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Cite this article: Kienle SS, Law CJ, Costa DP,
Berta A, Mehta RS. 2017 Revisiting the
behavioural framework of feeding in predatory
aquatic mammals. Proc. R. Soc. B 284:
Received: 19 May 2017
Accepted: 27 July 2017
Subject Category:
Author for correspondence:
Sarah S. Kienle
The accompanying reply can be viewed at
Electronic supplementary material is available
online at
Revisiting the behavioural framework of
feeding in predatory aquatic mammals
Sarah S. Kienle1, Chris J. Law1, Daniel P. Costa1, Annalisa Berta2
and Rita S. Mehta1
Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 95060, USA
Biology, San Diego State University, San Diego, CA 92182, USA
SSK, 0000-0002-8565-2870
Hocking et al. [1] (hereafter HEA) present a framework for defining and evalu-
ating feeding strategies in predatory aquatic mammals. While we appreciate the
review, we address three difficulties with the framework: (i) the tetrapod feed-
ing cycle needs minimal revision to accommodate aquatic mammals, (ii) the
proposed feeding strategies need further clarification and (iii) evolution
should not be described as a logical sequence. Our goal is to clarify and
expand on HEA’s feeding framework to ensure that predatory aquatic mammals
can be examined in a comparative framework with other tetrapods.
First, HEA argue that the four stages of the tetrapod feeding cycle—inges-
tion, intraoral transport, processing and swallowing [2]—do not adequately
address the problems faced by air-breathing aquatic mammals. HEA, therefore,
propose an alternative feeding cycle: (I) prey capture, (IIa) prey manipulation
and transport and (IIb) prey processing, (III) water removal and (IV) swallow-
ing. These changes constrain our ability to compare feeding behaviour across
tetrapod lineages. The tetrapod feeding cycle is already sufficiently flexible to
accommodate behaviourally diverse clades, so we propose using the existing
tetrapod feeding cycle [2] with some revisions based on HEA (figure 1).
In the tetrapod feeding cycle, ingestion encompasses all behaviours used to
capture, subdue, kill and process prey before it enters the oral cavity [2]. There-
fore, HEA’s stages I, IIa and IIb are already included in ingestion and can
distinguish between different behaviours prior to prey entering the mouth
(figure 1). For example, sea otters (Enhydra lutris) dive to grab benthic prey
(prey capture), move prey using their mouth/forepaws (prey manipulation)
and use tools/teeth to open hard-shelled prey (external prey processing) [3]. Fol-
lowing the existing tetrapod feeding cycle, intraoral transport (movement of food
inside the mouth towards the pharynx) occurs after ingestion and is followed by
1. Ingestion
prey manipulation external prey processing
2. Intraoral transport
3. Processing
4. Water removal
5. Swallowing
prey capture
Figure 1. Modified feeding cycle of aquatic tetrapods based on Schwenk [2] and Hocking et al. [1].
(Online version in colour.)
&2017 The Author(s) Published by the Royal Society. All rights reserved.
on September 27, 2017 from
intraoral processing (mechanical breakdown of food inside the
mouth) [2]. For most aquatic mammals, there is no intraoral
processing [1,4,5]. However, there are exceptions, as a few
species chew (some otariids) and others masticate (sea otters;
electronic supplementary material, table S1) [1,6,7]. We agree
with HEA’s addition of a water removal stage, which is
followed by swallowing (figure 1).
Under our revised framework, five stages—ingestion,
intraoral transport, processing, water removal and swallow-
ing—constitute the aquatic tetrapod feeding cycle (figure 1).
This revision retains all tetrapod feeding cycle stages [2], sub-
sumes HEA’s stages I– II under ingestion and incorporates
HEA’s water removal stage. These changes allow aquatic mam-
mals to be examined in the same framework as other tetrapods,
while providing the flexibility to accommodate these behav-
iourally diverse lineages. These stages are not static; animals
may not go through every feeding stage or follow this order
during each feeding event, and each stage can encompass a
range of behaviours.
Second, HEA describe five feeding strategies for predatory
aquatic mammals: semi-aquatic, raptorial, suction, suction
filter and ram filter feeding. The semi-aquatic strategy, defined
as when some feeding behaviours are performed at the surface,
does not follow the same convention as the other strategies
because it is defined by an animal’s position in the water
column rather than the behaviour(s) used during the feeding
cycle [1]. Under this definition, a humpback whale (Megaptera
novaeangliae) lunge feeding would be classified as afilter feeder
if underwaterand as a semi-aquatic feeder if it surfaced during
feeding. The classification of the same behaviour into two sep-
arate strategies leads us to conclude that semi-aquatic feeding
is not valid and should not be used. The four other feeding
strategies proposed by HEA are useful with some modifi-
cations. We have provided a revised glossary of terms
(electronic supplementary material, table S1).
Based on the tetrapod literature, we suggest three feeding
strategies for predatory aquatic mammals—suction, biting
and filter feeding—accompanied by subcategories (figure 2).
Suction is a common feeding strategy in aquatic mammals,
and we agree with HEA’s review.
We suggest that biting replace HEA’s raptorial strategy
because, while the terms are often used interchangeably, ‘rap-
torial’ is inconsistently defined; for example, raptorial refers to
predatory behaviour [8], biting [1,5] or rapidly moving appen-
dages [9]. We propose the addition of three subcategories
under biting (figure 2): (i) crushing—prey are fragmented by
the teeth during ingestion or intraoral processing. This is
exemplified by sea otters using molars to break down hard-
shelled prey [4,5]; (ii) grip and tear feeding—animals hold
prey with the jaws/forelimbs, shake prey and/or rip off smal-
ler pieces during ingestion. This category encompasses
multiple behaviours, including shake feeding and hold and
tear feeding [4,7,10], and has been documented in some odon-
tocetes [11], pinnipeds[7,12], polar bears (Ursus maritimus) [13]
and sea otters [6]; (iii) pierce feeding—animals bite prey during
ingestion, often swallowing prey whole with little manipu-
lation or external prey processing [10]. In pierce feeding,
suction can be used in combination with biting to pull prey
inside the mouth [14]; this has been described in some
pinnipeds and odontocetes [5,15,16].
In filter feeding a specialized structure is used to trap prey
in the mouth during water removal [5,17]. HEA define two
separate strategies: suction filter feeding and ram filter feed-
ing. We suggest nesting these terms under filter feeding
and that the word ‘ram’ (engulfing prey via ‘rapid accele-
ration of the whole body’ [18]) be avoided when naming
a feeding strategy because ram applies to most feeding
strategies and is inconsistently used [1,16,17]. Under our fra-
mework, filter feeding is first subdivided into two types:
continuous and intermittent ( figure 2) [5,17,19]. Continuous
filter feeders swim slowly and constantly through dense
prey patches with their mouths open and the prey passively
enters the oral cavity. Ingestion and water removal occur
simultaneously [17]. This behaviour is also called skim feed-
ing or continuous ram filter feeding and best exemplified by
balaenid whales [1,5,17]. By contrast, intermittent filter feed-
ers actively engulf a single mouthful of water during
ingestion and remove water via filtering structures during a
distinct water removal phase [17]. Intermittent filter feeding
can be further subdivided into lunge and suction filter feed-
ing based on the ingestion method (figure 2). Lunge feeding
(also called intermittent ram filter feeding, gulping and ram
gulping) is best exemplified by rorqual whales that swim
rapidly at a prey patch while opening their mouths to draw
in prey [5,17]. In suction filter feeding, animals such as gray
whales (Eschrichtius robustus) [20] and some phocids [21,22]
use suction to pull prey from the water or benthos into the
mouth. These changes highlight the repeated evolution of a
few feeding strategies in predatory aquatic mammals, while
also emphasizing the diversity of behaviours within each
strategy (figure 2).
Third, evolution is not a progression of linear events [23].
HEA use the phrases ‘logical sequence’ and ‘evolutionary
continuum’ to describe the evolution of feeding strategies in
skim feeding lunge feeding
filter feeding
suctiongrip and tearpierce feedingcrushing
suction filter
Figure 2. Overview of feeding strategies and subcategories in marine mammals. (Online version in colour.) Proc. R. Soc. B 284: 20171035
on September 27, 2017 from
predatory aquatic mammals, as depicted in their figure 3. This
incorrectly suggests that species have a tendency to become
increasingly specialized or complex over time [23]. HEA state
that filter feeding is the ‘most highly specialized’ aquatic feed-
ing strategy, which falsely suggests that all aquatic mammals
are predetermined to become filter feeders. This is not sup-
ported by the repeated evolution of biting and suction across
these disparate aquatic mammal lineages (figure 3).
Descriptions of individual feeding strategies as more or less
aquatic should be avoided. All strategies used by aquatic mam-
mals are aquatic and allow species to exploit different niches
and prey densities (figure 3).
Our recommendations are to (i) adopt our revised tetra-
pod feeding cycle ( figure 1), (ii) incorporate our revisions to
the glossary (electronic supplementary material, table S1),
(iii) use our feeding strategies and subdivisions (figure 2)
and (iv) model the evolution of feeding as a tree-like process
(figure 3). HEA’s review and the comments that they have
inspired provide a comprehensive framework that should
be adopted to refine our understanding of predatory aquatic
mammal feeding. Such a framework facilitates the investi-
gation of ecological mechanisms and evolutionary processes
in aquatic tetrapods.
Data Accessibility. Additional data are available as the electronic supp-
lementary material.
Authors’ contributions. All authors outlined the manuscript; S.S.K. drafted
it; C.J.L. designed the figures; all authors edited the manuscript
and gave final approval for publication.
Competing interests. We have no competing interests.
Funding. Funding for this work was provided by a NOAA Dr Nancy
Foster Scholarship and a Steve and Rebecca Sooy Graduate Fellow-
ship in Marine Mammals to S. S. K. and a NSF GRFP to C. J. L.
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blue whale (Balaenoptera musculus)
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orca (Orcinus orca)
Figure 3. Example framework for understanding the evolution of feeding
strategies in cetaceans under a tree-like process rather than a continuum.
Biting, suction and filter feeding are contemporary feeding strategies in
extant cetaceans. (Online version in colour.) Proc. R. Soc. B 284: 20171035
on September 27, 2017 from
... Early dolphins that lived 20 million years ago had long skulls and jaws that were filled with many small teeth [6][7][8] ; this skull morphology is associated with a type of biting called 'pierce feeding' where prey are bitten and then swallowed whole 9 . Pierce feeding is efficient for capturing small to medium-sized prey and is used by many disparate groups of marine mammals, including seals, sea lions, and toothed whales 9,10 . In contrast to pierce-feeding dolphins, both killer whales and false killer whales independently evolved skulls that were larger, blunter, and had fewer (but larger) teeth 6 ( Figure 1). ...
... In fact, false killer whales are named after killer whales because of this strong convergence in skull and dental morphology 4 . It turns out that large skulls with big teeth, along with a large body size, are adaptations for another type of biting called 'grip-and-tear feeding' 9 . In grip-and-tear feeding, medium to large prey are captured whole and then broken, ripped, shaken and torn into smaller pieces before swallowing. ...
... In grip-and-tear feeding, medium to large prey are captured whole and then broken, ripped, shaken and torn into smaller pieces before swallowing. Grip-and-tear feeding is most often associated with hunting large endothermic prey and, in addition to killer and false killer whales, is also used by some seals, sea lions and polar bears 9,10 . ...
A newly discovered fossil dolphin shows that modern killer and false-killer whales evolved from fish-eating ancestors. While today both species occasionally feed on large warm-blooded prey, including seals and other whales, this diet specialization has evolved only recently.
... Pinnipeds (along with all secondarily aquatic tetrapods) had to overcome a major obstacle in the land-to-water transition: capturing and consuming prey underwater (Kienle et al., 2017;Taylor, 1987;Werth, 2000). Prey capture underwater fundamentally differs from prey capture in air, as water is more viscous and denser than air. ...
... Prey capture underwater fundamentally differs from prey capture in air, as water is more viscous and denser than air. Pinnipeds have converged on three underwater feeding strategies: biting, filter feeding, and suction feeding (Hocking et al., 2017;Kienle et al., 2017;Taylor, 1987;Werth, 2000). Each of these feeding strategies is associated with specific skull and dental adaptations, feeding behaviors, and kinematics (Adam & Berta, 2002;Churchill & Clementz, 2015;Hocking et al., 2013Hocking et al., , 2015Hocking et al., , 2016Jones & Goswami, 2010;Jones et al., 2013;Kienle & Berta, 2016, 2018Kienle et al., , 2019Kienle et al., , 2020Marshall et al., 2008Marshall et al., , 2014. ...
... However, pinnipeds do not masticate, and this is also true for most marine mammals. Most prey is swallowed whole with little to no processing (Kienle et al., 2017;Taylor, 1987;Werth, 2000). Despite the lack of mastication, the mastication muscles in pinnipeds play an important role in prey capture and consumption. ...
Full-text available
Secondarily aquatic tetrapods have many unique morphologic adaptations for life underwater compared with their terrestrial counterparts. A key innovation during the land-to-water transition was feeding. Pinnipeds, a clade of air-breathing marine carnivorans that include seals, sea lions, and walruses, have evolved multiple strategies for aquatic feeding (e.g., biting, suction feeding). Numerous studies have examined the pinniped skull and dental specializations for underwater feeding. However, data on the pinniped craniofacial musculoskeletal system and its role in aquatic feeding are rare. Therefore, the objectives of this study were to conduct a comparative analysis of pinniped craniofacial musculature and examine the function of the craniofacial musculature in facilitating different aquatic feeding strategies. We performed anatomic dissections of 35 specimens across six pinniped species. We describe 32 pinniped craniofacial muscles—including facial expression, mastication, tongue, hyoid, and soft palate muscles. Pinnipeds broadly conform to mammalian patterns of craniofacial muscle morphology. Pinnipeds also exhibit unique musculoskeletal morphologies—in muscle position, attachments, and size—that likely represent adaptations for different aquatic feeding strategies. Suction feeding specialists (bearded and northern elephant seals) have a significantly larger masseter than biters. Further, northern elephant seals have large and unique tongue and hyoid muscle morphologies compared with other pinniped species. These morphologic changes likely help generate and withstand suction pressures necessary for drawing water and prey into the mouth. In contrast, biting taxa (California sea lions, harbor, ringed, and Weddell seals) do not exhibit consistent craniofacial musculoskeletal adaptations that differentiate them from suction feeders. Generally, we discover that all pinnipeds have well-developed and robust craniofacial musculature. Pinniped head musculature plays an important role in facilitating different aquatic feeding strategies. Together with behavioral and kinematic studies, our data suggest that pinnipeds’ robust facial morphology allows animals to switch feeding strategies depending on the environmental context—a critical skill in a heterogeneous and rapidly changing underwater habitat.
... Feeding morphology of extinct killer whales The feeding style of extant Orcinus orca and Pseudorca crassidens has been described as macroraptorial and grip-andtear 3,10,11 ; the former refers to capturing large prey with teeth, 12 whereas the latter refers to how the prey is broken into smaller pieces for consumption. 10,13 Overall, macroraptorial feeding in these taxa is associated with (1) large body size, reaching nine and six meters in length, respectively; (2) large temporal fossae; ...
... Its temporal fossa looks smaller than that of O. orca, although this region is only partially preserved in the only known skull of O. citoniensis. The rostrum of O. citoniensis is slightly longer and narrower than in O. orca, and the mandibular tooth count (14 teeth per dentary) corresponds to the maximum of the range observed in O. orca (10)(11)(12)(13)(14). The relative tooth sizes of extant and extinct species of Orcinus are comparable ( Figures 2B-2F). ...
The killer whale (Orcinus orca) and false killer whale (Pseudorca crassidens) are the only extant cetaceans that hunt other marine mammals, with pods of the former routinely preying on baleen whales >10 m in length and the latter being known to take other delphinids. Fossil evidence for the origins of this feeding behavior is wanting, although molecular phylogenies indicate that it evolved independently in the two lineages. We describe a new extinct representative of the killer whale ecomorph, Rododelphis stamatiadisi, based on a partial skeleton from the Pleistocene of Rhodes (Greece). Five otoliths of the bathypelagic blue whiting Micromesistius poutassou are associated with the holotype, providing unexpected evidence of its last meal. The evolutionary relationships of R. stamatiadisi and the convergent evolution of killer whale-like features were explored through a broad-ranging phylogenetic analysis that recovered R. stamatiadisi as the closest relative of P. crassidens and O. orca as the only living representative of a once diverse clade. Within the clade of Orca and kin, key features implicated in extant killer whale feeding, such as body size, tooth size, and tooth count, evolved in a stepwise manner. The tooth wear in Rododelphis and an extinct species of Orcinus (O. citoniensis) are consistent with a fish-based diet, supporting an exaptative Pleistocene origin for marine mammal hunting in both lineages. If correct, predation by the ancestors of Pseudorca and Orca did not play a significant role in the evolution of baleen whale gigantism.
... In extant crown mysticetes (baleen whales), tooth buds are expressed and then resorbed in fetal stages as baleen tissue begins to form (Ridewood 1923;Karlsen 1962;Ishikawa and Amasaki 1995;Thewissen et al. 2017;Lanzetti 2019). In completely edentulous neonates and adults, the keratinous baleen plates are arranged in racks that continuously grow from the left and right margins of the palate (Utrecht 1965;Fudge et al. 2009;Young et al. 2015), fray through abrasive wear, and permit efficient batch filter feeding via an array of behaviors -engulfment ('lunge'), benthic suction, and skimming (Werth 2000;Kienle et al. 2017) that are utilized singly or in combination by extant mysticetes. ...
Full-text available
The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CT scans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a 'transitional chimaeric feeder' scenario that best explains current evidence on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of ‘dental genes’ related to enamel formation before the emergence of crown Mysticeti, while ‘baleen genes’ that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti is one of the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.
... Based on these shared morphological characters, we propose for Zygophyseter and Acrophyseter a 'grip-and-shear' feeding strategy consisting of three phases: 1) grasping and piercing of the prey with the anterior teeth, 2) moving the food item backward along the mouth, and 3) cutting it with the posterior teeth. In Figure 3, this hypothetical trophic behaviour is integrated within the framework of feeding strategies proposed for extant marine mammals by Kienle et al. (2017) and Berta and Lanzetti (2020). It is our content that such a feeding strategy was also used by heterodont basilosaurids having anterior conical teeth (canine and incisors) and even more mediolaterally compressed posterior teeth (premolars and molars) (Uhen 2004;Fahlke 2012;Fahlke et al. 2013;Loch et al. 2015;Snively et al. 2015) and, as a plesiomorphic condition, by several heterodont basal neocetes (e.g., squalodontids; see Loch et al. 2015;Collareta et al. 2020a). ...
Full-text available
Differing from the extant physeteroids, macroraptorial sperm whales are currently regarded as apex predators of the Miocene seas based on several morphofunctional observations. Here, we estimate the bite force of Zygophyseter varolai, a macroraptorial physeteroid from lower upper Miocene strata of the Pietra leccese formation (Apulia, Italy) using the finite element analysis (FEA). To explore multiple bite scenarios, we set four different load cases on a 3D model of the cranium obtained via digital photogram-metry, considering the temporalis and masseter muscles as jaw adductors. Our FEA simulations indicate that Z. varolai exerted an anterior bite force of more than 4000 N and a posterior bite force of more than 10000 N. These values are similar to those estimated for other marine predators known for their powerful bite. This suggests that Z. varolai might have fed upon medium-sized marine vertebrates like other odontocetes. Considering the significant difference observed between the anterior and posterior bite forces, Z. varolai likely fed via 'grip-and-shear' feeding, snapping the food items with an anterior bite and then cutting them with a powerful posterior bite. Other macroraptorial sperm whales such as the roughly coeval Acrophyseter from Peru likely employed the same feeding technique. ARTICLE HISTORY
... Apparently, aquatic adaptations provided Carnivora of limited ecomorphological opportunities of diversification in a consistently different region of the morphospace (particularly for the mandible; see also: Polly, 2008). These ecological opportunities are bounded within the constraints associated with feeding in the water that includes, for aquatic carnivores: biting that implies crushing or pierce feeding, grip and tear of the prey and suction [framework originally proposed by Hocking et al. (2017), redefined by Kienle et al. (2017)]. Size evolution is equally bounded in pinnipeds due to the functional constraints imposed by the marine environment. ...
The mammalian order Carnivora is characterized by a broad taxonomic and ecological diversity. By using a large sample of extant species, we tested the impact of ecological factors on carnivoran skull (cranium and mandible) morphology, taking advantage of a combined geometric morphometrics and comparative method approach. We implemented several evolutionary models to account for different tempo and mode of evolution in size and shape data. These models validated the association between skull morphology and diet at the interspecific scale. The functional distinction between pinniped (aquatic) and fissiped (mostly terrestrial) taxa was found valid only in mandible shape and cranial size. High levels of morphological disparity and evolutionary rates were identified in specialized dietary groups, and positive association between rates and disparity was found for skull size. Cranium and mandible showed consistent patterns of covariation that reflect constrained functional processes, which stabilize the ecomorphological evolution of Carnivora. Aquatic adaptations allowed carnivorans to invade and persist within novel regions of the mandibular morphospace. This ecological shift did not increase morphological disparity but occurred at a faster rate than in terrestrial species. Those species exhibit a stronger level of cranio-mandibular covariation due to constraints imposed by more demanding masticatory adaptations.
... Despite this, fossil walrus diet, functional anatomy, and ecology still remain poorly studied. There is also substantial disagreement among researchers on how to describe and categorise methods of prey capture and stages of prey processing (Hocking et al., 2017b;Kienle et al., 2017), as well as a wide variety of feeding behaviours present in extant taxa, using cranial and dental modifications (Churchill and Clementz, 2015). Initial adaptations seen in walrus dentition are associated with the transition towards tooth usage focused on raptorial biting of fish prey (pierce-feeding) rather than mastication which had already been lost in their 'enaliarctine' ancestors (Churchill and Clementz, 2016). ...
The walrus (Odobenus rosmarus) is the last surviving representative of a diverse and successful family of pinnipeds. Walrus fossils are common and are represented by material ranging from complete skeletons to isolated skeletal and tusk fragments. They are typically preserved in inner and middle-shelf depositional environments. Walruses evolved from ‘enaliarctine’ ancestors, although whether they are more closely related to otariids (fur seals and sea lions) or phocids (earless seals) has been a matter of debate. The first walruses belong to a paraphyletic assemblage known as the ‘Imagotariinae’. These walruses were initially small in body size, but reached truly enormous sizes before giving rise to the Dusignathinae (double-tusked walruses) and Odobeninae (true walruses). Odobeninae are remarkable for the development of prominent tusks, specialisation in suction feeding and were the only clade to disperse into the North Atlantic. Several major trends can be observed in walrus evolution including: tooth simplification, acquisition of large body size, increased baculum size, development of tusks, and the development of an intermediate style of aquatic and terrestrial locomotion (ascompared to phocids and otariids). At least two separate dispersals into the North Atlantic from the North Pacific occurred via the Arctic Ocean, with Odobenus likely evolving in the North Pacific. Walruses, including Odobenus, showed a much greater tolerance for warmer climates in the past, which may imply some ability to adapt towards anthropogenic climate change.
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The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a transitional chimaeric feeder scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of dental genes related to enamel formation before the emergence of crown Mysticeti, while baleen genes that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.
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Understanding the trophic niches of marine apex predators is necessary to understand interactions between species and to achieve sustainable, ecosystem-based fisheries management. Here, we review the stable carbon and nitrogen isotope ratios for biting marine mammals inhabiting the Atlantic Ocean to test the hypothesis that the relative position of each species within the isospace is rather invariant and that common and predictable patterns of resource partitioning exists because of constrains imposed by body size and skull morphology. Furthermore, we analyze in detail two species-rich communities to test the hypotheses that marine mammals are gape limited and that trophic position increases with gape size. The isotopic niches of species were highly consistent across regions and the topology of the community within the isospace was well conserved across the Atlantic Ocean. Furthermore, pinnipeds exhibited a much lower diversity of isotopic niches than odontocetes. Results also revealed body size as a poor predictor of the isotopic niche, a modest role of skull morphology in determining it, no evidence of gape limitation and little overlap in the isotopic niche of sympatric species. The overall evidence suggests limited trophic flexibility for most species and low ecological redundancy, which should be considered for ecosystem-based fisheries management.
Living and fossil mammals are incredibly diverse in their feeding morphology and behaviours. For example, mammalian feeding adaptations range from filter feeding in whales to bats catching insects mid-flight. Mammals share aspects of their cranial morphology compared to other vertebrates including the bones of the skull, the dentition, the cheek and chewing muscles, the lips and the lip musculature, the palate, the tongue and the pharynx. In addition to their anatomy, mammals are behaviourally distinct from other vertebrates through their food-processing abilities inside and outside of the oral cavity, mastication, swallowing and the presence of suckling in infants. The appearance of these anatomical features and adaptations associated with these behaviours are key to distinguishing the earliest mammals in the fossil record. Key Concepts • Mammals are distinguished through aspects of their craniodental anatomy and their feeding behaviours. • Feeding in adult mammals can be divided into four stages: preingestion, ingestion, food transport and swallowing. • Ingestion is constrained by size and mechanical properties of the food item. • Infant mammals use two feeding stages: suckling and swallowing. • Early fossil mammals are distinguished by adaptations to the feeding system.
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Marine predators use prey handling behaviors that are best suited to the proper- ties (e.g., size, shape, and texture) of the prey species being targeted (Hocking et al. 2016, 2017). Predators that target large prey species that cannot be swal- lowed whole are required to process prey extensively before consumption (either breaking it into smaller pieces or softening it). For example, crocodiles and alliga- tors perform a spinning “death roll” to dismember large prey items (Fish et al. 2007). Leopard seals (Hydrurga leptonyx) thrash sea birds and seal pups to break them into edible pieces (Edwards et al. 2010). Australian fur seals (Arctocephalus pusillus doriferus) shake and toss large fish and cephalopods before consumption (Hocking et al. 2016). Similarly, for toothed whales, if prey items are too large to swallow whole they also need to spend time processing prey. For example, killer whales (Orcinus orca) shake sea lions and beluga whales (Delphinapterus leucas) (Lopez and Lopez 1985, Frost et al. 1992), and toss dusky dolphins (Lagenor- hynchus obscurus) and stingrays into the air (Constantine et al. 1998, Visser 1999). Bottlenose dolphins (Tursiops spp.) shake and toss fish to break them into smaller pieces and to soften them for ease of consumption (W€ursig and W€ursig 1979, Shane 1990). Bottlenose dolphins also use complex prey handling to break giant cuttlefish (Sepia apama) into manageable pieces, using a sequence of steps to remove the head, ink, and cuttlebone before the flesh of the mantle is consumed (Finn et al. 2009, Smith and Sprogis 2016). Prey handling behaviors vary among species and locations and are influenced by the availability of prey species. In this study, we describe the complex prey handling behavior of benthic octopus by T. aduncus in southwestern Australia. We investigate whether this behavior is (1) associated with specific ecological variables, (2) is age- or sex-specific, and (3) is a socially learned behavior.
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Extant aquatic mammals are a key component of aquatic ecosystems. Their morphology, ecological role and behaviour are, to a large extent, shaped by their feeding ecology. Nevertheless, the nature of this crucial aspect of their biology is often oversimplified and, consequently, misinterpreted. Here, we introduce a new framework that categorizes the feeding cycle of predatory aquatic mammals into four distinct functional stages (prey capture, manipulation and processing, water removal and swallowing), and details the feeding behaviours that can be employed at each stage. Based on this comprehensive scheme, we propose that the feeding strategies of living aquatic mammals form an evolutionary sequence that recalls the land-to-water transition of their ancestors. Our newconception helps to explain and predict the origin of particular feeding styles, such as baleen-assisted filter feeding in whales and raptorial ‘pierce’ feeding in pinnipeds, and informs the structure of present and past ecosystems.
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Pinnipeds generally target relatively small prey that can be swallowed whole, yet often include larger prey in their diet. To eat large prey, they must first process it into pieces small enough to swallow. In this study we explored the range of prey-processing behaviors used by Australian sea lions (Neophoca cinerea) when presented with large prey during captive feeding trials. The most common methods were chewing using the teeth, shaking prey at the surface, and tearing prey held between the teeth and forelimbs. Although pinnipeds do not masticate their food, we found that sea lions used chewing to create weak points in large prey to aid further processing and to prepare secured pieces of prey for swallowing. Shake feeding matches the processing behaviors observed in fur seals, but use of forelimbs for " hold and tear " feeding has not been previously reported for other otariids. When performing this processing method, prey was torn by being stretched between the teeth and fore-limbs, where it was secured by being squeezed between the palms of their flippers. These results show that Australian sea lions use a broad repertoire of behaviors for prey processing, which matches the wide range of prey species in their diet.
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Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time. Expected final online publication date for the Annual Review of Marine Science Volume 9 is January 03, 2017. Please see for revised estimates.
One adaptation crucial to the survival of mammalian lineages that secondarily transitioned from land to water environments was the ability to capture and consume prey underwater. Phocid seals have evolved diverse feeding strategies to feed in the marine environment, and the objectives of this study were to document the specialized feeding morphologies and identify feeding strategies used by extant phocids. This study used principal component analysis (PCA) to determine the major axes of diversification in the skull for all extant phocid taxa and the recently extinct Caribbean monk seal (n = 19). Prey data gathered from the literature and musculoskeletal data from dissections were included to provide a comprehensive description of each feeding strategy. Random Forest analysis was used to determine the morphological, ecological and phylogenetic variables that best described each feeding strategy. There is morphological evidence for four feeding strategies in phocids: filter; grip and tear; suction; and pierce feeding. These feeding strategies are supported by quantitative cranial and mandibular characters, dietary information, musculoskeletal data and, for some species, behavioral observations. Most phocid species are pierce feeders, using a combination of biting and suction to opportunistically catch prey. Grip and tear and filter feeding are specialized strategies with specific morphological adaptations. These unique adaptations have allowed leopard seals (Hydrurga leptonyx) and crabeater seals (Lobodon carcinophaga) to exploit novel ecological niches and prey types. This study provides the first cranial and mandibular morphological evidence for the use of specialized suction feeding in hooded seals (Cystophora cristata), northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The most important variables in determining the feeding strategy of a given phocid species were cranial and mandibular shape, diet, and phylogeny. These results provide a framework for understanding the evolution and adaptability of feeding strategies employed by extant phocid species, and these findings can be applied to other pinniped lineages and extinct taxa.