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Study design and European range of the highly invasive non‐indigenous round goby Neogobius melanostomus. (a) Map of distribution, with sites where fish were collected for the experiment (A: River Rhine, Germany; B: River Elbe, Germany; and C: Guldborgsund, Denmark) and highlighted sites where introduced round goby is known to exist in brackish harbours with access to both freshwater and seawater sites (white boxes 1, 2, 3). Green colour show native occurences, red colour shows introduced areas. Black arrows show possible routes of introduction into the Baltic Sea and Western Europe. The map is compiled from multiple sources (Hempel, 2017; Kornis et al., 2012; Kvach, 2014; Manné et al., 2013; Mastitsky et al., 2010; Puntila et al., 2018; Teletchea & Beisel, 2018; Vassilev et al., 2012). Also note that the species is introduced and widely spread in the North American Great Lakes (freshwater). (b) Experimental design showing treatment salinities (light blue = 0 PSU, dark blue = 16 PSU) of adults and gametes. Adults were initially placed in communal tubs without nest boxes. They were then separated into smaller spawning groups of 1 male and 2‐3 females with access to a nest box. Any spawned eggs were sampled from an acetate sheet in the nest box. The sheet was split in half, and one half‐clutch was kept in the adults’ spawning salinity, and the other was transferred to the opposite treatment salinity. Sperm were sampled from males and tested in either 0 or 16 PSU salinity. (c) Photograph of a round goby male caught in the river Elbe for the experiment. (d) Zygote development was measured as the proportion of eggs reaching eye spots present zygote stage at day 20, here visible on all normally developing eggs
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Aim
The few fish species able to reproduce across wide osmotic ranges either plastically acclimate sperm performance to, or are locally adapted to, different salinities. The invasive round goby (Neogobius melanostomus) is spreading in Eurasia and the Americas, into both fresh and brackish water. We aim to understand if reproduction in different sal...
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Background and aims:
Determining within-species large-scale variation in phenotypic traits is central to elucidate the drivers of species' ranges. Intraspecific comparisons offer the opportunity to understand how trade-offs and biogeographical history constrain adaptation to contrasted environmental conditions. Here we test whether functional trai...
Citations
... In adults, increased salinity can reduce egg production and fecundity (Pinder et al. 2005;Froneman 2023;Woodley et al. 2023), egg size (Lorrain-Soligon et al. 2023a), or the age at first reproduction (Woodley et al. 2023). In addition, increasing salinity is known to reduce sperm performance, motility, and velocity (Wilder and Welch 2014;Byrne et al. 2015Byrne et al. , 2022Green et al. 2021). Ultimately, salinization can alter community structure (Hart et al. 2003;Anufriieva and Shadrin 2018), across all trophic levels (Hintz and Relyea 2019). ...
... This result suggests that females produced eggs of comparatively lower quality in brackish water, as eggs produced in the freshwater treatment are marginally larger, and larger eggs often have higher hatching success and offspring fitness (Xu et al. 2019;Renoirt et al. 2023). The number of undeveloped eggs (presumably unfertilized given the negative effect of salinity on sperm (Wilder and Welch 2014;Green et al. 2021)) was also higher in brackish water. ...
Although coastal ecosystems are naturally submitted to temporal variations of salinity, salinization has been increasing over time threatening coastal biodiversity. Species that exploit such habitats can thus be exposed to brackish water at different life stages. However, the impacts of variations of salinity on wildlife remain poorly understood. This is particularly true for coastal amphibians, due to the strong dependency of early life stages (embryos and larvae) on aquatic environments. In order to investigate the effect of salinity during egg laying and embryonic and larval development of coastal amphibians, we used a full-factorial design to expose reproductive adults, eggs, and larvae of coastal spined toads (Bufo spinosus) to fresh (0 g.l⁻¹) or brackish water (4 g.l⁻¹). At egg laying, we evaluated parental investment in reproduction. During embryonic and larval development, we assessed effects on survival, development, and growth. We highlighted strong effects of environmental salinity on reproduction (reduced egg laying time, marginally reduced egg size, and reduced investment in reproduction). Responses to salinity were highly dependent on the developmental stages of exposure (stronger effects when individuals were exposed during embryonic development). These effects carried over when exposure occurred at egg laying or during embryonic development, highlighting the importance of the environmental conditions during early life on ontogenetic trajectories. We also highlighted partial compensation when individuals were transferred back to freshwater. Whether the magnitude of these responses can allow coastal biodiversity to overcome the observed detrimental effects of salinization remain to be assessed.
... Amphibian reproduction is negatively influenced by salinity (Karraker, 2007;Tornabene et al., 2021). For instance, salinity can directly affect sperm viability and fertilisation processes in these taxa characterised by external fertilisation (Green et al., 2021), and both field and experimental studies have shown that frogs avoid saline water for spawning (Albecker & McCoy, 2017;Viertel, 1999). In caudates, the salinities of ponds where larvae were found were similar to those of ponds where adults reproduced. ...
Coastal wetlands are naturally subjected to salinity, which is expected to increase through global climate changes. Most species will be affected by these changes, leading to major consequences for community structure and ecosystem functioning.
We investigated variation of salinity of temporary wetlands across spatial (1,000 m from the ocean) and temporal (across three breeding season) scales relevant to coastal biodiversity and used amphibians (six species, sampled across one breeding season) as a model to investigate the consequences of the spatio‐temporal variation of salinity in 24 ponds situated on the Atlantic coast of France.
We show that salinity is a highly dynamic environmental variable that varies widely both across spatial and temporal scales. The spatio‐temporal dynamics of salinity are a critical factor structuring amphibian communities that affect the main amphibian phylogenetic groups (caudates vs. anurans) differently. Temporal variation in salinity disrupts the match between salinity selected by reproductive adults and those experienced later by their developing offspring, which negatively affect reproductive success.
Future changes in coastal salinity are likely to affect the structure and functioning of these ecosystems, excluding salt‐intolerant species and eventually leading to less diverse communities of salt‐tolerant species.
... Behrens et al. [39] showed that more than 60% of analysed individuals survived salinities of 30 PSU in an experimental setup. However, there is no documented established population at oceanic salinity conditions [40][41][42]. In addition, increased salinity values may reduce physiological performance (e.g., feeding [39,41]), competition success, migration distance and individual growth in round goby. ...
... Lag phase a,c D [40] see: latency period 2001 K-strategy (Secondary invasions) a,d P [40] Invasive k-strategists are thought to replace opportunistic r-strategists over the course of time. ...
... Lag phase a,c D [40] see: latency period 2001 K-strategy (Secondary invasions) a,d P [40] Invasive k-strategists are thought to replace opportunistic r-strategists over the course of time. ...
Invasive “game-changer” species cause severe ecological impacts such as “phase shifts” in recipient ecosystems all over the world. Since the early 1990s, the ongoing global spread of the small but highly invasive Ponto-Caspian round goby Neogobius melanostomus into diverse freshwater and marine ecosystems has been observed. We postulate that this species is an ideal model to better understand and mitigate aquatic invasions. Its wide invaded range, as well as its diverse impacts on native species, have triggered a large body of research worldwide concerning its spread, ecology, and traits facilitating invasion. Several hypotheses related to invasiveness have been tested for the round goby, which are also applicable to other invasive species and for understanding general principles in invasion biology. However, a common theory explaining invasion success, especially in round goby, is still lacking. Many case studies do not consider time since invasion and use different sampling protocols and methodologies, hampering the comparability of results and conclusions. We thus propose strengthening the network of goby researchers and establishing long-term databases based on continuous and harmonized monitoring covering all stages of the invasion process as crucial requirements to better understand and manage aquatic invasions. In many cases, such monitoring can easily be integrated into existing survey schemes.
... As such, we should expect males to come under strong selection to produce sperm with flexible phenotypes that match the fertilization environment (Jensen et al., 2013). While there is a large body of evidence that the sperm of external fertilizers have evolved to maximize performance in response to specific abiotic environmental factors, such as water salinity, temperature, and pH (Green et al., 2020;Reinhardt et al., 2015), the potential for sperm plasticity in response to variable fertilization environments is yet to be widely investigated (Green, Niemax, et al., 2021;Jensen et al., 2013). ...
... Nevertheless, a small number of laboratory-based acclimation studies spanning six species of euryhaline fish and two marine spawning invertebrates (a tube worm and a sea urchin) have provided some compelling evidence for salinity-induced phenotypic plasticity in sperm activation. In these species, the optimal osmolality for the activation of sperm motility has been shown to shift and broaden to reflect the osmolality of the acclimation environment (Green, Niemax, et al., 2021;Jensen et al., 2013;Legendre et al., 2016;Linhart et al., 1999;Morita et al., 2004;Palmer & Able, 1987;Taugbol et al., 2017;Tiersch & Yang, 2012). ...
... To our knowledge, a lack of plasticity in sperm-motility activation following acclimation to different osmolalities has only been reported in two fish species: the sand goby (Pomatoschistus minutus), a species with a wide geographic distribution in relation to salinity (Svensson et al., 2017), and the euryhaline round goby (Neogobius melanostomus; Green, Niemax, et al., 2021), a highly invasive species that might respond to novel osmotic environments through rapid local adaptation (Green et al., 2020). The demonstration of plasticity in sperm-motility activation in response to osmotic environment in various vertebrate and invertebrate taxa suggests that this adaptive capacity might be widespread. ...
Evolutionary theory predicts that selection will favor phenotypic plasticity in sperm traits that maximize fertilization success in dynamic fertilization environments. In species with external fertilization, osmolality of the fertilization medium is known to play a critical role in activating sperm motility, but evidence for osmotic‐induced sperm plasticity is limited to euryhaline fish and marine invertebrates. Whether this capacity extends to freshwater taxa remains unknown. Here, we provide the first test for plasticity in sperm‐motility activation in response to osmotic environment in an anuran amphibian. Male common eastern froglets (Crinia signifera) were acclimated to either low (0 mOsmol kg−1) or high (50 mOsmol kg−1) environmental osmolality, and using a split‐sample experimental design, sperm were activated across a range of osmolality treatments (0, 25, 50, 75, 100, and 200 ± 2 mOsmol kg−1). Unexpectedly, there was no detectable shift in the optimal osmolality for sperm‐motility activation after approximately 13 weeks of acclimation (a period reflecting the duration of the winter breeding season). However, in both the low and high acclimation treatments, the optimal osmolality for sperm‐motility activation mirrored the osmolality at the natural breeding site, indicating a phenotypic match to the local environment. Previously it has been shown that C. signifera display among‐population covariation between environmental osmolality and sperm performance. Coupled with this finding, the results of the present study suggest that inter‐population differences reflect genetic divergence and local adaptation. We discuss the need for experimental tests of osmotic‐induced sperm plasticity in more freshwater taxa to better understand the environmental and evolutionary contexts favoring adaptive plasticity in sperm‐motility activation. Local adaptation to environmental osmolality
... These differences are based on differences in the environment, such as biotic toxins (Wendling & Mathias Wegner, 2015), salinity (Caputi et al., 2019;Chen et al., 2021;Green, Apostolou, et al., 2021;Renborg et al., 2014) and/or temperature refugia (Tepolt & Palumbi, 2015). During aquatic species invasions, these environmental factors also present physiological barriers and gradients that can shape the process by which a species establishes (Christensen et al., 2021;Green, Niemax, et al., 2021), evolves (Green, Apostolou, et al., 2021), spreads (Magellan et al., 2019) and interacts with other species in their surrounding environment (Moyle & Light, 1996). ...
Species invasions are a global problem of increasing concern, especially in highly connected aquatic environments. Despite this, salinity conditions can pose physiological barriers to their spread and understanding them is important for management. In Scandinavia’s largest cargo port, the invasive round goby (Neogobius melanostomus), is established across a steep salinity gradient. We used 12 937 SNPs to identify the genetic origin and diversity of three sites along the salinity gradient and round goby from western, central and northern Baltic Sea, as well as north European rivers. Fish from two sites from the extreme ends of the gradient were also acclimated to freshwater and seawater, and tested for respiratory and osmoregulatory physiology. Fish from the high salinity environment in the outer port showed higher genetic diversity, and closer relatedness to the other regions, compared to fish from lower salinity upstream the river. Fish from the high salinity site also had higher maximum metabolic rate, fewer blood cells and lower blood Ca2+. Despite these genotypic and phenotypic differences, salinity acclimation affected fish from both sites in the same way: seawater increased the blood osmolality and Na+ levels, and freshwater increased the levels of the stress hormone cortisol. Our results show genotypic and phenotypic differences over short spatial scales across this steep salinity gradient. These patterns of the physiologically robust round goby are likely driven by multiple introductions into the high salinity site, and a process of sorting, likely based on behaviour or selection, along the gradient. Since this euryhaline fish risks spreading from this area, seascape genomics and phenotypic characterisation can inform management strategies even within an area as small as a coastal harbour inlet.
... In addition, since CASA is an automated procedure, which objectively measures sperm movement according to analysis parameters that were identical for all treatments and experiments, the risk of unconscious bias according to expectations is very low. Of all the output traits from CASA, per cent motile sperm and velocity (mean sperm velocity along a smoothed curvilinear path, VCL) were chosen for further analysis, since these traits have been found to correlate with fertilisation in several teleosts of different clades (Casselman et al., 2006;Gage et al., 2004;Gasparini et al., 2010;Stockley et al., 1997), including gobies reproducing in saltwater (Green, Niemax, et al., 2021b;Locatello et al., 2013). These traits have also been researched in several other studies of both sand gobies Lindström et al., 2021;Svensson et al., 2017) and other gobies (e.g. Green et al., , 2020Green, Apostolou, et al., 2021a;Lindström et al., 2021;Poli et al., 2018), making them suitable for within and cross-species comparisons. ...
... For example, our work on environmental tolerance of sand goby sperm has been instrumental for answering questions on the very rapid spread over a wide environmental gradient by the highly invasive round goby N. melanostomus (e.g. Green, Apostolou, et al., 2021a;Green, Niemax, et al., 2021b). More generally, in the last decades, several species of gobies have become invasive throughout the world, and for most species their reproductive biology is one of the keys to their success (Gertzen et al., 2016;Green, Apostolou, et al., 2021a). ...
In species with alternative reproductive tactics, there is much empirical support that parasitically spawning males have larger testes and greater sperm numbers as an evolved response to a higher degree of sperm competition, but support for higher sperm performance (motility, longevity, speed) by such males is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding‐coloured males (small testes, large mucus‐filled sperm‐duct glands; build nests lined with sperm‐containing mucus, provide care) and parasitic sneaker‐morph males (no breeding colouration, large testes, rudimentary sperm‐duct glands; no nest, no care). We compared motility (proportion motile sperm), velocity, longevity of sperm, gene expression of testes, and sperm morphometrics between the two morphs. We also tested if sperm‐duct gland contents affected sperm performance. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding‐coloured males and two ATP‐related genes were upregulated in sneaker‐morph males. There was a partial evidence of higher sperm velocity in sneaker‐morph males, but no difference in sperm motility. Presence of sperm‐duct gland contents significantly increased sperm velocity, and non‐significantly tended to increase sperm motility, but equally so for the two morphs. The sand goby has remarkably long‐lived sperm, with only small or no decline in motility and velocity over time (5 min vs 22 h), but again, this was equally true for both morphs. Sperm length (head, flagella, total, flagella‐to‐head ratio) did not differ between morphs, and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that increased sperm performance as an adaptation to sperm competition is not a primary target of evolution.
... Theory predicts that selection on sperm in the round goby is strong, since they often reproduce under sperm competition, and detrimental environmental conditions may cause sperm limitation [35][36][37]. Recent studies suggest that the round goby is incapable of acclimating their sperm performance to match novel salinity conditions [38], but there is support for local adaptation in its sperm traits [39]. This has raised the hypothesis that reproduction in widely different environments may be possible due to different ancestral origins of the populations that are now spreading in different aquatic environments within Europe and North America. ...
... Sperm measurements were performed following the same protocol as used in the previous studies to which they were to be compared against ( [35,38,39]; Table 1). Fourteen males caught in Danube (freshwater origin, 0 PSU: N = 14) and twelve males caught near Sozopol on the Bulgarian coast (brackish origin,~16 PSU: N = 12) were kept in aerated tanks with water from their site of capture for less than 7 days, before they were sampled for sperm data at the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences' Laboratory of Marine Ecology, Sozopol, Bulgaria. ...
... Data on sperm motility and sperm velocity tested in freshwater (0 or 1 PSU), brackish (15 or 16 PSU) and marine (30 or 32 PSU) salinities were collected for a total of nine sites from three previously published sources where raw data were available (Green, Havenhand, et al., 2020 [39], Green, Niemax, et al., 2020 [35], 2021 [38]). See Table 1 for details on each site and test salinities. ...
For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salinity from a freshwater and a brackish population within their ancestral Ponto-Caspian region of the round goby, Neogobius melanostomus. These two ancestral populations were then compared to nine additional invaded sites across northern Europe, both in terms of their sperm traits and by using genomic SNP markers. Our results show clear patterns of ancestral adaptations to freshwater and brackish salinities in their sperm performance. Population genomic analyses show that the ancestral ecotypes have generally established themselves in environments that fit their sperm adaptations. Sites close to ports with intense shipping show that both outbreeding and admixture can affect the sperm performance of a population in a given salinity. Rapid adaptation to local conditions is also supported at some sites. Historical and contemporary evolution in the traits of the round goby sperm cells is tightly linked to the population and seascape genomics as well as biogeographic processes in these invasive fishes. Since the risk of a population establishing in an area is related to the genotype by environment match, port connectivity and the ancestry of the round goby population can likely be useful for predicting the species spread.
Identifying new areas of colonisation by alien species is important for early detection and management. Door-knocker species pose problems for traditional predictive models because of lacking presence–absence data, but habitat suitability modelling might overcome this. We here identify the most likely areas for introduction and first establishment of the invasive round goby Neogobius melanostomus to Norway, where it has not yet been registered. We implemented knowledge on dispersal pathways and the species’ biology in a simplified suitability model based on spatial data representing the most relevant environmental variables: distance to international harbours in Norway, distance to the closest population in neighbouring country, salinity, wave exposure, depth and water temperature. The results suggest that there are many potential localities for introduction and first establishment and reveal several hotspots of such areas, especially in less-exposed coastal brackish areas of southern Norway. Especially the region around the Oslo Fjord stands out as being associated with higher risk. Our results could guide future monitoring programmes and increase the chance of early detection of this potential new invader. The study illustrates how spatial analyses can be used to identify the most likely areas for future invasion by an aquatic door-knocker species despite lacking presence–absence data.
The Ponto-Caspian round goby Neogobius melanostomus is a fish well known for its invasion success in North America and Europe. Though it originates from eastern Europe, it is only native to a few rivers in this region. Since the species is physiologically tolerant of varying environmental conditions, rapid spread and establishment to adjacent water basins is likely. Establishment of the species is also associated with ecological consequences. It is therefore important to track its spread close to the native region, which is often overshadowed by reports from further away. Here we report the first evidence of alien invasion in the Aegean watershed by N. melanostomus following a regional monitoring program of the fish fauna. Size- and sex–related characteristics of the population are discussed in relation to its level of establishment.
