Sara J. Iverson

QUANTITATIVE FATTY ACID SIGNATURE ANALYSIS: A NEW METHOD OF ESTIMATING PREDATOR DIETS

Accurate estimates of the diets of predators are required in many areas of ecology, but for many species current methods are imprecise, limited to the last meal, and often biased. The diversity of fatty acids and their patterns in organisms, coupled with the narrow limitations on their biosynthesis, properties of digestion in monogastric animals, and the prevalence of large storage reservoirs of lipid in many predators, led us to propose the use of quantitative fatty acid signature analysis (QFASA) to study predator diets. We present a statistical model that provides quantitative estimates of the proportions of prey species in the diets of individual predators using fatty acid signatures. We conducted simulation studies using a database of 28 prey species (n = 954 individuals) from the Scotian Shelf off eastern Canada to investigate properties of the model and to evaluate the reliability with which prey could be distinguished in the model. We then conducted experiments on grey seals (Halichoerus grypus, n = 25) and harp seals (Phoca groenlandica, n = 5) to assess quantitative characteristics of fatty acid deposition and to develop calibration coefficients for individual fatty acids to account for predator lipid metabolism. We then tested the model and calibration coefficients by estimating the diets of experimentally fed captive grey seals (n = 6, switched from herring to a mackerel/capelin diet) and mink kits (Mustela vison, n = 46, switched from milk to one of three oil-supplemented diets). The diets of all experimentally fed animals were generally well estimated using QFASA and were consistent with qualitative and quantitative expectations, provided that appropriate calibration coefficients were used. In a final case, we compared video data of foraging by individual free- ranging harbor seals (Phoca vitulina, n = 23) fitted with Crittercams and QFASA estimates of the diet of those same seals using a complex ecosystem-wide prey database. Among the 28 prey species in the database, QFASA estimated sandlance to be the dominant prey species in the diet of all seals (averaging 62% of diet), followed primarily by flounders, but also capelin and minor amounts of other species, although there was also considerable individual variability among seals. These estimates were consistent with video data showing sandlance to be the predominant prey, followed by flatfish. We conclude that QFASA provides estimates of diets for individuals at time scales that are relevant to the ecological processes affecting survival, and can be used to study diet variability within individuals over time, which will provide important opportunities rarely possible with other indirect methods. We propose that the QFASA model we have set forth will be applicable to a wide range of predators and ecosystems.

Comparison of the bligh and dyer and folch methods for total lipid determination in a broad range of marine tissue

For many studies, it is important to measure the total lipid content of biological samples accurately. The Bligh and Dyer method of extraction was developed as a rapid but effective method for determining total lipid content in fish muscle. However, it is also widely used in studies measuring total lipid content of whole fish and other tissues. Although some investigators may have used modified Bligh and Dyer procedures, rarely have modifications been specified nor has their effectiveness been quantitatively evaluated. Thus, we compared this method with that of the classic. Folch extraction in determining total lipid content of fish samples ranging from 0.5 to 26.6% lipid. We performed both methods as originally specified, i.e., using the chloroform/methanol/water ratios of 1∶2∶0.8 and 2∶2∶1.8 (before and after dilution, respectively) for Bligh and Dyer and of 8∶4∶3 for Folch, and with the initial solvent/sample ratios of (3+1)∶1 (Bligh and Dyer) and 20∶1 (Folch). We also compared these with several other solvent/sample ratios. In samples containing <2% lipid, the results of the two methods did not differ. However, for samples containing <2% lipid, the Bligh and Dyer method produced significantly lower estimates of lipid content, and this underestimation increased significantly with increasing lipid content of the sample. In the highest lipid samples, lipid content was underestimated by up to 50% using the Bligh and Dyer method. However, we found a highly significant linear relationship between the two methods, which will permit the correction of reported lipid levels in samples previously analyzed using an unmodified Bligh and Dyer extraction. In the future, modifications to procedures and solvent/sample ratios should be described.

Aquatic animal telemetry: A panoramic window into the underwater world

A brave new world with a wider view Researchers have long attempted to follow animals as they move through their environment. Until relatively recently, however, such efforts were limited to short distances and times in species large enough to carry large batteries and transmitters. New technologies have opened up new frontiers in animal tracking remote data collection. Hussey et al. review the unique directions such efforts have taken for marine systems, while Kays et al. review recent advances for terrestrial species. We have entered a new era of animal ecology, where animals act as both subjects and samplers of their environments. Science, this issue 10.1126/science.1255642, 10.1126/science.aaa2478 BACKGROUND Global aquatic environments are changing profoundly as a result of human actions; consequently, so too are the ways in which organisms are distributing themselves through space and time. Our ability to predict organism and community responses to these alterations will be dependent on knowledge of animal movements, interactions, and how the physiological and environmental processes underlying them shape species distributions. These patterns and processes ultimately structure aquatic ecosystems and provide the wealth of ecosystem services upon which humans depend. Until recently, the vast size, opacity, and dynamic nature of the aquatic realm have impeded our efforts to understand these ecosystems. With rapid technological advancement over the past several decades, a suite of electronic tracking devices (e.g., acoustic and satellite transmitters) that can remotely monitor animals in these challenging environments are now available. Aquatic telemetry technology is rapidly accelerating our ability to observe animal behavior and distribution and, as a consequence, is fundamentally altering our understanding of the structure and function of global aquatic ecosystems. These advances provide the toolbox to define how future global aquatic management practices must evolve. ADVANCES Aquatic telemetry has emerged through technological advances in miniaturization, battery engineering, and software and hardware development, allowing the monitoring of organisms whose habitats range from the poles to the tropics and the photic zone to the abyssal depths. This is enabling the characterization of the horizontal and vertical movements of individuals, populations, and entire communities over scales of meters to tens of thousands of kilometers and over time frames of hours to years and even over the entire lifetimes of individuals. Electronic tags can now be equipped with sensors that measure ambient physical parameters (depth, temperature, conductivity, fluorescence), providing simultaneous monitoring of animals’ environments. By linking telemetry with biologgers (e.g., jaw-motion sensors), it is possible to monitor individual feeding events. In addition, other devices on instrumented animals can communicate with one another, providing insights into predator-prey interactions and social behavior. Coupling telemetry with minute nonlethal biopsy allows understanding of how trophic dynamics, population connectivity, and gene-level basis for organismal health and condition relate to movement. These advances are revolutionizing the scope and scales of questions that can be addressed on the causes and consequences of animal distribution and movement. OUTLOOK Aquatic animal telemetry has advanced rapidly, yet new challenges present themselves in coordination of monitoring across large-spatial scales (ocean basins), data sharing, and data assimilation. The continued advancement of aquatic telemetry lies in establishing and maintaining accessible and cost-effective infrastructure and in promoting multidisciplinary tagging approaches to maximize cost benefits. A united global network and centralized database will provide the mechanism for global telemetry data and will promote a transparent environment for data sharing that will, in turn, increase global communication, scope for collaboration, intellectual advancement, and funding opportunities. An overarching global network will realize the potential of telemetry, which is essential for advancing scientific knowledge and effectively managing globally shared aquatic resources and their ecosystems in the face of mounting human pressures and environmental change. Aquatic telemetry in action. A southern rock lobster (Jasus edwardsii) (A) and a lemon shark (Negaprion brevirostris) (D) fitted with acoustic tags are detected and logged by moored receivers (D) or mobile receivers attached to opportunistic platforms or carried by large animals (C). A juvenile green turtle (Chelonia mydas) (B) fitted with a satellite tag is monitored in real time via orbiting satellites. A grey seal (Halichoerus grypus) “bioprobe” (C), fitted with intercommunicating acoustic and satellite transmitters, transmits and receives data on animal interactions and ocean conditions. The distribution and interactions of aquatic organisms across space and time structure our marine, freshwater, and estuarine ecosystems. Over the past decade, technological advances in telemetry have transformed our ability to observe aquatic animal behavior and movement. These advances are now providing unprecedented ecological insights by connecting animal movements with measures of their physiology and environment. These developments are revolutionizing the scope and scale of questions that can be asked about the causes and consequences of movement and are redefining how we view and manage individuals, populations, and entire ecosystems. The next advance in aquatic telemetry will be the development of a global collaborative effort to facilitate infrastructure and data sharing and management over scales not previously possible.

POLAR BEAR DIETS AND ARCTIC MARINE FOOD WEBS: INSIGHTS FROM FATTY ACID ANALYSIS

We used quantitative fatty acid signature analysis (QFASA) to examine the diets of 1738 individual polar bears (Ursus maritimus) sampled across the Canadian Arctic over a 30-year span. Polar bear foraging varied over large and small spatial and temporal scales, and between demographic groups. Diets in every subpopulation were dominated by ringed seals (Phoca hispida) and, in the eastern Arctic, secondarily by harp seals (Pagophilus groenlandica). Beluga whales (Delphinapterus leucas) were an important food source for bears in the High Arctic, which is consistent with previous anecdotal reports. Foraging patterns were most similar among neighboring subpopulations with similar prey assemblages, but also differed geographically within Western Hudson Bay. The sexual size dimorphism of polar bears had an important effect on foraging, as large bearded seals (Erignathus barbatus) and walruses (Odobenus rosmarus) were consumed most often by older, male bears, whereas ringed seals and, where available, harbor seals (P. vitulina) were most important to younger age classes. Larger, older bears also had the greatest dietary diversity, apparently because of their ability to include larger-bodied prey. During spring and summer, polar bears in some areas increased predation on migratory harp seals and beluga whales. In Western Hudson Bay, bearded seal consumption declined between 1995 and 2001 for both male and female bears and continued to decline among females up to the most recent sampling (2004). Ringed seal consumption in Western Hudson Bay increased between 1998 and 2001, perhaps in response to increased ringed seal productivity, but was not significantly affected by date of sea-ice breakup. Overall, our data indicate that polar bears are capable of opportunistically altering their foraging to take advantage of locally abundant prey, or to some degree compensating for a decline in a dominant prey species. However, in other areas polar bears are dependent on the availability of ringed and bearded seals. Recent population data suggest that polar bears with the most specialized diets may be most vulnerable to climate-related changes in ice conditions. The results of this large-scale, ecosystem-based study indicate a complex relationship between sea-ice conditions, prey population dynamics, and polar bear foraging.

Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination

Food web structure, predator–prey dynamics, foraging behavior, and consequences of these factors for individual growth, reproduction and survival are central to our understanding of ecosystem structure and functioning. Moreover, in the current context of understanding (and managing) ecosystems in the face of ongoing environmental change, important questions include: What are the critical prey of key consumers in relation to prey abundance, availability, and nutritional quality? What are the ecosystem processes responsible for food web production? And, how do these processes respond to changes in physical forcing? A fundamental require-ment to understand any of these areas is an accurate assessment of trophic relationships and consumer diets. However, in aquatic, and especially marine ecosystems, such information is generally not easily or reliably obtained. In these systems, the relative inaccessibility of free-ranging organisms and the inability to directly observe species interactions make it difficult to accurately characterize diet. Traditional approaches, such as examining gut contents, have well-recognized biases in addition to representing only snapshots of recent meals and may therefore not be reliable indicators of long-term diet (Iverson et al. 2004). Thus, alternative approaches have been developed, which use various types of trophic markers. One of the most promising of these approaches is the use of lipids and fatty acids (FA) to study food web dynamics.

The Effect of Maternal Size and Milk Energy Output on Pup Growth in Grey Seals (Halichoerus grypus)

In phocid species in which females fast throughout lactation, maternal energy reserves at parturition must support lactation. Thus, differences in body size and energy stores may influence the magnitude of maternal energy transfer. We examined variation in milk energy transfer and its consequence for pup growth in grey seals over a wide range of maternal body sizes. Milk samples (n = 42) were collected from 28 females over the 16-d lactation period. Milk yields were measured in nine mother-pup pairs by deuterium oxide dilution. Milk fat and energy content increased dramatically over the first half of lactation. At mid-to late lactation milk composition averaged 71.1% dry matter, 59.8% fat, 9.2% protein, and 24.8 kJ/g (bomb calorimetry). Initial maternal mass (149-256 kg) and daily mass loss (3-9 kg/d) were correlated with daily milk output (1.3-4.1 kg/d). Milk energy output (29-92 MJ/d) in turn explained pup mass gain (0.8-2.8 kg/d, r² = 0.997). Pups with greater energy intakes had a greater ratio of fat to protein deposition and thus a greater efficiency of energy storage, increasing from 40% to 79%. Daily milk intake did not change over lactation, but growth rate was greater during the second half of lactation because milk energy intake was greater. Results of this study indicate that large females lose mass more rapidly, produce more milk, and wean larger, fatter pups than do small females. We conclude that differences in maternal mass and available energy stores may have substantial consequences for the pup and may account for much of the reported variation in pup growth both within and between populations of phocids such as the grey seal.

Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena)

Fatty acid composition of blubber was determined at four body sites of 19 male harbour porpoises. A total of 65 fatty acids were quantified in each sample. The array of fatty acids contained in harbour porpoise blubber was similar to those found in other marine mammals. While chemical composition of total blubber was uniform over the body, with the exception of the caudal peduncle, vertical stratification was evident between the deep (inner) and superficial (outer) blubber layers. Fatty acids with chain lengths shorter than 18 carbons were present in significantly greater amounts in the outer blubber layer, while the longer-chain unsaturated fatty acids were more prevalent in the inner layer. This distribution suggests that the inner blubber layer is more active metabolically than the outer layer in terms of lipid deposition and mobilization. The degree of stratification between the two layers appears to increase with age, indicating a predictable turnover in the blubber layer of male porpoises. Harbour porpoise blubber contained high levels (2–27%) of isovaleric acid in the outer blubber layer, and these levels were positively correlated with age.

Variation in Milk Production and Lactation Performance in Grey Seals and Consequences for Pup Growth and Weaning Characteristics

Phocid seals are one of the few groups of mammals capable of sustaining the energetic demands of lactation entirely through body nutrient stores while fasting. Lactation performance of the female in turn influences the rate and pattern of pup growth. We examined variation in and patterns of milk composition and production, maternal energy output, and pup growth and energy deposition over the entire lactation period in 18 grey seal mother‐pup pairs using hydrogen isotope (3H2O and D2O) dilution. Milk composition was independent of maternal mass and nutrient stores, indicating dependence on other physiological and genetic factors. Heavier females lactated longer ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape

LINKING MOVEMENT, DIVING, AND HABITAT TO FORAGING SUCCESS IN A LARGE MARINE PREDATOR

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