Impact assessment of an invasive flatworm, Convoluta convoluta, in the Southern Gulf of Maine

Convoluta convoluta (Abildgaard 1806) is a small (2-3 mm long) acoellous turbellarian flatworm from Europe that has invaded the Gulf of Maine within the last 5 years. Although it has been reported in densities of up to 19 individuals/cm², its ecological impact remains unknown. In its native habitat, it consumes harpacticoid copepods and primary settling mussels <0.5-mm shell length. This study estimated the impact of C. convoluta on juvenile blue mussel populations (Mytilus edulis Linnaeus 1758) around the Isles of Shoals in the southern Gulf of Maine, USA as well as looking at their distribution in their new habitat. We surveyed worm densities at sites of differing wave exposure over three substrates (hard substrates, bladed algae, filamentous algae) to quantify patterns of worm abundance. We found worms on all substrate types with their highest abundances occurring in areas of maximal sunlight exposure and minimal physical disturbance. We showed a definite pattern of consumption of mussels in the lab and found C. convoluta to consume up to 35% of primary settling mussels in the field, but only under certain conditions. Per capita impact on juvenile mussels was found to vary greatly in correlation with mussel recruitment rate and water temperature, but not with the consumption of harpacticoids. Our results also suggested that per capita interaction strength was reduced by intraspecific density-dependent competition and water temperature. The overall impact of C. convoluta on mussel populations in the southern Gulf of Maine is therefore estimated to be minimal.     

Spatial and temporal effects of pre-seeding plates with invasive ascidians: Growth, recruitment and community composition

Many shallow water subtidal habitats in Massachusetts, USA have recently been invaded by five non-indigenous ascidian species: Ascidiella aspersa, Botrylloides violaceus, Didemnum sp., Diplosoma listerianum and Styela clava. This study examined the effects of seawater temperature, as a proxy for climate change, on B. violaceus and D. listerianum and the impact these ascidians have on native sessile fouling communities. Field experiments were conducted over a four month period at two locations (Lynn and Woods Hole, MA) to examine growth dynamics over regional thermal and geographic ranges. Invasive ascidians occupied as much as 80% of the primary substratum and accounted for the majority of species richness. B. violaceus and D. listerianum growth were similar at both study sites, but initial colony growth of D. listerianum was positively affected by temperature. B. violaceus and D. listerianum exhibited rapid two-week growth rates during the summer months with more rapid growth at the warmer Woods Hole site. Competition for space between B. violaceus and D. listerianum typically resulted in neutral borders between colonies. Overgrowth occurred if the colony of one species was disproportionably larger than the colony of the other species. Recruitment and growth of native species influenced the long-term composition of experimental communities more than the pre-seeding with B. violaceus or D. listerianum colonies. Elevated temperatures, however, increased initial growth of B. violaceus and D. listerianum and may have facilitated the species success to invade the communities during crucial periods of introduction. With projected global climate change, a rise in sea surface temperatures may exacerbate the cumulative impacts of invasions on benthic communities and facilitate the invasion of other non-native ascidian species.     

Recent population expansions of non-native ascidians in The Netherlands

Over the last 50 yrs seven non-native ascidians have settled in The Netherlands, concentrated in the two periods 1974-1977 and 1991-2004 (i.e., Styela clava, Aplidium glabrum, Diplosoma listerianum, Didemnum sp., Botrylloides violaceus, Molgula complanata and Perophora japonica). The year of the introduction of B. violaceus remains a matter of dispute because many of the Botrylloides specimens that are recorded in western Europe, have been identified as the closely resembling species B. leachi. Only Didemnum sp. has become a true invasive species and has become a threat to native ecosystems, especially in the province of Zeeland, by its ability to overgrow virtually all hard substrata present. This includes rocks, stones, sand, algae and almost all sessile marine animals. The sudden population expansion of the didemnid from 1996 onward, coincided with the cold winter of 1995-1996, which caused decreased population sizes of many marine animals. The resulting increase in the availability of suitable substrates for settlement and the strong decrease of grazing sea urchins, may have triggered the population expansion. Studying its population dynamics, the optimal growing temperature for Didemnum sp. appears to be 14-18 °C. Virtually all colonies die when the water temperature gets colder than 5 °C. Colonies growing on live marine animals seem to be more resistant to the cold, than those growing on rocks, stones and plants. Two potential predators of the didemnid have also been recorded in Dutch waters: the gastropods Trivia arctica and Lamellaria sp.     

Natural chimerism in colonial urochordates

Natural chimeras are commonly distributed in the wild, challenging the traditional paradigm for the advantages of genetically homogenous entities, where uniclonality prevents within-organism conflicts. This essay focuses on the last two-decade studies on chimerism in the cosmopolitan urochordate Botryllus schlosseri, enlightening and focusing the idea of multichimeras as a primary tool for fending off the pervasiveness of super parasitic germ lines. Interacting Botryllus colonies may fuse or reject each other based on allelic compatibility on a single highly polymorphic gene locus. After fusion and establishment of a chimera, a second tier of allorecognition is developed, expressed as genetically controlled morphological resorption of one of the chimeric partners. This is followed by the third tier of allorecognition where somatic and germ cell lineages parasitism are developed. Studies revealed a complex network of costs and few suggested benefits for the state of chimerism in botryllid ascidians. Two life history traits (diversification of allorecognition allele repertoire, colonial programmed lifespan) were considered as selected to combat the major cost of chimeric associated germ cell parasitism. Three other ecological traits (heterosis, settlement of kin larvae in aggregates, multichimerism) have been suggested as selected to enhance the existence of chimerism in botryllid ascidians. Recent results revealing a fine-tuning of the chimerical somatic genetic components in response to changes in environmental conditions are discussed. Results further elucidate the possible existence of multichimeras, each made of several genotypes. It is proposed that natural multichimeras form more stable and vigorous entities, depicting a unique way for domesticating consortia of selfish cells that may otherwise seriously threaten survivorship of the entity.     

Molecular quantification of toxic Alexandrium fundyense in the Gulf of Maine using real-time PCR

The toxic dinoflagellate Alexandrium fundyense is widespread in the northeastern part of North America, including the Gulf of Maine, and is responsible for seasonal harmful algal blooms in these regions. Even at low cell densities, A. fundyense toxins can accumulate in shellfish and result in paralytic shellfish poisoning (PSP). PSP can be debilitating or lethal to humans and other shellfish consumers and is a public health concern. As a result, accurate measurements of A. fundyense distributions, particularly at low cell density, are critical to continued PSP monitoring and mitigation efforts. Towards this end we have developed a real-time quantitative PCR (qPCR) method to monitor A. fundyense. Laboratory validation indicates that the qPCR assay is sensitive enough to detect 10 cells per sample, and that it does not detect co-occurring dinoflagellates such as Alexandrium ostenfeldii. The qPCR methodology was used to quantify A. fundyense cell densities in samples collected during a spring 2003 transect in the Gulf of Maine, and the data were compared to those obtained in parallel from light microscope and DNA hybridization-based methods. Results show that A. fundyense cell density was low during this period relative to typical cell densities required for PSP contamination of local shellfish, and that qPCR values were comparable to numbers determined by independent methods.     

The Asian red seaweed <Emphasis Type="Italic">Grateloupia turuturu</Emphasis> (Rhodophyta) invades the Gulf of Maine

We report the invasion of the Gulf of Maine, in the northwest Atlantic Ocean, by the largest red seaweed in the world, the Asian Grateloupia turuturu. First detected in 1994 in Narragansett Bay, Rhode Island, south of Cape Cod, this alga had expanded its range in the following years only over to Long Island and into Long Island Sound. In July 2007 we found Grateloupia in the Cape Cod Canal and as far north (east) as Boston, Massachusetts, establishing its presence in the Gulf of Maine. Grateloupia can be invasive and may be capable of disrupting low intertidal and shallow subtidal seaweeds. The plant's broad physiological tolerances suggest that it will be able to expand possibly as far north as the Bay of Fundy. We predict its continued spread in North America and around the world, noting that its arrival in the major international port of Boston may now launch G. turuturu on to new global shipping corridors.     

Marine Foraging Birds As Bioindicators of Mercury in the Gulf of Maine

From existing databases, we compiled and evaluated 604 total mercury (Hg) levels in the eggs and blood of 17 species of marine foraging birds from 35 Gulf of Maine islands to provide baseline data and to determine the best tissue, age class, and species for future biomonitoring. While mean Hg levels in most species did not exceed adverse effects thresholds, levels in some individual eggs did; for all species arithmetic mean egg Hg levels ranged from 0.04 to 0.62 (μg/g, wet weight). Piscivorous birds had higher Hg levels than invertivores. Leach’s storm-petrel (Oceanodroma leucorhoa), razorbill (Alca torda), and black guillemot (Cepphus grylle) adult blood and egg Hg levels were higher than other species. Our results indicate that adult blood is preferable to chick blood for detecting long-term temporal trends because adult levels are higher and not confounded by metabolic effects. However, since we found that eggs and adult blood are comparable indicators of methylmercury bioavailability, we determined that eggs are the preferred tissue for long-term Hg monitoring because the relative ease in collecting eggs ensures consistent and robust datasets. We suggest specific sampling methods, and based on our results demonstrate that common eider (Somateria mollissima), Leach’s storm-petrel, double-crested cormorant, and black guillemot are the most effective bioindicators of Hg of the Gulf of Maine.     

Quantifying alosine prey in the diets of marine piscivores in the Gulf of Maine

The objectives of this work were to quantify the spatial and temporal distribution of the occurrence of anadromous fishes (alewife Alosa pseudoharengus, blueback herring Alosa aestivalis and American shad Alosa sapidissima) in the stomachs of demersal fishes in coastal waters of the north‐west Atlantic Ocean. Results show that anadromous fishes were detectable and quantifiable in the diets of common marine piscivores for every season sampled. Even though anadromous fishes were not the most abundant prey, they accounted for c. 5–10% of the diet by mass for several marine piscivores. Statistical comparisons of these data with fish diet data from a broad‐scale survey of the north‐west Atlantic Ocean indicate that the frequency of this trophic interaction was significantly higher within spatially and temporally focused sampling areas of this study than in the broad‐scale survey. Odds ratios of anadromous predation were as much as 460 times higher in the targeted sampling as compared with the broad‐scale sampling. Analyses indicate that anadromous prey consumption was more concentrated in the near‐coastal waters compared with consumption of a similar, but more widely distributed species, the Atlantic herring Clupea harengus. In the context of ecosystem‐based fisheries management, the results suggest that even low‐frequency feeding events may be locally important, and should be incorporated into ecosystem models.     

Programmed cell death in vegetative development: apoptosis during the colonial life cycle of the ascidian Botryllus schlosseri

Programmed cell death (PCD) by apoptosis is a physiological mechanism by which cells are eliminated during embryonic and post-embryonic stages of animal life cycle. During asexual reproduction, the zooids of colonial ascidians originate from an assorted cell population instead of a single zygote, so that we assume that regulation of the equilibrium among proliferation, differentiation and cell death may follow different pathways in comparison to the embryonic development. Here we investigate the presence of apoptotic events throughout the blastogenetic life cycle of the colonial ascidian Botryllus schlosseri, by means of terminal deoxynucleotidyl transferase dUTP Nick End Labeling (TUNEL) coupled with histochemical and electron microscopy techniques. The occurrence of low levels of morphogenetic cell death suggests that, in contrast to what happens during sexual development (embryogenesis and metamorphosis), apoptosis does not play a pivotal role during asexual propagation in botryllid ascidian. Nevertheless, PCD emerges as a key force to regulate homeostasis in adult zooids and to shape and modulate the growth of the whole colony.     

Atlantic bluefin tuna in the Gulf of Maine,II: precision of sampling designs in estimating seasonal abundance accounting for tuna behaviour

A primary challenge of animal surveys is to understand how to reliably sample populations exhibiting strong spatial heterogeneity. Building upon recent findings from survey, tracking and tagging data, we investigate spatial sampling of a seasonally resident population of Atlantic bluefin tuna in the Gulf of Maine, Northwestern Atlantic Ocean. We incorporate empirical estimates to parameterize a stochastic population model and simulate measurement designs to examine survey efficiency and precision under variation in tuna behaviour. We compare results for random, systematic, stratified, adaptive and spotter-search survey designs, with spotter-search comprising irregular transects that target surfacing schools and known aggregation locations (i.e., areas of expected high population density) based on a priori knowledge. Results obtained show how survey precision is expected to vary on average with sampling effort, in agreement with general sampling theory and provide uncertainty ranges based on simulated variance in tuna behaviour. Simulation results indicate that spotter-search provides the highest level of precision, however, measurable bias in observer-school encounter rate contributes substantial uncertainty. Considering survey bias, precision, efficiency and anticipated operational costs, we propose that an adaptive-stratified sampling alone or a combination of adaptive-stratification and spotter-search (a mixed-layer design whereby a priori information on the location and size of school aggregations is provided by sequential spotter-search sampling) may provide the best approach for reducing uncertainty in seasonal abundance estimates.

Vagile macrofauna and the hydrographic environment of the Saco River Estuary and adjacent waters of the Gulf of Maine

We studied the vagile epibenthic and nektonic macrofauna and hydrographic environments of the Saco River estuary and adjacent waters, including Biddeford Pool lagoon and Saco Bay (Gulf of Maine), over a 3-year period (1979–82). Twice as many species of vagile macrofauna were found in Saco Bay as in the estuarine environments, and none were found at the head of the estuary below the dam. Field distributions of various species and life stages agreed with their locomotor responses in the laboratory to physicochemical gradients, supporting the view that habitat correlations are at least in part determined by active habitat preference and/oor avoidance behavior of vagile species. We also examined the stomach contents of specimens of two common fish species to determine their local feeding habits. Yearling Pollachius virens fed primarily on Ammodytes americanus, while yearling Pseudopleuronectes americanus stomachs contained primarily small, whole Echinarachnius parma.     

Predation by gulls on crabs in rocky intertidal and shallow subtidal zones of the Gulf of Maine

Most organisms in intertidal areas are marine in origin; many have distributions that extend into the subtidal zone. Terrestrial predators such as mammals and birds may exploit these animals during low tide and can have considerable effects on intertidal food webs. Several studies have shown that avian predators are capable of reducing densities of sessile and slow-moving intertidal invertebrates but very few studies have considered avian predation on mobile invertebrate predators such as crabs. In this study, we investigated predation by Great Black-backed Gulls (Larus marinus Linnaeus) on three species of crabs (Cancer borealis Stimpson, Cancer irroratus Say, and Carcinus maenas Linnaeus). The study was at Appledore Island, ME (a gull breeding island) and 8 other sites throughout the Gulf of Maine, including breeding islands and mainland sites. On Appledore Island, intertidal and subtidal zones provided over one-third of prey remains found at gull nests, and crabs were a substantial proportion (∼ 30% to 40%) of the total remains. Similarly, collections of prey remains from intertidal areas indicated that crabs were by far the most common marine prey. C. borealis was eaten far more often and C. irroratus and C. maenas less often than expected at each site. Comparing numbers of carapaces to densities of crabs in low intertidal and shallow subtidal zones at each site, we estimated that gulls remove between 15% and 64% of C. borealis during diurnal low tides. The proportion of C. borealis eaten by gulls was independent of proximity to a gull colony. Approximately 97% of the outer coast of Maine is within 20 km of a breeding island. Thus, a lot of gull predation on crabs may occur throughout the Gulf of Maine during summer months. Crabs are important predators of other invertebrates; if predation by gulls reduces the number of crabs in intertidal and shallow subtidal areas, gulls may have important indirect effects on intertidal food webs.     

The annual gametogenic cycle of the sea anemone Metridium senile from the Gulf of Maine

A year-long study was conducted to quantify the reproductive cycle of the clonal sea anemone, Metridium senile, an important member of the benthic community in the Gulf of Maine (GOM). M.senile is an abundant sessile invertebrate that forms identifiable clonal aggregations that are maintained by pedal laceration but individuals can also reproduce sexually. Specimens were collected monthly from a shallow (< 10 m) subtidal site and the reproductive cycle of male and female anemones was described on a seasonal basis using histological preparation of the gonads and light microscopy. Gametogenesis was determined for both sexes and showed that females undergo spawning during the seasonal transition from summer to fall, while males have mature sperm within testicular cysts in the winter, spring, and summer. Environmental data recorded at the study site shows that the spawning period occurs during a period of peak water temperature (August-September), and rapid gametogenesis occurs during periods of high food availability (April). The low percentage of reproductively mature anemones and the dominance of asexual reproduction in this population are believed to be the result of the high flow regime at this site.     

Ecological observations on the colonial ascidian Didemnum sp. in a New England tide pool habitat

The colonial ascidian Didemnum sp. has colonized northwestern Atlantic coastal habitats from southern Long Island, New York, to Eastport, Maine. It is also present in offshore habitats of the Georges Bank fishing grounds. It threatens to alter fisheries habitats and shellfish aquacultures.Observations in a tide pool at Sandwich, MA from December 2003 to February 2006 show that Didemnum sp. tolerates water temperatures ranging from ≤ 1 to > 24 °C, with daily changes of up to 11 °C. It attaches to pebbles, cobbles, and boulders, and it overgrows other tunicates, seaweeds, sponges, and bivalves. From May to mid July, colonies appear as small patches on the bottoms of rocks. Colonies grow rapidly from July to September, with some growth into December, and they range in color from pink to pale yellow to pale orange. Colony health declines from October through April, presumably in response to changes in water temperatures, and this degenerative process is manifested by color changes, by the appearance of small dark brown spots that represent clumps of fecal pellets in the colony, by scavenging by periwinkles, and by a peeling-away of colonies from the sides of cobbles and boulders. At Sandwich, colonies died that were exposed to air at low tide. The species does not exhibit this seasonal cycle of growth and decline in subtidal habitats (40-65 m) on the Georges Bank fishing grounds where the daily climate is relatively stable and annual water temperatures range from 4 to 15 °C. Experiments in the tide pool with small colony fragments (5 to 9 cm²) show they re-attach and grow rapidly by asexual budding, increasing in size 6- to 11-fold in the first 15 days. Didemnum sp. at Sandwich has no known predators except for common periwinkles (Littorina littorea) that graze on degenerating colonies in the October to April time period and whenever colonies are stressed by desiccation.The tendencies of the ascidian (1) to attach to firm substrates, (2) to rapidly overgrow other species, (3) to tolerate a wide temperature range, (4) to be free from predation, and (5) to spread by colony fragmentation combine to make it a potential threat to benthic marine habitats and aquacultures. Didemnum sp. is known to overgrow mussels, oysters, and sea scallops, and it likely envelops other bivalves too.     

A comparison of relict versus equilibrium models for insular mammals of the Gulf of Maine

For the mammalian faunas of 24 landbridge islands in the Gulf of Maine (0.003–279 km² in size), area accounts for 86% of variance in species richness. The slope, z , of the species-area curve is 0.247. For the seven largest islands (>10km²), the non-equilibrium hypothesis of relaxation following saturation in the post-Pleistocene is suggested by (1) elevated slope of the species-area curve (0.353), (2) correlation of species richness with island age ( r =- 0.81) and water depth to mainland ( r = -0.70), (3) highly non-random nested subsets of species ranked by island area, and (4) discontinuity with the extremely depauperate faunas of oceanic islands of the eastern North Atlantic. The alternative hypothesis of a dynamic equilibrium determined by recurrent immigration and extinction is supported by (1) documented turnover in 16 species, (2) correlation of species-area residuals with distance ( r = - 0.90), (3) distribution dependent upon vagility with reduction or absence of hibernators and other poor dispersers, (4) low levels of endemism, and (5) congruence of community structure with that of mainland fauna for both trophic level and body size.
I conclude that while some insular populations may be relictual, the faunal composition of most of these islands is dependent on recurrent colonization, much of which takes place over ice bridges. However, true equilibrium is perturbed by climatic shifts, range expansions, and human disturbance.     

Suppression of programmed cell death regulates the cyclical degeneration of organs in a colonial urochordate

The survival of animal tissues and organs is controlled through both activation and suppression of programmed cell death. In the colonial urochordate Botryllus schlosseri, the entire parental generation of zooids in a colony synchronously dies every week as the asexually derived generation of buds reaches functional maturity. This process, called takeover, involves massive programmed cell death (PCD) of zooid organs via apoptosis followed by programmed removal of cell corpses by blood phagocytes within approximately 1 day. We have previously reported that developing buds in conjunction with circulating phagocytes are key effectors of zooid resorption and macromolecular recycling during takeover, and as such engineer the reconstitution of a functional asexual generation every week [Lauzon, R.J., Ishizuka, K.J., Weissman, I.L., 2002. Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: a model for development and regeneration. Dev. Biol. 249, 333-348]. Here, we demonstrate that zooid lifespan during cyclic blastogenesis is regulated by two independent signals: a bud-independent signal that activates zooid PCD and a bud-dependent, survival signal that acts in short-range fashion via the colonial vasculature. As zooids represent a transient, mass-produced commodity during Botryllus asexual development, PCD regulation in this animal via both activation and suppression enables it to remove and recycle its constituent zooids earlier when intra-colony resources are low, while maintaining the functional filter-feeding state when resources are adequate. We propose that this crosstalk mechanism between bud and parent optimizes survival of a B. schlosseri colony with each round of cyclic blastogenesis.     

Growth-mortality trade-offs along a depth gradient in Cancer borealis

Intertidal and shallow subtidal ecosystems experience steep environmental gradients over short distances. Individual foraging rate, predation risk, and physiologic stress vary along these gradients, resulting in growth-mortality trade-offs with depth. In the summer, Cancer borealis commonly forage in the shallow subtidal in the Gulf of Maine. C. borealis are the favored invertebrate prey of the Herring Gull and the Great Black-backed Gull, which consume 25%-50% of available C. borealis (those in < 1 m water) during each daytime low tide. We investigated three possible explanations for the presence of C. borealis in the risky gull-predation zone. First, we tested whether predation risk in the gull-predation zone was matched at deeper depths by subtidal predators; we found predation risk decreases with depth. Second, we tested whether water temperatures were warmer in the gull-predation zone and whether these warmer temperatures resulted in increased growth rates. We found that, while waters were warmer in the gull-predation zone, crabs grew at similar rates above and below the thermocline when fed similar diets. Finally, we tested for differences in food availability with depth and whether these differences influenced C. borealis growth rates. Our results suggest a growth-mortality trade-off, where increased food availability provides sufficient growth benefit to outweigh the risk of foraging at shallower depths.