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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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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
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... 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.
... Although some aquatic animals raptorially seize and bite prey, this is often combined with ram ingestion (where the predator acquires food by overtaking it via rapid locomotion) and by striking with protrusible body parts such as a flexible neck or jaws. Still, many general reviews of aquatic mammal feeding (Werth, 2000b;Marshall & Goldbogen, 2015;Hocking et al., 2014;Hocking et al., 2017a, b;Kienle et al., 2017;Marshall & Pyenson, 2019) rightly point out that aquatic animals frequently utilize a combination of mechanisms to ingest, transport, and process (and expel excess water from) prey. For example, gray whales, Eschrichtius robustus, are unique among baleen whales in using intraorally generated suction to draw prey into the mouth, but then like other mysticetes they trap their prey and purge unwanted water via filter feeding. ...
... In short, aquatic mammals are often resourceful opportunists, but even when specialized their foraging often combines multiple means of collecting and processing prey items, complicating simplistic schemes of feeding classification. Hocking et al. (2017a) argued that aquatic mammalian feeding strategies fall along a behavioral continuum that may reflect evolutionary history, with terrestrial feeding preceding semi-aquatic feeding, followed by increasingly specialized (in terms of form, function, and behavioral ecology) raptorial, suction, and filter feeding, but others (notably Kienle et al., 2017) dispute the likelihood of evolution following such a linear sequence. Crucially, Hocking et al. (2017b) distinguish foraging strategies (such as raptorial feeding) where water can be seen as an encumbrance from more specialized strategies (suction and filtration) where water is an essential tool needed to acquire food. ...
... Although some aquatic animals raptorially seize and bite prey, this is often combined with ram ingestion (where the predator acquires food by overtaking it via rapid locomotion) and by striking with protrusible body parts such as a flexible neck or jaws. Still, many general reviews of aquatic mammal feeding (Werth, 2000b;Marshall & Goldbogen, 2015;Hocking et al., 2014;Hocking et al., 2017a, b;Kienle et al., 2017;Marshall & Pyenson, 2019) rightly point out that aquatic animals frequently utilize a combination of mechanisms to ingest, transport, and process (and expel excess water from) prey. For example, gray whales, Eschrichtius robustus, are unique among baleen whales in using intraorally generated suction to draw prey into the mouth, but then like other mysticetes they trap their prey and purge unwanted water via filter feeding. ...
... In short, aquatic mammals are often resourceful opportunists, but even when specialized their foraging often combines multiple means of collecting and processing prey items, complicating simplistic schemes of feeding classification. Hocking et al. (2017a) argued that aquatic mammalian feeding strategies fall along a behavioral continuum that may reflect evolutionary history, with terrestrial feeding preceding semi-aquatic feeding, followed by increasingly specialized (in terms of form, function, and behavioral ecology) raptorial, suction, and filter feeding, but others (notably Kienle et al., 2017) dispute the likelihood of evolution following such a linear sequence. Crucially, Hocking et al. (2017b) distinguish foraging strategies (such as raptorial feeding) where water can be seen as an encumbrance from more specialized strategies (suction and filtration) where water is an essential tool needed to acquire food. ...
Several mammalian lineages, most notably cetaceans, sirenians, and pinnipeds, have independently reverted to the marine environment of their long-ago, pre-mammalian ancestors. Other mammals have also adapted to coastal, estuarine, or freshwater habitats. These include various members of the Carnivora and Rodentia, along with some other living and extinct mammals. Because water is dense, heavy, viscous, and incompressible, feeding in water poses challenges, especially for animals whose ancestors evolved in terrestrial settings. Many secondarily aquatic mammals separately adopted similar functional and structural solutions to acquire, ingest, and process food, particularly suction feeding, filter feeding, raptorial (“seizing”) grasping of prey, or adaptations to remove prey from benthic sediments. This led to striking examples of convergence with other mammals or with other aquatic animals, including sharks, bony fishes, marine reptiles, and birds. Most instances of convergence involve close similarities in jaws, dentition, and musculature, overall shape of the head and mouth, methods for separating food from water, and neural and behavioral adaptations to locate and capture prey. Following discussion of basic principles underlying aquatic mammalian feeding, we outline numerous examples of convergence in extant and extinct taxa.
... The balaenid whales, including bowhead and right whales, employ a skim filter feeding style in which they capture plankton from the water by swimming slowly with their mouth open [67]. In another filtering mode, the grey whale (Eschrichtius robustus) feeds mainly on benthic invertebrates that it ingests by swimming along the seabed on one side, using lateral suction feeding to take in sediment plus prey [5,68,69]. ...
Full-text available
Modern baleen whales are unique as large-sized filter feeders, but their roles were replicated much earlier by diverse marine reptiles of the Mesozoic. Here, we investigate convergence in skull morphology between modern baleen whales and one of the earliest marine reptiles, the basal ichthyosauromorph Hupehsuchus nanchangensis, from the Early Triassic, a time of rapid recovery of life following profound mass extinction. Two new specimens reveal the skull morphology especially in dorsal view. The snout of Hupehsuchus is highly convergent with modern baleen whales, as shown in a morphometric analysis including 130 modern aquatic amniotes. Convergences in the snout include the unfused upper jaw, specialized intermediate space in the divided premaxilla and grooves around the labial margin. Hupehsuchus had enlarged its buccal cavity to enable efficient filter feeding and probably used soft tissues like baleen to expel the water from the oral cavity. Coordinated with the rigid trunk and pachyostotic ribs suggests low speeds of aquatic locomotion, Hupehsuchus probably employed continuous ram filter feeding as in extant bowhead and right whales. The Early Triassic palaeoenvironment of a restrictive lagoon with low productivity drove Hupehsuchus to feed on zooplankton, which facilitated ecosystem recovery in the NanzhangYuan’an Fauna at the beginning of the Mesozoic.
... 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.
... Eisenberg (1981) provided one of the first attempts to more finely describe the full range of diversity in mammalian feeding behavior using a classification scheme with 16 states, each of which was based on a dominant food item (i.e. a specialization). These categori-426 cal states have been further refined over time by workers specializing on more restricted clades, each of which may exhibit their own range of unique predatory and dietary behaviors (Boyer, 2008;Fulwood et al., 2021;Kienle et al., 2017;Slater, 2015;Slater et al., 2010;Toljagić et al., 2018; 429 Van Valkenburgh, 1988;Verde Arregoitia and D'Elía, 2021;Williams and Kay, 2001). Still, it is apparent that most mammals make use of a mixture of food types and that dietary variation is more continuously distributed than the most complicated categorical classifications are able to 432 permit (Pineda-Munoz and Alroy, 2014). ...
Full-text available
Morphology often relates to ecology in a well-defined manner, enabling prediction of ecological roles for taxa that lack direct observations, such a fossils. Diet is a particularly important component of a species' ecology. However, in order to predict diet it must first be codified, and establishing metrics that effectively summarize dietary variability without excessive information loss remains challenging. We employed a dietary item relative importance coding scheme to derive multivariate dietary classifications for a sample of extant carnivoran mammals, and then used Bayesian multilevel modeling to assess whether these scores could be predicted from a set of dental metrics, with body size as a covariate. There is no "one size fits all" model for predicting dietary item importance; different topographical features best predict different foods at different body sizes, and model-averaged estimates perform especially well. We show how models derived from living taxa can be used to provide novel insights into the dietary diversity of extinct carnivoran species. Our approach need not be limited to diet as an ecological trait of interest, to these phenotypic traits, or to carnivorans. Rather, this framework serves as a general approach to predicting multivariate ecology from phenotypic traits.
Odontocetes first appeared in the fossil record by the early Oligocene, and their early evolutionary history can provide clues as to how some of their unique adaptations, such as echolocation, evolved. Here, three new specimens from the early to late Oligocene Pysht Formation are described further increasing our understanding of the richness and diversity of early odontocetes, particularly for the North Pacific. Phylogenetic analysis shows that the new specimens are part of a more inclusive, redefined Simocetidae, which now includes Simocetus rayi , Olympicetus sp. 1, Olympicetus avitus , O. thalassodon sp. nov., and a large unnamed taxon (Simocetidae gen. et sp. A), all part of a North Pacific clade that represents one of the earliest diverging groups of odontocetes. Amongst these, Olympicetus thalassodon sp. nov. represents one of the best known simocetids, offering new information on the cranial and dental morphology of early odontocetes. Furthermore, the inclusion of CCNHM 1000, here considered to represent a neonate of Olympicetus sp., as part of the Simocetidae, suggests that members of this group may not have had the capability of ultrasonic hearing, at least during their early ontogenetic stages. Based on the new specimens, the dentition of simocetids is interpreted as being plesiomorphic, with a tooth count more akin to that of basilosaurids and early toothed mysticetes, while other features of the skull and hyoid suggest various forms of prey acquisition, including raptorial or combined feeding in Olympicetus spp., and suction feeding in Simocetus . Finally, body size estimates show that small to moderately large taxa are present in Simocetidae, with the largest taxon represented by Simocetidae gen. et sp. A with an estimated body length of 3 m, which places it as the largest known simocetid, and amongst the largest Oligocene odontocetes. The new specimens described here add to a growing list of Oligocene marine tetrapods from the North Pacific, further promoting faunistic comparisons across other contemporaneous and younger assemblages, that will allow for an improved understanding of the evolution of marine faunas in the region.
Cetaceans are atypical mammals whose tongues often depart from the typical (basal) mammalian condition in structure, mobility, and function. Their tongues are dynamic, innovative multipurpose tools that include the world's largest muscular structures. These changes reflect the evolutionary history of cetaceans' secondary adaptation to a fully aquatic environment. Cetacean tongues play no role in mastication and apparently a greatly reduced role in nursing (mainly channeling milk ingestion), two hallmarks of Mammalia. Cetacean tongues are not involved in drinking, breathing, vocalizing, and other non-feeding activities; they evidently play no or little role in taste reception. Although cetaceans do not masticate or otherwise process food, their tongues retain key roles in food ingestion, transport, securing/positioning, and swallowing, though by different means than most mammals. This is due to cetaceans' aquatic habitat, which in turn altered their anatomy (e.g., the intranarial larynx and consequent soft palate alteration). Odontocetes ingest prey via raptorial biting or tongue-generated suction. Odontocete tongues expel water and possibly uncover benthic prey via hydraulic jetting. Mysticete tongues play crucial roles driving ram, suction, or lunge ingestion for filter feeding. The uniquely flaccid rorqual tongue, not a constant volume hydrostat (as in all other mammalian tongues), invaginates into a balloon-like pouch to temporarily hold engulfed water. Mysticete tongues also create hydrodynamic flow regimes and hydraulic forces for baleen filtration, and possibly for cleaning baleen. Cetacean tongues lost or modified much of the mobility and function of generic mammal tongues, but took on noteworthy morphological changes by evolving to accomplish new tasks.
Morphology often reflects ecology, enabling the prediction of ecological roles for taxa that lack direct observations, such as fossils. In comparative analyses, ecological traits, like diet, are often treated as categorical, which may aid prediction and simplify analyses but ignores the multivariate nature of ecological niches. Furthermore, methods for quantifying and predicting multivariate ecology remain rare. Here, we ranked the relative importance of 13 food items for a sample of 88 extant carnivoran mammals and then used Bayesian multilevel modeling to assess whether those rankings could be predicted from dental morphology and body size. Traditional diet categories fail to capture the true multivariate nature of carnivoran diets, but Bayesian regression models derived from living taxa have good predictive accuracy for importance ranks. Using our models to predict the importance of individual food items, the multivariate dietary niche, and the nearest extant analogs for a set of data-deficient extant and extinct carnivoran species confirms long-standing ideas for some taxa but yields new insights into the fundamental dietary niches of others. Our approach provides a promising alternative to traditional dietary classifications. Importantly, this approach need not be limited to diet but serves as a general framework for predicting multivariate ecology from phenotypic traits.
Marine mammals underwent a dramatic series of morphological transformations throughout their evolutionary history that facilitated their ecological transition to life in the water. Pinnipeds are a diverse clade of marine mammals that evolved from terrestrial carnivorans in the Oligocene (∼27 Ma). However, pinnipeds have secondarily lost the dental innovations emblematic of mammalian and carnivoran feeding, such as a talonid basin or shearing carnassials. Modern pinnipeds do not masticate their prey, but can reduce prey size through chopping behavior. Typically, small prey are swallowed whole. Nevertheless, pinnipeds display a wide breadth of morphology of the post-canine teeth. We investigated the relationship between dental morphologies and pinniped feeding by measuring the puncture performance of the cheek-teeth of seven extant pinniped genera. Puncture performance was measured as the maximum force and the maximum energy required to puncture a standardized prey item (Loligo sp). We report signficant differences in the puncture performance values across the seven genera, and identify three distinct categories based on cheek-teeth morphology and puncture performance: effective, ineffective, and moderate puncturers. In addition, we measured the overall complexity of the tooth row using two different metrics, Orientation Patch Count Rotated (OPCR) and Relif Index (RFI). Neither metric of complexity predicted puncture performance. Finally, we discuss these results in the broader context of known pinniped feeding strategies and lay the groundwork for subsequent efforts to explore the ecological variation of specific dental morphologies.
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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.