Phylogeny and evolution of Indo-Pacific shrimp-associated gobies (Gobiiformes: Gobiidae)

Despite the ubiquity of obligate mutualisms on coral reef ecosystems, little is known about the evolution of many participating species. The shrimp gobies, known primarily from the coral reef habitats of the Indo-Pacific, are small benthic fishes that participate in a remarkable mutualism with alpheid shrimp. In this mutualism, the shrimp build and maintain a burrow that is guarded by the goby, and the shrimp and goby engage in an intricate tactile communication system. The mutualism is obligate for most shrimp gobies as participating species are highly vulnerable to predation when separated from a shrimp partner. We use phylogenetic analysis of nuclear and mitochondrial DNA sequence data to infer evolutionary relationships among shrimp gobies, and between shrimp gobies and their non-mutualistic gobiid relatives. We show that the mutualist shrimp association has arisen twice among gobies, once in a clade composed of Amblyeleotris, Ctenogobiops, and Vanderhorstia, and a second time in a clade including Cryptocentrus, Mahidolia, Tomiamichthys and Stonogobiops. We then compare the evolution of traits within each shrimp goby clade and consider their intrarelationships. We document cryptic diversity among shrimp gobies, with three distinct clades delineated among Mahidolia mysticina specimens captured at the same locality, paired with the same shrimp species. Mahidolia is placed as sister to the Cryptocentrus species Cryptocentrus cinctus; both exhibit pronounced dichromatism, occurring in both brown and yellow (xanthic) forms. We additionally clarify species identities within Amblyeleotris, confirming that widespread similar species Amblyeleotris fasciata, Amblyeleotris steinitzi and Amblyeleotris wheeleri are all distinct. We hypothesize that the flexibility of gobiid gobies and alpheid shrimp to interact with mutualist partners, as well as the apparently highly beneficial nature of mutualism between them, has contributed to the dual evolution of shrimp-association among Indo-Pacific gobies.     

Ontogenetic variability in the external morphology of monkey goby, Neogobius fluviatilis (Pallas, 1814) and its relevance to invasion potential

In the previous decade, four species of non-native gobies have invaded the middle section of the river Danube and its tributaries. An effective tool for understanding biological invasions is the evaluation of various biological traits (morphological, life history, ontogenetic) within an epigenetic context. The present study examines the external morphology of monkey goby Neogobius fluviatilis (Pallas, 1814) from the mouth of the River Hron, the morphological differences among three goby species (monkey, bighead and round) and the relevance of these differences for invasive potential. Monkey goby reach their definite phenotype very early in their ontogeny and thus represent a strongly precocial (specialized) species with direct development. The morphological differences between monkey and two other goby species also reflect its strong specialization for sandy substrata and smaller prey types. Thus, monkey goby are not expected to spread to new areas as fast as the round and bighead gobies, and their distribution is likely to be limited to sandy and/or sandy-gravel substrata. If this assumption is correct, then the potential adverse impact of monkey goby on native fauna or even ecosystem is likely to be less than that of the bighead and round gobies. Handling editor: K. Martens     

Dynamics of demographically open mutualists: immigration, intraspecific competition, and predation impact goby populations

Although it is now recognized that mutualistic species are common and can have stable populations, the forces controlling their persistence are poorly understood. To better understand the mechanisms that impact the stability of obligate mutualists, I conducted several field experiments within a sandy coral reef lagoon in Moorea, French Polynesia that manipulated densities of fish (gobies) that interact mutualistically with shrimp. Obligate, mutualistic partnerships of gobies and shrimp are common on Indo-Pacific coral reefs and have been shown previously to interact as follows: shrimp construct burrows in which both species reside, and gobies warn shrimp of predators through tactile communication. Augmentation of gobies by up to 100% above ambient densities within 9 m² plots produced no change in overall density of gobies or shrimp because gobies competed intraspecifically for a limited number of shrimp burrows and smaller gobies were outcompeted by larger individuals. I used predators to assess the impact of goby removal on the stability of goby and shrimp populations. First, although surveys taken throughout the lagoon revealed no relationship between goby and predator densities, predators correlated negatively with the proportion of adult gobies and positively with the proportion of small gobies paired with large shrimp. Second, experimental augmentation of predators resulted in a dramatic reduction of adult gobies within predator-addition plots, but had no impact on overall densities as immigrants rapidly replaced the missing adult gobies. Furthermore, goby turnover resulted in an increase in the proportion of small gobies paired with large shrimp because body sizes of gobies and shrimp in a burrow were similar prior to predator introduction, and predators apparently had a greater impact on gobies than shrimp. The mechanisms that prevent expansion (intraspecific competition) and collapse (immigration) of goby-shrimp populations likely contribute to local-scale stability of mutualistic populations in other terrestrial and aquatic environments.     

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.     

Stonogobiops yasha, a new shrimp-associated goby from Japan

A new shrimp-associated goby, Stonogobiops yasha sp. nov., is described on the basis of nine specimens collected from the Ryukyu Islands, Japan. This species is easily distinguished from other congeneric species in having reddish-orange stripes on a white body and only two median cephalic sensory pores on the head. Received: July 21, 1999 / Revised: July 10, 2001 / Accepted: July 26, 2001     

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.     

A new goby (Teleostei: Gobiidae) from the South China Sea and its significance for gobioid classification

A new genus and species of gobiid fish, Egglestonichthys Patriciae , is described from the South China Sea. Certain features of the modified head lateral-line system resemble those seen in eleotrine genera with 'transverse' suborbital sensory papillae, but the skeleton of the new goby is essentially gobiine. Aspects of the lateral-line system indicate closest relationship with genera from both the IndoPacific area ( Callogobius complex, Psilogobius, Stonogobiops ) and the New World ( Microgobius ). Wider affinities with other gobiine and gobionelline genera are discussed. Discrepancies between arrangements based predominantly on lateral-line characters and on osteology are noted and their implications considered for future classification of the gobioid fishes.     

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.     

Correlation between body size and fatty acid and essential amino acid composition of round goby (Neogobius melanostomus) and monkey goby (Neogobius fluviatilis) from the Rhine River (Germany)

In this study correlations between body size and muscle fatty and amino acid content of two species of goby, round goby (Neogobius melanostomus) and monkey goby (Neogobius fluviatilis) caught from river Rhine (Germany) were investigated. Among saturated fatty acids (SFAs), mono- (MUFA) and polyunsaturated fatty acids (PUFAs) only SFAs were significantly higher in round goby than monkey goby (P < 0.05). In general, the correlation between body size of both gobies and the content of most of the individual fatty acids was not significant. In monkey goby, the content of palmitic acid (C16:0) and oleic acid (C18:1 n-9) was positively correlated with weight (r = 0.43) and total length (r = ?0.58), respectively, and the content of docosahexaenoic acid (DHA) increased with condition factor (r = 0.50). The content of threonine, arginine, valine, phenylalanine and isoleucine in monkey goby was higher than those of round goby (P < 0.05). In round goby the three essential amino acids arginine, valine and leucine were positively (P < 0.05) correlated with body length, which indicates that longer round gobies are of higher nutritional value.     

Gobies of the genus <Emphasis Type="Italic">Rhinogobius</Emphasis> (Gobiidae) of primorye and water bodies of Central Asia and Kazakhstan: II. Comparative craniological analysis of gobies introduced to Central Asia

The craniological analysis of the gobies introduced from China to Central Asia and identified previously as Rhinogobius cheni based on the sample from the Akkurgan fish farm (basin of the Chirchik River) and the sample from the Saryyazyn water reservoir (basin of the Murgab River) is given. The morphological characteristics of the studied gobies are discussed in connection with the data on the skull structure of the other species of the suborder Gobioidei. It is shown that the level of divergence by the craniological indices between two naturalized populations of the Chinese goby is higher than that between the local populations of the studied species of the European gobies and their populations from the basins of different seas, that can be explained on the basis of the founder principle proceeding from the start states of divergence deviating from the parameters modal for the species.     

Secondary invasion of the round goby into high diversity Great Lakes tributaries and species at risk hotspots: potential new concerns for endangered freshwater species

The round goby (Neogobius melanostomus) first invaded North America in 1990 when it was discovered in the St. Clair River. Despite more than 15 years of potential invasion, many Great Lakes’ lotic systems remained uninvaded. Recently, we captured the round goby from several Great Lakes tributaries known as species-at-risk hotspots. With a combination of field sampling of round gobies and literature review of the impact of round gobies on native taxa, we assess the potential impacts of the secondary invasion to native species using three mechanisms: competition; predation; and indirect impacts from the loss of obligate mussel hosts. We estimate that 89% (17/19) of benthic fishes and 17% (6/36) of mussels that occur in these systems are either known or suspected to be impacted by the secondary invasion of round goby. In particular, we note that the distribution of potential impacts of round goby invasion was largely associated with species with a conservation designation, including seven endangered species (1 fish, 6 mussels). As these recent captures of round goby represent novel occurrences in high diversity watersheds, understanding the potential impacts of secondary invasion to native biota is fundamental to prevent species declines and to allow early mitigation.     

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.     

Comparative energy allocation in two sympatric, closely related gobies: the black goby Gobius niger and the grass goby Zosterisessor ophiocephalus

Seasonal energy allocation of lipid reserves into different body tissues was analysed comparatively in two sympatric, closely related gobies: the grass goby Zosterisessor ophiocephalus and the black goby Gobius niger . Lipid reserves were measured in liver, muscle and ovary and compared between the two species within a given sex and seasonal period (reproductive v . non-reproductive). Furthermore, temporal patterns of lipid reserves were investigated in the two species in relation to gonado-somatic and liver-somatic indices, as well as the relationship between size and lipid content. Results showed that the grass goby allocated more lipid reserves in reproduction while the black goby accumulated more reserves in liver and muscle, at a given size, although the temporal patterns of lipid accumulation and depletion were basically similar. Results are discussed in the light of life-history theories, taking into account both adaptation and evolutionary constraints.     

Occupation,body size and sex ratio of round goby (<Emphasis Type="Italic">Neogobius melanostomus</Emphasis>) in established and newly invaded areas of an Ontario river

Invasive species represent a challenge because the particular characteristics of a species’ invasion are often unknown before the invasion. To provide some clarity as to how invasive species demographic structure might change as a population advances its range, we compared the proportion of occupied sites, size structure and sex ratio of round gobies in the area where they first invaded with more recently invaded areas at the extent of their range in a river in south-eastern Ontario. We used a standardized angling technique to sample gobies larger than 45-mm total length in the summer and early autumn of 2007. Round goby at the upstream and downstream extent of their range occupied a lower proportion of randomly selected sites, and contained a wider distribution of sizes as well as significantly larger individuals. Sex ratios in all areas were male-biased and the male-to-female ratio was significantly higher in the upstream segment of the river (2.2:1) compared to the area of first introduction (1.4:1). The difference between the newly invaded and the established sites suggests that round goby population structure may be affected by density. The results of this study help us further describe the demographic characteristics of biological invasions whilst examples of population structure and behaviour in gobies and other species provide a basis for generating hypotheses for range expansion.     

Seasonal habitat use indicates that depth may mediate the potential for invasive round goby impacts in inland lakes

1. The round goby (Neogobius melanostomus) is among the fastest-spreading introduced aquatic species in North America and is radiating inland from the Great Lakes into freshwater ecosystems across the landscape. Predicting and managing the impacts of round gobies requires information on the factors influencing their distribution in habitats along the invasion front, yet this information is not available for many recently invaded ecosystems. We evaluated the seasonal habitat use and biomass of round gobies in an inland temperate lake to define the spatiotemporal scope of biological interactions at the leading edge of the round goby invasion.
2. Using novel statistical approaches, we combined hierarchical models that control for imperfect species detection with flexible smooth terms to describe non-linear relationships between round goby abundance and environmental gradients. Subsequently, we generated accurate detection-corrected estimates of the standing stock biomass of round gobies.
3. Our results show seasonally differentiated habitat niches, where suitable round goby habitat in summer months is restricted to shallow depths (<18.4 m) with a mixture of vegetative and mussel cover. We found high round goby biomass of 122 kg/ha in occupied habitats during the summer, with a total lake-wide biomass of 766,000 kg. In winter, round gobies migrate to deep offshore habitats and disperse, dramatically altering their scope for biological interactions with resident aquatic species across summer and winter seasons.
4. The results of this study indicate that the scope of biological interactions in inland lakes may be seasonally variable, with potential for high round goby biomass in shallow lakes or at the periphery of deep lakes in the summer months. Such shallow-water habitats may therefore present higher risk of ecological impacts from round gobies in invaded lentic ecosystems. As round gobies expand inland, consideration of seasonal habitat use will be an important factor in predicting the impacts of this pervasive invader.

     

The Tactile Communication between Cryptocentrus steinitzi (Pisces,Gobiidae) and Alpheus purpurilenticularis (Crustacea,Alpheidae)

The tactile alarm system between the symbiotic goby Cryptocentrus steinitzi and its burrowing shrimp partner Alpheus purpurilenticularis was investigated by underwater observations in the northern Red Sea. Warning signals by the goby which elicit the retreat of the shrimp into its burrow consist mainly of rapid tail flicks transmitted to the shrimp through its long antenna. No warning signals are given without that contact. The daily rhythm of the antennal contacts was described. Warning signals are emitted by the goby in a selective manner only in response to the approach of certain species of fish to the burrow entrance. The response of the shrimp to warning signals was described. The goby-shrimp communication system was used to study predator recognition in a series of controlled experiments. The sequence of the acts of the goby and shrimp was analyzed.     

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.     

Invaders eating invaders: exploitation of novel alien prey by the alien shimofuri goby in the San Francisco Estuary,California

The shimofuri goby (Tridentiger bifasciatus), which is native to Asian estuaries, was recently introduced to the San Francisco Estuary, California, USA. We conducted gut content analyses to examine the gobys feeding ecology in this highly invaded estuary. Shimofuri gobies were generalist predators on benthic invertebrates, consuming seasonally abundant prey, especially amphipods (Corophium spp.). In addition, shimofuri goby utilized two novel prey items not exploited by other resident fishes – hydroids (Cordylophora caspia) and barnacle (Balanus improvisus) cirri, both of which are alien. The shimofuri gobys feeding ecology appears well-suited to the fluctuating environment of the San Francisco Estuary and may partially explain observed increases in shimofuri goby abundance compared with declines in populations of some native species.     

The Toxicity of Skin Secretions from Coral-Dwelling Gobies and their Potential Role as a Predator Deterrent

Coral-dwelling gobies in the genus Gobiodon (family Gobiidae) posses toxic skin secretions. We used bioassays to investigate interspecific variation in the toxicity of skin secretions from six species of Gobiodon from Lizard Island on the Great Barrier Reef. We then used feeding experiments with two common species of predatory fish to test if skin secretions might act as a chemical defence against predation. The skin secretions of all species were toxic to the bioassay species, Apogon fragilis, but there were marked differences in toxicity among Gobiodon species. Feeding experiments showed that both small- and large-gaped predators avoided food items to which goby skin secretions, or a whole goby, had been added. These experiments indicate that skin toxins could function as a predator deterrent in coral-dwelling gobies.     

Pharyngeal jaw morphology and homology in Sicydiine Gobies (Teleostei: Gobiidae) and allies

An extremely large number of fifth ceratobranchial teeth, with highly modified, striated, and hooked tips were observed in the central and western Pacific sicydiine goby genus Stiphodon.A scanning electron microscopic study of the form and arrangement of fifth ceratobranchial teeth was conducted to assess the distribution of these modifications in sicydiine gobies and their putative close relatives. Our goals were to explore a new set of characters in gobioid systematics, to test sicydiine monophyly, and to test hypotheses of relationships of sicydiine gobies. Sicydiines are hypothesized herein to be most closely related to the western Pacific Tukugobius and Rhinogobius,freshwater genera with which they share thickened pelvic-fin rays, no teeth on the anterior portion of the fifth ceratobranchial bones, fifth ceratobranchial teeth with differentiated and striated tips, and overlapping anterior rami of the fifth ceratobranchial bones. The latter two characters occur in some, but not all, sicydiines. The pantropical freshwater goby Awaous,often classified with sicydiines, is not considered the closest relative of the subfamily. The highly modified fifth ceratobranchials of Stiphodon are similar to, and concluded here to be homoplasious with, those of the mudflat-dwelling New World goby Evorthodus and the Indo-west Pacific oxudercine gobies, represented in this study by Pseudapocryptes. J. Morphol. 237:257–274, 1998. Published 1998 Wiley-Liss, Inc.