Direct and indirect effects of Littorina littorea (L.) on barnacles growing on mussel beds in the Wadden Sea

On the extensive sedimentary tidal flats of the Wadden Sea, beds of the blue mussel Mytilus edulis represent the only major hard substratum and attachment surface for sessile organisms. On this substratum, the barnacle Semibalanus balanoides is the most frequent epibiont. In summer 1998, it occurred on over 90% of the large mussels (>45 mm shell length) and the dry weight of barnacles reached 65% of mussel dry weight. However, the extent of barnacle overgrowth is not constant and differs widely between years. Periwinkles (Littorina littorea) may reach densities >2000 m^–2 on intertidal mussel beds. Field experiments were conducted to test the effect of periwinkle grazing on barnacle densities. An experimental reduction of grazing and bulldozing pressure by periwinkles resulted in increased recruitment of barnacles, while barnacle numbers decreased with increasing snail density. The highest numbers of barnacles survived in the absence of L. littorea. However, a lack of periwinkle grazing activity also facilitated settlement of ephemeral algae which settled later in the year. Field experiments showed that the growth rate of barnacles decreased in the presence of these ephemeral algae. Thus, L. littorea may reduce initial barnacle settlement, but later may indirectly increase barnacle growth rate by reducing ephemeral algae. It is suggested that periwinkle density may be a key factor in the population dynamics of S. balanoides on intertidal mussel beds in the Wadden Sea.     

Effect of barnacle fouling on ship resistance and powering

Predictions of added resistance and the effective power of ships were made for varying barnacle fouling conditions. A series of towing tests was carried out using flat plates covered with artificial barnacles. The tests were designed to allow the examination of the effects of barnacle height and percentage coverage on the resistance and effective power of ships. The drag coefficients and roughness function values were evaluated for the flat plates. The roughness effects of the fouling conditions on the ships’ frictional resistances were predicted. Added resistance diagrams were then plotted using these predictions, and powering penalties for these ships were calculated using the diagrams generated. The results indicate that the effect of barnacle size is significant, since a 10% coverage of barnacles each 5 mm in height caused a similar level of added power requirements to a 50% coverage of barnacles each 1.25 mm in height.     

Characterisation of the bacteria associated with barnacle,Balanus amphitrite,shell and their role in gregarious settlement of cypris larvae

The acorn barnacle Balanus amphitrite (syn. Amphibalanus amphitrite) is a model organism to investigate pelago-benthic transitions in marine invertebrates. A driver for larval settlement in this organism is the need to attach close to conspecifics, to allow reproduction to take place. Adult barnacles are covered by microbial biofilms and the contribution of these biofilms to conspecific recognition is not fully understood. Little information is available on microbial communities associated with B. amphitrite. We compared biofilm communities from the barnacle shell surface with those from the surrounding rocks using the culture-independent methods of quantitative PCR and denaturing gradient gel electrophoresis. Quantification of the relative abundances of higher bacterial taxa showed that barnacles hosted a greater proportion of α-Proteobacteria compared to rock-associated biofilms (p < 0.01). Differences in relative abundances of other taxa were not observed but DGGE profiling suggested that differences were present at lower taxonomic levels. The capacity of these communities to influence larval settlement was assessed by growing multispecies biofilms on artificial medium, obtained by extracting nutrients from adult barnacles. Biofilms composed of shell-associated bacteria were capable of promoting conspecific settlement by 67% compared to control surfaces (p < 0.05), while rock-associated communities showed contrasting effects. A taxonomic comparison of settlement-stimulating and -inhibiting bacteria was performed by DGGE and band sequencing. All partial 16S rRNA genes sequenced were similar to members of the Vibrio and Pseudoalteromonas genera, suggesting that larvae can detect and respond to variations in the composition of microbial biofilms at low taxonomic levels. Our results indicate that barnacle larvae may be able to detect parentally-associated biofilms and use this information to settle close to members of its own species.     

Desiccation,predation, and mussel-barnacle interactions in the northern Gulf of California

Summary Field experiments were conducted in order to determine the potential for desiccation and predation to mediate the effect of mussels (Brachidontes semilaevis) on barnacles (Chthamalus anisopoma) in the highly seasonal northern Gulf of California. We did this by removing both mussels and a common mussel predator (Morula ferruginosa: Gastropoda) and by spraying selected sites with sea water during summertime spring low tides. We also determined the effect of crowding on resistance to desiccation in barnacles, and the effect of barnacles on colonization by mussels. The mussel-barnacle community was not affected by keeping experimental quadrats damp during daytime low tides throughout the summer. Exposure to summertime low tides, however, did affect the survivorship of isolated, but not crowded, barnacles; and barnacle clumps enhanced the recruitment of mussels. Hence crowding in barnacles had a positive effect on both barnacle survivorship and mussel recruitment. Morula had a negative effect on mussel density, and mussels had a negative effect on barnacle density. The effect of Morula on barnacle density was positive, presumably due to its selective removal of mussels. These results suggest an indirect mutualism between barnacles and the gastropod predator, because barnacles attract settlement or enhance the survival of mussels, and the predator reduces the competitive effect of mussels on barnacles.     

Settlement Dynamics of the Encrusting Epibenthic Macrofauna in Two Creeks of the Caeté Mangrove Estuary (North Brazil)

The epibenthic encrusting fauna of 2 creeks of the Caeté mangrove estuary, northern Brazil, was studied over a 13 month period using collectors fixed at 2.5 and 3.5 m above the creek bottom and in which upper and lower sides of ceramic and wooden panels were used as settlement substrates. The number of individuals of the most abundant organisms (barnacles, oysters and mussels) settling per panel was determined each month, for each substrate type, panel orientation and height above creek bottom. The barnacle, Fistulobalanus citerosum has a peak settlement period during the wet season whereas both peaks in the numbers of settlers of the oyster Crassostrea rhizophorae were recorded during the dry season and such discrete temporal patterns in settlement have also been observed for barnacles and oysters in other mangroves and estuaries. In contrast to other studies, settlement of the mussel Mytella falcata was generally low during the study period and may be related to over-exploitation of stocks in the region. Overall, settler density was usually greater on the underside of ceramic panels close to the creek bottom, similar to results of other studies of epibenthic settlement in diverse habitats.     

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.     

Species specificity of barnacle settlement-inducing proteins

We previously isolated a larval settlement-inducing protein complex (SIPC) from adult extracts of the barnacle, Balanus amphitrite using a nitrocellulose membrane settlement assay. In the present study, we found that the extracts of other adult barnacles, Megabalanus rosa and Balanus eburneus, also induced the settlement of B. amphitrite cyprids although the inductive activity was slightly lower than that of conspecific extracts. Furthermore, we examined reactivity to anti-SIPC antibody in adult extracts from six species of Japanese barnacles other than B. amphitrite, brine shrimp and eight marine sessile organisms besides barnacles. The results showed that all barnacles examined contained SIPC-like proteins with slightly different molecular weight, while the other animals did not react to the antibody by immunoblot analysis. These findings suggest that species specificity in settlement-inducing proteins of barnacles is not so strict, but these proteins are characteristic to barnacle species.     

Larval influx of Diadema antillarum to the Florida Keys linked to passage of a Tortugas Eddy

Lack of recovery of the sea urchin Diadema antillarum in the Caribbean region following a widespread epizootic in 1983–1984 has garnered great interest due to the role of this species as a grazer of macroalgae that exclude reef-building corals. In the Florida Keys, USA, previous research suggests that reestablishment of D. antillarum is limited by low fertilization success and a lack of larval supply. However, the physical mechanisms determining larval supply in the Florida Keys remain poorly resolved. Here, we use coupled biological and physical oceanographic datasets of D. antillarum larval supply to settlement collectors, sea surface temperatures and heights, and the Okubo Weiss parameter to examine a link between influx of larvae to the middle Florida Keys and Tortugas Eddy activity in the Straits of Florida. The greatest magnitude of settlement over 3 months of measurements occurred from late May to late June 2015, coinciding with the passage and dissociation of a Tortugas Eddy. Settlement occurred on collectors only at offshore bank-barrier reef sites, consistent with a temperature signal of a passing eddy at these sites. No D. antillarum were observed by divers at sites 1 yr following settlement on the collectors. The results indicate that despite the lack of population recovery, D. antillarum larval influx can occur during intermittent oceanographic events.

     

Factors influencing initial larval settlement: temporal, spatial and surface molecular components

The impact of initial surface chemistry on settlement of barnacle, bryozoan, and hydroid larvae was assessed. Temporal (on a scale of weeks to months) and fine scale spatial (centimeter to meter) variation in settlement were quantified. Four arrays of silanized glass surfaces, deployed at ≈2-wk intervals, were monitored after 1 and 3 days of immersion. Settlement of all larval types exhibited strong temporal variation. There was a 25, 22- and 18-fold difference between the highest and lowest Day 1 settlement for barnacles, bryozoans and hydroids, respectively. Bryozoan and hydroid settlement was spatially variable, barnacle settlement was not. Barnacle and bryozoan settlement was influenced by inttial surface chemistry, hydroid settlement was not. For barnacles, there was a 2-fold difference between total settlement over the four arrays on untreated glass and diphenyl-silanized surfaces; for bryozoans, there was a 51-fold difference, and in the opposite direction. There was a negative correlation between barnacle and bryozoan settlement with respect to surface. This result was independent of the presence of the other species. Bryozoan settlement was also spatially and temporally quantified in a separate, single surface 56-h array, and total bryozoan settlement ·h⁻¹ was found to be correlated with light intensity. Patterns of initial colonization were strongly influenced by surface chemistry and spatial temporal variation in larval supply. These effects on initial colonization may influence subsequent community development.     

Assessment of current rates of Diadema antillarum larval settlement

The generally slow and incomplete recovery of the long-spined sea urchin, Diadema antillarum, from the 1983–84 Caribbean-wide die-off, particularly in the Florida Keys, USA, raises the question of factors limiting population recovery. This study sought to quantify larval settlement rates as an indicator of larval supply at two sites in the Florida Keys, utilizing methods comparable to an historic study. Settlement at two sites in southwest Puerto Rico was also examined as a comparison of present-day settlement rates at a site where D. antillarum recovery has been moderate. Monthly settlement rates were low (max < 2 m⁻²) and did not differ between the two sites examined in the Florida Keys. Settlement was significantly higher at only one of the Puerto Rico sites (max 16 m⁻²), but still an order of magnitude lower than that reported for historic populations in Cura?ao (1982–83). Results are consistent with the hypothesis of low larval supply limiting D. antillarum recovery in the Florida Keys.     

Early development and neurogenesis of Temnopleurus reevesii

Sea urchins are model non‐chordate deuterostomes, and studying the nervous system of their embryos can aid in the understanding of the universal mechanisms of neurogenesis. However, despite the long history of sea urchin embryology research, the molecular mechanisms of their neurogenesis have not been well investigated, in part because neurons appear relatively late during embryogenesis. In this study, we used the species Temnopleurus reevesii as a new sea urchin model and investigated the detail of its development and neurogenesis during early embryogenesis. We found that the embryos of T. reevesii were tolerant of high temperatures and could be cultured successfully at 15–30°C during early embryogenesis. At 30°C, the embryos developed rapidly enough that the neurons appeared at just after 24 h. This is faster than the development of other model urchins, such as Hemicentrotus pulcherrimus or Strongylocentrotus purpuratus. In addition, the body of the embryo was highly transparent, allowing the details of the neural network to be easily captured by ordinary epifluorescent and confocal microscopy without any additional treatments. Because of its rapid development and high transparency during embryogenesis, T. reevesii may be a suitable sea urchin model for studying neurogenesis. Moreover, the males and females are easily distinguishable, and the style of early cleavages is intriguingly unusual, suggesting that this sea urchin might be a good candidate for addressing not only neurology but also cell and developmental biology.     

Inhibition of larval barnacle attachment to bacterial films: An investigation of physical properties

The effects of films of two strains of a marine bacterium, Deleya marina (ATCC 25374 and 27129) on the attachment response of cypris larvae of the balanomorph barnacle, Balanus amphitrite, were examined in the laboratory. Tests showed that the cell-surface hydrophobicities of the two bacteria in suspension were different. In contrast, films derived from these cells were both highly wettable (i.e., displayed high surface free energy). Assays (22 hours) compared permanent attachment of larval barnacles to films derived from exponential and stationary phase cells for both bacteria. These films either had no effect or inhibited attachment of both 0-day- and 4-day-old cypris larvae when compared with unfilmed controls. Our data indicate that inhibition of larval barnacle attachment by films of the two bacteria is the result of factors other than surface free energy. Production of chemical barnacle settlement inhibitors by the bacteria is hypothesized.Offprint requests to: J. S. Maki.     

Experiments on orientation of the intertidal barnacle Tesseropora rosea (Krauss)

The intertidal barnacle Tesseropora rosea (Krauss) exhibits very marked directionality of orientation on sloping and vertical surfaces. The barnacles are orientated so that their cirral fans face the water current; this pattern was found within 1 wk after settlement. Adults also showed similar orientation to the water current at each site.Three manipulative experiments were done in the field to determine the consequences of incorrect orientation by the barnacles. Correct orientation was necessary for T. rosea to maintain its tissue weight, but experimental rotation of barnacles through 90° or 180° made no difference to rates of shell growth, mortality or weight of egg masses. Furthermore, this species was unable to re-orientate once it had metamorphosed, and orientation of newly-settled barnacles was not influenced by that of adults.     

Settlement in different-sized patches by the gregarious intertidal barnacle Chamaesipho tasmanica Foster and Anderson in New South Wales

Most models on settlement of open marine invertebrate populations are based on space-limitation. These models, however, do not recognise that free space may not drive the demography of populations when larval numbers are small or when larval supply varies along a gradient in the habitat. They also do not incorporate the effects of larval choice when settling. It has been hypothesised that, in gregarious barnacles, the effects of adult conspecifics, rather than available free space, may play a primary role in settlement. That is, cues from adults along perimeters of patches, rather than space available, may enhance colonisation. This study therefore aimed to distinguish between these separate influences on populations of Chamaesipho tasmanica, a gregarious barnacle characterised by relatively few larvae arriving to settle each year. Patches of 6, 3 and 1.5 cm diameter were cleared within aggregations of barnacles at three heights (Low, Mid, Upper) of Chamaesipho's distribution at two sites and during 2 years of settlement. Total numbers of settlers in each year were manipulated to determine the separate influences on settlement due to availability of substratum or the effects of conspecific adults. To test for the effects of available free space, numbers of settlers per unit area were analysed. To test for gregarious effects due to the presence of adults, numbers of settlers per unit perimeter were analysed. While available substratum was found not to affect settlement of this barnacle, gregarious settlement in response to adults at perimeters of patches was thought to be confounded by differential larval supply and differential conspecific cues among heights on the shore. Results from this study therefore have important implications for survival of gregarious populations following disturbances, especially in species where larval supply is poor.     

Development of nervous systems to metamorphosis in feeding and non-feeding echinoid larvae,the transition from bilateral to radial symmetry

The development of nervous system (NS) in the non-feeding vestibula larva of the sea urchin, Holopneustes purpurescens, and the feeding echinopluteus larva of Hemicentrotus pulcherrimus was examined by focusing on fate during metamorphosis. In H. purpurescens, the serotonergic NS (SerNS) appeared simultaneously and independently in larval tissue and adult rudiment, respectively, from 3-day post-fertilization. In 4-day vestibulae, an expansive aboral ganglion (450 × 100 μm) was present in the larval mid region that extended axons toward the oral ectoderm. These axons diverged near the base of the primary podia. An axonal bundle connected with the primary podia and the rim of vestopore on the oral side. Thus, the SerNS of the larva innervated the rudiment at early stage of development of the primary podia. This innervation was short-lived, and immediately before metamorphosis, it disappeared from the larval and adult tissue domains, whereas non-SerNS marked by synaptotagmin remained. The NS of 1-month post-fertilization plutei of H. pulcherrimus comprised an apical ganglion (50 × 17 μm) and axons that extended to the ciliary bands and the adult rudiment (AR). A major basal nerve of serotonergic and non-serotonergic axons and a minor non-serotonergic nerve comprised the ciliary band nerve. In 3-month plutei, axonal connection among the primary podia in the neural folds completed. The SerNS never developed in the AR. Thus, there was distinctive difference between feeding- and non-feeding larvae of the above sea urchins with respect to SerNS and the AR.     

Early events in sea urchin metamorphosis,description and analysis

The larval epithelium of the sea urchin, Lytechinus pictus, consists of squamous cells and bands of columnar epithelial cells bearing cilia. During metamorphosis this tissue undergoes a series of rapid, complex changes. Through the scanning and transmission electron microscope, we describe and analyse these changes. The changes can be divided into three steps. (1) The larval arms bend away from the left side of the larva, exposing the urchin rudiment. Cells which are identical to smooth muscle cells are in a position to bring about this bending. (2) The squamous epithelial cells assume a cuboidal shape. This change in shape results in the collapse of the larval epithelium onto the presumptive aboral surface. These cells possess a subapical band of microfilaments. The cellular shape change but not the bending of the arms is reversibly inhibited by Cytochalasin B. These observations suggest a mechanism for this change. (3) The former lining of the vestibule of the urchin rudiment comes to lie over the collapsed larval tissue and forms the adult epithelium. At this point, after only one hour, the larva has assumed the external shape of an adult sea urchin.     

Induction of Settlement and Metamorphosis of the Veliger Larvae of the Nudibranch,Onchidoris bilamellata

Summary

Onchidoris bilamellata veligers were reared in the laboratory on a combination of phytoñagellates and diatoms. They attained metamorphic competence after a period of 28 to 32 days at 11°C, or 60 to 80 days at a temperature averaging 7.5° C.

Experimental evidence suggests that settlement is stimulated by a diffusible chemical emanating from living barnacles, whereas metamorphosis is induced by a chemical or mechanochemical cue, which is also associated with barnacles. Settlement and metamorphosis are considered to be separable events in O. bilamellata. The settlement response is reversible and can be repeated; it involves a characteristic behavioral repertoire including descent to the bottom, foot contortions and crawling on the pedal sole. Settlement occurs only in seawater that contains, or had previously contained, living barnacles. Metamorphosis is irreversible and involves the resorption of the velum, loss of the larval shell, and incorporation of the visceral mass into the cephalopedal mass. Metamorphosis is triggered only when physical contact with living or dead barnacles is made (dead barnacles refers to shell and tissue fragments which are only effective in inducing metamorphosis when they are used in combination with seawater that had previously contained living barnacles).

Settlement and metamorphosis in O. bilamellata is compared with that of other nudibranch species, and its unique settlement response is discussed.     

Variation in barnacle recruitment over small scales: larval predation by adults and maintenance of community pattern

Over small spatial scales, variation in the density of settlers of benthic sessile species is the result of interactions among larval behavior, local hydrodynamic conditions, and the physical, chemical and biological characteristics of the benthic habitat. It has been shown repeatedly that adult benthic filter-feeders can consume larvae of their own and other species, but their effects on the distribution and abundance of recruits have rarely been demonstrated under natural conditions in the field, particularly on hard substrata. Here we experimentally quantified the effect of the large intertidal barnacle, Semibalanus cariosus (Pallas), on the density of recruits of three common barnacle species. The experiments were conducted at the peak of the barnacle recruitment season over three successive years, on the west coast of San Juan Island, Washington. A persistent and well documented community pattern in the mid intertidal zone of the study site is a sparse bed of adult S. cariosus with bare rock spaces essentially devoid of small barnacles among the large individuals. Field experiments consisted of small areas from which either all adult S. cariosus were killed leaving the shells attached to the rock, or live adult barnacles were left intact. Our results showed that over small spatial scales of a few to tens of centimeters, the large barnacle S. cariosus can interfere and significantly reduce net settlement and recruitment of conspecific as well as other barnacle species. Between 65 and 100% reduction in settlement could be attributed to larval predation by adults, as implied by barnacle settlement patterns on different treatments and by the presence of nauplius larvae in cirri and stomach contents of S. cariosus. The negative effect on barnacle settlement was consistent between years of relatively low barnacle recruitment, which appears to be the most common situation at the study site, but it disappeared on a year of unusually high recruitment, when settling larvae seem to have swamped the filtration ability of adult S. cariosus. The different barnacle species displayed contrasting settlement patterns on bare rock and on the lateral shells of the large barnacles, which appear to be a result of differences in larval behavior. Comparisons against the relative availability of these substrata in the experimental plots suggested that larvae of different species sample the benthic microhabitat in very different ways.     

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