Barnacle larval supply to sheltered rocky shores: a limiting factor?

In northwest Europe, sheltered rocky shores are dominated by fucoid canopy algae and barnacles are rare, although the latter are extremely abundant on exposed shores. The supply of the intertidal barnacle Semibalanus balanoides (L.) to sheltered, fucoid dominated rocky shores was investigated to determine the importance of larval supply in limiting the abundance of adults in shelter. Larval supply was measured at two spatial scales, at the scale of shore (100s of metres), by comparing larval concentrations at exposed and sheltered sites, and at a smaller spatial scale (m), by examining the role of fucoid canopies in limiting supply to the substratum. Replicate plankton trawls were carried out above the intertidal zone at high water at two sheltered sites and nearby exposed headlands. The concentration of S. balanoides cyprid larvae was significantly higher at the sheltered sites on two out of three sampling occasions with up to 14 times greater larvae on one occasion than the nearby exposed site. The effect of the macroalgal canopy on supply to the substratum was assessed in two ways: directly, by pumping water from the substratum in areas with and without Ascophyllum nodosum (L.) Le Jolis, and indirectly by measuring cyprid settlement in a canopy-manipulation experiment. Pumped plankton samples from mid tide level showed that the A. nodosum canopy did not form a barrier to larval supply and may have had a positive effect on larval concentrations at the substratum. Cyprid settlement was assessed in the mid shore A. nodosum and low shore Fucus serratus L. zones to areas with canopy algae (but protected from the sweeping effects of macroalgal fronds) and without canopy. Settlement over three consecutive 24-h periods showed a consistent pattern; settlement was consistently lower beneath the F. serratus canopy than in cleared areas, suggesting that this algal species forms a barrier, limiting supply of cyprid larvae to the substratum.     

Effects of small-scale disturbances of canopy and grazing on intertidal assemblages on the Swedish west coast

The effects of small-scale disturbances (80×30-cm plots) of canopy and grazers on intertidal assemblages were investigated in this 4-year experiment on sheltered rocky shores on the Swedish west coast. Canopy disturbances due to ice scouring were mimicked by removal of adult plants of the seaweed Ascophyllum nodosum (L.) Le Joli. Density of the main epilithic grazing gastropods, Littorina spp., was lowered by exclosure and handpicking. Based on earlier experiments in other areas, the general hypothesis was that canopy removal and grazer exclosure, alone or in combination, should increase the recruitment of A. nodosum or other fucoid juveniles, and change the structure of the understorey assemblage.There was an effect of canopy removal on the development of this assemblage, lasting for more than 31 months. Both increased and decreased abundances of species were found as short-term effects, but there was also a longer-term effect with increased abundance. Grazer exclosure was only effective in combination with canopy removal, causing a short-term increase in ephemeral green algae. Short-term effects of canopy removal were also the increase in recruitment of Semibalanus balanoides (Linnaeus) and the decrease of the red alga Hildenbrandia rubra (Sommerfelt) Meneghini. Fast recruitment and growth of fucoid species (Fucus serratus L. and F. vesiculosus L.) restored the canopy and conditions of the understorey within 18 months. Thus, the canopy removal changed the physical conditions for the understorey, making it possible for other species to coexist in this community. Surprisingly, no effect of canopy removal or grazer exclusion was found on the recruitment of juvenile A. nodosum, neither by canopy removal nor grazer exclosure. The lack of such effects might be due to the early mortality caused by other grazers (small, mobile crustaceans), or to the low density of periwinkles on these shores. However, despite the patchy and generally low recruitment of A. nodosum juveniles, observations suggested that the cover of A. nodosum in manipulated patches would return to initial levels, either by recruitment or regrowth of small holdfasts and from growth of edge plants.     

Isolation and cross‐species amplification of microsatellite loci from the fucoid seaweeds Fucus vesiculosus,F. serratus and Ascophyllum nodosum (Heterokontophyta,Fucaceae)

The Fucaceae is a family of brown seaweeds that dominate and frequently co‐occur on North Atlantic rocky shores. We developed nine polymorphic microsatellite markers for the fucoid seaweeds Fucus vesiculosus, F. serratus and Ascophyllum nodosum using a combined, enriched library. Six of these loci were polymorphic in at least two species, showing from two to eight alleles with heterozygosities ranging from 0.41 to 0.85. Loci were also tested on F. spiralis, revealing five polymorphic microsatellite loci in this species.     

Factors controlling the lower limits of fucoid algae on the shore

Field and culture studies on fucoid alga of the upper shore showed that their lower limits of distribution were determined largely by interspecific competition. Pelvetia canaliculata (L.) Dcne. et Thur., which is strictly confined to the highest algal zone, grew much more slowly, both in culture and on the shore, than did Fucus spiralis L., which occupies the zone immediately below Pelvetia. When transplanted to the Fucus spiralis zone, macroscopic Pelvetia thalli grew normally, but Pelvetia zygotes which germinated within this zone reached macroscopic size only when competing Fucus spiralis was repeatedly removed.Both species required high light levels to grow in culture, yet their embryos remained viable for long periods in total darkness. Thus, Pelvetia cannot grow in the shade of Fucus spiralis, but actual removal of the Pelvetia germlings from the Fucus spiralis zone must be affected by some other factor.F. spiralis grew vigorously when transplanted to M.T.L., a level at which it is normally rare. In culture, its embryos grew more slowly than those of the species found lower on the shore such as F. vesiculosus L. and F. serratus L.; hence interspecific competition may again be involvedYoung Ascophyltum nodosum (L.) Le Jol. plants grew almost as slowly as those of Pelvetia, yet Ascophyllum dominates the middle shore. In culture it showed only slightly greater tolerance of low light intensity than other fucoids but, unlike Pelvetia, persisted and grew beneath a Fucus canopy in the field. The possibility that differences in life history and palatibility to grazing molluscs contribute to the disparate competitive abilities of Pelvetia and Ascophyllum is discussed.     

The early development of the cement apparatus in the barnacle, Balanus balanoides (L.) (Crustacea: Cirripedia)

The development of the cement cells of Balanus balanoides (L.) has been followed over a 26-day post-settlement period. Cells of the cyprid cement glands de-differentiate to form part of the juvenile barnacle apparatus, but the majority of juvenile cement cells develop by differentiation of collecting duct cells. These latter cement cells are recognized by apical invaginations which are continuous with the collecting duct lumen. Collecting ducts are present in the cyprid. The cement duct system was not studied in detail, but preliminary observations of the arrangement in B. balanoides and Elminius modestus Darwin have shown them to differ, the system in E. modestus being simpler.     

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     

Factors controlling the upper limits of fucoid algae on the shore

Year-round observations on the condition of intertidal seaweeds growing in situ on the shore, show that the upper limits of the zones characterized by Pelvetia canaliculata (L.) Done et Thur., Fucus spiralis L. and Ascophyllum nodosum (L.) Le Jol. were periodically pruned back by environmental conditions. The uppermost plants of each species showed clear signs of tissue damage 21 to 28 days after a time when drying conditions coincided with neap tides which exposed the plant to aerial conditions for long periods. High air temperatures aggravated the damage, but neither frost nor prolonged rain had any obvious adverse effects. On spring tides the plants were wetted every day and no damage resulted regardless of the weather.These species clearly all reach up to their physiological limits on the shore investigated, but presumably Fucus vesiculosus L. and F. serratus L. do not, for they were never observed to show signs of tissue damage attributable to exposure to air. Transplant experiments did, however, prove that F. serratus cannot survive in the F. spiralis zone and nor can F. spiralis persist in the Pelvetia canaliculata zone.Laboratory experiments also demonstrated that the ability to tolerate desiccation and then to resume photosynthesis and growth when re-submerged was greatest in P. canaliculata, the species found highest on the shore, and was progressively less in species inhabiting successively lower levels.     

Characterization of microsatellite loci in the marine seaweeds,Fucus serratus and F. evanescens (Heterokontophyta; Fucaceae)

Fucus serratus and F. evanescens commonly occur on Northern European shores. Nine microsatellite loci were developed for F. serratus (8–22 alleles, observed heterozygosities = 0.367–0.850) and one for F. evanescens (seven alleles, observed heterozygosity = 0.804). Cross‐amplification was apparent, as five F. serratus loci were polymorphic in F. evanescens and 2–5 were polymorphic in F. vesiculosus, F. distichus, and F. spiralis.     

Improvements to a passive trap for quantifying barnacle larval supply to semi-exposed rocky shores

Planktonic cyprid larvae of the intertidal barnacle, Semibalanus balanoides (L.) and the infralittoral/sublittoral Balanus crenatus Brug., are readily captured in small, chambered, passive traps deployed on rocky shores. Several structural developments of a previous trap design improved urea (killing solution) retention and capture of cyprids of both species. The design adopted for assessment of the larval supply/settlement relationship of the focal species, S. balanoides, included additional internal baffles and the replacement of the cylindrical trap opening with a coned aperture. Three sizes of cone aperture area were compared, with the intermediate size (1 cm²) being optimal for measuring larval supply over the full range of wave action on local shores. Most daily catches included larvae that were recognizable as having been dead before they were trapped, and had recently passed through the guts of grazing limpets (Patella vulgata L.). One site showed that ∼32% of trapped S. balanoides were so-called ‘faecal’ cyprids. An inability to distinguish these in trap samples would lead to a significant over-estimation of larval supply. Preliminary data indicated that S. balanoides larval supply to the intertidal is enhanced by onshore winds (or perhaps increased wave turbulence), whereas B. crenatus supply was positively correlated with offshore winds (or decreased turbulence). A clear ‘supply/settlement’ relationship for S. balanoides at six sites along ∼40 km of coastline was derived from 1 cm² coned trap catches and daily counts of settlement on ceramic tiles. There were no instances of disproportionately high settlement in relation to larval supply, but at five sites there were days when settlement apparently failed. The identification and explanation of settlement success and failure is fundamental to understanding the importance of larval supply in structuring marine benthic populations and communities.     

Divergent succession and implications for alternative states on rocky intertidal shores

It has been hypothesized that rockweed stands and mussel beds in sheltered bays in the Gulf of Maine, USA, are alternative community states. As a test of this hypothesis, experimental clearings of different sizes were established in stands of the rockweed Ascophyllum nodosum (L.) Le Jolis to determine if successional changes in large clearings developed species assemblages distinctly different from the surrounding A. nodosum stands. Clearings ranging from 1 to 8 m in diameter were created at 12 sites in 4 bays on Swan's Island, Maine, in 1996 to mimic the effects of ice scour, and abundances of gastropods, barnacles, mussels and fucoid algae were monitored until 2002. ANOVAs and MDS showed strong effects of clearing size and divergent successional changes in large clearings. Large clearings were quickly filled in and remained dominated by the alga Fucus vesiculosus L. and the barnacle Semibalanus balanoides (L). There was no evidence for site-specific effects, and Mantel tests showed clearing size was a better predictor of species composition than geographic distances among sites. Results suggest that large pulse disturbances using clearings of 8 m in diameter can initiate divergent successional pathways and have a protracted effect on species composition. Results are also consistent with the hypothesis that mussel beds and rockweed stands in sheltered bays may be alternative community states.     

Competitive ranks of three<Emphasis Type="Italic"> Fucus</Emphasis> spp. (Phaeophyta) in laboratory experiments—testing of Keddy's competitive hierarchy model

Keddy's competitive hierarchy model describes species distribution patterns along gradients under equilibrium conditions and can potentially serve as an explanation for zonation patterns of intertidal seaweeds on rocky shores. One of the assumptions of the model is a competitive hierarchy with the top competitor occupying the benign end of the gradient. Another assumption is the consistency of competitive ranks of species in all environmental conditions included in the shared parts of species' fundamental niches. In laboratory replacement series experiments, the competitive ranks of pairs of Fucus species that occupy adjacent zones in the field were analysed and compared to ranks found in previous field experiments. Unattached thalli of Fucus serratus versus F. vesiculosus or F. vesiculosus versus F. spiralis, respectively, were held in aerated beakers to establish the competitive ranking of the three congeners. Each replacement series was conducted at three total densities. F. vesiculosus was clearly competitively dominant over F. serratus. In competition with F. spiralis, F. vesiculosus was only dominant at its lowest absolute input frequencies, but at higher frequencies dominance was reversed. At high densities, the total ranking was F. spiralis > F. vesiculosus > F. serratus, which is the opposite order to that which would be expected from Keddy's model. Although all three species thrived well under the laboratory conditions, the results did not reflect in situ competitive dominances, which may be an effect of nutrient competition in the laboratory. Keddy's assumption that competitive ranks are consistent over the whole range of fundamental niches cannot be supported for Fucus spp. Communicated by K. Lüning     

Influence of oil shale on intertidal organisms: Effect of oil shale extract on settlement of the barnacle Balanus balanoides (L.)

As part of a study to investigate the effect of oil seeps on intertidal organisms, oil extracts of Blackstone oil shale from Kimmeridge on the Dorset coast were used in laboratory experiments to test their effect on the settlement of the barnacle Balanus balanoides (L.). Thin films of oil extract painted on the surface of pits in slate panels had no effect on cyprid settlement when applied up to a surface density of 2.8 g · m^?2, representing a thickness of 3.3 μm. Larger surface densities of oil stimulated cyprids to settle in far greater numbers than on unoiled panels. The maximum effect was obtained at a surface density of between 14.0 and 56.0 g · m ^?2, representing a thickness of 16.5 μm and 66.0 μm. With higher concentration of oil in the pits, stimulation to settle was reduced although cyprid settlement was still encouraged at a surface density of oil of 112g · m^?2 or 132 μm thickness.The unfractionated crude oil shale extract was a less powerful stimulus for barnacle settlement than a partially purified solution of the integumental protein arthropodin, another strong settlement inducer for barnacle cyprids.     

Modeling variation in interaction strength between barnacles and fucoids

The strength by which species interact can vary throughout their ontogeny, as environments vary in space and time, and with the density of their populations. Characterizing strengths of interaction in situ for even a small number of species is logistically difficult and may apply only to those conditions under which the estimates were derived. We sought to combine data from field experiments estimating interaction strength of life stages of the barnacle, Semibalanus balanoides, on germlings of Ascophyllum nodosum, with a model that explored the consequences of variability at per capita and per population levels to the abundance of year-old algal recruits. We further simulated how this interaction affected fucoid germling abundance as the timing of their respective settlements varied relative to one another, as occurs regionally across the Gulf of Maine, USA. Juvenile S. balanoides have a weak estimated per capita effect on germlings. Germling populations are sensitive to variation in per capita effects of juvenile barnacles because of the typically large population sizes of the latter. However, high mortality of juvenile barnacles weakens the population interaction strength over time. Adult barnacles probably weakly facilitate fucoid germlings, but greater survival of adults sustains the strength of that interaction at the population level. Germling abundance is positively associated with densities of adult barnacles and negatively associated with that of juvenile barnacles. Metamorphosing cyprid larvae have the strongest per capita effect on germling abundance, but the interaction between the two stages is so short-lived that germling abundance is altered little. Variation in the timing of barnacle and A. nodosum settlement relative to one another had very little influence on the abundance of yearling germlings. Interactions between barnacles and germlings may influence the demographic structure of A. nodosum populations and the persistence of fucoid-dominated communities on sheltered rocky shores in New England. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Book review

Fucoid macroalgae are important primary producers and habitat modifiers on North Atlantic intertidal rocky shores. With decreasing latitude, western European fucoid populations display reduced levels of abundance, biomass and recruitment, while experiencing higher levels of physical environmental stress during summer months. We hypothesized that such reduction in the south is accompanied by a detectable decline in fucoid reproductive capacity. To test this hypothesis, morphological and reproductive traits of core (Welsh) and marginal (Portuguese) populations of two common fucoid species, Fucus vesiculosus and F. spiralis (Ochrophyta, Fucales), were examined. Morphological measurements showed that for a given thallus length, both fucoid species had smaller thallus volume and lower biomass in the southerly marginal part of the range. Significantly lower biomass of reproductive tissue of F. vesiculosus and a smaller number of receptacles per individual on specimens of both species indicate that levels of reproductive output are probably lower in southern populations. Despite the differences in reproductive traits observed between regions, reproductive effort (measured as the percentage of total dry biomass represented by reproductive tissue) of both species remained similar, as algae from both regions made similar investments in reproduction. The results indicate that stressful conditions reduced growth and number of receptacles of both species and amount of reproductive biomass of F. vesiculosus in the south but do not seem to change the way these algal species invest their energy. The decline in mass and reproductive biomass of specimens from southern shores found in this study, when combined with the lower abundance of adults and lower recruitment levels previously observed, is a strong indication of fucoid populations with lower levels of propagule output. This is an important factor when considering responses of these populations to a changing environment.     

Adventitious Bud Formation from Bulb-scale Explants of Lilium speciosum Thunb. in vitro Effects of aminoethoxyvinyl-glycine, 1-aminocyclopropane-1-carboxylic acid,and ethylene

Several representatives of marine brown macroalgae (Phaeophyceae) including Fucus serratus L., Fucus spiralis L. and Fucus vesiculosus L. as well as Laminaria digitata (Huds.) Lamour., Laminaria hyperborea (Gunn.) Foslie and Laminaria saccharina (L.) Lamour. were investigated with particular regard to features of biosynthesis of the storage product mannitol. The respective catalytic system involved in the last step of mannitol formation, mannitol-1-phosphate dehydrogenase, appears to be a cytoplasmic enzyme as may be judged from the degree of correlation with the chloroplast key enzyme ribulose-1,5-bisphosphate carboxylase in different tissues of Laminaria digitata and Laminaria saccharina. Activity of mannitol-1-phosphate dehydrogenase in vitro is not affected by mannitol-l-phosphate or free mannitol, suggesting that mannitol biosynthesis in vivo) is mainly controlled by the environment and/or developmental stage. Certain inorganic ions such as NO₃^- (including K⁺) exert a strong influence on the activity of mannitol1-phosphate dehydrogenase thus suggesting that the intracellular pools of stored NO₃^- and mannitol are confined to spatially separated cellular compartments.     

Characterization of microsatellite loci in the marine seaweed Ascophyllum nodosum (Phaeophyceae; Fucales)

Ascophyllum nodosum L. dominates rocky intertidal shores throughout the temperate North Atlantic. Six microsatellite loci were developed for A. nodosum using enriched libraries. The number of alleles ranged from 9 to 24 and heterozygosities from 0.2213 to 0.7785. Ascophyllum is monotypic. There was no cross‐reactivity observed with Fucus serratus, F. vesiculosus or F. evanescens.     

PROTEINS IMMUNOLOGICALLY RELATED TO DEHYDRINS IN FUCOID ALGAE

Adult fucoid algae on Atlantic shores have well-characterized, species-specific tolerances to the varying levels of desiccation that occur from the low to high intertidal zones; however, less is known about embryonic tolerances and their mechanistic basis. We investigated this by 1) exposing embryos of Fucus evanescens C. Agardh, F. spiralis L., and F. vesiculosus L. from the Maine shore to osmotic desiccation in hypersaline seawater and 2) examining whether these embryos contain species-specific dehydrins, proteins first identified in higher plants that are hypothesized to confer tolerance to dehydration. Embryonic survival when cultured in hypersaline seawater >100 practical salinity units (psu) correlated with the position of these species in the intertidal zone (F. spiralis > F. vesiculosus > F. evanescens), but all 1-day-old embryos of these species tolerated treatment with 100 psu or lower seawater. Proteins (17–105 kDa) immunologically related to dehydrins were detected on western blots with dehydrin antibodies raised against a synthetic peptide representing the conserved motif of dehydrins in higher plants. These proteins were constitutive and unstable when subjected to prolonged (>15 min) temperatures above 55° C, unlike most higher plant dehydrins, which are inducible and remain soluble at 75°–100° C. The presence of these proteins was species- and stage-specific. Sperm of F. vesiculosus had a characteristic protein of 76 kDa, whereas eggs and embryos (6 h to 3 days old) had a 92-kDa protein. By 1 week of age, expression of the 92-kDa protein decreased, and the 35-kDa protein of adults was present. Embryos of A. nodosum L. and Pelvetia compressa J. Agardh DeToni contained an 85-kDa protein rather than the 92-kDa protein of Fucus embryos (F. distichus L., F. evanescens, F. spiralis, and F. vesiculosus). The 92-kDa protein became more abundant in embryos exposed to hyperosmotic seawater at 50 psu (F. evanescens and F. vesiculosus) or 150 psu (F. spiralis); however, dehydrin-like proteins of some molecular masses decreased in abundance simultaneously. Further characterization of these proteins is required to establish whether they protect embryos against intertidal desiccation.     

Competitive interactions between Fucus spiralis L. and F. vesiculosus L. (Fucales,Phaeophyta)

Fucus spiralis forms a conspicuous belt in the upper intertidal on rocky shores of the NW Atlantic. The objective of this study was to determine whether competition among congeners plays a role in restricting the distribution of F. spiralis to the upper shore. A replacement series design was used to test the growth performance of F. spiralis and F. vesiculosus in monocultures and in mixtures set up in the mid shore level on an exposed rocky coast. For F. spiralis and F. vesiculosus, all individual and relative crowding coefficients were < 1 and > 1, respectively. Hence, F. vesiculosus succeeded relative to F. spiralis in all mixtures tested. This finding was confirmed by graphical analysis. Ratio diagrams showed that the outcome of long term interaction among the species is extinction of F. spiralis. The results lead to the conclusion that interaction among congeners is a major determinant of the restricted distribution of F. spiralis.     

The effect of zinc on the increase in length of five species of intertidal fucales

The growth rate of Pelvetia canaliculata (L.) Dec. et Thur., Fucus spiralis L., F. vesiculosus L., F. serratus L., and Ascophyllum nodosum (L.) Le Jolis was measured in six different concentrations of zinc (0.025–14 mg/l) during a period of ten days. No significant growth response was observed at 0.1 mg/l of zinc. A significant reduction of growth during the first two to three days of exposure to 1.4 mg/l or more was followed by no or small further decline. Apices of A. nodosum from localities with different background load of zinc (0.1–0.5 mg/l and <0.01 mg/l) showed no difference in response to 2.6 mg/l of zinc.     

Effects ofFucus vesiculosus covering intertidal mussel beds in the Wadden Sea

The brown algaFucus vesiculosus formamytili (Nienburg) Nienhuis covered about 70% of mussel bed (Mytilus edulis) surface area in the lower intertidal zone of Königshafen, a sheltered sandy bay near the island of Sylt in the North Sea. Mean biomass in dense patches was 584 g ash-free dry weight m^?2 in summer. On experimental mussel beds, fucoid cover enhanced mud accumulation and decreased mussel density. The position of mussels underneath algal canopy was mainly endobenthic (87% of mussels with >1/3 of shell sunk into mud). In the absence of fucoids, mussels generated epibenthic garlands (81% of mussels with <1/3 of shell buried in mud). Mussel density underneath fucoid cover was 40 to 73% of mussel density without algae. On natural beds, barnacles (Balanidae), periwinkles (Littorina littorea) and crabs (particularly juveniles ofCarcinus maenas) were significantly less abundant in the presence of fucoids, presumably because most of the mussels were covered with sediment, whereas in the absence of fucoids, epibenthic mussel clumps provided substratum as well as interstitial hiding places. The endobenthic macrofauna showed little difference between covered and uncovered mussel beds. On the other hand, grazing herbivores — the flat periwinkleLittorina mariae, the isopodJaera albifrons and the amphipodsGammarus spp. — were more abundant at equivalent sites with fucoid cover. The patchy growth ofFucus vesiculosus on mussel beds in the intertidal Wadden Sea affects mussels and their epibionts negatively, but supports various herbivores and increases overall benthic diversity.