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.     

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.     

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.     

The interphalangeal area of Rana pipiens: a light and electron microscopic study of the development of a fibrocartilaginous joint (symphysis)

The development of the distal interphalangeal joint in Rana pipiens hind limb was studied by light and electron microscopy. The joint was found to be a symphysis since the two articular surfaces originally capped by hyaline cartilage were separated by a joint area filled with fibrous connective tissue which ultimately was replaced by fibrocartilage. Ultrastructural studies demonstrated that the joint area development was divided into three phases. Phase I was concerned with the undifferentiated mesenchymal cells, phase II with fibroblastic and chondroblastic development, and phase III with the appearance of fibrocartilage. Changes in the cytoplasmic organelles of fibroblasts and chondroblasts, surrounding extracellular matrix, and factors related to extracellular matrix formation were described and discussed.     

Function and fusion at the mandibular symphysis.

The purpose of this investigation is to determine the functional significance of a fused mandibular symphysis, characteristic of all Anthropoidea. The trait may date to the origins of the suborder. A histological study of 11 prosimian species determined the anatomy of the symphysis. A cinefluorographic film ofGalago crassicaudatus mastication was studied to identify movements at the symphysis. A similar pattern of fibrocartilage and ligaments characterizes all prosimians studied. These tissues are arranged to resist (a) movements seen during mastication inG. crassicaudatus, i.e., antero-posterior shear and spreading of the inferior borders of the symphysis and (b) hypothesized dorso-ventral shear resulting from the transfer of force from the balancing side muscles to the bite point. Partial fusion of the symphysis was found in the folivorous speciesLemur fulvus, L. macaco, Propithecus verreauxi, andHapalemur griseus. Only those tissues associated with resisting occlusally or dorso-ventrally directed forces were calcifying or ossifying. This research suggests that the added occlusal force necessary for leaf-eating has resulted in the evolution of varying degrees of symphyseal fusion in the above species. It is suggested that the protoanthropoids also ate tough foods that required relatively large bite forces.     

The true body shape of rorqual whales

Live Sei and Minke whales were observed underwater off Japan by a new method using commercial catcher boats. A non-explosive harpoon was fired into the tail region of a whale and a diver approached the "tethered" live whale.
After initial flurries, Sei and Minke whales swam steadily ahead of the catcher and could easily be approached by a diver. They took absolutely no notice of the diver. Live Sei and Minke whales kept their mouths tight shut all the time, but immediately after death the lower jaw always fell open. Little blood was emitted from the harpoon wound. The flippers were raised laterally when a whale surfaced and held against the sides of the body when it dived.
The body shape of both rorqual species was streamlined and the throat region was quite flat, not in any way dilated. The classical baggy-throated illustrations of rorqual whales do not show the true shape of live animals.
Sperm whales harpooned by the same method swam about wildly, shed much blood and could not be observed underwater.     

Diversity and duplication of DQB and DRB-like genes of the MHC in baleen whales (suborder: Mysticeti)

The molecular diversity and phylogenetic relationships of two class II genes of the baleen whale major histocompatibility complex were investigated and compared to toothed whales and out-groups. Amplification of the DQB exon 2 provided sequences showing high within-species and between-species nucleotide diversity and uninterrupted reading frames consistent with functional class II loci found in related mammals (e.g., ruminants). Cloning of amplified products indicated gene duplication in the humpback whale and triplication in the southern right whale, with average nucleotide diversity of 5.9 and 6.3%, respectively, for alleles of each species. Significantly higher nonsynonymous divergence at sites coding for peptide binding (32% for humpback and 40% for southern right) suggested that these loci were subject to positive (overdominant) selection. A population survey of humpback whales detected 23 alleles, differing by up to 21% of their inferred amino acid sequences. Amplification of the DRB exon 2 resulted in two groups of sequences. One was most similar to the DRB3 of the cow and present in all whales screened to date, including toothed whales. The second was most similar to the DRB2 of the cow and was found only in the bowhead and right whales. Both loci showed low diversity among species and apparent loss of function or altered function including interruption of reading frames. Finally, comparison of inferred protein sequence of the DRB3-like locus suggested convergence with the DQB, perhaps resulting from intergenic conversion or recombination.Electronic Supplementary Material Supplementary material is available for this article at     

Evolution of the mandibular symphysis in Notharctinae (Adapidae,Primates)

The Eocene Notharctinae provide a record of increasing fusion of the mandibular symphysis. The two sympatric genera,Notharctus andSmilodectes, differed through time in two respects.Notharctus increased in body size and evolved a partially fused mandibular symphysis.Smilodectes changed little in body size and retained an unfused symphysis. Similarities in molar morphology between these two genera and extant leaf-eating mammals suggest thatNotharctus andSmilodectes were specialized for folivory, a dietary regime correlated with partial symphyseal fusion in many extant mammals. It is concluded that the presence and the extant of symphyseal fusion is a function of body size, diet, and jaw mechanics, complicated by lineagespecific factors that vary among higher mammalian taxa.     

Relaxin and β-estradiol modulate targeted matrix degradation in specific synovial joint fibrocartilages: progesterone prevents matrix loss

Relaxin, a 6-kDa polypeptide hormone, is a potent mediator of matrix turnover and contributes to the loss of collagen and glycosaminoglycans (GAGs) from reproductive tissues, including the fibrocartilaginous pubic symphysis of several species. This effect is often potentiated by β-estradiol. We postulated that relaxin and β-estradiol might similarly contribute to the enhanced degradation of matrices in fibrocartilaginous tissues from synovial joints, which may help explain the preponderance of diseases of specific fibrocartilaginous joints in women of reproductive age. The objective of this study was to compare the in vivo effects of relaxin, β-estradiol, and progesterone alone or in various combinations on GAG and collagen content of the rabbit temporomandibular joint (TMJ) disc fibrocartilage, knee meniscus fibrocartilage, knee articular cartilage, and the pubic symphysis. Sham-operated or ovariectomized female rabbits were administered β-estradiol (20 ng/kg body weight), progesterone (5 mg/kg), or saline intramuscularly. This was repeated 2 days later and followed by subcutaneous implantation of osmotic pumps containing relaxin (23.3 μg/kg) or saline. Tissues were retrieved 4 days later and analyzed for GAG and collagen. Serum relaxin levels were assayed using enzyme-linked immunosorbent assay. Relaxin administration resulted in a 30-fold significant (p < 0.0001) increase in median levels (range, approximately 38 to 58 pg/ml) of systemic relaxin. β-estradiol, relaxin, or β-estradiol + relaxin caused a significant loss of GAGs and collagen from the pubic symphysis and TMJ disc and of collagen from articular cartilage but not from the knee meniscus. Progesterone prevented relaxin- or β-estradiol-mediated loss of these molecules. The loss of GAGs and collagen caused by β-estradiol, relaxin, or β-estradiol + relaxin varied between tissues and was most prominent in pubic symphysis and TMJ disc fibrocartilages. The findings suggest that this targeted modulation of matrix loss by hormones may contribute selectively to degeneration of specific synovial joints.     

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.     

Developing protocols for in-water morphometric measurements of cetaceans using stereo-videogrammetry

Morphometry underpins the basic knowledge of any organism's population demographics and dynamics. Such understanding enables the investigation of trends with important conservation implications including monitoring the health of individuals and changes in population dynamics over time. By detecting declines in health prior to the onset of significant mortality, monitoring of body condition can potentially allow time for a management response to avert population decline. We trialed the use of a diver-operated stereo-video (SDOV) system for making morphometric measurements of dwarf minke whales (Balaenoptera acutorostrata subsp.), a small oceanic rorqual, in the Great Barrier Reef, Australia. The SDOV system produced 68% more precise replicate total body length measurements than a single-camera system, while both systems achieved a mean error below 0.5%. The increased precision offered by a SDOV system is desirable for longitudinal monitoring of growth rates and body condition. Optimal application of this method relied on adherence to protocols for both data collection and analysis beyond those dictated by the equipment user manuals. We provide recommendations for these field and analytical protocols, which may be suitable for use with other cetaceans when in-water access is available.     

Fight or flight: antipredator strategies of baleen whales

• 1 The significance of killer whale Orcinus orca predation on baleen whales (Mysticeti) has been a topic of considerable discussion and debate in recent years. Discourse has been constrained by poor understanding of predator‐prey dynamics, including the relative vulnerability of different mysticete species and age classes to killer whales and how these prey animals avoid predation. Here we provide an overview and analysis of predatory interactions between killer whales and mysticetes, with an emphasis on patterns of antipredator responses.
• 2 Responses of baleen whales to predatory advances and attacks by killer whales appear to fall into two distinct categories, which we term the fight and flight strategies. The fight strategy consists of active physical defence, including self‐defence by single individuals, defence of calves by their mothers and coordinated defence by groups of whales. It is documented for five mysticetes: southern right whale Eubalaena australis, North Atlantic right whale Eubalaena glacialis, bowhead whale Balaena mysticetus, humpback whale Megaptera novaeangliae and grey whale Eschrichtius robustus. The flight strategy consists of rapid (20–40 km/h) directional swimming away from killer whales and, if overtaken and attacked, individuals do little to defend themselves. This strategy is documented for six species in the genus Balaenoptera.
• 3 Many aspects of the life history, behaviour and morphology of mysticetes are consistent with their antipredator strategy, and we propose that evolution of these traits has been shaped by selection for reduced predation. Fight species tend to have robust body shapes and are slow but relatively manoeuvrable swimmers. They often calve or migrate in coastal areas where proximity to shallow water provides refuge and an advantage in defence. Most fight species have either callosities (rough and hardened patches of skin) or encrustations of barnacles on their bodies, which may serve (either primarily or secondarily) as weapons or armour for defence. Flight species have streamlined body shapes for high‐speed swimming and they can sustain speeds necessary to outrun pursuing killer whales (>15–20 km/h). These species tend to favour pelagic habitats and calving grounds where prolonged escape sprints from killer whales are possible.
• 4 The rarity of observed successful attacks by killer whales on baleen whales, especially adults, may be an indication of the effectiveness of these antipredator strategies. Baleen whales likely offer low profitability to killer whales, relative to some other marine mammal prey. High‐speed pursuit of flight species has a high energetic cost and a low probability of success while attacks on fight species can involve prolonged handling times and a risk of serious injury.

     

Preparation and Characterization of a Novel Decellularized Fibrocartilage “Book” Scaffold for Use in Tissue Engineering

At the tendon-to-bone insertion, there is a unique transitional structure: tendon, non-calcified fibrocartilage, calcified fibrocartilage, and bone. The reconstruction of this special graded structure after defects or damage is an important but challenging task in orthopedics. In particular, reconstruction of the fibrocartilage zone has yet to be successfully achieved. In this study, the development of a novel book-shape scaffold derived from the extracellular matrix of fibrocartilage was reported. Specifically, fibrocartilage from the pubic symphysis was obtained from rabbits and sliced into the shape of a book (dimensions: 10 mm × 3 mm × 1 mm) with 10 layers, each layer (akin to a page of a book) with a thickness of 100-μm. These fibrocartilage “book” scaffolds were decellularized using sequentially 3 freeze-thaw cycles, 0.1% Triton X-100 with 1.5 M KCl, 0.25% trypsin, and a nuclease. Histology and DNA quantification analysis confirmed substantial removal of cells from the fibrocartilage scaffolds. Furthermore, the quantities of DNA, collagen, and glycosaminoglycan in the fibrocartilage were markedly reduced following decellularization. Scanning electron microscopy confirmed that the intrinsic ultrastructure of the fibrocartilage tissue was well preserved. Therefore, the results of this study suggest that the novel “book” fibrocartilage scaffold could have potential applications in tissue engineering.     

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.     

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.     

The phylogenetic distribution and morphological variation of the ‘pouch’ in female snakes

Siegel D.S., Miralles A, Trauth S.E. and Aldridge R.D. 2011. The phylogenetic distribution and morphological variation of the ‘pouch’ in female snakes. —Acta Zoologica (Stockholm) 93 : 400–408. The urodaeum of female snakes is a chamber that receives the oviducts, urinary ducts, and intestine. Previous studies have indicated that a derived region of unknown function persists between the urodaeum and oviducts in some snakes of the Colubroides. This structure was recently termed the ‘pouch’; however, it is also commonly referred to as the vaginal pouch. A broad sampling of female snakes revealed that the pouch evolved once on the branch leading to Colubroides. The presence of the pouch in Colubroides is not unambiguous, as this feature was lost in some members of the Atractaspididae and Lamprophiidae. Variation was also observed in pouch morphology between taxa of the Colubroides. Variation included the following: (1) whether the pouch was bifurcated and if so, were the arms of the pouch separated caudally, (2) whether separated pouch arms were split by a caudal bifurcation of the urodaeum or through medial septa of the pouch arms, and (3) the absence or presence of oviducal papillae invading the cranial/lateral extremity of the pouch. The variation in pouch morphology observed does not appear to be correlated with the evolutionary history of Colubroides and polymorphism within families is common.     

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.     

Trophic level and fatty acids in harp seals compared with common minke whales in the Barents Sea

The objectives of this study were to explore trophic levels and possible diet overlap between harp seals (Pagophilus groenlandicus) and common minke whales (Balaenoptera acutoroostrata) in the Barents Sea using stable isotopes of nitrogen (δ¹⁵N) and carbon (δ¹³C) and fatty acid analyses, and to explore the energy pathways from the plankton to the top predators. Blubber and muscle samples from 93 harp seals and 20 minke whales were collected in the southern Barents Sea in May 2011. The study showed that harp seals were at a higher trophic level than minke whales during spring. This supported previous diet studies suggesting a more fish-dominant diet for seals, as compared with the whales, at this time of the year. The stable isotopes and fatty acids indicated niche separation between the seals and the whales, and between different age groups of the harp seals. Older seals had fatty acid profiles more equal to minke whales as compared with younger seals. Furthermore, while the fatty acid profiles suggested that krill were of particular importance for the young seals, the profiles from older seals and whales suggested that fish dominated their diets.     

Cephalopod remains from stomachs of sperm whales (Physeter macrocephalus) that mass‐stranded along the Oregon coast

On 16 June 1979, a herd of 41 sperm whales stranded near the mouth of the Siuslaw River in Florence, Oregon. The stomach contents from 32 whales were collected, identified to the lowest taxonomic level possible, enumerated, and measured. A total of 20,247 cephalopod lower beaks that represented 24 species from 14 different families were recovered. The most numerous species were Histioteuthis hoylei (25.9%), Taonius borealis (12.9%), Galiteuthis phyllura (11.2%), Gonatopsis/Berryteuthis type (10.9%), and Moroteuthis robusta (10.7%). Reconstructed estimates of mass indicated that M. robusta contributed almost 50% of the total mass of cephalopods consumed, followed by H. hoylei (19.3%), and T. borealis (7.0%). The most important species in the diet of stranded whales were M. robusta, H. hoylei, T. borealis, G. phyllura, Octopoteuthis deletron, and Gonatopsis/Berryteuthis type. There were significant differences in the diet of males and females, but no differences between sperm whales of different age groups. Overall, sperm whales primarily consumed small cephalopods that were likely eaten south of 45ºN in or near the California Current System. This study provides new estimates of the food habits of sperm whales in the northeast Pacific from one of the largest strandings of this species.     

Patterns and trends in the diet of long‐finned pilot whales (Globicephala melas) in the northeast Atlantic

There is little previous information on feeding habits of long‐finned pilot whales (Globicephala melas) in the northeast Atlantic. The present study analyzed stomach contents of pilot whales stranded in Portugal (n = 6), Galicia (northwest Spain) (n = 32), and Scotland (United Kingdom) (n = 10), from 1990 to 2011. These animals ranged from 213 to 555 cm in length (24 females, 19 males and 5 of unknown sex). The main prey identified were cephalopods of the families Octopodidae and Ommastrephidae, the former being numerically more important in Iberia (Portugal and Galicia) and the latter more important in Scotland, with Iberian whales also showing a more diverse diet. Multivariate analysis revealed evidence of geographical and seasonal variation in diet. Generalized Additive Modeling results indicated that more octopus (Eledone cirrhosa) were eaten in Iberia than in Scotland, more in the first half of the year, and more in larger whales. Numbers of ommastrephid squids in the stomach decreased over the study period and varied with season and whale length. This study confirms cephalopods as the main prey of pilot whales, as previously reported, although our results also suggest that, in the northeast Atlantic, ommastrephid squid are largely replaced as the main prey by octopods at lower latitudes.