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.     

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.     

A new baleen whale from the Late Miocene of Denmark and early mysticete hearing

Abstract:  The extinct mysticete fauna of the North East Atlantic is primarily known from the abundant but fragmented Belgian specimens. Compared to the well-preserved contemporary mysticete fauna from deposits in North America, there are only few near complete European Miocene mysticete fossils. Presented here is a new, almost complete fossil baleen whale Uranocetus gramensis gen. et sp. nov. from the Upper Miocene Gram Formation in South West Denmark. It is the first stem-balaenopterid that has an initial stage of reduction in the mandibular cavity and a rostral configuration that is intermediate between that of other stem-balaenopterids and true balaenopterids. It is likely that Uranocetus used a gulp feeding technique that approaches that of balaenopterids. Details of the periotic and mandibular morphology place Uranocetus in the family Diorocetidae Steeman 2007. The large mandibular cavity in Uranocetus and most other extinct mysticetes, when compared to the reduced condition in recent mysticetes, is not an indication that early mysticetes used odontocete-like echolocation. In Uranocetus and a distantly related mysticete, high frequency sounds in the range odontocetes use for echolocation would suffer a significant volume loss across the lateral mandibular wall on the passage towards the inner ear. A reduction in the mandibular cavity in separate evolutionary lineages of mysticetes may be the result of a shift towards the use of low frequency sounds.     

Geographical variation in mandible morphologies specialised for collembolan predation depend on prey size in the ant Strumigenys lewisi

1. Ants in the genus Strumigenys are predator ants that feed on tiny soil arthropods. The mandibles are modified into high‐speed traps to capture swift collembolan prey. The peculiar mandible morphologies of these ants have evolved depending on characteristics of the prey. Specifically, the evolution of mandible size and shape may be directly driven by prey size. 2. In the present study, the intraspecific variation of the morphological traits of Strumigenys lewisi populations were observed in central Japan. The relationships between the morphological variations and the prey body size were analysed. 3. In workers and queens, three morphological traits, head width, mandible length, and mandible width were significantly different among the multiple sites. Specifically, the mandible length was shorter in southwestern Japan than in other sampling locations. The ancova model revealed that the allometry of the mandible length to the head width was different among the sites. 4. As predicted, the mandible length was positively correlated with the average body size of collembolans in the Entomobryidae family. Furthermore, multiple regression analysis showed that the variation of the mandible length was affected by environmental factors represented as location information. However, the effect of collembolan body size was more effective at predicting mandible length. The study suggests that the geographical variation of mandible morphologies in S. lewisi has been selected by predator–prey interactions with collembolans.     

It's all relative: allometry and variation in the baculum (os penis) of the harp seal, Pagophilus groenlandicus (Carnivora: Phocidae)

We compared allometry and variation in the baculum (os penis), mandible, and humerus of the harp seal, Pagophilus groenlandicus. This species is presumed to have a promiscuous mating system in which choice of mate by females during intromission with different males is likely. The baculum is large and grows throughout life so may be an honest indicator of males' quality (size) or viability (age). We predicted that bacular size would exhibit stronger allometry relative to body size than mandibles or humeri. The baculum is less functionally (mechanically) constrained than mandibles or humeri so we also predicted it would be more variable, though less variable than sexually selected traits which do not function as honest indicators. Our sample (N=67 seals) represented broad ranges of size and age (0–35 yr) so we compared variation using residuals from allometric regressions of skeletal measurements on body length. Bacular size was isometric to body length until ∼ 137 cm (when some seals enter puberty) in body length then was highly positively allometric; mandibular and humeral size were negatively allometric to body length throughout growth. Bacula were more variable than mandibles or humeri. Bacular size in large specimens (>137 cm in body length) was related strongly to body length and weakly to age. We interpret bacular size to be an uncheatable honest indicator of male quality and viability. High bacular variation conforms with theoretical predictions of females' asymmetrical choice of mate and choice of extremes, and may reflect corresponding anatomical variation among females. Some bacular variation may also result incidentally from positive allometry coupled with lifelong bacular growth, which can amplify early differences between reproductive and somatic growth, enabled by weak selection on bacular form in relation to function.     

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.     

Allometric patterns of fetal head growth in mysticetes and odontocetes: Comparison of Balaena mysticetus and Stenella attenuata

Unlike other mammals, odontocetes and mysticetes have highly derived craniofacial bones. A growth process referred to as “telescoping” is partly responsible for this morphology. Here, we explore how changes in facial morphology during fetal growth relate to differences in telescoping between the adult odontocete Stenella attenuata and the mysticete Balaena mysticetus. We conclude that in both Stenella and Balaena head size increases allometrically. Similarly, odontocete nasal length and mysticete mouth size have strong positive allometry compared to total body length. However, the differences between odontocetes and mysticetes in telescoping are not directly associated with their fetal growth patterns. Our results suggest that cranial changes related to echolocation and feeding between odontocetes and mysticetes, respectively, begin during ontogeny before telescoping is initiated.     

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.     

The limits of elaboration: curved allometries reveal the constraints on mandible size in stag beetles

Many studies have demonstrated the adaptive advantage of elaborate secondary sexual traits, but few if any have shown compelling evidence for the limits to the elaboration of these traits that must exist. We describe such evidence in the exaggerated mandibles of stag beetles. In 1932, Huxley showed that the slope of the allometric relationship between mandible length and body size in some stag beetles declines in the largest males. We show that this curvature is most pronounced in species with relatively long mandibles, consistent with the hypothesis that the decrease in slope is caused by the increasing costs of large mandibles, which ultimately limit their size. Increasing depletion of resources in the prepupa and pupa by the rapidly growing mandibles is the most likely way in which these costs are manifested. The curved allometries have two components: intraspecific mandible allometry is steepest among small males of the species with the longest mandibles, but shallowest among the largest males of those same species. These patterns suggest that selection continues to favour positive allometry in species that invest relatively more in weaponry despite the limits to mandible exaggeration being reached in the largest males.     

Mandibular shape correlates of tooth fracture in extant Carnivora: implications to inferring feeding behaviour of Pleistocene predators

Percentages of tooth fracture and mandible shape are robust predictors of feeding habits in Carnivora. If these parameters co‐vary above the species level, more robust palaeobiological inferences could be made on fossil species. A test of association is presented between mandible shape and tooth fracture in a subset of extant carnivorans together with large Pleistocene fossil predators from Rancho La Brea (Canis dirus, Panthera atrox, and Smilodon fatalis). Partial least square (PLS) and comparative methods are employed to validate co‐variation of these two parameters in extant carnivorans. Association between mandible shape and percentage of tooth fracture is strongly supported, even if both blocks of data exhibit a phylogenetic signal to a different degree. Dietary adaptations drive shape/fracture co‐variation in extant species, although no significant differences occur in the PLS scores between carnivores and bone/hard food consumers. The fossil species project into PLS morphospace as outliers. Their position suggests a unique feeding behaviour. The increase in the size of prey, together with consumption of skin and hair from carcasses in a cold environment, might have generated unusual tooth breakage patterns in large predators from Rancho La Brea. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 70–80.     

Early Development and Orientation of the Acoustic Funnel Provides Insight into the Evolution of Sound Reception Pathways in Cetaceans

Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.     

滇金丝猴,藏酋猴和毛耳猴下颌骨的异速生长

本文对滇金丝猴(Rhinopithecus bieti)、藏酋猴(Macaca thibetana)和毛耳猴(Macacamulatta lasiota)下颌骨的33项指标进行了测量.经分析,下颌骨的生长存在有部位间、左右间及类群间的差异。表明这些动物下颌骨形态因适应某种生态环境而可能存在某些相似性,但因其食物性质、取食行为、系统及个体发育过程中存在差异而出现不同的生长模式。     

The scaling of tongue projection in the veiled chameleon,Chamaeleo calyptratus

Within a year of hatching, chameleons can grow by up to two orders of magnitude in body mass. Rapid growth of the feeding mechanism means that bones, muscles, and movements change as chameleons grow while needing to maintain function. A previous morphological study showed that the musculoskeletal components of the feeding apparatus grow with negative allometry relative to snout–vent length (SVL) in chameleons. Here, we investigate the scaling of prey capture kinematics and muscle physiological cross-sectional area in the veiled chameleon, Chamaeleo calyptratus. The chameleons used in this study varied in size from approximately 3 to 18 cm SVL (1–200 g). Feeding sequences of 12 chameleons of different sizes were filmed and the timing of movements and the displacements and velocities of the jaws, tongue, and the hyolingual apparatus were quantified. Our results show that most muscle cross-sectional areas as well as tongue and hyoid mass scaled with isometry relative to mandible length, yet with negative allometry relative to SVL. Durations of movement also scaled with negative allometry relative to SVL and mandible length. Distances and angles generally scaled as predicted under geometric similarity (slopes of 1 and 0, respectively), while velocities generally scaled with slopes greater than 0 relative to SVL and mandible length. These data indicate that the velocity of jaw and tongue movements is generally greater in adults compared to juveniles. The discrepancy between the scaling of cross-sectional areas versus movements suggests changes in the energy storage and release mechanisms implicated in tongue projection.     

Modulation in the feeding prey capture of the ant-lion, Myrmeleon crudelis

Ant-lions are pit-building larvae (Neuroptera: Myrmeleontidae), which possess relatively large mandibles used for catching and consuming prey. Few studies involving terrestrial arthropod larva have investigated prey capture behavior and kinematics and no study has shown modulation of strike kinematics. We examined feeding kinematics of the ant-lion, Myrmeleon crudelis, using high-speed video to investigate whether larvae modulate strike behavior based on prey location relative to the mandible. Based on seven capture events from five M. crudelis, the strike took 17.60 ± 2.92?msec and was characterized by near-simultaneous contact of both mandibles with the prey. Modulation of the angular velocity of the mandibles based on prey location was clearly demonstrated. M. crudelis larvae attempted to simultaneously contact prey with both mandibles by increasing mean angular velocity of the far mandible (65 ± 21?rad?sec(-1) ) compared with the near mandible (35 ± 14?rad?sec(-1) ). Furthermore, kinematic results showed a significant difference for mean angular velocity between the two mandibles (P<0.005). Given the lengthy strike duration compared with other fast-striking arthropods, these data suggest that there is a tradeoff between the ability to modulate strike behavior for accurate simultaneous mandible contact and the overall velocity of the strike. The ability to modulate prey capture behavior may increase dietary breadth and capture success rate in these predatory larvae by allowing responsive adjustment to small-scale variations in prey size, presentation, and escape response.     

Dental anomaly in a fossil squalodont dolphin from New Zealand,and the evolution of polydonty in whales

Abstract

A fragment of mandible of an indeterminate squalodontid dolphin (Upper Oligocene or lowermost Miocene, New Zealand) has 2 anomalous single-rooted teeth intercalated between typically squalodontid anterior cheek-teeth. The anomalous teeth are considered to be truly supernumerary, and not homologous with any erupted teeth in phylogenetically earlier Cetacea. This type of anomaly appears not to have been reported previously for any fossil cetacean. Polydonty, a characteristic of extant odontocetes, was probably attained initially in primitive odontocetes by intercalation of permanent and deciduous teeth, and later was elaborated by the addition of supernumerary teeth. The present specimen represents a morphological (but not phylogenetic) stage between odontocetes with limited and advanced polydonty. Some fossil mysticetes and embryonic extant mysticetes are also polydont, but mysticete polydonty and that of odontocetes have probably evolved convergently.     

Jaw morphology and function in living and fossil old world monkeys

This allometric investigation on a sample of 29 cercopithecine and 22 colobine taxa augments the data and implications of prior work on subfamilial variation in mandibular form and function in recent Cercopithecidae. To increase the size range encompassed by living cercopithecines and colobines, I included many of the larger-bodied fossil specimens. These analyses serve to fill a gap in our understanding of size-related changes in masticatory function and symphyseal morphology and curvature in extant and extinct Old World monkeys. Results of subfamilial scaling comparisons indicate that for a given jaw length, colobines possess significantly more robust corpora and symphyses than those of cercopithecines, especially at smaller sizes. Following from previous work, the most plausible explanation for why the subfamilies differ in relative corporeal and symphyseal dimensions is that colobine mandibles experience elevated loads and greater repetitive loading during mastication due, on average, to processing a diet of tough leaves and/or seeds. Although colobines have relatively larger symphyses, subfamilial analyses of symphyseal curvature demonstrate that they evince less symphyseal curvature vis-à-vis cercopithecines of a common size. Moreover, both subfamilies exhibit similar allometric changes in the degree of curvature, such that larger-bodied Old World monkeys have more curved symphyses than those of smaller taxa. Subfamilial scaling analyses also indicate that colobines possess a shorter M2 bite-point length relative to masseter lever-arm length, but not versus temporalis lever-arm length. Thus, as compared to cercopithecines, colobines can recruit less masseter-muscle force to produce similar bite forces during mastication. In both clades, M² bite-point length scales with positive allometry relative to masseter lever-arm length, such that larger species are less efficient at generating molar bite forces. This seems especially important due to the lack of subfamily difference in M² bite-point:temporalis lever-arm scaling (which is isometric across cercopithecids). A consideration of extinct cercopithecids indicates that many of the large-bodied papionins have more robust corpora, due perhaps to a diet which was of similar toughness to that of extant and extinct colobines. However, the biomechanical arrangements of the masseter and temporalis in all but one fossil cercopithecine and all of the fossil colobine specimens are much as predicted for a subfamilial member of its skull size. That most large-bodied papionins with tougher diets nonetheless maintain a less efficient jaw-muscle configuration may be due to stronger offsetting selection for increased relative canine size and gape.     

Osteological morphometrics of Australian chelonioid turtles

Extant and fossil Australian chelonioid turtles were examined for 57 osteological morphometric variables. Data were analysed using principal components analysis and canonical variates analysis, after Burnaby isometric 'size' removal, as well as multivariate allometry. Results indicate that Lepidochelys spp. are proportionately differentiated from other Cheloniidae. The majority of chelonioid osteological variables scale isometrically, with less than a third exhibiting positive or negative allometry. Skull length and width, postero-ventral skull, mandible length, scapular and pubic variables are found to be useful for differentiating between extant and extinct chelonioids. Skull length and width, mandible height, jaw symphysis length, premaxilla height, femoral length, scapular, pelvic, plastral and rib variables are established as useful differentiators of cheloniids. Australian fossil protostegids are morphometrically more similar to cheloniids than dermochelyids, and no cranial morphometric evidence could be found for the presence of more than one protostegid species. Some osteological allometric variables may be valuable for use in determining the relationships of chelonioids; however these should be examined in conjunction with morphology-based cladistic analyses to test established phylogenies.