Download Potential Influences of Whaling on the Status and Trends of

T W E N T Y- S E V E N
Potential Influences of Whaling on the Status and
Trends of Pinniped Populations
DAN I E L P. C O STA, M I C HAE L J. W E I S E, AN D J O H N P. Y. AR N O U LD
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
342
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
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 subAntarctic 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 S P EC I E S
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 1971. 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
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
343
TA B L E 27.1
Pinniped Population Numbers and Trends Worldwide
Common Name
Species
Population Size
Trend
Northern Hemisphere
Eared Seals
Guadalupe fur seal (GFS)
California sea lion (CSL)
Northern fur seal (NFS)
Steller sea lion (SSL)
Galápagos sea lion (GSL)
Galápagos fur seal (GAFS)
Japanese sea lion
Walruses
Pacific walrus
Atlantic walrus
Earless Seals
Hooded seal (HOS)
Gray seal (GS)
Ribbon seal (RIS)
Northern elephant seal (NES)
Harp seal (HAS)
Western Atlantic harbor seal (HS)
Western Pacific harbor seal (HS)
Mediterranean monk seal (MMS)
Hawaiian monk seal (HMS)
Ungava harbor seal (HS)
Caspian seal (CS)
Baikal seal (BS)
Eastern Atlantic harbor seal (HS)
Bearded seal (BS)
Eastern Pacific harbor seal (HS)
Spotted (Largha) seal (SS)
Ringed seal (RS)
Baltic seal (RS)
Ladoga seal (RS)
Sea of Okhotsk ringed seal (RS)
Saimaa seal (RS)
Caribbean monk seal
Otariidae
Arctocephalus townsendi
Zalophus californianus
Callorhinus ursinus
Eumatopias jubatus
Zalophus wollebaeki
Arctocephalus galapagoensis
Zalophus japonicus
7,000
237,000–244,000
1,400,000
<75,000
5,000
12,000
Extinct
Increasing
Increasing
Decreasing
Decreasinga
Fluctuating
Fluctuating
Extinct
Odobenidae
Odobenus rosmarus divergens
Odobenus rosmarus rosmarus
200,000
>14,000
Decreasing
Unknown
>400,000
Unknown
490,000
101,000
7,486,000
40,000–100,0000
146,900
250–500
1,400
120–600
<100,000
5,000–6,000
98,000
100,000s
7,300
335,000–450,000
2,500,000
5,000
5,000
800,000–1,000,000
2,000–5,000
Extinct
Increasing
Increasing
Increasing
Increasing
Increasing
Increasing
Stable
Decreasing
Decreasing
Decreasing
Decreasing
Decreasing
Fluctuating
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Extinct
Phocidae
Cystophora cristata
Halichoerus grypus
Histriophoca fasciata
Mirounga angustirostris
Pagophilus groenlandicus
Phoca vitulina concolor
Phoca vitulina richardsi
Monachus monachus
Monachus schauinslandi
Phoca vitulina mellonae
Phoca caspica
Phoca sibirica
Phoca vitulina vitulina
Erignathus barbatus
Phoca vitulina stejnegeri
Phoca largha
Pusa hispida hispida
Pusa hispida botnica
Pusa hispida ladogensis
Pusa hispida ochotensis
Pusa hispida saimensis
Monachus tropicalis
Southern Hemisphere
Eared Seals
South American fur seal (SAFS)
New Zealand fur seal (NZFS)
Juan Fernandez fur seal (JFS)
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CASE STUDIES
Otariidae
Arctocephalus australis
Arctocephalus forsteri
Arctocephalus philippii
235,000–285,000
135,000
18,000
Increasing
Increasing
Increasing
TA B L E 27.1 ( C O N T I N U E D )
Pinniped Population Numbers and Trends Worldwide
Common Name
Species
Population Size
Trend
Southern Hemisphere
Eared Seals
Otariidae
Australian fur seal (AFS)
Cape fur seal (CFS)
Subantarctic fur seal (SFS)
Antarctic fur seal (ANFS)
Australian sea lion (ASL)
New Zealand sea lion (NZSL)
South American sea lion (SASL)
Earless Seals
60,000
1,700,000
>310,000
1,600,000
9,300–11,700
13,000
275,000
Increasing
Increasing
Increasing
Increasing
Stable
Stable
Decreasing
Phocidae
Leopard seal (LS)
Weddell seal (WS)
Crabeater seal (CE)
Southern elephant seal (SES)
Ross seal (ROS)
aStock
Arctocephalus pusillus doriferus
Arctocephalus pusillus pusillus
Arctocephalus tropicalis
Arctocephalus gazella
Neophoca cinerea
Phocarctos hookeri
Otaria flavenscens
Hydruga leptonyx
Leptonychotes weddelli
Lobodon carcinophagus
Mirounga leonina
Ommatophoca rossi
220,000–440,000
500,000–1,000,000
10,000,000–15,000,000
640,000
100,000–650,000
Stable
Stable
Stable
Stable/decreasing
Unknown
specific
F I G U R E 27.1.
Present day distribution of Otariidae species. See Table 27.1 for species codes.
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
345
F I G U R E 27.2.
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
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CASE STUDIES
currently. Mass mortalities from morbillivirus (Likhoshway
et al. 1989) occurred in 1987–1988 and in 1998.
TE M P E RATE AN D TROP ICAL S P ECI E S
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
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).
F I G U R E 27.3.
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).
SOUTH E R N H E M I S P H E R E S P E C I E S
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
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
347
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
AUQ1 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
AUQ2
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,
348
CASE STUDIES
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 1977–1978. 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 1997–1998
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
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,
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
349
AUQ3
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.
F I G U R E 27.4.
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
350
CASE STUDIES
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
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).
F I G U R E 27.5.
AUQ5
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 1996. 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).
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
351
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.
F I G U R E 27.6.
F I G U R E 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
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
W H A L I N G E F F E C T S O N P I N N I P E D P O P U L AT I O N S
353
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.
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[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,
Yes this is correct
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.
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