little evidence for negative ecological interactions between ruffe and round goby in these laboratory experiments.     

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.”     

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.     

Updated invasion risk assessment for Ponto-Caspian fishes to the Great Lakes

Majority of invasive species discovered in the Great Lakes since 1985 are native to the Ponto-Caspian region, including species that have had strong negative impacts in the Great Lakes (for example, dreissenid mussels and the round goby). The rich biota of the Ponto-Caspian region coupled with a high volume of commercial shipping traffic strongly suggests that this region will continue to be a major source of invasive species to the Great Lakes. To assess invasion risk by Ponto-Caspian fishes that have not been included in previous studies, we reviewed English-language publications and untranslated European literature (published primarily in Russian), focusing on physiological and ecological traits that have proven useful in previous risk assessments. We then used discriminant analysis to identify fishes that had a high probability of becoming established, spreading, and having significant negative impacts in the Great Lakes. Our updated listing of high-risk Ponto-Caspian fishes includes five species identified previously (the Black and Caspian Sea sprat, Eurasian minnow, big-scale sand smelt, European perch, and monkey goby) and five additional species (the Black sea shad, Caspian tyulka, Volga dwarf goby, Caspian bighead goby, and black-striped pipefish). Of these ten species, four (the monkey goby, big-scale sand smelt, Caspian tyulka, and black-striped pipefish) are likely to survive ballast water exchange as eggs, larvae, or adults based on salinity tolerances. Our results can be used to focus ongoing surveillance and rapid response efforts by highlighting Ponto-Caspian fishes that pose the greatest risk of becoming established and having significant negative impacts in the Great Lakes.     

First records of ratan goby Ponticola ratan in the Kaniv Reservoir and Desna River (Ukraine): A discreet invader of rip-raps

Monitoring of nearshore fish communities carried out in 2019 and 2022 in the Kaniv Reservoir and lower Desna River (Dnieper River basin, Ukraine) showed the presence of the ratan goby (Ponticola ratan), which has never been observed in these water bodies before and naturally inhabited marine and brackish waters of the Black and Azov Sea basins. The ratan goby was detected only on rip-rap structures and not on any other surveyed substrates including sand, mud, clay, and gravel which suggests a narrow habitat preference for this species. In all instances, the ratan goby co-occurred with the round goby (Neogobius melanostomus). Occurrence on all surveyed rip-raps, high abundances and the presence of a variety of size classes of the ratan goby in samples suggest that this species penetrated the Kaniv Reservoir quite long ago and successfully established there and has become a common component of the local fish fauna. Based on the obtained data, this gobiid should be listed among freshwater fishes of Europe as a euryhaline species that can potentially colonize other rivers flowing into the Black Sea including the Danube.     

First genetically verified occurrence of Ligula pavlovskii outside its native range and characteristics of its infection in Neogobius fluviatilis

In this study, we provide the first genetically verified distribution record beyond its native range of Ligula pavlovskii, a high-impact endoparasite of Ponto-Caspian gobies. According to parasitological surveys, ligulosis was detected for the first time in monkey goby individuals collected from Lake Balaton in 2004, 34 years after the first record of monkey goby in the lake. During a Lake Balaton survey in 2018, we detected tapeworms in 44.4% of the sampled monkey gobies. This prevalence is about two to ten times higher than it was reported from within the native range of the fish hosts. The same survey revealed an uneven spatial distribution of the ligulosis in the monkey gobies inhabiting different shoreline sections of the lake. We assume that the occurrence and recent distribution data of this high-impact endoparasite may provide useful information for potential biocontrol measures of invasive Ponto-Caspian gobies in the future.     

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.     

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.     

Response to putative round goby (Neogobius melanostomus) pheromones by centrarchid and percid fish species in the Laurentian Great Lakes

Pheromone trapping is an increasingly viable strategy to reduce invasive fish populations, largely due to the pheromones' function of evoking behavioral responses among conspecifics. Prior to attempting such population control techniques, the pheromones must be identified and their possible influences on non-target species addressed. The round goby (Neogobius melanostomus) is a species invasive to the Great Lakes region, and negatively impacts the ecosystem by interfering with local fish populations. At least two 5β-reduced 3α-hydroxyl steroids released by reproductive N. melanostomus (11-O-ETIO and 11-O-ETIO-3s) evoke olfactory sensory responses from the olfactory epithelium of conspecifics, and water conditioned by reproductive males (containing these steroids) attracts female round gobies. In this study, we examined whether these putative pheromones, along with simultaneously-released 11-O-ETIO-17s, stimulate olfactory sensory responses from alternative fish species sharing the same ecosystem as N. melanostomus in the Great Lakes region. Rock bass (Ambloplites rupestris), bluegill sunfish (Lepomis macrochirus), pumpkinseed sunfish (Lepomis gibbosus), smallmouth bass (Micropterus dolomieu), and yellow perch (Perca flavescens) were the targets of an electro-olfactogram experiment designed to record responses to odors. When compared to round goby responses from previous studies, amino acids and the bile acid consistently elicited electro-olfactogram responses across all species, but only round gobies showed a response to the putative pheromones. This study supports the concept of conducting a pheromone trapping trial in the field without adversely affecting the olfactory responses of non-target fish in the area.     

Slimy sculpin depth shifts and habitat squeeze following the round goby invasion in the Laurentian Great Lakes

The collapse of Diporeia spp. and invasions of dreissenid mussels (zebra, Dreissena polymorpha; quagga, D. bugensis) and round goby (Neogobius melanostomus) have been associated with declines in abundance of native benthic fishes in the Great Lakes, including historically abundant slimy sculpin (Cottus cognatus). We hypothesized that as round goby colonized deeper habitat, slimy sculpin avoided habitat competition, predation, and aggression from round goby by shifting to deeper habitat. Accordingly, we predicted increased depth overlap of slimy sculpin with both round goby and deepwater sculpin (Myoxocephalus thompsonii) that resulted in habitat squeeze by both species. We used long-term bottom trawl data from Lakes Michigan, Huron, and Ontario to evaluate shifts in slimy sculpin depth and their depth overlap with round goby and deepwater sculpin. Lake Huron most supported our hypotheses as slimy sculpin shifted to deeper habitat coincident with the round goby invasion, and depth overlap between slimy sculpin and both species recently increased. Slimy sculpin depth trends in Lakes Michigan and Ontario suggest other ecological and environmental factors better predicted sculpin depth in these lakes.     

Quantifying the predatory effect of round goby on Saginaw Bay dreissenids

Invasive dreissenid mussels (D. polymorpha and D. r. bugensis) have fundamentally altered Laurentian Great Lake ecosystems, however in many areas their abundances have declined since the mid-1990s. Another invader, the benthic fish round goby (Neogobius melanostomus), is morphologically adapted to feed on dreissenids and likely affects dreissenid populations; however, the degree of this predatory effect is variable. In 2009 and 2010, we examined round goby abundances, size distributions, diet contents, and diet selectivity in Saginaw Bay, Lake Huron; a shallow bay that has been subjected to numerous anthropogenic stressors. We further used a consumption model to estimate dreissenid consumption by three different size classes of round goby. Round gobies were found throughout the bay and most were smaller than 80 mm total length. Round gobies of all sizes consumed dreissenids (including fish as small as 30 mm total length), though dreissenids were rarely preferred. The relative proportion of dreissenids (by biomass) present in diets of round gobies increased with fish size, but also throughout the year for all size classes. Despite this, overall consumptive effects of round gobies on dreissenids in Saginaw Bay were low. Many dreissenids present in the bay were larger than those consumed by round gobies. Bioenergetics-based model estimates suggest that the smallest round gobies are responsible for the majority of dreissenid consumption. While our findings are limited to soft substrates and influenced by sampling restrictions, our study design allowed us to put bounds on our estimates based upon these multiple sources of uncertainty.