Estuarine fouling communities are dominated by nonindigenous species in the presence of an invasive crab

Interactions between anthropogenic disturbances and introduced and native species can shift ecological communities, potentially leading to the successful establishment of additional invaders. Since its discovery in New Jersey in 1988, the Asian shore crab (Hemigrapsus sanguineus) has continued to expand its range, invading estuarine and coastal habitats in eastern North America. In estuarine environments, H. sanguineus occupies similar habitats to native, panopeid mud crabs. These crabs, and a variety of fouling organisms (both NIS and native), often inhabit man-made substrates (like piers and riprap) and anthropogenic debris. In a series of in situ experiments at a closed dock in southwestern Long Island (New York, USA), we documented the impacts of these native and introduced crabs on hard-substrate fouling communities. We found that while the presence of native mud crabs did not significantly influence the succession of fouling communities compared to caged and uncaged controls, the presence of introduced H. sanguineus reduced the biomass of native tunicates (particularly Molgula manhattensis), relative to caged controls. Moreover, the presence of H. sanguineus favored fouling communities dominated by introduced tunicates (especially Botrylloides violaceous and Diplosoma listerianum). Altogether, our results suggest that H. sanguineus could help facilitate introduced fouling tunicates in the region, particularly in locations where additional solid substrates have created novel habitats.     

Increase in density of genetically diverse invasive Asian shore crab (<Emphasis Type="Italic">Hemigrapsus sanguineus</Emphasis>) populations in the Gulf of Maine

Hemigrapsus sanguineus, the Asian shore crab, has rapidly replaced Carcinus maenas, the green crab, as the most abundant crab on rocky shores in the northwest Atlantic since its introduction to the United States (USA) in 1988. The northern edge of this progressing invasion is the Gulf of Maine, where Asian shore crabs are only abundant in the south. We compared H. sanguineus population densities to those from published 2005 surveys and quantified genetic variation using the cytochrome c oxidase subunit I gene. We found that the range of H. sanguineus had extended northward since 2005, that population density had increased substantially (at least 10-fold at all sites), and that Asian shore crabs had become the dominant intertidal crab species in New Hampshire and southern Maine. Despite the significant increase in population density of H. sanguineus, populations only increased by a factor of 14 in Maine compared to 70 in southern New England, possibly due to cooler temperatures in the Gulf of Maine. Genetically, populations were predominantly composed of a single haplotype of Japanese, Korean, or Taiwanese origin, although an additional seven haplotypes were found. Six of these haplotypes were of Asian origin, while two are newly described. Large increases in population sizes of genetically diverse individuals in Maine will likely have a large ecological impact, causing a reduction in populations of mussels, barnacles, snails, and other crabs, similar to what has occurred at southern sites with large populations of this invasive crab species.     

A comparison of reproductive patterns and adult dispersal in sympatric introduced and native marine crabs: implications for species characteristics of invaders

The introduction and translocation of nonindigenous marine species is widespread and can pose severe threats to biodiversity and ecosystem functioning. Predicting which species are potential invaders is of particular interest to ecologists. One approach is to identify characteristics that predispose a species to becoming a successful invader. Since its introduction in the 1980’s, the invasive Asian shore crab, Hemigrapsus sanguineus, has shown a remarkable ability to colonize rocky intertidal habitats along the east coast of the United States. In Long Island Sound H. sanguineus occurs sympatrically with the functionally equivalent, but non-invasive, native Atlantic mud crab, Panopeus herbstii. The presence of both species at the same site allowed us to make a detailed, simultaneous assessment of life history traits and adult dispersibility of co-occurring invading and native crab species. We investigated fecundity and maturation rates, length of breeding season and brood production for both species, and conducted field experiments using mark–recapture techniques to determine mobility patterns. Our results show that the nonindigenous Asian crab has a greater reproductive potential than the native mud crab as evidenced by a longer breeding season, multiple brood production and higher fecundity rates. Field experiments confirmed previous studies indicating H. sanguineus is a highly mobile crab, and further demonstrated that adult Asian crabs are more likely than mud crabs to disperse from their shelter/refuge sites. Recovery rates for native mud crabs were significantly higher than those for Asian crabs in three experimental trials, across sites and years. This work provides new information about life history characteristics of both species and supports the hypothesis that high reproductive potential combined with high adult dispersal ability may be important factors associated with the invasion/establishment success of the Asian shore crab. More study is needed, however, to determine the applicability of these findings to other highly successful marine invaders.     

Conspecific tolerance and heterospecific competition as mechanisms for overcoming resistance to invasion by an intertidal crab

The success of the invasive Asian shore crab, Hemigrapsus sanguineus, stems partly from its ability to exclude established crab species from preferred rocky and cobble intertidal habitat. Here, we assessed preference and competition for habitat types (cobble vs. sand) for H. sanguineus and two competitor species; the previous invasive green crab, Carcinus maenas, and the native rock crab, Cancer irroratus, in New England. In simple laboratory experiments, we paired similarly sized heterospecifics and conspecifics from each species, and also grouped combinations of C. maenas and H. sanguineus in a series of four-individual sets in order to dissect the outcome of intra- and inter-specific competition at different densities. Individually, all three species preferred cobble substrate. With paired conspecifics, H. sanguineus individuals would cohabitate in cobble, whereas C. maenas and C. irroratus individuals each excluded conspecifics from cobble. In heterospecific pairs, H. sanguineus excluded both C. maenas and C. irroratus from cobble. C. maenas and C. irroratus, were equally likely to exclude the other species, but rarely excluded H. sanguineus. In larger assemblages, H. sanguineus preferentially grouped under cobble, whereas C. maenas were more evenly distributed among habitat types. These observations demonstrate that conspecific tolerance and heterospecific competition can be effective, complementary mechanisms for overcoming invasion resistance. Such mechanisms help explain the well-studied success of H. sanguineus following its introduction into New England coastal habitats, and the resulting exclusion of preexisting crab species.     

Morphological and molecular evidence on the existence of a single estuarine and rocky intertidal acanthocephalan species of <Emphasis Type="Italic">Profilicollis</Emphasis> Meyer, 1931 (Acanthocephala: Polymorphidae) along the Atlantic and Pacific coasts of southern South America

Profilicollis chasmagnathi Holcman-Spector, Mañé-Garzón & Dei-Cas, 1977 (Acanthocephala: Polymorphidae) has been reported to parasitise different grapsid species as intermediate hosts along the South Atlantic shores, i.e. Cyrtograpsus angulatus (Dana) and Neohelice granulata (Dana) in Uruguay and Cyrtograpsus altimanus (Rathbun) in Argentina. Larvae of a similar acanthocephalan described as Profilicollis antarcticus Zdzitowiecki, 1985 were recorded in the crab Hemigrapsus crenulatus (Milne-Edwards) from an estuarine habitat on the Southeast Pacific shore in Chile. Earlier studies have questioned the specific assignation of the Chilean estuarine populations of Profilicollis Meyer, 1931. The aim of this study was to re-examine the identification of these acanthocephalans by means of morphological and molecular analyses of cystacanths of Profilicollis spp. gathered from C. angulatus, N. granulata, C. altimanus and H. crenulatus. Our analyses showed that a single species of Profilicollis, P. chasmagnathi, parasitises these four crab species. The assessment of specimens from the South Shetlands Islands, the type-locality of P. antarcticus, is needed before formally proposing that P. antarcticus is a junior subjective synonym of P. chasmagnathi.     

Evidence of multiple introductions and genetic admixture of the Asian brush-clawed shore crab <Emphasis Type="Italic">Hemigrapsus takanoi</Emphasis> (Decapoda: Brachyura: Varunidae) along the Northern European coast

The Asian brush-clawed shore crab Hemigrapsus takanoi is a non-indigenous species along the Northern European coast. Although the history of range expansion of European H. takanoi has been well-documented, little is known about the genetic compositions of either the introduced European populations or the native Asian ones. We therefore collected H. takanoi broadly from their native Asian sites and introduced European ranges, and genotyped them by sequencing the mitochondrial 16S RNA gene and by analyzing nuclear microsatellite loci. Our results revealed that the H. takanoi Bay of Seine (France) populations consisted of a genetic admixture between populations in Japan and those in the Yellow Sea region. These French populations should be carefully monitored in the future, since the genetic admixture of multiple source populations may accelerate range expansion in non-indigenous organisms. Our results also suggested that shipping lines from East Asia were more probable vectors than historical juvenile oyster transportations from Japan for the foundation of present European H. takanoi populations. Interestingly, gene flow between populations in Japan and those in the Yellow Sea region (i.e., domestic invasion) was not observed despite the higher potential for artificial translocations via shipping lines in the native Asian range compared with those from Asia to Europe. The lack of domestic invasions implied that intra-specific priority effects of the resident H. takanoi populations played an important role in preventing the successful colonization of artificially-transferred individuals.     

Distribution and ecological relations among the alien crab, <Emphasis Type="Italic">Percnon gibbesi</Emphasis> (H. Milne-Edwards 1853) and autochthonous species,in and out of an SW Mediterranean MPA

The distribution of the allochthonous crab Percnon gibbesi and its relationships with other benthic invertebrate species was assessed inside the marine reserve of Cabo de Palos—Islas Hormigas (Mediterranean sea, Spain) and neighbouring non-protected sites. Although a significant spatial variability was detected at finer spatial scale, there was no influence of protection measures or insularity on the abundance of P. gibbesi. The presence of small holes, encrusting algae and low slope favour the colonization success of this crustacean, and the spatial distribution of these habitat features could explain the observed pattern. The abundance of P. gibbesi was similar to that of native crab species; however, a non-significant negative relationship between the abundance of P. gibbesi and native crabs (Pachygrapsus marmoratus and Eriphia verrucosa), urchins (Arbacia lixula and Paracentrotus lividus) and a snail (Phorcus turbinatus) was observed. This work highlights the importance of monitoring alien crab population densities taking structural habitat and other potentially influential factors into account and the likely effect of this alien species on the native ones.     

Otolith variation in Pacific herring (<Emphasis Type="Italic">Clupea pallasii</Emphasis>) reflects mitogenomic variation rather than the subspecies classification

Pacific herring (Clupea pallasii) is divided into three subspecies: two in northeast Europe and one in the north Pacific Ocean. Genetic studies have indicated that the populations in northeast Europe have derived from the northwest Pacific herring recently, or during the last 10–15 kyr, and that they are distinct from the population in the northeast Pacific. In addition, hybridization between the Pacific herring and the Atlantic herring has been documented. Otolith variation has been considered to be largely affected by environmental variation, but here we evaluate whether the genetic differentiation is reflected in otolith shape differences. A clear difference in otolith shape was observed between the genetically differentiated herring species Clupea harengus from the Atlantic and C. pallasii. The otolith shape of C. p. suworowi in the Barents Sea was different from the shape of C. pallasii in northern Norway and C. p. pallasii from the Pacific. Populations of C. p. pallasii, sampled east and west of the Alaska Peninsula, which belong to two genetically different clades of the C. p. pallasii in the Pacific Ocean, show a clear difference in otolith shape. C. p. suworowi and the local C. pallasii peripheral population in Balsfjord in northern Norway are more similar to the northwest Pacific herring (C. p. pallasii) than to the northeast Pacific herring (C. p. pallasii), both genetically and in otolith shape. The Balsfjord population, known to be influenced by introgression of mtDNA from the Atlantic herring, does not show any sign of admixture in otolith shape between the two species. A revised classification, considering the observed genetic and morphological evidence, should rather group the northwest Pacific herring in the Bering Sea together with the European populations of C. pallasii than with the northeast Pacific herring in the Gulf of Alaska.     

Home and Away: Comparisons of Resource Utilization by a Marine Species in Native and Invaded Habitats

The exotic Asian shore crab, Hemigrapsus sanguineus, was recently introduced to the northeastern coast of North America and during the 1990's breeding populations were established throughout southern New England. In 1997–1998, ecological studies of several co-occurring brachyuran crabs were conducted and in native (Tanabe Bay, Japan) and invaded (Long Island Sound, USA) habitats of H. sanguineus. Standardized comparisons of H. sanguineus were made between the 2 habitats using data on crab sizes, utilization of space, and food habits. Results revealed that (1) the resource use of H. sanguineus was quite different from that of other resident species in its invaded habitat, and (2) there were no substantial changes in resource utilization by H. sanguineus after it became established in the invaded habitat (relative to native Tanabe Bay). Differing patterns of resource use by H. sanguineus and other crabs in the invaded habitat, the lack of restriction in resource use by H. sanguineus following its introduction, and the climatological and physical similarities between native and invaded regions likely contributed to the successful invasion of H. sanguineus into rocky intertidal habitats in southern New England.     

Parasitism of the rhizocephalan <Emphasis Type="Italic">Briarosaccus callosus</Emphasis> on the crab <Emphasis Type="Italic">Paralomis verrilli</Emphasis> (Crustacea: Lithodidae) in the waters of southeast Sakhalin

The crab Paralomis verrilli in the waters of southeast Sakhalin is infected by the parasitic rhizocephalan barnacle Briarosaccus callosus. The prevalence of parasitic infection was on the average 4.36% (6.29% for females, 3.28% for males) and varied between samples from none up to 14.9%. The degree of prevalence was not related to the average carapace width and the sex ratio of crabs in samples. Sterilization of female P. verrilli was caused by the B. callosus infestation or its consequences. No more than two parasite externae per crab were found. Crabs with two externae made up 5.6% of all infected specimens. The infestation of crab hosts with two B. callosus externae negatively influenced the growth of the externae. A positive relationship was found between the width of the crab carapace and the length of the parasitic externae. The survival rate of P. verrilli with either one or two parasite B. callosus externae did not differ substantially. The proportion of crabs with externae and those with “scars” (12.2% in our case) can be taken as the index of survival of the parasitized crabs.     

The bitter crab syndrome in commercial crabs in the Western part of the Bering and Chukchi Seas

We studied the distribution of the “bitter-crab” syndrome, a disease caused by the parasitic dinoflagellate Hematodinium sp., in eight commercial species of crabs in the west of the Bering and Chukchi seas. The crabs (25 388 individuals) were sampled during bottom trawl surveys of July?September 2010 and October?November 2012. The disease was first identified visually by a color change of the exoskeleton and the hemolymph of the animals and then using microscope analysis of hemolymph samples. Infestation was detected in crabs of three species, Chionoecetes opilio, C. bairdi, and Paralithodes platypus. The prevalence of the disease (the percent of infected individuals relative to all of those examined) in C. bairdi and P. platypus was very low, 0.1 and 0.3%, respectively. Infestation was widespread among C. opilio, its peak in the Bering Sea was in the fall. The average prevalence of the crab disease in different areas of the Bering Sea ranged from 0.8 to 10.8%. A high rate of crab infection was recorded in the Korfa Bay. In the Chukchi Sea, the average prevalence was 2%. Infestation by Hematodinium sp. was not revealed in the deep-sea snow crabs Chionoecetes tanneri and C. angulatus, and in three species of lithodid crabs, Paralithodes camtschaticus, P. brevipes, and Lithodes couesi. This can be explained by the small sample volume and/or ecology of these species, since the disease was registered in other areas in four of them.     

Comparative morphology of larvae of coastal crabs (Crustacea: Decapoda: Varunidae)

The larval development of three crabs of the Varunidae family, (Hemigrapsus sanguineus, H. penicillatus, and H. longitarsis), widely spread in Russian waters of the Sea of Japan, were studied under laboratory conditions. At a temperature of 20–22°C and a salinity of 32‰ about 30% of larvae a complete developmental cycle, including five zoeal stages and megalopa, took from 22 to 30 days. All larval stages are illustrated and described in detail. Zoea I and zoea II of the studied crabs are not distinguishable. Zoea III–V of these species differ in the number of dorsomedial setae on the abdominal somite I and in the number of setae on the posterodorsal arch. The megalopae of three Hemigrapsus species possess a different number of segments, aesthetascs and setae on the antennular exopod. In spite of the great similarity of larvae of genera Hemigrapsus and Eriocheir, the latter possesses a number of distinctive features in all developmental stages, supporting the separation of these genera.     

Heritable bacterial endosymbionts in native and invasive populations of <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

Harmonia axyridis Pallas (1773) (Coleoptera: Coccinellidae) is the well-studied system of invasive insect species. Native and invasive parts of the area of H. axyridis are isolated geographically. We studied the species composition and the distribution of bacterial symbionts Spiroplasma and Rickettsia in seven localities of the native area and six localities of the invasive area of H. axyridis. Rickettsia was detected in H. axyridis populations for the first time. We found that the proportion of beetles infected with Rickettsia in native and invasive populations of H. axyridis is about 0.03. Spiroplasma was found only in native populations of H. axyridis. The proportion of infected individuals with Spiroplasma in native populations of H. axyridis is about 0.08. All studied native populations of H. axyridis are infected with Spiroplasma, while all invasive populations are not. We discuss the possible influence of Spiroplasma and Rickettsia in the formation of invasive populations of H. axyridis.     

Native ecosystem engineer facilitates recruitment of invasive crab and native invertebrates

Native ecosystem engineers that add physical structure to ecosystems can facilitate invasive species. In this study we determined the effects of the native tube-forming serpulid worm, Galeolaria caespitose on the recruitment of the invasive New Zealand porcelain crab, Petrolisthes elongatus, and whether invasive crab recruitment was related to the recruitment of native species. P. elongatus is abundant beneath intertidal rocks around Tasmania, southern Australia, and the underside of these rocks is usually covered with a calcareous matrix formed by the serpulid. We used an experimental approach to investigate whether rocks, serpulids on the underside of rocks and adult P. elongatus influenced the recruitment P. elongatus and native communities. P. elongatus and native invertebrates only recruited in the presence of rocks indicating the importance of rock as primary recruitment habitat. Moreover, the presence of serpulids on the underside of rocks significantly increased the recruitment of P. elongatus and native invertebrates compared to rocks without serpulids. Rocks with higher densities of adult P. elongatus at the end of the experiment also had higher densities of P. elongatus recruits. The density of P. elongatus recruits did not influence native species richness and abundance although there was some evidence that high P. elongatus recruitment was correlated with shifts in native community structure. We have shown that a native ecosystem engineer facilitates recruitment of an invasive crab but this does not appear to influence the recruitment of native species.     

Extraction of hermit crabs from their shells by white-faced capuchin monkeys (<Emphasis Type="Italic">Cebus capucinus</Emphasis>)

We observed two capuchin monkeys (Cebus capucinus) feeding on hermit crabs (Coenobita compressus) on the coast, and the tactics they used to extract this well-protected prey. The observations took place during the dry season at Playa Escondida beach, Puntarenas, Costa Rica. The capuchins descended from trees at the back edge of the beach to capture passing hermit crabs. Both capuchins extracted the hermit crabs from their protective shells by holding the shell with one hand and pulling the crab out with the other. Even though this was accomplished within seconds, the extraction of hermit crabs from their shells did not appear to be a straightforward task. Once the capuchins succeeded in pulling the crabs out of their shells, they consumed the soft abdomen and discarded the rest of the crab's body. To our knowledge, the consumption of hermit crabs has not been previously reported for any capuchin monkey (Cebus or Sapajus). Our observations provide a new example of extractive foraging by capuchins, and thus an additional natural context for which fine motor skills (which are highly developed in capuchins) are necessary.     

Host location and selection by the symbiotic sargassum crab <Emphasis Type="Italic">Portunus sayi</Emphasis>: the role of chemical,visual and tactile cues

The Sargassum community consists of a unique and diverse assemblage of symbiotic fauna critical to pelagic food chains. Associated symbionts presumably have adaptations to assist in finding Sargassum. In situ scattered Sargassum patches accumulate as they are pushed toward the shoreline (via wind, waves, currents or tides) and are frequently less than 1 m apart and in depths of 10 cm or less as the patches approach the shoreline Crabs, and other symbiotic fauna, must relocate to another patch that is seaward in direction or likely perish as their current patch will likely become beached. This study investigated sensory cues used for host location and selection by the Sargassum crab, Portunus sayi. Chemical detection trials were conducted with a two-chamber choice apparatus with Sargassum spp. and Thalassia testudinum as habitat source odors. Visual detection trials (devoid of chemical cues) and habitat selection trials were conducted in which crabs were given a choice between hosts. Results showed that P. sayi responded to chemicals from Sargassum spp. Crabs visually located host habitats but did not visually distinguish between different hosts. In host selection trials, crabs selected Sargassum spp. over artificial Sargassum and T. testudinum. These results suggest that crabs isolated from Sargassum likely use chemoreception; within visual proximity of a potential patch, crabs likely use both chemical and visual information.     

The Structure and Density of Aggregations of the Hermit Crab <Emphasis Type="Italic">Pagurus proximus</Emphasis> Komai, 2000 in Epibiosis of the Brown Alga <Emphasis Type="Italic">Costaria costata</Emphasis> (C. Agardh) De A. Saunders, 1895 in the Sublittoral Zone of Vostok Bay,Sea of Japan

A study of epibiosis of the brown alga Costaria costata in the sublittoral zone of Vostok Bay, Sea of Japan during the spring and summer of 2016 showed that hermit crabs of the following four species accounted for approximately 85% of the total biomass: Pagurus proximus, P. minutus, P. brachiomastus, and P. middendorffii. Of these, the most abundant one (96.5% of the total number of hermit crabs) was P. proximus, the mean aggregation density of which on C. costata (429 ± 221 ind./m²) was higher by an order of magnitude than that in the adjacent area of the bouldery bottom. The size ranges of males and females of this species in aggregations on boulders and those on C. costata were similar, with a predominance of larger individuals on algae. In the size–frequency distribution, three groups of individuals corresponding to three size–age cohorts were differentiated. The male-to-female ratio was 1 : 1.7. Hermit crab aggregations on C. costata are ephemeral; their existence is determined by the duration of the period of algae development, that is, from late spring to the middle of the summer.     

Invasion dynamics on a temperate rocky shore: from early invasion to establishment of a marine invader

Populations of invading Asian shore crabs (Hemigrapsus sanguineus) and resident crabs (European green crab Carcinus maenas or species in the family Panopeidae) were monitored for up to 12 years along a south to north orientation on the open coast of Massachusetts and within the Narragansett Bay estuary, Rhode Island. At all sites, densities of resident crabs declined as H. sanguineus increased in abundance. Population dynamics were divided into 3 stages of the invasion (early, mid, late) based on statistically different densities of invading and resident crabs. Early in the invasion on the open coast, the relatively few H. sanguineus present had a wide range of individual sizes. By late in the invasion, relatively small crabs [<10 mm carapace width (CW)] constituted half of the population. Few seasonal differences occurred. Carcinus maenas, dominant at the coastal sites early in the invasion, showed strong recruitment of small individuals in the fall early in the invasion. Overall numbers of C. maenas declined as the H. sanguineus invasion progressed, and very few crabs >10 mm CW were present late in the invasion. In Narragansett Bay, a recruitment peak of H. sanguineus occurred shortly before it surged in population size, and large crabs were abundant late in the invasion. Geographic comparisons of H. sanguineus populations in southern New England showed similar growth trajectories. Monitoring populations of resident and invading species at multiple locations from early invasion through clear establishment of the invader allows a more complete understanding of the population dynamics of marine species invasions.     

Patterns of microbial food webs in Mediterranean shallow lakes with contrasting nutrient levels and predation pressures

Hygraula nitens is a New Zealand native moth with aquatic larvae that feed on submerged aquatic plants. The larvae have been mainly observed using native Potamogeton and Myriophyllum species as a food source, although some studies reported larvae feeding on the alien macrophytes Hydrilla verticillata, Lagarosiphon major and Ceratophyllum demersum. Experimental mesocosm studies showed larvae had a major effect on H. verticillata, C. demersum, L. major, Elodea canadensis and Egeria densa. In both no choice and choice experiments H. nitens larvae showed a clear preference for and the highest consumption of C. demersum, while the native macrophyte Myriophyllum triphyllum ranked fourth out of five alien and two native plant species, indicating a preference of the larvae for alien macrophytes. Additional choice experiments using C. demersum, sampled from different waters in NZ, illustrated that there was a clear difference in H. nitens preference for plants based on their source. However although C. demersum had the lowest leaf dry matter content (LDMC) compared with the other macrophytes, neither the LDMC nor leaf carbon, nitrogen, phosphorus or total phenolic contents alone could explain the preferences of H. nitens, and we conclude that food choice is based on a combination of these and/or additional factors.