Genetic analysis reveals the diversity of larval Gobiidae in a temperate estuary

Using molecular tools to examine Gobiidae, the second most abundant taxon in ichthyoplankton samples in the Gulf of Riga (Baltic Sea), the sand goby Pomatoschistus minutus was the most abundant taxon (82% of all individuals analysed), the common goby Pomatoschistus microps constituted 12% and the black goby Gobius niger 6%. The spatiotemporal distribution of P. microps and G. niger indicated a preference for habitats closer to the river inlet and their abundances increased slightly towards the end of the sampling period in summer. The species composition was interpreted in the context of the prevailing habitat conditions, characterized by extremely low water transparency, low salinity, limited spread of vegetated area and dominance of sandy–muddy substrata.     

Sperm adaptation in relation to salinity in three goby species

In externally fertilizing species, the gametes of both males and females are exposed to the influences of the environment into which they are released. Sperm are sensitive to abiotic factors such as salinity, but they are also affected by biotic factors such as sperm competition. In this study, the authors compared the performance of sperm of three goby species, the painted goby, Pomatoschistus pictus, the two-spotted goby, Pomatoschistus flavescens, and the sand goby, Pomatoschistus minutus. These species differ in their distributions, with painted goby having the narrowest salinity range and sand goby the widest. Moreover, data from paternity show that the two-spotted goby experiences the least sperm competition, whereas in the sand goby sperm competition is ubiquitous. The authors took sperm samples from dissected males and exposed them to high salinity water (31 PSU) representing the North Sea and low salinity water (6 PSU) representing the brackish Baltic Sea Proper. They then used computer-assisted sperm analysis to measure the proportion of motile sperm and sperm swimming speed 10 min and 20 h after sperm activation. The authors found that sperm performance depended on salinity, but there seemed to be no relationship to the species' geographical distribution in relation to salinity range. The species differed in the proportion of motile sperm, but there was no significant decrease in sperm motility during 20 h. The sand goby was the only species with motile sperm after 72 h.     

Spatiotemporal and gender‐specific parasitism in two species of gobiid fish

Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through aquatic invertebrates. Infections also showed significant spatiotemporal variation. Trematodes in the eyes were very few in some locations, but infection levels were higher among females than males, suggesting differences in exposure or resistance between the sexes. To test between these hypotheses, we experimentally exposed male and female sand gobies to infection with the eye fluke Diplostomum pseudospathaceum. These trials showed that the fish became readily infected and females had higher parasite numbers, supporting higher susceptibility of females. Eye fluke infections also caused high cataract intensities among the fish in the wild. Our results demonstrate the potential of these parasites to influence host condition and visual abilities, which may have significant implications for survival and mate choice in goby populations.     

Parasite transfer from crustacean to fish hosts in the Lübeck Bight,SW Baltic Sea

Four helminth parasites out of 19 species found in the Lübeck Bight, Baltic Sea, were chosen for investigations on the transfer from invertebrate to small-sized fish hosts: larvae of the tapewormsSchistocephalus sp. andBothriocephalus sp. (Cestoda) living in planktonic copepods as primary hosts;Podocotyle atomon (Digenea) andHysterothylacium sp. (Nematoda) were found in benthic crustaceans, especiallyGammarus spp. These hosts were the prey of 3 gobiid fishes,Gobiusculus flavescens (feeding mainly on plankton),Pomatoschistus minutus (preferring benthos), andP. pictus (feeding more on plankton than benthos). Because the fishes selected smaller sizes of crustaceans, they ingested all stages of the copepods but only the smaller-sized groups of gammarids which were often less infested by parasites. In order to evaluate the probability for a fish to be parasitized by a helminth, an infestation potential index (IP) was calculated.Podocotyle atomon andHysterothylacium sp. revealed an IP which was far lower in gobies than expected when the prevalences of the previous hosts were taken into consideration. The IP of tapeworm larvae was mainly influenced by the feeding pressure of the gobiid predators, which might change with developmental stage and season. It is concluded that parasite transfer to the next host decreases when sizes of prey and predator differ only moderately. This mechanism can reduce the numbers of parasites transferred to less suitable or wrong hosts.     

The importance of gobies (Gobiidae,Teleostei) as hosts and transmitters of parasites in the SW Baltic

The parasite fauna of five goby species (Gobiidae, Teleostei) was investigated in the Baltic Sea during the period 1987 to 1990. 13 parasite species were found in samples from the Lübeck Bight:Bothriocephalus scorpii, Schistocephalus sp. (Cestoda);Cryptocotyle concavum, Cryptocotyle lingua, Podocotyle atomon, Derogenes varicus (Digenea);Hysterothylacium sp. (cf.auctum),Contracaecum sp.,Anisakis simplex (Nematoda);Corynosoma sp.,Echinorhynchus gadi, Neoechinorhynchus rutili, Pomphorhynchus laevis (Acanthocephala). The number of parasite species were: 10 in the sand gobyPomatoschistus minutus, 8 in the black gobyGobius niger, 7 in the two-spotted gobyGobiusculus flavescens, 6 in the common gobyPomatoschistus microps, and 5 in the painted gobyPomatoschistus pictus. Neoechinorhynchus rutili occurred only inP. minutus, andCorynosoma sp. only inG. niger. The extent to which the gobies were parasitized clearly depended on the respective ways of life and, moreover, on the kind of prey ingested by the hosts. Additionally, the age of the hosts might be important. The highest rate of parasitism, more than 60%, was reached byHysterothylacium sp. inG. niger and byCryptocotyle concavum inP. microps. Infestation incidence lay mostly below 40% which means a satellite species status (Holmes, 1991). The number of parasite species was highest in summer; the highest intensities of single parasites occurred in spring (Podocotyle atomon) or autumn (Crytocotyle concavum).Bothriocephalus scorpii, Hysterothylacium sp. andPodocotyle infested their juvenile hosts very early, but onlyHysterothylacium was accumulated byG. niger during its whole life span, whereasBothriocephalus persisted also in older gobies in low intensities. The cercariae ofCryptocotyle spp. penetrate actively into their hosts; all the other parasites named were transmitted in larval form by prey organisms which consisted mainly of planktonic and benthic crustaceans. The gobies were final hosts for only 5 parasites; but two species may be transmitted to larger fish, and 6 species to sea birds or mammals. The parasite community of the five gobies may possibly be taken to characterize the ecological quality of the environment of the Lübeck Bight.     

Structure,growth and production of a remarkably abundant population of the common goby,Pomatoschistus microps (Actinopterygii: Gobiidae)

The common goby, Pomatoschistus microps, is a relevant species from estuarine food webs, playing important roles as predator of polychaetes and crustaceans and as prey for larger fishes and crustaceans. The Minho estuary (NW Portugal) is a relatively well-preserved and productive system. To assess the population structure and production of P. microps in this estuary, monthly samples were undertaken in three different areas along an estuarine gradient in the lower estuary. The density of P. microps varied considerably among seasons and sampling stations, with higher densities occurring in summer and autumn. The lowest densities were found closer to the sea. In general, the density of females was higher than the density of males in all sampling stations, while juveniles were more abundant within a salt marsh area. Compared with other European estuaries, our data showed a remarkable higher density and production values of P. microps. This may be related to the high freshwater input and the low salinities found in this estuary. In addition, we hypothesize that the lower density of the sympatric species P. minutus and the high availability of bivalve shells observed in the Minho estuary may have also contributed to the present results, once P. minutus and P. microps often display a diet overlap and the bivalve shells are crucial for the common goby reproduction.     

Isolation of microsatellite loci and cross‐species amplifications in three gobiid fish of the genus Pomatoschistus

Gobiids of the genus Pomatoschistus are increasingly being investigated as models for adaptation to coastal environments and for mating system studies. Among the dozen currently analysed species, microsatellite primers have been characterized only for Pomatoschistus minutus. This paper describes seven new polymorphic loci isolated from Pomatoschistus marmoratus and Pomatoschistus microps, two species that hybridize. Cross‐species amplification was tested for these new loci, together with seven already published P. minutus loci. Systematic amplification of samples of each of the three species provided a first indication of their polymorphism.     

Differential modes of selection on the rhodopsin gene in coastal Baltic and North Sea populations of the sand goby,Pomatoschistus minutus

An excellent model to elucidate the mechanisms and importance of evolution in the marine environment is the spectral tuning mechanism of the visual pigment in vertebrates. In the sand goby Pomatoschistus minutus (Teleostei; Gobiidae), a distribution‐wide study showed that spatial variation at the rhodopsin gene (RH1) matches the characteristics of specific light environments. This match suggests that populations are locally adapted to selective light regimes targeting the RH1 gene. If so, then the direction of selection should depend on the regional spatial and temporal stability of the light conditions. We tested this prediction by comparing goby populations from two regions: the Baltic Sea, characterized by divergent, but temporally stable light conditions, and the North Sea, characterized by locally heterogeneous and temporally variable light conditions. RH1 sequences of 491 Pomatoschistus minutus individuals from 15 locations were analysed. We found that variation at the RH1 gene in the Baltic populations showed signatures of diversifying selection, whereas the RH1 gene in the North Sea showed signatures of stabilizing selection. These different modes of selection are consistent with the regional light conditions and hence support our predictions, but may also be influenced by migration between the open sea and more turbid estuarine environments. An interesting observation is that within one gene, synonymous and non‐synonymous SNPs show a totally different pattern between populations. Population differentiation based on non‐synonymous SNPs of the RH1 gene correlated with spectral variation of the local environment of the sand goby populations. In contrast, the differentiation based on synonymous SNPs of RH1 reflects more the neutral historical pattern of the species.     

Food selectivity versus prey availability: a study using the marine fish Pomatoschistus microps

Summary The food selection of the common goby, Pomatoschistus microps Krøyer, was studied in the field and in laboratory experiments on the Swedish west coast. The three most important prey organisms for P. microps in the study area were Corophium volutator, chironomid larvae and Nereis spp. Corophium was consumed more than any other prey, even when it was not the most abundant prey species in the bottom. One reason may be the higher activity of Corophium above the sediment surface, which may increase its visibility and consequently its vulnerability to visual predators. When P. microps was offered Corophium and chironomid larvae with similar exposure in laboratory experiments, it showed no preference for either of the prey items. It always took the closest mobile prey, regardless of species and size.     

Environmental factors influencing the gobiid assemblage of a Mediterranean Lagoon: Empirical evidence from a long-term study

A severe freshwater inflow during our long-term ichthyological study of the brackish Vaccarès lagoon (1993–1998) helped us to assess the impact of sudden environmental changes on the specific biomass composition of the gobiid population and the catches per unit effort of the black goby Gobius niger, the common goby Pomatoschistus microps and the sand goby P. minutus. In 1993, the composition of the Gobiid fish assemblage of the Vaccarès lagoon was dominated by the black goby (63%) and finally evolved to an assemblage dominated by the common goby (80%). The black goby disappeared from the Vaccarès lagoon 2 years after the inflow, whereas catches of the common goby increased significantly after the environmental changes and reached maximum values in 1998. Catches of sand goby did not seem to be affected by environmental changes and depended on the communication between sea and lagoon. This study showed that evolution of an ecosystem after environmental changes is linked to the reaction that species developed to face perturbations.     

Prey selection of the shallow water fishPomatoschistus minutus (Gobiidae,Teleostei) in the SW Baltic

The aim of this investigation is to demonstrate the reasons of an opportunist feeder to select some components of the available food supply and to avoid others. Object of this test is the eurytopic and euryhaline sand goby,Pomatoschistus minutus (Pallas), from the Luebeck Bight. It inhabits both sand habitats as well as bottoms mixed with pebbles or continuous hard substrates. Therefore, it is often in close contact withMytilus-belts which present a very rich food supply of small crustaceans. The selectivity behaviour of sand gobies from a sand/clay ecotone was compared with that of populations from a stony pier and a sand bottom during the reproduction period. Regarding the numbers of prey organisms, crustaceans of the periphyton were generally preferred at the pier but avoided in the ecotone. The same is valid for prey organisms of the psammal which were preferred by gobies of the sand bottom but mostly avoided by populations of mixed bottoms. Analyses of size selections revealed that the preferred gammarids orJaera isopods were between 2 and 5 mm length. A balanced relation of goby biomass and utilizable food supply (predatory impact index) seems to effect positive selectivity of gammarids in theMytilus-belts or of harpacticoids in the sand bottom.     

Seasonal migrations of the common Goby,Pomatoschistusmicrops (Kroyer), in Morecambe Bay and elsewhere

Summary Seasonal changes in abundance, and also reproduction, of the gobiid Pomatoschistus microps in intertidal pools on mussel beds at Morecambe, Lancashire, were studied from 1956 to 1961. During winter the shore was largely vacated by this species which returned for breeding purposes in spring. Spawning took place in upper shore pools from April to August. After a planktonic life of between 6–9 weeks, young fishes were recruited to the demersal population usually from June to September. A correlation between seasonal migrations and sea temperature is postulated. Geographical variation in occurrence and extent of migration in P. microps and the related sublittoral P. minutus is considered in relation to minimum winter sea temperatures over the southern Boreal and Baltic sea areas. Offshore winter migration has been found to take place in areas where such temperatures normally fall below 5° C, but not where minimum sea temperature is above 7° C. The effect of the severe winter of 1962–63 on certain populations of P. microps is described.     

Small-sized euryhaline fish as intermediate hosts of the digenetic trematodeCryptocotyle concavum

Cercariae of the trematodeCryptocotyle concavum, which encyst in skin and/or kidney of sticklebacks and gobies, were studied in the Schlei Fjord (western Baltic Sea). Mean incidence of dermal cysts was 48 % inGasterosteus aculeatus and 37 % inPungitius pungitius. No cysts were found in the kidneys of sticklebacks. While 97 % ofPomatoschistus microps had encysted metacercariae in the kidneys, only 2 % had cysts in the skin.Pomatoschistus minutus, however, showed hardly any cyst infestation of either skin or kidney. InP. microps the intensity of infestation by metacercariae was frequently more than 50 cysts; in contrast, sticklebacks rarely exhibited more than 5 dermal cysts. Infested fish were larger than 10 mm in total length, the incidence rate increasing with growth. Parasitic infestation depends on ambient salinity:C. concavum was not found at salinities below 4 . In contrast to the high incidence in fish, the first hosts — the snailsHydrobia stagnalis andH. neglecta — showed remarkably low infection rates (3 to 5 %). The findings reported are related to the distribution ofC. concavum, the mode of life of infested fish, the feeding habits of the final hosts and the infestation ofP. microps by other parasites. Evidently,P. microps represents an optimal second host forC. concavum.     

Effects of current and historic habitat fragmentation on the genetic structure of the sand goby Pomatoschistus minutus (Osteichthys,Gobiidae)

Habitat fragmentation is a major force that will influence the evolution of a species and its distribution range. Pomatoschistus minutus, the sand goby, has a North Atlantic–Mediterranean distribution and shows various level of habitat fragmentation along its geographic repartition. The use of mitochondrial sequences of the cytochrome b (cyt b) gene and two co‐dominant sets of nuclear markers (introns and microsatellites) allowed us to describe the relationships between P. minutus populations belonging to several different geographical regions of Europe and to assess the structure of populations inhabiting the Golfe du Lion, along the French Mediterranean coast. The present study confirms that the taxon located in the Adriatic Sea (Venice) should be considered as a distinct species, separated approximately 1.75 Mya. The comparison of P. minutus between the Atlantic and western Mediterranean coasts using polymorphic co‐dominant markers revealed that they belong to two demographically independent units, and thus could be considered as well as distinct species, more recently separated (0.3 Mya). The Pleistocene glaciations seem therefore to have played an important role in the diversification of this complex. Finally, at a regional scale in the Golfe du Lion, P. minutus appears to form a single huge homogeneous population. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 175–198.     

Distributional and demographic consequences of Pleistocene climate fluctuations for a marine demersal fish in the north-eastern Atlantic

Aim The Pleistocene glaciations were the most significant historical event during the evolutionary life span of most extant species. However, little is known about the consequences of these climate changes for the distribution and demography of marine animals of the north‐eastern Atlantic. The present study focuses on the phylogeographic and demographic patterns of the sand goby, Pomatoschistus minutus (Teleostei: Gobiidae), a small marine demersal fish. Location North‐eastern Atlantic, Mediterranean, Irish, North and Baltic seas. Methods Analysis was carried out by sequencing the mtDNA cytochrome b gene of sand gobies from 12 localities throughout the species’ range, and using this information in combination with published data of allozyme markers and mtDNA control region sequences. Several phylogenetic methods and a network analysis were used to explore the phylogeographic pattern. The historical demography of P. minutus was studied through a mismatch analysis and a Bayesian skyline plot. Results Reciprocal monophyly was found between a Mediterranean Sea (MS) clade and an Atlantic Ocean (AO) clade, both with a Middle Pleistocene origin. The AO Clade contains two evolutionary significant units (ESUs): the Iberian Peninsula (IB) Group and the North Atlantic (NA) Group. These two groups diverged during Middle Pleistocene glacial cycles. For the NA Group there is evidence for geographic sorting of the ancestral haplotypes with recent radiations in the Baltic Sea, Irish Sea, North Sea and Bay of Biscay. The demographic histories of the Mediterranean Clade and the two Atlantic ESUs were influenced mainly by expansions dated as occurring during the Middle Pleistocene glaciations and post‐Eem, respectively. Main conclusions The pre‐LGM (Last Glacial Maximum) subdivision signals were not erased for P. minutus during the LGM. Middle Pleistocene glaciations yielded isolated and differently evolving sets of populations. In contrast to the case for most other taxa, only the northern Atlantic group contributed to the post‐glacial recolonization. The historical demography of Mediterranean sand gobies was influenced mainly by Middle Pleistocene glaciations, in contrast to that of the Atlantic populations, which was shaped by Late Pleistocene expansions.     

Has the invasive round goby caused new links in Baltic food webs?

The Ponto-Caspian round goby (Neogobius melanostomus, Pallas 1814) most probably was established in the Gulf of Gdańsk, Baltic Sea, in the late 1980’s and has since become one of the dominant species in the region. In this study we assess the role of round gobies as prey for two important fish species in the Gulf of Gdańsk, cod (Gadus morhua) and perch (Perca fluviatilis). We compared their present diet with stomach analyses from the area prior the round goby establishment, as well as with diet analysis from Baltic regions where round gobies are absent. There were large differences in the diet between cods from the Gulf of Gdańsk 2003–2006 compared to cods in earlier studies (1977–1981) from the Southern Baltic Sea. There were also large differences in cod and perch diets from areas with and without round goby. Presently, round goby constitutes the most important prey for medium sized cods in Gulf of Gdańsk, and perch from the same area almost exclusively feed on gobiids. Stomach analysis, trophic level estimates, and stable isotope analyses all indicated that cod and perch in Gulf of Gdańsk after the round goby establishment belonged to a similar trophic level. Beside round goby, no mussel feeding fish contributed much to the diet of cod or at all to the diet of perch. Thus, it is likely that round gobies constitute a new energetic pathway from mussels to top predators. However, due to the short time elapsed after round goby establishment, we can only speculate on the species future impacts on Baltic food webs.     

The forgotten feeding ground: patterns in seasonal and depth-specific food intake of adult cod Gadus morhua in the western Baltic Sea

This study presents the diet composition of western Baltic cod Gadus morhua based on 3150 stomachs sampled year-round between 2016 and 2017 using angling, gillnetting and bottom trawling, which enhanced the spatio-temporal coverage of cod habitats. Cod diet composition in shallow areas (<20 m depth) was dominated by benthic invertebrate species, mainly the common shore crab Carcinus maneas. Compared to historic diet data from the 1960s and 1980s (limited to depth >20 m), the contribution of herring Clupea harengus decreased and round goby Neogobius melanostomus occurred as a new prey species. Statistical modelling revealed significant relationships between diet composition, catch depth, fish length and season. Generalized additive modelling identified a negative relationship between catch depth and stomach content weight, suggesting reduced food intake in winter when cod use deeper areas for spawning and during peak summer when cod tend to avoid high water temperatures. The results of this study highlight the importance of shallow coastal areas as major feeding habitats of adult cod in the western Baltic Sea, which were previously unknown because samples were restricted to deeper trawlable areas. The results strongly suggest that historic stomach analyses overestimated the role of forage fish and underestimated the role of invertebrate prey. Eventually, this study shows the importance of a comprehensive habitat coverage for unbiased stomach sampling programmes to provide a more reliable estimation of top predator diet, a key information for food web analyses and multispecies models.     

Sex‐specific distribution and diet of Platichthys flesus at the end of spawning in the northern Baltic Sea

This study examined the relationship of seascape structure, prey availability and sex on the post‐spawning distribution and diet of European flounder Platichthys flesus in the northern Baltic Sea. The objectives were to determine whether: (1) wave exposure and substratum affect abundance and distribution of P. flesus, (2) diet reflects the benthic prey composition and (3) sex affects the distribution or diet of P. flesus. The results showed that P. flesus was evenly spread in the archipelago with no correlation to wave exposure. The distribution was, however, sex specific; reproductive males dominated the exposed zone and mainly post‐reproductive females dominated the intermediate and sheltered zones. Platichthys flesus fed mainly on two bivalve prey species: blue mussels Mytilus edulis and Baltic tellins Macoma balthica. Hard substratum invertebrates dominated the diet in all habitats and apart from some typical soft substratum species, there was no clear link between fish feeding and the dominance structure of benthic prey. Diet was further sex specific, with females showing a broader range of diet than males. Results suggest that P. flesus is a specialist molluscivore found commonly and equally in soft‐ and hard‐substratum habitats throughout the archipelago area. Previous studies on P. flesus in the Baltic Sea have yielded inconsistent results regarding diet and it has commonly been believed that the distribution of Baltic Sea P. flesus is linked to sand and soft substrata. The present findings emphasize the importance of including the entire range of habitats when diet and regional species distributions are assessed.