Rorqual whale (Balaenopteridae) surface lunge‐feeding behaviors: Standardized classification,repertoire diversity,and evolutionary analyses

Rorqual whales (Family: Balaenopteridae) are the world's largest predators and sometimes feed near or at the sea surface on small schooling prey. Most rorquals capture prey using a behavioral process known as lunge‐feeding that, when occurring at the surface, often exposes the mouth and head above the water. New technology has recently improved historical misconceptions about the natural variation in rorqual lunge‐feeding behavior yet missing from the literature is a dedicated study of the identification, use, and evolution of these behaviors when used to capture prey at the surface. Here we present results from a long‐term investigation of three rorqual whale species (minke whale, Balaenoptera acutorostrata; fin whale, B. physalus; and blue whale, B. musculus) that helped us develop a standardized classification system of surface lunge‐feeding (SLF) behaviors. We then tested for differences in frequency of these behaviors among the three species and across all rorqual species. Our results: (1) propose a unified classification system of six homologous SLF behaviors used by all living rorqual whale species; (2) demonstrate statistically significant differences in the frequency of each behavior by minke, fin, and blue whales; and (3) provide new information regarding the evolution of lunge‐feeding behaviors among rorqual whales.     

Shallow and deep lunge feeding of humpback whales in fjords of the West Antarctic Peninsula

Humpback whales (Megaptera novaeangliae) belong to the class of marine mammals known as rorquals that feed through extraordinarily energetic lunges during which they engulf large volumes of water equal to as much as 70% of their body mass. To understand the kinematics of humpback lunge feeding, we attached high‐resolution digital recording tags incorporating accelerometers, magnetometers, pressure and sound recording to whales feeding on euphausiids in fjords of the West Antarctic Peninsula. Instances of near vertical lunges gave us the unique opportunity to use the signal from the accelerometer to obtain a fine scale record of the body accelerations involved in lunging. We found that lunges contain extreme accelerations reaching 2.5 m/s² in certain instances, which are then followed by decelerations. When animals are intensively feeding the inter‐lunge interval is similar for both deep and shallow lunges suggesting a biomechanical constraint on lunges. However, the number of lunges per dive varies from one for shallow feeding (<25 m) to a median of six for deeper dives. Different feeding patterns were evident in the kinematic record, for deep and shallow feeding bouts with the much greater mean turn rates occurring in shallow feeding.     

Development of an automated method of detecting stereotyped feeding events in multisensor data from tagged rorqual whales

The introduction of animal‐borne, multisensor tags has opened up many opportunities for ecological research, making previously inaccessible species and behaviors observable. The advancement of tag technology and the increasingly widespread use of bio‐logging tags are leading to large volumes of sometimes extremely detailed data. With the increasing quantity and duration of tag deployments, a set of tools needs to be developed to aid in facilitating and standardizing the analysis of movement sensor data. Here, we developed an observation‐based decision tree method to detect feeding events in data from multisensor movement tags attached to fin whales (Balaenoptera physalus). Fin whales exhibit an energetically costly and kinematically complex foraging behavior called lunge feeding, an intermittent ram filtration mechanism. Using this automated system, we identified feeding lunges in 19 fin whales tagged with multisensor tags, during a total of over 100 h of continuously sampled data. Using movement sensor and hydrophone data, the automated lunge detector correctly identified an average of 92.8% of all lunges, with a false‐positive rate of 9.5%. The strong performance of our automated feeding detector demonstrates an effective, straightforward method of activity identification in animal‐borne movement tag data. Our method employs a detection algorithm that utilizes a hierarchy of simple thresholds based on knowledge of observed features of feeding behavior, a technique that is readily modifiable to fit a variety of species and behaviors. Using automated methods to detect behavioral events in tag records will significantly decrease data analysis time and aid in standardizing analysis methods, crucial objectives with the rapidly increasing quantity and variety of on‐animal tag data. Furthermore, our results have implications for next‐generation tag design, especially long‐term tags that can be outfitted with on‐board processing algorithms that automatically detect kinematic events and transmit ethograms via acoustic or satellite telemetry.     

Characteristics of Plantar Loads in Maximum Forward Lunge Tasks in Badminton

Background

Badminton players often perform powerful and long-distance lunges during such competitive matches. The objective of this study is to compare the plantar loads of three one-step maximum forward lunges in badminton.

Methods

Fifteen right-handed male badminton players participated in the study. Each participant performed five successful maximum lunges at three directions. For each direction, the participant wore three different shoe brands. Plantar loading, including peak pressure, maximum force, and contact area, was measured by using an insole pressure measurement system. Two-way ANOVA with repeated measures was employed to determine the effects of the different lunge directions and different shoes, as well as the interaction of these two variables, on the measurements.

Results

The maximum force (MF) on the lateral midfoot was lower when performing left-forward lunges than when performing front-forward lunges (p = 0.006, 95% CI = −2.88 to −0.04%BW). The MF and peak pressures (PP) on the great toe region were lower for the front-forward lunge than for the right-forward lunge (MF, p = 0.047, 95% CI = −3.62 to −0.02%BW; PP, p = 0.048, 95% CI = −37.63 to −0.16 KPa) and left-forward lunge (MF, p = 0.015, 95% CI = −4.39 to −0.38%BW; PP, p = 0.008, 95% CI = −47.76 to −5.91 KPa).

Conclusions

These findings indicate that compared with the front-forward lunge, left and right maximum forward lunges induce greater plantar loads on the great toe region of the dominant leg of badminton players. The differences in the plantar loads of the different lunge directions may be potential risks for injuries to the lower extremities of badminton players.     

Underwater acrobatics by the world's largest predator: 360° rolling manoeuvres by lunge-feeding blue whales

The extreme body size of blue whales requires a high energy intake and therefore demands efficient foraging strategies. As an obligate lunge feeder on aggregations of small zooplankton, blue whales engulf a large volume of prey-laden water in a single, rapid gulp. The efficiency of this feeding mechanism is strongly dependent on the amount of prey that can be captured during each lunge, yet food resources tend to be patchily distributed in both space and time. Here, we measured the three-dimensional kinematics and foraging behaviour of blue whales feeding on krill, using suction-cup attached multi-sensor tags. Our analyses revealed 360° rolling lunge-feeding manoeuvres that reorient the body and position the lower jaws so that a krill patch can be engulfed with the whale''s body inverted. We also recorded these rolling behaviours when whales were in a searching mode in between lunges, suggesting that this behaviour also enables the whale to visually process the prey field and maximize foraging efficiency by surveying for the densest prey aggregations. These results reveal the complex manoeuvrability that is required for large rorqual whales to exploit prey patches and highlight the need to fully understand the three-dimensional interactions between predator and prey in the natural environment.     

Scaling of lunge feeding in rorqual whales: An integrated model of engulfment duration

Rorqual whales (Balaenopteridae) obtain their food by lunge feeding, a dynamic process that involves the intermittent engulfment and filtering of large amounts of water and prey. During a lunge, whales accelerate to high speed and open their mouth wide, thereby exposing a highly distensible buccal cavity to the flow and facilitating its inflation. Unsteady hydrodynamic models suggest that the muscles associated with the ventral groove blubber undergo eccentric contraction in order to stiffen and control the inflation of the buccal cavity; in doing so the engulfed water mass is accelerated forward as the whale’s body slows down. Although the basic mechanics of lunge feeding are relatively well known, the scaling of this process remains poorly understood, particularly with regards to its duration (from mouth opening to closure). Here we formulate a new theory of engulfment time which integrates prey escape behavior with the mechanics of the whale’s body, including lunge speed and acceleration, gape angle dynamics, and the controlled inflation of the buccal cavity. Given that the complex interaction between these factors must be highly coordinated in order to maximize engulfment volume, the proposed formulation rests on the scenario of Synchronized Engulfment, whereby the filling of the cavity (posterior to the temporomandibular joint) coincides with the moment of maximum gape. When formulated specifically for large rorquals feeding on krill, our analysis predicts that engulfment time increases with body size, but in amounts dictated by the specifics of krill escape and avoidance kinematics. The predictions generated by the model are corroborated by limited empirical data on a species-specific basis, particularly for humpback and blue whales chasing krill. A sensitivity analysis applied to all possible sized fin whales also suggests that engulfment duration and lunge speed will increase intra-specifically with body size under a wide range of predator-prey scenarios. This study provides the theoretical framework required to estimate the scaling of the mass-specific drag being generated during engulfment, as well as the energy expenditures incurred.     

Prey capture attempts can be detected in Steller sea lions and other marine predators using accelerometers

We attached accelerometers to the head and jaw of a Steller sea lion (Eumetopias jubatus) to determine whether feeding attempts in a controlled setting could be quantified by acceleration features characteristic of head and jaw movements. Most of the 19 experimental feeding events that occurred during the 51 dives recorded resulted in specific acceleration patterns that were clearly distinguishable from swimming accelerations. The differential acceleration between the head-mounted and jaw-mounted accelerometers detected 84% of prey captures on the vertical axis and 89% on the horizontal axis. However, the jaw-mounted accelerometer alone proved to be equally effective at detecting prey capture attempts. Acceleration along the horizontal (surge)-axis appeared to be particularly efficient in detecting prey captures, and suggests that a single accelerometer placed under the jaw of a pinniped is a promising and easily implemented means of recording prey capture attempts.     

An approximate simulation model for initial luge track design

Competitive and recreational sport on artificial ice tracks has grown in popularity. For track design one needs knowledge of the expected speed and acceleration of the luge on the ice track. The purpose of this study was to develop an approximate simulation model for luge in order to support the initial design of new ice tracks. Forces considered were weight, drag, friction, and surface reaction force. The trajectory of the luge on the ice track was estimated using a quasi-static force balance and a 1d equation of motion was solved along that trajectory. The drag area and the coefficient of friction for two runs were determined by parameter identification using split times of five sections of the Whistler Olympic ice track. The values obtained agreed with experimental data from ice friction and wind tunnel measurements. To validate the ability of the model to predict speed and accelerations normal to the track surface, a luge was equipped with an accelerometer to record the normal acceleration during the entire run. Simulated and measured normal accelerations agreed well. In a parameter study the vertical drop and the individual turn radii turned out to be the main variables that determine speed and acceleration. Thus the safety of a new ice track is mainly ensured in the planning phase, in which the use of a simulation model similar to this is essential.     

A comparison of techniques for classifying behavior from accelerometers for two species of seabird

The behavior of many wild animals remains a mystery, as it is difficult to quantify behavior of species that cannot be easily followed throughout their daily or seasonal movements. Accelerometers can solve some of these mysteries, as they collect activity data at a high temporal resolution (<1 s), can be relatively small (<1 g) so they minimally disrupt behavior, and are increasingly capable of recording data for long periods. Nonetheless, there is a need for increased validation of methods to classify animal behavior from accelerometers to promote widespread adoption of this technology in ecology. We assessed the accuracy of six different behavioral assignment methods for two species of seabird, thick‐billed murres (Uria lomvia) and black‐legged kittiwakes (Rissa tridactyla). We identified three behaviors using tri‐axial accelerometers: standing, swimming, and flying, after classifying diving using a pressure sensor for murres. We evaluated six classification methods relative to independent classifications from concurrent GPS tracking data. We used four variables for classification: depth, wing beat frequency, pitch, and dynamic acceleration. Average accuracy for all methods was >98% for murres, and 89% and 93% for kittiwakes during incubation and chick rearing, respectively. Variable selection showed that classification accuracy did not improve with more than two (kittiwakes) or three (murres) variables. We conclude that simple methods of behavioral classification can be as accurate for classifying basic behaviors as more complex approaches, and that identifying suitable accelerometer metrics is more important than using a particular classification method when the objective is to develop a daily activity or energy budget. Highly accurate daily activity budgets can be generated from accelerometer data using multiple methods and a small number of accelerometer metrics; therefore, identifying a suitable behavioral classification method should not be a barrier to using accelerometers in studies of seabird behavior and ecology.     

Incorporating tides into the acoustic ecology of humpback whales

North Pacific humpback whales (Megaptera novaeangliae) migrate annually to foraging grounds in Southeast Alaska that are characterized by semidiurnal tidal cycles. Tidal activity is an important driver of marine mammal behavior on foraging grounds, but is often omitted in studies of acoustic ecology. To better understand the role of sound in this vocal species we investigated the influence of tidal height and direction on humpback whale nonsong calling behavior in Frederick Sound and described new call types for this population. The likelihood of detecting a call from the low‐frequency‐harmonic, pulsed, or noisy‐complex call classes was independent of tidal activity. The likelihood of detecting a call from the tonal call class, and a feeding call in particular, was 2.1 times higher during flood tides than during ebb tides (95% CI 1.1–4.4). This likely reflects an indirect relationship between humpback whale foraging and tides.     

The development of an intermediate‐duration tag to characterize the diving behavior of large whales

The development of high‐resolution archival tag technologies has revolutionized our understanding of diving behavior in marine taxa such as sharks, turtles, and seals during their wide‐ranging movements. However, similar applications for large whales have lagged behind due to the difficulty of keeping tags on the animals for extended periods of time. Here, we present a novel configuration of a transdermally attached biologging device called the Advanced Dive Behavior (ADB) tag. The ADB tag contains sensors that record hydrostatic pressure, three‐axis accelerometers, magnetometers, water temperature, and light level, all sampled at 1 Hz. The ADB tag also collects Fastloc GPS locations and can send dive summary data through Service Argos, while staying attached to a whale for typical periods of 3–7 weeks before releasing for recovery and subsequent data download. ADB tags were deployed on sperm whales (Physeter macrocephalus; N = 46), blue whales (Balaenoptera musculus; N = 8), and fin whales (B. physalus; N = 5) from 2007 to 2015, resulting in attachment durations from 0 to 49.6 days, and recording 31 to 2,539 GPS locations and 27 to 2,918 dives per deployment. Archived dive profiles matched well with published dive shapes of each species from short‐term records. For blue and fin whales, feeding lunges were detected using peaks in accelerometer data and matched corresponding vertical excursions in the depth record. In sperm whales, rapid orientation changes in the accelerometer data, often during the bottom phase of dives, were likely related to prey pursuit, representing a relative measure of foraging effort. Sperm whales were documented repeatedly diving to, and likely foraging along, the seafloor. Data from the temperature sensor described the vertical structure of the water column in all three species, extending from the surface to depths >1,600 m. In addition to providing information needed to construct multiweek time budgets, the ADB tag is well suited to studying the effects of anthropogenic sound on whales by allowing for pre‐ and post‐exposure monitoring of the whale's dive behavior. This tag begins to bridge the gap between existing long‐duration but low‐data throughput tags, and short‐duration, high‐resolution data loggers.     

Response of southern right whales to simulated swim‐with‐whale tourism at Península Valdés,Argentina

Guidelines for sustainable tourism involving swimming with large whales are not well‐developed compared to those focused on programs of swimming with delphinids. From September to November 2005 and August to September 2006, we collected behavioral and movement data for southern right whales (Eubalaena australis) exposed to interactions with boats and swimmers at Península Valdés, Argentina. Whales were tracked from shore using a theodolite before, during, and after a series of directed interactions with swimmers and a boat. Resting, socializing, and surface active behavior decreased, traveling increased, and whales swam faster and reoriented more often during interactions. Responses were variable by age/sex class, with mother/calf pairs showing strongest responses. Increased levels of tourism activity are a concern, as reduction in resting time and disruption of socialization among adults, juveniles, and mother/calf pairs have unknown long‐term consequences. Additional data should be collected for whale behavior in proposed tourism and nontourism areas to build a long‐term database which can be used to determine if reactions of whales change over time. Our data suggest that swimming with whales in Chubut Province should not be legalized until further investigations are completed, especially in light of the recent southern right whale die‐offs recorded in Península Valdés.     

Estimating the energy expenditure of free‐ranging polar bears using tri‐axial accelerometers: A validation with doubly labeled water

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free‐ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Although dynamic body acceleration has been shown to strongly correlate with oxygen consumption in captive animals, it has been validated in only a few studies on free‐ranging animals. Here, we use relationships between oxygen consumption and overall dynamic body acceleration in resting and walking polar bears Ursus maritimus and published values for the costs of swimming in polar bears to estimate the total energy expenditure of 6 free‐ranging polar bears that were primarily using the sea ice of the Beaufort Sea. Energetic models based on accelerometry were compared to models of energy expenditure on the same individuals derived from doubly labeled water methods. Accelerometer‐based estimates of energy expenditure on average predicted total energy expenditure to be 30% less than estimates derived from doubly labeled water. Nevertheless, accelerometer‐based measures of energy expenditure strongly correlated (r² = 0.70) with measures derived from doubly labeled water. Our findings highlight the strengths and limitations in dynamic body acceleration as a measure of total energy expenditure while also further supporting its use as a proxy for instantaneous, detailed energy expenditure in free‐ranging animals.     

'Megapclicks': acoustic click trains and buzzes produced during night-time foraging of humpback whales (Megaptera novaeangliae)

Humpback whales (Megaptera novaeangliae) exhibit a variety of foraging behaviours, but neither they nor any baleen whale are known to produce broadband clicks in association with feeding, as do many odontocetes. We recorded underwater behaviour of humpback whales in a northwest Atlantic feeding area using suction-cup attached, multi-sensor, acoustic tags (DTAGs). Here we describe the first recordings of click production associated with underwater lunges from baleen whales. Recordings of over 34000 'megapclicks' from two whales indicated relatively low received levels at the tag (between 143 and 154dB re 1 microPa pp), most energy below 2kHz, and interclick intervals often decreasing towards the end of click trains to form a buzz. All clicks were recorded during night-time hours. Sharp body rolls also occurred at the end of click bouts containing buzzes, suggesting feeding events. This acoustic behaviour seems to form part of a night-time feeding tactic for humpbacks and also expands the known acoustic repertoire of baleen whales in general.     

Octopamine in male aggression of Drosophila

BACKGROUND: In mammals and humans, noradrenaline is a key modulator of aggression. Octopamine, a closely related biogenic amine, has been proposed to have a similar function in arthropods. However, the effect of octopamine on aggressive behavior is little understood. RESULTS: An automated video analysis of aggression in male Drosophila has been developed, rendering aggression accessible to high-throughput studies. The software detects the lunge, a conspicuous behavioral act unique to aggression. In lunging, the aggressor rears up on his hind legs and snaps down on his opponent. By using the software to eliminate confounding effects, we now show that aggression is almost abolished in mutant males lacking octopamine. This suppression is independent of whether tyramine, the precursor of octopamine, is increased or also depleted. Restoring octopamine synthesis in the brain either throughout life or in adulthood leads to a partial rescue of aggression. Finally, neuronal silencing of octopaminergic and tyraminergic neurons almost completely abolishes lunges. CONCLUSIONS: Octopamine modulates Drosophila aggression. Genetically depleting the animal of octopamine downregulates lunge frequency without a sizable effect on the lunge motor program. This study provides access to the neuronal circuitry mediating this modulation.     

High genetic diversity in a small population: the case of Chilean blue whales

It is generally assumed that species with low population sizes have lower genetic diversities than larger populations and vice versa. However, this would not be the case for long‐lived species with long generation times, and which populations have declined due to anthropogenic effects, such as the blue whale (Balaenoptera musculus). This species was intensively decimated globally to near extinction during the 20th century. Along the Chilean coast, it is estimated that at least 4288 blue whales were hunted from an apparently pre‐exploitation population size (k) of a maximum of 6200 individuals (Southeastern Pacific). Thus, here, we describe the mtDNA (control region) and nDNA (microsatellites) diversities of the Chilean blue whale aggregation site in order to verify the expectation of low genetic diversity in small populations. We then compare our findings with other blue whale aggregations in the Southern Hemisphere. Interestingly, although the estimated population size is small compared with the pre‐whaling era, there is still considerable genetic diversity, even after the population crash, both in mitochondrial (N = 46) and nuclear (N = 52) markers (H_d = 0.890 and H_o = 0.692, respectively). Our results suggest that this diversity could be a consequence of the long generation times and the relatively short period of time elapsed since the end of whaling, which has been observed in other heavily‐exploited whale populations. The genetic variability of blue whales on their southern Chile feeding grounds was similar to that found in other Southern Hemisphere blue whale feeding grounds. Our phylogenetic analysis of mtDNA haplotypes does not show extensive differentiation of populations among Southern Hemisphere blue whale feeding grounds. The present study suggests that although levels of genetic diversity are frequently used as estimators of population health, these parameters depend on the biology of the species and should be taken into account in a monitoring framework study to obtain a more complete picture of the conservation status of a population.     

Hydrodynamic performance of the flippers of large‐bodied cetaceans in relation to locomotor ecology

Cetaceans evolved flippers that are unique in both size and shape probably due to selection pressures associated with foraging and body size. Flippers function as control surfaces for maneuverability and stability. Flippers of cetaceans and engineered hydrofoils are similar with streamlined cross‐sections and wing‐like planforms, which affect lift, drag and hydrodynamic efficiency. Scale models of the flippers from large‐bodied (body length > 6 m) cetaceans (fin whale, killer whale, sperm whale) were constructed from computed tomography (CT) scans of flippers. Flipper planforms were highly tapered for the fin whale, a rounded, paddle‐like design for the killer whale, and a square geometry for the sperm whale. Hydrodynamic properties of the models at varying angles of attack (?40º to 40^o) were determined in a water tunnel with a multi‐axis load cell. The flippers were found to have hydrodynamic characteristics similar to engineered wings. Differences in flipper morphology of large‐bodied cetaceans and their hydrodynamic performance are associated with the requirements of aquatic locomotion involved with ecology of the whales. The flippers of the killer whale provided the greatest maneuverability, whereas the flippers of the fin whale had low drag for lunging and the flippers of the sperm whale provided lift for diving.     

Cryptic speciation at organic‐rich marine habitats: a new bacteriovore annelid from whale‐fall and fish farms in the North‐East Atlantic

Vigtorniella ardabilia sp. nov. , a new chrysopetalid annelid, is described from a whale‐fall in Sweden and from sediment samples collected beneath fish farms in Norway. The new Vigtorniella species is morphologically almost identical to Vigtorniella flokati from whale‐falls in the Pacific Ocean, although molecular evidence from four genes shows that they are different species. Population genetic structure and phylogenetic relationships of V. ardabilia sp. nov. were assessed using molecular data from the nuclear genes 18S and 28S, and the mitochondrial 16S and cytochrome c oxidase subunit I (COI). High levels of gene flow are reported between contrasting organic‐rich environments in the North Atlantic (fish farms and whale‐fall). Observations of feeding biology and habitat suggest that V. ardabilia specializes on bacterial mats, rather than on whale‐falls, although the two species of Vigtorniella for which data were available show very different feeding behaviours. Our results further showed an unexpectedly low divergence rate in Vigtorniella for the mitochondrial markers, suggesting stabilizing selection. Analyses carried out with parsimony, maximum likelihood, and MrBayes all placed the genus Vigtorniella as sister group to Dysponetus, suggesting a close evolutionary link to sediment‐dwelling fauna. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 774–785.