Introduction to the symposium--barnacle biology: essential aspects and contemporary approaches

Barnacles have evolved a number of specialized features peculiar for crustaceans: they produce a calcified, external shell; they exhibit sexual strategies involving dioecy and androdioecy; and some have become internal parasites of other Crustacea. The thoroughly sessile habit of adults also belies the highly mobile and complex nature of their larval stages. Given these and other remarkable innovations in their natural history, it is perhaps not surprising that barnacles present a spectrum of opportunities for study. This symposium integrates research on barnacles in the areas of larval biology, biofouling, reproduction, biogeography, speciation, population genetics, ecological genomics, and phylogenetics. Pioneering comparisons are presented of metamorphosis among barnacles from three major lineages. Biofouling is investigated from the perspectives of biochemical and biomechanical mechanisms. Tradeoffs in reproductive specializations are scrutinized through theoretical modeling and empirical validation. Patterns of endemism and diversity are delineated in Australia and intricate species boundaries in the genus Chthamalus are elucidated for the Indo-Pacific. General methodological concerns with population expansion studies in crustaceans are highlighted using barnacle models. Data from the first, draft barnacle genome are employed to examine location-specific selection. Lastly, barnacle evolution is framed in a deep phylogenetic context and hypothetical origins of defined characters are outlined and tested.     

Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms

Trait-mediated indirect effects (TMIs) are changes in the density of one species that are caused by induced changes in one or more traits of an intervening species. For example, induced defense in a prey species may alter the nature of indirect effects that are mediated through that prey species. In the present study, we investigated the TMIs that stem from an interaction between a carnivorous whelk ( Acanthina angelica ) and an intertidal barnacle ( Chthamalus anisopoma) . Depending on the timing of the interaction, the predator either kills the barnacle or induces a predation-resistant morph. Based on previous work that addressed the direct interactions between Chthamalus and other species in the community we predicted and subsequently found that community structure varies as a function of these differing effects. Specifically, we found that Acanthina has a positive indirect effect on mussels when it interacts with (kills) undefended adult barnacles. In contrast, the predator has a positive indirect effect on an encrusting algae ( Ralfsia ) when it comes into contact with juvenile barnacles, causing the induction of the predator-resistant morph. We suggest that further research should consider the role of environmentally induced polymorphisms in structuring communities.     

The distribution and molecular diversity of the Eastern Atlantic and Mediterranean chthamalids (Crustacea, Cirripedia)

The three chthamalids Chthamalus stellatus , C. montagui and Euraphia depressa are common inhabitants of the intertidal zone in the Eastern Atlantic, Mediterranean Sea and Black Sea. In this study, we investigated the occurrence of these barnacles in a wide range of their distribution. Population divergences of these two species have been inferred using three molecular markers — internal transcribed spacer (ITS), elongation factor 1α (EF-1α) and cytochrome oxidase subunit I (COI). ITS sequences of C. stellatus were identical throughout the species range, whereas ITS sequences of C. montagui indicated that the Black Sea and Mediterranean populations are isolated from the Atlantic population. The COI and EF-1α sequences were the most variable and informative. They indicated a high genetic divergence between Atlantic, Mediterranean and Black Sea populations for C. montagui . In addition significant genetic structure was found among the populations of C. stellatus based on EF-1α but not COI. Interestingly, our molecular dating analysis correlated the pattern of diversification in C. montagui to major geological changes that occurred in the Mediterranean during the end of the Messinian and Pleiocene periods. We suggest that palaeohistory shaped the divergences between Chthamalus populations that have probably been maintained by current hydrographic conditions. Finally, COI phylogenetic analysis placed the genus Euraphia within the Chthamalus clade, suggesting the need for a taxonomic revision of Euraphia . This study represents the most detailed phylogeographical analysis of intertidal Mediterranean species to date, and shows that geological events have strongly shaped the current diversity pattern of this fauna.     

The natural history, thermal physiology, and ecological impacts of intertidal mesopredators, Oedoparena spp. (Diptera: Dryomyzidae)

Abstract. The ecological roles of small (1–1000 mg) predators in benthic marine systems are poorly understood. We investigated the natural history and predatory impact of one group of such mesopredators—larvae of dipteran flies in the genus Oedoparena —which prey on intertidal barnacles. We 1) quantified patterns of larval Oedoparena distribution and abundance in the Northwest Straits of Washington State, USA, 2) determined larval physiological tolerance limits in the laboratory, and 3) conducted a manipulative field experiment to assess the role of microhabitat temperature on predation rates in Oedoparena . Members of Oedoparena in Washington are univoltine, with peak larval abundance in late spring and early summer. Infestation frequencies in the barnacles Balanus glandula and Chthamalus dalli were as high as 22% and 35%, respectively. In laboratory studies, larvae of O . glauca were able to tolerate temperatures up to 37°C; however, this temperature is often exceeded in high intertidal habitats. In a field manipulation using experimental shades, we demonstrate that the alleviation of physiological stress greatly increased the abundance of larvae of Oedoparena spp. As a result of increased larval densities under shades, adult B. glandula mortality increased from 5% to nearly 30%, and C. dalli mortality increased from less than 20% to over 60%. Because high intertidal barnacles serve as food and habitat for a diverse array of species, Oedoparena spp. have the potential to play a major role in structuring high intertidal communities, particularly in cooler microhabitats.     

A new look at variation in Darwin's species of acorn barnacles

Darwin's studies on barnacles, begun to satisfy his curiosity about specimens from the Beagle , but later extended to the large collections of other naturalists, lasted for 8 years and produced a set of definitive monographs. Darwin was particularly troubled over the taxonomy of two groups of acorn barnacles, Balanus tintinnabulum and B. amphitrite , which he ultimately classified as clusters of wellmarked varieties. Recent studies, based on established taxonomic methods or on statistical treatment of morphometric data, suggest these are clusters of full species and that the 'intermediate' forms are just phenotypic variants. Darwin was also troubled by the small chthamalid intertidal barnacles, which he eventually grouped as varieties of a world-wide species, Chthamalus stellatur. Gel electrophoresis and morphometrics now show this to be a heterogenous assemblage of distinct species, some very different, others closer together, all with restricted geographical range, but all showing extreme variability in the characters normally used for classification.
Darwin's difficulties with the classification of the highly varying barnacles, and his anatomical studies on these peculiar animals, must have had considerable influence on the development of his theories about natural selection, more than is usually acknowledged by writers on evolution. These 'lost years' were in fact a period of intense zoological enquiry, and Darwin's change in attitude with regard to species and variation in nature underwent a big change, as can be seen from the letters and from the differences between the early drafts written before the barnacle work and the later Natural Selection and The Origin. Whether we regard the difficult groups of Balanus as clusters of species or clusters of varieties, they still draw attention to evolutionary processes as in Darwin's day.     

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.     

Boschmaella japonica,New Species,a Parasite on the Barnacles Chthamalus challengeri and Balanus amphitrite amphitrite from Japan (Crustacea: Cirripedia: Rhizocephala: Chthamalophilidae)

Abstract A new rhizocephalan parasite which infests the barnacles Chthamalus challengeri and Balanus amphitrite amphitrite is described. It is known only from the type locality, Aburatsubo, Kanagawa Prefecture, Japan. Its position in the family Chthamalophilidae is assured by the cyprids lacking a thorax, by the position of the mesenteric canal opposite to the stalk, and by its host being a balanomorph barnacle. Among the three previously described species of the Chthamalophilidae, the new species most closely resembles Boschmaella balani, but it differs in details of the internal root system and in the externa being found both on the host body and on the inner mantle. About two-thirds of the infested hosts carry more than one externa.     

A latitudinal gradient in northeast Pacific intertidal community structure: evidence for an oceanographically based synthesis of marine community theory

ABSTRACT Intertidal systems have been models for the study of the roles of competition, predation, and disturbance in determining community structure. These systems exhibit considerable regional variability in percentage cover and in the strength of interspecific interactions, which may be due largely to effects of varying larval supply. In Oregon and Washington, experimental studies of space allocation among sessile invertebrates have emphasized the role of benthic processes such as competition and predation. In contrast, studies in central California have emphasized the importance of larval supply. In this article, we identify a gradient in percentage cover in the middle and upper intertidal zone that is consistent with an oceanographically based explanation for these differences: percentage cover of mussels and barnacles is much higher in Oregon, where nearshore circulation promotes high recruitment, than in California, where strong offshore currents inhibit recruitment. A mathematical model incorporating larval transport and interspecific competition for space offers an explanation for the one violation of the hypothesis-higher percentage cover of Chthamalus spp. in California. The findings illustrate that attempts to synthesize regional differences in community structure and dynamics can benefit from considering both the benthic adult and pelagic larval environments.     

A phylogenetic study of chthamaloids (Cirripedia; Thorcica; Chthamaloidae) based on 16S rDNA and COI sequence analysis

The sequences of gene fragments encoding cytochrome  c oxidase subunit I (COI) and 16S rDNA were obtained and used to construct phylograms of eight taxa of chthamaloid barnacles using the scalpelloid Calantica as an out-group. The phylograms support the basal position of Catomerus within the chthamaloids . Analysis of 16S rDNA shows that Octomeris and the four-plated barnacle Chamaesipho are located on the same clade, while Chthamalus , Euraphia and Tetrachthamalus are located on a second clade, indicating that reduction in the number of shell plates occurred twice in the evolution of the chthamaloids. The topology of phylograms based on COI sequences is poorly resolved: 93% of third position nucleotides in this fragment are polymorphic while the amino acid sequences are strictly conserved. We assume that in the chthamaloids, at least at the generic level, polymorphism in the COI gene is saturated beyond phylogenetic information and cannot resolve the phylogenetic relationships within this superfamily.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 39–45.     

Biodiversity and Biogeography of Chthamalid Barnacles from the North-Eastern Pacific (Crustacea Cirripedia)

The biogeography and ecology of the species of Chthamalus present on the west coast of America are described, using data from 51 localities from Alaska to Panama, together with their zonation on the shore with respect to that of other barnacles. The species present were C. dalli, Pilsbry 1916, C. fissus, Darwin, 1854, C. anisopoma Pilsbry 1916 and four species in the C. panamensis complex. The latter are C. panamensis Pilsbry, 1916, C. hedgecocki, Pitombo & Burton, 2007, C. alani nom. nov. (formerly C. southwardorum Pitombo & Burton, 2007) and C. newmani sp. nov.). These four species were initially separated by enzyme electrophoresis. They could only be partially separated by DNA bar coding but may be separated using morphological characters.     

Survivorship of juvenile barnacles and mussels: spatial dependence and the origin of alternative communities

Mussels, barnacles, and rockweeds often form a distinct mosaic of patches on rocky intertidal shores, and it has been suggested that these communities may represent alternative community states. One way that alternative community states can arise is if early successional events are scale-dependent, but it is not known if juvenile survivorships of mussels and barnacles are, in fact, scale-dependent. Scale-dependence of barnacles (Semibalanus balanoides (L.)) and mussels (Mytilus edulis L.) was tested in the Gulf of Maine, USA. In winter 1997, clearings of 1, 2, 4 and 8 m in diameter and uncleared controls were made in stands of the rockweed Ascophyllum nodosum (L.) Le Jolis at 12 sites spread evenly across four bays on Swan's Island, ME. Summer and fall-winter survivorship of barnacles, which recruited in spring 1997, were estimated by tracking the 1997 cohort until late winter 1998. Survivorship of mussels was estimated from following the fate of transplanted juveniles over 4 days in late August 1997. Both barnacles and mussels showed better survival in 4 and 8 m clearings than in small clearings and controls. There was also significant variation in survivorship among sites. Densities of gastropods in the clearings did not reflect survivorship patterns of barnacles and mussels. Barnacle survivorship increased in fall and winter, and in large clearings was comparable to survivorship in barnacle-dominated habitats. Mussel survivorship was low in all clearing sizes suggesting that mussel beds develop slowly.     

The impact of desiccation on the adhesion of barnacles attached to non-stick coatings

Fouling-release coatings prevent fouling of ships' hulls through hydrodynamic forces generated as the ship moves through the water. The effectiveness of such coatings may be evaluated by measuring the adhesion strength of settled organisms, e.g. barnacles. The influence of desiccation of the barnacle adhesive on such measurements was investigated. Shear forces required to remove barnacles of the genus Balanus increased during the course of desiccation up to the point when the barnacles suddenly self-detached. The increase was thought to be due to the rising cohesive strength of the adhesive. Growing tensile forces within the weakly cross-linked adhesive, however, are suggested to have led to self-detachment. The shear forces required to remove barnacles of the genus Elminius were generally low and did not differ significantly during the course of desiccation. The different results may be attributed to specific base morphologies. It was concluded that measuring the adhesion strength of members of the Balanidae on non-stick surfaces in air could produce flawed results due to the influence of desiccation of the barnacle adhesive. The investigations have also provided new insights into the characteristics of barnacle adhesive.     

PREDATOR-INDUCED SHELL DIMORPHISM IN THE ACORN BARNACLE CHTHAMALUS ANISOPOMA

Field experiments were conducted in order to determine the nature of shell dimorphism in the acorn barnacle Chthamalus anisopoma and the adaptive significance of the atypical form. The typical morph has the conical shape which is characteristic of acorn barnacles, while the atypical morph appears bent over, with the rim of its aperture oriented perpendicular to its base. The experiments showed that: 1) the bent-over morphology is an environmentally-induced developmental response to the presence of a carnivorous gastropod (Acanthina angelica) and 2) that “bents” are more resistant than “conics” to specialized predation by this snail. The results also showed that predation by A. angelica is patchy and heaviest in the near vicinity of cracks and crevices, which it uses as refuges during periods of tidal inundation. Because predation is patchy and bents are less fecund and grow slower than conics, the conditional developmental strategy is likely to be favored over strict genetical control of shell morphology.     

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.     

Spatial distribution of turtle barnacles on the green sea turtle, Chelonia mydas

Distribution patterns of epibiotic barnacles on green sea turtles were investigated in waters neighboring Okinawa, Japan. A number of barnacle species were found to coexist on the turtles and were classified into three genera: Chelonibia, Platylepas and Stomatolepas. Attachment sites on the turtles varied among the barnacle species, suggesting that there is niche partitioning with respect to their microhabitat selection. Turtle bodies offer a “patchy” environment for barnacles, so we also analyzed coexistence patterns in the context of an aggregation model. Within each genus, individual barnacles showed a clumped distribution. The different genera do not have mutually exclusive distribution patterns, but instead occur on the same turtle to various degrees. However, when turtles were divided into two size classes, both the level of aggregation and the degree of interspecific overlap among the barnacles was significantly lower on large turtles. We suggest that obtaining basic information on turtle epibionts will shed light on the biology of wild turtles, which is still largely unknown.     

The Impact of Desiccation on the Adhesion of Barnacles Attached to Non-stick Coatings

Fouling-release coatings prevent fouling of ships' hulls through hydrodynamic forces generated as the ship moves through the water. The effectiveness of such coatings may be evaluated by measuring the adhesion strength of settled organisms, e.g. barnacles. The influence of desiccation of the barnacle adhesive on such measurements was investigated. Shear forces required to remove barnacles of the genus Balanus increased during the course of desiccation up to the point when the barnacles suddenly self-detached. The increase was thought to be due to the rising cohesive strength of the adhesive. Growing tensile forces within the weakly cross-linked adhesive, however, are suggested to have led to self-detachment. The shear forces required to remove barnacles of the genus Elminius were generally low and did not differ significantly during the course of desiccation. The different results may be attributed to specific base morphologies. It was concluded that measuring the adhesion strength of members of the Balanidae on non-stick surfaces in air could produce flawed results due to the influence of desiccation of the barnacle adhesive. The investigations have also provided new insights into the characteristics of barnacle adhesive.     

Too close for comfort: spatial patterns in acorn barnacle populations

Spatial patterns in aggregations form as a result of the interplay between costs and benefits experienced by individuals. Such self-organisation of aggregations can be explained using a zonal model in which a short-range zone of repulsion and longer-range zone of attraction surrounding individuals leads to emergent pattern properties. The signal of these processes can be detected using spatial pattern analyses. Furthermore, in sessile organisms, post-settlement mortality reveals the relative costs and benefits of positions within the aggregation. Acorn barnacles are known to require contact with conspecifics for reproduction and are therefore believed to aggregate for this purpose; isolated individuals may also be more susceptible to abiotic stress and predation. At short distances, however, competition for space and resources is likely to occur. In this study spatial patterns of barnacles (Semibalanus balanoides L.) were analysed using pair-correlation functions. Individuals were dispersed at distances below 0.30 cm, but peak relative density occurred at a distance of 0.36 cm from conspecifics. This is much closer than required for reproductive access, implying a strong aggregative drive, up to the point of physical contact with neighbours. Nevertheless, analysis of dead barnacles illustrated that such proximity carries a cost as barnacles with many neighbours were more likely to have died. The inferences obtained from these patterns are that barnacles aggregate as closely as they can, and that local neighbourhood competition is a powerful determinant of mortality. These processes give rise to the observed pattern properties.     

Optimal diet theory: behavior of a starved predatory snail

Summary The tenets of optimal foraging theory are used to contrast the behavior of the predatory snail Acantina spirata when feeding on the barnacles Balanus glandula and Chthamalus fissus under conditions of satiation and starvation. As predicted in optimal diet models, A. spirata is less selective (ratio of attack frequency on a prey species to number of individuals available) when the higher ranking prey has low abundance. When given a choice, starved snails attack both barnacle species equally, whereas satiated individuals preferentially attack B. glandula, the more profitable prey (ash-free dry weight of barnacles ingested per unit handling time). Under starvation conditions, equal attack frequency does not result in equal prey species consumption because Acanthina spirata is more successful at attacking C. fissus than B. glandula.The assumption of constant prey encounter rates in optimal diet models is not met when A. spirata goes from a state of satiation to starvation. The encounter rate on B. glandula is lowered due to a decrease in attack success. A loss of feeding skills in starved A. spirata is responsible for the greater difficulty snails have in gaining access through the opercular plates of B. glandula.Behavioral changes in A. spirata as snails pass from satiation to hunger translate into an energetic disadvantage during feeding for hungry snails for two reasons. First, higher prey handling times result in a decreased rate of biomass intake. Second, alteration in the relative attack frequency between barnacle species, combined with a decrease in attack success on the more profitable prey leads to more frequent ingestion of the less profitable prey.