Divergent trophic responses of sympatric penguin species to historic anthropogenic exploitation and recent climate change.

The Southern Ocean is in an era of significant change. Historic overharvesting of marine mammals and recent climatic warming have cascading impacts on resource availability and, in turn, ecosystem structure and function. We examined trophic responses of sympatric chinstrap (Pygoscelis antarctica) and gentoo (Pygoscelis papua) penguins to nearly 100 y of shared environmental change in the Antarctic Peninsula region using compound-specific stable isotope analyses of museum specimens. A century ago, gentoo penguins fed almost exclusively on low-trophic level prey, such as krill, during the peak of historic overexploitation of marine mammals, which was hypothesized to have resulted in a krill surplus. In the last 40 y, gentoo penguin trophic position has increased a full level as krill declined in response to recent climate change, increased competition from recovering marine mammal populations, and the development of a commercial krill fishery. A shifting isotopic baseline supporting gentoo penguins suggests a concurrent increase in coastal productivity over this time. In contrast, chinstrap penguins exhibited no change in trophic position, despite variation in krill availability over the past century. The specialized foraging niche of chinstrap penguins likely renders them more sensitive to changes in krill availability, relative to gentoo penguins, as evinced by their declining population trends in the Antarctic Peninsula over the past 40 y. Over the next century, similarly divergent trophic and population responses are likely to occur among Antarctic krill predators if climate change and other anthropogenic impacts continue to favor generalist over specialist species.

Two millennia of North Atlantic seasonality and implications for Norse colonies.

delta(18)O values of mollusks recovered from near-shore marine cores in northwest Iceland quantify significant variation in seasonal temperature over the period from approximately 360 B.C. to approximately A.D. 1660. Twenty-six aragonitic bivalve specimens were selected to represent intervals of climatic interest by using core sedimentological characteristics. Carbonate powder was sequentially micromilled from shell surfaces concordant with growth banding and analyzed for stable oxygen (delta(18)O) and carbon (delta(13)C) isotope values. Because delta(18)O values record subseasonal temperature variation over the lifetime of the bivalves, these data provide the first 2,000-year secular record of North Atlantic seasonality from ca. 360 cal yr B.C. to cal yr A.D. 1660. Notable cold periods (360 B.C. to 240 B.C.; A.D. 410; and A.D. 1380 to 1420) and warm periods (230 B.C. to A.D. 140 and A.D. 640 to 760) are resolved in terms of contrast between summer and winter temperatures and seasonal temperature variability. Literature from the Viking Age (ca. 790 to 1070) during the establishment of Norse colonies (and later) in Iceland and Greenland permits comparisons between the delta(18)O temperature record and historical records, thereby demonstrating the impact of seasonal climatic extremes on the establishment, development, and, in some cases, collapse of societies in the North Atlantic.

Wanted: dead or alive? Isotopic analysis (δ13C and δ15N) of Pygoscelis penguin chick tissues supports opportunistic sampling.

RATIONALE: Physiological stress and starvation have been shown to affect δ(13)C and δ(15)N isotope values and, given that animals often die from starvation, the cause of death may be an important factor to consider in stable isotope analyses of opportunistically collected samples. METHODS: We addressed this issue by comparing tissue stable isotope values of living and deceased Adélie (Pygoscelis adeliae) and Chinstrap Penguin (P. antarctica) chicks collected from the same respective populations. RESULTS: No significant difference was found between living and deceased penguin chick feather, down, and toenail isotope values and both groups displayed similar isotopic trends between tissue types. In addition, similar relationships were observed between both species and across several seasons. Furthermore, sub-dermal adiposity and cause of death (starvation and/or predation) had no significant effect on the δ(13)C and δ(15)N values. CONCLUSIONS: Our findings suggest that tissues from deceased penguins can be isotopically representative of tissues obtained from the living population, despite the cause of death, and support the use of opportunistic sampling in stable isotope analyses.

A millennium of trophic stability in Atlantic cod (Gadus morhua): transition to a lower and converging trophic niche in modern times.

Stable isotope analyses of zooarchaeological material can be used to examine ecological variability in exploited species at centennial to millennial scales. Climate change is a notable driver of marine ecosystem change, although historical fishing is also likely to have impacted past marine systems. Fishing removes the oldest and largest individuals and may thereby result in shorter trophic pathways and reduced niche width of predatory fish species. In the current study we examine the trophic niche of Atlantic cod, haddock and Atlantic wolffish, in the last millennium using δ13C and δ15N values of bone collagen. We report a lower trophic level of Atlantic cod and haddock but higher level of wolffish in present times, following centuries at consistent and higher trophic levels of Atlantic cod. This results in a concurrent converging trophic niche of the demersal fish. We suggest that the current data set provides a valuable historical baseline facilitating interpretation of current variability in the trophic ecology of northern demersal fish.

The rise and fall of an ancient Adélie penguin 'supercolony' at Cape Adare, Antarctica.

We report new discoveries and radiocarbon dates on active and abandoned Adélie penguin (Pygoscelis adeliae) colonies at Cape Adare, Antarctica. This colony, first established at approximately 2000 BP (calendar years before present, i.e. 1950), is currently the largest for this species with approximately 338 000 breeding pairs, most located on low-lying Ridley Beach. We hypothesize that this colony first formed after fast ice began blocking open-water access by breeding penguins to the Scott Coast in the southern Ross Sea during a cooling period also at approximately 2000 BP. Our results suggest that the new colony at Cape Adare continued to grow, expanding to a large upper terrace above Ridley Beach, until it exceeded approximately 500 000 breeding pairs (a 'supercolony') by approximately 1200 BP. The high marine productivity associated with the Ross Sea polynya and continental shelf break supported this growth, but the colony collapsed to its present size for unknown reasons after approximately 1200 BP. Ridley Beach will probably be abandoned in the near future due to rising sea level in this region. We predict that penguins will retreat to higher elevations at Cape Adare and that the Scott Coast will be reoccupied by breeding penguins as fast ice continues to dissipate earlier each summer, restoring open-water access to beaches there.

Oxygen and carbon isoscapes for the Baltic Sea: Testing their applicability in fish migration studies.

Conventional tags applied to individuals have been used to investigate animal movement, but these methods require tagged individuals be recaptured. Maps of regional isotopic variability known as "isoscapes" offer potential for various applications in migration research without tagging wherein isotope values of tissues are compared to environmental isotope values. In this study, we present the spatial variability in oxygen (δ18OH2O) and dissolved inorganic carbon (δ13 CDIC) isotope values of Baltic Sea water. We also provide an example of how these isoscapes can reveal locations of individual animal via spatial probability surface maps, using the high-resolution salmon otolith isotope data from salmon during their sea-feeding phase in the Baltic Sea. A clear latitudinal and vertical gradient was found for both δ18OH2O and δ13 CDIC values. The difference between summer and winter in the Baltic Sea δ18OH2O values was only slight, whereas δ13 CDIC values exhibited substantial seasonal variability related to algal productivity. Salmon otolith δ18Ooto and δ13Coto values showed clear differences between feeding areas and seasons. Our example demonstrates that dual isotope approach offers great potential for estimating probable fish habitats once issues in model parameterization have been resolved.

Differing foraging strategies influence mercury (Hg) exposure in an Antarctic penguin community.

Seabirds are ideal model organisms to track mercury (Hg) through marine food webs as they are long-lived, broadly distributed, and are susceptible to biomagnification due to foraging at relatively high trophic levels. However, using these species as biomonitors requires a solid understanding of the degree of species, sexual and age-specific variation in foraging behaviors which act to mediate their dietary exposure to Hg. We combined stomach content analysis along with Hg and stable isotope analyses of blood, feathers and common prey items to help explain inter and intra-specific patterns of dietary Hg exposure across three sympatric Pygoscelis penguin species commonly used as biomonitors of Hg availability in the Antarctic marine ecosystem. We found that penguin tissue Hg concentrations differed across species, between adults and juveniles, but not between sexes. While all three penguins species diets were dominated by Antarctic krill (Euphausia superba) and to a lesser extent fish, stable isotope based proxies of relative trophic level and krill consumption could not by itself sufficiently explain the observed patterns of inter and intra-specific variation in Hg. However, integrating isotopic approaches with stomach content analysis allowed us to identify the relatively higher risk of Hg exposure for penguins foraging on mesopelagic prey relative to congeners targeting epipelagic or benthic prey species. When possible, future seabird biomonitoring studies should seek to combine isotopic approaches with other, independent measures of foraging behavior to better account for the confounding effects of inter and intra-specific variation on dietary Hg exposure.

Chronic mercury exposure in Late Neolithic/Chalcolithic populations in Portugal from the cultural use of cinnabar.

Cinnabar is a natural mercury sulfide (HgS) mineral of volcanic or hydrothermal origin that is found worldwide. It has been mined prehistorically and historically in China, Japan, Europe, and the Americas to extract metallic mercury (Hg(0)) for use in metallurgy, as a medicinal, a preservative, and as a red pigment for body paint and ceramics. Processing cinnabar via combustion releases Hg(0) vapor that can be toxic if inhaled. Mercury from cinnabar can also be absorbed through the gut and skin, where it can accumulate in organs and bone. Here, we report moderate to high levels of total mercury (THg) in human bone from three Late Neolithic/Chalcolithic (5400-4100 B.P.) sites in southern Portugal that were likely caused by cultural use of cinnabar. We use light stable isotope and Hg stable isotope tracking to test three hypotheses on the origin of mercury in this prehistoric human bone. We traced Hg in two individuals to cinnabar deposits near Almadén, Spain, and conclude that use of this mineral likely caused mild to severe mercury poisoning in the prehistoric population. Our methods have applications to bioarchaeological investigations worldwide, and for tracking trade routes and mobility of prehistoric populations where cinnabar use is documented.

Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins.

Stomach content analysis (SCA) and more recently stable isotope analysis (SIA) integrated with isotopic mixing models have become common methods for dietary studies and provide insight into the foraging ecology of seabirds. However, both methods have drawbacks and biases that may result in difficulties in quantifying inter-annual and species-specific differences in diets. We used these two methods to simultaneously quantify the chick-rearing diet of Chinstrap (Pygoscelis antarctica) and Gentoo (P. papua) penguins and highlight methods of integrating SCA data to increase accuracy of diet composition estimates using SIA. SCA biomass estimates were highly variable and underestimated the importance of soft-bodied prey such as fish. Two-source, isotopic mixing model predictions were less variable and identified inter-annual and species-specific differences in the relative amounts of fish and krill in penguin diets not readily apparent using SCA. In contrast, multi-source isotopic mixing models had difficulty estimating the dietary contribution of fish species occupying similar trophic levels without refinement using SCA-derived otolith data. Overall, our ability to track inter-annual and species-specific differences in penguin diets using SIA was enhanced by integrating SCA data to isotopic mixing modes in three ways: 1) selecting appropriate prey sources, 2) weighting combinations of isotopically similar prey in two-source mixing models and 3) refining predicted contributions of isotopically similar prey in multi-source models.

Bioaccumulation of polychlorinated dibenzo-p-dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in fishes from the Tittabawassee and Saginaw Rivers, Michigan, USA.

Characterizing biological factors associated with species-specific accumulation of contaminants is one of the major focuses in ecotoxicology and environmental chemistry studies. In this study, polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and non- and mono-ortho-substituted polychlorinated biphenyl (PCB) congeners were analyzed in various fish species from the Tittabawassee and Saginaw Rivers (12 fish species; n=314 individuals), Michigan, USA. Due to their migratory habits, greater delta(13)C stable isotope values were found in walleye and white sucker among 12 fish species. Meanwhile, the delta(15)N values indicated that the trophic status was least in carp and greatest in largemouth bass. The greatest total concentrations of dioxins were found in fishes with the lowest trophic status (carp (n=50) followed by channel catfish (n=49)), and concentrations of SigmaPCDD/Fs (20-440pg/g ww (wet weight)), SigmaPCBs (16-690ng/g ww), and TEQs (6.8-350pg/g ww) in carp were also greater than the least mean concentrations in other fishes. Contributions of various biological factors to the species accumulation were assessed. Body weight and lipid content were found to be the most significant factors influencing accumulation of SigmaPCDD/Fs. Lipid content and trophic level seemed to be dominant factors determining accumulation of SigmaPCB and TEQs, but negative correlations between trophic status and concentrations of SigmaPCBs and TEQs were observed possibly due to the great concentrations in benthivorous fishes such as carp occupying lower trophic levels. These factors can be used to predict the contaminant levels of dioxins and health risks of the fishes in the river ecosystem.

Abrupt recent shift in delta 13C and delta 15N values in Adélie penguin eggshell in Antarctica.

Stable isotope values of carbon (delta13C) and nitrogen (delta15N) in blood, feathers, eggshell, and bone have been used in seabird studies since the 1980s, providing a valuable source of information on diet, foraging patterns, and migratory behavior in these birds. These techniques can also be applied to fossil material when preservation of bone and other tissues is sufficient. Excavations of abandoned Adélie penguin (Pygoscelis adeliae) colonies in Antarctica often provide well preserved remains of bone, feathers, and eggshell dating from hundreds to thousands of years B.P. Herein we present an approximately 38,000-year time series of delta13C and delta15N values of Adélie penguin eggshell from abandoned colonies located in three major regions of Antarctica. Results indicate an abrupt shift to lower-trophic prey in penguin diets within the past approximately 200 years. We posit that penguins only recently began to rely on krill as a major portion of their diet, in conjunction with the removal of baleen whales and krill-eating seals during the historic whaling era. Our results support the "krill surplus" hypothesis that predicts excess krill availability in the Southern Ocean after this period of exploitation.