Steller sea lion research > Nutritional Stress >Assessing Prey Quality

Assessing Prey Quality

All animals have individual energy and nutritional requirements that they must obtain from their food. Scientists are studying the potential effect of diet changes on Steller sea lions by measuring the nutrition and energy content of various prey items.

Nutrition and Energy Content
Scientists know that the energy contained in various fish species can differ tremendously. The proximate composition of these potential prey items can be analyzed as a first step in determining the energy that Steller sea lions obtain from different diets.

However, not all of the chemical energy (gross energy) contained in a fish is biologically available to a sea lion. A certain amount of energy is lost during the course of digestion. Consortium researchers have measured the energy lost through two major digestive processes - the heat increment of feeding and fecal energy loss. By quantifying the amount of energy lost from meals of different composition and sizes, scientists can more accurately calculate the amount of fish needed to satisfy the energy requirements of Steller sea lions.

Heat Increment of Feeding
The heat increment of feeding (HIF) is the increase in energy expended by an animal due to the work involved in breaking down, digesting, and assimilating food. Consortium scientists have measured the energy lost via HIF by feeding captive sea lions meals of different prey and size and measuring the increase in oxygen consumed (energy expended) over the following 10-16 hours.

The results of these experiments demonstrate that proportionately more energy is lost from a meal of low energy prey (e.g., Walleye pollock, squid) than from high energy prey items (e.g., herring). Additionally, proportionately more energy is lost from larger meals than smaller ones.

Digestive Efficiency and Dry-matter Digestibility
Although the digestive system of Steller sea lions is very efficient, some energy from food is lost in their feces. Scientists use a measurement known as 'digestive efficiency' to measure how little energy is lost in the feces - the less energy lost, the higher the digestive efficiency.

Consortium scientists have measured the digestive efficiency of captive Steller sea lions while they are consuming different potential prey items at different meal frequencies. In general, the sea lions have the lowest digestive efficiency with prey items that contain the least energy. In other words, proportionally more of the energy in a meal is lost in the feces from prey species such as squid, and less is lost from prey such as herring.

In the past, scientists have used the amount of material that passes through a sea lion to estimate the amount of energy lost in feces. This measure of dry-matter digestibility (also sometimes called assimilation efficiency) has also been measured by Consortium scientists with captive Steller sea lions. The results indicate that, although dry-matter digestibility is loosely related to digestive efficiency, the amount of material that passes through a sea lion's intestinal tract is more closely related to how boney the fish is than how much energy is lost in the digestive process. Therefore, the two measurements should not be used interchangeably.

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Proportion of prey consumed can be determined from faecal DNA using real-time PCR. Bowles, E., P.M. Schulte, D.J. Tollit, B.E. Deagle and A.W. Trites. 2011. Molecular Ecology Resources 11:530-540. abstract Reconstructing the diets of pinnipeds by visually identifying prey remains recovered in faecal samples is challenging because of differences in digestion and passage rates of hard parts. Analyzing the soft-matrix of faecal material using DNA-based techniques is an alternative means to identify prey species consumed, but published techniques are largely non-quantitative, which limits their usefulness for some studies. We further developed and validated a real-time PCR technique using species-specific mitochondrial DNA primers to quantify the proportion of prey in the diets of Steller sea lions (Eumetopias jubatus), a pinniped species thought to be facing significant diet related challenges in the North Pacific. We first demonstrated that the proportions of prey tissue DNA in mixtures of DNA isolated from four prey species could be estimated within a margin of ~12% of the percent in the mix. These prey species included herring Clupea palasii, eulachon Thaleichthyes pacificus, squid Loligo opalescens and rosethorn rockfish Sebastes helvomaculatus. We then applied real-time PCR to DNA extracted from faecal samples obtained from Steller sea lions in captivity that were fed 11 different combinations of herring, eulachon, squid and Pacific ocean perch rockfish (Sebastes alutus), ranging from 7-75% contributions per meal (by wet weight). The difference between the average percentage estimated by real-time PCR and the percentage of prey consumed was generally less than 12% for all diets fed. Our findings indicate that real-time PCR of faecal DNA can detect the approximate relative quantity of prey consumed for complex diets and prey species, including cephalopods and fish.
Environment and feeding change the ability of heart rate to predict metabolism in resting Steller sea lions (Eumetopias jubatus). Young, B. L., D.A.S. Rosen, M. Haulena, A. G. Hindle and A.W. Trites. 2011. Journal of Comparative Physiology-B 118:105-116. abstract The ability to use heart rate (fh) to predict oxygen consumption rates (VO2) in Steller sea lions and other pinnipeds has been investigated in fasting animals. However, it is unknown whether established fh:VO2 relationships hold under more complex physiological situations, such as when animals are feeding or digesting. We assessed whether fh could accurately predict VO2 in trained Steller sea lions while fasting and after being fed. Using linear mixed-effects models, we derived unique equations to describe the fh:VO2 relationship for fasted sea lions resting on land and in water. Feeding did not significantly change the fh:VO2 relationship on land. However, Steller sea lions in water displayed a different fh:VO2 relationship after consuming a 4 kg meal compared to the fasting condition. Incorporating comparable published fh:VO2 data from Steller sea lions showed a distinct effect of feeding after a 6 kg meal. Ultimately, our study illustrated that both feeding and physical environment are statistically relevant when deriving VO2 from telemetered fh, but that only environment affects the practical ability to predict metabolism from fh. Updating current bioenergetic models with data gathered using these predictive fh:VO2 equations will yield more accurate estimates of metabolic rates of free-ranging Steller sea lions under a variety of physiological, behavioral, and environmental states.
Seasonal oscillations in the mass and food intake of Steller sea lions. Allen, P.C. 2009. MSc thesis, University of British Columbia, Vancouver. 154 pages abstract Morphometric measurements and daily feeding records of 62 captive Steller sea lions (Eumetopias jubatus) were analyzed to provide information about seasonal growth and food consumption that has been impossible to collect from wild animals. Data from nursing pups, intact and castrated males, pregnant, lactating and non-reproductive females were also used to determine differences in rates of maturity between males and females, and the effects that climate, sexual maturity, castration and pregnancy and lactation have on growth and food intake. Data were fit with seasonal (sine function) and annual (von Bertalanffy, logistic, Gompertz, Richard’s and maturity) growth models, and showed that males achieved larger body sizes than females by undergoing a growth spurt during puberty and by extending their growth throughout adulthood. Annual increases in the length and mass of females slowed significantly following sexual maturity. Males and females both experienced seasonal oscillations in body mass, but the seasonal fluctuation in male mass peaked later (April) and was far more dramatic than that of females. The mass of lactating and non-reproductive females peaked in early spring (March), while increases in the mass of pregnant females paralleled fetal growth, reaching a maximum before parturition. Changes in mass did not parallel changes in consumption. Fish intake by males and females peaked during winter and bottomed during late spring, while seasonal changes in body mass reached their high and low 3 to 4 months later than food intake. Pregnant and non-reproductive females differed little in the amount of prey they consumed, unlike lactating females that significantly increased their consumption during summer and winter. The differences between females highlight the relatively low additional energetic requirements of pregnancy and the high costs of lactation. Differences between neutered and intact males further suggest that testosterone affected overall male growth, but had smaller effects of seasonal oscillations in mass and did not affect food intake. The reproductive cycle and thermoregulatory requirements appeared to drive seasonal changes in body mass and food intake of male and female Steller sea lions but at different time scales. Our findings also indicate that mass is not a simple reflection of food intake, which has important implications for future nutritional research and bioenergetic modeling of wild pinnipeds.
Determining the relative amounts of prey in Steller sea lion (Eumetopias jubatus) diet using real-time PCR. Bowles, E. 2009. In Zoology. MSc thesis, University of British Columbia, Vancouver. 54 pages abstract Determining diets of pinnipeds by visually identifying prey remains recovered in faecal samples is challenging because of differences in digestion and passage rates of hard parts. Analyzing the soft matrix of fecal material using DNA-based techniques is an alternative means to identify prey species consumed, but published techniques are largely non-quantitative, which limits their applicability. I developed and validated a real-time PCR technique using species-specific mitochondrial DNA primers to quantify the diets of Steller sea lions (Eumetopias jubatus). I first demonstrated that the proportions of prey tissue DNA in mixtures of DNA isolated from four prey species could be estimated within a margin of ~12% of the percent in the mix. These prey species included herring Clupea palasii, eulachon Thaleichthyes pacificus, squid Loligo opalescens and rosethorn rockfish Sebastes helvomaculatus. I then applied real-time PCR to DNA extracted from faecal samples obtained from Steller sea lions that had been fed 11 different combinations of herring, eulachon, squid and Pacific ocean perch rockfish (Sebastes alutus), ranging from 7-75% contributions to a meal mix (by wet weight). The difference between the average percentage estimated by real-time PCR and the percentage of prey consumed was generally less than 12% for all diets fed when percentages of prey consumed were corrected for differences in mtDNA density among the prey items. My findings indicate that real-time PCR can detect the quantity of prey consumed for a variety of complex diets and prey species, including cephalopods and fish.
Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus). Jeanniard du Dot T., Rosen D.A., Richmond, J.P., Kitaysky A.S., Zinn, S.A. and Trites A.W. 2009. Comparative Biochemistry and Physiology, Part A 152:524-534. abstract Physiological responses to changes in energy balance are tightly regulated by the endocrine system through glucocorticoids, IGF-I and thyroid hormones. Changes in these hormones were studied in eight captive female Steller sea lions that experienced changes in food intake, body mass, body composition, and blood metabolites during summer and winter. During a period of energy restriction, one group of sea lions was fed reduced amounts of Pacific herring and another was fed an isocaloric diet of walleye pollock, after which both groups returned to their pre-experimental diets of herring. Cortisol was negatively and IGF-I was positively associated with changes in body mass during periods of energy restriction (mass loss associated with increase in cortisol and decrease in IGF-I) and refeeding (body mass maintenance associated with stable hormone concentrations in summer and compensatory growth linked to decrease in cortisol and increase in IGF-I in winter). Cortisol and IGF-I were also correlated with changes in lipid and lean mass, respectively. Consequently, these two hormones likely make adequate biomarkers for nutritional stress in sea lions, and when combined provide indication of the energetic strategy (lipid vs lean mass catabolism) animals adopt to cope with changes in nutrient intake. Unlike type of diet fed to the sea lions, age of the animals also impacted hormonal responses, with younger animals showing more intense hormonal changes to nutritional stress. Thyroid hormones, however, were not linked to any physiological changes observed in this study.
Fecal triiodothyronine assay validation using captive Steller sea lions (Eumetopias jubatus) and subsequent application to free-ranging populations to examine nutritional stress. Keech, A.L. 2009. In Zoology. MSc Thesis, University of British Columbia, Vancouver. 97 pages abstract Reduced availability of high energy-content prey (nutritional stress) is a predominant hypothesis to explain the decline of Steller sea lion (Eumetopias jubatus) populations in western Alaska from the late 1970's to the late 1990's. Animals may respond to eating insufficient prey by increasing stress levels and decreasing metabolic rates. It may thus be possible to identify nutritional stress by measuring concentrations of GC metabolites (stress) and thyroid hormones (metabolism) shed in the feces of Steller sea lions. However, techniques to measure thyroid hormone concentrations from sea lion feces have not been developed. We quantified variation of triiodothyronine (T3) and thyroxine (T4) concentrations in Steller sea lion feces following two injections of thyrotropin (TSH) at 24 h intervals into four captive animals. Glucocorticoid (GC) metabolites were also assayed to examine any relationship to stimulated thyroid hormone secretion. We found that fecal T3 peaked 48 h post-injection and increased 25-57% in three sea lions (all animals, p=0.03). Pre-injection GC increases indicated stress from isolation for baseline fecal collections, but post-injection increases could not be confirmed as a response to TSH injections or as a product of the study design. The results demonstrated that pre- and post-injection changes in fecal GC and T3 concentrations were consistent with predictions of an increased stress response and metabolic rate within the animals. We then measured T3 and GC concentrations in 834 Steller sea lion fecal samples collected in 2005 and 2006 from 15 resting (haulout) and breeding (rookery) sites between British Columbia and the Central Aleutian Islands. Overall, GC concentrations did not differ between haulout populations (western 2006 pre-pupping and eastern 2005 post-pupping). Fecal hard-part analyses revealed a lower energy-content diet in the western population, suggesting that diet quality is a relevant hypothesis to explain slightly higher GC concentrations found in the western population, specifically the Aleutian Islands region. However, the nutritional stress hypothesis could not be substantiated through T3 concentrations. The rookeries possessed the highest energy-content diets, but also exhibited a nutritional stress response with a significantly higher GC and lower T3 concentration than either haulout population (possibly related to lactation or decreased leptin levels), but T3 comparisons performed at scales of site and region were inconclusive.
Steller sea lions Eumetopias jubatus and nutritional stress: evidence from captive studies. Rosen, D.A.S. 2009. Mammal Review 39:284-306. abstract 1. Numbers of Steller sea lions Eumetopias jubatus in the North Pacific have declined. According to the Nutritional Stress Hypothesis, this decline is due to reduced food availability. Data from studies conducted on pinnipeds in the laboratory are used here to test whether the Nutritional Stress Hypothesis can explain the decline of Steller sea lions. 2. Overall, there is strong evidence for biologically meaningful differences in the nutritional quality of major prey species. Steller sea lions can partly compensate for low-quality prey by increasing their food consumption. 3. There appear to be no detrimental effects of low-lipid prey on sea lion growth or body composition when sea lions can consume sufficient quantities of prey. However, the ability to increase consumption is physiologically limited, particularly in young animals. Overall, it is more difficult to maintain energy intake on a diet of low-quality prey than on a normal diet. 4. Under conditions of inadequate food intake (either due to decreased prey availability or quality, or increased energy requirements) the overall impacts of nutritional stress are complex, and are dependent upon season, prey quality, age, and the duration and intensity of the nutritional stress event. 5. Studies on pinnipeds in the laboratory have been instrumental in identifying the conditions under which changes in sea lion prey can result in nutritional stress, and the nature of the physiological impacts of nutritional stress events.
Steller sea lion foraging response to seasonal changes in prey availability. Sigler, M.F., D.J. Tollit, J.J. Vollenweider, J.F. Thedinga, D.J. Csepp, J.N. Womble, M.A. Wong, M.J. Rehberg and A.W. Trites. 2009. Marine Ecology Progress Series 388:243-261. abstract We hypothesized that: (1) Steller sea lion Eumetopias jubatus diet choice is a function of prey availability, (2) sea lions move to take advantage of times and locations of seasonal prey concentrations and (3) the number present depends on the amount of prey available (numerical response). Over 3 yr, typically on a quarterly basis, in Frederick Sound, SE Alaska, multiple measurements were taken of Steller sea lion abundance (aerial surveys), diet (scats), dive behavior (satellite telemetry)and prey availability and caloric density (nearshore, pelagic and demersal fish surveys). We found that Steller sea lions shifted diet composition in response to changes in prey availability of pollock Theragra chalcogramma, hake Merluccius productus, herring Clupea pallasi and salmon Oncorhynchus spp. They selected intermediate-sized fish and avoided small (<10 cm) and large (>60 cm) fish, and moved between areas as prey became available seasonally. The number of sea lions present depended on the amount of prey available; a standing biomass of 500 to 1700 t of prey in a nonbreeding area such as Frederick Sound, depending on species composition, can attract and sustain about 500 sea lions. Pollock was more frequent in sea lion diet in inside waters of SE Alaska including Frederick Sound, Stephens Passage and Lynn Canal than anywhere else in Alaska and contributed about one-third of the dietary energy in Frederick Sound. This finding implies that a diet with substantial year-round contributions from less nutritious, but abundant prey such as pollock can form part of a healthy diet as long as more nutritious prey such as herring, salmon or eulachon Thaleichthys pacificus also are consumed. Our study supports the conclusion that the Steller sea lion is an opportunistic marine predator with a flexible foraging strategy that selects abundant, accessible prey and shifts among seasonally available species.
Development and application of DNA techniques for validating and improving pinniped diet estimates. Tollit, D. J., A. D. Schulze, A. W. Trites, P. F. Olesiuk, S. J. Crockford, T. S. Gelatt, R. R. Ream, K. M. Miller. 2009. Ecological Applications 19:889-905. abstract Polymerase chain reaction techniques were developed and applied to identify DNA from >40 species of prey contained in fecal (scat) soft part matrix collected at terrestrial sites used by Steller sea lions (Eumetopias jubatus) in British Columbia and the Eastern Aleutian Islands, Alaska. Sixty percent more fish and cephalopod prey were identified by morphological analyses of hard parts compared with DNA analysis of soft parts (hard parts identified higher relative proportions of Ammodytes sp., Cottidae and certain Gadidae). DNA identified 213 prey occurrences of which 75 (35%) were undetected by hard parts (mainly Salmonidae, Pleuronectidae, Elasmobranchii and Cephalopoda), and thereby increased species occurrences by 22% overall and species richness in 44% of cases (when comparing 110 scats that amplified prey DNA). Prey composition was identical within only 20% of scats. Overall, diet composition derived from both identification techniques combined did not differ significantly from hard part identification alone, suggesting that past scat-based diet studies have not missed major dietary components. However, significant differences in relative diet contributions across scats (as identified using the two techniques separately) reflect passage rate differences between hard and soft digesta material and highlight certain hypothesized limitations in conventional morphological-based methods (e.g., differences in resistance to digestion, hard part regurgitation, partial and secondary prey consumption), as well as potential technical issues (e.g., resolution of primer efficiency and sensitivity, and scat subsampling protocols). DNA analysis of salmon occurrence (from scat soft part matrix and 238 archived salmon hard parts) provided species-level taxonomic resolution that could not be obtained by morphological identification, and showed that Steller sea lions were primarily consuming pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon. Notably, DNA from Atlantic salmon (Salmo salar) that likely originated from a distant fish farm was also detected in two scats from one site in the Eastern Aleutian Islands. Overall, molecular techniques are valuable for identifying prey in the fecal remains of marine predators. Combining DNA and hard part identification will effectively alleviate certain predicted biases, and will ultimately enhance measures of diet richness, fisheries interactions (especially salmon related ones) and the ecological role of pinnipeds and other marine predators, to the benefit of marine wildlife conservationist and fisheries managers.
Steller sea lions show diet-dependent changes in body composition during nutritional stress and recover more easily from mass loss in winter than in summer. Jeanniard du Dot, T., Rosen, D. A. S. , Trites, A. W. 2008. Journal of Experimental Marine Biology and Ecology 367(1):1-10. abstract Controlled feeding experiments were undertaken with captive Steller sea lions (Eumetopias jubatus) to assess seasonal (winter vs. summer) physiological responses of individual animals to reduced quantities and qualities of food that are hypothesised to occur in the wild. Eight animals were randomly divided into two experimental groups fed isocaloric diets: Group H ate Pacific herring (Clupea pallasi) throughout the experiment while Group P was switched to walleye pollock (Theragra chalcogramma) during a 28-day food restriction (after a 28-day baseline) and back to herring during a 28-day controlled re-feeding. Diet type did not impact the rates of body mass lost when food was restricted, but did influence the type of internal energy reserve (protein vs lipids) the sea lions predominantly used. In both summer and winter, Group H lost significantly more lipids and less lean mass than Group P that was fed pollock during the restriction phase. The response of Group H was consistent with the predicted pattern of nutritional stress physiology (i.e. protein sparing and utilization of lipid reserves). Group P lost a surprisingly high proportion of body protein while consuming restricted levels of pollock, which could lead to muscle impairment and vital organ failure on a long-term basis. When given increased amounts of herring during the controlled re-feeding phase, the capacity of both groups to compensate for the previous mass loss was found to depend on season and was independent of previous diet. All of the sea lions increased their rates of mass gain and returned to their pre-experimental weight during winter, but not during summer. Some intrinsic energetic plasticity related to seasonal adaptation to the environment may render winter an easier period than summer to recover from nutritional stress.
Diets of mature male and female Steller sea lions differ and cannot be used as proxies for each other. Trites, A.W., and D.G. Calkins. 2008. Aquatic Mammals 34:25-34. abstract Disturbance of otariid breeding sites (rookeries) to determine diet from fecal remains (scats) could be eliminated if the diets of males using adjoining bachelor haulouts could be used as a proxy for diets of breeding females. We collected scats from sexually mature Steller sea lions (Eumetopias jubatus) at one male resting site (haulout) and three female dominated breeding sites (rookeries) at Forrester Island, Southeast Alaska (June-July, 1994–1999) to test whether the diets of bachelor bulls differed from that of breeding females. Female diets were fairly evenly distributed between gadids, salmon and small oily fishes (forage fish), and contained lesser amounts of rockfish, flatfish, cephalopods and other fishes. Female diet did not differ significantly between the 3 rookeries, but did differ significantly from that of males. Males consumed significantly fewer salmon, and more pollock, flatfish and rockfish compared to females. The males also consumed larger pollock compared to females. These dietary differences may reflect a sex-specific difference in foraging areas or differences in hunting abilities related to the disparity in physical sizes of males and females. The similarity of the female diets between rookeries suggests that female diets can be determined from samples collected at a single site within a rookery complex. Unfortunately, summer diets of breeding females cannot be ascertained from hard parts contained in the scats of mature male Steller sea lions.
Quantitative analysis of prey DNA in pinniped faeces: potential to estimate diet composition? Deagle, B.E. and D.J. Tollit. 2007. Conservation Genetics 8:743-747. abstract Recent studies have shown prey DNA can be consistently recovered from faeces and effectively used to provide dietary information. We investigate the possibility of using the relative amounts of DNA recovered from different prey in faeces to obtain quantitative diet composition data. Faecal samples were obtained from captive Steller seas lions (Eumetopias jubatus) being fed a fish diet consisting of 50% Pacific herring (Clupea pallasii), 36% surf smelt (Hypomesus pretiosus) and 14% sockeye salmon (Oncorhynchus nerka) by mass. Quantitative real-time PCR was used to measure the amount of mtDNA from the three fish species in: (i) a blended tissue mix representative of the sea lion diet and (ii) the sea lion faecal samples. The percent composition of fish mtDNA extracted from the undigested tissue samples corresponded reasonably well to the mass of fish in the mixture. In the faecal samples (n = 23) the absolute amount of fish mtDNA recovered varied 100-fold, but the percent composition of the three fish was relatively consistent (57.5 ± 9.3% for herring, 19.3 ± 6.6% for smelt and 23.2 ± 12.2% for salmon). Differences between the mtDNA proportions in the tissue samples compared to the faecal samples indicate there are prey-specific biases in DNA survival during digestion. These biases may be less than those commonly observed in the conventional analysis of prey hard remains. Further investigation of this approach is warranted.
Population trends, diet, genetics, and observations of Steller sea lions in Glacier Bay National Park. Gelatt, T., A.W.Trites, K. Hastings, L. Jemison, K. Pitcher, and G. O’Corry-Crowe. 2007. In J.F. Piatt and S.M. Gende (eds), Proceedings of the Fourth Glacier Bay Science Symposium, U.S. Geological Survey, Juneau , Alaska. pp. 145-149. abstract We are using demographics, scat analysis, and genetic measurements of Steller sea lions (SSLs)to understand the factors affecting population status throughout Alaska. Steller sea lions are listed as threatened throughout Southeast Alaska including Glacier Bay National Park where they frequent at least five terrestrial sites, including a recently established rookery on Graves Rock. Breeding season counts in GBNP increased at ~6 percent/yr between 1989 and 2002. Brand resighting during 2003 revealed 16 western stock SSLs seen within the park. Survival to two months of age was 90 percent. Fifty pups were branded at Graves Rock in 2002. It is necessary to mark more animals to estimate annual survival rates of juveniles and adults. Sandlance and pollock were top prey items at Graves Rock and South Marble Island. Mitochondrial DNA analysis indicates that the Graves Rock rookery was established in part by females from the western sea lion stock (west of 144° W longitude).
Comparison of fatty acid profiles of spawning and non-spawning Pacific herring, Clupea harengus pallasi. Huynh, M.D., D.D. Kitts, C. Hu and A.W. Trites. 2007. Journal of Comparative Biochemistry and Physiology, Part B 146:504-511. abstract Crude lipid and fatty acid composition from liver, intestine, roe, milt and flesh of spawning and non-spawning Pacific herring Clupea harengus pallasi were examined to determine the relative effects of spawning on the nutritional value of herring. Depletion of lipid due to spawning condition was significant (Pb0.01) in all organ tissues and flesh of spawning herring. The lipid content ranged from an average of 1.9 to 3.4% (wet weight basis) in different organ tissues of spawning herring, to 10.5 to 16% in non-spawning fish. The fatty acid profile exhibited many differences in the relative distribution of individual fatty acids among organ tissues and between the two fish groups. Oleic acid (C18:1n-9), a major monounsaturated fatty acid (MUFA) found in all tissue lipids, decreased significantly (Pb0.01) in spawning fish. The two monoenes, C20:1n-9 and C22:1n-11, occurred at high concentrations in the flesh but at only minor proportion in the digestive organs and gonads. Spawning herring also had significantly (Pb0.01) higher polyunsaturated fatty acids (PUFA) content in the organ tissues, particularly in the milt and ovary, with docosahexaenoic acid (C22:6n-3, DHA) having the greatest proportion. Among the n-6 fatty acids, only C18:2n-6 and C20:4n-6 occurred at notable amounts and were present in higher proportions in spawning fish. We concluded that although relatively higher n-3 fatty acid content was found in the organ lipids of spawning herring, they are not an energy-dense prey food source due to the fact that both flesh and gonads contain a very low amount of lipid.
Diet quality and season affect physiology and energetic priorities of captive Steller sea lions during and after periods of nutritional stress. Jeanniard du Dot, T. 2007. MSc Thesis, University of British Columbia, Vancouver. 142 pages abstract The ability of animals to contend with unpredictable seasonal shifts in quality and quantity of prey has implications for the conservation of wildlife. Steller sea lions (Eumetopias jubatus) were subjected to different quantities and qualities of food to determine what physiological and endocrine responses would occur and whether they differed between season (summer and winter) or diet (high-lipid Pacific herring Clupea pallasi vs. low-lipid walleye pollock Theragra chalcogramma). Eight females were divided among two groups. One (Group H) were fed herring for 28 days (baseline), then received a reduced caloric intake for a subsequent 28 days (restriction) to induce a 15% loss of body mass. The second (Group P) were also fed herring during the baseline followed by a reduced isocaloric diet of pollock during the restriction. Both groups subsequently returned to their baseline intake of herring for a 28-day controlled re-feeding. The two groups of sea lions lost identical mass during restrictions independent of species eaten, but did differ in the type of internal energy reserve (protein vs. lipids) they predominantly used. Group H lost significantly more lipids and less lean mass than Group P in both seasons. In summer, Group H also increased activity levels and decreased thermoregulation capacity to optimize energy allocation. No such changes were observed for Group P whose capacity to adjust to the reduced caloric intake seemed to have been blocked by the pollock diet. During winter, the sea lions spared energy allocated to activity (especially Group H) and preserved thermoregulation capacity. Changes in body mass was negatively related to free cortisol and positively related to IGF-1 in winter, but only IGF-1 was related to changes in mass in summer when lean mass regulation seemed more important. Levels of IGF-1 were associated with changes in protein metabolism in both seasons for both groups, but changes in body condition were never explained by the measured metabolites or hormones. The cap! acity to compensate for mass loss was seasonally dependent with sea lions displaying compensatory growth (by restoring lipid stores) in winter but not in summer. Summer appears to be a more difficult season for sea lions to recover from mild nutritional stress. These physiological findings can be used to refine bioenergetic models needed for the conservation of Steller sea lion populations.
Impact of diet index selection and the digestion of prey hard remains on determining the diet of the Steller sea lion (Eumetopias jubatus). Tollit, D.J., S.G. Heaslip, R.L. Barrick and A.W. Trites. 2007. Canadian Journal of Zoology 85:1-15. abstract Abstract: Nine prey species (n = 7,431) were fed to four captive female Steller sea lions (Eumetopias jubatus (Schreber, 1776)) in eleven feeding trials over 75 days to investigate the effectiveness of different methods used to determine diet from prey hard remains. Trials aimed to replicate short (1-2 day) and long feeding bouts and consisted of single species and mixed daily diets. Overall, an average of 25.2% ± 22.2% (mean ± SD, range 0-83%) of otoliths were recovered, but recovery rates varied by species (ANOVA, P = 0.01) and were linearly related to otolith robustness (R2 = 0.88). Squid beaks were recovered at higher frequencies (mean = 96%) than the otoliths of all species. Enumerating both non-otolith skeletal structures and otoliths (together termed ?bones?) increased species recovery rates by twofold on average (P < 0.001), with increases up to 2.5 times for herring and 3-4 times for salmonids. Using bones reduced inter-specific differences (P = 0.08), but recovery ! varied among sea lions. Bones were distributed over more scats per meal (mean = 2.9 scats, range = 0-5) than otoliths (mean = 1.9 scats, range = 0-4). In three different 15-day mixed diet trials, biomass reconstruction (BR) indices performed better than frequency of occurrence indices in predicting diet fed. Applying our experimentally derived numerical correction factors (to account for species differences in complete prey digestion) further improved BR estimates, resulting in all twelve unweighted comparisons within 5% (for otoliths) and 12% (for bones) of the actual diet fed.
Killer whales, whaling and sequential megafaunal collapse in the North Pacific: a comparative analysis of the dynamics of marine mammals in Alaska and British Columbia following commercial whaling. Trites, A. W., V. B. Deecke, E. J. Gregr, J. K. B. Ford, and P. F. Olesiuk. 2007. Marine Mammal Science 23:751-765. abstract The hypothesis that commercial whaling caused a sequential megafaunal collapse in the North Pacific Ocean by forcing killer whales to eat progressively smaller species of marine mammals is not supported by what is known about the biology of large whales, the ecology of killer whales and the patterns of ecosystem change that took place in Alaska, British Columbia, and elsewhere in the world following whaling. A comparative analysis shows that populations of seals, sea lions and sea otters increased in British Columbia following commercial whaling, unlike the declines noted in the Gulf of Alaska and Aleutian Islands. The declines of seals and sea lions that began in western Alaska around 1977 were mirrored by increases in numbers of these species in British Columbia. A more likely explanation is the seal and sea lion declines and other ecosystem changes in Alaska stems from a major oceanic regime shift that occurred in 1977. Killer whales are unquestionably a significant predator of seals, sea lions and sea otters but not because of commercial whaling.
Diets of Steller sea lions (Eumetopias jubatus) in Southeast Alaska from 1993-1999. Trites, A.W., D.G Calkins and A.J. Winship. 2007. Fishery Bulletin 105:234-248. abstract Diet of Steller sea lions (Eumetopias jubatus) was determined from 1494 scats (feces) collected at breeding (rookeries) and non-breeding (haulout) sites in Southeast Alaska from 1993 to 1999. The most common prey of 61 species identified were walleye pollock (Theragra chalcogramma), Pacific herring (Clupea pallasii), Pacific sand lance (Ammodytes hexapterus), Pacific salmon (Salmonidae), arrowtooth flounder (Atheresthes stomias), rockfish (Sebastes spp.), skates (Rajidae), and cephalopods (squid and octopus). Sea lion diets at the three Southeast Alaska rookeries differed significantly from one another. Steller sea lions consumed the most diverse range of prey categories during summer, and the least diverse during fall. Diet was more diverse in Southeast Alaska during the 1990s than in any other region of Alaska (Gulf of Alaska and Aleutian Islands). Dietary differences between increasing and declining populations of sea lions in Alaska correlate with rates of population change, and add credence to the view that diet may have played a role in the decline of sea lions in the Gulf of Alaska and Aleutian Islands.
Relationship between Steller sea lion diets and fish distributions in the eastern North Pacific. Bredesen, E.L., A.P. Coombs, and A.W. Trites. 2006. In A.W. Trites, S. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea and K. Wynne (eds), Sea Lions of the World. Alaska Sea Grant College Program, University of Alaska, Fairbanks. pp. 131-139. abstract Distributions of fish species were compared with diet information for Steller sea lions (Eumetopias jubatus) to assess the level of correspondence between potential prey availability and sea lion feeding habits. Fish distributions were compiled as part of the Sea Around Us Project at the UBC Fisheries Centre, and were based on published distributions and habitat preferences (e.g., latitude, depth). Sea lion scat samples were collected during the 1990s from seven geographic regions from Oregon to the western and central Aleutian Islands. The frequencies of occurrence of four prevalent species (walleye pollock, Theragra chalcogramma ; Pacific herring, Clupea pallasii ; Pacific cod, Gadus macrocephalus ; and North Pacific hake, Merluccius productus ) in the Steller sea lion diet were compared to their distributions in the North Pacific Ocean. The data suggest that Steller sea lion diets broadly reflect the distributions of these major prey species. However, some of the fish species that were regionally predicted to be present in high abundance were not proportionally reflected in the Steller sea lion diet, suggesting that other factors in addition to fish abundance influence their diets.
Using simulations to evaluate reconstructions of sea lion diet from scat. Joy, R., D.J. Tollit, J.L. Laake, and A.W. Trites. 2006. In A.W. Trites, S. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea and K. Wynne (eds), Sea Lions of the World. Alaska Sea Grant College Program, University of Alaska, Fairbanks. pp. 205-222. abstract Models used to describe pinniped diet can provide very different composition estimates. Occurrence indices as well as biomass reconstruction models (which use estimates of the number and sizes of prey consumed) are commonly used and increasingly utilize a variety of fish hard remains (bones) found in scats. However, the importance of any single fish can be overestimated if its bones are deposited in a succession of scats assumed to be from different fish. Similarly, the importance of a species will be underestimated relative to other species if the bones of one species are more fragile and are completely digested or if bones from different fish of the same species are contained in a single scat and assumed to be from a single fish. Species differences in the proportion of fish bones that survive digestion can be assessed from captive feeding studies where the number and species of prey consumed is known. Numerical correction factors can be calculated to take into account the levels of complete digestion. We performed computer simulations using data from captive feeding studies to investigate levels and sources of error in reconstructing simulated mixed species diets. Our simulations used different combinations of hard remains, were conducted both with and without the application of numerical correction factors, and compared four different diet indices (1. Modified frequency of occurrence, 2. Split sample frequency of occurrence, 3. Variable biomass reconstruction, 4. Fixed biomass reconstruction). Simulations indicated that levels of error were related to the MNI method of inferring fish numbers from prey remains, prey size, the number of identifiable prey structures used, and the robustness of the remains to digestive processes (recovery rate). The fewer fish fed, the higher the relative probability of counting the fish, particularly when a multiple element structure or all structure techniques are used. If recovery rates were assumed to be consistent across species, then large fish (particularly when fed in small amounts) were overestimated relative to smaller sized prey in all models, but particularly biomass reconstruction models and when using more than one paired structure. When recovery rates of a paired structure (otoliths) were varied across species (as observed in captive feeding studies) then biomass models tended to overestimate the species with high recovery rates. In contrast, frequency of occurrence models overestimated the contribution of smaller prey (particularly when fed in small amounts). Simulations also indicated correction factors can reduce levels of error in biomass reconstruction models, but cannot solve problems related to counting fish using MNI. Our work shows simulations can form a valuable component in assessing diet indices and the level (and direction) of associated errors in each.
Body mass and composition responses to short-term low energy intake are seasonally dependent in Steller sea lions (Eumetopias jubatus). Kumagai, S., D.A.S Rosen and A.W. Trites. 2006. Comparative Biochemistry and Physiology 179:589-598. abstract Steller sea lions (Eumetopias jubatus) were fed restricted iso-caloric amounts of Pacific herring (Clupea pallasi) or walleye pollock (Theragra chalcogramma) for 8-9 days, four times over the course of a year to investigate effects of season and prey composition on sea lion physiology. At these levels, the sea lions lost body mass at a significantly higher rate during winter (1.6 ± 0.14 kg d-1), and at a lower rate during summer (1.2 ± 0.32 kg d-1). Decreases in body fat mass and standard metabolic rates during the trials were similar throughout the seasons and for both diet types. The majority of the body mass that was lost when eating pollock derived from decreases in lipid mass, while a greater proportion of the mass lost when eating herring derived from decreases in lean tissue, except in the summer when the pattern was reversed. Metabolic depression was not observed during all trials despite the constant loss of body mass. Our study supports the hypothesis that restricted energy intake may be more critical to Steller sea lions in the winter months, and that the type of prey consumed (e.g., herring or pollock) may have seasonally-specific effects on body mass and composition.
Effects of prey composition on the endocrine response to nutrient restriction and re-alimination in Steller sea lions (Eumetopias jubatus). Richmond, J. P., T. Jeanniard du Dot, D. A. S. Rosen and S. A. Zinn. 2006. Symposia of the Comparative Nutrition Society 63:136-141. abstract Little is known about the mechanism in which decreased nutrient intake influences the physiology of Steller sea lions. By investigating the factors that link nutrition, fat metabolism and lean tissue accretion, we can assess the impact of decreased nutrient intake on energy storage and lean tissue growth, which may have implications for survival. Captive Steller sea lion females (n = 8, 2 to 5 year of age) were used to examine changes in the somatotropic axis in response to decreased nutrient intake. Animals were placed on a normal herring maintenance diet for 1 month. After this 1 month ‘baseline’ period four animals were placed on a herring submaintenance diet and four animals were fed an isocaloric Pollock submaintenance diet for 1 month. During the 1 month submaintenance period, the animals lost 10 to 15% of their body mass. In the 1 month re-alimentation period, only three animals increased mass to their initial value. Concentrations of IGF-I followed the expected pattern paralleling changes in intake. Concentrations of GH were more variable than IGF-I. Concentrations of IGFBP generally followed the expected response based on domestic animal research. The overall concentration of IGFBP-3 declined with decreased nutrient intake. In contrast, IGFBP-2 increased with decreasing nutrient intake.
Potential effects of short-term prey changes on sea lion physiology. Rosen, D.A., D.J. Tollit, A.J. Winship, and A.W. Trites. 2006. In A.W. Trites, S. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea and K. Wynne (eds), Sea Lions of the World. Alaska Sea Grant College Program, University of Alaska, Fairbanks. pp. 103-116. abstract hanges in the proximate composition of prey can result in a nutritional imbalance in individual animals, regardless of total energy intake. This mechanism has been hypothesized to have contributed to the decline of Steller sea lions (Eumetopias jubatus). Yet little is known about how otariids react physiologically to short-term changes in prey quality and availability. A series of studies with young captive Steller sea lions tested several potential links between prey quality and sea lion health. Body composition (fat to total mass ratio) of animals fed constant, maintenance-level, isocaloric diets of high- or low-lipid prey changed with season, but overall was not aff ected by prey composition. The sea lions appeared to prioritize maintaining core growth rates even when energy was limited, electing to deplete lipid reserves to fulfi ll energy defi cits, resulting in changes in relative body condition. In contrast, sea lions subject to short- term, sub-maintenance diets of high- or low-lipid prey utilized a greater portion of their lipid reserves when losing body mass on low lipid prey. Experiments with diff erent ad libitum feeding regimes indicated that sea lions are readily able to alter food intake levels to compensate for diff erences in prey energy content and, to a lesser degree, prey availability. However, the results also suggest that decreases in prey quality and/or foraging opportunities can readily combine to require food intake levels that are greater than the digestive capacity of the individual. This is particularly true for young animals that may already be living ?on the edge? energetically.
Estimating diet composition in sea lions: which technique to choose? Tollit, D.J., S.G. Heaslip, B.E. Deagle, S.J. Iverson, R. Joy, D.A.S. Rosen and A.W. Trites. 2006. In A.W. Trites, S. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea and K. Wynne (eds), Sea Lions of the World. Alaska Sea Grant College Program, University of Alaska, Fairbanks. pp. 293-307. abstract Accurate estimates of diets are vital to monitor impacts of sea lion populations on their ecosystems, their interactions with fisheries and to understand the role of food to animal nutrition and health. Approaches include using: (1) prey remnants in stomach contents, spews and scats, (2) prey DNA in scats (3) fatty acid signatures in blubber and (4) stable isotope ratios in predator's tissue. Each methodology has particular advantages and limitations, many of which can be assessed and improved through controlled captive feeding trials. Analysis of prey remnants from captive sea lion scats have shown significant variability in digestion between and within prey species, which coupled with preferential regurgitation and enumeration biases, can confound accurate diet quantification, but does not prevent spatial or temporal comparisons. Correction for partial digestion and use of additional structures besides otoliths can provide accurate prey size estimates. Prey DNA can be reliably isolated from soft remains in scats from captive sea lions and with further development this approach may allow quantification of diet. Genetic methods can be expensive and representative of only one to two days foraging (like prey remnant analysis), but may be less affected by differential digestion and can identify prey in scats that could not be identified through structural remnants. Validation of fatty acid signature analysis to quantify diet at longer temporal scales in sea lions is ongoing, but this new technique promises to be particularly useful to assess biases in traditional methods, identify the onset of weaning and to highlight what prey most contribute to lipid reserves. Stable isotope analysis of predator tissues gives only trophic level data, but can provide data on diet changes on many temporal scales. Remote video monitoring of foraging events and lavage/enema techniques can provide valuable diet information, but, like many newer techniques, animal capture is required. Ideally a suite of techniques should be used to study diet. While methods and correction factors developed for Steller sea lions can likely be applied to the other five sea lion species, they should be verified experimentally.
Sea Lions of the World. Trites, A.W., S. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea, and K. Wynne (eds). 2006. Alaska Sea Grant Alaska College Program, University of Alaska, Fairbanks. 664 pages abstract The goal of the symposium was to bring together scientists and resource managers to address knowledge of world sea lion populations in order to compare them with Steller sea lions, and to identify research needs. managers to address knowledge of world sea lion populations in order to compare them with Steller sea lions, and to identify research needs. Changes in the worldwide abundance of sea lions is of growing concern to fisheries and conservation groups, because fisheries are feared to threaten sea lions, and/or because sea lions are feared to threaten fisheries. Over the past few decades, major changes have been noted in the abundance of all five species of sea lions around the world. In the North Pacific, the Steller sea lion has been declared endangered in parts of its range and is considered threatened with extinction in others. This is in contrast to the rapid increase in populations of California sea lions in Mexico and California. Elsewhere, the Japanese subspecies of the California sea lion is probably extinct and the Galapagos subspecies is in low numbers. Numbers of New Zealand sea lions and Australian sea lions are also extremely low, with major declines recently reported in Australia. Relatively little is known about the South American sea lion. This symposium brought the world community of sea lion researchers and policy makers together to share their experiences and knowledge with each other. Interspecies comparisons can shed light on why some populations might decline while others increase. Insights might also be gained on whether trends in the abundance of sea lions are related to fishing activities through food dependencies or more directly through control or conservation measures. A better understanding of the biology of sea lions is urgently needed. The symposium significantly contributed to the understanding of fluctuating sea lion populations, especially as they compare to the Steller sea lion, by synthesizing current knowledge and forging new directions.
Molecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions. Deagle, B.E., D.J. Tollit, S.N. Jarman, M.A. Hindell, A.W. Trites and N.J. Gales. 2005. Molecular Ecology 14:1831-1842. abstract The DNA of prey present in animal scats may provide a valuable source of information for dietary studies. We conducted a captive feeding trial to test whether prey DNA could be reliably detected in scat samples from Steller sea lions (Eumetopias jubatus). Two sea lions were fed a diet of fish (five species) and squid (one species), and DNA was extracted from the soft component of collected scats. Most of the DNA obtained came from the predator, but prey DNA could be amplified using prey-specific primers. The four prey species fed in consistent daily proportions throughout the trial were detected in more than 90% of the scat DNA extractions. Squid and sockeye salmon, which were fed as a relatively small percentage of the daily diet, were detected as reliably as the more abundant diet items. Prey detection was erratic in scats collected when the daily diet was fed in two meals that differed in prey composition, suggesting that prey DNA is passed in meal specific puls! es. Prey items that were removed from the diet following one day of feeding were only detected in scats collected within 48 hours of ingestion. Proportions of fish DNA present in eight scat samples (evaluated through the screening of clone libraries) was roughly proportional to the mass of prey items consumed, raising the possibility that DNA quantification methods could provide semi-quantitative diet composition data. This study should be of broad interest to researchers studying diet since it highlights an approach that can accurately identify prey species and is not dependent on prey hard parts surviving digestion.
Examining the potential for nutritional stress in young Steller sea lions: physiological effects of prey composition. Rosen, D.A.S. and A.W. Trites. 2005. Journal of Comparative Physiology 175:265-273. abstract The effects of high- and low-lipid prey on the body mass, body condition, and metabolic rates of young captive Steller sea lions (Eumetopias jubatus) were examined to better understand how changes in prey composition might impact the physiology and health of wild sea lions and contribute to their population decline. Results of three feeding experiments suggest that prey lipid content did not significantly affect body mass or relative body condition (lipid mass as a percent of total mass) when sea lions could consume sufficient prey to meet their energy needs. However, when energy intake was insufficient to meet daily requirements, sea lions lost more lipid mass (9.16±1.80 kg±SE) consuming low-lipid prey compared with eating high-lipid prey (6.52±1.65 kg). Similarly, the sea lions lost 2.7±0.9 kg of lipid mass while consuming oil-supplemented pollock at maintenance energy levels but gained 5.2±2.7 kg lipid mass while consuming identical energetic levels of herring. Contrary to expectations, there was a 9.7±1.8% increase in metabolism during mass loss on submaintenance diets. Relative body condition decreased only 3.7±3.8% during periods of imposed nutritional stress, despite a 10.4±4.8% decrease in body mass. These findings raise questions regarding the efficacy of measures of relative body condition to detect such changes in nutritional status among wild animals. The results of these three experiments suggest that prey composition can have additional effects on sea lion energy stores beyond the direct effects of insufficient energy intake.
Dietary analysis from fecal samples: how many scats are enough? Trites, A.W. and Joy, R. 2005. Journal of Mammalogy 86(4):704-712. abstract Diets of mammals are increasingly being inferred from identification of hard parts from prey eaten and recovered in fecal remains (scats). Frequencies with which particular prey species occur among collections of scats are easily compiled to describe the average diet, and can be used to compare diets between and within geographic regions, and across years and seasons. Important to these analyses is the question of statistical power. In other words, how many scats should be collected to compare the diet among and between species? We addressed this problem using Monte Carlo simulations to analytically determine the consequence of sample size on the dietary analysis of scats using frequency of occurrence methods. We considered two questions: 1) how is the statistical power affected by sample size; and 2) what is the likelihood of not identifying a prey species? We randomly sampled predetermined numbers of scats (n=10–200) from computer-generated populations of scats containing prey of known species and frequencies of occurrences. We also randomly sampled a large database of field-collected scats from Steller sea lions (Eumetopias jubatus). We then used standard contingency table tests such as chi-square and Fisher’s exact test to determine whether differences between our samples and populations were statistically significant. We found a minimum size of 59 scats is necessary to identify principal prey remains occurring in >5% of scats. However, 94 samples are required when comparing diets to distinguish moderate effect sizes over time or between areas. These findings have significant implications for the interpretation of published dietary data, as well as for the design of future scat-based dietary studies for pinnipeds and other species.
Season variation in nutrient composition of Alaskan walleye pollock. Kitts, D. D., Huynhl,M. D., Hu, C. and Trites, A.W. 2004. Canadian Journal of Zoology 82:1408-1415. abstract A popular hypothesis for the noted steady decline in the population of Steller sea lions in the regions from Prince William Sound through the Aleutian Islands relates to their nutritional status. Sea lion diets appear to have shifted from primarily small schooling fatty fishes to low fat fish such as walleye pollock (Theragra chalcogramma). We examined the seasonal changes in proximate nutrients of pollock collected in the Bering Sea. Mean energy density (dry-weight) of pollock peaked in October then declined and remained low throughout winter. Energy recovery occurred in the summer months with strong recovery observed in female fish caught in July. Contrary to whole fish carcass energy contents, both total protein and moisture contents were at their highest levels in winter (January) when total crude lipid content was at its lowest (p<0.05). This trend gradually declined to its lowest levels in the fall, when lipid content was high. The decline in total lipi! ds during winter seasons appeared to parallel gonad development during the pre-spawning period. Sex differences in energy densities were not found. Nor did proximate analysis data for moisture, protein, ash and lipid content show any significant variation between males and females. Protein digestibility of pollock was higher (p<0.05) in the summer than in the spring, but not different for winter or fall seasons. We conclude that the nutrient content of pollock may have some impact on the Steller sea lions that feed on them, particularly the energetic value that appears to be low during important feeding periods for this marine mammal.
Suckling attempts during winter by two non-filial Steller sea lion pups (Eumetopias jubatus). Porter, B.T. and Trites, A.W. 2004. Mammalia 63:23-26. abstract Milk stealing and fostering care is rare among mammals. Among pinnipeds, the nursing of offspring that are not their own has been noted for some species of seals, but rarely for sea lions or fur seals. Thousands of hours have been spent observing Steller sea lions in the wild, but only a few successful suckling attempts have been noted. From January to March 1996, we observed two non-filial pups repeatedly suckling lactating females at a winter haulout site at Timbered Island in southeast Alaska. These two observations are noteworthy because of their rarity and the bearing they have on the poorly understood process of weaning in Steller sea lions. The timing of weaning in Steller sea lions has been speculated to occur sometime during winter or spring when pups are 6 months or older. Both mothers and pups we observed were aggressive toward intruding conspecifics and were very protective of their mother’s teats. However, there was a range of individual variation in the tolerance of both mature females and their offspring to the distance they would allow strange pups near the teats. It is undoubtedly advantageous for nutritionally stressed pups to attempt to steal milk, compared with the alternative — starvation. However the potential for injury likely out-weighs any gain in resources and probably deters most young from attempting to approach strange females. The pups we observed stealing milk did not supplement their intake with fish despite the apparent ability of this age group to capture prey. The fact that they did not suggests that they may not have been behaviourally or physiologically capable of consuming fish. Compared with milk, they may also not be physically capable of consuming enough prey to meet their daily energy needs during this period of rapid growth and development. This further suggests that weaning of Steller sea lions pups may occur much later in spring or early summer than many have previously thought.
Sizes of walleye pollock (Theragra chalcogramma) consumed by the eastern stock of Steller sea lions (Eumetopias jubatus) in Southeast Alaska from 1994-1999. Tollit, D.J., Heaslip, S.G. and Trites, A.W. 2004. Fishery Bulletin 102(3):522-532. abstract Lengths of walleye pollock (Theragra chalcogramma) consumed by Steller sea lions (Eumetopias jubatus) were estimated using allometric regressions applied to seven diagnostic cranial structures recovered from 531 scats collected in Southeast Alaska between 1994-1999. Selected structural measurements were corrected for loss of size due to erosion using experimentally derived condition-specific digestion correction factors. Correcting for digestion increased the estimated length of fish consumed by 23%, and the average mass of fish consumed by 88%. Mean corrected fork length (FL) of pollock consumed was 42.4 11.6 cm (range=10.0-78.1 cm, n=909). Adult pollock (>45.0 cm FL) occurred more frequently in scats collected from rookeries along the open ocean coastline of Southeast Alaska during June and July (74% adults, mean FL=48.4 cm) than they did in scats from haulouts located in inside waters between October and May (51% adults, mean FL=38.4 cm). Overall, the contribution of juvenile pollock (20 cm) to the sea lion diet was insignificant, while adults contributed 44% to the diet by number and 74% by mass. On average, larger pollock were eaten in summer at rookeries throughout Southeast Alaska than at rookeries in the Gulf of Alaska or the Bering Sea. Overall it appears that Steller sea lions are capable of consuming a wide size range of pollock, with the bulk of fish falling between 20-60 cm. The use of cranial hard parts other than otoliths and the application of digestion correction factors are fundamental to correctly estimating the sizes of prey consumed by sea lions and for determining their overlap with commercial fisheries.
A method to improve size estimates of walleye pollock (Theragra chalcogramma) and Atka mackerel (Pleurogrammus monopterygius) consumed by pinnipeds: digestion correction factors applied to bones and otoliths recovered in scats. Tollit, D.J., Heaslip, S.G., Zeppelin, T.K., Joy, R., Call, K.A. and Trites, A.W. 2004. Fishery Bulletin 102(3):498-508. abstract The lengths of otoliths and other skeletal structures recovered from the scats of pinnipeds, such as Steller sea lions (Eumetopias jubatus), correlate with body size and can be used to estimate the length of prey consumed. Unfortunately, otoliths are often found in too few numbers or are too digested to usefully estimate prey size. Techniques are therefore required to account for the degree of digestion of alternative diagnostic bones prior to estimating prey size. We developed a method (using defined criteria and photo-reference material) to assign the degree of digestion for key cranial structures of two prey species (walleye pollock, Theragra chalcogramma and Atka mackerel, Pleurogrammus monopterygius). The method grades each structure into one of three condition categories; good, fair or poor. We also conducted captive feeding trials to determine the extent of erosion and derive condition-specific digestion correction factors to reconstruct the original sizes of the structures consumed. In general, larger structures were relatively more digested than smaller ones. Mean size reduction varied between different types of structures (3.3-26.3%), but was not influenced by the size of the prey consumed. Results from the observations and experiments were combined to reconstruct the size of prey consumed by sea lions and other pinnipeds. The proposed method has four steps: 1) measure the recovered structures and grade the extent of digestion using defined criteria and photo-reference collection; 2) exclude structures graded in poor condition; 3) multiply measurements of structures in good and fair condition by their appropriate digestion correction factors to derive their original size; and 4) calculate the size of prey from allometric regressions relating corrected structure measurements to body lengths. This technique can be readily applied to piscivore dietary studies that use fish hard remains.
Sizes of walleye pollock and Atka mackerel consumed by the Western stock of Steller sea lions (Eumetopias jubatus) in Alaska from 1998-2000. Zeppelin, T. K., Tollit, D.J., Call, K.A., Orchard, T. J. and Gudmundson, C. J. 2004. Fishery Bulletin 102(3):509-521. abstract Prey size selectivity by Steller sea lions (Eumetopias jubatus) is relevant for understanding the foraging ecology of this declining predator, but studies have been problematic due to the erosion or absence of prey skeletal structures and otoliths usually used to estimate fish length. We developed regression formulae to estimate fish length from seven diagnostic cranial structures of walleye pollock (Theragra chalcogramma) and Atka mackerel (Pleurogrammus monopterygius). For both species, all structure measurements were related with fork length of prey (r squared range: 0.78 - 0.99). Fork length of walleye pollock and Atka mackerel consumed by Steller sea lions was estimated by applying these regression models to cranial structures recovered from scats (feces) collected between 1998 and 2000 across the range of the Alaskan western stock of Steller sea lions. Experimentally derived digestion correction factors were applied to take into account loss of size due to digestion. Fork lengths (FL) of walleye pollock consumed by Steller sea lions ranged from 3.7 to 70.8 cm FL (mean = 1 39.3 cm, SD = 14.3 cm, n = 1 666) and Atka mackerel ranged from 15.3 to 49.6 cm FL (mean = 1 32.3 cm, SD = 5.9 cm, n = 1,685). Although sample sizes were limited, a greater proportion of juvenile (less than to 20 cm) walleye pollock were found in samples collected on summer (June - September) haul-out sites (64% juveniles, n = 1 11 scats) than on summer rookeries (9% juveniles, n = 1 132 scats) or winter (February - March) haul-out sites (3% juveniles, n = 1 69 scats). Annual changes in the size of Atka mackerel consumed by Steller sea lions corresponded to changes in the length distribution of Atka mackerel resulting from exceptionally strong year classes. Considerable overlap (> 51%) in the size composition of walleye pollock and Atka mackerel taken by Steller sea lions and the commercial trawl fishery was demonstrated.
Possible effects of pollock and herring on the growth and reproductive success of Steller sea lions: insights from feeding experiments using an alternative animal model, Rattus novegicus. Donnelly, C.P., A.W. Trites and D.D. Kitts. 2003. British Journal of Nutrition 89:71-82. abstract The decline of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska appears to have been associated with a switch of diet from one dominated by fatty forage fishes (such as her-ring; Clupea pallasi ) to one dominated by low-fat fish (such as pollock; Theragra chalco-gramma). Observations made during the decline include reduced body size of sea lions, low pregnancy rates, and high mortality. We used the general mammalian model, the laboratory rat (Rattus norvegicus ), to test whether changing the quality of prey consumed could cause changes in size and reproductive performance. Five groups of twelve fiale, weanling rats were fed diets composed of herring (H), pollock (P), pollock suppliented with herring oil (PH), pollock suppliented with pollock oil (PP), or a sii-purified diet (ICN). Mean body weights were greatest for H, followed by PH, P, PP and finally ICN, although ICN was the only group significantly different from the others (P 0·05). Food intakes before mating were 10 % higher for groups on the lower-fat diets (P and ICN), resulting in similar energy intakes in all groups. The protein efficiency ratio was highest for the H diet, slightly lower for all pollock diets, and significantly lower for ICN (P 0·05). The fetal weights for mothers fed P were significantly reduced (P 0·05). The present study shows that the energy content was a major limiting factor in the nutritional quality of pollock. When food intake was adjusted to meet energetic requirients, there were no detrimental consequences from eating pollock. However, supplientation of pollock meal with additional pollock oil may reduce growth and reproductive performance, although the reasons for this were not apparent.
Examining the evidence for killer whale predation on Steller sea lions in British Columbia and Alaska. Heise, K,. L.G. Barrett-Lennard, E. Saulitis, C. O. Matkin, D. Bain. 2003. Aquatic Mammals 29:325-334. abstract The discovery of flipper tags from 14 Steller sea lions (Eumetopias jubatus) in the stomach of a dead killer whale (Orcinus orca) in 1992 focused attention on the possible role of killer whale predation in the decline of Steller sea lions in western Alaska. In this study, mariners in British Columbia and Alaska were surveyed to determine the frequency and out-come of observed attacks on sea lions, the age classes of sea lions taken, and the areas where predatory attacks occurred. The 126 survey respondents described 492 killer whale/sea lion interactions, of which at least 32 were fatal attacks on the sea lion. The greatest rate of observed predation occurred in the Aleutian Islands. The stomach contents of dead and stranded whales also were examined. Stomachs that were not empty contained only fish or marine mammal remains, but not both. This supports earlier evidence of dietary segregation between fish-eating resident and marine mammal-eating transient killer whales in Alaska. Steller sea lion remains were found in two of 12 killer whale stomachs examined from Alaska between 1990 and 2001. Stomach contents fromtwo oVshore killer whales provided the first direct evidence that this third formof killer whale feeds on fish.
Quantifying errors associated with using prey skeletal structures from fecal samples to determine the diet of the Steller sea lion (Eumetopias jubatus). Tollit, D.J., M. Wong, A.J. Winship, D.A.S. Rosen and A.W. Trites. 2003. Marine Mammal Science pp. 724-744. abstract We examined the digestion and passage times of bones and other hard parts from pollock, herring, salmon, and sandlance recovered from two juvenile captive Steller's sea lions (Eumetopias jubatus) subjected to varying activity levels. Key bones that could be identified to species were distributed over an average of 3.2 scats (range 1–6) following a single meal, with pollock remains occurring in significantly more scats than other species. Relying on otoliths alone to determine the presence of prey resulted in significantly fewer prey being identified than if other structures were also used (such as vertebrae, jaw bones, and teeth), particularly for salmon. Using either technique, there were significant differences in the likelihood that bones would be recovered from the series of scats produced following a meal, with pollock recovery exceeding herring (by three-fold) and sandlance (by eight-fold). Differences between species were reduced when recovery was calculated on a per scat basis rather than over multiple scats. Active animals passed greater numbers of bones, but the overall effect on prey recovery estimates was not significant. Defecation times of prey structures from a meal were variable and ranged from an initial 2–56 h to a final 28–148 h. The time interval to pass 95% of recovered structures varied by a factor of two among prey species, and was highest for pollock due to retention beyond 65 h.
The decline of Steller sea lions in Alaska: A review of the nutritional stress hypothesis. Trites, A.W. and C.P. Donnelly. 2003. Mammal Review 33:3-28. abstract 1. The decline of Steller sea lions Eumetopias jubatus in the Gulf of Alaska and Aleutian Islands between the late 1970s and 1990s may have been related to reduced availability of suitable prey. Many studies have shown that pinnipeds and other mammals suffering from nutritional stress typically exhibit reduced body size, reduced productivity, high mortality of pups and juveniles, altered blood chemistry and specific behavioural modifications. 2. Morphometric measurements of Steller sea lions through the 1970s and 1980s in Alaska indicate reduced body size. Reduced numbers of pups born and an apparent increase in juvenile mortality rates also appear to be nutritionally based. Blood chemistry analyses have further shown that Steller sea lions in the Gulf of Alaska and Aleutian Islands area exhibited signs of an acute phase reaction, or immune reaction, in response to unidentified physical and/or environmental stress. Behavioural studies during the 1990s have not noted any changes that are indicative of an overall shortage in the quantity of prey available to lactating female sea lions. 3. The data collected in Alaska are consistent with the hypothesis that Steller sea lions in the declining regions were nutritionally compromised because of the relative quality of prey available to them (chronic nutritional stress), rather than because of the overall quantity of fish per se (acute nutritional stress). This is further supported by captive studies that indicate the overall quality of prey that has been available to Steller sea lions in the declining popu-lation could compromise the health of Steller sea lions and hinder their recovery.
Prey consumption of Steller sea lions (Eumetopias jubatus) off Alaska: how much prey do they require? Winship, A.J. and A.W. Trites. 2003. Fishery Bulletin 101:147-163. abstract The effects of seasonal and regional differences in diet composition on the food requirements of Steller sea lions (Eumetopias jubatus)were estimated by using a bioenergetic model. The model considered differences in the energy density of the prey, and differences in digestive effciency and the heat increment of feeding of different diets. The model predicted that Steller sea lions in southeast Alaska required 45–60% more food per day in early spring (March) than after the breeding season in late summer (August) because of seasonal changes in the energy density of the diets (along with seasonal changes in energy require ments).The southeast Alaska population,at 23,000 (±1660 SD)animals (all ages), consumed an estimated 140,000 (±27,800) of prey in 1998. In contrast, we estimated that the 51,000 (±3680) animals making up the western Alaska population in the Gulf of Alaska and Aleutian Islands consumed just over twice this amount (303,000 [±57,500 ] t). In terms of biomass removed in 1998 from Alaskan waters,we estimated that Steller sea lions accounted for about 5% of the natural mortality of gadids (pollock and cod) and up to 75% of the natural mortality of hexagram mids (adult Atka mackerel).These two groups of species were consumed in higher amounts than any other.The predicted average daily food require ment per individual ranged from 16 (±2.8)to 20 (±3.6)kg (all ages com bined). Per capita food requirements differed by as much as 24% between regions of Alaska depending on the rel ative amounts of low–energy-density prey (e.g.gadids)versus high–energy density prey (e.g. forage fish and salmon)consumed. Estimated require ments were highest in regions where Steller sea lions consumed higher proportions of low—energy-density prey and experienced the highest rates of population decline.
Classifying prey hard part structures recovered from fecal remains of captive Steller sea lions (Eumetopias jubatus). Cottrell, P.E. and A.W. Trites. 2002. Marine Mammal Science 18:525-539. abstract Feces were collected from six Steller sea lions (Eumetopias jubatus) that consumed known amounts of Atka mackerel (Pleurogrammus monopterygius), Pacific herring (Clupea harengus), pink salmon (Oncorhynchus gorbuscha), walleye pollock (Theragra chalcogramma), and squid (Loligo opalacens). The goal was to determine the numbers and types of taxon-specific hard parts that pass through the digestive tract and to develop correction factors for certain abundantly occurring structures. Over 20,000 fish and squid were consumed during 267 d of fecal collection. During this period, over 119,000 taxon-specific hard parts, representing 56 different structures, were recovered. Skeletal structures and non-skeletal structures accounted for 72% and 28% of all hard parts respectively. The branchiocranium, axial skeleton, and dermocranium regions of the skeletal system accounted for the greatest number of hard parts recovered. Over 70% of all recovered hard parts were represented by one to six taxa specific structures for each prey type. The average number of hard parts (3.1-3.12) and structure types (2.0-17.7) recovered per individual prey varied across taxa and were used to derive correction factors (to reconstruct original prey numbers). A measure of the variability of hard part recovery among sea lions showed no difference for certain herring, pollock, and squid structures, however, there was a significant difference for salmon and Atka mackerel structures. Identifying all taxon-specific prey hard parts increases the likelihood of identifying and estimating the number of prey consumed.
Cost of transport in Steller sea lions, Eumetopias jubatus. Rosen, D.A.S. and A.W. Trites. 2002. Marine Mammal Science 18:513-524. abstract The cost of swimming is a key component in the energy budgets of marine mammals. Unfortunately, data to derive predictive allometric equations are limited, and estimates exist for only one other species of otariid. Our study measured the oxygen consumption of three juvenile Steller sea lions (Eumetopias jubatus) swimming in a flume tank at velocities up to 2.2 m sec-1. Minimum measured cost of transport ranged from 3.5-5.3 J kg-1, m-1, and was reached at swimming speeds of 1.7-2.1 m s-1. These cost-of-transport values are higher than those reported for other marine mammals. However, once differences in stationary metabolic rate were accounted for, the locomotor costs (LC) for the Steller sea lions were commensurate with those of other marine mammals. Locomotor costs (LC in J m-1) appeared to be directly proportional to body mass (M in kg) such that LC = 1.651M1.01. These estimates for the cost of locomotion can be incorporated into bioenergetic models and used to determine the energetic consequences of observed swimming behavior in wild marine mammals.
Changes in metabolism in response to fasting and food restriction in the Steller sea lion (Eumetopias jubatus). Rosen, D.A.S. and A.W. Trites. 2002. Comparative Biochemistry and Physiology. 132:389-399. abstract Many animals lower their resting metabolism (metabolic depression) when fasting or consuming inadequate food. We sought to document this response by subjecting five Steller sea lions to periods of: (1) complete fasting; or (2) restricting them to 50% of their normal herring diet. The sea lions lost an average of 1.5% of their initial body mass per day (2.30 kg y d )during the 9 –14-day fast, and their resting metabolic rates decreased 31%, which is typical of a ‘fasting response ’. However, metabolic depression did not occur during the 28-day food restriction trials,despite the loss of 0.30% of body mass per day (0.42 kg y d). This difference in response suggests that undernutrition caused by reduced food intake may stimulate a ‘hunger response ’, which in turn might lead to increased foraging effort. The progressive changes in metabolism we observed during the fasts were related to, but were not directly caused by, changes in body mass from control levels. Combining these results with data collected from experiments when Steller sea lions were losing mass on low energy squid and pollock diets reveals a strong relationship between relative changes in body mass and relative changes in resting metabolism across experimental conditions.While metabolic depression caused by fasting or consuming large amounts of low energy food reduced the direct costs from resting metabolism, it was insufficient to completely overcome the incurred energy deficit.
What is it about food? Examining possible mechanisms with captive Steller sea lions. Rosen, D.A.S. and A.W. Trites. 2002. In D. DeMaster and S. Atkinson (eds), Steller sea lion decline: Is it food II. University of Alaska Sea Grant, AK-SG-02-02, Fairbanks. pp. 45-48. abstract Changes in the quality or quantity of food can have a dramatic effect on the population status of wild animals. Unfortunately, it is difficult to assess (or define) whether nutritional stress is a contributing factor to the decline of any particular species.The “nutritional quality ” of a diet to an animal is a complex matter to assess given the range of components that can influence its value.The effects of different diets on animal health are equally complex, and are particularly difficult to assess in large, wild animals. Research by the North Pacific Universities Marine Mammal Research Consortium with captive Steller sea lions is evaluating the possible mechanisms by which dietary changes might adversely affect the nutritional or health status of individual animals, and ultimately the population as a whole. The research investigates the three potential proximate mechanisms by which changes in diet might impact Steller sea lions:a decrease in energy intake, a decrease in the intake of some essential element, and the over-consumption of an element detrimental to sea lion health.
A bioenergetic model for estimating the food requirements of Steller sea lions (Eumetopias jubatus) in Alaska. Winship, A.J., A.W. Trites and D.A.S. Rosen. 2002. Marine Ecology Progress Series 229:291-312. abstract A generalized bioenergetic model was used to estimate the food requirements of Steller sea lions <i>Eumetopias jubatus</i> in Alaska, USA. Inputs included age and sex-specific energy require-ments by date, population size and composition, and diet composition and energy content. Error in model predictions was calculated using uncertainty in parameter values and Monte Carlo simulation methods. Our model suggests that energy requirements of individuals were generally lowest in the summer breeding season (June to August) and highest in the winter (December to February) and spring (March to May) mainly due to changes in activity budgets. Predicted relative daily food requirements were highest for young animals (12 ± 3% SD and 13 ± 3% of body mass for 1 yr old males and females respectively) and decreased with age (5 ± 1% and 6 ± 1% of body mass for 14 yr old males and 22 yr old females respectively). The mean daily food requirement of pregnant females predicted by the model was only marginally greater than the predicted mean daily food requirement of non-pregnant females of the same age. However, the model suggested that the mean daily food requirement of females nursing pups was about 70% greater than females of the same age without pups. Of the 3 sets of model parameters (diet, population, and bioenergetic), uncertainty in diet and bioenergetic parameters resulted in the largest variation in model predictions. The model provides a quantitative estimate of the Steller sea lion population’s food requirements and also suggests directions for future research.
Temporal records of d13C and d15N in North Pacific pinnipeds: inferences regarding environmental change and diet. Hirons, A.C., D.M. Schell and B.P. Finney. 2001. Oecologia 129:591-601. abstract Sea lion and seal populations in Alaskan waters underwent various degrees of decline during the latter half of the twentieth century and the cause(s) for the declines remain uncertain. The stable carbon ( 13 C/12 C) and nitrogen ( 15 N/14 N) isotope ratios in bone collagen from wild Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus) and harbor seals (Phoca vitulina) from the Bering Sea and Gulf of Alaska were measured for the period 1951–1997 to test the hypothesis that a change in trophic level may have occurred during this interval and contributed to the population declines. A significant change in d 15 N in pinniped tissues over time would imply a marked change in trophic level. No significant change in bone collagen d 15 N was found for any of the three species during the past 47 years in either the Bering Sea or the Gulf of Alaska. However, the 15 N in the Steller sea lion collagen was significantly higher than both northern fur seals and harbor seals. A significant decline in d 13 C (almost 2 ‰ over the 47 years) was evident in Steller sea lions, while a declining trend, though not significant, was evident in harbor seals and northern fur seals. Changes in foraging location, in combination with a trophic shift, may offer one possible explanation. Nevertheless, a decrease in d 13 C over time with no accompanying change in d 15 N suggests an environmental change affecting the base of the foodweb rather than a trophic level change due to prey switching. A decline in the seasonal primary production in the region, possibly resulting from decreased phytoplankton growth rates, would exhibit itself as a decline in d 13 C. Declining production could be an indication of a reduced carrying capacity in the North Pacific Ocean. Sufficient quantities of optimal prey species may have fallen below threshold sustaining densities for these pinnipeds, particularly for yearlings and subadults who have not yet developed adequate foraging skills.
Marine mammal trophic levels and interactions. Trites, Andrew W. 2001. In J. Steele, S. Thorpe and K. Turekian (eds), Encyclopedia of Ocean Sciences. Academic Press, London, UK. pp. 1628-1633. abstract Calculating trophic levels is necessary first step to quantifying and understanding trophic interactions between marine mammals and other species in marine ecosystems. This can be achieved using dietary information collected from stomachs and scats, or by measuring isotopic ratios contained in marine mammal tissues. These data indicate that marine mammals occupy a wide range of trophic levels beginning with dugong and manatees (trophic level 2.0), and followed by baleen whales (3.35), sea otters (3.45), seals (3.95), sea lions and fur seals (4.03), toothed whales (4.23), and polar bears (4.08). With the aid of ecosystem models and other quantitative analyses, the degree of competition can be quantified, and the consequences of changing predator-prey numbers can be predicted. These analyses show that many species of fish are major competitors of marine mammals. A number of field studies have also shown negative effects of reduced prey abundance on body size and survival of marine mammals. However, there are fewer examples of marine mammal populations affecting their prey due perhaps to the difficulty of monitoring such interactions, or to the complexity of most marine mammal food webs. keywords     PhdTLmarine mammalsdietbackground
The effects of food deprivation on serum lipid concentration and content in Steller sea lions (Eumetopias jubatus). Berman, M. and L. Rea. 2000. In C.L.K. Baer (ed.), Proceedings of the Third Comparative Nutrition Society Symposium. Pacific Grove, California, August 4-9, 2000. 3:13-16. abstract The western Alaska population of Steller sea lions has significantly declined over the past thirty-five years. A population estimate of 180,000 individuals in 1965 declined to a current estimate of 50,000. A widely accepted hypothesis for the cause of decline is from indirect competition with the commercial fishing industry. Analysis of Steller sea lion censuses have determined that decline is most evident in the juvenile portion of the population. This could be explained by a decrease in prey availability for juveniles which are physiologically and behaviorally limited in their ability to forage further and deeper for food. Although Steller sea lions naturally fast during their summer breeding season, they are not as biochemically adapted to handle food deprivation at other times of the year (Rea et al. 1999). This study addresses the physiological implications of food deprivation by analyzing the effects of fasting on serum lipid composition and content. Additionally, the breeding and non-breeding seasons were compared to determine if seasonality affects serum lipid composition and content.
Alternative models for assessing the role of nutrition in the population dynamics of marine mammals. Donnelly, C., A.W. Trites and D.D. Kitts. 2000. In C.L.K. Baer (ed.), Proceedings of the Third Comparative Nutrition Society Symposium. Pacific Grove, California, August 4-9, 2000. 3:41-45. abstract Alternative animal models are desirable to assess the role of nutrition on the population dynamics of marine mammals. If an appropriate model could be found, it might be possible to identify population consequences and risks that face sea otters forced to eat fish after depleting local invertebrates, or for sea lions which switch from a fatty fish to a lean fish. From the arguments raised above, the rat appears to be a feasible model for studying marine mammal nutrition. A preliminary study exploring the effects of nutrition on population dynamics via parameters of growth and reproductive success is feasible. Although mink and harbor seal models are superior in their similarity to other marine mammals, the difficulty and time involved in breeding them is either extremely labor intensive or prohibitive. Again, the regular, five day cycle of the rat and shorter generation time allow for parameters of fertility and offspring viability in response to different diets to be examined in a cost effective and economic way. Additionally, because of the extensive use of rats in other nutritional studies, many signs and symptoms of specific nutritional shortcomings are known and easily detected. If a reliable model can be implemented in the study of marine mammal population dynamics, research can explore aspects of physiology nor available when using captive marine mammals or mammals in the wild. Development of a model also has the potential to reduce the number of mammals taken from the wild for scientific study, thereby helping to preserve many threatened species.
Forage fish abundance and distribution at Forrester Island, Alaska. Norcross, B.L., B.A. Holladay and F. Mueter. 2000. Institute of Marine Science, University of Alaska, Fairbanks, Alaska. pp. 75 + appendices abstract This study examined the abundance and species composition of forage fishes near sea lion and seabird rookeries in Southeast Alaska, East Aleutians, Pribilofs, Central Aleutians, and West Aleutians (Figure 1). Bottom trawls, midwater trawls, surveys of large predatory fish stomach contents, and measurements of physical parameters were conducted at some or all of these five regions during summer 1997. Sixty-one bottom trawl tows from among all regions collected 4539 fishes of 62 taxa. There were significant differences among regional values of depth, % mud, bottom temperature, bottom salinity, towing speed, cumulative fish abundance, and size of fish. Differences were not detected among regional mean values of %gravel, %sand, and species diversity. Among the tows on sand substrate, there were significant regional differences in species diversity. Regional species abundance and species distribution relative to physical parameters are reported and contrasted; parameters important to distribution are identified. Fourteen midwater trawl tows from Southeast and the Pribilof Islands collected 23,345 fishes of 10 taxa. Salinity, number of taxa caught, and species diversity were all significantly greater in Southeast Alaska than in the Pribilofs. Regional differences were not detected between depths, temperatures, towing speed, or cumulative fish abundance. Regional values of species abundance are reported. The stomach contents of 126 Pacific halibut and Pacific cod captured in the Pribilofs and East, Central, and West Aleutians were examined. Frequency of occurrence and numerical composition of prey taxa are reported for each predator species and region. Fish species diversity, composition, abundance, and size differed between Southeast Alaska and western locations. There were higher species diversity, different species, and fewer individuals in Southeast Alaska than in the Aleutians and Pribilofs. There were also considerable differences between sampling sites in Southeast Alaska and the Aleutian and Pribilof Islands. Trawlable areas within Southeast Alaska were significantly deeper than in the other regions, and were all of sand substrate. Bottom temperatures at bottom trawl tow sites in Southeast Alaska and in the East Aleutian Islands were warmer than in the Pribilofs, Central Aleutians and West Aleutian Islands. Samples were collected from a different vessel in Southeast Alaska than in other regions, in part resulting in a higher tow speed in Southeast Alaska. While these physical differences between regions compound the regional differences detected in fish distribution and abundance, the differences in fish are real, just their magnitude is uncertain.
Metabolic response to fasting in 6-week-old Steller sea lion pups (Eumetopias jubatus). Rea, L.D., D.A.S. Rosen and A.W. Trites. 2000. Canadian Journal of Zoology 78:890-894. abstract Four Steller sea lions (Eumetopias jubatus) aged 6 weeks were fasted for 2.5 d to determine how young pups mobilize energy reserves during short periods of fasting similar to those experienced in the wild. At 6 weeks of age, the pups lost 5.1 ± 0.3% of their body mass during 2 d of fasting, with an average daily mass loss of 0.7 ± 0.1 kg·d –1 . Plasma blood urea nitrogen (BUN) concentration increased significantly from 3.0 ± 0.1 mM, after an over-night fast, to 4.8 ± 0.5 mM, after 2.5 d of fasting. It is apparent that BUN levels are quickly depressed, since after only an overnight fast, these pups showed BUN levels 2- to 4-fold lower than those measured after the same pups, when 9 months of age, had recently been fed fish. Plasma ketone body (b-HBA) concentrations of the 6-week-old pups increased significantly from 0.32 ± 0.08 to 0.42 ± 0.08 mM between 0.5 and 1.5 d of fasting. There was no significant change in mean plasma concentration beyond 1.5 d, owing to variable individual responses to extended fasting. Plasma b-HBA levels at 9 months of age ranged from 0.07 to 0.18 mM. Six-week-old Steller sea lion pups showed blood chemistry consistent with metabolic adaptation to fasting within 16 h but were unable to sustain a protein-sparing metabolism for a prolonged period. The pups appeared to revert to protein catabolism after only 2.5 d of fasting. This infers a decrease in lipid catabolism that might be due to the depletion of available lipid resources.
Assessing the role of nutritional stress in the decline of wild populations: a Steller case of scientific sleuthing. Rosen, D.A.S. and A.W. Trites. 2000. In C.L.K. Baer (ed.), Proceedings of the Third Comparative Nutrition Society Symposium. Pacific Grove, California, August 4-9, 2000. 3:182-186. abstract Dry-matter digestibility and energy digestive efficiency were measured in six juvenile Steller sea lions (Eumetopias jubatus) fed three diets each consisting of a single species: herring, pollock, and squid. Two of the animals were also fed pink salmon. Dry-matter digestibility (DMD) and digestive efficiency (DE) were measured using the energy and manganese concentration in fecal and food samples. DE values were high for all prey species (herring: 95.4 ± 0.7% (mean ± SD), pollock: 93.9 ± 1.4%, salmon: 93.4 ± 0.5%, squid: 90.4 ± 1.3%). Steller sea lions appear to digest prey of high energy density more efficiently than prey of low energy density. DMD values were also high for all prey species (herring: 90.1 ± 1.8%, pollock: 86.5 ± 3.4%, salmon: 87.3% ± 2.6, squid: 90.5 ± 1.2%). The low DMD value for pollock compared with herring and squid was due to the high proportion of bony material in pollock. There was a strong linear relationship between DE and DMD for each prey type, but the terms cannot be used interchangeably. DE measures are more meaningful than DMD in conveying the energetic benefits derived by sea lions from different types of prey. Species-specific measures of the digestible energy obtained from an array of prey items are a necessary component in understanding the bioenergetic consequences of consuming different prey species.
Digestive efficiency and dry-matter digestibility of Steller sea lions fed herring, pollock, salmon and squid. Rosen, D.A.S. and A.W. Trites. 2000. Canadian Journal of Zoology 78:234-239. abstract Dry-matter digestibility and energy digestive efficiency were measured in six juvenile Steller sea lions (Eumetopias jubatus) fed three diets each consisting of a single species: herring, pollock, and squid. Two of the animals were also fed pink salmon. Dry-matter digestibility (DMD) and digestive efficiency (DE) were measured using the energy and manganese concentration in fecal and food samples. DE values were high for all prey species (herring: 95.4 &amp;plusmn; 0.7% (mean &amp;plusmn; SD), pollock: 93.9 &amp;plusmn; 1.4%, salmon: 93.4 &amp;plusmn; 0.5%, squid: 90.4 &amp;plusmn; 1.3%). Steller sea lions appear to digest prey of high energy density more efficiently than prey of low energy density. DMD values were also high for all prey species (herring: 90.1 &amp;plusmn; 1.8%, pollock: 86.5 &amp;plusmn; 3.4%, salmon: 87.3% &amp;plusmn; 2.6, squid: 90.5 &amp;plusmn; 1.2%). The low DMD value for pollock compared with herring and squid was due to the high proportion of bony material in pollock. There was a strong linear relationship between DE and DMD for each prey type, but the terms cannot be used interchange-ably. DE measures are more meaningful than DMD in conveying the energetic benefits derived by sea lions from dif-ferent types of prey. Species-specific measures of the digestible energy obtained from an array of prey items are a necessary component in understanding the bioenergetic consequences of consuming different prey species.
Effect of ration size and meal frequency on assimilation and digestive efficiency in yearling Steller sea lions, Eumetopias jubatus. Rosen, D.A.S., L. Williams and A.W. Trites. 2000. Aquatic Mammals 26:76-82. abstract Assimilation and digestive efficiencies were measured in four juvenile Steller sea lions (Eumetopias jubatus) fed three ration sizes of herring (3%, 6%, or 9% of body mass) at three frequencies (2, 3, or 4 times daily). Assimilation efficiency (dry matter digestive efficiency) was 90.0 ± 2.0% (mean ± 1SD). Digestive efficiency (efficiency of energy digestion) was 95.5 ± 1.0%. There was a strong linear relationship between digestive and assimilation efficiency, but no significant differences in either assimilation or digestive efficiency with changes in feeding frequency or changes in daily food intake within the ranges offered.
Morphometric measurements and body condition of healthy and starving Steller sea lion pups (Eumetopias jubatus). Trites, Andrew W. and Remco A.H. Jonker. 2000. Aquatic Mammals 26:151-157. abstract The thickness and weight of skin, blubber, and body core were measured from 12 dead Steller sea lion pups (Eumetopias jubatus). These necropsied pups represented a wide range of body sizes and conditions (small to large, and fat to no-fat), and were chosen to compare the relative body conditions of healthy and starved pups. Seven of the pups lacked blubber and were significantly lighter for a given length compared to the five that had fat at their time of death. Volume exceeded mass by a factor of 1.3% with density averaging 0.987g cm-3. Skin and blubber were not uniformly thick over the body surface. Skin was thinnest on the head and around the flippers (3mm), and became thicker towards the rump (5mm). Skin thickness did not differ between dorsal and ventral sides, unlike blubber, which was thickest on the ventral side, increasing from the snout (1.5mm)to midtrunk (7mm) and decreasing posteriorly (5mm at the tail). Along the back, blubber increased from 1 mm at the snout to about 4.5mm at mid-trunk. The five pups that died of trauma had about 13% skin and 10% blubber (expressed as a proportion of total body mass). Starvelings lost an estimated 43% of their body mass before dying (10% blubber, and 33% body core). Morphometric measurements applied to three proposed indices of body condition suggest that girth is not a good predictor of body condition for Steller sea lion pups. Only the ratio of observed to predicted body mass derived from standardized mass-length relationships could distinguish starvelings from pups with body fat. keywords     morphometric measurements, body condition, Steller sea lions, pups, skin, volume, density, starvation, #2
Seasonal differences in adaptation to prolonged fasting in juvenile Steller sea lions (Eumetopias jubatus). Rea, L.D., D.A.S. Rosen and A.W. Trites. 1999. In The FASEB Journal (Federation of American Societies of Experimental Biology). Washington, D.C., April 17-21, 1999. Vol 13(5) pp. A740 abstract Five juvenile Steller sea lions (Eumetopias jubatus) between the ages of 3 and 4 years were experimentally fasted for 9 to 14 d to assess changes in mass and in key plasma metabolites indicative of biochemical adaptation to fasting. The 5 sea lions lost 20.4 to 35.1 kg each, at a rate of 1 to 2% of their initial body mass per day. Two animals fasted during the natural breeding season (June) exhibited a mean daily loss of 1.6 +/- 0.1kg d-1. This was significantly lower than the mean 2.8 +/- 0.1kg d-1 lost by sea lions fasted outside the normal breeding season in April, October and November (p<0.001). The two sea lion studied in June maintained low BUN concentrations throughout the remainder of the study, while the remaining 3 animals showed significant increases after 7 d of fasting. Only the two juveniles fasted during the breeding season maintained a protein sparing metabolism, typical of the species adapted to long-term fasting. With the exception of the smallest female (after 12 d of fasting), ketone body levels ranged from 0.03 to 0.17 mM. Seasonal differences in how sea lions adapt to fasting suggests that these animals would be more severely impacted by limited food resources during the non-breeding season.
Metabolic effects of low-energy diet on Steller sea lions, Eumetopias jubatus. Rosen, D.A.S. and A.W. Trites. 1999. Physiological Zoology 72:723-731. abstract Diets of six Steller sea lions (Eumetopias jubatus) were switched between a high (herring) and a low (squid) energy density food for 14 d to determine the effects on ingested prey mass, body mass, resting metabolic rate, and the heat increment of feeding. Body mass was measured daily, and resting metabolism was measured weekly by gas respiro-metry. Ingested food mass did not differ significantly be-tween the squid diet and the control or the recovery herring diet periods. As a result of differences in energy density, gross energy intake was significantly lower during the squid diet phase than during either the control or recovery pe-riods. As a result, sea lions lost an average of 1.1 kg/d, totaling 12.2% of their initial body mass by the end of the experimental period. The heat increment of feeding for a 4-kg squid meal was significantly lower than for a similarly sized meal of herring. Decreases in both absolute (24.0 to 18.0 MJ/d, 224%) and mass-corrected (903 to 697 kJ/d/ kg 0.67 , 220%) metabolism were observed by the end of the squid feedings. This study suggests that sea lions can depress their resting metabolism in response to decreases in energy intake or body mass, regardless of satiation level.
Remotely releasable instruments for monitoring the foraging behaviour of pinnipeds. Andrews, R.D. 1998. Marine Ecology Progress Series 175:289-294. abstract The use of stomach temperature data loggers to record prey ingestion has proven to be very valuable when combined with time-depth recorders and satellite tracking devices in studies of seabird foraging ecology. This paper presents a similar system that will allow biologists to determine the precise timing and location of foraging by pinnipeds. The system includes a stomach temperature transmitter and an animal-mounted instrument package. The instrument package contains a satellite transmitter, for remote tracking of movements, and a data logger, for recording dive depth, swim speed, water temperature, and stomach temperature (made possible by an incorporated telemetry receiver). The instrument package can be remotely released upon command to allow data recovery without animal recapture. The system was tested on 6 Steller sea lions Eumetopias jubatus in Southeast Alaska and found to be a powerful tool for quantifying foraging behaviour, although some suggestions for improvement are presented. keywords     swimming, telemetry, foraging, food, Steller sea lion
Diet composition and trophic levels of marine mammals. Pauly, D., A.W. Trites, E. Capuli and V. Christensen. 1998. ICES Journal of Marine Science 55:467-481. abstract Standardized diet compositions were derived for 97 species of marine mammals from published accounts of stomach contents as well as from morphological, behavioural and other information. Diet was apportioned among eight categories of prey types (benthic invertebrates, large zooplankton, small squids, large squids, small pelagic fishes, mesopelagic fishes, miscellaneous fishes and higher invertebrates). Trophic levels were estimated for each species of marine mammals and compared with published estimates derived using stable isotope ratios. Trophic levels ranged from 3.2–3.4 in baleen whales and sea otters, to 3.8–4.4 in most pinnipeds and odontocete whales, to 4.5–4.6 in killer whales. Such information can be used for ecosystem modelling and related studies. keywords     marine mammals; diets; trophic levels; food organisms; stomach content; Cetacea; Balaenoptera; Odontocetes; Orcinus orca; Pinnipedia; Enhydra lutris; cetaceans; whales; Finback whales; Rorquals; Sea otter; Killer whale; Bering Sea species;
Steller Sea Lions (Eumetopias jubatus): Causes for their Decline and Factors Limiting their Restoration. Trites, A.W. 1998. Marine Mammal Research Unit, University of British Columbia, Fisheries Centre. abstract Hatch, quoted by Francis et al. (1998), states that “the principal factor responsible for unfavorable trends in marine birds and pinnipeds in the Gulf of Alaska is availability of suitable food resources. Food limitation, in turn, may be caused by recent climatically driven ecosystem shifts forcing increased production of pelagic and demersal predatory fish (e.g., adult pollock, cod, salmon, and various flatfishes, especially arrow tooth founder and halibut) at the expense of forage species (capelin, sandlance, juvenile pollock, herring, and myctophids) on which marine bird and mammal species depend.” Reviewing the available information concerning Steller sea lions supports this view and provides no indication that Steller sea lions are limited because they cannot get enough pollock to eat. The data indicate the following:  The composition of major predator and prey populations in the Gulf of Alaska and Bering Sea underwent a rapid change beginning in the mid 1970s.  The diet of Steller sea lions reflects this change in prey available to them and shows a relationship between high rates of decline and consumption of large amounts of pollock.  There is no evidence that pollock are in short supply for either fisheries or sea lions, or that the two are competing. Catching adult pollock appears to reduce cannibalism and results in more juvenile pollock being available to Steller sea lions and other top predators.  There appear to be negative health consequences for Steller sea lions if they eat primarily pollock.  Recovery of Steller sea lions will probably occur if they can obtain a more diverse diet of fattier fishes. This appears to be a function of natural changes in the marine environment and not something that can be controlled by humans.  Changes that people can invoke by altering amounts of pollock caught in time and space can have unexpected and undesirable results.
Competition between fisheries and marine mammals for prey and primary production in the Pacific Ocean. Trites, A.W., V. Christensen and D. Pauly. 1997. Journal of Northwest Atlantic Fishery Science. 22:173-187. abstract The degree of competition between fisheries and marine mammals in the Pacific Ocean was estimated for 7 statistical areas defined by the Food and Agriculture Organization of the United Nations (FAO). Catch statistics compiled from FAO sources show that the amount of fish caught in the Pacific Ocean rose from 2 million tons in the late-1940s to over 50 million tons in the early-1990s. Recent stagnation and declines occurring in some areas of the Pacific suggest that Pacific fisheries cannot continue to expand as they had previously. Based on estimates of population size, total biomass and daily consumption rates, it was estimated that the 84 species of marine mammals inhabiting the Pacific Ocean con-sume about three times as much food as humans harvest. A large fraction (>60%) of the food caught by marine mammals consisted of deep sea squids and very small deep sea fishes not harvestable by humans, thus limiting the extent of direct competition between fisheries and marine mammals. Moreover, the most important consumers of commercially exploited fish are other predatory fish, not marine mammals. Although direct competition between fisheries and marine mammals for prey appears rather limited, there may be considerable indirect competition for primary production. The primary production required to sustain marine mammals in each of the 7 FAO areas varies within a narrow range, suggesting that the diversity and abundance of marine mam-mals may have slowly evolved to fully exploit their niche and maximize their use of avail-able primary production. This contrasts with the rapid expansion of fisheries and their relatively recent dependence on primary production, which may have led to what we call ‘ food web competition’. keywords     competition, fisheries, food, feeding, marine mammals, Pacific Ocean, #3
An analysis of groundfish fishing activities near Steller sea lion rookeries in Alaska. Sampson, D. 1995. Oregon State University, Hatfield Marine Science Centre, Newport, Oregon, OR 97365. pp. 40 abstract During the past few decades large commercial fisheries for groundfish developed in the Gulf of Alaska and Bering Sea. There has been speculation that these fishing operations may have reduced the available fish stocks and thereby contributed to the dramatic declines in the Alaskan populations of Steller sea lion (Eumetopias jubatus) that occurred during the same period. Previous studies that attempted to relate estimates of sea lion abundance with annual catches of walleye pollock (Theragra chalcogramma) produced inconclusive results. In this investigation principal component analysis was applied to data from 1979-90 on sea lion counts for 25 sea lion rookeries in the Gulf of Alaska and Aleutian Islands, and independently to fishery observer data from 1980-89 for the commercial groundfish fishing operations that occurred within a distance of about 37 kilometers of these rookeries. The component scores from the two data sets were then correlated to explore for similarities between the pattern of sea lion decline and the pattern of fishing operations. There was an unusually large correlation between the second principal component for the adult sea lion declines and the second component for the winter pollock catches. Rookeries that suffered relatively large declines in sea lion counts early in the study period generally experienced large winter pollock catches, but rookeries that suffered declines late in the study period experienced either no winter pollock catches or ones that occurred late in the study period. There were no strong correlations between the components for the adult sea lion declines and any other fishery components (quarterly fishing effort and total catches of groundfish, catches of Pacific cod, Gadus macrocephalus, and of Atka mackerel, Pleurogrammus monopterygius). Also, there were no strong correlations between the components for the sea lion pups and any fishery components.