Parasites as indicators of movement and population connectivity of a non-diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir

Temporal and spatial patterns in parasite assemblages were examined to evaluate the degree of movement and connectivity of post-recruitment life-history stages of a large, non-diadromous tropical estuarine teleost, king threadfin Polydactylus macrochir, collected from 18 locations across northern Australia. Ten parasites types (juvenile stages of two nematodes and seven cestodes, and adults of an acanthocephalan) were deemed to be suitable for use as biological tags, in that they were considered to have a long residence time in the fish, were relatively easy to find and were morphologically very different to each other which aided discrimination. Univariate and discriminant function analysis of these parasites revealed little difference in temporal replicates collected from five locations, suggesting that the parasite communities were stable over the timeframes explored. Univariate, discriminant function, and BrayCurtis similarity analyses indicated significant spatial heterogeneity, with BrayCurtis classification accuracies ranging from 55 to 100% for locations in north-western and northern Australia, 24 to 88% in the Gulf of Carpentaria, and 39 to 88% on the east coast of Queensland. Few differences were observed among locations separated by <200 km. The observed patterns of parasite infection are in agreement with concurrent studies of movement and connectivity of P. macrochir in that they indicate a complex population structure across northern Australia. These results should be considered when reviewing the management arrangements for this species.

Population connectivity among Dry Tortugas, Florida, and Caribbean populations of mutton snapper (Lutjanus analis), inferred from multiple microsatellite loci

Determining patterns of population connectivity is critical to the evaluation of marine reserves as recruitment sources for harvested populations. Mutton snapper (Lutjanus analis) is a good test case because the last known major spawning aggregation in U.S. waters was granted no-take status in the Tortugas South Ecological Reserve (TSER) in 2001. To evaluate the TSER population as a recruitment source, we genotyped mutton snapper from the Dry Tortugas, southeast Florida, and from three locations across the Caribbean at eight microsatellite loci. Both Fstatistics and individual-based Bayesian analyses indicated that genetic substructure was absent across the five populations. Genetic homogeneity of mutton snapper populations is consistent with its pelagic larval duration of 27 to 37 days and adult behavior of annual migrations to large spawning aggregations. Statistical power of future genetic assessments of mutton snapper population connectivity may benefit from more comprehensive geographic sampling, and perhaps from the development of less polymorphic DNA microsatellite loci. Research where alternative methods are used, such as the transgenerational marking of embryonic otoliths with barium stable isotopes, is also needed on this and other species with diverse life history characteristics to further evaluate the TSER as a recruitment source and to define corridors of population connectivity across the Caribbean and Florida.

Inferring population connectivity across the range of distribution of the stiletto shrimp Artemesia longinaris Spence Bate, 1888 (Decapoda, Penaeidae) from DNA barcoding: implications for fishery management

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Contrasting patterns of population connectivity between regions in a commercially important mollusc Haliotis rubra: integrating population genetics, genomics and marine LiDAR data

Estimating contemporary genetic structure and population connectivity in marine species is challenging, often compromised by genetic markers that lack adequate sensitivity, and unstructured sampling regimes. We show how these limitations can be overcome via the integration of modern genotyping methods and sampling designs guided by LIDAR and SONAR datasets. Here we explore patterns of gene flow and local genetic structure in a commercially harvested abalone species (Haliotis rubra) from South Eastern Australia, where the viability of fishing stocks is believed to be dictated by recruitment from local sources. Using a panel of microsatellite and genome-wide SNP markers we compare allele frequencies across a replicated hierarchical sampling area guided by bathymetric LIDAR imagery. Results indicate high levels of gene flow and no significant genetic structure within or between benthic reef habitats across 1400 km of coastline. These findings differ to those reported for other regions of the fishery indicating that larval supply is likely to be spatially variable, with implications for management and long-term recovery from stock depletion. The study highlights the utility of suitably designed genetic markers and spatially informed sampling strategies for gaining insights into recruitment patterns in benthic marine species, assisting in conservation planning and sustainable management of fisheries.

Caribbean connectivity: implications for Marine Protected Area Management. Proceedings of a Special Symposium, 9-11 November 2006, 59th Annual Meeting of the Gulf and Caribbean Fisheries Institute, Belize City, Belize

Executive Summary: Tropical marine ecosystems in the Caribbean region are inextricably linked through the movement of pollutants, nutrients, diseases, and other stressors, which threaten to further degrade coral reef communities. The magnitude of change that is occurring within the region is considerable, and solutions will require investigating pros and cons of networks of marine protected areas (MPAs), cooperation of neighboring countries, improved understanding of how external stressors degrade local marine resources, and ameliorating those stressors. Connectivity can be broadly defined as the exchange of materials (e.g., nutrients and pollutants), organisms, and genes and can be divided into: 1) genetic or evolutionary connectivity that concerns the exchange of organisms and genes, 2) demographic connectivity, which is the exchange of individuals among local groups, and 3) oceanographic connectivity, which includes flow of materials and circulation patterns and variability that underpin much of all these exchanges. Presently, we understand little about connectivity at specific locations beyond model outputs, and yet we must manage MPAs with connectivity in mind. A key to successful MPA management is how to most effectively work with scientists to acquire the information managers need. Oceanography connectivity is poorly understood, and even less is known about the shape of the dispersal curve for most species. Dispersal kernels differ for various systems, species, and life histories and are likely highly variable in space and time. Furthermore, the implications of different dispersal kernels on population dynamics and management of species is unknown. However, small dispersal kernels are the norm - not the exception. Linking patterns of dispersal to management options is difficult given the present state of knowledge. The behavioral component of larval dispersal has a major impact on where larvae settle. Individual larval behavior and life history details are required to produce meaningful simulations of population connectivity. Biological inputs are critical determinants of dispersal outcomes beyond what can be gleaned from models of passive dispersal. There is considerable temporal and spatial variation to connectivity patterns. New models are increasingly being developed, but these must be validated to understand upstream-downstream neighborhoods, dispersal corridors, stepping stones, and source/sink dynamics. At present, models are mainly useful for providing generalities and generating hypotheses. Low-technology approaches such as drifter vials and oceanographic drogues are useful, affordable options for understanding local connectivity. The “silver bullet” approach to MPA design may not be possible for several reasons. Genetic connectivity studies reveal divergent population genetic structures despite similar larval life histories. Historical stochasticity in reproduction and/or recruitment likely has important, longlasting consequences on present day genetic structure. (PDF has 200 pages.)

A multidisciplinary approach for puzzling over fish connectivity in the Mediterranean Sea: The role of early life history stages of red mullet (Mullus barbatus)

Integrating connectivity patterns into marine ecosystem management is a fundamental step, specially for stock subjected to the combined impacts of human activities (overfishing, habitat degradation, etc.) and climate changes. Thus, management of marine resources must incorporates the spatial scales over which the populations are connected. Notwithstanding, studying these dynamics remains a crucial and hard task and the predictions of the temporal and spatial patterns of these mechanisms are still particularly challenging. This thesis aims to puzzle over the red mullet Mullus barbatus population connectivity in the Western Mediterranean Sea, by implementing a multidisciplinary approach. Otolith sclerochronology, larval dispersal modelling and genetic techniques were gathered in this study. More particularly, this research project focused on early life history stages of red mullet and their role in the characterization of connectivity dynamics. The results show that M. barbatus larval dispersal distances can reach a range of 200 km. The differences in early life traits (i.e. PLD, spawning and settlement dates) observed between various areas of the Western Mediterranean Sea suggest a certain level of larval patchiness, likely due to the occurrence of different spawning pulses during the reproductive period. The dispersal of individuals across distant areas, even not significant in demographic terms, is accountable for the maintenance of the genetic flow among different demes. Fluctuations in the level of exchange among different areas, due to the variability of the source-sink dynamics, could have major implications in the population connectivity patterns. These findings highlight the reliability of combining several approaches and represent a benchmark for the definition of a proper resource management, with considerable engagements in effectively assuring the beneficial effects of the existent and future conservation strategies.

Population genetics of C. Maenas : oceanography and larval dispersal

Decifrar a complexa interacção entre os ciclos de vida de espécies marinhas e a oceanografia revela-se fundamental para a compreensão do fluxo genético e da conectividade no meio marinho. Nas espécies marinhas com desenvolvimento indirecto o fluxo de genes entre populações depende da distância que separa as populações, bem como da interacção entre a duração do desenvolvimento larvar, do comportamento das larvas e dos padrões de circulação oceânica. A conectividade larvar influencia uma variedade de processos como a dinâmica de stocks e de populações, a distribuição e limites geográficos das espécies, a estrutura genética das populações e a dispersão de espécies invasivas e reveste-se consequentemente de uma importância fundamental na identificação das unidades populacionais evolucionariamente relevantes e para a gestão e conservação marinhas. Os marcadores genéticos e os Modelos Individuais Acoplados a Modelos Físico-Biológicos (“ICPBMs”) são actualmente ferramentas fundamentais para o estudo dos padrões de dispersão larvar e para avaliar o nível de conectividade populacional. A presente tese respeita à avaliação das escalas espaciais de conectividade de populações de uma espécie costeira, o caranguejo Carcinus maenas, e utiliza conjuntamente informação de marcadores genéticos, análise de séries temporais de fornecimento de larvas e um modelo numérico de circulação oceânica. O primeiro capítulo introduz a temática da conectividade em espécies marinhas e inclui algumas referências aos métodos moleculares, analíticos e de modelação seguidos ao longo da tese. Através da utilização de múltiplas ferramentas – avaliação da estrutura genética geográfica de C. maenas na sua distribuição nativa com recurso a marcadores de DNA (microssatélites) (Capítulo 2), avaliação da estrutura genética temporal das larvas que formam os eventos de fornecimento larvar à Ria de Aveiro, NW Portugal (Capítulo 3), descrição da variabilidade inter-anual do fornecimento larvar à Ria de Aveiro, NW Portugal (Capítulo 4) e validação de um modelo ICPBM que descreve os padrões observados de fornecimento (Capítulo 5) – esta tese espera poder contribuir para uma melhor compreensão dos mecanismos que regulam o fluxo de genes e a conectividade entre populações de organismos marinhos. No Capítulo 6 são apresentadas as principais conclusões da investigação. A análise genética com recurso a microssatélites indicou que as populações de C. maenas são geneticamente homogéneas ao longo de várias centenas de km, dentro da distribuição nativa da espécie. Paralelamente, não foram encontrados indícios da existência de reprodução por “sweepstakes” em C. maenas de populações da costa oeste da Península Ibérica, visto que não se obtiveram diferenças genéticas significativas entre os eventos larvares. Também não se encontrou qualquer estrutura familiar entre as larvas que formam cada episódio de fornecimento, e não houve nenhuma redução significativa da variabilidade genética das larvas quando comparada com a de caranguejos adultos. A análise de séries temporais de suprimento de larvas na Ria de Aveiro em cinco anos estudados indica que este é um fenómeno episódico e variável, sendo os maiores episódios de fornecimento coincidentes com as marés vivas e acentuados por fortes ventos de sul. O modelo ICPBM foi validado com sucesso e parece fornecer uma estimativa realística das escalas espaciais e temporais de dispersão larvar, de acordo com as observações da estrutura genética e da ausência de reprodução por “sweepstake” em C. maenas da costa oeste da Península Ibérica

Connectivity patterns and early life history of the black-faced blenny Tripterygion delaisi (Cadenat and Blache, 1970)

Tese de doutoramento, Ciências do Mar, Faculdade de Ciências e Tecnologia, Universidade do Algarve, 2015

Microsatellite variation in the yellowhammer Emberiza citrinella : population structure of a declining farmland bird

In recent years, there has been much concern in the UK about population declines of widespread species in agricultural habitats. Conservation-orientated research on declining birds has focused on vital rates of survival and productivity. However, the environmental factors which may influence movements between populations of widespread species is poorly understood. Population genetic structure is an indirect description of dispersal between groups of individuals. To attempt to develop an understanding of genetic structuring in a widespread, but declining, farmland bird, we therefore investigated the yellowhammer, Emberiza citrinella, population in England and Wales using microsatellite data. Our first aim was to investigate whether there was genetic substructuring in the population. A second aim was to investigate if there was a relationship between genetic distances and various environmental variables. Finally, we analysed the microsatellite data for evidence of loss of genetic variation due to population decline. Our data showed a slight but significant structure within the yellowhammer population. This therefore cannot be considered a panmictic population. Our example from South Cumbria implies that high-altitude barriers may have a slight influence on population structure. However, on the whole, genetic distances between sample sites were not significantly correlated with geographical distances, degrees of population connectivity, high altitudes, or differences in precipitation between sites. Finally, we detected departures from mutation-drift equilibrium (excess heterozygosity), which is indicative of a loss of genetic variation through recent decline.

Population genetic structure of serotine bats (Eptesicus serotinus) across Europe and implications for the potential spread of bat rabies (European bat lyssavirus EBLV-1).

Understanding of the movements of species at multiple scales is essential to appreciate patterns of population connectivity and in some cases, the potential for pathogen transmission. The serotine bat (Eptesicus serotinus) is a common and widely distributed species in Europe where it frequently harbours European bat lyssavirus type 1 (EBLV-1), a virus causing rabies and transmissible to humans. In the United Kingdom, it is rare, with a distribution restricted to south of the country and so far the virus has never been found there. We investigated the genetic structure and gene flow of E. serotinus across the England and continental Europe. Greater genetic structuring was found in England compared with continental Europe. Nuclear data suggest a single population on the continent, although further work with more intensive sampling is required to confirm this, while mitochondrial sequences indicate an east-west substructure. In contrast, three distinct populations were found in England using microsatellite markers, and mitochondrial diversity was very low. Evidence of nuclear admixture indicated strong male-mediated gene flow among populations. Differences in connectivity could contribute to the high viral prevalence on the continent in contrast with the United Kingdom. Although the English Channel was previously thought to restrict gene flow, our data indicate relatively frequent movement from the continent to England highlighting the potential for movement of EBLV-1 into the United Kingdom.

High interannual variability in connectivity and genetic pool of a temperate clingfish matches oceanographic transport predictions

Adults of most marine benthic and demersal fish are site-attached, with the dispersal of their larval stages ensuring connectivity among populations. In this study we aimed to infer spatial and temporal variation in population connectivity and dispersal of a marine fish species, using genetic tools and comparing these with oceanographic transport. We focused on an intertidal rocky reef fish species, the shore clingfish Lepadogaster lepadogaster, along the southwest Iberian Peninsula, in 2011 and 2012. We predicted high levels of self-recruitment and distinct populations, due to short pelagic larval duration and because all its developmental stages have previously been found near adult habitats. Genetic analyses based on microsatellites countered our prediction and a biophysical dispersal model showed that oceanographic transport was a good explanation for the patterns observed. Adult sub-populations separated by up to 300 km of coastline displayed no genetic differentiation, revealing a single connected population with larvae potentially dispersing long distances over hundreds of km. Despite this, parentage analysis performed on recruits from one focal site within the Marine Park of Arrábida (Portugal), revealed self-recruitment levels of 2.5% and 7.7% in 2011 and 2012, respectively, suggesting that both long- and short-distance dispersal play an important role in the replenishment of these populations. Population differentiation and patterns of dispersal, which were highly variable between years, could be linked to the variability inherent in local oceanographic processes. Overall, our measures of connectivity based on genetic and oceanographic data highlight the relevance of long-distance dispersal in determining the degree of connectivity, even in species with short pelagic larval durations.

Statistical phylogeographic tests of competing 'Lake Carpentaria hypotheses' in the mouth-brooding freshwater fish, Glossamia aprion (Apogonidae)

Glacial cycles during the Pleistocene reduced sea levels and created new land connections in northern Australia, where many currently isolated rivers also became connected via an extensive paleo-lake system, 'Lake Carpentaria'. However, the most recent period during which populations of freshwater species were connected by gene flow across Lake Carpentaria is debated: various 'Lake Carpentaria hypotheses' have been proposed. Here, we used a statistical phylogeographic approach to assess the timing of past population connectivity across the Carpentaria region in the obligate freshwater fish, Glossamia aprion. Results for this species indicate that the most recent period of genetic exchange across the Carpentaria region coincided with the mid- to late Pleistocene, a result shown previously for other freshwater and diadromous species. Based on these findings and published studies for various freshwater, diadromous and marine species, we propose a set of 'Lake Carpentaria' hypotheses to explain past population connectivity in aquatic species: (1) strictly freshwater species had widespread gene flow in the mid- to late Pleistocene before the last glacial maximum; (2) marine species were subdivided into eastern and western populations by land during Pleistocene glacial phases; and (3) past connectivity in diadromous species reflects the relative strength of their marine affinity.

Review on hard coral recruitment (Cnidaria: Scleractinia) in Colombia

Recruitment, defined and measured as the incorporation of new individuals (i.e. coral juveniles) into a population, is a fundamental process for ecologists, evolutionists and conservationists due to its direct effect on population structure and function. Because most coral populations are self-feeding, a breakdown in recruitment would lead to local extinction. Recruitment indirectly affects both renewal and maintenance of existing and future coral communities, coral reef biodiversity (bottom-up effect) and therefore coral reef resilience. This process has been used as an indirect measure of individual reproductive success (fitness) and is the final stage of larval dispersal leading to population connectivity. As a result, recruitment has been proposed as an indicator of coral-reef health in marine protected areas, as well as a central aspect of the decision-making process concerning management and conservation. The creation of management plans to promote impact mitigation,rehabilitation and conservation of the Colombian coral reefs is a necessity that requires firstly, a review and integration of existing literature on scleractinian coral recruitment in Colombia and secondly, larger scale field studies. This motivated us to summarize and analyze all existing information on coral recruitment to determine the state of knowledge, isolate patterns, identify gaps, and suggest future lines of research.

The life history and ecology of black scabbardfish (Aphanopus carbo Lowe 1839) in the north-east Atlantic

The black scabbardfish is a deep water species that supports commercial fisheries across a large area of the NE Atlantic shelf. The life history of black scabbardfish is poorly understood and a major unresolved issue is population structure. In this study it was used a combination of methodologies to get further knowledge in the life history and population structure of A. carbo over its wide distribution range in the Northeast Atlantic. The new knowledge acquired during this study, will increase our ability to better manage this species in the NE Atlantic. It has been postulated that fish caught to the west of the British Isles are pre-adults that migrate further south (to Madeira) for spawning, implying a single panmictic population. In this study, specimens of Aphanopus carbo were sampled between September 2008 and May 2010 from two different areas: NW Scotland (French trawlers and deep water surveys) and Madeira Islands (longliners commercial landings). Geographical differences in reproductive state of scabbardfish were evident, supportive of a north-south migration theory. In the northern area, all specimens found were immature, while in Madeira all maturity stages were observed. In Madeira, spawning occurred during the fourth quarter, with peak maturity in October (males) and in November (females). The age of this species has proven difficult and has led to different and contradictory age and growth estimates. For this study, we used two reading interpretations to determine age and estimate the growth parameters. To the west of the British Isles, specimens reached a lower maximum age and had a higher growth rate than those caught off Madeira. These differences are consistent with the theory of a single population of black scabbardfish in the NE Atlantic, highly segregate, with smaller, immature and younger fish caught to the west of the British Isles and bigger and mature caught in Madeira Islands. The feeding ecology showed strong evidence that the diet of black scabbardfish is associated with the spawning migration of blue whiting, which may support a northerly feeding migration theory for black scabbardfish. The stable isotope analyses in the muscle of black scabbardfish identified that black scabbardfish feeds on species with epipelagic and benthopelagic affinities. Comparison with stable isotope analysis in Madeira samples indicated that black scabbardfish feed at a similar trophic level and has the same trophic niche width in both areas, assuming similar baseline isotope compositions. Otolith stable isotopes (oxygen - δ18O and nitrogen - δ15N) analyses were used as a tool to clarify migratory behaviour. Otolith isotope ratios can provide insight into whether adults caught around Madeira fed in an isotopically depleted northerly ecosystem (NW Scotland) during their pre-adult period and then migrate towards south to spawn. Overall, the results support a south-north migration of pre adult fish from spawning areas around Madeira and a north-south migration from the west of Scotland to the spawning areas. Given its life cycle there is an urgent need that the management process recognizes the existence of a continuous widely distributed stock of black scabbardfish between the west of the British Isles and Madeira. The results highlight large scale dispersal in this species which needs to be treated as a highly migratory species and be managed as a single population.

Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast

Extreme variation in early life-history strategies is considered a moderately good predictor of genetic subdivision and hence dispersal for a range of marine species. In reality, however, a good deal of population differentiation must reflect historical effects, more subtle variation in life histories, and, particularly, the interaction of larvae with oceanographic processes. Using a combination of allozyme and microsatellite markers, we show that the large-scale genetic structure of populations of three species (direct and planktonically developing cushion stars and a planktonic developing sea anemone that is also asexually viviparous) varies consistently, in line with the predicted capacity for dispersal within three geographic regions. We detected high levels of genetic subdivision for the direct developing cushion star (FST = 0.6), low levels for the planktonically developing cushion star (FST = 0.009), and intermediate levels for the sexual/asexual sea anmone (FST = 0.19). These patterns are exhibited despite the highly variable patterns of current movement and the presence of biogeographic barriers. Our results suggest that, although there is large scale genetic differentiation for two species, patterns of population connectivity are remarkably consistent within major regions and do not reflect variation in major oceanographic processes or genetic discontinuity coincident with biogeographic boundaries.