A re‐evaluation of the role of killer whales Orcinus orca in a population decline of sea otters Enhydra lutris in the Aleutian Islands and a review of alternative hypotheses

• 1 During the past 15–20 years, sea otters Enhydra lutris in the Aleutian Islands, Alaska, USA, experienced a drastic decrease in population size. It has been hypothesized that an increase in killer whale Orcinus orca predation was the primary cause of this decline.
• 2 Causation of the decline by increased killer whale predation is now considered a textbook case of top‐down predator control. The purpose of this review is to re‐evaluate the evidence for killer whale predation and to review evidence for alternative causes.
• 3 The killer whale predation hypothesis is based on three lines of evidence: (i) there was an increase in the number of observed killer whale attacks on sea otters during the 1990s, coincident with a decline in sea otters, (ii) sea otter populations did not decline in areas considered inaccessible to killer whales, while they declined in adjacent areas considered accessible to killer whales, and (iii) the estimated number of attacks necessary to account for the rate of decline is similar to the observed number of attacks. Our re‐evaluation indicates that although the killer whale hypothesis is by no means disproved, the supporting data are limited and inconclusive.
• 4 Increases in shark populations in the Aleutian Islands concurrent with the sea otter population declines indicate the need for further research into the role of alternative marine predators in the population decline.
• 5 High contaminant levels observed in sea otters in the Aleutian Islands warrant further investigation into the impact of these toxins on sea otter health and vital rates, and their possible role on the population decline.
• 6 Disease has not been ruled out as a significant contributor to the population decline, particularly in the early stages of the decline.

     

KILLER WHALES AND MARINE MAMMAL TRENDS IN THE NORTH PACIFIC—A RE-EXAMINATION OF EVIDENCE FOR SEQUENTIAL MEGAFAUNA COLLAPSE AND THE PREY-SWITCHING HYPOTHESIS

Springer et al . (2003) contend that sequential declines occurred in North Pacific populations of harbor and fur seals, Steller sea lions, and sea otters. They hypothesize that these were due to increased predation by killer whales, when industrial whaling's removal of large whales as a supposed primary food source precipitated a prey switch. Using a regional approach, we reexamined whale catch data, killer whale predation observations, and the current biomass and trends of potential prey, and found little support for the prey-switching hypothesis. Large whale biomass in the Bering Sea did not decline as much as suggested by Springer et al ., and much of the reduction occurred 50–100 yr ago, well before the declines of pinnipeds and sea otters began; thus, the need to switch prey starting in the 1970s is doubtful. With the sole exception that the sea otter decline followed the decline of pinnipeds, the reported declines were not in fact sequential. Given this, it is unlikely that a sequential megafaunal collapse from whales to sea otters occurred. The spatial and temporal patterns of pinniped and sea otter population trends are more complex than Springer et al . suggest, and are often inconsistent with their hypothesis. Populations remained stable or increased in many areas, despite extensive historical whaling and high killer whale abundance. Furthermore, observed killer whale predation has largely involved pinnipeds and small cetaceans; there is little evidence that large whales were ever a major prey item in high latitudes. Small cetaceans (ignored by Springer et al .) were likely abundant throughout the period. Overall, we suggest that the Springer et al . hypothesis represents a misleading and simplistic view of events and trophic relationships within this complex marine ecosystem.     

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.     

A century of Chinook salmon consumption by marine mammal predators in the Northeast Pacific Ocean

As many marine mammal populations have increased following bans on their harvest, there has been a growing need to understand potential impacts of these population changes on coastal marine ecosystems. Quantifying consumption of prey species, such as fish, is particularly important when those same prey are also targeted by commercial fisheries. Estimating the impact of marine mammal predators on prey fish depends upon knowledge of marine mammal diet composition; scientific advances over the last century have improved understanding of diets but have also led to inconsistent methods that challenge attempts at synthesis and comparison. Meta-analysis techniques offer the opportunity to overcome such challenges, yet have not been widely applied to synthesize marine mammal diets over space and time. As a case study, we focus on synthesizing diet studies of Chinook (king) salmon (Oncorhynchus tshawytscha) by four species of marine mammal predators in the Northeast Pacific Ocean: Steller sea lions (Eumetopias jubatus), California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and killer whales (Orcinus orca). We also highlight several simple meta-analyses for which these types of diet databases may be employed. Our assembled database consists of > 330 records, spanning more than 100 years. Results indicate that the frequency of occurrence of Chinook salmon in killer whale studies is high (63%) relative to pinniped studies (< 10%). They also suggest a strong increasing ability to discriminate Chinook salmon from other salmonids, which we attribute to switches in diet studies from lethal or observational sampling toward molecular methods (DNA, fatty acids). Our database and analysis code are published as supplementary material, which we hope will be useful for other researchers and will inspire more of these syntheses.     

ISOLATION AND EXPRESSION OF THE INTERLEUKIN-2 GENE FROM THE KILLER WHALE, ORCINUS ORCA

Complementary DNA encoding interleukin-2 (IL-2) was isolated, cloned, and sequenced from the killer whale, Orcinus orca . The sequence of the killer whale IL-2 coding region consists of 455 nucleotides which translate into a polypeptide containing 151 amino acids. Killer whale IL-2 displays 88%, 88%, 87%, 87%, 85%, 84%, 80%, and 71% nucleotide sequence homology and 76%, 76%, 76%, 73%, 68%, 73%, 64%, and 56% amino acid homology with the cow, sheep, pig, red deer, horse, human, manatee, and mouse, respectively. High levels of killer whale recombinant IL-2 were generated by transiently transfecting killer whale IL-2/pCMV Blue plasmid DNA into cultured monkey kidney cells (Cos-1). Generation of this recombinant IL-2 will allow the development of assays useful for assessing IL-2 levels in the serum and from isolated lymphocytes of killer whales and possibly other species of cetaceans. A major contribution and significance of the in vitro expression of killer whale IL-2 exists in its potential to be used as a therapeutic agent.     

Hearing in the sea otter (Enhydra lutris): auditory profiles for an amphibious marine carnivore

In this study we examine the auditory capabilities of the sea otter (Enhydra lutris), an amphibious marine mammal that remains virtually unstudied with respect to its sensory biology. We trained an adult male sea otter to perform a psychophysical task in an acoustic chamber and at an underwater apparatus. Aerial and underwater audiograms were constructed from detection thresholds for narrowband signals measured in quiet conditions at frequencies from 0.125–40 kHz. Aerial hearing thresholds were also measured in the presence of octave-band masking noise centered at eight signal frequencies (0.25–22.6 kHz) so that critical ratios could be determined. The aerial audiogram of the sea otter resembled that of sea lions and showed a reduction in low-frequency sensitivity relative to terrestrial mustelids. Best sensitivity was ?1 dB re 20 µPa at 8 kHz. Under water, hearing sensitivity was significantly reduced when compared to sea lions and other pinniped species, demonstrating that sea otter hearing is primarily adapted to receive airborne sounds. Critical ratios were more than 10 dB higher than those measured for pinnipeds, suggesting that sea otters are less efficient than other marine carnivores at extracting acoustic signals from background noise, especially at frequencies below 2 kHz.     

The complete mitochondrial DNA sequence of the harbor seal,Phoca vitulina

Summary The nucleotide sequence of the mitochondrial DNA (mtDNA) of the harbor seal, Phoca vitulina, was determined. The total length of the molecule was 16,826 bp. The organization of the coding regions of the molecule conforms with that of other mammals, but the control region is unusually long. A considerable portion of the control region is made up of short repeats with the motif GTACAC particularly frequent. The two rRNA genes and the 13 peptide-coding genes of the harbor seal, fin whale, cow, human, mouse, and rat were compared and the relationships between the different species assessed. At ordinal level the 12S rRNA gene and 7 out of the 13 peptide-coding genes yielded a congruent topological tree of the mtDNA relationship between the seal, cow, whale, human, and the rodents. In this tree the whale and the cow join first, and this clade is most closely related to the seal.Offprint requests to: Ú. Árnason     

Comments on Allard and Carpenter (1996), or the "Aquatic Ape" Hypothesis Revisited

The results of Allard and Carpenter's ( Cladistics 12, 183–198, 1996) paper on weighting and congruence among mammalian mitochondrial genes are an artefact of errors in their data matrix; their "blue whale" ATPASE8 sequence is human, the actual blue whale sequence is assigned to the grey seal, and the "horse" sequence is that of the harbor seal. When these errors are corrected there is no evidence that the mitochondrial genes are incongruent.     

Molecular cloning and characterization of CD4 in an aquatic mammal, the white whale Delphinapterus leucas

 Given the importance of the cell surface recognition protein, CD4, in immune function, the cloning and characterization of CD4 at the molecular level from an odontocete cetacean, the white whale (Delphinapterus leucas), was carried out. Whale CD4 cDNA contains 2662 base pairs and translates into a protein containing 455 amino acids. Whale CD4 shares 64% and 51% identity with the human and mouse CD4 protein, respectively, and is organized in a similar manner. Unlike human and mouse, however, the cytoplasmic domain, which is highly conserved, contains amino acid substitutions unique to whale. Moreover, only one of the seven potential N-linked glycosylation sites present in whale is shared with human and mouse. Evolutionarily, the whale CD4 sequence is most similar to pig and structurally similar to dog and cat, in that all lack the cysteine pair in the V2 domain. These differences suggest that CD4 may have a different secondary structure in these species, which may affect binding of class II and subsequent T-cell activation, as well as binding of viral pathogens. Interestingly, as a group, species with these CD4 characteristics all have high constituitive expression of class II molecules on T lymphocytes, suggesting potential uniqueness in the interaction of CD4, class II molecules, and the immune response. Molecular characterization of CD4 in an aquatic mammal provides information on the CD4 molecule itself and may provide insight into adaptive evolutionary changes of the immune system. Received: 1 July 1998 / Revised: 6 October 1998     

Killer whale (Orcinus orca) predation in a multi-prey system

Predation can regulate prey numbers but predator behaviour in multiple-prey systems can complicate understanding of control mechanisms. We investigate killer whale (Orcinus orca) predation in an ocean system where multiple marine mammal prey coexist. Using stochastic models with Monte-Carlo simulations, we test the most likely outcome of predator selection and compare scenarios where killer whales: (1) focus predation on larger prey which presumably offer more energy per effort, (2) generalize by feeding on prey as encountered during searches, or (3) follow a mixed foraging strategy based on a combination of encounter rate and prey size selection. We test alternative relationships within the Hudson Bay geographic region, where evidence suggests killer whales seasonally concentrate feeding activities on the large-bodied bowhead whale (Balaena mysticetus). However, model results indicate that killer whales do not show strong prey specialization and instead alternatively feed on narwhal (Monodon monoceros) and beluga (Delphinapterus leucas) whales early and late in the ice-free season. Evidence does support the conjecture that during the peak of the open water season, killer whale predation can differ regionally and feeding techniques can focus on bowhead whale prey. The mixed foraging strategy used by killer whales includes seasonal predator specialization and has management and conservation significance since killer whale predation may not be constrained by a regulatory functional response.     

Cooperative hunting behavior,prey selectivity and prey handling by pack ice killer whales (Orcinus orca), type B,in Antarctic Peninsula waters

Currently, there are three recognized ecotypes (or species) of killer whales (Orcinus orca) in Antarctic waters, including type B, a putative prey specialist on seals, which we refer to as “pack ice killer whale” (PI killer whale). During January 2009, we spent a total of 75.4 h observing three different groups of PI killer whales hunting off the western Antarctic Peninsula. Observed prey taken included 16 seals and 1 Antarctic minke whale (Balaenoptera bonaerensis). Weddell seals (Leptonychotes weddellii) were taken almost exclusively (14/15 identified seal kills), despite the fact that they represented only 15% of 365 seals identified on ice floes; the whales entirely avoided taking crabeater seals (Lobodon carcinophaga; 82% relative abundance) and leopard seals (Hydrurga leptonyx; 3%). Of the seals killed, the whales took 12/14 (86%) off ice floes using a cooperative wave‐washing behavior; they produced 120 waves during 22 separate attacks and successfully took 12/16 (75%) of the Weddell seals attacked. The mean number of waves produced per successful attack was 4.1 (range 1–10) and the mean attack duration was 30.4 min (range 15–62). Seal remains that we examined from one of the kills provided evidence of meticulous postmortem prey processing perhaps best termed “butchering.”     

Haul-out behavior of harbor seals (Phoca vitulina) in Hood Canal, Washington

The goal of this study was to model haul-out behavior of harbor seals (Phoca vitulina) in the Hood Canal region of Washington State with respect to changes in physiological, environmental, and temporal covariates. Previous research has provided a solid understanding of seal haul-out behavior. Here, we expand on that work using a generalized linear mixed model (GLMM) with temporal autocorrelation and a large dataset. Our dataset included behavioral haul-out records from archival and VHF radio tag deployments on 25 individual seals representing 61,430 seal hours. A novel application for increased computational efficiency allowed us to examine this large dataset with a GLMM that appropriately accounts for temporal autocorellation. We found significant relationships with the covariates hour of day, day of year, minutes from high tide and year. Additionally, there was a significant effect of the interaction term hour of day : day of year. This interaction term demonstrated that seals are more likely to haul out during nighttime hours in August and September, but then switch to predominantly daylight haul-out patterns in October and November. We attribute this change in behavior to an effect of human disturbance levels. This study also examined a unique ecological event to determine the role of increased killer whale (Orcinus orca) predation on haul-out behavior. In 2003 and 2005 these harbor seals were exposed to unprecedented levels of killer whale predation and results show an overall increase in haul-out probability after exposure to killer whales. The outcome of this study will be integral to understanding any changes in population abundance as a result of increased killer whale predation.     

Entry and Elimination of Marine Mammal Brucella spp. by Hooded Seal (Cystophora cristata) Alveolar Macrophages In Vitro

A high prevalence of Brucella pinnipedialis serology and bacteriology positive animals has been found in the Northeast Atlantic stock of hooded seal ( Cystophora cristata ); however no associated gross pathological changes have been identified. Marine mammal brucellae have previously displayed different infection patterns in human and murine macrophages. To investigate if marine mammal Brucella spp. are able to invade and multiply in cells originating from a presumed host species, we infected alveolar macrophages from hooded seal with a B . pinnipedialis hooded seal isolate. Hooded seal alveolar macrophages were also challenged with B . pinnipedialis reference strain (NCTC 12890) from harbor seal ( Phoca vitulina ), B . ceti reference strain (NCTC 12891) from harbor porpoise ( Phocoena phocoena ) and a B . ceti Atlantic white-sided dolphin ( Lagenorhynchus acutus ) isolate (M83/07/1), to evaluate possible species-specific differences. Brucella suis 1330 was included as a positive control. Alveolar macrophages were obtained by post mortem bronchoalveolar lavage of euthanized hooded seals. Phenotyping of cells in the lavage fluid was executed by flow cytometry using the surface markers CD14 and CD18. Cultured lavage cells were identified as alveolar macrophages based on morphology, expression of surface markers and phagocytic ability. Alveolar macrophages were challenged with Brucella spp. in a gentamicin protection assay. Following infection, cell lysates from different time points were plated and evaluated quantitatively for colony forming units. Intracellular presence of B . pinnipedialis hooded seal isolate was verified by immunocytochemistry. Our results show that the marine mammal brucellae were able to enter hooded seal alveolar macrophages; however, they did not multiply intracellularly and were eliminated within 48 hours, to the contrary of B. suis that showed the classical pattern of a pathogenic strain. In conclusion, none of the four marine mammal strains tested were able to establish a persistent infection in primary alveolar macrophages from hooded seal.     

Dietary habits of polar bears in Foxe Basin,Canada: possible evidence of a trophic regime shift mediated by a new top predator

Polar bear (Ursus maritimus) subpopulations in several areas with seasonal sea ice regimes have shown declines in body condition, reproductive rates, or abundance as a result of declining sea ice habitat. In the Foxe Basin region of Nunavut, Canada, the size of the polar bear subpopulation has remained largely stable over the past 20 years, despite concurrent declines in sea ice habitat. We used fatty acid analysis to examine polar bear feeding habits in Foxe Basin and thus potentially identify ecological factors contributing to population stability. Adipose tissue samples were collected from 103 polar bears harvested during 2010–2012. Polar bear diet composition varied spatially within the region with ringed seal (Pusa hispida) comprising the primary prey in northern and southern Foxe Basin, whereas polar bears in Hudson Strait consumed equal proportions of ringed seal and harp seal (Pagophilus groenlandicus). Walrus (Odobenus rosmarus) consumption was highest in northern Foxe Basin, a trend driven by the ability of adult male bears to capture large‐bodied prey. Importantly, bowhead whale (Balaena mysticetus) contributed to polar bear diets in all areas and all age and sex classes. Bowhead carcasses resulting from killer whale (Orcinus orca) predation and subsistence harvest potentially provide an important supplementary food source for polar bears during the ice‐free period. Our results suggest that the increasing abundance of killer whales and bowhead whales in the region could be indirectly contributing to improved polar bear foraging success despite declining sea ice habitat. However, this indirect interaction between top predators may be temporary if continued sea ice declines eventually severely limit on‐ice feeding opportunities for polar bears.     

Molecular cloning and expression of an IL-6 signal transducer, gp130

Interleukin-6 (IL-6) signal is transduced through a membrane glycoprotein, gp130, which associates with IL-6 receptor (IL-6-R). A cDNA encoding human gp130 has been cloned, revealing that it consists of 918 amino acids with a single transmembrane domain. The extracellular region comprises six units of a fibronectin type III module, and part of this region of approximately 200 amino acids has features typical of a cytokine receptor family. A cDNA-expressed gp130 showed no binding property to IL-6 or several other cytokines. Although a transfectant with an IL-6-R cDNA expressed mainly low affinity IL-6 binding sites, an increase in high affinity binding sites was observed after cotransfection with a gp130 cDNA. This confirmed that a gp130 is involved in the formation of high affinity IL-6 binding sites. A cloned gp130 could associate with a complex of IL-6 and soluble IL-6-R and transduce the growth signal when expressed in a murine IL-3-dependent cell line.     

Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews

Background

Killer whales (Orcinus orca) are the most widely distributed cetacean, occurring in all oceans worldwide, and within ocean regions different ecotypes are defined based on prey preferences. Prey items are largely unknown in the eastern Canadian Arctic and therefore we conducted a survey of Inuit Traditional Ecological Knowledge (TEK) to provide information on the feeding ecology of killer whales. We compiled Inuit observations on killer whales and their prey items via 105 semi-directed interviews conducted in 11 eastern Nunavut communities (Kivalliq and Qikiqtaaluk regions) from 2007-2010.

Results

Results detail local knowledge of killer whale prey items, hunting behaviour, prey responses, distribution of predation events, and prey capture techniques. Inuit TEK and published literature agree that killer whales at times eat only certain parts of prey, particularly of large whales, that attacks on large whales entail relatively small groups of killer whales, and that they hunt cooperatively. Inuit observations suggest that there is little prey specialization beyond marine mammals and there are no definitive observations of fish in the diet. Inuit hunters and elders also documented the use of sea ice and shallow water as prey refugia.

Conclusions

By combining TEK and scientific approaches we provide a more holistic view of killer whale predation in the eastern Canadian Arctic relevant to management and policy. Continuing the long-term relationship between scientists and hunters will provide for successful knowledge integration and has resulted in considerable improvement in understanding of killer whale ecology relevant to management of prey species. Combining scientists and Inuit knowledge will assist in northerners adapting to the restructuring of the Arctic marine ecosystem associated with warming and loss of sea ice.     

Marine Mammal Strandings and Environmental Changes: A 15-Year Study in the St. Lawrence Ecosystem

Understanding the effects of climatic variability on marine mammals is challenging due to the complexity of ecological interactions. We used general linear models to analyze a 15-year database documenting marine mammal strandings (1994–2008; n = 1,193) and nine environmental parameters known to affect marine mammal survival, from regional (sea ice) to continental scales (North Atlantic Oscillation, NAO). Stranding events were more frequent during summer and fall than other seasons, and have increased since 1994. Poor ice conditions observed during the same period may have affected marine mammals either directly, by modulating the availability of habitat for feeding and breeding activities, or indirectly, through changes in water conditions and marine productivity (krill abundance). For most species (75%, n = 6 species), a low volume of ice was correlated with increasing frequency of stranding events (e.g. R² _adj = 0.59, hooded seal, Cystophora cristata). This likely led to an increase in seal mortality during the breeding period, but also to increase habitat availability for seasonal migratory cetaceans using ice-free areas during winter. We also detected a high frequency of stranding events for mysticete species (minke whale, Balaenoptera acutorostrata) and resident species (beluga, Delphinapterus leucas), correlated with low krill abundance since 1994. Positive NAO indices were positively correlated with high frequencies of stranding events for resident and seasonal migratory cetaceans, as well as rare species (R² _adj = 0.53, 0.81 and 0.34, respectively). This contrasts with seal mass stranding numbers, which were negatively correlated with a positive NAO index. In addition, an unusual multiple species mortality event (n = 114, 62% of total annual mortality) in 2008 was caused by a harmful algal bloom. Our findings provide an empirical baseline in understanding marine mammal survival when faced with climatic variability. This is a promising step in integrating stranding records to monitor the consequences of environmental changes in marine ecosystems over long time scales.     

KILLER WHALES, ORCINUS ORCA, IN THE SOUTHEASTERN BERING SEA: RECENT SIGHTINGS andPREDATION ON OTHER MARINE MAMMALS

An unusual number of killer whales appeared in inshore waters of the southeastern Bering Sea in summer 1989 and 1990. Multiple sightings occurred in Bristol and Kuskokwim bays where killer whales had been seen only rarely in previous years. Three animals became stranded on mud flats in Kuskokwim Bay but were able to free themselves on a high tide. Killer whales were observed interacting with salmon, harbor seals, Steller sea lions, walruses, and beluga whales. Detailed observations were made of killer whales attacking belugas in the Naknek River. Local conditions and behavioral adaptations may reduce the susceptibility of belugas to killer whale predation. Continued killer whale activity in this area would be unlikely to affect fish resources, but might have some influence on beluga whales.