Nudibranch-sponge feeding dynamics: Benefits of symbiont-containing sponge to Archidoris montereyensis (Cooper, 1862) and recovery of nudibranch feeding scars by Halichondria panicea (Pallas, 1766)

Selected interactions between the encrusting sponge Halichondria panicea and its primary predator, the dorid nudibranch Archidoris montereyensis, were investigated in a high-latitude rocky intertidal community spatially dominated by H. panicea. Feeding experiments were conducted in which A. montereyensis pairs were provided with sponge containing symbiotic zoochlorellae or sponge in which the zoochlorellae population had been reduced or removed by shading. Nudibranchs consuming H. panicea with symbiotic zoochlorellae had higher feeding, growth, and egg production rates than individuals eating aposymbiotic sponge. We simulated A. montereyensis predation on H. panicea by creating typically sized feeding grooves in the sponge. H. panicea's response was high linear growth rates into the experimental feeding grooves, generally recovering most of the groove area within 4 weeks. Overall, the sponge's rapid response to tissue damage minimizes grazing impacts and substrate loss and reduces susceptibility to wave removal.     

Effect of excretory-secretory products of some fouling organisms on settling and metamorphosis of the larvae of <Emphasis Type="Italic">Styela rustica</Emphasis> (Ascidiae)

The effect of the excretory-secretory products of some fouling animals on the settling and metamorphosis of larvae of the solitary ascidian Styela rustica was assessed. The substances secreted by the sponge Halichondria panicea stimulated settling of larvae, but concurrently blocked their metamorphosis. The excretory-secretory products of the mussel Mytilus edulis and the ascidian Molgula citrine did not affect settling of the S. rustica larvae but impeded their subsequent development. Water conditioned by the bivalve Hiatella arctica, stimulated settling and, apparently, metamorphosis of the larvae of S. rustica. The chemical substances produced by adult individuals of S. rustica facilitated settling of conspecific larvae but slightly delayed their metamorphosis.     

The impact of waterborne cues from conspecifics and other species on the larvae of Halichondria panacea Pallas, 1766 (Porifera: Demospongiae)

The impacts of different concentrations of the excretory-secretory products (ESPs) of the solitary ascidian Styela rustica (Linnaeus, 1767) and the sponge Halichondria panacea (Pallas, 1766) on the settlement, metamorphosis, and mortality rates of H. panacea larvae were studied in a laboratory experiment. At high concentrations, substances released into the environment by the ascidian S. rustica exerted a negative impact on the metamorphosis rate of sponge larvae. The exposure to moderate or high concentrations of ESPs from conspecific adults led to high mortality of larval sponges; however, low conspecific ESP concentrations markedly stimulated metamorphosis; larval mortality was low. Apparently, different concentrations of the same ESPs can have effects with a different strength and focus. This should be taken into account in the study of chemically mediated interactions between aquatic organisms.     

Experimental study of the ability of the sponge <Emphasis Type="Italic">Halichondria panicea</Emphasis> (Porifera: Demospongiae) to compete for a substrate in shallow-water fouling communities of the White Sea

The ability of the sponge Halichondria panicea to assimilate into the fouling communities of the blue mussel Mytilus edulis and the solitary ascidian Styela rustica has been studied in a field experiment, in which sponge fragments have been introduced artificially into epibenthic communities. The growth of H. panicea was suppressed greatly in the presence of young mussels; its survival rate averaged 40%. In the communities where S. rustica dominated, the survival rate of H. panicea reached 100%, but the growth rate was lower than in the control group (without competitor species). Despite the high natural growth rate and toxicity, the settlement success of H. panicea was low on the substrate occupied by another fouling species.     

Effects of ocean acidification on the early life history processes of the breadcrumb sponge Halichondria panicea

Ocean acidification (OA) is predicted to result in reduced survival, growth, reproduction, and overall biodiversity of marine invertebrates, and yet we lack information about the response to OA of some major groups of marine organisms. In particular, we know relatively little about how OA will impact temperate sponges, which will experience more extreme low pH conditions than tropical species. In this study, we quantified OA-induced changes in early life history patterns (larval mortality and condition, settlement rate, recruit survival, and size) in the non-calcifying breadcrumb sponge Halichondria panicea collected from a temperate intertidal site in the California Current Large Marine Ecosystem. Sponge larvae were exposed to OA conditions for 15 days, and early life history patterns were observed. Compared with baseline (“present”) conditions, larval mortality and settlement rates increased in the acidified treatment (“future”). This effect was restricted to larval stages; treatment had no effect on the growth and survival of recruits. This study is significant in that it shows that H. panicea may be particularly vulnerable to changes in ocean pH during the larval stage, which could ultimately reduce total sponge abundance by diminishing the number of larvae that survive to settlement.     

Effects of GABA and epinephrine on the settlement and metamorphosis of the larvae of four species of bivalve molluscs

Competent larvae of different marine bivalve species were treated with GABA and epinephrine at different concentrations and times of exposure to test the ability of the drugs to induce settlement and metamorphosis. GABA induced both settlement and metamorphosis in the mussel Mytilus galloprovincialis, the clams Venerupis pullastra and Ruditapes philippinarum and the oyster Ostrea edulis. Maximum induction of settlement (>39%) was achieved after exposure of V. pullastra larvae to 10⁻⁴ M GABA; this concentration of GABA also induced the highest percentages of metamorphosis in the four species studied. Epinephrine was identified as an active inducer of settlement and metamorphosis in bivalve molluscs. Exposure to 10⁻⁵ M epinephrine induced significant levels of settlement in Mytilus, Venerupis and Ostrea. In contrast, epinephrine failed to induce settlement behaviour in Ruditapes. Maximum induction of metamorphosis was produced by 10⁻⁵ M epinephrine in mussels, clams and oysters; Ruditapes showed the highest percentage of metamorphosis (>78%). This is the first report in which the involvement of GABA in the settlement and metamorphosis of bivalve molluscan larvae is demonstrated. It was also recognised that epinephrine plays a role not only in inducing metamorphosis but also in initiating settlement.     

Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis

The settlement specificity of two threatened Caribbean corals, Acropora palmata and A. cervicornis, was tested by measuring their rates of larval metamorphosis in response to crustose coralline algae (CCA) and other substrata. In the no-choice experiments, the coral larvae were placed in six treatments: filtered seawater (FSW), a fragment of biofilmed dead skeleton of A. palmata, or a fragment of one of four species of CCA (Hydrolithon boergesenii, Porolithon pachydermum, Paragoniolithon solubile, and Titanoderma prototypum). Within each CCA treatment, there were three different substrata on which to settle and metamorphose: (1) the CCA surface, (2) the rock under the CCA, or (3) the plastic dish. The 5-day-old larvae of both A. palmata and A. cervicornis had similar rates of total metamorphosis (all substrata combined) in every treatment (excluding FSW) even in the absence of CCA. However, there were differences in larval behavior among the CCA species since the larvae settled and metamorphosed on different substrata in the presence of different CCA species. In the no-choice experiments the larvae of both corals had higher rates of metamorphosis on the top surfaces of H. boergesenii and/or T. prototypum than on P. pachydermum. In the choice experiments, the coral larvae were offered two species of CCA in the same dish. When given a choice, both species of coral larvae had more settlement and metamorphosis on the surface of H. boergesenii or T. prototypum or clean rock than onto the surface of P. solubile. After 6 weeks in the field, transplanted A. palmata recruits had approximately 15% survival on both T. prototypum and H. boergesenii, but A. cervicornis recruits only survived on T. prototypum (13%). Some, but not all, CCA species facilitated the larval settlement and post-settlement survival of these two threatened corals, highlighting the importance of benthic community composition for successful coral recruitment.     

Tissue sloughing in the sponge Halichondria panicea: a fouling organism prevents being fouled

Summary Specimens of the sponge Halichondria panicea Pallas kept in running sea-water aquaria at 15° C slough off their complete outer tissue layer in regular intervals of three weeks. Sloughing starts at the rim of the oscula and extends over the whole surface within two weeks. Microscopic inspection of the tissue flakes shows them to harbour large numbers of different live organisms, as well as biogenic debris such as pieces of copepod carapaces and diatom frustules. No such community is found on freshly sloughed sponge tissue. After sloughing, the surface skeletal structure of H. panicea is markedly altered, as the characteristic halichondroid reticulum has been replaced by the irregular spicule array typical for the inner sponge tissue. When H. panicea is kept in closed aquaria filled with 0.2 m filtered sea-water, no sloughing occurs during 3 months of maintenance. As those sponges shedding their outer tissue grow steadily at the same time, the tissue sloughing can be regarded as a reaction to sedimentation of organic material and settlement of small organisms on the sponge surface. The sponge thus counteracts clogging of its ostia and prevents the establishment of a micro fouling community on its surface, inhibiting further fouling processes.     

On natural metamorphosis inducers of the cnidarians Hydractinia echinata (Hydrozoa) and Aurelia aurita (Scyphozoa)

 Hydractinia echinata and Aurelia aurita produce motile larvae which undergo metamorphosis to sessile polyps when induced by external cues. The polyps are found at restricted sites, A. aurita predominantly on rocks close to the shore, H. echinata on shells inhabited by hermit crabs. It has been argued that the differential distribution of the polyps in their natural environment largely reflects the distribution of the natural metamorphosis-inducing cues. In the case of H. echinata, bacteria of the genus Alteromonas were argued to meet these conditions. We found that almost all substrates collected in the littoral to induce metamorphosis in H. echinata, and several bacterial strains isolated from the sea, including the common E. coli, induce metamorphosis efficiently. In A. aurita metamorphosis may be induced by the water–air interface, whereby metamorphosis precedes (final) settlement. Received: 7 December 1998 / Accepted: 8 July 1999     

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.     

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.     

Larval Behaviours and Their Contribution to the Distribution of the Intertidal Coral Reef Sponge Carteriospongia foliascens

Sponges (Phylum Porifera) are an evolutionary and ecologically significant group; however information on processes influencing sponge population distributions is surprisingly limited. Carteriospongia foliascens is a common Indo-Pacific sponge, which has been reported from the intertidal to the mesophotic. Interestingly, the distribution of C. foliascens at inshore reefs of the Great Barrier Reef is restricted to the intertidal with no individuals evident in adjacent subtidal habitats. The abundance of C. foliascens and substrate availability was first quantified to investigate the influence of substrate limitation on adult distribution. Pre-settlement processes of larval spawning, swimming speeds, phototaxis, vertical migration, and settlement to intertidal and subtidal substrate cues were also quantified. Notably, suitable settlement substrate (coral rubble) was not limiting in subtidal habitats. C. foliascens released up to 765 brooded larvae sponge⁻¹ day⁻¹ during the day, with larvae (80%±5.77) being negatively phototactic and migrating to the bottom within 40 minutes from release. Subsequently, larvae (up to 58.67%±2.91) migrated to the surface after the loss of the daylight cue (nightfall), and after 34 h post-release >98.67% (±0.67) of larvae had adopted a benthic habit regardless of light conditions. Intertidal and subtidal biofilms initiated similar settlement responses, inducing faster (as early 6 h post-release) and more successful metamorphosis (>60%) than unconditioned surfaces. C. foliascens has a high larval supply and larval behaviours that support recruitment to the subtidal. The absence of C. foliascens in subtidal habitats at inshore reefs is therefore proposed to be a potential consequence of post-settlement mortalities.     

Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae

Settlement specificity can regulate recruitment but remains poorly understood for coral larvae. We studied larvae of the corals, Acropora palmata and Montastraea faveolata, to determine their rates of settlement and metamorphosis in the presence of ten species of red algae, including eight species of crustose coralline algae, one geniculated coralline and one encrusting peyssonnelid. Twenty to forty percent of larvae of A. palmata settled on coralline surfaces of Hydrolithon boergesenii, Lithoporella atlantica, Neogoniolithon affine, and Titanoderma prototypum, whereas none settled and metamorphosed on Neogoniolithon mamillare. Larvae of M. faveolata had 13–25 % settlement onto the surface of Amphiroa tribulus, H. boergesenii, N. affine, N. munitum, and T. prototypum, but had no settlement on the surface of N. mamillare, Porolithon pachydermum, and a noncoralline crust Peyssonnelia sp. Some of these algal species were common on Belizean reefs, but the species that induced the highest rates of larval settlement and metamorphosis tended to be rare and primarily found in low-light environments. The shallow coral, A. palmata, and the deeper coral, M. faveolata, both had increased larval settlement rates in the presence of only a few species of red algae found at deeper depths suggesting that patterns of coral distribution can only sometimes be related to the distribution of red algae species.     

Cultivation of Sponge Larvae: Settlement,Survival, and Growth of Juveniles

The aim of this study was to culture sponge juveniles from larvae. Starting from larvae we expected to enhance the survival and growth, and to decrease the variation in these parameters during the sponge cultures. First, settlement success, morphological changes during metamorphosis, and survival of Dysidea avara, Ircinia oros, Hippospongia communis, under the same culture conditions, were compared. In a second step, we tested the effects of flow and food on survival and growth of juveniles from Dysidea avara and Crambe crambe. Finally, in a third experiment, we monitored survival and growth of juveniles of D. avara and C. crambe transplanted to the sea to compare laboratory and field results. The results altogether indicated that sponge culture from larvae is a promising method for sponge supply and that laboratory culture under controlled conditions is preferred over sea cultures in order to prevent biomass losses during these early life stages.     

Induction of larval settlement and metamorphosis in the donkey-ear abalone,Haliotis asinina Linnaeus,by chemical cues

The effects of the chemical inducers, gamma-aminobutyric acid (GABA) and potassium chloride (KCl), on the larval settlement and metamorphosis of the donkey-ear abalone, Haliotis asinina, was investigated. H. asinina larvae (5–6 h post-hatch) were exposed to a range of GABA (0.125–2.00 μM) and KCl (1.00–12.00 mM) concentrations for 72 h. Results of the dose response experiments showed that settlement and metamorphosis vary according to the dose levels of the inducer compounds. Under controlled laboratory conditions, 0.45–0.50 μM and 6.0 mM seemed to be the optima for GABA and KCl, respectively, as these concentrations elicited the greatest number of postlarvae that metamorphosed, settled or survived. However, GABA generally promoted better attachment and metamorphic response as well as survival than KCl in H. asinina postlarvae.     

Larval settlement and metamorphosis in the slipper limpet Crepidula onyx (Sowerby) in response to conspecific cues and the cues from biofilm

In the marine environment, aggregated distribution in the genus Crepidula is a very common phenomenon. Works from Pechenik's group suggested that this is the result of gregarious settlement of larvae in response to cues associated with conspecific adults. In this study, we investigated the existence of larval metamorphic cues associated with adults of C. onyx, a slipper limpet introduced to Hong Kong from the U.S. in the 1970s, through a series of laboratory bioassays. The results showed that derived cues in adult C. onyx were waterborne and the waterborne cues were not derived from bacteria associated with the shell and soft body of the adult Crepidula. The natural biofilm also induced the larval metamorphosis of C. onyx. The cues from the biofilm were associated with the surface of the biofilm and were not waterborne. The aggregated distribution in nature of adult C. onyx may result from a selective larval settlement process. On a small scale in the water column near the conspecific adults, larvae of C. onyx initially detect the waterborne conspecific cues, which then lead to positive downward swimming or passive sinking. This activity increases the chances for larvae to make contact with the biofilm and to be exposed into the higher concentration of waterborne conspecific cues. This may eventually lead to the enhanced larval settlement pattern on or near the conspecific adults.     

Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea)

Larval development to metamorphosis and early juvenile growth and survivorship were examined in Clypeaster subdepressus (Gray) and C. rosaceus (Linnaeus). C. subdepressus has an obligatorily planktotrophic larva that metamorphoses after 16 to 28 days at 27°C. The larva of C. rosaceus can, but need not feed prior to metamorphosis, which occurs after 5 to 7 days at 27°C. Feeding by larvae of C. rosaceus does not change the time to metamorphosis but does increase size at metamorphosis, early juvenile growth and may increase juvenile survivorship relative to unfed larvae. Size at metamorphosis increases in larvae of C. rosaceus that feed for several days after they are competent to metamorphose, but there may be a limit to this increase because the condition of the rudiment degenerates after a period of time. The development of C. rosaceus may represent a transition between planktotrophy and lecithotrophy. This intermediate state has advantages for the juvenile stage that are not included in the trade of fecundity against risk to offspring usually considered in life history discussions of developmental mode of marine invertebrates.     

The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina

Biofilms of marine bacteria and diatoms and their combinations were examined in laboratory choice assays to determine their effects on the attachment and successful metamorphosis of the larvae of the bryozoan Bugula neritina (Linnéus). The larval settlement in response to unfilmed surfaces, a natural biofilm (NBF) and adsorbed cells of three strains of bacteria, five strains of pennate diatoms and combinations of the two at different densities. Bacterial and diatom strains showed different effects on the larval settlement of B. neritina. Bacterial monospecific strains of an unidentified α-Proteobacterium and Vibrio sp. mediated the same percentage of settlement as a filtered seawater control. Biofilms of Pseudoalteromonas sp. caused significantly lower larval settlement. Larval settlement of B. neritina was negatively correlated with increasing densities of Pseudoalteromonas sp. The highest percentages of settlement were mediated by the biofilms of the diatom species Achnanthes sp., Amphora cofeaeformis, Amphora tenerrima, Nitzschia constricta and a 5-day-old natural biofilm, while the lowest settlement was found on a N. frustulum film. A three-way analysis of variance demonstrated that the density of bacteria and the presence of particular species of diatoms and bacteria in combined biofilms, significantly affected the settlement of B. neritina larvae. High settlement of larvae (50-90%) at all treatments indicated that B. neritina larvae are much more indiscriminate settlers than previously expected. Hence, using this species as a monitoring organism to trace ecologically relevant subtle changes of settlement cues in the natural environment should be carefully re-examined.     

Can benthic algae mediate larval behavior and settlement of the coral Acropora muricata?

The resilience of coral reefs relies significantly on the ability of corals to recover successfully in algal-dominated environments. Larval settlement is a critical but highly vulnerable stage in the early life history of corals. In this study, we analyzed how the presence of two upright fleshy algae, Sargassum mcclurei (SM) and Padina australis (PA), and one crustose coralline algae, Mesophyllum simulans (MS), affects the settlement of Acropora muricata larvae. Coral larvae were exposed to seawater flowing over these algae at two concentrations. Larval settlement and mortality were assessed daily through four variables related to their behavior: swimming, substratum testing, metamorphosis, and stresses. Temperature, dissolved oxygen, pH, algal growth, and photosynthetic efficiency were monitored throughout the experiment. Results showed that A. muricata larvae can settle successfully in the absence of external stimuli (63 ± 6 % of the larvae settled in control treatments). While algae such as MS may stimulate substrate testing and settlement of larvae in the first day after competency, they ultimately had a lower settlement rate than controls. Fleshy algae such as PA, and in a lesser measure SM, induced more metamorphosis than controls and seemed to eventually stimulate settlement. A diverse combination of signals and/or modifications of microenvironments by algae and their associated microbial communities may explain the pattern observed in coral settlement. Overall, this study contributes significantly to the knowledge of the interaction between coral and algae, which is critical for the resilience of the reefs.     

The B Vitamins Nicotinamide (B3) and Riboflavin (B2) Stimulate Metamorphosis in Larvae of the Deposit-Feeding Polychaete Capitella teleta: Implications for a Sensory Ligand-Gated Ion Channel

Marine sediments can contain B vitamins, presumably incorporated from settled, decaying phytoplankton and microorganisms associated with decomposition. Because B vitamins may be advantageous for the energetically intensive processes of metamorphosis, post-metamorphic growth, and reproduction, we tested several B vitamins to determine if they would stimulate larvae of the deposit-feeding polychaete Capitella teleta to settle and metamorphose. Nicotinamide and riboflavin individually stimulated larvae of C. teleta to settle and metamorphose, generally within 1–2 hours at nicotinamide concentrations as low as 3 µM and riboflavin concentrations as low as 50 µM. More than 80% of the larvae metamorphosed within 30 minutes at a nicotinamide concentration of 7 µM. The pyridine channel agonist pyrazinecarboxamide also stimulated metamorphosis at very low concentrations. In contrast, neither lumichrome, thiamine HCl, pyridoxine HCl, nor vitamin B₁₂ stimulated larvae of C. teleta to metamorphose at concentrations as high as 500 µM. Larvae also did not metamorphose in response to either nicotinamide or pyrazinecarboxamide in calcium-free seawater or with the addition of 4-acetylpyridine, a competitive inhibitor of the pyridine receptor. Together, these results suggest that larvae of C. teleta are responding to nicotinamide and riboflavin via a chemosensory pyridine receptor similar to that previously reported to be present on crayfish chela and involved with food recognition. Our data are the first to implicate B vitamins as possible natural chemical settlement cues for marine invertebrate larvae.