Alan M. Springer

KILLER APPETITES: ASSESSING THE ROLE OF PREDATORS IN ECOLOGICAL COMMUNITIES

Large body size, carnivory, and endothermic costs lead to exceptionally high caloric demands in many mammalian predators. The potential impact on prey resources may be marked but is difficult to demonstrate because of the mobility, sparseness, and cryptic nature of these animals. In this study, we developed a method based on comparative bioenergetics and demographic modeling to evaluate predator effects and then used this approach to assess the potential impact of killer whales on sea otter and Steller sea lion populations in the Aleutian Islands. Daily caloric requirements of killer whales determined from allometric regressions for field metabolic rate show that an adult killer whale requires 51-59 kcal·kg 21 ·d 21 (2.5-2.9 W/kg). Caloric values of prey items determined by bomb calorimetry ranged from 41 630 kcal for an adult female sea otter to sequentially higher values for male otters, sea lion pups, and adult Steller sea lions. Integrating these results with demographic changes in marine mammal populations show that fewer than 40 killer whales could have caused the recent Steller sea lion decline in the Aleutian archipelago; a pod of five individuals could account for the decline in sea otters and the continued suppression of sea lions. The collapse of the historical prey base of killer whales due to human whaling may have contributed to a sequential dietary switch from high to low caloric value prey, thereby initiating these declines. This study demonstrates that a combined physiological-demographic approach increases our ability to critically evaluate the potential impact of a predator on community structure and enables us to define underlying mechanisms

The paradox of pelagic food webs in the northern Bering Sea—III. Patterns of primary production

Abstract The advective supply of nutrients to the Bering-Chukchi continental shelf via a north-flowing “river” of oceanic water originating along the continental slope in the Bering Sea maintains a large portion of these shelf waters in eutrophic bloom summer-long. Known as the Anadyr Stream, this nutrient injection sustains conditions of high phytoplankton productivity and biomass in a region of the western Arctic that would otherwise be unproductive, as are adjacent shelf areas unaffected by the current. A production plume dominated by large chain-forming diatoms extends from the Gulf of Anadyr in the south to the southern Chukchi Sea in the north, has daily carbon uptake rates as high as 16 g C m −2 day −1 , and has an estimated annual production of about 470 g C m −2 year −1 . Maximum production occurs in three pools of especially prolific growth (Gulf of Anadyr, Chirikov Basin and southern Chukchi Sea) where rates could be as great as 720–840 g C m −2 year −1 . Outside of the plume, nutrients remain low following the spring bloom and a typical successional flora is dominated by flagellates and small diatoms throughout summer. Post-bloom productivity in this region is generally about 0.5 g C m −2 day −1 , and annual production is approximately 80 g C m −2 year −1 . The contrasting primary production regimes lead to major differences in food webs and in the energy transferred to higher trophic levels within the western Arctic.

The paradox of pelagic food webs in the northern Bering Sea—II. Zooplankton communities

Abstract Anadyr Water, a “river” of oceanic water originating over the continental slope of the Bering Sea, transports oceanic zooplankton onto the shallow northern shelf and into the Chukchi Sea through western Bering Strait. The oceanic copepods Neocalanus cristatus, N. plumchrus, Eucalanus bungii and Metridia pacifica dominated the biomass of herbivorous zooplankton in Anadyr Water on the Bering-Chukchi shelf, averaging about 5 g m −2 (dry weight) in midsummer and 2 g m −2 in later summer of 1985 and 1986. The biomass of copepods was at times augmented considerably by that of a larvacean, Oikopleura spp. Oceanic water was replaced to the east, and often overlain by, lighter water formed on the continental shelf. The oceanic species were not present in waters of shelf origin, where Calanus marshallae was the major herbivore, averaging about 1 g m −2 in summer 1985, but only 0.2–0.5 g m −2 in 1986. In the low salinity, nearshore water, C. marshallae was uncommon and Pseudocalanus spp. and Acartia longiremis predominated. A preliminary estimate indicated that in the order of 1.8 × 10 12 g C of boreal zooplankton were carried into the Chukchi Sea during summer 1985. On average, the grazers were unable to control prodigious diatom growth that resulted from concentrated nutrients also carried by Anadyr Water into the area. In contrast, the smaller biomass of grazers in the shelf community, away from the region of high diatom biomass, might have had a much greater influence over the standing stock of phytoplankton following the spring bloom, and, at times, could have consumed the daily primary production. The highly productive pelagic food web of oceanic origin in the north does not have close coupling between primary producers and zooplankton, or between zooplankton and their predators, and contrasts with the oceanic community in the southeastern Bering Sea, where the same species of herbivores apparently have a much greater effect on phytoplankton biomass, and provide an efficient transfer of the available fixed energy to upper trophic levels in pelagic food webs.

High annual variability in reproductive success of kittiwakes (Rissa tridactyla L.) at a colony in western Alaska

(1) All aspects of reproductive performance of kittiwakes (Rissa tridactyla L.) fluctuated markedly in 1975-89 at a colony of about 10000 nesting pairs in the north-eastern Bering Sea, Alaska. (2) In breeding seasons following cold springs, breeding was delayed, fewer nests were built, fewer nests contained eggs, and clutch size, hatching success and the number of chicks fledging per nest were reduced. Complete reproductive failures followed the three coldest springs in the 15-year period. (3) Reproductive success (chicks fledged per nest) was highest following moderately warm springs; however, growth rates of chicks and fledging success were extremely low following the warmest spring on record. (4) Spring air temperatures were highly correlated with break-up of sea ice and these factors probably influenced seasonal warming trends in the sea water and the consequent availability of prey such as sandeels (Ammodytes hexapterus Pallas) near the colony. (5) During this 15-year period, interannual variability in spring air temperature was pronounced in comparison to that during the previous 68-year period; however, simulations using May temperature as a predictor of reproductive success suggested that high annual variability in reproduction has occurred throughout this century. (6) Numbers of adult-plumaged birds on the cliffs in mid-season were markedly lower and more variable in years when few nests were built, suggesting that relatively few experienced adults breed and consistently are present at the colony in years when overall reproductive performance is poor.

Marine birds and mammals of the Pacific Subarctic Gyres

The importance of the subarctic gyres of the North Pacific Ocean to marine birds and mammals is poorly known because of a paucity of data spanning appropriate scales of time and space. The little information that is available indicates the western subarctic gyre (WSAG) is more productive than the eastern subarctic gyre (ESAG). In summer the WSAG supports a greater density and higher biomass of seabirds than the ESAG, including at least two species that are more abundant at nesting colonies in the eastern subarctic. Perhaps most revealing of the seabird distributions in this regard is that of southern hemisphere shearwaters (Puffinus spp. ) that overwinter in the North Pacific. Their biomass is an order of magnitude greater than that of any northern hemisphere species and is three-fold greater in the WSAG than in the ESAG. Several species of cetaceans also appear to be, or to have been prior to commercial depletions, more abundant in the WSA. Among the many prey species consumed by marine birds and mammals, squids and fishes in the family Myctophidae predominate overall. Other forage species, notably euphausiids, Pacific saury (Cololabis saira) and Atka mackerel (Pleurogrammus monopterygius) are important at times to certain species. The principal exceptions to this generalization are baleen whales and small seabirds that consume zooplankton. Interannual and decadal-scale variability in the physical environment and food web production affect seabirds and marine mammals at sea and at coastal breeding locations around the margins of the gyres.

The paradox of pelagic food webs in the northern Bering Sea—I. Seabird food habits

Two distinct environmental settings in the Bering Strait region of the northern Bering Sea lead to characteristic pathways of energy flow through primarily pelagic food webs to avian consumers. In Norton Sound, a large, shallow embayment on the northeastern coast, the physical environment is dominated by the discharge of the Yukon River and by a large seasonal temperature signal. Seabirds breeding at Bluff, the largest colony in Norton Sound, number in the order of 5 × 104 and require 1.2 × 106 g C d−1. Two piscivorous species constitute the bulk of all seabirds there and are supported by a pelagic food web typical of the coastal zone of the Bering and Chukchi seas. This food web also is present around St. Lawrence Island, on the northwestern shelf, and is important to at least one species of seabird there. In addition, and generally more important, St. Lawrence Island is in a biologically rich environment resulting from the northward flow of water that originates along the continental shelf break of the Bering Sea. This flow apparently accounts for the unexpected presence of oceanic zooplankton and a diversity of forage fishes on the shallow northern shelf that support an abundant and taxonomically rich avifauna. In comparison to Norton Sound, breeding seabirds on St. Lawrence Island number in the order of 2 × 106, with planktivores consuming about 8 × 106 g C d−1 and piscivores consuming about 16 × 106 g C d−1.

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.

From the Cover: PNAS Plus: Climate change, pink salmon, and the nexus between bottom-up and top-down forcing in the subarctic Pacific Ocean and Bering Sea

Significance Wild salmon in the North Pacific Ocean, particularly pink salmon, have grown greatly since the mid-1970s apparently due to bottom-up effects of climate change on ocean physics and production processes. Pink salmon spend less than 2 y at sea and most stocks alternate between high and low levels of abundance every other year. In years of high abundance, they now constitute a pelagic consumer front as they return to their spawning rivers, exert top-down control over the open ocean ecosystem by outcompeting other species for shared prey resources, and drive major ecological shifts between years of high and low abundance. Their effect on competing species must be considered in international conservation policies and when developing informed ecosystem-based management strategies. Climate change in the last century was associated with spectacular growth of many wild Pacific salmon stocks in the North Pacific Ocean and Bering Sea, apparently through bottom-up forcing linking meteorology to ocean physics, water temperature, and plankton production. One species in particular, pink salmon, became so numerous by the 1990s that they began to dominate other species of salmon for prey resources and to exert top-down control in the open ocean ecosystem. Information from long-term monitoring of seabirds in the Aleutian Islands and Bering Sea reveals that the sphere of influence of pink salmon is much larger than previously known. Seabirds, pink salmon, other species of salmon, and by extension other higher-order predators, are tightly linked ecologically and must be included in international management and conservation policies for sustaining all species that compete for common, finite resource pools. These data further emphasize that the unique 2-y cycle in abundance of pink salmon drives interannual shifts between two alternate states of a complex marine ecosystem.

Temporal variability in abundance of Marbled Murrelets at sea in southeast Alaska

-We examined effects of season, time of day, tide stage, tidal oscillation, and sea surface temperature on Marbled Murrelet (Brachyramphus marmoratus) abundance and distribution at sea. We also evaluated whether constraining surveys to specific time periods or tide stages would reduce temporal variability in counts. Murrelets were surveyed daily from small boats and from shore in Auke Bay and Fritz Cove, Alaska, from May through August in 1992 and 1993. Murrelet numbers were high before egg-laying, declined by more than half during egg-laying and incubation and were highly variable during chick-rearing and fledging. Murrelet numbers were highest in early and late morning and declined throughout the day, sometimes increasing slightly in the evening. Peak murrelet numbers occurred on high or falling morning tides, especially in shallow areas where Pacific sand lance (Ammodytes hexapterus) were abundant. Differences between years in murrelet abundance and breeding phenology probably resulted from interannual differences in the pattern of seasonal warming and subsequent effects on production at lower trophic levels. We recommend that surveys for trends in abundance in Southeast Alaska be conducted in early morning, in June, at high or falling tides. Power analyses indicated that surveys conducted in this manner would minimize the number of years required to detect a significant change in abundance. Received 6 April 2000, accepted 3June 2000.

The sun, moon, wind, and biological imperative-shaping contrasting wintertime migration and foraging strategies of adult male and female northern fur seals (Callorhinus ursinus).

Adult male and female northern fur seals (Callorhinus ursinus) are sexually segregated in different regions of the North Pacific Ocean and Bering Sea during their winter migration. Explanations for this involve interplay between physiology, predator-prey dynamics, and ecosystem characteristics, however possible mechanisms lack empirical support. To investigate factors influencing the winter ecology of both sexes, we deployed five satellite-linked conductivity, temperature, and depth data loggers on adult males, and six satellite-linked depth data loggers and four satellite transmitters on adult females from St. Paul Island (Bering Sea, Alaska, USA) in October 2009. Males and females migrated to different regions of the North Pacific Ocean: males wintered in the Bering Sea and northern North Pacific Ocean, while females migrated to the Gulf of Alaska and California Current. Horizontal and vertical movement behaviors of both sexes were influenced by wind speed, season, light (sun and moon), and the ecosystem they occupied, although the expression of the behaviors differed between sexes. Male dive depths were aligned with the depth of the mixed layer during daylight periods and we suspect this was the case for females upon their arrival to the California Current. We suggest that females, because of their smaller size and physiological limitations, must avoid severe winters typical of the northern North Pacific Ocean and Bering Sea and migrate long distances to areas of more benign environmental conditions and where prey is shallower and more accessible. In contrast, males can better tolerate often extreme winter ocean conditions and exploit prey at depth because of their greater size and physiological capabilities. We believe these contrasting winter behaviors 1) are a consequence of evolutionary selection for large size in males, important to the acquisition and defense of territories against rivals during the breeding season, and 2) ease environmental/physiological constraints imposed on smaller females.