European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population

Aim The European green crab (Carcinus maenas) expanded dramatically after its introduction to the west coast of North America, spreading over 1000 km in < 10 years. We use samples of Carcinus maenas collected over time and space to investigate the genetic patterns underlying the species’ initial establishment and spread, and discuss our findings in the context of the species’ life history characteristics and demography. Location The central west coast of North America, encompassing California, Oregon, and Washington (USA) and British Columbia (Canada). Methods We collected 1040 total samples from 21 sites representing the major episodes of population establishment and expansion along the west coast of North America. Microsatellite markers were used to assess genetic diversity and structure at different time points in the species’ spread, to investigate connectivity between embayments and to estimate both short‐term effective population sizes and the number of original founders. Assignment testing was performed to determine the likely source of the introduction. Results Carcinus maenas in western North America likely derived from a single introduction of a small number of founders to San Francisco Bay, CA from the east coast of North America. Throughout its western North American range, the species experiences periodic migration between embayments, resulting in a minor loss of genetic diversity in more recently established populations versus the populations in the area of initial establishment. Main conclusions Low genetic diversity has not precluded the ability of C. maenas to successfully establish and spread on the west coast of North America. An efficient oceanographic transport mechanism combined with highly conducive life history traits are likely the major drivers of C. maenas spread. Evidence for a single introduction underscores the potential utility of early detection and eradication of high‐risk invasive species.     

Learning in an invasive and a native predatory crab

The invasion of the green crab Carcinus maenas in the northeastern U.S. and its competition with the native blue crab Callinectes sapidus and other native crustaceans has been well-documented and researched. Various reasons for the invader’s success against native crabs have been examined (juvenile predation, food source flexibility, etc.), but another possibility is a difference in the learning ability of invasive versus native crab species. In this study, the learning ability of C. maenas and C. sapidus was tested by their increased speed in locating hidden food over successive days. The data suggest that C. maenas possesses a learning ability significantly greater than that of C. sapidus, which may partially contribute to its success.     

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.     

Sex pheromone in the shore crab Carcinus maenas,and the site of its release from females

Sex pheromones are demonstrated in premoult and recently‐moulted female Carcinus maenas (L.) and Macropipus holsatus (Fabr.) (Crustacea Decapoda, Portunidae). Male conspecifics respond with searching activity. Dilute solutions of urine aspirated from the antennal glands of females of each species release characteristic responses in conspecific males, but males of other species respond differently, if at all. Aspects of responses of test animals in bioassays are discussed.     

Thermogeography predicts the potential global range of the invasive European green crab (Carcinus maenas)

Aim The highly adaptable estuarine crab (Carcinus maenas) has successfully invaded five temperate geographic regions outside of its native Europe. Here, we determine which environmental factors predict the current distribution of C. maenas and what the potential geographic range of this species might be. We also investigated whether the invasion potential of C. maenas differs with respect to the origin of a native subpopulation. Location Models were developed using global observation records of C. maenas. Methods Boosted regression trees were used to model observations from the (1) native, (2) invasive, (3) southern European, (4) northern European and (5) the combined native and invasive geographic ranges of C. maenas. Results Most established invasions were predicted mainly based on temperature. Interestingly, the environment encountered by established invasions failed to predict the majority of northern European populations; suggesting that invasion potential may differ between distinct native populations. Supporting this suggestion, a model of northern European populations, distinguished from southern European populations based on genetic structure, only predicted established invasions south of Nova Scotia. By contrast, a model of southern European populations predicted most established invasions. Main conclusions These results suggest that invasion potential depends on the European origin of an invasive population and that most invasions have arisen from southern Europe. Finally, a model based on combined native and invasive ranges of C. maenas identified potential geographic range extension along many currently invaded coastlines and the potential invasion of countries like Chile, China, Russia, Namibia and New Zealand.     

Community impacts of two invasive crabs: the interactive roles of density, prey recruitment, and indirect effects

Assessing the implications of species invasion for native communities requires determining whether effects of invaders are novel, or are redundant with effects of species that are already present. Using a pair of field experiments conducted over two successive years, we examined factors that influence community impacts of a recent predatory crab invader (Hemigrapsus sanguineus) and a previously established invasive crab (Carcinus maenas) on New England coasts. We demonstrate that effects of these species differ temporally with changes in the ambient prey community, and are influenced by density differences between the two species and by different strengths and types of indirect effects that each elicits. Our study highlights the importance of including bottom-up processes (i.e., prey recruitment) when examining the redundancy of consumers.     

Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus

The European green crab Carcinus maenas is one of the world's most successful aquatic invaders, having established populations on every continent with temperate shores. Here we describe patterns of genetic diversity across both the native and introduced ranges of C. maenas and its sister species, C. aestuarii, including all known non‐native populations. The global data set includes sequences from the mitochondrial cytochrome c oxidase subunit I gene, as well as multilocus genotype data from nine polymorphic nuclear microsatellite loci. Combined phylogeographic and population genetic analyses clarify the global colonization history of C. maenas, providing evidence of multiple invasions to Atlantic North America and South Africa, secondary invasions to the northeastern Pacific, Tasmania, and Argentina, and a strong likelihood of C. maenas × C. aestuarii hybrids in South Africa and Japan. Successful C. maenas invasions vary broadly in the degree to which they retain genetic diversity, although populations with the least variation typically derive from secondary invasions or from introductions that occurred more than 100 years ago.     

Conditioning the crab Carcinus maenas against instinctive light avoidance

Carcinus maenas is an invasive species found in Northern American waters overtaking the less adaptable species and responding to various forms of conditioning. In this study, we conditioned C. maenas to reverse its innate light avoidance behavior. Within 6 days of testing, 21 out of 30 crabs were successfully trained to enter a beam of light to receive food, although their instincts are to seek shelter from predators in dark areas. Some took as little as 2 days to reverse their light aversion. They also responded faster once trained. Larger crabs had faster response times than smaller ones, while there was no difference between sexes. The conditioned response lasted for at least 4 days without reinforcement. The rapid learning abilities observed during this experiment may help to explain the pervasive success of C. maenas as an invasive species.     

RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction‐site‐associated DNA sequencing‐derived SNPs to explore fine‐scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise F_ST ~0.001 to 0.15) and spread across many loci, with a mean F_ST ~0.052 and 52% of loci examined characterized by F_ST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.     

Comparative brain architecture of the European shore crab <Emphasis Type="Italic">Carcinus maenas</Emphasis> (Brachyura) and the common hermit crab <Emphasis Type="Italic">Pagurus bernhardus</Emphasis> (Anomura) with notes on other marine hermit crabs

The European shore crab Carcinus maenas and the common hermit crab Pagurus bernhardus are members of the sister taxa Brachyura and Anomura (together forming the taxon Meiura) respectively. Both species share similar coastal marine habitats and thus are confronted with similar environmental conditions. This study sets out to explore variations of general brain architecture of species that live in seemingly similar habitats but belong to different major malacostracan taxa and to understand possible differences of sensory systems and related brain compartments. We examined the brains of Carcinus maenas, Pagurus bernhardus, and three other hermit crab species with immunohistochemistry against tyrosinated tubulin, f-actin, synaptic proteins, RF-amides and allatostatin. Our comparison showed that their optic neuropils within the eyestalks display strong resemblance in gross morphology as well as in detailed organization, suggesting a rather similar potential of processing visual input. Besides the well-developed visual system, the olfactory neuropils are distinct components in the brain of both C. maenas and P. bernhardus as well as the other hermit crabs, suggesting that close integration of olfactory and visual information may be useful in turbid marine environments with low visibility, as is typical for many habitats such as, e.g., the Baltic and the North Sea. Comparing the shape of the olfactory glomeruli in the anomurans showed some variations, ranging from a wedge shape to an elongate morphology. Furthermore, the tritocerebrum and the organization of the second antennae associated with the tritocerebrum seem to differ markedly in C. maenas and P. bernhardus, indicating better mechanosensory abilities in the latter close to those of other Decapoda with long second antennae, such as Astacida, Homarida, or Achelata. This aspect may also represent an adaptation to the “hermit lifestyle” in which competition for shells is a major aspect of their life history. The shore crab C. maenas, on the other hand seems to rely much less on mechanosensory information mediated by the second antennae but in water, the visual and the olfactory senses seem to be the most important modalities.     

Le fer dans la branchie des crustacés décapodes Carcinus maenas (L.) et Homarus americanus Milne Edw.: étude quantitative et histochimique

Carcinus maenas (L.) gills accumulate iron. This iron occurs in a ferric and inorganic state. Up to 99.9 % of this metal is included in the chitinous-cellular debris fraction as isolated by centrifugation. The remaining iron belongs to the soluble protein and mitochondrial fractions. At the site of the iron polymucosaccharic acids and polysaccharides are also observed. The iron content of Homarus americanus Milne Edw. gills is smaller than that of Carcinus maenas gills. In Homarus americanus the iron is accumulated as scattered ‘tablets’ along the branchial tubes, while in Carcinus maenas it coats the branchial lamellae. It seems that the accumulation of iron in Carcinus maenas is related to the rôle of filtration or adsorption by the chitin against the particulate iron of the sea water. The differences observed between Carcinus maenas and Homarus americanus are probably related to morphological and structural differences.     

Biotic resistance experienced by an invasive crustacean in a temperate estuary

Communities high in species diversity tend to be more successful in resisting invaders than those low in species diversity. It has been proposed that the biotic resistance offered by native predators, competitors and disease organisms plays a role. In Yaquina Bay, Oregon, we observed very little overlap in the distribution of the invasive European green crab, Carcinus maenas, and the larger red rock crab, Cancer productus. C. productus dominates the more saline, cooler lower estuary and C. maenas, the less saline, warmer upper estuary. Because caged C. maenas survive well in the lower estuary, we decided to test the hypothesis that C. productus prey on C. maenas and thus contribute to their exclusion from the more physically benign lower estuary. A laboratory species interaction experiment was designed to determine whether C. productus preys on smaller C. maenas at a higher rate than on smaller crabs of their own species. Crabs of both species were collected and sorted by weight into three size classes: small, medium and large. Small and medium crabs of both species were paired with C. maenas and C. productus of various sizes. When conspecifics were paired, mortality was less than 14%, even in the presence of larger crabs. Smaller C. productus survived well in the presence of larger C. maenas, but the reverse was not true. When small C. maenas (60–67 mm carapace width) were matched with medium and large C. productus, their mortality increased to 52% and 76%, respectively. A less dramatic pattern was observed for medium C. maenas (73–80 mm) in the presence of medium and large C. productus. Thus on the West Coast of North America, the more aggressive red rock crab, C. productus, has the potential to reduce the abundance of C. maenas in the more saline and cooler lower estuaries.     

Zur Technik der Aktivitäts-Registrierung beiCarcinus maenas

Zusammenfassung 1. Zur Registrierung der Aktivitätsphasen der StrandkrabbeCarcinus maenas wird eine Versuchsanordnung beschrieben, die dem Krebs freie Beweglichkeit bietet.2. Die Versuchsanordnung beruht darin, daß in dem Hälterungsbecken in geeignetem Abstand vom Boden eine federnd aufgehängte Schwingscheibe angebracht ist. Am Rand der Schwingscheibe befindet sich eine Durchtrittsöffnung. Der Krebs kann sich also auf der Schwingscheibe aufhalten oder unter ihr verkriechen. In beiden Fällen wird seine Bewegungsaktivität sowie der Ort seines Aufenthaltes registriert.3. Die Registrierung erfolgt mit Hilfe eines einfachen Parallelschreibers, die Zeitgebung durch eine an das Getriebe des Kymographions angeschlossene Kontakteinrichtung.

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On the technique of activity registration inCarcinus maenas

In order to investigate the activity patterns of the shore crabCarcinus maenas, an apparatus was developed which allows the crab to move freely about in its container. The crab has the possibility to move on or under the free swinging partition (A; Abb. 1) of the apparatus via a square opening. Moving about, on or under the swinging partition, the crab dislocates the plate either by its weight or by lifting it. In this manner the locomotory activity of the crab is constantly registered under relatively natural conditions. For a better evaluation of the curves, a parallel recording device is employed. The new method of registration has proved useful for analyses of the complicated activity patterns ofCarcinus maenas.

     

Population genetics,gene flow,and biogeographical boundaries of Carcinus aestuarii (Crustacea: Brachyura: Carcinidae) along the European Mediterranean coast

Carcinus aestuarii Nardo, 1847 is a widespread coastal crab species throughout the Mediterranean Sea with a pelagic larval phase. This species tolerates a wide range of environmental conditions and typically inhabits fragmented habitats, such as embayments, lagoons and estuaries. It is therefore a good candidate species for studying and testing different phylogeographical hypotheses in the Mediterranean Sea. By contrast to its Atlantic sister species, Carcinus maenas, studies on the population genetic structure of C. aestuarii in its native range are still scarce. In the present study, specimens from along the European Mediterranean Sea were collected and DNA‐sequenced and analyses were applied to discriminate between present day and historical factors influencing the population genetic structure of this species. The results obtained demonstrate the existence of two genetically distinct geographical groups, corresponding to the eastern and western Mediterranean, with further subdivision within the East Mediterranean Basin. A strong asymmetric gene flow was recorded toward the Eastern Basin, which may play a crucial role in shaping the present day biogeographical patterns of this species and potentially other sympatric ones with pelagic larvae. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 771–790.     

Incorporation of ω6 polyunsaturated fatty acids into phospholipids of the crab Carcinus maenas

The incorporation in vivo of ¹⁴C-18:2 ω6 and ³H-20:4 ω6 fatty acids in phospholipids isolated from gills, hepatopancreas and hemolymph of the crab Carcinus maenas was analysed. PC was the most heavily labelled phospholipid from these ω6-unsaturated fatty acids and appeared to play an important part in the phospholipids metabolism in Crustaceans. The pathway of fatty acids synthesis in phospholipids of C. maenas seems to be similar to those described for mammals. It is at the level of tissue Pl of C. maenas that the renewal of the 20:4 ω6 fatty acid is the most important. It is suggested that the rapid reorganization of phospholipid molecular species composition in the crab is checked by deacylation—reacylation cycle.     

A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long‐distance dispersal of an invasive marine crab to Newfoundland

Aim To determine timing, source and vector for the recent introduction of the European green crab, Carcinus maenas (Linnaeus, 1758), to Newfoundland using multiple lines of evidence. Location Founding populations in Placentia Bay, Newfoundland, Canada and potential source populations in the north‐west Atlantic (NWA) and Europe. Methods We analysed mitochondrial and microsatellite genetic data from European and NWA populations sampled during 1999–2002 to determine probable source locations and vectors for the Placentia Bay introduction discovered in 2007. We also analysed Placentia Bay demographic data and shipping records to look for congruent patterns with genetic analyses. Results Demographic data and surveys suggested that C. maenas populations are established and were in Placentia Bay for several years (c. 2002) prior to discovery. Genetic data corroboratively suggested central/western Scotian Shelf populations (e.g., Halifax) as the likely source area for the anthropogenic introduction. These Scotian Shelf populations were within an admixture zone made up of genotypes from both the earlier (early 1800s) and later (late 1900s) introductions of the crab to the NWA from Europe. Placentia Bay also exhibited this mixed ancestry. Probable introduction vectors included vessel traffic and shipping, especially vessels carrying ballast water. Main conclusions Carcinus maenas overcame considerable natural barriers (i.e., coastal and ocean currents) via anthropogenic transport to become established and abundant in Newfoundland. Our study thus demonstrates how non‐native populations can be important secondary sources of introduction especially when aided by human transport. Inference of source populations was possible owing to the existence of an admixture zone in central/western Nova Scotia made up of southern and northern genotypes corresponding with the crab’s two historical introductions. Coastal vessel traffic was found to be a likely vector for the crab’s spread to Newfoundland. Our study demonstrates that there is considerable risk for continued introduction or reintroduction of C. maenas throughout the NWA.     

Methodical aspects of rearing decapod larvae,Pagurus bernhardus (Paguridae) andCarcinus maenas (Portunidae)

Improved methods for experimental rearing ofPagurus bernhardus andCarcinus maenas larvae are presented. Isolated maintenance was found essential for reliable statistical evaluation of results obtained from stages older than zoea-1. Only by isolated rearing is it possible to calculate mean values ±95% confidence intervals of stage duration. Mean values (without confidence intervals) can only be given for group-reared larvae if mortality is zero. Compared to group rearing, isolated rearing led to better survival, shorter periods of development and stimulated growth. Due to different swimming behaviorP. bernhardus zoeae needed larger water volumes thanCarcinus maenas larvae.P. bernhardus zoeae were reared with best results when isolated in Petri dishes (ca. 50 ml). They fed on newly hatched brine shrimp nauplii (Artemia spp.).P. bernhardus megalopa did not require any gastropod shell or substratum; it developed best in glass vials without any food.C. maenas larvae could be reared most sucessfully in glass vials (ca 20 ml) under a simulated day-night regime (LD 16:8); constant darkness had a detrimental effect on development, leading to prolonged stage-duration times.C. maenas larvae were fed a mixture of newly hatched brine shrimp naupli and rotifers (Brachionus plicatilis).     

Méthylations biologiques chez le crabe Carcinus maenas; inhibition in vitro par une fraction purifiée extraite des glandes androgènes

Extracts from muscles, testis, seminal vesicles and ovaries of the Crab, Carcinus maenas, have been studied in vitro, in presence of [¹⁴C]-methyl S-adenosylmethionine, with an E. coli tRNA as methyl acceptor. The highest level of methylases is found in the testis. It has been reported previously that a purified fraction extracted from the androgenic glands of Carcinus maenas inhibits the vitellogenesis in ovaries. We now show that the same fraction inhibits tRNA methylation in an extract of testis as methylase; a 50 per cent inhibition is obtained with about 10 μg of a purified fraction corresponding to 15 glands. With an enzymatic preparation from the ovaries, a 50 per cent inhibition of the tRNA methylase is observed with the purified extract from 4 glands.