Inferring population trends for the world's largest fish from mark-recapture estimates of survival

1. Precise estimates of demographic rates are key components of population models used to predict the effects of stochastic environmental processes, harvest scenarios and extinction probability. 2. We used a 12-year photographic identification library of whale sharks from Ningaloo Reef, Western Australia to construct Cormack-Jolly-Seber (CJS) model estimates of survival within a capture-mark-recapture (CMR) framework. Estimated survival rates, population structure and assumptions regarding age at maturity, longevity and reproduction frequency were combined in a series of age-classified Leslie matrices to infer the potential trajectory of the population. 3. Using data from 111 individuals, there was evidence for time variation in apparent survival (phi) and recapture probability (p). The null model gave a phi of 0.825 (95% CI: 0.727-0.893) and p = 0.184 (95% CI: 0.121-0.271). The model-averaged annual phi ranged from 0.737 to 0.890. There was little evidence for a sex effect on survival. 4. Using standardized total length as a covariate in the CMR models indicated a size bias in phi. Ignoring the effects of time, a 5-m shark has a phi = 0.59 and a 9 m shark has phi = 0.81. 5. Of the 16 model combinations considered, 10 (63%) indicated a decreasing population (lambda < 1). For models based on age at first reproduction (alpha) of 13 years, the mean age of reproducing females at the stable age distribution (A) ranged from 15 to 23 years, which increased to 29-37 years when alpha was assumed to be 25. 6. All model scenarios had higher total elasticities for non-reproductive female survival [E(s(nr))] compared to those for reproductive female survival [E(s(r))]. 7. Assuming relatively slow, but biologically realistic, vital rates (alpha = 25 and biennial reproduction) and size-biased survival probabilities, our results suggest that the Ningaloo Reef population of whale sharks is declining, although more reproductive data are clearly needed to confirm this conclusion. Combining relatively precise survival estimates from CMR studies with realistic assumptions of other vital rates provides a useful heuristic framework for determining the vulnerability of large oceanic predators for which few direct data exist.     

Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus)

Large pelagic vertebrates pose special conservation challenges because their movements generally exceed the boundaries of any single jurisdiction. To assess the population structure of whale sharks (Rhincodon typus), we sequenced complete mitochondrial DNA control regions from individuals collected across a global distribution. We observed 51 single site polymorphisms and 8 regions with indels comprising 44 haplotypes in 70 individuals, with high haplotype (h = 0.974 +/- 0.008) and nucleotide diversity (pi = 0.011 +/- 0.006). The control region has the largest length variation yet reported for an elasmobranch (1143-1332 bp). Phylogenetic analyses reveal no geographical clustering of lineages and the most common haplotype was distributed globally. The absence of population structure across the Indian and Pacific basins indicates that oceanic expanses and land barriers in Southeast Asia are not impediments to whale shark dispersal. We did, however, find significant haplotype frequency differences (AMOVA, Phi(ST) = 0.107, P < 0.001) principally between the Atlantic and Indo-Pacific populations. In contrast to other recent surveys of globally distributed sharks, we find much less population subdivision and no evidence for cryptic evolutionary partitions. Discovery of the mating and pupping areas of whale sharks is key to further population genetic studies. The global pattern of shared haplotypes in whale sharks provides a compelling argument for development of broad international approaches for management and conservation of Earth's largest fish.     

Single nucleotide polymorphisms in the interferon gamma gene are associated with distinct types of retinochoroidal scar lesions presumably caused by Toxoplasma gondii infection

The association of single nucleotide polymorphisms (SNPs) in the interferon (IFN)-γ gene ( IFNG ) with different types of retinal scar lesions presumably caused by toxoplasmosis were investigated in a cross-sectional population-based genetic study. Ten SNPs were investigated and after Bonferroni correction, only the associations between SNPs rs2069718 and rs3181035 with retinal/retinochoroidal scar lesions type A (most severe scar lesions) and C (least severe scar lesions), respectively, remained significant. The associations of two different IFNG SNPs with two different types of retinal lesions attributable to toxoplasmosis support the hypothesis that different inflammatory mechanisms underlie the development of these lesions. The in vitro analysis of IFN-γ secretion by peripheral blood mononuclear cells stimulated with Toxoplasma gondii antigens was also investigated. The association between SNP rs2069718 and type A scar lesions revealed that differential IFN-γ levels are correlated with distinct genotypes. However, no correlation was observed with IFN-γ secretion levels and the SNP rs3181035 , which was significantly associated with type C scar lesions. Our findings strongly suggest that immunogenetic studies of individuals with congenital or postnatally acquired infection are needed to better understand the role of IFN-γ and its polymorphisms in the pathogenesis of ocular toxoplasmosis.     

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.     

Identification of rays through DNA barcoding: an application for ecologists

DNA barcoding potentially offers scientists who are not expert taxonomists a powerful tool to support the accuracy of field studies involving taxa that are diverse and difficult to identify. The taxonomy of rays has received reasonable attention in Australia, although the fauna in remote locations such as Ningaloo Reef, Western Australia is poorly studied and the identification of some species in the field is problematic. Here, we report an application of DNA-barcoding to the identification of 16 species (from 10 genera) of tropical rays as part of an ecological study. Analysis of the dataset combined across all samples grouped sequences into clearly defined operational taxonomic units, with two conspicuous exceptions: the Neotrygon kuhlii species complex and the Aetobatus species complex. In the field, the group that presented the most difficulties for identification was the spotted whiptail rays, referred to as the 'uarnak' complex. Two sets of problems limited the successful application of DNA barcoding: (1) the presence of cryptic species, species complexes with unresolved taxonomic status and intra-specific geographical variation, and (2) insufficient numbers of entries in online databases that have been verified taxonomically, and the presence of lodged sequences in databases with inconsistent names. Nevertheless, we demonstrate the potential of the DNA barcoding approach to confirm field identifications and to highlight species complexes where taxonomic uncertainty might confound ecological data.     

Does behaviour explain the larval dispersal of coral reef fishes better than oceanography?– An individual based model simulation approach

We housed offspring from northern (70° N) and southern (60° N) coastal cod ( Gadus morhua ) together in a 'common garden' rearing experiment at a temperature and light regime representative of the southern population. Through a more active feeding behaviour and a higher success, the northern cod achieved a larger food share and a higher growth rate and condition than their southern conspecifics. This is contrary to what was demonstrated by field data of fish from their natural habitats. The northern cod also allocated more energy to the liver throughout the experiment. Our results agree with the theory of countergradient variation, suggesting that genetic influences on growth and condition have been opposed by environmental constraints in their natural habitat. The observation that the offspring from these populations differ in behavior and growth when housed together support the idea that the growth response to selection would be through a behavioral response.
The field data suggest that density‐dependent population process and high juvenile density relative to prey limit the growth and condition in the wild and not necessarily the length of the growth season per se as assumed in the literature. The topographic distance (over 2000 km) limit mixing of early life stages of cod from the northern and southern population, and the different environmental stimuli (seasonality, temperature, food‐web interactions and habitat heterogeneity) in north and south are likely to evolve genetic differences.     

Multi-Year Impacts of Ecotourism on Whale Shark (Rhincodon typus) Visitation at Ningaloo Reef,Western Australia

In-water viewing of sharks by tourists has become a popular and lucrative industry. There is some concern that interactions with tourists with ecotourism operations might harm sharks through disruption of behaviours. Here, we analysed five years of whale shark (Rhincodon typus) encounter data by an ecotourism industry at Ningaloo Reef, Western Australia, to assess the impact of ecotourism interactions on shark visitation, within the context of the biological and physical oceanography of the region. Our data base consisted of 2823 encounter records for 951 individual whale sharks collected by ecotourism operators between 2007 and 2011. We found that total encounters per whale shark and encounters per boat trip increased through time. On average, whale sharks re-encountered in subsequent years were encountered earlier, stayed longer and tended to be encountered more often within a season than sharks that were only encountered in a single year. Sequential comparisons between years did not show any patterns consistent with disturbance and the rate of departure of whale sharks from the aggregation was negatively correlated to the number of operator trips. Overall, our analysis of this multi-year data base found no evidence that interactions with tourists affected the likelihood of whale shark re-encounters and that instead, physical and biological environmental factors had a far greater influence on whale shark visitation rates. Our approach provides a template for assessing the effects of ecotourism interactions and environmental factors on the visitation patterns of marine megafauna over multiple years.