524 Habitat Use

in UK-stranded harbour ( phocoena ) . Environ. Toxicol. Chem. 24 , 238 – 248 . Kenney , R. D. , Payne , P. M. , Heinemann , D. W. , and Winn , H. E. (1996 ). Habitat Use Shifts in northeast shelf cetacean distributions relative to trends in Gulf of Maine/Georges Bank fi nfi sh abundance. In “ The Northeast Shelf LEJANDRO CEVEDO UTIÉRREZ Ecosystem: Assessment, Sustainability, and Management ” ( K. Sherman , A A -G N. A. Jaworski , and T. J. Smayda , eds) , pp. 169 – 196 . Blackwell , Oxford . Kingsley, M. C. S. ( 2001 ). Beluga surveys in the St Lawrence: A reply to I. Introduction Michaud and Béland. Mar. Mamm. Sci. 17 , 213 – 218 . Laws , R. M. ( 1985 ). The ecology of the Southern . Am. Sci. 73 , A. Temporal and Spatial Scales in Ecology 2 6 – 4 0 . cology is the study of interactions between organisms and their Loughlin , T. R. ( 1994 ). “ Marine and the Exxon Valdez . ” environment, and the distribution and abundance of organ- Academic Press , San Diego . isms resulting from these interactions. The environment of Martineau , D. , Lair , S. , DeGuise , S. , Lipscomb , T. P. , and Béland , P. E any organism includes abiotic factors—non-living chemical and physi- ( 1999 ). Cancer in beluga from the St. Lawrence estuary, cal factors such as temperature and light—and biotic factors—living Quebec, Canada: A potential biomarker of environmental contamina- organisms with which any individual interacts. For instance, other tion . J. Cet. Res. Manag. ( Special Issue 1) , 249 – 265 . Michaud , R. , and Béland , P. ( 2001 ). Looking for trends in the endan- organisms may compete with an individual for food and resources, gered St. Lawrence beluga population. A critique of Kingsley, M.C.S. prey upon it, or change its physical and chemical environment. At the 1998 . Mar. Mamm. Sci. 17 , 206 – 212 . core of both ecology and conservation biology are questions that exam- Nowacek , D. P. , Thorne , L. P. , Johnston , D. W. , and Tyack , P. L. ( 2007 ). ine the relative importance of various environmental components in Responses of cetaceans to anthropogenic noise. Mamm. Rev. 37 , determining the distribution and abundance of organisms. 81 – 115 . Habitat use studies attempt to describe, explain, and predict the O’Shea , T. J. ( 1999 ). Environmental contaminants and marine mammals . In distribution and abundance of organisms. In these studies, identify- H “ Biology of Marine Mammals ” ( J. E. Reynolds , III , and S. A. Rommel , ing the factors that infl uence distribution and abundance at differ- eds) , pp. 485 – 563 . Smithsonian Institution Press, Washington, DC . ent spatial and temporal scales is fundamental. This concept can Reeves , R. R. , and Leatherwood , S. ( 1994 ). Dams and river : be illustrated by examining the distribution and abundance of blue Can they co-exist? Ambio 23 , 172 – 175 . Reeves, R. R., and Smith, B. D. (1999). Interrupted migrations and dis- whales ( musculus ) from the California/Mexico popula- persal of river dolphins: Some ecological effects of riverine develop- tions and fi n whales ( B. physalus ) from the Gulf of California popu- ment. In “ Proceedings of the CMS Symposium on Migration,” lation. Blue whales and to a lesser extent fi n whales depend on krill Gland, Switzerland, April 13, 1997 (UNEP/CMS, Ed.), pp. 9–18. (Euphausiacea) as a prey item. Krill form large, dense swarms during Convention on Migratory Species, Technical Series Publication No. the day and have their largest concentrations below 100 m in depth. 2. United Nations Environment Programme, Bonn/The Hague. At night, krill come near the surface but are scattered over large Reeves , R. R. , and Reijnders , P. J. H. ( 2002 ). Conservation and man- areas. During winter in Bahía de Loreto, Gulf of California, México, agement . In “ Marine Biology: An Evolutionary Approach ” blue and fi n whales engage in deep foraging dives during the day ( A. R. Hoelzel , ed. ) , pp. 388 – 415 . Blackwell Publishing , Oxford . while at night they perform shallow dives, very few of which appear Reeves , R. R. , Chaudhry, A. A. , and Khalid , U. ( 1991 ). Competing for to be foraging dives. During the day, krill swarms are found around water on the Indus plain: Is there a future for Pakistan’s river dol- phins? Environ. Conserv. 18 , 341 – 350 . underwater edges, where depth diminishes rapidly, and blue and Reijnders , P. J. H. , Aguilar , A. , and Donovan , G. P. ( 1999 ). Chemical fi n whales concentrate their movements and feeding in those areas. Pollutants and Cetaceans . J. Cet. Res. Manag. ( Special Issue 1) . Both blue and fi n whales move out of Loreto around early spring. Reynolds , J. E. , III ( 1999 ). Efforts to conserve manatees. In “ Conservation Bahía de Loreto is thus a short-term feeding site for both whales, and Management of Marine Mammals ” ( J. R. Twiss , Jr , and R. R. Reeves , which behavior and movements closely match those of krill. eds ) , pp. 267 – 295 . Smithsonian Institution Press , Washington, DC . By combining the information from Loreto to that from other Richardson , W. J. , Greene , C. R. , Jr. , Malme , C. I. , and Thomson , D. H. studies, the following general picture of the California/Mexico pop- ( 1995 ). “ Marine Mammals and Noise. ” Academic Press , San Diego . ulation of blue whales emerges: In late spring, blue whales move Rosas , F. C. W. ( 1994 ). Biology, conservation and status of the Amazonian north to feed during summer and early fall along the California manatee Trichechus inunguis . Mamm. Rev. 24 , 4 9 – 5 9 . coast in the Farallones Islands, Cordell Banks, and Monterey Bay, Shane , S. H. ( 1995 ). Relationship between pilot whales and Risso’s dol- phins at Santa Catalina Island, California, USA. Mar. Ecol. Prog. Ser. on large swarms of krill. The whales move back south in fall, feed- 123 , 5 – 1 1 . ing around the Channel Islands and perhaps off Bahia Magdalena, Trillmich , F. , and Dellinger, T. ( 1991 ). The effects of El Niño on Mexico. During winter, whales are back in the Gulf of California, Galapagos . In “ Pinnipeds and El Niño: Responses to including Bahía de Loreto. However, there is a large degree of varia- Environmental Stress ” ( F. Trillmich , and K. A. Ono , eds ) , pp. 66 – 74 . tion, and many whales may winter in the Costa Rica Dome, an ocea- Springer-Verlag , Berlin . nographic feature in the Pacifi c Ocean. Although the picture of the Tynan , C. T. , and DeMaster , D. P. ( 1997 ). Observations and predic- Gulf of California population of fi n whales is less complete, we know tions of Arctic climate change: Potential effects on marine mammals. that they feed during the spring in the southern region of the Gulf Arctic 50 , 308 – 322 . of California, including Loreto. During the summer, a time of year Würsig , B. , and Evans , P. G. H. ( 2002 ). Cetaceans and humans: in which krill are less abundant in the gulf, they move further north Infl uences of noise . In “ Marine Mammals: Biology and Conservation ” ( P. G. H. Evans , and J. A. Raga , eds ) , pp. 555 – 576 . Plenum Press/ into the gulf to prey on schooling fi sh. Kluwer Academic , New York . This example illustrates the importance of defi ning temporal and Würsig , B. , Reeves , R. R. , and Ortega-Ortiz , J. G. ( 2002 ). Global climate spatial scales in an ecological study, and documents how the distribu- change and marine mammals. In “ Marine Mammals—Biology and tion of marine mammals is infl uenced by the environment at different Conservation ” ( P. G. H. Evans , and J. A. Raga , eds ) , pp. 589 – 608 . spatial and temporal scales. At scales of days and tens of kilometers, Kluwer Academic/Plenum Publishers , New York . blue whales are found during the day along canyon edges, feeding on Habitat Use 525

krill swarms. At scales of months and hundreds to thousands of kil- whales occur in areas with a northeast aspect, intermediate gradi- ometers, blue whales move to different coastal areas to exploit krill ents, and depths between 200 and 1000 m where bottom topogra- swarms. In the case of fi n whales, at scales of days and tens of kilom- phy forces the Deep Western Boundary Current toward the surface eters, they are also found during the day along canyon edges feeding (MacLeod and Zuur, 2005). The authors hypothesize that prey are on krill swarms. However, at scales of months and hundreds to thou- concentrated in these same areas. In the Faroe-Shetland Channel sands of kilometers, they move within the same oceanographic area north of the United Kingdom, a GAM analysis of sounds (the Gulf of California) and switch prey items, from krill to schooling indicates that dolphin distribution is best predicted by a combination fi sh. Even closely related species of marine mammals can make dif- of water noise level, time of day, month, and water depth (Hastie ferent decisions regarding their distribution: blue whales move out et al. , 2005 ). of the Gulf of California and look for the same prey item; fi n whales Despite our inability to determine causality and hence fully remain in the Gulf of California and switch prey items. Given that explain the relationship between distribution and marine mammals are generally long lived and that their cost of loco- abundance, and several biotic and abiotic factors, several tools such motion in the water is relatively low, understanding their distribution as remote-sensing techniques and GAM analysis allow scientists to and abundance at multiple temporal and spatial scales is even more describe, predict, and partially explain the determinants of such crucial than for shorter-lived or less mobile organisms. relationships.

B. Research on Marine Mammal Habitat Use C. Habitat Use and Evolution Understanding the distribution and abundance of marine mam- Marine mammals are highly mobile, tend to cover large areas, mals is important not only to ecologists, conservation biologists, envi- move in three spatial dimensions, and spend the vast majority of ronmentalists, managers, and tour operators, but also to evolutionary their lives under water. Hence, controlled experiments are next to biologists. This is because the interactions of organisms with their impossible to conduct, and describing, explaining, and predicting dis- environment that occur over a long period of time are important tribution and abundance present unusual challenges to researchers. causes of evolutionary change. Lake Apoyo, a volcanic crater lake H In general, studies are unable to show a causal explanation between in Nicaragua, was seeded only once by the ancestral benthic spe- a factor or factors and the observed distribution and abundance of cies citrinellus from which the new limnetic species A. a marine mammal population; rather, scientists rely on quantita- zaliosus evolved within less than 10,000 years by exploiting a dif- tive correlations that are indicative of potential causal factors. For ferent habitat (Barluenga et al. , 2006 ). These two species are both instance, several studies document that during the summer belugas reproductively isolated and eco-morphologically distinct; thus pro- (Delphinapterus leucas ) in Alaska are distributed near coastal mud viding a convincing example of habitat use as an agent of evolu- fl ats and river mouths; however, it is unclear whether the observed tionary change via sympatric speciation. Sympatric speciation is a distribution is caused by prey availability, breeding, calving, molting, contentious concept in evolutionary biology, for which few convinc- or shelter from predators (Goetz et al. , 2007 ). ing examples exist worldwide. Hence, documenting evolutionary Our understanding of marine mammal habitat use has been change in marine mammals due to habitat use has been extremely improved by employing remote-sensing techniques and sophisticated diffi cult. The apparent incipient speciation of sympatric resident statistical analyses. Remote-sensing techniques allow scientists to and transient killer whales ( orca ) off the west coast of correlate marine mammal distribution with dynamic environmental Washington State and Canada may be such an example (Baird et al. , variables that take into account spatial or temporal scales. For exam- 1992). However, it has been suggested that the division was origi- ple, in the Gulf of St. Lawrence, the distribution of blue whales, fi n nally cultural (Whitehead et al. , 2004 ). whales, minke whales (Balaenoptera acutorostrata), and humpback whales (Megaptera novaeangliae ) is highly correlated with thermal fronts, which were described from -surface-temperature satellite II. Intrinsic Factors in Habitat Use images (Doniol-Valcroze et al. , 2007 ). Remote-sensing techniques Most explanations on habitat use by marine mammals refer to also allow scientists to describe the three-dimensional space distribu- environmental factors, such as prey availability, predation, or temper- tion of marine mammals and correlate it with environmental factors. ature, which are extrinsic to the organisms. However, traits intrinsic For instance, the amount of time that Weddell seals ( Leptonychotes to the organisms themselves may affect their ability to exploit certain weddellii ) in Antarctica spend at the bottom phase of a dive corre- habitats and hence determine their distribution and abundance. lates with an index of prey abundance (Mitani et al. , 2003 ; Watanabe et al. , 2003 ; Mitani et al., 2004). These results were obtained by attaching recorders to individual seals, which recorded dive behav- A. Body Size ior, acceleration, geomagnetic intensity, and digital still pictures. This Body size affects many important traits in organisms, including methodology allows scientists to describe three-dimensional spatial morphology, metabolic rate, and reproductive costs. Species with large use of seals, which spent their time under water on a small region body size and large amounts of fat stored in are able to travel with a steep bottom contour, apparently searching for bentho-pelagic far or to exploit very patchy resources. An example of the relationship prey throughout the water column (Mitani et al. , 2004 ). between habitat use and large body size is the northern elephant seal Sophisticated statistical analyses allow scientists to simultaneously (Mirounga angustirorstris ). This species makes a double migration correlate the distribution and abundance of marine mammals with each year: one after molting and one after breeding, with individual many different environmental factors. In the Bahamas, the occur- annual movements of 18,000–21,000 km ( Stewart and DeLong, 1993, rence of Blainville’s beaked whales (Mesoplodon densirostris ) is cor- 1995). Adults stay at sea for 8–9 months of the year to forage, using the related in decreasing order of importance with seabed aspect (facing California Current as a corridor to foraging areas further north that direction), seabed gradient (slope), and water depth, an analysis are related to water masses and the distribution of squid. While at sea, conducted with generalized additive modeling (GAM). Blainville’s both sexes dive almost continuously, remaining submerged for about 526 Habitat Use

90% of the total time. Large body size has also predisposed marine by reducing intersexual foraging competition. Southern elephant seals mammals to long dives, because body size augments oxygen stores (Mirounga leonina) from Kerguelen Island travel to the Antarctic and diminishes specifi c metabolic rate (use of oxygen per unit of mass) shelf (Bailleul et al., 2007). As the ice expands during winter, females ( Hoelzel, 2002 ). Because deep dives require longer dives than shal- appear to shift from benthic to pelagic foraging, while males continue low dives, large marine mammals such as the sperm (Physeter to forage almost exclusively benthically over the continental shelf. It macrocephalus ) are able to exploit deep-water habitats. However, is hypothesized that this difference in habitat use is related to the dif- given the many different physiological adaptations for diving found in ferent energetic requirements between the two sexes, or to the need marine mammals, body size alone cannot predict the vertical distribu- for females to return to Kerguelen in the spring to give birth, whereas tion of marine mammals. males can remain in the ice.

D. Individual Variability B. Age Differences in habitat use may also be related to individual Given that marine mammals are long-lived predators, the habitat variability. For instance, there is signifi cant variation between indi- that they are able to exploit may change over time to refl ect increased vidual female Antarctic fur seals (Arctocephalus gazella ) in trip dura- physiological capabilities as body size increases and by increased learn- tions and the maximum distance reached from the breeding beach ing. Dive and depth duration in Australian sea lions (Neophoca cinerea ) ( Staniland et al., 2004). Apparently, there is a strong individual com- increase with age; however, such development is slow (Fowler et al. , ponent to where a seal forages, especially in terms of the distance 2006 ). Pups at 6 months of age show minimal diving activity, they are traveled. The authors suggest that once the foraging area is selected weaned at about 17 months of age, and as 23-month-old juveniles by an individual seal, the dive behavior within that area is deter- they tend to dive to 40–50 m depths (62% the depth of adults). Pup mined by the area itself, perhaps related to the spatial and temporal and juveniles do not reach adult depth or durations and hence occupy distribution of the prey within it, and not by the individual seal. shallower habitats than those exploited by adults. Adult New Zealand H fur seals (Arctocephalus forsteri) utilize continental shelf waters and deep waters over the shelf break, where presumably high densities of E. Life History fi shes and cephalopods are found, while juveniles use pelagic waters Life history refers to the patterns of resource allocation to mainte- up to 1000 km from the habitats used by adults ( Page et al. , 2006 ). nance (survival), growth, and reproduction. Life history traits appear It is hypothesized that due to their small body size, juveniles cannot also to infl uence habitat use in marine mammals. As described earlier, effi ciently utilize prey in the same habitats as adults because they do blue whales migrate from the Gulf of California to the California coast not have the capacity to spend enough time under water at the greater searching for krill aggregations, while fi n whales remain in the Gulf of depths. Hence, adult male and female New Zealand fur seals are large California and switch prey items. In this case, the pattern enough to engage in benthic feeding in shelf breaks, whereas the is to move to another body of water and feed on the same prey; the fi n smaller-sized juveniles are constrained to epipelagic feeding at night. whale pattern is to remain in the same body of water and feed on dif- ferent prey. Along the Scandinavian coast, harbor porpoises (Phocoena phocoena) experience different ecological regimes during the year and C. Sex shift from pelagic prey species in deep waters to more coastal and/or Many marine mammal species segregate by sex. The harbor seal demersal prey in relatively shallow waters (Fontaine et al. , 2007 ). In (Phoca vitulina ) provides a good example of such segregation (Boness this case, the harbor pattern is similar to that of fi n whales: et al. , 1994 ; Coltman et al., 1997). Females and males have similar they both adapt their foraging to local oceanographic conditions rather body sizes (females weigh about 85 kg; males about 110 kg) and mate than perform an extensive migration. at sea. Females nurse their pups for about 24 days, fasting for about Larger body size implies a longer dive time. However, whales of 1 week and then having to take regular foraging trips while lactating. the family Balaenopteridae () dive less than expected based Most males forage early in the season and in doing so most individu- on body size because their foraging strategy of lunging is costly als maintain or increase body mass during this period. During the lat- ( Acevedo-Gutiérrez et al. , 2002 ). Apparently, the effort needed to ter part of the breeding season, males rarely forage and spend time accelerate a large mass increases the costs of feeding and reduces reproducing when females are receptive. Hence, the habitat occupied time under water. Despite engaging in behaviors to reduce such by both sexes is different: during the fi rst 10 days after birth, females costs—such as gliding gaits during dive descent, accelerating at the are on land while males are at sea diving to depths exceeding 60 m ; beginning of a lunge and gliding throughout the rest of the lunge— between 10 and 20 days after birth, females make trips at sea and dive rorquals do not exploit the deep waters that smaller species use. In to 50–60 m while males are also at sea in areas where females move this case, the pattern is to exploit relatively shallow habitats but diving to only 20 m. It appears that the different habitat use in due to the constraints imposed by their foraging behavior. which females and males engage represents a balance between forag- ing and reproduction to maximize reproductive success. The relationship between habitat use and sex is also related to III. Extrinsic Factors in Habitat Use body size in sexually dimorphic marine mammal species. Such body Most habitat use studies attempt to explain the distribution and size differences may require the sexes to use different habitats. For abundance of marine mammals in relationship to external biotic and instance, gray seals (Halichoerus grypus) are sexually dimorphic in size abiotic factors. Two important extrinsic factors infl uencing the distri- ( Breed et al. , 2006 ). At Sable Island, Nova Scotia, males and females bution of a species are food availability and predation risk. In gen- utilized different habitats, differences that were most pronounced just eral, marine mammals should exploit areas of high prey density and before and immediately after breeding. Females mainly used mid- avoid areas of high predator density. However, it is also important to shelf regions whereas males primarily used areas along the continental understand the temporal and spatial scales, given that the predict- shelf break. It is hypothesized that these differences maximize fi tness ability of prey distribution tends to decrease with the spatial scale. Habitat Use 527

A. Prey Availability habitats. It is believed that shallow habitats are also inherently risky Prey availability is the most frequently factor invoked to explain because shark detection apparently decreases as dolphin echolocation the distribution and abundance of marine mammals, regardless of the effi ciency and visual detection of sharks camoufl aged over seagrass spatial and temporal scale of the study. However, understanding the diminish in shallow habitats. Hence, shallow habitats are the best mechanism infl uencing prey availability itself has proved as challeng- places to forage for dolphins, but are also the most risky. As a result, ing as determining the causality of marine mammal distributions. Croll in seasons of high shark abundance, dolphins foraged much less in et al. (2005) took advantage of a relatively straightforward system: the productive but risky shallow habitats than expected if food was blue whales feed exclusively upon dense but patchy schools of pelagic the only relevant factor. These results suggest that dolphin habitat krill; hence, understanding krill distribution will assist in understand- use refl ects a trade-off between predation risk and prey availability. ing blue whale distribution. By employing remote-sensing techniques Besides showcasing the importance of predation risk in explaining and concurrent measurements, they examined the temporal and spa- habitat use, this study also indicates that the distribution and abun- tial linkages between intensity of upwelling, primary production, dis- dance of marine mammals is simultaneously affected by more than tribution of krill, and distribution and abundance of blue whales in one factor. Further, because the distribution and abundance of tiger Monterey Bay, California. The study indicated that seasonally high sharks are infl uenced by species other than dolphins, the distribution primary production supported by coastal upwelling combined with of the primary prey of the sharks may indirectly infl uence dolphin topographic breaks off California maintained high densities to allow habitat use. Hence, as also exemplifi ed by the studies described in the exploitation by blue whales. Blue whales appeared in the area in late section on prey availability, it is important to consider the community summer and early fall and fed exclusively upon adult krill Thysanoessa context in studies of habitat use. spinifera and Euphausia pacifi ca aggregations, diving to depths between 150 and 200 m on the edge of the Monterey Bay Submarine C. Intraspecifi c Competition Canyon. High krill densities were supported by high primary pro- duction between April and August and a submarine canyon that pro- In many species, differences in habitat use between sexes are vided deep water down-current from an upwelling region. Peak krill apparently a consequence of social interactions. A recent study of H densities occurred in late summer and early fall, lagging the seasonal the Galápagos sea lion (Zalophus wollebaeki ) indicates that sexual increase in primary production by 3–4 months, due to the growth to segregation on land was high both during the reproductive and non- adulthood of krill spawned around the spring-increase in primary pro- reproductive periods ( et al. , 2005 ). A generalized linear model duction, and to decreased upwelling in late summer. It is predicted of habitat use showed that adult males frequented habitat types that that the annual migratory movements of the California blue whale adult females used much less, with males being most abundant in population refl ect seasonal patterns in productivity in other foraging suboptimal inland habitats. It is hypothesized that this habitat seg- areas in the Northeast Pacifi c. The annual increase in the abundance regation resulted as a by-product of social processes, primarily intra- of blue whales was linked to wind-driven upwelling, but these linkages sexual competition and female avoidance of male harassment. occurred through a sequence of bottom-up biological processes that lagged in time. Consequently, models that attempt to predict the dis- D. Human Infl uence tribution and abundance of marine mammals need to include bottom- up processes and temporal scales. Human activities, also termed anthropogenic infl uences, are an Another example of the importance of understanding the spatial important extrinsic factor affecting the distribution and abundance of and temporal distribution of prey to describe, explain, and predict marine mammals. Boat traffi c is an activity with many documented marine mammal distribution is found in dugongs (Dugong dugon ). cases of impact on marine mammal habitat use. In the short term, Like other herbivores, dugongs must select quality food plants this activity may cause marine mammals to temporarily abandon to optimize their nutrient intake. Across multiple spatial scales, or avoid a particular site. For instance, the number of harbor seals they appear to prefer some seagrass pastures and avoid others. At hauled out in a particular site may diminish dramatically in relation medium spatial scale remote sensing, it was confi rmed that a 24 km2 to boat traffi c ( Suryan and Harvey, 1999; Johnson and Acevedo- seagrass meadow in Hervey Bay, Australia, is an important dugong Gutiérrez, 2007). In New Zealand, the frequency of bottlenose dol- habitat due to the presence of fi ve species of seagrasses, which cov- phin (Tursiops truncatus) visits to Milford Sound has diminished ered 91% of the total habitat area (Sheppard et al. , 2007 ). However, as a result of boat traffi c; additionally, when dolphins visit the fjord at a small spatial scale, dugong use within the meadow is still not well they remain at the entrance, away from tour boats (Lusseau, 2005). understood because the infl uence of seagrass food quality on dug- In the long term, boat traffi c may create a permanent abandonment ong grazing patterns and nutritional ecology is poorly understood. of areas visited by marine mammals and hence creating a perma- Consequently, understanding the dynamics of seagrass communities nent shift in distribution. For example, boat traffi c may cause harbor is essential for predicting patterns of habitat use by dugongs. seals to abandon haulout sites where alternative haulout locations are limited (Suryan and Harvey, 1999). In Shark Bay, Australia, the abundance of Indo-Pacifi c bottlenose dolphins has declined in areas B. Predation Risk operated by two or more dolphin-watching boats compared to areas Predation risk is an important factor explaining the distribution with no boats or with only one boat (Bejder et al. , 2006 ). and abundance of marine mammals regardless of the spatial and tem- Human activities may also cause marine mammals to visit rather poral scale of the study. For instance, tiger shark (Galeocerdo cuvier ) than leave a particular area. For instance, two sympatric communi- predation risk correlates well with the habitat use of Indo-Pacifi c bot- ties of Indo-Pacifi c bottlenose dolphins are found in Moreton Bay, tlenose dolphins (Tursiops aduncus ) in Shark Bay, Western Australia Australia (Chilvers et al. , 2007 ). The non-trawler community does (Heithaus and Dill, 2002, 2006). The biomass of dolphin prey is not associate with trawler vessels, whereas the trawler community greater in shallow habitats than in deeper ones; however, when tiger associates with trawlers to feed on fl ushed prey. While the distribu- sharks are present in the area, their density is highest in shallow tion of the non-trawler community is explained by season and tide, 528 Habitat Use

the distribution of the trawler community is explained by the distri- Doniol-Valcroze, T. , Berteaux , D. , Larouche , P. , and Sears , R. ( 2007 ). bution of trawler boats. I n fl uence of thermal fronts on habitat selection by four rorqual whale species in the Gulf of St. Lawrence. Mar. Ecol. Prog. Ser. 335 , 207 – 216 . Fontaine , M. C. , Tolley , K. A. , Siebert , U. , Gobert , S. , Lepoint , G. , IV. Conclusion Bouquegneau , J. M. , and Das , K. ( 2007 ). Long-term feeding ecol- The habitat use of marine mammals is affected by abiotic and ogy and habitat use in harbour porpoises Phocoena phocoena from biotic factors, including intrinsic and extrinsic factors. The scientists’ Scandinavian waters inferred from trace elements and stable iso- goal is to describe, explain, and understand the relative importance topes . BMC Ecol. 7 , doi:10.1186/1472-6785-7-1 . of each factor in the distribution and abundance of marine mammals. Fowler , S. L. , Costa , D. P. , Arnould , J. P. Y. , Gales , N. J. , and Kuhn , C. E . ( 2006 ). Ontogeny of diving behaviour in the Australian sea lion: Trials To reach this goal, the temporal and spatial scales of the study system of adolescence in a late bloomer. J. Anim. Ecol. 75 , 358 – 367 . need to be clearly defi ned. Given the challenges inherent in study- Goetz , K. T. , Rugh , D. J. , Read , A. J. , and Hobbs , R. C. ( 2007 ). Habitat ing marine mammals, the use of sophisticated remote-sensing tech- use in a marine ecosystem: Beluga whales Delphinapterus leucas in nologies and statistical models has been very successful in gathering Cook Inlet, Alaska. Mar. Ecol. Prog. Ser. 330 , 247 – 256 . and integrating data on habitat use. Long-term studies and studies in Hastie , G. D. , Swift , R. J. , Slesser, G. , Thompson , P. M. , and Turrell , W. R. new regions are fundamental to answering questions on habitat use. ( 2005 ). Environmental models for predicting habitat However, the most promising line of work is to conduct integrative in the Northeast Atlantic. ICES J. Mar. Sci. 62 , 760 – 770 . studies that consider community and ecosystem structure at differ- Heithaus , M. R. , and Dill , L. M. ( 2002 ). Food availability and tiger shark ent spatial and temporal scales, such as the study on the California/ predation risk infl uence habitat use . Ecology 83 , Mexico population of blue whales described throughout this chapter. 480 – 491 . Heithaus , M. R. , and Dill , L. M. ( 2006 ). Does tiger shark predation risk infl uence foraging habitat use by bottlenose dolphins at multiple spa- See Also the Following Articles tial scales? Oikos 114 , 257 – 264 . H Hoelzel , A. R. (ed.) ( 2002 ). “ Marine Mammal Biology. An Evolutionary Cetacean Ecology ■ Distribution ■ Ecology. Approach . ” Blackwell Publishing , Oxford . Johnson , A. , and Acevedo-Gutiérrez , A. ( 2007 ). Regulation compli- ance and harbor seal (Phoca vitulina ) disturbance . Can. J. Zool. 85 , References 290 – 294 . Lusseau , D. ( 2005 ). Residency pattern of bottlenose dolphins Tursiops Acevedo-Gutiérrez , A. , Croll , D. , and Tershy , B. ( 2002 ). High spp. in Milford Sound, New Zealand, is related to boat traffi c . Mar. feeding costs limit dive time in large whales. J. Exp. Biol. 205 , Ecol. Prog. Ser. 295 , 265 – 272 . 1747 – 1753 . MacLeod , C. D. , and Zuur, A. F. ( 2005 ). Habitat utilization by Blainville’s Bailleul , F. , Charrassin , J.-B. , Ezraty , R. , Girard-Ardhuin , F. , beaked whales off Great Abaco, northern Bahamas, in relation to sea- McMahon , C. R. , Field , I. C. , and Guinet , C. ( 2007 ). Southern ele- bed topography. Mar. Biol. 147 , 1 – 1 1 . phant seals from Kerguelen Islands confronted by Antarctic sea ice. Mann , J. , Connor , R. C. , Tyack , P. L. , and Whitehead , H. (eds) ( 2000 ). Changes in movements and in diving behaviour . Deep Sea Res. II 54 , “ Cetacean Societies. Field Studies of Dolphins and Whales . ” 343 – 355 . University of Chicago Press , Chicago, IL . Baird , R. W. , Abrams , P. A. , and Dill , L. M. ( 1992 ). Possible indi- Mitani , Y. , Sato , K. , Ito , S. , Cameron , M. F. , Siniff , D. B. , and Naito , Y. rect interactions between transient and resident killer whales: ( 2003 ). A method for reconstructing three-dimensional dive profi les Implications for the evolution of foraging specialization in the of marine mammals using geomagnetic intensity data: results from Orcinus . Oecologia 89 , 125 – 132 . two lactating Weddell seals. Polar Biol. 26 , 311 – 317 . Barluenga , M. , Stölting , K. N. , Salzburger , W. , Muschick , M. , and Meyer , A. Mitani , Y. , Watanabe , Y. , Sato , K. , Cameron , M. F. , and Naito , Y. ( 2004 ). ( 2006 ). Sympatric speciation in Nicaraguan crater lake fi sh. 3D diving behavior of Weddell seals with respect to prey accessibility Nature 439 , 719 – 723 . and abundance. Mar. Ecol. Prog. Ser. 281 , 275 – 281 . Bejder, L . , et al . (10 authors) ( 2006 ). Decline in relative abundance of Page , B. , McKenzie , J. , Sumner, M. D. , Coyne , M. , and Goldsworthy , S. D. bottlenose dolphins exposed to long-term disturbance. Conserv. Biol. ( 2006 ). Spatial separation of foraging habitats among New Zealand 20 , 1791 – 1798 . fur seals . Mar. Ecol. Prog. Ser. 323 , 263 – 279 . Berta , A. , Sumich , J. L. , and Kovacs , K. M. ( 2006 ). “ Marine Mammals. Sheppard , J. K. , Lawler , I. R. , and Marsh , H. ( 2007 ). Seagrass as pas- Evolutionary Biology , ” 2nd Ed. Academic Press , San Diego . ture for seacows: Landscape-level dugong habitat evaluation. Estuar. Boness , D. J. , Bowen , W. D. , and Oftedal , O. T. ( 1994 ). Evidence of a Coast. Shelf Sci. 71 , 117 – 132 . maternal foraging cycle resembling that of otariid seals in a small Staniland , I. J. , Reid , K. , and Boyd , I. L. ( 2004 ). Comparing individual phocid, the harbor seal. Behav. Ecol. Sociobiol. 34 , 95 – 104 . and spatial infl uences on foraging behaviour in Antarctic fur seals Breed , G. A. , Bowen , W. D. , McMillan , J. I. , and Leonard , M. L. Arctocephalus gazella . Mar. Ecol. Prog. Ser. 275 , 263 – 274 . ( 2006 ). Sexual segregation of seasonal foraging habitats in a non- Stewart , B. S. , and DeLong , R. L. ( 1993 ). Double migrations of the migratory marine mammal. Proc. R. Soc. Lond., B, Biol. Sci. 273 , northern elephant seal, Mirounga angustirostris . Symp. Zool. Soc. 2319 – 2326 . Lond. 66 , 179 – 194 . Chilvers , B. L. , Corkeron, P. J. , and Puotinen , M. L. ( 2007 ). Infl uence of Stewart , B. S. , and DeLong , R. L. ( 1995 ). Seasonal dispersion and habi- trawling on the behaviour and spatial distribution of Indo-Pacifi c bot- tat use of foraging northern elephant seals. J. Mammal. 76 , 196 – 205 . tlenose dolphins (Tursiops aduncus) in Moreton Bay, Australia. Can. Suryan , R. M. , and Harvey , J. T. ( 1999 ). Variability in reactions of Pacifi c J. Zool. 81 , 1947 – 1955 . harbor seals, Phoca vitulina richardsi , to disturbance. . Bull. 97 , Coltman , D. W. , Bowen , W. D. , Boness , D. J. , and Iverson , S. J. ( 1997 ). 332 – 339 . Balancing foraging and reproduction in male harbour seals: An aquat- Watanabe , Y. , Mitani , Y. , Sato , K. , Cameron , M. F. , and Naito , Y. ( 2003 ). ically mating pinniped. Anim. Behav. 54 , 663 – 678 . Dive depths of Weddell seals in relation to vertical prey distribution Croll , D. A. , Marinovic , B. , Benson , S. , Chavez , F. P. , Black , N. , Ternullo , R. , as estimated by image data. Mar. Ecol. Prog. Ser. 252 , 283 – 288 . and Tershy , B. R. ( 2005 ). From wind to whales: Trophic links in a Whitehead , H. , Rendell , L. , Osborne , R. W. , and Würsig , B. ( 2004 ). coastal upwelling system. Mar. Ecol. Prog. Ser. 289 , 117 – 130 . Culture and conservation of non-humans with reference to whales Hair and Fur 529

and dolphins: Review and new directions. Biol. Conserv. 120 , 431 – 441 . Wolf , J. B. W. , Kauermann , G. , and Trillmich , F. ( 2005 ). Males in the shade: Habitat use and sexual segregation in the Galápagos sea lion (Zalophus californianus wollebaeki ) . Behav. Ecol. Sociobiol. 59 , 293 – 302 .

Hair and Fur

PAMELA K. YOCHEM AND BRENT S. STEWART

I. Structure and Function he presence of hair is one of the characteristics that distin- guishes mammals from other vertebrates. Hair consists of Figure 1 Catastrophic-type molt in the northern elephant seal Tkeratinized epidermal cells, formed in hair follicles located in ( Mirounga angustirostris ), where the upper epidermis and hairs the dermal layer of the skin. Adaptations to an aquatic or amphibi- are shed in large patches within a few weeks. Photograph by B. S. ous lifestyle are apparent in marine mammal skin and hair (Ling, Stewart. 1974 ; Williams et al. , 1992 ; Pabst et al. , 1999 ; Reeves et al. , 2002 ). H Pinniped and sea otter (Enhydra lutris) hairs are fl attened in cross- section rather than round as in other . This is evidently an adaptation for enhancing streamlining of the body and reducing II. Molt drag during swimming. Pinnipeds and sea otters have diffuse smooth Many phocid seals possess a white lanugo coat in utero; this may muscle in their dermis, but they lack true arrector pili muscles. be lost before birth, or may persist for several weeks (as in some arc- Pinnipeds, sea otters, and polar bears (Ursus maritimus ) possess tic and antarctic species). This pelage provides insulation for neonates sebaceous glands and sweat glands, but these are absent in cetaceans of ice-breeding seals until they develop a blubber layer and also may and sirenians. Cetacean skin is hairless except for a few vibrissae or serve as camoufl age or protective coloration. Other examples of dis- bristles occurring mostly on the rostrum or around the mouth. These tinct neonatal pelage include the wooly black coat of elephant seals, are usually lost before or soon after birth. Sirenians have widely which is replaced by a silvery hair coat after the pup is weaned, and scattered hairs. The integument of pinnipeds, sea otters, and polar the fl uffy buff-colored pelage of sea otter pups, which persists for sev- bears generally has two layers of hair. The outer protective layer con- eral months. The signals for initiation and control of the annual pelage sists of long, coarse guard hairs and the inner layer is composed of cycle are not known for most species but are thought to include endo- softer intermediate hairs or underfur. Polar bear, sea otter, and ota- crine (thyroid, adrenal, and gonadal hormones), thermal, and nutri- rid guard hairs are medullated (having a sheath), whereas phocid tional infl uences ( Ling, 1970; Ashwell-Erickson et al., 1986). Molt is and walrus hairs (Odobenus rosmarus) are not. The hairs typically generally seasonal, beginning shortly after breeding. Sea otters may grow in groups or clumps, with a single guard hair emerging cranial molt year-round, although more hairs are generally replaced in sum- to one or more underfur hairs. Each hair grows from a separate fol- mer than in winter. The duration of molt in pinnipeds ranges from a licle, but the underfur follicles feed into the guard hair canal so that very rapid and “catastrophic ” shedding of large patches of superfi cial all hairs in a particular clump emerge from a single opening in the epidermis and associated hairs (elephant seals, monk seals) (Fig. 1 ) to skin. Some pinnipeds have a relatively sparse hair coat [walrus, ele- the more gradual pattern seen in otariids, with hairs replaced over sev- phant seals (Mirounga spp.), and monk seals (Monachus spp.) with eral months. A disruption of the molt process, resulting in breakdown a single guard hair per canal], whereas others have a lush, thick coat of the protective skin barrier, appears to underly Northern Elephant (fur seals, with dozens of underhair or fur follicles feeding into each Seal Skin Disease (Beckmen et al. , 1997 ; Yochem, 2008 ), an ulcera- guard hair canal). Sea otters have the densest fur of any mammal, tive dermatopathy affecting primarily yearling northern elephant seals with approximately 130,000 hairs/cm2 , about twice as dense as that (Mirounga angustirostris ). of northern fur seals (Callorhinus ursinus). Albinism and other skin and hair color anomalies have been reported in pinnipeds and ceta- ceans (Fertl et al. , 1999 ; Bried and Haubreux, 2000). See Also the Following Articles The appendages of some pinnipeds and the pads of sea otters are Blubber ■ Energetics ■ Pinniped Physiology ■ Streamlining ■ hairless, allowing these species to readily lose excess body heat by Thermoregulation conduction to the environment. Although most marine mammals rely on blubber for insulation, a layer of air trapped within the hair or fur serves as the primary insulator in fur seals and sea otters and keeps the References skin dry when the are submerged. Sea otter pelage is coated Ashwell-Erickson , S. , Fay , F. H. , and Elsner, R. ( 1986 ). Metabolic and with squalene, a hydrophobic lipid that aids in waterproofi ng the fur. hormonal correlates of molting and regeneration of pelage in Alaskan Skin secretions in pinnipeds also assist in waterproofi ng, and provide harbor and spotted seals (Phoca vitulina and Phoca largha ) . Can. defense against microbial infections (Meyer et al. , 2003 ). J. Zool. 64 , 1086 – 1094 .