Climate change-informed dietary modeling in Pacific cod: Experimentally-derived effects of temperature and dietary quality on carbon and nitrogen stable isotope trophic discrimination factors.

Stable isotope analysis is a powerful tool for dietary modeling and trophic ecology research. A crucial piece of information for isotopic dietary modeling is the accurate estimation of trophic discrimination factors (TDFs), or the isotopic offset between a consumer's tissue and its diet. In order to parameterize stable isotope dietary models for future climate scenarios, we investigated the effect of water temperature and dietary protein and lipid content on TDFs in juvenile Pacific cod (Gadus macrocephalus). Pacific cod are a commercially and ecologically important species, with stock numbers in the northeast Pacific recently having dropped by more than 70%. We tested four water temperatures (6, 8, 10, and 12°C) and two dietary regimens (low and high lipid content), representing a range of potential ocean temperature and prey quality scenarios, in order to determine carbon and nitrogen TDFs in juvenile Pacific cod. Additionally, we assessed dietary intake and proximate composition of the experimental fish in order to estimate consumption, assimilation, and retention of dietary nutrients. The results of this study suggest that dietary protein catabolism is a primary driver of nitrogen TDF variability in juvenile Pacific cod. Across all temperature treatments from 6 to 12°C, fish reared on the lower quality, lower lipid content diet had higher nitrogen TDFs. The mean TDFs for fish raised on the higher lipid, lower protein diet were +3.40 ‰ for nitrogen (Δ15N) and +0.36 ‰ for lipid-corrected carbon (Δ LC 13C). The mean TDFs for fish raised on the lower lipid, higher protein diet were +4.09 ‰ for nitrogen (Δ15N) and 0.00 ‰ for lipid-corrected carbon (Δ LC 13C). Lipid-corrected carbon isotope data showed that, regardless of temperature, fish consuming the lower lipid diet had essentially no trophic discrimination between diet and bulk tissues. We found no ecologically meaningful differences in TDFs due to water temperature across the 6°experimental range. The results of this experiment demonstrate that dietary quality, and more specifically the use of dietary protein for energetic needs, is a primary driver of trophic discrimination factors. The TDFs determined in this study can be applied to understanding trophic ecology in Pacific cod and closely related species under rapidly changing prey availability and ocean temperature conditions.

Long-Term Ecological Impacts from Oil Spills: Comparison of Exxon Valdez, Hebei Spirit, and Deepwater Horizon.

The long-term ecological impacts of the Exxon Valdez oil spill (EVOS) are compared to two extensively studied and more recent large spills: Deepwater Horizon (DWH) and the Hebei Spirit oil spill (HSOS). Each of the three spills differed in magnitude and duration of oil released, environmental conditions, ecological communities, response and clean up measures, and ecological recovery. The EVOS began on March 24, 1989, and released 40.8 million liters of Alaska North Slope crude oil into the cold, nearly pristine environment of Prince William Sound, Alaska. EVOS oiled wildlife and rocky intertidal shorelines and exposed early life stages of fish to embryotoxic levels of polycyclic aromatic hydrocarbons (PAH). Long-term impacts following EVOS were observed on seabirds, sea otters, killer whales, and subtidal communities. The DWH spill began on April 20, 2010, and released 507 million liters of light Louisiana crude oil from 1600 m on the ocean floor into the Gulf of Mexico over an 87-day period. The DWH spill exposed a diversity of complex aquatic communities in the deep ocean, offshore pelagic areas, and coastal environments to petroleum hydrocarbons. Large-scale persistent ecological effects included impacts to deep ocean corals, failed recruitment of oysters over multiple years, damage to coastal wetlands, and reduced dolphin, sea turtle, and seabird populations. The HSOS began on December 7, 2007, and released approximately 13 million liters of Middle East crude oils into ecologically sensitive areas of the Taean area of western Korea. Environmental conditions and the extensive initial cleanup of HSOS oil stranded on shorelines limited the long-term impacts to changes in composition and abundance of intertidal benthic communities. Comparisons of EVOS, DWH, and HSOS show the importance and complexity of the interactions among the environment, oil spill dynamics, affected ecological systems, and response actions.

Return of warm conditions in the southeastern Bering Sea: Phytoplankton - Fish.

In 2014, the Bering Sea shifted back to warmer ocean temperatures (+2 oC above average), bringing concern for the potential for a new warm stanza and broad biological and ecological cascading effects. In 2015 and 2016 dedicated surveys were executed to study the progression of ocean heating and ecosystem response. We describe ecosystem response to multiple, consecutive years of ocean warming and offer perspective on the broader impacts. Ecosystem changes observed include reduced spring phytoplankton biomass over the southeast Bering Sea shelf relative to the north, lower abundances of large-bodied crustacean zooplankton taxa, and degraded feeding and body condition of age-0 walleye pollock. This suggests poor ecosystem conditions for young pollock production and the risk of significant decline in the number of pollock available to the pollock fishery in 2-3 years. However, we also noted that high quality prey, large copepods and euphausiids, and lower temperatures in the north may have provided a refuge from poor conditions over the southern shelf, potentially buffering the impact of a sequential-year warm stanza on the Bering Sea pollock population. We offer the hypothesis that juvenile (age-0, age-1) pollock may buffer deleterious warm stanza effects by either utilizing high productivity waters associated with the strong, northerly Cold Pool, as a refuge from the warm, low production areas of the southern shelf, or by exploiting alternative prey over the southern shelf. We show that in 2015, the ocean waters influenced by spring sea ice (the Cold Pool) supported robust phytoplankton biomass (spring) comprised of centric diatom chains, a crustacean copepod community comprised of large-bodied taxa (spring, summer), and a large aggregation of midwater fishes, potentially young pollock. In this manner, the Cold Pool may have acted as a trophic refuge in that year. The few age-0 pollock occurring over the southeast shelf consumed high numbers of euphausiids which may have provided a high quality alternate prey. In 2016 a retracted Cold Pool precluded significant refuging in the north, though pollock foraging on available euphausiids over the southern shelf may have mitigated the effect of warm waters and reduced large availability of large copepods. This work presents the hypothesis that, in the short term, juvenile pollock can mitigate the drastic impacts of sustained warming. This short-term buffering, combined with recent observations (2017) of renewed sea ice presence over southeast Bering Sea shelf and a potential return to average or at least cooler ecosystem conditions, suggests that recent warm year stanza (2014-2016) effects to the pollock population and fishery may be mitigated.

Spatial match-mismatch between juvenile fish and prey provides a mechanism for recruitment variability across contrasting climate conditions in the eastern Bering Sea.

Understanding mechanisms behind variability in early life survival of marine fishes through modeling efforts can improve predictive capabilities for recruitment success under changing climate conditions. Walleye pollock (Theragra chalcogramma) support the largest single-species commercial fishery in the United States and represent an ecologically important component of the Bering Sea ecosystem. Variability in walleye pollock growth and survival is structured in part by climate-driven bottom-up control of zooplankton composition. We used two modeling approaches, informed by observations, to understand the roles of prey quality, prey composition, and water temperature on juvenile walleye pollock growth: (1) a bioenergetics model that included local predator and prey energy densities, and (2) an individual-based model that included a mechanistic feeding component dependent on larval development and behavior, local prey densities and size, and physical oceanographic conditions. Prey composition in late-summer shifted from predominantly smaller copepod species in the warmer 2005 season to larger species in the cooler 2010 season, reflecting differences in zooplankton composition between years. In 2010, the main prey of juvenile walleye pollock were more abundant, had greater biomass, and higher mean energy density, resulting in better growth conditions. Moreover, spatial patterns in prey composition and water temperature lead to areas of enhanced growth, or growth 'hot spots', for juvenile walleye pollock and survival may be enhanced when fish overlap with these areas. This study provides evidence that a spatial mismatch between juvenile walleye pollock and growth 'hot spots' in 2005 contributed to poor recruitment while a higher degree of overlap in 2010 resulted in improved recruitment. Our results indicate that climate-driven changes in prey quality and composition can impact growth of juvenile walleye pollock, potentially severely affecting recruitment variability.

Effects of Environmental Temperature on the Dynamics of Ichthyophoniasis in Juvenile Pacific Herring (Clupea pallasii).

The effects of temperature and infection by Ichthyophonus were examined in juvenile Pacific herring (Clupea pallasii) maintained under simulated overwinter fasting conditions. In addition to defining parameters for a herring bioenergetics model (discussed in Vollenweider et al. this issue), these experiments provided new insights into factors influencing the infectivity and virulence of the parasite Ichthyophonus. In groups of fish with established disease, temperature variation had little effect on disease outcome. Ichthyophonus mortality outpaced that resulting from starvation alone. In newly infected fish, temperature variation significantly changed the mortality patterns related to disease. Both elevated and lowered temperatures suppressed disease-related mortality relative to ambient treatments. When parasite exposure dose decreased, an inverse relationship between infection prevalence and temperature was detected. These findings suggest interplay between temperature optima for parasite growth and host immune function and have implications for our understanding of how Ichthyophonus infections are established in wild fish populations.

Energetic Cost of Ichthyophonus Infection in Juvenile Pacific Herring (Clupea pallasii).

The energetic costs of fasting and Ichthyophonus infection were measured in juvenile Pacific herring (Clupea pallasii) in a lab setting at three temperatures. Infected herring incurred significant energetic costs, the magnitude of which depended on fish condition at the time of infection (fat versus lean). Herring that were fed continually and were in relatively good condition at the time of infection (fat) never stored lipid despite ad libitum feeding. In feeding herring, the energetic cost of infection was a 30% reduction in total energy content relative to controls 52 days post infection. Following food deprivation (lean condition), infection caused an initial delay in the compensatory response of herring. Thirty-one days after re-feeding, the energetic cost of infection in previously-fasted fish was a 32% reduction in total energy content relative to controls. Body composition of infected herring subsequently recovered to some degree, though infected herring never attained the same energy content as their continuously fed counterparts. Fifty-two days after re-feeding, the energetic cost of infection in previously-fasted fish was a 6% reduction in total energy content relative to controls. The greatest impacts of infection occurred in colder temperatures, suggesting Ichthyophonus-induced reductions in body condition may have greater consequences in the northern extent of herring's range, where juveniles use most of their energy reserves to survive their first winter.

Seasonal cycles in whole-body proximate composition and energy content of forage fish vary with water depth.

Quantifying the nutritional quality of forage fish is integral for understanding upper trophic levels as forage fish are the dominant prey for top predator fish, marine mammals, and sea birds. Many existing reports documenting body composition of forage species are not comparable due to confounding effects. This study systematically assessed the variability in proximate composition and energy content of 16 forage species in southeastern Alaska (57.2626 N/133.7394 W) between 2001 and 2004. Variation in energy and lipid contents was related to habitat, epipelagic planktivores varying most, mesopelagics intermediate, and demersal species relatively invariable. Season was the greatest source of variation as a result of short growing seasons at high latitude and energy allocation strategies for reproduction and growth. Among species that varied seasonally, energy and lipid increased over summer and declined during winter. Annual differences in body composition occurred during periods of peak energy content. Sampling recommendations and guidance for bioenergetics models are provided.

Chronic exposure to polynuclear aromatic hydrocarbons in natal habitats leads to decreased equilibrium size, growth, and stability of pink salmon populations.

The immediate and delayed effects of embryonic exposure to low levels of polynuclear aromatic hydrocarbons (PAHs) have been shown to reduce survival to maturity by 50% in exposed pink salmon populations. This suggests that chronically exposed populations could be extirpated over relatively few generations, but the effect of density dependence on extirpation rate is unknown. This study examines the interaction of PAH effects and randomly varying density dependence on a simulated population. The simulation derives from 70 years of observations made on a single pink salmon population and toxicity studies involving a hatchery population in the same watershed. Results from simulations involving exposure of 100% of the population to effects consistent with an aqueous PAH concentration of 18 nL/L indicate an 80% decrease in population productivity and an 11% probability of extinction after 35 generations. In contrast, population growth rate declined by only 5%. Further decreases in survival relative to that of observed PAH effects rapidly increase the probability of extinction. Data from these simulations demonstrate that, at low levels of exposure, density dependence can compensate for reduced population size and buffer the population against extinction. However, if equilibrium size is depressed sufficiently, random environmental variation overcomes the buffering effect of density dependence and extinction probability increases. These data demonstrate that extinction probability and population size are more sensitive measures of population effects than growth rate for wild populations regulated by density dependence.

Assessment of the phototoxicity of weathered Alaska North Slope crude oil to juvenile pink salmon.

Petroleum products are known to have greater toxicity to the translucent embryos and larvae of aquatic organisms in the presence of ultraviolet radiation (UV) compared to toxicity determined in tests performed under standard laboratory lighting with minimal UV. This study assessed the acute phototoxicity of the water accommodated fractions of weathered Alaska North Slope crude oil (ANS) to juvenile pink salmon, which are a heavily pigmented life stage. Fish in the highest ANS treatments exhibited melanosis, less mobility, reduced startle response, erratic swimming, and loss of equilibrium. Gills from fish exposed to ANS had elevated levels of hydroperoxides in oil-only, UV-only, and oil+UV treatments compared to control fish, which was indicative of increased lipid peroxidation in gill tissue. Under the test conditions of moderate salinity, low UV and high short-term oil exposure there were no indications of photoenhanced toxicity as assessed by elevation of mortality, behavioral impairment, or gill lipid peroxidation in oil+UV treatments. The results of this study suggest that pink salmon may be at less risk from photoenhanced toxicity compared to the translucent early-life stages of several other Alaska species.

Monitoring polynuclear aromatic hydrocarbons in aqueous environments with passive low-density polyethylene membrane devices.

Low-density polyethylene membranes, typically filled with triolein, have been previously deployed as passive environmental samplers designed to accumulate nonpolar hydrophobic chemicals from water, sediments, and air. Hydrocarbons in such samplers, known as semipermeable membrane devices (SPMDs), diffuse through pores in the membranes and are trapped in the central hydrocarbon matrix, mimicking uptake by living organisms. Here, we describe laboratory and field verification that low-density polyethylene membrane devices (PEMDs) without triolein provide reliable, relatively inexpensive, time-integrated hydrocarbon sampling from water. For comparison, polynuclear aromatic hydrocarbon (PAH) uptake in SPMDs and pink salmon eggs also was studied. Total concentrations of PAH accumulated by PEMDs were highly correlated with concentrations in water (r2 > or = 0.99) and linear over the range tested (0-17 microg/L). Higher-molecular-mass PAH preferentially accumulated in PEMDs and in pink salmon eggs, but the source of oil in PEMDs remained identifiable. Accumulations of PAH were highly similar to those in SPMDs. The PEMDs retained approximately 78% of accumulated total PAH for 40 d in clean water. Thus, a simple plastic membrane can be conveniently used for environmental monitoring, particularly during situations in which contaminant concentrations are low (in the parts-per-billion range), variable, and intermittent.