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Metabolic Consequences of Carnivory in Marine Mammals

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Metabolic Consequences of Carnivory in Marine Mammals See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/11900119 A killer appetite: Metabolic consequences of carnivory in marine mammals Article in Comparative Biochemistry and Physiology - Part A Molecular & Integrative Physiology · August 2001 Impact Factor: 1.97 · DOI: 10.1016/S1095-6433(01)00347-6 · Source: PubMed CITATIONS READS 75 177 5 authors, including: Terrie M Williams Suzanne Kohin University of California, Santa Cruz Southwest Fisheries Science Center 165 PUBLICATIONS 5,706 CITATIONS 34 PUBLICATIONS 746 CITATIONS SEE PROFILE SEE PROFILE 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 Biology, 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 Marine Biology, 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 gastrointestinal tract reflects the metabolic demands of the animal and individual requirements for processing, distributing, and absorbing nutrients. 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 pinnipeds and cetaceans. Oxygen consumption was measured for resting bottlenose dolphins and Weddell seals, and the results combined with data for four additional species of carnivorous marine mammal. 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 water 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 marine mammal 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 vertebrate and invertebrate prey. ᮊ 2001 Elsevier Science Inc. All rights reserved. Keywords: Basal metabolic rate; 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 energy 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 , food 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 pressure 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 blood, 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 metabolism 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 , birds Piersma et al., 2.1. Animals 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 diet, as gramŽ. SPAWAR, San Diego, CA , and had been well as digestive tract design and function. 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 vitamins. Water temperature 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 ocean. 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 sea ice open-flow respirometry systems. Breathing 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.
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