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.     

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.     

Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): the largest vertebrate skeletal element and its role in rorqual lunge feeding

Rorqual whales (crown Balaenopteridae) are unique among aquatic vertebrates in their ability to lunge feed. During a single lunge, rorquals rapidly engulf a large volume of prey‐laden water at high speed, which they then filter to capture suspended prey. Engulfment biomechanics are mostly governed by the coordinated opening and closing of the mandibles at large gape angles, which differentially exposes the floor of the oral cavity to oncoming flow. The mouth area in rorquals is delimited by unfused bony mandibles that form kinetic linkages to each other and with the skull. The relative scale and morphology of these skeletal elements have profound consequences for the energetic efficiency of foraging in these gigantic predators. Here, we performed a morphometric study of rorqual mandibles using a data set derived from a survey of museum specimens. Across adult specimens of extant balaenopterids, mandibles range in size from ～1–6 m in length, and at their upper limit they represent the single largest osteological element of any vertebrate, living or extinct. Our analyses determined that rorqual mandibles exhibit positive allometry, whereby the relative size of these mandibles becomes greater with increasing body size. These robust scaling relationships allowed us to predict mandible length for fragmentary remains (e.g. incomplete and/or fossil specimens), as we demonstrated for two partial mandibles from the latest Miocene of California, USA, and for mandibles from previously described fossil balaenopterids. Furthermore, we showed the allometry of mandible length to body size in extant mysticetes, which hints at fundamental developmental constraints in mysticetes despite their ecomorphological differences in feeding styles. Lastly, we outlined how our findings can be used to test hypotheses about the antiquity and evolution of lunge feeding. © 2012 The Linnean Society of London     

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.     

Feeding strategy of the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae)

The feeding biology of the planktivorous megamouth shark Megachasma pelagios was investigated. Morphological examination disclosed that the megamouth has a suite of unique characteristics among sharks, such as large mouth, large bucco-pharyngeal cavity, elongate jaw cartilages, long palatoquadrate levator and preorbital muscles, long ethmopalatine ligament and elastic skin around the pharynx. The combination of these characters suggests that the megamouth shark performs engulfment feeding that is typically seen in the rorqual and humpback whales. Engulfment is a new feeding method for sharks, and the detailed mechanism of the engulfment feeding is discussed.     

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.     

Low genetic diversity in pygmy blue whales is due to climate-induced diversification rather than anthropogenic impacts

Unusually low genetic diversity can be a warning of an urgent need to mitigate causative anthropogenic activities. However, current low levels of genetic diversity in a population could also be due to natural historical events, including recent evolutionary divergence, or long-term persistence at a small population size. Here, we determine whether the relatively low genetic diversity of pygmy blue whales (Balaenoptera musculus brevicauda) in Australia is due to natural causes or overexploitation. We apply recently developed analytical approaches in the largest genetic dataset ever compiled to study blue whales (297 samples collected after whaling and representing lineages from Australia, Antarctica and Chile). We find that low levels of genetic diversity in Australia are due to a natural founder event from Antarctic blue whales (Balaenoptera musculus intermedia) that occurred around the Last Glacial Maximum, followed by evolutionary divergence. Historical climate change has therefore driven the evolution of blue whales into genetically, phenotypically and behaviourally distinct lineages that will likely be influenced by future climate change.     

Killer whale predation on penguins in Antarctica

We report here the first published observations of killer whales (Orcinus orca) feeding on penguins in Antarctica. The sightings took place in the Gerlache Strait off the western Antarctic Peninsula during February 2010. Two species of pygoscelid penguins were taken—gentoo (Pygoscelis papua, at least four individuals) and chinstrap (P. antarctica, 2). From remains left at the surface, it was clear that the killer whales fed mainly on the breast muscles, although some penguins may have been swallowed whole. The killer whales were ecotype B, which are purported seal specialists, but we also saw ecotype A, prey specialists on Antarctic minke whales Balaenoptera bonaerensis, chase, but not catch penguins. Because of their small relative size, if penguins are regularly targeted by killer whales in Antarctica, the impact on their populations could be significant.     

Blue whales respond to simulated mid-frequency military sonar

Mid-frequency military (1–10 kHz) sonars have been associated with lethal mass strandings of deep-diving toothed whales, but the effects on endangered baleen whale species are virtually unknown. Here, we used controlled exposure experiments with simulated military sonar and other mid-frequency sounds to measure behavioural responses of tagged blue whales (Balaenoptera musculus) in feeding areas within the Southern California Bight. Despite using source levels orders of magnitude below some operational military systems, our results demonstrate that mid-frequency sound can significantly affect blue whale behaviour, especially during deep feeding modes. When a response occurred, behavioural changes varied widely from cessation of deep feeding to increased swimming speed and directed travel away from the sound source. The variability of these behavioural responses was largely influenced by a complex interaction of behavioural state, the type of mid-frequency sound and received sound level. Sonar-induced disruption of feeding and displacement from high-quality prey patches could have significant and previously undocumented impacts on baleen whale foraging ecology, individual fitness and population health.     

Observations of blue whales feeding in Antarctic waters

There are no published accounts of blue whales (Balaenoptera musculus) feeding in Antarctic waters. This note describes the behaviour of two groups of blue whales feeding in Antarctic pelagic waters. Whales were observed during the 18th IWC/IDCR southern hemisphere minke whale assessment cruise. Feeding behaviour in both cases resembled those described previously for both northern hemisphere blue whales and fin whales (B. physalus). These observations suggest that a programme of comparative behavioural observations could be developed to test the “feeding competition” hypothesis, which suggests that recovery of populations of blue whales will be impeded by feeding competition with sympatric minke whales. Accepted: 29 April 1999     

Feeding, respiration and life history of the hyperiid amphipod Themisto libellula in the Arctic marginal ice zone of the Greenland Sea

Daily ingestion rates of the pelagic hyperiid amphipod Themisto libellula were studied in the marginal ice zone of the Arctic Fram Strait by feeding experiments, respiration measurements and an allometric approach based on body mass. Amphipods were collected by stratified multiple opening/closing net hauls and Rectangular Midwater Trawl (RMT 8) in August 2000 during the expedition ARK XVI/2 of R/V “Polarstern”. T. libellula occurred with abundances of 0.043 and 0.015 ind. m⁻³ in the upper 30 m of the water column at two RMT 8 stations. Based on respiration data, the daily ingestion necessary to cover metabolic energy demands measured 1.9±0.6% of body carbon per day. Actual prey consumption during feeding experiments with Calanus copepodids as prey was very similar and accounted for 1.9±1.5% day⁻¹, indicating that feeding on Calanus can meet the energy demands of T. libellula. In general, experimental results were slightly lower than the maximum potential ingestion (2% day⁻¹ for an individual of median body dry mass of 32 mg) estimated by an allometric equation based on body mass, but feeding experiments showed a strong variability. Reduced metabolism and low ingestion rates of T. libellula are consistent with low ambient temperature, large body size, slow growth and long life span of this polar species. The effect of the active pelagic life style of T. libellula on metabolism and ingestion rate is discussed in comparison to the sympagic (i.e. ice-associated) amphipod Gammarus wilkitzkii of similar body size living in the same environment. In relation to the mesozooplankton biomass in the investigation area, the predation impact by T. libellula was low. However, high-Arctic conditions also limit the secondary production of principal prey species, such as Calanus glacialis and Calanus hyperboreus, so that even low predation rates may affect the growth of prey populations.     

MOVEMENTS OF NORTH PACIFIC BLUE WHALES DURING THE FEEDING SEASON OFF SOUTHERN CALIFORNIA AND THEIR SOUTHERN FALL MIGRATION1

The satellite-acquired locations of 10 blue whales (Balaenoptera musculus) tagged off southern California with Argos radio tags were used to identify (1) their movements during the late summer feeding season; (2) the routes and rate of travel for individuals on their southern fall migration; and (3) a possible winter calving/breeding area. Whales were tracked from 5.1 to 78.1 d and from 393 to 8,668 km. While in the Southern California Bight, most of the locations for individual whales were either clumped or zigzagged in pattern, suggesting feeding or foraging (searching for prey). Average speeds ranged from 2.4 to 7.2 km/h. One whale moved north to Cape Mendocino, and four migrated south along the Baja California, Mexico coast, two passing south of Cabo San Lucas on the same day. One of the latter whales traveled an additional 2,959 km south in 30.5 d to within 450 km of the Costa Rican Dome (CRD), an upwelling feature. The timing of this migration suggests the CRD may be a calving/breeding area for North Pacific blue whales. Although blue whales have previously been sighted in the Eastern Tropical Pacific (ETP), this is the first evidence that whales from the feeding aggregation off California range that far south. The productivity of the CRD may allow blue whales to feed during their winter calving/breeding season, unlike gray whales (Eschrichtius robustus) and humpbacks (Megaptera novaeangliae) which fast during that period.     

Morphological specializations of baleen whales associated with hydrodynamic performance and ecological niche

Feeding behavior, prey type, and habitat appear to be associated with the morphological design of body, fluke, and flippers in baleen whales. Morphometric data from whaling records and recent stranding events were compiled, and morphometric parameters describing the body length, and fluke and flipper dimensions for an "average" blue whale Balaenoptera musculus, humpback whale Megaptera novaeangliae, gray whale Eschrichtius robustus, and right whale Eubalaena glacialis were determined. Body mass, body volume, body surface area, and fluke and flipper surface areas were estimated. The resultant morphological configurations lent themselves to the following classifications based on hydrodynamic principles: fast cruiser, slow cruiser, fast maneuverer, and slow maneuverer. Blue whales have highly streamlined bodies with small, high aspect ratio flippers and flukes for fast efficient cruising in the open ocean. On the other hand, the rotund right whale has large, high aspect ratio flukes for efficient slow speed cruising that is optimal for their continuous filter feeding technique. Humpbacks have large, high aspect ratio flippers and a large, low aspect ratio tail for quick acceleration and high-speed maneuvering which would help them catch their elusive prey, while gray whales have large, low aspect ratio flippers and flukes for enhanced low-speed maneuvering in complex coastal water habitats.     

Estimating maximal force output of cetaceans using axial locomotor muscle morphology

Cetaceans span a large range of body sizes and include species with the largest known locomotor muscles. To date, force output and thrust production have only been directly measured in the common bottlenose dolphin (Tursiops truncatus), although thrust forces have been hydrodynamically modeled for some whales. In this study, two metrics of epaxial muscle size—cross‐sectional area (CSA) and mass—were used to estimate force output for 22 species (n = 83 specimens) ranging in size from bottlenose dolphins to blue whales (Balaenoptera musculus). Relative to total body length (TL), maximum force output estimated based upon both muscle CSA (TL^{1.56 ± 0.05}) and mass (TL^{2.64 ± 0.07}) scaled at rates lower than those predicted by geometric scaling, suggesting relative force output decreases with increasing body size in cetaceans. Estimated maximal force outputs were compared to both published drag forces and to the breaking strengths of commercial fishing lines known to entangle whales. The breaking strengths of these lines are within the same order of magnitude, and in some cases, exceed the estimated maximal force output of whales. These results suggest that while powerful animals, large whales may be unable to break the extremely strong fishing line used today.     

Genetic diversity and structure of blue whales (Balaenoptera musculus) in Australian feeding aggregations

The worldwide distribution of blue whales (Balaenoptera musculus) has not prevented this species from becoming endangered due to twentieth century whaling. In Australia there are two known feeding aggregations of blue whales, which most likely are the pygmy subspecies (B. m. brevicauda). It is unknown whether individuals from these feeding aggregations belong to one breeding stock, or multiple breeding stocks that either share or occupy separate feeding grounds. This was investigated using ten microsatellite loci and mitochondrial DNA control region sequences (N = 110). Both sets of markers revealed no significant genetic structure, suggesting that these whales are likely to belong to the same breeding stock.     

Morphometric analysis of Chilean blue whales and implications for their taxonomy

In the Southern Hemisphere, blue whales are currently divided into two subspecies, Antarctic blue whales (Balaenoptera musculus intermedia) and pygmy blue whales (B. m. brevicauda), but there is some debate about whether Chilean blue whales should also be considered as a separate subspecies. Here, we provide novel morphometric data to directly address this taxonomic question from a biological survey of 60 blue whales taken during the 1965/1966 Chilean whaling season. The data show that maximum body length and mean body length of both sexually mature females and males for Chilean blue whales are intermediate between pygmy and Antarctic blue whales; and that fluke-anus lengths of Chilean blue whales are significantly different from pygmy blue whales, but not necessarily from Antarctic blue whales. There is also some support from the data that snout-eye measurements are different among all three groups. These data provide further confirmation that Chilean blue whales are a distinct population requiring separate management from other blue whale populations, and are also consistent with suggestions that Chilean blue whales are not the same subspecies as pygmy blue whales.     

Feeding behaviour in Meganyctiphanes norvegica (M. Sars) (Crustacea: Euphausiacea)

Meganyctiphanes norvegica (M. Sars) will feed upon the centric diatom Thalassiosira weissflogii (Grunow) G. Fryxell & Hasle but cannot fulfil its energy requirement for metabolism on this food. Its daily metabolic requirement can be exceeded when the euphausiid feeds upon the copepods Calanus finmarchicus Gunner or Centropages typicus Krøeyer, but not when feeding upon the smaller copepods Pseudocalanus spp. or Acartia spp. When feeding upon a natural copepod assemblage Meganyctiphanes norvegica requires high concentrations of copepods to achieve its metabolic requirements, suggesting that the euphausiid may exploit vertically patchy concentrations of prey. Short-term predation rates on Pseudocalanus spp. were also used to estimate feeding rates. Feeding in Meganyctiphanes norvegica appears to be adapted to a spatially variable food supply and rapid exploitation of food sources concentrated into patches or layers. The filter area of the feeding basket of M. norvegica is proportionally smaller than the filter area of Euphausia superba Dana, but has the same allometric length exponent. The filter area probably reflects the difference between the primarily carnivorous diet of Meganyctiphanes norvegica and herbivorous diet of Euphausia superba.     

Multiaxial movements at the minke whale temporomandibular joint

Mandibular mobility accompanying gape change in Northern and Antarctic minke whales was investigated by manipulating jaws of carcasses, recording jaw movements via digital instruments (inclinometers, accelerometers, and goniometers), and examining osteological and soft tissue movements via computed tomography (CT)-scans. We investigated longitudinal (α) rotation of the mandible and mediolateral displacement at the symphysis (Ω₁) and temporomandibular joint (Ω₂) as the mouth opened (Δ). Results indicated three phases of jaw opening. In the first phase, as gape increased from zero to 8°, there was slight (<1°) α and Ω rotation. As gape increased between 20 and 30°, the mandibles rotated slightly laterally (Mean 3°), the posterior condyles were slightly medially displaced (Mean 4°), and the anterior ends at the symphysis were laterally displaced (Mean 3°). In the third phase of jaw opening, from 30° to full (≥90°) gape, these motions reversed: mandibles rotated medially (Mean 29°), condyles were laterally displaced (Mean 14°), and symphyseal ends were medially displaced (Mean 1°). Movements were observed during jaw manipulation and analyzed with CT-images that confirmed quantitative inclinometer/accelerometer data, including the unstable intermediate (Phase 2) position. Together these shifting movements maintain a constant distance for adductor muscles stretched between the skull's temporal fossa and mandible's coronoid process. Mandibular rotation enlarges the buccal cavity's volume as much as 36%, likely to improve prey capture in rorqual lunge feeding; it may strengthen and stabilize jaw opening or closure, perhaps via a simple locking or unlocking mechanism. Rotated lips may brace baleen racks during filtration. Mandibular movements may serve a proprioceptive mechanosensory function, perhaps via the symphyseal organ, to guide prey engulfment and water expulsion for filtration.     

Cetacean mitochondrial DNA control region: sequences of all extant baleen whales and two sperm whale species

The sequence of the mitochondrial control region was determined in all 10 extant species commonly assigned to the suborder Mysticeti (baleen or whalebone whales) and to two odontocete (toothed whale) species (the sperm and the pygmy sperm whale). In the mysticetes, both the length and the sequence of the control region were very similar, with differences occurring primarily in the first approximately 160 bp of the 5' end of the L-strand of the region. There were marked differences between the mysticete and sperm whale sequences and also between the two sperm whales. The control region, less its variable portion, was used in a comparison including the 10 mysticete sequences plus the same region of an Antarctic minke whale specimen and the two sperm whales. The difference between the minke whales from the North Atlantic and the Antarctic was greater than that between any acknowledged species belonging to the same genus (Balaenoptera). The difference was similar to that between the families Balaenopteridae (rorquals) and Eschrichtiidae (gray whales). The findings suggest that the Antarctic minke whale should have a full species status, B. bonaerensis. Parsimony analysis separated the bowhead and the right whale (family Balaenidae) from all remaining mysticetes, including the pygmy right whale. The pygmy right whale is usually included in family Balaenidae. The analysis revealed a close relationship between the gray whale (family Eschrichtiidae) sequence and those of the rorquals (family Balaenopteridae). The gray whale was included in a clade together with the sei, Bryde's, fin, blue, and humpback whales. This clade was separated from the two minke whale types, which branched together.