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Revisiting the behavioural framework of feeding in predatory aquatic mammals

September 2017
Proceedings of the Royal Society B: Biological Sciences 284(1863):20171035

DOI:10.1098/rspb.2017.1035

Authors:

Sarah Kienle

Baylor University

Chris J Law

University of Texas at Austin

Daniel P Costa

University of California, Santa Cruz

Annalisa Berta

San Diego State University

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Modified feeding cycle of aquatic tetrapods based on Schwenk [2] and Hocking et al. [1]. (Online version in colour.)

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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

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.)

on September 27, 2017http://rspb.royalsocietypublishing.org/Downloaded 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

intermittent

filter feeding

suctiongrip and tearpierce feedingcrushing

suctionbiting

continuous

suction filter

feedin

Figure 2. Overview of feeding strategies and subcategories in marine mammals. (Online version in colour.)

rspb.royalsocietypublishing.org Proc. R. Soc. B 284: 20171035

on September 27, 2017http://rspb.royalsocietypublishing.org/Downloaded 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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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.

A behavioural framework for the evolution of feeding in predatory aquatic mammals

Article

Full-text available

Mar 2017
Proc Biol Sci

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.

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.

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.

Evolution of prey capture strategies and diet in the Pinnipedimorpha (Mammalia, Carnivora)

Article

Full-text available

Jan 2002

Polar Bears

Book

Jan 1990

Ian Stirling

A review of gray whale feeding ecology

Article

Jan 1984

M. Nerini

Habits of the southern sea otter

Article

E.M. Fisher

A Review of Gray Whale Feeding Ecology

Article

Jan 2012

M. Nerini

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.