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Revisiting the behavioural framework of feeding in predatory aquatic mammals

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Proceedings of the Royal Society B
Authors:
Sarah Kienle at Baylor University
Sarah Kienle
Chris J Law at University of Washington
Chris J Law
Daniel P Costa at University of California, Santa Cruz
Daniel P Costa
Annalisa Berta at San Diego State University
Annalisa Berta
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Comment
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.)
rspb.royalsocietypublishing.org Proc. R. Soc. B 284: 20171035
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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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  • Dec 2023
  • CURR BIOL
Toothed whales (odontocetes) emit high-frequency underwater sounds (echolocate)—an extreme and unique innovation allowing them to sense their prey and environment. Their highly specialized mandible (lower jaw) allows high-frequency sounds to be transmitted back to the inner ear. Echolocation is evident in the earliest toothed whales, but little research has focused on the evolution of mandibular form regarding this unique adaptation. Here, we use a high-density, three-dimensional geometric morphometric analysis of 100 living and extinct cetacean species spanning their ∼50-million-year evolutionary history. Our analyses demonstrate that most shape variation is found in the relative length of the jaw and the mandibular symphysis. The greatest morphological diversity was obtained during two periods of rapid evolution: the initial evolution of archaeocetes (stem whales) in the early to mid-Eocene as they adapted to an aquatic lifestyle, representing one of the most extreme adaptive transitions known, and later on in the mid-Oligocene odontocetes as they became increasingly specialized for a range of diets facilitated by increasingly refined echolocation. Low disparity in the posterior mandible suggests the shape of the acoustic window, which receives sound, has remained conservative since the advent of directional hearing in the aquatic archaeocetes, even as the earliest odontocetes began to receive sounds from echolocation. Diet, echolocation, feeding method, and dentition type strongly influence mandible shape. Unlike in the toothed whale cranium, we found no significant asymmetry in the mandible. We suggest that a combination of refined echolocation and associated dietary specializations have driven morphology and disparity in the toothed whale mandible.
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... 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]. ...
First filter feeding in the Early Triassic: cranial morphological convergence between Hupehsuchus and baleen whales
Article
Full-text available
  • Aug 2023
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.
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New Evidence of the Feeding Behaviors of Coronodon and the Origin of Filter Feeding in Mysticetes (Mammalia: Cetacea) Revisited
Article
Full-text available
Coronodon includes species of basal toothed mysticetes that were initially interpreted as engaging in raptorial feeding and dental filtration. Here, the feeding of this extinct genus is revisited based on recently described specimens and species. Associations between tooth position and types of dental wear were tested, and evidence for feeding behaviors was tabulated using scores from 14 craniodental characters, each mapped onto five alternate phylogenetic hypotheses. Individual character states were interpreted as being supportive, neutral, or contradictory evidence to raptorial feeding, suction feeding, baleen filtration, or dental filtration. Wear in Coronodon was found to be significantly more concentrated on mesial teeth, mesial cusps, higher cusps, and upper teeth. Upper teeth also had mesial cusps more worn than distal cusps, inconsistent with predictions of the dental filtration hypothesis. Wear in notches was correlated with wear on neighboring cusps, and side wear was concentrated on occlusal sides, suggesting both were caused by raptorial feeding. These observations raise the possibility that raptorial feeding was the primary, and maybe even the only, mode of feeding for Coronodon. The feeding scores of reconstructed ancestors leading to crown mysticetes typically display a stepwise decrease in raptorial feeding, a stepwise increase in baleen filtration, and, occasionally, an intermediate but weakly supported stage of dental filtration. For most toothed mysticetes, there is little evidence for or against suction feeding. The method we have developed for studying the origin of baleen can be expanded and allows for multiple hypotheses to be tested without undue emphasis on any particular taxon or set of characters.
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Tool use increases mechanical foraging success and tooth health in southern sea otters (Enhydra lutris nereis)
Article
  • May 2024
  • SCIENCE
Although tool use may enhance resource utilization, its fitness benefits are difficult to measure. By examining longitudinal data from 196 radio-tagged southern sea otters (Enhydra lutris nereis), we found that tool-using individuals, particularly females, gained access to larger and/or harder-shelled prey. These mechanical advantages translated to reduced tooth damage during food processing. We also found that tool use diminishes trade-offs between access to different prey, tooth condition, and energy intake, all of which are dependent on the relative prey availability in the environment. Tool use allowed individuals to maintain energetic requirements through the processing of alternative prey that are typically inaccessible with biting alone, suggesting that this behavior is a necessity for the survival of some otters in environments where preferred prey are depleted.
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Complex prey handling of octopus by bottlenose dolphins (Tursiops aduncus)
Article
Full-text available
  • Apr 2017
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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A behavioural framework for the evolution of feeding in predatory aquatic mammals
Article
Full-text available
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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Chew, shake, and tear: Prey processing in Australian sea lions (Neophoca cinerea)
Article
Full-text available
  • Dec 2016
  • MAR MAMMAL SCI
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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How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration
Article
Full-text available
  • Jan 2017
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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The better to eat you with: The comparative feeding morphology of phocid seals (Pinnipedia, Phocidae)
Article
  • Dec 2015
  • J ANAT
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.
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