Energetics DANIEL P. COSTA. Energetics. I. Introduction Energetics provide a method to quantitatively assess the effort

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1 nergetics 383 Ortiz, R. M., Wade, C.., and Ortiz, C. L. ( 2000b ). Prolonged fasting increases the response of the renin angiotensin aldosterone system, but not vasopressin levels, in postweaned northern elephant seal pups. Gen. Comp. ndocrinol. 119, Ortiz, R. M., Wade, C.., and Ortiz, C. L. (2001a ). ffects of prolonged fasting on plasma cortisol and TH in post weaned northern elephant seal pups. Am. J. Physiol. 280, R790 R795. Ortiz, R. M., Noren, D. P., Litz, B., and Ortiz, C. L. (2001b). A new perspective on adiposity in a naturally obese mammal. Am. J. Physiol. ndocrinol. Metabol. 281, Ortiz, R. M., Wade, C.., Costa, D. P., and Ortiz, C. L. ( 2002 a). Renal effects of fresh water-induced hypo-osmolality in a marine adapted seal. J. Comp. Physiol. B 172, Ortiz, R. M., Wade, C.., Costa, D. P., and Ortiz, C. L. (2002b). Renal responses to plasma volume expansion and hyperosmolality in fasting seal pups. Am. J. Physiol. Regul. Inter. Comp. Physiol. 282, R805 R817. Ortiz, R. M., Houser, D. S., Wade, C.., and Ortiz, C. L. (2003a ). Hormonal changes associated with the transition between nursing and natural fasting in northern elephant seals (Mirounga angustirostris). Gen. Comp. ndocrinol. 130, Ortiz, R. M., Noren, D. P., Ortiz, C. L., and Talamantes, F. ( 2003b ). Ghrelin and growth hormone increase with fasting in a naturally adapted species, the northern elephant seal. J. ndocrinol. 178, Ortiz, R. M., Wade, C.., Ortiz, C. L., and Talamantes, F. ( 2003c ). Acutely elevated vasopressin increases circulating concentrations of cortisol and aldosterone in fasting northern elephant seal (Mirounga angustirostris ) pups. J. xp. Biol. 206, Ortiz, R. M., Crocker, D.., Houser, D. S., and Webb, P. M. (2006 ). Angiotensin II and aldosterone increase with fasting in breeding adult male northern elephant seals (Mirounga angustirostris). Physiol. Biochem. Zool. 79, Petrauskas, L., Tuomi, P., and Atkinson, S. ( 2006 ). Noninvasive monitoring of stress hormone levels in a female Steller sea lion (umetopias jubatus) pup undergoing rehabilitation. J. Zoo. Wildl. Med. 37 ( 1 ), Pietraszek, J., and Atkinson, S. (1994 ). Concentrations of estrone sulfate and progesterone in plasma and saliva, vaginal cytology, and bioelectric impedance during the estrous cycle of the Hawaiian monk seal (Monachus schaunslandi). Mar. Mamm. Sci. 10, Richmond, J. P., Burns, J. M., Rea, L. D., and Mashburn, K. L. (2005 ). Postnatal ontogeny of erythropoietin and hematology in free-ranging Steller sea lions (umetopias jubatus). Gen. Comp. ndocrinol. 141, Robeck, T. R., Schneyer, A. L., McBain, J. F., Dalton, L. M., Walsh, M. T., Czekala, N. M., and Kraemer, D. C. ( 1993 ). Analysis of urinary immunoreactive steroid metabolities and gonadotropins for characterization of estrous cycle, breeding period and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biol. 12, Skog,. B., and Folkow, L. P. (1994 ). Nasal heat and water exchange is not an effector mechanism for water balance regulation in grey seals. Acta Physiol. Scand. 151, St. Aubin, D. J. ( 2001 ). ndocrinology. In CRC Handbook of Marine Mammal Medicine (L. A. Dierauf, and F. M. D. Gulland, eds ), 2nd d, pp CRC Press, Boca Raton, FL. St. Aubin, D. J., and Geraci, J. R. (1986 ). Adrenocortical function in pinniped hyponatremia. Mar. Mamm. Sci. 2, St. Aubin, D. J., and Dierauf, L. A. (2001 ). Stress and marine mammals. In CRC Handbook of Marine Mammal Medicine (L. A. Dierauf, and F. M. Gulland, eds ), 2nd d, pp CRC Press, Boca Raton, FL. St. Aubin, D. J., Ridgway, S. H., Wells, R. S., and Rhinehart, H. (1996 ). Dolphin thyroid and adrenal hormones: Circulating levels in wild and semidomesticated Tursiops truncatus, and influence of sex, age, and season. Mar. Mamm. Sci. 12, Stokkan, K. A., Vaughan, M. K., Reiter, R. J., Folkow, L. P., Martensson, P.., Sager, G., Lydersen, C., and Blix, A. S. (1995). Pineal and thyroid functions in newborn seals. Gen. Comp. ndocrinol. 98, Theodorou, J., and Atkinson, S. (1998). Monitoring of total androgen concentrations in saliva from captive Hawaiian monk seals (Monachus schuainslandi). Mar. Mamm. Sci. 14(2 ), Tsubokawa, M., Kawauchi, H., and Li, C. H. (1980). Isolation and partial characterization of growth hormone from fin whale pituitary glands. Int. J. Biochem. (Tokyo) 88, Wallis, O. C., Maniou, Z., and Wallis, M. (2005). Cloning and characterization of the gene encoding growth hormone in finback whale (Balaenoptera physalus). Gen. Comp. ndocrinol. 143, West, K. L., Atkinson, S., Carmichael, M. J., Sweeney, J. C., Krames, B., andkrames, J. (2000). Concentrations of progesterone in milk from bottlenose dolphin during different reproductive status. Gen. Comp. ndo. 117, Yoshioka, M., Mohri,., Tobayama, T., Aida, K., and Hanyu, I. (1986). Annual changes in serum reproductive hormone levels in the captive bottlenosed dolphins. Bull. Japan Soc. Sci. Fish. 52, Zapol, W. M., Liggins, G. C., Schneider, R. C., Qvist, J., Snider, M. T., Creasy, R. K., and Hochachka, P. W. (1979). Regional blood flow during simulated diving in the conscious Weddell seal. J. Appl. Physiol. 47, Zenteno-Savin, T. and Castellini, M. A. ( 1998 ). Changes in the plasma levels of vasoactive hormones during apnea in seals. Comp. Biochem. Physiol. 119C, nergetics DANIL P. COSTA I. Introduction nergetics provide a method to quantitatively assess the effort animals spend acquiring resources, as well as the relative way in which they allocate those resources. nergy flow models are analogous to cost benefit models used in economics. Costs take the form of energy expended to acquire and process prey, and to maintain body functions. The energetic benefits are manifest as food energy used for growth and reproduction. Measurement of energy acquisition and allocation provide a quantitative assessment of how animals organize their daily or seasonal activities, and how they prioritize their behaviors. Thus, energy flow can be described as what goes into the animal as food and what comes out in the form of growth, reproduction, repair, waste, or metabolic work. Survival requires a positive balance between the costs of maintenance and the acquisition of food energy. If a marine mammal cannot compensate for decreases in energy acquisition, it must either reduce its overall rate of energy expenditure or utilize stored energy reserves. Conversely, in order to grow and reproduce, animals must obtain more energy than is needed to survive. Marine mammals undergo profound variations in this feast or famine dynamic equilibrium as they can gain significant amounts of food energy while feeding in highly productive environments, followed by prolonged negative energy balance while fasting during migration or reproduction (Brodie, 1975; Costa, 1993; Lockyer, 1993) (Fig. 1 ). The balance of how energy acquisition and expenditure is achieved differs for individual species and environments. For

2 384 nergetics Fecal energy (F) Urinary energy (U) Heat output Prey availability and quality Prey acquisition (I) Metabolism and synthesis (M) BMR Thermoregulation HIF Activity Growth Storage Reproduction Repair Production of young Metabolic cost of acquiring prey Figure 1 A conceptual diagram of energy flow through a typical mammal. The outer oval represents the animal. Anything that passes through that envelope is material (straight line) or energy (waved line) entering or leaving the animal. I, ingested energy; M, metabolic energy; F, fecal energy; and U, urinary energy. Figure 2 A minke whale, Balaenoptera acutorostrata, feeding in the Antarctic ice. Photograph by Dan Costa. some species, sea otters (nhydra lutris), sea lions, and fur seals (Otariidae), very high rates of energy expenditure are met by high rates of energy acquisition ( Costa and Williams, 2000 ). These animals preferentially live in nearshore environments or upwelling regions where food is abundant ( Costa, 1993 ). Sirenians represent the opposite extreme. These marine mammals exhibit comparatively low existence costs and are able to survive on a low-quality diet. They have adapted to a diet of grasses that is in high abundance but of low quality, energetically. They are able to do this because; they live in the climatically benign tropics where maintenance costs are low (Gallivan and Best, 1980; Gallivan et al., 1983; Irvine, 1983). The seasonal migrations of large cetaceans demonstrate this interrelationship between energetic demand, energy availability, and local productivity ( Brodie, 1975 ). Although maintenance costs may be elevated in polar regions, the ability to take advantage of the seasonally high productivity associated with the sea ice during the polar summer more than compensates ( Fig. 2 ). When confronted with the high energetic costs of reproduction and of winter conditions, the mysticete whales opt for the more benign tropics. Further, their large body size makes the cost of migration extremely low (see Locomotion, this volume). While prey availability may be low in the tropics, so too are the existence costs, especially for a large animal that is able to utilize energy reserves stored in the blubber. A conceptual diagram of the relationship between energy acquisition and allocation is shown in Fig. 1. The rate of energy consumed by the animal is referred to as Ingested nergy (I). The energy that remains after the losses associated with the production of feces and urine is the Metabolic nergy (M). This is the energy available for maintenance and repair, growth or reproduction. nergy expended for maintenance includes key processes such as basal metabolism, digestion (heat increment of feeding, HIF), thermoregulation, and activity (locomotion, grooming, feeding, etc.). The rate of prey energy acquired is directly related to the availability and quality of prey. As prey becomes less available, the cost of finding it increases and the animal spends a greater proportion of its time and therefore energy searching for it. ventually, there is a threshold when more energy is spent searching for prey than is obtained and the animal goes into negative energy balance (Winship et al., 2002; Rosen and Trites, 2005). While the best situation is to have access to abundant high energy prey, in some scenarios low-quality prey that is more abundant may be more optimal than searching for high-quality prey that is difficult to find. II. nergy Acquisition Not all of the ingested material consumed is digestible. Food energy remaining after digestion and elimination of Fecal nergy (F) is known as the Apparently Digested nergy (AD). The proportion of AD to I is called the assimilation efficiency and ranges from 88% to 97.9%, for a diet of fish to 72.2% for invertebrate prey with a high chitin content (Martensson et al., 1994; Lawson et al., 1997; Costa and Williams, 2000; Rosen and Trites, 2000). The assimilation efficiency decreases as the rate of prey intake increases, but is greater when a diet composed of different species of fish with

3 nergetics 385 different proximate compositions is consumed ( Trumble and 10,000 Castellini, 2005 ). Sirenians extract less energy from their food than other marine mammals (84.6%), because plant material, which contains cellulose and requires bacterial fermentation to digest, is harder to digest. However, they are more efficient than other hindgut fermenters, such as horses, quus caballus (45 59%) ( Burn, 1986 ). 0 Chemical energy lost as urea and other metabolic end products in the urine is defined as Urinary nergy (U). Metabolizable nergy (M) is the net energy remaining after fecal and urinary energy loss, and represents the energy available for growth or reproduction and for supporting metabolic processes such as work (locomotion) and respiration (thermoregulation, maintenance metabolism, HIF). The M for pinnipeds varies between 78.3% for a squid diet to 91.6% for an anchovy diet ( Costa and Williams, 2000 ). 10 III. nergy xpenditure A. Cost of Maintenance Functions Maintenance costs are those associated with homeostasis and include basal metabolism, HIF, repair (molt, fighting disease, and/or parasites), thermoregulation, and activity (see Thermoregulation and Locomotion, this volume). 1. Basal Metabolism It has generally been assumed that the basal metabolic rates of aquatic mammals are elevated when compared to terrestrial mammals of similar size. The current view of basal metabolic rates of marine mammal is more complex as many studies did not conform to standardized criteria for measurements of basal metabolism ( Lavigne et al., 1986 ). These criteria require that the subjects be adults, resting, thermoneutral, non-reproductive, and post-absorptive. This has been further confused by the expectation that all marine mammals should employ the same metabolic response. Specialization for marine living has occurred independently in three mammalian orders: the sirenians, cetaceans, and carnivores. Further, within the carnivores there are three separate transitions to a marine existence: pinnipeds, sea otters, and polar bears, Ursus maritimus. Based on this diversity, we might expect different metabolic adaptations between the groups ( Fig. 3 ). West Indian manatees, Trichechus manatus, have BMRs lower than values predicted, while phocid seals have BMRs closer to those of similar sized terrestrial mammals. Conversely, sea otters, otariids, and odontocetes appear to have BMRs greater than terrestrial mammals of equal size. The BMR of an animal is not constant, but varies seasonally (Rosen and Renouf, 1995; Williams et al., 2007), with the animal s nutritional state ( Rosen and Trites, 1999 ), as well as with the animal s body composition ( Rea and Costa, 1992 ). Some species such as sirenians and walrus, Odobenus rosmarus, have dense bone, whereas seals may be composed of as much as 50% fat. When metabolic rates are expressed relative to body mass, a disproportionate amount of fat or particularly dense bone will lower the apparent metabolic rate. This is due to the low metabolic rates of bone and adipose tissue in comparison to lean tissue. Many marine mammals undergo prolonged fasts that are accompanied by profound changes in body composition. Most of the mass change during fasting is due to loss of adipose tissue with a comparatively smaller change in lean tissue. For example, northern elephant seal females, Mirounga angustirostris, loose 42% of their initial mass, but of this only 14.9% comes from lean tissue with 57.9% coming from adipose tissue ( Costa et al., 1986 ). This results in an overall change in body composition of 39% fat at parturition to 24% fat at weaning (see Pinnipedia Physiology, this volume). Since lean mass is the primary contributor to whole Resting metabolic rate (W) Odontoceti Sirenia Phocidae Otariidae. lutris 2 X Predicted Predicted 10 0 Mass (kg) Figure 3 Resting metabolic rate (RMR) of marine mammals in relation to body mass. Measurements were made for the animals resting in water. The solid line denotes the predicted metabolic rate for equal sized terrestrial animals; the dashed line represents 2 times the predicted levels. Species included are: Odontoceti Stenella attenuata, Tursiops truncatus ; Phocidae Phoca vitulina, Phoca hispida, Leptonychotes weddellii, Pagophilus groenlandicus, Haliochoerus grypus; Otariidae Zalophus californianus; Sirenia Trichechus manatus. animal metabolism, the animals whole body metabolism is likely to change little even though there has been a major change in its body mass ( Rea and Costa, 1992 ). The ability to digest and process the greater amount of prey associated with the higher metabolic rates of marine mammals may have also required changes in their morphology. Specifically, all carnivorous marine mammals, regardless of their ancestry (carnivore or herbivore) have comparatively longer small intestines than similarly sized terrestrial carnivores. Further, there is a high correlation between small intestine length and BMR in mammals ( Williams et al., 2001 ). 2. Heat Increment of Feeding When food is consumed, the animal s metabolic rate increases over fasting levels. The HIF, also known as the Specific Dynamic Action (SDA), may be considered the tax that is required to process food energy for conversion to Metabolizable nergy (M). The magnitude of energy allocated to HIF varies between 5% and 17% of the M (Costa and Kooyman, 1984; Markussen et al., 1994; Rosen and Trites, 1997). In addition, the duration of HIF following a meal will depend on the amount of food consumed and its composition. In many mammals, the HIF is considered excess or waste heat. However, sea otters incorporate the additional heat produced from HIF to meet their high thermoregulatory costs associated with their small size (they are the smallest marine mammal) ( Costa and Kooyman, 1984 ). While grooming, feeding, and swimming sea otters use the heat produced from activity to supplement their thermoregulatory needs, while at rest sea otters incorporate the heat produced from HIF to augment their thermoregulatory needs ( Fig. 4 ). 3. Fur vs BlubberIt is important to consider the potential differences in the energy budgets of animals that use fur or blubber for insulation. The overall time energy budget of an animal that uses fur (fur seal or sea otter) is fundamentally different from an animal that uses blubber (sea lion, seal, or dolphin). Although fur is not a living

4 386 nergetics SDA Activity 80 % Above SMR Time since feeding (min) Figure 4 The thermal budget of sea otters relies on heat production above BMR (or SMR). The contribution of HIF (or SDA) to the overall metabolism is highest immediately after feeding and reaches zero within 390 min after feeding. As HIF decreases the animal becomes more active and thus compensates for the decrease in heat production from HIF ( Costa and Kooyman, 1984 ). Figure 5 A group of California sea lions, Zalophus californianus, huddling on a California beach. A behavior typical in the cool winter months or during the cool mornings. Photograph by Dan Costa. tissue, it requires the maintenance of an air layer, which is done by frequent grooming. Sea otters spend up to 16% of their day grooming. While sea lions, seals and dolphins, spend no time grooming, they must take in sufficient food to lay down a thick blubber layer, which is a living tissue and must be supplied with blood. Furthermore, blubber serves dual roles as an insulator and as an energy store. During fasting or periods of low food availability a marine mammal must balance its utilization of blubber for energy needs with the potential loss of the blubber layer as an insulator. For pinnipeds a way of increasing blood flow to the skin and keeping thermoregulatory costs low while ashore is to huddle together. This reduces their effective surface area that is exposed to the cold ( Fig. 5 ). Such behavior is commonly observed in cold climates and can change during the day. For example, in the morning when it is cold, animals clump together and as it gets warmer they separate. Finally, huddling behavior is less common in fur seals, as there isn t much of an incentive to huddle if you use fur for insulation. B. Cost of Growth and Reproduction For growth and reproduction to occur, an animal must acquire energy and nutrients in excess of that required for supporting maintenance functions. These additional energetic costs vary with the species of marine mammal, the sex, and reproductive pattern. In pinnipeds, polar bears, sea otters (and probably mysticetes and sirenians) the cost of reproduction in males is limited to the cost of finding and maintaining access to estrous females. volution favors a pattern of energy expenditure that maximizes reproductive success in males. The costs associated with reproduction in aquatic and terrestrially breeding males is quite similar when normalized for differences in body mass. Larger body size is preferred in terrestrially breeding male pinnipeds since it confers both an advantage in fighting and allows the male to maintain terrestrial territories longer ( Fig. 6 ) (see Pinnipedia Physiology, this volume). In addition, larger animals can fast longer because they have a lower mass specific metabolic rate than smaller animals ( Costa, 1993 ). In species that compete Figure 6 The extreme difference in body size between a male (on top) and female (underneath) northern elephant seal (Mirounga angustirostris). The animals are copulating in this picture. Photograph by Dan Costa. for females in the water, males are comparatively smaller than the species that breed on land. For the aquatic breeders, underwater agility is more important than large size when competing for mates. The cost of reproduction for females can be broken down into the energetic requirements of gestation and lactation. The cost of gestation is small relative to the cost of lactation. ven given the strikingly different reproductive patterns in marine mammals, there is little variation in fetal mass at birth among marine mammals, but as a group they appear to invest more energy into fetal birth mass (and thus more into gestation) than terrestrial mammals ( Fig. 7 ). This higher investment in gestation by all marine mammals except polar bears is associated with the production of precocial young ( Fig. 8 ). The young of cetaceans, sirenians, pinnipeds, and sea otters need to be capable of dealing with life in the water or on a crowded rookery within seconds of birth. As a group marine mammals exhibit considerable variation in both the duration and pattern of maternal investment ( Fig. 9 ). Phocid seals and mysticete whales have extremely short lactation durations, which are compensated for by higher rates of energy transfer that enable the young to grow rapidly ( Fig. 10 ). Although phocid pups are weaned early, they still rely on maternally derived energy, stored as blubber, for weeks or months after weaning. The disadvantage of this rapid growth is that most of the

5 nergetics 387 mass and energy is stored as fat with proportionately little protein. The advantage of longer lactation is that young get more protein and other nutrients allowing greater growth of lean tissue. However, longer lactation is energetically more expensive (Costa, 1991a, b, 1993 ). Birth mass (kg) 10, Odontoceti Mysticeti Sirenia Phocidae Otariidae Odobenidae U. maritimus. lutris Terrestrial mammals ,000,000 Maternal mass (kg) Figure 7 Birth mass plotted in relation to maternal mass for marine and terrestrial mammals. Species of marine mammals included are: Odontoceti Inia geoffrensis, Pontoporia blainvillei, 1400 Stenella attenuata, Globicephala melaena, Physeter macrocephalus, T. truncatus, Phocoena spinnipinnis, P. phocoena, Delphinapterus leucas ; Mysticeti Balaenoptera musculus, B. physalus, B. acutorostrata, B. borealis, Megatpera novaengliae, schrictius robustus ; Phocidae Mirounga angustirostris, M. leonina, Cystophora cristata, Phoca vitulina, P. hispida, Leptonychotes weddelli, Monachus schauinslandi, Pagophilus groenlandicus, rignathus barbatus, Lobodon carcinophagus, Histriophoca fasciata, Haliochoerus grypus ; Otariidae Arctocephalus gazella, A. forsteri, A. galagagoensis, 1. Variation in Milk CompositionThe rapid growth of marine mammal young is made possible by the ingestion of extremely lipid rich milk. With a few exceptions, terrestrial animals produce milk that is low in fat; cows, Bos taurus and humans, Homo sapiens, produce milk that contains 3.7% and 3.8% milk fat, respectively. Lipidrich milk allows the mother to transfer high levels of energy in a very short period. Hooded seals, Cystophora cristata, are most impressive with a 4-day lactation interval and a milk fat of 65% lipid ( Bowen et al., 1985 ). In view of this, it is not surprising that marine mammals with the highest growth rates produce milk with the highest lipid content. Lactation also enables mothers to optimize the delivery of energy to their young. The energy content of the milk is independent of the type or quality of prey consumed, or the distance or time taken to obtain it. Although milk is ultimately derived from the prey consumed, a mother can process, concentrate, or utilize stored reserves to produce milk. For example, some species feed on fish, while others feed on fish or squid. Yet, all of these species provision their offspring with milk of significantly greater energy density than the prey consumed ( Costa, 1991b ). 2. Body Size and Maternal Resources: The Role of Maternal OverheadFasting during lactation is a unique component of the Time to weaning (days) Odontoceti Mysticeti Sirenia Phocidae Otariidae Odobenidae U. maritimus lutris A. tropicalis, A. pusillis, Callorhinus ursinus, Zalophus californianus, 0 Neophoca cinerea, umatopias jubatus, Otaria byronia ; Sirenia Dugong dugon, Trichechus manatus ,000,00 Maternal mass (kg) Figure 9 Time to weaning plotted as a function of maternal mass for marine mammals. Lactation durations of phocid seals and mysticete whales are shorter than in all other marine mammals. Species are same as in Fig. 3. Growth rate of young (kg day 1 ) Odontoceti Mysticeti Phocidae Otariidae Odobenidae U. maritimus. lutris ,000,000 Figure 8 A harbor seal ( Phoca vitulina), mother and pup on a Maternal mass (kg) California beach. The pup was recently born and shows the extreme level of precociality typical for marine mammals. In harbor seals the Figure 10 Growth rate of suckling marine mammals as a function pup is born with the adult pelage and it can go to sea within an hour of maternal mass. Lines represent least squares regressions for each of birth. Photograph by Dan Costa. taxonomic group. Species are same as in Fig. 3.

6 388 nergetics life history pattern of marine mammals (Costa, 1993; Oftedal, 2000). With the exception of bears, no other mammal is capable of producing milk without feeding. By undertaking this energetic challenge, mysticetes and pinnipeds are able to separate where and when they feed from where and when they breed. In mysticete whales, this allows them to feed in the highly productive polar regions of the world s oceans, but retain the thermal advantage of breeding in the calm tropical regions ( Fig. 2 ) ( Brodie, 1975 ). Migrating to warmer waters for parturition reduces the thermal demands on the newborn calf and additional thermal savings for the mother. Figure 11 A recently born northern elephant seal (Mirounga angustirostris) pup suckles from its mother (below) is compared to a recently weaned pup (30 days old). The mother does not eat or drink during the 26- to 28-day lactation interval, and after weaning the pup fasts for 2 3 months before going to sea. lephant seals, like many true seals, fast during the entire lactation interval. Photograph by Dan Costa. Among pinnipeds, the separation of feeding from lactation is necessary to allow for terrestrial parturition ( Bartholomew, 1970 ). Most phocids store sufficient energy reserves for the entire lactation period, whereas all otariids must feed during lactation (see Pinnipedia Physiology and Pinniped Reproduction, this volume) (Costa, 1991a, b ). A phocid mother typically remains on or near the rookery continuously from the birth of the pup until it is weaned; whereas milk is produced from body reserves stored prior to parturition ( Fig. 11 ). Although some phocids feed during lactation, most of the maternal investment is derived from body stores. Their reproductive pattern is less constrained by the time it takes to travel and exploit distant prey, which allows utilization of a more dispersed or patchy food resource ( Costa, 1993 ). By spreading out the acquisition of prey energy required for lactation over many months at sea, northern elephant seal females only need to increase their daily food intake by 12% to cover the entire cost of lactation. The ability of a marine mammal female to fast while providing milk to her offspring is related to the size of her energy and nutrient reserves and the rate at which she utilizes them. When food resources are far from the breeding grounds, as may occur for some phocids and large mysticete whales, the optimal solution is to maximize the amount of energy and nutrients provided to the young and to minimize the amount of energy expended on the mother. The term metabolic overhead refers to the amount of energy a female expends on herself while onshore (seals) or while in the calving grounds (whales). Larger females have a lower metabolic overhead than smaller females. This is because maintenance metabolism scales as mass 0.75, and fat stores scale as mass 1.0. As body size increases, energy reserves increase proportionately faster than maintenance metabolism. 3. nergy Investment and Trip DurationMany phocids fast throughout the lactation interval, whereas otariid females feed intermittently between suckling bouts onshore ( Fig. 12 ) ( Costa, 1991a, b ). Otariid mothers modify the timing and patterning of energy and nutrient investment to optimize energy delivery to their young (Boyd, 1998; Trillmich and Weissing, 2006). Otariid mothers making short feeding trips that provide their pups with less milk energy than mothers that make long trips. In comparison to otariids, phocids may have a reproductive pattern that is better suited for dealing Figure 12 A Galapagos sea lion ( Zalophus wollebaeki) female suckling her pup on left, and on a trip to sea on right. Fur seals and sea lions intermittently suckle their pup on shore between trips to sea to forage. Photograph by Dan Costa.

7 nergetics 389 with dispersed or unpredictable prey, or prey that is located at great distances from the rookery ( Costa, 1993 ). However, fasting during lactation places a limit on the duration of investment and this limits the total amount of energy that a phocid mother can invest in her pup. Phocids are buffered from short-term fluctuations in prey availability due to their unique reproductive pattern. In phocids, reproductive performance (maternal investment) during a given season reflects prey availability over the preceding year and represents the mother s foraging activities over a much larger spatial and temporal scale than the foraging activities of otariids ( Costa, 1993 ). It follows that the weaning mass of a phocid pup is an indicator of the mother s foraging success over the previous year, whereas the subsequent post-weaning survival of the pup is related to both its weaning mass (energy reserves provided by the mother) and the resources available to the pup after weaning. C. Field Metabolic Rates A number of approaches have been used to study the metabolic rate of animals at sea. One approach, time budget analysis, sums the daily metabolic costs associated with various activities ( Williams et al., 2004 ). Other methods rely on predictive relationships between physiological variables and metabolic rate. For example, metabolic costs can be indirectly assessed by measurements of changes in body mass and composition, variations in heart rate or ventilation rate, or with the dilution of isotopically labeled water (Folkow and Blix, 1992; Boyd et al., 1999; Costa and Gales, 2000). Field metabolic rates (FMR) provide insight into the energetic strategies used by marine mammals (Costa, 1993; Costa and Gales, 2003). The best data exist for pinnipeds and the common bottlenose dolphin, Tursiops truncatus ( Fig. 13 ), and indicate that foraging otariids and bottlenose dolphins expend energy at 6 times the predicted basal metabolic level ( Costa and Williams, 2000 ). In contrast, the metabolic rate of diving elephant seals (Mirounga spp.) and Weddell, Leptonychotes weddellii, seals are only times the predicted basal rate ( Castellini et al., 1992 ). The lower diving metabolic rate of phocid seals contributes to their superb diving ability ( Costa, 1993 ) (see Diving Physiology, this volume). The importance of the thermal environment on field metabolic rate can also be seen in Galapagos fur seals, Arctocephalus galapagoensis, which due to the warm equatorial climate have a substantially reduced field metabolic rate compared to other otariids ( Trillmich and Kooyman, 2001 ). An interesting consequence of the high metabolic rate of marine mammals is that the presence of a few foraging individual can have a significant impact on community structure (stes et al., 1998; Springer et al., 2003). FMR are quite variable both between and within species ( Fig. 13 ). Such variation is thought to be associated with year-to-year changes in both the abundance and availability of prey ( Costa, 2007 ). In response to reduced availability of prey, fur seals and sea lions mothers increased their foraging effort in an effort to keep the duration of their foraging trip the same. However, there reaches a point where they can no longer increase their foraging effort and have to spend more time at sea to obtain the same amount of prey energy. If a mother spends more time to deliver the same amount of energy, the offspring receives less overall energy. As a result, more of the offspring s energy is spent on maintenance and its growth will slow and in the worst case the pup will eventually die. 1. nergetics of Prey ChoiceThe amount of work, and therefore energy expenditure that an animal puts into locating prey varies At sea metabolic rate (W) 0 Predicted BMR Body mass (kg) Z. californianus L. weddelli A. gazella T. truncatus C. ursinus Otariidae A. galapagoensis Predicted BMR M. angustirostris Figure 13 At sea metabolic rate measurements determined from the O-18 doubly labeled water method as a function of body mass. Data on Weddell seals ( Leptonychotes weddellii) were measured using open circuit respirometry on seals diving from an ice hole. The solid line represents the predicted basal metabolic rate for a terrestrial animal of equal size; the dashed line is the best-fit linear regression for the otariidae with the exception of the data from Arctocephalus galapagoensis (r ). rror bars represent one standard deviation. Multiple points for each species reflect measurements taken over different years and show the range of interannual variation within a species. as a function of the energy content, availability, and location of the prey both geographically as well as its depth in the water column. Both size and proximate composition (fat, carbohydrate, protein, and water content) affect the energy content of prey. Prey availability varies as a function of the absolute abundance of prey (amount of prey per unit of habitat) and its distribution in the environment. A predator is more efficient when foraging on prey that is clumped than on prey that is evenly dispersed. Similarly, prey that is near the surface is easier to obtain than prey located at depth. Marine mammals forage in areas where prey has been concentrated as a result of oceanographic processes like eddies, fronts, and upwelling regions associated with bottom topography. Sea otters provide an excellent example of the factors that determine the energetics of prey choice ( Fig. 14 ) (Riedman and stes, 1990 ). In recently occupied areas, sea otters feed on preferred prey items like clams, abalone, Haliotis spp., or sea urchins. In such environments they find large, energy-rich, abundant prey that is easy to handle, consume, and digest. In such situations, lower quality prey items (turban snails, sea stars, mussels, chitons) are generally not eaten. These items may be abundant, but they are energy poor, and difficult to eat and digest. As the abundance and size of their preferred prey declines, sea otters switch to less preferred but more accessible prey like turban snails, kelp crabs, and in some cases, chitons and sea stars. Some sea otters specialize on different types of prey and are more efficient predators than non-specialists ( stes et al., 2003 ).

8 390 nergetics Figure 14 A California sea otter feeds on a crab. Photograph by Dan Costa. Polar bears represent another example of optimal prey choice and its relation to the prey energy quality. Feeding predominately on ring seals, Phoca hispida, polar bears eat the energy-rich blubber layer and leave behind the lean core of the carcass ( Stirling and Mcwan, 1975 ). Due to its high lipid content the blubber has a per unit mass energy content almost 10 times greater than that of the lean tissue of the ring seal. Thus, polar bears consume the most energy dense part of the ring seal and then move on to find another kill. 2. Variations in Foraging nergetics Different foraging behaviors are associated with different metabolic costs. For example, in sea lions benthic foraging is more expensive than epipelagic or near surface feeding (Costa and Gales, 2000, 2003 ). The gulping behavior of blue, Balaenoptera musculus, fin, B. physalus, and other whales of the family Balaenopteridae also appears to be quite costly due to the tremendous drag created as they open their enormous mouths to engulf entire schools of prey ( Croll et al., 2001 ). The blue whale finds a school of krill, and opens its mouth engulfing the entire school of krill. The whale then expels the water through its baleen plates, retaining the krill in its mouth. Consider how much drag, and thus increased effort, it takes to swim with an open mouth the size of a blue whale through the water! See Also the Following Articles Diving Physiology Pinniped Physiology Thermoregulation References Bartholomew, G. A. ( 1970 ). A model for the evolution of pinniped polygyny. volution 24, Bowen, W. D., Oftedal, O. T., and Boness, D. J. (1985 ). Birth to weaning in 4 days: Remarkable growth in the hooded seal, Cystophora cristata. Can. J. Zool. 63, Boyd, I. L. (1998 ). Time and energy constraints in pinniped lactation. Am. Nat. 152, Boyd, I. L., Bevan, R. M., Woakes, A. J., and Butler, P. J. ( 1999 ). Heart rate and behavior of fur seals: Implications for measurement of field energetics. Am. J. Physiol. Heart Circ. Physiol. 45, H844 H857. Brodie, P. F. (1975 ). Cetacean energetics, an overview of intraspecific size variation. cology 56, Burn, D. M. (1986 ). The digestive strategy and efficiency of the West Indian manatee, Trichechus manatus. Comp. Biochem. Physiol. 85A, Castellini, M. A., Kooyman, G. L., and Ponganis, P. J. ( 1992 ). Metabolic rates of freely diving Weddell seals correlations with oxygen stores, swim velocity and diving duration. J. xp. Biol. 165, Costa, D. P. (1991a). Reproductive and foraging energetics of pinnipeds: Implications for life history paterns. In Behaviour of Pinnipeds (D. Renouf, ed. ), pp Chapman and Hall Ltd., London. Costa, D. P. (1991b). Reproductive and foraging energetics of high latitude penguins, albatrosses and pinnipeds: Implications for life history patterns. Am. Zool. 31, Costa, D. P. (1993 ). The relationship between reproductive and foraging energetics and the evolution of the Pinnipedia. In Marine Mammals: Advances in Behavioural and Population Biology (I. L. Boyd, ed. ), 66, pp Oxford University Press, Symposium Zoological Society of London, Oxford. Costa, D. P. (2007 ). A model of the variation in parental attendance in response to environmental fluctuation: Foraging energetics of lactating sea lions and fur seals. Aquat. Conserv.: Mar. Freshw. cosys. 17, S44 S52. Costa, D. P., and Kooyman, G. L. (1984 ). Contribution of specific dynamic action to heat balance and thermoregulation in the sea otter nhydra lutris. Physiol. Zool. 57, Costa, D. P., and Williams, T. M. ( 2000 a). Marine mammal energetics. In The Biology of Marine Mammals (J. Reynolds, and J. Twiss, eds ), pp Smithsonian Institution Press, Washington, DC. Costa, D. P., and Gales, N. J. ( 2000b ). Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. J. xp. Biol. 203, Costa, D. P., and Gales, N. J. ( 2003 ). nergetics of a benthic diver: Seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. col. Monogr. 73, Costa, D. P., Le Boeuf, B. J., Huntley, A. C., and Ortiz, C. L. ( 1986 ). The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J. Zool. 209, Croll, D. A., Acevedo-Gutierrez, A., Tershy, B. R., and Urban-Ramirez, J. (2001 ). The diving behavior of blue and fin whales: Is dive duration shorter than expected based on oxygen stores? Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 129, stes, J. A., Tinker, M. T., Williams, T. M., and Doak, D. F. ( 1998 ). Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, stes, J. A., Riedman, M. L., Staedler, M. M., Tinker, M. T., and Lyon, B.. (2003 ). Individual variation in prey selection by sea otters: Patterns, causes and implications. J. Anim. col. 72, Folkow, L. P., and Blix, A. S. (1992 ). Metabolic Rates of minke whales (Balaenoptera acutorostrata ) in cold water. Acta Physiol. Scand. 146, Gallivan, G. J., and Best, R. C. ( 1980 ). Metabolism and respiration of the Amazonian manatee (Trichechus inunguis). Physiol. Zool. 53, Gallivan, G. J., Best, R. C., and Kanwisher, J. W. ( 1983 ). Temperature regulation in the Amazonian Manatee Trichechus inunguis. Physiol. Zool. 56, Irvine, A. B. (1983 ). Manatee metabolism and its influence on distribution in Florida. Biol. Conserv. 25, Lavigne, D. M., Innes, S., Worthy, G. A. J., Kovacks, K. M., Schmitz, O. J., and Hickie, J. P. ( 1986 ). Metabolic rates of seals and whales. Can. J. Zool. 64, Lawson, J. W., Miller,. H., and Noseworthy,. ( 1997 ). Variation in assimilation efficiency and digestive efficiency of captive harp seals (Phoca groenlandica) on different diets. Can. J. Zool. 75, Lockyer, C. (1993 ). Seasonal changes in body fat condition of northeast Atlantic pilot whales, and their biological significance. In Reports of the International Whaling Commission Special Issue, 14. Biology of Northern Hemisphere Pilot Whales (G. P. C. H. L. Donovan,

9 ntrapment and ntanglement 391 anda. R. Martin, eds ), pp Cambridge University Press, Cambridge. Markussen, N. H., Ryg, M., and Øritsland, N. A. (1994 ). The effect of feeding on the metabolic rate in harbor seals (Phoca vitulina). J. Comp. Physiol. [B] 164, Martensson, P.., Nordoy,. S., and Blix, A. S. ( 1994 ). Digestibility of krill (uphausia superba and Thysanoessa sp.) in minke whales (Balaenoptera acutorostrata) and crabeater seals (Lobodon carcinophagus). Br. J. Nutr. 72, Oftedal, O. T. (2000 ). Use of maternal reserves as a lactation strategy in large mammals. Proc. Nutr. Soc. 59, Oftedal, O. T., Boness, D. J., and Tedman, R. A. ( 1987 ). The behavior, physiology, and anatomy of lactation in the Pinnipedia. Curr. Mammal. 1, Rea, L. D., and Costa, D. P. ( 1992 ). Changes in standard metabolism during long-term fasting in northern elephant seal pups (Mirounga angustirostris). Physiol. Zool. 65, Riedman, M. L., and stes, J. A. ( 1990 ). The sea otter nhydra lutris behavior ecology and natural history. US Fish Wildl. Serv. Biol. Rep. 90, Rosen, D., and Renouf, D. ( 1995 ). Variation in the metabolic rates of captive harbour seals. In Whales, Seals, Fish and Man (A. S. Blix, L. Walloe, and O. Ulltang, eds ), pp lsevier Science B.V, Amsterdam. Rosen, D. A., and Trites, A. W. (1997 ). Heat increment of feeding in Steller sea lions, umetopias jubatus. Comp. Biochem. Physiol. A 118, Rosen, D. A. S., and Trites, A. W. (1999 ). Metabolic effects of low-energy diet on Steller sea lions, umetopias jubatus. Physiol. Biochem. Zool. 72, Rosen, D. A. S., and Trites, A. W. (2000 ). Digestive efficiency and drymatter digestibility in Steller sea lions fed herring, pollock, squid, and salmon. Can. J. Zool. 78, Rosen, D. A., and Trites, A. W. ( 2005 ). xamining the potential for nutritional stress in young Steller sea lions: Physiological effects of prey composition. J. Comp. Physiol. [B] 175, Springer, A. M., et al. (8 authors) (2003 ). Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? Proc. Natl. Acad. Sci. USA, Stirling, I., and Mcwan,. H. (1975 ). The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can. J. Zool. 53, Trillmich, F., and Kooyman, G. L. (2001 ). Field metabolic rate of lactating female Galapagos fur seals (Arctocephalus galapagoenis): The influence of offspring age and environment. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 129, Trillmich, F., and Weissing, F. J. (2006 ). Lactation patterns of pinnipeds are not explained by optimization of maternal energy delivery rates. Behav. col. Sociobiol. 59, Trumble, S. J., and Castellini, M. A. (2005 ). Diet mixing in an aquatic carnivore, the harbour seal. Can. J. Zool. 83, Williams, T. M., Haun, J., Davis, R. W., Fuiman, L. A., and Kohin, S. (2001 ). A killer appetite: Metabolic consequences of carnivory in marine mammals. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 129, Williams, T. M., Fuiman, L. A., Horning, M., and Davis, R. W. ( 2004 ). The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: Pricing by the stroke. J. xp. Biol. 207, Williams, T. M., Rutishauser, M., Long, B., Fink, T., Gafney, J., Mostman-Liwanag, H.,, and Casper, D. ( 2007 ). Seasonal variability in otariid energetics: Implications for the effects of predators on localized prey resources. Physiol. Biochem. Zool. 80, Winship, A. J., Trites, A. W., and Rosen, D. A. S. (2002 ). A bioenergetic model for estimating the food requirements of Steller sea lions umetopias jubatus in Alaska, USA. Mar. col. Prog. Ser. 229, ntrapment and ntanglement JON LIN Fishermen use a variety of techniques to capture fish. A common method is the use of gill nets that hang passively in the water, like curtains, and ensnare fish that blunder into them, or with barriers such as cod traps that direct the fish into traps that hold them until they are removed. Because fishing nets are an unusual barrier, cryptic, and hard to detect, they on occasion catch marine mammals. When non-target species are accidentally caught in nets, they are termed bycatch. Bycatches of some species of marine mammals, such as harbor porpoises, Phocoena phocoena, are common in several areas. Because of the strength of modern materials now used in constructing nets, even larger species of cetaceans are sometimes captured incidentally in fishing gear. Such entrapments seriously threaten the North Atlantic right whale, ubalaena glacialis, population ( Johnson et al., 2007 ). Any species can be captured in nets. However, humpback whales, Megaptera novaeangliae, perhaps because of their abundance in coastal waters where nets are commonly used or because of the many barnacles they carry, seem extremely vulnerable to entanglement in fishing gear. I present here a case history of whale entrapment from Newfoundland and Labrador, Canada; there are other areas of the world with entrapment and entanglement problems of many species of marine mammals (Lien, 1995). In the late 1970s, humpback whales were seen in greater numbers in inshore waters of Newfoundland and Labrador as the bait fish capelin, Mallotus villous, which is their major prey, was seriously depleted offshore on the Grand Banks. The humpbacks moved inshore to feed on spawning capelin that occurs in the same areas where fishermen place their nets. Inevitably, this meant trouble. Fishermen began to report whale collisions which left nets badly damaged. On occasion, humpback whales would actually be caught and held in the nets. Initially, about 50% of the animals that were caught died. Because this was a new anthropogenic source of mortality in this recovering humpback population, it was a serious conservation concern. Because of the problem, a program was established by the Whale Research Group of Memorial University of Newfoundland to aid both the whales and the fishermen when incidental captures occurred. Fishermen anywhere along Newfoundland and Labrador s 17,000 km of coastline that accidentally caught a whale could call the ntrapment Assistance Program by a toll-free phone number. A trained team would be dispatched to release the whale alive and to save as much of the fishing gear as possible. Because there were real benefits for fishermen in minimizing gear losses and lost fishing time, they cooperated very well with the program, and it benefited whales as well. Humpback mortality as a result of entrapment was reduced to about 10% of the animals that were captured. Those fewer whales died before help could reach the animal. However, during the 1980s, groundfish populations were being seriously depleted by overfishing. To make a living, fishermen responded by fishing more nets, and inshore effort increased dramatically. With more barriers, the frequency of collisions and entrapments by whales increased. In one fishing season, the ntrapment Assistance Program received over 150 reports of entrapped humpback whales. In addition, other species, such as common minke whales, Balaenoptera