Will Brookfield Zoo Have Elephants Again

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Open Access

Peer-reviewed

Research Article

Elephant Management in North American Zoos: Environmental Enrichment, Feeding, Do, and Preparation

• Cheryl L. Meehan,
• Lance J. Miller,
• David J. Shepherdson,
• Kari A. Morfeld,
• Jeff Andrews,
• Anne M. Bakery,
• Kathy Carlstead,
• Joy A. Mench

Elephant Management in Northward American Zoos: Environmental Enrichment, Feeding, Exercise, and Training

• Brian J. Greco,
• Cheryl L. Meehan,
• Lance J. Miller,
• David J. Shepherdson,
• Kari A. Morfeld,
• Jeff Andrews,
• Anne M. Baker,
• Kathy Carlstead,
• Joy A. Mench

x

• Published: July 14, 2016
• https://doi.org/10.1371/journal.pone.0152490

Figures

Abstract

The management of African (Loxodonta africana) and Asian (Elephas maximus) elephants in zoos involves a range of practices including feeding, do, training, and environmental enrichment. These practices are necessary to meet the elephants' nutritional, healthcare, and husbandry needs. However, these practices are not standardized, resulting in likely variation among zoos also every bit differences in the way they are applied to individual elephants within a zoo. To characterize elephant direction in North America, we collected survey data from zoos accredited by the Association of Zoos and Aquariums, adult 26 variables, generated population level descriptive statistics, and analyzed them to place differences attributable to sex and species. Sixty-vii zoos submitted surveys describing the direction of 224 elephants and the training experiences of 227 elephants. Asian elephants spent more time managed (defined as interacting directly with staff) than Africans (hateful time managed: Asians = 56.9%; Africans = 48.vi%; p<0.001), and managed time increased by 20.2% for every twelvemonth of age for both species. Enrichment, feeding, and do programs were evaluated using diversity indices, with mean scores beyond zoos in the midrange for these measures. There were an average of 7.ii feedings every 24-hour catamenia, with but i.ii occurring during the nighttime. Feeding schedules were predictable at 47.5% of zoos. We also calculated the relative apply of rewarding and aversive techniques employed during training interactions. The population median was seven on a scale from one (representing but aversive stimuli) to nine (representing only rewarding stimuli). The results of our study provide essential information for understanding management variation that could be relevant to welfare. Furthermore, the variables we created have been used in subsequent elephant welfare analyses.

Citation: Greco BJ, Meehan CL, Miller LJ, Shepherdson DJ, Morfeld KA, Andrews J, et al. (2016) Elephant Management in Due north American Zoos: Environmental Enrichment, Feeding, Practise, and Preparation. PLoS Ane 11(7): e0152490. https://doi.org/10.1371/journal.pone.0152490

Editor: Elissa Z. Cameron, University of Tasmania, AUSTRALIA

Received: June 1, 2015; Accepted: March 15, 2016; Published: July xiv, 2016

Copyright: © 2016 Greco et al. This is an open up access article distributed under the terms of the Creative Eatables Attribution License, which permits unrestricted use, distribution, and reproduction in whatsoever medium, provided the original writer and source are credited.

Information Availability: For reasons relating to protection of the facilities and animals included in this study, admission restrictions utilise to the private-level information underlying the findings. A data set of de-identified, population-level information is available at doi: ten.6084/m9.figshare.3383554.

Funding: Funding for this work was provided past a National Leadership Grant to the Honolulu Zoological Society from the Institute of Museum and Library Services (www.imls.gov) grant number: LG-25-10-0033-10. Employers provided fiscal support in the form of authors' salaries as follows: Oregon Zoo (DS); Chicago Zoological Lodge-Brookfield Zoo (LM); Busch Gardens (JA); Lincoln Children'due south Zoo and Smithsonian's National Zoo (KM); Honolulu Zoo (KC). Later on the IMLS-funded catamenia of performance (November 2010 – December 2013) Enlightened Institute provided support in the form of salaries for author CM. The specific roles of these authors are articulated in the 'author contributions' department. Neither the funders nor authors' employers had any role in written report pattern, information collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: LM is affiliated with the Chicago Zoological Society – Brookfield Zoo (an AZA-accredited zoo), DS is affiliated with Oregon Zoo (an AZA-Accredited zoo), and JA is affiliated with Busch Gardens (an AZA-accredited zoo). KC was employed past the Honolulu Zoo (an AZA-accredited zoo) at the time of the report. KM is affiliated with the Smithsonian National Zoo (an AZA-accredited zoo) and was employed past the Lincoln Children's Zoo (an AZA-accredited zoo) at the fourth dimension of the written report. JM is a member of the PLOS ONE Brute Research Advisory Grouping. CM and BG are affiliated with Aware Institute. AWARE Institute is a commercial entity founded past CM in 2014 and provides animal welfare cess, inquiry and teaching services to zoos and aquariums. These interests exercise non modify the authors' adherence to all the PLOS 1 policies on sharing data and materials, every bit detailed online in the guide for authors.

Introduction

In that location is significant interest within and beyond the zoological community in agreement the management of Asian (Elephas maximas) and African (Loxodonta africana) elephants in zoos, especially as it relates to evaluating practices that are relevant to welfare [1,2], such equally feeding, training, exercise, husbandry and environmental enrichment. While these practices are required elements of all elephant programs accredited by the Association of Zoos and Aquariums (AZA) [3], they are not standardized. Because they are not standardized, there may be significant variation among zoos with respect to daily care, which could in turn touch elephant welfare.

Assessing elephant management at the population level requires the evolution of systematic methods for measuring and quantifying these varying practices. Notwithstanding, little research has been conducted that either describes management practices or compares them across multiple zoos. This lack of inquiry on direction has been cited as ane of the major impediments to formally assessing the welfare of zoo animals [iv].

In addition to gaining an understanding of the direction of zoo elephants in full general, information technology is also important to empathise how management practices differ betwixt African and Asian elephant zoo populations. 1 might expect the two species to exist managed differently given that they are adapted to different ecological niches [5,6] and may have different life history characteristics. For instance, a larger proportion of Asian elephants (38%) than African elephants (21%) in Northward American zoos are captive born [7] and, for those elephants imported from dwelling house range countries, Asian elephants are more likely to have previous captive experiences than African elephants [8]). Similarly, ane might also expect management practices to be shaped by the different physiological (east.g., size, reproductive cycles, metabolic demands) and behavioral (eastward.thou., social development and grouping dynamics) characteristics of female person and male elephants [5].

This paper focuses on the development and analysis of management variables relating to feeding, exercise, preparation and enrichment. The dual purpose was to provide a comprehensive review of elephant management in zoos and to generate appropriate independent variables to exist used in subsequent epidemiological analyses of behavioral [ix–11], physiological [12], and wellness-related [13,14] welfare indicators. A like approach was taken in a related paper that characterizes the housing and social management of these same elephants [15].

Our study focused on feeding, enrichment, exercise and training, because enquiry in many species demonstrates that animals' experiences of these components of managed care play a critical function in their welfare. In the remainder of the introduction, we present the rationale for investigating each management category in the context of welfare assessment.

Management Schedules

Direction routines can vary considerably at the zoo and individual elephant level depending on staffing, management philosophy, and the needs of each elephant. Still, AZA accreditation standards [iii] require that all elephants participate in an exercise program, beliefs training, and a variety of husbandry activities including baths, foot and pare care, and physical assessments. Each of these activities requires staff to collaborate directly with the elephants. When not interacting with staff members, elephants spend fourth dimension independently, housed either lone or in social groups of varying sizes and compositions [15] and in enclosures that are visible (on exhibit) or not visible (off showroom) to the public.

Management schedules may accept important implications for elephant welfare. For instance, elephants who spend more than time interacting with staff may perceive healthcare or medical procedures as less stressful, as demonstrated by studies conducted with other species (due east.one thousand., chimpanzees [16], cats [17]). Conversely, elephants who spend more time independently may have more opportunity to exercise choice and behave autonomously, both of which have been suggested to raise welfare [18,nineteen]. Thus, nosotros were interested in characterizing the pct of daytime hours elephants spend interacting directly with staff and the amount of time spent during those hours in either training, exercise, husbandry, play, or public demonstrations (in an education or show setting).

Ecology Enrichment

Within the zoo and aquarium community, the term enrichment (or environmental enrichment) covers a wide range of practices intended to improve beast welfare by facilitating the expression of important behaviors, such equally foraging or self-maintenance, and by providing opportunities for play, exploration, problem solving, and exercising choice [20,21]. Enrichment in zoos can accept many forms, ranging from permanent or semi-permanent exhibit features, such as the provision of pools, items that require animals to use an assortment of skills to access food (e.g., nutrient-balls, puzzles), or other rewarding stimuli [21]. Numerous studies with various species of zoo animals have demonstrated the positive bear on of environmental enrichment on welfare outcomes including reductions in stereotypic behavior [22,23] and physiological stress responses [24]. However, there are very few published studies of enrichment practices for elephants, and those focus exclusively on food-based enrichment at single zoos (e.yard., Stoinski et al. [25],Wiedenmayer [26]).

Our goal was to decide the enrichment methods used by zoos. We also wanted to assess whether enrichment was applied systematically, which can enhance its effectiveness [27]. This research was informed by the work of Mellen and Sevenich MacPhee [27], who proposed the "SPIDER" framework. This model, which starts with Setting Goals and proceeds through Planning, Implementation, Documenting, Evaluation, and Readjustment, presents a framework that emphasizes the importance of regularly assessing enrichment for its biological relevance and its ability to appoint the animals.

Feeding

As big herbivores, elephants spend a significant proportion of time (in the wild [5,6] and in zoos [28]) manipulating and consuming plant textile to meet metabolic needs. In the wild, food resources are temporally and spatially dispersed, and elephants apply a range of foraging skills to locate and admission them [5,six]. Given the fact that the acquisition and ingestion of food plays such a central role in elephant behavioral repertoire, the timing, frequency, and methods of food provision are important components of zoo feeding programs. In zoos, feeding opportunities are, of necessity, spatially and temporally concentrated [25], but information technology has been suggested that this limitation can be addressed by utilizing a diversity of feeding methods and schedules [29,30]. To better understand the not-nutritional aspects of elephant feeding programs, nosotros sought to decide the patterns in and diversity of food delivery methods. In addition, we were interested in the temporal predictability of food presentation. Although the effects of feeding predictability on elephant welfare have not been evaluated, temporally unpredictable feeding schedules take been shown to improve welfare in other species past increasing exploratory behavior, enhancing memory, and reducing the performance of stereotypic behavior [31,32].

Do

AZA accreditation standards require that all zoos have a staff-directed elephant exercise programme [3]. Elephants can be trained to participate in exercise routines including activities such as stretching and staff-directed walking. Exercise programs have been implemented, in part, considering zoo elephants are prone to developing pododermatitis and degenerative bone affliction [33,34]. Many zoo elephants are also overweight or obese [fourteen]. Research in humans [35–38] and other species (rodents [39–42], dogs [43–45], swine [46]) demonstrates that exercise can reduce the risk of developing health issues and mitigate complications associated with these ailments once developed. Our goal was to assess the frequency and types of staff-directed exercise employed.

Training

Care staff railroad train elephants to participate in a number of management practices, including daily foot and skin care, moving betwixt exhibit areas on cue, and veterinary procedures. Elephant training involves pedagogy an individual elephant to perform, or abjure from performing, behaviors on request [47]. Withal, the methods past which elephants are trained in zoos across N America vary considerably depending on the philosophy and feel of the trainers too as the age, species, sex, and background of the individual elephant (for a review, see Wemmer and Christen [8]). Although the specific techniques and tools used may vary, all elephant training is based on the awarding of operant workout methods that are designed to either: one) increase the frequency of desired behaviors, typically past either presenting stimuli the animal finds rewarding or removing stimuli the creature finds aversive or 2) decrease the frequency of undesired behaviors, typically by presenting aversive stimuli or removing rewarding stimuli [48,49]. Additionally, trainers may use neutral techniques (e.m., taking a short pause or not reacting to the elephant's behavior) when they wish to provide the animal with some other opportunity to be successful [l].

The furnishings of utilizing rewarding and aversive stimuli in the learning environs take been investigated with humans and other species. For example, humans who learn tasks under weather where aversive stimuli are utilized are more probable to experience negative affective states and/or frustration than those who are taught tasks with merely the apply of rewarding or neutral stimuli [51,52]. Similarly animals trained with aversive stimuli show behavioral and neurological responses considered indicative of negative affect [51,53,54].

In that location has been no systematic investigation into how the techniques and tools utilized in elephant training influence welfare. All the same, controversy has arisen with regard to one of the tools used for grooming elephants: the pole/stick, called a guide. The guide is also known as an ankus or bullhook, since there is a metal hook with a pointed tip at the distal terminate. Some speculate that guide use creates an aversive grooming environment, because of its potential to cause physical discomfort [55,56], while others fence that its apply has few adverse welfare consequences if rewarding stimuli are used more frequently than the guide during grooming [47]. Since the methods utilized past elephant trainers have never been rigorously documented these assertions cannot be tested empirically. Thus, our goals were to collect data on the use of guides and operant conditioning techniques and to develop variables to characterize the different approaches to elephant training across the North American zoo population.

Methods

Ethics statement

The management at each participating zoo authorized this study, and the University of California, Davis Institutional Review Board adamant that the surveys used in this study did not constitute Human being Subject Research (IRB #739963–1).

Surveys

We derived the information from 2 online surveys, referred to as the Management Survey and the Training Techniques Survey. Survey content was developed from multiple sources including expert stance, focus group interviews with elephant intendance professionals, and electric current elephant management literature. For both surveys, we asked respondents to report on their practices during the 2012 calendar twelvemonth. Online surveys were generated dynamically based on response-dependent branching architecture to avoid presenting redundant or extraneous questions to respondents. All data were stored upon submission in a relational database using an SQL server, and we ensured confidentiality by using randomly generated unique alpha-numeric codes.

We used customized web-links to invite elephant managers to participate in the Management Survey. The survey included five sections, each consisting of one to five questions. 2 of these sections collected information at the zoo level (enrichment and feeding), while three nerveless information at the individual elephant level (direction schedules, employ of training tools, and exercise). Questions at the individual elephant level were presented in the survey sequentially for each elephant at the zoo and were based on elephant population data that we nerveless prior to developing the survey.

We targeted the Training Techniques Survey at elephant care staff, who had worked with a given elephant for at least one year. Elephants were randomly matched with between ane and iv qualified intendance staff respondents depending on the elephant to care staff ratio at that zoo. The survey characterized each individual elephant'southward training experience by focusing on techniques used during training both when the elephant was compliant and non-compliant. Response choice ranged from Never (1) to Very Oft (5) on a v-point Likert calibration. A complete list of the Training Techniques Survey questions can be plant in Tables one and 2.

Data Processing and Variable Creation

We excluded all data from partially completed sections of the surveys. Data from elephants that were born, died, or experienced an inter-zoo transfer during the report twelvemonth were also excluded from all analyses. We used the data to create a number of novel variables characterizing management schedules, environmental enrichment, feeding, practise, and training practices. Some of these variables draw raw data and others were calculated to synthesize composite values. Throughout the balance of this paper, we capitalize all calculated and synthesized variables. Variable descriptions are presented below and in Tables 3 and iv.

Direction Schedules.

All management schedule variables were derived from the Direction Survey. Managers completed a management schedule for each elephant by estimating the average percentage of the daytime hours (zoo operating hours) per month that the individual spent in various contexts. The contexts were: exercise, husbandry (including footwork, baths, veterinary intendance), preparation known (practicing known behaviors), preparation new (learning new behaviors), training mixed (mixed sessions of known and new behaviors), play and human relationship sessions (interactions with elephant outside of training or husbandry activities), public demonstrations (staff-directed activities in education or show setting), on showroom (non interacting with staff), off showroom (not interacting with staff) and other (non specified). Data were confirmed upon entry to sum to 100%.

Variables for analysis were created by summing percent fourth dimension across groups of behaviors equally follows: Percentage Fourth dimension Training = sum of grooming known, training new, and training mixed; Percentage Time Managed = sum of exercise, husbandry, Training Time, play, human relationship sessions and demonstrations; Percentage Time Contained = sum Percent Time On and Percent Fourth dimension Off Exhibit.

Environmental Enrichment.

All environmental enrichment variables were derived from the Management Survey. Managers indicated the percentage of days in the year the elephants had admission to xxx dissimilar types of enrichment or exhibit features. They also reported how often their staff used the enrichment program components based on the SPIDER framework (due east.k., setting goals, scheduling activities, documentation, evaluation, and program readjustment). Nosotros used these data to generate ii enrichment variables, Enrichment Diversity and Enrichment Programme, both of which provide composite descriptions of enrichment program implementation and structure. We used the Shannon-Weaver diversity index [57] to create the Enrichment Diversity score (as well as feeding and exercise. See method sections below). This index is near commonly used to characterize ecosystem communities, and scores increase as the number of species sampled rises and the affluence of these species become more even [57]. Thus, Enrichment Diverseness scores characterize the diverseness of enrichment types utilized also every bit the relative frequency with which enrichment types were presented. High Diversity Scores bespeak equal and frequent use of all enrichment types, while low diverseness scores indicate infrequent use of enrichment in general or reliance on frequent use of merely a few enrichment types. The Enrichment Diverseness scores we calculated had a possible score range of 0 (ane type of enrichment always used) to 3.four (equal frequency apply across all 30 enrichment items). We used principal components factor assay with a polychoric matrix (to account for the ordinal data) [58] to develop a factor matrix describing enrichment program component use. Cistron loadings were retained using the proportion of variance method, and these loadings were used to calculate the standardized Enrichment Plan factor scores.

Feeding.

Feeding questions addressed the various ways food was presented to the elephants at each zoo. Managers reported the number of feeding events offered to their elephants during specific time frames (Feed Day, Feed Dark, Feed Full) and the frequency with which various feeding methods were used (eastward.1000., piled on ground, spread through exhibit, presented in an open container, suspended, presented in a foraging device, and hidden). Managers too rated the predictability of their feeding activities on a three-indicate scale ranging from "predictable" to "unpredictable" (Feeding Predictability). We further processed the feeding methods data to generate three synthesized variables: Feeding Multifariousness, Spread, and Alternative Feeding Types. The Shannon-Weaver Index was used to derive the Feeding Diverseness score, with a possible range of 0 (one blazon of feeding always used) to 1.eight (equal frequency use of 6 feeding types). 2 variables measured the utilize of particular types of feeding methods: Spread (the proportion of feedings where food was spread through the showroom) and Culling Feeding Types (the proportion of feedings where food was hidden, hung upwardly, or presented in a foraging device).

Practice.

Practice questions addressed the percentage of time individual elephants spent engaged in staff-directed exercise methods [east.g., A to Bs (directed walking from point A to signal B, repeated equally needed), calisthenics (e.g., climbing upward and downwardly blocks and lifting objects), intervals, slow walks, strengthening exercises, stretching, swimming, and water walking], and the number of hours per week individual elephants engaged in directed walks (Walking Calendar week) and general exercise (Exercise Week). Walk Week and Practise Calendar week were categorical variables on a seven-signal calibration, ranging from less than ane hour per week to more 14 hours per week. We farther processed the exercise data to create the Exercise Diversity variable, a score calculated using the Shannon Weaver Index with a possible range of 0 (ane type of do always used) to 2.ane (equal frequency use across eight practice types).

Training.

Guide use was determined from the Management Survey, which asked managers whether in that location was a guide at the facility (Guide Exposure) and the frequency with which each elephant at the zoo was exposed to a guide during staff interactions (Percentage Guide Interaction).

The Training Techniques Survey asked qualified care staff to charge per unit their use of 19 unlike preparation techniques when working with the assigned elephant(south). We used these responses to create two types of synthesized variables: Training Item Scores and a Rewarding Stimuli Techniques Score (Table 4). To calculate the Training Item scores, we averaged the staff responses on each of the 19 training techniques for every elephant and so rounded these values to the nearest half integer, forming a nine-point half-integer scale that included the following categories: Never (1), Never/Rarely (1.5), Rarely (ii), Rarely/Sometimes (2.five), Sometimes (3), Sometimes/Frequently (three.5), Oftentimes (4), Frequently/Very Frequently (iv.five), and Very Frequently (v).

To calculate the Rewarding Stimuli Techniques Score, we first categorized 12 of the nineteen training techniques according to whether stimuli were added or removed, so according to the valence of the stimuli (rewarding or aversive; Tabular array 5). The remaining seven training techniques were categorized as neutral, because they did non take a clear valence. Following categorization, the scores from techniques that involved the provision of rewarding stimuli and the removal of rewarding stimuli for each elephant were summed and divided past the sum of their scores on all techniques. We categorized these values to a nine-indicate calibration that ranged from one, pregnant that grooming interactions lacked the use of rewarding stimuli, to nine, significant that they utilized rewarding stimuli exclusively.

In improver to developing these two synthesized variables, we besides investigated the effect of Guide Exposure on the training experience of elephants. Mann-Whitney U (Wilcoxon Rank Sum) tests were used to decide whether Training Item and Rewarding Stimuli Techniques Scores differed betwixt the Guide Exposure subgroups.

Statistical Analyses.

We calculated descriptive statistics for all variables, and conducted Mann-Whitney U (Wilcoxon Rank Sum) tests to determine species and sex differences for all variables except the zoo-level variables, which could just be assessed for species furnishings. Where the Isle of mann-Whitney U results indicated a species or sexual practice difference that could be meliorate interpreted with further analyses, nosotros used linear regression models fitted using generalized estimating equations (GEE), which allow for the individual elephant to exist used as the unit of analysis and account for the clustering of individuals within zoos [59,sixty]. Zoos were treated as random effects and an independent correlation construction was specified [61]. We used the forwards option arroyo to build the models [62] and continued to add together variables until the addition no longer resulted in significant models. Interactions among the variables contained in whatsoever significant multi-variable models were assessed during the final model edifice stage. Microsoft Excel (Microsoft Corporation, Redmond, WA) and SAS version 9.3 (SAS Found, Cary, NC) were used for all statistical analyses. We used regression modeling lawmaking: [PROC GENMOD, with options DIST = Normal, LINK = Identity, Type = Ind, and REPEATED]. For all analyses, p-values ≤ 0.05 were considered statistically pregnant.

Results and Give-and-take

Our surveys generated a large number of variables that are important for understanding how elephants are managed in North American zoos. In the results and discussion, nosotros volition focus just on the subset of those variables that tin be direct related to existing literature or take clear links to fauna welfare. Although African and Asian elephants are different species and are behaviorally and physiologically sexually dimorphic, there were surprisingly few species or sexual activity differences; those nosotros did find are discussed farther below. Results from variables not discussed in the text can be institute in the appropriate department Tables.

Response Rates

Lx-three of seventy invited zoos (90%) submitted completed Management Surveys. Iv zoos (5.7%) submitted partially completed surveys, and three (4.iii%) zoos declined participation. The number of elephants included in each variable analysis ranged betwixt 83 and 224 based on data availability and applicability. Completed Training Techniques Surveys were submitted past 62 zoos for a total of 602 surveys on 227 elephants.

Management Schedule

Nosotros identified significant species level differences in vii of the xi Management Schedule variables (Tabular array 6), with the primary difference being that Asian elephants were managed for a significantly greater proportion of their day (hateful = 56.9% p<0.001) than African elephants (mean = 48.6). During managed time, Asian elephants also spent significantly more fourth dimension engaged with staff in husbandry activities (mean = xv.five%), exercise (mean = 6.eight%), and play (mean = 4.0%), than did African elephants (mean = 12.2%, 4.3%, and 1.ix% respectively). Conversely, African elephants spent significantly more time independent (mean = 51.4%, p<0.001), than did Asian elephants (mean = 43.1%). The just sex deviation was that females spent more than time in exercise (mean = v.5%) than males (mean = 4.3%).

Linear regression analysis of Percent Time Managed demonstrated that age and species contributed to the corporeality of time an elephant spent in managed activities (Tables 7 and viii). Managed time increased by twenty.2% for every year of historic period, and Asian elephants were half dozen.2 times more probable to spend more fourth dimension in managed activities than African elephants. There were no significant interactions between historic period and species, indicating that increases in age influence managed fourth dimension at the same rate for the two species. Age is a known correspondent to foot pathology in both species [thirteen,33], and it may be that additional time is existence spent in pes care with older elephants to mitigate risks. Even so, since both age and species are main furnishings in this model, we can infer that there is something about being an Asian elephant (other than the fact that Asians in this population are older than Africans [vii]) driving species differences in managed time. One possibility is that more managed time is being allocated to address musculoskeletal health issues [33,34] or stereotypic behaviors [nine] which are more than prevalent in Asian elephants. Since research in humans [37,38] and other species (rodents [40,41], dogs [44]) demonstrates that physical activity tin can reduce wellness risks associated with musculoskeletal health bug, managers may be engaging older and Asian elephants in active managed activities (e.g., practice and play) in an effort to mitigate these problems. Similarly, managers may exist engaging older and Asian elephants in more foot care related husbandry activities in an effort to treat existing pes pathologies.

It should exist noted that the dark period was not included in whatsoever of the Management Schedule analyses. In almost cases, elephants are independent for the entire nighttime which, for this population, averaged betwixt eight–18 hours depending on the season, with a modal value of 14 hours in both the summer and wintertime [15].

Environmental Enrichment

All threescore-iii zoos provided their elephants with enrichment (Table 9), (median = 73% of enrichment options included in our survey, max 97%, min 43%). Of these, the most mutual types were clay piles and scan, which were used to some degree by all zoos (Fig 1). With respect to frequency of provision, most zoos provided dirt piles, pools, logs, and scratching posts nearly every day (median = 10; available on ninety–99% of days) (Figs two and 3). These features could be of import to facilitate self-maintenance behaviors and maintain skin status and, as such, are integrated into enrichment programs as permanent or semi-permanent showroom features. Our data also show that while problem-solving opportunities were components of most enrichment programs (97% of zoos), they were provided infrequently (problem-solving opportunities with nutrient rewards median = 3; problem-solving opportunities with non-food rewards median = 1). Taken together these findings are consistent with a survey-based study that examined enrichment practices for mammals at threescore Oceanian, North American, and European zoos. Hoy et al. [63] found that permanent or semi-permanent exhibit features were perceived by staff to be the almost important types of enrichment, and that enrichment types that required considerable time to set or were difficult to gear up were provided less frequently. Logistical problems associated with time or training difficulty may explain why our data also show lower frequencies of use of problem solving methods, equally they may need to be tailored to private animals and regularly updated to ensure the animals continue to utilize their cognitive and behavioral skills in novel ways [xx]. Since problem-solving requires animals to use cognitive and behavioral skills to exert control over their environment and tin be self-reinforcing [20,64], we had hoped to test the effects of problem solving enrichment in the subsequent welfare models. However, we were unable to do then, since the frequency of apply was and then low.

Fig ii. Median-enrichment and exhibit-characteristic use scores of the 63 zoos.

Each chiselled calibration score shows ranges in 10% increments (eastward.m., 1 = 1–9%, ii = 10–19%, etc.). Scores of 0 stand for no use and scores of 11 represent use 100% of the fourth dimension.

https://doi.org/10.1371/periodical.pone.0152490.g002

Fig 3. Median-enrichment and exhibit-feature utilize scores from zoos that used these methods.

Each categorical scale score shows ranges in 10% increments (east.grand., one = 1–9%, two = x–xix%, etc.). Scores of 0 represent no use and scores of 11 represent use 100% of the time.

https://doi.org/10.1371/journal.pone.0152490.g003

Like Hoy et al. [63] we found that scheduling enrichment with a calendar was the most frequently used enrichment plan component (median = 4; frequently) derived from the SPIDER framework. The other four plan components were only used sometimes (median = 3 for each component) by most zoos, resulting in mid-range Enrichment Program scores (hateful = 0; on a scale from -two.2 to two.one). Equal and integrated employ of all five of these components is probable to ensure that enrichment activities go on to be stimulating for animals [27].

Enrichment Diversity scores were moderate (hateful = 2.ix on a scale from 0 to three.four), indicating that there is opportunity to increase the variety and frequency of enrichment presentation for zoo elephants. To our knowledge, but two other large scale studies take attempted to quantify enrichment complexity, just using different indices than the Shannon Weaver. One [65] used an index that places less emphasis on evenness and gives more weight to the nearly ascendant types experienced, and thus underestimates multifariousness[57], while the other [66] generated a novel "environmental complexity" score. Given the complex nature of enrichment programs, information technology is necessary that methods for quantifying this practice go on to evolve such that variability within and betwixt programs tin be robustly assessed. For instance, both measures that account for how individual animals utilize enrichment items and how novelty is incorporated into enrichment provisioning are topics that could be included to strengthen assessment methods.

Feeding

Inquiry on elephants and other species has shown that providing animals with smaller portions of food more than frequently can ameliorate body condition (sows [67]), reduce abnormal behavior (Asian elephants, giraffe, okapi [28,68]), and increase naturalistic feeding behavior (African elephants [25]). Since elephants in the wild feed during diurnal and nocturnal periods [5,six], a pattern of smaller more frequent meals could be beneficial during the daytime and the nighttime. However, most elephants were fed only once during the nighttime (Tables x and xi). While nosotros did non collect data on the timing of this feeding, other studies have shown that nocturnal feedings are often offered at the beginning of the nighttime management period [69,70]. Providing nutrient in this manner has been linked to rapid consumption early on in the evening and a linear decrease in feeding behavior every bit the dark progresses [lxx].

Virtually half (47.5%) of all zoos feed their elephants on a predictable schedule, with food most commonly presented in clumps (i.e., piles composed of multiple flakes of hay, scan items, or pellet) on the ground (median = 4; 30–39% of feedings included this method) (Figs 4 and 5). The low average Spread scores (hateful = 0.ii, on a calibration from 0 to one) and Feeding Variety scores (mean = 1.three on a calibration ranging from 0 to 1.8) too signal that nutrient is typically provided in concentrated locations with a moderate amount of variety in nutrient presentation. Taken together, these results indicate that many elephants are fed on temporally predictable schedules with high spatial predictability and only moderate feeding method variation. Relying on temporally and spatially predictable feeding programs is potentially problematic. Animals are capable of anticipating the arrival of predictable events, even in the absenteeism of external cues [71], and this ability is hypothesized to play an important part in stimulating appetitive searching behaviors [32]. Withal when food is presented in a temporally and spatially anticipated manner, these appetitive behaviors can become dissociated from their original part and develop into stereotypic behaviors [32]. In some species, food-associated anticipatory stereotypies can be disrupted and reduced by providing animals with temporally and spatially unpredictable feeding events [31], and information technology seems possible the same may apply to elephants.

Fig 4. Median scores for feed presentation methods from 64 zoos.

Each categorical calibration score represents use ranges in 10% increments (e.yard., 1 = ane–9%, two = 10–19%). Scores of 0 represent no utilise and scores of xi correspond use 100% of the time. Categories included clumped [food placed in piles composed of multiple flakes of hay, scan items, or pellet], spread [food distributed through the exhibit], suspended [food suspended by rope, in a bag, open sided barrel, etc.], foraging [food provisioned in a feeding apparatus], subconscious [food hidden around the exhibit], trough [nutrient place in an open trough].

https://doi.org/10.1371/journal.pone.0152490.g004

Fig v. Median scores for feed presentation methods from zoos that used each method.

Each categorical scale score represents use ranges in ten% increments (e.g., 1 = i–9%, two = 10–xix%). Scores of 0 stand for no use and scores of 11 represent utilise 100% of the fourth dimension. Categories included clumped [nutrient placed in piles equanimous of multiple flakes of hay, browse items, or pellet] (66 zoos used this method), spread [food distributed through the exhibit] (66 zoos used this method), suspended [food suspended by rope, in a pocketbook, open sided barrel, etc.] (63 zoos used this method), foraging [nutrient provisioned in a feeding appliance], hidden [food hidden around the exhibit] (59 zoos used this method), trough [nutrient placed in an open up trough] (29 zoos used this method).

https://doi.org/ten.1371/journal.pone.0152490.g005

Do

Asian elephants had higher scores on all exercise variables than African elephants (Tables 12 and 13), confirming and expanding upon the direction schedule findings. African elephants were rarely given whatsoever practice (Fig 6), while elephant managers typically engaged Asian elephants in a variety of types of exercise, including stretching, calisthenics, and slow walks. Because that the AZA's exercise program requirement is intended to mitigate complications associated with degenerative bone disease and obesity [3], it is interesting that aerobic exercise types are non used more oftentimes. Aerobic exercise has been shown in humans [35,36] and other species (rodents [39,42], dogs [43,45], swine [46]) to reduce the risk of obesity and, when combined with force edifice exercises, is as well of import for treating and reducing the take chances of bone and joint diseases (humans [37,38], rodents [40,41], dogs [44]).

Fig 6. Median scores for do methods used for African and Asian elephants.

Each categorical scale score represents utilise ranges in x% increments (due east.g., 1 = 1–9%, ii = 10–19%, etc.). Scores of 0 represent no utilise and scores of 11 represent utilise 100% of the time. Categories included: stretching, calisthenics (e.thou., climbing up and down blocks or lifting objects), A to Bs (directed walking from point A to point B, repeated as needed), intervals (directed walking at dissimilar rates), slow walking, strength building (e.yard., lifting or pulling heavy objects), swimming, and h2o walking (directed walking in shallow h2o).

https://doi.org/ten.1371/journal.pone.0152490.g006

Grooming

Most of the elephants in this written report were trained using a diverseness of methods, the majority of which involved rewarding stimuli (Rewarding Stimuli Technique Score median = 7) (Tables fourteen and 15). The predominance of these techniques may reflect awareness that their use tin minimize the animals' negative states (i.east., frustration) during preparation and lead to more efficient individualized learning [51,72] past increasing communication clarity [51,73]. Additionally, the removal of rewarding stimuli as a ways of reducing undesired behavior is less likely to cause negative melancholia states and/or frustration than the addition of aversive stimuli [51,52].

Providing food rewards and positive verbal stimuli were the most common techniques utilized when elephants complied with a request (Fig 7A), and neutral techniques such as repeating the request for a behavior and not giving a food advantage were most frequently used when elephants did non comply with a request (Fig 7B). Saying "No" was the aversive stimulus used about oft to reduce the frequency of undesired beliefs [experienced past 72% of elephants, median frequency = iii.five (sometimes/frequently)], while aversive techniques involving physical contact were experienced by 44% percent of elephants, with a median frequency of 2 (rarely) (Fig 8).

Fig seven.

Median Training Particular scores at the level of the full population (A-B) for elephants with Guide Exposure scores equal to nada (C-D), and for elephants with Guide Exposure scores equal to ane (East-F). Training Particular scores were sorted according to whether an elephant complied with a request. Scores range in half integer values between one (never) and 5 (very frequently) and bars stand for score ranges. Meaning differences in Training Particular scores past guide exposure and response blazon are lettered (p<0.05). Matching case-sensitive letters indicate a significant divergence for specific median training item scores between guide exposure groups. Training techniques experienced by elephants when compliant (those designed to increase the frequency of desired beliefs) are left unshaded. Training techniques experienced past elephants when non-compliant (those designed to decrease the frequency of undesired behavior) are shaded to aid distinguish betwixt the unlike stimuli involved when addressing non-compliant behavior. Neutral items are shaded in low-cal grayness. Rewarding items are shaded with hash marks. Verbally-aversive items are shaded in medium grey. Visually-aversive items are shaded with a wave pattern. Physically-aversive items are shaded in dark grey.

https://doi.org/10.1371/periodical.pone.0152490.g007

Fig 8. The frequency with which elephants feel each of the various aversive training techniques when non-compliant.

Frequency scores range betwixt 1 (never) and 5 (very frequently). Verbal and visual stimuli are patterned, and physical stimuli are shaded in grey tones.

https://doi.org/10.1371/journal.pone.0152490.g008

When nosotros subdivided the population co-ordinate to Guide Exposure, nosotros found that 81 elephants were housed at 27 zoos that did not keep guides on their premises, while 138 elephants were housed at 38 zoos with guides onsite (Table 14). Of these 138 elephants, however, 52 were never trained with a guide (Table 16), which indicates that guides were not used for routine management of these elephants only may take been kept onsite for emergencies. At 9 zoos, we found that some elephants were trained with guides, while others were not. This within-zoo variation highlights the demand to assess training at the level of the individual elephant rather than the herd. Analyses of Training Particular scores by Guide Exposure revealed several meaning differences (Fig 7C–7F). These differences showed a general trend for elephants that were exposed to guides to experience techniques that involved the removal (e.g., remove negative) or add-on of aversive stimuli (e.thousand., gentle pressure, "No," showing an aversive stimulus) at a significantly college frequency than elephants that were not exposed to guides. Appropriately, Rewarding Stimuli Technique Scores were lower for elephants with guide exposure (median_{(GE = one)} = 7, median_{(GE = 0)} = 8; U = 11,474.v, p<0.05). All of these findings demonstrate that exposure to guides coincides with more frequent use of aversive stimuli in preparation interactions. Interestingly, the antipodal appears not to be true, since 97.five% of all elephants at zoos where guides were non on site experienced aversive stimuli during training when non-compliant. Therefore, our study shows that while the frequency with which these techniques are utilized is higher for animals that are trained with guides, the absence of guides in the training environments does non guarantee that techniques that have been shown to evoke negative emotional states [51,53] or behavioral responses [54,74] in humans and other animals are not being used. However, it is also important to note that across the whole population, these types of techniques are used with much less frequency [median = 1.5 (never/rarely)] than techniques involving rewarding stimuli [median = iii.5 (sometimes/frequently)] and neutral techniques [median = 3.v (sometimes/frequently)].

The few studies that have attempted to evaluate the welfare effects of preparation categorize methods according to whether they rely entirely on the add-on of rewarding stimuli, aversive stimuli, or a mix of methodologies (techniques involving the removal of rewarding stimuli are nearly always excluded from examination) without quantification of the relative proportion with which rewarding stimuli or aversive stimuli are experienced (dogs [54,74] horses [75]). Our study demonstrates that elephant preparation (and likely the training of many other zoo species) is practiced forth a continuum. Thus, categorizing training without quantifying the degree to which different methods are used, or classifying training programs simply based on the presence or absence of guides, may mask valuable information well-nigh the variability in grooming experiences of individual elephants. It is also possible that, within the operant conditioning framework, different techniques take dissimilar furnishings on welfare. The Rewarding Stimuli Techniques Score and Grooming Item scores nosotros developed in this written report are the kickoff to quantify the continuum of experiences of animals with respect to the operant conditioning framework, including those trained with mixed workout methods. The challenge from here forward is to test the association between these types of operationalized training variables and behavioral or physiological outcomes, such that training protocols may be optimized to support positive welfare.

Conclusion

Assessing the welfare of zoo animals requires detailed descriptions of their physical and social environments as well every bit the day-to-twenty-four hour period care practices they feel. Remarkably few studies have examined the practices used in managing zoo animals, and ours is the first multi-institutional study to practice and then in a systematic manner. Our methodology provides a model that could exist practical to assessments of management practices for a variety of zoo-housed species. In particular, our methods for assessing enrichment program quality and diversity and the utilization of training techniques should exist broadly applicable. In addition to describing animal populations of interest, a major force of the types of variables nosotros have synthesized is that they tin be readily used as resource based measures to assess and improve welfare [76]. For example, nosotros and our colleagues have found that the management factors described in this newspaper play an important role in predicting stereotypic behavior rates, walking rates, female reproductive physiology, and trunk status in zoo elephants. More specifically, stereotypic beliefs rates were negatively associated with Percent Time Managed [9], distances walked were positively associated with Feeding Diverseness scores and an unpredictable Feed Schedule [x]. Too, the likelihood of a female African elephant having normal ovarian cyclicity was improved with her Enrichment Variety score [12]; normal prolactin levels were more likely for female person elephants with higher Alternate Feeding Methods and Enrichment Diversity scores [12]. Finally, ideal body status was associated with higher Walk Week scores and an unpredictable Feed Schedule [14]. The results of our study and the subsequent welfare analyses clearly illustrate that elephant management exists on a continuum, tin be modified to back up all-time practices, and are pertinent to elephant welfare.

Acknowledgments

This project was role of a large-scale collaboration entitled Using Science to Understand Zoo Elephant Welfare. The authors would like to acknowledge the pregnant efforts of the full projection team: Christy Alligood, Jeff Bolling, Mary Bonaparte-Saller, Janine Brownish, Anne-Marie de Passillé, Candice Dorsey, Greg Guagnano, Jennifer Hogan, Matthew Holdgate, Mike Keele, Katherine Leighty, John Lehnhardt, Georgia Stonemason, Jill Mellen, Michele Miller, Steve Paris, Harry Peachey, Josh Plotnik, Natalia Prado-Oviedo, Jeff Rushen, Daniel Sneed, Joseph Soltis, Nadja Wielebnowski, and James Witte.

In improver, special thanks to the AZA Elephant TAG and TAG Chair Martha Fischer for logistical back up, Jackie Ogden for communications support, and Vistalogic, Inc., for technological support and software services.

Likewise, thanks to Guy Lichty, Erin Ivory, Michael Boos and Tim Sinclair-Smith for their contributions to the development of the Grooming Techniques Survey.

Finally, sincere thanks to the people and elephants at each of the following zoos for their enthusiastic participation and support of the project:

Africam Safari, Albuquerque Biological Park, Audubon Found, Birmingham Zoo, BREC's Baton Rouge Zoo, Buffalo Zoological Gardens, Busch Gardens, Buttonwood Park Zoo, Caldwell Zoo, Calgary Zoo, Cameron Park Zoo, Cheyenne Mount Zoological Park, Cincinnati Zoo & Botanical Garden, Cleveland Metroparks Zoo, Columbus Zoo, Dallas Zoo, Denver Zoo, Dickerson Park Zoo, Disney's Animal Kingdom, El Paso Zoo, Fresno Chaffee Zoo, Greenville Zoo, Honolulu Zoo, Houston Zoological Gardens, Indianapolis Zoological Society, Inc., Jacksonville Zoological Gardens, Knoxville Zoological Gardens, Lee Richardson Zoo, Little Rock Zoological Garden, Los Angeles Zoo and Botanical Gardens, Louisville Zoological Garden, Lowry Park Zoological Garden, Maryland Zoo, Memphis Zoological Garden and Aquarium, Metropolitan Toronto Zoo, Milwaukee Canton Zoological Gardens, Montgomery Zoo, Nashville Zoo, National Zoo, Niabi Zoo, North Carolina Zoological Park, Oakland Zoo, Oklahoma City Zoological Park, Oregon Zoo, Parque Zoologico de Leon, Phoenix Zoo, Signal Disobedience Zoo and Aquarium, Reid Park Zoo, Riverbanks Zoological Park, Roger Williams Park Zoo, Rosamond Gifford Zoo at Burnet Park, San Antonio Zoological Gardens & Aquarium, San Diego Safari Park, San Diego Zoo, Santa Barbara Zoological Gardens, Sedgwick County Zoo, Seneca Park Zoo, Saint Louis Zoo, The Kansas City Zoo, Topeka Zoological Park, Tulsa Zoological Park, Utah's Hogle Zoo, Virginia Zoological Park, Wildlife Conservation Social club—Bronx Zoo, Wildlife Safari, Woodland Park Zoo, Zoo Atlanta, Zoo de Granby, Zoo Miami.

Author Contributions

Conceived and designed the experiments: CLM BJG JA KC LJM DJS JAM KAM AB. Performed the experiments: CLM. Analyzed the data: BJG LJM CLM. Contributed reagents/materials/analysis tools: BJG CLM LJM JAM. Wrote the paper: BJG CLM JAM LJM DJS.

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