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Energetic Costs and Thermoregulation in Northern Fur

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Energetic Costs and Thermoregulation in Northern Fur See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/47447500 Energetic Costs and Thermoregulation in Northern Fur Seal (Callorhinus ursinus) Pups: The Importance of Behavioral Strategies for Thermal Balance in Furred Marine Mammals Article in Physiological and Biochemical Zoology · October 2010 Impact Factor: 2.4 · DOI: 10.1086/656426 · Source: PubMed CITATIONS READS 12 51 1 author: Heather Liwanag California Polytechnic State University, San L… 21 PUBLICATIONS 117 CITATIONS SEE PROFILE Available from: Heather Liwanag Retrieved on: 11 April 2016 898 Energetic Costs and Thermoregulation in Northern Fur Seal (Callorhinus ursinus) Pups: The Importance of Behavioral Strategies for Thermal Balance in Furred Marine Mammals Heather E. M. Liwanag* Introduction Department of Ecology and Evolutionary Biology, University The high thermal conductivity and heat capacity of water com- of California, Santa Cruz, California 95060 pared with air make the ocean especially thermally challenging to endotherms (Dejours 1987). Numerous studies have shown Accepted 7/23/2010; Electronically Published 10/15/2010 elevated resting metabolic costs for aquatic and semiaquatic mammals in water (Fish 1979; Dawson and Fanning 1981; Costa and Kooyman 1982; Williams 1986; Williams et al. 2001). ABSTRACT While raising metabolic rate is an effective mechanism by which to counteract heat loss, it represents an added energetic expense Behavioral thermoregulation represents an important strategy to the animal if employed over the long term. for reducing energetic costs in thermally challenging environ- In terrestrial environments, the importance of behavioral ments, particularly among terrestrial vertebrates. Because of the strategies for maintaining a favorable body temperature and cryptic lifestyle of aquatic species, the energetic benefits of such reducing the energetic costs of thermoregulation has been dem- behaviors in marine endotherms have been much more difficult to demonstrate. In this study, I examined the importance of onstrated for a wide variety of endotherms. Thermoregulatory behavioral thermoregulation in the northern fur seal (Callo- behaviors include postural changes, the selection of microhab- rhinus ursinus) pup, a small-bodied endotherm that spends itats, and huddling behavior (reviewed in Hafez 1964). These prolonged periods at sea. The thermal neutral zones of three behaviors can impart a significant metabolic savings by reduc- weaned male northern fur seal pups (body mass range p 11.8– ing thermoregulatory costs and promoting survival in harsh 12.8 kg) were determined by measuring resting metabolic rate environments (reviewed in Gilbert et al. 2009). One would using open-flow respirometry at water temperatures ranging expect in marine systems, where endotherms are faced with mL additional thermal challenges, that similar behavioral strategies 2.26 ע from 2.5Њ to 25.0ЊC. Metabolic rate averaged10.03 Ϫ1 Ϫ1 may be used to offset the costs of thermoregulation. As such, O2 kg min for pups resting within their thermal neutral 2.5ЊC , approxi- behavioral modification may represent an important strategyעzone; lower critical temperature was8.3Њ mately 8ЊC higher than the coldest sea surface temperatures for reducing thermoregulatory costs in the ocean. However, encountered in northern Pacific waters. To determine whether because of the cryptic habits of marine endotherms, the extent behavioral strategies could mitigate this potential thermal lim- to which behavioral thermoregulation is utilized and its relation itation, I measured metabolic rate during grooming activities to overall energetic costs or savings are unknown for most and the unique jughandling behavior of fur seals. Both sed- species. entary grooming and active grooming resulted in significant One known strategy for offsetting thermoregulatory costs is increases in metabolic rate relative to rest (P p 0.001 ), and the recycling of metabolic heat produced by activity, termed percent time spent grooming increased significantly at colder thermal substitution. The concept of thermal substitution of water temperatures (P ! 0.001 ). Jughandling metabolic rate heat produced by exercise is not new and has been demon- Ϫ1 Ϫ1 strated in several species of birds and rodents (reviewed in ע (mLO12.71 2.73 2 kg min ) was significantly greater than resting rates at water temperatures within the thermal neutral Lovvorn 2007). In marine systems, an increase in metabolic zone (P ! 0.05 ) but less than resting metabolism at colder water heat production associated with swimming exercise has been temperatures. These data indicate that behavioral strategies may demonstrated for sea otters, pinnipeds, and cetaceans (Costa help to mitigate thermal challenges faced by northern fur seal and Kooyman 1982, 1984; Williams 1999; Liwanag et al. 2009). pups while resting at sea. The use of thermal substitution to mitigate thermal stress has also been demonstrated for other at-sea behaviors. Grooming behavior has been shown to be an important part of the thermal budget of the sea otter (Costa and Kooyman 1982; Yeates 2006), * Present address: University of California, San Diego, La Jolla, California 92093; both because of its restoration of the insulating air layer in the e-mail: [email protected]. fur and because of its potential for thermal substitution. The sea otter also uses the metabolic increase associated with newly Physiological and Biochemical Zoology 83(6):898–910. 2010. ᭧ 2010 by The University of Chicago. All rights reserved. 1522-2152/2010/8306-9164$10.00. ingested food (heat increment of feeding [HIF]) for thermo- DOI: 10.1086/656426 regulation (Costa and Kooyman 1984). It has been argued that Fur Seal Energetics and Behavioral Thermoregulation 899 the sea otter requires these behavioral strategies to maintain weaning fur seal pups. To evaluate the importance of behavioral thermal balance because of its small body size and lack of a strategies for thermoregulation, I measured the energetic con- blubber layer (Costa and Kooyman 1982, 1984; Yeates et al. sequences of resting, jughandling positions, and grooming be- 2007). haviors on thermal metabolic responses in northern fur seals. Northern fur seals (Callorhinus ursinus L.), like sea otters, Together these tests provided quantitative measurements of the rely primarily on dense, waterproof fur for thermal insulation. energetic costs and benefits associated with thermoregulatory The pups of this species wean at 4 mo of age at a body size behaviors in a small-bodied marine endotherm. approximately 85% that of an adult sea otter. On weaning, northern fur seal pups remain at sea on a pelagic migration Material and Methods lasting up to 21 mo (Gentry and Holt 1986; Baker 2007; Lea Animals et al. 2009). Previous studies have shown that the combination of small body size and immature physiology makes fur seal Three weaned male northern fur seal pups were used in this pups and juveniles especially vulnerable to thermal stress in the study (Table 1). The animals were rescued by the Marine Mam- water (Donohue et al. 2000; Rutishauser et al. 2004). mal Center in Sausalito, California, at approximately 6 mo of While at sea, fur seal species display an unusual posture age (2 mo past the average weaning date for these animals), known as the jughandle position, floating with both hind flip- rehabilitated, and subsequently transferred to Long Marine pers and one foreflipper tucked and held above the water sur- Laboratory (University of California, Santa Cruz) for research. face in an arc (Fig. 1). The purpose of this behavior is largely Fur seals were fully rehabilitated and determined by veterinary unknown, but popular hypotheses suggest opposing thermo- staff to be in releasable condition before experimentation. Ex- regulatory consequences: the animals may remove the flippers periments were conducted for 2 mo, during which the animals from the water to avoid excessive heat loss to cold water, or were approximately 7–9 mo of age. Fur seals were maintained they may position the flippers in the air to increase convective in seawater pools and fed a daily diet of herring, capelin, and heat loss when warm (Bartholomew and Wilke 1956). Because squid supplemented with vitamins. Water temperatures in the the physiological consequences of jughandling behavior have holding pools reflected ambient coastal water conditions and yet to be measured, it has been difficult to distinguish the averaged 14.2ЊC (range: 10.7Њ–17.9ЊC) during the experimental thermoregulatory significance of this behavior for fur seals. period. Animal use was approved by the University of California In this study, I examined how behavioral strategies might Santa Cruz Chancellor’s Animal Research Committee, approval help to mitigate thermal challenges encountered by northern Will05.01. fur seal pups during their first at-sea migration. This was ac- complished by assessing the metabolic responses of weaned Protocol northern fur seal pups to different water temperatures. By de- termining the size of the thermal neutral zone (TNZ) and com- For metabolic measurements, fur seals were conditioned over paring the results to other marine mammals, I was able to several weeks to enter a seawater pool (2.3 m # 2.3 m quantify the relative thermal challenge experienced by post- wide # 1.0 m deep) of known water temperature, over which Figure 1. Northern fur seal pup in the jughandle position, with one foreflipper held between both hind flippers above the water. The other foreflipper
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