Julie R. Marentette

Demography and substrate affinity of the round goby (Neogobius melanostomus) in Hamilton Harbour

ABSTRACT The invasive round goby, Neogobius melanostomus, consumes eggs and fry of other fishes, competes for resources with native fish species, and hence poses a threat to Great Lakes aquatic communities. We provide the first description of round goby demographic patterns in Hamilton Harbour, in the western tip of Lake Ontario, and the connected Cootes Paradise Marsh, a recently restored wetland. By monitoring round goby populations on a variety of distinct habitats for 7 years (2002–2008), we found that populations have declined at all sample locations and that average fish body size also has decreased. We also related abundance, body size, and reproductive patterns to seasonality, to substrate types (mud, sand, cobble and boulder) and to water quality in all locations. Round gobies were found on all substrates sampled including mud, although they were less abundant on mud than on other substrates, and to date have not extensively colonized Cootes Paradise Marsh. Our work confirms previous studies, which have suggested that habitats lacking hard structures will have fewer round gobies because they lack substrates on which round gobies can breed. However, our results also indicate that muddy and sandy substrates are not resistant to round goby invasion and will not prevent round goby colonization, a potential concern for Cootes Paradise Marsh an important spawning, nursery, and refuge habitat for warmwater native fishes and for other similar wetlands.

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

ABSTRACT 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.

Signatures of contamination in invasive round gobies (Neogobius melanostomus): A double strike for ecosystem health?

The invasive round goby has a recognised role in transferring contaminants through foodwebs, but little work has been done on contaminant impacts on round gobies themselves. Here we present the first case study of contaminant biomarkers and subpopulation structure variation in round gobies, in relation to habitat contamination, within a Canadian Area of Concern, Hamilton Harbour. Copper and cadmium were elevated in livers of fish from contaminated habitats. Although catch abundances were similar across sites, fish were smaller, a greater proportion of fish were female and more males were in reproductive condition in contaminated sites. Fish from contaminated areas showed more fin loss. Males from contaminated sites showed intersex gonads and genitalia. Ethoxyresorufin-o-deethylase (EROD) activity was higher in fish collected near polycyclic aromatic hydrocarbon (PAH)-rich sediments. The results indicate that contaminants impact the characteristics of round goby populations, which could affect ecosystems beyond toxicant biomagnification. This study also confirms that round gobies can be abundant in polluted habitats, which may draw predators-facilitating mobilisation of contaminants in foodwebs.

Is there a role for aggression in round goby invasion fronts

The role of aggression as a factor promoting invasiveness remains hotly debated. Increased aggression or a lack of tolerance for conspecifics may promote population spread. Some previous research suggests that more aggressive or bold individuals are increasingly likely to disperse and as such these individuals may be overrepresented at the invasion front. In contrast, it has also been argued that individuals at the invasion front represent the least aggressive or least competitive individuals in the population, as these animals are excluded from established areas. Accordingly, the invasion front should be made up of shy, submissive individuals that exhibit reduced aggression. In this study we explore these alternative predictions by quantifying the levels of intra-specific aggression in the round goby (Neogobius melanostomus), an invasive fish that continues to spread rapidly through the Laurentian Great Lakes region in North America. We collected size matched male round goby from an invasion front as well as from an area with an established population, and we staged resource contests between them. Invasion front fish won 65% of the contests and tended to perform more aggressive acts overall. Invasion front fish were not more active or bold prior to the contest, and used the same types of aggressive displays as fish from established areas. Our results also showed that body size asymmetry was an overriding determinant of competitive outcomes, and that body size rather than individual variation in aggressiveness might be the most important contributing factor determining the composition of round goby invasion fronts throughout the Laurentian Great Lakes and its tributaries.

Impact of contaminant exposure on resource contests in an invasive fish.

There is increasing concern for the disruptive effects seen in aquatic species exposed to environmental contaminants. However, few studies have investigated the impact of such contaminants on the behavior of individuals living in exposed waters. Contaminant exposure can affect animal populations by disrupting behaviors including feeding, locomotion, and mating. In this study, we examined how living in an ecosystem polluted by combinations of polycyclic aromatic hydrocarbons, polychlorinated biphenyls, and heavy metals (arsenic, cadmium, iron, lead, zinc) impacts contest behavior in the round goby (Neogobius melanostomus). Fish collected from heavily contaminated and cleaner sites in Lake Ontario were subjected to a resource contest to determine the effect of these contaminants on aggression and the establishment of dominance hierarchies, which in turn influence access to food, shelter, and mating opportunities. Dominance establishment (a clear resource winner) was less obvious among fish from the contaminated site compared to the more stable hierarchies that formed between pairs of fish from the clean site. Pairs of fish from the contaminated site performed more assessment displays compared to fish from clean sites. These results suggest that the costs of living in an environment under exposure can shape behavioral repertoires. The altered conflict resolution strategies of contaminated fish may reflect impaired cognitive function, sensory perception, and/or higher metabolic load associated with aggression. This study provides support for the utilization of quantifiable behavioral differences as ecologically relevant measures of contaminant exposure.

Characterization of vitellogenin gene expression in round goby (Neogobius melanostomus) using a quantitative polymerase chain reaction assay

A growing concern over endocrine disruption in aquatic species has prompted the development of molecular assays to monitor environmental impacts. This study describes the development of quantitative polymerase chain reaction (qPCR) assays to characterize the expression of two vitellogenin (Vtg) genes in the invasive round goby (Neogobius melanostomus). Fragments from the 18SrRNA (housekeeping gene), Vtg II, and Vtg III genes were cloned and sequenced. The qPCR assays were developed to detect hepatic Vtg expression in goby. The assays detected induction of both Vtg genes in nonreproductive males following a two-week laboratory exposure to 17β-estradiol (≥1 mg/kg i.p. injection). The assays were applied to goby from Hamilton Harbour, Lake Ontario (Canada), including those from sites where feminization and intersex of goby has been documented. Both Vtg genes had significantly higher expression in females compared to males. Male reproductive goby adopt either parental or sneaker tactics; Vtg II expression was higher in sneaker than in parental males but parental and nonreproductive males did not differ from each other. The Vtg III expression was significantly higher in sneaker males followed by parental males and nonreproductive males, respectively. The Vtg II and III expression in nonreproductive males was elevated in the contaminated site with documented intersex. This assay provides an important tool for the use of an invasive species in monitoring endocrine disruption in the Great Lakes region.

Behavior as biomarker? Laboratory versus field movement in round goby (Neogobius melanostomus) from highly contaminated habitats

Changes in animal movement (frequency or speed of locomotion) following exposure to a toxicant are frequently considered a biomarker of contaminant exposure and are some of the most widely reported behavioral results in toxicological literature. However, the ecological consequences of such behavioral changes, such as effects on toxicant transfer in foodwebs, are far less well understood, complicated in part by the short-term nature of laboratory experiments and the lack of complementary field studies where the nature of toxicant exposure is more complex. Here we examine whether naturally exposed individuals of the round goby, a benthic, site-loyal fish, move in a manner similar to conspecifics from less contaminated habitats. In the laboratory, round goby from a relatively cleaner site showed greater activity and exploration than goby from two highly contaminated sites. Male fish were more active than females but the site effects were similar in both sexes. In contrast to laboratory findings, a field mark-recapture study of 881 round goby showed that fish from the cleaner site did not move greater distances or exhibit shorter residence times within the site than round goby from highly contaminated sites. Our results indicate that while behavioral changes in the laboratory may be one of several useful diagnostics of toxicant exposure of wild-exposed animals, they do not necessarily translate readily into measurable differences in a natural context. Thus, the potential fitness consequences of toxicant exposure based on behavioral changes need to be assessed carefully.

Molecular responses of Walleye (Sander vitreus) embryos to naphthenic acid fraction components extracted from fresh oil sands process-affected water

Naphthenic acid fraction components (NAFCs) are constituents of oil sands process-affected water (OSPW), which is generated as a result of unconventional oil production via surface mining in the Athabasca oil sands region. NAFCs are often considered to be major drivers of OSPW toxicity to various taxa, including fishes. However, the molecular targets of these complex mixtures are not fully elucidated. Here we examined the effects in walleye (Sander vitreus) embryos after exposure to NAFCs extracted from fresh OSPW. Eleutheroembryos (exposed to 0, 4.2 or 8.3mg/L NAFCs from 1day post-fertilization to hatch) were subsampled, measured for growth and deformities, and molecular responses were assessed via real-time polymerase chain reaction (PCR). Fourteen genes were evaluated, with a focus on the aryl-hydrocarbon receptor (AhR) - cytochrome P450 pathway (arnt, cyp1a1), the oxidative stress axis (cat, gst, sod, gpx1b), apoptosis (e.g. casp3, bax and p53), growth factor signaling (e.g. insulin-like growth factors igf1, igf1b, and igf1bp), and tissue differentiation (vim). NAFC exposure was associated with an increase in the expression of cyp1a1, and a decrease in gpx1b and ribosomal protein rps40. These results indicate that NAFC effects on walleye early-life stages may be mediated through oxidative stress via pathways that include AhR.

Diet and foraging of Round Goby (Neogobius melanostomus) in a contaminated harbour

Anthropogenic pollution and the introduction of invasive species are two contributing factors to ecosystem degradation. Although Hamilton Harbour (Ontario, Canada), a highly impacted ecosystem, is well-studied, the diet, trophic position, and foraging behaviour of the invasive Round Goby (Neogobius melanostomus) in this area is not well understood. In this study, we compared digestive tract contents, foraging behaviour, and stable isotope values of Round Goby from sites of low and high sediment contamination in Hamilton Harbour. We also assessed prey availability by conducting sediment invertebrate abundance analyses at these sites. Regardless of site, Chironomids, Cladocerans, Copepods and Dreissenids were the most common food items found in Round Goby digestive tracts, and females always had heavier gut contents compared to males. Fish from the high contamination site consumed fewer prey items, had lower gut fullness scores, and fed at a lower trophic level based on lower δ13C and δ15N values. Our results suggest that Round Goby living in highly contaminated areas are feeding less than Round Goby from areas of lower contamination, but that these diet differences do not reflect differences in prey availability. Fish from the high contamination site also typically moved more slowly while foraging. Taken together, these results provide an analysis of the main prey items of Round Goby in Hamilton Harbour, and demonstrate how polluted environments can impact diet, trophic position, and foraging of an introduced fish species.

Growth and otolith morphology vary with alternative reproductive tactics and contaminant exposure in the round goby Neogobius melanostomus

Round goby Neogobius melanostomus sagittal (saccular) otolith morphology was compared between males of the two alternative reproductive tactics (termed guarder and sneaker males) and between males captured from sites of high or low contamination. Otolith size increased with fish size and also displayed an ontogenetic shift in shape, becoming relatively taller as otoliths grew in size. Despite a considerable overlap in age between males adopting the two reproductive tactics, size-at-age measurements revealed that guarder males are significantly larger than sneakers at any given age and that they invest more into somatic growth than sneaker males. Controlling for body size, sneaker males possessed heavier sagittal otoliths than guarder males. Subtle otolith shape differences were also found between the two male tactics and between sites of high and low contaminant exposure. Sneaker males had relatively shorter otoliths with more pronounced notching than guarder males. Fish captured at sites of high contamination had otoliths showing slower growth rates in relation to body size and their shapes had more pronounced caudal points and ventral protrusions when compared with fish captured at sites of low contamination. The results are discussed in relation to life-history tradeoffs between the male tactics in terms of reproductive and somatic investment as well as the putative metabolic costs of exposure to contaminants. Overall, this study reveals that male alternative reproductive tactics and environmental contaminants can have small, yet measurable, effects on otolith morphology and these factors should be accounted for in future research when possible.