Settlement of larval blacklip abalone, Haliotis rubra, in response to green and red macroalgae

Surfaces from the habitat of adult Haliotis rubra were tested as inducers of larval settlement to determine the cues that larvae may respond to in the field. Settlement was high on the green algal species Ulva australis and Ulva compressa (Chlorophyta), the articulated coralline algae Amphiroa anceps and Corallina officinalis, and encrusting coralline algae (Rhodophyta). Biofilmed abiotic surfaces such as rocks, sand and shells did not induce settlement. Ulvella lens was also included as a control. Treatment of U. australis, A. anceps and C. officinalis with antibiotics to reduce bacterial films on the surface did not reduce the settlement response of H. rubra larvae. Similarly, treatment of these species and encrusting coralline algae with germanium dioxide to reduce diatom growth did not significantly reduce larval settlement. These results suggest that macroalgae, particularly green algal species, may play an important role in the recruitment of H. rubra larvae in the field and can be used to induce larval settlement in hatchery culture.     

Comparison of larval duration and pre- and post-settlement growth in two species of damselfish,Chromis atripectoralis andPomacentrus coelestis (Pisces: Pomacentridae), from the Great Barrier Reef

Light traps were used to capture larval fishes, immediately before settlement, at two localities 500 km apart on the Great Barrier Reef (GBR) in December, 1987. Samples from Lizard Island, in the northern GBR, and Davies Reef, in the central GBR, were dominated by two species of damselfish:Chromis atripectralis andPomacentrus coelestis. Analysis of otoliths revealed significant differences in both size and age at settlement between the two localities forP. coelestis, but not forC. atripectoralis. Growth rates determined for pre- and post-settlementP. coelestis suggested a sigmoidal growth trajectory through the larval life, with growth slowing as fishes approached the time of settlement. Post-settlement growth rates were faster than growth prior to settlement in both species. Growth in both species was, however, similar between localities. The relationship between fish size and otolith size was complex, varying both between pre- and post-settlement fishes, and among localities. This emphasizes the need to validate the relationship between fish size and otolith size before otoliths may be used to back-calculate individual growth trajectories.Contribution No. 500 from the Australian Institute of Marine Science     

Ingestion of a medusa (Aegina citrea) by the nematocyst-containing ctenophore Haeckelia rubra (formerly Euchlora rubra): phylogenetic implications

The rare ctenophore Haeckelia rubra (formerly Euchlora rubra) has long been known to have nematocysts rather than colloblasts in its tentacles. Five specimens were collected in the San Juan Archipelago, Washington State, USA in 1980 and 1981, and their feeding behavior was observed in the laboratory. We found that H. rubra readily eats the tentacles of a medusa, Aegina citrea, whose nematocysts (apotrichous isorhizas) are nearly identical in morphology to the nematocysts of the ctenophore. When H. rubra was offered 16 other species of hydromedusae and 1 siphonophore in the laboratory, the ctenophores showed little or no tendency to ingest these potential prey items. In addition to its routinely positive response to A. citrea, the ctenophore could be induced by manipulation and starvation to accept and ingest bits of the bodies of 4 additional species of hydromedusae and 1 siphonophore. These results, combined with the histological and rearing experiments of other investigators, leave little doubt that the nematocysts in H. rubra are not endogenous, but are kleptocnidae similar to those nematocysts retained and subsequently used by some species of nudibranchs that feed on Cnidaria. A close phylogenetic link between the Cnidaria and the Ctenophora is most unlikely.     

Genetic evidence for hybridisation between Haliotis rubra and H. laevigata

Seventeen abalone whose appearance was intermediate between the two commonly fished species in south-eastern Australia, blacklip (Haliotis rubra) and greenlip (H. laevigata), were collected between 1986 and 1989. Protein electrophoresis revealed that rare, morphologically intermediate abalone are predominantly F₁ hybrids; others are backcross individuals. There is also evidence of possible local introgression of H. rubra genes into H. laevigata and vice versa in sympatric populations. These two species exhibit marked morphological, behavioural and genetic differences, and yet hybridisation, although rare, occurs in at least several regions of sympatry. The commonly invoked explanations for the breakdown of species barriers, environmental disturbance and rarity of one of the parent species, do not appear applicable, unless microhabitat separation creates local rarity of one species. The frequency of hybridisation is discussed in relation to regional biogeography.     

Analysis of genetic structure of blacklip abalone (Haliotis rubra) populations using RAPD, minisatellite and microsatellite markers

 We investigated the utility of three polymerase chain-reaction (PCR)-based DNA molecular markers in analysing genetic structure of the populations of the blacklip abalone Haliotis rubra (Leach) of Victoria, Australia. The DNA markers included 84 randomly amplified polymorphic DNA (RAPD) bands amplified using six random primers, two minisatellites, GHR (putative growth-hormone-gene-repeat) and MIPR (putative mollusca-insulin-like peptide-gene-repeat), and three microsatellites, RUBGT1 [containing (GT)_n repeats], RUBCA1 [containing (CA)_n repeats] and RUBGACA1 [containing (GACA)_n repeats]. All three types of DNA markers revealed significant subdivision in the H. rubra populations along the coastline. This is postulated as being related to the abalone's relatively short pelagic period and limited dispersion. Further analysis revealed that a Point Cook population sampled from within the semi-enclosed Port Phillip Bay was distinct from two other central zone populations (Apollo Bay and Cape Schanck). The genotypes of microsatellites indicated excessive homozygotes across all the populations at all three microsatellite loci, and possible causes such as larval recruitment pattern and asynchronous spawning are discussed. The excessive homozygotes recorded for the three microsatellite loci contrast with those observed in the minisatellite loci GHR and MIPR, the heterozygosities of which were at Hardy–Weinberg equilibrium. Received: 17 March 1999 / Accepted: 24 November 1999     

Differences in abalone growth and morphology between locations with high and low food availability: morphologically fixed or plastic traits?

Many species of sedentary marine invertebrates exhibit large spatial variation in their morphology, which allow them to occupy a broad geographic distribution and range of environmental conditions. However, the detection of differences in morphology amongst variable environments cannot determine whether these differences represent a plastic response to the local environment, or whether morphology is genetically fixed. We used a reciprocal transplant experiment to test whether ‘stunted’ blacklip abalone (Haliotis rubra) are the result of a plastic response to the environment or fixed genetic trait. Furthermore, we related environmental factors, that affect food availability (density of abalone, water movement, algal cover and reef topography), to differences in growth and morphology. Morphological plasticity was confirmed as the mechanism causing morphological variation in H. rubra. Individuals transplanted to sites with ‘non-stunted’ H. rubra grew significantly faster when compared to stunted controls, whilst individuals transplanted to stunted sites grew significantly slower compared to non-stunted controls. The growth response was greater for individuals transplanted from ‘non-stunted’ to ‘stunted’ sites, suggesting that the environmental stressors in morphologically ‘stunted’ habitat are stronger compared to locations of faster growing morphology. We propose that these differences are related to resource availability whereby low algal cover and topographic simplicity results in stunted populations, whereas high algal abundance and topographic complexity results in non-stunted populations.     

Larval settlement in the serpulid polychaete Hydroides elegans in response to bacterial films: an investigation of the nature of putative larval settlement cue

Larval settlement in the marine polychaete Hydroides elegans (Haswell) is induced by certain bacteria in marine biofilms. The exact nature of the settlement cue that larvae of H. elegans receive from these bacteria remains unknown. In this study, we revealed some properties of the bacterially derived larval settlement cue by investigating the larval settlement inductive activity of two bacterial strains after various treatments. These two bacterial strains, Roseobacter sp. and an α-subclass Proteobacteria, are highly inductive to larval settlement of H. elegans. The larvae responded similarly to Roseobacter and Proteobacteria in all the larval settlement bioassays, suggesting that the larval settlement-inducing substances produced by these bacteria may share common characteristics. First of all, the larvae did not settle in the seawater conditioned by the bacteria attached as a film or by the bacteria that were freely suspended in seawater. The results suggest that the putative larval settlement cue is not released into seawater and, therefore, should be associated with the surface of the bacteria. Secondly, formaldehyde treatment entirely eliminated the larval settlement induction activity of the bacterial films, and streptomycin treatment reduced the percentage of larval settlement on the bacterial films in a concentration-dependent manner. Since both treatments can kill bacteria with little damage to the surface chemistry of bacterial cells, the decline in larval settlement is suggested be due to a reduction of the viable bacterial population in the bacterial films. In fact, the reduction of larval settlement in the streptomycin treatments coincided with the decrease in viable bacterial populations in broth cultures containing respective concentrations of streptomycin. These results suggest that the viability of Roseobacter and Proteobacteria is important to their settlement induction effect. Since the larval settlement induction activity of the bacterial strains appears to correlate with their viability, we suggest that the putative larval settlement cue is derived from a metabolic pathway in the bacteria and that the cue is exported to and concentrated at the extracellular polymer matrix of the bacterial cell, at which the larvae establish contact with the bacteria. The larval settlement cue may be highly susceptible to degradation so that a metabolically active bacterial film is needed to maintain the putative cue at a concentration that surpasses the threshold for induction of larval settlement. Received: 14 October 1998 / Accepted: 5 September 2000     

Low genetic differentiation between isolated populations of the colonial ascidian Symplegma rubra Monniot, C. 1972

Pelagic larvae are highly important for maintaining the gene flow among populations of sessile marine invertebrates. Colonial ascidians consist, exclusively, of brooding species, with lecithotrophic larvae that have a limited dispersal. As a result, there is a marked differentiation among populations. In this work, we used allozyme electrophoresis to access the genetic variation in four populations of Symplegma rubra, a colonial ascidian frequently found in the intertidal zone of Southeastern Brazilian coast. High variability was found at three of the four sites sampled, the exception being Praia Grande in the State of Rio de Janeiro. At this site, there was a great preponderance of clones, which possibly reflected the enclosed nature of the location and its low water circulation that reduce the dispersal capabilities of these animals. S. rubra did not conform to expectations for random mating (Hardy–Weinberg equilibrium): there was a deficit of heterozygotes that was more related to the small population size than to inbreeding processes, since F _is analysis per locus revealed a deficiency of heterozygotes at only one locus—MDH*. The greatest variation in allele frequency was found for GPI-2*. Analyses of genetic variability revealed moderate differentiation among the populations (F _ST=0.051), which was unexpected for a species with a low dispersal capability. Rafting, a frequently underestimated means of dispersal, may be the main mode of gene flow in this species over large areas, since colonies of S. rubra are frequently seen growing on drift material and there is no evidence that the larva survive for a long time in the plankton.     

Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans

The serpulid polychaete Hydroides elegans Haswell, 1883 is an early colonist of new substrata in Pearl Harbor, Oahu, Hawaii. When metamorphically competent, larvae of H. elegans will settle rapidly upon an acceptably biofilmed surface, but not on a clean surface. In this study we found the ability of larvae to respond selectively to inductive surfaces to be retained for at least 3 wk. Of a series of bacterial strains isolated from Hawaiian marine biofilms, 13 induced larval settlement, 11 gave moderate or mixed results, and 10 others did not stimulate the settlement of H. elegans. The amount of settlement induced by monospecific strains was rarely as great as with natural, multispecies films. Most of the isolated bacteria were motile Gram-negative rods, but Gram-positive strains were also present, and diverse metabolic types were represented in the study. Biofilms killed by treatment with heat, ultraviolet radiation or chemical fixatives were no longer inductive. Soluble, dialyzable, heat-stable bacterial products induced settlement and metamorphosis more slowly. The range of bacteria producing an inductive signal suggests either that there are multiple cues, or that the cue is common to many bacteria. Chemical signals characteristic of early microbial biofilms may indicate freshly available substrata with optimal potential for the growth and survival of H. elegans. Received: 30 January 1998 / Accepted: 12 September 1998     

Larval recruitment in response to manipulated field flows

Settlement responses to boundary-layer flow of several invertebrate taxa, including the hydroid Tubularia crocea, the bryozoans Bugula turrita and Schizoporella unicornis, and the tube-building polychaete Hydroides dianthus were studied in manipulated field flows in Great Harbor, Massachusetts, USA. During three experiments in 1989 and two in 1990, densities of newly-recruited larvae were measured on flat plates, whose flow regimes had been manipulated by altering the leading-edge configurations. Settlement responses to flow were strongly species-specific, with T. crocea preferring regions of both high turbulence and strong shear stress, and S. unicornis settling a most exclusively in regions of high shear stress. B. turrita settled most prominently in regions of reduced shear stress, exhibiting settlement patterns that closely approximated predictions from a model of passive particle contact. H. dianthus showed a moderate avoidance of regions with high shear stress. These results indicate that boundary-layer flows affect settlement of several common encrusting species, a probable consequence of larval behaviors such as substrate rejection or exploration in response to flow. These responses are likely to generate patchiness during initial colonization of natural habitats, and certainly affect colonization of settlement panels commonly used in marine ecological studies.     

Effects of salinity and adult extract on settlement of the oligohaline barnacle Balanus subalbidus

Balanus subalbidus (Henry) has the most oligohaline distribution of three congeneric barnacles in Chesapeake Bay and tolerates prolonged exposure to fresh water. We studied larval settlement (i.e., permanent attachment and metamorphosis) of B. subaldius in the laboratory, over a 3 yr period, May 1989 to March 1992, under the following conditions: (1) across an array of salinities at 25°C in the presence and absence of settlement factor consisting of adult B. subalbidus extract; (2) in the presence of conspecific or congeneric settlement factors; and (3) cyprids which were, and were not, induced to delay metamorphosis were compared in their capacities to settle in a range of salinities. Discrepancies between salinity profiles of larval settlement in the laboratory and adult oligohaline distribution in the estuary were striking, and there was a significant interaction between salinity and settlement factor. Averaging results of four different batches of larvae, although peak settlement (87±9%) of B. subalbidus occurred at 2 ppt salinity in the presence of adult cue, substantial settlement also occurred at higher salinities: >70% at 5, 10 and 15 ppt; and 47% at 20 and 25 ppt. In addition, settlement in the absence of settlement factor was relatively high (>50%) and peaked at mid-salinity ranges (e.g. 56±10% at 15 ppt). Variation observed in settlement among larval batches reflected detailed differences in settlement between adjacent test salinities. No difference in settlement occurred between replicate aliquots of cyprids within a batch. Cyprids of B. subalbidus settled most abundantly in the presence of settlement factor extracted from conspecifics, followed in decreasing order by settlement factor extracted from B. improvisus and B. eburneus. Delay of metamorphosis produced by keeping B. subalbidus cyprids for 8 d at 5°C resulted in a decreased level of settlement, but settlement frequency patterns of delayed and non-delayed cyprids were indistinguishable relative to salinity. These results indicate that the oligohaline distribution of adult B. subalbidus is probably not determined by larval behavior at settlement. We suggest that pre-settlement behavior, resulting in larval retention in low saline waters, could be an important factor in determining distribution of this species.     

Temporal and spatial variability in settlement of the sea urchin<Emphasis Type="Italic"> Paracentrotus lividus</Emphasis> in the NW Mediterranean

Settlement into the benthic habitat may be an important process in regulating sea urchin abundance, which potentially modifies the structure of benthic communities. Strong settlement events may increase sea urchin abundance beyond a certain threshold, leading to the formation of coralline barrens (overgrazed communities with a dominance of encrusting coralline algae). To understand the role of settlement in regulating sea urchin populations we first need to determine settlement variability. Temporal variation in settlement of the sea urchin Paracentrotus lividus was monitored at three sites in the Medes Islands, NW Mediterranean, during three settlement seasons (March 1998 through October 2000). Spatial variation in settlement was studied in 1999 at 50 sites along a gradient of exposures to waves and currents, inside and outside the archipelago, and separated by distances from tens to thousands of meters. Bathymetric distribution of settlement was also studied in 2000 at six sites at 5, 10, 15 and 20 m depths. Settlement of P. lividus occurred in a single annual peak within 3 weeks in May–June. Differences in settlement between years were more than two orders of magnitude. Spatial variability was found at all scales investigated, showing strong patchiness at the smallest spatial scales (tens of meters). Sea urchins settled preferentially at depths between 5 and 10 m. Substratum type, level of protection, and adult population densities were not significant in determining settlement. However, settlement was found to be related to the degree of exposure to waves and currents, indicating that physical processes are very important at the spatial scales investigated. This greatly variable settlement is a necessary, although not sufficient, condition to create gradients of adult P. lividus abundance. Further studies should be designed to investigate the interaction between settlement strength and post-settlement mortality.Communicated by O. Kinne, Oldendorf/Luhe     

The role of root organic acids in the tolerance of Festuca rubra to zinc,lead and cadmium

Abstract

Festuca rubra L. plants are pseudometallophytes colonizing abandoned Pb/Zn mine areas, successfully employed in phytostabilization. To study the contribution of low-molecular weight organic acids to metal tolerance, F. rubra plants were grown for three months in hydroponics with Cd (1.8, 18 and 36 µmol?L^?1), Pb (50, 250 and 500?µmol?L^?1) and Zn (0.3, 3 and 6?mmol?L^?1), separately, and in ternary combination (18?µmol?L^?1 Cd + 250?µmol?L^?1 Pb + 0.3?mmol?L^?1 Zn). The roots retained most of the metals but their distribution from shoot to root was altered when the plants were treated with the ternary combination. The main organic acids in roots were citrate and malate. At the lowest concentrations, the metals caused small reductions in biomass, had no effects on photosynthetic pigments nor on malondialdehyde, but led to increases in root organic acids. At higher concentrations, phytotoxic responses were observed, associated with a decline of citrate and malate in the roots.     

Effect of microbial films on settlement of bryozoan larvae (Bugula simplex,B. stolonifera and B. turrita)

The influence of microbial films on larval settlement was studied for sympatric species of cellularioid cheilostome bryozoans (Bugula simplex, B. stolonifera, and B. turrita). Settlement experiments were conducted in the laboratory in 1981 with and without a choice of filmed or unfilmed substrates. When given a choice of substrates, the larvae of all three bryozoan species significantly preferred the filmed substrate. When not given a choice of substrates, both B. simplex and B. turrita larvae tended not to settle on the unfilmed substrate, while the filmed and unfilmed substrates were equally attractive to B. stolonifera. Microbial films enhanced the settlement of all three species.     

Settlement, recruitment and potential predators and competitors of juvenile echinoderms in the rocky subtidal zone

Recruitment patterns of marine invertebrates are affected both by settlement and early post-settlement events. This study examined the settlement and recruitment patterns of echinoderms at three sites in the rocky subtidal zone of Bocabec Cove, Bay of Fundy, Canada using artificial turf collectors and quadrats on the natural substrate. Potential predators were quantified at two of the sites along transects and in 1-m² quadrats. Both potential predators and competitors were quantified in 0.0625-m² quadrats. Settlement varied across sites (1.5–3 km apart) and two years of sampling (2004, 2005). The site of most potential settlement differed for the three groups of echinoderms: sea urchins (Strongylocentrotus droebachiensis), sea stars (Asterias spp.) and sea cucumber (Psolus fabricii). Settlement densities on the artificial turf collectors tended to be greater than the densities of settlers on the natural substrate. On the natural substrate, the only significant difference between densities of juveniles over time was that newly settled sea stars were found in July and were not found the following October. Large lobsters and carnivorous worms were potential predators with densities that varied between sites. Potential competitors that differed in abundance between sites were herbivorous gastropods and conspecifics for sea urchins; and carnivorous worms for sea stars. This study suggests that patterns of recruitment are either set up by patterns of settlement or by events during the first few weeks/months on the benthic substrate for these echinoderms.     

Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement

Settlement sites of marine invertebrate larvae are frequently influenced by positive or negative cues, many of which are chemical in nature. Following from the observation that many shallow-water, Hawai'ian marine macroalgae are free of fouling by sessile invertebrates, we predicted that the algae are chemically protected and dependent on either surface-bound or continuously released soluble compounds to deter settling invertebrate larvae. To address the importance of waterborne algal compounds, we experimentally determined whether larvae of two of Hawai'i's dominant hard-surface fouling organisms, the polychaete tube worm Hydroides elegans and the bryozoan Bugula neritina, would settle in the presence of waters conditioned by 12 species of common Hawai'ian macroalgae (representing the Phaeophyta, Chlorophyta, Rhodophyta and Cyanophyta). The results included a full spectrum of biological responses by each larval species to waterborne algal compounds. Larval responses to conditioned water were consistent for each algal species, but the outcomes were not predictable based on the taxonomic relationships of the algae. For example, among the species of Phaeophyta examined, different conditioned waters were: (1) toxic, (2) inhibited settlement, (3) simulated settlement, or (4) had no effect, compared to larvae in control dishes containing filtered seawater. Additionally, larval responses to aged (24 h) conditioned waters could not be predicted from the results of assays run with conditioned waters utilized immediately after preparation. Finally, settlement by larvae of one species did not predict outcomes of tests for the other species. Four of 12 shallow-reef Hawai'ian macroalgae tested released compounds into surrounding waters that immediately killed or inhibited settlement by both H. elegans and B. neritina (toxic: Dictyota sandvicensis; inhibitory: Halimeda discoidea, Sphacelaria tribuloides, Ulva reticulata); the remaining 8 algal species prevented settlement by one of these fouling organisms but for the other had no effect or, in some cases, even stimulated settlement     

Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat

One of the great mysteries of coral-reef fish ecology is how larvae locate the relatively rare patches of coral-reef habitat on which they settle. The present study aimed to estimate, by experiments in aquaria, the sensory modalities of coral-reef fish larvae for senses used in searching for their species settlement habitat. Larval recognition of settlement habitat can be based on the detection of conspecifics and/or of characteristics of coral habitat using visual, chemical and mechanical cues. For this study, larvae were captured with crest nets and were then introduced into experimental tanks that allowed testing of each type of cue separately (visual, chemical or mechanical cues). Among the 18 species studied, 13 chose their settlement habitat due to the presence of conspecifics and not based on the characteristics of coral habitat, and 5 species did not move toward their settlement habitat (e.g. Scorpaenodes parvipinnis, Apogon novemfasciatus). Among the different sensory cues tested, two species used the three types of cues (Parupeneus barberinus and Ctenochaetus striatus: visual, chemical and mechanical cues), six used two types (e.g. Myripristis pralinia: visual and chemical cues; Naso unicornis: visual and mechanical cues), and five used one type (e.g. Chrysiptera leucopoma: visual cues; Pomacentrus pavo: chemical cues). These results demonstrate that many coral-reef fish larvae could in practice use sensory cues for effective habitat selection at settlement, and have the ability to discriminate species-specific sensory cues.Communicated by J. Krause     

Population dynamics of the barnacle <Emphasis Type="Italic">Chthamalus montagui</Emphasis> at two spatial and temporal scales in northern Spain

This study describes spatial and temporal patterns of variability in population parameters in the barnacle Chthamalus montagui Southward in three localities of northern Spain and evaluates whether density-dependent settlement may regulate population dynamics. The sampling design considered two spatial scales, localities and sites within localities, and two temporal scales, years and six month intervals. Density, amount of free space, mortality, growth rate and magnitude of settlement (both absolute and per unit of free space) were obtained from photographs of permanent quadrats and from direct counts in the field. The number of settlers in scraped and untouched quadrats was used to estimate the importance of the presence of conspecifics in settlement. Significant variation at the two spatial and temporal scales was found for most parameters. Large spatial and temporal variations in adult mortality rate, density, and settlement were observed. Patterns of mortality were not consistent with differences in density among localities. Differences in settlement among localities were maintained through time. We suggest that magnitude of settlement is regulated by persistent features such as topography or local water circulation. We assume that early post-settlement mortality does not differ among localities. In the absence of differential mortality, settlement determines average population density within localities. Within localities, settlement was independent of density and free space. No consistent evidence was found on preferential settlement at the vicinity of conspecifics. The main conclusion is that density-dependent settlement is not relevant for the regulation of the populations of C. montagui in the northern Spain. Regulation might occur by density-dependent processes within the adult fraction of the population and/or the larval phase before settlement.