MARINE MAMMAL RESEARCH UNIT - UBC

Welcome to the Marine Mammal Research Unit

WELCOME TO THE MARINE MAMMAL RESEARCH UNIT

MMRU conducts research of the highest standards to enhance marine mammal conservation and reduce conflicts with human uses of our shared oceans.

MARINE MAMMAL RESEARCH NEWS

You can’t beat a healthy heart
New research is shedding light on the hearts of healthy marine mammals, and how they compare to human hearts
CANCELLED: BC Marine Mammal Symposium – November 2021

In late September, we made the difficult decision to cancel this year’s symposium.

No apparent shortage of prey for southern resident killer whales in the Salish Sea during summer

Researchers found four to six times more Chinook salmon in the Salish Sea in summertime compared with numbers of fish available to the growing population of northern resident killer whales.

2021 MMRU Students

After more than a year of working remotely, our graduate students are starting to head back to campus. They have been busy studying grey whales, killer whales, sea otters, sea lions, and much, much more….

 RECENT PUBLICATIONS


(in press)
 
New colony of Guadalupe fur seals (Arctocephalus townsendi) discovered on El Farallón de San Ignacio Island, Gulf of California.
del Carmen, G.-O.M., J.M. Díaz-Gaxiola, A.W. Trites and C.J. Hernández-Camacho. (in press).
Marine Mammal Science
abstract
Guadalupe fur seals (Arctocephalus townsendi) have established a second colony in the Gulf of California on El Farallón de San Ignacio Island, along the mainland coast of Mexico. They appear to have been coming to this island since 2014, and numbered as many as 771 in 2020 (mostly juveniles). The discovery of this new haulout brings the total number of sites where this species is known to rest and breed to just four. Guadalupe fur seals remain vulnerable and may require additional protection in the southern Gulf of California to secure their future.

keywords     Guadalupe, fur seal, endangered, Mexico, El Farallón de San Ignacio Island, Gulf of California, haulout
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Modelling multi-scale state-switching functional data with hidden Markov models.
Sidrow, E., N. Heckman, S. M. E. Fortune, A. W. Trites, I. Murphy and M. Auger-Méthé. (in press).
Canadian Journal of Statistics
abstract
Data sets comprised of sequences of curves sampled at high frequencies in time are increasingly common in practice, but they can exhibit complicated dependence structures that cannot be modelled using common methods of Functional Data Analysis (FDA). We detail a hierarchical approach which treats the curves as observations from a hidden Markov model (HMM). The distribution of each curve is then defined by another fine-scale model which may involve auto-regression and require data transformations using moving-window summary statistics or Fourier analysis. This approach is broadly applicable to sequences of curves exhibiting intricate dependence structures. As a case study, we use this framework to model the fine-scale kinematic movement of a northern resident killer whale (Orcinus orca) off the western coast of Canada. Through simulations, we show that our model produces more interpretable state estimation and more accurate parameter estimates compared to existing methods.

keywords     Accelerometer data; animal movement; biologging; diving behaviour; hierarchical modelling; killer whales; state-switching; statistical ecology; time series
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2021
 
The First Records of Antarctic Type B and C Killer Whales (Orcinus orcas) in Australian Coastal Waters.
Donnelly, D.M., J.D. McInnes, K.C.S. Jenner, M.N.M. Jenner and M. Morrice. 2021.
Aquatic Mammals 47(3):292-302.
abstract
Five ecotypes of killer whales occur in the southern hemisphere: Types A, B (B1 and B2), C, and D. Antarctic Type A has a circumpolar distribution around Antarctica, and are often associated with their preferred prey (minke whales, seals and penguins) in ice-free waters. Ecotype B typically occurs near or within pack ice where they predomi­nantly consume seals, as well as fish, squid, and penguins. Type C killer whales have been predominantly sighted in East Antarctica, and relatively little is known about the Type D individuals. We report seven sightings of Antarctic Type B and C killer whales in Australian coastal waters—as well as a third morphological form, closely resembling the Antarctic Type A ecotype. These records confirm that at least two of the five Antarctic eco-types described from the Southern Hemisphere also occur in Australian coastal waters.
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Body growth of North Atlantic right whales (Eubalaena glacialis) revisited.
Fortune, S. M. E., M. J. Moore, W. L. Perryman and A. W. Trites. 2021.
Marine Mammal Science 37:433-447.
abstract
Knowing size‐at‐age is important for determining food requirements and making inferences about the nutritional status of individuals and their populations. Accurate growth curves are also needed to quantify drug dosages to treat wounded or entangled animals. However, body sizes are often based on small numbers of measured animals that must be improved as new data become available. We updated an existing body growth model for North Atlantic right whales (NARWs) using new data from dead animals and from older individuals. Our models indicate that NARWs attain mean lengths and weights of 4.3 m and 1.0 mt at birth, and 13.1 m and 31.7 mt when sexually mature. Calves more than double their length and attain nearly three‐quarters of their asymptotic adult size during their first year of life. Overall, our length estimates agreed well with previous estimates, but our mass‐at‐age values were considerably higher. These differences revealed that necropsy data used alone in allometric models underestimate mass due possibly to several of the stranded animals in the database having been chronically entangled and in poor body condition. Augmenting the database with healthier individuals, such as harvested North Pacific right whales, yielded mass predictions that reflect both healthy and unhealthy individuals.

keywords     body size, Eubalaena glacialis, growth models, length, mass, morphometry, photogrammetry
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Foraging habitat of North Atlantic right whales has declined in the Gulf of St. Lawrence, Canada, and may be insufficient for successful reproduction.
Gavrilchuk, K., V. Lesage, S.M.E. Fortune, A.W. Trites, and S. Plourde. 2021.
Endangered Species Research. 44:113-136.
abstract
North Atlantic right whale (Eubalaena glacialis) population fed in the Gulf of St. Lawrence (Canada) in recent years. However, little is known about the distribution of copepods in the Gulf, and whether their abundance is sufficient to energetically sustain right whales. We used a mechanistic modeling approach to predict areas within the Gulf that have foraging potential for adult female right whales, based on the annual energetic needs of resting, pregnant, and lactating females, and their theoretical prey density requirements. We identified suitable foraging areas for right whales by coupling a foraging bioenergetics model with a 12-year data set (2006-2017) describing the abundance and three-dimensional distribution of late-stage Calanus spp. in the Gulf. Prey densities in the southern Gulf (from Shediac Valley to the Magdalen Islands) supported all three reproductive states in most (≥ 6) years. However, foraging habitat became progressively sparse in the southern Gulf over time, with noticeably less suitable habitat available after 2014. Few other potentially suitable foraging areas were identified elsewhere in the Gulf. Overall, the availability of foraging habitat in the Gulf varied considerably between years, and was higher for resting females than for pregnant and lactating females. Our findings are consistent with the recent low calving rates, and indicate that prey biomass in the Gulf of St. Lawrence may be insufficient in most years to support successful reproduction of North Atlantic right whales.

keywords     nutritional stress, bioenergetics, endangered, copepods, energy requirements, foraging, habitat, Calanus, right whale, Gulf of St Lawrence, prey density
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Transient Killer Whales of Central and Northern California and Oregon: A Catalog of Photo-Identified Individuals.
McInnes, J.D., C.R. Mathieson, P.J. West-Stap, S.L. Marcos, V.L. Wade, P.A. Olson and A.W. Trites. 2021.
NOAA Technical Memorandum NMFS-SWFSC-644:149 p.
abstract
Photo-identification studies of transient killer whales (Orcinus orcas) off western North America have primarily been conducted in the coastal inland waterways of Washington State, British Columbia, and southeastern Alaska. Less is known about transient killer whales along the outer coast and offshore waters of Oregon and central and northern California. We examined 13 years of photo-identification data to identify individuals and obtain a minimum census for this region, and to summarize information that could be useful for evaluating a hypothesis that whales using this area belong to a distinct assemblage. Data contributions came from opportunistic marine mammal surveys, whale watch ecotours, and dedicated line transect surveys. Transient killer whale photographs were obtained from 146 encounters between 2006 – 2018. These included 136 encounters in Monterey Bay, California, 5 encounters off central and northern California, and 5 encounters off Oregon. The number of unique individuals seen during this time totaled 155, of which 150 were considered to be alive (as of 2018). These included 34 adult males, 51 adult females, 24 sub-adults, and 41 juveniles. Through repeated observations of association patterns, a total of 30 matrilineal groups were identified. New whales were identified each year, including previously unidentified adults and new calves. Identification images of the dorsal fins, saddle patches and postocular patches were obtained. Details on sex, maternal ancestry, sighting history, and distribution are provided where known. These cataloged transient killer whales were predominantly encountered off the outer coast near the continental shelf break or in deep pelagic waters overlying the Monterey Submarine Canyon. The vast majority (>83 %) of whales identified in the study area could not be matched to transient killer whales in photo ID catalogs for coastal waters of the Pacific Northwest. These factors are consistent with there being a distinct “outer coast” assemblage within the west coast population of transient killer whales, but more research is needed to investigate this further.
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Resting and swimming metabolic rates in juvenile walruses (Odobenus rosmarus).
Rosen, D.A.S. 2021.
Marine Mammal Science 37:162-172.
abstract
Changes in Arctic ice conditions have raised concerns regarding potential impacts on energy expenditure and food requirements of walruses. Modelling the repercussions of environmental changes requires accurate species-specific measures of bioenergetic expenditures. This is particularly true for walruses, who have a unique anatomy and foraging ecology from other pinnipeds. This study measured resting metabolic rate (RMR) and subsurface swimming metabolism in two juvenile walruses over a 13-month period. The walruses had relatively low RMR compared to studies of other young pinnipeds. RMR was greater for the male than the female, as expected given his larger size; the reverse was true on a mass-specific basis. There was also considerable variability in RMR for each walrus during the year that could not be accounted for by changes in body mass. Metabolism while swimming was about twice RMR, and locomotor costs were higher than generally predicted for other marine mammals. The lower calculated swimming efficiency may reflect the fact that walruses are not “high velocity” pursuit predators. The estimates of metabolic expenditure obtained in this study for young walruses are invaluable for quantifying the energetic consequences of behavioral changes induced by environmental shifts in the wild.

keywords     bioenergetics, metabolism, swimming, walrus
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The effect of food restriction on growth rates in Steller sea lions, Eumetopias jubatus.
Rosen, D.A.S. 2021.
Marine Mammal Science 37:1524-1530.
abstract
This study quantified the effect of changes in prey intake on the growth of individual Steller sea lions. Data from 12 female sea lions subject to various experimental episodes of restricted food intake were used to produce an overall model predicting changes in growth rates from different levels of unpredicted reductions in energy intake. The resulting equation was robust across different types and levels of restriction, seasons, and age classes. This predictive relationship between changes in food intake and growth is invaluable for incorporating into bioenergetic models estimating the effects of environmental changes on wild Steller sea lions.

keywords     Steller sea lion, food intake, growth, body mass, energy intake, bioenergetics
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Seasonal and developmental patterns of energy intake and growth in Alaskan ice seals.
Rosen, D.A.S., N.M. Thometz and C. Reichmuth. 2021.
Aquatic Mammals 47(6):559-573.
abstract
Quantifying the energy needs of individual animals and understanding the relationship between food intake and physical growth are necessary to determine species-level food requirements and model potential responses to changing environmental conditions. To provide fine-scale information about developmental and seasonal patterns in the energetic requirements of Arctic phocid seals, we documented longitudinal changes in food intake, body mass, and standard length in four spotted seals (Phoca largha), three ringed seals (Pusa hispida), and two bearded seals (Erignathus barbatus). The seals were studied for up to 9 years in sub-Arctic and/or temperate climates while living under human care. Seals were fed using behavioral criteria that allowed their food intake and body mass to vary naturally. Gross energy intake (GEI) increased with age in all species, reaching a plateau as seals matured. GEI was greatest for the largest species (bearded seals) and lowest for the smallest (ringed seals). Mass-specific GEI declined with age, and was similar between spotted and ringed seals, with bearded seals consuming about half that of the smaller species. Overlaid upon long-term developmental changes were predictable seasonal cycles in food intake and body mass which became more pronounced as seals matured. Seasonal cycles in food intake and body mass did not always reflect simple cause-and-effect relationships. For example, seasonal peaks in food intake were regularly associated with simultaneous declines in body mass. The consistency of energy intake patterns, despite seals being maintained in semi-artificial conditions in different local climates, supports the hypothesis that seasonal oscillations are guided by underlying hormonal changes linked to key life history events and mediated by the physical environment. The described physiological patterns serve to highlight times of year when free-ranging Arctic seals may be more sensitive to environmental perturbations.

keywords     Phoca largha, Pusa hispida, Erignathus barbatus, food intake, caloric intake, body mass, growth, development, environmental conditions, nutrition
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Southern resident killer whales encounter higher prey densities than northern resident killer whales during summer.
Sato, M., A.W. Trites and S. Gauthier. 2021.
Canadian Journal of Fisheries and Aquatic Sciences, dx.doi.org/10.1139/cjfas-2020-0445
abstract
The decline of southern resident killer whales may be due to a shortage of prey, but there is little data to test this hypothesis. We compared the availability of prey (Chinook salmon) sought by southern residents in Juan de Fuca Strait during summer with the abundance and distribution of Chinook available to the much larger and growing population of northern resident killer whales feeding in Johnstone Strait. We used ship-based multifrequency echosounders to identify differences in prey fields that may explain the dynamics of these two killer whale populations. Contrary to expectations, we found that both killer whale habitats had patchy distributions of prey that did not differ in their frequencies of occurrence, nor in the size compositions of individual fish. However, the density of fish within each patch was 4-6 times higher in the southern resident killer whale habitat. These findings do not support the hypothesis that southern resident killer whales are experiencing a prey shortage in the Salish Sea during summer and suggest a combination of other factors is affecting overall foraging success.
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Pacific great blue herons consume thousands of juvenile salmon.
Sherker, Z.T., K. Pellett, J. Atkinson, J. Damborg and A.W. Trites. 2021.
Canadian Journal of Zoology 99:349-361.
abstract
An array of predators that consume juvenile salmon may account for the poor returns of adult salmon to the Salish Sea. However, the Pacific great blue heron (Ardea herodias fannini) is rarely listed among the known salmon predators, despite being regularly seen near salmon streams. Investigating heron predation by scanning nesting sites within 35 km of three British Columbia rivers for fecal remains containing Passive Integrated Transponder (PIT) tags implanted in >100,000 juvenile salmon from 2008-2018 yielded 1,205 tags, representing a minimum annual predation rate of 0.3-1.3% of all juvenile salmon. Most of this predation (99%) was caused by ~420 adult herons from three heronries. Correcting for tags defecated outside of the heronry raised the predation rates to 0.7-3.2%-and was as high as 6% during a year of low river flow. Predation occurs during chick-rearing in late spring, and accounts for 4.1-8.4% of the heron chick diet. Smaller salmon smolts were significantly more susceptible to heron predation than larger conspecifics. The proximity of heronries relative to salmon bearing rivers is likely a good predictor of heron predation on local salmon runs, and can be monitored to assess coast-wide effects of great blue herons on salmon recovery.

keywords     predation, salmon, smolts, herons, chicks, diet
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Cardiac examinations of anesthetized Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus), and a walrus (Odobenus rosmarus).
Storlund, R.L., D.A.S. Rosen, M. Margiocco, M. Haulena and A.W. Trites. 2021.
Journal of Zoo and Wildlife Medicine 52(2):507-519.
abstract
Pinniped hearts have been well described via dissection, but in vivo measurements of cardiac structure, function, and electrophysiology are lacking. Electrocardiograms (ECGs) were recorded under anesthesia from 8 Steller sea lions (Eumetopias jubatus), 5 northern fur seals (Callorhinus ursinus), and 1 walrus (Odobenus rosmarus) to investigate cardiac electrophysiology in pinnipeds. In addition, echocardiograms were performed on all 8 anesthetized Steller sea lions to evaluate in vivo cardiac structure and function. Measured and calculated ECG parameters included P‑wave, PQ, QRS, and QT interval durations, P‑, R‑, and T‑wave amplitudes, P‑ and T‑wave polarities, and the mean electrical axis (MEA). Measured and calculated echocardiographic parameters included left ventricular internal diameter, interventricular septum thickness, and left ventricular posterior wall thickness in systole and diastole (using M-mode), left atrium and aortic root dimensions (using 2D), and maximum aortic and pulmonary flow velocities (using pulsed wave spectral Doppler). ECG measurements were similar to those reported for other pinniped species, but there was considerable variation in the MEAs of Steller sea lions and northern fur seals. Echocardiographic measurements were similar to those reported for southern sea lions (Otaria flavenscens), including 5 out of 8 Steller sea lions having a left atrial to aortic root ratio < 1, which may indicate that they have an enlarged aortic root compared to awake terrestrial mammals. Isoflurane anesthesia likely affected some of the measurements as evidenced by the reduced fractional shortening found in Steller sea lions compared to awake terrestrial mammals. The values reported are useful reference points for assessing cardiac health in pinnipeds under human care.
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Electrocardiographic scaling reveals differences in electrocardiogram interval durations between marine and terrestrial mammals.
Storlund, R.L., D.A.S. Rosen and A.W. Trites. 2021.
Frontiers in Physiology 12:690029
abstract
Although the ability of marine mammals to lower heart rates for extended periods when diving is well documented, it is unclear whether marine mammals have electrophysiological adaptations that extend beyond overall bradycardia. We analyzed electrocardiographic data from 50 species of terrestrial mammals and 19 species of marine mammals to determine whether the electrical activity of the heart differs between these two groups of mammals. We also tested whether physiological state (i.e., anesthetized or conscious) affects electrocardiogram (ECG) parameters. Analyses of ECG waveform morphology (heart rate, P-wave duration, and PQ, PR, QRS, and QT intervals) revealed allometric relationships between body mass and all ECG intervals (as well as heart rate) for both groups of mammals and specific differences in ECG parameters between marine mammals and their terrestrial counterparts. Model outputs indicated that marine mammals had 19% longer P-waves, 24% longer QRS intervals, and 21% shorter QT intervals. In other words, marine mammals had slower atrial and ventricular depolarization, and faster ventricular repolarization than terrestrial mammals. Heart rates and PR intervals were not significantly different between marine and terrestrial mammals, and physiological state did not significantly affect any ECG parameter. On average, ECG interval durations of marine and terrestrial mammals scaled with body mass to the power of 0.21 (range: 0.19 - 0.23) rather than the expected 0.25—while heart rate scaled with body mass to the power of -0.22 and was greater than the widely accepted -0.25 derived from fractal geometry. Our findings show clear differences between the hearts of terrestrial and marine mammals in terms of cardiac timing that extend beyond diving bradycardia. They also highlight the importance of considering special adaptations (such as breath-hold diving) when analyzing allometric relationships.

keywords     ECG, electrocardiogram, marine mammal, heart rate, anesthesia, allometry, cardiac timing, comparative electrophysiology
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Molting strategies of Arctic seals drive annual patterns in metabolism.
Thometz, N.M., H. Hermann-Sorensen, B. Russell, D.A.S. Rosen and C. Reichmuth. 2021.
Conservation Physiology coaa112
abstract
Arctic seals, including spotted (Phoca largha), ringed (Pusa hispida), and bearded (Erignathus barbatus) seals, are directly affected by sea ice loss. These species use sea ice as a haul-out substrate for various critical functions, including their annual molt. Continued environmental warming will inevitably alter the routine behavior and overall energy budgets of Arctic seals, but it is difficult to quantify these impacts as their metabolic requirements are not well known—due in part to the difficulty of studying wild individuals. Thus, data pertaining to species-specific energy demands is urgently needed to better understand the physiological consequences of rapid environmental change. We used open-flow respirometry over a four-year period to track fine-scale, longitudinal changes in the resting metabolic rate (RMR) of four spotted, three ringed, and one bearded seal trained to participate in research. Simultaneously, we collected complementary physiological and environmental data. Species-specific metabolic demands followed expected patterns based on body size, with the largest species, the bearded seal, exhibiting the highest absolute RMR (0.48±0.04 L O2 min-1) and the lowest mass-specific RMR (4.10±0.47 ml O2 min-1 kg-1), followed by spotted (absolute: 0.33±0.07 L O2 min-1; mass-specific: 6.13±0.73 ml O2 min-1 kg-1) and ringed (absolute: 0.20±0.04 L O2 min-1; mass-specific: 7.01±1.38 ml O2 min-1 kg-1) seals. Further, we observed clear and consistent annual patterns in RMR that related to the distinct molting strategies of each species. For species that molted over relatively short intervals—spotted (33±4 days) and ringed (28±6 days) seals—metabolic demands increased markedly in association with molt. In contrast, the bearded seal exhibited a prolonged molting strategy (119±2 days), which appeared to limit the overall cost of molting as indicated by a relatively stable annual RMR. These findings highlight energetic trade-offs associated with different molting strategies and provide quantitative data that can be used to assess species-specific vulnerabilities to changing conditions.

keywords     Arctic seals, spotted seal, ringed seal, bearded seal, sea ice, molt, climate change, respirometry, resting metabolic rate, energetic trade-offs
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Behavioral insights into the decline and natural history of Steller sea lions.
Trites, A.W. 2021.
In C. Campagna and R.G. Harcourt (eds), Ethology and behavioral ecology of otariids and the odobenid. Springer, Cham, Switzerland. pp. 489-519.
abstract
Two competing hypotheses were proposed to explain why Steller sea lions had declined in the Gulf of Alaska, Bering Sea and Aleutian Islands. One of the theories was that young sea lions were starving because fisheries had reduced the abundance of groundfish-the overfishing hypothesis. The other was that these low-fat species of fish had increased in abundance as the sea lion population declined following the 1976-1977 oceanic regime shift, and were compromising sea lion reproductive and survival rates-the junk-food hypothesis. Behavioral ecologists tested these hypotheses by comparing sea lion behaviors in the declining region (Gulf of Alaska and Aleutian Islands) with sea lion behaviors in an increasing region (Southeast Alaska) to determine whether the populations exhibited behavioral differences consistent with food shortages. These studies involved comparing dive depths, dive durations, time spent foraging, and time spent nursing by regions and seasons. Research also focused on weaning-a critical life-history stage-to determine when and how it occurs. Collectively, these observations and measures of behavioral responses revealed that most dependent young begin supplementing their milk diet with fish between April and May, and wean just before the start of the upcoming June breeding season. However, the proportion of young sea lions that wean at 1, 2 or 3 years of age appears to vary by year due to regional and temporal differences in the quantity and quality of prey available to them once weaned. None of the behavioral studies of adult and juvenile Steller sea lions supported the overfishing hypothesis-but were, instead, consistent with the junk-food hypothesis. It appears that lactating females that consume large amounts of low-energy fish (such as walleye pollock and Pacific cod) have a high probability of miscarriage, and will keep their dependent young for an extra one or two years-thereby causing birth rates and population size to decline. In contrast, lactating females that consume larger amounts of fattier fish (such as sand lance and Pacific herring) can successfully wean a pup every year. Plasticity in age at weaning appears to be an evolutionary adaptation to natural shifts in community prey structure in the North Pacific Ocean-and is an adaptation that successfully slows population declines of Steller sea lions until the ocean shifts to an alternative state containing greater portions of energy-rich fish that allows sea lion numbers to increase again.

keywords     Eumetopias jubatus, Life history, Population decline,Endangered, Maternal strategies, Phenology,Weaning, Abortions, Breeding, Junk food, Overfishing,Regime shifts
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Behavioral context of echolocation and prey-handling sounds produced by killer whales (Orcinus orcas) during pursuit and capture of Pacific salmon (Oncorhynchus spp.).
Wright, B. M., V. B. Deecke, G. M. Ellis, A. W. Trites and J. K. B. Ford. 2021.
Marine Mammal Science 37:1428-1453.
abstract
Availability of preferred salmonid prey and a sufficiently quiet acoustic environment in which to forage are critical to the survival of resident killer whales (Orcinus orcas) in the northeastern Pacific. Although piscivorous killer whales rely on echolocation to locate and track prey, the relationship between echolocation, movement, and prey capture during foraging by wild individuals is poorly understood. We used acoustic biologging tags to relate echolocation behavior to prey pursuit and capture during successful feeding dives by fish-eating killer whales in coastal British Columbia, Canada. The significantly higher incidence and rate of echolocation prior to fish captures compared to afterward confirms its importance in prey detection and tracking. Extremely rapid click sequences (buzzes) were produced before or concurrent with captures of salmon at depths typically exceeding 50 m, and were likely used by killer whales for close-range prey targeting, as in other odontocetes. Distinctive crunching and tearing sounds indicative of prey-handling behavior occurred at relatively shallow depths following fish captures, matching concurrent observations that whales surfaced with fish prior to consumption and often shared prey. Buzzes and prey-handling sounds are potentially useful acoustic signals for estimating foraging efficiency and determining if resident killer whales are meeting their energetic requirements.

keywords     biologging tag, echolocation, foraging behavior, killer whale, Orcinus orca, prey handling, salmon predation
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