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  • For Peer Review O

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    Olfactory enrichment in California sea lions (Zalophus

    californianus): An effective tool for captive welfare?

    Journal: Journal of Applied Animal Welfare Science

    Manuscript ID HAAW-2016-0004

    Manuscript Type: Zoo/Wildlife

    Keywords: Animal Welfare, California sea lions, Enrichment, Olfaction, Pinnipeds

    URL: http://mc.manuscriptcentral.com/jaaws Email: ken.shapiro@animalsandsociety.org

    Journal of Applied Animal Welfare Science

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    Running head: OLFACTORY ENRICHMENT IN CALIFORNIA SEA LIONS 1

    Olfactory Enrichment in California Sea Lions (Zalophus californianus): An

    Effective Tool for Captive Welfare?

    In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of

    sensory information, which cannot be replicated in captive environments. Therefore,

    unique procedures are necessary for the maintenance of physiological and psychological

    health in captive animals. The effects of introducing of natural scents to captive

    enclosures has been investigated in a variety of species, yet this has not been examined in

    marine mammals. This project explores the behavioral effect of scent added to the

    environment, with the goal of improving the welfare of captive sea lions. By introducing

    two scent types: 1.) Natural scents, found in their native environment, and 2.) Non-

    natural scents, not found in their native environment; this study examines not only scent

    enrichment but the possible evolutionary underpinnings of pinniped olfaction. Scent

    enrichment was found to significantly impact sea lion behavior as demonstrated by a

    reduction in pattern swimming, an increase in habitat utilization, and a reduction in

    stereotypical behavior. However, there were no differences in behavior between natural

    and non-natural scent conditions.

    Keywords: animal welfare, California sea lions, enrichment, olfaction, pinnipeds

    Page 1 of 21

    URL: http://mc.manuscriptcentral.com/jaaws Email: ken.shapiro@animalsandsociety.org

    Journal of Applied Animal Welfare Science

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    OLFACTORY ENRICHMENT IN CALIFORNIA SEA LIONS 2

    Olfactory stimulation in California sea lions (Zalophus californianus): An effective

    tool for captive welfare?

    Introduction

    In nature, wild animals encounter environmental stimulation from nearly infinite

    sources. However, captive environments simply cannot compete with this diversity. As a

    result, the environment must become more complex in order to maintain both the

    physiological and psychological wellbeing of captive wildlife such as California sea lions

    (Zalophus californianus; Carlstead, Seidensticker & Baldwin, 1991).

    Scent is critical for effective foraging (Apfelbach, 1992; Gittleman, 1991;

    Hughes, Price & Banks, 2010; Schwartz, Miller & Haroldson, 2003; Ylnen, Sundell,

    Tiilikainen, Eccard, & Horne, 2003), navigation (Rogers, 1988), and social behaviors

    (Beckoff, 1981; Rothman & Mech, 1979) within the caniform taxon, to which sea lions

    belong. For the majority of caniform species, environmental enrichment has focused on

    scent (i.e., Andrews & Ha, 2014; Kitchener & Asa, 2010; Leonard, 2008; Nelson, 2009;

    Price, 2010; Rafacz & Santymire, 2014; Schneider, Nogge, & Kolter, 2014). Despite

    extensive exploration of olfaction and scent enrichment in other caniform species, the

    behavioral effects of scent enrichment has not previously been examined in pinnipeds.

    Sea lions have maintained genes necessary for olfaction (Kishida, Kubota,

    Shirayama, & Fukami, 2007), as well as extensive nasal turbinates (Van Valkenburgh,

    Samuels, Bird, Fulkerson, Meachen Samuels, & Slater, 2011) indicating some need for

    scent detection to survive in the wild. Therefore, it is likely that sea lions are biologically

    prepared to obtain meaningful information from scents in their natural environment. For

    example, South African fur seals (Arctocephalus pusillus), closely related to California

    sea lions, have been shown to possess the capability to distinguish between chemically

    Page 2 of 21

    URL: http://mc.manuscriptcentral.com/jaaws Email: ken.shapiro@animalsandsociety.org

    Journal of Applied Animal Welfare Science

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    OLFACTORY ENRICHMENT IN CALIFORNIA SEA LIONS 3

    similar odorants when relevant to their natural environment (Laska, Lord, Selin, &

    Amundin, 2010). Thus, the introduction of natural scents into the environment may have

    a greater impact on behavior than would non-natural scents.

    The present study investigated whether scent can be utilized to enhance the

    captive environment for California sea lions by introducing both natural and non-natural

    scents and recording instances of abnormal and repetitive behavioral repertoires, called

    stereotypical behaviors. In this study, the following hypotheses were examined: (1) Scent

    enrichment will increase habitat utilization, indicated by a change in habitat usage

    patterns, and reduce stereotypic behavior patterns; (1a) If present, these trends will

    continue to be evident at both the enclosure and individual level; (2) Natural scents will

    have a greater effect on behavior than non-natural scents, as indicated by a stronger effect

    on habitat utilization patterns and a statistically significant difference in instances of

    stereotypical behaviors; (2a) These trends will continue to be evident at both the

    enclosure and individual level.

    Methodology

    Research was conducted at the Institute for Marine Mammal Studies (IMMS) in

    Gulfport, Mississippi. Subjects included four, two-year-old female California sea lions

    (Zalophus californianus). The sea lions were housed in pairs, with each enclosure

    displaying differences in pattern swims and stereotypical behaviors (Table 1).

    Scent enrichment was of two types, natural scents and non-natural scents. Natural

    scents were those that are likely to be present in the animals natural environment. Non-

    natural odorants were those that would be introduced through exposure to humans (Table

    2).

    Page 3 of 21

    URL: http://mc.manuscriptcentral.com/jaaws Email: ken.shapiro@animalsandsociety.org

    Journal of Applied Animal Welfare Science

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    OLFACTORY ENRICHMENT IN CALIFORNIA SEA LIONS 4

    Baseline Procedure

    To begin this study, researchers collected baseline data over the span of one week

    (six days) at IMMS. Researchers filmed one thirty-minute session in the morning, and

    one in the afternoon (to parallel the experimental pre- and post- sessions). To eliminate

    the confounding effect of a visual cue, this process included the introduction of a chalk

    mark on the wall (with no added scent) during baseline pre-sessions. No scent treatment

    was applied during the baseline post-session. In addition obtaining baseline data, the

    animals were able to habituate to the researchers presence prior to the experimental

    trials.

    Experimental Procedure: Natural and Non-Natural Scents

    Each trial consisted of a pre- and post-session. The pre-session data collection

    period consisted of video data taken thirty minutes prior to the introduction of scent

    stimulus. Similarly, the post-session data collection period consisted of video data taken

    thirty minutes after the introduction of the scent stimulus. This approach allowed for the

    assessment of the animals behavioral state prior to the introduction of scent enrichment,

    and any potential changes as a result of this intervention.

    Experimental trials were split into two scent types: natural and non-natural scents.

    A total of 8 scents were presented three times each, resulting in twenty-four trials for per

    animal (n = 4). Each trial consisted of a baseline pre-session in which a chalk mark was

    placed on the wall and a post-session in which the scent was applied on top of the chalk

    mark.

    The order of presentation and placement of these scents within the enclosure were

    pseudo-randomized. Each scent was presented once per cycle, and excluded placement

    Page 4 of 21

    URL: http://mc.manuscriptcentral.com/jaaws Email: ken.shapiro@animalsandsociety.org

    Journal of Applied Animal Welfare Science

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    OLFACTORY ENRICHMENT IN CALIFORNIA SEA LIONS 5

    on the fourth wall (which was located on the same wall as the researcher, and was

    obscured from view due to the film angle; see Figure 1). Trials were run simultaneously

    in both enclosures in order to avoid the scent being detected by animals in the adjacent

    enclosure. After the trial, the scent location was cleaned with a bleach solution to ensure

    the enclosure was free of the scent for the subsequent trial. One trial was executed each

    day so that the scent had been eliminated

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