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Home , Antarctic fur seal, Arctocephalus forsteri, Baikal seal, California sea lion, Caribbean monk seal, Caspian seal

TWENTY-SEVEN

Potential Influences of on the Status and Trends of Populations

DANIEL P. COSTA, MICHAEL J. WEISE, AND JOHN P. Y. ARNOULD

Although this volume focuses on and whaling, the are. are 1 to 2 orders of magnitude smaller in mass depletion of great whales over the last 50 to 150 per- than whales, which result in greater mass-specific rates of turbed the marine interaction web, thus influencing many food consumption. Thus the pinnipeds have physiological other and ecosystem processes (Estes, Chapter 1 of and environmental scaling functions that must be consid- this volume; Paine, Chapter 2 of this volume). Such interac- erably different from those of the great whales. For example, tion web effects have been hypothesized for several pinniped although some pinnipeds have remarkable abilities to fast, species. For example, the reduction of great whales in the even the most extreme durations of fasting in pinnipeds fall may have caused seal and popula- easily within the abilities of large cetaceans. The relatively tions to increase because of reduced competition for their small size of pinnipeds compared with cetaceans results in shared prey, (Laws 1977; Ballance et al., Chapter 17 of a much higher mass-specific and thus a shorter this volume). In addition, pinnipeds share some of the same fasting duration. These differences should constrain pin- predators, especially killer whales, as large whales do. nipeds to operate at smaller spatial and temporal scales Declines in populations may thus have caused the than the large cetaceans, thus making pinnipeds more sen- decline of certain pinniped populations because of redirected sitive to variations in prey abundance and distribution. by killer whales (Springer et al. 2003; Branch and Smaller size is also linked to a shorter generation time in Williams, Chapter 20 of this volume). These purported indi- pinnipeds, which makes their populations more vulnerable rect effects of whales on pinnipeds are poorly documented to environmental disturbances but also affords them a and controversial. Since most of the arguments are area- or greater potential for population growth. All of these char- species-specific, a global overview of the known patterns acteristics suggest that pinniped populations should be and causes for pinniped population change is topical and more responsive to changes in their environment than the relevant. large whales are. Because of differences in body size and life history, Pinnipeds have a nearly cosmopolitan distribution in pinnipeds are both easier to study, and possibly more the world oceans, although most species occur in temper- sensitive to environmental fluctuations, than most cetaceans ate to polar regions. Abundances range across species from

342 a few hundred to tens of millions of individuals. Estimates and Cape seals—all forage in seasonally productive, of abundance or trends in population numbers are the high-latitude ecosystems. most useful indicators of population status. Most popula- tions were severely depleted by commercial harvesting. Phocid Population Trends However, species distributions and population abundances before sealing are often unknown, because sealing ships SPECIES did not keep adequate records. Furthermore, reliable mod- There are six species of ice-breeding phocids in the northern ern abundance estimates are lacking for many species. hemisphere (harp, hooded, bearded, ringed, spotted, and Despite these problems, the history and trends in abun- ribbon seals), many of which annually migrate between sub- dance of the majority of pinnipeds is reasonably well arctic and arctic regions. Because of the difficulty in con- known. ducting surveys in this harsh environment, the abundance of In this chapter we review the current status and trends of many of these species is not well known. pinniped populations worldwide, and, where possible, we Harp and hooded seals are both divided into three stocks summarize the known or suspected reasons for recent (eastern , White , and West Ice), each identified declines. Trends in pinniped populations attributed to natu- with a specific breeding site. Recent modeling efforts indicate ral biological processes are evaluated in terms of reproductive that a harvest of 460,000 young harp seals per is hold- strategies, physiological limitations, and the resultant sus- ing the eastern Canada stock stable at about 5.2 million ceptibility to disturbance in prey resources and predation individuals (Healey and Stenson 2000). The other brought about by these factors. stocks are smaller—approximately 1.5 to 2.0 million in the Pinniped Population Trends White Sea and 286,000 on the West Ice. The best current population estimate for hooded seals is 400,000 to 450,000 The present-day abundances of species do not always (Stenson et al. 1993). Marked increases in the reflect their pre-exploitation numbers. Some species that number of harp and hooded seals occurred on were decimated to near- are now very abundant, in the mid-1990s (Lucas and Daoust 2002). whereas others have either not recovered or have recov- Populations of bearded seals were decimated by early com- ered and subsequently declined. Population abundance in mercial sealing. continued a commercial harvest of pinnipeds ranges over four orders of magnitude across bearded seals, with catches exceeding 10,000 animals yr−1 species from the Mediterranean and Hawaiian monk seals, during the 1950s and 1960s. In the 1970s and 1980s quotas which number in the hundreds of individuals, to the were introduced to limit harvests on declining populations with an estimated abundance of 10 to 15 to a few thousand animals annually (Kovacs 2002). Today, million individuals (Table 27.1). Phocids are generally bearded seals are an important subsistence resource to arctic more abundant than otariids. Fifteen of the 19 phocid peoples, with a few thousand animals taken annually for use species number greater than 100,000 individuals, whereas as human food, food, and clothing. Reliable estimates of only 8 of the 17 otariid species number greater than the total population of bearded seals do not exist. Early esti- 100,000 individuals. mates of just the Bering- population ranged from Pinnipeds range throughout the world oceans. Although 250,000 to 300,000. Discrepancies in recent survey efforts in the preponderance of species occurs in the northern hemi- 1999 and 2000 have precluded an updated estimate, but the sphere (Figures 27.1 and 27.2), the abundance may be much greater than previously described contains far more individuals. The abundance of crabeater (Waring et al. 2002). and fur seals alone exceeds the combined abun- Currently, five distinct subspecies of ringed seals are dance of all northern hemisphere species. The lesser num- recognized. Population estimates for most of these are ber of species in the southern hemisphere may reflect a outdated, and there are many uncertainties in the estima- northern hemisphere center of origin for otariids and pho- tion and sampling methods. Nonetheless, Bychkov (in cids (Costa 1993; Demere 1994; Demere et al. 2003). The Miyazaki 2002) estimated that there were 2.5 million in the larger numbers of individuals in the southern hemisphere and 800,000 to 1 million in the Sea of likely result from highly productive Antarctic and sub- Okhotsk in 1971. The Baltic population Antarctic coupled with an abundance of predator- decreased from 190,000 to 220,000 animals at the begin- free . The relative scarcity of human settlements ning of the twentieth century to approximately 5,000 dur- (which invariably lead to loss, direct and indirect ing the 1970s. In the mid-1960s, the remaining seals were pinniped/fisheries interactions, and pressure) may afflicted by sterility, likely caused by organochlorides also contribute to the larger sizes of southern hemisphere (Harding and Harkonen 1999; Reijnders and Aguilar 2002), pinnipeds. The relative abundance of phocids is likely due which inhibited natural population growth during the sub- to their generally inhabiting the highly productive polar sequent 25-year period. Ringed seals are hunted in many and subpolar regions (Bowen 1997). Similarly, the three regions (Miyazaki 2002). Thus, the decrease in seal numbers most abundant otariid species—the northern, Antarctic, was a consequence of excessive hunting in combination

WHALING EFFECTS ON PINNIPED POPULATIONS 343 TABLE 27.1 Pinniped Population Numbers and Trends Worldwide

Common Name Species Population Size Trend

Northern Hemisphere

Eared Seals Otariidae

Guadalupe (GFS) townsendi 7,000 Increasing sea (CSL) californianus 237,000–244,000 Increasing (NFS) Callorhinus ursinus 1,400,000 Decreasing Steller (SSL) Eumatopias jubatus <75,000 Decreasinga Galápagos sea lion (GSL) Zalophus wollebaeki 5,000 Fluctuating Galápagos fur seal (GAFS) Arctocephalus galapagoensis 12,000 Fluctuating Japanese sea lion Zalophus japonicus Extinct Extinct

Walruses

Pacific Odobenus rosmarus divergens 200,000 Decreasing walrus Odobenus rosmarus rosmarus >14,000 Unknown

Earless Seals Phocidae

Hooded seal (HOS) cristata >400,000 Increasing Gray seal (GS) Halichoerus grypus Unknown Increasing (RIS) Histriophoca fasciata 490,000 Increasing Northern seal (NES) Mirounga angustirostris 101,000 Increasing Harp seal (HAS) Pagophilus groenlandicus 7,486,000 Increasing Western Atlantic (HS) vitulina concolor 40,000–100,0000 Increasing Western Pacific harbor seal (HS) Phoca vitulina richardsi 146,900 Stable Mediterranean (MMS) Monachus monachus 250–500 Decreasing (HMS) Monachus schauinslandi 1,400 Decreasing Ungava harbor seal (HS) Phoca vitulina mellonae 120–600 Decreasing (CS) Phoca caspica <100,000 Decreasing Baikal seal (BS) Phoca sibirica 5,000–6,000 Decreasing Eastern Atlantic harbor seal (HS) Phoca vitulina vitulina 98,000 Fluctuating (BS) Erignathus barbatus 100,000s Unknown Eastern Pacific harbor seal (HS) Phoca vitulina stejnegeri 7,300 Unknown Spotted (Largha) seal (SS) Phoca largha 335,000–450,000 Unknown Ringed seal (RS) hispida hispida 2,500,000 Unknown Baltic seal (RS) Pusa hispida botnica 5,000 Unknown Ladoga seal (RS) Pusa hispida ladogensis 5,000 Unknown ringed seal (RS) Pusa hispida ochotensis 800,000–1,000,000 Unknown Saimaa seal (RS) Pusa hispida saimensis 2,000–5,000 Unknown monk seal Monachus tropicalis Extinct Extinct

Southern Hemisphere

Eared Seals Otariidae

South American fur seal (SAFS) Arctocephalus australis 235,000–285,000 Increasing fur seal (NZFS) 135,000 Increasing Juan Fernandez fur seal (JFS) Arctocephalus philippii 18,000 Increasing

344 CASE STUDIES TABLE 27.1 ( CONTINUED) Pinniped Population Numbers and Trends Worldwide

Common Name Species Population Size Trend

Southern Hemisphere

Eared Seals Otariidae

Australian fur seal (AFS) Arctocephalus pusillus doriferus 60,000 Increasing Cape fur seal (CFS) Arctocephalus pusillus pusillus 1,700,000 Increasing fur seal (SFS) Arctocephalus tropicalis >310,000 Increasing (ANFS) Arctocephalus gazella 1,600,000 Increasing (ASL) cinerea 9,300–11,700 Stable (NZSL) Phocarctos hookeri 13,000 Stable (SASL) Otaria flavenscens 275,000 Decreasing

Earless Seals Phocidae

Leopard seal (LS) Hydruga leptonyx 220,000–440,000 Stable (WS) Leptonychotes weddelli 500,000–1,000,000 Stable Crabeater seal (CE) Lobodon carcinophagus 10,000,000–15,000,000 Stable Southern (SES) Mirounga leonina 640,000 Stable/decreasing (ROS) Ommatophoca rossi 100,000–650,000 Unknown

aStock specific

FIGURE 27.1. Present day distribution of Otariidae species. See Table 27.1 for species codes.

WHALING EFFECTS ON PINNIPED POPULATIONS 345 FIGURE 27.2. Present day distribution of Phocidae species. See Table 27.1 for species codes.

with lowered fertility rates after 1965 (Harding and Harkonen currently. Mass mortalities from (Likhoshway 1999). et al. 1989) occurred in 1987–1988 and in 1998. The best estimate of ribbon seal abundance in the is 120,000 to 140,000 animals, recorded in 1987 (Angliss TEMPERATE AND TROPICAL SPECIES and Lodge 2002). Two additional populations occur in the Okhotsk Sea. The estimated total abundance for the species Harbor seals occur widely in coastal, estuarine, and occasion- is 370,000 animals (Fedoseev 2000). An average of 9,000 to ally freshwater across the North Atlantic and Pacific 11,000 ribbon seals were harvested annually from the 1950s oceans. The nonmigratory nature of this species apparently through the 1960s. has resulted in considerable regional genetic differentiation. In 1973, Burns (1973) estimated the world Harbor seal population trends vary widely depending upon population at 335,000 to 450,000 animals. Fedoseev (1971) area and habitat. Populations are increasing at 3.5% to 7% per estimated a population of 168,000 in the Okhotsk Sea. Aerial year in California, , and (Jeffries et al. surveys of spotted seals hauled-out on the Bering Sea pack ice 1997; Carretta et al. 2001). These increases contrast with and along the western Alaskan produced an estimate reported declines of 65% to 85% during the 1970s and 1980s of 59,214 for this region (Angliss and Lodge 2002). Because in the Gulf of , Prince William Sound, and the Bering of the uncertainties in the population estimates for this Sea (Pitcher 1990; Small et al. 2003; see Figure 27.3). Harbor species, there is no information of population trends. seal numbers in the western North Atlantic have generally However, because spotted seals rely on ice, they are likely to increased during the past several decades, although there have respond to climate changes that have been observed in the been significant local declines. For example, the number of Bering Sea over the last 10 to 15 years (Tynan and DeMaster harbor seal pups born on Sable Island declined by about 95% 1997). between 1989 and 1997 (Bowen et al. 2003), apparently from The Caspian seal declined from an estimated 1 million indi- predation by (Lucas and Stobo 2000) and competition viduals at the beginning of the twentieth century to about with a rapidly growing gray seal population (Bowen et al. 70,000 by the late 1980s (Miyazaki 2002) This species is 2003). Harbor seal numbers have also declined substantially presently considered to be one of the twenty most threatened in the Eastern Atlantic, but here the apparent cause was a marine in the world. The Caspian seal population phocine distemper epidemic (Heide-Jorgensen and Harkonen decline was largely a consequence of — 1992; Heide-Jorgensen et al. 1992; Thompson et al. 2002). 115,000 to 174,000 have been harvested annually since the Once-abundant northern elephant seals were exploited early nineteenth century (Miyazaki 2002). The decline of extensively for oil during the eighteenth and nineteenth Caspian seals was exacerbated by a mass mortality event of centuries. By 1900 the species had been reduced to 20 to epizootic origin in 1997, which killed several thousand ani- 30 individuals (Hoelzel et al. 1993; Hoelzel 1999). Despite the mals. The has also declined steadily in recent years, resulting reduction in (Hoelzel 1999), from about 70,000 animals in the 1970s to about 5,000 animals northern elephant seals have recovered at an estimated

346 CASE STUDIES FIGURE 27.3. Population trends for Pacific harbor seal populations off the California coast (Carretta et al. 2003), the (Kodiak Island), Southeastern Alaska (Sitka and Ketchikan) (Small et al. 2003), and Tugidak Island (Pitcher 1990).

8.3% yr−1 throughout the species’ range (Cooper and Stewart seal populations increased in most areas. The current world 1983). Northern elephant seals in California were estimated population is estimated at 640,000 individuals, with major at 101,000 individuals in 2001 (Carretta et al. 2002). breeding colonies located on (113,000 pups Monk seals are the only tropical/subtropical phocid. per year), the Kerguelen Archipelago (43,000 pups per year), Populations of these species may never have been numerous (19,000 pups per year), Heard Island (17,000 because of the generally low productivity of tropical oceans. pups per year), and Peninsula Valdes (14,500 pups per year). Because of their small population size, monk seals are Paradoxically, despite their recovery following commercial vulnerable to die-offs resulting from disease, inbreeding and sealing and a lack of subsequent hunting pressure, southern low genetic variability, and human disturbance. Of the three elephant seal populations in the Pacific and Indian oceans recent species, the Hawaiian and Mediterranean monk seals declined remarkably (50% to 80%) between the 1950s and are endangered, and the is considered 1990s (McMahon et al. 2003). The proximate causes of theses extinct (Kenyon 1977). Although overall numbers are currently decreases are poorly understood. Some authors have attrib- stable, some Hawaiian monk seal colonies are increasing uted them to long-term environmental change leading to while others are in decline. Reasons for the declines include resource limitation (Burton et al. 1997; McMahon et al. 2003), human disturbance, habitat loss, disease, competition with whereas others have proposed the cause to be increased killer fisheries, predation, intraspecific , and entan- whale predation (Barrat and Mougin 1978; Guinet et al. 1992; glement with fisheries gear. Mediterranean monk seals are Branch and Williams, Chapter 20 of this volume). presently estimated at 250 to 500 individuals. The largest The remaining southern hemisphere phocids (Weddell, known aggregation of this species, which occurs at the Ross, crabeater, and seals) are restricted to the of Cape Blanc in the , suffered a continent and its surrounding pack ice. Although these mass mortality event of unknown origin in 1997 that reduced species have been harvested irregularly in past years, they its numbers from 317 to 109 individuals (Forcada et al. 1999). were never so extensively depleted as pinnipeds elsewhere in A hitherto unknown colony was recently discovered in the the world. Current harvest levels are regulated under the Cilician Bay off (Gucu et al. 2004). Convention on the Conservation of Antarctic Seals (CCAS). For various logistical reasons, estimates of abundance for the Antarctic phocids have been difficult to obtain. Current SOUTHERN HEMISPHERE SPECIES estimates are 220,000 to 440,000 for leopard seals; 500,000 Like the , the once-abundant southern to 1 million for Weddell seals; 10 to 15 million for crabeater elephant seal was heavily exploited during the eighteenth seals; and 100,000 to 650,000 for Ross seals. Given the and nineteenth centuries. Populations were severely reduced absence of historical estimates and the large uncertainties at all major breeding sites. Although controlled harvests were associated with modern-day population estimates, it is not reinstituted early in the twentieth century, southern elephant possible to ascertain current population trends for any of

WHALING EFFECTS ON PINNIPED POPULATIONS 347 the Antarctic phocids. Nonetheless, the relatively small have increased to an estimated 1.7 million individuals and number of animals harvested (ca. 39,000 since 1892) over a are growing at 3% per year (Butterworth et al. 1995). In con- wide geographical range is unlikely to have adversely trast, Australian fur seal populations, which have not been affected populations of any of these species; thus, changes hunted since 1923, have increased only to an estimated in distribution and abundance are likely due to other fac- 60,000 individuals, well below the presealing estimate of tors. Testa et al. (1991) documented cyclic patterns in the 175,000 to 225,000 individuals. These different population age structure and cohort strength of crabeater, Weddell, and growth rates and abundances have been attributed to varia- leopard seals related to the Southern Oscillation Index tion in food availability and differing strategies (SOI). Furthermore, Bengtson and Laws (1985) and Ballance (Arnould and Warneke 2002). et al. (Chapter 17 of this volume) suggested that a reported Other fur seal populations were also nearly hunted to decline in the age of first reproduction of crabeater seals was extinction during the commercial sealing era but have sim- caused by an increased availability of krill, which ostensi- ilarly rebounded. The sub-Antarctic fur seal, which breeds bly resulted from the depletion of baleen whales. The age of just north of the Antarctic polar front on sub-Antarctic and first reproduction increased again between 1963 through subtemperate islands, numbers more than 235,000 to 1976, a presumed physiological response to reduced prey 285,000 individuals and is increasing by as much as 9% to availability. 14% yr−1 in a few colonies (Wickens and York 1997). The , which occurs along the Pacific coast of South America, in the islands west of , in Otariid Population Trends the , and in and along the south- Like temperate-latitude phocids, most otariid species were ern coast of Brazil, was hunted during the sealing era and, nearly extirpated by overharvesting by the end of the nine- more recently, in regular small, controlled harvests in teenth century. With the cessation of harvest, most stocks Uruguay until the 1990s. While numbers of South Ameri- recovered to varying degrees. Overall, fur seal populations can fur seals are increasing, they remain diminished, appar- appear to have recovered more rapidly than sea lion popula- ently due to the recent commercial harvest. The New tions. Fur seals also outnumber sea by an of mag- Zealand fur seal, an estimated 135,000 animals, is protected nitude (nearly 8 million fur seals worldwide, in contrast to and increasing throughout its range in New Zealand and just over 600,000 sea lions). Variation in diet, foraging strate- (Wickens and York 1997). The , gies, and regional productivity may explain the differences in now the rarest of all fur seal species (about 7,000 individu- abundance and recovery rates between the two groups. als), was presumed extinct until a small breeding group Antarctic fur seals were thought to be extinct until a rem- was discovered at Isla de Guadalupe in 1928 (Townsend nant population of 1,000 to 1,200 animals was discovered 1928). This small colony was then nearly exterminated by at Bouvetøya in 1928 (Fevoden and Sømme 1976), and museum collectors (Bartholomew 1950; Hubbs 1956). The another 100 animals were discovered off Bird Island in the population bottleneck resulted in a substantial loss of AUQ1 1930s (Laws 1973). Since that time the Antarctic fur seal genetic variability (Weber et al. 2004). The Galápagos fur population has grown at about 10% yr−1, to a 1990 estimate seal, which is limited to the Galápagos Islands and was of 1.6 million animals (Boyd 1993). Although Antarctic fur greatly depleted during the sealing era, recovered to its esti- seals have increased throughout their range, Boveng et al. mated presealing population level of about 40,000 animals (1998) suggested that the slower recovery rate on the South by 1977–1978. However, population size in this species Shetland Islands is a result of predation. fluctuates considerably in response to El Niño events Northern fur seals inhabit the North Pacific Ocean and (Trillmich et al. 1991). For example, 90% pup mortality the Bering Sea, with primary breeding rookeries on the Pribilof and 45% overall mortality reduced the population to an and and smaller colonies in the Sea of estimated 6,000–8,000 animals following the 1997–1998 Okhotsk and Kurile Islands. An outlying colony also occurs El Niño event (Salazar 2002). The Juan Fernandez fur seal, on off the coast of southern California. which is confined to the islands off the coast of , con- Following the overharvest and depletion of Northern fur tained an estimated four million animals before the sealing seals during the eighteenth and nineteenth centuries, they era. This species, thought to be extinct until a small popu- were protected in 1911 and recovered significantly during the lation was rediscovered in 1966, is currently estimated at first half of the twentieth century, However, in contrast with approximately 18,000 animals and growing (Wickens and Antarctic fur seals, northern fur seal numbers began to York 1997). decline again in the 1950s, a trend that has continued to the In contrast to the fur seals, most sea lion populations are in AUQ2 present day (Angliss and Lodge 2004; Carretta et al. 2002). decline, and one species (the Japanese sea lion) is probably The cause of this ongoing decline is unknown. extinct. Galápagos sea lions have continued to decline from The closely related Cape and Australian fur seals were both anthropogenic impacts, El Niño events, and disease outbreaks, greatly depleted by commercial sealing. However, their pop- with a most recent count in 2002 of between 14,000 and ulations have since taken rather different trajectories. Cape 16,000 animals (Salazar 2002). The New Zealand (or Hooker’s) fur seal populations, while subjected to controlled hunts, sea lion, which once occurred all around New Zealand, was

348 CASE STUDIES depleted by subsistence and commercial hunting. Presently, its 2002), and an additional 44,000 to 53,000 animals in breeding range is restricted to a few sub-Antarctic islands (Aurioles-Gamboa and Zavala-Gonzalez 1994). (Gales and Fletcher 1999). Australian sea lions also were depleted by sealing, even though the larger populations of Potential Causes of Population Declines sympatric fur seals were the primary targets. This species is now one of the world’s rarest and most unusual sea lions, on In the preceding sections of this chapter we have provided a account of its 17.5-month breeding cycle (Higgins 1993), in broad overview of the population status and trends of pin- contrast to the 12-month cycle typical of this group. Popula- nipeds worldwide. Most species were reduced substantially tions of both New Zealand and Australian sea lions, while far during the era of commercial sealing. The explanation for below their estimated pre-exploitation levels of about 13,000 these early declines is clear and certain—humans killed them. and 10,000 (Gales et al. 1994; P. D. Shaughnessy et al., in However, populations have not all responded to the cessation review) respectively, are presently stable. However, unlike the of commercial sealing in the same way. Some species or local New Zealand sea lion, the Australian sea lion is widely dis- populations increased, often rapidly. Here again there is little tributed among 67 scattered colonies in southern and Western mystery as to why—reduced mortality, together with resource Australia. surpluses created by the earlier population reduction, prob- The South American sea lion, which ranges from Brazil to ably fueled population growth in a manner expected from , was decimated in the hunt for oil. Today’s populations simple demographic and ecological theory. However, other stand at approximately 20% of their historical numbers species and populations either did not recover from sealing (Cappozzo 2002). Although populations along the Pacific or did recover but have subsequently again declined. These coast of South America are poorly known, many animals latter cases are more difficult to understand. In the final apparently abandon this region during severe El Niño events. sections of this chapter we attempt to shed light on these Thompson et al. (2005) reported population declines in the perplexing trends by mapping known or suspected patterns Falkland Islands to <1.5% of the 1937 abundance estimate of variation in life history, behavior, and environment with between 1965 and 1990, for reasons that remain unclear. reported population trajectories. Our synthesis focuses on Pup production in the Falklands since 1990 has increased at three key patterns and processes: differing reproductive 3.8% to 8.5% per year, thus putting this population on a strategies between phocids and otariids; physiological limi- similar growth trajectory to the adjacent Argentinean tations associated with particular foraging and diving behavior; population. and the resulting susceptibility to disturbance in prey The northern or (SSL), which ranges from resources and predation. California to , was hunted for various reasons until the early 1970s. There is still a small subsistence take by Alaska Life History and Behavioral Correlates natives. Two stocks are currently recognized in U.S. waters, with Cape Suckling, Alaska (144°W) the demarcation point Phocids and otariids have solved the conflicting demands of between the eastern and western stocks. Despite the cessation terrestrial parturition and marine feeding in different ways of hunting and protection from other disturbances, the west- (Bartholomew 1970; Costa 1993). Most phocids are capital ern stock began a precipitous decline in the late 1970s or breeders, storing, prior to parturition, sufficient energy for early 1980s (Loughlin et al. 1992; NRC 2003). The western the entire lactation period. Otariids, in contrast, are income stock is currently listed as Endangered and the eastern stock breeders, feeding more or less continuously during lactation as Threatened under the U.S. Act. The (Costa 1991a,b, 1993; Boyd 2000). These different strategies known or suspected causes of SSL mortality include inciden- confer differing benefits and costs to phocids and otariids. tal losses in fisheries gear, entanglement in , Capital breeding disassociates reproductive success from local shooting, competition with fisheries for food, ocean climate food availability. The nutritional provisioning of pups by change, and predation by killer whales. SSL and their associ- phocid mothers is thus largely unconstrained by traveling ated ecosystem have been the objects of intensive research, time to and from the foraging grounds, thereby allowing yet there is still no widely accepted explanation for sea lions’ them to utilize prey that are more dispersed, patchy, unpre- recent decline (NRC 2003). dictable, or distant from the rookery. The necessity of feed- The , which ranges from Mexico to British ing during lactation constrains otariid females to forage Columbia, is the most abundant of all sea lion species. , closer to the rookery, thus linking reproductive success and largely because of perceived damage to commercial catches local prey abundance (Costa 1993) and thereby potentially and competition for salmonid fishery resources (Everitt and connecting population status to localized environmental Beach 1982), reduced the abundance of California sea lions in changes such as El Niño/Southern Oscillation events southern California and Mexico to approximately 1,500 indi- (Trillmich et al. 1991; see Figure 27.4 for the California sea viduals by the 1920s. The species has increased steadily at 5% lion). Significant alterations in trip duration, female condi- to 6.2% yr−1 through the latter part of the twentieth century tion, fecundity, pup growth rate, and survival in response to (NMFS 1997). Presently, there are an estimated 204,000 to reductions in prey availability caused by changing oceano- 214,000 California sea lions in U.S. waters (Carretta et al. graphic conditions are common in otariids (Costa et al. 1989, AUQ3

WHALING EFFECTS ON PINNIPED POPULATIONS 349 FIGURE 27.4. Pup production of California sea lions off the California coast (Carretta et al. 2002). Notice the different effect of the 1983 and 1998 strong El Niño/Southern Oscillation (ENSO) events.

Testa et al. 1991; Trillmich et al. 1991; Boyd et al. 1994; Boyd Island. As a capital breeder, the northern elephant seal can for- and Murray 2001). On the other hand, fasting or reduced age almost anywhere in the North Pacific Ocean (Stewart and feeding during lactation limits the total amount of energy DeLong 1993; LeBoeuf et al. 2000), thus providing this species and protein that can be invested in phocid young, resulting with greater access to prey resources. in a smaller relative pup mass at nutritional independence. Variation in dive behavior can also influence foraging effi- Phocid weaning mass reflects the mother’s foraging success ciency and, thus, the potential for prey limitation in popula- over the previous year; postweaning survival is related to tion regulation. That is, pinnipeds that operate at or near their both weaning mass (energy reserves provided by the mother) physiological limits should have little capacity to adjust for- and postweaning resource availability (Stewart and Lavigne aging effort in response to food availability, whereas those 1984). Furthermore, weaning in phocids is abrupt, thus pre- that operate below their physiological limits should not be so venting pups from learning from their mothers how to for- constrained. Thus, one would expect stronger covariation age—a potential disadvantage in times of food shortage. between population trends and food availability for species in Weaning is often synchronous within species, which means the former than in the latter group (Costa et al. 2001; Costa large numbers of inexperienced individuals will be simulta- and Gales 2003; Costa et al. 2004). This proposed relationship neously testing the waters near breeding colonies, thus should be particularly evident between benthic and making them susceptible to predation. The typically short column foragers, because benthic foragers may be working at breeding period in phocids also allows them to utilize unsta- levels closer to their maximum physiological diving capacity. ble breeding substrates, such as pack ice (Stirling 1975, 1983; Benthic foraging requires longer transit times, thus reducing Costa 1993). the time beneath the surface that is available to search for Implications of the aforementioned differences in repro- prey (Costa and Williams 1999). Because adults of benthic for- duction and foraging between phocids and otariids are poten- aging species are working at or near their physiological limit, tially exemplified by the striking differences in recovery rates the smaller juveniles, with their reduced physiological capa- of fur seals, elephant seals, and sea lions on , bilities and oxygen stores, should be particularly vulnerable to Mexico. While fur seals and elephant seals both increased fol- resource limitation. Survival of juveniles in benthic foraging lowing the cessation of hunting, the elephant seal recovery species might thus be a major determinant of demographic has been far more dramatic (Figure 27.5). During this same trends. Furthermore, benthic foraging species might be par- period, sea lion numbers at Guadalupe Island have remained ticularly sensitive to bottom trawlers, which disrupt the habi- low but relatively stable, whereas populations elsewhere have tat and remove the larger size-classes of fishes upon which they increased rapidly. As income breeders, California sea lions often depend (Thrush et al. 1998). On the other hand, the and Guadalupe fur seals must remain with their pups for benthos may be a more predictable source of prey than the almost a year, thus constraining them to feed near Guadalupe water column, and thus benthic foraging species may be less

350 CASE STUDIES FIGURE 27.5. Population trends from the three species of pinniped that are found on Guadalupe Island, Mexico: California sea lion, Guadalupe fur seal, and Northern elephant AUQ5 seal (data from Pablo-Gallo, unpublished).

affected by oceanographic perturbations such as El Niños than and jackals, , sharks, and killer whales (Weller water column feeders (Miller and Sydeman 2004). 2002). In the northern hemisphere, land- or ice-based pred- Observed relationships between aerobic dive limit (ADL), ators (people, , ) are particularly important, which is a measure of physiological dive capability, and foraging whereas in the southern hemisphere, ice seals are free from behavior across five otariid species (Antarctic and Australian fur terrestrial predators but are subjected to several aquatic seals; Australian, California, and New Zealand sea lions) pro- predators. The clearly divergent predator avoidance tactics vides an initial test of these predictions (Costa et al. 2004). The between Arctic and Antarctic pinnipeds, with Arctic species Antarctic fur seal makes short, shallow dives, while the Aus- fleeing into the water to escape predation and Antarctic tralian and New Zealand sea lions and the Australian fur seal species seeking refuge on the ice (Stirling 1975, 1983; Weller make deep prolonged dives to the benthos (Boyd et al. 1991; 2002), attest to the strength and importance of these predator- Costa and Gales 2000, 2003). California sea lions are especially prey interactions. interesting because they (at least the females and juveniles) dive Killer whales (Orcinus orca) are probably the most impor- epipelagically off the coast of southern California (Feldkamp et tant aquatic predator of marine mammals. Harbor seals are al. 1989), whereas they forage much deeper on mesopelagic prey the most commonly reported prey of killer whales in the in the Sea of Cortez (C. E. Kuhn, D. Aurioles-Gamboa, and D. P. northern hemisphere (Jefferson et al. 1991). However, killer Costa, unpublished). The near-surface-feeding Antarctic fur seal whales are also known to prey on many other species of and California sea lion in southern California forage well within pinnipeds, including the crabeater seal (Smith et al. 1981), their calcu-lated ADL (cADL), whereas the three benthically for- southern sea lion and (López and aging species/populations routinely exceed their cADL (Figure López 1985; Guinet et al. 2000), northern fur seal (M. Goebel, 27.6). For both fur seals and sea lions, the benthic foragers spend personal communication), and California sea lion. In some >40% of their time at sea diving, whereas the epipelagic foragers areas, killer whales intentionally strand themselves in order spend <30% of their time at sea diving (Figure 27.7). These find- to seize pinniped prey, such as southern sea lions and south- ings may explain why populations of many fur seal species (and ern elephant seals, on the beach (López and López 1985). the pelagic foraging California sea lion) have increased whereas Although predator control of pinniped populations is most sea lions (many of which occupy the same area as near-sur- difficult to verify, several studies either demonstrate or face-feeding fur seal species; Costa and Gales 2003) have suggest significant population level impacts of predation. remained stable or declined (Boyd et al. 1995; Sydeman and Harbor seal pup production at Sable Island declined from Allen 1999; Gales and Fletcher 1999; Gales et al. 1994). 600 in 1989 to just 32 in 1997 (Lucas and Stobo 2000; Bowen et al. 2003). An estimated 45% of the total pup production was killed by sharks during 1996. The increas- Risk of Predation ing population may have indirectly influenced Pinnipeds are preyed on by a variety of species, including harbor seals by attracting sharks to the region and com- other pinnipeds, humans, polar bears, , foxes, , peting with harbor seals for prey (Bowen et al. 2003).

WHALING EFFECTS ON PINNIPED POPULATIONS 351 FIGURE 27.6. Dive performance, defined as the ratio of average dive duration to the calculated aerobic dive limit (cADL), as a function of dive depth in five pinniped species. Range of cADL outlined by the box is the cADL plus 50% to account for the variability in FMR estimates. Notice that both the dive duration and tendency to exceed the cADL are greater in benthic foraging species.

FIGURE 27.7. The relative time spent foraging while at sea, compared across eight species of otariids. The group to the left consists of fur seals and the group to the right consists of sea lions. Of the sea lions only the California sea lion forages epipelagically, whereas only one fur seal forages benthically. Data for Antarctic fur seals comes from Cape Shirreff (CS) and Bird Island (BI) (Costa and Gales 2003).

352 CASE STUDIES Springer et al. (2003) recently speculated that incidentally entangled and damage fishing gear and remove or predation was principally responsible for widespread popu- damage fish caught in nets or on fishing lines. A currently lation declines of sea and pinnipeds in southwest expanding and largely unregulated trade in seal products Alaska. Their argument was based largely on feasibility (Reeves 2002), poor or misguided population management, analyses from demographic and energetic modeling and continued overexploitation of some populations are con- (Williams et al. 2004), strong evidence that killer whale pre- tributing factors. For example, although commercial sealing dation caused the sea decline (Estes et al. 1998), and has declined considerably since the 1960s, native hunters kill AUQ4 various inconsistencies in the available information with more than 100,000 ringed, bearded, ribbon, harp, hooded, and other purported explanations for the declines (NRC 2003). spotted seals annually (Reeves 2002). In addition, after a reduc- Branch and Williams (Chapter 20 of this volume), on the tion in takes of harp seals in the 1980s, government subsidies basis of similar evidence and analyses, have concluded have reinvigorated the Canadian commercial hunt, with that killer whale predation might also have figured promi- approximately 350,000 harp seals being taken in eastern nently in the decline of various Southern Ocean pinniped Canada and in 1998 (Lavigne 1999). Norwegian populations. In support of this latter suggestion, killer and Russian ships also take tens of thousands of harp and whales were observed taking up to 25% of the southern hooded seals annually in the Greenland and Barents . In elephant seal weanlings from one beach at Crozet Island the southern hemisphere, South American fur seals were and have been implicated in the decline of that population harvested in Uruguay until the 1990s. and the centuries-old (Guinet 1992; Guinet et al. 1992). hunt of Cape fur seals in southwestern Africa continues to take Pinnipeds also prey on one another. A single Hooker’s sea thousands of fur seals annually. lion on Macquarie Island killed 43% of the 130 Antarctic and Pinniped populations also have suffered adverse impacts by sub-Antarctic fur seal pups born over a two year period human modifications of coastal and marine environments, (Robinson et al. 1999). Similarly, leopard seals killed an esti- thus resulting in disturbance, loss of breeding and resting sites, mated 34% of the Antarctic fur seal pup production at Seal and alteration of foraging grounds (Reeves 2002). Exposure to Island (Boveng et al. 1998). In Punta San Juan, Peru, up to various pollutants is a problem in some areas, and disease 8.3% of South American fur seal pups are reportedly killed by outbreaks are often related to immune-response suppression Southern sea lions (Harcourt 1992). Northern fur seal pups are caused by a variety of pollutants (Reijnders and Aguilar 2002). killed and eaten by adult male Steller sea lions (Gentry and In addition to environmental forcing, pinniped popula- Johnson 1981). tion trends are influenced by variation in life history, behav- ior, and physiological capacity. Capital breeders or species Summary that have life history patterns that allow them to forage across ocean basins have a greater capability of recovery from In this chapter we have reviewed the current status and exploitation, whereas income breeders are more sensitive to trends of pinniped populations worldwide, with a focus on local oceanographic variations and associated limitations in the anthropogenic and natural biological processes that prey resources may recover more slowly. Similarly, differ- might be responsible for these trends. Although little or no ences in the foraging strategy of otariids may also be a factor data are available for some species, useful time series exist in their ability to respond to environmental fluctuations. for many others. Increasing populations include most of the Benthic diving otariids (e.g., Steller, Australian, southern, southern hemisphere fur seals, the California sea lion, har- and New Zealand sea lions) have a lower reproductive output bor seal populations off the west coast of the , than epipelagic species because they spend more time at sea and the northern elephant seal. Populations in decline diving and they push their physiological limits. This is fur- include northern and southern sea lions, the northern fur ther compounded by a potential for reduced juvenile survival seal, the southern elephant seal in parts of the Southern in benthic foraging species because of the reduced diving Ocean, and the harbor seal in southwest Alaska. The tropi- capability of juveniles. Differences in the foraging strategies cal monk seals are either stable at low levels or in decline. and reproductive patterns also may make certain pinnipeds Population trends for polar species are poorly known, more susceptible than others to predation. With both repro- although by and large these species appear to be both abun- ductive strategies the young are exposed to predation, but dant and fairly stable. adult female otariids will be more susceptible to increased Recovery failures or recent population declines are most predation because income breeders must make multiple visits commonly attributed to interactions with fisheries and envi- to and from the rookery. ronmental change. Pinniped interactions with fisheries include Although our review provides an overview of pinniped both operational and ecological effects (Harvey 1987; Mate population trends worldwide and a synthetic effort to under- and Harvey 1987). Ecological effects largely result from direct stand reasons for recent population declines and the failure competition, thus ostensibly reducing both potential fishery of various other populations to even recover from overex- yields and the environmental carrying capacity for pinnipeds. ploitation, in truth these patterns are poorly understood. Operational effects occur when pinnipeds and fishery opera- Although capital breeding would seem to convey an advan- tions come into direct contact. For example, pinnipeds can be tage to phocids over otariids, it cannot explain why both

WHALING EFFECTS ON PINNIPED POPULATIONS 353 harbor seals and Steller sea lions have declined at the same ———. 1970. A model for the evolution of pinniped . rate and magnitude over largely the same regions of south- Evolution 24: 546–559. west Alaska or why northern elephant seals have recovered Bengtson, J.L. and R.M. Laws. 1985. Trends in crabeater seal age so spectacularly whereas many southern elephant seal pop- Lobodon carcinophagus at sexual maturity: an insight into Antarctic marine interactions, in Antarctic nutrient cycles and ulations have collapsed. Similarly, although diving behavior food webs. W.R. Siegfried, P.R. Condy, and R.M. Laws, eds. and physiological limitation would seem to convey a relative Berlin: Springer-Verlag, pp. 667–675. disadvantage to benthic foraging over epipelagic foraging Boveng, P.L., L.M. Hiruki, M.K. Schwartz, and J.L. Bengtson. otariids, this explanation alone cannot account for the spec- 1998. Population growth of Antarctic fur seals: limitation by tacular population collapse of the benthically foraging Steller a top predator, the leopard seal? 79: 2863–2877. sea lion. On the other hand, although there is compelling Bowen, W.D. 1997. Role of marine mammals in aquatic ecosys- evidence that predators have driven the declines of small tems. Marine Ecology Progress Series 158: 267–274. isolated pinniped colonies and there have been arguments Bowen, W.D., S.L. Ellis, S.J. Iverson, and D.J. Boness. 2003. for the importance of killer whale predation in the large scale Maternal and newborn life-history traits during periods of population declines of seals, sea lions, and otters of the North contrasting population trends: Implications for explaining the Pacific, conclusive evidence is lacking. decline of harbour seals (Phoca vitulina), on Sable Island. Jour- nal of 261: 155–163. Given the extremely dynamic nature of pinniped popula- Boyd, I.L. 1993. Pup production and distribution of breeding tions and the high degree of uncertainty over ultimate causes Antarctic fur seals (Arctocephalus gazella) at South Georgia. of pinniped population irruptions and declines, it is not Antarctic Science 5(1): 17–24. unreasonable to imagine that these dynamics were influ- ———. 2000. State-dependent fertility in pinnipeds: contrasting enced at least to some degree by the effects of whaling on capital and income breeders. Functional Ecology 14: 623–630. ocean ecosystems. As Croll et al. (Chapter 16 of this volume) Boyd, I.L., J.P.Y. Arnould, T. Barton, and J.P. Croxall. 1994. point out, the great whales co-opted a significant proportion Foraging behaviour of Antarctic fur seals during periods of of the world’s marine production before whaling, and if contrasting prey abundance. Journal of Ecology 63: Roman and Palumbi’s (2003) prewhaling abundance esti- 703–713. mates are even close to being accurate, the magnitude of this Boyd, I.L., J.P. Croxall, N.J. Lunn, and K. Reid. 1995. Population effect would have been even greater. In a simplistic sense, less demography of Antarctic fur seals: the costs of reproduction and implications for life-histories. Journal of Animal Ecology production being co-opted by whales means potentially more 64: 505–518. for other ocean consumers. Such effects have been proposed Boyd, I.L., N.J. Lunn, and T. Barton. 1991. Time budgets and for- in the southern ocean, where the removal of krill-eating aging characteristics of lactating Antarctic fur seals. Journal of whales ostensibly led to increases in other krill consumers, Animal Ecology 60: 577–592. including some of the pinnipeds (Ballance et al., Chapter 17 Boyd, I.L. and A.W.A. Murray. 2001. Monitoring a marine ecosys- of this volume). However, as Paine (Chapter 2 of this volume) tem using responses of upper trophic level predators. Journal points out, food web dynamics are rarely so simple. Although of Animal Ecology 70: 747–760. complex food web dynamics of this sort are poorly known for Boyd, I.L., T.R. Walker, and J. Poncet. 1996. Status of southern ocean ecosystems, the very fact that pinniped population elephant seals at South Georgia. Antarctic Science 8: 237–244. dynamics fit so poorly into traditional explanatory molds Burns, J.J. 1973. Marine report. Pittman-Robertson Pro- raises the distinct possibility that the ecological influences of ject Report W-17-3, W-17-4, and W-17-5. Juneau: Alaska Department of and Game. whaling are associated with some of this uncertainty. Burton, H.R., T. Arnbom, I.L. Boyd, M. Bester, D. Vergani, and I. Wilkinson. 1997. Significant differences in weaning mass of Literature Cited southern elephant seals from five sub-Antarctic islands in rela- tion to population declines, in Antarctic communities: species, Angliss, R.P. and K.L. Lodge. 2002. Alaska stock structure and survival. D.W.H. Walton, ed. Cambridge, UK: assessments, 2002. U.S. Department of Commerce, NOAA Tech- Cambridge University Press, pp. 335–338. nical Memorandum NMFS-AFSC-133. Seattle: Alaska Butterworth, D.S., A.E. Punt, W.H. Oosthuizen, and P.A. Wick- Science Center. ens. 1995. The effects of future consumption by the Cape fur Arnould, J.P.Y., and R.M. Warneke. 2002. Growth and condition seal on catches and catch rates of the Cape hakes. 3. Model- in Australian fur seals (Arctocepha pusillus doriferus) (: ling the dynamics of the Cape fur seal Arctocephalus pusillus Pinnipedia). Australian Journal of Zoology 50: 53–66. pusillus. South African Journal of Marine Science 16: 161–183. Aurioles-Gamboa, D. and A. Zavala-Gonzalez. 1994. Ecological Cappozzo, H.L. 2002. South American sea lion, in Encyclopedia of factors that determine distribution and abundance of the marine mammals. W.F. Perrin, B. Würsig, and J.G.M. Thewis- California sea lion Zalophus californianus in the Gulf of sen, eds. San Diego: Academic Press, pp. 348–351. California. Ciencias Marinas 20: 535–553. Carretta, J.V., J. Barlow, K.A. Forney, M.M. Muto, and J. Baker. Barrat, A. and J.L. Mougin. 1978. The Southern elephant seal, 2001. U.S. Pacific marine mammal stock assessments: 2001. Mirounga leonina, of Possession Island, Crozet Archipelago, NOAA Technical Memorandum NMFS-SWFSC-317. La Jolla, 46°25´ south, 51°45´ east. Mammalia 42: 143–174 (in French). CA: Southwest Fisheries Science Center. Bartholomew, G.A. 1950. A male GFS on San Nicolas Island, Carretta, J.V., M.M. Muto, J. Barlow, J. Baker, K.A. Forney, and M. California. Journal of Mammalogy 31:175–180. Lowry. 2002. U.S. Pacific marine mammal stock assessments:

354 CASE STUDIES 2002. NOAA Technical Memorandum NMFS-SWFSC-346. Feldkamp, S.D., R.L. DeLong, and G.A. Antonelis. 1989. Diving La Jolla, CA: Southwest Fisheries Science Center. patterns of California sea lions, Zalophus californianus. Cooper, C.F. and B.S. Stewart. 1983. Demography of northern Canadian Journal of Zoology 67: 872–883. elephant seals Mirounga angustirostris 1911–1982. Science 219: Fevoden, S.E. and L. Sømme. 1976. Observations on birds and 969–971. seals at Bouvetøya. Norsk Polarinstitutt Årbok 1976: 367–371. Costa, D.P. 1991a. Reproductive and foraging energetics of high- Forcada, J., P.S. Hammond, and A. Aguilar. 1999. Status of the latitude , albatrosses, and pinnipeds: implications for Monachus monachus in the Western life history patterns. American Zoologist 31: 111–130. Sahara and the implications of a mass mortality event. Marine ———. 1991b. Reproductive and foraging energetics of pin- Ecology-Progress Series 188: 249–261. nipeds: implications for life history patterns, in Behaviour of Gales, N.J. and D.J. Fletcher. 1999. Abundance, distribution and pinnipeds. D. Renouf, ed. : Chapman and Hall, pp. status of the New Zealand sea lion, Phocarctos hookeri. Wildlife 300–344. Research 26: 35–52. ———. 1993. The relationship between reproductive and for- Gales, N.J., P.D. Shaughnessy, and T.E. Dennis. 1994. Distribu- aging energetics and the evolution of the Pinnipedia, in tion, abundance and breeding cycle of the Australian sea lion Marine mammals: advances in behavioural and population Neophoca cinerea (Mammalia: Pinnipedia). Journal of Zoology biology. I.L. Boyd, ed. Oxford: Oxford University Press, pp. (London) 234: 353–370. 293–314. Gentry, R.L. and J.H. Johnson. 1981. Predation by sea lions on Costa D.P. and N.J. Gales. 2000. Foraging energetics and diving northern fur seal neonates. Mammalia 45: 423–430. behaviour of lactating New Zealand seal lions, Phocarctos Gucu, A.C., G. Gucu, and H. Orek. 2004. Habitat use and pre- hookeri. Journal of Experimental Biology 203: 3655–3665. liminary demographic evaluation of the critically endangered ———. 2003. Energetics of a benthic diver: seasonal foraging Mediterranean monk seal (Monachus monachus) in the Cilician ecology of the Australian sea lion, Neophoca cinerea. Ecological Basin (Eastern Mediterranean). Biological Conservation 116: Monographs 73: 27–43. 417–431. Costa, D.P., N.J. Gales, and M.E. Goebel. 2001. Aerobic dive Guinet, C. 1992. Hunting behavior of killer whales (Orcinus orca) limit: How often does it occur in nature? Comparative around the . Canadian Journal of Zoology 70: Biochemistry and Physiology Part A: Molecular and Integrative 1656–1667 (in French). Physiology 129A: 771–783. Guinet, C., P. Jouventin, and H. Weimerskirch. 1992. Population Costa, D.P., C.E. Kuhn, M.J. Weise, S.A. Shaffer, and J.P.Y. changes, movements of southern elephant seals on Crozet and Arnould. 2004. When does physiology limit the foraging Kerguelen Archipelagos in the last decades. Polar Biology 12: behaviour of freely diving mammals? in Animals and environ- 349–356. ments: proceedings of the 3rd International Conference on Compar- Guinet, C., L.G. Barrett-Lennard, and B. Loyer. 2000. Co-ordi- ative Physiology and Biochemistry, KwaZulu/Natal, , nated attack behavior and prey sharing by killer whales at 7–13 August 2004. S. Morris and A. Vosloo, eds. International Crozet Archipelago: strategies for feeding on negatively buoy- Congress Series 1275. Amsterdam: Elsevier, pp. 359–366. ant prey. Marine Mammal Science 16: 829–834. Costa, D.P. and T.M. Williams. 1999. Marine mammal energet- Harcourt, R. 1992. Factors affecting early mortality in the South ics, in Biology of marine mammals. J.E. Reynolds and S.A. Rom- American fur seal Arctocephalus australis in Peru: density- mel, eds. Washington, DC: Smithsonian Institution Press, pp. related effects and predation. Journal of Zoology 226: 176–217. 259–270. Demere, T.A. 1994. The family Odobenidae: A phylogenetic Harding, K.C. and Harkonen, T.J. 1999. Development in the analysis of fossil and living taxa. Proceedings of the San Diego Baltic grey seal (Halichoerus grypus) and ringed seal (Phoca Society of Natural History 29: 99–123. hispida) populations during the 20th century. Ambio 28(7): Demere, T.A., A. Berta, and P.J. Adam. 2003. Pinnipedimorph 619–627. evolutionary biogeography. Bulletin of the American Museum of Harvey, J.T. 1987. Population dynamics, annual food consump- Natural History 279: 32–76. tion, movements, and dive behavior of harbor seals, Phoca Estes, J.A., M.T. Tinker, T.M. Williams, and D.F. Doak. 1998. vitulina, in Oregon. Ph.D. thesis, Oregon State University, Killer whale predation on sea otters linking oceanic and Corvallis. nearshore ecosystems. Science 282: 473–476. Healey, B.P., and G.B. Stenson. 2000. Estimating pup production Everitt, R.D. and R.J. Beach. 1982. Marine mammal-fisheries and population size of the northwest Atlantic harp seal (Phoca interactions in Oregon and Washington: an overview, in groenlandica). CSAS Research Document 2000/081. Ottawa: Marine mammals: conflicts with fisheries, other management prob- Canadian Science Advisory Secretariat. lems, and research needs. D.G. Chapman and L.L. Eberhardt, Heide-Jorgensen, M.P., and T. Harkonen. 1992. Epizootiology of eds. Transactions of the 47th North American Wildlife and the seal disease in the eastern . Journal of Applied Natural Resources Conference. Washington, DC: Wildlife Ecology 29: 99–107. Management Institute, pp. 253–263. Heide-Jorgensen, M.P., T. Harkonen, R. Dietz, and P.M. Thompson. Fedoseev, G.A. 1971. Distribution and population of seals at pup 1992. Retrospective of the 1988 European seal epizootic. and molting rookeries in the Sea of Okhotsk. Trudy Atlantich- Diseases of Aquatic Organisms 13: 37–62. eskogo Nauchno-Issledovatel’Skogo Instituta Rybnogo Khozyaistva Higgins, L.V. 1993. The nonannual, nonseasonal breeding cycle i Okeanografii 39: 87–99 (in Russian). of the Australian sea lion, Neophoca cinerea. Journal of Mam- ———. 2000. Population biology of ice-associated forms of seals and malogy 74: 270–274. their role in the Northern Pacific ecosystems. Moscow: Center for Hoelzel, A.R. 1999. Impact of population bottlenecks on genetic Russian Environmental Policy. variation and the importance of life-history: a case study of the

WHALING EFFECTS ON PINNIPED POPULATIONS 355 northern elephant seal. Biological Journal of the Linnean Society NMFS. 1997. Impacts of California sea lions and Pacific harbor seals 68: 23–39. on salmonids and the coastal ecosystems of Washington, Oregon, Hoelzel, A.R., J. Halley, S.J. O’Brien, C. Campagna, T. Arnbom, and California. NOAA Technical Memorandum NMFS-NWFSC- B. Le Boeuf, K. Ralls, and G.A. Dover. 1993. Elephant seal 28. Seattle: Northwest Fisheries Science Center. genetic variation and the use of simulation models to inves- NRC. 2003. The decline of the Steller sea lion in Alaskan waters: tigate historical population bottlenecks. Journal of Heredity 84: untangling food webs and fishing nets. Washington, DC: National 443–449. Academies Press. Hubbs, C.L. 1956. Back from oblivion, Guadalupe fur seal: still a Pitcher, K.W. 1990. Major decline in number of harbor seals living species. Pacific Discovery 9: 14–21. Phoca vitulina richardsi on Tugidak Island, Gulf of Alaska, North Jefferson, T.A., P.J. Stacey, and R.W. Baird. 1991. A review of Pacific Ocean. Marine Mammal Science 6: 121–134. killer whale interactions with other marine mammals: preda- Reeves, R.R. 2002. Conservation efforts, in Encyclopedia of marine tion to co-existence. Mammal Review 21: 151–180. mammals. W.F. Perrin, B. Würsig, and J.G.M. Thewissen eds. Jeffries, S.J., R.F. Brown, H.R. Huber, and R.L. DeLong. 1997. San Diego: Academic Press, pp. 276–297 Assessment of harbor seals in Washington and Oregon, 1996, Reijnders, P.J.H. and A. Aguilar. 2002. Pollution and marine in Marine Mammal Protection Act and Endangered Species Act mammals, in Encyclopedia of marine mammals. W.F. Perrin, B. implementation program, 1996. P.S. Hill and D.P. DeMaster, eds. Würsig, and J.G.M. Thewissen, eds. San Diego: Academic AFSC Processed Report 97-10. Seattle: Alaska Fisheries Science Press, pp. 948–957. Center, pp. 83–94. Robinson, S., L. Wynen, and S. Goldsworthy. 1999. Predation by Kenyon, K.W. 1977. Caribbean monk seal extinct. Journal of a Hooker’s sea lion (Phocarctos hookeri) on a small population Mammalogy 58: 97–98. of fur seals (Arctocephalus spp.) at Macquarie Island. Marine Kovacs, K.M. 2002. Bearded seal, in Encyclopedia of marine mam- Mammal Science 15: 888–893. mals. W.F. Perrin, B. Würsig, and J.G.M. Thewissen, eds. San Roman, R. and S.R. Palumbi. 2003. Whales before whaling in the Diego: Academic Press, pp. 84–87. North Atlantic. Science 301: 508–510. Lavigne, D.M. 1999. Estimating total kill of Northwest Atlantic Salazar, S.K. 2002. Lobo marino y lobo peletero, in Reserva marina harp seals, 1994–1998. Marine Mammal Science 15: 871–878. de Galápagos: línea base de la biodiversidad. E. Danulat and G.J. Laws, R.M. 1977. Seals and whales of the Southern Ocean. Philo- Edgar, eds. Puerto Ayora, Santa Cruz, Galápagos, : sophical Transactions of the Royal Society of London Series B: Charles Darwin Foundation, pp. 267–289. Biological Sciences 279: 81–96. Small, R.J., G.W. Pendleton, and K.W. Pitcher. 2003. Trends in LeBoeuf, B.J., D.E. Crocker, D.P. Costa, S.B. Blackwell, P.M. Webb, abundance of Alaska harbor seals, 1983-2001. Marine Mammal and D.S. Houser. 2000. Foraging ecology of northern elephant Science 19: 344–362. seals. Ecological Monographs 70: 353–382. Smith, T.G., D.B. Siniff, R. Reichle, S. Stone. 1981. Coordinated Likhoshway, Y.V., M.A. Grachev, V.P. Kumarev, Y.V. Solodun, behavior of killer whales, Orca orcinus hunting crab-eater seal, O.A. Goldberg, O.I. Belykh, F.G. Nagiev, V.G. Nikulina, and Lobodon carcinophagus. Canadian Journal of Zoology 59(6): B.S. Kolesnik. 1989. Baikal seal virus. Nature 339(6222): 266. 1185–1189. López, J.C. and D. López. 1985. Killer whales (Orcinus orca) of Springer, A.M., J.A. Estes, G.B. van Vliet, T.M. Williams, D.F. and their behavior of intentional stranding while Doak, E.M. Danner, K.A. Forney, and B. Pfister. 2003. Sequen- hunting nearshore. Journal of Mammalogy 66: 181–183. tial megafaunal collapse in the North Pacific Ocean: an ongo- Loughlin, T.R., A.S. Perlov, and V.A. Vladimirov. 1992. Range- ing legacy of industrial whaling? Proceedings of the National wide survey and estimation of total number of Steller sea lions Academy of Sciences 100: 12223–12228. in 1989. Marine Mammal Science 8: 220–239. Stenson, G.B., R.A. Myers, M.O. Hammill, I.H. Ni, W.G. Warren, Lucas, Z. and P.Y. Daoust. 2002. Large increases of harp seals and M.C.S. Kingsley. 1993. Pup production of harp seals, Phoca (Phoca groenlandica) and hooded seals (Cystophora cristata) on groenlandica, in the northwest Atlantic. Canadian Journal of Sable Island, , since 1995. Polar Biology 25: Fisheries and Aquatic Sciences 50: 2429–2439. 562–568. Stewart, B.S. and R.L. De Long. 1993. Seasonal dispersion and Lucas, Z. and W.T. Stobo. 2000. Shark-inflicted mortality on a habitat use of foraging northern elephant seals. Symposia of the population of harbour seals (Phoca vitulina) at Sable Island, Zoological Society of London 66: 179–194. Nova Scotia. Journal of Zoology 252: 405–414. Stewart, R.E.A. and D.M. Lavigne. 1984. Energy transfer and Mate, B.R. and J.T. Harvey (editors). 1987. Acoustical deterrents in female condition in nursing harp seals Phoca groenlandica. marine mammal conflicts with fisheries: a workshop held February Holarctic Ecology 7: 182–194. 17–18, 1986, at Newport, Oregon. Publ. No. ORESU-W-86-001. Stirling, I. 1975. Factors affecting the evolution of social behav- Corvallis: Oregon State University. ior in the pinnipedia. Rapports et Procès-verbaux des Réunions McMahon, C.R., H.R. Burton, and M.N. Bester. 2003. A demo- du Conseil International pour l’Exploration de la Mer 169: graphic comparison of two southern elephant seal popula- 205–212. tions. Journal of Animal Ecology 72: 61–74. ———. 1983. The evolution of mating systems in pinnipeds, in Miller, A.K. and W.J. Sydeman. 2004. Rockfish response to low- Advances in the study of mammalian behavior. J.F. Eisenberg and frequency ocean as revealed by the diet of a D.G. Kleiman, eds. American Society of Mammalogists, Special marine bird over multiple time scales. Marine Ecology Progress Publication No. 7. Lawrence, KS: Allen Press, pp. 489–527. Series 281: 207–216. Sydeman, W.J. and S.G. Allen. 1999. Pinniped population Miyazaki, N. 2002. Ringed, Caspian, and Baikal seals, in Encyclo- dynamics in central California: correlations with sea surface pedia of marine mammals. W.F. Perrin, B. Würsig, and J.G.M. temperature and upwelling indices. Marine Mammal Science Thewissen, eds. San Diego: Academic Press, pp. 1033–1037. 15: 446–461.

356 CASE STUDIES Testa, J.W., G. Oehlert, D.G. Ainley, J.L. Bengtson, D.B. Siniff, responses to environmental stress. F. Trillmich and K.A. Ono R.M. Laws, and D. Rounsevell. 1991. Temporal variability in (eds.). Ecological Studies, vol. 88. Berlin: Springer-Verlag, pp. Antarctic marine ecosystems: periodic fluctuations in the pho- 247–270. cid seals. Canadian Journal of Fisheries and Aquatic Sciences 48: Tynan, C.T. and D.P. DeMaster. 1997. Observations and predic- 631–639. tions of Arctic climatic change: potential effects on marine Thompson, D., I. Strange, M. Riddy, and C.D. Duck. 2005. The mammals. Arctic 50: 308–322. size and status of the population of southern sea lions Otaria Waring, G.T., J.M. Quintal, and C.P. Fairfield. 2002. U.S. Atlantic flavescens in the Falkland Islands. Biological Conservation 121: and marine mammal stock assessments 2002. 357–367. NOAA Technical Memorandum NMFS-NE-169. Woods Hole, Thompson. P.M., H. Thompson, and A.J. Hall. 2002. Prevalence MA: Northeast Fisheries Science Center. of morbillivirus antibodies in Scottish harbour seals. Veterinary Weber, D.S., B.S. Stewart, and N. Lehman. 2004. Genetic conse- Record 151(20): 609–610. quences of a severe population bottleneck in the Guadalupe Thrush, S.F., J.E. Hewitt, V.J. Cummings, P.K. Dayton, M. Cryer, fur seal (Arctocephalus townsendi). Journal of Heredity 95: S.J. Turner, G.A. Funnell, R.G. Budd, C.J. Milburn, and M.R. 144–153. Wilkinson. 1998. Disturbance of the marine benthic habitat by Weller, D.W. 2002. Predation on marine mammals, in Ency- commercial fishing: impacts at the scale of the fishery. Ecological clopedia of marine mammals. W.F. Perrin, B. Würsig, and Applications 8: 866–879. J.G.M. Thewissen, eds. San Diego: Academic Press, pp. Townsend, C.H. 1928. Reappearance of the lower California fur 985–994. seal. Bulletin of the Zoological Society 31: 173–174. Wickens, P., and A.E. York. 1997. Comparative population Trillmich, F., K.A. Ono, D.P. Costa, R.L. DeLong, S.D. Feldkamp, dynamics of fur seals. Marine Mammal Science 13: 241–292. J.M. Francis, R.L. Gentry, C.B. Heath, B.J. LeBoeuf, P. Majluf, Williams, T.M., J.A. Estes, D.F. Doak, and A.M. Springer. 2004. and A.E. York. 1991. The effects of El Niño on pinniped pop- Killer appetites: assessing the role of predators in ecological ulations in the eastern Pacific, in Pinnipeds and El Niño: communities. Ecology 85: 3373–3384.

[AUQ1] (Pinniped Population Trends, Otariid Population Trends, 2nd paragraph) Please add Laws 1973 to Literature Cited. [AUQ2] (Pinniped Population Trends, Otariid Population Trends, 3rd paragraph) Unless you mean Angliss and Lodge 2002, please add Angliss and Lodge 2004 to Lit Cited. [AUQ3] (Potential Causes of Population Decline, Life History and Behavioral Correlates) Please add Costa et al. 1989 to Lit Cited. [AUQ4] (Potential Causes of Population Decline, Risk of Predation, 4th para) Please check that Williams et al. 2004 citation, added to Lit Cited from a different chapter, is the document you intended. [AUQ5] (Figure 27.5, formerly Figure 27.4) Please provide initials for Pablo-Gallo.

WHALING EFFECTS ON PINNIPED POPULATIONS 357