Impact of changing diet regimes on Steller sea lion body condition

MARINE MAMMAL SCIENCE, 24(2): 276–289 (April 2008)C© 2008 by the Society for Marine MammalogyDOI: 10.1111/j.1748-7692.2008.00188.x

Impact of changing diet regimes on Steller sealion body condition

SHANNON ATKINSON

Alaska SeaLife Center,301 Railway Avenue, P. O. 1329,

Seward, Alaska 99664-1329, U.S.A.and

School of Fisheries and Ocean Sciences,University of Alaska Fairbanks,

201 Railway Avenue, P.O. 730, Seward, Alaska 99664, U.S.A.E-mail: shannon [email protected]

DONALD CALKINS


Seward, Alaska 99664-1329, U.S.A.

VLADIMIR BURKANOV

National Marine Mammal Laboratory,National Oceanic and Atmospheric Administration,

7600 Sand Point Way NE, Seattle, Washington 98115, U.S.A.and

Kamchatka Branch of the Pacific Institute of Geography,Russian Academy of Sciences,

6, Partizanskaya Street,Petropavlovsk-Kamchatsky, 683000, Russia

MICHAEL CASTELLINI


245 O’Neil Building, Fairbanks, Alaska 99775, U.S.A.

DANIEL HENNEN


Seward, Alaska 99664-1329, U.S.A.

SUSAN INGLIS


Seward, Alaska 99664-1329, U.S.A.and


245 O’Neil Building, Fairbanks, Alaska 99775, U.S.A.

276

ATKINSON ET AL.: STELLER SEA LION DIET 277

ABSTRACT

A leading theory for the cause of the decline of Steller sea lions is nutritional stress,which led to chronic high juvenile mortality and possibly episodic adult mortality.Nutritional stress may have resulted from either poor quality or low abundance ofprey. The objective of this study was to determine whether we could predict shifts inbody condition (i.e., body mass or body fat content) over different seasons associatedwith a change in diet (i.e., toward lower quality prey). Captive Steller sea lions(n = 3) were fed three different diet regimes, where Diet 1 approximated the dietin the Kodiak area in the 1970s prior to the documented decline in that area, Diet2 approximated the species composition in the Kodiak area after the decline hadbegun, and Diet 3 approximated the diet in southeast Alaska where the Steller sealion population has been increasing for over 25 yr. All the animals used in this studywere still growing and gained mass regardless of diet. Body fat (%) varied between13% and 28%, but was not consistently high or low for any diet regime or season.Mean intake (in kg) of Diet 2 was significantly greater for all sea lions during allseasons. All animals did, however, tend to gain less body mass on Diets 2 and 3, aswell as during the breeding and postbreeding seasons. They also tended to gain moremass during the winter and on Diet 1, though these differences were not statisticallysignificant. Thus, changing seasonal physiology of Steller sea lions appears to havemore impact on body condition than quality of prey, provided sufficient quantity ofprey is available. Steller sea lions are opportunistic predators and are evidently ableto thrive on a variety of prey. Our results indicate that Steller sea lions are capableof compensating for prey of low quality.

Key words: steller sea lion, Eumetopias jubatus, nutritional stress, diet, body mass,body composition, dietary intake.

A leading theory for the cause of the decline of the western population of Stellersea lion (Eumetopias jubatus) is nutritional stress, which presumably led to chronichigh juvenile mortality and episodic adult mortality (York 1994, Merrick 1995,NMFS 1995, Calkins et al. 1998, Calkins et al. 1999). Investigations of nutritionalstress using captive Steller sea lions have mostly been conducted to determine nu-tritional responses to single species diets (Rosen and Trites 1999, 2000; Kumagaiet al. 2006). However, Steller sea lion diets that have been identified in the wildrarely consist of single prey species and probably represent only a few days of for-aging activity. Additionally, some captive Steller sea lion diet studies have mostlybeen conducted for short periods of time, some for as little as 8–9 d (Kumagaiet al. 2006), and have generally not included potential seasonal differences (Rosenand Trites 1999).

Essential to the nutritional stress hypothesis is that an inadequate quantity orquality of prey available to Steller sea lions has a negative impact on the healthor reproductive success of Steller sea lions. Controlled feeding studies to test thistheory in captive Alaska SeaLife Center (ASLC) harbor seals (Phoca vitulina) wereconducted over a three-y period. The results from one study suggest that diet couldnot be used to predict body condition in harbor seals and that other factors (e.g.,season, age, reproductive status) overpowered dietary manipulations (Trumble et al.2003, 2006; Castellini et al. 2002). In a separate study no significant differencesin blood chemistries or blubber fatty acid profiles could be detected in harbor sealswhen switched from a high-fat diet to a low-fat diet (Stanberry 2003, Bleakney et al.2005).

278 MARINE MAMMAL SCIENCE, VOL. 24, NO. 2, 2008

Seasonal changes in physiology also play a role in determining the impact ofdiet on body mass or body composition. Free-ranging gray seals (Halichoerus gry-pus) exhibit seasonal patterns of foraging behavior and energy storage to maximizeenergy availability for reproduction (Sparling et al. 2006). Resting metabolic rates,as measured by oxygen consumption, were highest in spring and declined throughsummer and autumn, whereas body mass and body fat increased during the sameperiod. Hedd et al. (1997) also found seasonal shifts in metabolic rate in captiveharp seals (Pagophilus groenlandicus), with peak rates in spring and summer decreas-ing throughout fall and winter. In Atlantic harbor seals (Phoca vitulina) the energyexpenditure was a better predictor of changes in metabolism than was gross en-ergy intake or body mass (Rosen and Renouf 1998). They concluded that seasonalchanges in metabolism were not the cause of variation in energy expenditure. Al-though phocid seals have been the more common experimental models for metabolicstudies than otariids, their dietary and metabolic strategies appear to differ from theotariids.

To determine how captive Steller sea lions respond to changes in diet associatedwith different diet regimes observed in the wild, we conducted an experiment wherewe varied the diet of captive Steller sea lions. We tested whether we could predictspecific changes in body condition in response to changing the diet of three Steller sealions held in captivity at the ASLC. The experiment consisted of a crossover designin which each sea lion served as its own control. Diets were manipulated according todiet parameters reflected in studies of wild Steller sea lions around Kodiak, Alaska,prior to and following the beginning of the documented decline in that area, and thediet of wild Steller sea lions in southeast Alaska where a separate population (i.e., theeastern population) has been increasing since the 1970s (Calkins and Goodwin 1988,Calkins and Pitcher 1982).

The objective of this study was to determine whether it was possible to predicta change in body condition in response to a change in diet. Proximate compositionand caloric content of each of the three diets was known and dietary intake wasmonitored daily. The response of each animal to changes in each diet regime wasmeasured through changes in body mass and percent body fat.

METHODS

Animals and Diet Regimes

This experiment was conducted on three (one male and two females) captive Stellersea lions at the ASLC between April 1999 and September 2002. At the beginningof this experiment all three sea lions were in their sixth year of age. Three dif-ferent diet regimes were fed, with each sea lion maintained on each regime for aperiod of 4 mo. Each diet regime was fed such that each sea lion was maintainedon each regime through three different seasonal cycles. Three seasonal periods wereused for this experiment: the breeding period from May through July, postbreed-ing from August through November, and winter from December through April.Diet regimes were designed to follow as closely as possible diets found in wild sealions under differing prey resource conditions with potentially different responsesto each diet regime (Table 1). The first diet was designed to approximate the dietreported by Calkins and Pitcher (1982) in the Kodiak area in the 1970s prior towhat was generally accepted as the beginning of the decline of Steller sea lions inthat area. The animals remained on this diet for a period of 4 mo. The diet was


Table 1. Annual diet regimes fed to captive Steller sea lions.

Diet regime 1 Diet regime 2 Diet regime 3

Species %a Species %a Species %c

Pollock 56 Pollock 45 Pollock 30Herring 14 Octopus 25 Pacific cod 17Squid 12 Flatfish 25 Salmon 15Capelin 8 Sand lance Flatfish 14Pacific cod 6 Pacific cod 5b Herring 11Salmon 4 Salmon Sandlance 8

Cephalopods 5d

aPercentages of diet were estimated from Calkins and Pitcher (1982) for Diet regime 1 andCalkins and Goodwin (1988) for Diet regime 2. Percentages fed were by weight and wereestimated by adding the percent volume and percent frequency of occurrence reported. Thesum of all six percent weights and frequency of occurrences was then used to calculate thepercent weight to be fed.

bSandlance, Pacific cod, and salmon comprised 5% of the diet in total to be fed at thediscretion of the trainers but fed in equal portion over a week period.

cComposition of Diet regime 3 was estimated from scat samples collected in southeasternAlaska (Trites et al. 2007). Although rock fish were found as a significant prey in southeasternAlaska, they were not available commercially to be fed in this experiment.

dCephalopods consisted primarily of octopus and squid. Diet regime 1 was only squid forthe cephalopods portion, Diet regime 2 contained 35.4% more octopus than squid, and Dietregime 3 contained 2.2% more octopus than squid.

then switched to the species composition found in the Kodiak area after the declinebegan (Calkins and Goodwin 1988). This diet was also maintained for a period of 4mo. At 8 mo into the experiment, the diet was switched to that found in southeastAlaska where the number of animals in the area is increasing (Calkins et al. 1999,Trites et al. 2007). The diets were switched and repeated so that each animal ex-perienced each diet for each of the 4-mo seasons (i.e., all three seasons for an entireyear).

Frozen whole products of prey species were used in the experiment. All prey specieswere procured from commercial sources with the exception of pollock (Theragrachalcogramma), which was donated to the ASLC.

To approximate the relative proportion of each prey species in a given diet regime,we calculated an index of prey use based on the reported percent volume and percentfrequency of occurrence for Diet regimes 1 (Calkins and Pitcher 1982) and 2 (Calkinsand Goodwin 1988) and simple frequency of occurrence of prey remains found inscats for Diet regime 3 (Trites et al. 2007). We added the reported percent volume andthe reported frequency of occurrence for each species to derive the index of prey usefor each species. Addition of the two values smoothed the effect of biases generatedwhen sea lions fed on large numbers of small prey that tended to exaggerate theimportance of that prey in the frequency of occurrence value when used alone. Whenthe sea lions fed on fewer but larger prey, percent volume tended to be exaggeratedfor that species (Calkins and Pitcher 1982). This index was converted to a percentweight for each of the six or seven prey species in each of the three diets. The speciescomposition of the diet fed to an individual animal was based on percentage weightof each prey item (see Table 1 for details).


Table 2. Proximate composition and gross energy of prey in diets fed to captive Steller sealions. Water content, protein, fat, and ash are expressed as percent of the total diet. Grossenergy is expressed as kcal/g of the wet mass of the diet (data from Bondo 2002).

Diet regime Water% Protein% Fat% Ash% Gross energy

1 76.4 15.1 5.5 2.5 1.292 78.5 13.9 3.1 2.6 1.113 74.8 15.6 6.0 2.5 1.37

All food species comprising the diet were stored in a −20◦C freezer until thawedfor feeding and not separated by age class or sex. Each day a weighed proportionby species was fed to the sea lions, usually in three to five separate feeding boutsdepending on training requirements. Each prey species was fed according to theproportions in Table 1 for each diet regime. Because food was used as a trainingincentive, sea lions were fed to trainable satiation. Trainable satiation is essentiallyad libitum as the only time food was limited was when the sea lions were full enoughthat they began to play with their food instead of consuming it. Adjustments weremade by training staff periodically within weeks in order to maintain the properproportions in each diet under training conditions.

Diet samples analyzed for this study were randomly selected (n = 10) from singlebatches of frozen prey. Different batches of prey species represented different sources.Therefore, each batch of prey was analyzed separately for caloric value and proxi-mate composition to allow us to measure between batch and seasonal variation inthe composition and energy content of a given prey species. Individual whole preyitems were measured, weighed, and homogenized in commercial grinders and foodprocessors, and then freeze-dried to constant mass (VirTis Freeze Dryer Model 5463,VirTis Company, Gardiner, NY) to obtain moisture content. The homogenate wasthen ground to a fine powder using a food mill. Subsequent analyses were conductedon the dried, homogenized samples. The caloric value of each batch of prey was deter-mined with an adiabatic bomb calorimeter (Parr Instrument Co., Moline, IL) usingthe freeze-dried samples (Bando 2002). Data for the proximate composition (Table2) were reanalyzed from Bando (2002).

Body Condition and Composition

At the beginning of this study and at the end of each 4-mo diet regime, each sealion was thoroughly tested for basic condition indices. Morphometric measurementsincluding standard length, girth, and weight were taken weekly. General health ofthe animals was monitored through monthly blood samples that were analyzed forstandard blood chemistries.

All three Steller sea lions were assessed for body condition (% body fat) at thebeginning and end of each diet regime. That is, the body condition at the end ofone diet period was used as the starting point for the body condition of the nextperiod. Determination of total body water in sea lions followed previously describedmethods (ADF&G 1996). On the measurement day, the animal was weighed and acontrol blood sample was collected. Approximately 6–9 g of 99% enriched deuter-ated, sterile water (D20) per 100 kg body mass was injected intramuscularly intothe hip of the sea lion. The injection syringe was weighed before and after injectionto calculate the delivered dose. The animals were allowed to rest for 2 h and then a


post-injection blood sample was collected. The sea lions were held either in a squeezecage or were under general anesthesia for blood sampling. The pre-injection back-ground blood sample, and postD2O samples were collected from the hip vein plexususing percutaneous venipuncture. Serum was collected and frozen at −80◦C untilanalysis.

Data Analysis

For D2O analysis, the samples and an aliquot of the dose were sent to a commer-cial laboratory (Metabolic Solutions, Nashua, NH, USA). Using standard dilutionequations, the percent body water was derived from the enrichment of samples andthe calculated percent body fat (Bowen and Iverson 1998). Metabolic Solutions rec-ommends that the percent body water (% BW) values be adjusted upward by 4% tocorrect for known pool distribution limitations in calculating total body water usingdeuterium dilution. Thus, reported% BW was multiplied by 1.04. A verificationof the assumptions in the latter equation specific to Steller sea lions has not beenpublished. Therefore, it is possible that the absolute percent fat values may requirea systematic adjustment. However, the relative changes in body fat under the givendietary conditions are valid.

Comparisons of change in body mass between diet regime treatments required thatthe data be corrected for growth, because none of the subjects in this study were fullyphysically mature. The body mass measurements for each individual were plottedagainst time and fit with a simple linear regression. The residuals from this fit wereused in all subsequent analyses that employed body mass as a response variable. Thus,change in body mass in this analysis was the deviation from monotonic growth. Foodintake values and change in % body fat did not show monotonic trends in relationto time and were not corrected.

The repeated measures analysis of variance (RMANOVA) model used here considersinteractions between diet, or season and subject, as well as between diet and seasonand diet, season and subject. All response variables were standardized to have a meanof zero and a standard deviation of 1:

Yi jk = � + �i + � j + �k + ��i j + ��ik + ��jk + ��i jk, (1)

where

� = overall mean

�i = levels of diet

� j = levels of season

�k = different subjects

�� ij = interaction between diet and season

�� ik = interaction between diet and subject

�� jk = interaction between season and subject

�� ijk = interaction between diet, season, and subject.


Because we have only one observation (cell mean) per individual and factor-levelcombination, we cannot estimate both the �� ijk interaction and the within-cellerror. In this model, the levels of diet and season are fixed effects. Subject is considereda random effect, which assumes that the Steller sea lions used in this experiment wererepresentative of the population as a whole. F-tests were based on the ratio betweeneach factor and its error term. The error term for each factor was the interactionbetween that factor and subject. If F tests indicated that the means of any of thefactor levels, or if interactions were nonzero (P < 0.05), Bonferroni t-tests were usedto determine whether differences between the factor levels were significant.

RESULTS

The three different diet regimes varied in both prey species composition (Table 1)as well as proximate composition of the diet and gross energy (Table 2). The majordifferences in the diets were seen in the relative amounts of protein and fat, which wasreflected in differences in gross energy results. Specifically, Diet 2 had the lowest grossenergy, fat and protein contents, and the highest water content (Table 2). Conversely,Diet 3 had the highest gross energy, fat, and protein contents, and the lowest watercontent (Table 2). The variation in the proximate composition in species by batchwas substantial, and likely due to age, time of year, and catch location differences ofthe batches of fish fed over the study.

All the sea lions were growing throughout the study period (Fig. 1), althoughthe rate of growth was approximately six times greater for the male (Fig. 1A) thanfor either of the females (Fig, 1B, C). All slope estimates were significantly differentfrom 0.0 (t > 18.0, P < 0.001 for each sea lion).

Changes in body mass did not differ significantly between the three diet regimes(F = 0.41, P > 0.9) or over season (F = 4.52, P = 0.094) (Fig. 2, Table 3); however,season had a larger effect on body mass than did diet. The sea lions tended to gainmore mass on Diet regime 1 and either gained less mass or stayed neutral (relative tomonotonic growth) on Diet regimes 2 and 3 (Fig. 2). Likewise, all sea lions tended togain less mass during the breeding and postbreeding seasons, but gained more massduring winter (Fig. 2). There was no significant interaction between diet and season(Table 3).

When average weekly intake of food in kg was used as the response variable, F-ratiotests indicated that there were significant differences between diets (F = 12.588, P =0.019) but not season and that the interaction between diet and season was significant(F = 15.157 P < 0.001; Fig. 3A, Table 4). Intake (in kg) of Diet 2 was highest (Fig.3A). It is important to note that it is impossible to have negative dietary intake, thenegative values reflect variation about the mean intake of individual animals, whichis a zero value on the y-axis. Average weekly intake in kcal did not significantly varyby diet or season, but did show a significant interaction between diet and season (F= 8.507, P = 0.006; Fig. 3B, Table 5).

Mean change in body fat (%) was not significantly different among diets or seasons;however, the interactions between diet and season tended toward significance (F =3.687, P = 0.055; Fig. 4, Table 6).

DISCUSSION

The results of this study demonstrate that neither diet shifts nor season alone isadequate to predict observed shifts in body mass or percent body fat in these captive


Figure 1. Regressions of body mass over time for a male (A) and two female (B and C)Steller sea lions.

Steller sea lions. The species composition of each diet was different as was the grossenergy (caloric value), reflecting a different protein-to-energy ratio and water contentin each prey species or at least in aggregate. Along with the differences in nutrientcomposition between species, there were also differences within a species. That is,between different batches of the same species, likely due to temporal, geographical,


Figure 2. Mean, standardized, residual body mass (kg) for all sea lions for each diet regimeand during each season (see Table 3).

maturity, and reproductive-related factors in individuals contained in each batch.The proximate composition of fish is known to change between seasons and withstages of life (Vollenweider et al. 2006). This study was not designed to track theseasonal/maturation changes in fish, based on the assumption that the condition ofprey purchased from commercial fishermen at various times of the year would more orless reflect the general condition of prey in the wild at that time of year. However, theproximate composition of the prey species significantly changed the dietary intakeof the sea lions; that is, sea lions on the low-energy diet (Diet 2) consumed a greatermass of food than they did when they were on the higher-energy diets (Diets 1and 3).

Diet analysis results support previous findings (Perez 1994, Payne et al. 1999,Bando 2002, Castellini et al. 2002) that the energy density of fish and invertebratesvaried both between species and within a species. Within a species, the variability isattributed to temporal, spatial, and maturity-related factors. The different batches ofprey obtained for the Steller sea lion diet regimes reflected many of these physiological

Table 3. ANOVA results using body mass as the response variable.

Source of variation df SS MS F P

Subject 2.000 1.079 0.540Diet 2.000 0.037 0.019 0.041 0.960Diet × subject 4.000 1.808 0.452Season 2.000 2.969 1.484 4.520 0.094Season × subject 4.000 1.314 0.328Diet × season 4.000 4.142 1.036 0.870 0.522Residual 8.000 9.518 1.190Total 26.000 20.867 0.803


Figure 3. Mean standardized intake, in (A) kg and (B) kcal for all sea lions of each dietregime and during each season (see Tables 4 and 5).

and environmental variables. Also, there was a documented strong inverse correlationbetween the moisture and lipid content of prey (Bando 2002, Castellini et al. 2002,Carpenter et al. 2005). A significant difference in energy density between herring,pollock, and octopus translated to a much smaller difference in % protein and moisturecontent. Thus, the use of energy density as an approximation of lipid content in preymay not be appropriate for every prey species.

RMANOVA results using both the caloric intake and the mass of intake as responsevariables indicated the presence of significant interactions between season and diet(Tables 4 and 5). The sea lions however, did not respond in a consistent manner tothe different season and diet combinations. Some of the disparities may have beendue to sex differences, but more subjects are needed to make meaningful inferenceon these interactions.

The effect of diet was significant on the feeding behavior of captive Steller sealions, with increased intake in Diet regime 2. Animals tended to consume more inthe nonbreeding season, though intake in all seasons was variable and the differences


Table 4. ANOVA results using mean weekly intake (kg) as the response variable.


Subject 2.000 0.006 0.003Diet 2.000 3.926 1.963 12.588 0.019Diet × subject 4.000 0.624 0.156Season 2.000 3.590 1.795 4.124 0.107Season × subject 4.000 1.741 0.435Diet × season 4.000 1.251 0.313 15.157 <0.001Residual 8.000 0.165 0.021Total 26.000 11.304 0.435

were not significant. This likely reflects a compensatory response to decreased foodintake during the breeding season. The interactions for mean caloric intake were alsosignificant, yet neither diet nor season alone had a significant effect. The lack of adifference in caloric intake by diet coupled with the shifts in intake by weight probablyreflects self-regulation. That is, animals are consuming larger amounts of lower-quality food in order to reach a caloric goal. This is a strategy that many terrestrialand captive marine animals adopt in response to low-quality forage (Trumble et al.2003, Bleakney et al. 2005). However, to accomplish this in a free-ranging setting,animals must adopt a compensatory feeding strategy and the behaviors that go alongwith it. In the case of free-ranging Steller sea lions, an increase in prey capture maybe difficult (and energetically costly) to make up for a lower caloric diet. As a result,free-ranging sea lions with the equivalent of Diet regime 2 may lose body mass overtime depending on their ability to balance the cost of capturing prey relative to thecaloric benefit of that prey.

The ability of marine mammals in high latitudes to deposit body fat is dependantupon not only prey resources and season, but also on environmental changes and cues.There were near-significant interactions between season and diet (P = 0.055) usingchange in body fat as a response variable. The largest decrease in body fat occurred onDiet regime 2 during the breeding season, whereas the largest increase occurred onDiet regime 1 in winter. Given that the sea lions consumed a greater mass of food onDiet regime 2, and they consumed more calories in the nonbreeding season, it is likelythat they were responding to a physiological need to replenish body reserves. Thesefindings are consistent with the notion that the content of prey may have seasonallyspecific effects on body mass and composition (Kumagai et al. 2006).

Table 5. ANOVA results using mean weekly intake (kcal) as the response variable.




Figure 4. Mean (± SD) change in body fat (%) in all sea lions for each diet regime andduring each season (see Table 6).

The same diet in three different seasons showed different results for each of thethree animals. Because the diet regime order was not randomized, there was somepossibility of a carryover effect, that is, a previous diet regime influencing the resultsof later diet regimes; however, no consistent evidence of this occurring was evident.Moreover, it is clear that the interactions between diet, season, and subject cannot beignored.

We conclude that season was generally a better predictor of body condition thandiet in this controlled study; however, as we have noted previously our sample size wassmall. This introduces the possibility that our captive population does not accuratelyrepresent the free-ranging population of Steller sea lions. Nonetheless, based on theevidence reported herein, we cannot support the hypothesis that there is a consistent orphysiologically significant response in body condition to shifts in the caloric quality ofdiet alone, provided sufficient quantity of prey is available. As opportunistic predators,the physiology of Steller sea lions has likely evolved to compensate for low-qualityprey.

Table 6. ANOVA results using change in body fat (%) as the response variable.




ACKNOWLEDGMENTS

Pollock used in this study was kindly provided by At-Sea Processors Association. We thankthe staff and volunteers of the research, husbandry, and veterinary services departments atAlaska SeaLife Center. We appreciate Dr. Douglas DeMaster and two anonymous reviewersfor their assistance in improving this paper. We also appreciate the administrative support ofMs. Angie Steeves. This project was supported by the Alaska SeaLife Center Steller Sea LionResearch Program with funds from the National Fish and Wildlife Foundation and NationalMarine Fisheries Services. All research reported here was conducted under NMFS ResearchPermit 881–1443 issued by NMFS Office of Protected Resources.

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Received: 8 November 2006Accepted: 26 September 2007

Impact of changing diet regimes on Steller sea lion body condition

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