body fat and condition in sperm whales, physeter macrocephalus, from southern australian waters

Comparative Biochemistry and Physiology Part A 134(2003) 847–862

1095-6433/03/$ - see front matter� 2003 Elsevier Science Inc. All rights reserved.doi:10.1016/S1095-6433(03)00045-X

Body fat and condition in sperm whales,Physeter macrocephalus,from southern Australian waters

Karen Evans *, Mark A. Hindell , Deborah Thielea, a b

Antarctic Wildlife Research Unit, School of Zoology, University of Tasmania, G.P.O. Box 252-05, Hobart, Tasmania 7001, Australiaa

Department of Ecology and Environment, Deakin University, Warnambool, Victoria 3280, Australiab

Received 6 October 2002; received in revised form 23 January 2003; accepted 24 January 2003

Abstract

Blubber thickness(ns102) and lipid content(ns37) were measured in sperm whales from three mass strandingevents on the west and north-west coasts of Tasmania, Australia in February 1998. Blubber thickness was highly variable,ranging from 43.0 to 168.0 mm(mean 98.4"18.4 mm) while lipid fat content, also highly variable, ranged from 16.19to 89.34%(mean 49.2"17.9%). Blubber thickness was significantly and positively related to total length, but a blubberthickness index based on the residuals of this relationship was not related to age, sex or reproductive condition. Norelationship was found between blubber thickness index and blubber lipid content, indicating that blubber thickness maynot provide a comprehensive indication of body fat condition in sperm whales when only measured at a single site.Blubber lipid content was not related to total length, age or sex. Blubber lipid content was stratified vertically throughoutthe blubber layer, suggesting that the inner blubber layer may be a more active site for lipid deposition and mobilisation,while the outer blubber layer may serve in a structural or thermoregulatory role. The social structure and foragingecology of this species may serve to minimise the need to rely on stored energy reserves to meet reproductive energyrequirements. In addition, the broader role of blubber for structural, buoyancy and insulative functions coupled with highindividual variability may cause a lack of obvious relationships between these variables and body size, age, sex andreproductive state in this species.� 2003 Elsevier Science Inc. All rights reserved.

Keywords: Body fat condition; Blubber lipid content; Blubber thickness; Mass stranding;Physeter macrocephalus; Sperm whale;Australia; Southern Ocean

1. Introduction

The body condition of an animal is often relatedto the probability of an individual’s survival andreproductive success, and by extension, the futuresurvival and success of the population as a whole(Caughley, 1977; Hanks, 1981). Body condition is

*Corresponding author. Tropical and Pelagic Ecosystems,CSIRO Marine Research, G.P.O. Box 1358, Hobart, Tasmania7001, Australia. Tel.: q61-3-62325007; fax: q61-3-62325000.

E-mail address: [email protected](K. Evans).

represented by any number of physiological indi-ces representing an animal’s energy reserves, suchas fat deposits, blood chemistry and growth rates(Hanks, 1981). Changes in these indices are oftenused as measures of an individual’s or population’sresilience to environmental stresses(Hanks, 1981).Variation in deposited fat reserves in mammals isknown to influence reproductive performance,affecting the onset of sexual maturity, inter-birthintervals, pregnancy rates, foetal growth rates andthe onset of menopause(Aguilar and Borrell,

848 K. Evans et al. / Comparative Biochemistry and Physiology Part A 134 (2003) 847–862

1990; Trites, 1991; Guinet et al., 1998). Energeticdemands associated with reproduction are high andin turn have substantial impacts on energy stores(Lockyer 1978, 1981a,b, 1986). Future reproduc-tive success is therefore reliant on how well ananimal can maintain a balance between meetingincreased energetic demands associated with repro-duction and maintaining body energy stores(Boydand McCann 1989; Lunn and Boyd 1993).The blubber layer of a cetacean may contain as

much as 90% lipid(e.g. harbour porpoises,Pho-coena phocoena, Worthy and Edwards, 1990;Lockyer, 1995; fin whales,Balaenoptera physalus,Aguilar and Borrell, 1990; Commerson’s dolphins,Cephalorhynchus commersonii, Abarnou et al.,1986). Other organs(e.g. muscle, liver and kid-ney), while containing some lipid deposits, appearto contain substantially lower lipid contents, andalthough visceral fats can contain as high as 80%lipid content in sperm whales(Lockyer, 1991),the blubber layer contributes by far the greatestproportion of total body fat mass. Blubber istherefore considered to be an important and pri-mary energy store(Lockyer, 1986, 1987; Iverson,2002) in this group of mammals. Variations in thethickness of this layer are thought to reflect chang-es in the amount of stored energy and havetherefore been related to changes in body condition(Lockyer, 1986, 1987).The thickness of the blubber layer in baleen

whales demonstrates marked seasonal variationassociated with annual migrations between polarfeeding grounds and subtropicalytemperate breed-ing grounds (Gambell, 1972; Lockyer, 1981a).Feeding does not generally occur outside the polarfeeding grounds, so all insulation, growth, repro-ductive and maintenance costs associated withmigration must be met by energy stores, resultingin annual minimum blubber thickness at the startof the feeding season following migration fromthe breeding grounds(Lockyer, 1981a). Relianceon endogenous energy stores during a reproductiveperiod involving fasting is typical of the reproduc-tive strategies of capital breeders(Jonssen, 1997).¨Such a reproductive strategy often entails relativelyshort lactation periods involving high energy trans-fer to young, therefore allowing rapid growth andshorter dependence periods(Oftedal, 1997) and istypical of many marine mammals, including baleenwhales and some phocids. The opposite strategyis that of continual energy acquisition throughoutthe reproductive period and entails adjustments to

this acquisition in reply to changes in energy costs(income breeders). Lactation in such animals isoften prolonged, and energy transfer is less con-centrated and is associated with slower growth andlonger dependence periods of young. This strategyis used by less migratory species of cetaceans andmost otariid seals.Many baleen whales have a reproductive cycle

involving 5–7 months of lactation, after whichcalves are weaned, while toothed whales oftenhave lactation periods of 1–3 years and weaningdoes not occur until at least 1–2 years(Oftedal,1997). Toothed whales such as sperm whales(Physeter macrocephalus) do not undertake large-scale migrations and their feeding and breedinggrounds are less spatially segregated. Movementsof individuals are generally driven by food avail-ability, and feeding probably occurs with the sameintensity year-round(Lockyer and Brown, 1981;Jaquet et al., 2000). As a result, the blubber layermay not serve the same role of long-term energystorage that it does in baleen whales. Rather,blubber may serve a wider role, being an importantenergy buffer during reproduction, and additionallyserving structural, insulative and possibly buoy-ancy roles(Lockyer, 1991).The view that blubber thickness may provide an

indication of the body fat condition of theseanimals may be over-simplistic. This is becausethe lipid content of blubber can vary independentlyof the thickness of the blubber layer(Ackman etal., 1975a). The mechanisms behind variations inblubber thickness are not related to cellular loss orgain, but by the enlargement or reduction ofadipocyte vacuoles(Klem, 1935; Iverson, 2002).Up to a point, there may be movement of lipidsfrom the blubber layer without an associated reduc-tion in the thickness of the blubber layer. Blubberthickness in harbour porpoises, a species lackingcyclical changes in feeding intensity, demonstratesan increasing trend with increasing blubber mass,but exhibits a poor relationship with blubber masswhen measured at only one site(Read, 1990a).Blubber thickness, as a result, when taken as asingle measurement, may be a poor indicator ofbody condition.Multiple measurements of blubber thickness are

often difficult to obtain, especially in large ani-mals. A more easily attained indicator of bodycondition can be derived by measuring the amountof lipid stored within the blubber layer. Thesemeasures can be readily attained through the col-

849K. Evans et al. / Comparative Biochemistry and Physiology Part A 134 (2003) 847–862

lection of small samples of the blubber, either fromdeceased stranded animals or via biopsy tech-niques. However, blubber is not a homogeneoustissue in cetaceans, and is variable in compositionover the body and with depth from the skininterface to the muscle interface(Ackman et al.,1975b; Lockyer, 1987, 1991). The middle sectionof blubber in sperm whales has been observed tocontain double the amount of lipid compared tothe outer and inner portions of the blubber(Lock-yer, 1991). However, documented variation inblubber lipid content observed to date has beenderived from samples taken from only one adultmale and may not be representative of other sexand age groups.Three mass strandings of sperm whales on the

west and north coasts of Tasmania, Australia in1998 (Evans et al., 2002) provided a uniqueopportunity to investigate:(i) variation in the lipidcontent and(ii) the blubber thickness of individ-uals with age and sex and whether such variationrevealed differences in the condition of animals onthe basis of these variables;(iii ) the relationshipbetween blubber thickness and blubber lipid con-tent in this species and in light of this, therobustness of blubber thickness as a measure ofbody fat condition; and(iv) possible stratificationof lipid deposits within the blubber in females andmales and the implications of any stratification tointer-study comparisons in this species.

2. Materials and methods

2.1. Sample collection

Samples of between 50 and 100 g of blubberwere collected from individuals involved in threemass strandings in February 1998(STR1, OceanBeach, Strahan,ns63; STR2, Greens Point BeachMarrawah,ns35; and STR3, Black River Beach,Stanley,ns10; Evans et al., 2002). Samples weretaken from a standardised site on the dorsal surfacein line with the posterior insertion of the flipperapproximating the dorsal sampling site detailed inGeraci and Lounsbury(1993) between 48 and 72h after death. Where possible the full depth ofblubber was sampled(ns37). All samples werewrapped in foil, stored in ice on site and thenfrozen aty20 8C.Blubber thickness from the skin interface to the

muscle interface was measured at the same loca-tion on the animal as the blubber sample before

extraction using vernier calipers to within 0.1 mm(STR1,ns57; STR2,ns35; STR3,ns10).The sex and total length of all animals from the

three strandings(tip of upper jaw to deepest notchin fluke taken in a straight line dorsally; Norris,1961) were recorded. Each individual was assignedto an age group based on counts of the number ofgrowth layers(GLGs) in a tooth taken from thatanimal (Evans and Robertson, 2001; Evans et al.,2002). These age groups corresponded to:(1)juvenile or immature(female F13 years; maleF19 years); (2) sexually mature but not physicallymature (female)13F30 years; male)19F35years); and (3) sexually and physically mature(female)30 years; male)35 years). Animalsfor which age estimates were not available werenot assigned to an age group, as total lengthsoverlapped substantially between age classes andcould not be used as an approximation of age.Lactation status were determined by applying pres-sure to teats and through identification of milk viathe in situ dissection of mammary glands.

2.2. Sample analyses

2.2.1. Stratification of samplesTo investigate the possible differential deposi-

tion of lipids within the blubber layer, a randomsubsample(ns10) of blubber samples from STR2,which encompassed the total depth of blubber, wassectioned into three parts following Lockyer(1991). These were then treated as separate sam-ples for the determination of blubber lipid content.This sample excluded any immature animals.

2.2.2. Determination of blubber lipid contentApproximately 3 g(mean 2.9"0.3 g) of clean

(all outer surfaces removed) blubber was groundin a mortar and pestle with anhydrous sodiumsulfate and extracted for 4 h in a 125-ml Soxhletapparatus with 80 ml ofn-hexane. Extracts weretransferred to a hot water bath and evaporated to40 ml and then divided into two portions: 30 mlfor pollutant analysis(Evans et al., unpublisheddata) and 10 ml to determine lipid content. Thesolvent from the 10-ml extract was evaporatedunder a stream of N and the total lipid content of2

the sample determined gravimetrically after cool-ing. Lipid content was expressed as a percentageof the wet weight of the tissue after accountingfor division of the fat extract volume.


2.3. Statistical analyses

Because individuals from the three strandingswere all sampled within the same month, it wasconsidered that seasonal effects on any trends inblubber thickness and blubber content would benegligible. Subsequently, all data from the threestrandings were pooled and analysed as one dataset. This increased our power to assess importantfactors such as sex, age, total length and reproduc-tive condition.Before blubber thickness could be compared

between sexes and the relationship with age couldbe determined, it was necessary to account forvariation due to body size. Blubber thickness datawere regressed against associated total length andthe residuals produced were used as a blubberthickness index. This method has been used toremove variation due to body size in other studiesinvestigating various body condition measures(Read, 1990a; Guinet et al., 1998). Blubber thick-ness index was compared between sexes with anindependent-samplet-test and in females betweenage groups with an ANOVA. The relationship withage was determined using a linear regression onall animals pooled, females only and males only.In an effort to minimise potential effects of any

stratification in lipid content throughout the depthof the blubber layer, only those samples encom-passing the complete blubber layer(STR1 andSTR2,ns37) were used for comparisons of per-centage lipid content. The relationship betweenlipid content and total length, age and blubberthickness(on all animals pooled and females only)was tested using a linear regression. Potentialdifferences in blubber lipid content of females inage groups 2 and 3(the small number of blubberlipid content values for animals in age group 1prevented the inclusion of these values in anystatistical tests) were tested with an independent-samplet-test.Because of the small number of blubber thick-

ness values for lactating females and males, andthe small number of blubber lipid content valuesfor males, the testing of differences in these valuesbetween reproductive groups and sexes was con-ducted using Monte Carlo randomisation tests(Manly, 1997). Mean values of blubber thicknessor lipid content were calculated for each test group.The test then randomly selected four values in thecase of lactating and non-lactating females, andfive values in the case of males and females,

calculated the mean of these values and comparedthat to the mean of the original data set. Theprobability of obtaining a particular mean valuewas estimated from 1000 randomisations run foreach test.To determine if the lipid content of blubber

varied with depth throughout the blubber layer,data from the three strata were compared using arepeated-measures ANOVA.All statistical analyses were conducted at the

95% significance level.

3. Results

3.1. Blubber thickness

The blubber thickness of individual spermwhales varied substantially, ranging from 43.0 to168.0 mm(Table 1). The lowest blubber thicknessmeasurements(43.0 and 48.0 mm) both occurredin animals aged at less than 1 year(Fig. 1). Thehighest blubber measurements(154.0 and 168.0mm) both occurred in non-lactating adult females,one aged at 36 year and the other not aged, but of1120 cm in total length.

3.1.1. Blubber thickness and blubber thicknessindex in relation to total length, age, sex andreproductive conditionBlubber thickness was weakly, but significantly

positively related to total length(r s0.2,F s21,101

23.4,P-0.001; all animals pooled,ns102). Therelationship of blubber thickness to total lengthwas stronger amongst females only(r s0.3,2

F s40.4, P-0.001, ns91; Fig. 2). Blubber1,90

thickness was observed to be negatively signifi-cantly related to length in males(r s0.5, F s2

1,10

8.4, Ps0.02, ns11; Fig. 2). However, theserelationships were highly influenced by the polar-isation of animals based on total length in allgroups tested. Because the relationship of blubberthickness to length was stronger when individualsexes were tested, sex-specific blubber thicknessindices based on these regressions were used whendetermining possible relationships between blubberthickness index and age(Table 2).Blubber thickness index was not related to age

when all animals were pooled(r s0.01, F s21,85

0.7,Ps0.4, ns86), nor when only females(r s2

0.1, F s0.06, Ps0.8, ns78) or males(r s21,77

0.1,F s0.1,Ps0.8, ns8) were included.1,7

Although no relationship was observed between


Table 1Blubber thickness of southern Australian sperm whales

Reproductive group N Age Total length Blubber thickness(mm)(GLGs) (cm)

Mean"SD Range

All 102 0.75–64.0(86) 417.0–1200.0 98.4"18.4 43.0–168.0All females 91 0.75–64.0(78) 417.0–1200.0 97.6"18.8 43.0–168.0Immature females 4 0.75–7.0 417.0–720.0 69.0"35.3 43.0–120.0Sexually mature females 29 17.0–30.0 910.0–1200.0 96.7"13.2 76.0–126.0(age group 2)

Physically mature females 45 31.0–64.0 980.0–1162.0 97.6"15.5 76–154.0(age group 3)

Non-lactating females 34 22.0–61.0(27) 980.0–1144.0 103.1"20.9 78.0–168.0(excluding immature)

Lactating females 4 24.0–64.0 1020.0–1122.0 100.3"19.3 84.0–124.0All males 11 1.9–24.0(8) 667.0–1150.0 104.7"13.0 92.0–140.0Immature males 3 1.9–19.0 667.0–1010.0 113.7"22.9 98.0–140.0Sexually mature males 5 20.0–24.0 1000.0–1150.0 99.6"5.2 92.0–105.0(age group 2)

Sample size for age and total length are presented in parentheses if different to number of blubber thickness measurements.

Fig. 1. The distribution of average blubber thickness(mm) throughout age classes(no. of GLGs) of female and male southern Australiansperm whales.

blubber thickness index and age in either sex, welimited the comparison of the blubber thicknessindex between males and females to age groups 1and 2 (there were no males in age group 3) andto those females positively identified as non-lactating(to account for any differences attributa-ble to energetic demands associated withreproduction). There was no difference in theblubber thickness index of females and males

(t sy1.5, Ps0.2, ns14). As no differences12

were found between these two groups, all malesand all females were pooled. Again, no significantdifferences were found in the blubber thicknessindex of males and females(t -0.001,Ps1.0,100

ns102). Nor were there significant differencesbetween the blubber thickness index of the threeage groups(immature, sexually mature and phys-ically mature) of females(F s0.3,Ps0.7, ns2,77


Fig. 2. The relationship between blubber thickness(mm) and total length(cm) in (a) female and(b) male southern Australian spermwhales.

78). Age differences in blubber thickness indexcould not be tested among males due to smallsample sizes.Average blubber thickness in males was not

significantly higher than that in females(results ofstatistical analyses), nor was the average blubberthickness of non-lactating females in comparisonto lactating females(Monte Carlo randomisation,P s0.5, ns38; Table 1).1000

3.2. Lipid content

The blubber lipid content of individual spermwhales varied from 16.2 to 89.3%(Table 3). Thelowest blubber lipid content occurred in a non-lactating female aged at 30 years with a blubberthickness of 80 mm and the highest blubber lipidcontents(86.0 and 89.3%) occurred in two femalesfor whom reproductive condition was not deter-


Table 2Mean residuals of blubber thickness regressed against total length among southern Australian sperm whales

Reproductive group N Regression residual

Mean SD Range

All 102 y2.0=10y4 0.07 y0.2–0.3All females 91 y0.003=10y4 0.07 y0.1–0.2Immature females 4 189.4=10y4 0.1 y0.1–0.2Sexually mature females(age group 2) 29 y81.9=10y4 0.1 y0.1–0.1Physically mature females(age group 3) 45 62.8=10y4 0.1 y0.1–0.2Non-lactating females(excluding immature) 34 166.8=10y4 0.1 y0.1–0.2Lactating females 4 53.6=10y4 0.1 y0.1–0.1All males 11 y0.009=10y4 0.04 y0.1–0.1Immature males 3 y113.2=10y4 0.1 y0.1–0.1Sexually mature males(age group 2) 5 47.9=10y4 0.02 y0.03–0.02

mined, but who were aged at 30 and 21 years andhad a blubber thickness of 107 and 76 mm,respectively.

3.2.1. Lipid content in relation to total length andageOverall lipid content was not significantly relat-

ed to total body length(r s0.03,F s1.0, Ps21,36

0.3, ns37; all animals pooled) or age(r s0.01,2

F s0.3, Ps0.6, ns31; all animals pooled).1,30

While small samples sizes prevented testing forsuch relationships in males, blubber lipid contentwas not related to total length(results of statisticalanalyses) or to age(results of statistical analyses)in females. The blubber lipid content of sexuallymature and physically mature females was notsignificantly different(t s0.7,Ps0.5, ns24).22

3.2.2. Blubber lipid content in relation to sex andreproductive conditionA Monte Carlo randomisation test demonstrated

that the average blubber lipid content in maleswas not significantly lower than that in females(P s0.20,ns37; Table 3). Small sample sizes1000

for immature animals and lactating females pre-vented comparisons of the blubber lipid content ofthese animals with the other age and reproductivegroups.

3.2.3. Blubber lipid content in relation to blubberthicknessBlubber lipid content was not related to blubber

thickness(r s0.01,F s0.2;Ps0.7,ns36; all21,35

animals pooled). Blubber lipid content additionallywas not related to blubber thickness when onlyfemales were included(r s0.004,F s0.1,Ps2

1,30

0.7, ns31).

3.2.4. Stratification of lipid contentBlubber lipid content varied significantly

throughout the vertical aspect of the blubber layer(F s7.47, Ps0.02, ns10). On average, the2,9

middle strata of blubber contained higher meanlipid percentages(47.7"10.7%) than the outer(35.7"14.2%) and inner (32.7"13.5%) strata(Table 4). However, stratification was marked byhigh individual variation. All female groups, onaverage, appeared to follow a similar pattern ofstratification, whereas males, on average, whilstcontaining the highest mean lipid percentages inthe middle strata(43.9"6.1%), contained highermean lipid percentages in the inner strata(37.5"15.7%) than in the outer strata(35.8"10.6%; Table 4). However, stratificationamongst sexes was marked by high individualvariation.

4. Discussion

The results of this study highlight the influenceof individual variability in the size of the blubberlayer and the energy stores it contains. Bothblubber thickness and lipid content varied substan-tially and appeared to be independent of each otherand the influence of age and sex, suggesting thatin this species, at least at this sample site, blubberserves a much wider role than strictly energystorage. However, high individual variabilityobserved in this study and small sizes of lactatingfemales may also serve to mask any relationshipsbetween blubber thickness and lipid content andwith age, sex or reproductive state.


Table 3Blubber lipid content of southern Australian sperm whales

Reproductive group N Age Total length Blubber Blubber lipid(GLGs) (cm) thickness content(%)

(mm)Mean"S.D. Range

All 37 0.75–64.0(31) 428.0–1150.0 43.0–168.0(36) 49.2"17.9 16.2–89.3All females 32 0.75–64.0(27) 428.0–1144.0 43.0–168.0(31) 50.4"18.1 16.2–89.3Immature females 3 0.75–7.0 428.0–720.0 43.0–120.0 56.8"27.8 24.7–73.2Sexually mature females 5 21.0–29.0 1040.0–1127.0 91.0–124.0 54.8"19.4 45.1–89.3(age group 2)

Physically mature females 19 30.0–64.0 1005.0–1144.0 76.0–103.0(18) 48.8"18.3 16.2–86.0(age group 3)

Non-lactating females 16 29.0–53.0(12) 1020.0–1144.0 78.0–168.0 44.4"14.1 16.2–63.7(excluding immature)

Lactating females 2 24.0, 64.0 1050.0, 1108.0 84.0, 124.0 41.8"0.1 34.8, 48.9All males 5 1.9–23.0(4) 667.0–1150.0 98.0–140.0 41.3"15.6 25.6–63.7Immature males 2 1.9, 5.0 667.0, 780.0 103.0, 140.0 44.6"26.9 25.6, 63.7Sexually mature males 2 23.0, 23.0 1080.0, 1150.0 98.0, 99.0 42.3"12.1 33.8, 50.9(age group 2)

All values derived from blubber samples encompassing the complete blubber layer. Sample size for age, total length and blubberthickness measurements are presented in parentheses if different to the number of blubber lipid content samples.

Table 4Lipid content of the outer, middle and inner strata of blubber in southern Australian sperm whales from STR2

Reproductive group N Age Total length Lipid content(%)(GLGs) (mm)

Outer Middle Inner

All 10 23.0–64.0(8) 1020–1150 35.7"14.2 47.7"10.7 32.7"13.5(13.2–63.1) (28.9–65.5) (19.8–61.2)

All females 7 29.0–64.0(6) 1020–1130 35.7"16.2 49.3"12.3 30.6"10.7(13.2–63.1) (28.9–65.5) (19.8–52.4)

Sexually mature females 1 29.0 1050 63.1 45.0 28.9(age group 2)

Physically mature females 5 43.0–64.0 1040–1130 30.3"13.1 50.1"14.9 26.6"5.4(age group 3) (13.2–46.9) (28.9–65.5) (19.8–32.7)

Non-lactating females 5 29.0–52.0(4) 1020–1100 41.6"14.6 49.6"14.1 32.5"11.7(excluding immature) (23.9–63.1) (28.9–65.5) (24.1–52.4)

Lactating females 1 64.0 1050 28.6 56.0 19.8All males 3 23.0(2) 1080–1150 35.8"10.6 43.9"6.1 37.5"15.7

(23.7–42.9) (37.5–48.5) (22.9–61.2)Sexually mature males 2 23.0(2) 1080, 1150 41.9"1.3 43.0"7.8 42.1"27.1(age group 2) (40.9, 42.9) (37.5, 48.5) (22.9, 61.2)

Sample size for age estimates are presented in parentheses if different to the number of blubber lipid content samples.

4.1. Blubber thickness

4.1.1. Blubber thickness in relation to length, age,sex and reproductive conditionWhile the thickness of the blubber layer was

related to total length, there was considerablevariation in the data. When sexes were consideredseparately, the relationship was stronger, largelydue to the polarisation of the samples on the basisof total length. The low numbers of small animalswere observed to largely drive the positive rela-

tionship observed in females and the negativerelationship observed in males, although individualvariation was still pronounced. It is not clearwhether the opposing relationships observed infemales and males are representative of sexualdifferences. Larger sample sizes including highernumbers of younger animals are required to sub-stantiate these relationships. Stronger positive rela-tionships between blubber thickness and totallength have been found elsewhere in both femaleand male sperm whales(Gambell, 1972) and in


other cetacean species(Slijper, 1948; Ash, 1956;Read, 1990a; Lockyer, 1995).The high individual variability observed in this

study may be the result of:(i) the nature of thedata set and compromises in the body fat conditionof individuals related to disease and poor nutrition,factors often associated with strandings; or(ii)additional energetic demands in some individualsassociated with reproduction.It has been argued that samples from stranded

animals are unlikely to reflect normal, healthypopulations, because they may be compromisedby disease, poor nutrition and biased age and sexratios (Aguilar et al., 1999). However, spermwhales derived from whaling operations(and sotherefore more likely to reflect healthy popula-tions) demonstrated similar ranges and variabilityin blubber thickness amongst individuals(Table5).Care must be taken in comparing the ranges of

blubber thickness of sperm whales between studiesfor two reasons. Firstly, the majority of otherstudies presented data from animals sampled atdiffering times of the year. If blubber thicknessdemonstrates seasonal variation associated withchanges in prey availability or reproductivedemands, differences in blubber thickness valuesbetween studies may be reflective of this variation.Secondly, it is not clear whether blubber thicknesswas measured at the same site on the body of eachanimal, and thus measurements may be confound-ed by regional variation in blubber thickness.However, blubber thickness measured at a similarsite on sperm whales sampled at a similar temporalperiod (late summer) also appears to demonstratehigh individual variability (Table 5). A generallinear model(GLM) including total length as acovariate(to account for variation related to bodysize) was used to compare blubber thickness fromsperm whales caught at Durban(Lockyer, 1991)to those in this study. Blubber thickness of animalsin this study was found to be significantly differentto both groups of sperm whales sampled fromDurban(F s6.1, Ps0.003). However, exami-2,120

nation of the residuals and calculation of thestandard deviation of the marginal means of eachdata set(Australia, 0.091; Durban, 1972, 0.089;Durban, 1973, 0.096) suggests that the variabilitywithin each of these data sets is similar. Highindividual variability in blubber thickness maytherefore be typical of this species.

Considerable individual variation in blubberthickness attributed to age and sex has beenobserved in harbour porpoises(Lockyer, 1995). Inaddition, variations in the relationship betweenbody size and age with blubber thickness associ-ated with reproductive state in sperm whales havebeen reported elsewhere(Clarke et al., 1988). Itis difficult to determine whether the individualvariation observed in our study is solely associatedwith reproductive state due to the low numbers oflactating females identified and substantial num-bers of females for which reproductive state wasnot determined. The high individual variabilityobserved throughout these sperm whales may alsoserve to mask any relationships between blubberthickness, age, sex and reproductive condition.While no differences were observed in blubberthickness between sexes, sample sizes of groupsaccounting for age and reproductive state weresmall, and even when all animals of each sex werepooled, sample sizes for males were still small.However, it would seem that rather than reflectingone parameter(reproductive state), it would bemore likely that individual variation is associatedwith both reproductive state and variation in thediet of individuals and their subsequent influenceon energy stores.

4.1.2. Blubber thickness in relation to blubberlipid contentThe blubber thickness of individuals in this

study did not reflect blubber lipid content, sug-gesting (i) that such a measurement when onlymeasured at one site does not appear to provide agood indication of condition in this species or,conversely(ii) lipid content at this sampling siteis not reflective of condition in this species or acombination of the two. Individuals with similarblubber thickness were observed to contain mark-edly different blubber lipid contents(e.g. adultfemales with 76 and 80 mm of blubber thicknesscontained 86% and 16% blubber lipid content,respectively). The lack of a relationship betweenthese two variables may be the result of threeissues:(i) errors associated with the measurementof blubber thickness and lipid content;(ii) abroader role of the blubber layer in this speciesinvolving not only energy storage, but also buoy-ancy and maintenance of body structure, resultingin the two variables being largely independent ofeach other; and(iii ) small sample sizes and high

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Table 5Blubber thickness of sperm whale groups from other areas

Japan South Africa Iceland Southeast Pacific

Period sampled September 1965a November 1966a November 1966a March 1972b March 1973b July 1985b 1959–1961c

All 116.7"52.6 88.3"10.5 74.9"11.6 107.9"39.2 104.6"65.6 250.0 –(60.0–210.0; 16) (70.0–105.0; 12) (45.0–100.0; 39) (40.0–167.0; 10) (38.0–233.0; 9) (250.0; 1)

All females 116.7"52.6 86.5"10.1 76.3"12.3 124.7"34.1 85.0"38.1 – –(60.0–210.0; 16) (70.0–105.0; 10) (45.0–100.0; 29) (75.0–167.0; 6) (63.0–129.0; 3)

Immature females 73.6"14.4 80.0"8.2 73.0"17.9 – 63.0 – 74.9"8.7(60.0–100.0; 7) (70.0–90.0; 4) (50.0–100.0; 5) (63.0, 63.0; 2) (60.0–100.0; 69)

Mature females 149.4"46.9 90.8"9.2 77.0"11.5 124.7"34.1 129.0 – –(85.0–210.0; 9) (85.0–105.0; 6) (45.0–100.0; 23) (75.0–167.0; 6) (129.0; 1)

Non–lactating 87.5"3.5 92.0"9.7 72.5"12.3 116.8"34.9 129.0 y 83.5"9.7mature females (85.0–90.0; 2) (85.0–105.0; 5) (45.0–90.0; 10) (75.0–160.0; 4) (129.0; 1) (70.0–110.0; 43)

Lactating females 167.1"35.9 85.0 80.4"9.5 140.5"37.5 – – 79.3"8.6(110.0–200.0; 7) (85.0; 1) (60.0–100.0; 14) (114.0–167.0; 2) (60.0–110.0; 395)

Immature males 97.5"10.6 70.5"8.3 82.8"35.6 90.6"56.8 – 84.1"13.5(90.0–105.0; 2) (55.0–80.0; 10) (40.0–114.0; 4) (38.0–160.0; 5) (60.0–120.0; 71)

Mature males – – – – 233.0 250.0 103.2"14.5(233.0; 1) (250.0; 1) (70.0–140.0; 628)

Values are given as mean"S.D. (range;N). Maturity in females is based on sexual maturity.Ohsumi(1971).a

Lockyer (1991).b

Clarke et al.(1988). Male values based on sexually mature but not physically mature males, non-lactating female values based on mature resting females.c


individual variability masking any possible rela-tionships between the two.Variation in blubber thickness and lipid content

can be derived from a number of sources:(i)variation associated with human error in measure-ment;(ii) variation associated with the position ofthe animal and the consequent distortion of theblubber layer at the time of measurement;(iii )regional variation in the sampling site; and(iv)variation associated with decomposition of theanimal. In this study we consider the likelihood ofall these errors to be minimal due to:(i) theminimisation of people conducting measurements;(ii) the standardised dorsal position of the sam-pling site, minimising variation associated with thenon-uniformity of blubber thickness and blubberlipid content across the body(Slijper, 1948; Lock-yer et al., 1985; Lockyer, 1991; Koopman, 1998)and the effects of any distortions of the blubberwith animals’ positions;(iii ) similar post-mortemsampling times, resulting in relative consistency ofany decomposition effects across samples; and(iv)similar handling of samples post-mortem, minim-ising any variability in the handling or processingof samples.Blubber in sperm whales is thought not only to

function as an energy reserve, but also to havethermoregulatory, buoyancy and structural roles(Lockyer, 1991; Iverson, 2002). Liquid–solidphase changes in blubber lipids with temperaturecould result in changes in density and thereforebuoyancy, which may in turn influence rates ofdescent and ascent(Lockyer, 1991). Blubber alsoprovides an insulative layer critical to the ther-moregulatory requirements of a mammal living ina thermally conductive and cold environment, aswell as providing an external shape required toprovide streamlining, thereby reducing energydemands created by moving throughout a high-density, high-viscosity environment(Iverson,2002). Associated with these roles, there may bea minimum thickness(relative to body size) atwhich blubber may properly function. Energyreserves may vary through biochemical alterationof the blubber tissue, involving the replacement oftissue water by lipid during times of fattening andthe reverse when energy reserves are required(Lockyer, 1993). This may result in changes inthe lipid content of the blubber without an asso-ciated change in the size of the layer. If so,variation in energy demands between sexes, orwith reproductive demands and their effects on

energy stores may not necessarily be reflected inblubber thickness.

4.2. Blubber lipid content

4.2.1. Blubber lipid content in relation to length,age and sexAs with blubber thickness, blubber lipid content

varied substantially between individuals(range16.2–89.3%). Lipid content was not related tolength or age, and there also appeared to be littledifference in lipid content between sexes.The lipid content of near-term foetuses in long-

finned pilot whales is similar to that of calves andadults(Lockyer, 1993). This is thought to be dueto the need for blubber to play a greater role thanjust as an energy store, and to also be importantin buoyancy, thermoregulatory, physiological andstructural functions in newborn calves. The threeanimals in this study below the age of 2 yearscontained blubber lipid content ranging from 25to 72%, similar to the range of values in adults.Blubber may also serve a similar wider role abovethat of strictly an energy store in sperm whales,and as a result, may not demonstrate a distinctrelationship with length or age.Pond(1984) postulated that energy storage is a

mammalian strategy primarily associated withreproduction, freeing females from large amountsof foraging activity to provide young with closesupervision and regular food, and allowing malesto meet additional energy demands associated withcompetition for mates. Female sperm whales aregregarious, forming socially cohesive groups of10–30 adult females and immature individualsbased on mostly permanent units of 12–13 indi-viduals (Whitehead et al., 1991; Richard et al.,1996). The principal function of this sociality hasbeen hypothesised to be associated with communalcare of young and defence(Best, 1979; Richardet al., 1996). These strategies would serve to freelactating mothers from supervisory roles overyoung, allowing continual foraging and the costsof reproduction to be met by continued feeding,rather than placing demands on energy reserves.A reproductive strategy involving the continuousacquisition of energy throughout the reproductiveperiod, allowing adjustments in energy acquisitionin response to changes in energy demands and aprolonged lactation period, is typical of that ofincome breeders(Jonssen, 1997). Body energy¨stores may thereby vary independently of energetic


Table 6Lipid content of the blubber of sperm whales from other areas

Lipid content(%)

North Seaa North Seab North Seac South Africad Eastern NortheasternN. Atlantice N. Atlanticf

Month November November November Unknown Unknown UnknownAll 64.0"3.8 58.3"10.7 36.3"11.7 63.3"8.4 – 40.3"6.7

(57.8–69.6; 7) (47.0–74.0; 7) (8.0–53.0; 21) (48.8–79.2; 12) (10)Female – – – 58.8 68.8 –

(58.8; 1) (6)Male 64.0"3.8 58.3"10.7 36.3"11.7 63.7"8.7 66.4 40.3"6.7

(57.8–69.6; 7) (47.0–74.0; 7) (8.0–53.0; 21) (48.8–79.2; 11) (8) (10)

Values are given as mean"S.D. (range;N).Holsbeek et al.(1999); single, stranded animals, sample composed of only adult males.a

Law et al.(1996); single, stranded animals, sample composed of only adult males.b

Wells et al.(1997); single, stranded animals, sample composed of only adult males.c

Henry and Best(1983).d

Aguilar (1983).e

Borrell (1993); sample composed of only adult males.f

requirements associated with sex, age or reproduc-tive state, providing that those requirements aremet by substantive, continuous energy acquisition.Long-finned pilot whales, similarly to sperm

whales, are highly social and appear to have asimilar reproductive cycle(Amos et al., 1993;Bloch et al., 1993). Reproduction in long-finnedpilot whales appears to coincide with movementsinto areas to feed, possibly so that energetic costsassociated with reproduction may be met byincreased feeding in the beginning of the season,followed by a drawing of energy reserves later inthe season when food is not as abundant(Lockyer,1993). This pattern in the utilisation of lipidreserves has been found to occur across all pilotwhales, regardless of sex or reproductive state(Lockyer, 1993). Sperm whales may employ asimilar strategy as a means of meeting energydemands associated with reproduction. However,it is difficult to establish the effects of reproductivedemands on blubber lipid content due to smallnumber of lactating females included in this study.Conclusions on whether the diet of individualssampled from these strandings varies in associationwith reproductive status or sex are restricted bythe small sample size of lactating females andmales (Evans and Hindell, unpublished data).However, dietary analyses suggest that there maybe some segregation of foraging groups by sex,although this is confounded by high individualvariability. Further studies involving larger samplesizes are required to determine if this possible

dietary segregation is a result of differences inenergetic requirements between sexes associatedwith reproduction.

4.2.2. Blubber lipid content in relation to spermwhales elsewhereMaximum blubber lipid-content values(89.3%)

were higher than those reported from sperm whaleselsewhere, although mean values were similar orlower (Table 6). Blubber lipid content has beenreported as low as 8% in sperm whales from theNorth Sea(Wells et al., 1997) and in most areasis typified by high individual variability(Table 6).It is difficult to draw conclusions from these

comparisons for several reasons.(i) The majorityof lipid content values presented in other studiesare derived from males. Differences in blubberlipid content have been found between sexes infin and sei whales,(Lockyer et al., 1985; Lockyer,1986, 1987; Aguilar and Borrell, 1990), but werenot found between sexes in long-finned pilotwhales (Lockyer, 1993). It is unclear from ourdata whether sexual differences in blubber lipidcontent occur in this species.(ii) A number oflipid content values reported are derived fromsamples collected from single strandings(Law etal., 1996; Wells et al., 1997; Holsbeek et al.,1999), in which the animals involved were knownto have had severe weight deficits(Jauniaux et al.,1997). Such animals are unlikely to be represen-tative of natural populations.(iii ) Sperm whalesin the other studies presented were either sampled


at the beginning of winter(compared to the endof summer in this study) or else the samplingperiods were not stated. If variation in blubberlipid content is associated with seasonal preyabundance or with varying timing of periods ofhigh energy requirements associated with repro-duction (see Best et al., 1984 for a synopsis ofgeographic variation in the breeding season ofsperm whales) in this species, differences in blub-ber lipid content values between studies may bereflective of this variation.(iv) The location fromwhich blubber samples were collected was eithernot specified or was different to that in this study,and the extent of the blubber samples(whetherthe full blubber depth was sampled) was often notspecified. Blubber lipid content has been found tovary regionally and to demonstrate stratification ina number of cetacean species, including spermwhales (Ackman et al., 1975a; Lockyer et al.,1984; Lockyer, 1991; this study). As a result,comparison of lipid content values are limited insamples collected from different sites and incor-porating differing depths of the blubber.(v)Extraction methods varied between studies. Thesedifferences may have resulted in variation in theefficiency of lipid extraction, and therefore in thereporting of total lipids. It may be argued thathexane-based extraction methods(such as themethods used in this study and those regularlyused for the extraction of lipids for organic pollut-ant analyses) may not be as efficient at extractingall lipids, particularly wax esters, which are foundin high proportions in sperm whales(Lockyer,1991; Bedard 1998) as other extraction methods,such as those based on chloroform–methanol.However, the relative variation in blubber lipidcontent values among individuals appears to behigh in other studies, as in this study. High indi-vidual variation in blubber lipid content, as withblubber thickness, may therefore be typical of thisspecies.Although it is not clear that blubber thickness

and blubber lipid content are not influenced byage, sex of reproductive state, if we do assumethat this is the case, what factors may cause thehigh amount of variability in these measures doc-umented both in this study and elsewhere. It ispossible that individuals may not be compromisedas long as the mass and composition of blubber inan individual can meet the physiological require-ments for energy, insulation, buoyancy and struc-tural roles. Any variation in these variables in the

blubber may be a reflection of individual differ-ences in either the(i) acquisition or(ii) utilisationof energy. The diet of sperm whales from thesestrandings is typified by high individual variability(Evans and Hindell, unpublished data), suggestingdifferences in the feeding intensity and foragingsuccess of individuals. Associated with this, ifdiffering foraging strategies are employed by indi-viduals (e.g. differences in the spatial distributionof foraging individuals or differences in dive pro-files), this may be reflected in differing metabolicdemands on energy stores. Both factors wouldultimately result in high individual variability inenergy stores.

4.2.3. Stratification of lipid contentThe overall pattern of blubber lipid stratification

presented in this study differed from that previous-ly observed at a similar sampling site in an adultmale sperm whale sampled in the middle of thenorthern hemisphere summer(Lockyer, 1991), butwas similar to that observed in fin whales(Ack-man et al., 1975a; Lockyer et al., 1984). BothLockyer (1991) and this study found that thehighest blubber lipid content occurs the middlelayer of the blubber. Lockyer(1991) observed ahigher lipid content in the inner layer than theouter blubber layer, whilst overall mean blubberlipids in this study were higher in the outer layerthan the inner layer. The overall mean pattern ofstratification among young males in this study wassimilar to that observed by Lockyer(1991). How-ever, in our study the sample number of maleswas small(ns3) and no fully mature male spermwhales were analysed, whilst Lockyer(1991) sam-pled only one adult male. As a result, it isimpossible to determine if this pattern of stratifi-cation is typical of males in general, and thereforewhether the differences in stratification are repre-sentative of gender differences in lipid depositionand mobilisation. Average lipid content of the outerand inner blubber layers did not differ substantially(outer 35.7"14.2%, inner 32.7"13.5%; all ani-mals pooled), and given the large individual vari-ation observed in this study, the different patternsobserved between sexes are not easilyinterpretable.Stratification of constituent fatty acids has been

observed in the blubber of a female fin whale(Lockyer et al., 1984), grey, harbour, ringed andharp seals(Fredheim et al., 1995), male harbourporpoises (Koopman et al., 1996) and female


elephant seals(Best et al., 2003) but not in onemale sperm whale(Lockyer, 1991). This stratifi-cation has been attributed to differential depositionand mobilisation of lipids associated with energyacquisition and metabolism(Koopman et al.,1996) and with structural demands associated withthermal regulation(Fredheim et al., 1995). Higherlevels of polyunsaturated fatty acids have beenobserved in the inner layer of blubber and mediumchain-fatty acids in the outer blubber layer of somephocid seal species(Fredheim et al., 1995; Bestet al. 2003), fin whales(Lockyer et al., 1984) andharbour porpoises(Koopman et al., 1996), sug-gesting the inner layer is more metabolically activeand the outer layer has a more structural role.However, direct comparisons between studies areconfounded by temporal differences in sampling,differences in the sex of animals sampled, regionalvariation in sampling sites on animals and differ-ences in analytical techniques. It is also unclear towhat extent the differential energetic budgets ofcapital (some phocids, fin whales) and incomebreeders(sperm whales; harbour porpoises appearto exhibit a life history somewhere between thetwo; Read, 1990b; Read and Hohn, 1995) mayhave on the deposition and mobilisation of lipidsand their subsequent stratification within the blub-ber layer. The stratification of lipids observed inthis study is supported by preliminary analysis offatty acids in the blubber of two female spermwhales (Bedard, 1998). Analysis for constituentfatty acids suggests that blubber lipids are com-posed of higher levels of medium-chain fatty acids(16:1v7c and 19:1v9c monosaturates) in the outerlayer of blubber, while the inner layer, althoughstill dominated by the 16:1v7c and 19:1v9c mon-osaturates, contains higher amounts of polyunsat-urated fatty acids(e.g. 20:1v9c). It is difficult todraw conclusions from these results in comparisonto that previously reported in one adult male spermwhale (Lockyer, 1991) because of differences inthe gender of animals sampled and subsequentpossible sexual differences in stratification pat-terns, differences in analytical techniques used(seeBest et al., 2003 for a description of the methodsused for the Tasmanian samples) and the smallsample sizes.The stratification of lipids within the blubber of

sperm whales has implications for studies basedon lipid extractions from the blubber, such aslipophilic pollutant and dietary fatty acid studies,as does any potential regional variation in lipids.

Both potential sources of variation, when compar-ing data between animals from different studies,must be estimated, particularly in those samplescollected from live whales obtained with the useof biopsy darts. Sampling by biopsy dart cannotprovide a standardised sampling site and does notpenetrate the whole blubber depth in large whales(Hooker et al., 2001). These samples will notprovide a comprehensive, comparable indicationof blubber lipid content or composition in spermwhales, particularly if the function of the outerlayer of blubber is primarily structural and doesnot provide a good representation of energy stores.In conclusion, it appears that blubber thickness,

when only measured at one site, may not providea comprehensive indication of body fat conditionin sperm whales. The social structure and foragingecology of this species may serve to minimise theneed to rely on stored energy reserves, and blubberlipid content is therefore reflective of an individ-ual’s ability to balance between the acquisition(foraging success) and utilisation of energy(met-abolic and reproductive demands), rather thanbeing directly reflective of energetic demands asso-ciated with reproduction. Further studies involvinglarger number of animals across all age and repro-ductive groups and a larger number of measure-ment sites are required to establish theeffectiveness of blubber thickness as a measure-ment of body fat condition. This would furtherserve to establish the effects of reproductive stateand individual variation on blubber thickness andblubber lipid content. These studies should addi-tionally involve an investigation of blubber lipidcontent throughout the blubber layer and moredetailed investigations into the composition ofblubber fatty acids in an effort to substantiateregional stratification variation and the physiolog-ical functions of this tissue.

Acknowledgments

The authors wish to thank all of the volunteerswho helped with the necropsy of whales andcollection of samples, particularly Margie Morricefor her help in the co-ordination of the collectionand sample archival. Other volunteers wereGraeme McKenzie, John Van den Hoff, MalcolmLambert, Rebecca Pirtzl, Dave Slip, Louise Billett,Graham Robertson, Samantha Lake, Ros Minchin,and Ian Raymond. The Parks and Wildlife Service,Tasmania, particularly Hans Wapstra, kindly


helped with logistics. The Australian AntarcticDivision, particularly Harry Burton, kindly provid-ed storage for samples. Analytical Services Tas-mania, particularly Mike Johnson, Ros Pyrke andAndrew Griffiths, are thanked for their assistancewith laboratory techniques and providing access totheir laboratories and equipment. Corey Bradshawkindly provided assistance with some of the statis-tical analyses and, with two anonymous referees,provided useful comments on earlier drafts of thismanuscript. This study was funded by Environ-ment Australia. Samples were collected under theParks and Wildlife Service Tasmania permit 97y16.

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body fat and condition in sperm whales, physeter macrocephalus, from southern australian waters

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