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.     

The diving behavior of blue and fin whales: is dive duration shorter than expected based on oxygen stores?

Many diving seabirds and marine mammals have been found to regularly exceed their theoretical aerobic dive limit (TADL). No animals have been found to dive for durations that are consistently shorter than their TADL. We attached time-depth recorders to 7 blue whales and 15 fin whales (family Balaenopteridae). The diving behavior of both species was similar, and we distinguished between foraging and traveling dives. Foraging dives in both species were deeper, longer in duration and distinguished by a series of vertical excursions where lunge feeding presumably occurred. Foraging blue whales lunged 2.4 (+/-1.13) times per dive, with a maximum of six times and average vertical excursion of 30.2 (+/-10.04) m. Foraging fin whales lunged 1.7 (+/-0.88) times per dive, with a maximum of eight times and average vertical excursion of 21.2 (+/-4.35) m. The maximum rate of ascent of lunges was higher than the maximum rate of descent in both species, indicating that feeding lunges occurred on ascent. Foraging dives were deeper and longer than non-feeding dives in both species. On average, blue whales dived to 140.0 (+/-46.01) m and 7.8 (+/-1.89) min when foraging, and 67.6 (+/-51.46) m and 4.9 (+/-2.53) min when not foraging. Fin whales dived to 97.9 (+/-32.59) m and 6.3 (+/-1.53) min when foraging and to 59.3 (+/-29.67) m and 4.2 (+/-1.67) min when not foraging. The longest dives recorded for both species, 14.7 min for blue whales and 16.9 min for fin whales, were considerably shorter than the TADL of 31.2 and 28.6 min, respectively. An allometric comparison of seven families diving to an average depth of 80-150 m showed a significant relationship between body mass and dive duration once Balaenopteridae whales, with a mean dive duration of 6.8 min, were excluded from the analysis. Thus, the short dive durations of blue whales and fin whales cannot be explained by the shallow distribution of their prey. We propose instead that short duration diving in large whales results from either: (1) dispersal behavior of prey; or (2) a high energetic cost of foraging.     

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.     

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.     

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.     

Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size

Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations.     

Detecting surface‐feeding behavior by rorqual whales in accelerometer data

The movement of marine animals feeding at the sea surface is restricted by wave drag and a reduction in propulsive efficiency. Many rorqual whale species lunge feed at the surface, yet existing methodologies for detecting lunges in accelerometer data have not been applied to surface‐feeding behavior. Our study aimed to develop a method to detect surface‐feeding behavior in accelerometer data and in doing so, determine whether wave drag influences the detection of surface‐feeding behavior. A new acceleration parameter is described that considers the forward acceleration of the animal relative to its pitch. The new parameter, along with information on the deceleration and pitch angle, was then used in an automatic lunge detecting algorithm followed by a visual classification method that detected approximately 70% of the lunges observed during focal follow sampling. The forward acceleration of lunges decreased significantly with increasing proximity to the surface. This lower acceleration at the surface may influence the ability to detect lunge feeding behavior close to the surface. Future research should attempt to determine the cause of this relationship, which may be the influence of changes in the forces acting on the whale or behavioral flexibility by the whale.     

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.     

The distribution of zooplankton and bowhead whales, <Emphasis Type="Italic">Balaena mysticetus</Emphasis> Linnaeus, 1758, in Akademiya Bay,Sea of Okhotsk

The modern pattern of distribution and feeding habits of the bowhead whale, Balaena mysticetus, in the Sea of Okhotsk are studied. The existence of a feeding aggregation of this whale species in the southwesternmost portion (apex) of Ulban Bay has been confirmed. There, the animals feed in shallow waters with depths of 3–5 m, which are only slightly larger than their body height. The quantitative composition and species structure of zooplankton at the stations that were set near feeding whales have been analyzed. In the samples taken in the immediate proximity to the feeding whales, the abundance of zooplankton reached 31409 ind./m³, with the average value of 17565 ind./m³. The lowest abundance, from 56 to 1879 ind./m³ (mean 927 ind./m³), was in the samples from western Konstantin Bay, where bowhead whales were not observed. In 16 samples collected in the immediate proximity to the feeding whales in the shallow waters of Ulban Bay, the average zooplankton biomass was 547.9 mg/m³, which is 3.9 times higher than that in the samples from waters where the whales were absent. Copepods dominated quantitatively at all the stations in Akademiya Bay. The proportion of euphausiids in the zooplankton biomass was lower than 1%, both near the feeding whales and in the absence of whales.     

Foraging costs and accessibility as determinants of giving-up densities in a swan-pondweed system

We measured the patch use behaviour of Bewick's swans (Cygnus columbianus bewickii) feeding on below ground tubers of fennel pondweed (Potamogeton pectinatus). We compared the swans’ attack rates, foraging costs and giving‐up densities (GUDs) in natural and experimental food patches that differed in water depth. Unlike most studies that attribute habitat‐specific differences in GUDs to predation risk, food quality or foraging substrate, we quantified the relative importance of energetic costs and accessibility. Accessibility is defined as the extent to which the animal's morphology restricts its harvest of all food items within a food patch. Patch use behaviours were measured at shallow (ca 0.4 m) and deep (ca 0.6 m) water depths on sandy sediments. In a laboratory foraging experiment, when harvesting food patches, the swan's attack rate (m³ s^?1) did not differ between depths. In deep water the energetic costs of surfacing, feeding and trampling were 1.13 to 1.21 times higher than in shallow water with a tendency to spend relatively more time trampling, the most expensive activity. Taking time allocation as measured in the field into account, foraging in deep water was 1.26 times as expensive as in shallow water. In the lake the GUD in shallow water was on average 12.9 g m^?2. If differences in energetic costs were the only factor determining differences in GUDs, then the deep water GUD should be 14.2 g m^?2. Instead, the mean GUD in deep water was 20.2 g m^?2, and therefore energetic costs explain just 18% of the difference in GUDs. At deep sites, 24% of tuber biomass was estimated to be out of reach, and we calculated a maximum accessible foraging depth of 0.86 m. This is close to the published 0.84 m based on body measurements. A laboratory experiment with food offered at a depth of 0.89 m confirmed that it was just out of reach. The agreement between calculated and observed maximum accessible foraging depths suggests that accessibility largely explains the remaining difference in GUDs with depth, and it confirms the existence of partial prey refuges in this system.     

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.     

'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.     

Stable carbon and nitrogen isotope ratios in muscle and epidermis of arctic whales

Collection of minimally invasive biopsy samples has become an important method to establish normal stable isotopes reference ranges in various wildlife species. Baseline data enhance the understanding of feeding ecology, habitat use, and potential food limitation in apparently healthy, free‐ranging cetaceans. Epidermis and muscle were collected from subsistence‐hunted northern Alaskan bowhead (n= 133 epidermis/134 muscle) and beluga whales (n= 42/49) and subsistence‐hunted Russian gray whales (n= 25/17). Additional samples were obtained from gray whales stranded in California (n= 18/11) during mortality events (1999, 2000). Both δ¹⁵N and δ¹³C are trophic position and benthic/pelagic feeding indicators, respectively, in muscle and epidermis. Epidermis is generally enriched in ¹⁵N over muscle, while epidermal ¹³C is more depleted. Lipid extraction does not alter δ¹⁵N in either tissue, but affects epidermal δ¹³C. Nitrogen‐15 is enriched in muscle, but not epidermis of stranded compared to subsistence‐hunted gray whales, indicating probable protein catabolism and nutritional stress in stranded whales. Similarly, epidermal δ¹³C of harvested whales is lower than in stranded whales, suggesting depleted lipid stores and/or food limitation in stranded animals. Epidermal isotope signatures are similar in both present‐day bowheads and in an ancient sample from the Northern Bering Sea region. Although only one specimen, this suggests trophic level of the ancient whale compares to modern bowheads after a millennium.     

APPARENT LATERALIZED BEHAVIOR IN GRAY WHALES FEEDING OFF THE CENTRAL BRITISH COLUMBIA COAST

A digital acoustic recording tag was used to examine the 3‐D orientation of gray whales feeding along the central British Columbia coast. A total of 96 feeding dives were recorded from six different whales. More than half (53.1%) of the whales' bottom time was spent rolled at an angle greater than 45°. Whales rolled an average of 2.9 times per feeding dive, and rolling behavior was often accompanied by a negative pitch angle. Out of 282 recorded rolls, 274 (97.2%) were to the right. Likewise, 98.5% of the total time spent rolled at an angle greater than 45° was spent rolled to the right. The gray whales in this study showed a significant right‐side bias on both an individual (P≤ 0.009) and group level (P < 0.001). Based on the findings of this study and previous reports of uneven baleen wear ( Kasuya and Rice 1970 ), it is proposed that gray whales exhibit a population‐wide right‐side rolling bias similar in character to the 90/10 split of right handedness in humans.     

Food consumption of five deep‐sea fishes in the Balearic Basin (western Mediterranean Sea): are there daily feeding rhythms in fishes living below 1000 m?

Predation and food consumption of five deep‐sea fish species living below 1000 m depth in the western Mediterranean Sea were analysed to identify the feeding patterns and food requirements of a deep‐sea fish assemblage. A feeding rhythm was observed for Risso's smooth‐head Alepocephalus rostratus, Mediterranean grenadier Coryphaenoides mediterraeus and Mediterranean codling Lepidion lepidion. Differences in the patterns of the prey consumed suggest that feeding rhythms at such depths are linked with prey availability. The diets of those predators with feeding rhythms are based principally on active‐swimmer prey, including pelagic prey known to perform vertical migrations. The diets of Günther's grenadier Coryphaenoides guentheri and smallmouth spiny eel Polyacanthonotus rissoanus, which did not show any rhythm in their feeding patterns, are based mainly on benthic prey. Food consumption estimates were low (<1% of body wet mass day^?1). Pelagic feeding species showing diel feeding rhythms consumed more food than benthic feeding species with no feeding rhythms.     

Morphological divergence between three Arctic charr morphs – the significance of the deep‐water environment

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow‐, deep‐water resource axis in a subarctic postglacial lake (Norway). The two deep‐water (profundal) spawning morphs, a benthivore (PB‐morph) and a piscivore (PP‐morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep‐water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small‐sized PB‐morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep‐water sediments. The PP‐morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO‐morph) predominantly utilizes the shallow benthic–pelagic habitat and food resources. Compared to the deep‐water morphs, the LO‐morph had smaller head relative to body size. The LO‐morph exhibited traits typical for both shallow‐water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep‐water habitat for the PB‐ and PP‐morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep‐water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep‐water piscivore morph has to our knowledge not been described elsewhere.     

Fishing gears involved in entanglements of minke whales (Balaenoptera acutorostrata) in the East Sea of Korea

Entanglement of marine mammals in fishing gear is a global issue. It is considered a significant threat to minke whales (Balaenoptera acutorostrata) in the East Sea of Korea. A total of 214 entanglements of minke whales in this area between 2004 and 2007 were used to investigate types and parts of fishing gears involved in entanglements. The majority of entanglements were mainly caused by three types of fishing gears: set nets, pots, and gill nets (n= 207, 96.7%). Other entanglements were associated with bottom trawls, purse seines, and trawls. A total of 65 entanglements were attributed to the main and branch lines of fishing gears. The most common body part of minke whales which attached to fishing gears was the mouth (n= 63, 30.4%). Most entanglements took place within 10 nmi from land (n= 179, 86.5%), and between 10 and 220 m of water depth. The mean length of entangled minke whales in set nets was significantly smaller than that of whales in pots and gill nets samples (P < 0.001). Also, the mean body length of minke whales that entangled in the coastal area and shallow waters was significantly shorter than that of whales in the offshore area and deep waters (P < 0.001). This information can be used as fundamental data to conserve and manage this population of minke whales in the East Sea of Korea, and also to modify fishing gear to reduce entanglements. Future studies should focus on investigating the impact of these entanglements on the population and the effectiveness of mitigation measures to reduce entanglements of minke whales in this area.