Aaron B. Carlisle

Using Stable Isotope Analysis to Understand the Migration and Trophic Ecology of Northeastern Pacific White Sharks (Carcharodon carcharias)

The white shark (Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (δ13C) and nitrogen (δ15N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle δ13C and δ15N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.

Tissue Turnover Rates and Isotopic Trophic Discrimination Factors in the Endothermic Teleost, Pacific Bluefin Tuna (Thunnus orientalis)

Stable isotope analysis (SIA) of highly migratory marine pelagic animals can improve understanding of their migratory patterns and trophic ecology. However, accurate interpretation of isotopic analyses relies on knowledge of isotope turnover rates and tissue-diet isotope discrimination factors. Laboratory-derived turnover rates and discrimination factors have been difficult to obtain due to the challenges of maintaining these species in captivity. We conducted a study to determine tissue- (white muscle and liver) and isotope- (nitrogen and carbon) specific turnover rates and trophic discrimination factors (TDFs) using archived tissues from captive Pacific bluefin tuna (PBFT), Thunnus orientalis, 1–2914 days after a diet shift in captivity. Half-life values for 15N turnover in white muscle and liver were 167 and 86 days, and for 13C were 255 and 162 days, respectively. TDFs for white muscle and liver were 1.9 and 1.1‰ for δ 15N and 1.8 and 1.2‰ for δ 13C, respectively. Our results demonstrate that turnover of 15N and 13C in bluefin tuna tissues is well described by a single compartment first-order kinetics model. We report variability in turnover rates between tissue types and their isotope dynamics, and hypothesize that metabolic processes play a large role in turnover of nitrogen and carbon in PBFT white muscle and liver tissues. 15N in white muscle tissue showed the most predictable change with diet over time, suggesting that white muscle δ 15N data may provide the most reliable inferences for diet and migration studies using stable isotopes in wild fish. These results allow more accurate interpretation of field data and dramatically improve our ability to use stable isotope data from wild tunas to better understand their migration patterns and trophic ecology.

Stable Isotope Analysis Challenges Wasp-Waist Food Web Assumptions in an Upwelling Pelagic Ecosystem

Eastern boundary currents are often described as ‘wasp-waist’ ecosystems in which one or few mid-level forage species support a high diversity of larger predators that are highly susceptible to fluctuations in prey biomass. The assumption of wasp-waist control has not been empirically tested in all such ecosystems. This study used stable isotope analysis to test the hypothesis of wasp-waist control in the southern California Current large marine ecosystem (CCLME). We analyzed prey and predator tissue for δ13C and δ15N and used Bayesian mixing models to provide estimates of CCLME trophic dynamics from 2007–2010. Our results show high omnivory, planktivory by some predators, and a higher degree of trophic connectivity than that suggested by the wasp-waist model. Based on this study period, wasp-waist models oversimplify trophic dynamics within the CCLME and potentially other upwelling, pelagic ecosystems. Higher trophic connectivity in the CCLME likely increases ecosystem stability and resilience to perturbations.

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.

Climate mediates hypoxic stress on fish diversity and nursery function at the land–sea interface

Significance Human populations are rapidly expanding along Earths coastlines, increasing stress to coastal ecosystems and the services they provide. One of these stressors comes from an increase in nutrient inputs from coastal land development that can enter estuaries and coastal seas leading to algal blooms that deplete oxygen from the water, a condition known as hypoxia. In this study, we investigated how coastal hypoxia influences fish diversity, the nursery habitat for juvenile fish, and fisheries production in adjacent offshore waters. We found that severity in hypoxia corresponded with declines to fish diversity, nursery quality, and offshore fisheries. Furthermore, intensification of El Niño mediated hypoxia by improving dissolved oxygen conditions, demonstrating that climate can influence anthropogenic stressors affecting coastal ecosystem services. Coastal ecosystems provide numerous important ecological services, including maintenance of biodiversity and nursery grounds for many fish species of ecological and economic importance. However, human population growth has led to increased pollution, ocean warming, hypoxia, and habitat alteration that threaten ecosystem services. In this study, we used long-term datasets of fish abundance, water quality, and climatic factors to assess the threat of hypoxia and the regulating effects of climate on fish diversity and nursery conditions in Elkhorn Slough, a highly eutrophic estuary in central California (United States), which also serves as a biodiversity hot spot and critical nursery grounds for offshore fisheries in a broader region. We found that hypoxic conditions had strong negative effects on extent of suitable fish habitat, fish species richness, and abundance of the two most common flatfish species, English sole (Parophrys vetulus) and speckled sanddab (Citharichthys stigmaeus). The estuary serves as an important nursery ground for English sole, making this species vulnerable to anthropogenic threats. We determined that estuarine hypoxia was associated with significant declines in English sole nursery habitat, with cascading effects on recruitment to the offshore adult population and fishery, indicating that human land use activities can indirectly affect offshore fisheries. Estuarine hypoxic conditions varied spatially and temporally and were alleviated by strengthening of El Niño conditions through indirect pathways, a consistent result in most estuaries across the northeast Pacific. These results demonstrate that changes to coastal land use and climate can fundamentally alter the diversity and functioning of coastal nurseries and their adjacent ocean ecosystems.

Reconstructing transoceanic migration patterns of Pacific bluefin tuna using a chemical tracer toolbox

Large pelagic predators play important roles in oceanic ecosystems, and may migrate vast distances to utilize resources in different marine ecoregions. Understanding movement patterns of migratory marine animals is critical for effective management, but often challenging, due to the cryptic habitat of pelagic migrators and the difficulty of assessing past movements. Chemical tracers can partially circumvent these challenges by reconstructing recent migration patterns. Pacific bluefin tuna (Thunnus orientalis; PBFT) inhabit the western and eastern Pacific Ocean, and are in steep decline due to overfishing. Understanding age-specific eastward transpacific migration patterns can improve management practices, but these migratory dynamics remain largely unquantified. Here, we combine a Fukushima-derived radiotracer (134Cs) with bulk tissue and amino acid stable isotope analyses of PBFT to distinguish recent migrants from residents of the eastern Pacific Ocean. The proportion of recent migrants to residents decreased in older year classes, though the proportion of older PBFT that recently migrated across the Pacific was greater than previous estimates. This novel toolbox of biogeochemical tracers can be applied to any species that crosses the North Pacific Ocean.

Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark

Ontogenetic changes in habitat are driven by shifting life-history requirements and play an important role in population dynamics. However, large portions of the life history of many pelagic species are still poorly understood or unknown. We used a novel combination of stable isotope analysis of vertebral annuli, Bayesian mixing models, isoscapes and electronic tag data to reconstruct ontogenetic patterns of habitat and resource use in a pelagic apex predator, the salmon shark (Lamna ditropis). Results identified the North Pacific Transition Zone as the major nursery area for salmon sharks and revealed an ontogenetic shift around the age of maturity from oceanic to increased use of neritic habitats. The nursery habitat may reflect trade-offs between prey availability, predation pressure and thermal constraints on juvenile endothermic sharks. The ontogenetic shift in habitat coincided with a reduction of isotopic niche, possibly reflecting specialization upon particular prey or habitats. Using tagging data to inform Bayesian isotopic mixing models revealed that adult sharks primarily use neritic habitats of Alaska yet receive a trophic subsidy from oceanic habitats. Integrating the multiple methods used here provides a powerful approach to retrospectively study the ecology and life history of migratory species throughout their ontogeny.

Assessing niche width of endothermic fish from genes to ecosystem

Significance In large pelagic fish, as in birds and mammals, significant questions remain concerning the selective pressures that drove the evolution of endothermy. We examined cold tolerance and niche breadth on molecular, organism, and food web levels in three closely related tuna species. We show that energetic benefits of increased cold tolerance in fishes are context dependent: advantageous when quality prey is abundant, but not when such prey is scarce. We broaden our findings to the global level using published literature to show that endothermic bluefin species in all the world’s oceans specialize, to some degree, on high energy prey. Our multifaceted approach demonstrates the concept that the advantage of a “beneficial” adaptation is dependent on environmental and anthropogenic influences. Endothermy in vertebrates has been postulated to confer physiological and ecological advantages. In endothermic fish, niche expansion into cooler waters is correlated with specific physiological traits and is hypothesized to lead to greater foraging success and increased fitness. Using the seasonal co-occurrence of three tuna species in the eastern Pacific Ocean as a model system, we used cardiac gene expression data (as a proxy for thermal tolerance to low temperatures), archival tag data, and diet analyses to examine the vertical niche expansion hypothesis for endothermy in situ. Yellowfin, albacore, and Pacific bluefin tuna (PBFT) in the California Current system used more surface, mesopelagic, and deep waters, respectively. Expression of cardiac genes for calcium cycling increased in PBFT and coincided with broader vertical and thermal niche utilization. However, the PBFT diet was less diverse and focused on energy-rich forage fishes but did not show the greatest energy gains. Ecosystem-based management strategies for tunas should thus consider species-specific differences in physiology and foraging specialization.

A global perspective on the trophic geography of sharks

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.Carbon isotopic analysis reveals global biogeographic traits in shark trophic interactions, and sheds light on the diverse foraging behaviour of sharks.

The complete mitochondrial genome of the salmon shark, Lamna ditropis (Chondrichthyes, Lamnidae).

Abstract The complete mitochondrial genome of the salmon shark consists of 16,699 bp and includes 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, 1 replication origin region and 1 control region. The mitochondrial gene arrangement of the salmon shark is the same as that of most vertebrates. Base composition of the genome is A (29.6%), T (28.6%), C (27.1%), and G (14.8%).