Effect of meiofauna on macrofauna recruitment: settlement inhibition of the polychaete Hydroides elegans by the harpacticoid copepod Tisbe japonica

Various aspects of marine macroinvertebrate ecology cannot be understood without detailed knowledge of larval settlement processes. An important effect underscored during the settlement process is the disturbance of marine invertebrate larvae by predators. We demonstrated that biotic disturbance, comprising physical elimination and mortality due to predation and the behavioral irritation of larvae by the harpacticoid copepod Tisbe japonica, prevent a significant portion of larvae of the polychaete Hydroides elegans from settlement on otherwise suitable substrata. Experiments were performed both in the laboratory and the field showing reproducible significant differences in larval settlement and mortality rates between gender-specific copepod treatments and the control. The trend of decreased larval settlement in the presence of copepods coincided with increased larval mortality in these treatments. In the corresponding field experiments, larval settlement and mortality were similar to the ones obtained under laboratory conditions.     

Complex offspring size effects: variations across life stages and between species

Classical optimality models of offspring size and number assume a monotonically increasing relationship between offspring size and performance. In aquatic organisms with complex life cycles, the size–performance function is particularly hard to grasp because measures of performance are varied and their relationships with size may not be consistent throughout early ontogeny. Here, we examine size effects in premetamorphic (larval) and postmetamorphic (juvenile) stages of brooding marine animals and show that they vary contextually in strength and direction during ontogeny and among species. Larger offspring of the sea anemone Urticina felina generally outperformed small siblings at the larval stage (i.e., greater settlement and survival rates under suboptimal conditions). However, results differed when analyses were conducted at the intrabrood versus across‐brood levels, suggesting that the relationship between larval size and performance is mediated by parentage. At the juvenile stage (15 months), small offspring were less susceptible than large ones to predation by subadult nudibranchs and both sizes performed similarly when facing adult nudibranchs. In a sympatric species with a different life history (Aulactinia stella), all juveniles suffered similar predation rates by subadult nudibranchs, but smaller juveniles performed better (lower mortalities) when facing adult nudibranchs. Size differences in premetamorphic performance of U. felina were linked to total lipid contents of larvae, whereas size‐specific predation of juvenile stages followed the general predictions of the optimal foraging strategy. These findings emphasize the challenge in gathering empirical support for a positive monotonic size–performance function in taxa that exhibit complex life cycles, which are dominant in the sea.     

Spatially coupled larval supply of marine predators and their prey alters the predictions of metapopulation models

Oceanographic forces can strongly affect the movement of planktonic marine larvae, often producing predictable spatial patterns of larval delivery. In particular, recent empirical evidence suggests that in some coastal systems, certain locations consistently receive higher (or lower) larval supplies of both predators and their prey. As a consequence, rates of settlement and predation may be coupled spatially, a phenomenon I term the "coupled settlement effect." To investigate the metapopulation consequences of this phenomenon, I created discrete-time, patch-based analytical and simulation models with a common larval pool and uneven larval supply among patches. Using two complementary measures of subpopulation value as a basis of comparison, I found that models with and without the coupled settlement effect yielded strikingly different predictions. When prey and predator larval supplies were not coupled, patches supplied with a larger proportion of the larval pool made a greater contribution to the metapopulation. When settlement of prey and predator was strongly coupled, however, the opposite was true: subpopulations with lower rates of larval supply (above some minimum) were more essential to metapopulation persistence. These considerations could facilitate more effective selection of sites for protection in marine reserves.     

Fitness consequences of larval traits persist across the metamorphic boundary

Metamorphosis is thought to provide an adaptive decoupling between traits specialized for each life-history stage in species with complex life cycles. However, an increasing number of studies are finding that larval traits can carry-over to influence postmetamorphic performance, suggesting that these life-history stages may not be free to evolve independently of each other. We used a phenotypic selection framework to compare the relative and interactive effects of larval size, time to hatching, and time to settlement on postmetamorphic survival and growth in a marine invertebrate, Styela plicata. Time to hatching was the only larval trait found to be under directional selection, individuals that took more time to hatch into larvae survived better after metamorphosis but grew more slowly. Nonlinear selection was found to act on multivariate trait combinations, once again acting in opposite directions for selection acting via survival and growth. Individuals with above average values of larval traits were most likely to survive, but surviving individuals with intermediate larval traits grew to the largest size. These results demonstrate that larval traits can have multiple, complex fitness consequences that persist across the metamorphic boundary; and thus postmetamorphic selection pressures may constrain the evolution of larval traits.     

A model of the predatory impact of larval marine fish on the population dynamics of their zooplankton prey

A simulation model of the population dynamics of two speciesof calanoid copepods (Calanus.r pacificus and Pseudocalanussp.) was forced with predation pressure from a genetic, hypotheticalpopulation of larval marine fish. Results of the model are sensitiveto changes in parameters describing the dynamics of both predatorand prey populations, including initial numbers, fecundity,growth, mortality, size of prey organisms and feeding selectivityof the predators; the relative importance of these parametersis tested by way of a brute-force sensitivity analysis. Usingresults from recent ichthyoplankton surveys in Dabob Bay, WA,USA, the model was also forced with predation from populationsof larval Pacific herring (Clupea harengus pallasi) and Pacificwhiting (Merluccius productus). Results of the various simulationruns lead to the conclusion that marine fish larvae can significantlyimpact the population dynamics of their calanoid copepod prey,but that the magnitude of this impact is highly dependent onspecies-specific values of various population parameters.     

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.     

Larval ecology and morphology in fossil gastropods

The shell of marine gastropods conserves and reflects early ontogeny, including embryonic and larval stages, to a high degree when compared with other marine invertebrates. Planktotrophic larval development is indicated by a small embryonic shell (size is also related to systematic placement) with little yolk followed by a multiwhorled shell formed by a free‐swimming veliger larva. Basal gastropod clades (e.g. Vetigastropoda) lack planktotrophic larval development. The great majority of Late Palaeozoic and Mesozoic ‘derived’ marine gastropods (Neritimorpha, Caenogastropoda and Heterobranchia) with known protoconch had planktotrophic larval development. Dimensions of internal moulds of protoconchs suggest that planktotrophic larval development was largely absent in the Cambrian and evolved at the Cambrian–Ordovician transition, mainly due to increasing benthic predation. The evolution of planktotrophic larval development offered advantages and opportunities such as more effective dispersal, enhanced gene flow between populations and prevention of inbreeding. Early gastropod larval shells were openly coiled and weakly sculptured. During the Mid‐ and Late Palaeozoic, modern tightly coiled larval shells (commonly with strong sculpture) evolved due to increasing predation pressure in the plankton. The presence of numerous Late Palaeozoic and Triassic gastropod species with planktotrophic larval development suggests sufficient primary production although direct evidence for phytoplankton is scarce in this period. Contrary to previous suggestions, it seems unlikely that the end‐Permian mass extinction selected against species with planktotrophic larval development. The molluscan classes with highest species diversity (Gastropoda and Bivalvia) are those which may have planktotrophic larval development. Extremely high diversity in such groups as Caenogastropoda or eulamellibranch bivalves is the result of high phylogenetic activity and is associated with the presence of planktotrophic veliger larvae in many members of these groups, although causality has not been shown yet. A new gastropod species and genus, Anachronistella peterwagneri, is described from the Late Triassic Cassian Formation; it is the first known Triassic gastropod with an openly coiled larval shell.     

Size-specific predation on marine invertebrate larvae

Predation on planktonic larval stages is frequently a major source of mortality for the offspring of benthic marine invertebrates. Mortality rate likely varies with larval size and developmental stage, but few experiments have measured how these factors affect predation rates. I used experimental reductions in egg size to test how variation in larval size affects the likelihood of predation during planktonic development. Blastomeres of the sand dollar Dendraster excentricus were separated at the two-cell stage to produce half-sized zygotes. Larvae resulting from this manipulation were tested for their susceptibility to predation relative to whole-sized siblings at four ages. Individuals from each size class were simultaneously presented as prey items to five predators (crab zoeae, crab megalopae, chaetognaths, solitary tunicates, and postlarval fish) in the laboratory. Four predators consumed significantly more half-sized larvae than whole-sized larvae, but one predator type (postlarval fish) consumed more whole-sized larvae. Predators that consumed more half-sized larvae also preferentially consumed younger larvae. In contrast, postlarval fish showed no significant prey preference based on larval age. These results suggest that assumptions of constant mortality rates during development should be modified to account for the effects of larval size and age.     

Larvae of cryptic species of Anopheles gambiae respond differently to cues of predation risk

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Predation risk assessment by larval reef fishes during settlement-site selection

Predation rates of marine species are often highest during the transition from the pelagic to the benthic life stage. Consequently, the ability to assess predation risk when selecting a settlement site can be critical to survival. In this study, pairwise choice trials were used to determine whether larvae of three species of anemonefish (Amphiprion melanopus, A. percula and Premnas biaculeatus) are able to (1) assess the predation risk of potential anemone settlement sites through olfactory cues alone and (2) alter their settlement choices depending on the options available (host or non-host anemone). When predation risk was assessed with host and non-host anemone species independently, all species of anemonefish significantly chose the odor associated with the low-risk settlement option over the high-risk site. Most importantly, all species of anemonefish selected water with olfactory cues from their host anemone regardless of predation risk when paired against non-host anemone odor. These results demonstrate that larval reef fishes can use olfactory cues for complex risk assessment during settlement-site selection; however, locating the correct habitat is the most important factor when selecting a settlement site.     

The influence of adult density on larval settlement in a coral reef fish Coryphopterus glaucofraenum

 For marine species with open populations, patterns of larval settlement can have important consequences for performance and abundance at later life-stages. In this study, I tested whether larvae of a reef-dwelling goby (Coryphopterus glaucofraenum) settled differentially to reefs occupied by varying numbers of adults. I monitored settlement daily to reefs on which the density of adult gobies varied naturally, or was manipulated experimentally. Rates of settlement were constant across a broad range of adult densities, suggesting that larvae do not choose settlement sites based on the number of adults in their immediate vicinity. Accepted: 30 October 1998     

Natural variability in size and condition at settlement of 3 species of marine invertebrates

Experimental studies have demonstrated that for many marineinvertebrate species, variability in larval condition or qualityat settlement may have important effects on post-settlement,early juvenile performance. Relatively few studies, however,explicitly examine natural variability in larval condition atsettlement. This study examines natural variability in larvalattributes (size and lipid index) at settlement for terminal-stagelarvae of intertidal mussels (Mytilus sp.) and barnacles (Pollicipespolymerus and Chthamalus dalli) from southern California. Despitesignificant differences among cohorts in larval attributes,for all 3 species a greater percentage of the variance in larvallength (80–100%) and lipids (58–83%) occurred amongindividuals within a cohort, rather than among cohorts. Forall 3 species, coefficients of variation within a cohort forlength were much smaller (3–8%) than those for lipid index(30–93%), suggesting that lipid storage is a much moreplastic attribute than size for larvae. For mussels, settlementintensity and larval attributes were decoupled, such that averagelarval condition of a cohort was not related to the number oflarvae that settled. At the cohort level, Mytilus and Pollicipessettling together across 3 dates showed similar trends of decreasinglipid index over time, suggesting that environmental conditionsmay influence co-occurring planktonic larvae similarly acrossspecies. This work highlights the need for further experimentsin the field on the effects of larval history on recruitmentsuccess in natural populations, and further studies to determinewhat factors influence larval attributes for planktonic larvaein the field.     

Inhibition of common fouling organisms by marine bacterial isolates ith special reference to the role of pigmented bacteria

Two questions of relevance to the establishment of marine biofouling communities were addressed, viz (1) what is the frequency with which bacterial strains isolated from living and inanimate surfaces in the marine environment show inhibitory activity against the settlement of common fouling organisms, and (2) is the antifouling bacterium, D2, an inhabitant of different marine waters, and how unique is this bacterium, in its mode of action against different target organisms? With respect to the first question, ninety three marine bacteria isolated from various rock surfaces from the marine environment were tested against larvae of Balanus amphitrite and spores of Ulva lactuca. Settlement assays against the diatom Amphora sp. were also performed on 10 of these strains. Nine bacterial isolates were shown to be inhibitory against larval settlement and eight of these strains were also inhibitory against algal spores. Altogether 16 strains were inhibitory against the settlement of algal spores while none of the bacterial strains inhibited diatom settlement. With respect to the second question, D2, a dark green pigmented bacterium, isolated from an adult tunicate off the Swedish west coast, has been found to be a very effective inhibitor against common fouling organisms. In order to see if this bacterium can be found in other marine waters, bacteria from living surfaces of marine plants and animals from waters around Sydney, Australia, were isolated and screened for inhibitory activity against barnacle larvae. Seventy four percent of the 23 plant isolates were shown to be inhibitory against larval settlement while only 30% of the 23 isolates from marine animals reduced settlement. Twenty two of the isolates from different seaweeds were dark pigmented and 20 of these strains inhibited settlement of barnacle larvae and algal spores. Three of the strains showed the same phenotypic expression as D2, and the results indicate that these strains may be D2 or closely related strains, suggesting that D2 may be a common inhabitant in the marine environment.     

Geographical variation in offspring size effects across generations

Offspring size is thought to strongly affect offspring fitness and many studies have shown strong offspring size/fitness relationships in marine and terrestrial organisms. This relationship is strongly mitigated by local environmental conditions and the optimal offspring size that mothers should produce will vary among different environments. It is assumed that offspring size will consistently affect the same traits among populations but this assumption has not been tested. Here I use a common garden experiment to examine the effects of offspring size on subsequent performance for the marine bryozoan Bugula neritina using larvae from two very different populations. The local conditions at one population (Williamstown) favour early reproduction whereas the other population (Pt. Wilson) favours early growth. Despite being placed in the same habitat, the effects of parental larval size were extremely variable and crossed generations. For larvae from Williamstown, parental larval size positively affected initial colony growth and larval size in the next generation. For larvae from the other population, parental larval size positively affected colony fecundity and negatively affected larval size in the next generation. Traditionally, exogenous factors have been viewed as the sole source of variation in offspring size/fitness relationship but these results show that endogenous factors (maternal source population) can also cause variation in this crucial relationship. It appears offspring size effects can be highly variable among populations and organisms can adapt to local conditions without changing the size of their offspring.     

Lack of preference for low-predation-risk habitats in larval damselflies explained by costs of intraspecific interactions

Many studies indicate prey organisms select microhabitats with high structural complexity as a way of reducing risk of predation. We used laboratory experiments to show that damselfly larvae, Ischnura verticalis, suffer higher predation rates from pumpkinseed sunfish in low-density vegetation. However, larvae do not preferentially occupy microhabitats with high vegetation density in either the presence or absence of sunfish; when given a choice, the number of larvae per stem of vegetation was equal across all densities of vegetation. That larvae do not congregate in dense vegetation may reflect costs of aggressive interactions. Results from laboratory experiments indicated larval interactions increase conspicuous behaviours (most notably swimming) and consequently increase fish predation. A subsequent experiment indicated that frequency of larval interactions increases with increased vegetation density when number of larvae/stem is constant. Thus, larval microhabitat selection may reflect a trade-off between reduced risk of predation in areas of high vegetation density, caused by reduced fish foraging ability, and increased aggressive larval interactions, due to decreased proximity of larvae. Copyright 2000 The Association for the Study of Animal Behaviour.     

Breedng season, larval development and diseprsal of Lingula anatina (Brachiopoda, Inarticulata) from Townsville, Australia

A discrete but protracted breeding season, extending from October to April, was defined for Lingula anatina from Townsville, Australia, using gonad indices, sizes of developing ova, occurrence of planktonic larvae and analysis of size frequency distribution of an adult population. Comparison of temperate and tropical records suggests that the duration of the breeding season is regulated by temperature. The minimum age at which larvae achieve competence to settle is approximately the same in temperate and tropical waters, but in both regions development and growth occur at a very variable rate. A number of morphological features which can be considered precursors to settlement are closely associated in their development, which may proceed in response to settlement cues provided by proximity to the substratum. The varying intensity of such cues in different environments may be responsible for delays before some larvae realize competence to settle, accounting for much of the variability in the development process. Accordingly, differences between collections of Indo-West Pacific Lingula larvae can be rationalized; all records are now referred to L. anatina . Extension of pelagic larval life in lingulid larvae appears to involve a strategy different from that of most other marine invertebrates.     

Successful determination of larval dispersal distances and subsequent settlement for long-lived pelagic larvae

Despite its importance, we still have a poor understanding of the level of connectivity between marine populations in most geographical locations. Taking advantage of the natural features of the southeast coast of New Zealand's North Island, we deployed a series of settlement stations and conducted plankton tows to capture recent settlers and planktonic larvae of the common intertidal gastropod Austrolittorina cincta (6-8 week larval period). Satellite image analysis and ground truthing surveys revealed the absence of suitable intertidal rocky shore habitat for A. cincta over a 100 km stretch of coastline between Kapiti Island to the south and Wanganui to the north. Fifteen settlement stations (3 replicates × 5 sites), which were used to mimic intertidal habitat suitable for A. cincta, were deployed for two months around and north of Kapiti Island (at 0.5, 1, 5, 15, 50 km). In addition, we also conducted plankton tows at each settlement station when the stations were first deployed to collect A. cincta larvae in the water column. On collection, all newly settled gastropods and larvae in the plankton samples were individually isolated, and a species-specific microsatellite marker was used to positively identify A. cincta individuals. Most of the positively identified A. cincta settlers and larvae were collected at the first three sampling stations (<5 km). However, low numbers of A. cincta settlers and larvae were also recorded at the two more distant locations (15 and 50 km). Dispersal curves modeled from our data suggested that <1% of gastropod larvae would travel more than 100 km. While our data show that most larvae are retained close to their natal populations (<5 km), a small proportion of larvae are able to travel much larger geographic distances. Our estimates of larval dispersal and subsequent settlement are one of only a few for marine species with a long-lived larva.     

Why Life Histories Evolve Differently in the Sea

Marine life histories differ from terrestrial life historiesbecause seawater is denser and more viscous than air, becausedesiccation is not a problem for organisms in water, and becausefood is abundant in suspension and solution. (1) Mating andcompetition for paternity in the sea often differs. Female gametesare often spawned freely. Passively dispersed spermatophorescould in some cases provide single paternity to an entire clutchof offspring. Penises of sessile animals reach far for copulation.There are no pollinators. (2) In many clades of benthic marineanimals, greater dispersal of offspring is associated with largeadult size, and greater parental care of offspring and reducedplanktonic larval periods are associated with small adult size.(3) Many benthic marine animals are colonies with modular construction,and these also commonly brood embryos and have short-lived larvae,in contrast to related solitary forms. (4) Unlike dispersalof terrestrial animals, larval dispersal of marine animals isoften obligate with sexual reproduction and often includes aprecompetent period during which larvae cannot settle at goodsites. Unlike terrestrial seeds, marine larvae have no clearadaptations for dispersal, often grow during dispersal, andoften leave bad sites. Feeding planktonic larvae are commonamong marine animals and rare among other aquatic animals, perhapsbecause of persistent aquatic routes between habitable sitesfor marine animals. Peculiarities in marine life histories mayinfluence many aspects of evolution in the sea. Closely relatedsedentary marine animals can differ greatly in larval dispersalwith consequences for recruitment to populations, genetic exchangebetween benthic populations, adaptation to local conditions,sex allocation, interaction with kin, speciation, and extinction.     

Settlement in different-sized patches by the gregarious intertidal barnacle Chamaesipho tasmanica Foster and Anderson in New South Wales

Most models on settlement of open marine invertebrate populations are based on space-limitation. These models, however, do not recognise that free space may not drive the demography of populations when larval numbers are small or when larval supply varies along a gradient in the habitat. They also do not incorporate the effects of larval choice when settling. It has been hypothesised that, in gregarious barnacles, the effects of adult conspecifics, rather than available free space, may play a primary role in settlement. That is, cues from adults along perimeters of patches, rather than space available, may enhance colonisation. This study therefore aimed to distinguish between these separate influences on populations of Chamaesipho tasmanica, a gregarious barnacle characterised by relatively few larvae arriving to settle each year. Patches of 6, 3 and 1.5 cm diameter were cleared within aggregations of barnacles at three heights (Low, Mid, Upper) of Chamaesipho's distribution at two sites and during 2 years of settlement. Total numbers of settlers in each year were manipulated to determine the separate influences on settlement due to availability of substratum or the effects of conspecific adults. To test for the effects of available free space, numbers of settlers per unit area were analysed. To test for gregarious effects due to the presence of adults, numbers of settlers per unit perimeter were analysed. While available substratum was found not to affect settlement of this barnacle, gregarious settlement in response to adults at perimeters of patches was thought to be confounded by differential larval supply and differential conspecific cues among heights on the shore. Results from this study therefore have important implications for survival of gregarious populations following disturbances, especially in species where larval supply is poor.     

Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete, Pygospio elegans

Population genetic structure of sedentary marine species is expected to be shaped mainly by the dispersal ability of their larvae. Long-lived planktonic larvae can connect populations through migration and gene flow, whereas species with nondispersive benthic or direct-developing larvae are expected to have genetically differentiated populations. Poecilogonous species producing different larval types are ideal when studying the effect of developmental mode on population genetic structure and connectivity. In the spionid polychaete Pygospio elegans, different larval types have been observed between, and sometimes also within, populations. We used microsatellite markers to study population structure of European P. elegans from the Baltic Sea (BS) and North Sea (NS). We found that populations with planktonic larvae had higher genetic diversity than did populations with benthic larvae. However, this pattern may not be related to developmental mode, since in P. elegans, developmental mode may be associated with geography. Benthic larvae were more commonly seen in the brackish BS and planktonic larvae were predominant in the NS, although both larval types also are found from both areas. Significant isolation-by-distance (IBD) was found overall and within regions. Most of the pair-wise F(ST) comparisons among populations were significant, although some geographically close populations with planktonic larvae were found to be genetically similar. However, these results, together with the pattern of IBD, autocorrelation within populations, as well as high estimated local recruitment, suggest that dispersal is limited in populations with planktonic larvae as well as in those with benthic larvae. The decrease in salinity between the NS and BS causes a barrier to gene flow in many marine species. In P. elegans, low, but significant, differentiation was detected between the NS and BS (3.34% in AMOVA), but no clear transition zone was observed, indicating that larvae are not hampered by the change in salinity.