Ten polymorphic microsatellite markers in the invasive round goby (Neogobius melanostomus) and cross‐species amplification

Ten tetranucleotide, dinucleotide and compound microsatellite loci were isolated and characterized for the round goby, Neogobius melanostomus. Analysis of 64 gobies from one nonindigenous population in Lake Erie, Ontario, Canada, indicated that allele number varied from three to 12 per locus, while observed heterozygosity ranged between 0.33 and 0.86. Eight of these primers showed some amplification in other species in four genera. These newly developed microsatellite markers are a powerful tool that will provide insights into population structure and dispersal of the round goby in their novel environment.     

Carcass feeding as a cryptic foraging mode in round goby Neogobius melanostomus

Round gobies Neogobius melanostomus were observed readily consuming soft tissue from carcasses of larger fishes under both laboratory and field conditions. Consumption normally progressed in a typical sequence, starting with soft and easily accessible tissues such as the eyes, followed by puncture of the abdominal cavity, gut consumption and then muscle consumption. Carcass feeding has not previously been seen in N. melanostomus and has potential consequences for transfer of nutrients and contaminants.     

Little association of biological trait values with environmental variables in invasive alien round goby (Neogobius melanostomus)

The relative importance of species‐specific biological trait characteristics and environmental factors in invasions of nonindigenous species remains controversial because both have mostly been studied independently. Thus, the main objective of this study was to examine the correlation of biological traits with environmental variation in the globally invasive round goby Neogobius melanostomus from the upper Danube River. Based on a sample of 653 specimens along a continuous 200 km river pathway, links between nine environmental factors (substrate‐type, six water measurements, and the communities of fishes and macroinvertebrates) and seven biological traits (nutritional and energetic status, trade‐offs of parasite resistance and resource allocation, and three growth proxies) were analyzed. Biological trait values of N. melanostomus hardly correlated with the environment, could not explain invasion progress and imply a general low overall importance for invasion success. Instead, alternative individual life‐history trajectories appear to determine invasion success. This is in line with up to 15% of all specimens having outlying biological trait values of potential adaptive value, suggesting a considerable importance of adaptive trait variation among single individuals for the whole invasion progress. This “individual trait utility hypothesis” gives an alternative explanation for success of invasive species by single individuals carrying particular traits, and it should be specifically targeted and analyzed at currently invaded sites.     

Effects of sampling techniques on population assessment of invasive round goby Neogobius melanostomus

In this study, a comparison of point abundance sampling (PAS) electrofishing, angling with two different hook sizes and trap‐based fishing was performed in a non‐wadeable river to analyse their effects on catch per unit effort (CPUE) and population characteristics of invasive round goby Neogobius melanostomus. PAS electrofishing was identified as the most effective (mean ± s.e . CPUE = 57 ± 4 N. melanostomus min^?1) and least selective method in terms of size, feeding status and species composition. Angling had the second highest CPUE, but was more size selective and resulted in a higher proportion of males compared to electrofishing [overall sex ratio angling (female:male) = 1:0·92, electrofishing 1:0·65]. Owing to low CPUE (0·012 ± 0·004) and low frequency of occurrence, minnow traps were least suitable for N. melanostomus population assessment. The results of this study suggest that a higher degree of standardization and inter‐calibration is useful to achieve better comparability of population data of invasive N. melanostomus and other benthic fish species.     

The seminal vesicle synthesizes steroids in the round goby Neogobius melanostomus

In this study, we examine the possible contribution of the seminal vesicles of the male round goby to the production of putative steroidal pheromones. A previous study showed that the testes of the round goby are rich in steroid-producing Leydig-like cells; and when incubated in vitro, convert tritiated androstenedione to at least six other steroids, including one not previously identified in fish--namely 3alpha-hydroxy-5beta-androstane-11,17-dione (11-oxo-etiocholanolone, 11-oxo-ETIO). The seminal vesicles of reproductively mature males were examined by conventional histology, transmission electron microscopy and immunocytochemistry (utilizing an antibody against 3beta-hydroxysteroid dehydrogenase--a key enzyme in vertebrate steroid synthesis). All three procedures identified Leydig cells in the proximal and medial regions of the seminal vesicles. In vitro incubation of seminal vesicles with tritiated androstenedione demonstrated biosynthesis of 11-oxo-androstenedione, 11-oxo-testosterone (more commonly known as 11-ketotestosterone) and 11 oxo-ETIO. These data indicate that the seminal vesicles, as well as the testes are involved in the synthesis of steroidal compounds that may function as pheromones.     

Range expansion dynamics of the invasive round goby (Neogobius melanostomus) in a river system

The rates of upstream and downstream range expansion of the round goby (Neogobius melanostomus) were examined in the Trent-Severn Waterway in 2009 and 2010. Relative abundance, demographics, and habitat use were also compared between areas of range expansion and a longer established area to determine how these characteristics varied along the invasion pathway. Round gobies were sampled using an angling removal method in May and August of 2009 and 2010 at 75 sites at each area of range expansion and 25 sites near the center of their range where they first became established in the waterway. Areas of range expansion had initially low abundance and low site occupancy in May 2009 relative to the longer established area. Large increases in abundance and site occupancy were observed over the first summer of occupation, but with limited range expansion. Rapid range expansion was observed during the non-reproductive season at the upstream edge of range. Individuals sampled in the expanded upstream range were small and female biased relative to other range locations. Round gobies also exhibited higher habitat selectivity for rocky substrates at range edges than in the longer established area. These characteristics of seasonal dispersal, biased demographics of dispersers, and high habitat selectivity may be important components of successful range expansion of the round goby in invaded ecosystems.     

Temporal patterns in growth and survival of the round goby Neogobius melanostomus

Monthly, overwinter and annual instantaneous growth rates for round goby Neogobius melanostomus were calculated with maximal growth occurring in July and August and almost no growth observed between ice appearance (October) and melt (March). Annual absolute growth rates averaged 27·3 ± 1·9 mm for males and 19·8 ± 2·4 mm for females. The most parsimonious Cormack–Jolly–Seber model indicated that both the survival and recapture probabilities were dependent on sampling date, but not sex. Survival estimates remained high throughout the 13 month study with a median weekly survival probability of 0·920 (25 and 75% quartiles: 0·767 and 0·991), an overwinter survival probability of 99% and an annual survival rate of 67%. Survival probabilities were lowest for both sexes near the completion of the N. melanostomus reproductive season in July and August which supports existing evidence of higher mortality after reproduction, while challenging the paradigm that male N. melanostomus suffer comparatively higher mortality as a result of reproduction than females. Evidence indicating that growth and mortality rates are highest at the end of the reproductive season not only highlights seasonal variability in N. melanostomus natural history, but may also guide the control of this invasive species to periods when they are most vulnerable.     

Finding round goby Neogobius melanostomus (Pallas, 1814) in the Rybinsk Reservoir

The data from finding a female round goby in June 2010 near the dam in the Central Reach of the Rybinsk Reservoir are presented. The presence of mature reproductive products may indicate the possibility of the successful acclimatization of this species in the Rybinsk Reservoir.     

Ontogenetic variability in external morphology of round goby Neogobius melanostomus from Middle Danube, Slovakia

In the previous decade, four species of non‐native goby have invaded the middle section of the River Danube. To understand the problems associated with these invasions better, we examined the external morphology of 184 round goby Neogobius melanostomus specimens using both triple regression (distance‐based measurements) and geometrical (coordinates‐based measurements) analysis within an ontogenetical and epigenetical aspect. Using geometrical analysis of distance‐based characters, we found that the external body shape in four size groups of round goby remained essentially unchanged. Such direct development represents a strongly precocial (i.e. specialized) life‐history, whereas earlier maturation in this non‐native population suggests a shift back towards more altricial (i.e. less specialized, more generalized) life history. This combination of altricial–precocial trajectories seems to be typical for invasive round gobies and may be one of key factors for their successful colonization of new environments.     

Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns

The Eurasian round goby Neogobius melanostomus ( Apollonia melanostoma ) invaded the North American Great Lakes in 1990 through ballast water, spread rapidly, and now is widely distributed and moving through adjacent tributaries. We analyse its genetic diversity and divergence patterns among 25 North American ( N  = 744) and 22 Eurasian ( N  = 414) locations using mitochondrial DNA cytochrome b gene sequences and seven nuclear microsatellite loci in order to: (i) identify the invasion's founding source(s), (ii) test for founder effects, (iii) evaluate whether the invasive range is genetically heterogeneous, and (iv) determine whether fringe and central areas differ in genetic diversity. Tests include F _ST analogues, neighbour-joining trees, haplotype networks, Bayesian assignment, Monmonier barrier analysis, and three-dimensional factorial correspondence analysis. We recovered 13 cytochrome b haplotypes and 232 microsatellite alleles in North America and compared these to variation we previously described across Eurasia. Results show: (i) the southern Dnieper River population was the primary Eurasian donor source for the round goby's invasion of North America, likely supplemented by some alleles from the Dniester and Southern Bug rivers, (ii) the overall invasion has high genetic diversity and experienced no founder effect, (iii) there is significant genetic structuring across North America, and (iv) some expansion areas show reduced numbers of alleles, whereas others appear to reflect secondary colonization. Sampling sites in Lake Huron's Saginaw Bay and Lake Ontario significantly differ from all others, having unique alleles that apparently originated from separate introductions. Substantial genetic variation, multiple founding sources, large number of propagules, and population structure thus likely aided the goby's ecological success.     

Differential effect of inter- and intraspecific competition on the performance of invasive and native Taraxacum species

Inter- and intraspecific competitive abilities are significant determinants of invasive success and the ecological impact of non-native plants. We tested two major hypotheses on the competitive ability of invasive species using invasive (Taraxacum officinale) and native (T. platycarpum) dandelions: differential interspecific competitive ability between invasive and native species and the kin recognition of invasive species. We collected seeds from two field sites where the two dandelion species occurred nearby. Plants were grown alone, with kin (plants from the same maternal genotype) or strangers (plants from different populations) of the same species, or with different species in a growth chamber, and the performance at the early developmental stage between species and treatments was compared. The invasive dandelions outcompeted the native dandelions when competing against each other, although no difference between species was detected without competition or with intraspecific competition. Populations of native species responded to interspecific competition differently. The effect of kinship on plant performance differed between the tested populations in both species. A population produced more biomass than the other populations when grown with a stranger, and this trend was manifested more in native species. Our results support the hypothesis that invasive plants have better competitive ability than native plants, which potentially contributes to the establishment and the range expansion of T. officinale in the introduced range. Although kin recognition is expected to evolve in invasive species, the competitive ability of populations rather than kinship seems to affect plant growth of invasive T. officinale under intraspecific competition.     

Predator and prey: the role of the round goby Neogobius melanostomus in the western Baltic

Different studies on the position of the non-indigenous species Neogobius melanostomus within the coastal food web of the Pomeranian Bay (western Baltic) were performed, resulting in a quantitative and qualitative species list of prey organisms found in the stomachs of the invader and an estimation concerning the importance of round goby as prey for different resident predators. It seems that the colonization process is not fully completed yet, but the results reveal that the species is already established in the food web 16 years after the first observation within the study area. The results show that N. melanostomus feed upon a wide range of different resident organisms. While a direct predation effect on native fish species appears rather unlikely, indirect effects such as competition cannot yet be excluded. In addition, our results reveal an ontogenetic diet shift and that the round goby itself already serves as an important prey for piscivorous fish and seabirds. Finally, we formulate different hypotheses based on our results which will require further research.     

Structure of the gut of the racer goby Neogobius gymnotrachelus (Kessler, 1857)

The morphological and histological features of the gut of juvenile racer goby Neogobius gymnotrachelus [range of body mass 0·2–0·9 g and standard length ( L _S) 20·0–38·8 mm] were examined in fish collected from the Włocławek Reservoir on the Vistula River, Poland. Evidence is provided of the stomachless nature of the gut of the racer goby. The intestine of the juveniles lacks the intestinal bulb. A particular feature of the racer goby gut is the secretory oesogaster (the transitional region where the secretory oesophagus merges into the intestine) with multicellular alveolar glands that secrete via a common duct to the surface between the mucosal folds. The cells in the secretory oesogaster alveolar glands are periodic-acid-Schiff (PAS) positive indicating the presence of neutral mucopolysaccharides. It is hypothesized that the secretory oesogaster is evidence of the loss of the functional stomach in this species. There are two sphincters: the oesogaster–intestinal and the intestinal–rectal in the racer goby gut. It can be concluded that the oesogaster–intestinal sphincter is functionally related to the gastro-intestinal sphincter described in many fish species having a stomach. Enterocytes with a distinct brush border and only a few goblet cells are observed in the epithelium along the whole intestine. The existence of vacuoles in the supranuclear region of the rectal enterocytes is also confirmed.     

How old are you—Evaluation of age reading methods for the invasive round goby (Neogobius melanostomus,Pallas 1814)

In the Baltic, the first observation of the round goby (Neogobius melanostomus, Pallas 1814) was made in 1990. Within the past decade the species became invasive and spread rapidly throughout the Baltic Sea. Studies about the fishes potential impacts on resident species promote the need for an increasing knowledge of their basic stock structures such as growth rates, longevity and mortality, which all rely on accurate estimates of age. Former studies on the round goby have used several different age reading techniques. In this study, we compared three standard otolith preparation methods for ageing and present the best procedure for the invasive round goby. The results showed significant differences in age estimates of the same fish between the different preparation methods and between readers. The estimation of the first annulus, the first year, was the most problematic. The overall agreement was lowest when reading the whole otoliths while the best performance was achieved with sectioned and stained preparation method. Depending on method used the growth estimates also differed. The results question comparability between previous studies and highlight the importance of harmonised aging procedures for the round goby for obtaining correct estimates of population parameters such as growth rate, age at maturity, and longevity.     

Morphology and histochemistry of the peripheral olfactory organ in the round goby,Neogobius melanostomus (Teleostei: Gobiidae)

This first comprehensive study of the peripheral olfactory organ from a representative of the large and economically important order of teleost fishes, the Perciformes, shows a compact structure with olfactory sensory neurons distributed widely throughout the olfactory chamber. The spatial organization of the nasal cavity in the bottom-dwelling round goby (Gobiidae, Neogobius melanostomus) was examined using impression material injection, immunocytochemistry, and transmission electron microscopy. The olfactory chamber contains a single olfactory lamella; prominent dorsocaudal lachrymal and ethmoidal accessory nasal sacs are situated ventrocaudal to the chamber. The location of the olfactory mucosa within the olfactory chamber is novel for teleost fish, as it extends beyond the ventral surface to the lateral and dorsal regions. Microvillar olfactory sensory neurons and ciliated olfactory sensory neurons were identified by transmission electron microscopy and the spatial distribution of these two cell types was assessed through immunocytochemistry against olfactory receptor coupled G-proteins. Both G(alphaolf)-immunoreactive ciliated olfactory sensory neurons and the G(alphao)-immunoreactive microvillar form were located throughout the olfactory epithelium. Ciliated crypt cells were G(alphao) immunoreactive and were found throughout the olfactory epithelium of some specimens. The widespread occurrence of olfactory sensory neurons in the olfactory chamber supports the idea that olfactory signaling is important to the survival of the round goby. The prominence of the lachrymal and ethmoidal accessory nasal sacs indicates the capacity to regulate the flow of odorant molecules over the sensory surface of the olfactory sensory neurons, possibly through a pump-like mechanism driven by opercular activity associated with gill ventilation.     

Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications

The round goby Neogobius melanostomus is one of the most wide-ranging invasive fish on earth, with substantial introduced populations within the Laurentian Great Lakes watershed, the Baltic Sea and several major European rivers. Rapid expansion and deleterious ecosystem effects have motivated extensive research on this species; here this research is synthesized. Maps of the global distribution are provided and the invasion history of N. melanostomus, which spread more rapidly at first in North America, but has undergone substantial expansion over the past decade in the Baltic Sea, is summarized. Meta-analyses comparing their size at age, diet, competitors and predators in North American and European ecosystems are provided. Size at age is region specific, with saline habitats typically supporting larger and faster growing individuals than fresh water. Neogobius melanostomus prey differs substantially between regions, demonstrating a capacity to adapt to locally abundant food sources. Neogobius melanostomus comprise at least 50% of the diet of eight taxa in at least one site or life stage; in total, 16 predator taxa are documented from the Laurentian Great Lakes v. five from Eurasia. Invasive N. melanostomus are the only common forage fish to heavily exploit mussels in the Laurentian Great Lakes and the Baltic Sea, facilitating the transfer of energy from mussels to higher trophic levels in both systems. Neogobius melanostomus morphology, life history, reproduction, habitat preferences, environmental tolerances, parasites, environmental effects, sampling strategies and management are also discussed. Neogobius melanostomus inhabit a wide range of temperate freshwater and brackish-water ecosystems and will probably continue to spread via ballast water, accidental bait release and natural dispersal worldwide. Climate change will probably enhance N. melanostomus expansion by elevating water temperatures closer to its energetic optimum of 26° C. Future research needs are presented; most pressing are evaluating the economic effects of N. melanostomus invasion, determining long-term population level effects of egg predation on game-fish recruitment and comparing several variables (density, ecological effects morphology and life history) among invaded ecosystems. This review provides a central reference as researchers continue studying N. melanostomus, often as examples for advancing basic ecology and invasion biology.