Larval behaviour and choice of settlement site: Correlation with environmental distribution pattern in an erect bryozoan

Summary This paper concerns the preferred environmental conditions for settlement and metamorphosis of larvae of the erect, rigidly calcified cheilostome bryozoanSchizotheca serratimargo and compares the settlement preferences with in situ distribution of adult colonies. A review of bryozoan larval behaviour and responses to environmental parameters is given in order better to understand larval settlement and metamorphosis in this species. Release of larvae ofS. serratimargo (Hincks) was induced so that each travelled down a path with a limited set of microenvironments in which it could choose to settle. Four different flow velocities, three different depths below the water surface, two different light intensities, three different orientations of plexiglas surfaces, and subdivision of distance of travel into three segments, yielded 216 microenvironments. 466 larvae successfully settled and metamorphosed within the experimental chamber. They metamorphosed in significantly higher numbers in microenvironments with low flow velocity, in the shallowest of the three possible depths, in darker areas, and on nonoverhanging surfaces with little or no sediment. The most important stimulus for settlement was darkness, especially where there was a strong gradient in light intensity.S. serratimargo grows as erect bilaminate bushes on protected flanks of boulders, in small caves, and just within the entrances of larger caves at depths of 5–30 m, as well as on hard debris on open muddy sand floors at 30–35 m depth in the Adriatic and Mediterranean Seas. The experimentally-determined settlement patterns suggest that recruitment is more important than post-settlement interactions or exposure to physical damage in determining local distribution of the species.     

Temporal settlement patterns of larvae of the broadcast spawning reef coral Favites chinensis and the broadcast spawning and brooding reef coral Goniastrea aspera from Okinawa, Japan

The faviid corals, Favites chinensis and Goniastrea aspera are widely distributed in the Indo-Pacific region. Both corals are hermaphroditic broadcast spawners, but G. aspera is also known to brood planula larvae in Okinawa. This study investigated the temporal settlement patterns of planula larvae of the scleractinian corals F. chinensis and G. aspera that developed from spawned gametes, and planula release and settlement of brooded larvae of G. aspera from Okinawa, Japan. Some of the broadcast-spawned larvae of F. chinensis and G. aspera had very short pre-competency periods of 1–2 and 2–3 days after spawning, and relatively long maximum settlement-competency periods of 56–63 and 63–70 days after spawning, respectively. These pre-competency periods are among the shortest reported for larvae of broadcast spawning coral species, and appear to be negatively correlated with seawater temperature. F. chinensis larvae tended to settle rapidly with 34–39% of larvae settling in the first week after spawning, while broadcast-spawned G. aspera larvae had a slower settlement pattern with 11–15% of larvae settling in the first week after spawning. Brooded larvae of G. aspera settled more rapidly, with settlement rates of 27–31% within the first 24 h and 45–65% within the first week after the start of the experiment. The production of planula larvae with rapid settlement capabilities may enable F. chinensis and G. aspera to establish and maintain populations in shallow reef sites at Okinawa. The release of the brooded planulae for up to 2 months may explain why G. aspera is locally more dominant on shallow reefs in Okinawa than F. chinensis. On a broader scale, the longer settlement competency periods of some of the broadcast-spawned larvae of these species increase their potential for longer-distance dispersal and may partly explain the wide biogeographic distribution of these species in the Indo-Pacific region.     

The effects of larval abundance, settlement and juvenile mortality on the depth distribution of a colonial ascidian

The colonial ascidian Didemnum candidum (Savigny) is more abundant at shallow depths on floating docks than at greater depths along pilings in Pearl Harbor, Oahu, Hawaii. To compare the effects of selective settlement and postsettlement mortality on adult distribution, I determined if settlement was nonrandom relative to depth, if differences in adult abundance were responsible for the depth distribution of settlement, and if juvenile mortality varied with depth. A plankton pump was used to measure variation in larval abundance with depth. Acrylic settling plates were suspended at different depths and sampled nondestructively to measure settlement intensity and juvenile mortality. Settlement and mortality of the didemnid ascidians Diplosoma listerianum Milne-Edwards and Diplosoma sp. were also measured in the field and compared to that of D. candidum. Settlement of D. candidum was indeed nonrandom over depth. Both planktonic larvae and settled juvenils were more numerous at 0.5 than 3 or m. Settlement intensity on vertical plates was greatest within 1–2 cm of the water surface in the laboratory and within 2–3 cm in the field. Directly adjacent to the floating dock, where adults were equally abundant, settlement on horizontal plates was greater at shallow depths, suggesting directed movement of larvae upward. However, the ratio of settled juveniles to planktonic larvae (number of settlers: number of larvae) did not significantly differ with depth, suggesting that larvae were not more likely to settle at a particular depth. Settlement of the Diplosoma species was also heaviest near the surface. Juvenile mortality was greater at 0.5 than at 3 or 6 m for both D. candidum and the Diplosoma species. Experimental settlement showed that mortality, per se, of D. candidum was independent of depth. Rather, mortality was density-dependent, and the higher mortality near the surface was due to the greater number of larvae settling there. At this location, nonrandom settlement appears to determine the adult distribution of D. candidum, despite greater juvenile mortality at shallow depths. The pattern of settlement over depth is largely determined by adult proximity, rather than active larval behavior.     

Characteristics of Settling Coral Reef Fish Are Related to Recruitment Timing and Success

Many marine populations exhibit high variability in the recruitment of young into the population. While environmental cycles and oceanography explain some patterns of replenishment, the role of other growth-related processes in influencing settlement and recruitment is less clear. Examination of a 65-mo. time series of recruitment of a common coral reef fish, Stegastes partitus, to the reefs of the upper Florida Keys revealed that during peak recruitment months, settlement stage larvae arriving during dark lunar phases grew faster as larvae and were larger at settlement compared to those settling during the light lunar phases. However, the strength and direction of early trait-mediated selective mortality also varied by settlement lunar phase such that the early life history traits of 2–4 week old recruit survivors that settled across the lunar cycle converged to more similar values. Similarly, within peak settlement periods, early life history traits of settling larvae and selective mortality of recruits varied by the magnitude of the settlement event: larvae settling in larger events had longer PLDs and consequently were larger at settlement than those settling in smaller pulses. Traits also varied by recruitment habitat: recruits surviving in live coral habitat (vs rubble) or areas with higher densities of adult conspecifics were those that were larger at settlement. Reef habitats, especially those with high densities of territorial conspecifics, are more challenging habitats for young fish to occupy and small settlers (due to lower larval growth and/or shorter PLDs) to these habitats have a lower chance of survival than they do in rubble habitats. Settling reef fish are not all equal and the time and location of settlement influences the likelihood that individuals will survive to contribute to the population.     

Settlement patterns of Chthamalus spp. at Praia da Oliveirinha (SW Portugal)

Recruitment of Chthamalus spp. is intense during spring and summer but the number of settled cypris larvae is very low when compared to the high number of Chthamalus spp. metamorphs. In the summer of 1997 at Praia da Oliveirinha (SW Portugal), two hypotheses were tested: 1) the cypris larvae of Chthamalus spp. metamorphose in one tidal cycle; and 2) the settlement of Chthamalus spp. is higher during diurnal high tide compared with nocturnal high tide. The results indicate that cypris larvae of Chthamalus spp. can metamorphose in one tidal cycle. The hypothesis of higher settlement during diurnal high tide could not be tested at the mid and upper levels of C. montagui distribution due to a significative heterogeneity of variances. At the lower level, the results support this hypothesis. In spite of these data having been collected on a single shore and on a few sampling dates, these results suggest that more studies using different spatial and temporal scales are needed to see if this pattern is general.     

Fatal errors in set as a cost of dispersal and the influence of intertidal flora on set of barnacles

Summary Cyprid larvae of Balanus cariosus settle preferentially on slate plates with a biota characteristic of the lower intertidal shore, and the cyprids also prefer plates with more algae. Cyprid larvae of Balanus glandula had the same preferences in two out of three experiments. We conclude that some component of the flora guides both species during settling and metamorphosis. Data on vertical distribution and fecundity of B. glandula show that the preference for the lower shore decreases fitness of B. glandula at the site of the settling experiments and at most other sites sampled in or near the San Juan Islands, though in some restricted habitats in the San Juans and extensive areas in the adjacent regions of Puget Sound a preference for the lower shore is appropriate. Extensive dispersal among sites is possible in the planktonic period of 2 to 4 weeks. This example supports the hypothesis that a cost to large scale dispersal is lower fitness at many sites within a species' range. In this case the cost is through poorer correlation between stimuli guiding choice of habitat and favorability of habitat.     

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.     

The influence of resident adults on larval settlement: experiments with four species of ascidians

Residents within any community can affect the larval settlement of both their own and other species. In marine sessile communities resident adults can affect larval settlement by preying on settling larvae, removing or adding space for the larvae to colonize, or stimulating or prohibiting larval settlement on available substratum nearby. To examine those processes by which residents affect settlement, we exposed experimental substrata with three densities of adults of a single species at a site in eastern Long Island Sound, USA for a 24-h period. Four species of common ascidians, Botryllus schlosseri (Pallas), Botrylloides diegensis Ritter and Forsyth, Diplosoma macdonaldi Herdman, and Molgula manhattensis (De Kay), were used in 11 separate experiments. Few individuals of any species settling attached to the surfaces of these species and this resulted in the main effect of these residents being the usurpation of space and the restricting of settlement to unoccupied areas. A model is also presented to explain the apparent aggregated settlement of several species in open areas adjacent to the resident ascidians. From this model we suggest that the aggregated settlement can result from limited larval mobility such that some larvae that contact and reject the resident species as settlement sites may subsequently contact open surfaces of the same substratum and increase settlement densities there over those observed on control substrata. Finally, settlement data for several species indicate that Molgula may influence settlement by preying on larvae.     

Substratum preferences of settling larvae of marine fishes reared in the laboratory

Various species of marine fish larvae were reared in the laboratory to allow observation of the substratum preferences of newly settling fish. The range of preferences for settling larvae of intertidal species corresponded to the adult niche breadth. The preferred substratum was always an element of the adult habitat, although not necessarily the same substratum preferred by the adults. Experiments with artificial substrata indicated that settlement preferences are based on tactile cues and light transmission. Depending upon the species, other factors such as current speed or salinity can also influence settlement.     

Observations on the settling of Simulium damnosum larvae on artificial substrates,in the Ivory Coast

The settling rates of the larvae of the blackfly Simulium damnosum Theobald, were monitored at a Simulium breeding site on the Bandama River in the Ivory Coast. Significantly greater numbers of larvae were found to settle during the night than during the day, and there was a significant increase in the settling rate immediately following the onset of darkness.The drifting larval population contained significantly greater numbers of smaller larvae than the general population.     

Life History of the Barnacle Balanus Amphitrite Darwin and Its Role in Fouling Communities of Peter the Great Bay, Sea of Japan

The life history of the barnacle Balanus amphitrite Darwin and its role in fouling communities of Golden Horn Bay (Peter the Great Bay), which is subjected to thermal pollution, were studied. The warm-water B. amphitrite occurs as a common minor species on operational vessels and waterworks in Peter the Great Bay, where it was brought by ocean-going ships operating on Russia–Japan lines. Even in the conditions of the higher temperature regime of Golden Horn Bay, the reproductive season of B. amphitrite is confined to the summer and autumn months. The adult individuals brought by ships in summer produce 2–3 generations of larvae. The development of larvae and their settling on the substrate occurs from August to October within a broad temperature range from 22.5 up to 12°C. Even in the low temperatures of Golden Horn Bay the larvae attain a greater size than those in tropical and subtropical waters. The juveniles have time to reach maturity and to produce their own progeny, but most often they perish with winter drop in the water temperature. It was shown that in Peter the Great Bay there is dependent population of B. amphitrite inhabiting the anthropogenic substrates only in the warm season: water works, idle vessels, and operational offshore vessels. The water temperature is the limiting factor of successful acclimation of that species.     

Rising CO2 concentrations affect settlement behaviour of larval damselfishes

Reef fish larvae actively select preferred benthic habitat, relying on olfactory, visual and acoustic cues to discriminate between microhabitats at settlement. Recent studies show exposure to elevated carbon dioxide (CO₂) impairs olfactory cue recognition in larval reef fishes. However, whether this alters the behaviour of settling fish or disrupts habitat selection is unknown. Here, the effect of elevated CO₂ on larval behaviour and habitat selection at settlement was tested in three species of damselfishes (family Pomacentridae) that differ in their pattern of habitat use: Pomacentrus amboinensis (a habitat generalist), Pomacentrus chrysurus (a rubble specialist) and Pomacentrus moluccensis (a live coral specialist). Settlement-stage larvae were exposed to current-day CO₂ levels or CO₂ concentrations that could occur by 2100 (700 and 850 ppm) based on IPCC emission scenarios. First, pair-wise choice tests were performed using a two-channel flume chamber to test olfactory discrimination between hard coral, soft coral and coral rubble habitats. The habitat selected by settling fish was then compared among treatments using a multi-choice settlement experiment conducted overnight. Finally, settlement timing between treatments was compared across two lunar cycles for one of the species, P. chrysurus. Exposure to elevated CO₂ disrupted the ability of larvae to discriminate between habitat odours in olfactory trials. However, this had no effect on the habitats selected at settlement when all sensory cues were available. The timing of settlement was dramatically altered by CO₂ exposure, with control fish exhibiting peak settlement around the new moon, whereas fish exposed to 850 ppm CO₂ displaying highest settlement rates around the full moon. These results suggest larvae can rely on other sensory information, such as visual cues, to compensate for impaired olfactory ability when selecting settlement habitat at small spatial scales. However, rising CO₂ could cause larvae to settle at unfavourable times, with potential consequences for larval survival and population replenishment.     

Variation in barnacle recruitment over small scales: larval predation by adults and maintenance of community pattern

Over small spatial scales, variation in the density of settlers of benthic sessile species is the result of interactions among larval behavior, local hydrodynamic conditions, and the physical, chemical and biological characteristics of the benthic habitat. It has been shown repeatedly that adult benthic filter-feeders can consume larvae of their own and other species, but their effects on the distribution and abundance of recruits have rarely been demonstrated under natural conditions in the field, particularly on hard substrata. Here we experimentally quantified the effect of the large intertidal barnacle, Semibalanus cariosus (Pallas), on the density of recruits of three common barnacle species. The experiments were conducted at the peak of the barnacle recruitment season over three successive years, on the west coast of San Juan Island, Washington. A persistent and well documented community pattern in the mid intertidal zone of the study site is a sparse bed of adult S. cariosus with bare rock spaces essentially devoid of small barnacles among the large individuals. Field experiments consisted of small areas from which either all adult S. cariosus were killed leaving the shells attached to the rock, or live adult barnacles were left intact. Our results showed that over small spatial scales of a few to tens of centimeters, the large barnacle S. cariosus can interfere and significantly reduce net settlement and recruitment of conspecific as well as other barnacle species. Between 65 and 100% reduction in settlement could be attributed to larval predation by adults, as implied by barnacle settlement patterns on different treatments and by the presence of nauplius larvae in cirri and stomach contents of S. cariosus. The negative effect on barnacle settlement was consistent between years of relatively low barnacle recruitment, which appears to be the most common situation at the study site, but it disappeared on a year of unusually high recruitment, when settling larvae seem to have swamped the filtration ability of adult S. cariosus. The different barnacle species displayed contrasting settlement patterns on bare rock and on the lateral shells of the large barnacles, which appear to be a result of differences in larval behavior. Comparisons against the relative availability of these substrata in the experimental plots suggested that larvae of different species sample the benthic microhabitat in very different ways.     

Supply-side control over the survivorship of Chthamalus spp. recruits in northern Baja California

The constant supply of larvae to coastal habitats is important for the persistence of populations and can vary depending on oceanic conditions that may affect physical transport processes. We evaluated the survivorship of Chthamalus recruits in Playa San Miguel, Baja California, for over a year to evaluate if the supply of new recruits was of greater importance than the post-recruitment factors of competition and predation in determining adult population size. We hypothesized that the number of Chthamalus recruits would predict the number of adults present and that predation and competition would not play a significant role in determining adult densities. Recruit density was a robust predictor of adult density despite the presence of weak density-dependent mortality. Neither predation nor competition significantly affected the survivorship of recruits and did not decouple the relationship between recruit and adult densities, suggesting that these post-recruitment controls did not play an important role in determining the population size of Chthamalus barnacles at this site. The data support the hypothesis that supply-side control is the primary factor structuring the population of Chthamalus in the intertidal community at Playa San Miguel.     

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.     

The influence of resident adults on recruitment: a comparison to settlement

For species recruiting into established sessile communities, the adult colonies and individuals already present form a significant part of the environment and have the potential to alter both larval settlement rates and post-settlement mortality. Settlement rates can be reduced by predation on larvae, by the removal or addition of substratum space, or by stimulation or prohibition of larvae from settling on adjacent substratum. Once attached, the recruiting individual can still be influenced by predation or overgrowth by residents, by the added physical structure for firmer attachment, or by being camouflaged from motile predators. To examine those processes by which residents affect recruitment we exposed experimental substrata with three densities of adults of a single species at a site in eastern Long Island Sound, USA for a 1-wk period. Seven different species of common invertebrates were used in nine separate experiments. The major effect of most resident species was the usurpation of space and the restricting of recruitment to adjacent unoccupied areas. This was particularly true for resident ascidians and bryozoans, but less so for barnacles and oysters. In fact several species recruited in higher densities on or next to oysters and barnacles. Comparison to 1-day settlement experiments indicated that the encrusting ascidian species Diplosoma and possibly Botryllus reduced recruitment relative to settlement, probably by overgrowing newly-settled individuals. However, in the presence of most resident species, recruitment patterns were not greatly different from settlement patterns, indicating that the effects of the attached community on recruitment may result from influences on settlement.     

Habitat preference and the marine-speciation paradox

Marine organisms challenge the classical theories of local adaptation and speciation because their planktonic larvae have the potential to maintain high gene flow. The marine-speciation paradox is illustrated by contact zones between incipient species that are so large that allopatric divergence seems unlikely. For this reason any mechanism preventing sympatric larvae of two incipient species from coexisting in the same habitats can be a powerful promoter of speciation. The contact zone between two hybridizing taxa of mussel, Mytilus edulis and M. galloprovincialis, in Europe provides an excellent example. Although the zone itself extends over thousands of kilometres, the opportunities for interbreeding are considerably reduced by the small-scale mosaic structure of the zone, where local patches of each taxon alternate at scales of kilometres or less, in response to locally variable ecological factors. Habitat choice by settling larvae would be a less costly mechanism than post-settlement selection to maintain such a mosaic structure. Unfortunately the role of selective settlement has remained hypothetical because larvae could not be scored by classical genetic markers. PCR markers allowed us to study larvae and settlement in ecologically contrasting sites within the zone. We show that only a subset of the genotypes present in the plankton settle in some sites, and that the adults on these sites show the same genetic bias. Genetically based variation in pre-settlement processes therefore accounts for the ecological segregation observed, though it is not the only factor involved in limiting successful interbreeding. The present dataset also supports previous reports of partial spawning asynchrony.     

Demersal schooling prior to settlement by larvae of the naked goby

Synopsis Field observations and collections indicate that the naked goby, Gobiosoma bosci, undergoes a near-bottom schooling phase prior to settlement. The size of these demersal larvae was intermediate between the sizes of larvae collected in plankton tows and of metamorphosed juveniles collected from the benthos. Two larvae that were captured unharmed quickly settled and metamorphosed. Otoliths of demersal larvae contained 20–41 daily increments. Most larvae were in schools made up of at least 25 individuals although single larvae were also seen. The dispersion pattern of demersal larvae was far more aggregated than that of recently settled juveniles indicating that larvae in schools probably do not settle to the benthos en masse.     

Larval biology of butterflyfishes (Pisces,Chaetodontidae): what do we really know?

Synopsis Relatively little is known of the pelagic portion of the life history of butterflyfishes. Eggs are small (<1 mm), pelagic and hatch in less than 30 hours. Most species pass through a so-called tholichthys larval interval characterized by elaborate, distinctive head spination:Coradion larvae have different head spination. While older chaetodontid larvae can be identified by adult characters, young (preflexion) larvae generally cannot now be identified below family. In tropical plankton studies chaetodontid larvae averaged <0.1% of larvae captured, and occurred in 13% of samples. This rarity is a major hindrance to further work, but is not unexpected in view of adult abundance. Larvae of a few taxa are most abundant in shelf waters, but larvae of many chaetodontid taxa seem to be most abundant in oceanic waters. In either case, waters near reefs have the fewest chaetodontid larvae. Offshore maxima of larvae appear to exist a few kilometers seaward of Great Barrier Reef ribbon reefs. Chaetodontid larvae may prefer the upper portion of the water column. Both size and age at settlement vary widely within the family and the large genusChaetodon, and the latter varies widely within species. Average size at settlement is less than 20 mm and age is less than 40 days. No correlation was found between size and age at settlement. Behaviour and feeding of chaetodontid larvae are essentially unstudied. Chaetodontid larvae seem to be least abundant in winter. The implications of these conclusions are discussed and some suggestions for further research are made. In all areas more work is needed.