Genetic evidence for kin aggregation in the intertidal acorn barnacle (Semibalanus balanoides)

It is generally assumed that larvae of benthic species are thoroughly mixed in the plankton and distributed randomly at settlement. Yet, it has also been hypothesized that a combination of larval gregarious behaviour coupled with particular oceanographic conditions may prevent larvae from mixing completely, and result in nonrandom spatial distributions following settlement. Using microsatellite markers, the main objective of this study was to investigate the occurrence of statistical connections between relatedness and settlement in the intertidal acorn barnacle from the Gulf of St Lawrence, Canada. A second objective was to test the hypothesis that patches of kin-related individuals came from a common parental site. Our results indicated that a significant number of barnacles within a given sample were more closely related than expected by chance despite the enormous potential for admixture during the planktonic phase. Thus, eight out of 37 samples analysed had relatedness values significantly higher than expected from random settlement. Moreover, analyses of sibship network construction and network complexity tests provided evidence for the occurrence of networks within several samples that were characterized by strong connections among individuals. Thus, nonrandom planktonic dispersal associated with relatively stable oceanic currents, as well as additional ecological factors to be rigorously investigated (e.g. behavioural mechanisms), may be more important in determining patterns of genetic structure in marine benthic invertebrates than generally assumed. Therefore, documenting genetic patterns associated with kin aggregation should be a fruitful and an important avenue for future studies in marine invertebrates.     

The 'ghost of settlement past' determines mortality and fecundity in the barnacle, Semibalanus balanoides

Intraspecific competition is common in many organisms. For many sessile marine invertebrates high settlement densities can lead to competition with conspecifics that can affect the probability of mortality, morphology, and reproductive output. This work aims to determine the affect of recruit density on shell morphology and fecundity and the temporal nature of intraspecific competition for the acorn barnacle, Semibalanus balanoides . Two tile arrays were used; experiment 1 was deployed at the start of the settlement season (43,264 recruits, 4.1% survivorship to adult), experiment 2 was deployed in the middle of the season (5,454 recruits, 42.8% survivorship). Experiment 2 displayed density dependent mortality between recruits and juveniles and adults, whereas no relationship was found for exp. 1. Experiment 2 had higher egg production per individual, but also higher egg production per area of tile compared to exp. 1. A negative relationship was found between recruit density and egg production, however during the summer period, this relationship switched to a positive relationship between juvenile density and egg production, due to high mortality on tiles with high recruit density. Cumulative population density (CPD) was calculated as the cumulative mean density of barnacles per cm^-2 of tile and was used as an index of intraspecific competition. There was a linear negative relationship between mass of eggs per individual and CPD. However, CPD over the summer period more fully explained egg production per individual. A time window was identified when cumulative intraspecific competitive effects were shown to have a strong negative effect on egg production and an increase in mortality, causing a flip from density independent fecundity to density dependent fecundity. These results suggest that recruit density is an important driver of subsequent population processes.     

Climate change and historical biogeography of the barnacle Semibalanus balanoides

Aim Marine sessile inter‐tidal invertebrates are expected to undergo shifts in distribution due to climate change. Using a combination of survey and transplant data with thermal modelling, we investigated the role of climate on the poleward contraction of the southern range edge of the north temperate barnacle Semibalanus balanoides. Location Western Atlantic of the United States. Methods Barnacle surveys were conducted along the east coast of the United States in 1963 and 2007. Presence, absence and abundance data were collected and the time periods were compared. Transplant experiments monitoring survival with relation to temperature were conducted upon S. balanoides along the more southerly portion of their range, and modelling predicting barnacle survival with relation to biogeography was completed. Results The southern limit of S. balanoides has contracted approximately 350 km to the north. Main conclusions The changes thus far observed in climate along the east coast of the United States have contributed to the southern limit range contraction of S. balanoides. Further changes in the biogeography of S. balanoides are expected with continued climate warming.     

Selective settlement of the barnacle Semibalanus balanoides (L.) facilitates its growth and reproduction on mussel beds in the Wadden Sea

On the unstable sedimentary tidal flats of the Wadden Sea, a suitable attachment substrate for sessile organisms is generally lacking. Epibenthic mussel beds (Mytilus edulis L.) provide the only and strongly limited settlement sites available for the barnacle, Semibalanus balanoides (L.). Field investigations showed that barnacles were non-randomly distributed within a mussel bed. They preferentially occurred near the siphonal apertures of living mussels but rarely grew on dead mussels or shell fragments. Field experiments revealed that this was due to selective settlement of barnacle cyprid larvae. Growth of barnacles was significantly higher upon living mussels than on empty mussel shells. Moreover, a higher reproductive output was obtained by individuals on living mussels which produced twice as many nauplii larvae than barnacles attached to empty shells. This study shows that selective settlement of S. balanoides cyprid larvae on living mussels is adaptive with respect to individual fitness. Received in revised form: 15 January 2001 Electronic Publication     

Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides

The northern acorn barnacle Semibalans banlanoides occupies several intertidal microhabitats which vary greatly in their degree of physical stress. This environmental heterogeneity creates distinct selection regimes which can maintain genetic variation in natural populations. Despite considerable attention placed on the link between spatial variation in fitness and balancing selection at specific loci, experimental manipulations and fitness estimates for molecular polymorphisms have rarely been conducted in the wild. The aim of this transplant experiment was to manipulate the level of physical stress experienced by a cohort of barnacles in the field and then investigate the spatial variation in fitness for genotypes at three loci: two candidate allozymes and the mitochondrial DNA control region. The viability of mannose-6-phosphate isomerase (Mpi) genotypes was dependent on the level of physical stress experienced in the various treatments; alternative homozygotes were favoured in alternative high stress-low stress environments. In contrast, the fitness of genotypes at other loci was equivalent among treatments and unaffected by the manipulation. Evaluated in the light of balancing selection models, these data indicate that the presence of multiple environmental niches is sufficient to promote a stable Mpi polymorphism in barnacle populations and that allelic variation at this locus reflects the process of adaptation to the heterogeneous intertidal landscape.     

Recruitment density can determine adult morphology and fecundity in the barnacle, Semibalanus balanoides

Although consequences of the settlement preference of larvae have been well documented, the consequence of these settlement choices on subsequent mortality, morphology and fecundity has been little studied. The aim of this study was to determine the relationship between recruit and adult density and to determine the effect of recruitment on adult morphology and egg tissue mass. This study follows 48,718 barnacles (Semibalanus balanoides) from recruitment at the end of the settling season to reproductively mature adults at a field site in the Clyde Sea (UK). Overall survivorship of the recruits to adulthood was 8.5%, although survivorship was up to 42% on low density settlement panels. In low density colonies (< 10 recruits cm-2), recruitment density was related to adult density (P < 0.001), whereas no relationship was found for higher density colonies. A shell morphology index measured at adulthood was related to recruitment density for low density recruited colonies (P < 0.001) but not high density colonies. Using ANCOVA, variations between the colonies in shell and egg tissue mass were not explained by mass of somatic tissue. However, egg mass was explained by recruitment density (P < 0.01). These results show that adult density is not a reliable indicator of the previous population density of the colony. Moreover, there are marked differences in population development between colonies with high and low recruit densities in terms of impact upon shell morphology and egg production. The dynamics that operate between recruits at the end of the settlement season and sexually mature adults to create the patterns elucidated in this paper, and other literature, remain unclear.     

Genetic structure and the North American postglacial expansion of the barnacle, Semibalanus balanoides

Population genetic characteristics are shaped by the life-history traits of organisms and the geologic history of their habitat. This study provides a neutral framework for understanding the population dynamics and opportunities for selection in Semibalanus balanoides, a species that figures prominently in ecological and evolutionary studies in the Atlantic intertidal. We used mitochondrial DNA (mtDNA) control region (N = 131) and microsatellite markers (～40 individuals/site/locus) to survey populations of the broadly dispersing acorn barnacle from 8 sites spanning 800 km of North American coast and 1 site in Europe. Patterns of mtDNA sequence evolution were consistent with larger population sizes in Europe and population expansion at the conclusion of the last ice age, approximately 20?000 years ago, in North America. A significant portion of mitochondrial diversity was partitioned between the continents (?(ST) = 0.281), but there was only weak structure observed from mtDNA within North America. Microsatellites showed significant structuring between the continents (F(ST) = 0.021) as well as within North America (F(ST) = 0.013). Isolation by distance in North America was largely driven by a split between populations south of Cape Cod and all others (P < 10(-4)). The glacial events responsible for generating allelic diversity at mtDNA and microsatellites may also be responsible for generating selectable variation at metabolic enzymes in S. balanoides.     

The relative magnitude of the effects of biological and physical settlement cues for cypris larvae of the acorn barnacle, Semibalanus balanoides L

Barnacle cypris larvae respond to many cues when selecting a settlement site. The settlement of over a million larvae on tiles of different textures, orientations and densities of incumbent settlers was measured on the rocky intertidal at Great Cumbrae, Scotland. Half of the tiles were replaced every tide whereas the others simultaneously accumulated settlers. Factor effects varied on each tide, and converged in the accumulating deployment. Increasing incumbent density led to net loss of settlement, which was less probable on the textures on which fastest settlment occurred ('very fine'), and more probable on those on which settlement was slowest ('smooth'). More settlement occurred on down-facing orientations during daylight and vice versa. Cue ranks were non-linear, so a path analysis model quantified the relative influence of each factor. Gregariousness was the most influential cue measured, although unmeasured factors had greater effects, highlighting the complexity of settlement influences in this species.     

Effects of herbivorous snails and macroalgal canopy on recruitment and early survivorship of the barnacle Semibalanus balanoides (L.)

This study investigated the effects of grazing by the herbivorous snail Littorina littorea (L.) and the presence of a macroalgal canopy on recruitment and early survivorship of the barnacle Semibalanus balanoides (L.) at four sites of various distances from the mouth of Toothacher Cove on Swans Island in the Gulf of Maine in 1998. Recruitment plates were attached to the substrate at each site in all possible treatment combinations, including either presence of absence of macroalgal canopy, presence or absence of the herbivore, and presence or absence of a cage. Significant differences in recruitment were observed among sites in April and May, but not in June. The average number of recruits also varied significantly among herbivore treatments in May and June, and in the May macroalgaexherbivore interaction. Survivorship did not differ among sites, but did vary significantly among herbivore treatments. These differences were due almost entirely to consistently low recruitment and survival in the uncaged or open controls. Comparisons of the caged and open treatments explained between 88 and 99% of the variation in the respective main effects tests. The presence or absence of L. littorea or of macroalgal canopy had little effect on S. balanoides recruitment or survivorship. Results support previous conclusions that recruitment is greater on more exposed shores and suggest that exclusion cages may protect barnacle recruits from factors such as desiccation and the whiplash effect of macroalgal fronds.     

Regional variation in the spatial scale of selection at MPI* and GPI* in the acorn barnacle Semibalanus balanoides (Crustacea)

Elucidating the ecological processes by which adaptive genetic polymorphism is maintained in heterogeneous environments requires knowledge on the spatial scale at which alternate habitats affect genotype-specific fitness. The general objective of this study was to document patterns of temporal and spatial variation of genetic polymorphism in the acorn barnacle (Semibalanus balanoides) at MPI* and GPI* allozyme loci. A total of 7261 barnacles were sampled in the intertidal at various locations north and south of the Miramichi estuary, New Brunswick, Canada. The results of this study supported the hypothesis that both MPI* and GPI* are under the effect of strong directional selection south of the Miramichi, whereas neutrality cannot be ruled out at sampling sites located north of the estuary. Comparisons between this study and previous ones also question the generality of current hypotheses regarding ecological processes that are responsible for maintaining polymorphism at MPI* and GPI* in the acorn barnacle.     

Speciation and the establishment of zonation in an intertidal barnacle: specific settlement vs. selection

The tropical barnacle Tetraclita forms a belt on hard substrates in the intertidal zone of the Red Sea. Based on morphological data, three distinct species were suggested to exist, occupying different vertical levels - T. barnesorum, T. rufotincta and T. achituvi. In this study we used molecular (12S mitochondrial ribosomal DNA) and ecological data to examine whether this morphological variability reflects genetic differences, or is a result of environmental factors. Adults and spats, collected from settlement plates, were censused and screened genotypically using single strand conformation polymorphism (SSCP) analysis, and settlement dynamics was recorded. We provide evidence for the existence of only two distinct species, and point out both phenotypic plasticity and convergence within and between the proposed species. Cyprids of T. achituvi settle specifically at the lower part of the Tetraclita belt, and feature one phenotype. In contrast, T. rufotincta, occupying the upper and middle portions of the Tetraclita belt, settles throughout the range, shows phenotypic plasticity (three variants), and presumably undergoes selection at the lower part. Thus, the vertical zonation of Tetraclita is produced by the combination of pre-settlement and post-settlement factors, in T. achituvi and T. rufotincta, respectively. The examined system may offer a model in which to study the mechanisms underlying sympatric speciation.     

No effect of naturally-occurring rock types on settlement or survival in the intertidal barnacle, Tesseropora rosea (Krauss)

The settlement and early survival of young barnacles, Tesseropora rosea (Krauss), on four different, naturally-occurring rock substrata were investigated in a four-factor experiment. Three factors assessed variation on three spatial scales: among shores on the New South Wales coast in eastern Australia i.e., 10 to 600 km apart; among sites within these shores i.e., 20 to 50 m apart; within these sites, i.e., < 3 m². Variation on these scales was usually significant for settlement density and proportional survival 30–60 days post-settlement. The fourth factor, different rock types, showed no consistent trends for settlement density or proportional survival. Previously observed differences in these phenomena among shores cannot, therefore, be ascribed to differences in rock substrata.     

Larval development and settlement of a whale barnacle

Larval development and settlement of whale barnacles have not previously been described, unlike intertidal barnacles. Indeed, the mechanisms of the association between barnacles and whales have not been studied. Here we describe the larval development and settlement of the whale barnacle, Coronula diadema, and possible involvement of a cue from the host in inducing larval settlement. Eight-cell stage embryos were collected from C. diadema on a stranded humpback whale, incubated in filtered seawater for 7 days, and nauplius larvae hatched out. When fed with Chaetoceros gracilis, the nauplii developed to stage VI, and finally metamorphosed to the cypris stage. The larval development looked similar to that of intertidal barnacles with planktotrophic larval stages. The cyprids did not settle in normal seawater, but did settle in polystyrene Petri dishes when incubated in seawater with a small piece of skin tissue from the host whale. This strongly suggests the involvement of a chemical cue from the host whale tissue to induce larval settlement.     

Fluctuating asymmetry in Semibalanus balanoides (Crustacea: Cirripedia) at different heights on the shore

Population level studies of fluctuating asymmetry (FA) need to incorporate clinal variation in FA for proper sampling methodologies to be employed to ensure appropriate comparisons between populations are made. FA of adult acorn barnacles. Semibalanus balanoides , in the intertidal zone offers an excellent model system for looking for such variation. This study looked at the magnitude of FA of S. balanoides at each of three vertical heights in the barnacle zone, in two sites on the Isle of Mull, Scotland. Unsigned FA of width of sutures between tergal and scutal plates, after correcting for size and numbers of others touched, showed significant variation across the upper, mid and lower barnacle zone. Specifically, this was a U-shaped pattern, with individuals in the mid-Zone being more symmetrical than those at the two extremes. It is proposed that high levels of FA in the upper zone are due to exposure stresses, while biotic factors such as competition impose developmental stress in the lower zone.     

Nature and perception of barnacle settlement pheromones

It is now almost 50 years since the gregarious settlement of barnacles and its chemical basis was first described. Although originally noted for Elminius modestus, mechanistic studies of gregariousness have focused on two species, Semibalanus balanoides and Balanus amphitrite. By virtue of its ease of study and its economic importance as a fouling organism, the latter species has assumed increasing importance in recent years. This paper will provide an overview of studies on settlement pheromones and their perception. An adult glycoprotein, arthropodin (now known as settlement-inducing protein complex or SIPC), was once thought to be the sole pheromone involved in the induction of cypris larval settlement. At least two other pheromones are now known to be involved, a waterborne cue originating from the adult and the cypris temporary adhesive. The latter is related, immunologically, to SIPC. In keeping with many other examples of chemical communication, the available evidence suggests that barnacle settlement induction involves receptor-ligand interactions and a signal transduction pathway(s) that translates into attachment and metamorphosis. Similar findings have been reported for some, but not all, marine invertebrate larvae examined thus far and the implications for antifoulant development are discussed.     

Identification and egg hatching activity of monohydroxy fatty acid eicosanoids in the barnacle Balanus balanoides.

Monohydroxy fatty acids (MHFAs) were isolated from homogenates of the barnacle Balanus balanoides and identified by gas chromatography-mass spectrometry (GC-MS) as 14- and 17-hydroxy docosahexaenoic acids, 8-, 11-, 12-, 15- and 18-hydroxy eicosapentaenoic acids, 13- and 16-hydroxyoctadecatrienoic acids and 9-, 13- and 15-hydroxyoctadecadienoic acids. Each monohydroxy fatty acid was tested for egg hatching activity in a bioassay using Elminius modestus egg masses, but 8-hydroxy-5, 9, 11, 14, 17-eicosapentaenoic acid (8-HEPE) was the only MHFA with barnacle egg hatching activity. Studies on the egg hatching activity of MHFAs prepared from the oxidation of polyunsaturated fatty acids showed that activity was confined to the 8-hydroxy isomer of eicosapentaenoic acid and arachidonic acid, and that unsaturation at C5 and C14, but not C17, was essential for activity. In addition, the 8(R) conformation is necessary for activity, as 8(R)-HEPE caused egg hatching at 10(-7) M whereas the enantiomer 8(S)-HEPE was inactive.     

The morphology of the central nervous system of the barnacle,Semibalanus cariosus (Pallas)

The central nervous system of the sessile barnacle, Semibalanus cariosus (Pallas), has been studied with the particular aim of determining the locations of neuron somata in relation to peripheral nerves. This was accomplished by tracing peripheral nerves using dissection and methylene blue staining techniques, histological methods, and by permitting cobaltous chloride to diffuse via axons into ganglia (“backfilling”). The neuron maps resulting from the study reveal some well-defined sub-systems, a considerable degree of functional clumping of neuron somata, and some unexpected projections of neurons in the CNS. Neurophysiological studies based on these findings are in progress.     

Evaluating the occurrence of cryptic invasions of a rocky shore barnacle,Semibalanus cariosus,between the north-eastern Pacific and Japan

Many coastal barnacles are introduced to non-native regions. However, data are lacking on cryptic invasion, which is defined as an invasion that remains unrecognised because the invader is mistaken for a native or previously introduced species or clade. In this work, cryptic invasions of an intertidal barnacle, Semibalanus cariosus, between Japan and the north-eastern Pacific were evaluated based on population genetic analyses. A significant genetic differentiation was found between the Japanese and north-eastern Pacific populations, suggesting a limited introduction of non-native genotypes between these regions. Haplotype frequencies did not differ significantly between the past (museum samples collected in 1971 from Hokkaido, Japan) and present Japanese populations, implying the rare occurrence of human-mediated migration from the north-eastern Pacific to Japan. Migrate-n analysis revealed a low level of directional gene flow in S. cariosus from the north-eastern Pacific to Japan, possibly by natural stepping-stone dispersal via directional water currents or human-mediated transport.     

Yeasts of the White Sea intertidal zone and description of Glaciozyma litorale sp. nov.

The intertidal yeast communities inhabiting various environments in the territories of the White Sea Biological Station “Kartesh” (WSBS ZIN RAS) and the N.A. Pertsov White Sea Biological Station (WSBS MSU) were studied. A total of 31 yeast species were isolated using a conventional plating technique and identified using molecular methods. The yeast community of the White Sea intertidal zone consists of members that are typical for marine substrates, ubiquist species that are common in water and in low-temperature terrestrial environments, and a group of species that was isolated from marine substrates for the first time. The most diverse yeast communities formed on the surface of marine algae and in silt. Metschnikowia zobellii, which is a typical inhabitant of northern seas, was the most abundant yeast on algae from both biological stations. A new basidiomycetous yeast species, which was described in this work as Glaciozyma litorale sp. nov., dominated in the silt samples. The type strain of this new species is K94b^T (=KBP 4246^T = VKPM Y-3850^T = PYCC 6252^T = CBS 12957^T = DSM 28204^T); MycoBank registration number is MB 805475.