The Round Goby, Neogobius melanostomus, a Fish Invader on both sides of the Atlantic Ocean

During the past decade, a bottom-dwelling, aggressive, multiple-spawning fish, the round goby (Gobiidae: Neogobius melanostomus), has spread from its native region in the Ponto-Caspian throughout Europe and to the Laurentian Great Lakes in North America. An international workshop, held at the Hel Marine Station, Poland, was organized to summarize population features of the round goby. Common fish predators of round gobies in the Great Lakes and in native regions are obligate and facultative benthic fishes and occasionally, pelagic fishes. In contrast, the main predator of the round goby in the Gulf of Gdansk is the Great Cormorant (Phalacrocorax carbo). In the Great Lakes, round gobies have lead to the decline of mottled sculpin (Cottus bairdi) and logperch (Percina caprodes) and reduced the hatching success of native fishes by feeding on their eggs. In the Gulf of Gdansk, round gobies have increased in abundance, while three-spined sticklebacks (Gasterosteus aculeatus) have declined. Round gobies have a broad diet throughout their range; larger specimens are molluscivores. There are fewer species of parasites and lower infection rates of round gobies in recently colonized areas than in native areas. Overall, newly colonized round gobies in brackish waters and lakes are smaller, mature earlier, have a male biased operational sex ratio and are more short-lived compared with round gobies from marine (native) habitats.     

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.     

Detection of a diverse marine fish fauna using environmental DNA from seawater samples

Marine ecosystems worldwide are under threat with many fish species and populations suffering from human over-exploitation. This is greatly impacting global biodiversity, economy and human health. Intriguingly, marine fish are largely surveyed using selective and invasive methods, which are mostly limited to commercial species, and restricted to particular areas with favourable conditions. Furthermore, misidentification of species represents a major problem. Here, we investigate the potential of using metabarcoding of environmental DNA (eDNA) obtained directly from seawater samples to account for marine fish biodiversity. This eDNA approach has recently been used successfully in freshwater environments, but never in marine settings. We isolate eDNA from ½-litre seawater samples collected in a temperate marine ecosystem in Denmark. Using next-generation DNA sequencing of PCR amplicons, we obtain eDNA from 15 different fish species, including both important consumption species, as well as species rarely or never recorded by conventional monitoring. We also detect eDNA from a rare vagrant species in the area; European pilchard (Sardina pilchardus). Additionally, we detect four bird species. Records in national databases confirmed the occurrence of all detected species. To investigate the efficiency of the eDNA approach, we compared its performance with 9 methods conventionally used in marine fish surveys. Promisingly, eDNA covered the fish diversity better than or equal to any of the applied conventional methods. Our study demonstrates that even small samples of seawater contain eDNA from a wide range of local fish species. Finally, in order to examine the potential dispersal of eDNA in oceans, we performed an experiment addressing eDNA degradation in seawater, which shows that even small (100-bp) eDNA fragments degrades beyond detectability within days.Although further studies are needed to validate the eDNA approach in varying environmental conditions, our findings provide a strong proof-of-concept with great perspectives for future monitoring of marine biodiversity and resources.     

Ecological plasticity of tubenose goby,a small invader in South Moravian waters

Hydrobiologia - The western tubenose goby Proterorhinus semilunaris, an invasive Ponto-Caspian fish species, has established populations in a wide range of habitat types in the Dyje/Morava river...     

The Relationship between the Distribution of Common Carp and Their Environmental DNA in a Small Lake

Although environmental DNA (eDNA) has been used to infer the presence of rare aquatic species, many facets of this technique remain unresolved. In particular, the relationship between eDNA and fish distribution is not known. We examined the relationship between the distribution of fish and their eDNA (detection rate and concentration) in a lake. A quantitative PCR (qPCR) assay for a region within the cytochrome b gene of the common carp (Cyprinus carpio or ‘carp’), an ubiquitous invasive fish, was developed and used to measure eDNA in Lake Staring (MN, USA), in which both the density of carp and their distribution have been closely monitored for several years. Surface water, sub-surface water, and sediment were sampled from 22 locations in the lake, including areas frequently used by carp. In water, areas of high carp use had a higher rate of detection and concentration of eDNA, but there was no effect of fish use on sediment eDNA. The detection rate and concentration of eDNA in surface and sub-surface water were not significantly different (p≥0.5), indicating that eDNA did not accumulate in surface water. The detection rate followed the trend: high-use water > low-use water > sediment. The concentration of eDNA in sediment samples that were above the limit of detection were several orders of magnitude greater than water on a per mass basis, but a poor limit of detection led to low detection rates. The patchy distribution of eDNA in the water of our study lake suggests that the mechanisms that remove eDNA from the water column, such as decay and sedimentation, are rapid. Taken together, these results indicate that effective eDNA sampling methods should be informed by fish distribution, as eDNA concentration was shown to vary dramatically between samples taken less than 100 m apart.     

Occurrence of non‐native fishes in the Danube east of Vienna (Austria) and potential interactions of invasive gobiids with native fishes

Non‐native fish species pose a major threat to local fish populations and aquatic ecosystems in general. Invasive gobies are a particular focus of research, but with partly inconsistent results. While some studies reported severe detrimental impacts on native species, others have concluded less serious or neutral effects. We provide results from a large‐scale, multi‐annual fish monitoring program on the occurrence and abundance of non‐native fishes in the main stem of a free‐flowing section of the Austrian Danube. Special emphasis was placed on identifying positive or negative interactions of invasive gobies with native species. Whereas most non‐native species occurred too sporadically or were too few in number to infer a direct threat on the local fish community, invasive gobies were among the most common fishes throughout all sampling years. Co‐occurrence analyses revealed species‐ and mesohabitat type‐specific associations of gobies with native species, which were primarily positive. Notably, native predators such as asp, burbot, or perch probably benefit from the ubiquitous gobies. Two characteristic fluvial fishes revealed negative associations with invasive gobies, namely barbel (Barbus barbus) and Danube whitefin gudgeon (Romanogobio vladykovi): they appear to avoid habitats occupied by gobies. Accordingly, high abundances of round and bighead goby most likely resulted in population losses of barbel and whitefin gudgeon, respectively. Overall, our results indicate a limited negative impact of non‐native species in the sampling area. This is because only two out of 51 occurring species were found to be adversely affected by gobies, the share of co‐occurrences with native species was high, and other non‐native species were generally rare. Nevertheless, invasions are highly dynamic, and new non‐native species are likely to occur in the Austrian Danube, calling for continued monitoring and awareness.     

Improved Methods for Capture,Extraction, and Quantitative Assay of Environmental DNA from Asian Bigheaded Carp (Hypophthalmichthys spp.)

Indirect, non-invasive detection of rare aquatic macrofauna using aqueous environmental DNA (eDNA) is a relatively new approach to population and biodiversity monitoring. As such, the sensitivity of monitoring results to different methods of eDNA capture, extraction, and detection is being investigated in many ecosystems and species. One of the first and largest conservation programs with eDNA-based monitoring as a central instrument focuses on Asian bigheaded carp (Hypophthalmichthys spp.), an invasive fish spreading toward the Laurentian Great Lakes. However, the standard eDNA methods of this program have not advanced since their development in 2010. We developed new, quantitative, and more cost-effective methods and tested them against the standard protocols. In laboratory testing, our new quantitative PCR (qPCR) assay for bigheaded carp eDNA was one to two orders of magnitude more sensitive than the existing endpoint PCR assays. When applied to eDNA samples from an experimental pond containing bigheaded carp, the qPCR assay produced a detection probability of 94.8% compared to 4.2% for the endpoint PCR assays. Also, the eDNA capture and extraction method we adapted from aquatic microbiology yielded five times more bigheaded carp eDNA from the experimental pond than the standard method, at a per sample cost over forty times lower. Our new, more sensitive assay provides a quantitative tool for eDNA-based monitoring of bigheaded carp, and the higher-yielding eDNA capture and extraction method we describe can be used for eDNA-based monitoring of any aquatic species.     

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.     

Using occupancy modelling to compare environmental DNA to traditional field methods for regional‐scale monitoring of an endangered aquatic species

Environmental DNA (eDNA) monitoring approaches promise to greatly improve detection of rare, endangered and invasive species in comparison with traditional field approaches. Herein, eDNA approaches and traditional seining methods were applied at 29 research locations to compare method‐specific estimates of detection and occupancy probabilities for endangered tidewater goby (Eucyclogobius newberryi). At each location, multiple paired seine hauls and water samples for eDNA analysis were taken, ranging from two to 23 samples per site, depending upon habitat size. Analysis using a multimethod occupancy modelling framework indicated that the probability of detection using eDNA was nearly double (0.74) the rate of detection for seining (0.39). The higher detection rates afforded by eDNA allowed determination of tidewater goby occupancy at two locations where they have not been previously detected and at one location considered to be locally extirpated. Additionally, eDNA concentration was positively related to tidewater goby catch per unit effort, suggesting eDNA could potentially be used as a proxy for local tidewater goby abundance. Compared to traditional field sampling, eDNA provided improved occupancy parameter estimates and can be applied to increase management efficiency across a broad spatial range and within a diversity of habitats.     

Repurposing environmental DNA samples—detecting the western pearlshell (Margaritifera falcata) as a proof of concept

Information on the distribution of multiple species in a common landscape is fundamental to effective conservation and management. However, distribution data are expensive to obtain and often limited to high‐profile species in a system. A recently developed technique, environmental DNA (eDNA) sampling, has been shown to be more sensitive than traditional detection methods for many aquatic species. A second and perhaps underappreciated benefit of eDNA sampling is that a sample originally collected to determine the presence of one species can be re‐analyzed to detect additional taxa without additional field effort. We developed an eDNA assay for the western pearlshell mussel (Margaritifera falcata) and evaluated its effectiveness by analyzing previously collected eDNA samples that were annotated with information including sample location and deposited in a central repository. The eDNA samples were initially collected to determine habitat occupancy by nonbenthic fish species at sites that were in the vicinity of locations recently occupied by western pearlshell. These repurposed eDNA samples produced results congruent with historical western pearlshell surveys and permitted a more precise delineation of the extent of local populations. That a sampling protocol designed to detect fish was also successful for detecting a freshwater mussel suggests that rapidly accumulating collections of eDNA samples can be repurposed to enhance the efficiency and cost‐effectiveness of aquatic biodiversity monitoring.     

Short-term predator avoidance behavior by invasive and native amphipods in the Great Lakes

Understanding predator avoidance behavior by prey remains an important topic in community and invasion ecology. Recently, the Ponto-Caspian amphipod Echinogammarus ischnus (Stebbing 1898) was accidentally introduced into the Great Lakes. Since its introduction, it has displaced the native amphipod, Gammarus fasciatus (Say 1818), from several locations in the lower lakes. To assess whether behavioral differences in predator avoidance might be a causal mechanism increasing the success of the invasive amphipods, two experiments were conducted examining (1) native and invasive amphipod behavioral responses to five fish species with different foraging behaviors, and (2) amphipod responses to different densities of round gobies, a hyper-abundant benthic invertivore. Echinogammarus reduced its distance moved in the presence of all fish species tested, whereas Gammarus reduced its distance moved only after exposure to round gobies, black crappies, and rainbow darters. Both amphipod species increased the time spent motionless following exposure to round gobies, but not after encountering the scent of most of the remaining fish predators. The exception was that Echinogammarus also responded to black crappie scent whereas Gammarus did not. Although both amphipod species exhibited behavioral responses to many of the fish predators, the magnitude of their responses differed only after exposure to the brown bullhead. In the bullhead trials, Echinogammarus reduced its distance traveled significantly more than Gammarus. Both amphipod species increased their avoidance response to increasing goby density, however, the pattern of avoidance behavior was different. Invasive E. ischnus exhibited a consistently strong avoidance response to round gobies over the test duration. Native G. fasciatus initially avoided goby scent, but then either ceased their avoidance response or showed a hyper-avoidance response, depending on goby density. These results suggested (1) both species of amphipods were able to differentiate and react to a variety of fish predators, (2) invasive Echinogammarus amphipods avoided a larger range of fish predators than the native Gammarus, (3) increased avoidance behavior was associated with an increased density of fish, and (4) the avoidance response patterns of invasive Echinogammarus when faced with round goby predators might lead to increased predation on native Gammarus in habitats where they co-occur.     

Identifying spawning sites and other critical habitat in lotic systems using eDNA “snapshots”: A case study using the sea lamprey Petromyzon marinus L.

Many aquatic species of conservation concern exist at low densities and are inherently difficult to detect or monitor using conventional methods. However, the introduction of environmental (e)DNA has recently transformed our ability to detect these species and enables effective deployment of limited conservation resources. Identifying areas for breeding, as well as the ecological distribution of species, is vital to the survival or recovery of a conservation species (i.e., areas of critical habitat). In many species, spawning events are associated with a higher relative abundance of DNA released within an aquatic system (i.e., gametes, skin cells etc.), making this the ideal time to monitor these species using eDNA techniques. This study aims to examine whether a “snapshot” eDNA sampling approach (i.e., samples taken at fixed points in chronological time) could reveal areas of critical habitat including spawning sites for our target species Petromyzon marinus. We utilized a species‐specific qPCR assay to monitor spatial and temporal patterns in eDNA concentration within two river catchments in Ireland over three consecutive years. We found that eDNA concentration increased at the onset of observed spawning activity and patterns of concentration increased from downstream to upstream over time, suggesting dispersal into the higher reaches as the spawning season progressed. We found P. marinus to be present upstream of several potential barriers to migration, sometimes in significant numbers. Our results also show that the addition of a lamprey‐specific fish pass at an “impassable” weir, although assisting in ascent, did not have any significant impact on eDNA concentration upstream after the pass had been installed. eDNA concentration was also found to be significantly correlated with both the number of fish and the number of nests encountered. The application of snapshot sampling techniques for species monitoring therefore has substantial potential for the management of low‐density species in fast‐moving aquatic systems.     

Performance of eDNA assays to detect and quantify an elusive benthic fish in upland streams

The sensitivity and specificity of eDNA-based monitoring, coupled with its potential utility to estimate population density or biomass, makes it a useful tool in invasive species management. In this study, we investigated the potential of the eDNA method to improve the detection of the elusive invasive fish, oriental weatherloach (Misgurnus anguillicaudatus), in a river system where a density gradient of the species occurs. We compared detection rates between eDNA and conventional monitoring methods and examined the relationship between eDNA and abundance in a flowing environment. The eDNA method had a higher site detection rate than conventional methods (63 vs. 38%). Weatherloach eDNA was detected at all sites where the fish has been previously caught and none of the sites where the species has not been caught for the past 7 years. There was an increasing density trend going downstream based on long-term conventional monitoring, but the eDNA concentration in water samples reflected this trend only in a continuous section of the river where impoundments were absent. We did not find a positive relationship between eDNA concentration and contemporary abundance estimates in our study area. A high eDNA concentration was recorded at a site (DVC) which was designated a low density site based on long-term catch data. This discrepancy was a likely result of physical habitat characteristics which influenced the efficiency of the conventional methods used. This study highlighted the challenges of inferring density from eDNA data in flowing water because habitat features may confound results, necessitating careful consideration for results to be useful to management.     

Phylogeography and origin of freshwater populations of tubenose gobies of genus Proterorhinus (Gobiidae: Pisces) in Ponto-Caspian Basin

Representatives of the genus Proterorhinus (tubenose gobies) from the water bodies of the Ponto-Caspian Basin were examined for sequence polymorphism of the mitochondrial DNA fragment containing the cytochrome b (Cyt-b) gene. A total of ten haplotypes were discovered, which formed two groups. Thus, the data obtained indicated the existence of only two taxonomically valid phylogenetic lineages, represented by (1) marine and brackish-water populations of the Black Sea and (2) freshwater populations of the whole Ponto-Caspian Basin, along with the brackish-water population of the Caspian Sea. Based on an analysis of the tubenose goby haplotype distribution patterns, the colonization patterns of this group of fishes (phylogeography) in the freshwater drainages of Ponto-Caspian Basin are examined. It was established that the basin of the ancient Caspian Sea was the major donor area for the formation of the freshwater and brackish-water populations. In the Ponto-Caspian Basin, two centers of the tubenose gobies speciation and distribution are distinguished. One of these centers is associated with the modern northwestern part of the Black Sea, and another one is confined to the Caspian Sea. It is suggested that the modern colonization of the Volga River by tubenose goby occurred from the Caspian Sea.     

Environmental DNA detects a rare large river crayfish but with little relation to local abundance

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A probabilistic model for designing and assessing the performance of eDNA sampling protocols

Environmental DNA (eDNA) sampling, the detection of species‐specific genetic material in water samples, is an emerging tool for monitoring aquatic invasive species. Optimizing eDNA sampling protocols can be challenging because there is imperfect understanding of how each step of the protocol influences its sensitivity. This paper develops a probabilistic model that characterizes each step of an eDNA sampling protocol to evaluate the protocol's overall detection sensitivity for one sample. The model is then applied to analyse how changes over time made to the eDNA sampling protocol to detect bighead (BH) and silver carp (SC) eDNA have influenced its sensitivity, and hence interpretation of the results. The model shows that changes to the protocol have caused the sensitivity of the protocol to fluctuate. A more efficient extraction method in 2013, new species‐specific markers with a qPCR assay in 2014, and a more efficient capture method in 2015 have improved the sensitivity, while switching to a larger elution volume in 2013 and a smaller sample volume in 2015 have reduced the sensitivity. Overall, the sensitivity of the current protocol is higher for BH eDNA detection and SC eDNA detection compared to the original protocol used from 2009 to 2012. The paper shows how this model of eDNA sampling can be used to evaluate the effect of proposed changes in an eDNA sampling and analysis protocol on the sensitivity of that protocol to help researchers optimize their design.     

Detection of Adult Green Sturgeon Using Environmental DNA Analysis

Environmental DNA (eDNA) is an emerging sampling method that has been used successfully for detection of rare aquatic species. The Identification of sampling tools that are less stressful for target organisms has become increasingly important for rare and endangered species. A decline in abundance of the Southern Distinct Population Segment (DPS) of North American Green Sturgeon located in California’s Central Valley has led to its listing as Threatened under the Federal Endangered Species Act in 2006. While visual surveys of spawning Green Sturgeon in the Central Valley are effective at monitoring fish densities in concentrated pool habitats, results do not scale well to the watershed level, providing limited spatial and temporal context. Unlike most traditional survey methods, environmental DNA analysis provides a relatively quick, inexpensive tool that could efficiently monitor the presence and distribution of aquatic species. We positively identified Green Sturgeon DNA at two locations of known presence in the Sacramento River, proving that eDNA can be effective for monitoring the presence of adult sturgeon. While further study is needed to understand uncertainties of the sampling method, our study represents the first documented detection of Green Sturgeon eDNA, indicating that eDNA analysis could provide a new tool for monitoring Green Sturgeon distribution in the Central Valley, complimenting traditional on-going survey methods.     

环境DNA技术在贻贝入侵监测中的应用挑战

沼蛤(Limnoperna fortunei)和斑马贻贝(Dreissena polymorpha)是淡水系统中常见的入侵贻贝物种,对其种群规模的持续监测是入侵贻贝防治管控中的关键环节。随着分子生物学技术的发展,入侵物种监测中逐渐尝试利用环境DNA(eDNA)技术实现快速、灵敏检测。然而,在入侵物种引入-定植-扩散过程的监测中,eDNA技术的灵敏度及定量效果受到诸多因素的影响,给实际应用带来挑战。系统梳理了国内外学者利用eDNA技术监测沼蛤、斑马贻贝等入侵物种的研究进展;分析了eDNA技术的采样方案、引物设计、定量分析、质量保证、原位便携仪器设计等影响监测效率与准确率的关键环节;进一步探讨了eDNA技术在贻贝入侵监测中的优势和局限性,以及未来的改进方向。     

Establishing an environmental DNA method to detect and estimate the biomass of Sakhalin taimen,a critically endangered Asian salmonid

For field ecologists, detecting a target species in the wild is a severe bottleneck to understanding its distribution and population status. Recently, environmental DNA (eDNA) techniques have been developed as a noninvasive monitoring tool for aquatic organisms. While applications of eDNA techniques for biomass estimation have been proposed, little is known about an applicable size range of the organisms, which might affect relationships between biomass and eDNA concentration. Here, we investigated eDNA from Sakhalin taimen (Parahucho perryi), a giant salmonid species of northern Japan. This species is critically endangered and difficult to detect in the wild by conventional sampling methods. Using quantitative real-time PCR, we tested correlations between eDNA concentration and fish density using fish with a wide range of ages and body sizes in aquarium experiments. We found that our new primers and probe were truly species-specific, and that the eDNA concentration was significantly correlated with fish density and body size (p < 0.001). Furthermore, based on our calculation, the eDNA concentrations were rather constant among aquaria with fish in different age and size groups when their total weight was adjusted. These results suggest that eDNA concentrations can be an indicator of biomass of Sakhalin taimen, although further research is needed for its application in natural environments.