Filtration area scaling and evolution in mysticetes: trophic niche partitioning and the curious cases of sei and pygmy right whales

Werth, Alexander J.; Potvin, J; Shadwick, Robert E.; Jensen, Megan M.; Cade, David E.; Goldbogen, Jeremy A.

doi:10.1093/biolinnean/bly121

Cited by 33 publications

(56 citation statements)

References 75 publications

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“…() noted that the zone of baleen growth (Zone 2) expands caudally in bowhead fetuses, possibly implying that this species also has a posterior‐to‐anterior baleen development pattern, even if the adult bowhead has a very different baleen rack structure compared with rorqual whales, due to their different filter‐feeding style (Werth et al. ). Given the available information and the phylogenetic position of these species, with the Balaenidae representing the earliest diverging mysticete lineage and the minke whale the earliest diverging lineage of Balaenopteridae (Gatesy et al.…”

Section: Discussionmentioning

confidence: 99%

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Prenatal developmental sequence of the skull of minke whales and its implications for the evolution of mysticetes and the teeth‐to‐baleen transition

Lanzetti

2019

Journal of Anatomy

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Baleen whales (Mysticeti) have an extraordinary fossil record documenting the transition from toothed raptorial taxa to modern species that bear baleen plates, keratinous bristles employed in filter-feeding. Remnants of their toothed ancestry can be found in their ontogeny, as they still develop tooth germs in utero. Understanding the developmental transition from teeth to baleen and the associated skull modifications in prenatal specimens of extant species can enhance our understanding of the evolutionary history of this lineage by using ontogeny as a relative proxy of the evolutionary changes observed in the fossil record. Although at present very little information is available on prenatal development of baleen whales, especially regarding tooth resorption and baleen formation, due to a lack of specimens. Here I present the first detailed description of prenatal specimens of minke whales (Balaenoptera acutorostrata and Balaenoptera bonaerensis), focusing on the skull anatomy and tooth germ development, resorption, and baleen growth. The ontogenetic sequence described consists of 10 specimens of both minke whale species, from the earliest fetal stages to full term. The internal skull anatomy of the specimens was visualized using traditional and iodine-enhanced computed tomography scanning. These highquality data allow detailed description of skull development both qualitatively and quantitatively using threedimensional landmark analysis. I report distinctive external anatomical changes and the presence of a denser tissue medial to the tooth germs in specimens from the final portion of gestation, which can be interpreted as the first signs of baleen formation (baleen rudiments). Tooth germs are only completely resorbed just before the eruption of the baleen from the gums, and they are still present for a brief period with baleen rudiments. Skull shape development is characterized by progressive elongation of the rostrum relative to the braincase and by the relative anterior movement of the supraoccipital shield, contributing to a defining feature of cetaceans, telescoping. These data aid the interpretation of fossil morphologies, especially of those extinct taxa where there is no direct evidence of presence of baleen, even if caution is needed when comparing prenatal extant specimens with adult fossils. The ontogeny of other mysticete species needs to be analyzed before drawing definitive conclusions about the influence of development on the evolution of this group. Nonetheless, this work is the first step towards a deeper understanding of the most distinctive patterns in prenatal skull development of baleen whales, and of the anatomical changes that accompany the transition from tooth germs to baleen. It also presents comprehensive hypotheses to explain the influence of developmental processes on the evolution of skull morphology and feeding adaptations of mysticetes.

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Section: Discussionmentioning

confidence: 99%

“…; Werth et al. ). Rorquals (Balaenopteridae) are the most speciose group of modern baleen whales (Berta et al.…”

Section: Introductionmentioning

confidence: 99%

Prenatal developmental sequence of the skull of minke whales and its implications for the evolution of mysticetes and the teeth‐to‐baleen transition

Lanzetti

2019

Journal of Anatomy

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“…Drag increases linearly with area, but with the square of velocity (Vogel, ). While the baleen area primarily affects drag forces and the outflow speed after water is filtered through the baleen (Potvin & Werth, ; Werth & Potvin, ; Werth et al, ), the mouth opening area affects the inflow volume of prey‐laden water. The trade‐offs in the relationship between mouth friction drag, area and speed have been illustrated by Potvin and Werth (); we present the estimated open‐mouth friction drag relative to bowhead whales (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…The bowhead whale is a closely related balaenid species with similar foraging ecology and behaviour to right whales; both target calanoid copepod prey by continuous ram filtration (Laidre, Heide-Jørgensen, & Nielsen, 2007;Pomerleau et al, 2011;Walkusz et al, 2012). Bowhead and right whales share similar morphology (Figures 8 and 9) but differ considerably in the magnitude of their gape area, as well as their baleen areas, widths and lengths for a similar body size (George et al, 2016;Lambertsen et al, 2005;Omura et al, 1969;Werth, 2004;Werth et al, 2018). We have shown that right whales slow to 1.1 (±0.3) m/s during presumed foraging bouts, faster than the estimate by Simon et al (2009) of 0.7 (±0.1) m/s for foraging bowhead whales.…”

Section: Previous Descriptions Of Right Whale Diving Behaviour In Deep-mentioning

confidence: 99%

Foraging rates of ram‐filtering North Atlantic right whales

et al. 2019

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North Atlantic right whales spend their summer months foraging primarily in American and Canadian Atlantic waters on high‐energy‐density prey. Here, they rapidly accumulate and store energy obtained within a few months to support future migrations and reproduction while fasting. High drag from their ram‐filter foraging strategy places a limit on what prey densities will be energetically efficient to target. Our understanding of the volume of prey‐laden water filtered by right whales during a dive or foraging bout, and what information they use to decide to forage or not, has been limited by the difficulties of measuring when they feed at depth, how fast they swim during continuous ram filtration and how often they might swallow accumulated prey. We used 10 DTAG deployments from right whales in the Bay of Fundy, Canada, to quantify swimming speeds and estimate the volume of prey‐laden water filtered per dive. We used the tag's inertial sensors to evaluate the timing of frequent biomechanical changes that likely indicate the truncation of continuous filtration, and whether the number or timing of these fluking bouts relates to longer feeding dives or other foraging decisions. During foraging dives, right whales descended at 1.4 (±0.2 SD) m/s and slowed to swim at 1.1 (±0.3) m/s while filtering. We found consistent pauses in the fluking behaviour of foraging right whales, every 56 (±22) s. Whales filtered on average 78 (±30) m3 of water per fluking bout and on average 673 (±201) m3 per dive. Right whales filter large volumes of water at low speeds with a high duty cycle, but require sufficiently high prey energy densities to compensate for a high‐drag foraging strategy. Closely related bowhead whales have a larger gape but swim more slowly, filtering greater volumes with lower drag. Our findings highlight that right whales acquire their energy in a relatively short period of intense foraging; even moderate changes in their feeding behaviour or their prey energy density are likely to negatively impact their yearly energy budgets and therefore reduce fitness substantially. A plain language summary is available for this article.

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“…Rorquals include humpback ( Megaptera novaeangliae ), fin ( Balaenoptera physalus ), and blue whales ( Balaenoptera musculus ), the largest animals that have ever lived. During ram‐propelled lunge feeding on schooling zooplankton and fish (Figure ), the mouth opens wide to engulf enormous volumes (5–80+ m 3 ) of prey‐laden water (Goldbogen, ; Goldbogen et al, ; Lambertsen, ; Pivorunas, ; Potvin, Goldbogen, & Shadwick, ; Werth et al, ; Werth & Ito, ).…”

Section: Introductionmentioning

confidence: 99%

Multiaxial movements at the minke whale temporomandibular joint

Werth

Ito

2020

Journal of Morphology

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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.

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Filtration area scaling and evolution in mysticetes: trophic niche partitioning and the curious cases of sei and pygmy right whales

Cited by 33 publications

References 75 publications

Prenatal developmental sequence of the skull of minke whales and its implications for the evolution of mysticetes and the teeth‐to‐baleen transition

Prenatal developmental sequence of the skull of minke whales and its implications for the evolution of mysticetes and the teeth‐to‐baleen transition

Foraging rates of ram‐filtering North Atlantic right whales

Multiaxial movements at the minke whale temporomandibular joint

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