Defenses and refuges: alternative mechanisms of coexistence between a predatory gastropod and its ascidian prey

Only five of the 14 species of solitary ascidians in the San Juan Islands, Washington, USA commonly co-occur with an abundant predator of the rocky subtidal, the gastropod Fusitriton oregonensis. None of the common subtidal species is defended by vanadium or sulfuric acid; concentrations of these substances are highest in species that are eaten readily by F. oregonensis and are uncommon in the rocky subtidal. Experimental manipulations indicate that Halocynthia igaboja are protected by stiff spines of the tunic. The defense mechanism of Pyura haustor consists of a tough, leathery tunic with inorganic inclusions, and microscopic spines around the siphons. Boltenia villosa and Styela gibbsii are eaten by snails in the laboratory, but live in areas where the predator is abundant. Both find refuge as epizooites on P. haustor and H. igaboja. The mechanisms by which Cnemidocarpa finmarkiensis persists in the presence of F. oregonensis is unknown.     

The structure of subtidal algal and invertebrate assemblages at the Chatham Islands,New Zealand

We examined the distribution and abundance of organisms on subtidal rocky reefs at nine sites around the Chatham Islands, a remote group 780 km east of southern New Zealand. We sampled five depth strata ranging from 1 to<16 m to identify spatial patterns in the abundance of algae and invertebrates and to assess their variation within and among sites. This information is used to discuss hypotheses concerning community structure at this remote locality. Several patterns were apparent. The immediate subtidal was occupied by the southern bull kelp Durvillaea spp. A suite of 11 fucalean species were dominant to a depth of 10 m with an average abundance of 28 m^-2, while one species, Carpophyllum flexuosum, occurred mostly in deeper water. Only two laminarian species of algae were present at the islands. The indigenous Lessonia tholiformis was abundant at 2.5 to 15 m and was not found in deeper water, while the giant kelp Macrocystis pyrifera was abundant at two sites in 12 to 18 m. The commercially valuable abalone Haliotis iris was extremely abundant in shallow water, with an overall mean of 6 m^-2 at 5 m. The sea urchin Evechinus chloroticus was common, but reached high densities only in small (<25 m²) patches. The characteristic urchin-dominated zones reported in kelp beds world-wide were not seen. There was considerable site-to-site variation in the occurrence and abundance of individual species. Some differences between sites were associated with shelter from swell (e.g. M. pyrifera was found only in sheltered sites) and physical habitat (e.g. juvenile H. iris were found only beneath boulders inshore), but much of the variation could not be explained by physical or depth-related factors alone. We hypothesize that the differences in these kelp bed assemblages compared to mainland New Zealand are partially due to the high degree of endemism at the Chatham Islands. Local variation cannot be explained by herbivory, and is most likely the result of the various life-history characteristics of the major habitat-forming species, the large brown algae.     

Microhabitat-associated variability in survival and growth of subtidal solitary ascidians during the first 21 days after settlement

Newly settled juvenile ascidians were transplanted into shaded and unshaded sites at two subtidal depths to test the hypothesis that photonegative settlement behavior enhances juvenile survival. Silt, filamentous algae and grazing gastropods (Margarites pupillus) were identified as sources of mortality associated primarily with non-cryptic microhabitats. Silt inflicted heavy mortality on all six species tested. Algal overgrowth was important in shallow water, where it increased mortality and depressed growth rates over a 14-d period. Laboratory experiments demonstrated that gastropods can remove juvenile ascidians from the substratum. The sources of post-settlement mortality investigated may help determine distributional patterns of ascidians in the San Juan Islands, Washington, USA, and may also represent selective pressures that maintain negative phototaxis in the behavioral repertoires of ascidian tadpoles.     

Settlement, recruitment and potential predators and competitors of juvenile echinoderms in the rocky subtidal zone

Recruitment patterns of marine invertebrates are affected both by settlement and early post-settlement events. This study examined the settlement and recruitment patterns of echinoderms at three sites in the rocky subtidal zone of Bocabec Cove, Bay of Fundy, Canada using artificial turf collectors and quadrats on the natural substrate. Potential predators were quantified at two of the sites along transects and in 1-m² quadrats. Both potential predators and competitors were quantified in 0.0625-m² quadrats. Settlement varied across sites (1.5–3 km apart) and two years of sampling (2004, 2005). The site of most potential settlement differed for the three groups of echinoderms: sea urchins (Strongylocentrotus droebachiensis), sea stars (Asterias spp.) and sea cucumber (Psolus fabricii). Settlement densities on the artificial turf collectors tended to be greater than the densities of settlers on the natural substrate. On the natural substrate, the only significant difference between densities of juveniles over time was that newly settled sea stars were found in July and were not found the following October. Large lobsters and carnivorous worms were potential predators with densities that varied between sites. Potential competitors that differed in abundance between sites were herbivorous gastropods and conspecifics for sea urchins; and carnivorous worms for sea stars. This study suggests that patterns of recruitment are either set up by patterns of settlement or by events during the first few weeks/months on the benthic substrate for these echinoderms.     

Association among ascidians: facilitation of recruitment inPyura spinifera

Subtidal benthic communities on hard substrata are usually characterised by intense competition for space; neighbouring organisms are generally viewed as a threat to the maintenance of this limited resource. Here, I describe an association between two species of subtidal ascidians where the abundance of one appears to be wholly determined by the abundance of the other.Pyura spinifera is a large subtidal stalked ascidian that is common in south-eastern Australia and usually occurs in clumps. At the base of these clumps the unstalked ascidianCnemidocarpa pedata is often present. Between February and May 1992, I used a removal experiment to test the prediction that the recruitment ofP. spinifera was dependent on the presence ofC. pedata. There were three treatments at two sites: (i)C. pedata were totally removed, (ii)C. pedata densities were reduced by half, and (iii) ascidians were left untouched (control). The removal ofC. pedata significantly reducedP. spinifera recruitment relative to controls; recruitment ofP. spinifera was only observed onC. pedata. Results were consistent between sites. Furthermore, laboratory settlement trials indicated thatP. spinifera settle preferentially in response to cues with which recruits are normally associated, while settlement is poor or does not occur in the absence of such cues. Laboratory trials also indicate that these responses are mediated by water-borne compounds.     

Differences in relative abundance and size structure of the sea stars Pisaster ochraceus and Evasterias troschelii among habitat types in Puget Sound, Washington, USA

We surveyed patterns in the relative abundance and size structure of the sea stars Pisaster ochraceus and Evasterias troschelii in five habitat types of varying structural complexity and prey availability (sand/cobble, boulder, and rocky intertidal; pilings; and floating docks) in Puget Sound and the San Juan Islands, Washington. For both species, small sea stars were most abundant in the most structurally complex habitat type (boulder), where they occurred almost exclusively under boulders during low tide. Larger individuals became more abundant as structural complexity decreased, occurring more frequently in open habitat types (rocky shores, pilings, and docks) known to have greater abundances of prey resources. Gull foraging observations and experiments demonstrated that exposed small sea stars of both species were highly vulnerable to predation, suggesting that small sea stars require structural complexity (crevice microhabitat) as a predation refuge. Large sea stars, once attaining a size refuge from predation, appear to migrate to more exposed habitat types with more abundant food resources. These results suggest parallel ontogenetic habitat shifts in two co-occurring consumer species related to a shared predation risk at early life stages and demonstrate how the relative importance of top-down and bottom-up processes may differ with ontogeny.     

Role of competition and predation in determining habitat occupancy of Cerithiidae (Gastropoda: Prosobranchia) on the rocky,intertidal, Red Sea coasts of Sinai

Six cerithiid snail species occur on rocky intertidal flats along the Sinai coasts of the Red Sea: Clypeomorus moniliferum, Cerithium caeruleum, C. scabridum, C. columna, Clypeomorus tuberculatum and Cerithium echinatum. The present study, conducted at 22 stations covering almost the whole length of Sinai, covered the 4 yr period from October 1972 to August 1976, and describes the habitat occupancy of 5 of these species (C. echinatum is excluded for lack of data). Several of these species (sometimes all) often occur together, and in such cases are distincly segregated by habitat. However all species considerably overlap in their distribution along the axes of four major interrelated abiotic gradients, thus excluding the possibility that habitat segregation is determined by larval settlement preferences. Other distributional patterns observed at some sites, such as lack of overlap or contact between belts of the various species and the relative abundance of food available to all species, make postlarval competitive interactions unlikely. The existence and the degree of proximity of a coral reef with its associated predatory fishes, influence the cerithiids' distributional patterns. Differences between the cerithiid species in their vulnerability to fish predation, associated with differences between sites in the abundance and the accessibility of predatory fishes, and in the availability of refuges for each cerithiid species, can satisfactorily explain the observed distributional patterns including co-occurrence with habitat segregation. It is proposed that habitat segregation is caused by predation on young stages by generalist fishes which may totally eliminate a certain species at a given site; the same site may provide refuges for recruits of another species, allowing these to survive to an advanced age. In general, the flat's structural complexity is associated with its diversity of refuges from predation, and hence with the number of co-existing species. This mechanism for co-existence and habitat segregation in tropical Cerithiidae may also be instrumental in maintaining the high species diversity of other tropical benthic communities.Paper No. 12 in the series Colonization of the Eastern Mediterrancan by Red Sea species immigrating through the Suez Canal     

Biological traits of three closely related species of <Emphasis Type="Italic">Pycnoclavella</Emphasis> (Ascidiacea) in the Western Mediterranean

The reproductive cycles and abundance of the sympatric colonial ascidians Pycnoclavella brava, Pycnoclavella aurilucens and Pycnoclavella communis from two Northwestern Mediterranean sites over a period of 2.5 years are reported. The species showed some differences in their biological patterns. Gonad maturation and larval brooding took place during autumn and early winter for P. communis, during spring for P. aurilucens and during late winter and spring for P. brava. Summer was found to be the unfavorable season for all species, and an aestivation period occurred in P. communis and P. brava. Maximum abundance for the three species was observed during winter. Growth rates of the most abundant species, P. communis, were also monitored and found to peak during the initial phases of reactivation after aestivation. Growth rates decreased afterwards, becoming negative as water temperature started to increase after the winter minima. Reproductive activity and growth rates for P. communis displayed a temporal lag that suggested partitioning of resources to either reproduction or growth in this species.     

Community development on subtidal temperate reefs: the influences of wave energy and the stochastic recruitment of a dominant kelp

Patterns of community development on subtidal rocky reefs in Marmion Lagoon, southwest Australia, were investigated with a settlement panel experiment. We tested the hypothesis that community development would differ between outer and inner reefs lines, because exposure to swell and wave energy was significantly greater on outer reefs. Following a 14-month deployment, we recorded pronounced variability between panels and sites, but did not detect any effect of wave exposure on the structure of panel assemblages. Subsequent data exploration suggested the importance of the presence of kelp recruits (Ecklonia radiata) in structuring the overall assemblage. Panel assemblages with kelp recruits were significantly different in structure to those without, principally because of greater space coverage of encrusting coralline algae and less coverage of red turfing algae, spirorbids, and bryozoans. Mature E. radiata act as ecosystem engineers in subtidal rocky reefs in southwest Australia. Our results suggested the importance of young, recruiting kelps in determining patterns of early community development on newly available hard substrata.     

Differences in morphology and habitat use among the native mussel <Emphasis Type="Italic">Mytilus trossulus</Emphasis>, the non-native <Emphasis Type="Italic">M. galloprovincialis,</Emphasis> and their hybrids in Puget Sound,Washington

Mytilus galloprovincialis (Mg), the Mediterranean blue mussel, is sympatric with the native M. trossulus (Mt) throughout much of the north Pacific, likely as the result of human introduction. We investigated the distribution of the two species and their hybrids (Mgt) in Puget Sound, Washington, to determine whether differences occur in habitat preference between the two species and hybrids. In addition, we investigated whether there were consistent size and shape differences between the native and introduced mussels and hybrids. Measurements of over 6,000 mussels from 30 sites, of which 1,460 were genotyped for a species-specific genetic marker, revealed that Mg and Mgt can be found throughout Puget Sound. Mg and Mgt were larger and exhibited a greater height:length ratio than Mt. Frequencies of Mg and Mgt were higher in subtidal habitats, such as docks, than on intertidal rocks, walls or pilings. Within intertidal habitats, Mg and Mgt were more frequent than Mt in the lower reaches of the intertidal. At slightly more than half the sites the frequency of the three genotypes accorded with random mating expectations suggesting no consistent barriers to gene flow between species. The standardized random sampling methods and simple morphometric identification techniques described here can be used to test whether the frequency of invasive mussels changes over time and space in Puget Sound.     

Influence of occupant microhabitat on the composition of encrusting communities on gastropod shells

The exploitation of microhabitats is widely considered to increase biodiversity in marine ecosystems. Although intertidal hermit crabs and gastropods may inhabit the same shell type and shore level, their microhabitat may differ depending on the state of the tide. On the south coast of Wales the hermit crab Pagurus bernhardus mainly inhabits the shells of Nucella lapillus (84%). Hermit crab shells had a significantly different encrusting community compared with live N. lapillus shells. At low tide the live gastropods were found on exposed rock surfaces whereas hermit crabs were restricted to tidal pools. Communities encrusting live gastropod shells were characterised by lower species richness and abundance compared with shells inhabited by hermit crabs (12 species found in total). A greater abundance and richness of epibionts was recorded from both shell types during the summer compared with winter. Differences in community composition between shell occupant types were attributed to microhabitats used by gastropods and hermit crabs and the associated desiccation pressures, rather than competitive interactions or shell characteristics. This contradicts earlier studies of subtidal shells where biological processes were considered more important than physical factors in controlling species abundance and richness patterns. The use of rockpool microhabitats by hermit crabs increases the biodiversity of rocky shores, as some species commonly found on hermit-crab-inhabited shells were rare in other local habitats.Communicated by J.P. Thorpe, Port Erin     

Reproduction of Halicarcinus planatus (crustacea, decapoda, hymenosomatidae) in the Deseado River estuary, southwestern Atlantic Ocean

The small spider crab Halicarcinus planatus, is a common resident in the rocky coasts of the Magellanic region in South America. The H. planatus population in the Deseado River estuary differs from other populations of the same species in the spatial segregation of sexes. Between March 2002 and October 2003, samples were taken monthly from the lower intertidal and upper subtidal levels. All crabs captured were females. Additional samplings were carried out at the subtidal level to search for the presence of males. A total of 3,346 females were captured and their relative age was determined. Some of these females were maintained in the laboratory to study the terminal moult and the spawning seasons. The analysis of the ovary development of adolescents (ADO) and mature (MAT) females, and the times when females of different ages appear, when spermatophores are found inside spermathecae, and when post-spawning mortality takes place allowed us to establish the whole reproductive process. Adolescents are impregnated only once before the terminal moult. There are seven or eight spawnings after the moult, with a brief resting period between two successive reproductive seasons. The life span of mature females ranges between 15 and 22 months. Results indicate that the H. planatus population of the Deseado River estuary differs greatly from that of the Kerguelen Islands.     

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.     

The adaptive value of larval behavior of a colonial ascidian

Didemnum candidum Savigny, 1816 is an abundant member of the fouling community encrusting docks in Pearl Harbor, Hawaii. In the laboratory, larvae of D. candidum are positively phototactic upon release, but become indifferent to the direction of light prior to settlement. In both the laboratory and the field, settlement is most abundant on shaded, downward-facing surfaces, the location where juvenile survival is greatest. The colonial ascidians Diplosoma listerianum Milne-Edwards, 1842 and Diplosoma sp. also settle abundantly on shaded undersurfaces in the field. Juvenile survival of the Diplosoma species is not affected by exposure to direct light, while survival is greatest on downward-facing surfaces. For Didemnum candidum, light is an important environmental cue used by larvae to locate settlement sites on shaded, downward-facing surfaces where juvenile survival is enhanced.     

Effects of temperature,size, and food on the growth of <Emphasis Type="Italic">Membranipora membranacea</Emphasis> in laboratory and field studies

In the rocky subtidal ecosystem of the western North Atlantic outbreaks of the introduced epiphytic bryozoan Membranipora membranacea cause defoliation of kelp beds and facilitate the introduction of other non-native benthic species. We quantified size- and temperature-dependent growth rates of M. membranacea colonies in the field and the laboratory for durations of 8–23 days. Also, we examined the interaction between food abundance and temperature on growth rates of newly settled colonies in the laboratory. Growth rates were positively related to temperature and increased exponentially with size of colonies over the ranges examined (5.7–16.2°C and 0.5–192 mm, respectively), and were significantly higher in the field than in the laboratory. There was an interactive effect between food and temperature on the size and growth rates of colonies, with the most pronounced effects of food limitation on colonies grown at the warmest temperatures, and no effect of food on colonies grown at the coldest temperatures. Quantifying the growth rates of introduced species is essential to understanding their population dynamics, particularly when outbreaks can have severe impacts on the native community.     

Spatiotemporal coupling/decoupling of planktonic larvae and benthic settlement in decapods in the Scottish east coast

Settlement patterns and the relationship between meroplanktonic larvae and settlement in decapods were studied on the Scottish east coast. Artificial settlement substrates (ASS), deployed at two locations (sandy vs. rocky sea substrates), were employed to collect megalopae and newly settled juveniles. Abundance of meroplanktonic larvae was used as an indicator of larval supply. The results showed a clear seasonality in settlement rates, and in some cases, significant differences between sites were detected. Nevertheless, the interference of the ASS with the surrounding habitat limits the study of spatial variability in settlement rates. Significant cross-correlation was found between the abundance of megalopae and juveniles in the collectors and planktonic larval abundance a month earlier. For individual species, this relationship was observed only in Pisidia longicornis. Complexities caused by the great variety of pre- and post-settlement processes, alongside effects of secondary dispersals of early juveniles may have obscured the relationship between meroplanktonic larvae and juveniles in other species.     

Influences of abundance,behavior, species composition,and ontogenetic stage on active emergence of meiobenthic copepods in subtropical habitats

The emergence of meiobenthic copepods in subtidal sand and seagrass sites in Tampa Bay, Florida (USA), was investigated on nine dates from March 1983 to August 1984. Numbers of emerging copepods were dependent on habitat, date and diel sampling period. Greater numbers typically emerged in seagrass sites, and differences between habitats may be related to lower copepod abundances in sand sites. Both copepod abundance and behavior significantly affected numbers emerging among dates. An increase in emergent behavior alone resulted in consistently greater numbers emerging during postsunset periods. Over 30 species in 15 families were found to emerge. Total numbers of emerging copepods were affected by the sporadic presence and seasonal behavior of certain species. Numbers of the predominant speciesParadactylopodia brevicornis, Tisbe furcata, Parategastes sp.,Mesochra pygmea, Laophontid sp., andHarpacticus sp. emerging depended on differences in both species abundance and behavior. The emergent behavior ofParategastes sp.,Harpacticus sp., andT. furcata also was influenced by total copepod densities in the sediment. Juvenile copepods constituted only a small proportion of the total numbers emerging. The consistent postsunset entry of between 10³ to 10⁵ copepods m^?2 into the water column in subtidal sand and seagrass habitats will contribute to the increased probability of copepod dispersal and reassortment of the benthic community, while providing a pathway for benthic-pelagic exchange.     

Ultrastructural investigations on sperm penetration and gamete fusion in the ascidians Boltenia villosa and Phallusia mammillata

Sperm-egg interactions during fertilization were studied by scanning and transmission electron microscopy in the two ascidian species, Boltenia villosa (collected in 1990 near Friday Harbor, Washington, USA) and Phallusia mammillata (collected in 1990 near Brest, France). Emphasis was put on sperm-egg vitelline coat (VC) and sperm-egg plasma membrane interaction. In both species the sperm activation as revealed by translocation of the mitochondrion was exhibited by sperm binding firmly to or penetrating the VC. Vesicles are present in the sperm apex of both species. Their persistence in late stages of VC penetration suggests for them a function rather in Sperm-egg fusion than in VC penetration. In P. mammillata sperm which are about to make contact and to start fusion with the egg plasma membrane, two types of vesicles, one located at the tip and the other slightly behind the apical cap, were detected. Function and fate of these prominent vesicles remain to be determined. Membrane fusion starts between the sperm membrane of the cap-like structure and short microvilli of the egg surface and then proceeds simultaneously at several sites of the apical region. In B. villosa conspicuous microvilli which are formed at the contact site and interdigitate with the corkscrew-like sperm represent fusion sites on the egg. In both ascidian species sperm are incorporated into the egg at an acute angle. Once fully embodied the sperm lie close and almost parallel to the egg membrane. Our findings are compared with observations in Ciona intestinalis, the only other ascidian species in which Sperm-egg interactions have been thoroughly investigated so far. We suggest that observed differences in the fusion processes are based on morphological differences in sperm structure which reflect phylogenetic modifications.     

Effects of seasonality on the reproductive cycle of <Emphasis Type="Italic">Diadema</Emphasis> aff. <Emphasis Type="Italic">antillarum</Emphasis> in two contrasting habitats: implications for the establishment of a sea urchin fishery

Reproduction of Diadema aff. antillarum was examined between 2002 and 2005 at subtidal rocky bottoms around the Canary Islands. Two contrasting habitats (urchin barrens and grazing fronts) characterized by different levels of food availability were chosen, and factors thought to influence reproductive periodicity were monitored, including temperature, photoperiod, phytoplankton abundance and benthic food availability. Histological analyses showed that D. aff. antillarum had an annual reproductive cycle that was relatively synchronous across the studied sites and habitats. Photoperiod was the most significant factor that correlated with gonad periodicity; benthic food availability of 2 month lag was also correlated. However, some differences were detected between males and females in the timing of the onset of gametogenesis. Spawning was synchronized between both sexes from June to August. Results suggest that the optimum time of year to harvest urchin gonads would be between May and June when gonads were maximal in size but not full of gametes. This species may not provide optimal conditions for an industrial scale fishery, as sea urchins occurring in high density had small gonads and those producing larger volume or more marketable gonad tissue occurred in low densities where harvesting costs would exceed profit.     

Composition and temporal fluctuations of inshore juvenile fish populations in the Kornati Archipelago, eastern middle Adriatic

Temporal fluctuations of species composition and abundance of fish juveniles in the National Park Kornati were studied over 12 months from January to December 1992. A total of 40 168 individuals, representing 24 families and 69 species, were collected using a 50 m long beach seine. The community was dominated numerically by a few species: Atherina hepsetus (45.90%), Sarpa salpa (21.21%), Diplodus vulgaris (10.49%), and Symphodus ocellatus (6.98%), constituting over 84.58% of the total catch. Similarity between patterns in the abundance of the 17 most common species were examined using correlation matrix-based principal component analysis. Results were compared to the abiotic factors leading to the conclusion that only a low amount of variation in the abundance field can be explained by temperature, salinity and dissolved oxygen. Received: 23 March 1997 / Accepted: 11 April 1997