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.     

Size-selective predation by round gobies (Neogobius melanostomus) on dreissenid mussels in the field

Although numerous studies have shown that round gobies (Neogobius melanostomus) prey on dreissenid mussels (Dreissena polymorpha and Dreissena bugensis), there is an apparent shortage of detailed field studies on the subject. The 5-month field study described here quantifies predation by round gobies on dreissenids in Presque Isle Bay, Lake Erie. Dreissenids dominated the diet of round gobies, composing 92% of the prey items recovered. Over half of the 3870 valves (1935 mussels) recovered from 155 round gobies were crushed, while the remainder were swallowed whole. Crushed dreissenids were larger than those swallowed whole, and the tendency to crush dreissenids did not vary among three length classes of round goby. Round goby length was positively related to average size of dreissenids consumed, average size of whole and crushed dreissenids, largest whole dreissenid consumed, and largest crushed dreissenid consumed. Indices of selectivity revealed similarly shaped curves for three length classes of round gobies, a shift toward larger dreissenid size classes with an increase in round goby length, and peak preferences for 8-11 mm dreissenids. Factors such as gape limitation, availability and accessibility of differently sized dreissenids, forces generated while removing mussels from the substrate and crushing them, and caloric content of dreissenids all likely play roles in the observed size-selectivity and differential processing of dreissenids. Although factors influencing size-selectivity are not completely understood, the observed preference of round gobies for dreissenids near the size when they are first reproductive could impact the demography of dreissenid populations.     

Evaluating gonadosomatic index as an estimator of reproductive condition in the invasive round goby, Neogobius melanostomus

Using gonadosomatic index cut-off scores has become a standard protocol for selecting reproductive fish in studies on the reproductive biology of round goby, Neogobius melanostomus, a significant invader of the Laurentian Great Lakes, but the validity of this practice has not been validated with histological staging. The goal of the current study was to evaluate the effectiveness of using gonadosomatic index (GSI) cut-off scores to classify reproductive status in male and female round goby by documenting associations between GSI, sex steroids, and gonad development. Gonadal stage was determined in both sexes using hematoxylin and eosin histology. Plasma 11-ketotestosterone and testosterone were measured in males, and testosterone and 17β-estradiol were measured in females. Gonadosomatic index cut-off scores were effective in selecting spawning capable individuals at higher GSI values, but GSI values were limited in the ability to make further distinctions of gonadal stage and missed many spawning capable females. In females, testosterone levels were highest during vitellogenic growth and declined prior to ovulation. 17β-estradiol displayed a similar, but non-statistically significant pattern. Males with developing testes had higher levels of 11-ketotestosterone —but not testosterone —than reproductively immature males, although levels of these androgens were overall positively correlated in males. The findings indicate that the conventional GSI cut-off scores (1% in males, 8% in females) accurately assign spawning capable condition in both sexes; however, they may also exclude some spawning capable females with lower GSIs.     

First documentation of spawning and nest guarding in the laboratory by the invasive fish,the round goby (Neogobius melanostomus)

Although the round goby, Neogobius melanostomus, is widespread in the Great Lakes and has an extended breeding season with a high reproductive rate; its spawning behaviour remains elusive. We present the first reported accounts of spawning by the round goby in the laboratory. By simulating winter conditions and restoring spring conditions, we induced round gobies to spawn in October 2007, March 2008, May 2008, and January 2009. In one case, fanning by the nest-holding male began 10 days before egg deposition and, during this period, the male rubbed secretions along the ceiling of the nest. Males were choosy about which gravid females entered the nest and prevented entry by some females. Spawning involved repeated inversions by females and males releasing gametes on the ceiling of the nest. Males guarded the nest by blocking the entrance, producing agonistic vocalizations and chasing intruders. Inside the nest, eggs were regularly inspected by the males and constantly ventilated using pectoral and caudal fins. Up to three gravid females spawned sequentially in a nest. Peak ventilation occurred after egg deposition and declined with time until the parental male ate the eggs. The decline of parental care and egg cannibalism was likely an artifact of laboratory conditions and small brood size. Our findings offer new information on the reproductive habits of the invasive round goby. Because the reproductive sequence in the laboratory seems easy to disrupt, the procedures may lead to a management tool to control the spread of the species into new areas.     

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.     

Ontogenetic changes in pharyngeal morphology correlate with a diet shift from arthropods to dreissenid mussels in round gobies (Neogobius melanostomus)

The potential of predators to regulate populations of dreissenid mussels (Dreissena polymorpha and Dreissena rostriformis bugensis) has been addressed since early in the dreissenid invasion of North America. Round gobies (Neogobius melanostomus) larger than approximately 60 mm have been shown to prey extensively on dreissenids, whereas smaller round gobies feed mainly on aquatic insects and crustaceans. We propose that ontogenetic changes in pharyngeal morphology may contribute to this diet shift in round gobies. Pharyngeals of 69 round gobies ranging from 31 to 164 mm total length were investigated using light microscopy and scanning electron microscopy. Areas of lower pharyngeals and pharyngobranchial 2 increased allometrically with fish length. Pharyngeals of round gobies smaller than 50 mm contained narrow (< 0.1 mm diameter) papilliform teeth that are consistent with eating soft-bodied prey. By the time round gobies reached approximately 80 mm in length, pharyngeals contained larger diameter (0.3-0.5 mm) molariform teeth typical of those found in molluscivorous fish. Pharyngeal teeth of the largest round gobies also showed considerable wear. Although changes in pharyngeal morphology may contribute to the previously described diet shift in round gobies as they age, genetic and environmental factors both likely influence pharyngeal remodeling and therefore merit further investigation.     

Round goby (Neogobius melanostomus) population structure,biomass, prey consumption and mortality from predation in the Bay of Quinte,Lake Ontario

We compared round goby (Neogobius melanostomus) population structure and biomass, estimated the quantity of prey consumed by round goby and assessed predation on round goby in two areas of the Bay of Quinte (upper and lower bay) that were invaded by this species two years apart. A bioenergetics approach was used to estimate round goby consumption and to illustrate the influence of changes in the round goby biomass, from May to October in both areas of the bay. Mean round goby biomass was 5 tonnes/km² for the upper bay and 11.2 tonnes/km² for the lower bay. Round goby populations were dominated by age-0 to age-2 individuals; older individuals were rare although they constituted a greater portion of total biomass in the earlier invaded lower bay than the upper bay. Estimated round goby consumption was 78.4 tonnes/km² for the upper bay and 127.1 tonnes/km² for the lower bay; dreissenids were the most important prey followed by chironomids, zooplankton and amphipods. Diet analysis showed that round gobies were consumed by all predator species analyzed, and constituted a high percentage of stomach content biomass in yellow perch (Perca flavescens), largemouth bass (Micropterus salmoides) and northern pike (Esox lucius). Age structure differences between the upper and lower bay are consistent with those expected between expanding and stable populations.     

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.     

Multiple male reproductive morphs in the invasive round goby (Apollonia melanostoma)

Alternative male reproductive tactics are taxonomically widespread. In such species, parental, or conventional, males express secondary sexual characteristics, court females and guard offspring, while smaller parasitic or sneaker males avoid the costs of courtship and parental care by performing sneak fertilizations. Theory predicts that sneakers will invest more in testes mass and produce more competitive ejaculates than parentals because sneakers always experience sperm competition while parental males experience sperm competition only when a sneaker is present. Here we present convergent lines of evidence supporting the existence of alternative male reproductive tactics in round gobies (Apollonia melanostoma, formerly Neogobius melanostomus), a recent invader in the Great Lakes. Dark morph males exhibited secondary sexual characteristics, were larger and had higher plasma 11-ketotestosterone concentrations than light morphs, while light morph males invested more in ejaculates (both testes mass and sperm density). Both male morphs had enlarged urogenital papillae, but papillae were relatively longer in light morph males. Sperm tail length did not differ between morphs, and sperm from dark morphs swam faster than sperm from light morphs. Our data strongly argue for the presence of alternative tactics in round gobies, support some predictions from sperm competition theory and align with empirical observations in other taxa. For species of concern like the invasive round goby, it is critical to consider such evidence of alternative male mating tactics when constructing population growth models and assessment of invasion success and impacts.     

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.     

First report of tubenose goby (Proterorhinus semilunaris) in the eastern basin of Lake Erie

The tubenose goby (Proterorhinus semilunaris), native to the Ponto-Caspian region, was first discovered in the Laurentian Great Lakes in 1990 after it was introduced through ballast water discharge. Compared with Neogobius melanostomus, another exotic gobiid from the Ponto-Caspian, colonization of the Great Lakes by P. semilunaris has been slow, with reports of the species being largely confined to the Huron-Erie Corridor (HEC) and western portions of Lake Erie and Lake Superior. This is the first report of P. semilunaris in the Great Lakes east of the western basin of Lake Erie. Between 28 June and 27 July, 2012, 176 P. semilunaris were collected from shallow (< 1.2 m) water of Marina Lake, a 40 ha embayment in Presque Isle State Park (Erie, PA). The large number of P. semilunaris collected at the site and the presence of individuals as small as 17 mm total length suggest an established population. However, the mechanism by which P. semilunaris was introduced to Presque Isle Bay is not clear.     

A review of estimates of daily energy expenditure and food intake in cormorants (Phalacrocorax spp.)

Daily energy expenditure (DEE) and daily food intake (DFI) are key parameters in estimating population level consumption by cormorants. A number of different methods are still employed in estimating these parameters along with different estimates for assimilation efficiency (if used) and prey energy density. The pellet/fish size reconstruction and percent adult body weight methods underestimate DFI for a number of reasons including an implied underestimation of DEE. In the absence of study-specific data, an assimilation efficiency of 0.80 and prey energy density of 5.42 kJ?g^− 1 are recommended. The bioenergetic model for field metabolic rate from Ellis and Gabrielsen (2002) is recommended for adults during the nesting season and their model for basal metabolic rate (BMR × 2.5) is recommended for adults or sub-adults outside the nesting season. Comparisons between empirical and bioenergetic models for chick DFI are also made with recommendations on estimating DFI.     

Impacts of the Introduced Round Goby (Apollonia melanostoma) on Dreissenids (Dreissena polymorpha and Dreissena bugensis) and on Macroinvertebrate Community between 2003 and 2006 in the Littoral Zone of Green Bay,Lake Michigan

We show that the invasion of round gobies (Apollonia melanostoma) in Green Bay, Lake Michigan, has changed the benthic food web in fundamental ways related to their impact on invasive dreissenid mussels. Dreissenid mussels are of specific interest because they are one of the primary dietary items for round gobies. In this study, we collected rocks from each of 10 study sites along approximately 60 km of the eastern shoreline of Green Bay, Lake Michigan, to assess a temporal change in macroinvertebrate abundance related to the northward movement of the round goby invasion front from a point about midway along the shoreline in 2003 to the entire coast in 2006. The pattern of macroinvertebrate abundance in 2003 suggested that round gobies had already caused significant decreases in macroinvertebrate abundances south of the invasion front (interpretation of the data could have been compromised by confounding environmental gradients). In subsequent sampling in 2006 macroinvertebrates were picked off of sampled rocks in the field and underwater transects were videotaped to estimate round goby abundance at each site. Round gobies were collected for stomach analysis to assist in determining which invertebrates would likely be impacted by goby predation. Our results indicated that by 2006, round gobies had become abundant at those sites where they were absent in 2003 and zebra mussels (Dreissena polymorpha), quagga mussels (Dreissena bugensis), isopods, amphipods, trichopterans, and gastropods in the newly invaded sites had significantly decreased at the newly invaded sites.     

Status and trends of the Asian clam (Corbicula fluminea) in the lower Fox River and Green Bay

In the upper Great Lakes region, survival and population growth of the non-indigenous Asian clam Corbicula fluminea has been limited by cold climates that cause severe overwinter mortality. At these northern latitudes, Asian clam populations are often limited to thermal refugia – particularly warmwater discharges from industrial facilities. Several such facilities exist in the lower Fox River in Green Bay. Asian clams were first documented in the lower Fox River in 1999 and were extensively surveyed near the river mouth in 2011, but the few individuals found were restricted to the warmwater discharge from the Pulliam Power Plant. We performed a follow-up survey during 2017 to re-assess the population status of Asian clams in the lower Fox River at four industrial discharges, including the Pulliam Power Plant. We found more widespread evidence of Asian clams throughout the lower Fox River than previous surveys, but only one live individual was captured. We suspect that the back-to-back severe winters of 2013–2014 and 2014–2015 caused widespread overwinter mortality. Our investigation highlights the significant challenges for establishment of Asian clam populations in the upper Great Lakes region, and provides an example of a potential invasive species struggling to establish a viable population in a hostile climate.     

The influence of habitat and environment on smallmouth bass (Micropterus dolomieu) nest sites and nest success in northern Lake Michigan

Information on smallmouth bass nesting ecology is lacking in northern Lake Michigan, despite available information for other Great Lakes ecosystems. Our objectives were to identify factors that influenced nesting sites and nest success in a smallmouth bass population in northern Lake Michigan. Temperature, substrate firmness, and lake bottom rugosity were measured and related to the number of smallmouth bass nests in four bays. We also investigated the role of temperature, effective fetch, and storms to explain nest success. Temperature appeared to be most important in explaining the number of nests and nest success; transects that experienced the greatest number of cumulative degree days above 15 °C during nesting contained more nests and increased nest success. Our results suggest that warmer areas during spawning in northern latitude lentic systems should be protected from anthropogenic disturbances because these areas may be important for future recruitment of smallmouth bass.     

Spatial genetic structure and recruitment dynamics of burbot (Lota lota) in Eastern Lake Michigan and Michigan tributaries

Burbot (Lota lota) are the only freshwater member of the Cod like (Lotidae) family that have a circumpolar distribution and occupy the widest geographic distribution of all Laurentian Great Lakes fish species. Information regarding burbot spatial genetic structure and recruitment dynamics is critical for the development of effective management strategies. Although burbot are a species of conservation concern throughout their range, little demographic or behavioral information exists. We estimated levels of genetic diversity within, and the degree of spatial population structure between samples collected from Lake Michigan and tributaries of the Manistee River, MI. Measures of genetic diversity across 10 microsatellite loci were moderately high. Disparities between adult groups sampled in Lake Michigan and the Manistee River were notable for observed heterozygosity (0.662 vs 0.488) and allelic richness (11.7 vs 6.6). Significant levels of inter-population variance in microsatellite allele frequencies (F_ST 0.154 to 0.208) were detected between Lake Michigan and the Manistee River samples. Results indicate reproductive isolation between what plausibly may be riverine and lacustrine spawning life history types. Pedigree analyses for three cohorts sampled in the Manistee River revealed that a sizeable number of adults contributed reproductively to multiple cohorts, indicating spawning philopatry. While data were collected from restricted areas in lacustrine and river habitats, analyses revealing microgeographic genetic structuring, potentially attributed to life history polymorphisms, have significant implications for burbot management in the Great Lakes.     

Shifting status and distribution of range margin chorus frog (Pseudacris) populations in eastern Great Lakes watersheds

Contiguous with their range across major rivers into Canada, two different species of chorus frogs are now thought to inhabit the Great Lakes watersheds of New York. Pseudacris triseriata is found along the western Lake Ontario and Lake Erie plains while P. maculata (tentatively a new frog species in NY) inhabits the lowlands of eastern Lake Ontario and the St. Lawrence River. Both species are on their extreme range margins in NY. In 2010 we detected distributional declines of both putative chorus frog species based on a broad survey following standardized occupancy detection protocols. Causes are unclear but could relate to reforestation and urbanization of formerly more extensive agricultural lands, climate change, pathogenic fungal outbreaks and/or the contaminant effects of intensive agriculture. On the other hand, the prior overestimation of ranges because of misidentification may have inflated earlier perceived distributions (positive survey bias) because false positives are problematical for this cryptic frog. At broad geographical scales, chorus frog (meta)populations are highly dynamic and are likely shifting their ranges in response to rapidly changing overall environmental conditions in the northeastern U.S. and Canada.