Sabine P. Wintner

Rescaling the trophic structure of marine food webs.

Measures of trophic position (TP) are critical for understanding food web interactions and human-mediated ecosystem disturbance. Nitrogen stable isotopes (δ15N) provide a powerful tool to estimate TP but are limited by a pragmatic assumption that isotope discrimination is constant (change in δ15N between predator and prey, Δ15N = 3.4‰), resulting in an additive framework that omits known Δ15N variation. Through meta-analysis, we determine narrowing discrimination from an empirical linear relationship between experimental Δ15N and δ15N values of prey consumed. The resulting scaled Δ15N framework estimated reliable TPs of zooplanktivores to tertiary piscivores congruent with known feeding relationships that radically alters the conventional structure of marine food webs. Apex predator TP estimates were markedly higher than currently assumed by whole-ecosystem models, indicating perceived food webs have been truncated and species-interactions over simplified. The scaled Δ15N framework will greatly improve the accuracy of trophic estimates widely used in ecosystem-based management.

Preliminary Study of Vertebral Growth Rings in the Whale Shark, Rhincodon typus, from the East Coast of South Africa

Growth rings (GR) in vertebral centra of 15 whale sharks, Rhincodon typus, four female (418–750 cm precaudal length), 10 male (422–770 cm), and one of unknown sex (688 cm), were examined using x-radiography. GR counts were made from scanned images and count precision was determined using the average percentage error index (4.19%) and the index of precision D (3.31%). In females, counts ranged from 19 GR (418 cm) to 27 GR (750 cm); in males from 20 GR (670 cm) to 31 GR (770 cm). Three mature males had 20 GR (670 cm), 24 GR (744 cm) and 27 GR (755 cm). A female with 22 GR (445 cm) was adolescent. There was a linear relationship between centrum dorsal diameter and body length, and back-calculated body lengths at number of GR are presented. A linear relationship between body length and number of GR prevented the calculation of von Bertalanffy parameters from either observed or back-calculated values.

Maternal investment and size-specific reproductive output in carcharhinid sharks

1. Life-history theory predicts that organisms will provide an optimal level of parental investment for offspring survival balanced against the effects on their own survival and future reproductive potential. 2. Optimal resource allocation models also predict an increase in reproductive output with age as expected future reproductive effort decreases. To date, maternal investment in sharks has received limited attention. 3. We found that neonatal dusky sharks (Carcharhinus obscurus) are not independent from maternal resource allocation at the point of parturition but instead are provisioned with energy reserves in the form of an enlarged liver that constitutes approximately 20% of total body mass. 4. Analysis of long-term archived data sets showed that a large proportion of this enlarged liver is utilized during the first weeks or months of life suggesting that the reported weight loss of newborn sharks signifies a natural orientation process and is not necessarily related to prey abundance and/or indicative of high mortality rates. 5. Interrogation of near-term pup mass in two carcharhinids, the dusky and spinner shark (Carcharhinus brevipinna), further revealed an increase in reproductive output with maternal size, with evidence for a moderate decline in the largest mothers. 6. For the dusky shark, there was a trade-off between increasing litter size and near-term pup mass in support of optimal offspring size theory. 7. For both the dusky and spinner shark, there was a linear increase in near-term pup mass with month, which may indicate variable parturition strategies and/or that carcharhinids are able to adjust the length of the gestation period. 8. The identification of optimal size-specific reproductive output has direct implications for improving the reproductive potential of exploited shark populations and for structuring future management strategies.

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

Manta and devil rays are an iconic group of globally distributed pelagic filter feeders, yet their evolutionary history remains enigmatic. We employed next generation sequencing of mitogenomes for nine of the 11 recognized species and two outgroups; as well as additional Sanger sequencing of two mitochondrial and two nuclear genes in an extended taxon sampling set. Analysis of the mitogenome coding regions in a Maximum Likelihood and Bayesian framework provided a well-resolved phylogeny. The deepest divergences distinguished three clades with high support, one containing Manta birostris, Manta alfredi, Mobula tarapacana, Mobula japanica and Mobula mobular; one containing Mobula kuhlii, Mobula eregoodootenkee and Mobula thurstoni; and one containing Mobula munkiana, Mobula hypostoma and Mobula rochebrunei. Mobula remains paraphyletic with the inclusion of Manta, a result that is in agreement with previous studies based on molecular and morphological data. A fossil-calibrated Bayesian random local clock analysis suggests that mobulids diverged from Rhinoptera around 30 Mya. Subsequent divergences are characterized by long internodes followed by short bursts of speciation extending from an initial episode of divergence in the Early and Middle Miocene (19-17 Mya) to a second episode during the Pliocene and Pleistocene (3.6 Mya - recent). Estimates of divergence dates overlap significantly with periods of global warming, during which upwelling intensity - and related high primary productivity in upwelling regions - decreased markedly. These periods are hypothesized to have led to fragmentation and isolation of feeding regions leading to possible regional extinctions, as well as the promotion of allopatric speciation. The closely shared evolutionary history of mobulids in combination with ongoing threats from fisheries and climate change effects on upwelling and food supply, reinforces the case for greater protection of this charismatic family of pelagic filter feeders.

Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator

The copper or bronze whaler shark (Carcharhinus brachyurus) is a large, coastal top predator that is vulnerable to overexploitation. We test the null hypothesis that copper sharks are panmictic throughout the southern hemisphere. We analysed part of the mitochondrial control region (mtCR) in 120 individuals from eight sampling areas, defining 20 mtCR haplotypes (h = 0.76 ± 0.06, π = 0.016 ± 0.0007). Significant genetic structure was detected among the following three major coastal regions separated by oceanic habitat: Australia–New Zealand, South Africa–Namibia and Peru (AMOVA ΦST = 0.95, P < 0.000001). A major phylogeographic discontinuity exists across the Indian Ocean, indicating an absence of at least female-mediated gene flow for ~3 million years. We propose that this species originated in the Atlantic, experienced vicariant isolation of Pacific and Atlantic lineages by the rise of the Isthmus of Panama and, subsequently, dispersed across the Pacific to colonise Australasia. Oceanic expanses appear to be traversed over evolutionary but not ecological timescales, which means that regional copper-shark populations should be assessed and managed independently.

Variable δ15N Diet-Tissue Discrimination Factors among Sharks: Implications for Trophic Position, Diet and Food Web Models

The application of stable isotopes to characterize the complexities of a species foraging behavior and trophic relationships is dependent on assumptions of δ15N diet-tissue discrimination factors (∆15N). As ∆15N values have been experimentally shown to vary amongst consumers, tissues and diet composition, resolving appropriate species-specific ∆15N values can be complex. Given the logistical and ethical challenges of controlled feeding experiments for determining ∆15N values for large and/or endangered species, our objective was to conduct an assessment of a range of reported ∆15N values that can hypothetically serve as surrogates for describing the predator-prey relationships of four shark species that feed on prey from different trophic levels (i.e., different mean δ15N dietary values). Overall, the most suitable species-specific ∆15N values decreased with increasing dietary-δ15N values based on stable isotope Bayesian ellipse overlap estimates of shark and the principal prey functional groups contributing to the diet determined from stomach content analyses. Thus, a single ∆15N value was not supported for this speciose group of marine predatory fishes. For example, the ∆15N value of 3.7‰ provided the highest percent overlap between prey and predator isotope ellipses for the bonnethead shark (mean diet δ15N = 9‰) whereas a ∆15N value < 2.3‰ provided the highest percent overlap between prey and predator isotope ellipses for the white shark (mean diet δ15N = 15‰). These data corroborate the previously reported inverse ∆15N-dietary δ15N relationship when both isotope ellipses of principal prey functional groups and the broader identified diet of each species were considered supporting the adoption of different ∆15N values that reflect the predators’ δ15N-dietary value. These findings are critical for refining the application of stable isotope modeling approaches as inferences regarding a species’ ecological role in their community will be influenced with consequences for conservation and management actions.

Maximum age and missing time in the vertebrae of sand tiger shark (Carcharias taurus): validated lifespan from bomb radiocarbon dating in the western North Atlantic and southwestern Indian Oceans

Bomb radiocarbon analysis of vertebral growth bands was used to validate lifespan for sand tiger sharks (Carcharias taurus) from the western North Atlantic (WNA) and southwestern Indian Oceans (SIO). Visual counts of vertebral growth bands were used to assign age and estimate year of formation (YOF) for sampled growth bands in eight sharks from the WNA and two sharks from the SIO. Carbon-14 results were plotted relative to YOF for comparison with regional Δ14C reference chronologies to assess the accuracy of age estimates. Results from the WNA validated vertebral age estimates up to 12 years, but indicated that ages of large adult sharks were underestimated by 11–12 years. Age was also underestimated for adult sharks from the SIO by 14–18 years. Validated lifespan for C. taurus individuals in the present study reached at least 40 years for females and 34 years for males. Findings indicated that the current age-reading methodology is not suitable for estimating the age of C. taurus beyond ~12 years. Future work should investigate whether vertebrae of C. taurus record age throughout ontogeny, or cease to be a reliable indicator at some point in time.

Laser photogrammetry improves size and demographic estimates for whale sharks.

Whale sharks Rhincodon typus are globally threatened, but a lack of biological and demographic information hampers an accurate assessment of their vulnerability to further decline or capacity to recover. We used laser photogrammetry at two aggregation sites to obtain more accurate size estimates of free-swimming whale sharks compared to visual estimates, allowing improved estimates of biological parameters. Individual whale sharks ranged from 432–917 cm total length (TL) (mean ± SD = 673 ± 118.8 cm, N = 122) in southern Mozambique and from 420–990 cm TL (mean ± SD = 641 ± 133 cm, N = 46) in Tanzania. By combining measurements of stranded individuals with photogrammetry measurements of free-swimming sharks, we calculated length at 50% maturity for males in Mozambique at 916 cm TL. Repeat measurements of individual whale sharks measured over periods from 347–1,068 days yielded implausible growth rates, suggesting that the growth increment over this period was not large enough to be detected using laser photogrammetry, and that the method is best applied to estimating growth rates over longer (decadal) time periods. The sex ratio of both populations was biased towards males (74% in Mozambique, 89% in Tanzania), the majority of which were immature (98% in Mozambique, 94% in Tanzania). The population structure for these two aggregations was similar to most other documented whale shark aggregations around the world. Information on small (<400 cm) whale sharks, mature individuals, and females in this region is lacking, but necessary to inform conservation initiatives for this globally threatened species.

Population Expansion and Genetic Structure in Carcharhinus brevipinna in the Southern Indo-Pacific

Background Quantifying genetic diversity and metapopulation structure provides insights into the evolutionary history of a species and helps develop appropriate management strategies. We provide the first assessment of genetic structure in spinner sharks (Carcharhinus brevipinna), a large cosmopolitan carcharhinid, sampled from eastern and northern Australia and South Africa. Methods and Findings Sequencing of the mitochondrial DNA NADH dehydrogenase subunit 4 gene for 430 individuals revealed 37 haplotypes and moderately high haplotype diversity (h = 0.6770 ±0.025). While two metrics of genetic divergence (ΦST and F ST) revealed somewhat different results, subdivision was detected between South Africa and all Australian locations (pairwise ΦST, range 0.02717–0.03508, p values ≤ 0.0013; pairwise F ST South Africa vs New South Wales = 0.04056, p = 0.0008). Evidence for fine-scale genetic structuring was also detected along Australia’s east coast (pairwise ΦST = 0.01328, p < 0.015), and between south-eastern and northern locations (pairwise ΦST = 0.00669, p < 0.04). Conclusions The Indian Ocean represents a robust barrier to contemporary gene flow in C. brevipinna between Australia and South Africa. Gene flow also appears restricted along a continuous continental margin in this species, with data tentatively suggesting the delineation of two management units within Australian waters. Further sampling, however, is required for a more robust evaluation of the latter finding. Evidence indicates that all sampled populations were shaped by a substantial demographic expansion event, with the resultant high genetic diversity being cause for optimism when considering conservation of this commercially-targeted species in the southern Indo-Pacific.

Genetic Diversity of White Sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa

The white shark, Carcharodon carcharias, is both one of the largest apex predators in the world and among the most heavily protected marine fish. Population genetic diversity is in part shaped by recent demographic history and can thus provide information complementary to more traditional population assessments, which are difficult to obtain for white sharks and have at times been controversial. Here, we use the mitochondrial control region and 14 nuclear-encoded microsatellite loci to assess white shark genetic diversity in 2 regions: the Northwest Atlantic (NWA, N = 35) and southern Africa (SA, N = 131). We find that these 2 regions harbor genetically distinct white shark populations (Φ ST = 0.10, P < 0.00001; microsatellite F ST = 0.1057, P < 0.021). M-ratios were low and indicative of a genetic bottleneck in the NWA (M-ratio = 0.71, P < 0.004) but not SA (M-ratio = 0.85, P = 0.39). This is consistent with other evidence showing a steep population decline occurring in the mid to late 20th century in the NWA, whereas the SA population appears to have been relatively stable. Estimates of effective population size ranged from 22.6 to 66.3 (NWA) and 188 to 1998.3 (SA) and evidence of inbreeding was found (primarily in NWA). Overall, our findings indicate that white population dynamics within NWA and SA are determined more by intrinsic reproduction than immigration and there is genetic evidence of a population decline in the NWA, further justifying the strong domestic protective measures that have been taken for this species in this region. Our study also highlights how assessment of genetic diversity can complement other sources of information to better understand the status of threatened marine fish populations.