Christine L. Dudgeon

A review of the application of molecular genetics for fisheries management and conservation of sharks and rays

Since the first investigation 25 years ago, the application of genetic tools to address ecological and evolutionary questions in elasmobranch studies has greatly expanded. Major developments in genetic theory as well as in the availability, cost effectiveness and resolution of genetic markers were instrumental for particularly rapid progress over the last 10 years. Genetic studies of elasmobranchs are of direct importance and have application to fisheries management and conservation issues such as the definition of management units and identification of species from fins. In the future, increased application of the most recent and emerging technologies will enable accelerated genetic data production and the development of new markers at reduced costs, paving the way for a paradigm shift from gene to genome-scale research, and more focus on adaptive rather than just neutral variation. Current literature is reviewed in six fields of elasmobranch molecular genetics relevant to fisheries and conservation management (species identification, phylogeography, philopatry, genetic effective population size, molecular evolutionary rate and emerging methods). Where possible, examples from the Indo-Pacific region, which has been underrepresented in previous reviews, are emphasized within a global perspective.

Evidence for Sympatric Speciation by Host Shift in the Sea

The genetic divergence and evolution of new species within the geographic range of a single population (sympatric speciation) contrasts with the well-established doctrine that speciation occurs when populations become geographically isolated (allopatric speciation). Although there is considerable theoretical support for sympatric speciation, this mode of diversification remains controversial, at least in part because there are few well-supported examples. We use a combination of molecular, ecological, and biogeographical data to build a case for sympatric speciation by host shift in a new species of coral-dwelling fish (genus Gobiodon). We propose that competition for preferred coral habitats drives host shifts in Gobiodon and that the high diversity of corals provides the source of novel, unoccupied habitats. Disruptive selection in conjunction with strong host fidelity could promote rapid reproductive isolation and ultimately lead to species divergence. Our hypothesis is analogous to sympatric speciation by host shift in phytophagous insects except that we propose a primary role for intraspecific competition in the process of speciation. The fundamental similarity between these fishes and insects is a specialized and intimate relationship with their hosts that makes them ideal candidates for speciation by host shift.

IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo‐West Pacific

The Indo‐West Pacific (IWP), from South Africa in the western Indian Ocean to the western Pacific Ocean, contains some of the most biologically diverse marine habitats on earth, including the greatest biodiversity of chondrichthyan fishes. The region encompasses various densities of human habitation leading to contrasts in the levels of exploitation experienced by chondrichthyans, which are targeted for local consumption and export. The demersal chondrichthyan, the zebra shark, Stegostoma fasciatum, is endemic to the IWP and has two current regional International Union for the Conservation of Nature (IUCN) Red List classifications that reflect differing levels of exploitation: ‘Least Concern’ and ‘Vulnerable’. In this study, we employed mitochondrial ND4 sequence data and 13 microsatellite loci to investigate the population genetic structure of 180 zebra sharks from 13 locations throughout the IWP to test the concordance of IUCN zones with demographic units that have conservation value. Mitochondrial and microsatellite data sets from samples collected throughout northern Australia and Southeast Asia concord with the regional IUCN classifications. However, we found evidence of genetic subdivision within these regions, including subdivision between locations connected by habitat suitable for migration. Furthermore, parametric FST analyses and Bayesian clustering analyses indicated that the primary genetic break within the IWP is not represented by the IUCN classifications but rather is congruent with the Indonesian throughflow current. Our findings indicate that recruitment to areas of high exploitation from nearby healthy populations in zebra sharks is likely to be minimal, and that severe localized depletions are predicted to occur in zebra shark populations throughout the IWP region.

Integrating research using animal‐borne telemetry with the needs of conservation management

Animal-borne telemetry has revolutionized our ability to study animal movement, species physiology, demography and social structures, changing environments and the threats that animals are experiencing. While there will always be a need for basic ecological research and discovery, the current conservation crisis demands we look more pragmatically at the data required to make informed management decisions. Here, we define a framework that distinguishes how research using animal telemetry devices can influence conservation. We then discuss two critical questions which aim to directly connect telemetry-derived data to applied conservation decision-making: (i) Would my choice of action change if I had more data? (ii) Is the expected gain worth the money and time required to collect more data? Policy implications. To answer questions about integrating telemetry-derived data with applied conservation, we suggest the use of value of information analysis to quantitatively assess the return-on-investment of animal telemetry-derived data for conservation decision-making.

A Citizen Science Approach: A Detailed Ecological Assessment of Subtropical Reefs at Point Lookout, Australia

Subtropical reefs provide an important habitat for flora and fauna, and proper monitoring is required for conservation. Monitoring these exposed and submerged reefs is challenging and available resources are limited. Citizen science is increasing in momentum, as an applied research tool and in the variety of monitoring approaches adopted. This paper aims to demonstrate an ecological assessment and mapping approach that incorporates both top-down (volunteer marine scientists) and bottom-up (divers/community) engagement aspects of citizen science, applied at a subtropical reef at Point Lookout, Southeast Queensland, Australia. Marine scientists trained fifty citizen scientists in survey techniques that included mapping of habitat features, recording of substrate, fish and invertebrate composition, and quantifying impacts (e.g., occurrence of substrate damage, presence of litter). In 2014 these volunteers conducted four seasonal surveys along semi-permanent transects, at five sites, across three reefs. The project presented is a model on how citizen science can be conducted in a marine environment through collaboration of volunteer researchers, non-researchers and local marine authorities. Significant differences in coral and algal cover were observed among the three sites, while fluctuations in algal cover were also observed seasonally. Differences in fish assemblages were apparent among sites and seasons, with subtropical fish groups observed more commonly in colder seasons. The least physical damage occurred in the most exposed sites (Flat Rock) within the highly protected marine park zones. The broad range of data collected through this top-down/bottom-up approach to citizen science exemplifies the projects’ value and application for identifying ecosystem trends or patterns. The results of the project support natural resource and marine park management, providing a valuable contribution to existing scientific knowledge and the conservation of local reefs.

Integrating acoustic telemetry into mark-recapture models to improve the precision of apparent survival and abundance estimates

Capture–mark–recapture models are useful tools for estimating demographic parameters but often result in low precision when recapture rates are low. Low recapture rates are typical in many study systems including fishing-based studies. Incorporating auxiliary data into the models can improve precision and in some cases enable parameter estimation. Here, we present a novel application of acoustic telemetry for the estimation of apparent survival and abundance within capture–mark–recapture analysis using open population models. Our case study is based on simultaneously collecting longline fishing and acoustic telemetry data for a large mobile apex predator, the broadnose sevengill shark (Notorhynchus cepedianus), at a coastal site in Tasmania, Australia. Cormack–Jolly–Seber models showed that longline data alone had very low recapture rates while acoustic telemetry data for the same time period resulted in at least tenfold higher recapture rates. The apparent survival estimates were similar for the two datasets but the acoustic telemetry data showed much greater precision and enabled apparent survival parameter estimation for one dataset, which was inestimable using fishing data alone. Combined acoustic telemetry and longline data were incorporated into Jolly–Seber models using a Monte Carlo simulation approach. Abundance estimates were comparable to those with longline data only; however, the inclusion of acoustic telemetry data increased precision in the estimates. We conclude that acoustic telemetry is a useful tool for incorporating in capture–mark–recapture studies in the marine environment. Future studies should consider the application of acoustic telemetry within this framework when setting up the study design and sampling program.

Switch from sexual to parthenogenetic reproduction in a zebra shark

Parthenogenesis is a natural form of asexual reproduction in which embryos develop in the absence of fertilisation. Most commonly found in plants and invertebrate organisms, an increasing number of vertebrate species have recently been reported employing this reproductive strategy. Here we use DNA genotyping to report the first demonstration of an intra-individual switch from sexual to parthenogenetic reproduction in a shark species, the zebra shark Stegostoma fasciatum. A co-housed, sexually produced daughter zebra shark also commenced parthenogenetic reproduction at the onset of maturity without any prior mating. The demonstration of parthenogenesis in these two conspecific individuals with different sexual histories provides further support that elasmobranch fishes may flexibly adapt their reproductive strategy to environmental circumstances.

Strong population structure deduced from genetics, otolith chemistry and parasite abundances explains vulnerability to localized fishery collapse in a large Sciaenid fish, Protonibea diacanthus

As pressure on coastal marine resources is increasing globally, the need to quantitatively assess vulnerable fish stocks is crucial in order to avoid the ecological consequences of stock depletions. Species of Sciaenidae (croakers, drums) are important components of tropical and temperate fisheries and are especially vulnerable to exploitation. The black‐spotted croaker, Protonibea diacanthus, is the only large sciaenid in coastal waters of northern Australia where it is targeted by commercial, recreational and indigenous fishers due to its food value and predictable aggregating behaviour. Localized declines in the abundance of this species have been observed, highlighting the urgent requirement by managers for information on fine‐ and broad‐scale population connectivity. This study examined the population structure of P. diacanthus across north‐western Australia using three complementary methods: genetic variation in microsatellite markers, otolith elemental composition and parasite assemblage composition. The genetic analyses demonstrated that there were at least five genetically distinct populations across the study region, with gene flow most likely restricted by inshore biogeographic barriers such as the Dampier Peninsula. The otolith chemistry and parasite analyses also revealed strong spatial variation among locations within broad‐scale regions, suggesting fine‐scale location fidelity within the lifetimes of individual fish. The complementarity of the three techniques elucidated patterns of connectivity over a range of spatial and temporal scales. We conclude that fisheries stock assessments and management are required at fine scales (100 s of km) to account for the restricted exchange among populations (stocks) and to prevent localized extirpations of this species. Realistic management arrangements may involve the successive closure and opening of fishing areas to reduce fishing pressure.

Fine scale population structure of dugongs (Dugong dugon) implies low gene flow along the southern Queensland coastline

Populations of marine mammals can show the signature of phylogeographical breaks and restricted connectivity despite the apparent lack of physical boundaries in the marine environment and their high dispersal abilities. Dugongs (Dugong dugon) do not appear to undertake regular migrations but may show localised movement related to water temperature or seagrass availability. Previous mitochondrial DNA studies suggested that despite a strong phylogeographic break in the Torres Strait, there is local panmixia in Australian waters. In this study, we conducted a comprehensive study of the four major dugong populations in southern Queensland. We analysed genotypes of 1,293 dugongs based on 24 microsatellite loci from the four major dugong locations in the region (from south to north): Moreton Bay, Great Sandy Straits, Hervey Bay and Shoalwater Bay. Diversity levels were similar across locations (observed heterozygosity 0.48–0.52, allelic richness 4.3–4.5). There was low but significant population differentiation in southern Queensland (FST ranged from 0.005 to 0.040 and Jost’s DEST ranged from 0.001 to 0.031 for microsatellite data). Bayesian clustering analysis implemented in STRUCTURE largely distinguished the southern Moreton Bay population from the three more northern populations. Twelve mitochondrial control region haplotypes identified from a subset of 182 samples confirmed significant population structuring (FST ranged from 0.16 to 0.28). These data suggested that the frequency and extent of dugong movements are insufficient to disrupt the long-term existence of at least two breeding populations in southern Queensland.

Stock structure of Lethrinus laticaudis (Lethrinidae) across northern Australia determined using genetics, otolith microchemistry and parasite assemblage composition

The grass emperor Lethrinus laticaudis is a conspicuous element of the commercial and recreational catch from nearshore reef systems across northern Australia. The nearshore reef systems across northern Australia are exposed to increasing levels of fishing pressure from commercial and recreational fishers. To inform ongoing management of this species, the present study examined the stock structure of L. laticaudis across northern Australia using a combination of complementary techniques. In all, 342 L. laticaudis samples were collected from 13 locations in the coastal waters of northern Australia ranging from the Pilbara region of Western Australia to Moreton Bay in south-east Queensland. Population genetic analyses using microsatellite markers demonstrated that there were at least four genetically distinct populations across northern Australia with gene flow between management jurisdictions (with significantly more separation between Western Australian and Northern Territory locations than between Northern Territory and Queensland locations). An isolation by distance effect was evident (genetic differences increasing linearly with distance). Otolith microchemistry and parasitology analyses indicated some spatial structuring of populations within broader regions. These findings of restricted connectivity at small spatial scales suggest that L. laticaudis is vulnerable to localised depletion in areas where fishing effort is concentrated. This conclusion is consistent with recent observations of fishery declines in heavily fished locations.