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Food caching by a marine apex predator, the (Hydrurga leptonyx)

Journal: Canadian Journal of Zoology

Manuscript ID cjz-2018-0203.R1

Manuscript Type: Note

Date Submitted by the 01-Oct-2018 Author:

Complete List of Authors: Krause, Douglas; NOAA Fisheries Southwest Fisheries Science Center, Antarctic Ecosystem Research Division Rogers, Tracey; University of New South Wales, School of Biological, Earth and DraftEnvironmental Science Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?:

food hoarding, food storage, intraspecific competition, behavior, Keyword: CARNIVORES < Taxon, pilfering, leopard seal (Hydrurga leptonyx)

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Food caching by a marine apex predator, the leopard seal (Hydrurga leptonyx)

Douglas J. Krause (DJK)1* and Tracey L. Rogers (TLR)2

1Antarctic Ecosystem Research Division, NOAA Fisheries-Southwest Fisheries Science Center,

8901 La Jolla Shores Dr., La Jolla, California, United States of America. Email:

[email protected].

2 Evolution & Research Centre, School of BEES, University of New South Wales,

Sydney, Sydney NSW, 2052, . Email: [email protected]. Draft

*Corresponding author: Douglas J. Krause, (858) 546-5675, [email protected]

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Food caching by a marine apex predator, the leopard seal (Hydrurga leptonyx)

Douglas J. Krause (DJK) and Tracey L. Rogers (TLR)

Abstract

The foraging behaviors of apex predators can fundamentally alter ecosystems through cascading predator-prey interactions. Food caching is a widely-studied, taxonomically-diverse behavior which can modify competitive relationships and affect population viability. We address predictions that food caching would not be observed in the marine environment by summarizing recent caching reports from two marine and one marine reptile . We also provide multiple caching observations from disparate locations for a fourth marine predator, the leopard seal (Hydrurga leptonyx (de Blainville, Draft1820)). Drawing from consistent patterns in the terrestrial literature, we suggest the unusual diversity of caching strategies observed in leopard seals is due to high variability in their polar marine habitat. We hypothesize that caching is present across the spectrum of leopard seal social dominance; however, prevalence is likely to increase in smaller, less-dominant that hoard to gain competitive advantage. Given the importance of this behavior, we draw attention to the high probability of observing food caching behavior in other marine species.

Keywords: food hoarding, food storage, intraspecific competition, foraging behavior, pilferage, carnivore, leopard seal, Hydrurga leptonyx.

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Introduction

Rapid shifts in the abundance or foraging behavior of apex predators can fundamentally alter

ecosystems through cascading predator-prey interactions (Paine 1966; Dayton et al. 1995;

Ballance et al. 2006; Estes et al. 2011). The behavioral mechanisms of large marine predators, in

particular, are important to understand because ecosystem-level changes may be induced by

relatively few individuals (Estes et al. 1998; Williams et al. 2004). Food caching, for example, is

a widely-studied, taxonomically-diverse behavior which can modify competitive relationships

and affect population viability (Vander Wall 1990). Draft For carnivores, food caching describes a satiated predator that continues to kill prey and either

store or defend it for later consumption (Vander Wall 1990). Food caching, also called hoarding

or storage, is a behavioral hedge against resource competition (Andersson and Krebs 1978) and

is associated with variable food availability (Smith and Reichman 1984). Caching manifests

differently depending upon the species, resource, and environment, but successful strategies are

driven by a need to prevent pilfering or to tolerate pilfering by recovering other caches

reciprocally (Vander Wall and Jenkins 2003). While many birds and small engage in

reciprocal pilfering, large carnivorous mammals typically take a larder hoarding approach with

one or a few large prey items that they: 1) hide (e.g., Gulo gulo (Linnaeus, 1758),

spotted Crocuta crocuta (Erxleben, 1777), red vulpes (Linnaeus, 1758),

leopards pardus (Linnaeus, 1758)) (Haglund 1966; Kruuk 1972; Macdonald 1976;

Eltringham 1979), 2) defend (e.g., lions Panthera leo (Linnaeus, 1758)) (Schaller 1972), or 3)

both (e.g., mountain lions concolor (Linnaeus, 1771), brown arctos

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(Linnaeus, 1758), Weddell seals Leptonychotes weddellii (Lesson, 1826)) (Hornocker 1970;

Elgmork 1982; Kim et al. 2005).

Although a taxonomically-broad spectrum of terrestrial birds and mammals store food (Roberts

1979; Sherry 1985), it has only recently been reported for marine animals. In fact, Smith and

Reichman (1984) erroneously suggested marine carnivores likely do not cache food due to low environmental variability in marine habitats. Marine environments do not lack environmental variability; however, predator-prey size dynamics frequently differ. Compared to terrestrial carnivorous mammals, fully-aquatic (e.g., whales and dolphins) and semi-aquatic (e.g., seals and sea lions) mammals typically select small prey relative to their body size (Tucker and Rogers

2014a, 2014b; Tucker et al. 2016). SmallDraft prey are swallowed whole obviating the need to process food into smaller meals and, accordingly, the need to protect an uneaten carcass from pilfering. Unsurprisingly, reported marine food caching species feed upon large prey, typical of the predator-prey body mass relationships of terrestrial mammals. In the northeastern Pacific transient killer whales (Orcinus orca (Linnaeus, 1758)) were reported to kill and then return on subsequent days to feed on the submerged carcasses of gray whales (Eschrichtius robustus

(Lilljeborg, 1861)) (Barrett-Lennard et al. 2011). And, while Weddell seals target a variety of prey sizes, they have been observed in the Ross Sea caching and defending large (~1 m)

Antarctic toothfish (Dissostichus mawsoni Norman, 1937) in breathing holes (Kim et al. 2005;

Ponganis and Stockard 2007). Similarly, salt water crocodiles (Crocodylus porosus Schneider,

1801) more frequently cache their largest prey items including agile wallaby (Macropus agilis

(Gould, 1841)) and water buffalo (Bubalus bubalis (Linnaeus, 1758)) (Doody 2009).

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Leopard seals (Hydrurga leptonyx (de Blainville, 1820)) are numerous, apex mammalian

predators within Antarctic and sub-Antarctic coastal ecosystems (Laws 1984; Rogers 2017).

Their large size and gape, maneuverability, wide distribution, and carnivorous-and-plankton-

sieving dentition (Hamilton 1939; Kooyman 1981; Rogers 2017) enable them to exploit a range

of prey from Antarctic ( superba Dana, 1852) to seabirds, otariids, and phocids

(Siniff and Stone 1985; Hall-Aspland and Rogers 2004). Their affinity for consuming other seals

is unrivaled among , and they have a demonstrated ability to effect Antarctic seal

( gazella (Peters, 1875)) abundance (Boveng et al. 1998; Goebel and Reiss 2014).

The leopard seal, like the , is one of the few marine mammals that consumes large

prey relative to its body size (Tucker andDraft Rogers 2014a,b; Tucker et al. 2016). As such they are

an ideal candidate to display food caching behavior. A recent study at Cape Shirreff in the

Antarctic Peninsula identified scavenging behavior that suggested food caching (Krause et al.

2015). Here we provide multiple, geographically-diverse observations (Table 1) confirming that

leopard seals engage in all three carnivoran caching behaviors: hiding, defense, and a

combination of both. Given that any single terrestrial species typically employs only one caching

strategy (Sherry 1985), the intraspecific variety of leopard seal food caching behaviors is

notable.

Methods and Results

With exceptions (e.g., Rogers and Bryden 1995, Vera et al. 2005), there have been few studies

dedicated to observing leopard seal foraging behavior. The majority of leopard seal caching

observations reported here were obtained opportunistically during daylight hours. These

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observations were made visually from above the waterline and frequently by biologists focused on other taxa. -borne cameras deployed by Krause et al. (2015) provided the first continuous, underwater surveillance of foraging leopard seals. Based on those recordings of cache recoveries, these historical reports from other Antarctic programs were offered.

According to multiple (n=11), independent observations (Table 1), leopard seals employ food caching strategies across disparate Antarctic locations. These include seals using either one or a combination of food-hiding (n=6 observations; e.g., hiding kills in ice leads or kelp beds and returning later to consume), direct defense (n=1 observation; e.g., hauling out with the carcass,

Figure 1), or a dual guarding and storage (n=4 observations; e.g., hiding carcasses in ice leads but remaining close and patrolling, FigureDraft 2) strategies.

Discussion

Leopard seal food caching behavior has been reported regularly in recent decades across a wide geographical area. The relatively low number of observations likely relates to the opportunistic surveillance, and the limitations of land-based observations of marine predators that are often submerged.

However, non-dedicated observers saw caching consistently, and underwater recordings revealed a high rate (3 of 7 animals studied, Krause et al. 2015) of occurrence. This suggests that the behavior is prevalent despite being difficult to observe using traditional methods.

In general, caching strategies are adapted in light of food type, available microhabitats, competition type (intra- versus interspecific), and intensity (Smith and Reichman 1984; Vander

Wall 1990). Therefore, it is plausible that the unusual plasticity observed in leopard seal caching

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behavior is a result of adaption to an elevated variety of prey, habitat, and competition. In fact,

leopard seal diets are considered to be catholic (Laws 1984; Hall-Aspland and Rogers 2004),

although there may be prey specialization by individuals (Krause et al. 2015). Their circum-

Antarctic distribution is vast and variable, ranging from within the pack ice (Rogers et al. 2005;

Meade et al. 2015) up through the sub-Antarctic Islands (Southwell et al. 2012; Rogers 2017).

Leopard seals are territorial to varying degrees, and they typically process and consume their

kills at the water’s surface (Kooyman 1965; Rogers and Bryden 1995). As such, competition for

prey items is both inter- and intraspecific. For example, leopard seals thrash, vocalize at, and

chase predatory birds, including brown (Stercorarius antarcticus (Lesson, 1831)), giant

petrels (Macronectes giganteus (Gmelin,Draft 1789)), and Wilson’s storm petrels (Oceanites

oceanicus (Kuhl, 1820)) to reduce scavenging of their food. Intraspecific competition has also

been observed, particularly in high density areas (Rogers and Bryden 1995; Hiruki et al. 1999;

Vera et al. 2005; Krause et al. 2015). Densities of this typically-solitary predator range from

0.003 seals/km2 near the pack ice edge (Rogers and Bryden 1997; Southwell et al. 2008) to over

68.6 seals/km2 near and penguin colonies at Cape Shirreff in the

(Krause et al. 2015). These concentrations are two orders of magnitude higher than previous

regional surveys (Forcada et al. 2012). Niche partitioning is a hallmark of carnivoran

competition (Hairston et al. 1960; Palomares and Caro 1999) and, evidence of prey, spatial, and

temporal niche partitioning was observed at Cape Shirreff (Krause et al. 2016).

When prey is limited there is adaptive advantage to caching. The resultant competitive

asymmetry allows hoarding animals to gather a larger share of the resource because they are not

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restrained by food consumption rate (Vander Wall 1990). Additionally, species which demonstrate preferred foraging times (e.g., the leopard seal, Krause et al. 2016) may decouple prey acquisition and consumption to maximize access during peak periods (Sherry 1985). This strategy may also reduce kleptoparasitism, or direct prey theft, especially for short-term hoarders

(Balme et al. 2017). Therefore, temporal decoupling is a likely driver of caching behavior in high density leopard seal foraging grounds where kleptoparasitism has been consistently observed

(Hiruki et al. 1999; Vera et al. 2005; Krause et al. 2015; Forcada (personal communication,

2018)).

Conclusions Draft

Given the consistent observation of food caching by leopard seals, it is likely a widely adapted behavior. This catalog of observations is demure and variable; however, some patterns emerge.

In areas of low to moderate intraspecific competition, leopard seals show a preference for larder hoarding in or under coastal ice or in kelp beds; where neither are available, caches are submerged in shallow water and secured with rocks (Table 1). At high densities they tend to hide prey. Given that social dominance within a species or guild can play an integral role in determining caching strategy (Brodin et al. 2001), we hypothesize that the choice to hide or defend a cache will be driven by an individual’s dominance. As intraspecific competition increases and larder hoarding becomes untenable, the prevalence of hiding prey underwater and away from prey acquisition sites is likely to increase (Vander Wall 1990). Finally, we expect caching to be more prevalent in smaller, less dominant animals that hoard to gain competitive advantage and reduce the incidence of kleptoparasitism (Balme et al. 2017). Overall, it is likely

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that variability in the leopard seal’s polar marine habitat and conspecific density necessitates a

greater diversity of caching strategies compared to terrestrial bioregions.

Despite earlier predictions that food caching would not be observed in the marine environment

(Smith and Reichman 1984), the last decade provides convincing evidence for caching in one

marine reptile and three species--all of which exhibit atypical predator-prey

body size strategies (Tucker and Rogers 2014a, 2014b; Tucker et al. 2016). Considering the

importance of these foraging behaviors, we draw attention to the high probability of observing

food caching in other marine species. As more attention is focused and as bio-logging tools

improve (Cooke et al. 2004; Rutz and Hays 2009), observations are likely to increase. We

anticipate other marine mammals employDraft food caching; particularly those which target large,

preservable prey (e.g., gray seals Halichoerus grypus (Fabricius, 1791), polar bears Ursus

maritimus Phipps, 1774, other killer whale ecotypes). Additional observations and manipulated

experiments are needed to test these hypotheses and illustrate behavioral mechanisms such as

cache location cues or the potential presence of reciprocal pilfering.

Acknowledgements

This note was greatly improved by suggestions and comments from P. Dayton, R. Pitman, J. Forcada and

two anonymous reviewers. We are grateful to K. Pietrzak, M. Mudge, J. Wright, N. Cook, M.

Zimmerman, M. Goh, T. Joyce, N. Pussini, D. Vejar, J. Hinke, K. Abernathy, T. Joyce, G. Marshall, A.

Kroeger, N. de Gracia, M. Klostermann, W. Archibald, W. Taylor, S. Woodman, J. Senzer and NOAA

AMLR program leader M. Goebel for their assistance in the field. The financial, infrastructure

and logistical support of the US-AMLR Program made this work possible. Leopard seal interactions and

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observations at Cape Shirreff were conducted in accordance with Marine Mammal Protection Act Permit

No. 16472 granted by the Office of Protected Resources, National Marine Fisheries Service, the Antarctic

Conservation Act Permit Nos. 2012-005, and the NMFS-SWFSC Institutional Animal Care and Use

Committee Permit No. SWPI2011-02.

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predators in ecological communities. Ecology, 85(12): 3373-3384. Draft

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Figure 1. A male leopard seal (Hydrurga leptonyx, nicknamed “Melvin”) that hauled out on a beach at Bird Island, with a recently- killed, uneaten gentoo penguin (Pygoscelis papua) and defended it from scavenging birds. Photo credit: S. Tarrant British Antarctic Survey.

Figure 2. An adult leopard seal (Hydrurga leptonyx) near Elephant Rocks, Antarctica consuming a small portion (~10%) of a recently-killed southern (Mirounga leonina) pup. The rest of the carcass was cached nearby. Photo credit: B. Cook.

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Table 1. Observations of food caching behaviors by leopard seals (Hydrurga leptonyx). Source Sex, Prey Location, Relative Caching Behavior Age Class Species Year Leopard Seal Strategy Density Patrolled within 10 meters of a previously-killed, partially- Krause et al. (2015), Cape stripped emperor penguin in an ice lead. That seal made P. Ponganis and G. Female, EMPE Washington, Low B aggressive movements and vocalizations when researchers Marshall pers. comm. Adult 2011 approached the penguin carcass, and it eventually consumed (2014) the carcass (photo in Krause et al. 2015). B. Cook et al., pers. Unknown, DeLaca Island, Submerged and stored a dead SES pup carcass under an SES Low B Comm. (2018) Adult 2016 iceberg; Defended and later consumed it. B. Cook et al., pers. Unknown, Elephant Rocks, Killed a SES pup, and stored most of the carcass while it SES Low B Comm. (2018) Adult 2017 consumed a small portion (ca. 10%) at the surface (Figure 2). Bird Island, Fed on a SES pup carcass in a series of 1-2 hour bouts over J. Forcada pers. comm. Female, SES South Georgia, Medium B the course of 3 days in the same location, proximate to (2018) Adult 2008 shallow kelp beds where the prey may have been stored. Bird Island, Carried dead penguin in its mouth as it hauled out onto a S. Tarrant pers. comm. Male, GEPE South Georgia, Medium D rocky beach. It defended the prey from snowy sheathbills (2016) Juvenile Draft 2016 (Figure 1). Female, Prydz Bay, Stored a WS pup in an ice lead and fed on over the course of 2 This manuscript WS Medium H Adult 2001 days. Regularly observed killing and eating SES pups. Observers Female, Heard Island, believed that after initially feeding, the leopard seal hid the This manuscript SES Medium H Adult 1990’s SES carcasses under rocks underwater. She returned to feed on the carcasses over the course of days. Carried a recently killed, unprocessed penguin into the Cape Shirreff, intertidal zone, hid the penguin under a large rock, and hauled Female, This manuscript CHPE Livingston High H out above the cache. The low tide exposed the cache while the Adult Island 2015 animal slept. The seal departed during the next high tide and the cached penguin was gone by the following low tide.

Of the 7 leopard seals carried animal-borne video cameras, Cape Shirreff, Female, AFS, three were observed to eat previously-hidden, submerged Krause et al. (2015) Livingston High H Adult UNPE carcasses (1 UNPE, 2 AFS) from coastal, shallow water Island 2013-14 benthos (18-32 m). Prey Species: gentoo penguin (Pygoscelis papua, GEPE), (Pygoscelis antarcticus,CHPE), emperor penguin (Aptenodytes forsteri, EMPE), unidentified penguin (UNPE), Antarctic fur seal (Arctocephalus gazella), Weddell seal (Leptonychotes weddellii, WS), southern elephant seal (Mirounga leonina, SES). Relative Leopard Seal Density is a subjective category based on a locations relative position within the range of reported leopard seal densities across the Antarctic and sub-Antarctic. Caching Strategy: Defense (D), Hiding (H), or Both hiding and defense (B).

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Figure 1. A male leopard seal (Hydrurga leptonyx, nicknamed “Melvin”) that hauled out on a beach at Bird Island, South Georgia with a recently-killed, uneaten gentoo penguin (Pygoscelis papua) and defended it from scavenging birds. Photo credit: S. Tarrant British Antarctic Survey.

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Figure 2. An adult leopard seal (Hydrurga leptonyx) near Elephant Rocks, Antarctica consuming a small portion (~10%) of a recently-killed southernDraft elephant seal (Mirounga leonina) pup. The rest of the carcass was cached nearby. Photo credit: B. Cook.

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