Kady Lyons

Effects of trophic ecology and habitat use on maternal transfer of contaminants in four species of young of the year lamniform sharks

Organic contaminant and total mercury concentrations were compared in four species of lamniform sharks over several age classes to examine bioaccumulation patterns and gain insights into trophic ecology. Contaminants found in young of the year (YOY) sharks were assumed to be derived from maternal sources and used as a proxy to investigate factors that influence maternal offloading processes. YOY white (Carcharodon carcharias) and mako (Isurus oxyrinchus) sharks had comparable and significantly higher concentrations of PCBs, DDTs, pesticides, and mercury than YOY thresher (Alopias vulpinus) or salmon (Lamna ditropis) sharks. A significant positive relationship was found between YOY contaminant loads and maternal trophic position, suggesting that trophic ecology is one factor that plays an important role in maternal offloading. Differences in organic contaminant signatures and contaminant concentration magnitudes among species corroborated what is known about species habitat use and may be used to provide insights into the feeding ecology of these animals.

Evidence of maternal offloading of organic contaminants in white sharks (Carcharodon carcharias).

Organic contaminants were measured in young of the year (YOY) white sharks (Carcharodon carcharias) incidentally caught in southern California between 2005 and 2012 (n = 20) and were found to be unexpectedly high considering the young age and dietary preferences of young white sharks, suggesting these levels may be due to exposure in utero. To assess the potential contributions of dietary exposure to the observed levels, a five-parameter bioaccumulation model was used to estimate the total loads a newborn shark would potentially accumulate in one year from consuming contaminated prey from southern California. Maximum simulated dietary accumulation of DDTs and PCBs were 25.1 and 4.73 µg/g wet weight (ww) liver, respectively. Observed ΣDDT and ΣPCB concentrations (95±91 µg/g and 16±10 µg/g ww, respectively) in a majority of YOY sharks were substantially higher than the model predictions suggesting an additional source of contaminant exposure beyond foraging. Maternal offloading of organic contaminants during reproduction has been noted in other apex predators, but this is the first evidence of transfer in a matrotrophic shark. While there are signs of white shark population recovery in the eastern Pacific, the long-term physiological and population level consequences of biomagnification and maternal offloading of environmental contaminants in white sharks is unclear.

Ultrastructural and developmental features of the tessellated endoskeleton of elasmobranchs (sharks and rays)

The endoskeleton of elasmobranchs (sharks and rays) is comprised largely of unmineralized cartilage, differing fundamentally from the bony skeletons of other vertebrates. Elasmobranch skeletons are further distinguished by a tessellated surface mineralization, a layer of minute, polygonal, mineralized tiles called tesserae. This ‘tessellation’ has defined the elasmobranch group for more than 400 million years, yet the limited data on development and ultrastructure of elasmobranch skeletons (e.g. how tesserae change in shape and mineral density with age) have restricted our abilities to develop hypotheses for tessellated cartilage growth. Using high‐resolution, two‐dimensional and three‐dimensional materials and structural characterization techniques, we investigate an ontogenetic series of tessellated cartilage from round stingray Urobatis halleri, allowing us to define a series of distinct phases for skeletal mineralization and previously unrecognized features of tesseral anatomy. We show that the distinct tiled morphology of elasmobranch calcified cartilage is established early in U. halleri development, with tesserae forming first in histotroph embryos as isolated, globular islets of mineralized tissue. By the sub‐adult stage, tesserae have increased in size and grown into contact with one another. The intertesseral contact results in the formation of more geometric (straight‐edged) tesseral shapes and the development of two important features of tesseral anatomy, which we describe here for the first time. The first, the intertesseral joint, where neighboring tesserae abut without appreciable overlapping or interlocking, is far more complex than previously realized, comprised of a convoluted bearing surface surrounded by areas of fibrous attachment. The second, tesseral spokes, are lamellated, high‐mineral density features radiating outward, like spokes on a wheel, from the center of each tessera to its joints with its neighbors, likely acting as structural reinforcements of the articulations between tesserae. As tesserae increase in size during ontogeny, spokes are lengthened via the addition of new lamellae, resulting in a visually striking mineralization pattern in the larger tesserae of older adult skeletons when viewed with scanning electron microscopy (SEM) in backscatter mode. Backscatter SEM also revealed that the cell lacunae in the center of larger tesserae are often filled with high mineral density material, suggesting that when intratesseral cells die, cell‐regulated inhibition of mineralization is interrupted. Many of the defining ultrastructural details we describe relate to local variation in tissue mineral density and support previously proposed accretive growth mechanisms for tesserae. High‐resolution micro‐computed tomography data indicate that some tesseral anatomical features we describe for U. halleri are common among species of all major elasmobranch groups despite large variation in tesseral shape and size. We discuss hypotheses about how these features develop, and compare them with other vertebrate skeletal tissue types and their growth mechanisms.

Quantification of maternal offloading of organic contaminants in elasmobranchs using the histotrophic round stingray (Urobatis halleri) as a model.

Maternal offloading is one route by which young animals may accumulate persistent organic pollutants, such as dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCBs), but has not been well documented in elasmobranchs despite their propensity to accumulate high concentrations of contaminants. Using the round stingray (Urobatis halleri) as a coastal elasmobranch model, we examined maternal offloading processes at two stages in the stingrays entire reproductive cycle. Post-ovulated and near-term pregnant female stingrays were sampled from southern California, and organic contaminants were measured in the ova and embryonic tissues and compared to concentrations measured in corresponding female livers to determine route and extent of transfer. Total organic contaminant loads measured in ovulated eggs were about two times lower than loads measured in embryos (p < 0.001) indicating mothers have the ability to transfer contaminants throughout pregnancy. Contaminant loads measured in pups showed a positive relationship with mothers contaminant concentrations (p < 0.001); however, mothers offloaded relatively low percentages (1.5 ± 1.7%) of their total contaminant load using contaminants measured in the liver as a proxy. However, histotrophy is only one form of supplemental provisioning utilized by elasmobranchs and variation in reproductive modes likely influences the extent to which female elasmobranchs may maternally offload contaminants.

Who's My Daddy? Considerations for the influence of sexual selection on multiple paternity in elasmobranch mating systems

Abstract Polyandry resulting in multiply‐sired litters has been documented in the majority of elasmobranch species examined to date. Although commonly observed, reasons for this mating system remain relatively obscure, especially in batoids. The round stingray (Urobatis halleri) is an abundant, well‐studied elasmobranch distributed throughout the northeastern Pacific that we used to explore hypotheses regarding multiple paternity in elasmobranchs. Twenty mid‐ to late‐term pregnant females were sampled off the coast of southern California and their litters analyzed for the occurrence of multiple paternity using five nuclear microsatellite loci. In addition, embryo sizes and their position within the female reproductive system (i.e., right or left uterus) were recorded and used to make inferences for patterns of ovulation. Multiple paternity was observed in 90% of litters and male reproductive success within litters was relatively even among sires. High variability in testes mass was observed suggesting that sperm competition is high in this species, although male reproductive success per litter appeared to be relatively even. Using embryo size as a proxy for fertilization, females were found to exhibit a variety of ovulation patterns that could function to limit a males access to eggs and possibly promote high rates of multiple paternity. Our study highlights that elasmobranch mating systems may be more varied and complex than presumed and further investigation is warranted.

An evaluation of body condition and morphometric relationships within southern California juvenile white sharks Carcharodon carcharias

Length, mass and girth relationships are presented for 112 juvenile white sharks (JWS) Carcharodon carcharias caught in the Southern California Bight (SCB) nursery area between June 2008 and August 2017. No difference was found between male and female JWS length-mass relationships, but data suggest that JWS in the SCB gain more mass per unit length for the juvenile size classes compared with other C. carcharias populations. Condition-factor-to-liver-mass and condition-factor-to-liver-lipid-content relationships revealed that length and mass (i.e., condition factor) can be used as a non-invasive proxy for body condition for juveniles of this species. The parameters estimated in this study are key information for population assessments of juvenile C. carcharias in the north-east Pacific Ocean and will contribute to the conservation and management of this IUCN Red List Vulnerable species.

Influence of ontogeny and environmental exposure on mercury accumulation in muscle and liver of male Round Stingrays

Mercury tissue distribution and its dynamics are poorly understood in elasmobranchs. Total mercury was measured in liver and muscle of male Round Stingrays (Urobatis halleri) from Seal Beach, California, an anthropogenically impacted site, and from the offshore island of Santa Catalina, a less impacted site. Stable isotope analysis was also performed on the muscle and red blood cells (RBCs) of a subset of rays over a range of age classes to investigate mercury accumulation with respect to trophic ecology. Mercury in both tissues was found to be significantly greater in adults than juveniles in mainland rays; however, liver mercury accumulation drastically increased after maturity and was significantly greater in mainland adult rays than Catalina rays. There were no patterns in δ15N or δ13C with size in muscle; however, there were indications of seasonal changes in RBC δ15N, suggesting short term shifts in diet or behavior is likely linked to reproductive status as is mercury accumulation.