Journal of Experimental Marine Biology and Ecology 405 (2011) 18–24

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Journal of Experimental Marine Biology and Ecology

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Assessment of nutritional condition indices across reproductive states in the stripeddolphin (Stenella coeruleoalba)

E. Gómez-Campos ⁎, A. Borrell, A. AguilarBiodiversity Research Institute (IrBio), Department of Animal Biology, Faculty of Biology, University of Barcelona, 08028 Barcelona, Spain

⁎ Corresponding author. Tel.: +34 93 402 14 53; faxE-mail address: engomez@ub.edu (E. Gómez-Campo

0022-0981/$ – see front matter © 2011 Elsevier B.V. Adoi:10.1016/j.jembe.2011.05.013

a b s t r a c t

a r t i c l e i n f o

Article history:Received 23 November 2010Received in revised form 12 May 2011Accepted 13 May 2011Available online 2 June 2011

Keywords:BlubberIndicesLipidsNutritional conditionStriped dolphin

The aim of this study was to identify reliable and accurate nutritional condition indices in small cetaceans.Samples from 115 stranded striped dolphins along the eastern coast of Spain (Western Mediterranean) werecollected during two die-off events (1990–1991 and 2007–2008), including animals of different reproductivestates and varying nutritional conditions.We segmented the data according to sex and reproductive condition, because energetic demands varyconsiderably among these collectives, and they were considered a good sample to represent groups withdifferent nutritional conditions.We compared five variables as indices to measure nutritional condition. They were: a) blubber lipid content,b) blubber trunk lipid mass (BTLM), c) muscle/blubber trunk mass ratio, d) maximum girth, and e) blubberthickness.Since the dolphins differed in size, each variable was regressed against standard body length, and the residualsof these regressions were used as indices of nutritional condition. Only the mean residuals of BTLM (pb0.001)and blubber lipid content (p=0.005) varied significantly among reproductive classes. However, the meanresiduals of BTLM appeared to be the most sensitive index of nutritional condition, because it discriminatedbetter among reproductive states.

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1. Introduction

In marine mammals, energy reserves are mostly stored in the formof lipids that accrue in the adipocytes of the blubber. Therefore, it hasbeen assumed that the indices that reflect the relative amount ofblubber in the body, such as blubber thickness, body girth, or otherblubber-related morphometric measurements, are reliable indicatorsof nutritional condition (e.g., Konishi, 2006; Lockyer, 1986; Lockyeret al., 1985). However, this approach is overly simplistic, because themajority of these indices are derived from the assumption thatblubber thickness or blubber mass is directly proportional to changesin lipid mass or, by extension, in body energy stores. Indeed, thisassumptionmay be erroneous inmost cases, because the pressures formarine mammals to preserve the blubber layer are multi-faceted.Aside from serving as a depot of energy, blubber also serves as theprimary thermal barrier, streamlines the body, facilitates hydrody-namic locomotion, contributes to water balance, and provides buoy-ancy (Iverson, 2009). These functions limit the range of acceptablechanges in mass and thickness (Ackman et al., 1965, 1975a, 1975b;Lockyer et al., 1984; Ryg et al., 1988, 1993). Moreover, an additionalfactor that weakens the validity of morphometric data as a reflection

of blubber energy content is the fact that the lipid content of the tissuehas been found to vary independently of its thickness (Ackman et al.,1975a; Aguilar et al., 2007; Dunkin et al., 2005; Evans et al., 2003).

Historically, studies of nutritional or body condition conducted onmarine mammals have focused primarily on pinnipeds and baleenwhales (e.g. Ackman et al., 1975a, 1975b; Aguilar and Borrell, 1990;Arnould, 1995; Konishi, 2006; Lockyer et al., 1984; Pitcher andCalkins, 2000; Worthy and Lavigne, 1983). Conversely, few re-searchers have studied odontocetes, and the results from the studiesthat did assess these animals were not conclusive (Caon et al., 2007;Evans et al., 2003; Kastelein et al., 2002; Lockyer, 1995; Read, 1990).Moreover, some studies suggested the inadequateness of blubberthickness as a good index because it is frequently unrelated to blubberlipid content.

The reproductive cycle is one of the most energy demandingprocesses through the life span of an animal (Lockyer, 2001). Theenergetic cost of reproduction involves both sexes, but it is especiallyevident in the case of females due to pregnancy and lactationdemands. The energetic cost of pregnancy includes fetus production,associated maternal tissues, such as the placenta, and an increase inmetabolism to supply metabolic demands of new tissues (Worthy,2001). A greater amount of energy and nutrients are invested inlactation compared to pregnancy, implying that this state has a majorimpact on maternal energy reserves and nutrient requirements(Oftedal, 1984, 1985). Furthermore, it should be noted that in many

19E. Gómez-Campos et al. / Journal of Experimental Marine Biology and Ecology 405 (2011) 18–24

species, both processes occur simultaneously (e.g., Danil and Chivers,2007; Stephenson and Racey, 1993; Van Waerebeek and Read, 1994;Willig, 1985).

In a population, reproductive condition and seasonal fluctuationsin the availability of food are two factors that significantly affectnutritional condition (Iverson, 2009). During the feeding season,pregnant females usually have the richest nutritional conditionbecause they store energy in anticipation of the future requirementsof raising a calf. Lactating or recent post-lactating females exhibit thepoorest condition, because they are at the end of an extremely highenergy-demanding reproductive cycle. Juveniles of both sexes andmature males usually show intermediate values between these twoextremes. These fluctuations tend to bemore noticeable inmysticetes,because their seasonality in feeding is stronger than in odontocetes(Aguilar et al., 1999; Aguilar and Borrell, 1990; Lockyer, 1987; Oftedal,1997).

In the present study, we analyzed five promising variables asindices of nutritional condition in stranded striped dolphins (Stenellacoeruleoalba) from the coast of eastern Spain (western Mediterra-nean). Since the dolphins differed in size, each variable was regressedagainst standard body length, and the residuals of these regressionswere used as indices of nutritional condition. We investigateddifferences among reproductive states in these indices in order toasses their validity as indicators of nutritional condition.

2. Material and methods

We examined and collected tissues from 115 striped dolphins (60females and 55 males) stranded along the eastern coast of Spain(western Mediterranean) (Fig. 1) during the 1990 (n=97) (Aguilarand Raga, 1993) and 2007 epizootics (n=18) (Raga et al., 2008),including animals of different body sizes and reproductive states.

To minimize potential post-mortem changes in tissue mass orcomposition, only animals with a Smithsonian Institute code of 1 (livestranded animals, aswell as those that died naturally or by euthanasia)or 2 (freshly dead) (Geraci and Lounsbury, 1993) were used. Whenpossible, we recorded standard body length, maximum body girth,blubber thickness, and blubber andmuscle trunkmass for each animal.Blubber thickness was assessed in the medium lateral region at thepoint determined by the end of the flipper when it was folded againstthe body (Fig. 2), and measured as the perpendicular line extendingfrom the skin to the base of the blubber tissue, but not including the

Fig. 1. Map of sample collection sites of strande

skin or any adhering connective tissue at the base. Trunk blubbermasswas measured as that corresponding to the blubber between twoplanes perpendicular to the body axes, one located at the posteriorlimit of the eye and the other at the middle of the anal opening, asshown in Fig. 2. Trunk blubber mass included the skin as well as themass of bothflippers, since itwas difficult to separate the blubber fromthe forelimb bones. Trunk muscle mass was measured as thatcorresponding to the dorsal muscle running along both sides of thevertebral column and between the two above mentioned planes.

A sample of blubber, which included the entire thickness, was alsocollected at the same location at which blubber thickness wasmeasured and preserved at −20 °C to determine the lipid content ofthe tissue. Once in the laboratory, the sample was ground withanhydrous sodium sulfate and extracted with n-hexane in a Soxhletapparatus for 4 h. The solution obtained was concentrated to 40 mland a portion of this extract (10 ml) was used to determine the quan-tity of extractable lipids by gravimetry. The resultswere expressed as apercentage of the tissue wet weight.

Five condition variables were investigated to establish theirvalidity as suitable indices of nutritional condition. These were:

1) Blubber lipid content (%).2) Blubber Trunk Lipid Mass (BTLM), considered as the total amount

of lipids stored in the trunk blubber mass:

BTLMðkgÞ = %lipids in blubber × blubber weight

3) Muscle/blubber trunk mass ratio (M/B ratio), calculated as theratio between the masses of the trunk muscle and the trunkblubber. This index was used to investigate the sequence ofdepletion of lipids vs. protein reserves concomitant with changesin overall body condition. A decrease in this ratio would reflect aloss of protein in relation to blubber, and therefore fastermobilization of energy in this body compartment.

4) Maximum girth (cm), whichwould reflect both changes in blubberthickness and in internal tissues.

5) Blubber thickness (cm).

Since nutritional condition varies between sexes and reproductivestates, we established six categories according to these variables:1) calves, including neonates (90–95 cm, Aguilar, 1991) and in-dividuals up to 1 year. We considered this age range for this categorybecause the lactation period in the striped dolphin lasts for an average

d striped dolphins (Stenella coeruleoalba).

Fig. 2. Diagram showing the limits of the trunk region (between the two planes) asdefined to measure blubber mass and muscle mass (shared area). The red pointindicates where the blubber samples were collected for lipid content analysis andwhere blubber thickness was measured.

Table 1Mean and standard deviations for the five variables considered split by sex andreproductive state.

Reproductive state n Mean±SD

Blubber lipid content (%) Calves 10 63.38±16.08Immature 30 59.13±16.60Pregnant ♀ 5 67.67±13.87Lactating ♀ 26 48.36±13.86Resting ♀ 11 36.43±12.25Mature ♂ 33 46.40±18.57

BTLM (kg) Calves 10 123.11±40.42Immature 30 490.28±180.03Pregnant ♀ 5 936.67±264.97Lactating ♀ 26 555.70±201.86Resting ♀ 11 355.65±132.84Mature ♂ 33 606.97±265.35

M/B ratio Calves 10 0.48±0.17Immature 29 1.02±0.21Pregnant ♀ 5 1.08±0.17Lactating ♀ 26 1.13±0.37Resting ♀ 10 1.35±0.23Mature ♂ 32 1.16±0.23

Maximum girth (cm) Calves 5 47.80±4.97Immature 8 84.75±10.42Pregnant ♀ 3 104.67±6.43Lactating ♀ 3 84.00±12.49Resting ♀ 3 93.33±4.04Mature ♂ 5 95.40±4.78

Blubber thickness (cm) Calves 9 0.87±0.26Immature 26 1.01±0.29Pregnant ♀ 4 1.08±0.05Lactating ♀ 25 1.14±0.39Resting ♀ 10 0.89±0.19Mature ♂ 28 1.10±0.27

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of 16 months (Calzada et al., 1996); 2) immature animals, asidentified by macroscopic examination of reproductive tissues.When this approach was not possible, any animal measuring lessthan 187 cm for females and less than 190 cm for males wasconsidered immature, since these are the mean lengths at sexualmaturation in this population (Calzada et al., 1996); 3) pregnantfemales, established by the presence of a fetus in the uterus. Becausethis was determined by simple visual inspection, an early pregnancywould likely go unnoticed and the individual would be classified asresting; 4) lactating females, as determined by the presence of milk inthe mammary glands; 5) resting females, a category that included allsexually mature females that did not display indications of pregnancyor lactation; and 6) mature males, as determined by histologicalexamination of the testicular tissue or, when that was not possible, bythe length of the individual (see above).

Before analyzing thedata, normalitywas testedwith theKolmogorov–Smirnoff test and the homogeneity of variances was tested with Levene'stest.

Firstly, we investigated possible variations in nutritional conditionvariables with standard body size. Blubber lipid content, M/B ratio,maximum girth, and blubber thickness were regressed against thestandard body length, which is the most common measurement ofbody size in marine mammals (Innes et al., 1981). However, BTLM(measured in kg) was regressed with (standard length)3 in order tomaintain dimensional similarity (Stahl, 1962).

Residuals derived from these regression equations were used asindices of condition, as they showed other biological variations of thecondition variables that were different than those due to body size. Toinvestigate differences in the mean residual values among reproduc-tive categories, each variable was analyzed using ANOVA followed bya post-hoc Tukey test. Statistical significance was considered at a pvalueb0.05 for all analyses. Statistical analyses were carried out usingthe SPSS 15.0 statistical package (IBM, USA).

3. Results

All data sets distributed normally and displayed homogenousvariances (blubber lipid content p=0.570; BTLM p=0.876; M/B ratiop=0.533; maximum girth p=0.113; and blubber thickness p=0.273). Table 1 details the mean and standard deviation for the fivevariables considered split by sex and reproductive state.

The five indices analyzed were significantly correlated withstandard body length independently of sex (pb0.01) (Fig. 3). How-ever, the relationships were different; while blubber lipid contentdecreasedwith standard body length, the other four indices increased.

3.1. Differences in nutritional condition indices among reproductivestates

3.1.1. Blubber lipid contentIn females, themean residuals of blubber lipid content for the different

reproductive states were ranked as follows: pregnantN lactatingNresting(Fig. 4a). Significant differences were only detected between resting and

pregnant females (p=0.007) and between resting females and imma-tures individuals (p=0.018). The lack of significant differences betweenlactating and pregnant females (p=0.140) was probably due to thelimited number of pregnant females (n=5) in the sample, whichprecluded adequate testing. Calves showed the lowest values, except forresting females, although significant differences between them were notdetected.

3.1.2. Blubber trunk lipid mass (BTLM)The trends of mean residual variation in BTLM among reproductive

states were very similar to those shown in the previous index, but thedifferences were larger and the standard deviations were smalleramong groups (Fig. 4b).

Pregnant females showed significantly higher values of BTLMresiduals than all other groups (pb0.009). Resting females showedlower values of BTLM residuals than all other groups (pb0.05), withthe exception of calves. Although calves showed the lowest values forBTLM residuals, no significant differences were detected with theother groups.

3.1.3. M/B ratioNo significant differences in the residuals of M/B ratio were found

among the categories considered (Fig. 4c; p=0.276).

3.1.4. Maximum body girthNo significant differences in the residuals of maximum body girth

were found among the categories considered (Fig. 4d; p=0.058). Asshown in Fig. 4d, pregnant females seemed to have a higher valuethan the other groups. However, the reduced number of pregnantfemales was most likely the reason for not detecting a differencebetween the groups.

3.1.5. Blubber thicknessNo significant differences in the residuals of blubber thickness

were found among the categories considered (Fig. 4e; p=0.335).

Fig. 3. Relationships between the variables assessed and standard body length (m) or (standard body length)3 (m3) in order to maintain dimensional similarity. Open circlesrepresent males and solid circles represent females.

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4. Discussion

The five variables explored in the present study showed a significantrelationship with animal body length independent of the sex. Whereasthe blubber lipid content significantly declined with body size, theremaining four indices increasedwith blubber lipid content (Fig. 3). Theincreases in BTLM, blubber thickness, and maximum girth with body

size were as expected, since all of these parameters are related to bodymorphometrics.

The inverse relationship between the blubber lipid content andstandard body length is not simple and is in contrast with studies onterrestrial mammals, which have shown that old animals are typicallyfatter than young animals (Allen, 1984; Moulton, 1923; Pond, 1978;Schulte-Hostedde et al., 2001). However, the blubber lipid content has

Fig. 4.Mean residuals and standard deviation of nutritional condition indices by sexes and reproductive state. Letters on top depict homogeneous statistical subgrouping by ANOVA.

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been shown to decrease in many cetacean species in a similar mannerto that observed in this study, including fin whales (Balaenopteraphysalus) (Aguilar and Borrell, 1990), common dolphins (Delphinusdelphis) (Tornero et al., 2006), harbor porpoises (Phocoena phocoena),and several populations of bottlenose dolphins (Tursiops truncatus)(Dunkin et al., 2005; Montie et al., 2007; Tornero et al., 2005).Conversely, no variation in blubber lipid content was found betweenyoung and adult dolphins of sperm whales (Physeter macrocephalus)(Evans et al., 2003) or in franciscana (Pontoporia blainville) (Caonet al., 2007).

Young dolphins, due to their small size, expose a larger surface areato the environment in relation to their volume compared to largeranimals, which suggests a higher degree of heat loss (Dunkin et al.,

2005, McLellan et al., 2002, Montie et al., 2007; Worthy and Edwards,1990). Thus, the increased blubber lipid content in immature animalscompared to adults may address the need for a more efficient thermalbarrier in addition to other functions, such as the gain in positivebuoyancy and extra energy reserves (Dearolf et al., 2000; McLellanet al., 2002; Read, 1990). This finding supports the hypothesis thatlarge dolphins have less of a demand for insulation because the surfacearea to volume ratio decreaseswith growth, and consequently blubberis less enriched in lipids. However, an additional explanation for thistrend could be that immature marine mammals show a feeding ratethat is noticeably greater than mature animals (Tanabe, 1999). Thedecrease in feeding rate with age most likely contributes to less lipidstorage in the blubber of older animals.

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TheM/B ratio is not directly related to dolphinmorphometrics, butwas shown to increase with body length in both females and males(pb0.001) (Fig. 4). This increment suggests that the blubber in smalldolphins has a larger contribution to body mass than the internalmuscle core does as a result of the higher surface are to volume ratioof small dolphins compared to larger dolphins (Lockyer, 1995).

4.1. Differences in nutritional condition indices among reproductivestates

4.1.1. Blubber lipid content and BTLMAmong the proposed variables, only the mean residuals of BTLM

and blubber lipid content were able to discriminate reproductivestates. With variable sensitivity, both described changes wereobserved in females throughout the reproductive cycle. This suggeststhat these variables are appropriate indices of nutritional condition,because the reproductive cycle in females appears to be an importantfactor for determining nutritional condition. Therefore, fatteningduring gestation is a typical physiological response that allowsfemales to store large reserves of energy before delivery with theobjective of safeguarding the reproductive investment and ensuringan adequate energy transfer to the calf during lactation (Friggens,2003; Pond, 1984). According to this hypothesis, pregnant femalesdisplayed the best nutritional condition (higher mean residuals ofblubber lipid content and BTLM). This result is consistent with thatfound in other cetaceans as well as in other species of large mammals(Aguilar and Borrell, 1990; Atkinson and Ramsay, 1995; Gerhart et al.,1997; Harlow et al., 2002; Lockyer, 1986; Montie et al., 2007).

However, the bulk of the energy transfer to the calf takes placeduring lactation, which is reflected by both the progressive depletionof energy stores in the lactating females and the concomitant trend ofincreased lipid stores observed in calves. Furthermore, lactation is themost energetically demanding stage in the life cycle of mammals, andusually has a 3–5 fold greater energy cost than that of gestation(Gittleman and Thompson, 1988; Kastelein et al., 2002; Young, 1976).Accordingly, the mean residuals of blubber lipid content and BTLMhad the lowest values in these females as well as resting females(Fig. 4). The results obtained in this study support the widespread andaccepted theory that the deposition of lipids (increasing blubber lipidcontent) is associated with pregnancy, while the mobilization oflipids (decreasing blubber lipid content) is associated with lactation(Aguilar and Borrell, 1990; Gittleman and Thompson, 1988; Montieet al., 2007).

Although resting females did not differ significantly in the meanresiduals of blubber lipid content compared to lactating females,differences were observed in the mean residuals of BTLM (p=0.043).We expected that those indices indicated that the nutritional con-dition in resting females would be better than that in lactatingfemales, because resting females should be recovering from gestationand lactation processes (Fig. 4). However, the resting group showedthe lowest values for BTLM and blubber lipid content among all of thegroups. This finding suggests that the resting group is composed ofpost-lactating females that are still in a poor nutritional condition dueto the gestation and long lactation period, which extends for morethan 1 year in the striped dolphins. In addition, some females of thisgroup could have a poor nutritional condition, which prevented themfrom having a normal reproductive cycle.

The mean residuals of blubber lipid content and of BTLM showedthat the calves of the striped dolphin presented the lowest nutritionalcondition (with the exception of those from resting females, Fig. 4).This finding can be easily explained, since at birth, calves show apoorly developed blubber layer that increases rapidly during thesuckling phase in preparation for nutritional stress at weaning. Similarto the results obtained here, Lockyer (1995) found that the lowestblubber lipid levels occurred in neonates and yearling harbor por-poises compared to older animals.

4.1.2. M/B ratioThe M/B ratio was a variable designed to investigate the sequence

of depletion of protein vs. lipid reserves concomitantlywith changes inoverall body condition. In mammals, energy is stored in the form oflipids, proteins, or carbohydrates. The energetic density of each ofthese materials is inversely proportional to its readiness to bemetabolized and produce energy based on the descending order oflipidsNproteinsNcarbohydrates. Consequently, fat is the main bodytissue for long-term energetic storage, while carbohydrates are themost immediate and accessible source of energy that are used to covershort-term needs (Hill et al., 1987). However, blubber, which is themain fat reservoir in marine mammals, has additional functions. Inorder to preserve this tissue, the required energy in undernourishedanimals could be obtained from other compartments, such as muscle,as observed in some terrestrial mammals and birds (Barboza andParker, 2008; Boismenu et al., 1992). Our hypothesis was that adecrease in the M/B ratio would reflect the mobilization and loss ofprotein (muscle) in relation to blubber. However, no significant dif-ferences in residuals of M/B ratio were found among the reproductivecategories considered. Thus, we concluded that this index was notappropriate to measure nutritional condition in the striped dolphin,and furthermore, no protein mobilization was initiated to supplyenergy during periods of high demand, such as pregnancy or lactation.

4.1.3. Maximum body girth and blubber thicknessThe maximum body girth and blubber thickness residuals did not

provide any advantage for the discrimination of female reproductivestates in the striped dolphin. Blubber thickness, different girths,and other morphometric measurements along the body axis of theanimals have been utilized as suitable indices to assess nutritionalcondition. These indices are widely accepted and are currently in use,especially for baleen whales and pinnipeds (Konishi, 2006; Lockyeret al., 1985; Naess et al., 1998; Pitcher, 1986; Pitcher and Calkins,2000). However, in odontocetes, aside from the relationship estab-lished between blubber thickness and reproductive state in the harborporpoise (Phocoena phocoena) (Koopman, 1998), these parametershave not always successful results (Caon et al., 2007; Evans et al.,2003; Lockyer, 1995; Read, 1990). Currently, there are reservationsregarding their reliability to accurately reflect the nutritional con-dition of each individual. Various evidences have shown that theseindices are biased, not sensitive, characterized by intrinsic errors ofmeasurement, and lack a correlation with changes in overall body fatreserves (Aguilar et al., 2007).

The maximum girth and blubber thickness residuals showed novariation among reproductive states. Therefore, these conditionvariables are inadequate tools for assessing variation in the nutritionalcondition of striped dolphins among groups with clear differences inenergy requirements.

5. Conclusions

Among the five variables investigated here, BTLMprovided themostaccurate reflection of nutritional condition in the striped dolphin. Itvaried significantly among reproductive states with different energydemands, such as pregnancy or lactation. Blubber lipid content alsovaried among reproductive categories, but was not as accurate as BTLM.In addition, the M/B ratio, maximum girth, and blubber thickness failedto reflect the nutritional condition of the striped dolphin.

Acknowledgments

We are grateful to all who collaborated in the necropsy work.While doing this research, E. Gómez-Campos was supported by a FPIdoctoral fellowship from the Ministry of Science and Education ofSpain. The study was funded by the Programa Nacional de Biodiversi-dad, Ciencias de la Tierra y Cambio Global of the Ministry of Science and

24 E. Gómez-Campos et al. / Journal of Experimental Marine Biology and Ecology 405 (2011) 18–24

Education of Spain (project CGL2005-00922/BOS). We thank the “Zoode Barcelona”, Ajuntament de Barcelona, for financial support. [SS]

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