Comparative feeding ecology of invasive Ponto-Caspian gobies

Invasions of Ponto-Caspian gobiid fishes are suspected to cause regime shifts in freshwater ecosystems. This study compared the trophic niche differentiations of Neogobius melanostomus and Ponticola kessleri in the upper Danube River using stable isotope analyses (δ¹³C and δ¹⁵N), gut content analyses and morphometric analyses of the digestive tract. Both species were identified as predacious omnivores with high dietary overlap and a generalistic feeding strategy. Amphipods (especially invasive Dikerogammarus spp.) contributed 2/3 to the index of food importance. δ¹⁵N-signatures of N. melanostomus revealed an ontogenetic diet shift and significantly exceeded those in P. kessleri by ~1.5‰, indicating a niche separation of half a trophic level. P. kessleri had shorter uncoiled intestinal tracts than N. melanostomus, indicating a narrower niche and adaptation to animal food. Trophic niches in both species expanded during the growth period with increasing intraguild predation and cannibalism in P. kessleri and increasing molluscivory in N. melanostomus. P. kessleri showed a higher degree of specialization and more stable feeding patterns across seasons, whereas N. melanostomus adapted its diet according to the natural prey availability. The feeding patterns of both species observed in the upper Danube River strongly differ from those in their native ranges, underlining their great plasticity. Both goby species consumed mainly other non-native species (~92% of gut contents) and seemed to benefit from previous invasions of prey species like Dikerogammarus villosus. The invasive success of gobies and their prey mirror fundamental ecological changes in large European freshwater ecosystems.     

What can morphology tell us about ecology of four invasive goby species?

This study presents a detailed comparative analysis of external morphology of four of the most invasive goby species in Europe (round goby Neogobius melanostomus, bighead goby Ponticola kessleri, monkey goby Neogobius fluviatilis and racer goby Ponticola gymnotrachelus) and interprets some ecological requirements of these species based on their morphological attributes. The results are evaluated within an ontogenetic context, and the morphological differences between the species are discussed in terms of the question: can special external shape adaptations help to assess the invasive potential of each species? The morphometric analyses demonstrate important differences between the four invasive gobies. Neogobius melanostomus appears to have the least specialized external morphology that may favour its invasive success: little specialization to habitat or diet means reduced restraints on overall ecological requirements. The other three species were found to possess some morphological specializations (P. kessleri to large prey, N. fluviatilis to sandy habitats and P. gymnotrachelus to macrophytes), but none of these gobies have managed to colonize such large areas or to reach such overall abundances as N. melanostomus.     

Condition status and parasite infection of Neogobius kessleri and N. melanostomus (Gobiidae) in their native and non-native area of distribution of the Danube River

The success of introduced species is often facilitated by escape from the effects of natural predators and parasites. Introduced species can profit from this favourable situation, attaining higher population densities and greater individual sizes in novel areas. In this study, somatic condition and parasite infection were compared between native and non-native populations of Neogobius kessleri Günther; introduced only within the interconnected Danube and Rhine River system, and N. melanostomus (Pallas); widely introduced throughout several river systems in Europe and North America. Higher values of Fulton’s condition factor were observed in non-native populations of both goby species. Neogobius melanostomus attained higher gonadosomatic index values in non-native populations, indicating potential increased investment in reproduction in its new area. A lower splenosomatic index was observed in non-native populations, especially in N. melanostomus. Parasite infracommunity richness and mean abundance were higher in N. kessleri in both native and non-native populations, suggesting higher susceptibility of N. kessleri to these parasites. Non-native populations of both hosts showed higher infra-community richness as a result of acquiring parasites native to the new area, but lower parasite abundance. Differences in success of the introduction and establishment in new areas between the two fish species may be associated with a relatively low parasite infection rate and a higher gonadosomatic index in non-native populations of N. melanostomus in comparison to N. kessleri.     

The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube

The distributions of invasive Neogobius species were investigated in the Slovak section of the River Danube from Bratislava downstream to the village of Chl'aba. During October 2004, the main channel of the Danube was sampled, including by‐pass, head‐race and tail‐race canals of the Gab?íkovo dam, backwaters and the lower‐most sections of the tributaries Malý Dunaj, Hron, Váh and Ipel’. Three Neogobius species already documented in Slovakia were captured (monkey goby Neogobius fluviatilis, bighead goby N. kessleri, round goby N. melanostomus), with the latter two species being found in almost all stretches of the Slovak Danube. Monkey goby had a most limited distribution, and no racer goby N. gymnotrachelus were observed. The abundance of particular Neogobius species appeared to depend on the character of the shoreline habitat, and a possible association between larger towns and the abundance of bighead and round gobies requires further investigation.     

Invasion Genetics of Ponto-Caspian Gobies in the Great Lakes: A ‘Cryptic’ Species, Absence of Founder Effects, and Comparative Risk Analysis

Genetic variability and structure of nonindigenous vs native populations are compared for the Eurasian round goby Neogobius melanostomus and the tubenose goby Proterorhinus marmoratus, which both invaded Lake St. Clair of the North American Great Lakes about 1990. The round goby spread rapidly to all of the Great Lakes and the tubenose goby largely has been restricted to Lake St. Clair, with some recent range extension into western Lake Erie. Risk analyses may indicate whether genetic variability of colonizers is predictive of their relative invasive and establishment successes. The present investigation examined DNA sequence variation across the left domain of the mitochondrial DNA cytochrome b gene in round and tubenose gobies from Eurasian and Great Lakes locations. We also sequenced six additional Neogobius species (including the monkey N.␣fluviatilis, racer N. gymnotrachelus, and bigheadN. kessleri gobies that have been ‘on the move’ in Europe) and the knout goby Mesogobius batrachocephalus from the Black Sea in order to develop diagnostic genetic characters to identify them in case of future and/or undetected invasions and to delineate their phylogenetic relationships. Results show that a diverse number of haplotypes characterize round and tubenose goby populations from both North America and Eurasian sites, fitting a risk analysis prediction of high genetic variability in their successful introductions. Phylogenetic results indicate that the current genus Neogobius is paraphyletic and that the subgenusApollonia thus should be elevated to the level of genus, containingApollonia (N.) melanostomus (the round goby) andA. (N.) fluviatilis (the monkey goby). In addition, there appear to be two separate species of Proterorhinus marmoratus, a marine P. marmoratus Pallas 1814 in the Black Sea (matching the original type locality), and a ‘cryptic’ freshwater species in the Danube and Dnieper Rivers and probably other Eurasian freshwater habitats, as well as invasive in the Great Lakes. We suggest resurrecting the name P. semilunaris Heckel 1837 for the freshwater species (a taxon that was originally described from rivers draining into the Aegean Sea and the Danube River, but was later placed in synonymy with P. marmoratus). An erratum to this article is available at .     

Getting What Is Served? Feeding Ecology Influencing Parasite-Host Interactions in Invasive Round Goby Neogobius melanostomus

Freshwater ecosystems are increasingly impacted by alien invasive species which have the potential to alter various ecological interactions like predator-prey and host-parasite relationships. Here, we simultaneously examined predator-prey interactions and parasitization patterns of the highly invasive round goby (Neogobius melanostomus) in the rivers Rhine and Main in Germany. A total of 350 N. melanostomus were sampled between June and October 2011. Gut content analysis revealed a broad prey spectrum, partly reflecting temporal and local differences in prey availability. For the major food type (amphipods), species compositions were determined. Amphipod fauna consisted entirely of non-native species and was dominated by Dikerogammarus villosus in the Main and Echinogammarus trichiatus in the Rhine. However, the availability of amphipod species in the field did not reflect their relative abundance in gut contents of N. melanostomus. Only two metazoan parasites, the nematode Raphidascaris acus and the acanthocephalan Pomphorhynchus sp., were isolated from N. melanostomus in all months, whereas unionid glochidia were only detected in June and October in fish from the Main. To analyse infection pathways, we examined 17,356 amphipods and found Pomphorhynchus sp. larvae only in D. villosus in the river Rhine at a prevalence of 0.15%. Dikerogammarus villosus represented the most important amphipod prey for N. melanostomus in both rivers but parasite intensities differed between rivers, suggesting that final hosts (large predatory fishes) may influence host-parasite dynamics of N. melanostomus in its introduced range.     

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.     

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.     

Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube

Metazoan parasites were investigated in three non‐native fishes (monkey goby Neogobius fluviatilis, bighead goby Neogobius kessleri and round goby Neogobius melanostomus) collected from the former and current main channel of the River Danube and from the River Hron, Slovakia, in November 2003. Thirteen parasite species were identified: Triaenophorus crassus, Diplostomum sp., Tylodelphys clavata, Metorchis xanthosomus, Nicolla skrjabini, Gyrodactylus proterorhini, Pomphorhynchus laevis, Contracoecum sp., Raphidascaris acus, Anguillicola crassus, Unio tumidus, Anodonta anatina and Pseudoanodonta complanata. The maximum parasite diversity was found in N. fluviatilis. Total parasite abundance was significantly higher in N. kessleri, but no significant differences among sampling sites were observed. Pomphorhynchus laevis and glochidia of Anodonta anatina reached 100% prevalence in N. kessleri in the new channel of the Danube and, in general, these species were also the most prevalent parasites in all three goby species. For endoparasites, gobies served mostly as intermediate (digenean, cestodes and nematodes) or paratenic (acantocephalan and nematodes) hosts. All parasite species found are common parasites in the Middle Danube basin. No parasites specific to Neogobius, known from their native populations, were observed.     

Ontogenetic variability in external morphology of bighead goby Neogobius kessleri from the Middle Danube, Slovakia

Over the last decade, four species of goby have invaded the Middle Danube area, and all of them have spread rapidly. In the early 1990s, bighead goby Neogobius kessleri appeared in the Middle Danube, where it now seems to thrive. Relatively little is known of the environmental biology and ontogeny of this species in its native and non‐native ranges. In this paper, preliminary results on the external morphology of bighead goby from the Slovak stretch of the Danube are presented within an ontogenetic context. Patterns of relative growth with no apparent changes at small size suggest direct development in bighead goby, although not as profoundly direct as observed in round goby N. melanostomus. Differences in life history between these two closely related species may have important implications for their success in novel environments, favouring the latter in short term (several years) and the former in long term (decades and longer) perspective.     

No effect of round goby <Emphasis Type="Italic">Neogobius melanostomus</Emphasis> colonisation on young-of-the-year fish density or microhabitat use

The round goby Neogobius melanostomus has recently invaded several major freshwater systems in Europe and North America. Despite numerous studies predicting an impact on native fish assemblages, few have attempted to demonstrate it. In this case study, we monitored the effect of N. melanostomus colonisation on abundance and habitat utilisation of both young-of-the-year (YOY) native fish and YOY western tubenose goby Proterorhinus semilunaris in a typical, medium-sized European river. Colonisation by N. melanostomus had no apparent effect on either native fish abundance and species richness or P. semilunaris abundance. Moreover, after colonisation, both native fish and P. semilunaris occupied similar niches (i.e. microhabitats) to those occupied before colonisation. While niche use of YOY N. melanostomus and P. semilunaris overlapped significantly, YOY native fish utilised different habitats from the gobiids. We suggest that N. melanostomus did not compete for resources with YOY fish in our study area due to lack of niche overlap and/or surplus resources. As N. melanostomus rapidly dominated the fish assemblage at our site, we further suggest that utilisation of an empty niche, rather than competitive superiority, was the main factor facilitating its success.     

Parasite fauna of native and non‐native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube River

Parasite fauna of round goby Neogobius melanostomus (Pallas, 1814) in the Danube River was investigated in both its native range (two sites in the Bulgarian stretch of the Danube) and non‐native range of distribution (Croatian, Slovak and Austrian stretches) during 2005 and 2006. The aim was to identify possible changes in parasite communities associated with the introduction of a host into the new environment. A total of 29 metazoan parasite species were found to parasitize round goby in the Danube River; twelve of these parasite species were found in both the native and non‐native range of distribution. Introduction of a novel parasite species to the non‐native range via the round goby was not found. Eight parasite species occurred only in the native range and nine species only in the non‐native range of the round goby distribution. Losses of native parasite species in non‐native round goby populations and/or acquiring of novel parasite species in a new environment were not significant. Thirteen parasite taxa were recorded for the first time in round gobies. Three parasite taxa (Diplostomum spp., Pomphorhynchus laevis and Raphidascaris acus) were found in high prevalence and abundance at each sampling site in both the native and non‐native range. Parasite species diversity was assessed for each sampling site and season using three diversity indices (the Shannon, Simpson and Equitability indices), with the highest same‐season values found in a non‐native site in Slovakia (1.38, 0.69 and 0.60, respectively) and the lowest in a native site in Bulgaria (0.28, 0.12 and 0.14, respectively). Species diversity was higher in both non‐native round goby populations (Slovak and Austrian) compared to native Bulgarian populations. However, diversity indices values varied among almost all sampling sites.     

Isolation and characterization of microsatellites in Neogobius kessleri (Perciformes,Gobiidae) and cross‐species amplification within the family Gobiidae

Fourteen polymorphic microsatellites were isolated from Neogobius kessleri, a benthic fish of Ponto‐Caspian origin which has been recently introduced into the Middle and Upper Danube River. Number of alleles and heterozygosity per locus in a sample of 32 fish individuals ranged from two to four and from 0.13 to 0.75, respectively. These primers will be useful in determining the population structure of N. kessleri. In addition, successful cross‐amplification was obtained for four related species, N. melanostomus, N. fluviatilis, N. gymnotrachelus and Proterorhinus marmoratus. These microsatellite loci may be useful for the evaluation of the origin of non‐native goby populations.     

Invasive Ponto-Caspian Amphipods and Fish Increase the Distribution Range of the Acanthocephalan Pomphorhynchus tereticollis in the River Rhine

Non-indigenous species that become invasive are one of the main drivers of biodiversity loss worldwide. In various freshwater systems in Europe, populations of native amphipods and fish are progressively displaced by highly adaptive non-indigenous species that can perform explosive range extensions. A total of 40 Ponto-Caspian round gobies Neogobius melanostomus from the Rhine River near Düsseldorf, North Rhine-Westphalia, Germany, were examined for metazoan parasites and feeding ecology. Three metazoan parasite species were found: two Nematoda and one Acanthocephala. The two Nematoda, Raphidascaris acus and Paracuaria adunca, had a low prevalence of 2.5%. The Acanthocephala, Pomphorhynchus tereticollis, was the predominant parasite species, reaching a level of 90.0% prevalence in the larval stage, correlated with fish size. In addition, four invasive amphipod species, Corophium curvispinum (435 specimens), Dikerogammarus villosus (5,454), Echinogammarus trichiatus (2,695) and Orchestia cavimana (1,448) were trapped at the sampling site. Only D. villosus was infected with P. tereticollis at a prevalence of 0.04%. The invasive goby N. melanostomus mainly preys on these non-indigenous amphipods, and may have replaced native amphipods in the transmission of P. tereticollis into the vertebrate paratenic host. This study gives insight into a potential parasite-host system that consists mainly of invasive species, such as the Ponto-Caspian fish and amphipods in the Rhine. We discuss prospective distribution and migration pathways of non-indigenous vertebrate (round goby) and invertebrates (amphipods) under special consideration of parasite dispersal.     

Age and growth of invasive round goby <Emphasis Type="Italic">Neogobius melanostomus</Emphasis> from middle Danube

Age and growth of the invasive population of round goby Neogobius melanostomus from the Slovak stretch of River Danube was examined. The samples (n=1130) were collected soon after the invasion was recorded (2004–2005), and later, when the population was already established (2008–2010). Invasive round goby in newly-occupied areas were found to reach smaller body size (15–153 mm standard length) compared to native populations. Age from 0+ to 4+, determined from scales, was recorded in both sexes. Annulus formed in April–May, which varied with age. Growth of freshly established gobies was negative allometric, suggesting increased allocation of their sources to reproduction, which corresponds to less specialized life-history. However, positive allometric growth found in longer established individuals suggests a shift in allocation towards somatic growth, which corresponds to more specialized life-history typical for native populations. None of the three parameters predicted by the theory of alternative ontogenies and invasive potential met the expectations, though two parameters, i.e. growth rate and age at maturation remain equivocal. This can be explained by too short of a time span that has elapsed from the beginning of invasion, or by ecological disturbances that have broken up otherwise stable environment in the habitat studied.     

On the finding of round goby <Emphasis Type="Italic">Neogobius melanostomus</Emphasis> (Pallas) (Gobiidae) in the food of burbot <Emphasis Type="Italic">Lota lota</Emphasis> (L.) of the Rybinskoe water reservoir

The fish swallowed by the burbot caught with gill nets in the Volzhskii reach of the Rybinskoe water reservoir in 2007 are investigated. Based on the teretial body shape, the absence of a swim bladder, the presence of a pelvic disc, the dimensions of the skull, the body length, the body weight, and the age, the specimens found in the gut of the burbot are identified as round goby Neogobius melanostomus (Pallas). The round goby should be regarded as an adventive (invasive) species because it is not distributed in different biotopes of the Rybinskoe water reservoir.     

Experimental evidence that ecological effects of an invasive fish are reduced at high densities

Understanding the relationship between invasive species density and ecological impact is a pressing topic in ecology, with implications for environmental management and policy. Although it is widely assumed that invasive species impact will increase with density, theory suggests interspecific competition may diminish at high densities due to increased intraspecific interactions. To test this theory, we experimentally examined intra- and interspecific interactions between a globally invasive fish, round goby (Neogobius melanostomus), and three native species at different round goby densities in a tributary of the Laurentian Great Lakes. Eighteen 2.25 m² enclosures were stocked with native fish species at natural abundances, while round gobies were stocked at three different densities: 0 m^?2, 2.7 m^?2, and 10.7 m^?2. After 52 days, native fish growth rate was significantly reduced in the low density goby treatment, while growth in the high density goby treatment mirrored the goby-free treatment for two of three native species. Invertebrate density and gut content weight of native fishes did not differ among treatments. Conversely, gut content weight and growth of round gobies were lower in the high goby density treatment, suggesting interactions between round gobies and native fishes are mediated by interference competition amongst gobies. Our experiment provides evidence that invasive species effects may diminish at high densities, possibly due to increased intraspecific interactions. This is consistent with some ecological theory, and cautions against the assumption that invasive species at moderate densities have low impact.     

Abundance and night-time habitat use patterns of Ponto-Caspian gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, Hungary

We examined the abundance and meso‐habitat use of gobiid species during both day and night along 43 stretches (500‐m long) of the littoral zone at five locations of the Middle Danube, Hungary, in spring and in summer 2004. Electro‐fishing catch per unit effort sampling revealed significantly higher relative densities at night than during the day. Gobiids occupied all the available habitats encountered during sampling. Habitat‐abundance relationships from night‐time samples revealed that the two most abundant species, round goby Neogobius melanostomus and bighead goby Neogobius kessleri, were found in highest relative density along gravel beach and artificial rip‐rap habitats; these species were in relatively low density in sandy areas. Monkey goby Neogobius fluviatilis was more abundant in natural shorelines than in rip‐rap habitats and dispersed more consistently between sandy and gravel beaches. Tubenose goby Proterorhinus marmoratus demonstrated great plasticity in meso‐habitat use. In conclusion, Ponto‐Caspian gobies occurred rather consistently along the Hungarian section of the Danube, occupying all available habitats examined. Abundance‐habitat relations suggest plasticity in meso‐habitat use but partial segregation between species. Further studies are required at multiple spatial scales to assess how micro‐ and meso‐habitat use varies with fluctuating population densities.     

Historic speciation and recent colonization of Eurasian monkey gobies (Neogobius fluviatilis and N. pallasi) revealed by DNA sequences,microsatellites, and morphology

Aim Hidden diversity within an invasive ‘species’ can mask both invasion pathways and confound management goals. We assessed taxonomic status and population structure of the monkey goby Neogobius fluviatilis across Eurasia, comparing genetic variation across its native and invasive ranges. Location Native populations were analysed within the Black and Caspian Sea basins, including major river drainages (Dnieper, Dniester, Danube, Don and Volga rivers), along with introduced locations within the upper Danube and Vistula river systems. Methods DNA sequences and 10 nuclear microsatellite loci were analysed to test genetic diversity and divergence patterns of native and introduced populations; phylogenetic analysis of mtDNA cytochrome b and nuclear RAG‐1 sequences assessed taxonomic status of Black and Caspian Sea lineages. Multivariate analysis of morphology was used to corroborate phylogenetic patterns. Population genetic structure within each basin was evaluated with mtDNA and microsatellite data using F_ST analogues and Bayesian assignment tests. Results Phylogenetic analysis of mitochondrial and nuclear sequences discerned a pronounced genetic break between monkey gobies in the Black and Caspian Seas, indicating a long‐term species‐level separation dating to c. 3 million years. This pronounced separation further was confirmed from morphological and population genetic divergence. Bayesian inference showed congruent patterns of population structure within the Black Sea basin. Introduced populations in the Danube and Vistula River basins traced to north‐west Black Sea origins, a genetic expansion pattern matching that of other introduced Ponto‐Caspian gobiids. Main conclusions Both genetic and morphological data strongly supported two species of monkey gobies that were formerly identified as subspecies: N. fluviatilis in the Black Sea basin, Don and Volga Rivers, and the Kumo‐Manych Depression, and Neogobius pallasi in the Caspian Sea and Volga River delta. Genetic origins of introduced N. fluviatilis populations indicated a common invasion pathway shared with other introduced Ponto‐Caspian fishes and invertebrates.     

Discrimination between invasive Ponto‐Caspian gobies using a PCR‐RFLP method

Accurate identification of invaders, and especially their juveniles and eggs, is a difficult task if several morphologically similar species co‐occur. The aim of the study was to develop and test a rapid and cost‐effective procedure for identification of five species of invasive gobies occurring in the middle Danube basin, namely round goby Neogobius melanostomus, bighead goby Ponticola kessleri, monkey goby Neogobius fluviatilis, racer goby Babka gymnotrachelus and tubenose goby Proterorhinus semilunaris. First, a 708 bp fragment of the cytochrome oxidase I gene was amplified and sequenced for representative samples of these five species. Appropriate sequences of the five species available in public databases were used for in silico analysis. A digestion of the amplified fragment with the BfaI enzyme was found to be suitable for the species identification, as it showed unique restriction patterns for each species. The technique was also successfully applied for fish remains from burbot Lota lota stomachs. Thus the technique could be a useful tool in monitoring biological invasions, especially by identifying specimens that could not be determined on the basis of morphological features. The results demonstrate that the PCR‐RFLP method may in some cases be more reliable for species identification than a standard DNA sequencing.