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The once common belief that populations steadily rise to a stable equilibrium, or carrying capacity, and then remain at a more or less constant size, has been challenged repeatedly. Andrewartha & Birch (1954) showed that stochastic events can depress populations such that they never attain a stable equilibrium. Their examples dealt mainly with insects, whose populations tend to be especially variable, and some of their cases may have represented anomalies rather than generalities; gradually their ideas fell into disfavour. More recently, the concept that populations may be periodically and significantly perturbed has re-emerged (Sousa 1984), prompting greater consideration of such events in population dynamics (Lewin 1983; Mangel & Tier 1993, 1994; Brook & Kikkawa 1998; Root 1998). Evidence of sudden, severe (i.e. catastrophic) change is now available for many invertebrates (Dungan, Miller & Thomson 1982; Lessios, Robertson & Cubit 1984; Fiori & Cazzaniga 1999), small vertebrates (Blaustein, Wake & Sousa 1994; Valone, Brown & Jacobi 1995; Everson et al. 1999), large mammals (Young 1994) and even whole ecosystems (Botkin 1990; Lockwood & Lockwood 1993; Hughes 1994). Examples of natural environmental disturbances that can severely disrupt animal populations include fires (Singer et al. 1989), volcanic eruptions (Franklin et al. 1985), storms (Spiller, Losos & Schoener 1998) and the El Niño Southern Oscillation (Bodkin & Jameson 1991; Pounds & Crump 1994; Wright et al. 1999). While often calamitous, these events provide opportunities to investigate the dynamics of natural systems.
Our study examined the demographic consequences of a major oil spill on a population of sea otters Enhydra lutris L., a species known to be especially sensitive to contamination of its pelage (Geraci & Williams 1990). The spill occurred in March 1989, when, after filling with Prudhoe Bay crude oil, the tanker Exxon Valdez ran aground in Valdez Arm, Prince William Sound (PWS), Alaska, USA (Fig. 1). Approximately 41 million litres of oil leaked into the water, much of which floated southward and was washed ashore on islands in the western sound.
Figure 1. Study areas (shaded) in western Prince William Sound, Alaska, USA. Population dynamics in the sound varied by geographical area. We divided the sound into three regions, as shown: western (oiled), northern (un-oiled area with deep fjords), and eastern (un-oiled area with shallow bays and the best food supply).
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Sea otters became a target of media attention (Batten 1990) and litigation (Estes 1991) after the spill, as a conspicuously large number died or were debilitated by the oil. Our study focused on counts of live otters that remained. We hypothesized that their numbers would be significantly reduced and that recovery to pre-spill levels could be delayed by long-term depression of their reproduction or survival caused by the oiling of habitat and prey. Unexpectedly, in the 2 years following the spill, we counted as many or more otters in some of the most heavily oiled areas of PWS as were observed 5 years before the spill (Johnson & Garshelis 1995). These high counts seemed inconsistent with studies that estimated losses of > 2500 otters in PWS, or about 40% of the population (Garrott, Eberhardt & Burn 1993; DeGange, Doroff & Monson 1994), and warned of prolonged injurious effects (Ballachey, Bodkin & DeGange 1994).
In this paper we try to reconcile these contradictory assessments. We examined counts conducted since our previous report (Johnson & Garshelis 1995) plus new data on pup production, food habits and activity time budgets. We also reanalysed count data from another study whose conclusions differed markedly from our study. We attempted to resolve the discrepancies and unexpected results by teasing out potentially confounding factors.
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We believe there is strong evidence, both from our study and that of Burn (1994), to conclude that sea otter abundance in the oil-affected part of PWS was as high or higher during the 7-year period after the spill as it was during the early mid-1980s. This result is surprising.
Although Garshelis (1997) and Garshelis & Estes (1997) found that other investigators (Garrott, Eberhardt & Burn 1993; DeGange, Doroff & Monson 1994) probably overestimated sea otter mortality due to the spill, the loss was nonetheless substantial (probably 600–1000 otters). It would seem that a decline of this magnitude, constituting 15–25% of the resident population, should have been detectable from boat surveys. Previously we considered various hypotheses to explain the failure to detect this loss (Johnson & Garshelis 1995), the most probable being that spill-related mortality was masked by a population increase in the late 1980s, when no counts were made. At the time of our earlier report, the only support for this proposed late-1980s population growth was an increase in otter numbers at Montague Island, an un-oiled site in the western sound, and high pup production during 1991, which if characteristic of the period immediately preceding the spill could have spurred such an increase.
Subsequent data, presented here, indicated that high pup production (in both oiled and un-oiled areas) continued during 1993 and 1994, but returned to near pre-spill levels at four of our five survey sites in 1996 (Fig. 4). Significant year-to-year variation in sea otter pup production, as observed in the past (Johnson 1987; Johnson & Garshelis 1995), may be related to year-specific weather conditions. However, the number of exceedingly good years of pup production post-spill strongly suggests the presence of a more pervasive environmental factor that elevated the pupping baseline above what it was in the late 1970s and early 1980s. The relatively young age of first reproduction discovered among the reproductive tracts of otters killed during the spill (Bodkin, Mulcahy & Lensink 1993), compared with ages of primiparity observed earlier (Garshelis, Johnson & Garshelis 1984; Jameson & Johnson 1993), is evidence that pupping rates were increasing by the late 1980s.
We postulate that this heightened pup production was triggered by an enhanced food supply (Fig. 6). Although the diet in the early 1990s remained unchanged from that of the early 1980s, with clams being the dominant component (60–70%; Doroff & Bodkin 1994; Johnson & Garshelis 1995), our results indicate that otters obtained more and larger clams per dive during the early 1990s. Moreover, in 1991 these clams were obtained on shorter dives in shallower water than in the early 1980s, enabling otters potentially to make more foraging dives and hence obtain more food per unit time. Foraging success did not change between the early 1980s and the early 1990s, but foraging success tends to be related more to dietary composition than to food abundance (Estes, Jameson & Johnson 1981; Garshelis 1983; Doroff & DeGange 1994).
Our time budget data provide further evidence of more plentiful food during the 1990s. We observed less feeding during our daytime scan samples than had been observed using the same technique at the same observation sites during the late 1970s and early 1980s. The premise that time budgets of otters reflect food availability is well supported by other studies (Estes, Jameson & Rhode 1982; Garshelis, Garshelis & Kimker 1986; Gelatt 1996). Collectively, the time budget and foraging data are a compelling indication of an increased food supply in the area around Gibbon Anchorage, Green Island. Moreover, our observation that post-spill pup production was high throughout western PWS (Fig. 4) suggests that this increased food supply was not a local phenomenon.
The scenario that we propose is that, in response to an increasing food supply before the spill, pup production increased, resulting in a population increase. The rate of population increase probably varied with year-to-year changes in pup production, as witnessed during our study, as well as yearly variation in juvenile survival, as observed in two post-spill telemetry studies (Rotterman & Monnett 1991; B. Ballachey & A. Doroff, personal communication). We suspect that the population surged during years with good pup production and survival, but remained stationary or declined following poorer years. Thus, an overall increasing trend in otter numbers might not be obvious from a short series of counts. Additionally, in our study, incomplete data (missing years and partial surveys) probably obscured trends in otter abundance at each particular site (Fig. 2). However, the combined count for all surveyed sites (Table 1) and the trend data from Gibbon Anchorage, the only individual site with a large number of surveys (Fig. 3), provide persuasive evidence of an overall increasing population.
Research from the late 1970s and early 1980s led Johnson (1987) to conclude that otters around Green Island were at carrying capacity. We concur with this interpretation, and suggest that otters remained at carrying capacity through the late 1980s. This is not a contradiction to our belief that otter numbers were increasing. Populations at carrying capacity are not necessarily stationary; they can remain food-limited but track changes in food abundance. We suggest that food supplies were constant or even declining during the early 1980s, but then increased during the mid-1980s; consequently, otter numbers followed this same trajectory.
The cause of this increased size and abundance of otter prey is unknown, but we theorize that it may represent long-term recovery from the massive earthquake of 1964, which was centred in the northern part of the sound (near Unakwik Inlet; Fig. 1). This earthquake was the second largest ever measured (moment magnitude 9·2); the last seismic event of this magnitude in this area occurred at least 800 years ago (Plafker 1990). The 1964 earthquake uplifted the western sound, including Knight Island (1–2 m), Green Island (Gibbon Anchorage = 2·5 m) and Montague Island (Port Chalmers = 3 m), whereas the northern part of the sound, including Harriman Fiord, Barry Arm and Unakwik Inlet, subsided (0·6–2 m) (Baxter 1971; Hanna 1971). Significant immediate clam mortality occurred, averaging 30–40% in areas that rose 1·4 m (the average uplift for the sound) and > 80% in places like Gibbon Anchorage that rose more (Baxter 1971).
Prior to the earthquake, butter clams Saxidomus giganteus DeShayes were probably the most common prey of sea otters at Green Island. Butter clam shells, imbedded in uplifted sediments in the posture in which they died, are still evident in many places in the sound (D. L. Garshelis & C. B. Johnson, personal observations). Beds of these stranded shells indicate that at the time of the earthquake many dense patches of medium–large butter clams occurred at Green Island (Estes & VanBlaricom 1985). During the 1970s (Calkins 1978), 1980s (Johnson 1987; D. L. Garshelis, unpublished data) and early 1990s (Doroff & Bodkin 1994; this study), this species remained common in the diet of otters in the western sound; however, even though sea otters tend to select the largest available clams (Kvitek et al. 1992), the ones they obtained in Gibbon Anchorage in the 1980s and 1990s (Fig. 6) were smaller than the ‘earthquake fossil’ clams present there (haphazard sampling; mean = 8·0 cm, range = 6·6–9·0 cm, n = 35). Butter clams are the major food of sea otters in soft-bottom habitats in parts of Alaska that were further from the earthquake (Kvitek & Oliver 1992; Doroff & DeGange 1994); where otters have not yet had a major impact on this prey, shell sizes are equivalent (mean ≈ 8 cm) (Kvitek & Oliver 1992; Kvitek et al. 1992) to those that apparently were abundant at Green Island at the time of the earthquake.
Shells from the littleneck Protothaca staminea Conrad, another common (but smaller) clam consumed by sea otters, also occur in dense earthquake-stranded patches at Green Island (Estes & VanBlaricom 1985). Surveys made at a site in the eastern sound 10 years after the earthquake indicated that littleneck densities had recovered to only about 40% of what they had been before (Paul, Paul & Feder 1976).
Besides the enormous outright mortality of clams caused by the earthquake, habitat alteration negatively affected their recovery. The lower vertical distribution for species like S. giganteus and P. staminea is limited by a layer of soft decaying organic silty mud (possibly oxygen deficient), which reduces survival of larvae. When the sound was uplifted by the earthquake, the vertical zone that had been preferred clam habitat was exposed above water level, and the new preferred zone was covered by the silty mud, which impeded clam recruitment (Baxter 1971). Paul, Paul & Feder (1976) indicated that clam recruitment remained poor through 1971 in an area of the eastern sound that was uplifted by about 1 m. We know of no data on persistent effects of the earthquake in western PWS, but we presume that clams there fared even worse, because the uplift was greater than in other parts of the sound.
The initial loss of clams following the earthquake would have severely depressed the carrying capacity of the area for sea otters. At the time, the otter population in the sound was growing and expanding, as it recovered from over-exploitation during the fur trade. Counts at Green Island rose from 42 in 1959 to 116 in 1964 (7 months after the earthquake) and continued to rise through the early 1970s (Pitcher 1975). We suspect that otters were not food-limited at this time. Had it not been for the earthquake, otter numbers probably would have climbed even more quickly and ultimately would have attained higher levels. At Green Island, otters apparently reached carrying capacity by the late 1970s (Estes, Jameson & Johnson 1981; Johnson 1987), and by the early 1980s counts in Gibbon Anchorage showed a decline (Fig. 3).
We believe that the availability of clams limited otter numbers at Green Island during the early 1980s. Medium–large sized clams (i.e. ≥ 6 cm by our definition) that survived the earthquake would have been reduced by otter predation and other mortality, and replacement of this size class would have been minimal, due to the gap in recruitment following the earthquake and the slow growth of clams (Paul & Feder 1973, 1976; Feder & Paul 1974; Paul, Paul & Feder 1976). Clams recruited during the mid-1970s, when habitat conditions in the western sound may have normalized, would still have been small in the early 1980s, and moreover, densities of clams big enough to constitute sea otter prey (> 3 cm) would have been low due to the long period of poor recruitment. These conditions would have improved by the mid–late 1980s as clams born in the early 1980s became sufficiently large to be preyed upon by otters, and some clams born in the 1970s reached the larger size class (Fig. 8). Because the edible biomass of clams increases by roughly the cube of their shell length (Feder & Paul 1973, 1974), increased availability of larger clams would have provided substantially more nourishment for otters. Ten-year-old clams of the species most frequently consumed by otters at Green Island [S. giganteus, P. staminea and Mya truncata L. (a clam intermediate in size between S. giganteus and P. staminea)] contain > 10 times more meat than 5-year-old clams (calculated from data presented by Feder & Paul 1973, 1974; Paul & Feder 1976; Kvitek et al. 1992).
Figure 8. Hypothesized trajectory of the sea otter population in western Prince William Sound, Alaska, USA, in response to changing biomass of prey-sized clams and the 1989 Exxon Valdez oil spill. Trend in otter numbers was surmised from data presented by Pitcher (1975), Johnson (1987) and this study. The portion of the curve between 1978 and 1996 approximately follows the count data from Gibbon Anchorage (Fig. 3). Clam biomass was significantly reduced (more than shown on graph) from the uplift caused by the 1964 earthquake in Prince William Sound (Baxter 1971) and recruitment was depressed for several years afterwards (Paul, Paul & Feder 1976). The slow growth rate of clams caused a lag between the normalization of clam recruitment in the mid-1970s and increased biomass of prey-sized clams for otters during the 1980s (data from this study).
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We found that 19% of the clams consumed by otters at Green Island in the early 1990s were 6–12 cm in length, compared with only 11% in this size category during the early 1980s, and whereas otters in this area were never seen preying upon > 12-cm clams in the early 1980s, 1% of the clams retrieved in the early 1990s were this large (Fig. 6). In 1984, A. M. Johnson (personal communication) found, for the first time since beginning his sea otter study in the mid-1970s, a large accumulation of otter-cracked butter clam shells (mean = 6·2 cm) on an intertidal beach in Gibbon Anchorage. We observed several accumulations of medium-sized butter clams that had been cracked open and consumed by otters in Gibbon Anchorage during our study. No data on clam sizes from the early 1980s were available for other sites in the western sound, but our data from the early 1990s at Knight Island indicate that clams obtained by otters there were at least as large as at Green Island (Fig. 7). We hypothesize that the increased availability of larger clams (and also crabs) promoted renewed growth of otter numbers in the western sound during the mid-1980s (Fig. 8).
Improving food conditions and growing otter numbers in the western sound seemed not to have been mirrored in the northern sound. Clam population dynamics there differed radically because this area subsided rather than uplifted during the earthquake. Unlike the uplifted area, subsided habitats appeared to be immediately suitable for deposition and survival of larval clams, and the subsidence appeared not to increase mortality of living clams (Baxter 1971). At the time of the earthquake, otters had not yet reoccupied the northern sound (Pitcher 1975). After they did, in about 1973, numbers probably grew quickly, as they took advantage of unexploited food resources. This pattern was observed after otters reoccupied the last stretches of eastern PWS in the late 1970s and early 1980s (Garshelis & Garshelis 1984; Simon-Jackson 1986; Monnett & Rotterman 1989). However, by the late 1980s otters had apparently reduced their preferred prey within shallower habitats along the edges of the deep fjords of the northern sound and were subsisting mainly on mussels, a low-quality food (Anthony 1995). This may have prompted the decline or movement further offshore that was reported by Burn (1994) and attributed to the oil spill.
It appears that at least three catastrophic events, the 19th-century fur trade, the 1964 earthquake, and 25 years afterwards, the Exxon Valdez oil spill, profoundly shaped the population dynamics of sea otters in PWS. Also, in the early 1990s, killer whales Orcinus orca L. started attacking and killing sea otters in western PWS (Hatfield et al. 1998), adding yet another confounding variable to their demography (Estes 1999; Garshelis & Johnson 1999). Distinguishing population effects of the oil spill from this bewildering array of background noise was far more complex than sea otter investigators, including ourselves, initially recognized.