Population structure, growth and distribution of Lingula anatina (Brachiopoda) in Queensland, Australia

Size-frequency data collected in large samples from five populations of Lingula anatina from North Queensland intertidal sandflats conformed to previously known brachiopod size-frequency distributions. Probability paper analysis of the samples and constituent sub-samples confirmed that all the distributions had a hidden poly-modality resulting from a long but defined breeding season. Two patterns of annual recruitment were revealed; the first is the periodic failure of the populations to gain recruits and the second is one of patchy distribution of settlement cohorts. These patterns introduce sampling bias into the derivation of lingulid size frequency curves unless compensated by more extensive sampling methods than have previously been considered adequate. The interpretation of year classes has enabled a growth curve to be derived. The populations inhabited predominantly sandy sub-strates and displayed aggregated distributions. Littoral distribution of the species is regarded as optimal rather than marginal.     

Temporal patterns of breeding and larval settlement in a temperate population of the tropical anemonefish,Amphiprion clarkii

The breeding of the anemonefish,Amphiprion clarkii, and the settlement of larvae were observed in temperate Japan. Spawning had two peaks near the first and the third quarter of the moon in 1983, but did not in 1984. The clutch size varied greatly during the breeding season, with a peak from the second half of June to the second half of July. Adult fishes inhibited larval settlement. The proportion of disappeared 0-year olds to the total was higher in 1984 than in 1983. This difference might be mainly due to the difference in the degree of crowding in each sea anemone. The period of larval settlement closely paralleled the breeding season. The larvae settled abundantly around the first quarter and the third quarter of the moon in 1983, and did from the third quarter to the first quarter in 1984. In both years, the number of settled larvae was more from the full moon to the new moon than the new moon to the full moon. The daily pattern of larval settlement did not reflect that of breeding.     

Transcriptional signature of accessory cells in the lateral line, using the Tnk1bp1:EGFP transgenic zebrafish line

Background

A metamorphic life-history is present in the majority of animal phyla. This developmental mode is particularly prominent among marine invertebrates with a bentho-planktonic life cycle, where a pelagic larval form transforms into a benthic adult. Metamorphic competence (the stage at which a larva is capable to undergo the metamorphic transformation and settlement) is an important adaptation both ecologically and physiologically. The competence period maintains the larval state until suitable settlement sites are encountered, at which point the larvae settle in response to settlement cues. The mechanistic basis for metamorphosis (the morphogenetic transition from a larva to a juvenile including settlement), i.e. the molecular and cellular processes underlying metamorphosis in marine invertebrate species, is poorly understood. Histamine (HA), a neurotransmitter used for various physiological and developmental functions among animals, has a critical role in sea urchin fertilization and in the induction of metamorphosis. Here we test the premise that HA functions as a developmental modulator of metamorphic competence in the sea urchin Strongylocentrotus purpuratus.

Results

Our results provide strong evidence that HA leads to the acquisition of metamorphic competence in S. purpuratus larvae. Pharmacological analysis of several HA receptor antagonists and an inhibitor of HA synthesis indicates a function of HA in metamorphic competence as well as programmed cell death (PCD) during arm retraction. Furthermore we identified an extensive network of histaminergic neurons in pre-metamorphic and metamorphically competent larvae. Analysis of this network throughout larval development indicates that the maturation of specific neuronal clusters correlates with the acquisition of metamorphic competence. Moreover, histamine receptor antagonist treatment leads to the induction of caspase mediated apoptosis in competent larvae.

Conclusions

We conclude that HA is a modulator of metamorphic competence in S. purpuratus development and hypothesize that HA may have played an important role in the evolution of settlement strategies in echinoids. Our findings provide novel insights into the evolution of HA signalling and its function in one of the most important and widespread life history transitions in the animal kingdom - metamorphosis.     

Studies on the factors influencing larval settlement in Balanus amphitrite and Mytilus galloprovincialis

Understanding of factors influencing settlement(attachment and metamorphosis) of marine invertebratelarvae is of great importance in aquaculture andcontrol of biofouling. The influence of two factors onsettlement of larvae was assessed from two separateinvestigations: 1, the influence of age (endogenousfactor) on cyprids of the barnacle Balanusamphitrite; and 2, the influence of a microbial film(exogenous factor) on pediveligers of the mussel Mytilus galloprovincialis.The settlement response of cypris larvae of B.amphitrite was found to be age-dependent. Oldercyprids responded more readily to settlement factorsthan newly molted ones. In M.galloprovincialis, competent pediveligers settled inresponse to a microbial filmed surface but not toan unfilmed surface. Moreover, a factor with MW of lessthan 5000 dalton, derived from culture medium of abacterial strain C1.1 (Pseudomonas-Alteromonasgroup), induced the settlement of M. galloprovincialis larvae.Thus, marine invertebrate larvae may require a periodof competence acquisition, during which they arepoorly responsive to settlement inducers. Uponacquisition of competence, larvae readily respondto external cues (e.g. microbial film, bacterialextracellular products).     

Genetic structure of three populations of the 'living fossil' brachiopod Lingula from Queensland, Australia

An electrophoretic survey of enzyme variation demonstrates that the genomes of three populations of the inarticulate brachiopod Lingula contain a higher level of variability than the average for marine, tropical invertebrates, and for other brachiopods. Genetic distances between populations from localities up to 1200 km apart were very small, indicating that the populations belong to a single species, L. anatina Lamarck. These data suggest that larval dispersal is capable of maintaining a homogeneous gene pool over this range. It is predicted that the dispersal mechanism is sufficiently efficacious to ensure gene-flow throughout most of the Indo-West Pacific distribution of Lingula. Further investigations of genetic distance should support the hypothesis, based on studies of adult and larval morphology, that many presently recognized species should be reassigned to L. anatina.     

Induction of settlement in mussel (Perna canaliculus) larvae by vessel noise

Underwater sound plays an important role in the settlement behaviour of many coastal organisms. Large steel-hulled vessels are known to be a major source of underwater sound in the marine environment. The possibility that underwater sound from vessels may promote biofouling of hulls through triggering natural larval settlement cues was investigated for the mussel, Perna canaliculus. The mussel larvae showed significantly faster settlement when exposed to the underwater noise produced by a 125-m long steel-hulled passenger and freight ferry. Median time to attachment on the substrata (ie settlement) was reduced by 22% and the time taken for all experimental larvae to settle was reduced by 40% relative to a silent control. There was no difference in the survival of the mussel larvae among the various noise treatments. The decrease in settlement time of the mussel larvae appeared to correlate with the intensity of the vessel sound, suggesting that underwater sound emanating from vessels may be an important factor in exacerbating hull fouling by mussels.     

Evidence of postbreeding prospecting in a long‐distance migrant

1. Organisms assess biotic and abiotic cues at multiple sites when deciding where to settle. However, due to temporal constraints on this prospecting, the suitability of available habitat may be difficult for an individual to assess when cues are most reliable, or at the time they are making settlement decisions. For migratory birds, the postbreeding season may be the optimal time to prospect and inform settlement decisions for future breeding seasons.
2. We investigated the fall movements of flammulated owls (Psiloscops flammeolus) within breeding habitat after fledglings had gained independence and before adults left for migration. From 2013 to 2016, we trapped owls within a breeding population wherein all nesting owls and their young have been banded since 1981. We used stable isotopes in combination with mark–recapture data to identify local individuals and differentiate potential prospecting behavior from other seasonal movements such as migration or staging.
3. We commonly captured owls in the fall—predominantly hatch‐year owls—that were not known residents of the study area. Several of these nonresident owls were later found breeding within the study area. Stable isotope data suggested a local origin for virtually all owls captured during the fall.
4. Our results suggest that hatch‐year flammulated owls, but also some after‐hatch‐year owls, use the period between the breeding season and fall migration to prospect for future breeding sites. The timing of this behavior is likely driven by seasonally variable costs associated with prospecting.
5. Determining the timing of prospecting and the specific cues that are being assessed will be important in helping predict the extent to which climate change and/or altered disturbance regimes will modify the ecology, behavior, and demographics associated with prospecting.

     

Localization of sensory mechanisms utilized by coral planulae to detect settlement cues

Coral planulae are induced to settle and metamorphose by contact with either crustose coralline algae or marine bacterial biofilms. Larvae of two coral species, Pocillopora damicornis and Montipora capitata, which respond to different metamorphic cues, were utilized to investigate the sensory mechanisms used to detect metamorphic cues. Because the aboral pole of the coral planula is the point of attachment to the substratum, we predicted that it is also the point of detection for cues. To determine where sensory cells for cues are localized along the body, individual larvae were transversely cut into oral and aboral portions at various levels along the oral–aboral axis, and exposed to settlement‐inducing substrata. Aboral ends of M. capitata metamorphosed, while oral ends continued to swim. However, in larvae of P. damicornis, ¾ oral ends (i.e., lacking the aboral pole) were also able to metamorphose, indicating that the cells that detect cues may be distributed along the sides of the body. These cells do not correspond to FMRFamide‐immunoreactive cells that are present throughout the body. Cesium ions induced both aboral and oral ends of larvae of both species to settle, suggesting that oral ends have not lost their capacity to metamorphose, despite lacking sensory cells to detect natural cues. To determine whether sensory cells in larvae of P. damicornis are restricted to one side of the body, swimming behavior over substrata was observed in larvae labeled with diI, a red fluorescent lipophilic membrane stain. The larvae were found to rotate around the oral–aboral axis, with their surface against the substratum, not favoring a particular side for detecting cues. While clarifying the regions of the larval body important for settlement and metamorphosis in coral planulae, we conclude that significant differences between coral species may be due to differences in the distribution of sensory structures in relation to different planular sizes.     

Articulated coralline algae of the genus Amphiroa are highly effective natural inducers of settlement in the tropical abalone Haliotis asinina

The initiation of metamorphosis in marine invertebrates is strongly linked to the environment. Planktonic larvae typically are induced to settle and metamorphose by external cues such as coralline algae (Corallinaceae, Rhodophyta). Although coralline algae are globally abundant, invertebrate larvae of many taxa settle in response to a very limited suite of species. This specificity impacts population structure, as only locations with the appropriate coralline species can attract new recruits. Abalone (Gastropoda, Haliotidae) are among those taxa in which closely related species are known to respond to different coralline algae. Here we identify highly inductive natural cues of the tropical abalone Haliotis asinina. In contrast to reports for other abalone, the greatest proportion of H. asinina larvae are induced to settle and metamorphose (92.8% to 100% metamorphosis by 48 h postinduction) by articulated corallines of the genus Amphiroa. Comparison with field distribution data for different corallines suggests larvae are likely to be settling on the seaward side of the reef crest. We then compare the response of six different H. asinina larval families to five different coralline species to demonstrate that induction by the best inductive cue (Amphiroa spp.) effectively extinguishes substantial intraspecific variation in the timing of settlement.     

Field-based video observations of wild barnacle cyprid behaviour in response to textural and chemical settlement cues

Many marine invertebrate larvae respond behaviourally to environmental settlement cues, yet behaviours are often only inferred from settlement patterns or are limited to laboratory studies. The behaviour of wild cypris larvae of Semibalanus balanoides L. was filmed on settlement tiles in the field. Tiles were of five different textures with a nested treatment of crude conspecific adult extract (AE). The effects of texture and AE on eleven defined behaviours were analysed. Texture affected the gross and net exploratory distances, velocity, acceleration and time spent exploring. AE attracted more cyprids during the first minute of immersion and increased the time spent on surfaces. Relatively few arrivals that either travel far and fast, or exit the surface rapidly, may indicate a lower chance of settlement. An increase in time spent on a surface may increase the probability of being in contact with the surface when the sign stimulus to settle occurs.     

Settlement behavior of Chthamalus anisopoma larvae largely determines the adult distribution

Summary In the northern Gulf of California the adult distribution of the intertidal barnacle species, Chthamalus anisopoma, on exposed shores is approximately between 0.0 and 2.0 m above mean low water (MLW). The species is typically absent in protected (from wave splash) areas. In this study, I examined a series of alternative hypotheses relating to the factors that could be responsible for limiting the distribution. Post-settlement factors appear to be unimportant because settlement was largely restricted to areas within the adult distribution. Two processes could account for the high correlation between settlement and adult distributions. First, hydrodynamic factors could restrict deposition of larvae to sites that coincidently were in areas in which individuals could survive to maturity. Second, larvae may choose to settle only on sites where they can survive to maturity. Of the two, the later was supported as settlement could be induced on surfaces outside the adult distribution using transplanted adult conspecifics as cues. Thus, competent larvae were present outside the adult distribution of Chthamalus zone but did not settle under normal conditions. Also, there was no evidence that pre-emption of space by other sessile species, by itself, restricted the distribution of Chthamalus. Settlement within the existing adult distribution may be an evolutionary response to increased mortality for individuals settling outside the adult distribution compared to those settling within it.     

Temporal variability of settlement in Carapidae larvae at Rangiroa atoll

Carapidae (or pearlfish) are eel-like fishes living inside different invertebrates, such as holothurians, sea stars or bivalves. In some Polynesian areas where they live in sympatry, several species (Carapus homei, Carapus mourlani, Carapus boraborensis and Encheliophis gracilis) are able to inhabit the same host species. The heterospecific infestation rate is very rare, suggesting that the four species can compete for their hosts. Some differences in settlement period, breeding period and in pelagic larval duration (PLD) could allow better characterisation of the life history of each species. More than 700 larvae were collected during an entire year on the Rangiroa atoll (French Polynesia). Each species was identified; their settlement pattern was examined and their PLD was deduced from otolith (sagittae) increments. In the four collected species, the settlement pattern differed: C. homei and C. mourlani settle on the reef during the entire year, and show an asynchronous and diffuse breeding cycle. C. boraborensis and E. gracilis have a shorter settlement period which could be compatible with breeding synchronisation. As most reef fishes, Carapidae larvae mainly settle during moonless nights. Moreover, each species presents some plasticity, allowing it to settle on the reef under suitable conditions.     

Coral larvae settle at a higher frequency on red surfaces

Although chemical cues serve as the primary determinants of larval settlement and metamorphosis, light is also known to influence the behavior and the settlement of coral planulae. For example, Porites astreoides planulae settle preferentially on unconditioned red substrata. In order to test whether this behavior was a response to color and whether other species also demonstrate color preference, settlement choice experiments were conducted with P. astreoides and Acropora palmata. In these experiments, larvae were offered various types of plastic substrata representing three to seven different color choices. Both species consistently settled on red (or red and orange) substrata at a higher frequency than other colors. In one experiment, P. astreoides settled on 100% of red, plastic cable ties but failed to settle on green or white substrata. In a second experiment, 24% of larvae settled on red buttons, more than settled on six other colors combined. A. palmata settled on 80% of red and of orange cables ties but failed to settle on blue in one experiment and settled on a greater proportion of red acrylic squares than on four other colors or limestone controls in a second experiment. The consistency of the response across a variety of plastic materials suggests the response is related to long-wavelength photosensitivity. Fluorescence and reflectance spectra of experimental substrata demonstrated that the preferred substrata had spectra dominated by wavelengths greater than 550 nm with little or no reflection or emission of shorter wavelengths. These results suggest that some species of coral larvae may use spectral cues for fine-scale habitat selection during settlement. This behavior may be an adaptation to promote settlement in crustose coralline algae (CCA)-dominated habitats facilitating juvenile survival.     

Can settlement in natal-like habitat explain maladaptive habitat selection?

The study of habitat selection has long been influenced by the ideal free model, which maintains that young adults settle in habitat according to its inherent quality and the density of conspecifics within it. The model has gained support in recent years from the finding that conspecifics produce cues inadvertently that help prebreeders locate good habitat. Yet abundant evidence shows that animals often fail to occupy habitats that ecologists have identified as those of highest quality, leading to the conclusion that young animals settle on breeding spaces by means not widely understood. Here, we report that a phenomenon virtually unknown in nature, natal habitat preference induction (NHPI), is a strong predictor of territory settlement in both male and female common loons (Gavia immer). NHPI causes young animals to settle on natal-like breeding spaces, but not necessarily those that maximize reproductive success. If widespread, NHPI might explain apparently maladaptive habitat settlement.     

Field-based video observations of wild barnacle cyprid behaviour in response to textural and chemical settlement cues

Many marine invertebrate larvae respond behaviourally to environmental settlement cues, yet behaviours are often only inferred from settlement patterns or are limited to laboratory studies. The behaviour of wild cypris larvae of Semibalanus balanoides L. was filmed on settlement tiles in the field. Tiles were of five different textures with a nested treatment of crude conspecific adult extract (AE). The effects of texture and AE on eleven defined behaviours were analysed. Texture affected the gross and net exploratory distances, velocity, acceleration and time spent exploring. AE attracted more cyprids during the first minute of immersion and increased the time spent on surfaces. Relatively few arrivals that either travel far and fast, or exit the surface rapidly, may indicate a lower chance of settlement. An increase in time spent on a surface may increase the probability of being in contact with the surface when the sign stimulus to settle occurs.     

Developmental dimorphism: consequences for larval behavior and dispersal potential in a marine gastropod

Specific effects of alternative developmental programs on swimming and settlement behavior for marine larvae have not been identified experimentally. A major impediment to this research has been the rarity of species with variable development. Here, we compared traits related to movement and habitat selection for different ontogenetic stages of long-lived, feeding larvae (planktotrophic) and short-lived, nonfeeding larvae (lecithotrophic) of the herbivorous gastropod Alderia modesta. Newly hatched planktotrophic larvae swam in meandering paths with equal rates of upward and downward movement. As planktotrophic larvae developed towards competence (physiological ability to metamorphose), their swimming paths became straighter, faster, and increasingly directed towards the bottom, traits shared by newly hatched lecithotrophic larvae. Despite differing in developmental history, competent planktotrophic (32-d-old) and lecithotrophic larvae (competent upon hatching) exhibited qualitatively similar swimming behaviors and substrate specificity. However, lecithotrophic larvae moved downward at twice the speed of competent planktotrophic larvae, potentially producing a 5-fold higher rate of contact with the bottom in natural flows. Competent larvae swam downwards rather than passively sinking, even though sinking rates were faster than swimming speeds; active swimming may allow larvae to keep the velum extended, permitting rapid response to chemical settlement cues and promoting successful habitat colonization. Differences between larvae of the two development modes may reflect fine-tuning by selection of traits important for dispersal and settlement into patchy adult habitats.     

Metamorphic Competence, a Major Adaptive Convergence in Marine Invertebrate Larvae

Larvae from diverse marine-invertebrate phyla are able to respondrapidly to environmental cues to settlement and to undergo veryrapid metamorphic morphogenesis because they share the developmentaltrait of metamorphic competence. The competent state, characteristicof larvae as diverse as those of cnidarian planulae, molluscanveligers, and barnacle cyprids, is one in which nearly all requisitejuvenile characters are present in the larva prior to settlement.Thus metamorphosis, in response to more or less specific environmentalcues (inducers), is mainly restricted to loss of larva-specificstructures and physiological processes. Competent larvae oftwo "model marine invertebrates" studied in the authors' laboratory,the serpulid polychaete Hydroides elegans and the nudibranchPhestilla sibogae, complete metamorphosis in about 12 and 20hr, respectively. Furthermore, little or no de novo gene actionappears to be required during the metamorphic induction processin these species. Contrasting greatly with the slow, hormonallyregulated metamorphic transitions of vertebrates and insects,competence and consequent rapid metamorphosis in marine invertebratelarvae are conjectured to have arisen in diverse phylogeneticclades because they allow larvae to continue to swim and feedin the planktonic realm while simultaneously permitting extremelyfast morphological transition from larval locomotory and feedingmodes to a different set of such modes that are adaptive tolife on the sea bottom.     

Rapid settlement in broadcast spawning corals: implications for larval dispersal

Broadcast spawning of gametes with planktonic development of larvae is the most common reproductive mode in tropical corals, and is generally thought to optimize the dispersal potential of larvae. To this end, many previous studies of coral larval dispersal have focused on the maximum time larvae can remain competent to settle and consequently how far they might disperse. However, dispersal ability of broadcast-spawned coral larvae will be linked, at least in part, to the minimum time to settlement competency as well as the length of the planktonic period—although estimates of minimum time to competency remain largely anecdotal, with few rigorous studies of the pre-competent period. To determine the minimum time to larval settlement in two species of broadcast-spawning coral ( Platygyra daedalea and Goniastrea favulus), we monitored larval settlement rates in aquaria every 6 h from the time larvae commenced swimming (i.e. were ciliated, fully developed larvae) for a period of approximately 10 days. For P. daedalea, peak settlement occurred between 60 and 66 h following fertilization (2.5 and 2.75 days), which is markedly earlier than the 4- to 6-day time period commonly cited as the minimum time before broadcast-spawned coral larvae are competent to settle. Surprisingly, it was also clear from our experimental results that settlement in P. daedalea occurred as a distinct pulse during the 60- to 66-h period, rather than continuously throughout the study period. G. favulus larvae also appear to be able to settle quickly (from 54 h following fertilization). We argue, on the basis of these short competency times and apparently rapid settlement, that dispersal in broadcast-spawning coral larvae may not be as great as has previously been assumed.