Potential Influences of Whaling on the Status and Trends of Pinniped Populations

Transcription

1 TWENTY-SEVEN Potential Influences of Whaling on the Status and Trends of Pinniped Populations DANIEL P. COSTA, MICHAEL J. WEISE, AND JOHN P. Y. ARNOULD Although this volume focuses on whales and whaling, the depletion of great whales over the last 50 to 150 years perturbed the marine interaction web, thus influencing many other species and ecosystem processes (Estes, Chapter 1 of this volume; Paine, Chapter 2 of this volume). Such interaction web effects have been hypothesized for several pinniped species. For example, the reduction of great whales in the Southern Ocean may have caused seal and penguin populations to increase because of reduced competition for their shared prey, krill (Laws 1977; Ballance et al., Chapter 17 of this volume). In addition, pinnipeds share some of the same predators, especially killer whales, as large whales do. Declines in whale populations may thus have caused the decline of certain pinniped populations because of redirected predation by killer whales (Springer et al. 2003; Branch and Williams, Chapter 20 of this volume). These purported indirect effects of whales on pinnipeds are poorly documented and controversial. Since most of the arguments are area- or species-specific, a global overview of the known patterns and causes for pinniped population change is topical and relevant. Because of differences in body size and life history, pinnipeds are both easier to study, and possibly more sensitive to environmental fluctuations, than most cetaceans are. Pinnipeds are 1 to 2 orders of magnitude smaller in mass than whales, which result in greater mass-specific rates of food consumption. Thus the pinnipeds have physiological and environmental scaling functions that must be considerably different from those of the great whales. For example, although some pinnipeds have remarkable abilities to fast, even the most extreme durations of fasting in pinnipeds fall easily within the abilities of large cetaceans. The relatively small size of pinnipeds compared with cetaceans results in a much higher mass-specific metabolism and thus a shorter fasting duration. These differences should constrain pinnipeds to operate at smaller spatial and temporal scales than the large cetaceans, thus making pinnipeds more sensitive to variations in prey abundance and distribution. Smaller size is also linked to a shorter generation time in pinnipeds, which makes their populations more vulnerable to environmental disturbances but also affords them a greater potential for population growth. All of these characteristics suggest that pinniped populations should be more responsive to changes in their environment than the large whales are. Pinnipeds have a nearly cosmopolitan distribution in the world oceans, although most species occur in temperate to polar regions. Abundances range across species from 342

2 a few hundred to tens of millions of individuals. Estimates of abundance or trends in population numbers are the most useful indicators of population status. Most populations were severely depleted by commercial harvesting. However, species distributions and population abundances before sealing are often unknown, because sealing ships did not keep adequate records. Furthermore, reliable modern abundance estimates are lacking for many species. Despite these problems, the history and trends in abundance of the majority of pinnipeds is reasonably well known. In this chapter we review the current status and trends of pinniped populations worldwide, and, where possible, we summarize the known or suspected reasons for recent declines. Trends in pinniped populations attributed to natural biological processes are evaluated in terms of reproductive strategies, physiological limitations, and the resultant susceptibility to disturbance in prey resources and predation brought about by these factors. Pinniped Population Trends The present-day abundances of species do not always reflect their pre-exploitation numbers. Some species that were decimated to near-extinction are now very abundant, whereas others have either not recovered or have recovered and subsequently declined. Population abundance in pinnipeds ranges over four orders of magnitude across species from the Mediterranean and Hawaiian monk seals, which number in the hundreds of individuals, to the crabeater seal with an estimated abundance of 10 to 15 million individuals (Table 27.1). Phocids are generally more abundant than otariids. Fifteen of the 19 phocid species number greater than 100,000 individuals, whereas only 8 of the 17 otariid species number greater than 100,000 individuals. Pinnipeds range throughout the world oceans. Although the preponderance of species occurs in the northern hemisphere (Figures 27.1 and 27.2), the southern hemisphere contains far more individuals. The abundance of crabeater and Antarctic fur seals alone exceeds the combined abundance of all northern hemisphere species. The lesser number of species in the southern hemisphere may reflect a northern hemisphere center of origin for otariids and phocids (Costa 1993; Demere 1994; Demere et al. 2003). The larger numbers of individuals in the southern hemisphere likely result from highly productive Antarctic and sub- Antarctic waters coupled with an abundance of predatorfree islands. The relative scarcity of human settlements (which invariably lead to habitat loss, direct and indirect pinniped/fisheries interactions, and hunting pressure) may also contribute to the larger sizes of southern hemisphere pinnipeds. The relative abundance of phocids is likely due to their generally inhabiting the highly productive polar and subpolar regions (Bowen 1997). Similarly, the three most abundant otariid species the northern, Antarctic, and Cape fur seals all forage in seasonally productive, high-latitude ecosystems. Phocid Population Trends ARCTIC SPECIES There are six species of ice-breeding phocids in the northern hemisphere (harp, hooded, bearded, ringed, spotted, and ribbon seals), many of which annually migrate between subarctic and arctic regions. Because of the difficulty in conducting surveys in this harsh environment, the abundance of many of these species is not well known. Harp and hooded seals are both divided into three stocks (eastern Canada, White Sea, and West Ice), each identified with a specific breeding site. Recent modeling efforts indicate that a harvest of 460,000 young harp seals per year is holding the eastern Canada stock stable at about 5.2 million individuals (Healey and Stenson 2000). The other harp seal stocks are smaller approximately 1.5 to 2.0 million in the White Sea and 286,000 on the West Ice. The best current population estimate for hooded seals is 400,000 to 450,000 animals (Stenson et al. 1993). Marked increases in the number of harp and hooded seals occurred on Sable Island in the mid-1990s (Lucas and Daoust 2002). Populations of bearded seals were decimated by early commercial sealing. Russia continued a commercial harvest of bearded seals, with catches exceeding 10,000 animals yr 1 during the 1950s and 1960s. In the 1970s and 1980s quotas were introduced to limit harvests on declining populations to a few thousand animals annually (Kovacs 2002). Today, bearded seals are an important subsistence resource to arctic peoples, with a few thousand animals taken annually for use as human food, dog food, and clothing. Reliable estimates of the total population of bearded seals do not exist. Early estimates of just the Bering-Chukchi Sea population ranged from 250,000 to 300,000. Discrepancies in recent survey efforts in 1999 and 2000 have precluded an updated estimate, but the abundance may be much greater than previously described (Waring et al. 2002). Currently, five distinct subspecies of ringed seals are recognized. Population estimates for most of these are outdated, and there are many uncertainties in the estimation and sampling methods. Nonetheless, Bychkov (in Miyazaki 2002) estimated that there were 2.5 million in the Arctic Ocean and 800,000 to 1 million in the Sea of Okhotsk in The Baltic ringed seal population decreased from 190,000 to 220,000 animals at the beginning of the twentieth century to approximately 5,000 during the 1970s. In the mid-1960s, the remaining seals were afflicted by sterility, likely caused by organochlorides (Harding and Harkonen 1999; Reijnders and Aguilar 2002), which inhibited natural population growth during the subsequent 25-year period. Ringed seals are hunted in many regions (Miyazaki 2002). Thus, the decrease in seal numbers was a consequence of excessive hunting in combination WHALING EFFECTS ON PINNIPED POPULATIONS 343

3 TABLE 27.1 Pinniped Population Numbers and Trends Worldwide Common Name Species Population Size Trend Northern Hemisphere Eared Seals Otariidae Guadalupe fur seal (GFS) Arctocephalus townsendi 7,000 Increasing California sea lion (CSL) Zalophus californianus 237, ,000 Increasing Northern fur seal (NFS) Callorhinus ursinus 1,400,000 Decreasing Steller sea lion (SSL) Eumatopias jubatus <75,000 Decreasing a 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 Odobenidae Pacific walrus Odobenus rosmarus divergens 200,000 Decreasing Atlantic walrus Odobenus rosmarus rosmarus >14,000 Unknown Earless Seals Phocidae Hooded seal (HOS) Cystophora cristata >400,000 Increasing Gray seal (GS) Halichoerus grypus Unknown Increasing Ribbon seal (RIS) Histriophoca fasciata 490,000 Increasing Northern elephant seal (NES) Mirounga angustirostris 101,000 Increasing Harp seal (HAS) Pagophilus groenlandicus 7,486,000 Increasing Western Atlantic harbor seal (HS) Phoca vitulina concolor 40, ,0000 Increasing Western Pacific harbor seal (HS) Phoca vitulina richardsi 146,900 Stable Mediterranean monk seal (MMS) Monachus monachus Decreasing Hawaiian monk seal (HMS) Monachus schauinslandi 1,400 Decreasing Ungava harbor seal (HS) Phoca vitulina mellonae Decreasing Caspian seal (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 Bearded seal (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 Unknown Ringed seal (RS) Pusa hispida hispida 2,500,000 Unknown Baltic seal (RS) Pusa hispida botnica 5,000 Unknown Ladoga seal (RS) Pusa hispida ladogensis 5,000 Unknown Sea of Okhotsk ringed seal (RS) Pusa hispida ochotensis 800,000 1,000,000 Unknown Saimaa seal (RS) Pusa hispida saimensis 2,000 5,000 Unknown Caribbean monk seal Monachus tropicalis Extinct Extinct Southern Hemisphere Eared Seals Otariidae South American fur seal (SAFS) Arctocephalus australis 235, ,000 Increasing New Zealand fur seal (NZFS) Arctocephalus forsteri 135,000 Increasing Juan Fernandez fur seal (JFS) Arctocephalus philippii 18,000 Increasing 344 CASE STUDIES

4 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 Subantarctic fur seal (SFS) Arctocephalus tropicalis >310,000 Increasing Antarctic fur seal (ANFS) Arctocephalus gazella 1,600,000 Increasing Australian sea lion (ASL) Neophoca cinerea 9,300 11,700 Stable New Zealand sea lion (NZSL) Phocarctos hookeri 13,000 Stable South American sea lion (SASL) Otaria flavenscens 275,000 Decreasing Earless Seals Phocidae Leopard seal (LS) Hydruga leptonyx 220, ,000 Stable Weddell seal (WS) Leptonychotes weddelli 500,000 1,000,000 Stable Crabeater seal (CE) Lobodon carcinophagus 10,000,000 15,000,000 Stable Southern elephant seal (SES) Mirounga leonina 640,000 Stable/decreasing Ross seal (ROS) Ommatophoca rossi 100, ,000 Unknown a Stock specific FIGURE Present day distribution of Otariidae species. See Table 27.1 for species codes. WHALING EFFECTS ON PINNIPED POPULATIONS 345

5 FIGURE Present day distribution of Phocidae species. See Table 27.1 for species codes. with lowered fertility rates after 1965 (Harding and Harkonen 1999). The best estimate of ribbon seal abundance in the Bering Sea is 120,000 to 140,000 animals, recorded in 1987 (Angliss and Lodge 2002). Two additional populations occur in the Okhotsk Sea. The estimated total abundance for the species is 370,000 animals (Fedoseev 2000). An average of 9,000 to 11,000 ribbon seals were harvested annually from the 1950s through the 1960s. In 1973, Burns (1973) estimated the world spotted seal population at 335,000 to 450,000 animals. Fedoseev (1971) estimated a population of 168,000 in the Okhotsk Sea. Aerial surveys of spotted seals hauled-out on the Bering Sea pack ice and along the western Alaskan coast produced an estimate of 59,214 for this region (Angliss and Lodge 2002). Because of the uncertainties in the population estimates for this species, there is no information of population trends. However, because spotted seals rely on ice, they are likely to respond to climate changes that have been observed in the Bering Sea over the last 10 to 15 years (Tynan and DeMaster 1997). The Caspian seal declined from an estimated 1 million individuals at the beginning of the twentieth century to about 70,000 by the late 1980s (Miyazaki 2002) This species is presently considered to be one of the twenty most threatened marine mammals in the world. The Caspian seal population decline was largely a consequence of overexploitation 115,000 to 174,000 have been harvested annually since the early nineteenth century (Miyazaki 2002). The decline of Caspian seals was exacerbated by a mass mortality event of epizootic origin in 1997, which killed several thousand animals. The Baikal seal has also declined steadily in recent years, from about 70,000 animals in the 1970s to about 5,000 animals currently. Mass mortalities from morbillivirus (Likhoshway et al. 1989) occurred in and in TEMPERATE AND TROPICAL SPECIES Harbor seals occur widely in coastal, estuarine, and occasionally freshwater habitats across the North Atlantic and Pacific oceans. The nonmigratory nature of this species apparently has resulted in considerable regional genetic differentiation. Harbor seal population trends vary widely depending upon area and habitat. Populations are increasing at 3.5% to 7% per year in California, Oregon, and Washington (Jeffries et al. 1997; Carretta et al. 2001). These increases contrast with reported declines of 65% to 85% during the 1970s and 1980s in the Gulf of Alaska, Prince William Sound, and the Bering Sea (Pitcher 1990; Small et al. 2003; see Figure 27.3). Harbor seal numbers in the western North Atlantic have generally increased during the past several decades, although there have been significant local declines. For example, the number of harbor seal pups born on Sable Island declined by about 95% between 1989 and 1997 (Bowen et al. 2003), apparently from predation by sharks (Lucas and Stobo 2000) and competition with a rapidly growing gray seal population (Bowen et al. 2003). Harbor seal numbers have also declined substantially in the Eastern Atlantic, but here the apparent cause was a phocine distemper epidemic (Heide-Jorgensen and Harkonen 1992; Heide-Jorgensen et al. 1992; Thompson et al. 2002). Once-abundant northern elephant seals were exploited extensively for oil during the eighteenth and nineteenth centuries. By 1900 the species had been reduced to 20 to 30 individuals (Hoelzel et al. 1993; Hoelzel 1999). Despite the resulting reduction in genetic diversity (Hoelzel 1999), northern elephant seals have recovered at an estimated 346 CASE STUDIES

6 FIGURE Population trends for Pacific harbor seal populations off the California coast (Carretta et al. 2003), the Gulf of Alaska (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 1983). Northern elephant seals in California were estimated at 101,000 individuals in 2001 (Carretta et al. 2002). Monk seals are the only tropical/subtropical phocid. Populations of these species may never have been numerous because of the generally low productivity of tropical oceans. Because of their small population size, monk seals are vulnerable to die-offs resulting from disease, inbreeding and low genetic variability, and human disturbance. Of the three recent species, the Hawaiian and Mediterranean monk seals are endangered, and the Caribbean monk seal is considered extinct (Kenyon 1977). Although overall numbers are currently stable, some Hawaiian monk seal colonies are increasing while others are in decline. Reasons for the declines include human disturbance, habitat loss, disease, competition with fisheries, shark predation, intraspecific aggression, and entanglement with fisheries gear. Mediterranean monk seals are presently estimated at 250 to 500 individuals. The largest known aggregation of this species, which occurs at the peninsula of Cape Blanc in the Western Sahara, suffered a mass mortality event of unknown origin in 1997 that reduced its numbers from 317 to 109 individuals (Forcada et al. 1999). A hitherto unknown colony was recently discovered in the Cilician Bay off Turkey (Gucu et al. 2004). SOUTHERN HEMISPHERE SPECIES Like the northern elephant seal, the once-abundant southern elephant seal was heavily exploited during the eighteenth and nineteenth centuries. Populations were severely reduced at all major breeding sites. Although controlled harvests were reinstituted early in the twentieth century, southern elephant seal populations increased in most areas. The current world population is estimated at 640,000 individuals, with major breeding colonies located on South Georgia (113,000 pups per year), the Kerguelen Archipelago (43,000 pups per year), Macquarie Island (19,000 pups per year), Heard Island (17,000 pups per year), and Peninsula Valdes (14,500 pups per year). Paradoxically, despite their recovery following commercial sealing and a lack of subsequent hunting pressure, southern elephant seal populations in the Pacific and Indian oceans declined remarkably (50% to 80%) between the 1950s and 1990s (McMahon et al. 2003). The proximate causes of theses decreases are poorly understood. Some authors have attributed them to long-term environmental change leading to resource limitation (Burton et al. 1997; McMahon et al. 2003), whereas others have proposed the cause to be increased killer whale predation (Barrat and Mougin 1978; Guinet et al. 1992; Branch and Williams, Chapter 20 of this volume). The remaining southern hemisphere phocids (Weddell, Ross, crabeater, and leopard seals) are restricted to the Antarctic continent and its surrounding pack ice. Although these species have been harvested irregularly in past years, they were never so extensively depleted as pinnipeds elsewhere in the world. Current harvest levels are regulated under the 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 estimates are 220,000 to 440,000 for leopard seals; 500,000 to 1 million for Weddell seals; 10 to 15 million for crabeater seals; and 100,000 to 650,000 for Ross seals. Given the absence of historical estimates and the large uncertainties associated with modern-day population estimates, it is not possible to ascertain current population trends for any of WHALING EFFECTS ON PINNIPED POPULATIONS 347

7 AUQ1 AUQ2 the Antarctic phocids. Nonetheless, the relatively small number of animals harvested (ca. 39,000 since 1892) over a wide geographical range is unlikely to have adversely affected populations of any of these species; thus, changes in distribution and abundance are likely due to other factors. Testa et al. (1991) documented cyclic patterns in the age structure and cohort strength of crabeater, Weddell, and leopard seals related to the Southern Oscillation Index (SOI). Furthermore, Bengtson and Laws (1985) and Ballance et al. (Chapter 17 of this volume) suggested that a reported decline in the age of first reproduction of crabeater seals was caused by an increased availability of krill, which ostensibly resulted from the depletion of baleen whales. The age of first reproduction increased again between 1963 through 1976, a presumed physiological response to reduced prey availability. Otariid Population Trends Like temperate-latitude phocids, most otariid species were nearly extirpated by overharvesting by the end of the nineteenth century. With the cessation of harvest, most stocks recovered to varying degrees. Overall, fur seal populations appear to have recovered more rapidly than sea lion populations. Fur seals also outnumber sea lions by an order of magnitude (nearly 8 million fur seals worldwide, in contrast to just over 600,000 sea lions). Variation in diet, foraging strategies, and regional productivity may explain the differences in abundance and recovery rates between the two groups. Antarctic fur seals were thought to be extinct until a remnant population of 1,000 to 1,200 animals was discovered at Bouvetøya in 1928 (Fevoden and Sømme 1976), and another 100 animals were discovered off Bird Island in the 1930s (Laws 1973). Since that time the Antarctic fur seal population has grown at about 10% yr 1, to a 1990 estimate of 1.6 million animals (Boyd 1993). Although Antarctic fur seals have increased throughout their range, Boveng et al. (1998) suggested that the slower recovery rate on the South Shetland Islands is a result of leopard seal predation. Northern fur seals inhabit the North Pacific Ocean and the Bering Sea, with primary breeding rookeries on the Pribilof and Commander Islands and smaller colonies in the Sea of Okhotsk and Kurile Islands. An outlying colony also occurs on San Miguel Island off the coast of southern California. Following the overharvest and depletion of Northern fur seals during the eighteenth and nineteenth centuries, they were protected in 1911 and recovered significantly during the first half of the twentieth century, However, in contrast with Antarctic fur seals, northern fur seal numbers began to decline again in the 1950s, a trend that has continued to the present day (Angliss and Lodge 2004; Carretta et al. 2002). The cause of this ongoing decline is unknown. The closely related Cape and Australian fur seals were both greatly depleted by commercial sealing. However, their populations have since taken rather different trajectories. Cape fur seal populations, while subjected to controlled hunts, have increased to an estimated 1.7 million individuals and are growing at 3% per year (Butterworth et al. 1995). In contrast, Australian fur seal populations, which have not been hunted since 1923, have increased only to an estimated 60,000 individuals, well below the presealing estimate of 175,000 to 225,000 individuals. These different population growth rates and abundances have been attributed to variation in food availability and differing foraging strategies (Arnould and Warneke 2002). Other fur seal populations were also nearly hunted to extinction during the commercial sealing era but have similarly rebounded. The sub-antarctic fur seal, which breeds just north of the Antarctic polar front on sub-antarctic and subtemperate islands, numbers more than 235,000 to 285,000 individuals and is increasing by as much as 9% to 14% yr 1 in a few colonies (Wickens and York 1997). The South American fur seal, which occurs along the Pacific coast of South America, in the islands west of Tierra del Fuego, in the Falkland Islands, and in Uruguay and along the southern coast of Brazil, was hunted during the sealing era and, more recently, in regular small, controlled harvests in Uruguay until the 1990s. While numbers of South American fur seals are increasing, they remain diminished, apparently due to the recent commercial harvest. The New Zealand fur seal, an estimated 135,000 animals, is protected and increasing throughout its range in New Zealand and Australia (Wickens and York 1997). The Guadalupe fur seal, now the rarest of all fur seal species (about 7,000 individuals), was presumed extinct until a small breeding group was discovered at Isla de Guadalupe in 1928 (Townsend 1928). This small colony was then nearly exterminated by museum collectors (Bartholomew 1950; Hubbs 1956). The population bottleneck resulted in a substantial loss of genetic variability (Weber et al. 2004). The Galápagos fur seal, which is limited to the Galápagos Islands and was greatly depleted during the sealing era, recovered to its estimated presealing population level of about 40,000 animals by However, population size in this species fluctuates considerably in response to El Niño events (Trillmich et al. 1991). For example, 90% pup mortality and 45% overall mortality reduced the population to an estimated 6,000 8,000 animals following the El Niño event (Salazar 2002). The Juan Fernandez fur seal, which is confined to the islands off the coast of Chile, contained an estimated four million animals before the sealing era. This species, thought to be extinct until a small population was rediscovered in 1966, is currently estimated at approximately 18,000 animals and growing (Wickens and York 1997). In contrast to the fur seals, most sea lion populations are in decline, and one species (the Japanese sea lion) is probably extinct. Galápagos sea lions have continued to decline from anthropogenic impacts, El Niño events, and disease outbreaks, with a most recent count in 2002 of between 14,000 and 16,000 animals (Salazar 2002). The New Zealand (or Hooker s) sea lion, which once occurred all around New Zealand, was 348 CASE STUDIES

8 depleted by subsistence and commercial hunting. Presently, its breeding range is restricted to a few sub-antarctic islands (Gales and Fletcher 1999). Australian sea lions also were depleted by sealing, even though the larger populations of sympatric fur seals were the primary targets. This species is now one of the world s rarest and most unusual sea lions, on account of its 17.5-month breeding cycle (Higgins 1993), in contrast to the 12-month cycle typical of this group. Populations of both New Zealand and Australian sea lions, while far below their estimated pre-exploitation levels of about 13,000 and 10,000 (Gales et al. 1994; P. D. Shaughnessy et al., in review) respectively, are presently stable. However, unlike the New Zealand sea lion, the Australian sea lion is widely distributed among 67 scattered colonies in southern and Western Australia. The South American sea lion, which ranges from Brazil to Peru, was decimated in the hunt for oil. Today s populations stand at approximately 20% of their historical numbers (Cappozzo 2002). Although populations along the Pacific coast of South America are poorly known, many animals apparently abandon this region during severe El Niño events. Thompson et al. (2005) reported population declines in the Falkland Islands to <1.5% of the 1937 abundance estimate between 1965 and 1990, for reasons that remain unclear. Pup production in the Falklands since 1990 has increased at 3.8% to 8.5% per year, thus putting this population on a similar growth trajectory to the adjacent Argentinean population. The northern or Steller sea lion (SSL), which ranges from California to Japan, was hunted for various reasons until the early 1970s. There is still a small subsistence take by Alaska natives. Two stocks are currently recognized in U.S. waters, with Cape Suckling, Alaska (144 W) the demarcation point between the eastern and western stocks. Despite the cessation of hunting and protection from other disturbances, the western stock began a precipitous decline in the late 1970s or early 1980s (Loughlin et al. 1992; NRC 2003). The western stock is currently listed as Endangered and the eastern stock as Threatened under the U.S. Endangered Species Act. The known or suspected causes of SSL mortality include incidental losses in fisheries gear, entanglement in marine debris, shooting, competition with fisheries for food, ocean climate change, and predation by killer whales. SSL and their associated ecosystem have been the objects of intensive research, yet there is still no widely accepted explanation for sea lions recent decline (NRC 2003). The California sea lion, which ranges from Mexico to British Columbia, is the most abundant of all sea lion species. Culling, largely because of perceived damage to commercial catches and competition for salmonid fishery resources (Everitt and Beach 1982), reduced the abundance of California sea lions in southern California and Mexico to approximately 1,500 individuals by the 1920s. The species has increased steadily at 5% to 6.2% yr 1 through the latter part of the twentieth century (NMFS 1997). Presently, there are an estimated 204,000 to 214,000 California sea lions in U.S. waters (Carretta et al. 2002), and an additional 44,000 to 53,000 animals in Mexico (Aurioles-Gamboa and Zavala-Gonzalez 1994). Potential Causes of Population Declines In the preceding sections of this chapter we have provided a broad overview of the population status and trends of pinnipeds worldwide. Most species were reduced substantially during the era of commercial sealing. The explanation for these early declines is clear and certain humans killed them. However, populations have not all responded to the cessation of commercial sealing in the same way. Some species or local populations increased, often rapidly. Here again there is little mystery as to why reduced mortality, together with resource surpluses created by the earlier population reduction, probably fueled population growth in a manner expected from simple demographic and ecological theory. However, other species and populations either did not recover from sealing or did recover but have subsequently again declined. These latter cases are more difficult to understand. In the final sections of this chapter we attempt to shed light on these perplexing trends by mapping known or suspected patterns of variation in life history, behavior, and environment with reported population trajectories. Our synthesis focuses on three key patterns and processes: differing reproductive strategies between phocids and otariids; physiological limitations associated with particular foraging and diving behavior; and the resulting susceptibility to disturbance in prey resources and predation. Life History and Behavioral Correlates Phocids and otariids have solved the conflicting demands of terrestrial parturition and marine feeding in different ways (Bartholomew 1970; Costa 1993). Most phocids are capital breeders, storing, prior to parturition, sufficient energy for the entire lactation period. Otariids, in contrast, are income breeders, feeding more or less continuously during lactation (Costa 1991a,b, 1993; Boyd 2000). These different strategies confer differing benefits and costs to phocids and otariids. Capital breeding disassociates reproductive success from local food availability. The nutritional provisioning of pups by phocid mothers is thus largely unconstrained by traveling time to and from the foraging grounds, thereby allowing them to utilize prey that are more dispersed, patchy, unpredictable, or distant from the rookery. The necessity of feeding during lactation constrains otariid females to forage closer to the rookery, thus linking reproductive success and local prey abundance (Costa 1993) and thereby potentially connecting population status to localized environmental changes such as El Niño/Southern Oscillation events (Trillmich et al. 1991; see Figure 27.4 for the California sea lion). Significant alterations in trip duration, female condition, fecundity, pup growth rate, and survival in response to reductions in prey availability caused by changing oceanographic conditions are common in otariids (Costa et al. 1989, AUQ3 WHALING EFFECTS ON PINNIPED POPULATIONS 349

9 FIGURE 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 and Murray 2001). On the other hand, fasting or reduced feeding during lactation limits the total amount of energy and protein that can be invested in phocid young, resulting in a smaller relative pup mass at nutritional independence. Phocid weaning mass reflects the mother s foraging success over the previous year; postweaning survival is related to both weaning mass (energy reserves provided by the mother) and postweaning resource availability (Stewart and Lavigne 1984). Furthermore, weaning in phocids is abrupt, thus preventing pups from learning from their mothers how to forage a potential disadvantage in times of food shortage. Weaning is often synchronous within species, which means large numbers of inexperienced individuals will be simultaneously testing the waters near breeding colonies, thus making them susceptible to predation. The typically short breeding period in phocids also allows them to utilize unstable breeding substrates, such as pack ice (Stirling 1975, 1983; Costa 1993). Implications of the aforementioned differences in reproduction and foraging between phocids and otariids are potentially exemplified by the striking differences in recovery rates of fur seals, elephant seals, and sea lions on Guadalupe Island, Mexico. While fur seals and elephant seals both increased following the cessation of hunting, the elephant seal recovery has been far more dramatic (Figure 27.5). During this same period, sea lion numbers at Guadalupe Island have remained low but relatively stable, whereas populations elsewhere have increased rapidly. As income breeders, California sea lions and Guadalupe fur seals must remain with their pups for almost a year, thus constraining them to feed near Guadalupe Island. As a capital breeder, the northern elephant seal can forage almost anywhere in the North Pacific Ocean (Stewart and DeLong 1993; LeBoeuf et al. 2000), thus providing this species with greater access to prey resources. Variation in dive behavior can also influence foraging efficiency and, thus, the potential for prey limitation in population regulation. That is, pinnipeds that operate at or near their physiological limits should have little capacity to adjust foraging effort in response to food availability, whereas those that operate below their physiological limits should not be so constrained. Thus, one would expect stronger covariation between population trends and food availability for species in the former than in the latter group (Costa et al. 2001; Costa and Gales 2003; Costa et al. 2004). This proposed relationship should be particularly evident between benthic and water column foragers, because benthic foragers may be working at levels closer to their maximum physiological diving capacity. Benthic foraging requires longer transit times, thus reducing the time beneath the surface that is available to search for prey (Costa and Williams 1999). Because adults of benthic foraging species are working at or near their physiological limit, the smaller juveniles, with their reduced physiological capabilities and oxygen stores, should be particularly vulnerable to resource limitation. Survival of juveniles in benthic foraging species might thus be a major determinant of demographic trends. Furthermore, benthic foraging species might be particularly sensitive to bottom trawlers, which disrupt the habitat and remove the larger size-classes of fishes upon which they often depend (Thrush et al. 1998). On the other hand, the benthos may be a more predictable source of prey than the water column, and thus benthic foraging species may be less 350 CASE STUDIES

10 AUQ5 FIGURE Population trends from the three species of pinniped that are found on Guadalupe Island, Mexico: California sea lion, Guadalupe fur seal, and Northern elephant seal (data from Pablo-Gallo, unpublished). affected by oceanographic perturbations such as El Niños than water column feeders (Miller and Sydeman 2004). Observed relationships between aerobic dive limit (ADL), which is a measure of physiological dive capability, and foraging behavior across five otariid species (Antarctic and Australian fur seals; Australian, California, and New Zealand sea lions) provides an initial test of these predictions (Costa et al. 2004). The Antarctic fur seal makes short, shallow dives, while the Australian and New Zealand sea lions and the Australian fur seal make deep prolonged dives to the benthos (Boyd et al. 1991; Costa and Gales 2000, 2003). California sea lions are especially interesting because they (at least the females and juveniles) dive epipelagically off the coast of southern California (Feldkamp et al. 1989), whereas they forage much deeper on mesopelagic prey in the Sea of Cortez (C. E. Kuhn, D. Aurioles-Gamboa, and D. P. Costa, unpublished). The near-surface-feeding Antarctic fur seal and California sea lion in southern California forage well within their calcu-lated ADL (cadl), whereas the three benthically foraging species/populations routinely exceed their cadl (Figure 27.6). For both fur seals and sea lions, the benthic foragers spend >40% of their time at sea diving, whereas the epipelagic foragers spend <30% of their time at sea diving (Figure 27.7). These findings may explain why populations of many fur seal species (and the pelagic foraging California sea lion) have increased whereas most sea lions (many of which occupy the same area as near-surface-feeding fur seal species; Costa and Gales 2003) have remained stable or declined (Boyd et al. 1995; Sydeman and Allen 1999; Gales and Fletcher 1999; Gales et al. 1994). Risk of Predation Pinnipeds are preyed on by a variety of species, including other pinnipeds, humans, polar bears, wolves, foxes, coyotes, hyenas and jackals, eagles, sharks, and killer whales (Weller 2002). In the northern hemisphere, land- or ice-based predators (people, bears, foxes) are particularly important, whereas in the southern hemisphere, ice seals are free from terrestrial predators but are subjected to several aquatic predators. The clearly divergent predator avoidance tactics between Arctic and Antarctic pinnipeds, with Arctic species fleeing into the water to escape predation and Antarctic species seeking refuge on the ice (Stirling 1975, 1983; Weller 2002), attest to the strength and importance of these predatorprey interactions. Killer whales (Orcinus orca) are probably the most important aquatic predator of marine mammals. Harbor seals are the most commonly reported prey of killer whales in the northern hemisphere (Jefferson et al. 1991). However, killer whales are also known to prey on many other species of pinnipeds, including the crabeater seal (Smith et al. 1981), southern sea lion and southern elephant seal (López and López 1985; Guinet et al. 2000), northern fur seal (M. Goebel, personal communication), and California sea lion. In some areas, killer whales intentionally strand themselves in order to seize pinniped prey, such as southern sea lions and southern elephant seals, on the beach (López and López 1985). Although predator control of pinniped populations is difficult to verify, several studies either demonstrate or suggest significant population level impacts of predation. Harbor seal pup production at Sable Island declined from 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 The increasing grey seal population may have indirectly influenced harbor seals by attracting sharks to the region and competing with harbor seals for prey (Bowen et al. 2003). WHALING EFFECTS ON PINNIPED POPULATIONS 351

11 FIGURE 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 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

12 AUQ4 Springer et al. (2003) recently speculated that killer whale predation was principally responsible for widespread population declines of sea otters and pinnipeds in southwest Alaska. Their argument was based largely on feasibility analyses from demographic and energetic modeling (Williams et al. 2004), strong evidence that killer whale predation caused the sea otter decline (Estes et al. 1998), and various inconsistencies in the available information with other purported explanations for the declines (NRC 2003). Branch and Williams (Chapter 20 of this volume), on the basis of similar evidence and analyses, have concluded that killer whale predation might also have figured prominently in the decline of various Southern Ocean pinniped populations. In support of this latter suggestion, killer whales were observed taking up to 25% of the southern elephant seal weanlings from one beach at Crozet Island and have been implicated in the decline of that population (Guinet 1992; Guinet et al. 1992). Pinnipeds also prey on one another. A single Hooker s sea lion on Macquarie Island killed 43% of the 130 Antarctic and sub-antarctic fur seal pups born over a two year period (Robinson et al. 1999). Similarly, leopard seals killed an estimated 34% of the Antarctic fur seal pup production at Seal Island (Boveng et al. 1998). In Punta San Juan, Peru, up to 8.3% of South American fur seal pups are reportedly killed by Southern sea lions (Harcourt 1992). Northern fur seal pups are killed and eaten by adult male Steller sea lions (Gentry and Johnson 1981). Summary In this chapter we have reviewed the current status and trends of pinniped populations worldwide, with a focus on the anthropogenic and natural biological processes that might be responsible for these trends. Although little or no data are available for some species, useful time series exist for many others. Increasing populations include most of the southern hemisphere fur seals, the California sea lion, harbor seal populations off the west coast of the United States, and the northern elephant seal. Populations in decline include northern and southern sea lions, the northern fur seal, the southern elephant seal in parts of the Southern Ocean, and the harbor seal in southwest Alaska. The tropical monk seals are either stable at low levels or in decline. Population trends for polar species are poorly known, although by and large these species appear to be both abundant and fairly stable. Recovery failures or recent population declines are most commonly attributed to interactions with fisheries and environmental change. Pinniped interactions with fisheries include both operational and ecological effects (Harvey 1987; Mate and Harvey 1987). Ecological effects largely result from direct competition, thus ostensibly reducing both potential fishery yields and the environmental carrying capacity for pinnipeds. Operational effects occur when pinnipeds and fishery operations come into direct contact. For example, pinnipeds can be incidentally entangled and damage fishing gear and remove or damage fish caught in nets or on fishing lines. A currently expanding and largely unregulated trade in seal products (Reeves 2002), poor or misguided population management, and continued overexploitation of some populations are contributing factors. For example, although commercial sealing has declined considerably since the 1960s, native hunters kill more than 100,000 ringed, bearded, ribbon, harp, hooded, and spotted seals annually (Reeves 2002). In addition, after a reduction in takes of harp seals in the 1980s, government subsidies have reinvigorated the Canadian commercial hunt, with approximately 350,000 harp seals being taken in eastern Canada and Greenland in 1998 (Lavigne 1999). Norwegian and Russian ships also take tens of thousands of harp and hooded seals annually in the Greenland and Barents seas. In the southern hemisphere, South American fur seals were harvested in Uruguay until the 1990s. and the centuries-old hunt of Cape fur seals in southwestern Africa continues to take thousands of fur seals annually. Pinniped populations also have suffered adverse impacts by human modifications of coastal and marine environments, thus resulting in disturbance, loss of breeding and resting sites, and alteration of foraging grounds (Reeves 2002). Exposure to various pollutants is a problem in some areas, and disease outbreaks are often related to immune-response suppression caused by a variety of pollutants (Reijnders and Aguilar 2002). In addition to environmental forcing, pinniped population trends are influenced by variation in life history, behavior, and physiological capacity. Capital breeders or species that have life history patterns that allow them to forage across ocean basins have a greater capability of recovery from exploitation, whereas income breeders are more sensitive to local oceanographic variations and associated limitations in prey resources may recover more slowly. Similarly, differences in the foraging strategy of otariids may also be a factor in their ability to respond to environmental fluctuations. Benthic diving otariids (e.g., Steller, Australian, southern, and New Zealand sea lions) have a lower reproductive output than epipelagic species because they spend more time at sea diving and they push their physiological limits. This is further compounded by a potential for reduced juvenile survival in benthic foraging species because of the reduced diving capability of juveniles. Differences in the foraging strategies and reproductive patterns also may make certain pinnipeds more susceptible than others to predation. With both reproductive strategies the young are exposed to predation, but adult female otariids will be more susceptible to increased predation because income breeders must make multiple visits to and from the rookery. Although our review provides an overview of pinniped population trends worldwide and a synthetic effort to understand reasons for recent population declines and the failure of various other populations to even recover from overexploitation, in truth these patterns are poorly understood. Although capital breeding would seem to convey an advantage to phocids over otariids, it cannot explain why both WHALING EFFECTS ON PINNIPED POPULATIONS 353

13 harbor seals and Steller sea lions have declined at the same rate and magnitude over largely the same regions of southwest Alaska or why northern elephant seals have recovered so spectacularly whereas many southern elephant seal populations have collapsed. Similarly, although diving behavior and physiological limitation would seem to convey a relative disadvantage to benthic foraging over epipelagic foraging otariids, this explanation alone cannot account for the spectacular population collapse of the benthically foraging Steller sea lion. On the other hand, although there is compelling evidence that predators have driven the declines of small isolated pinniped colonies and there have been arguments for the importance of killer whale predation in the large scale population declines of seals, sea lions, and otters of the North Pacific, conclusive evidence is lacking. Given the extremely dynamic nature of pinniped populations and the high degree of uncertainty over ultimate causes of pinniped population irruptions and declines, it is not unreasonable to imagine that these dynamics were influenced at least to some degree by the effects of whaling on ocean ecosystems. As Croll et al. (Chapter 16 of this volume) point out, the great whales co-opted a significant proportion of the world s marine production before whaling, and if Roman and Palumbi s (2003) prewhaling abundance estimates are even close to being accurate, the magnitude of this effect would have been even greater. In a simplistic sense, less production being co-opted by whales means potentially more for other ocean consumers. Such effects have been proposed in the southern ocean, where the removal of krill-eating whales ostensibly led to increases in other krill consumers, including some of the pinnipeds (Ballance et al., Chapter 17 of this volume). However, as Paine (Chapter 2 of this volume) points out, food web dynamics are rarely so simple. Although complex food web dynamics of this sort are poorly known for ocean ecosystems, the very fact that pinniped population dynamics fit so poorly into traditional explanatory molds raises the distinct possibility that the ecological influences of whaling are associated with some of this uncertainty. Literature Cited Angliss, R.P. and K.L. Lodge Alaska marine mammal stock assessments, U.S. Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-133. Seattle: Alaska Fisheries Science Center. Arnould, J.P.Y., and R.M. Warneke Growth and condition in Australian fur seals (Arctocepha pusillus doriferus) (Carnivora: Pinnipedia). Australian Journal of Zoology 50: Aurioles-Gamboa, D. and A. Zavala-Gonzalez Ecological factors that determine distribution and abundance of the California sea lion Zalophus californianus in the Gulf of California. Ciencias Marinas 20: Barrat, A. and J.L. Mougin The Southern elephant seal, Mirounga leonina, of Possession Island, Crozet Archipelago, south, east. Mammalia 42: (in French). Bartholomew, G.A A male GFS on San Nicolas Island, California. Journal of Mammalogy 31: A model for the evolution of pinniped polygyny. Evolution 24: Bengtson, J.L. and R.M. Laws Trends in crabeater seal age Lobodon carcinophagus at sexual maturity: an insight into Antarctic marine interactions, in Antarctic nutrient cycles and food webs. W.R. Siegfried, P.R. Condy, and R.M. Laws, eds. Berlin: Springer-Verlag, pp Boveng, P.L., L.M. Hiruki, M.K. Schwartz, and J.L. Bengtson Population growth of Antarctic fur seals: limitation by a top predator, the leopard seal? Ecology 79: Bowen, W.D Role of marine mammals in aquatic ecosystems. Marine Ecology Progress Series 158: Bowen, W.D., S.L. Ellis, S.J. Iverson, and D.J. Boness Maternal and newborn life-history traits during periods of contrasting population trends: Implications for explaining the decline of harbour seals (Phoca vitulina), on Sable Island. Journal of Zoology 261: Boyd, I.L Pup production and distribution of breeding Antarctic fur seals (Arctocephalus gazella) at South Georgia. Antarctic Science 5(1): State-dependent fertility in pinnipeds: contrasting capital and income breeders. Functional Ecology 14: Boyd, I.L., J.P.Y. Arnould, T. Barton, and J.P. Croxall Foraging behaviour of Antarctic fur seals during periods of contrasting prey abundance. Journal of Animal Ecology 63: Boyd, I.L., J.P. Croxall, N.J. Lunn, and K. Reid Population demography of Antarctic fur seals: the costs of reproduction and implications for life-histories. Journal of Animal Ecology 64: Boyd, I.L., N.J. Lunn, and T. Barton Time budgets and foraging characteristics of lactating Antarctic fur seals. Journal of Animal Ecology 60: Boyd, I.L. and A.W.A. Murray Monitoring a marine ecosystem using responses of upper trophic level predators. Journal of Animal Ecology 70: Boyd, I.L., T.R. Walker, and J. Poncet Status of southern elephant seals at South Georgia. Antarctic Science 8: Burns, J.J Marine mammal report. Pittman-Robertson Project Report W-17-3, W-17-4, and W Juneau: Alaska Department of Fish and Game. Burton, H.R., T. Arnbom, I.L. Boyd, M. Bester, D. Vergani, and I. Wilkinson Significant differences in weaning mass of southern elephant seals from five sub-antarctic islands in relation to population declines, in Antarctic communities: species, structure and survival. D.W.H. Walton, ed. Cambridge, UK: Cambridge University Press, pp Butterworth, D.S., A.E. Punt, W.H. Oosthuizen, and P.A. Wickens The effects of future consumption by the Cape fur seal on catches and catch rates of the Cape hakes. 3. Modelling the dynamics of the Cape fur seal Arctocephalus pusillus pusillus. South African Journal of Marine Science 16: Cappozzo, H.L South American sea lion, in Encyclopedia of marine mammals. W.F. Perrin, B. Würsig, and J.G.M. Thewissen, eds. San Diego: Academic Press, pp Carretta, J.V., J. Barlow, K.A. Forney, M.M. Muto, and J. Baker U.S. Pacific marine mammal stock assessments: NOAA Technical Memorandum NMFS-SWFSC-317. La Jolla, CA: Southwest Fisheries Science Center. Carretta, J.V., M.M. Muto, J. Barlow, J. Baker, K.A. Forney, and M. Lowry U.S. Pacific marine mammal stock assessments: 354 CASE STUDIES