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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:
20171035.
http://dx.doi.org/10.1098/rspb.2017.1035
Received: 19 May 2017
Accepted: 27 July 2017
Subject Category:
Evolution
Author for correspondence:
Sarah S. Kienle
e-mail: skienle@ucsc.edu
The accompanying reply can be viewed at
http://dx.doi.org/10.1098/rspb.2017.1836.
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.3882961.
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
1
Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 95060, USA
2
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.
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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
intermittent
filter feeding
suctiongrip and tearpierce feedingcrushing
suctionbiting
continuous
suction filter
feedin
g
Figure 2. Overview of feeding strategies and subcategories in marine mammals. (Online version in colour.)
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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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biting
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feeding
blue whale (Balaenoptera musculus)
sperm whale (Physeter macrocephalus)
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.)
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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 . ...
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... 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). ...
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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.
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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 http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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