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     

Crustose coralline algae and a cnidarian neuropeptide trigger larval settlement in two coral reef sponges

In sessile marine invertebrates, larval settlement is fundamental to population maintenance and persistence. Cues contributing to the settlement choices and metamorphosis of larvae have important implications for the success of individuals and populations, but cues mediating larval settlement for many marine invertebrates are largely unknown. This study assessed larval settlement in two common Great Barrier Reef sponges, Coscinoderma matthewsi and Rhopaloeides odorabile, to cues that enhance settlement and metamorphosis in various species of scleractinian coral larvae. Methanol extracts of the crustose coralline algae (CCA), Porolithon onkodes, corresponding to a range of concentrations, were used to determine the settlement responses of sponge larvae. Cnidarian neuropeptides (GLW-amide neuropeptides) were also tested as a settlement cue. Settlement in both sponge species was approximately two-fold higher in response to live chips of CCA and optimum concentrations of CCA extract compared to 0.2 μm filtered sea water controls. Metamorphosis also increased when larvae were exposed to GLW-amide neuropeptides; R. odorabile mean metamorphosis reached 42.0±5.8% compared to 16.0±2.4% in seawater controls and in C. matthewsi mean metamorphosis reached 68.3±5.4% compared to 36.7±3.3% in seawater controls. These results demonstrate the contributing role chemosensory communication plays in the ability of sponge larvae to identify suitable habitat for successful recruitment. It also raises the possibility that larvae from distinct phyla may share signal transduction pathways involved in metamorphosis.     

Pharmacological Induction of Larval Settlement and Metamorphosis in the Blue Mussel Mytilus edulis L.

The blue mussel Mytilus edulis L. is an important aquaculture and fouling species in northern seas. Although the general role of chemical cues for settlement of larvae of the blue mussel has been proposed, few studies have focused on induction of settlement and metamorphosis by pharmacological agents. In this study, the induction of larval settlement of the blue mussel by pharmacological compounds was investigated through a series of laboratory experiments with an aim of identifying artificial cues for laboratory bioassay systems in fouling and antifouling research. Gamma-aminobutiric acid (GABA), dihydroxyphenyl L-alanine (DOPA), isobutyl methylxanthine (IBMX) and acetylcholine chloride (ACH) at 10^{m 7}-10^{m 2} M as well as KCl at 10-40 mM K⁺ in excess of the level in normal seawater were tested for their inductive effect on larval settlement. In filtered seawater (FSW) <9% of the larvae settled after 48 h. Elevated K⁺ and GABA levels had no effect on larval settlement and metamorphosis. DOPA at 10^{m 5} M and IBMX at 10^{m 6}-10^{m 4} M induced 41-83% larval settlement and ACH at 10^{m 7}-10^{m 5} M induced < 40% larval settlement. While the highest settlement rates were observed after 48 h exposure to the chemicals, most of the larvae settled within 24 h. Compounds at concentrations of 10^{m 3}-10^{m 2} M were either toxic to larvae or retarded the growth of the post-larvae shell. Juveniles resulting from induction by lower concentrations of chemicals had a very high survival rate, completed metamorphosis and grew as well as the juveniles that metamorphosed spontaneously. IBMX at 10^{m 6}-10^{m 4} M and L-DOPA at 10^{m 5} M are effective agents for induction of settlement and metamorphosis for future studies using juvenile M. edulis.     

Behavior,metamorphosis, and muscular organization of the predatory rotifer Acyclus inquietus (Rotifera,Monogononta)

Abstract. The atrochid rotifer, Acyclus inquietus, is a sedentary predator that lives within the colonies of its prey, the rotifer Sinantherina socialis. After larvae infiltrate and become associated with the colony, they secrete a permanent gelatinous tube and undergo metamorphosis to the adult stage. We followed settlement and metamorphosis using bright-field microscopy to document specific larval behaviors after eclosion, and used epifluorescence and confocal microscopy of phalloidin-labeled specimens to visualize some of the morphological changes that occur during metamorphosis. Upon eclosion, larvae possess paired eyespots and a ciliated corona that functions strictly in locomotion. After leaving the parent's gelatinous tube, larvae eventually settle on unoccupied colonies of S. socialis or on other substrates if colonies are unavailable. Settlement involves a period of gliding among colony members before attachment with the foot and the secretion of a gelatinous tube. After settlement, there is a drastic reconfiguration of the corona that involves loss of the eyespots, loss of the coronal cilia, and the formation of the cup-shaped infundibulum, a deep depression in the anterior of the head that leads to the mouth. The development of the infundibulum involves the expansion of tissues around the mouth and is accompanied by a reorientation of the underlying musculature that supplies the infundibulum and allows its use in prey capture. The arrangement of the muscles in the trunk and foot regions, which contain outer circular (complete and incomplete) and inner longitudinal bands, remains unchanged between ontogenetic stages, and reflects the condition characteristic of other rotifers.     

A fine structural study of metamorphosis of the hydrozoan Mitrocomella polydiademata

This report is a comprehensive fine structural analysis of the morphological changes occurring during metamorphosis of the marine hydrozoan Mitrocomella polydiademata. Five stages are recognized during metamorphosis: planulae just prior to settlement, ball and filiform stages, immature polyps, and primary feeding polyps. Settlement and metamorphosis of cnidarian planulae involve such changes as ciliary arrest, discharge of nematocytes, secretion of glandular cells, differentiation of cells, and changes in cell and body shape.     

Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to natural biofilms

Settlement and metamorphosis of pediveliger larvae of Mytilus coruscus in response to natural biofilms was investigated in the laboratory. Pediveliger larvae settled and metamorphosed in response to biofilms and post-larval settlement and metamorphosis increased with biofilm age. The activity of the biofilm was positively correlated with biofilm age, dry weight, bacterial density and diatom density, but had no apparent relationship with chlorophyll a concentration. The change in bacterial community composition corresponding to biofilm age may explain differences in the age-dependent inducing activities of biofilms, which in turn may play an important role in larval settlement in this species.     

Bioerosion of gastropod shells: with emphasis on effects of coralline algal cover and shell microstructure

Organisms boring into fifty nine species of gastropod shells on reefs around Guam were the bryozoan Penetrantia clionoides; the acrothoracian barnacles Cryptophialus coronorphorus, Cryptophialus zulloi and Lithoglyptis mitis; the foraminifer Cymbaloporella tabellaeformis, the polydorid Polydora sp. and seven species of clionid sponge. Evidence that crustose coralline algae interfere with settlement of larvae of acrothoracian barnacles, clionid sponges, and boring polychaetes came from two sources: (1) low intensity of boring in limpet shells, a potentially penetrable substrate that remains largely free of borings by virtue of becoming fully covered with coralline algae at a young age and (2) the extremely low levels of boring in the algal ridge, a massive area of carbonate almost entirely covered by a layer of living crustose corallines. There was a strong negative correlation between microstructural hardness and infestation by acrothoracian barnacles and no correlation in the case of the other borers. It is suggested that this points to a mechanical rather than a chemical method of boring by the barnacles. The periostracum, a layer of organic material reputedly a natural inhibitor of boring organisms, was bored by acrothoracican barnacles and by the bryozoan. The intensity of acrothoracican borings is shown to have no correlation with the length of the gastropod shell.     

The distribution and abundance of barnacles in a mangrove forest

Abstract The grey mangrove tree, Avicennia marina, forms a hard substratum in an area otherwise dominated by soft-sediment. Various intertidal organisms attach to and move about on the trees. The abundant barnacles Elminius covenus, Hexaminius popeiana and Hexaminius foliorum live on a variety of substrata in mangrove forests. Their patterns of distribution and abundance were recorded and models proposed to explain these patterns. Densities of barnacles on bark, leaves and twigs of A. marina were estimated in a locality near Sydney. Elminius covenus were more abundant on bark than on leaves or twigs of A. marina. Hexaminius popeiana, although less abundant on bark than E. covenus, were not found on twigs or leaves. In contrast, H. foliorum were more abundant on twigs than leaves and were not found on the bark of A. marina. Densities of barnacles were greater in the seaward than in landward parts of the forest. Elminius covenus were the most abundant barnacles, H. foliorum were less abundant and H. popeiana were virtually absent in the landward zone. Barnacles in the seaward zone were most abundant at mid-tidal levels, less at high and low tidal levels of trunks and more abundant on lower than upper surfaces of trunks and leaves. The densities of barnacles differed according to the orientation of the bark or leaf. Models are proposed to explain the patterns of distribution and abundance of these barnacles. Each involves larval supply, settlement and post-settlement mortality. It is concluded that similar processes determining patterns of distribution and abundance for sessile organisms living on rock platforms may be applicable to sessile organisms living in the very different habitats of mangrove forests.     

The site of settlement indicates commensalism between bluemussel and its epibiont

Summary The site of settlement of barnacles (Balanus improvisus) attached on shells of bluemussels (Mytilus edulis) was mapped from a sample of mussels collected in the Baltic Sea. Most barnacles had settled near the siphonal apertures of the mussel. An experiment was made to measure the disadvantages and advantages that living in close association brings to barnacles and mussels. The barnacles on shells of living mussels were shown to grow significantly faster than those on empty mussel shells. Presence of barnacles had no effects on growth of mussels. The two-species association under study was demonstrated to be a case of commensalism.     

Structures of six cDNAs expressed specifically at cypris larvae of barnacles, Balanus amphitrite

We cloned six cDNAs by screening cDNA libraries of cypris larvae from barnacles, Balanus amphitrite, and studied their expression by Northern blot analysis. All of them are expressed in the cypris larvae at the settlement stage, but not in the earlier nauplii larvae nor in later adult barnacles. Therefore, we designated them as barnacle cypris larva-specific genes (bcs); bcs-1, bcs-2, bcs-3, bcs-4, bcs-5 and bcs-6. During the process of larval attachment and metamorphosis, the amounts of bcs-1 and bcs-2 mRNAs decreased, whereas the bcs-3, bcs-4, bcs-5 and bcs-6 mRNAs increased. A homology search showed that all cDNAs encode novel peptides containing characteristic amino acid sequences. This study strongly suggests that these bcs gene products are involved in the cypris larval attachment and metamorphosis of barnacles.     

Metamorphosis season from megalopa to the first crab stage in snow crab Chionoecetes opilio and red snow crab C. japonicus (Crustacea,Decapoda, Majoidea) in the Sea of Japan,estimated from captive culture

ABSTRACT

Metamorphosis season of megalopae to the first crab stage in snow crab Chionoecetes opilio and red snow crab C. japonicus was inferred by culturing wild-born megalopae collected from the Sea of Japan. Metamorphosis occurred from late June to late July (mainly in July) in snow crab, and from early July to early October (mainly from August to September) in red snow crab. The number of days required from the time of collection to metamorphosis was less than the intermoult period previously reported for snow crab megalopae. However, the developmental period of the megalopae was estimated as substantially longer in red snow crab than in snow crab. Previous studies have shown that the hatching season and the period of the zoeal stage in both two species are similar. These results suggest that a different metamorphosis season between the two species would be due to a difference in their megalopal intermoult period.     

Exploring the regulatory role of nitric oxide (NO) and the NO-p38MAPK/cGMP pathway in larval settlement of the bryozoan Bugula neritina

The bryozoan Bugula neritina is a cosmopolitan marine fouling species that causes major fouling problems in sub-tropical waters. Settlement of B. neritina larvae can be triggered without an obvious external cue. Here, the negative regulatory role of nitric oxide (NO) during larval settlement of B. neritina was demonstrated to be mediated by cyclic guanosine monophosphate (cGMP). Although the regulatory role of the NO-p38 MAPK signaling axis in larval settlement was not evident, inhibition of nitric oxide synthase (NOS) led to the deactivation of p38 MAPK. Exclusive localization of NO and NO signaling components in sensory-related organs of the larvae is consistent with its signal transduction function in metamorphosis. Overall, this study provides new insights into the regulatory roles of the NO-p38MAPK/cGMP pathway in B. neritina settlement.     

Probing the settlement signals of Amphibalanus amphitrite

To achieve their reproductive potential, barnacles combine tactile exploration of surface structural properties and integration of cellular signals originating from their antennular sensory setae within a developmentally defined, temporally narrow window of settlement opportunity. Behavioural assays with cyprids coupled with biometric analysis of scanning electron microscopy-acquired images in the presence of specific chemical compounds were used to investigate how settlement on a substratum is altered in response to the presence of these compounds. Impeding tactile exploration was shown which altered cellular signalling and/or induced malformation of anatomical features of the antennular sensory setae, which disrupted the settlement behaviour of the model barnacle species Amphibalanus amphitrite. It is concluded that surface exploration by the cyprids relies on mechanical and nociception-related and calcium-mediated signals while a protein kinase C signalling cascade controls the timely metamorphosis of the cyprids to sessile juveniles.     

The relation between cypris ultrastructure and metamorphosis in male and female Sacculina carcini (Crustacea,Cirripedia)

Summary To elucidate current controversies on sex in rhizocephalan barnacles, broods of Sacculina carcini, infesting the shore crab Carcinus maenas, were raised to cyprids in the laboratory and followed through settlement and metamorphosis. Free-swimming cyprids were studied by transmission electron microscopy and occur in male and female morphological types, which differ in the structure of carapace cuticle, antennular cuticle, antennular glands, and the cells suspected of being the stem cells during metamorphosis. These dissimilarities are in addition to the already known differences in cypris size, in number of antennular sense organs, and in substrata settled on by morphological males and females. Metamorphosing males (trichogons) and females (kentrogons) are illustrated in interference phase-contrast micrographs. The morphological differences between male and female cyprids are directly related to their dissimilar metamorphosis. Hence, cyprids of male morphology are anatomically incapable of metamorphosing into kentrogons, while cyprids of female morphology cannot metamorphose into trichogons. The determination of sex in rhizocephalan barnacles is discussed.The results refute the hypothesis that sex in Sacculina carcini is determined environmentally, e.g., by the substratum encountered by the cyprids at settlement. It is concluded that sex is determined already in the free-swimming larvae and, most probably, already in the ovary. This agrees with the mode of sex determination in other species of the Rhizocephala Kentrogonida.     

Induction of metamorphosis with potassium ions requires development of competence and an anterior signalling centre in the ascidian Herdmania momus

 Increased K⁺ concentration in seawater induces metamorphosis in the ascidian Herdmania momus. Larvae cultivated at 24°C exhibit highest rates of metamorphosis when treated with 40 mM KCl-elevated seawater at 21°C. At 24°C, H. momus larvae develop competence to respond to KCl-seawater and initiate metamorphosis approximately 3 h after hatching. Larval trunks and tails separated from the anterior papillae region, but maintained in a common tunic at a distance of greater than 60 μm, do not undergo metamorphosis when treated with KCl-seawater; normal muscle degradation does not occur in separated tails while ampullae develop from papillae-containing anterior fragments. Normal programmed degradation of myofibrils occurs when posterior fragments are fused to papillae-containing anterior fragments. These data indicate that H. momus settlement and metamorphosis only occurs when larvae have attained competence, and suggest that an anterior signalling centre is stimulated to release a factor that induces metamorphosis. Received: 15 May 1996 / Accepted: 19 September 1996     

Bewuchsuntersuchungen auf Natursteinsubstraten im Gezeitenbereich des Nordsylter Wattenmeeres: Sessile und hemisessile Tiere

Six different types of test substrates, arranged in order of texture from smooth (Solnhofen limestone, Bunter sandstone, and basalt) to rough surfaces (Middle Triassic limestone, granite, and basaltic lava), were exposed in tidal zone of the wadden sea near the harbour of List (Island of Sylt, North Sea). The test substrates were fixed to panels at the midtide to high-water level, the midtide to low-water level, and 75 cm below the latter (sublittoral level). Animal settlement was primarily influenced by abiotic factors at the two higher levels. In the sublittoral zone, however, influences of biotic factors (competitors and predators) predominated. Therefore, the physical quality of the chosen substrates more decisively affected the growth of settling animals above the midtide to low-water mark than in the deeper zone. At the midtide to high-water levelBalanus balanoides only settled on the rough surface of the Middle Triassic limestone and in the troughs of the Bunter sandstone; barnacles attached to the even surface of the latter, were destroyed by wave beating. They died on the rough surface of the dark-coloured granite, when this stone was warmed during low-water. At the midtide to low-water level, the barnacles survived best on the rough surface of the Middle Triassic limestone and the granite. Only the larvae ofB. crenatus andB. improvisus preferred to settle on the even surface of the Bunter sandstone and the basalt; but there they died from wave beating or desiccation. The surface of the basaltic lava, formed by sharp-edged pores, was unsuitable for settling of barnacles. Colonies of Hydrozoa covered each substrate with a somewhat rough surface structure, even the basaltic lava. At the sublittoral level, differences in settling between the single substrates disappeared more and more. Nevertheless, the three species of barnacles showed the same preferences in settling, as they did at the higher levels. In August,Asterias rubens destroyed all barnacles and thus restricted the lower limit of barnacle settlement at the low-water mark. The distribution of epibiotic organisms is dependent upon the density of their living substrates, directly attached to the stone surfaces. During the short time of their growth, hemisessile young,Mytilus edulis settled on thready forms like algae, or on raised areas like the top of barnacle shells. Therefore, young mussels could be found on stones, that already carried a compact cover ofEnteromorpha sp. or a dense settlement of adult barnacles. The polychaetePolydora ciliata rarely burrowed directly into stony substrates (Middle Triassic limestone, Solnhofen limestone). It settled primarily between barnacle shells where it was sheltered from wave beating and at the same time profited from the current produced by the filter-feeding organs of the barnacles. The density of this polychaete was directly proportional to the density of the barnacles. AfterA. rubens had destroyed the barnacles in the sublittoral zone,P. ciliata disappeared too. At the low-water mark, however, theP. ciliata population between living and active barnacles increased. Hence, the lower limit ofP. ciliata — as those of barnacles and mussels — was fixed by this predator.

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Herrn Professor W. E. Ankel zur Vollendung des 80. Lebensjahres in Dankbarkeit gewidmet.     

Surface active adrenoceptor compounds prevent the settlement of cyprid larvae of Balanus improvisus

The barnacle Balanus improvisus is the major fouling macroorganism in Swedish waters and it colonizes most man‐made surfaces submerged in the sea. New or impending legislation restricts the use of traditional, hazardous antifouling coatings based on heavy metals, mainly copper and tin. This calls for the development of new non‐toxic methods that prevent barnacle settlement. In this work several adrenoceptor compounds are shown to be very efficient in preventing the settlement of cyprid larvae of B. improvisus. The settlement rate of laboratory‐reared cyprids was studied in hydrophilised polystyrene dishes containing adrenoceptor antagonists and agonists dissolved in seawater. Two of these drugs, medetomidine and clonidine, repeatedly inhibited settlement at concentrations between 1 nM and 10 nM. In the vertebrate adrenoceptor classification system, which separates pharmacological substances according to their receptor affinity, both of these substances are classified as α₂ adrenoceptor agonists. An inhibiting effect on presyn‐aptic receptors is suggested, but the localization of the receptor effect requires futher studies. Experiments also revealed that the inhibiting effect of medetomidine was reversible. Cyprids incubated with medetomidine for 20 h attached and metamorphosed into juvenile barnacles after washing and transferrence to seawater. The antagonizing compound atipamezole reversed the effect of medetomidine. This observation supports the assumption that this substance acts at the receptor level. Studies of the surface affinity of medetomidine revealed a strong tendency to accumulate in solid/ liquid phase boundaries. This ability makes it particularly attractive as a candidate for the development of a slow‐release carrier in marine coatings. Panels coated with medetomidine in an acrylate polymer and exposed in the field reduced the recruitment of B. improvisus by 96% after 4 weeks and by 70% after 8 weeks.     

Proteomic analysis during larval development and metamorphosis of the spionid polychaete Pseudopolydora vexillosa

Background  

While the larval-juvenile transition (metamorphosis) in the spionid polychaete Pseudopolydora vexillosa involves gradual morphological changes and does not require substantial development of juvenile organs, the opposite occurs in the barnacle Balanus amphitrite. We hypothesized that the proteome changes during metamorphosis in the spionids are less drastic than that in the barnacles. To test this, proteomes of pre-competent larvae, competent larvae (ready to metamorphose), and juveniles of P. vexillosa were compared using 2-dimensional gel electrophoresis (2-DE), and they were then compared to those of the barnacle.     

Chemical induction of settlement and metamorphosis of Capitella capitata Sp. I (Polychaeta) larvae by juvenile hormone-active compounds

Summary

The influence of juvenile hormone (JH)-active chemicals on the settlement and metamorphosis of metatrochophore larvae of the polychaete annelid Capitella sp. I of the Capitella complex has been investigated. These studies demonstrate that JH-active chemicals are able to induce settlement and metamorphosis of Capitella larvae, and that these effects may possibly be mediated by protein kinase C induction. Evidence for the presence of JH-active compounds in marine sediments is also presented, suggesting that these chemicals may serve a natural role as chemical cues for settlement and metamorphosis for Capitella larvae in the marine environment.