Marine reserves and the complexity of larval dispersal

Reviews in Fish Biology and Fisheries -     

Modelling the larval dispersal of Acanthaster planci

The desire to understand the observed patterns of Acanthaster population spread throughout the Great Barrier Reef (GBR) has necessitated the development of numerical models which are capable of simulating the hydrodynamics associated with large assemblages of reefs over the time scale of larval dispersal. Models are presented which provide an overview of the physical processes controlling the advection of larvae within the Cairns Section of the GBR Marine Park, on the scale of tens to hundreds of kilometres. The relevant scales and relative importance of the distinct processes are discussed. The models are based on a previously tested numerical hydrodynamic model and are validated by comparison with observations documented in the physical oceanographic literature. Overall, model outputs correspond well to our understanding of the large-scale features and dynamics of water circulation over the continental shelf. Regional variation in circulation predicted by the models may result in significant differences in the movement of larvae.     

Beta-thalassemia in the Po Delta: selection, geography, and population structure

The allele frequencies for beta-thalassemia for 51 localities in the province of Rovigo, and in 25 localities in the province of Ferrara, were studied. It was observed that in the province of Ferrara there is a significant cline of frequencies; these decrease from the coast of the Adriatic Sea toward the west. No such gradient was visible in Rovigo. It was advanced, also on the basis of geography documented by ancient maps, that in the province of Rovigo there were multiple foci of selection for the thalassemia gene, and that in the province of Ferrara selection was stronger in the Oriental part of the area. Examination of the isolation by distance model with these data showed that the Malécot-Morton model fits for the Ferrara data and geography, whereas it does not for Rovigo.     

Larval dispersal of intertidal organisms and the influence of coastline geography

The dispersal stages of organisms with sessile adults must be able to select habitats with suitable environmental conditions for establishment and survival, and also must be able to reach those locations. For marine planktonic larvae, movement due to currents is often orders of magnitude greater than movement due to swimming behaviour. Current patterns are determined by interactions between underlying geography and tidal forces, modified by meteorological conditions. These linkages impose an area‐specific focus to connectivity studies. Yet, how geographical features and meteorological forcing combine to produce specific current patterns and resultant connectivity among populations remains unclear. In this study of a complex fjordic region (the Firth of Lorn, Scotland), we followed tracks of generic particles driven by modelled hydrodynamic currents to investigate how connectivity between evenly spaced habitat sites varies in relation to coastal topography. We studied a range of larval durations (1–28 d), and two different but typical meteorological forcing scenarios. Particles released from regions of high current velocity, open coastline and low local habitat availability travelled furthest but were less likely to disperse successfully to other coastal sites. Extensive natal habitat in the vicinity of a site generally had a positive impact on the number of arriving particles, as did low current velocities. However, relationships between numbers of arriving particles and local geographical indices were complex, particularly at longer larval durations. Local geography alone explained up to 50% of the variance in success of particles released and closer to 10% of the variation in the number of particles arriving at each site. General patterns are evident, but coastline properties fall short of predicting dispersal measures for particular locations. The study shows that meteorological variation and broad scale current patterns interact strongly with local geography to determine connectivity in coastal areas.     

Natural dispersal mechanisms and dispersal potential of the invasive ascidian Didemnum vexillum

Over the past decade, several species of non-indigenous ascidians have had adverse effects on a range of coastal ecosystems, and associated industries like aquaculture. One such species, the colonial ascidian Didemnum vexillum, poses a threat to the highly-valued New Zealand green-lipped mussel industry, and there is interest in whether and to what extent its spread can be managed at a regional scale (<100 km). An important component in the decision-making process for managing human-mediated pathways of spread is an understanding of D. vexillum’s natural dispersal potential. Here we use a weight-of-evidence approach, combining laboratory and field studies, to assess the role of natural dispersal mechanisms in the spread of D. vexillum. Under laboratory conditions, >70 % of D. vexillum larvae remained viable and were able to settle and undergo metamorphosis successfully following an artificial delay of 2 h. Larval viability decreased with increasing delay duration, although 10 % of larvae remained viable following a 36 h delay. A field-based study documented larval dispersal from two discrete source populations, with recruitment consistently detected on settlement plates at 250 m from source populations at one experimental site. Exponential decay models used to predict maximum larval dispersal distances at this site indicated that dispersal greater than 250 m is theoretically possible (>1 km in some situations). That being so, we recognise that the successful establishment and persistence of populations will depend on a wide range of processes not taken into account here. Our findings are supported by surveillance of D. vexillum spread in the wider study region; there are a number of instances where the species established on artificial structures that were several kilometres from known source populations, at a time when intensive regional-scale management of anthropogenic vectors was underway. Collectively, our findings indicate that D. vexillum has the ability to spread further by natural dispersal than previously assumed; probably hundreds of metres to kilometres depending on the local hydrological conditions, which has important implications for the ongoing management of this pest species world-wide.     

The larval stages of the sea urchin, Strongylocentrotus purpuratus

The adult body plan of Strongylocentrotus purpuratus is established within the imaginal rudiment during the larval stages. To facilitate the study of these stages, we have defined a larval staging scheme, which consists of seven stages: Stage I, four-arm stage; Stage II, eight-arm stage; Stage III, vestibular invagination stage; Stage IV, rudiment initiation stage; Stage V, pentagonal disc stage; Stage VI, advanced rudiment stage; and Stage VI, tube-foot protrusion stage. Each stage is characterized by significant morphological features observed for the first time at that stage. This scheme is intended as a guide for determining the degree of larval development, and for identifying larval and adult structures. Larval anatomy was visualized using light and confocal microscopy as required on living material, whole mount fixed specimens, and serial sections. Antibody staining to localize specific gene products was also used. Detailed analysis of these data has furthered our understanding of the morphogenesis of the rudiment, and has suggested provocative questions regarding the molecular basis for these events. We intend this work to be of use to investigators studying gene expression and morphogenesis in postembryonic larvae.     

Co-option and dissociation in larval origins and evolution: the sea urchin larval gut

SUMMARY The origin of marine invertebrate larvae has been an area of controversy in developmental evolution for over a century. Here, we address the question of whether a pelagic "larval" or benthic "adult" morphology originated first in metazoan lineages by testing the hypothesis that particular gene co-option patterns will be associated with the origin of feeding, indirect developing larval forms. Empirical evidence bearing on this hypothesis is derivable from gene expression studies of the sea urchin larval gut of two closely related but differently developing congenerics, Heliocidaris tuberculata (feeding indirect-developing larva) and H. erythrogramma (nonfeeding direct developer), given two subsidiary hypotheses. (1) If larval gut gene expression in H. tuberculata was co-opted from an ancestral adult expression pattern, then the gut expression pattern will remain in adult H. erythrogramma despite its direct development. (2) Genes expressed in the larval gut of H. tuberculata will not have a coordinated expression pattern in H. erythrogramma larvae due to loss of a functional gut. Five structural genes expressed in the invaginating archenteron of H. tuberculata during gastrulation exhibit substantially different expression patterns in H. erythrogramma with only one remaining endoderm specific. Expression of these genes in the adult of H. erythrogramma and larval gut of H. tuberculata , but not in H. erythrogramma larval endoderm, supports the hypothesis that they first played roles in the formation of adult structures and were subsequently recruited into larval ontogeny during the origin and evolution of feeding planktotrophic deuterostome larvae.     

Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history

We examine estimates of dispersal in a broad range of marine species through an analysis of published values, and evaluate how well these values represent global patterns through a comparison with correlates of dispersal. Our analysis indicates a historical focus in dispersal studies on low-dispersal/low-latitude species, and we hypothesize that these studies are not generally applicable and representative of global patterns. Large-scale patterns in dispersal were examined using a database of correlates of dispersal such as planktonic larval duration (PLD, 318 species) and genetic differentiation (FST, 246 species). We observed significant differences in FST (p<0.001) and PLD (p<0.001) between taxonomic groups (e.g. fishes, cnidarians, etc.). Within marine fishes (more than 50% of datasets), the prevalence of demersal eggs was negatively associated with PLD (R2=0.80, p<0.001) and positively associated with genetic structure (R2=0.74, p<0.001). Furthermore, dispersal within marine fishes (i.e. PLD and FST) increased with latitude, adult body size and water depth. Of these variables, multiple regression identified latitude and body size as persistent predictors across taxonomic levels. These global patterns of dispersal represent a first step towards understanding and predicting species-level and regional differences in dispersal, and will be improved as more comprehensive data become available.     

Modelling larval dispersal and behaviour of coral reef fishes

Coral reef fish spend their first few weeks developing in the open ocean, where eggs and larvae appear merciless to tides and currents, before attempting to leave the pelagic zone and settle on a suitable reef. This pelagic dispersal phase is the process that determines population connectivity and allows replenishment of harvested populations across multiple coral reef habitats. Until recently this pelagic larval dispersal phase has been poorly understood and has often been referred to as the ‘black-box’ in the life-history of coral reef fishes. In this perspective article we highlight three areas where mathematical and computational approaches have been used to aid our understanding of this important ecological process. We discuss models that provide insights into the evolution of the pelagic larval phase in coral reef fish, an unresolved question which lends itself well to a modelling approach due to the difficulty in obtaining empirical data on this life history strategy. We describe how studies of fish hearing and physical sound propagation models can be used to predict the detection distance of reefs for settling larval fish, and the potential impact of anthropogenic noise. We explain how random walk models can be used to explore individual- and group-level behaviour in larval fish during the dispersal and settlement stage of their life-history. Finally, we discuss the mutual benefits that mathematical and computational approaches have brought to and gained from the field of larval behaviour and dispersal of reef fishes.     

Relationship between adult and larval host plant selection and larval performance in the generalist moth, Trichoplusia ni

Adult oviposition preferences are expected to correlate with host plant suitability for the development of their offspring. For most lepidopteran species, this is particularly important as the hatching neonate larvae of many species are relatively immobile. Thus, the site of oviposition chosen by a female adult can greatly influence the probability of survival for her offspring. In the present study, we investigated the oviposition preference of adult Trichoplusia ni moths for six plant species to determine whether they could accurately rank the suitability of the plants for larval development. We also compared oviposition preferences to neonate larval acceptance and preference to determine whether the adult host range matched that of larval diet breath. Our results indicate that in two-choice and no-choice tests adult T. ni were able to rank the plants accurately, with the exception of anise hyssop. However, when given a choice of all six plants together, they laid more eggs on a plant that was not suitable for larval survival. Larvae accepted and fed on all plants in no-choice tests, and accurately ranked them according to larval performance. We conclude that neonate larvae are better able than adults to rank plants according to larval performance, and that larval diet breadth is wider than the range of plants accepted by adults. We also provide a discussion of the reduced accuracy of adult oviposition preference with increased plant choices.     

Bird dispersal of the larval stage of a seed predator

Multiflora rose seeds containing larvae of the phytophagous wasp Megastigmus aculeatus nigroflavus were fed to a caged mockingbird (Mimus polyglottos). Ninety percent of the seeds were recovered from the bird's feces, and there was no significant difference in subsequent emergence of the wasps from these seeds when compared to controls. This study indicates the dispersal of seed-feeding hymenoptera by avian frugivores may be a widespread and significant phenomenon.     

The adaptive significance of larval dispersal in coral reef fishes

Synopsis Coral reef fishes almost universally disperse over relatively great distances during a pelagic larval phase. Barlow (1981) suggested that this dispersal is adaptive because adult fishes inhabit a patchy, uncertain environment. This reiterated an older idea that the random extinction of local populations necessarily favours dispersal, since ultimately all populations of non-dispersers will disappear. Whereas this view is based on adult survival, we emphasize a less frequent view that substantial larval dispersal may be adaptive when offspring experience patchy and unpredictable survival in the pelagic habitat. We do not address the question of why these animals ‘broadcast’ rather than ‘brood’, but suggest that species committed to pelagic offspring will be under selection to disperse siblings to spread the risk of failure among members of a cohort. Our arguments are supported by a heuristic computer simulation.     

Life history,larval dispersal,and connectivity in coral reef fish among the Scattered Islands of the Mozambique Channel

The Western Indian Ocean harbors one of the world’s most diverse marine biota yet is threatened by exploitation with few conservation measures in place. Primary candidates for conservation in the region are the Scattered Islands (Îles Éparses), a group of relatively pristine and uninhabited islands in the Mozambique Channel. However, while optimal conservation strategies depend on the degree of population connectivity among spatially isolated habitats, very few studies have been conducted in the area. Here, we use highly variable microsatellite markers from two damselfishes (Amphiprion akallopisos and Dascyllus trimaculatus) with differing life history traits [pelagic larval duration (PLD), adult habitat] to compare genetic structure and connectivity among these islands using classic population structure indices as well as Bayesian clustering methods. All classical fixation indexes F _ST, R _ST, G′_ST, and Jost’s D show stronger genetic differentiation among islands for A. akallopisos compared to D. trimaculatus, consistent with the former species’ shorter PLD and stronger adult site attachment, which may restrict larval dispersal potential. In agreement with these results, the Bayesian analysis revealed clear genetic differentiation among the islands in A. akallopisos, separating the southern group (Bassas da India and Europa) from the center (Juan de Nova) and northern (Îles Glorieuses) islands, but not for D. trimaculatus. Local oceanographic patterns such as eddies that occur along the Mozambique Channel appear to parallel the results reported for A. akallopisos, but such features seem to have little effect on the genetic differentiation of D. trimaculatus. The contrasting patterns of genetic differentiation between species within the same family highlight the importance of accounting for diverse life history traits when assessing community-wide connectivity, an increasingly common consideration in conservation planning.

     

Kin competition,natal dispersal and the moulding of senescence by natural selection

Most theoretical models for the evolution of senescence have assumed a very large, well mixed population. Here, we investigate how limited dispersal and kin competition might influence the evolution of ageing by deriving indicators of the force of selection, similar to Hamilton (Hamilton 1966 J. Theor. Biol. 12, 12–45). Our analytical model describes how the strength of selection on survival and fecundity changes with age in a patchy population, where adults are territorial and a fraction of juveniles disperse between territories. Both parent–offspring competition and sib competition then affect selection on age-specific life-history traits. Kin competition reduces the strength of selection on survival. Mutations increasing mortality in some age classes can even be favoured by selection, but only when fecundity deteriorates rapidly with age. Population structure arising from limited dispersal however selects for a broader distribution of reproduction over the lifetime, potentially slowing down reproductive senescence. The antagonistic effects of limited dispersal on age schedules of fecundity and mortality cast doubts on the generality of conditions allowing the evolution of ‘suicide genes’ that increase mortality rates without other direct pleiotropic effects. More generally, our model illustrates how limited dispersal and social interactions can indirectly produce patterns of antagonistic pleiotropy affecting vital rates at different ages.     

Antixenosis and larval and adult dispersal in the Mediterranean corn borer,Sesamia nonagrioides,in relation to Bt maize

Sesamia nonagrioides Lefèbvre (Lepidoptera: Noctuidae) is a key pest of maize [Zea mays L. (Poaceae)] and a main target of Bt maize in the Mediterranean area. To choose the most suitable non‐Bt refuge strategy for preventing or delaying resistance development in this maize borer, we examined its biology and behaviour. No antixenotic effects were found on numbers of eggs and egg batches per plant in choice (Bt vs. non‐Bt plants) and no‐choice assays. However, a greater ratio of young larvae dispersed from Bt than from non‐Bt plants. In addition, larvae that hatched on Bt plants tended to disperse more than those that hatched on non‐Bt plants, particularly during young growth stages. Many adults, especially females, could fly at least up to 400 m, as was found in a dispersal study with rubidium‐marked adults. The stimulation of larval dispersal by the Bt trait and the dispersal capacity of adults might compromise the efficacy of seed mixtures as an insecticide resistance management strategy.     

Recent progress in understanding larval dispersal: new directions and digressions

Larvae have been difficult to study because their small sizelimits our ability to understand their behavior and the conditionsthey experience. Questions about larval transport focus largelyon (a) where they go [dispersal] and (b) where they come from[connectivity]. Mechanisms of transport have been intensivelystudied in recent decades. As our ability to identify larvalsources develops, the consequences of connectivity are garneringmore consideration. Attention to transport and connectivityissues has increased dramatically in the past decade, fueledby changing motivations that now include management of fisheriesresources, understanding of the spread of invasive species,conservation through the design of marine reserves, and predictionof climate-change effects. Current progress involves both technologicaladvances and the integration of disciplines and approaches.This review focuses on insights gained from physical modeling,chemical tracking, and genetic approaches. I consider how newfindings are motivating paradigm shifts concerning (1) life-historyconsequences; (2) the openness of marine populations, self-recruitment,and population connectivity; (3) the role of behavior; and (4)the significance of variability in space and time. A challengefor the future will be to integrate methods that address dispersalon short (intragenerational) timescales such as elemental fingerprintingand numerical simulations with those that reflect longer timescalessuch as gene flow estimates and demographic modeling. Recognitionand treatment of the continuum between ecological and evolutionarytimescales will be necessary to advance the mechanistic understandingof larval and population dynamics.     

Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula

? Shifts in sexual systems are among the most common and important transitions in plants and are correlated with a suite of life-history traits. The evolution of sexual systems and their relationships to gametophyte size, sexual and asexual reproduction, and epiphytism are examined here in the liverwort genus Radula. ? The sequence of trait acquisition and the phylogenetic correlations between those traits was investigated using comparative methods. ? Shifts in sexual systems recurrently occurred from dioecy to monoecy within facultative epiphyte lineages. Production of specialized asexual gemmae was correlated to neither dioecy nor strict epiphytism. ? The significant correlations among life-history traits related to sexual systems and habitat conditions suggest the existence of evolutionary trade-offs. Obligate epiphytes do not produce gemmae more frequently than facultative epiphytes and disperse by whole gametophyte fragments, presumably to avoid the sensitive protonemal stage in a habitat prone to rapid changes in moisture availability. As dispersal ranges correlate with diaspore size, this reinforces the notion that epiphytes experience strong dispersal limitations. Our results thus provide the evolutionary complement to metapopulation, metacommunity and experimental studies demonstrating trade-offs between dispersal distance, establishment ability, and life-history strategy, which may be central to the evolution of reproductive strategies in bryophytes.