Causes and consequences of marine mammal population declines in southwest Alaska: a food-web perspective.

Populations of sea otters, seals and sea lions have collapsed across much of southwest Alaska over the past several decades. The sea otter decline set off a trophic cascade in which the coastal marine ecosystem underwent a phase shift from kelp forests to deforested sea urchin barrens. This interaction in turn affected the distribution, abundance and productivity of numerous other species. Ecological consequences of the pinniped declines are largely unknown. Increased predation by transient (marine mammal-eating) killer whales probably caused the sea otter declines and may have caused the pinniped declines as well. Springer et al. proposed that killer whales, which purportedly fed extensively on great whales, expanded their diets to include a higher percentage of sea otters and pinnipeds following a sharp reduction in great whale numbers from post World War II industrial whaling. Critics of this hypothesis claim that great whales are not now and probably never were an important nutritional resource for killer whales. We used demographic/energetic analyses to evaluate whether or not a predator-prey system involving killer whales and the smaller marine mammals would be sustainable without some nutritional contribution from the great whales. Our results indicate that while such a system is possible, it could only exist under a narrow range of extreme conditions and is therefore highly unlikely.

Patterns of growth and body condition in sea otters from the Aleutian archipelago before and after the recent population decline.

1. Growth models for body mass and length were fitted to data collected from 1842 sea otters Enhydra lutris shot or live-captured throughout south-west Alaska between 1967 and 2004. Growth curves were constructed for each of two main year groups: 1967-71 when the population was at or near carrying capacity and 1992-97 when the population was in steep decline. Analyses of data collected from animals caught during 2004, when the population density was very low, were precluded by a small sample size and consequently only examined incidentally to the main growth curves. 2. Growth curves demonstrated a significant increase in body mass and body length at age in the 1990s. Asymptotic values of body mass were 12-18% higher in the 1990s than in the 1960s/70s, and asymptotic values for body length were 10-11% higher between the same periods. Data collected in 2004 suggest a continued increase in body size, with nearly all data points for mass and length falling significantly above the 1990s growth curves. 3. In addition to larger asymptotic values for mass and length, the rate of growth towards asymptotic values was more rapid in the 1990s than in the 1960s/70s: sea otters reached 95% of asymptotic body mass and body length 1-2 years earlier in the 1990s. 4. Body condition (as measured by the log mass/log length ratio) was significantly greater in males than in females. There was also an increasing trend from the 1960s/70s through 2004 despite much year-to-year variation. 5. Population age structures differed significantly between the 1960s/70s and the 1990s with the latter distribution skewed toward younger age classes (indicating an altered lx function) suggesting almost complete relaxation of age-dependent mortality patterns (i.e. those typical of food-limited populations). 6. This study spanned a period of time over which the population status of sea otters in the Aleutian archipelago declined precipitously from levels at or near equilibrium densities at some islands in the 1960s/70s to < 5% of estimated carrying capacity by the late 1990s. The results of this study indicate an improved overall health of sea otters over the period of decline and suggest that limited nutritional resources were not the cause of the observed reduced population abundance. Our findings are consistent with the hypothesis that the decline was caused by increased killer whale predation.

Introduced predators transform subarctic islands from grassland to tundra.

Top predators often have powerful direct effects on prey populations, but whether these direct effects propagate to the base of terrestrial food webs is debated. There are few examples of trophic cascades strong enough to alter the abundance and composition of entire plant communities. We show that the introduction of arctic foxes (Alopex lagopus) to the Aleutian archipelago induced strong shifts in plant productivity and community structure via a previously unknown pathway. By preying on seabirds, foxes reduced nutrient transport from ocean to land, affecting soil fertility and transforming grasslands to dwarf shrub/forb-dominated ecosystems.

Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling?

Populations of seals, sea lions, and sea otters have sequentially collapsed over large areas of the northern North Pacific Ocean and southern Bering Sea during the last several decades. A bottom-up nutritional limitation mechanism induced by physical oceanographic change or competition with fisheries was long thought to be largely responsible for these declines. The current weight of evidence is more consistent with top-down forcing. Increased predation by killer whales probably drove the sea otter collapse and may have been responsible for the earlier pinniped declines as well. We propose that decimation of the great whales by post-World War II industrial whaling caused the great whales' foremost natural predators, killer whales, to begin feeding more intensively on the smaller marine mammals, thus "fishing-down" this element of the marine food web. The timing of these events, information on the abundance, diet, and foraging behavior of both predators and prey, and feasibility analyses based on demographic and energetic modeling are all consistent with this hypothesis.

Historical overfishing and the recent collapse of coastal ecosystems.

Ecological extinction caused by overfishing precedes all other pervasive human disturbance to coastal ecosystems, including pollution, degradation of water quality, and anthropogenic climate change. Historical abundances of large consumer species were fantastically large in comparison with recent observations. Paleoecological, archaeological, and historical data show that time lags of decades to centuries occurred between the onset of overfishing and consequent changes in ecological communities, because unfished species of similar trophic level assumed the ecological roles of overfished species until they too were overfished or died of epidemic diseases related to overcrowding. Retrospective data not only help to clarify underlying causes and rates of ecological change, but they also demonstrate achievable goals for restoration and management of coastal ecosystems that could not even be contemplated based on the limited perspective of recent observations alone.

Inter-decadal patterns of population and dietary change in sea otters at Amchitka Island, Alaska.

After having been hunted to near-extinction in the Pacific maritime fur trade, the sea otter population at Amchitka Island, Alaska increased from very low numbers in the early 1900s to near equilibrium density by the 1940s. The population persisted at or near equilibrium through the 1980s, but declined sharply in the 1990s in apparent response to increased killer whale predation. Sea otter diet and foraging behavior were studied at Amchitka from August 1992 to March 1994 and the data compared with similar information obtained during several earlier periods. In contrast with dietary patterns in the 1960s and 1970s, when the sea otter population was at or near equilibrium density and kelp-forest fishes were the dietary mainstay, these fishes were rarely eaten in the 1990s. Benthic invertebrates, particularly sea urchins, dominated the otter's diet from early summer to mid-winter, then decreased in importance during late winter and spring when numerous Pacific smooth lumpsuckers (a large and easily captured oceanic fish) were eaten. The occurrence of spawning lumpsuckers in coastal waters apparently is episodic on a scale of years to decades. The otters' recent dietary shift away from kelp-forest fishes is probably a response to the increased availability of lumpsuckers and sea urchins (both high-preference prey). Additionally, increased urchin densities have reduced kelp beds, thus further reducing the availability of kelp-forest fishes. Our findings suggest that dietary patterns reflect changes in population status and show how an ecosystem normally under top-down control and limited by coastal zone processes can be significantly perturbed by exogenous events.

The diving physiology of bottlenose dolphins (Tursiops truncatus). III. Thermoregulation at depth.

During diving, marine mammals initiate a series of cardiovascular changes that include bradycardia and decreased peripheral circulation. Because heat transfer from thermal windows located in peripheral sites of these mammals depends on blood flow, such adjustments may limit their thermoregulatory capabilities during submergence. Here, we demonstrate how the thermoregulatory responses of bottlenose dolphins (Tursiops truncatus) are coordinated with the diving response. Heart rate, skin temperature and heat transfer from the dorsal fin and flank were measured while dolphins rested on the water surface, stationed 5-50 m under water and floated at the surface immediately following a dive. The results showed that heat flow ranged from 42.9+/-7.3 to 126.2+/-23.1 W m(-)(2) and varied with anatomical site and diving activity. Upon submergence, heat flow declined by 35 % from the dorsal fin and by 24 % from the flank. An immediate increase in heat flow to levels exceeding pre-dive values occurred at both sites upon resurfacing. Changes in heart rate during diving paralleled the thermoregulatory responses. Mean pre-dive heart rate (102.0+/-2.6 beats min(-)(1), N=26) decreased by 63.4 % during dives to 50 m and immediately returned to near resting levels upon resurfacing. These studies indicate that heat dissipation by dolphins is attenuated during diving. Rather than challenge the diving response, heat transfer is delayed until post-dive periods when the need for oxygen conservation is reduced.

A new assay for quantifying brown algal phlorotannins and comparisons to previous methods.

Quantitative measurement of phlorotannins (polyphenolics) in brown algae (Phaeophyta) by colorimetric assays can be confounded because: (1) most such assays also react to nonphlorotannin substances (interferences) and (2) the appropriate reference compound for such assays is not always clear, although phloroglucinol is typically used. We developed a new assay in which 2,4-dimethoxybenzaldehyde (DMBA) reacts specifically with 1,3-and 1,3,5-substituted phenols (e.g., phlorotannins) to form a colored product. This new assay, as well as eliminating the problem of measuring interferences, is inexpensive, rapid, and can be used with small sample volumes. We recommend it for all assays of phlorotannins from one or a set of closely related species where the structural types of phlorotannins present are likely to be similar among samples. It is also appropriate for broader surveys of phlorotannin levels across many species, but in this case a reference must be chosen with care. We also compared the DMBA assay to existing assays, including the Folin-Denis [both before and after the samples were mixed with polyvinylpolypyrrolidone (PVPP)] and the Prussian blue assays. PVPP was not 100% efficient (and often much less) at removing phlorotannins from solution, and its effectiveness varied among different phlorotannins. Thus, in contrast to previous studies, measuring phenolic levels in extracts before and after treatment with PVPP will not necessarily result in an interference-free measure of phlorotannins. Based on an analysis of reactive substances in red and green algae (which do not contain phlorotannins) in the Folin-Denis and Prussian blue assays, we estimate that the average level of interferences (nonphlorotannins) in brown algae measured in these two assays is on the order of 0.5% by dry weight.

Evolutionary consequences of food chain length in kelp forest communities.

Kelp forests are strongly influenced by macroinvertebrate grazing on fleshy macroalgae. In the North Pacific Ocean, sea otter predation on macroinvertebrates substantially reduces the intensity of herbivory on macroalgae. Temperate Australasia, in contrast, has no known predator of comparable influence. These ecological and biogeographic patterns led us to predict that (i) the intensity of herbivory should be greater in temperate Australasia than in the North Pacific Ocean; thus (ii) Australasian seaweeds have been under stronger selection to evolve chemical defenses and (iii) Australasian herbivores have been more strongly selected to tolerate these compounds. We tested these predictions first by measuring rates of algal tissue loss to herbivory at several locations in Australasian and North Pacific kelp forests. There were significant differences in grazing rates among sea otter-dominated locations in the North Pacific (0-2% day-1), Australasia (5-7% day-1), and a North Pacific location lacking sea otters (80% day-1). The expectations that chronically high rates of herbivory in Australasia have selected for high concentrations of defensive secondary metabolites (phlorotannins) in brown algae and increased tolerance of these defenses in the herbivores also were supported. Phlorotannin concentrations in kelps and fucoids from Australasia were, on average, 5-6 times higher than those in a comparable suite of North Pacific algae, confirming earlier findings. Furthermore, feeding rates of Australasian herbivores were largely unaffected by phlorotannins, regardless of the compounds' regional source. North Pacific herbivores, in contrast, were consistently deterred by phlorotannins from both Australasia and the North Pacific. These findings suggest that top-level consumers, acting through food chains of various lengths, can strongly influence the ecology and evolution of plantherbivore interactions.

Magnification of secondary production by kelp detritus in coastal marine ecosystems.

Kelps are highly productive seaweeds found along most temperate latitude coastlines, but the fate and importance of kelp production to nearshore ecosystems are largely unknown. The trophic role of kelp-derived carbon in a wide range of marine organisms was assessed by a natural experiment. Growth rates of benthic suspension feeders were greatly increased in the presence of organic detritus (particulate and dissolved) originating from large benthic seaweeds (kelps). Stable carbon isotope analysis confirmed that kelp-derived carbon is found throughout the nearshore food web.

Aleuts, sea otters, and alternate stable-state communities.

Reexamination of stratified faunal components of a prehistoric Aleut midden excavated on Amchitka Island, Alaska, indicates that Aleut prey items changed dramatically during 2500 years of aboriginal occupation. Recent ecological studies in the Aleutian Islands have shown the concurrent existence of two alternate stable nearshore communities, one dominated by macroalgae, the other by epibenthic herbivores, which are respectively maintained by the presence or absence of dense sea otter populations. Thus, rather than cultural shifts in food preference, the changes in Aleut prey were probably the result of local overexploitation of sea otters by aboriginal Aleuts.

Sea otters: their role in structuring nearshore communities.

A comparison of western Aleutian Islands with and without sea otter populations shows that this species is important in determining littoral and sublittoral community structure. Sea otters control herbivorous invertebrate populations. Removal of sea otters causes increased herbivory and ultimately results in the destruction of macrophyte associations. The observations suggest that sea otter reestablishment indirectly affects island fauna associated with macrophyte primary productivity.