Daniel J. Madigan

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.

Insights into the life history and ecology of a large shortfin mako shark Isurus oxyrinchus captured in southern California

In June 2013, a record-breaking female Isurus oxyrinchus (total length 373 cm, mass 600 kg) was captured by rod and reel off Huntington Beach, California, where it was subsequently donated to research and provided a rare opportunity to collect the first data for a female I. oxyrinchus of this size. Counts of vertebral band pairs estimate the shark to have been c. 22 years old, depending upon assumptions of band-pair deposition rates, and the distended uteri and spent ovaries indicated that this shark had recently given birth. The stomach contained a c. 4 year-old female California sea lion Zalophus californianus that confirmed the high trophic position of this large I. oxyrinchus, which was corroborated with the high levels of measured contaminants and tissue isotope analyses.

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.

Stable isotope analysis in deep-sea chondrichthyans: recent challenges, ecological insights, and future directions

Deep-sea chondrichthyans are cryptic species subject to increasing anthropogenic exploitation. Defining their role in deep-water ecosystems is therefore crucial for predicting the ecosystem-wide effects of their removal. Stable isotope analyses (SIA) of carbon and nitrogen have been increasingly used in chondrichthyan studies as a non-lethal method to investigate aspects of their ecology. In recent years these methods have been applied to deep-sea chondricthyans to investigate their trophic structure, niche width, and describe energy flow in the deep sea. Despite the increasing popularity of SIA in deep-sea chondrichthyan studies, methods rely on a multitude of assumptions, such as the need to determine accurate trophic discrimination and tissue turnover rates, which are currently lacking for most species. These uncertainties may preclude the reliability of isotope-based approaches, and as a result inferences from isotopic data must be viewed with relative caution. Due to the growing use of isotopic-based approaches in deep-sea chondrichthyans, we review the literature in the context of current methodological challenges and ecological inferences. We provide recommendations and novel approaches that may help develop and refine a rapidly growing field of study.

Perspectives and reflections on the public reaction to recent Fukushima-related radionuclide studies and a call for enhanced training in environmental radioactivity.

Recent scientific publications addressing the release of radionuclides into the Pacific Ocean from the damaged Fukushima nuclear reactor in Japan, and in particular their bioaccumulation in marine fish (including some that have migrated to the west coast of the United States), have received remarkable public interest and extensive media attention. Most concern understandably focused on the public health impacts on seafood consumers, primarily reflecting fear about the impacts of any released radioactivity on human health. Equally as interesting as some of the scientific findings regarding biogeochemical cycling of radiocesium in the Pacific, or using this radionuclide to trace physical currents and migratory patterns of fish, was the public reaction to the finding that popular seafood items contained anthropogenic radioactivity. While radionuclide concentrations in fish that migrated to the United States were shown to be detectable, albeit very low, the public reaction was one of alarm and seemed to ignore the low probability of risk from these demonstrably low doses. Why? Since the 1960s, the scientific community and the general public have expressed concern over the presence of environmental contaminants in aquatic ecosystems and the influence that these contaminants may exert on whole ecosystems and/or individual species. Frequently, there is also pronounced concern about dangers to public health associated with contaminants. Indeed, many of these concerns are well founded as a wide variety of potentially toxic substances that are “new” to wildlife have been introduced into natural ecosystems. These include an ever-increasing array of organic compounds associated with agricultural or industrial practices. They also include inorganic contaminants, such as human-made radionuclides that are produced in the nuclear fuel cycle or by detonation of nuclear weapons. However, most contaminants in most aquatic ecosystems are well below concentrations that would elicit toxic effects in aquatic organisms, with perhaps the exception of methylmercury and certain persistent organic pollutants that tend to biomagnify in higher–trophic level fish, which in turn could lead to elevated contaminant exposures to the fishconsuming population. Nonetheless public concern occurs for both naturally occurring contaminants, whose presence may be amplified by human activities (e.g., As, Hg, Cr, others), and human-made contaminants (e.g., pesticides, halogenated hydrocarbons, and nuclear wastes). Such concern is expressed even when contaminant levels are well below those that present a public health risk. There have been, of course, rare and extreme instances involving high contamination leading to severe human health consequences. These include the methyl isocyanate gas poisoning in Bhopal, India, in 1984; the Chernobyl nuclear accident in 1986; and the methylmercury poisoning in Minamata, Japan, over many years. Some contaminants lead to neurological damage, intestinal problems, and cancer; carcinogenic substances typically elicit the greatest fears. Out of proportion to other possible contaminants, even other carcinogens, it has been our experience that radionuclides cause the greatest anxiety for the public. This is probably a legacy, in part, of the ColdWar era and all the attendant fears associated with nuclear warfare. It may also be attributable to cinematic depictions of nuclear mishaps and the creation of mutated monsters that decimate whole communities. It seems that people flock to these movies in part because they are intrigued by a novel danger (radioactivity) and in part because, based on the general success of the horror movie genre, people seem to enjoy getting scared. The psychology of this, however, may be a bit more complex. People in the 1950s and 1960s were terrified of the new nuclear threat. The job of nuclear monster movies may have been to “lift [people] out of the unbearably humdrum” and “normalize what is psychologically unbearable, thereby inuring [people] to it” [1]. Complex psychological underpinnings aside, people were (and still are) afraid of radioactivity. Much of the intrigue and sense of terror regarding radioactivity stem from the fact that the public is largely uninformed on the basic facts relating to environmental radioactivity. For example, there is little appreciation of naturally occurring (i.e., not created by human activities), “background” radioactivity which occurs in soils, seawater, and natural foods. The fear of radioactivity, without regard to radiation dose or type, was most recently made clear in the public response to our 2012 and 2013 reports on the presence of cesium radioisotopes in Pacific bluefin tuna as a result of the Fukushima accident in 2011 [2,3]. In those articles, the combined radioactivity attributable to Cs (entirely from In This Issue:

East not least for Pacific bluefin tuna

More Pacific bluefin migrate across the ocean than previously recognized High market values have incentivized extensive fisheries for Pacific bluefin tuna (Thunnus orientalis, see the photo), a species whose longevity, commercial value, and long generation time make it particularly susceptible to overfishing (1, 2). Today, the population of Pacific bluefin tuna stands at an estimated 2.6% of prefished levels (1). Yet, knowledge of its basic life history is incomplete. Recent studies (3, 4) suggest that the fundamental distribution of Pacific bluefin across the North Pacific has been misunderstood. The results underscore the need for basic movement ecology information to assist science-based fisheries management.

Mercury Stable Isotopes Reveal Influence of Foraging Depth on Mercury Concentrations and Growth in Pacific Bluefin Tuna

Pelagic ecosystems are changing due to environmental and anthropogenic forces, with uncertain consequences for the oceans top predators. Epipelagic and mesopelagic prey resources differ in quality and quantity, but their relative contribution to predator diets has been difficult to track. We measured mercury (Hg) stable isotopes in young (<2 years old) Pacific bluefin tuna (PBFT) and their prey species to explore the influence of foraging depth on growth and methylmercury (MeHg) exposure. PBFT total Hg (THg) in muscle ranged from 0.61 to 1.93 μg g-1 dw (1.31 μg g-1 dw ±0.37 SD; 99% ± 6% MeHg) and prey ranged from 0.01 to 1.76 μg g-1 dw (0.13 μg g-1 dw ±0.19 SD; 85% ± 18% MeHg). A systematic decrease in prey δ202Hg and Δ199Hg with increasing depth of occurrence and discrete isotopic signatures of epipelagic prey (δ202Hg: 0.74 to 1.49‰; Δ199Hg: 1.76-2.96‰) and mesopelagic prey (δ202Hg: 0.09 to 0.90‰; Δ199Hg: 0.62-1.95‰) allowed the use of Hg isotopes to track PBFT foraging depth. An isotopic mixing model was used to estimate the dietary proportion of mesopelagic prey in PBFT, which ranged from 17% to 55%. Increased mesopelagic foraging was significantly correlated with slower growth and higher MeHg concentrations in PBFT. The slower observed growth rates suggest that prey availability and quality could reduce the production of PBFT biomass.