Journal of Mammalogy, 90(3):629–637, 2009 BLUBBER DEPOSITION DURING ONTOGENY IN FREE-RANGING BOTTLENOSE DOLPHINS: BALANCING DISPARATE ROLES OF INSULATION AND LOCOMOTION SHAWN R. NOREN* AND RANDALL S. WELLS Institute of Marine Science, Center for Ocean Health, University of California, Santa Cruz, CA 95060, USA (SRN) Chicago Zoological Society, c/o Mote Marine Laboratory, Sarasota, FL 34236, USA (RSW) Key words: blubber, buoyancy, cetacean, cost of descent, development, dolphin, marine mammal, morphology, thermoregulation, surface-area-to-volume ratio Marine mammals contain a specialized hypodermis called blubber (Parry 1949), which is a layer of lipid-rich tissue between the epidermis and the underlying muscles. Blubber is a critical component of mammalian adaptations to the aquatic environment, as evidenced by the fact that it has evolved in parallel in cetaceans (whales, dolphins, and porpoises) and pinnipeds (seals, sea lions, and walrus). Marine mammals have a large investment in the structure and maintenance of blubber, which can constitute 15–55% of body mass (e.g., McLellan et al. 2002; Ryg et al. 1993). Unlike pinnipeds, cetaceans do not have fur or hair, thus the blubber layer provides the primary insulation for these animals by decreasing heat flow from the body core to the external environment (Dunkin et al. 2005; Worthy and Edwards 1990). Insulation via blubber may be particularly important in young cetaceans. Cetaceans are born in water, which conducts heat away from a body 25 times faster than air at the same temperature (Parry 1949; Schmidt-Nielsen 1997; Scholander et al. 1950). This heat loss is exacerbated by the relatively small body size of young dolphins, which results in larger surface area to volume ratios than in adult conspecifics, promoting heat loss to the environment (Dunkin et al. 2005). This scaling constraint may be further confounded by underdeveloped thermoregulatory characteristics. For example, in most terrestrial mammals fat accumulates postparturition and continues to increase with age (Adolph and Heggeness 1971), providing for increased cold tolerance with age (Mount 1979). Similarly, the insulative layer of cetaceans increases after birth; fetal and neonatal dolphins (Dunkin et al. 2005; Struntz et al. 2004), porpoises (Lockyer 1995), and whales (Blix and Steen 1979) have thinner blubber than adult conspecifics. In addition, lipid content increases steadily from fetal through juvenile (,1 year old) life-history stages (Dunkin et al. 2005). As a result of ontogenetic changes in blubber morphology and composition, the thermal insulation of dolphin blubber, a measure of blubber quality (i.e., conductivity) and quantity (i.e., thickness), increases 3-fold from fetal to subadult life-history stages (Dunkin * Correspondent: snoren@biology.ucsc.edu Ó 2009 American Society of Mammalogists www.mammalogy.org 629 Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 Blubber is a critical component of thermoregulation for marine mammals, particularly for cetaceans. However, the cost of overcoming blubber’s buoyant force during descent could constrain blubber deposition. One- to 12-year-old healthy, free-ranging common bottlenose dolphins (Tursiops truncatus) were studied in Sarasota Bay, Florida, during summer (mean water temperature: 29.78C 6 0.1 SE) and winter (mean water temperature: 19.2 6 0.48C) to examine ontogenetic and seasonal trends in morphology and blubber deposition. Surface-areato-volume ratio decreased significantly with age. During summer, yearlings had significantly thicker blubber than 2- to 12-year-old animals but this difference diminished by winter because blubber deposition in response to the colder water temperature was smaller in yearlings (2-mm increase) compared to 2- to 12-year-old animals (3- to 6-mm increase). During summer, buoyancy was highest in yearlings (6.24 N 6 0.41 SE), compared to a buoyant force of 0.98 6 0.90 N (neutrally buoyant) for 12-year-old animals. Conversely, all dolphins converged upon a similar buoyant force (8.01 6 0.56 N) in winter. The elevated buoyancy of yearlings in summer presumably limits seasonal blubber adjustments, because all yearlings (regardless of season) converged upon a similar calculated mass-specific cost of descent that was greater than all other age classes. Balancing energetic demands of thermoregulation and locomotion may limit the flexibility of yearlings to adjust blubber deposition in response to fluctuating water temperatures. 630 JOURNAL OF MAMMALOGY MATERIALS AND METHODS Animals.— This research on wild dolphins met guidelines approved by the American Society of Mammalogists (Gannon et al. 2007), was approved by an institutional animal care and use committee, and was conducted under a series of scientific research permits issued by the National Marine Fisheries Services. Wild common bottlenose dolphins (age: 1–12 years) in a long-term, multigenerational resident community of approximately 150 individuals near Sarasota, Florida, were sampled as part of an ongoing health assessment program. The long-term study of this population has spanned more than 5 generations (Wells 1991a, 2003). Individuals were identifiable from dorsal fin markings, and ages of known dolphins were determined from monitoring mothers and calves through time (Scott et al. 1990). For older, unidentified animals, a tooth was examined for age determination following the methods of Hohn et al. (1989). The capture–release program involving this population allowed for morphological measurements to be taken while each dolphin was held temporarily for veterinary examination and sampling; details of the program are described elsewhere (Wells et al. 2004). Morphological measurements included body mass, girths, segmental lengths, and blubber thicknesses. These measurements were taken from 65 animals over 10 winter field seasons (November, December, January, or February, 1986–1989, 1993–1994, 2002–2005; mean water temperature ¼ 19.28C 6 0.4 SE) and 258 animals over 21 summer field seasons (June or July, 1984–1995, 1997–2005; mean water temperature ¼ 29.7 6 0.18C). Morphology and measurements of blubber thickness.— Morphological measurements were taken while the dolphins were resting quietly in a boat. Body mass was determined using a digital scale (Western Scale DF 2000 Indicator, Western Scale Company Limited, Port Coquitlam, British Columbia, Canada). Body length was measured as the straight-line body length from rostrum to fluke notch, and blubber thickness was measured at the thoracic–abdominal area (center of flank directly below dorsal fin) using a portable ultrasound unit (Scanoprobe II; Scanco, Ithaca, New York). These methods were adapted from Wells (1991a, 1993). Interage and interseason comparisons of blubber thickness were made at the thoracic–abdominal site because this is the standard site used to show variability among age and reproductive classes in cetaceans (Koopman 1998). Additional measurements of girth (taken at the nuchal crest, axilla, anterior dorsal fin, posterior dorsal fin, and anus), blubber thickness (measured every 10 cm along each girth on the left side of the body), and segmental lengths (between each girth measurement along the entire body length) were recorded from a subset of these animals (summer n ¼ 73 and winter n ¼ 21) so that surface area, volume, and blubber mass could be determined. Calculations.— Surface area and total body volume, excluding appendages (fins and flukes), were determined by standard geometric equations for a series of truncated cones following methods of Gales and Burton (1987). It was not possible to measure appendage surface area in the wild bottlenose dolphins. Therefore, to account for appendage surface area, measurements of flukes and fins were taken from a captive bottlenose dolphin population (The Dolphin Experience, Grand Bahama Island, Bahamas). The animals represented an age range of 1.7 years to adult. We have observed that regardless of age, extremity surface area represented approximately 19% of total body surface area. Thus, surface area for the wild dolphins was corrected to include extremity surface areas using this 19% correction factor; the reported surface-area-to-volume ratios use these corrected surface area values. The blubber volume for each body segment was calculated using the average blubber thickness for the body segment, which was determined from the series of blubber thickness measurements taken along each of the 2 girths defining the body segment. The blubber volumes of each segment were then summed to determine the total blubber volume for the dolphin, following the methods of Gales and Burton (1987). Blubber mass was calculated by multiplying total blubber volume by the density of bottlenose dolphin blubber (0.969 g/cm3—Kipps et al. 2002). The same value for blubber density was used for all dolphins in this study because the density of bottlenose dolphin blubber is similar across life-history stages (fetal through adult—Dunkin 2004). The proportion of the body composed of blubber was calculated by dividing blubber mass by total body mass. Buoyancy was calculated from adaptations of the equations in Skrovan et al. (1999) and Webb et al. (1998): Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 et al. 2005). Interestingly, the thermal conductivity of dolphin blubber, which is independent of thickness, remains stable across these stages (Dunkin et al. 2005). These results suggest that neonatal blubber is not specialized to provide enhanced insulation, but rather that fetal, neonatal, and juvenile lifehistory stages represent a period of continual blubber growth (Dunkin et al. 2005). The blubber layer also serves to streamline the body (Hamilton et al. 2004; Pabst 2000), provide a metabolic energy storage site (Aguilar and Borrell 1991; Koopman et al. 1996, 2002; Struntz et al. 2004), provide some measure of protection from the full effect of a predator bite or other trauma such as a boat strike (Wells 1993; Wells et al. 2008), and contribute to buoyancy (Dearolf et al. 2000; Kipps et al. 2002; McLellan et al. 2002; Webb et al. 1998). Given that blubber is multifunctional and dynamic, it is likely that multiple factors influence blubber deposition patterns. We explored the effects of ontogeny (body size) and thermal demands (season) on blubber deposition and the influence of blubber deposition on buoyancy and the resulting cost of descent in common bottlenose dolphins (Tursiops truncatus). We used a unique long-term data set across age classes and seasons taken from live, presumably healthy, wild dolphins in Sarasota Bay, Florida. Marine mammal species serve as models for quantifying adaptation to extreme environments, and immature animals can provide clues to limitations in thermoregulatory characteristics. Ultimately, our study will increase our understanding of the thermal lability of mammals. Vol. 90, No. 3 June 2009 NOREN AND WELLS—BLUBBER DEPOSITION IN BOTTLENOSE DOLPHINS 631 BT ¼ ð1:0228  0:60V  gÞ þ ð0:5568  MT  AÞ FIG. 1.—Surface-area-to-volume ratio (SA:VOL) in relation to age for bottlenose dolphins (Tursiops truncatus). Points represent means 6 1 SEM for summer (black circles) and winter (white circles). Sample sizes are denoted in parentheses for age classes with .1 sample. Age and surface-area-to-volume ratio were significantly correlated according to a nonlinear relationship. The solid and dashed lines represent this relationship during summer (SA:VOL ¼ 20.07 age0.13, F ¼ 266.56, d.f. ¼ 1, 10, P , 0.0001) and winter (SA:VOL ¼ 20.38 age0.16, F ¼ 80.767, d.f. ¼ 1, 9, P , 0.0001), respectively. Slopes and intercepts were similar across seasons. See text for statistics. parameters were used in these analyses so that each age class contributed equally. The significance of these relationships was determined using an F-test. The relationships for age versus surface-area-to-volume ratio, proportion of blubber, and massspecific cost of descent were significant within both seasons; thus, t-tests were used to compare the slopes and intercepts for these relationships across seasons. Meanwhile, the relationship for age versus buoyancy was only significant in summer; therefore, within–age-class comparisons across seasons were made using Student’s t-tests. Means are reported 61 SEM. Sigma Plot and Sigma Stat (Jandel Scientific, San Rafael, California) were used for all statistical analyses, and results were deemed significant at P , 0.05, with the exception that Student’s-t tests or Mann-Whitney rank sum tests for age-class comparisons of thoracic–abdominal blubber thickness were deemed significant at P , 0.10 because of limited sample sizes. RESULTS Surface-area-to-volume ratio showed a significant nonlinear decrease with age both during summer and winter (Fig. 1). This suggests that yearlings have a theoretically greater propensity for heat loss compared to older age classes. The slopes (t ¼ 1.554, d.f. ¼ 21, P ¼ 0.135) and intercepts (t ¼ 0.482, d.f. ¼ 21, P ¼ 0.635) for these relationships were similar across seasons. A potential means of countering heat loss is to increase blubber deposition. Blubber deposition in the thoracic– abdominal region was significantly different across age classes during summer (H ¼ 17.969, d.f. ¼ 11, P ¼ 0.082), but not Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 þ ð0:6689  MT  LÞ; ð1Þ where BT is total buoyancy (N), V is lung volume, g is acceleration due to gravity (9.81 m/s2), MT is total body mass (kg), A is percentage of adipose tissue, and L is percentage of lean tissue. Unlike seals, dolphins dive on inspiration, thus the equation takes into account the buoyancy of the diving lung volume. According to Kooyman (1989), the diving lung volume of marine mammals is approximately 60% of total lung volume (V), where V ¼ 0.1MT0.96. For each dolphin, the percentage composed of adipose tissue was assumed to be the percentage of body mass composed of blubber based on the total blubber volume calculation; the remainder of body mass was assumed to represent lean tissue. The constant 1.0228 is the difference between the density of salt water and air at 208C and 1 atm. The constant 0.5568 assumes an adipose density of 0.969 g/cm3 for bottlenose dolphins (Kipps et al. 2002). The constant 0.6689 is based on a lean density of 1.07 g/cm3 for seals (Nordøy and Blix 1985) because similar data are not available for cetaceans. The cost of descent, specifically the mass-specific locomotor costs (J/kg) associated with overcoming buoyancy on a 10-m dive, was calculated for each dolphin by multiplying the distance traveled (m) by the dolphin’s buoyant force (N) divided by body mass (kg; adapted from Skrovan et al. 1999). A relatively shallow dive (10 m) was chosen for comparison because immature dolphins have limited diving capacity (Noren 2002, 2004; Noren et al. 2001, 2002, 2004) and thrust for swimming (Noren et al. 2006) because of developmental factors. In addition, we have observed that the average depth utilized by Sarasota Bay dolphins is 3.8 m 6 2.9 SD, with a maximum of only 9.97 m. Statistics.—Thoracic–abdominal blubber thicknesses across sexes within age class and season were compared using Student’s t-tests or Mann-Whitney rank sum tests when normality failed. The majority of comparisons showed no significant differences between the sexes (exceptions were 7-year age class in summer: T ¼ 58.00, n ¼ 8, 13, P ¼ 0.032; 12-year age class in summer: t ¼ 3.528, d.f. ¼ 7, P ¼ 0.010; 5-year age class in winter: t ¼ 2.997, d.f. ¼ 4, P ¼ 0.040 ; 9- to 12-year age classes in winter had too few samples for cross-sex comparisons), therefore, data across sexes within seasonal age class were combined for all analyses. Age-class thoracic– abdominal blubber thicknesses within season were compared using 1-way analysis of variance (ANOVA) for summer and 1-way ANOVA on ranks for winter because normality failed; subsequently Student’s t-tests or Mann-Whitney rank sum tests were used for age-class comparisons within season. Within– age-class comparisons of thoracic–abdominal blubber thickness across seasons also were compared using Student’s t-tests or Mann-Whitney rank sum tests. Nonlinear regression analyses were used to assess the relationship of age with surface-area-to-volume ratio, proportion of blubber, buoyancy, and mass-specific cost of descent independently for each season (summer and winter); age-class means for these 632 JOURNAL OF MAMMALOGY Vol. 90, No. 3 TABLE 1.—Blubber deposition in the midthoracic region was significantly different across age classes measured during summer. Yearling age class had significantly thicker blubber than 2- to 11-year-old animals. No other age-class comparisons were significant (NS). 1 2 3 4 5 6 7 8 9 10 11 12 1 — NS NS NS NS NS NS NS NS NS NS NS t ¼ 2.814 d.f. ¼ 29 P ¼ 0.009 NS — NS NS NS NS NS NS NS NS NS t ¼ 1.815 d.f. ¼ 29 P ¼ 0.080 NS NS — NS NS NS NS NS NS NS NS T ¼275.5 n ¼ 10, 29 P ¼ 0.016 NS NS NS — NS NS NS NS NS NS NS t ¼ 3.852 d.f. ¼ 21 P , 0.001 NS NS NS NS — NS NS NS NS NS NS T ¼213.5 n ¼ 10, 21 P ¼ 0.025 NS NS NS NS NS — NS NS NS NS NS t ¼ 3.678 d.f. ¼ 21 P ¼ 0.001 NS NS NS NS NS NS — NS NS NS NS t ¼ 1.783 d.f. ¼ 18 P ¼ 0.091 NS NS NS NS NS NS NS — NS NS NS t ¼ 1.975 d.f. ¼ 17 P ¼ 0.065 NS NS NS NS NS NS NS NS — NS NS t ¼ 1.828 d.f. ¼ 16 P ¼ 0.086 NS NS NS NS NS NS NS NS NS — NS NS 2 3 4 5 6 7 8 9 10 11 12 t ¼ 4.166 d.f. ¼ 36 P , 0.001 — NS NS NS NS NS NS NS NS NS NS during winter (F ¼ 1.288, d.f. ¼ 11, 60, P ¼ 0.259). During summer, yearlings had significantly thicker blubber than 2- to 11-year-old animals; no other age-class comparisons were significant (Table 1; Fig. 2). Blubber deposition also differed seasonally; for all age classes blubber was thinner in summer compared to winter (1 year old: t ¼ 3.025, d.f. ¼ 18, P ¼ 0.007; 2 years old: T ¼ 150.000, n ¼ 5, 28, P ¼ 0.001; 3 years old: t ¼ 4.577, d.f. ¼ 23, P , 0.001; 4 years old: t ¼ 3.697, d.f. ¼ 26, P ¼ 0.001; 5 years old: T ¼ 187.00, n ¼ 6, 29, P , 0.001; 6 years old: t ¼ 4.330, d.f. ¼ 16, P , 0.001; 7 years old: T ¼ 115.00, n ¼ 5, 21, P ¼ 0.002; 8 years old: T ¼ 61.00, n ¼ 4, 13, P ¼ 0.005; 9 years old: t ¼ 3.194, d.f. ¼ 10, P ¼ 0.010; 10 years old: t ¼ 1.852, d.f. ¼ 9, P ¼ 0.097; FIG. 2.—Thoracic–abdominal blubber thickness in bottlenose dolphins (Tursiops truncatus). Points represent means 6 1 SEM for summer (black circles) and winter (white circles). Sample sizes are denoted in parentheses. The asterisk denotes that during summer the blubber of yearlings was significantly thicker than that of 2- to 11year-old animals; no other age-class differences were found. During winter, all dolphins had similar blubber thicknesses regardless of age. See Table 1 for statistics. Seasonal comparisons showed that for all age classes, blubber was significantly thicker during winter compared to summer. See text for statistics. NS NS NS NS NS NS NS NS NS NS — 11 years old: t ¼ 6.047, d.f. ¼ 10, P , 0.001; 12 years old: t ¼ 3.330, d.f. ¼ 14, P ¼ 0.005). In general, yearlings demonstrated small seasonal adjustments in blubber, with only a 2-mm increase in thoracic–abdominal blubber from summer  ¼ 5 6 0.3 mm) to winter compared to a 3- to 6-mm increase (X found for 2- to 12-year-old animals. Proportion of blubber, buoyancy, and mass-specific cost of descent were correlated with age (Figs. 3–5). All variables showed a significant nonlinear decrease with age, with the exception of buoyancy during winter months. Thus, seasonal comparisons of slopes and intercepts for proportion of blubber FIG. 3.—Proportion of blubber (percentage of total body mass) in relation to age for bottlenose dolphins (Tursiops truncatus). Points represent means 6 1 SEM for summer (black circles) and winter (white circles). Sample sizes are denoted in parentheses for age classes with .1 sample. Age and proportion of blubber were significantly correlated according to a nonlinear relationship. The solid and dashed lines represent this relationship during summer (proportion of blubber ¼ 20.09 age0.16, F ¼ 229.980, d.f. ¼ 1, 10, P , 0.0001) and winter (proportion of blubber ¼ 22.93 age0.10, F ¼ 17.026, d.f. ¼ 1, 9, P ¼ 0.003), respectively. Slopes and intercepts across seasons were significantly different. See text for statistics. Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 Age June 2009 NOREN AND WELLS—BLUBBER DEPOSITION IN BOTTLENOSE DOLPHINS and mass-specific cost of descent were conducted, whereas a similar analysis for buoyancy was not possible. The slopes (t ¼ 2.395, d.f. ¼ 21, P ¼ 0.026) and intercepts (t ¼ 2.964, d.f. ¼ 21, P ¼ 0.007) for age versus proportion of blubber across seasons were different, suggesting that the proportion of blubber changes markedly with season (Fig. 3). Yearlings only had a small seasonal increase in proportion of blubber from summer to winter (1%) compared to the 2–5% increase found for 2- to 12-year-old animals. A result of ontogenetic and seasonal change in the proportion of blubber is change in buoyancy. However, buoyancy was only significantly correlated with age for dolphins measured during summer months (Fig. 4). All dolphins measured during winter months  ¼ 8.01 6 0.56 converged upon a similar buoyant force (X N) that surpassed the buoyant force of dolphins during summer months as evident by intra–age-class seasonal comparisons (1 year old: t ¼ 3.701, d.f. ¼ 7, P ¼ 0.008; 4 years old: t ¼ 2.983, d.f. ¼ 7, P ¼ 0.020; 5 years old: t ¼ 4.069, d.f. ¼ 12, P ¼ 0.002; 12 years old: t ¼ 2.668, d.f. ¼ 6, P ¼ 0.037; limited winter samples precluded additional age-class comparisons; Fig. 4). Yearlings had the smallest seasonal difference in buoyancy (Fig. 4), which is consistent with this age group’s convergence upon a similar mass-specific cost of descent across seasons (t ¼ 1.501, d.f. ¼ 7, P ¼ 0.177; mean yearling mass-specific cost of descent ¼ 0.97 6 0.05 J; Fig. 5). In addition, the intercepts for age- versus mass-specific cost of descent across seasons were similar (t ¼ 1.785, d.f. ¼ 21, P ¼ 0.089). Meanwhile, the slopes for these relationships were different between summer and winter (t ¼ 3.352, d.f. ¼ 21, FIG. 5.—Mass-specific cost of descent (COD) associated with overcoming buoyancy for a 10-m dive. Points represent means 6 1 SEM for summer (black circles) and winter (white circles). Sample sizes are denoted in parentheses for age classes with .1 sample. Age and mass-specific cost of descent were significantly correlated according to a nonlinear relationship. The solid and dashed lines represent this relationship during summer (mass-specific COD ¼ 0.94 age1.16, F ¼ 65.398, d.f. ¼ 1, 10, P , 0.0001) and winter (massspecific COD ¼ 1.31 age0.44, F ¼ 22.315, d.f. ¼ 1, 9, P ¼ 0.001), respectively. Slopes across seasons were different, whereas intercepts across seasons were similar. See text for statistics. P ¼ 0.003). These results indicate that with the exception of yearlings, age-specific cost of descent varies with season. DISCUSSION As a group, cetaceans have relatively low surface area for their body size compared to terrestrial mammals of similar size. For bottlenose dolphins, we have observed that total body surface area is only 67–87% of the surface area predicted by Brody (1945) for terrestrial animals of similar body size (see also Ridgway 1972). Similarly, Kasting et al. (1989) determined that the surface areas for beluga and killer whales only represented 63–91% of that predicted by Brody (1945). This adaptation in cetaceans likely minimizes heat loss from the body to the highly conductive marine environment. However, the same thermal advantage may not be afforded to immature cetaceans. Compared to adults, young cetaceans have small body sizes that result in relatively high surface area to volume ratios (Fig. 1). Without appropriate insulation, immature animals will theoretically lose comparatively more body heat to the environment than adult conspecifics. A thick blubber layer in cetaceans is the primary thermal adaptation that insulates against heat loss to the water (Kanwisher and Sundnes 1966). Therefore, dolphin calves and yearlings may rely on intrinsically greater amounts of blubber to decrease relatively high rates of heat loss to the environment due to proportionately greater body surface area. However, this does not appear to be the case for newborn cetaceans. Although we were unable to measure the blubber thicknesses of fetal and neonatal bottlenose dolphins, previous Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 FIG. 4.—Buoyancy in relation to age for bottlenose dolphins (Tursiops truncatus). Points represent means 6 1 SEM for summer (black circles) and winter (white circles). Sample sizes are denoted in parentheses for age classes with .1 sample. During summer, age and buoyancy was significantly correlated according to the nonlinear relationship shown by the solid line (buoyancy ¼ 7.12 age1.05, F ¼ 18.376, d.f. ¼ 1, 10, P ¼ 0.002). In contrast, buoyancy was not correlated with age during winter (F ¼ 0.431, d.f. ¼ 1, 9, P ¼ 0.528). The dashed line represents the mean buoyancy across all age classes in winter (8.01 6 0.56 N). 633 634 JOURNAL OF MAMMALOGY may be the confounding factor that alterations in blubber thickness affect buoyancy. In marine mammals, buoyancy is determined by the ratio of adipose to lean body tissue and by the overall mass of the animal. For animals of equal size, the animal with a higher ratio of blubber to lean tissue is more buoyant, whereas for animals of similar body composition, the smaller animal is more buoyant (Beck et al. 2000; Biuw et al. 2003; Webb et al. 1998). In consequence, individuals of the same species that are positively buoyant must expend more energy to maintain position in the water column than individuals that are neutrally buoyant (Lovvorn and Jones 1991), and it has been demonstrated that diving bottlenose dolphins increase energy expenditure with the work of overcoming buoyancy (Skrovan et al. 1999). Regardless of season, the youngest, smallest age class (yearlings) had the highest proportion of blubber (Fig. 3) and resulting buoyant force (Fig. 4). The minute seasonal blubber adjustments in these young dolphins suggests that blubber deposition may have been limited by a maximum buoyant force (9.22 6 0.52 N; Fig. 4) and the associated locomotor costs to overcome this force while diving to 10 m (1.02 6 0.05 J/kg; Fig. 5). Given that yearlings are increasingly reliant on foraging at depth for energy intake (Wells 1991b), limits to costs of descent may be set by the inability of yearlings to produce large amounts of thrust for swimming (Noren et al. 2006) due to diminutive body size and underdeveloped locomotor muscles (Dearolf et al. 2000; Noren 2002, 2004; Noren et al. 2001). In contrast, positive buoyancy may be considered adaptive for neonatal dolphins (Dearolf et al. 2000) to compensate for extremely limited swimming capabilities (Noren et al. 2006), because neonates do not forage, being completely reliant on nursing for energy intake (Wells 1991b). Thus, yearlings may have the most difficulty balancing the energetic demands of thermoregulation and locomotion. Admittedly, our calculations of buoyancy and the resulting cost of descent only provide deductive estimates because these values were not measured directly. We assumed that all tissue that was not blubber was lean tissue, for which we used 1 density value; we did not take into account possible differences in the densities of muscle, bone, and organ. If bone and organ densities are higher than that of muscle then the buoyancy of the animal would be decreased. Conversely, the positive buoyancy of gaseous intestines also was not accounted for; this would serve to increase the buoyancy of the animal (Kipps et al. 2002). Thus, the magnitude of the actual buoyant force of the dolphins may be different than the values presented in this study. Nonetheless, given that the density of bottlenose dolphin blubber is similar across life-history stages (fetal through adult—Dunkin 2004), and that similar assumptions were used for all animals in this study, the inter–age-class differences in buoyant force we posit are likely to be real. Furthermore, it also is important to note that only the costs of descent associated with overcoming buoyancy were calculated in this study. While diving, drag forces also act upward against dolphins as they descend (Skrovan et al. 1999). Thus, the actual locomotor cost incurred by a dolphin diving to 10 m is likely to be greater than the values presented in this study. Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 studies on carcasses demonstrated that average blubber thicknesses of fetal and neonatal bottlenose dolphins were only 5–6 mm and 11–12 mm, respectively (Dunkin et al. 2005; Struntz et al. 2004). Blubber-thickness measurements of neonates from other cetacean species demonstrate similar results; newborn arctic whales (Blix and Steen 1979) and harbor porpoises (Phocoena phocoena) 90 cm (Lockyer 1995) are equipped with relatively thin blubber layers compared to adult conspecifics. This result also has been found for newborn pinnipeds (for review see Blix and Steen 1979). However, pinniped pups are born and nurse on land, allowing for physiological changes that enhance thermal capacity to occur before weaning and before encountering the thermal challenges of the marine environment (Blix and Steen 1979; Elsner et al. 1977). Cetaceans are born into the highly conductive ocean and immediately experience the high thermal demands of this environment. This thermal demand may drive immature dolphins to quickly acquire enhanced blubber thickness to decrease heat loss. The present study demonstrates that by 1 year postpartum, immature dolphins are able to maintain a greater proportion of blubber than older conspecifics (Fig. 3). This result is similar to that found for bottlenose dolphins (Dearolf et al. 2000), harbor porpoises (Lockyer 1995; McLellan et al. 2002), and franciscana dolphins (Pontoporia blainvillei—Caon et al. 2007) carcasses. Although the greater proportion of blubber found in immature dolphins may be a result of constraints to muscle growth (McLellan et al. 2002), the elevated blubber levels in immature cetaceans does presumably limit excessive heat loss from the body. In addition, 1-year-old bottlenose dolphins acclimated to warm water (summer) maintained thicker blubber at the thoracic–abdominal area comparable to that by older age classes acclimated to warm water (Fig. 2). This result is similar to that found for harbor porpoise carcasses (Koopman 1998; Lockyer 1995), but differs from that found for bottlenose dolphin carcasses, which demonstrated lower (Struntz et al. 2004) or equivalent (Dunkin et al. 2005) blubber thicknesses in 1-year-old animals (their juvenile age class) compared to older age classes. The disparity among bottlenose dolphin studies could be associated with the inability of the previous studies to control for the season during which carcasses were collected. In contrast to age-specific differences in blubber thickness for summer-acclimated dolphins, winteracclimated dolphins had similar blubber thickness irrespective of age (Fig. 2). This occurred because yearlings had the smallest increase in blubber thickness (Fig. 2) and proportion of blubber (Fig. 3) in response to the increased thermal demands of colder water during winter. Thus, seasonal adjustments in blubber thickness are greater for older dolphins than for yearlings. Initially this result seems counterintuitive; the increased thermal gradient imposed by the colder water temperatures of winter would favor vastly thicker blubber for increased insulation in dolphins of all ages. This would be especially important for the small-bodied yearlings. Thus, overall blubber deposition, particularly in the youngest age classes, may be limited by some other factor. One explanation for these results Vol. 90, No. 3 June 2009 NOREN AND WELLS—BLUBBER DEPOSITION IN BOTTLENOSE DOLPHINS the lower water temperatures of winter without compromising locomotor demands. Conversely, yearlings needed to balance thermoregulatory and locomotor demands. This trade-off seemed to limit their blubber deposition in winter, likely exacerbating relatively high rates of heat loss theoretically associated with relatively high surface area-to-volume ratios. Ultimately, this trade-off could constrain the lower temperature limits of yearlings. Given that dolphin calves must maintain proximity with their mothers for nourishment and protection, they may find themselves in environments outside their thermal neutral zones, the range of environmental temperatures over which metabolic rate remains relatively constant and independent of ambient environmental temperatures (Mount 1979). Similar to recent findings for Weddell seal (Leptonychotes weddellii) pups (Noren et al. 2008), bottlenose dolphin calves may rely on elevated heat production to safeguard against heat loss. ACKNOWLEDGMENTS We thank the volunteers, staff, and graduate students based at Mote Marine Laboratory working with the Chicago Zoological Society’s Sarasota Dolphin Research Program for making the dolphin measurements possible. In particular, we thank S. Hofmann, W. McLellan, S. Nowacek, A. Read, M. Scott, K. Urian, and G. Worthy for assistance in collecting some morphological measurements. We also thank Dr. Terrie Williams and an anonymous reviewer for their comments, which have improved this manuscript. Data collection from the dolphins was supported by the National Science Foundation, Office of Naval Research, Earthwatch Institute, National Marine Fisheries Service, Dolphin Quest, and International Whaling Commission. S. R. Noren held an American Fellowship from the American Association of University Women Educational Foundation during the preparation of this manuscript. LITERATURE CITED ADOLPH, E. F., AND F. W. HEGGENESS. 1971. Age changes in body water and fat in fetal and infant mammals. Growth 35:55–63. AGUILAR, A., AND A. BORRELL. 1991. Heterogeneous distribution of organochlorine contaminants in the blubber of baleen whales: implications for sampling procedures. Marine Environmental Research 31:275–286. BECK, C. A., W. D. BOWEN, AND S. J. IVERSON. 2000. Seasonal changes in buoyancy and diving behaviour of adult grey seals. Journal of Experimental Biology 203:2323–2330. BIUW, M., B. MCCONNELL, C. J. A. BRADSHAW, H. BURTON, AND M. FEDAK. 2003. Blubber and buoyancy: monitoring the body condition of free-ranging seals using simple dive characteristics. Journal of Experimental Biology 206:3405–3423. BLIX, A. S., AND J. B. STEEN. 1979. Temperature regulation in newborn polar homeotherms. Physiological Reviews 59:285–304. BRODY, S. 1945. Bioenergetics and growth, with special reference to the efficiency complex in domestic animals. Reinhold, New York. CAON, G., C. BERNHARDT FIALHO, AND D. DANILEWICZ. 2007. Body fat condition in franciscanas (Pontoporia blainvillei) in Rio Garnde do Sul, southern Brazil. Journal of Mammalogy 88:1335–1341. DEAROLF, J. L., W. A. MCLELLAN, R. M. DILLAMAN, D. FRIERSON, JR., AND D. A. PABST. 2000. Precocial development of axial locomotor muscle in bottlenose dolphins (Tursiops truncatus). Journal of Morphology 244:203–215. Downloaded from https://academic.oup.com/jmammal/article/90/3/629/874589 by guest on 03 March 2024 Age-specific and seasonal differences in blubber deposition also may be explained by another primary role of blubber for marine mammals. In addition to thermal insulation and influences on buoyancy, the blubber layer serves in energy storage (Nordøy and Blix 1985; Parry 1949). Seasonal fluctuations in prey abundance and age-related differences in maternal milk energy intake or foraging efficiency, or both, may affect blubber deposition. However, it is unlikely that the observed differences in the wild dolphins were associated with these factors, because we have observed similar patterns to occur in captive bottlenose dolphins, where food is constantly available and the diet of calves 6 months postpartum is subsidized with fish. Captive yearlings residing in warm water (28.9 6 0.118C) showed significantly greater thoracic– abdominal blubber thickness (14 6 0.5 mm) than older conspecifics (11 6 0.2 mm; t ¼ 6.329, d.f. ¼ 5, P ¼ 0.001). Meanwhile, captive dolphins acclimated to colder water (20.6 6 08C) demonstrated similar thoracic–abdominal blubber thicknesses irrespective of age class (yearlings ¼ 14 6 0.5 mm, and older dolphins ¼ 15 6 0.4 mm). Also similar to that shown for wild dolphins, older, captive dolphins acclimated to colder water had significantly thicker thoracic–abdominal blubber than older, captive dolphins acclimated to warmer water (t ¼ 7.303, d.f. ¼ 9, P , 0.001). Presumably the thicker blubber of dolphins acclimated to colder water, both in the wild (Fig. 3) and as we have observed for dolphins in captivity, provides for the ability to maintain a greater thermal gradient between the body core and the environment. Ultimately, small body size and potential limitations to blubber deposition in dolphin calves and yearlings may constrain thermal capacity, which may impact behavior. This has been demonstrated previously in pinnipeds. For example, hauling out for pupping in harbor seals (Phoca vitulina) in the Moray Firth occurs during June and July because thermoregulatory costs for newborn pups and lactating mothers are lowest during these warm months (Hind and Gurney 1998). Limitations of thermal capacity in cetacean calves also may be a potential factor influencing both the location and season for calving. For example, movement of pregnant belugas (Delphinapterus leucas) into warmer estuaries and lagoons for calf delivery has been attributed to the lower thermal capacity of the calf (Sergeant 1973). In addition, harbor porpoises off the British Isles tend to give birth in June when water temperatures are highest, which favors the survivorship of the neonates with thin, low-lipid-content blubber (Lockyer 1995). A similar pattern has been noted for the calving of bottlenose dolphins in Sarasota Bay, Florida. Peak calving occurs in spring and early summer when water temperatures are approaching their warmest (Scott et al. 1990; Urian et al. 1996; Wells et al. 1987). Finally, this may be an explanation for the migration of some baleen whales from their cold polar feeding grounds to lower latitudes to give birth and nurse. 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