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A killer : Metabolic consequences of carnivory in

Article in Comparative and - Part A Molecular & Integrative Physiology · August 2001 Impact Factor: 1.97 · DOI: 10.1016/S1095-6433(01)00347-6 · Source: PubMed

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Terrie M Williams Suzanne Kohin University of California, Santa Cruz Southwest Science Center

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Available from: Terrie M Williams Retrieved on: 11 April 2016 Comparative Biochemistry and Physiology Part A 129Ž. 2001 785᎐796

A killer appetite: metabolic consequences of carnivory in ଝ marine mammals

Terrie M. Williamsa,U, J. Haunb, R.W. Davisc, L.A. Fuimand, S. Kohine

aDepartment of , EMS-A316, Uni¨ersity of California, Santa Cruz, CA 95064, USA bSPAWAR Systems Center, D35, 53560 Hull Street, San Diego, CA 92152-6506, USA cDepartment of , Texas A&M Uni¨ersity, 5007 A¨enue U, Gal¨eston, TX 77553, USA dDepartment of Marine Science, Uni¨ersity of Texas at Austin, 750 Channel View Dri¨e, Port Aransas, TX 78373, USA eDepartment of Physiology, Uni¨ersity of California, San Diego, CA 92093, USA

Received 25 September 2000; received in revised form 21 February 2001; accepted 22 February 2001

Abstract

Among terrestrial mammals, the morphology of the reflects the metabolic demands of the and individual requirements for processing, distributing, and absorbing . To determine if gastrointesti- nal tract morphology is similarly correlated with metabolic requirements in marine mammals, we examined the relationship between basal metabolic rateŽ. BMR and small intestinal length in and cetaceans. consumption was measured for resting bottlenose dolphins and Weddell seals, and the results combined with data for four additional species of carnivorous marine . Data for small intestinal length were obtained from previously published reports. Similar analyses were conducted for five species of carnivorous terrestrial mammal, for which BMR and intestinal length were known. The results indicate that the BMRs of Weddell seals and dolphins resting on the surface are 1.6 and 2.3 times the predicted levels for similarly sized domestic terrestrial mammals, respectively. Small intestinal lengths for carnivorous marine mammals depend on body size and are comparatively longer than those of terrestrial carnivores. The relationship between basal metabolic rateŽ kcal dayy1.Ž. and small intestinal length m for both marine and terrestrial carnivores was, BMRs142.5 intestinal length1.20 Žr 2 s0.83. . We suggest that elevated metabolic rates among carnivores are associated with comparatively large alimentary tracts that are presumably required for supporting the energetic demands of an aquatic lifestyle and for feeding on and prey. ᮊ 2001 Elsevier Science Inc. All rights reserved.

Keywords: ; Carnivore; Dolphin; Marine mammal; Small intestine; Weddell seal; Herbivore

ଝ This paper was originally presented at a symposium to honour Gerald Kooyman held on 19 April 2000, in La Jolla, California. U Corresponding author. Tel.: q1-831-459-5123; fax: q1-831-459-4882. E-mail address: [email protected]Ž. T.M. Williams .

1095-6433r01r$ - see front matter ᮊ 2001 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3Ž. 0 1 00347-6 786 T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796

1. Introduction tained metabolic rates and metabolic ceilings, which ultimately set the limits for foraging behav- Diving marine mammals spend considerable ior, reproductive output and geographic distribu- time and in locating, pursuing, capturing tion, are linked to the digestive tract’s ability to and processing prey. For these activities to be process foodŽ. Peterson et al., 1990 . As a conse- energetically profitable, two physiological require- quence, the size of the organs comprising the ments must be met. First, more energy must be gastrointestinal tract often reflects the immediate acquired from the intake of prey than is spent in metabolic demands of the animal. For example, obtaining and processing them. Second, marine cold exposureŽ. Koteja, 1996 , habits Ž Mc- mammals that forage while submerged must be Nab, 1986.Ž. , foraging methods Jackson, 1992 and capable of hunting under a constraint of limited ecological conditionsŽ. Piersma et al., 1996 that oxygen availabilityŽ Dunstone and O’Connor, lead to variability in basal metabolic rate have 1979. . been associated with alterations in the size of the Based on these requirements, there is consider- alimentary tract. able selective for energetic efficiency To provide a better understanding of the during underwater hunting by marine mammals. metabolic demands of marine mammals and the In conventional foraging models, energetic prof- organs that must support these demands, we ex- itability of specific prey and the efficiency of the amined the relationship between BMR and gas- predator are often expressed in terms of costrbe- trointestinal length in cetaceans and pinnipeds. nefit ratios calculated from the ratio of energy Metabolic measurements were conducted on two gained to energy expended during foraging species: an odontocete, the bottlenose dolphin Ž.Stephens and Krebs, 1986 . The duration of Ž.Tursiops truncatus and a phocid, the Weddell hunting by marine mammal predators is also de- seal Ž.Leptonychotes weddelli . These data were fined by energy expenditure, as oxygen reserves in combined with basal metabolic rates reported for the , muscles and lungs are consumed dur- other carnivorous marine mammals measured un- ing a diveŽ. Kooyman, 1989 . der comparable conditions. The relationship Despite the importance of energy expenditure between gastrointestinal tract morphology and in evaluating foraging costs and overall energetic metabolic demand was determined using data for efficiency of a predator, there is much confusion six species of marine mammal, in which both regarding the metabolic rates of marine mam- BMR and small intestinal length were measured mals. Even the relatively simple measure of basal or known. Similar analyses were conducted for metabolic rateŽ. BMR has not been clearly de- five species of carnivorous terrestrial mammal. fined for this group. Currently, a question re- The results of this study indicate that the BMR of mains regarding whether or not the basal marine mammals resting on the water surface is metabolic rates of marine mammals are higher higher than predicted for terrestrial mammals. Ž.Irving, 1973; Liao, 1990 , lower, or identical This elevated is associated with a Ž.Lavigne et al., 1986; Innes and Lavigne, 1991 to comparatively large alimentary tract that is pre- predictions for terrestrial mammals of compara- sumably required for supporting an aquatic ble size. The confusion is due, in part, to a poor lifestyle and for feeding on vertebrate and inver- understanding of the underlying factors that set tebrate prey. metabolic rates in marine mammals, and the im- pact of diving responses on these factors. Recent studies on a variety of small verte- 2. Materials and methods brates, including rodentsŽ Konarzewski and Dia- mond, 1995; Koteja, 1996.Ž , Piersma et al., 2.1. 1996; Burness et al., 1998.Ž and lizards Garland, 1984. , indicate that the organs associated with the Three mature, male bottlenose dolphinsŽ mean processing and distribution of nutrients are cou- body masss148.6 kg. were used in the metabolic pled to the metabolic rate of the animal. Among studies. The animals were maintained in floating a wide variety of terrestrial animals, metabolic net pens at the US Navy Marine Mammal Pro- rates are influenced by the quality of the , as gramŽ. SPAWAR, San Diego, CA , and had been well as digestive tract design and . Sus- at the facility for over 2 years before the mea- T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 787 surements were conducted. All animals were fed released into the ice hole and were free to dive daily on a diet of mackerel, herring, and smelt and rest. Resting metabolic measurements were supplemented with . Water made on sedentary animals as they floated on the in the pens reflected seasonal ambient conditions water surface. Only resting periods lasting at least in the . Average water temperature in the 2 h were used in the analyses. Respiratory rate pens during the experimental period was 15.4ЊC. and apneic periods were recorded visually and Њ Tair was 15.5 C. The dolphins were trained for acoustically on videotape. 2᎐3 weeks prior to experimentation to rest qui- etly in a water-filled metabolic box 2.2.3. Oxygen consumption Seven mature, male Weddell sealsŽ mean body Oxygen consumption was determined using masss388.5 kg. were captured on the ice open-flow systems. by the near McMurdo Station, Antarctica. The animals animals was restricted to a Plexiglas domeŽ 1.1 m were transported approximately 7 miles from the long=0.8 m wide=0.8 m high for dolphins; 2.4 point of capture to an isolated ice holeŽ 2.4-m- m long=1.1 m wide=0. 4 m high for seals. long=1.1-m-wide shelf with a 1.0-m-diameter mounted at the water level of the metabolic box hole. that had been cut into the sea ice. All seals or ice hole. Air was drawn through the chamber were held for 24᎐48 h and fitted with dive with a vacuum pumpŽ Sears 2.0 Hp WetrDry recorders and video instrumentation packsŽ Davis Vac. . Flow rate was monitored with a calibrated, et al., 1999. before release into the isolated hole. dry gas-flow meterŽ American Meter Co Inc, A video recording system and camera mounted DTM-325, San Leandro, CA. and was maintained on the animals continuously monitored hunting at 45᎐65 l miny1 for the dolphins and 510᎐550 l behavior to ensure that the animals were post- miny1 for the seals. At these flow rates, the absorptive prior to the metabolic measurements. fractional of oxygen in the domes Water temperature in the ice hole was y1.4 to remained above 0.2000. Samples of air from the y Њ 0.8 C during the experimental period. Tair was exhaust port of the domes were driedŽ. Drierite ᎐ Њ 1.7 3.6 C. and scrubbed of CO2 Ž. Sodasorb before entering the oxygen analyzerŽ AEI Technologies S3-A, 2.2. Basal metabolic rate Pittsburgh, PA. . The percentage of oxygen in the exhaust air was monitored continuously during 2.2.1. Dolphins the , and recorded with a personal Metabolic measurements were carried out dur- computer using Sable Systems softwareŽ Salt Lake ing March᎐April. Each animal was fasted City, UT. . The output from the oxygen analyzer overnight and placed in an insulated metabolic was monitored every second and averaged for box the following morning. Water temperature in each minute. These values were converted to the box was controlled by a saltwater heat ex- oxygen consumption Ž.V˙ using equations from O 2 changer and ranged from 3.7 to 28.9ЊC. Only one Fedak et al.Ž. 1981 and an assumed respiratory water temperature was tested on each experimen- quotient of 0.77. The lowest value for oxygen tal day. Depending on the animal and the experi- consumption averaged over 10᎐30 min during mental water temperature, metabolic measure- each 2᎐3-h experimental session was used in the ments were carried out continuously over 2᎐3h. analyses of basal metabolic rate. All values were Experiments were conducted on sedentary ani- corrected to STPD. mals and were terminated if the animal became Theentiresystemwascalibrateddaily active. Core body temperature was determined Ž.dolphins or immediately before and after mea- continuously during the experiments with a digital surementsŽ. seals with dry ambient air Ž 20.94% thermometer and flexible rectal probeŽ Physitemp O2 . and 100% gas according to Fedak et Inc, Clifton, NJ. . al.Ž. 1981 . The theoretical fraction of O2 leaving the dome was calculatedŽ. Davis et al., 1985 and 2.2.2. Weddell seals compared to the measured values from the oxy- All metabolic measurements were carried out gen analyzer. The flow of calibration gases into during the Antarctic austral summerŽ Octo- the dome was controlled and monitored by an ber᎐December. and followed the protocols of electronic flowmeterŽ Omega, Model ࠻FMA- Castellini et al.Ž. 1992 . Instrumented seals were 772V. that was accurate to within 1%. Calibra- 788 T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 tions of the flow meter were conducted with ni- it was not possible to conduct a similar analysis trogen gas and a rotameterŽ Cole-Palmer Instru- for the upper critical temperature. Instead, upper ments. before and after the studies. critical temperature for the dolphins was based on fluctuations in core body temperature and 2.3. Length of the small intestine t-tests conducted for metabolic rates determined at 16, 23 and 29ЊC. Differences in the means for the metabolic The length of the small intestine for a wide rates of resting and intermittently breathing seals variety of terrestrial and marine mammals was were determined from t-tests using statistical compiled from published literature. Because diet softwareŽ. Jandel Scientific Software, 1995 . Allo- influences gastrointestinal morphology, including metric regressions for basal metabolic rate in intestinal length in mammalsŽ Stevens and Hume, relation to body mass, and relationships for basal 1995. , the published data used in the present metabolic rate . intestinal length, and intestinal study were limited to carnivorous species, except length ratio vs. body length, were determined for comparisons with herbivores. Care was also using least squares methodsŽ Jandel Scientific taken to limit the data to adult, non-pregnant, Software, 1995. . Data are reported as means" non-lactating animals. Values for post-prandial S.E.M., unless otherwise indicated. animals were excluded whenever the presence of food in the intestinal tract was indicated.

2.4. Statistics 3. Results

The lower critical temperature for the dolphins 3.1. Basal metabolic rate was determined from the intersection of multiple regressions using Yeager and UltschŽ. 1989 . Be- The metabolic rate of dolphins resting on the cause warm water tests were terminated if core water surface was dependent on water tempera- temperature of the dolphins fluctuated )0.1ЊC, tureŽ. Fig. 1 . Metabolic rates recorded in this

Fig. 1. Resting metabolic rate of three adult, post-absorptive bottlenose dolphins in relation to water temperature. Acclimatization s Њ temperature for the dolphins was Twater 15.4 C. Each point represents a single metabolic measurement for an individual dolphin. The horizontal line represents the average metabolic rate within the thermal neutral zoneŽ. defined in text . T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 789

y1 ranged from 5.78 to 10.12 ml O2 kg of metabolic rates previously reported for resting miny1, with higher metabolic rates occurring at and sleeping Weddell seals by Castellini et al. both the high and low water-temperature ex- Ž.1992 , measured under identical conditions. tremes. The mean minimum metabolic rate for the three dolphins resting on the water surface 3.2. Length of the small intestine " y1 y1 s was 6.53 0.16 ml O2 kg min Ž.n 9at s Њ Intestinal length for marine carnivores corre- Twater 15.4 CŽ. acclimatization temperature , and was within 8% of that reported by Ridgway and lated with body size and ranged from 11.4 m in s the smallest species, the Ž Enhydra lutris; PattonŽ. 1971 for a 128-kg dolphin at Twater 17ЊC. Metabolic rate of the dolphins remained at Kenyon, 1969. , to 100 m in the largest species, the Ž this level until T was lower than 5.9 or higher fin whale Balaenoptera physalus; Stevens and water . than 23.0ЊC. These water were con- Hume, 1995 . Values for similarly sized otariids sidered the lower and upper critical temperatures, and phocids ranged from 14.5 to 38.0 m in adult animalsŽ , 1981a,b; King, 1983; Stevens and respectively, for bottlenose dolphins acclimatized Hume, 1995; Martensson et al., 1998. . Owing to to 15.4ЊC, as defined by a significant increase in their comparatively large body size, small intesti- metabolic rate at 3.9 Ž.ns4, Ps0.029 and 29.0ЊC nal length was greater for mysticete whalesŽ range Ž.ns4, Ps0.004 . 61.2᎐100.0 m.Ž than for odontocetes range Weddell seals rested on the water surface for 30.0᎐66.0 m.Ž Stevens and Hume, 1995 . . The periods of up to 6 h. Respiratory cycles alternated ratio of small intestinal length to total body length between eupnea during quiescent, alert periods correlated negatively with body length in marine and intermittent breathing patterns during . mammalsŽ. Fig. 3a , and was described by the The metabolic rate of alert Weddell seals resting regression sy y Њ " at Twater1.4 to 0.8 C was 3.58 0.24 ml O 2 y1 y1 kg minŽ. Fig. 2 . This decreased to 3.20"0.06 Intestinal lengthrbody length ratio ml O kgy1 miny1 when the seal was sleeping 2 s y0.41 and breathing intermittently. However, the dif- 17.6 body length ference in metabolic rates between the two condi- Ž ns25 species, r 2 s0.49. tions was not statistically significant Žns7 seals, s s t 1.892, P 0.09. . These results are within 14% where body length is in m. In comparison, small intestinal length increased with body length in these marine mammalsŽ. Fig. 3b and was de- scribed by:

Intestinal length s16.7 body length0.60 Ž ns25 species, r 2 s0.77.

where lengths are in m. Comparable measurements for carnivorous ter- restrial mammals ranging in mass from 1.0 to 190.0 kg showed relatively smaller intestinal lengths than for marine speciesŽ. Fig. 3a,b . Like marine mammals, the length of the small in- testines depended on body size, and ranged from 1.2 m for the domestic ŽFelis catus; Stevens Fig. 2. Metabolic rate of seven adult, post-absorptive Weddell and Hume, 1995. to 8.7 m for a male African lion seals resting or sleeping on the water surface. Resting values Ž.Panthera leo; Davis, 1962 . The ratio of intestinal are for alert, inactive animals breathing continuously. These length to body length was 2.4᎐4.9 and did not data are compared to values for the same seals breathing intermittently during sleep. Height of the columns and lines change with body length for the range of terres- represent meansqS.E.M. Numbers in parentheses indicate trial species examined in this studyŽ Davis, 1962; the number of seals. Stevens and Hume, 1995. . 790 T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796

4. Discussion rates for marine mammals, Lavigne et al.Ž. 1986 recognized that, in many cases, the defined condi- 4.1. Interrelationships between resting metabolic rate tions for assessing basal metabolism had not and the alimentary tract of carni¨orous marine been met. These conditions specify mature, post- mammals absorptive animals resting in a thermally neutral environment. Consequently, the authors sug- In a review of studies reporting basal metabolic gested that the elevated BMRs reported for many

Fig. 3. The ratio of small intestinal length to total body lengthŽ. a and intestinal length Ž. b in relation to body length for carnivorous mammals. Data for marine mammals are denoted by the closed symbols and include sea ottersŽ. diamonds , odontocetes Ž. circles , phocid sealsŽ. squares , otariids Ž triangles . , and mysticete whales Ž down-pointed triangles . . Terrestrial carnivores are shown by the open circles and include mink, human, cat, dog, leopard, and African lions. The solid lines denote the least squares regressions through the data points and are presented in the text for marine mammals. The regression for terrestrial mammals inŽ. b is intestinal lengths 3.1 body length1.22 Žns6 species, r 2 s0.90. . T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 791 marine mammals were an artifact due to inap- metabolic rate that was 2.1-fold that predicted propriate comparisons with terrestrial mammals. Ž.Liao, 1990 . Sea otters, with an admittedly ele- Results from the present study, in which these vated mustelid metabolismŽ. Iverson, 1972 , show conditions were metŽ assuming acclimatization resting rates that are 2.8-fold the predictions when temperature and minimum oxygen consumption resting quietly on the water surface in a metabolic s Њ occur within the thermal neutral zone; hood at Twater 20.0 CŽ. Williams, 1989 . Bartholomew, 1977. , indicate that other factors A better predictor of the basal metabolic rates may also be involved. for these species of marine mammal can be found In general, we find that the metabolic rates of in the scaling equation for vertebrate-eaters pre- marine mammals resting on the water surface are sented in McNabŽ.Ž. 1988 Fig. 4 . This agreement higher than those of terrestrial mammals resting may not be surprising, since the species repre- in airŽ. Fig. 4 . Basal metabolic rates of the bot- sented in this equation include marine, terrestrial tlenose dolphins and Weddell seals measured here and semi-aquatic mammals. When only terrestrial were 2.3- and 1.6-fold the predicted levels for carnivorous mammals are considered, the differ- domestic terrestrial mammalsŽ. Kleiber, 1975 , re- ences in BMR between marine and terrestrial spectively. When measured under similar condi- groups remain, despite similar food habits. For tions, the metabolic rates of other species of example, the BMR of a 73-kg California sea lion resting marine mammal follow a similar pattern. Ž.Liao, 1990 is 2.3-fold that of a 59-kg cougar Killer whales trained to breathe into a respiratory Ž.Corts, 1984 ; a 20-kg sea otter Ž Williams, 1989 . balloonŽ. Kriete, 1995 showed metabolic rates maintains a BMR that is 3.5-fold that of a 14.1-kg that were 1.6-fold those predicted by Kleiber for a dogŽ. Kleiber, 1975 . In general, the BMRs re- 3750-kg adult male, and 1.4-fold those predicted ported for many carnivorous terrestrial mammals, for a 2692-kg adult female. A 73-kg adult female including , dogs, arctic foxes, red foxes and California sea lion resting in a water-filled cougarsŽ. reviewed by McNab, 1988 , are within metabolic chamber had a minimum resting 4᎐23% of the predictions of KleiberŽ. 1975 . In

Fig. 4. Basal metabolic rate for marine mammals resting on the water surface in relation to body mass. Each point represents the mean values for sea ottersŽ.Ž E.l. diamond; Williams, 1989 , harbor P.p. circle; Kanwisher and Sundnes, 1965 . , California sea lions Ž.Ž.Ž.Z.c. triangle; Liao, 1990 , bottlenose dolphins T.t. circle; present study , Weddell seals L.w. square, present study , and killer whales Ž.O.o. circle; Kriete, 1995 . The solid line is the predicted regression for basal metabolic rate in domestic terrestrial mammals according to KleiberŽ. 1975 . The dashed line is the regression for vertebrate eaters, which includes marine, semi-aquatic and terrestrial mammals from McNabŽ. 1988 . 792 T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 comparison, the BMR of carnivorous marine variation in the mass of metabolically active or- mammals ranges from 1.4- to 2.8-fold that pre- gans that support the processing and delivery of dicted. nutrients. Thus, the small intestines, as well as One confounding factor for marine mammals is the , , and , comprise a small the physiological adjustment that occurs with the proportion Ž.-17% of the total body mass of dive response. In a study using adult California mice, but account for nearly 50% of the variation sea lions trained to submerge in a pool, Hurley in BMR in this speciesŽ Konarzewski and Dia- Ž.1996 found a graded resting metabolic response mond 1995. . that correlated with the duration of submergence. The proposed demand on the gastrointestinal Metabolic rates measured on the water surface tract of marine mammals is reflected in the length were 2᎐3-fold those predicted for domestic ter- of the small intestines for otariids, phocids, odon- restrial mammals by KleiberŽ. 1975 . These rates tocetes, mysticetes and a mustelid, the sea otter were reduced and approached the predicted lev- Ž.Fig. 3a,b . Many investigators have noted the els when the measurement period included pro- exceptional length of the small intestines of ma- longed submergence. Undoubtedly, the variation rine mammals. It remains one of the most striking in measured BMR for these sea lions can be features of the gastrointestinal tract of both pin- attributed in part to changes in metabolic de- nipedsŽ. Eastman and Coalson, 1974; King, 1983 mands of specific tissues during submergence. and cetaceansŽ Slijper, 1976; Stevens and Hume, This may also explain the variability in basal 1995. . Although the length of the small intestine metabolic rate reported for marine mammals in in many terrestrial carnivores approaches six-fold comparison to terrestrial mammals. total body length, it ranges from seven- to 40-fold Several studies have provided explanations to body length in otariids and phocidsŽ. King 1983 . account for the comparatively high metabolic rates Among odontocetes and mysticetes, this length of resting marine mammals, regardless of their ratio ranges from four- to 23-fold body length, surface or submerged positionŽ reviewed in Lavi- depending on the speciesŽ Stevens and Hume, gne et al., 1986. . These include elevated food 1995. . consumption of captive subjects, cold acclimatiza- Currently, the reason for the exceptional length tion leading to high thermoregulatory energetic of the small intestines in marine mammals is not costs, body composition, and high diets. known. Thermoregulatory factors, parasitic infes- Certainly, the high thermal conductivity of water tation necessitating a larger gut, and increased in comparison to air at the same temperature can time for enzymatic or microbial breakdown and result in elevated levels of heat loss and increased absorption of ingested whole prey have been sug- metabolic demands for mammals resting in water gestedŽ. Eastman and Coalson, 1974; King, 1983 . Ž.Dejours, 1987 . In addition, the maintenance of The linked ancestral history of cetaceans and metabolically active tissues will influence overall herbivorous mammals may also explain similari- metabolic rate, which in turn could limit dive ties in alimentary tract length for both of these Ž. duration in marine mammals Ridgway, 1985 . groupsŽ. Stevens and Hume, 1995 , but does not An especially relevant factor in setting the apply to other marine mammal lineages. The cur- metabolic rate of an animal is the capacity of the rent study indicates that metabolic demands asso- body to deliver nutrients to active tissues ciated with an aquatic lifestyle and with carnivory Ž. Armstrong, 1983 . Consequently, the high ener- may be key factors. The length of the small in- getic requirements of marine mammals may place testines is a major distinguishing feature between a correspondingly high demand on the gastroin- marine and terrestrial carnivores, and is corre- testinal tract. Previous studies examining diverse lated with metabolic rate. A single regression vertebrate species with different food habits have describes the relationship between basal demonstrated that the metabolic demands faced metabolic rate and total length of the small intes- by an animal have an important bearing on the tine for both mammalian groupsŽ. Fig. 5 : design and function of the gastrointestinal tract Ž.ŽStevens and Hume, 1995 . Both inter- Daan et al., 1990.Ž and intraspecific Konarzewski and Dia- Basal metabolic rates142.5 intestinal length1.20 mond, 1995. variation in basal metabolic rate among terrestrial mammals may be explained by Ž ns11 species, r 2 s0.83. T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 793 where metabolic rate is in kcal dayy1 and intesti- absorbed when it is suddenly availableŽ Slijper, nal length is in m. This relationship differs from 1976. . The processing of prey items that are high that of mammalian herbivores, which shows cor- in content or possess chitinous exoskeletons respondingly lower basal metabolic rates and will also be facilitatedŽ. Stevens and Hume, 1995 . shorter intestinal lengthsŽ. Fig. 5 . Based on these By enhancing efficiency, compara- differences, there appears to be a cost with car- tively high metabolic rates can be supported, with nivory that is associated with an increase in length the concomitant advantages of higher rates of of the small intestines. For both carnivorous and sustained activity, independence from environ- herbivorous groups, marine-living species repre- mental temperature fluctuations, faster growth, sent the upper extremes of these relationships. and higher reproductive outputŽ Konarzewski and Thus, an aquatic lifestyle appears to add a second Diamond, 1995. . influencing factor on the relationship between Despite these advantages, there is a metabolic basal metabolic rate and intestinal length. trade-off associated with maintaining a large di- By maintaining a large alimentary tract, marine gestive tract. Because the gastrointestinal tract is mammals obtain both the advantages inherent a metabolically intense in , both with being able to meet elevated metabolic de- in terms of protein synthesis and energy utiliza- mands and the disadvantages associated with sup- tion, it is expensive to maintainŽ Stevens and porting a metabolically active . A large di- Hume, 1995. . Comparative tissue rates gestive tract provides an advantage for marine and organ masses indicate a disproportionate predators that feed on prey that is only intermit- metabolic demand by the alimentary tract, which tently available or patchily distributed in the envi- ranks fourth in whole-organ oxygen consumption ronmentŽ. Gaskin, 1978 . In this way, large quanti- out of 14 organs examined in the ratŽ Schmidt- ties of prey can be consumed, processed and Nielsen, 1984. .

Fig. 5. Basal metabolic rate of carnivorous marineŽ. closed circles and terrestrial Ž. open circles mammals in relation to intestinal length. Each point represents the mean value for each species. The solid line for carnivores is the least squares linear regression through the data, as described in the text. Basal metabolic rates for marine mammals are from Fig. 4; intestinal lengths are from Fig. 3. Terrestrial mammal basal rates are from BrodyŽ. 1945 ; human . , Kleiber Ž. 1975 ; dog, cat . , McNab Ž. 1986 ; mink . , and Corts Ž 1984, cougar.Ž.Ž. ; intestinal lengths are from Fig. 3. Values for representative marine closed square and terrestrial open square herbivorous mammals are provided for comparison, and include vole, woodchuck, rabbit, sheep and manateeŽ metabolic rates reviewed in McNab, 1988; intestinal lengths for terrestrial herbivores are from Stevens and Hume, 1995; intestinal length for the is from Reynolds and Rommel, 1996.Ž. . The least squares regression solid line for herbivores is BMRs61.6 intestinal length1.10 Žns5 species, r 2 s0.99. . 794 T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796

Interestingly, selective redistribution of blood comparative physiology. This study was supported away from the alimentary tract during diving could by grants from the Office of Naval Research reduce these costs in marine mammals, and may Ž.N00014-95-1-1023 , the National Science Foun- explain part of the variability in resting metabolic dationŽ. Polar Programs ࠻OPP-9618384 , and an rates of surface and submerged California sea ASSEE-ONT fellowship to T.M. Williams. The lions reported by HurleyŽ. 1996 . Previous studies authors thank the trainers and research assistants have demonstrated that the function of splanch- associated with these studies, including R. nic organs varies with dive durationŽ Davis et al., Skrovan, S. Kanatous, M. Horning, and the many 1983. , and that blood flow is markedly reduced to personnel of the SPAWAR Marine Mammal Pro- the intestines during forced dives in Weddell seals gram. In addition, the authors are grateful for the Ž.Zapol et al., 1979 . In a study of seven species of insightful comments of two anonymous reviewers, polar phocid seals, Martensson et al.Ž. 1998 re- which significantly improved the manuscript. All ported no correlation between intestinal length experimental procedures involving animals fol- relative to body length and diving capacity. This lowed NIH guidelines and were evaluated and would be expected if the metabolic demands of approved by institutional Animal Use Commit- maintaining the gastrointestinal tract were re- tees. duced during submergence. Crocker et al.Ž. 1997 have suggested a trade-off between the metabolic References demands of processing food and locomotion in northern seals. Rather than try to simul- Armstrong, E., 1983. Relative brain size and metabolism taneously meet the energetic demands of both, in mammals. Science 220, 1302᎐1304. elephant seals may reduce locomotor costs by Bartholomew, G.A., 1977. Body temperature and en- drifting when increased energy is needed for pro- ergy metabolism. In: Gordon, M.S.Ž. Ed. , Animal cessing ingested prey. Clearly, further studies ex- Physiology: Principles and . MacMillan Publishing Co Inc, New York, pp. 364᎐449. amining the function of these tissues will be Brody, S., 1945. and Growth, with Special needed to assess differences in metabolic costs Reference to the Efficiency Complex in Domestic for maintaining gastrointestinal activity for ma- Animals. Reinhold Publishing Co, NY. rine and terrestrial predators. Burns, J.J., 1981a. Ribbon seal ᎏ Phoca fasciata. In: In summary, the present study demonstrates Ridgway, S.H., Harrison, R.J.Ž. Eds. , Seals. Hand- that the metabolic rates of many species of car- book of Marine Mammals, 2. Academic Press, New nivorous marine mammal are elevated when com- York, pp. 89᎐110. pared to levels for carnivorous terrestrial mam- Burns, J.J., 1981b. Bearded seal ᎏ Erignathus barbatus. mals. These elevated metabolic rates are associ- In: Ridgway, S.H., Harrison, R.J.Ž. Eds. , Seals. Hand- ated with comparatively large alimentary tracts in book of Marine Mammals, 2. Academic Press, New ᎐ marine mammals that are likely required for sup- York, pp. 145 170. Burness, G.P., Ydenberg, R.C., Hochachka, P.W., 1998. porting the energetic demands of an aquatic Interindividual variability in body composition and lifestyle and for feeding on vertebrate and inver- resting oxygen consumption rate in breeding tree tebrate prey. Although a large alimentary tract swallows, Tachycineta bicolor. Physiol. Zool. 71Ž. 3 , affords several adaptive advantages for marine 247᎐256. mammals, it is energetically expensive to main- Castellini, M.A., Kooyman, G.L., Ponganis, P.J., 1992. tain. It is possible that physiological changes asso- Metabolic rates of freely diving Weddell seals: corre- ciated with the dive response may aid in defraying lations with oxygen stores, swim velocity and diving these costs during submergence, and this war- duration. J. Exp. Biol. 165, 181᎐194. rants further investigation of gastrointestinal Corts, K.E., 1984. Basal metabolism and the energetic function in marine predators. cost of walking in cougars. J. Wildl. Manage. 48Ž. 4 , 1456᎐1458. Crocker, D.E., Le Boeuf, B.J., Costa, D.P., 1997. in female northern elephant seals: implica- Acknowledgements tions for . Can. J. Zool. 75Ž. 1 , 27᎐39. Daan, S., Masman, D., Groenewold, A., 1990. Avian This paper was inspired by the of Gerald basal metabolic rates: their association with body L. Kooyman; it is dedicated to him in celebration composition and energy expenditure in . Am. of his 65th birthday and remarkable career in J. Physiol. 259, R333᎐R340. T.M. Williams et al. rComparati¨e Biochemistry and Physiology Part A 129() 2001 785᎐796 795

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