Susceptibility of non-indigenous ascidian species in British Columbia (Canada) to invertebrate predation

Non-indigenous ascidians are known to significantly alter the structure and composition of benthic communities and adversely affect shellfish aquaculture by fouling both the cultured species and the infrastructure. The ability of these species to persist in new locations and their current and potential distributions are dependent upon physiological tolerances to environmental factors and biotic resistance to competition and predation. Despite significant data on global invasion patterns, potential biotic resistance to non-indigenous ascidians is poorly understood. We identified potential predators of four non-indigenous ascidians (Styela clava, Botryllus schlosseri, Botrylloides violaceus, and Didemnum vexillum) in British Columbia (BC), Canada in order to: (1) assess the potential for biotic interference to limit the establishment and/or spread of these ascidian species in BC, and (2) identify candidate species to be used as ascidian biofouling control agents in shellfish aquaculture. Using a series of single- and multiple-choice laboratory experiments, potential benthic predators (including various species of molluscs, echinoderms, and arthropods) were offered non-indigenous ascidians as prey. The sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus franciscanus, the sea stars Dermasterias imbricata and Evasterias troschelii, the nudibranch Hermissenda crassicornis, and the crabs Cancer productus and Carcinus maenas were found to consume one or more species of non-indigenous ascidians in single-choice experiments. However, when provided a choice, all predators chose their respective preferred food over ascidians. Thus, predation alone is unlikely to prevent large-scale establishment and spread of non-indigenous ascidians in BC, but it may have the potential to significantly reduce localized populations of ascidians. Green sea urchins, S. droebachiensis, were found to be efficient grazers of all four ascidian species, consuming 12.7 ± 5.14 cm² (mean ± SD) of adult B. violaceus over a 3-day period, 15 ± 3.7 juvenile colonies of B. violaceus over a 2-day period, and 63 ± 28.8 juvenile colonies of B. schlosseri over a 2-day period. Using sea urchins as biological control organisms may significantly reduce ascidian fouling in shellfish aquaculture.     

Dopamine,noradrenaline and serotonin during hypo-osmotic stress of Carcinus maenas

Dopamine, noradrenaline and serotonin were measured in the haemolymph and gills of Carcinus maenas before and after transferring them into diluted seawater. A remarkable variation of the above-mentioned compounds was observed as a function of time of osmotic stress. C. maenas were captured in the Venetian lagoon near Chioggia, Italy in 1986.     

Foraging behavior of juvenile Carcinus maenas (L.) and Cancer pagurus L.

Information concerning the way juvenile crabs choose their diet from a variety of prey types can be useful for a better understanding of community dynamics, as well as for the adequate management of natural resources. Prey size and species selection by juvenile Carcinus maenas (15-35 mm carapace width, CW) and Cancer pagurus (20-40 mm CW) feeding on four bivalves of contrasting shell morphology were investigated. When offered a wide size range of Mytilus edulis, Ostrea edulis, Crassostrea gigas, and Cerastoderma edule presented individually, crabs generally showed evidence of size-selective predation. Cancer pagurus selected larger mussels relative to the size of their chelae (relative prey size, RPS) than did Carcinus maenas of similar and even larger carapace width. However, the RPS of selected O. edulis and Cerastoderma edule were similar for all crabs, suggesting that certain prey features constitute effective barriers even to the powerful chelae of Cancer pagurus. When offered a wide size range of mussels and oysters simultaneously, all crabs consistently selected mussels. When offered O. edulis and Crassostrea gigas, crabs consumed both these oyster species in similar numbers. Carcinus maenas consumed similar numbers of mussels and cockles; Cancer pagurus, however, showed no preference for either prey in the smaller size classes but selected more mussels than cockles as prey increased in size. Although previous studies report that adult Carcinus maenas select prey species according to their profitability (amount of food ingested per unit of handling time, milligrams per second), consumption rates of the size classes of prey selected by juvenile shore crabs did not always parallel prey value. Although variations in crab strength can account for many of the differences between the foraging strategy of juvenile and adult C. maenas, our results suggest that juvenile crabs are less species selective than adults as a result of the restrictions imposed on small individuals that have limited access to larger prey.     

In situ variation in heart rate of the shore crab Carcinus maenas in relation to environmental factors and physiological condition

Heart rate of Carcinus maenas was recorded continuously for two days in situ, together with water temperature, salinity, depth and light intensity. Of each sex, 25 crabs were used and assigned to groups on the basis of size and colour (the carapace changes colour with prolongation of the intermoult phase). Wet weight:dry weight ratios of midgut gland, muscle, gonads and whole body were examined together with midgut gland lipid content and haemolymph protein concentration. Heart rates and wet wt:dry wt ratios for all the tissues examined were higher in early intermoult than in late intermoult stages of the adult C. maenas (P<0.05). Heart rate, lipid content and haemolymph protein concentrations were higher and wet wt:dry wt ratios of midgut gland, gonads and whole body were lower in juvenile crabs than in adults (P<0.05). The relationship between heart rate and wet wt:dry wt of whole body differed among C. maenas in early and late intermoutl. Heart rate was positively correlated with midgut gland lipid content (a Darwinian fitness parameter) in crabs that were in late intermoult. Physico-chemical environmental parameters, sex and colour accounted for 12% of the variation in heart rate of C. maenas recorded in situ. Temperature and prolonged intermoult were the most important factors influencing heart rate. The findings are discussed in relation to laboratory studies of cardiac activity and observed behaviour of C. maenas in the field.     

Spread and potential impact of the recently introduced European green crab,Carcinus maenas,in central California

Our study examines the potential impact of the European green crab Carcinus maenas on communities of coastal embayments of western North America. We document the current distribution and range expansion of this species beyond San Francisco Bay, where C. maenas first became established along this coast in 1989–1990, and we test the effect of C. maenas predation on different species and sizes of infaunal invertebrates in field and laboratory experiments. In our samples from eight coastal locations in central California collected between June 1993 and May 1994, we found no green crabs at the two closest embayments south of San Francisco Bay and found the crabs in all four embayments sampled within 120 km north of San Francisco Bay, up to and including Bodega Harbor. C. maenas was not present in samples from sites farther north. This northward range expansion is apparently the result of larval recruitment by a single cohort, corresponding to the predominant northern transport of surface waters and the approximate distance water moves during larval green crab development. At Bodega Harbor, the current northern range limit, the C. maenas population is now well established and reproducing. Females and males became sexually mature within their first year at 40 mm carapace width, molting approximately monthly from summer through fall, and females were ovigerous in late fall of their first year at 50 mm. We expect larvae from this population to recruit locally and to the north, promoting episodic range extensions as new populations are established and reproduce. Enclosure experiments conducted during the summer of 1993 at the intertidal sandflats of Bodega Harbor showed that C. maenas significantly reduced densities of the most abundant taxa, including the bivalves Transennella confusa and T. tantilla, the cumacean Cumella vulgaris, and the amphipod Corophium sp. Furthermore, Carcinus maenas selectively removed larger (>3 mm) rather than smaller (<1 mm) Transennella spp. in both field and laboratory experiments. Based on the available data from this and other studies of green crabs, and our 10 yr study of community dynamics at Bodega Harbor, we predict C. maenas will significantly alter community structure, ecological interactions, and evolutionary processes in embayments of western North America.     

Studies to establish an optimal diet for Carcinus maenas II. Protein and lipid requirements

Carcinus maenas (L.) was maintained on synthetic foods containing various proteins and lipids. Food quality was evaluated in terms of the crustacean's growth, duration of intermoult periods, and time of survival. Casein was found to be an adequate source of protein. Substituting amino acids or hydrolysates for casein results in reduced growth and delayed moults or absence of moulting. Animal proteins like casein are better suited than vegetable proteins. Correspondingly cod liver oil is more adequate than the vegetable lipid maize oil. The amount of salts and the pH-value also influence the quality of food-stuff for C. maenas.     

Studies to establish an optimal diet for the decapod crab Carcinus maenas under culture conditions

The maintenance of a uniform diet for Carcinus maenas (L.), where this crab is used as test animal in the laboratory, precludes the use of fresh food, e. g. mussels, for many reasons; not the least of these is the seasonal variation in the nutritive value of such food. Different types of fresh food are variably accepted by C. maenas, dependent on such factors as taste and the consistency of the food. The crabs will eat freeze-dried food set in agar-agar. A diet of this food is, however, inferior to one of fresh food as its preparation destroys essential substances and storage causes aging. In order to eliminate these disadvantages, a better quality artificial diet was developed, one which nevertheless does not attain the quality of fresh food. This diet can be further improved by varying the proportions of the individual constitutents.     

Larval development rate predicts range expansion of an introduced crab

Introduced populations can cause ecological and economic damage and are difficult to eradicate once they have established. It is therefore important to be able to predict both where species may become established and their capacity to spread within recipient regions. Here, we use a new method to assess potential for intraregional spread of a marine crab introduced to North America, Carcinus maenas. We determined survivorship and development rates throughout a range of temperatures in the laboratory for C. maenas larvae from non-native populations on the Atlantic and Pacific coasts of North America. The larvae exhibited narrower physiological tolerances than adults, and no lab-cultured larvae completed larval development below 10.0°C or above 22.5°C. Survivorship peaked at intermediate water temperatures of 12.5–20.0°C, and development time decreased with increasing temperatures within this range. Based upon these laboratory development rates, we used nearshore sea-surface temperature data from both coasts of North America to predict development times required for larvae at different months and sites. Taken together, survivorship and development data indicate that C. maenas has the capacity to continue its northward spread and establish populations at numerous additional sites in North America. Moreover, decadal temperature data at two Alaskan sites predicted little variability in development duration across years, suggesting that development duration predictions are robust to interannual water temperature differences.     

Effect of the presence of the shore crab, <Emphasis Type="Italic">Carcinus maenas</Emphasis>, on burrowing behaviour and clearance rate of the common cockle, <Emphasis Type="Italic">Cerastoderma edule</Emphasis>

Bivalves demonstrate various morphological and behavioural adaptations to reduce the risk of being attacked by predators. This paper examines how the presence of the crab Carcinus maenas (L.), a natural predator of the cockle Cerastoderma edule (L.), affects its burrowing depth and clearance or feeding rate. Cockles were placed in experimental tanks and treated with three levels of predatory disturbance: (1) unfed crab loose inside the tank, (2) unfed crab inside a cage suspended in the water column and (3) no crab present. Cockles’ burrowing depth was measured in two sediment types: mud and sand. Cockles burrowed more deeply in treatments with no crabs. Burrowing depth in sand was significantly greater than in mud. Two factors may contribute to the reduction in burial depth of C. edule in the presence of C. maenas: the change in the vertical orientation of the cockle and the ‘cough response’. No significant difference was found in the cockles’ clearance rate among the different levels of predator threat.     

Interaction and impacts of two introduced species on a soft-sediment marine assemblage in SE Tasmania

Introduced species are having major impacts in terrestrial, freshwater and marine ecosystems world-wide. It is increasingly recognised that effects of multiple species often cannot be predicted from the effect of each species alone, due to complex interactions, but most investigations of invasion impacts have examined only one non-native species at a time and have not addressed the interactive effects of multiple species. We conducted a field experiment to compare the individual and combined effects of two introduced marine predators, the northern Pacific seastar Asterias amurensis and the European green crab Carcinus maenas, on a soft-sediment invertebrate assemblage in Tasmania. Spatial overlap in the distribution of these invaders is just beginning in Tasmania, and appears imminent as their respective ranges expand, suggesting a strong overlap in food resources will result from the shared proclivity for bivalve prey. A. amurensis and C. maenas provide good models to test the interaction between multiple introduced predators, because they leave clear predator-specific traces of their predatory activity for a number of common prey taxa (bivalves and gastropods). Our experiments demonstrate that both predators had a major effect on the abundance of bivalves, reducing populations of the commercial bivalves Fulvia tenuicostata and Katelysia rhytiphora. The interaction between C. maenas and A. amurensis appears to be one of resource competition, resulting in partitioning of bivalves according to size between predators, with A. amurensis consuming the large and C. maenas the small bivalves. At a large spatial scale, we predict that the combined effect on bivalves may be greater than that due to each predator alone simply because their combined distribution is likely to cover a broader range of habitats. At a smaller scale, in the shallow subtidal, where spatial overlap is expected to be most extensive, our results indicate the individual effects of each predator are likely to be modified in the presence of the other as densities increase. These results further highlight the need to consider the interactive effects of introduced species, especially with continued increases in the number of established invasions.Communicated by M.S. Johnson, Crawley     

Feeding and non-feeding aggression can be induced in invasive shore crabs by altering food distribution

Human activity can have a large impact on surrounding ecosystems. For example, humans alter resource distributions for other species, potentially modifying these species competitive dynamics. These changes in local competitive processes are frequently associated with species invasions. Here, we investigate how differences in resource distribution affect competitive behaviour using the highly invasive European shore crab (Carcinus maenas). Using a controlled laboratory experiment in combination with behaviour assays and social network analysis, we show that individuals feeding in habitats with clumped food distributions are more aggressive than individuals feeding in habitats where food is evenly dispersed, and this aggression is present even on days where crabs are not feeding. Additionally, this persistent aggression can be induced, suggesting that individuals of this invasive species possess the flexibility to modify their competitive behaviours in response to differences in food distributions. Furthermore, we show how these individual responses can lead to changes in overall organisation of aggressive interactions within a population. We discuss these results in relation to how human impacts can have long-term effects on competitive behavioural strategies, and how behavioural flexibility can allow invasive species to colonise and persist in highly impacted sites such as urban ecosystems.     

Les variations de la phototaxie des larves de crustacés sous l'action de divers polluants métalliques: mise au point d'un test de toxicité subléthale

Variations in orientation and photokinesis of Carcinus maenas and Palaemon serratus Zoeas I were studied in the presence of excess cobalt and strontium chlorides or silver nitrate. The speed of movement of larvae toward light (phototaxis) appears to constitute a good parameter for testing sublethal toxicity. The salts are toxic to crab larvae in the following decreasing order of toxicity: silver nitrate, cobalt chloride, strontium chloride. Within 4 days, orientation of C. maenas Zoea I was disturbed by excess CoCl₂ and AgNO₃ in the range 0.01 to 0.1 mg/l, and by excess SrCl₂ in the order of 100 mg/l. For P. serratus Zoea I, the corresponding values were 100 to 500 mg/l CoCl₂, 100 mg/l AgNO₃, and above 500 mg/l SrCl₂. C. maenas photokinesis was decreased by amounts of 0.001 mg/l of CoCl₂ or AgNO₃ within a period of only 2 to 3 days.     

Occurrence and distribution of antioxidant enzymes in the haemolymph of the shore crab Carcinus maenas

The haemocytes and cell-free haemolymph of the shore crab Carcinus maenas were examined for the presence of the antioxidant enzymes, catalase (EC 1.11.1.6), glutathione peroxidase (GPX) (EC 1.11.1.9) and superoxide dismutase (SOD) (EC 1.15.1.1) by biochemical assay and immunocytochemistry. The results show that all three enzymes are present in the haemocytes, but vary in distribution and amount. Catalase was detected principally in the phagocytic hyaline cells, whereas GPX and SOD were found in both the hyaline and granular cells. Catalase and glutathione peroxidase activities were absent from the semi-granular cells, and although SOD was detected in some samples, there was enormous variation in the level of this enzyme between individuals. Cell-free haemolymph, by contrast, was found to be positive for GPX and SOD but lacked catalase activity. Immunocytochemical analyses further showed that only 2 to 16% of the cells stain positively for these enzymes, and where present the enzymes tended to be distributed throughout the cytoplasm. With the granular cells, however, there was some localization of GPX and SOD around the granules. Since the phagocytes of C. maenas are known to produce superoxide anion radicals, hydrogen peroxide, and possible other reactive oxygen species upon stimulation with phorbol myristate acetate, lipopolysaccharide, or concanavalin A in vitro, it is likely that catalase, GPX and SOD are present in the haemolymph to assist in protection of the host tissues against oxyradical damage during host defence in vivo.     

Effects of copper and cadmium on osmoregulation and oxygen consumption in two species of estuarine crabs

Green crabs (Carcinus maenas) and rock crabs (Cancer irroratus) were exposed to various concentrations of copper as cupric chloride (CuCl₂ · 2 H₂O), and cadmium as cadmium chloride (CdCl₂ · 21/2 H₂O) for 48 h. The exposures were conducted at 5 different salinities. At the end of each exposure period, tests of blood-serum osmolality and gill-tissue oxygen consumption were performed. Copper-exposed crabs exhibited loss of osmoregulatory function with increasing copper concentration until normally hyperosmotic serum became isosmotic with the surrounding medium. Cadmium elevated greencrab serum above its normal hyperosmotic state. Copper had no effect on gill-tissue oxygen consumption; however, cadmium reduced the rate of oxygen consumption in both species tested.     

Predator-induced alarm responses in the common periwinkle, Littorina littorea: dependence on season, light conditions, and chemical labelling of predators

Chemically mediated alarm reactions of the common periwinkle, Littorina littorea (L.), were studied in laboratory experiments during two consecutive summers, and one intermediate autumn season. Responses to chemical stimuli were detected as crawl-out responses, i.e. movements of snails out of the water. Snails were exposed to extracts of injured conspecifics, extracts of the mussel Modiolus modiolus (L.), and water conditioned by the predatory crab Carcinus maenas (L.), which had been maintained on different diets. In experiments carried out during the summer, a significantly larger number of snails moved out of the water when exposed to chemical stimuli from injured conspecifics, compared to chemical stimuli from injured mussels or filtered seawater. These results suggest that chemical alarm substances are present in L. littorea. Water conditioned by crabs that had been fed L. littorea released significantly more crawl-out responses compared to water conditioned by crabs that had been kept on a fish diet. When tested in autumn, no significant differences were found in responses to the above-mentioned water samples. Crawl-out responses under different light regimes were also investigated. All series of experiments carried out in the dark evoked a higher number of responses compared to series that took place in light. These findings may indicate an adaptation of snails to night-active predators. In total, the current results suggest that a L. littorea diet may chemically “label” the predator crab with snail alarm substances, and that predator-induced responses of L. littorea are actually responses to conspecific alarm substances released from crabs that have been maintained on a L. littorea diet. The response to the alarm signal, however, appears to be dependent on season and light conditions; some ecological implications of these findings are also discussed. Received: 8 January 1999 / Accepted: 29 March 1999     

Variations of hemolymph proteins of the common shore crab Carcinus maenas after a bacterial infection

The influence of a bacterial infection in Carcinus maenas both generally and with specific respect to hemolymph proteins is described. The infection shows severe effects upon the moulting cycle and general activity. The total protein concentration remains constant. Qualitative and quantitative differences between healthy and infected crabs appear, however, after electrophoretical separation (Disc-PAGE), indicating the importance of this method as an analytical tool in animal disease research. The protein pattern of the diseased crabs shows two new protein components. The origin of these additional fractions is discussed. Moreover, the levels of most other proteins, which are identified as hemocyanin subunits and a nonrespiratory protein, are higher in diseased crabs, thus indicating an elevated metabolic rate.     

Introduction,dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay,California

The North Atlantic portunid crab Carcinus maenas (Linnaeus, 1758) has invaded the North Pacific Ocean following more than two centuries of global dispersal due to human activities. C. maenas was first collected in San Francisco Bay, California, in 1989–1990, where its distribution and prey selectivity were investigated in 1992–1994. It has become abundant in shallow, warm lagoons (which as favorable and retentive microhabitats may have served as invasion incubators) and spread throughout the north, central and south bays. It may have arrived in ballast water, on fouled ships, amongst algae with imported live bait or lobsters, or by intentional release; genetic comparisons of the Bay population with possible source populations may aid in defining the transport mechanism. C. maenas' eurytopic nature, its high breeding potential, and its diet and feeding behavior suggest the potential for extensive ecosystem alterations through predator-prey interactions, competition, disturbance, and indirect effects. Although both negative economic impacts through reduction or disruption of fisheries and positive impacts of providing bait and human-food fisheries have been documented in a few regions, the potential economic impacts in San Francisco Bay remain largely unknown.     

Mating behaviour of male Carcinus maenas in relation to a putative sex pheromone: behavioural changes in response to antennule restriction

Temporary suspension of the receptivity of the male antennules confirmed these organs as the site of putative pheromone detection in the crab Carcinus maenas. Comparative analysis of male performance in individual components of sexual behaviour failed to identify any difference between male crabs with antennules restricted and others without, when individuals from each group were placed in contact with receptive females. However, even though pheromone perception by males was not a prerequisite for the initiation of sexual behaviour, in its absence the control of normal sequence and duration of pairing behaviour was disrupted.     

Variability in dry weight and vertical distributions of decapod larvae in the Irish Sea and North Sea during the spring

Accumulation of waterborne cadmium in Littorina littorea, Mytilus edulis and Carcinus maenas (collected in 1988 and 1989 around the island of Funen, Denmark) was investigated in a matrix of salinities (10 to 30) and calcium concentrations (2.9 to 8.9 mM Ca⁺⁺). Cadmium accumulation rates in soft parts of L. littorina, soft parts and shells of M. edulis and whole bodies and exoskeletons of C. maenas decreased with increasing salinity. Changes in the calcium concentrations accounted for 72% of the salinity effect on cadmium accumulation rates in L. littorina, whereas calcium concentrations had little or no effect on cadmium accumulation in M. edulis. Cadmium accumulation in the whole body of C. maenas was affected equally by calcium concentrations and total salinity, whereas accumulation in the exoskeleton was mainly affected by changes in total salinity. Individual variability in cadmium accumulation in the organs of C. maenas was greater than the variation attributable either to changes in ambient calcium concentrations or total salinity. An appreciable amount of the inter-individual variability in the cadmium accumulation in all three species was correlated with wet:dry weight ratios of the tissues and size of the organisms.     

Effects of experimental feeding and starvation on the proximate composition of the European bass Dicentrarchus labrax

Juvenile bass, Dicentrarchus labrax (L.), fed ad libitum on trout pellets, the shore crab Carcinus maenas and filleted saithe, Gadus virens, did not differ significantly in proximate composition although the diets were absorbed with high efficiencies of 94 to 99% and differed greatly in composition. Compared with wild fish, the white muscle, dark muscle, liver and mesenteric fat bodies of laboratory-reared bass were lower in moisture and higher in lipid. Starvation caused a rapid initial decrease in carbohydrate and a progressive decline in lipid in all tissues, coupled with an increase in moisture and ash contents. The liver and fat body somatic indices also declined, indicating that these organs are the major lipid storage depots in bass, in contrast with the skeletal muscle which has this role in other active fishes such as salmonids and clupeids. Lipid and protein are inversely related to moisture content in whole specimens.