MARINE MAMMAL SCIENCE, 27(2): 334–349 (April 2011) C 2010 by the Society for Marine Mammalogy DOI: 10.1111/j.1748-7692.2010.00408.x Extreme physiological adaptations as predictors of climate-change sensitivity in the narwhal, Monodon monoceros TERRIE M. WILLIAMS SHAWN R. NOREN Department of Ecology and Evolutionary Biology, University of California-Santa Cruz, Center for Ocean Health, 100 Shaffer Road, Santa Cruz, California 95060, U.S.A. E-mail: [email protected] MIKE GLENN Sea World of San Diego, 500 Sea World Drive, San Diego, California 92109, U.S.A. ABSTRACT Rapid changes in sea ice cover associated with global warming are poised to have marked impacts on polar marine mammals. Here we examine skeletal muscle charac- teristics supporting swimming and diving in one polar species, the narwhal, and use these attributes to further document this cetacean’s vulnerability to unpredictable sea ice conditions and changing ecosystems. We found that extreme morphological and physiological adaptations enabling year-round Arctic residency by narwhals limit behavioral flexibility for responding to alternations in sea ice. In contrast to the greyhound-like muscle profile of acrobatic odontocetes, the longissimus dorsi of narwhals is comprised of 86.8% ± 7.7% slow twitch oxidative fibers, resembling the endurance morph of human marathoners. Myoglobin content, 7.87 ± 1.72 g/100 g wet muscle, is one of the highest levels measured for marine mammals. Calculated maximum aerobic swimming distance between breathing holes in ice is <1,450 m, which permits routine use of only 2.6%–10.4% of ice-packed foraging grounds in Baffin Bay. These first measurements of narwhal exercise physiology reveal extreme specialization of skeletal muscles for moving in a challenging ecological niche. This study also demonstrates the power of using basic physiological attributes to pre- dict species vulnerabilities to environmental perturbation before critical population disturbance occurs. Key words: narwhal, Monodon monoceros, sea ice, physiology, climate change, myoglobin, skeletal muscle, aerobic dive limit, slow twitch fiber. 334 WILLIAMS ET AL.: NARWHAL PHYSIOLOGY 335 Some of the most obvious and marked impacts associated with recent warming of the earth’s lower atmosphere have occurred in polar marine environments. In both arctic and antarctic regions, alterations in climate have been linked to changes in sea ice cover, sea level, water temperature, and ocean currents (Rothrock et al. 1999, Parkinson and Cavalieri 2002, Comiso and Parkinson 2004, Walsh 2008). The rate of change within arctic ecosystems in particular exceeds trends recorded over the past several millennia (Root et al. 2003, Overpeck et al. 2005, Walsh 2008). These climate-related environmental events are poised to initiate population extinctions, range expansions and contractions, and serve as major driving forces behind evolution in natural populations of marine mammals (O’Corry-Crowe 2008). Despite this, such biological impacts often remain unrecorded due to the cryptic behaviors of oceanic mammals and the remote location of events. As highly derived, long-lived (i.e., K-selected) species, Arctic marine mammals are poorly equipped to respond quickly to sudden alterations in climate (Moore and Huntington 2008). Furthermore, the sensitivity to environmental perturbation is heightened for many specialized species due to small population size following centuries of commercial or subsistence harvest, slow reproduction rates, reliance on specific sea ice conditions for foraging, as well as their position at the apex of the food web (O’Corry-Crowe 2008). This is supported by recent evidence indicating that the observed changes in the arctic marine environment are already impacting marine mammals (Derocher et al. 2004, Ferguson et al. 2005, Laidre and Heide-Jørgensen 2005a, Laidre et al. 2008). Consequently, the three year-round cetacean occupants of arctic waters, the narwhal (Monodon monoceros), beluga whale (Delphinapterus leu- cas), and bowhead whale (Balaena mysticetus), have been listed by the International Whaling Commission (IWC 1997) as “vulnerable” to climate-induced disturbance. As one of the three most vulnerable arctic marine mammal species (Laidre et al. 2008), the West Greenland narwhal populations have experienced significant declines (Heide-Jørgensen and Acquarone 2002, Heide-Jørgensen 2004). Reasons for this trend include limited geographical range and a relatively small worldwide population size. Exceptional site fidelity, dependence on predictable, seasonal changes in sea ice, and a geographically narrow and specialized feeding pattern (Heide-Jørgensen et al. 2003; Laidre et al. 2004; Laidre and Heide-Jørgensen 2005a,b; Thiemann et al. 2008) likely exacerbate the problem. For example, narwhal populations from Canada and Western Greenland rely on intense periods of foraging in localized wintering areas in Baffin Bay to meet annual energetic demands. While affording access to high prey densities at depth, these areas must also provide sufficient open leads and cracks to allow for breathing (Heide-Jørgensen et al. 2003, Laidre and Heide-Jørgensen 2005a), an enormous environmental challenge during the winter months. With limited access to this species especially during the polar winter, it has been difficult to document the impact of recent, rapid environmental changes on narwhals or to predict future impacts. In this study, we approached this problem by examining the morphological (Table 1) and physiological characteristics required for supporting specialized winter foraging by the narwhal. Specifically, fiber type composition and myoglobin concentration were determined for the primary locomotory muscle, the longissimus dorsi, and used as indicators of swimming (Hulten et al. 1975, Costill et al. 1976) and diving (Blessing 1972, Kooyman 1989, Noren and Williams 2000) capability, respectively. These attributes were then used to examine the factors con- tributing to sub-ice range limits as well as the capacity of the narwhal to adapt to changing ice conditions. 336 MARINE MAMMAL SCIENCE, VOL. 27, NO. 2, 2011 Table 1. Morphological characteristics of adult narwhals in the present study. Length represents total body length from the rostrum to the fluke notch, excluding the tusk. Girths and diameters are for the maximum values recorded along the body. Sex is indicated by the ID (M = male, F = female). Age classification was based on overall size including body mass according to Hay (1984). Length Maximum Maximum Estimated Fineness Animal ID (cm) girth (cm) diameter (cm) mass (kg) ratio 1M 506.0 258 82.1 1,647 6.2 2M 320.0 228 72.6 529 4.4 3F 335.3 214 68.1 593 4.9 METHODS Field Site and Animals Field research was conducted in the Pond Inlet coastal region of northern Baffin ◦ Island (Nunavut Territory, Canada) during August–September (Tair = 1.7–5.4 C, ◦ Twater surface = 2.3–5.2 C) to coincide with the narwhals’ movements onto summering grounds within the local inlets. All animals were considered members of the Eclipse Sound subpopulation. Routine swimming behaviors (relative speed, maneuvering and predatory evasive movements) of individual narwhals and pods in Milne Inlet and western Eclipse Sound were recorded during this period by observers either in small skiffs or from surrounding cliff sites. The degree of ice cover ranged markedly during this period and depended on wind direction. Morphological measurements and tissue samples were collected opportunistically from three mature narwhals (Table 1) during a local Inuit subsistence hunt. Body Morphology Maximum girth and straight-line body length from maxilla tip to the notch of the tail flukes were recorded for each animal. Because of the large size of the animals, half of the girth (from mid-dorsal ridge to the ventral line) was measured and doubled for total girth. Body mass was calculated from length measurements using the equation of Hay (1984): M = 0.0003231L2.48 (1) where M is body mass in kilograms and L is body length in centimeters. The fineness ratio, an index of body streamlining, was calculated according to Webb (1975): FR = LD−1 (2) where FR is the fineness ratio, L is total body length in centimeters, and D is maximum body diameter in centimeters. Tissue Samples Samples of skeletal muscle and heart were collected within 30 min of death and placed in cooled, airtight containers on ice until fixation or freezing in liquid WILLIAMS ET AL.: NARWHAL PHYSIOLOGY 337 nitrogen within 5 h. For each animal, samples of the longissimus dorsi were taken half way between the dorsal ridge and fluke from the mid belly of the muscle bundle after removal of the overlying tendon sheath (Howell 1930). In addition, samples of the left ventricle of the heart were obtained for one adult (1M). All tissue samples were divided into two sections for use in histochemical and biochemical analyses. The histochemical sample was cut, embedded in optimum cutting temperature (O.C.T.) compound, and frozen in isopentane cooled by liquid nitrogen according to the procedures of Dubowitz (1985). The remaining sample was frozen in a container immersed directly in liquid nitrogen. All samples were stored in airtight vials and shipped in a dry nitrogen container. Once at the laboratory, the vials were transferred to a freezer and stored at −70◦C until analysis. To avoid dehydration of the samples, ice crystals were placed in the vials before transfer to the freezer. Histochemistry Details of the muscle analyses have been reported previously (Williams et al. 1997). Briefly,