Ari S. Friedlaender

Key Questions in Marine Megafauna Movement Ecology

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

Integrative Approaches to the Study of Baleen Whale Diving Behavior, Feeding Performance, and Foraging Ecology

For many marine organisms, especially large whales that cannot be studied in laboratory settings, our ability to obtain basic behavioral and physiological data is limited, because these organisms occupy offshore habitats and spend a majority of their time underwater. A class of multisensor, suction-cup-attached archival tags has revolutionized the study of large baleen whales, particularly with respect to the predatory strategies used by these gigantic bulk filter feeders to exploit abundant oceanic resources. By integrating these data with those from other disciplines, researchers have uncovered a diverse and extraordinary set of underwater behaviors, ranging from acrobatic diving maneuvers to extreme feeding events during which whales engulf volumes of prey-laden water that are much larger than their own body. This research framework not only improves our knowledge of the individual performance and behavior of these keystone predators but also informs our ability to understand the dynamics of complex marine ecosystems.

Prey density and distribution drive the three‐dimensional foraging strategies of the largest filter feeder

Summary Despite their importance in determining the rate of both energy gain and expenditure, how the fine-scale kinematics of foraging are modified in response to changes in prey abundance and distribution remain poorly understood in many animal ecosystems. In the marine environment, bulk-filter feeders rely on dense aggregations of prey for energetically efficient foraging. Rorqual whales (Balaenopteridae) exhibit a unique form of filter feeding called lunge feeding, a process whereby discrete volumes of prey-laden water are intermittently engulfed and filtered. In many large rorqual species the size of engulfed water mass is commensurate with the whales body size, yet is engulfed in just a few seconds. This filter-feeding mode thus requires precise coordination of the body and enlarged engulfment apparatus to maximize capture efficiency. Previous studies from whale-borne tags revealed that many rorqual species perform rolling behaviours when foraging. It has been hypothesized that such acrobatic manoeuvres may be required for efficient prey capture when prey manifest in small discrete patches, but to date there has been no comprehensive analysis of prey patch characteristics during lunge feeding events. We developed a null hypothesis that blue whale kinematics are independent of prey patch characteristics. To test this hypothesis, we investigated the foraging performance of blue whales, the largest filter-feeding predator and their functional response to variability in their sole prey source, krill using a generalized additive mixed model framework. We used a combination of animal-borne movement sensors and hydroacoustic prey mapping to simultaneously quantify the three-dimensional foraging kinematics of blue whales (Balaenoptera musculus) and the characteristics of targeted krill patches. Our analyses rejected our null hypothesis, showing that blue whales performed more acrobatic manoeuvres, including 180° and 360° rolling lunges, when foraging on low-density krill patches. In contrast, whales targeting high-density krill patches involved less manoeuvring during lunges and higher lunge feeding rates. These data demonstrate that blue whales exhibit a range of adaptive foraging strategies that maximize prey capture in different ecological contexts. Because first principles indicate that manoeuvres require more energy compared with straight trajectories, our data reveal a previously unrecognized level of complexity in predator–prey interactions that are not accounted for in optimal foraging and energetic efficiency models.

Blue whales (Balaenoptera musculus) optimize foraging efficiency by balancing oxygen use and energy gain as a function of prey density

The world’s largest predators, blue whales, switch strategies to maximize foraging efficiency as a function of prey density and depth. Terrestrial predators can modulate the energy used for prey capture to maximize efficiency, but diving animals face the conflicting metabolic demands of energy intake and the minimization of oxygen depletion during a breath hold. It is thought that diving predators optimize their foraging success when oxygen use and energy gain act as competing currencies, but this hypothesis has not been rigorously tested because it has been difficult to measure the quality of prey that is targeted by free-ranging animals. We used high-resolution multisensor digital tags attached to foraging blue whales (Balaenoptera musculus) with concurrent acoustic prey measurements to quantify foraging performance across depth and prey density gradients. We parameterized two competing physiological models to estimate energy gain and expenditure based on foraging decisions. Our analyses show that at low prey densities, blue whale feeding rates and energy intake were low to minimize oxygen use, but at higher prey densities feeding frequency increased to maximize energy intake. Contrary to previous paradigms, we demonstrate that blue whales are not indiscriminate grazers but instead switch foraging strategies in response to variation in prey density and depth to maximize energetic efficiency.

Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis)

Body size and feeding mode are two fundamental characteristics that determine foraging performance and ecological niche. As the smallest obligate lunge filter feeders, minke whales represent an ideal system for studying the physical and energetic limits of filter feeding in endotherms. We used multi-sensor suction cup tags to quantify the feeding performance of Antarctic minke whales. Foraging dives around and beneath sea ice contained up to 24 lunges per dive, the highest feeding rates for any lunge-feeding whale. Their small size allows minke whales access to krill in sea-ice environments not easily accessible to larger baleen whales. Furthermore, their ability to filter feed provides an advantage over other smaller sympatric krill predators such as penguins and seals that feed on individual prey. The unique combination of body size, feeding mechanism and sea-ice habitat of Antarctic minke whales defines a previously undocumented energetic niche that is unique among aquatic vertebrates.

Using accelerometers to determine the calling behavior of tagged baleen whales

Low-frequency acoustic signals generated by baleen whales can propagate over vast distances, making the assignment of calls to specific individuals problematic. Here, we report the novel use of acoustic recording tags equipped with high-resolution accelerometers to detect vibrations from the surface of two tagged fin whales that directly match the timing of recorded acoustic signals. A tag deployed on a buoy in the vicinity of calling fin whales and a recording from a tag that had just fallen off a whale were able to detect calls acoustically but did not record corresponding accelerometer signals that were measured on calling individuals. Across the hundreds of calls measured on two tagged fin whales, the accelerometer response was generally anisotropic across all three axes, appeared to depend on tag placement and increased with the level of received sound. These data demonstrate that high-sample rate accelerometry can provide important insights into the acoustic behavior of baleen whales that communicate at low frequencies. This method helps identify vocalizing whales, which in turn enables the quantification of call rates, a fundamental component of models used to estimate baleen whale abundance and distribution from passive acoustic monitoring.

Evidence for ship noise impacts on humpback whale foraging behaviour

Noise from shipping activity in North Atlantic coastal waters has been steadily increasing and is an area of growing conservation concern, as it has the potential to disrupt the behaviour of marine organisms. This study examines the impacts of ship noise on bottom foraging humpback whales (Megaptera novaeangliae) in the western North Atlantic. Data were collected from 10 foraging whales using non-invasive archival tags that simultaneously recorded underwater movements and the acoustic environment at the whale. Using mixed models, we assess the effects of ship noise on seven parameters of their feeding behaviours. Independent variables included the presence or absence of ship noise and the received level of ship noise at the whale. We found significant effects on foraging, including slower descent rates and fewer side-roll feeding events per dive with increasing ship noise. During 5 of 18 ship passages, dives without side-rolls were observed. These findings indicate that humpback whales on Stellwagen Bank, an area with chronically elevated levels of shipping traffic, significantly change foraging activity when exposed to high levels of ship noise. This measureable reduction in within-dive foraging effort of individual whales could potentially lead to population-level impacts of shipping noise on baleen whale foraging success.

Studying cetacean behaviour: new technological approaches and conservation applications

Animal behaviour can provide valuable information for wildlife management and conservation. Studying the detailed behaviour of marine mammals involves challenges not faced by most animal behaviour researchers due to the size, mobility and lack of continuous visibility of these animals. We describe several methods developed by marine mammal scientists to study behaviour, primarily of cetaceans, focusing on technological advances: unmanned aerial systems (UAS), satellite-linked telemetry, passive acoustics and multisensor high-resolution acoustic recording tags. We then go on to explain how the data collected by these methods have contributed to and informed conservation actions. We focus on examples including: satellite data informing the interactions between cetaceans and offshore oil and gas development; passive acoustics used to track distributions of several species of cetaceans, including their movements near shipping lanes; and high-resolution acoustic recording tags used to document responses of cetaceans to anthropogenic activities. Finally, we discuss recent efforts to link animal behaviour to individual fitness and, particularly for behavioural disturbances, to population-level consequences, which can be helpful for informing conservation efforts. The infusion of technological advancements into studies of cetacean behaviour combined with emerging analytical techniques brings us to the next 20+ years of studying these animals. These developments will improve our capabilities in areas such as testing whether their behaviour adheres to traditional behavioural theory, and will certainly assist the guiding of conservation efforts.

Mysterious bio-duck sound attributed to the Antarctic minke whale (Balaenoptera bonaerensis)

For decades, the bio-duck sound has been recorded in the Southern Ocean, but the animal producing it has remained a mystery. Heard mainly during austral winter in the Southern Ocean, this ubiquitous sound has been recorded in Antarctic waters and contemporaneously off the Australian west coast. Here, we present conclusive evidence that the bio-duck sound is produced by Antarctic minke whales (Balaenoptera bonaerensis). We analysed data from multi-sensor acoustic recording tags that included intense bio-duck sounds as well as singular downsweeps that have previously been attributed to this species. This finding allows the interpretation of a wealth of long-term acoustic recordings for this previously acoustically concealed species, which will improve our understanding of the distribution, abundance and behaviour of Antarctic minke whales. This is critical information for a species that inhabits a difficult to access sea-ice environment that is changing rapidly in some regions and has been the subject of contentious lethal sampling efforts and ongoing international legal action.

A multivariate mixed hidden Markov model for blue whale behaviour and responses to sound exposure

A MULTIVARIATE MIXED HIDDEN MARKOV MODEL FOR BLUE WHALE BEHAVIOUR AND RESPONSES TO SOUND EXPOSURE1 BY STACY L. DERUITER∗,†, ROLAND LANGROCK‡,†, TOMAS SKIRBUTAS†, JEREMY A. GOLDBOGEN§, JOHN CALAMBOKIDIS¶, ARI S. FRIEDLAENDER‖,∗∗ AND BRANDON L. SOUTHALL∗∗ Calvin College∗, University of St Andrews†, Bielefeld University‡, Stanford University§, Cascadia Research Collective¶, Oregon State University‖ and SEA, Inc.∗∗