2022, 9999, 1–26
NUMBER
9999 ()
Applied behavior analysis and the zoo: Forthman and Ogden
(1992) thirty years later
Eduardo J. Fernandez
School of Animal and Veterinary Sciences, University of Adelaide
Allison L. Martin
Department of Psychological Science, Kennesaw State University
The field of applied behavior analysis has been directly involved in both research and applications of
behavioral principles to improve the lives of captive zoo animals. Thirty years ago, Forthman and
Ogden (1992) wrote one of the first papers documenting some of these efforts. Since that time, considerable work has been done using behavioral principles and procedures to guide zoo welfare efforts.
The current paper reexamines and updates Forthman and Ogden’s original points, with attention to
the 5 categories they detailed: (a) promotion of species-typical behavior, (b) reintroduction and repatriation of endangered species, (c) animal handling, (d) pest control, and (e) animal performances. In
addition, we outline 3 current and future directions for behavior analytic endeavors: (a) experimental
analyses of behavior and the zoo, (b) applied behavior analysis and the zoo, and (c) single-case designs
and the zoo. The goal is to provide a framework that can guide future behavioral research in zoos, as
well as create applications based on these empirical evaluations.
Key words: animal training, animal welfare, applied animal behavior, behavioral engineering,
environmental enrichment, zoos
(Fernandez, 2017; Lukas et al., 1998;
Maple, 2007, 2008, 2017; Maple & Perdue,
2013). Dr. Maple, along with distinguished
behavior analytic scholar Dr. M. Jackson (Jack)
Marr, trained many researchers who went on to
advance the application of behavior analytic principles in zoo settings (Maple, 2016, 2017, 2021;
Maple & Segura, 2015).
At the time, single-case designs to examine the
effects of environmental enrichment were becoming an important cornerstone of zoo behavioral
welfare research (Carlstead et al., 1991; Carlstead
et al., 1993; Carlstead & Seidensticker, 1991;
Newberry, 1995; Shepherdson et al., 1993; see
later section on the use of single-case designs in
zoos). The concept of enrichment itself was
largely derived from Markowitz’s work on using
operant conditioning to create desired behavioral
changes in zoo animals, which was the focus of
many of his publications in the late 1970s and
1980s (Markowitz, 1978, 1982; Markowitz &
LaForse, 1987; Markowitz et al., 1978; for a
Thirty years ago, Forthman and Ogden
(1992) published one of the first papers to review
the contributions of applied behavior analysis to
zoos. Both authors were associated with the
TECHLab (later, Georgia Tech Center for Conservation and Behavior), a partnership between
Zoo Atlanta and the Georgia Institute of Technology led by Dr. Terry Maple (Maple, 2017).
Dr. Maple pioneered, developed, and
championed the concept of the empirical zoo, recognizing the potential of university–zoo collaborations to impact basic and applied research, animal
management and welfare practices, and education
Conflict of Interest: The authors declare no conflict of
interest.
Open access publishing facilitated by The University of
Adelaide, as part of the Wiley - The University of Adelaide agreement via the Council of Australian University
Librarians.
Address correspondence to: Eduardo J. Fernandez, School
of Animal and Veterinary Sciences, University of Adelaide,
Adelaide, SA, 5005, Australia. Email:
[email protected]
doi: 10.1002/jaba.969
© 2022 The Authors. Journal of Applied Behavior Analysis published by Wiley Periodicals LLC on behalf of Society
for the Experimental Analysis of Behavior (SEAB).
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited.
1
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Applied Behavior Analysis
Eduardo J. Fernandez and Allison L. Martin
review, see Fernandez & Martin, 2021). Thus,
Markowitz’s behavioral engineering practices,
along with Forthman and Ogden’s (1992) paper
and the work of Dr. Terry Maple and the
TECHLab, would help pave the way for this past
30 years of applied behavior analytic endeavors
into behavioral welfare efforts in zoos.
The current review reexamines the topics
introduced by Forthman and Ogden (1992) as
ways in which applied behavior analysis can promote the conservation, education, entertainment,
and welfare goals of modern zoos. Below, we
address the five topics they discussed (i.e., promotion of species-typical behavior, reintroduction
and repatriation of endangered species, animal
handling, pest control, and animal performances). The focus of each section is to provide
updated examples of applied behavior analytic
research and efforts that have occurred in each
area since Forthman and Ogden’s original publication. In addition, the review concludes with
behavior analytic areas of interest and emphasizes
current and future zoo-based studies, including
(a) experimental analyses of behavior and the
zoo, (b) applied behavior analysis and the zoo,
and (c) single-case designs and the zoo. The primary goal is to provide both a historical and theoretical foundation to guide the future of applied
behavior analytic work in zoos.
Literature Review Criteria, Variables Coded,
and Intercoder Agreement
At its core, behavior analysis examines the relation between the environment and behavior.
Thus, almost all zoo-based behavioral studies can
be viewed through a behavior analytic lens.
Given the breadth of this topic, our goal was not
to write a systematic review, but instead was to
further the discussion begun by Forthman and
Ogden (1992) about what the science of behavior analysis can contribute to the zoo. Nonetheless, to assist the reader in understanding our
review process, we have provided additional
information about our publication selection
criteria. Our inclusion of literature was based
largely on knowledge of publications within the
field by both authors, including articles cited in
prior literature reviews (Fernandez, 2022;
Fernandez & Martin, 2021; Forthman &
Ogden, 1992; Martin, 2017; 102 total papers) as
well as literature familiar to us through the typical ways in which scholars stay current in their
field (e.g., reading journals, conducting literature
searches, citation alerts; 122 total papers). In
addition, we conducted a supplemental Google
Scholar search (July, 2022) and then additional
searches via PsycINFO, PubMed, and Web of
Science (September, 2022) based on the following criteria: “zoo” AND “animal” AND “applied
behavior analysis” OR “applied behaviour analysis.” The Google Scholar search produced
885 results, and the other search engines produced eight results that overlapped with the
Google Scholar findings. Based on titles and
abstracts, we selected articles that: (a) were peerreviewed research studies, (b) involved nonhuman animals in some component of the
research, and (c) were conducted at a zoo or similar facility that housed exotic animals. Based on
these eligibility criteria, the search yielded
34 results. Articles were also removed if they
were already included as one of the 224 papers
identified in our preliminary review (18 papers
removed). This exclusion criterion left 16 results.
We then assessed the full text of articles to determine relevance for our review. We excluded
papers if they were (a) not of an applied nature
(observation-only or otherwise not directly aimed
at improving welfare; seven papers removed), or
(b) limited to a traditional enrichment-focused
manipulation (not assessed for potential function;
see Physical Variables section; three papers
removed). Following the application of these
exclusion criteria, six articles were added to the
review, resulting in a total of 230 sources
included in the review. Figure 1 details the
results of our literature search.
Finally, given the large number of papers
published in two emerging areas of research
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2
3
PREVIOUS
REVIEWS
AUTHOR
KNOWLEDGE
DATABASE SEARCHES
Sources identified
from previous reviews
(Fernandez, 2022;
Fernandez & Martin,
2021; Forthman &
Ogden, 1992; Martin,
2017)
n = 102
Sources identified
based on authors'
knowledge of
publications in the
field
n = 122
Sources identified through keyword search: "zoo"
AND "animal" AND ("applied behavior analysis" OR
"applied behaviour analysis)" in Google Scholar (n =
885), PsycINFO (n = 4), PubMed (n = 2), Web of
Science (n = 4)
n = 885 unique sources
SCREENING
IDENTIFICATION
Figure 1
Flowchart of Literature Search
Titles and abstracts screened for
eligibility criteria:
1. Peer-reviewed research study
2. Involved nonhuman animals
3. Conducted at a zoo or similar
facility
n = 885
Sources
excluded
(n = 851)
Sources screened for duplicates
(already in manuscript)
n = 34
Sources
excluded
(n = 18)
Full texts examined for relevance.
Papers excluded if they were
a. Not of an applied nature
b. Limited to a traditional
enrichment-focused manipulation .
n = 16
Sources
excluded
a. n = 7
b. n = 3
INCLUSION
Papers added to the review:
Baker et al. (2010); English et al.
(2014); Farmer et al. (2011);
Lauderdale et al. (2021); Padrell et
al. (2021); Troxell-Smith et al.
(2017)
n=6
Sources included in review
N = 230
(functional analysis and preference assessments), we summarized these studies in tables
(see Applied Behavior Analysis and the Zoo
section later in the paper). This tabular summary required the categorization of articles on
several dimensions. Exact agreement was used
to assess intercoder agreement for functional
analysis and preference assessment articles. Both
authors independently coded 40% of the functional analysis articles for author and year
(100% agreement), species (100% agreement),
target behavior (100% agreement), experimental design (100% agreement), and primary
function identified (100% agreement). Both
authors also independently coded 32% of the
preference assessment articles on author and
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
year (100% agreement); species (100% agreement); type of stimuli used in each study (food,
nonfood, symbols, or mixed/multiple; 90%
agreement); and whether the study presented
stimuli singly, in pairs, in arrays with three or
more stimuli, or in mixed/multiple ways (90%
agreement).
Forthman and Ogden Revisited
Promotion of Species-Typical Behavior
For the better part of a century, zoos and
zoo-like facilities have been concerned with getting animals to behave similarly to their wild
counterparts
(Hediger,
1950,
1955;
Morris, 1964; Yerkes, 1925). Early applied
behavior analytic endeavors in zoos, such as the
work of Markowitz and colleagues noted above
(Markowitz 1978, 1982; Markowitz &
LaForse, 1987; Markowitz et al., 1978),
achieved some of these goals by developing
simple operational definitions of the desired
responses and using mechanical devices
installed in exhibits to reinforce these contrived
behaviors. However, these efforts were met
with criticism, particularly with regard to how
they related to nonnatural behaviors and nonnaturalistic environments (Hancocks, 1980;
Hutchins et al., 1984). The eventual resolution
would be an integrative approach that used
both learning principles and understandings of
species-typical behaviors and settings to guide
welfare-based activities, such as environmental
enrichment (Forthman-Quick, 1984). Modern
examples include using wild-like enrichment
activities and devices to encourage speciestypical foraging behaviors, such as foraging patches with Parma wallabies (Macropus parma)
and Patagonian cavies (Dolichotus patagonum;
Troxell-Smith et al., 2017), as well as the use
of artificial termite mounds with chimpanzees
(Pan troglodytes; Padrell et al., 2021).
Although a detailed historical examination of
the convergence of learning and evolution to
understand behavior is beyond the scope of this
paper, it is worth noting that the interest of
Forthman and Ogden (1992) in species-typical
behavior from a learning perspective echoes concerns raised by Breland and Breland (1961), as
well as Herrnstein (1977) when addressing the
importance of attending to the evolutionary history of the organisms that are learning. Likewise,
Skinner himself would make similar points about
the importance of understanding the phylogeny
of behavior to better understand how any
response is selected (Morris et al., 2004;
Skinner, 1966a; Skinner, 1984). In addition,
behavior systems researchers emphasized nonlearned, biological components of behavior that
would influence an organism’s learning
(Domjan,
1983;
Shettleworth,
1993;
Timberlake, 1993; Timberlake & Lucas, 1989),
and more recently, behavior analysts such as
Baum (2012) have echoed the importance of
Phylogenetically Important Events (PIEs) on
learned behavior. Finally, the extent to which
researchers use species-typical or “natural” behavior as an animal welfare metric across a variety of
settings has been discussed and debated
(Browning, 2020; Fraser, 2008; Hutchins, 2006).
Nonetheless, species-typical behavior serves as an
important assessment and improvement welfare
measure, particularly for the diversity of wild animals typically displayed in zoos.
Below, we consider two subcategories of promoting species-typical behavior that Forthman
and Ogden (1992) originally outlined:
(a) physical variables, such as exhibit space,
feeding schedules, and potential enrichment
items; and (b) social variables, such as the way
zoo animals are housed with other animals. For
both subcategories, we focus on more recent
behavioral advancements published after
Forthman and Ogden, as well as how related
research has been used in application to benefit
the lives of zoo animals.
Physical Variables
Applied behavior analysis as a field is certainly familiar with understanding the
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4
importance of the environment on behavior,
particularly as it relates to antecedents
(e.g., discriminative stimuli and setting events)
and consequences. One of the key physical variables studied in zoos and noted by Forthman
and Ogden (1992) is environmental enrichment. Since the time of their original publication, hundreds of studies on enrichment in
zoos have been published. Thus, an extensive
examination of each of these studies is not possible within this review (see Shyne, 2006;
Swaisgood & Shepherdson, 2005; Zhang
et al., 2022 for a selection of meta-analyses
conducted on aspects of enrichment involving
zoos or aquariums). However, a few noteworthy studies include examinations that have used
common applied behavior analytic procedures
to assess and enhance the welfare benefit of
enrichment practices. For instance, preference
assessments have been used to determine both
the type and effectiveness of potential enrichment (Clayton & Shrock, 2020; Dorey
et al., 2015; Fernandez et al., 2004;
Fernandez & Timberlake, 2019b; Mehrkam &
Dorey, 2014, 2015), and feeding schedules,
including fixed- and variable-time schedules,
predictable versus unpredictable feeding schedules, and live prey feeding events have been
used as forms of enrichment (Andrews &
Ha, 2014; Bloomsmith & Lambeth, 1995;
Fernandez, 2020; Fernandez, Myers, &
Hawkes, 2021; Wagman et al., 2018). In all of
the above, a core element, as stressed by
Forthman and Ogden, is a functional evaluation of the physical variables of interest. This
necessarily means using experimental manipulations, ideally those that include single-case
designs (e.g., reversal, multiple-baseline designs;
Alligood et al., 2017; Fernandez &
Timberlake, 2008; Maple & Segura, 2015).
Another set of physical variables important
for promoting desired species-typical behaviors
in zoo animals are the exhibits themselves. Following Forthman and Ogden’s (1992) publication, a few zoo researchers and personnel have
5
emphasized the importance of understanding
how exhibit design influences the behavior and
welfare of zoo animals, including the effects of
using rotating exhibits (Coe, 2004), the effects
of exhibit space use and choice (Owen
et al., 2005; Ritzler et al., 2021), the effects of
different exhibit structures and changes to
exhibits (Carlstead et al., 1993; Fernandez
et al., 2020), and the use of computer technology to modify exhibit interactions (Carter
et al., 2021; Coe & Hoy, 2020). Again, like
environmental enrichment, the emphasis here
is on understanding the function of the physical exhibit variable on the behavior of the
exhibited animal and for applied purposes.
From a behavior analytic perspective, this is
most readily accomplished through experimental analysis using single-case designs (see SingleCase Designs and the Zoo section below).
Social Variables
Forthman and Ogden (1992) stressed the
importance of understanding social factors,
including how animals in zoos are exhibited
with other animals. Nonetheless, only a few
studies have directly examined how changes in
social structures, specifically changes in the
number of individuals housed together, benefits
the behavior of zoo animals. For example, several studies have explored changes in the number of elephants housed together on the
behaviors
of
those
elephants
(Lasky
et al., 2021; Schmid et al., 2001). Other
researchers have examined differences in the
social housing of black and gold howler monkeys (Alouatta caraya), including the reproductive success of monkeys under different social
housing conditions (Farmer et al., 2011). Likewise, researchers have investigated the social
dynamic of giraffes (Giraffa camelopardalis)
under different management and housing conditions (Bashaw, 2011; Bashaw et al., 2007),
including maternally raised or deprived giraffes
(Siciliano-Martina & Martina, 2018). One difficulty with these studies is that the changes in
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
how animals are housed are not systematically
manipulated. Zoos rarely have the luxury of
engaging in such manipulations because they
are both cost prohibitive and potentially detrimental to the welfare of their animals. However, a couple of studies have implemented
systematic changes in the social housing of zoo
animals, thus allowing for such experimental
control. Rowden (2001) studied social interactions in Bulwer’s wattled pheasants (Lophura
bulweri) by changing the number of individuals
housed together, either in pairs or larger
groups. Similarly, Fernandez and Harvey
(2021) used quasi-experimental reversals to
examine how changes in the social housing of
African wild dogs (Lycaon pictus) impacted
enclosure use. In both studies, these experimental manipulations allowed for greater prediction
and control of the social variables of interest,
which itself could allow for greater specificity in
the social housing and management of zoo
animals.
It is also worth noting that social variables
can include the human–animal interactions
observed in zoos, a concept often described as
animal–visitor interactions (Davey, 2007;
Fernandez et al., 2009; Hosey, 2000;
Sherwen & Hemsworth, 2019). Historically,
animal–visitor interactions were seen as problematic for the conservation education of visitors, as well as generally having a negative
impact on the welfare of zoo animals
(Kreger & Mench, 1995). However, in the past
two-plus decades, greater emphasis has been
placed on the positive impact that visitors can
have on zoo animals (i.e., visitor effects;
Hosey, 2000) and that the zoo animals and the
zoo itself can have on visitors (i.e., visitor experiences; Godinez & Fernandez, 2019;
Learmonth et al., 2021). In addition, others
have discussed human–animal interactions in
zoos that do not involve visitors, including
keepers or staff (Hosey et al., 2018; Ward &
Melfi, 2015). The relevant factor is that behavior analysis offers a unique perspective for
understanding all human–animal interactions
observed in zoos, particularly as they relate to
the directly observable behaviors offered by
both animals and visitors. In addition, the use
of experimental manipulations is necessary for
distinguishing between visitor effects and visitor
experiences. The assumption is often that
changes observed in animal activity are the
result of visitor presence; but, without proper
experimental control, researchers cannot assume
that visitors cause changes in animal activity or
vice versa, or whether they are even causally
related (Fernandez & Chiew, 2021).
Reintroduction and Repatriation of
Endangered Species
The
conservation
of
species
via
reintroduction of animals born and reared in
zoos has been a major goal of the modern zoo
(Fa
et
al.,
2011;
Fernandez
&
2008).
Although
many
Timberlake,
reintroduction efforts are carefully assessed, the
assessments often do not involve quantitative
data. Forthman and Ogden (1992) describe
one species, the golden lion tamarin
(Leontopithecus rosalia), for which empirical
evaluations have been conducted to evaluate
the effects of introducing captive-bred zoo animals into the wild (Kleiman et al., 1986). Since
1992, these efforts have continued, including
comparisons of wild-born and captive-born
tamarins, examinations of semi-free-ranging
populations in captivity, and the use of different types of environmental enrichment in captivity and in relation to species-typical
behaviors necessary for wild tamarins (Bryan
et al., 2017; Castro et al., 1998; Price
et al., 2012; Ruiz-Miranda et al., 2019;
Sanders & Fernandez, 2020; Stoinski
et al., 1997, 2003). Other notable species
examples include examinations of wild-like captive conditions for the endangered black-footed
ferret (Mustela nigripes; Miller et al., 1998), the
effects of releasing Oldfield mice (Peromyscus
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6
polionotus subgriseus) into testing settings meant
to mimic the wild (McPhee, 2003), and captive
breeding and rearing practices of Key Largo
woodrats (Neotoma floridana smalli) to improve
their successful reintroductions (Alligood
et al., 2008, 2011; Wheaton et al., 2013).
These empirical studies that focus on how the
arrangement of environmental contingencies
impact behavior and, as a result, the success of
reintroductions, offer glimpses at how applied
behavior analytic research efforts that focus on
quantitative, experimental methods could help
assess and improve reintroduction efforts for a
variety of species found in zoos.
Animal Handling
Forthman and Ogden (1992) detailed the
importance of applied behavior analysis in
improving the husbandry practices that are
commonplace within zoos. As they noted,
using behavioral principles, zoos have been able
to move away from chemical or physical immobilization practices to conduct the routine veterinary care necessary for their animals. This in
large part was a result of the work of Keller
Breland and Marian Breland, who effectively
demonstrated the use of positive reinforcement
to increase voluntary participation of a wide
variety of animal species in many diverse settings (for a review, see Fernandez &
Martin, 2021).
Although the use of positive reinforcement
to improve animal handling practices in zoos
and similar exotic animal settings is now commonplace, only a handful of publications have
empirically examined its effects. Denver Zoo
personnel trained two species of antelope, nyala
(Tragelaphus angasi) and bongo (Tragelaphus
eurycerus), to voluntarily enter crates for blood
draws and other veterinary procedures
(Grandin et al., 1995; Phillips et al., 1998).
Bloomsmith et al. (1998) and Veeder et al.
(2009) successfully used reward-based methods
to train large groups of chimpanzees (Pan
7
troglodytes) and mangabeys (Cercocebus atys atys)
to move (i.e., shift) to different areas within
their enclosures. Savastono et al. (2003)
detailed reward-based procedures to train a
variety of behaviors for a dozen different zoohoused new world monkey species. Cheyenne
Mountain Zoo personnel trained giraffes
(Giraffa camelopardalis reticulata) to participate
in radiographs and hoof care (Dadone
et al., 2016). Researchers have also examined
the potential enriching or behavioral welfare
effects of training Asian elephants (Elephas
maximus) to paint (English et al., 2014), as well
as training rhesus macaques (Macaca mulatta)
to present various body parts or emit simple
responses on cue (e.g., sit or stand; Baker
et al., 2010). Finally, Zoo Atlanta researchers
documented the changes in both trainer and
elephant (Loxodonta africana africana) behaviors
(e.g., frequency of trainer-delivered cues;
latency of elephant compliance) during a transition to protected contact (i.e., no human enters
the elephant’s habitat), positive reinforcementbased
management
system
(Wilson
et al., 2015).
All the above studies involved before/after
comparisons of various reinforcement-based
procedures to increase targeted behaviors. More
recently, several studies have directly examined
the shaping process to train petting zoo sheep
(Ovis aries), a petting zoo goat (Capra hircus),
and an African crested porcupine (Hystrix
cristata) for different desired behaviors, such as
walking on a halter or touching and holding to
a target (Fernandez, 2020; Fernandez &
Dorey, 2021; Fernandez & Rosales-Ruiz, 2021).
In addition, Lauderdale et al. (2021) examined
various features of training sessions on
bottlenose dolphins’ (Tursiops truncatus)
beaching/shifting responses, including number
of sessions and trials, mean trials per session,
time between sessions, criteria changes between
trials, and magnitude of reinforcers delivered.
Shaping research focused on continuous learning achievements, rather than pre- posttest
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
training results, should facilitate our understanding of the conditions that are more likely
to improve zoo animal handling practices.
Regardless, the idea is simple: Positive
reinforcement-based animal handling and training practices can increase the likelihood of better physiological welfare for zoo animals, in
addition to potentially functioning as behavioral enrichment (Fernandez, 2022).
Pest Control
Forthman and Ogden (1992) proposed that
applied behavior analytic techniques could be
useful in managing free ranging “pest” species
such as rodents and birds that enter zoo
exhibits and pose potential for disease transmission and other hazards. Although this area
has not seen a large growth in behavior analytic research, the potential remains. Before
implementing a pest-management program,
zoo personnel must take the behavior of both
pest species and zoo-housed species into
account. Applied behavior analysis could offer
guidance in this area. Most pest control techniques focus on antecedents that attract or
repel animals, and preference assessments can
be useful in determining traps an animal is
likely to enter (Carey et al., 1997) or baits an
animal is likely to consume (Allsop
et al., 2017; Morgan, 1990). In addition, if a
potentially harmful bait will be used in a zoo
enclosure, preference assessments and/or conditioned taste aversion can help to ensure that
the bait is unlikely to be consumed by nontarget animals (Clapperton et al., 2015, 2014).
Taking a more natural approach, antecedent
manipulations could be used to attract natural
predators such as barn owls to zoo grounds to
help reduce nuisance rodent populations
(Antkowiak & Hayes, 2004). The presumption is that the increased natural predators
themselves would impose no direct threat to
the exhibited zoo animals, which itself is an
empirical question worthy of applied behavior
analytic study.
Animal Performances
The training of marine mammals for shows
played a key role in the promotion of regular
husbandry training procedures in zoos, which
has been essential as an application for
improving zoo animal lives. As noted earlier,
this was due in large part to the influence of
Keller and Marian Breland in bringing behavior analytic principles to a variety of settings,
which included show animals located in dolphinariums (for a review, see Fernandez &
Martin, 2021). Since then, the use of positive
reinforcement to promote voluntary involvement in husbandry practices and improve
behavioral welfare has been a hallmark for
show animals (Brando, 2012; Eskelinen
et al., 2015). Nonetheless, in recent years
greater concern has been placed on the use of
animals for shows or performance, including
whether animals such as cetaceans (whales
and dolphins) should exist in any form of
captivity (Rose & Parsons, 2019). It is also
worth noting that modern zoos have updated
their focus on animal performances to include
educational efforts that promote the conservation and welfare of the individuals and species involved in such shows (D’Cruze
et al., 2019). In the past 30 years, the public
and the zoos themselves have had a dramatic
change in the perceptions of the purpose of
animal performances, including the outcomes
of these activities on the well-being of those
animals.
Although Forthman and Ogden (1992)
suggested that animal performances improve
the physiological and psychological welfare of
animals, it is only more recently that studies
have investigated the behavioral effects of animal performances or similar performance-like
interactions on the welfare of those animals.
For instance, Kyngdon et al. (2003) found that
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8
short-beaked common dolphins (Delphinus
delphis) trained to engage in a Swim-withDolphins program increased their surfacing and
use of outside areas during programs, but otherwise showed few behavioral changes before,
during, or after the interactions (thus
suggesting little to no negative welfare impact
from such programs). Similarly, Trone et al.
(2005) found few behavioral differences for
bottlenose dolphins (Tursiops truncatus) in the
times before or after interaction programs.
They additionally noted an increase in play
behaviors following interactions, which may
have indicated potential positive welfare effects
of the interactions. Finally, Fernandez,
Upchurch, and Hawkes (2021) examined the
effects of a visitor feeding program on the activity of the exhibited elephants. They successfully
demonstrated that the feeding programs
increased overall activity and decreased undesired behaviors, such as stereotypies. Thus, as
the purpose of animal performances in zoos has
changed, this should require greater understanding of the impact of such shows on the
animals. Future applied behavioral research in
zoos could focus more directly on some of
these direct welfare impacts, as well as what visitors learn from such shows.
Current and Future Directions
Below, we consider additional areas of focus
that are of mutual interest to both the field of
behavior analysis and zoos. These three foci
include: (a) experimental analyses of behavior
and the zoo, (b) applied behavior analysis and
the zoo, and (c) single-case designs and the
zoo. We consider each of these areas because
basic and applied research have been traditional
distinctions for the field of behavior analysis,
and each focus has benefits they could bring to
future zoo research and application through
some of their areas of interest. Likewise, singlecase designs have been a staple of behavior analytic research and practice, and greater use of
9
such methods could directly benefit the welfare
of zoo animals.
Experimental Analyses of Behavior and
the Zoo
Although a detailed examination of all the
potential contributions of the experimental
analysis of behavior to zoo research exceeds the
purpose of this review, it is worth pointing out
several areas of overlap that are of mutual interest to both zoos and basic research in behavior
analysis. These three areas include studies that
involve (a) contrafreeloading, (b) autoshaping,
and (c) conditioned reinforcement. Below we
focus on how experimental studies of these
topics could simultaneously improve our scientific understanding of behavior while contributing to behavioral welfare improvements or
other applications meant to improve the lives
of zoo animals.
Contrafreeloading
Contrafreeloading describes the phenomenon
where animals will choose to work for food
(e.g., press a lever or operate similar operanda)
over freely available food (Jensen, 1963;
Neuringer, 1969). Although the concept of
contrafreeloading has been investigated across
multiple species and settings (for a review, see
Inglis et al., 1997), only a few studies have
examined contrafreeloading in zoos. For
instance, McGowan et al. (2010) demonstrated
that captive grizzly bears (Ursus arctos horribilis)
would spend at least a portion of their time
retrieving food from ice blocks or enrichment
boxes over consuming free food alone.
Vasconcellos et al. (2012) showed that captive
maned wolves (Chrysocyon brachyurus) would
spend more time searching for food scattered
across vegetation, as well as consume half their
diet from scattered feedings when compared to
food delivered on a tray in one section of their
enclosures. Sasson-Yenor and Powell (2019)
demonstrated that several zoo-housed giraffes
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
(Giraffa camelopardalis) were more likely to
contrafreeload when presented simultaneously
with easily accessed or more time-consuming
enrichment foraging devices.
The topic of contrafreeloading itself raises interesting theoretical questions about the interplay
between learning and evolved foraging patterns
(Killeen, 2019; Timberlake, 1984). In addition,
contrafreeloading should be of great interest to
zoos, because many of the problem behaviors
observed in exhibited animals (e.g., stereotypies)
have been associated with species-typical foraging
patterns (Fernandez, 2021; Fernandez &
Timberlake, 2019a). It could be argued that all
food-based enrichment deliveries elicit or set the
occasion for behavior like that observed in contrafreeloading procedures, and therefore should
equally be of interest for testing behavioral theories of contrafreeloading while benefiting
exhibited animals by increasing species-typical foraging patterns and increasing overall activity.
Autoshaping
Autoshaping describes a phenomenon in
which voluntary behavior, such as key pecking,
is respondently conditioned (Brown &
Jenkins, 1968; Williams & Williams, 1969).
Since the time of its discovery, it has been the
focus of intense theoretical scrutiny, including
the extent to which operant contingencies alone
can successfully describe the behaviors observed
under
standard
laboratory
conditions
(Timberlake, 2004; Timberlake & Lucas,
1989). The concept of autoshaping itself
should be of interest to both basic researchers
and practitioners when examining their effects
on zoo animals. For example, researchers have
been able to use respondent conditioning procedures to increase the reproductive success of
animals (Domjan et al., 1998; Gaalema, 2013;
Hollis et al., 1997). Given that reproductive
behavior is both a voluntary activity and of
great applied interest for zoo animals on Species
Survival Plans (SSP; AZA, 2022), behavior analysts would do well to help foster empirical
studies done on autoshaping and reproduction
in zoos. Likewise, autoshaping has been used as
a training procedure to increase time spent contacting a pool-based enrichment feeding device,
and therefore time spent swimming, in zoo
penguins (Fernandez et al., 2019). Again, like
efforts using autoshaping to increase reproductive efforts, autoshaping could be studied across
a plethora of species in zoos, while simultaneously increasing enrichment device interactions, and thus have applied welfare benefits in
the process of conducting such theoretical
examinations.
Conditioned Reinforcement
Conditioned reinforcement, whereby a secondary stimulus associated with a primary
reinforcer comes to maintain operant behavior,
has been an important concept for the experimental analysis of behavior (Lattal &
Fernandez, 2022; Pierce & Cheney, 2013). As
early as 1938, Skinner described how a clicking sound initially paired with food
reinforced lever pressing in the absence of food
deliveries. Both Skinner (1951) and Breland
and Breland (1951) would later describe the
importance of using conditioned reinforcement to train animals outside of the lab. The
idea was popularized by Pryor (1984) as a
form of “clicker training” that could be used
to train dogs, as well as other animals, for a
variety of applied purposes. In the lab, the
concept would become a focal point for
understanding operant procedures (for reviews,
see Fantino & Romanovich, 2007; Kelleher &
Gollub, 1962). Similarly, the use of conditioned reinforcement for applied purposes has
been examined, including whether conditioned reinforcement successfully improves
some dimension of responding, such as speed
of acquisition (Chiandetti et al., 2016; Dorey
et al., 2020; Dorey & Cox, 2018; Gilchrist
et al., 2021; Pfaller-Sadovsky et al., 2020).
Although the importance of understanding
conditioned reinforcement for both basic and
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10
applied research purposes remains, a divide still
exists between information obtained from the
lab and the field. For instance, early confusion
existed on delivering conditioned reinforcers in
the absence of primary reinforcers, an idea originally thought of as a form of intermittent reinforcement (often incorrectly described as
“variable reinforcement”; Fernandez, 2001).
Likewise, laboratory research on the importance
of delay-reduction and information hypotheses
of conditioned reinforcement (each relating to
the ability of some stimulus to successfully predict the occurrence of a following primary reinforcer more rapidly or accurately, respectively)
have rarely been acknowledged outside of the
lab, or only loosely identified or contrasted to
marking/bridging hypotheses as they might
apply in and outside of the lab (Dorey &
Cox, 2018; Egger & Miller, 1962;
Fantino, 1969; Williams, 1994). Zoos could
provide a testing ground for translational
research that experimentally examines the theoretical underpinnings of conditioned reinforcement, while providing a better connection
between lab and field studies of conditioned
reinforcement and improving the training procedures vital to the welfare of zoo animals.
Applied Behavior Analysis and the Zoo
In addition to using behavioral science to
optimize existing animal management practices
such as environmental enrichment, researchers
and zoo personnel have also borrowed specific
techniques and protocols from applied behavior
analytic clinical practices and modified them
for use in applied animal settings. This represents a unique reverse-translational cycle
(Dixon et al., 2016; Edwards & Poling, 2011;
Gray & Diller, 2017), where (a) basic principles from animal laboratory studies are used to
(b) develop effective behavioral assessments and
treatments in human clinical settings, and then
(c) these human clinical protocols are used to
improve captive animal care and welfare. As
11
pointed out by others (Bloomsmith
et al., 2007; Gray & Diller, 2017; Maple &
Segura, 2015; Martin, 2017), the research and
clinical approaches of behavior analysts have
commonalities with the needs of zoos that
make the transfer of behavioral technologies
between the two settings beneficial. These commonalities include treatments developed for
and evaluated at the individual level (Alligood
et al., 2017; DeRosa et al., 2021; Fisher,
Groff, & Roane, 2021; Saudargas &
Drummer, 1996) and a focus on both building
skills (Fisher, Piazza, & Roane, 2021; or, in
zoos, promoting species-typical behaviors) and
decreasing behavioral excesses, including some
of the same topographies of problem behavior
seen
in
both
settings
(Bloomsmith
et al., 2007). Below, we focus on two areas in
which methods developed in applied behavior
analytic clinical practice have been used in animal settings: (a) functional analysis, and
(b) preference assessments, as well as on
(c) untapped applications of applied behavior
analytic protocols.
Functional Analysis
One example of this reverse translational
research is the functional analysis technique.
Drawing from his work with laboratory animals, Skinner (1953) developed the conceptual
foundation for the functional analysis, emphasizing the impact of environmental events on
behavior. Iwata et al. (1982/1994) then formalized a behavioral protocol that identified the
existing environmental contingencies that reinforce and maintain problem behaviors. Over
the past four decades, behavior analysts have
successfully used function-based treatments in
human clinical settings to reduce behaviors
including self-injury, aggression, disruptiveness,
and food refusal (Beavers et al., 2013; Hanley
et al., 2003). More recently, researchers have
used this same approach to successfully assess
and treat problem behaviors in captive animals,
including in zoo-housed species. Functional
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
analysis has been used to assess and treat selfdirected behaviors as well as disruptive or
aggressive behaviors in nonhuman primates and
in birds (Table 1). In all cases, a function-based
treatment consisting of some combination of
extinction, differential reinforcement, noncontingent reinforcement, or some combination, have successfully reduced these problem
behaviors (Dorey et al., 2009; FarmerDougan, 2014; Franklin et al., 2022; Martin
et al., 2011; Morris & Slocum, 2019).
This functional approach to reducing
abnormal behaviors exhibited by animals has
many benefits, but it also has some limitations. Although most of the functional analyses conducted with zoo-housed species have
involved primates (Table 1), the inclusion of a
vulture (Morris & Slocum, 2019) as well as
the success of this approach in companion
dogs (Canis lupus familiaris) and cats (Felis
catus; Dorey et al., 2012; Hall et al., 2015;
Mehrkam et al., 2020; Pfaller-Sadovsky
et al., 2019; Salmeron et al., 2021; Winslow
et al., 2018) suggests that it can be useful
across a range of species. However, these
assessments are time- and labor-intensive, and
they can only be used to assess antecedents
and consequences that can be systematically
presented and withdrawn. Indeed, most functional analyses of zoo-housed species identified
either attention (i.e., attention function),
human-delivered food items (i.e., tangible
function), or both, as the reinforcer for the
problem behaviors (Table 1). Thus, in zoo settings, this approach seems especially useful to
assess problem behaviors that may be
maintained by interactions with zookeepers or
visitors. However, many abnormal behaviors
in zoo-housed animals are likely to be
maintained by consequences from other animals or by nonsocial (or “automatic”) reinforcers such as sensory stimulation or a
decrease in arousal. These behaviors are more
challenging to assess and treat; however, the
behavior analytic literature can offer some
guidance in these areas as well, including possibilities like antecedent assessments, noncontingent reinforcement, sensory extinction,
or
sensory-matched
enrichment
(see
Martin, 2017).
Table 1
Summary of Functional Analysis Studies Involving Zoo-Housed Species
Author(s) (Year)
Dorey et al.
(2009)
Farmer-Dougan
(2014)
Franklin et al.
(2022)
Martin et al.
(2011)
Morris &
Slocum
(2019)
Species
Target Behavior(s)
Experimental Design
Primary Function*
Olive baboon (Papio
hamadryas anubis)
Self-directed behavior (hair
pulling, hand biting, foot
biting)
Disruptive/aggressive
behavior (aggression
toward humans)
Disruptive/aggressive
behavior (noise)
Disruptive/aggressive
behavior (human-directed
feces throwing, object
throwing, and spitting;
screaming, cage shaking)
Self-directed (featherplucking)
Multielement
Positive reinforcement
(attention from
humans)
Other/unable to
determine
Black-and-white ruffed
lemur (Varecia
variegate variegata)
Rhesus macaque (Macaca
mulatta)
Chimpanzee (Pan
troglodytes)
Black vulture (Coragyps
atratus)
Other/unable to
determine
Multielement
Reversal
Multielement
* Primary function is the function identified as having the highest levels of behavior.
Positive reinforcement
(food)
Positive reinforcement
(attention and juice
from humans)
Positive reinforcement
(attention from
humans)
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Eduardo J. Fernandez and Allison L. Martin
12
Preference Assessments
Another behavioral protocol developed in
human clinical settings that has been of use in
zoos is the stimulus or reinforcer preference
assessment. In applied behavior analytic work
with children, empirical preference assessments
are conducted in educational settings, clinics,
and hospitals to determine items or activities
that are likely to serve as positive reinforcers for
desired behaviors (Saini et al., 2021). Protocols
include those in which items are presented one
at a time (Pace et al., 1985), in pairs (Fisher
et al., 1992), or in an array with multiple stimuli (DeLeon & Iwata, 1996), and selection is
measured. Items ranked higher in preference
(i.e., those that were selected most) using these
methods were often found to function as more
effective reinforcers for various desired behaviors than lower preference items (e.g., Carr
et al., 2000; Lee et al., 2010; Pace et al., 1985;
Piazza et al., 1996). Given the wide use of positive
reinforcement
training
in
zoos
(Fernandez & Martin, 2021), researchers and
zoo personnel recognize the importance of
using highly preferred items to make training
as efficient as possible. In addition, foods chosen by human or animal caregivers have been
found to have low correlation with preferences
determined empirically (e.g., Cote et al., 2007;
Gaalema et al., 2011; Green et al., 1988;
Mehrkam & Dorey, 2015), emphasizing the
need for empirical assessments.
The three decades since Forthman and
Ogden’s (1992) paper have seen a surge in the
use of empirical preference assessments in zoohoused species. As summarized in Table 2,
researchers have empirically determined preferences for a wide variety of species, from invertebrates to apes. Most preference assessments
have involved food, but some have involved
other stimuli, including enrichment items,
scents, and activities (see Table 2). Most studies
have used some variation of free-operant or
paired-choice presentations, but methods
involving single-item presentations and arrays
13
with three or more stimuli have also been used
(see Table 2). Additionally, there have been
some novel research extensions in that some
researchers have used symbolic representations
of items (e.g., images, tokens) to facilitate
choice whereas others have adapted methods by
presenting stimuli to groups of animals rather
than single animals (see Table 2).
In most of these animal preference studies,
some measure of choice (e.g., approach, consumption) was the main dependent variable.
However, some studies took an additional step
to determine if preference translated to reinforcer efficacy. Similar to findings in the
human literature, most studies have shown that
higher preference items served as more effective
reinforcers than lower preference items,
resulting in more lever presses (Dixon
et al., 2016), more touchscreen touches
(Hopper et al., 2019), more touches to training
targets (Martin et al., 2018), more enrichment
use (Fay & Miller, 2015; Fernandez &
Timberlake, 2019b; Mehrkam & Dorey, 2014;
Woods et al., 2020), higher engagement in
husbandry training (Martin et al., 2018), or
swimming against stronger currents (Sullivan
et al., 2016). However, one study (Schwartz
et al., 2016) showed no difference in amount
of work capuchin monkeys (Cebus apella) were
willing to perform (as measured by weight
lifted) based on preference as assessed via pairwise presentation. Preference assessments have
also been used to investigate concepts such as
preference for novelty (Addessi et al., 2005),
variety (Addessi, 2008; Addessi et al., 2010),
work/contrafreeloading (Sasson-Yenor & Powell, 2019), or choice (Perdue et al., 2014). Preference stability across time has also been
investigated (Addessi et al., 2010; Clay
et al., 2009; Hopper et al., 2019; Martin
et al., 2018; Vonk et al., 2022). All these findings can be used to guide animal management
practices to optimize welfare (see Broom &
Johnson, 2019). These protocols also offer zoo
animals choice, which is increasingly considered
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
14
Table 2
Summary of Preference Assessment Studies Involving Zoo-Housed Species
Author(s) (Year)
Addessi (2008)
Addessi et al. (2005)
Addessi et al. (2010)
Bloomfield et al. (2015)
Clayton & Shrock (2020)
Cox et al. (1996)
Dixon et al. (2016)
Dorey et al. (2015)
Fay & Miller (2015)
Fernandez & Timberlake
(2019b)
Fernandez et al. (2004)
Gaalema et al. (2011)
Hopper et al. (2019)
Huskisson et al. (2020)
Huskisson et al. (2021)
Martin et al. (2018)
Mehrkam & Dorey (2014)
Mehrkam & Dorey (2015)
Stimuli
Presentation
Capuchin monkeys (Cebus apella)
Capuchin monkeys (Cebus apella)
Capuchin monkeys (Cebus apella)
Food
Food
Mixed/multiple (food, symbols/tokens
representing foods)
Nonfood (views of humans)
Paired
Paired
Mixed/multiple (paired, array)
Food
Food
Paired (presented to groups)
Paired
Mixed/multiple (scents; food-based enrichment;
nonfood enrichment)
Mixed/multiple (Paired, Array)
Symbols (drawings representing foods)
Food
Paired
Array
Mixed/multiple (food-based enrichment;
symbols / items representing training
activities)
Nonfood (scents)
Paired
Food
Paired
Food
Food
Paired
Paired
Mixed/multiple (food, symbol/images of food)
Symbols (images of food)
Paired
Paired
Symbols (images of food, computer icon
representing a random food)
Paired
Food
Mixed/multiple (non-food/enrichment, symbol/
items representing human interaction
activities)
Mixed/multiple (nonfood enrichment, scents)
Array
Paired
Sumatran orangutans (Pongo pygmaeus abelii),
Bornean (Pongo pygmaeus pygmaeus) and
Sumatran orangutan hybrid
Slender-tailed meerkats (Suricata suricatta)
Sumatran organutans (Pongo pygmaeus abelii);
Bornean orangutan (Pongo pygmaeus pygmaeus)
Bengal tigers (Panthera tigris tigris); Siberian
(Panthera tigris altaica) and Bengal tiger
hybrid
California sea lion (Zalophus californianus)
Madagascar hissing cockroach (Gromphordahina
portentosa)
Gray wolves (Canis Lupus) and Artic wolves
(Canis Lupus Arctos)
Rothschild giraffes (Giraffa camelopardalis
rothschildi)
Ring-tailed lemurs (Lemur catta), red ruffed
lemurs (Varecia rubra), collared lemurs
(Eulemur collairs), and blue-eyed black lemurs
(Eulemur flavifrons)
Cotton-top tamarins (Saguinus oedipus)
Giant pandas (Ailuropoda melanoleuca) and
African elephants (Loxodonta africana)
Gorilla (Gorilla gorilla gorilla)
Gorillas (Gorilla gorilla gorilla), chimpanzees
(Pan troglodytes), Japanese macaques (Macaca
fuscata)
Western lowland gorillas (Gorilla gorilla gorilla),
chimpanzees (Pan troglodytes), Japanese
macaques (Macaca fuscata)
Rhesus macaques (Macaca mulatta)
Galapagos tortoises (Chelonoidis nigra)
Single
Paired
Eduardo J. Fernandez and Allison L. Martin
Brox et al. (2021)
Clay et al. (2009)
Species
Mixed/multiple (paired, single)
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Table 2
Continued
Author(s) (Year)
Perdue et al. (2014)
Remis (2002)
Sasson-Yenor & Powell
(2019)
Schwartz et al. (2016)
Slocum & Morris (2022)
Sullivan et al. (2016)
Truax & Vonk (2021)
Vonk et al. (2022)
Woods et al. (2020)
Squirrel monkeys (Saimiri); springbok
(Antidorcas marsupialis), red-billed hornbirds
(Tockus erythrorhynchus), Eastern indigo snake
(Drymarchon couperi), American bullfrog
(Lithobates catesbeianus), Mexican redknee
tarantula (Brachypelma)
Japanese macaques (Macaca fuscata)
Tortoises (Chelonoidis denticulata)
Capuchin monkeys (Cebus), rhesus macaques
(Macaca mulatta)
Western lowland gorillas (Gorilla gorilla gorilla),
chimpanzees (Pan troglodytes)
Rothschild’s giraffe (Giraffa camelopardalis
rothschildi)
Capuchin monkeys (Cebus apella)
Black vultures (Coragyps atratus), turkey vulture
(Cathartes aura)
Goldfish (Carassius auratus)
Western lowland gorillas (Gorilla gorilla gorilla)
Western lowland gorillas (Gorilla gorilla gorilla)
lions (Panthera leo)
Stimuli
Presentation
Symbols (thumbnails of videos)
Mixed/multiple (food-based enrichment,
nonfood enrichment)
Symbols (icons representing computer tasks)
Array
Mixed/multiple (single, array)
Mixed/multiple (paired, array)
Foods
Paired
Mixed/multiple (food, food-based enrichment)
Food
Food
Mixed/multiple (paired with duplication,
presented to group)
Paired
Paired
Nonfood (plant enrichment)
Symbols (icons representing sounds)
Mixed/multiple (foods, symbols/images of foods)
Mixed/multiple (scents, nonfood enrichment)
Paired
Mixed/multiple (paired, array)
Paired
Paired
Applied Behavior Analysis and the Zoo
Ogura & Matsuzawa (2012)
Passos et al. (2014)
Species
15
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Eduardo J. Fernandez and Allison L. Martin
an important component of animal welfare
(Melfi & Ward, 2020; Patterson-Kane
et al., 2008; Wickins-Drazilova, 2006).
Untapped Applications of Applied Behavior
Analysis Protocols
Although we have highlighted two behavioral
protocols that were developed in human treatment clinics and adapted for use in the zoo
(functional analysis and preference assessments), there are many other behavioral protocols that could be useful in zoo settings. For
example, a veterinarian having difficulty getting
an animal to consume oral medications could
borrow from the applied behavior analytic literature related to blending (Mueller et al., 2004)
or the use of chasers (Vaz et al., 2012; see Daly
et al., 2019) to increase food consumption.
A zookeeper working to train a long-duration
behavior could model their training after other
applied research involving percentile schedules
(e.g., Athens et al., 2007; Galbicka, 1994; Hall
et al., 2009). Continued and additional bidirectional translation from applied research
with humans to applied research with zoo animals has considerable potential. However, realizing the full potential of applied behavior
analysis in zoo settings will require the training
of more individuals who are both well-versed in
the fundamentals of behavior analysis and who
have experience in animal management, so that
new behavioral protocols can be developed and
implemented to maximize animal welfare
(Fernandez & Timberlake, 2008; Friedman
et al., 2021; Gray & Diller, 2017; Maple &
Perdue, 2013; Maple & Segura, 2015;
Martin, 2017).
Single-Case Designs and the Zoo
A final note worth making is the importance
of single-case designs in the study and improvement of the behavioral welfare of zoo animals.
Single-case methods are used to analyze how
the behavior of an individual changes over time
(Skinner, 1957; Skinner, 1966b). The zoo
environment has a strong need for understanding how individuals change over time, given
the limited number of animals often exhibited
in any one enclosure, as well as the demand for
determining the function of any event, such as
environmental enrichment, on the individual
behaviors of those zoo-housed animals
(Alligood et al., 2017; Fernandez &
Timberlake, 2008; Maple & Segura, 2015).
Unfortunately, a common misconception made
by those working in zoos and similar applied
settings is that without sufficient numbers of
individuals to perform between-subject comparisons, the only options left are case studies
or observation-only designs (Fernandez, 2022;
Kazdin, 2021). However, as noted in the paragraph above and by the title of this section,
single-case designs offer quantitative, empirical
solutions to optimally understand zoo animal
behavior. Some of the many benefits of singlecase designs (over between-subject designs)
include (a) a focus on many data points from a
few individuals (as opposed to few data points
from many individuals), (b) an emphasis on
inductive data collection that modifies procedures based on real-time results (as opposed to
a priori hypothesis testing), and (c) the assessment of an individual’s learning repeatedly and
over time (as opposed to pre- vs. posttest analyses; Bailey & Burch, 2017; DeRosa
et al., 2021; Johnston & Pennypacker, 2010).
In short, all research efforts aimed at improving
the lives of individual animals are studies of
n = 1 (Walker & Carr, 2021). Even if it were
possible to produce enough subjects to run a
standard between-subject study on some welfare advancement (generally not the case, given
the limitations of exhibit space size and/or species numbers within zoos), providing individualized welfare plans based on differences
between the average of some group is of limited
use if the animal in question does not respond
in the average way. Single-case designs allow
for the empirical examination of each
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
16
individual animal’s important behavior contingencies to best promote welfare.
Forthman and Odgen (1992) saw the great
potential for applied behavior analysis and zoo
collaborations. In the three decades since their
publication, applied behavior analysis has provided the scientific basis for many empirical
studies that have both advanced applied science
and have improved the welfare of zoo animals.
Behavior analytic methodologies and their focus
on the overt behaviors of individuals is ideally
suited for improving the lives of zoo animals,
and it is our hope that this updated review of
applied behavior analysis in zoos provides a
proper framework for both past efforts and
future endeavors to continue making such
research possible.
REFERENCES
*References marked with an asterisk indicate studies summarized in a table rather than in text.
Addessi, E. (2008). Food variety-seeking in tufted capuchin monkeys (Cebus apella). Physiology & Behavior,
https://doi.org/10.1016/j.
93(1–2),
304–309.
physbeh.2007.09.001
Addessi, E., Mancini, A., Crescimbene, L., Ariely, D., &
Visalberghi, E. (2010). How to spend a token?
Trade-offs between food variety and food preference
in tufted capuchin monkeys (Cebus apella). Behavioural Processes, 83(3), 267–275. https://doi.org/10.
1016/j.beproc.2009.12.012
Addessi, E., Stammati, M., Sabbatini, G., &
Visalberghi, E. (2005). How tufted capuchin monkeys (Cebus apella) rank monkey chow in relation to
other foods. Animal Welfare, 14(3), 215–222.
Alligood, C. A., Daneault, A. J., Carlson, R. C.,
Dillenbeck, T., Wheaton, C. J., & Savage, A.
(2011). Development of husbandry practices for the
captive breeding of Key Largo woodrats (Neotoma
floridana smalli). Zoo Biology, 30(3), 318–327.
https://doi.org/10.1002/zoo.20205
Alligood, C. A., Dorey, N. R., Mehrkam, L. R., &
Leighty, K. A. (2017). Applying behavior-analytic
methodology to the science and practice of environmental enrichment in zoos and aquariums. Zoo Biology, 36(3), 175–185. https://doi.org/10.1002/zoo.
21368
Alligood, C. A., Wheaton, C. J., Forde, H. M.,
Smith, K. N., Daneault, A. J., Carlson, R. C., &
Savage, A. (2008). Pup development and maternal
17
behavior in captive Key Largo woodrats (Neotoma
floridana smalli). Zoo Biology, 27(5), 394–405.
https://doi.org/10.1002/zoo.20205
Allsop, S. E., Dundas, S. J., Adams, P. J., Kreplins, T. L.,
Bateman, P. W., & Fleming. P. A. (2017). Reduced
efficacy of baiting programs for invasive species: Some
mechanisms and management implications. Pacific
Conservation Biology, 23(3), 240–257. https://doi.org/
10.1071/PC17006
Andrews, N. L., & Ha, J. C. (2014). The effects of automated scatter feeders on captive grizzly bear activity
budgets. Journal of Applied Animal Welfare Science,
17(2), 148–156. https://doi.org/10.1080/10888705.
2013.856767
Antkowiak, K., & Hayes, T. (2004). Rodent pest control
through the reintroduction of an extirpated raptor
species. Endangered Species Update, 21(4), 124–128.
Association of Zoos and Aquariums (2022). Species Survival Plan Programs [On-line]. https://www.aza.org/
species-survival-plan-programs
Athens, E. S., Vollmer, T. R., & St. Peter Pipkin, C. C.
(2007). Shaping academic task engagement with percentile schedules. Journal of Applied Behavior Analysis,
40(3), 475–488. https://doi.org/10.1901/jaba.2007.
40-475
Bailey, J. S., & Burch, M. R. (2017). Research methods in
applied behavior analysis. Routledge.
Baker, K. C., Bloomsmith, M. A., Neu, K., Griffis, C., &
Maloney, M. (2010). Positive reinforcement training
as enrichment for singly housed rhesus macaques
(Macaca mulatta). Animal Welfare, 19(3), 307–313.
https://pubmed.ncbi.nlm.nih.gov/25960611
Bashaw, M. J. (2011). Consistency of captive giraffe
behavior under two different management regimes.
Zoo Biology, 30(4), 371–378. https://doi.org/10.
1002/zoo.20338
Bashaw, M. J., Bloomsmith, M. A., Maple, T. L., &
Bercovitch, F. B. (2007). The structure of social relationships among captive female giraffe (Giraffa camelopardalis). Journal of Comparative Psychology, 121(1),
46. https://doi.org/10.1037/0735-7036.121.1.46
Baum, W. M. (2012). Rethinking reinforcement: Allocation, induction, and contingency. Journal of the
Experimental Analysis of Behavior, 97(1), 101–124.
https://doi.org/10.1901/jeab.2012.97-101
Beavers, G. A., Iwata, B. A., & Lerman, D. C. (2013).
Thirty years of research on the functional analysis of
problem behavior. Journal of Applied Behavior Analysis, 46(1), 1–21. https://doi.org/10.1002/jaba.30
*Bloomfield, R. C., Gillespie, G. R., Kerswell, K. J.,
Butler, K. L., & Hemsworth, P. H. (2015). Effect of
partial covering of the visitor viewing area window on
positioning and orientation of zoo orangutans:
A preference test. Zoo Biology, 34(3), 223–229.
https://doi.org/10.1002/zoo.21207
Bloomsmith, M. A., & Lambeth, S. P. (1995). Effects of
predictable versus unpredictable feeding schedules on
chimpanzee behavior. Applied Animal Behaviour
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
Science, 44(1), 65–74. https://doi.org/10.1016/01681591(95)00570-I
Bloomsmith, M. A., Marr, M. J., & Maple, T. L. (2007).
Addressing nonhuman primate behavioral problems
through the application of operant conditioning: Is
the human treatment approach a useful model?
Applied Animal Behaviour Science, 102(3–4), 205–
222. https://doi.org/10.1016/j.applanim.2006.05.028
Bloomsmith, M. A., Stone, A. M., & Laule, G. E.
(1998). Positive reinforcement training to enhance
the voluntary movement of group-housed chimpanzees within their enclosures. Zoo Biology, 17(4), 333–
https://doi.org/10.1002/(SICI)1098-2361
341.
(1998)17:4<333::AID-ZOO6>3.0.CO;2-A
Brando, S. I. (2012). Animal learning and training: Implications for animal welfare. Veterinary Clinics: Exotic
Animal Practice, 15(3), 387–398. https://doi.org/10.
1016/j.cvex.2012.06.008
Breland, K., & Breland, M. (1951). A field of applied animal psychology. American Psychologist, 6(6), 202.
https://doi.org/10.1037/h0063451
Breland, K., & Breland, M. (1961). The misbehavior of
organisms. American Psychologist, 16(11), 681.
https://doi.org/10.1037/h0040090
Broom, D. M., & Johnson, K. G. (2019). Preference
studies and welfare. In D. M. Broom & K. G. Johnson (Eds.), Stress and animal welfare (Vol. 19,
pp. 173–191). Springer. https://doi.org/10.1007/
978-3-030-32153-6_7
Brown, P. L., & Jenkins, H. M. (1968). Auto-shaping of
the pigeon’s key-peck. Journal of the Experimental
Analysis of Behavior, 11(1), 1–8. https://doi.org/10.
1901/jeab.1968.11-1
Browning, H. (2020). The natural behavior debate: Two
conceptions of animal welfare. Journal of Applied Animal Welfare Science, 23(3), 325–337. https://doi.org/
10.1080/10888705.2019.1672552
*Brox, B. W., Edwards, K., Buist, N. A., &
Macaskill, A. C. (2021). Investigating food preference
in zoo-housed meerkats. Zoo Biology, 40(6), 517–
526. https://doi.org/10.1002/zoo.21640
Bryan, K., Bremner-Harrison, S., Price, E., &
Wormell, D. (2017). The impact of exhibit type on
behaviour of caged and free-ranging tamarins. Applied
Animal Behaviour Science, 193, 77–86. https://doi.
org/10.1016/j.applanim.2017.03.013
Carey, P. W., O’Connor, C. E., McDonald, R. M., &
Matthews, L. R. (1997). Comparison of the attractiveness of acoustic and visual stimuli for brushtail
possums. New Zealand Journal of Zoology, 24(4),
273–276. https://doi.org/10.1080/03014223.1997.
9518124
Carlstead, K., Brown, J. L., & Seidensticker, J. (1993).
Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo
Biology, 12(4), 321–331. https://doi.org/10.1002/
zoo.1430120403
Carlstead, K., & Seidensticker, J. (1991). Seasonal variation in stereotypic pacing in an American black bear
(Ursus americanus). Behavioural Processes, 25(2–3),
https://doi.org/10.1016/0376-6357(91)
155–161.
90017-T
Carlstead, K., Seidensticker, J., & Baldwin, R. (1991).
Environmental enrichment for zoo bears. Zoo Biology,
https://doi.org/10.1002/zoo.
10(1),
3–16.
1430100103
Carr, J. E., Nicolson, A. C., & Higbee, T. S. (2000).
Evaluation of a brief multiple-stimulus preference
assessment in a naturalistic context. Journal of Applied
Behavior Analysis, 33(3), 353–357. https://doi.org/10.
1901/jaba.2000.33-353
Carter, M., Sherwen, S., & Webber, S. (2021). An evaluation of interactive projections as digital enrichment
for orangutans. Zoo Biology, 40(2), 107–114. https://
doi.org/10.1002/zoo.21587
Castro, M. I., Beck, B. B., Kleiman, D. G., RuizMiranda, C. R., & Rosenberger, A. L. (1998). Environmental enrichment in a reintroduction program
for golden lion tamarins. In D. J. Shepherdson, J. D.
Mellen, & M. Hutchins (Eds.), Second nature: Environmental enrichment for captive animals (pp. 97–
128). Smithsonian Books.
Chiandetti, C., Avella, S., Fongaro, E., & Cerri, F.
(2016). Can clicker training facilitate conditioning in
dogs? Applied Animal Behaviour Science, 184, 109–
116. https://doi.org/10.1016/j.applanim.2016.08.006
Clapperton, B. K., Morgan, D. K. J., Day, T. D.,
Oates, K. E., Beath, A. M., Cox, N. R., &
Matthews, L. R. (2014). Efficacy of bird repellents at
deterring North Island robins (Petroica australis
longipes) and tomtits (P. macrocephala toitoi) from
baits. New Zealand Journal of Ecology, 38(1), 116–
123. http://www.jstor.org/stable/24060829
Clapperton, B. K., Day, T. D., Morgan, D. K. J.,
Huddart, F., Cox, N., & Matthews, L. R. (2015).
Palatability and efficacy to possums and rats of pest
control baits containing bird repellents. New Zealand
Journal of Zoology, 42(2), 104–118. https://doi.org/
10.1080/03014223.2015.1029496
Clay, A. W., Bloomsmith, M. A., Marr, M. J., &
Maple, T. L. (2009). Systematic investigation of the
stability of food preferences in captive orangutans:
Implications for positive reinforcement training. Journal of Applied Animal Welfare Science, 12(4), 306–
313. https://doi.org/10.1080/10888700903163492
Clayton, M., & Shrock, T. (2020). Making a tiger’s day:
Free-operant assessment and environmental enrichment to improve the daily lives of captive Bengal
tigers (Panthera tigris tigris). Behavior Analysis in Practice, 13(4), 883–893. https://doi.org/10.1007/
s40617-020-00478-z
Coe, J. (2004). Mixed species rotation exhibits. In 2004
ARAZPA Conference Proceedings. https://docslib.org/
doc/935621/mixed-species-rotation-exhibits-2004arazpa-conference-proceedings-australia-on-cd
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
18
Coe, J., & Hoy, J. (2020). Choice, control and computers: Empowering wildlife in human care. Multimodal Technologies and Interaction, 4(4), 92–109.
https://doi.org/10.3390/mti4040092
Cote, C. A., Thompson, R. H., Hanley, G. P., &
McKerchar, P. M. (2007). Teacher report and direct
assessment of preferences for identifying reinforcers
for young children. Journal of Applied Behavior Analysis, 40(1), 157–166. https://doi.org/10.1901/jaba.
2007.177-05
*Cox, M., Gaglione, E., Prowten, P., & Noonan, M.
(1996). Food preferences communicated via symbol
discrimination by a California sea lion (Zalophus californianus). Aquatic Mammals, 22(1), 3–10.
D’Cruze, N., Khan, S., Carder, G., Megson, D.,
Coulthard, E., Norrey, J., & Groves, G. (2019). A
global review of animal–visitor interactions in modern zoos and aquariums and their implications for
wild animal welfare. Animals, 9(6), 332–352. https://
doi.org/10.3390/ani9060332
Dadone, L. I., Schilz, A., Friedman, S. G., Bredahl, J.,
Foxworth, S., & Chastain, B. (2016). Training giraffe
(Giraffa camelopardalis reticulata) for front foot radiographs and hoof care. Zoo Biology, 35(3), 228–236.
https://doi.org/10.1002/zoo.21279
Daly, M. B., Clayton, A. M., Ruone, S., Mitchell, J.,
Dinh, C., Holder, A., Jolly, J., GarciaLerma, J. G., & Weed, J. L. (2019). Training rhesus
macaques to take daily oral antiretroviral therapy for
preclinical evaluation of HIV prevention and treatment strategies. Plos One, 14(11), e0225146. https://
doi.org/10.1371/journal.pone.0225146
Davey, G. (2007). Visitors’ effects on the welfare of animals in the zoo: A review. Journal of Applied Animal
Welfare Science, 10(2), 169–183. https://doi.org/10.
1080/10888700701313595
DeLeon, I. G., & Iwata, B. A. (1996). Evaluation of a
multiple-stimulus presentation format for assessing
reinforcer preferences. Journal of Applied Behavior
Analysis, 29(4), 519–533. https://doi.org/10.1901/
jaba.1996.29-519
DeRosa, N. M., Sullivan, W. E., Roane, H. S.,
Craig, A. R., & Kadey, H. J. (2021). Single-case
experimental design. In W. W. Fisher, C. C.
Piazza, & H. S. Roane (Eds). Handbook of applied
behavior analysis (2nd ed., pp. 155–171). Guilford
Press.
Dixon, M. R., Daar, J. H., Gunnarsson, K.,
Johnson, M. L., & Shayter, A. M. (2016). Stimulus
preference and reinforcement effects of the
Madagascar hissing cockroach (Gromphordahina
portentosa): A case of reverse translational research.
The Psychological Record, 66(1), 41–51. https://doi.
org/10.1007/s40732-015-0149-9
Domjan, M. (1983). Biological constraints on instrumental and classical conditioning: Implications for general
process theory. Psychology of Learning & Motivation,
19
17, 215–277. https://doi.org/10.1016/S0079-7421
(08)60100-0
Domjan, M., Blesbois, E., & Williams, J. (1998). The
adaptive significance of sexual conditioning: Pavlovian control of sperm release. Psychological Science,
9(5), 411–415. https://doi.org/10.1111/1467-9280.
00077
Dorey, N. R., Blandina, A., & Udell, M. A. (2020).
Clicker training does not enhance learning in mixedbreed shelter puppies (Canis familiaris). Journal of
Veterinary Behavior, 39, 57–63. https://doi.org/10.
1016/j.jveb.2020.07.005
Dorey, N. R., & Cox, D. J. (2018). Function matters: A
review of terminological differences in applied and
basic clicker training research. PeerJ, 6, e5621.
https://doi.org/10.7717/peerj.5621
Dorey, N. R., Mehrkam, L. R., & Tacey, J. (2015). A
method to assess relative preference for training and
environmental enrichment in captive wolves (Canis
lupus and Canis lupus arctos). Zoo Biology, 34(6),
513–517. https://doi.org/10.1002/zoo.21239
Dorey, N. R., Rosales-Ruiz, J., Smith, R., & Lovelace, B.
(2009). Functional analysis and treatment of selfinjury in a captive olive baboon. Journal of Applied
Behavior Analysis, 42(4), 785–794. https://doi.org/10.
1901/jaba.2009.42-785
Dorey, N. R., Tobias, J. S., Udell, M. A., &
Wynne, C. D. (2012). Decreasing dog problem
behavior with functional analysis: Linking diagnoses
to treatment. Journal of Veterinary Behavior, 7(5),
276–282. https://doi.org/10.1016/j.jveb.2011.10.002
Edwards, T. L., & Poling, A. (2011). Animal research in
the Journal of Applied Behavior Analysis. Journal of
Applied Behavior Analysis, 44(2), 409–412. https://
doi.org/10.1901/jaba.2011.44-409
Egger, M. D., & Miller, N. E. (1962). Secondary reinforcement in rats as a function of information value
and reliability of the stimulus. Journal of Experimental
Psychology, 64(2), 97. https://doi.org/10.1037/
h0040364
English, M., Kaplan, G., & Rogers, L. J. (2014). Is painting by elephants in zoos as enriching as we are led to
believe? PeerJ, 2, e471. https://doi.org/10.7717/
peerj.471
Eskelinen, H. C., Winship, K. A., & Borger-Turner, J. L.
(2015). Sex, age, and individual differences in
bottlenose dolphins (Tursiops truncatus) in response
to environmental enrichment. Animal Behavior and
Cognition, 2(3), 241–253. https://doi.org/10.12966/
abc.08.04.2015
Fa, J. E., Funk, S. M., & O’Connell, D. (2011). Zoo conservation biology. Cambridge University Press.
Fantino, E. (1969). Choice and rate of reinforcement.
Journal of the Experimental Analysis of Behavior,
12(5), 723–730. https://doi.org/10.1901/jeab.1969.
12-723
Fantino, E., & Romanowich, P. (2007). The effect of
conditioned reinforcement rate on choice: A review.
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
Journal of the Experimental Analysis of Behavior,
87(3), 409–421. https://doi.org/10.1901/jeab.2007.
44-06
Farmer, H. L., Plowman, A. B., & Leaver, L. A. (2011).
Role of vocalisations and social housing in breeding
in captive howler monkeys (Alouatta caraya). Applied
Animal Behaviour Science, 134(3–4), 177–183.
https://doi.org/10.1016/j.applanim.2011.07.005
Farmer-Dougan, V. (2014). Functional analysis of aggression in a black-and-white ruffed lemur (Varecia variegata variegata). Journal of Applied Animal Welfare
Science, 17(3), 282–293. https://doi.org/10.1080/
10888705.2014.917029
Fay, C., & Miller, L. J. (2015). Utilizing scents as environmental enrichment: Preference assessment and
application with Rothschild giraffe. Animal Behavior
and Cognition, 2(3), 285–291. https://doi.org/10.
12966/abc.08.07.2015
Fernandez, E. J. (2001). Click or treat: A trick or two in
the zoo. American Animal Trainer Magazine, 2(2),
41–44.
Fernandez, E. J. (2017). The empirical zoo in the 21st
century: The professor in the zoo, Maple, T. L Red
Leaf Press, Tequesta, FL, 2016. pp. 360. Zoo Biology,
36(2), 170–171. https://doi.org/10.1002/zoo.21356
Fernandez, E. J. (2020). Training petting zoo sheep to act
like petting zoo sheep: An empirical evaluation of
response-independent schedules and shaping with
negative reinforcement. Animals, 10(7), 1122–1135.
https://doi.org/10.3390/ani10071122
Fernandez, E. J. (2021). Appetitive search behaviors and
stereotypies in polar bears (Ursus maritimus). Behavioural Processes, 182, 104299. https://doi.org/10.
1016/j.beproc.2020.104299
Fernandez, E. J. (2022). Training as enrichment: A critical review. Animal Welfare, 31(1), 1–12. https://doi.
org/10.7120/09627286.31.1.001
Fernandez, E. J., & Chiew, S. J. (2021). Animal-visitor
interactions: Effects, experiences, and welfare. Animal
Behavior and Cognition, 8(4), 462–467. https://doi.
org/10.26451/abc.08.04.13.2021
Fernandez, E. J., & Dorey, N. R. (2021). An examination
of shaping with an African crested porcupine (Hystrix
cristata). Journal of Applied Animal Welfare Science,
24(4), 372–378. https://doi.org/10.1080/10888705.
2020.1753191
Fernandez, E. J., Dorey, N., & Rosales-Ruiz, J. (2004). A
two-choice preference assessment with five cotton-top
tamarins (Saguinus oedipus). Journal of Applied Animal
Welfare Science, 7(3), 163–169. https://doi.org/10.
1207/s15327604jaws0703_2
Fernandez, E., & Harvey, E. (2021). Enclosure use as a
measure of behavioral welfare in zoo-housed African
wild dogs (Lycaon pictus). Journal of Zoo and Aquarium Research, 9(2), 88–93. https://doi.org/10.19227/
jzar.v9i2.526
Fernandez, E. J., Kinley, R. C., & Timberlake, W.
(2019). Training penguins to interact with
enrichment devices for lasting effects. Zoo Biology,
38(6), 481–489. https://doi.org/10.1002/zoo.21510
Fernandez, E. J., & Martin, A. L. (2021). Animal training, environment enrichment, and animal welfare: A
history of behavior analysis in zoos. Journal of Zoological and Botanical Gardens, 2(4), 531–543. https://
doi.org/10.3390/jzbg2040038
Fernandez, E. J., Myers, M., & Hawkes, N. C. (2021).
The effects of live feeding on swimming activity and
exhibit use in zoo Humboldt penguins (Spheniscus
humboldti). Journal of Zoological and Botanical Gardens, 2(1), 88–100. https://doi.org/10.3390/
jzbg2010007
Fernandez, E. J., Ramirez, M., & Hawkes, N. C. (2020).
Activity and pool use in relation to temperature and
water changes in zoo hippopotamuses (Hippopotamus
amphibious). Animals, 10(6), 1022. https://doi.org/
10.3390/ani10061022
Fernandez, E. J., & Rosales-Ruiz, J. (2021). A comparison
of fixed-time food schedules and shaping involving a
clicker for halter behavior in a petting zoo goat. The
Psychological Record, 71(3), 487–491. https://doi.org/
10.1007/s40732-020-00420-3
Fernandez, E. J., Tamborski, M. A., Pickens, S. R., &
Timberlake, W. (2009). Animal–visitor interactions
in the modern zoo: Conflicts and interventions.
Applied Animal Behaviour Science, 120(1–2), 1–8.
https://doi.org/10.1016/j.applanim.2009.06.002
Fernandez, E. J., & Timberlake, W. (2008). Mutual benefits of research collaborations between zoos and academic institutions. Zoo Biology, 27(6), 470–487.
https://doi.org/10.1002/zoo.20215
Fernandez, E. J., & Timberlake, W. (2019a). Foraging
devices as enrichment in captive walruses (Odobenus
rosmarus). Behavioural Processes, 168, 103943. https://
doi.org/10.1016/j.beproc.2019.103943
Fernandez, E. J., & Timberlake, W. (2019b). Selecting
and testing environmental enrichment in lemurs.
Frontiers in Psychology, 10, 2119. https://doi.org/10.
3389/fpsyg.2019.02119
Fernandez, E. J., Upchurch, B., & Hawkes, N. C.
(2021). Public feeding interactions as enrichment for
three zoo-housed elephants. Animals, 11(6), 1689.
https://doi.org/10.3390/ani11061689
Fisher, W., Piazza, C. C., Bowman, L. G.,
Hagopian, L. P., Owens, J. C., & Slevin, I. (1992).
A comparison of two approaches for identifying reinforcers for persons with severe and profound disabilities. Journal of Applied Behavior Analysis, 25(2), 491–
498. https://doi.org/10.1901/jaba.1992.25-491
Fisher, W. W., Groff, R. A., & Roane, H. S. (2021).
Applied behavior analysis: History, philosophy, principles, and basic methods. In W. W. Fisher, C. C.
Piazza, & H. S. Roane (Eds.), Handbook of applied
behavior analysis (2nd ed., pp. 3–12). Guilford
Publications.
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
20
Fisher, W. W., Piazza, C. C., & Roane, H. S. (Eds.).
(2021). Handbook of applied behavior analysis (2nd
ed.). Guilford Publications.
Forthman, D. L., & Ogden, J. J. (1992). The role of
applied behavior analysis in zoo management: Today
and tomorrow. Journal of Applied Behavior Analysis,
25(3), 647–652. https://doi.org/10.1901/jaba.1992.
25-647
Forthman-Quick, D. L. (1984). An integrative approach
to environmental engineering in zoos. Zoo Biology,
https://doi.org/10.1002/zoo.
3(1),
65–77.
1430030107
Franklin, A. N., Martin, A. L., Perlman, J. E., &
Bloomsmith, M. A. (2022). Functional analysis and
treatment of disruptive behavior in a rhesus macaque.
Journal of Applied Animal Welfare Science, 25(3),
287–296. https://doi.org/10.1080/10888705.2021.
1931868
Fraser, D. (2008). Understanding animal welfare. Acta
Veterinaria Scandinavica, 50(1), 1–7. https://doi.org/
10.1186/1751-0147-50-S1-S1
Friedman,
S.
G.,
Stringfield,
C.
E.,
&
Desmarchelier, M. R. (2021). Animal behavior and
learning: Support from applied behavior analysis. Veterinary Clinics: Exotic Animal Practice, 24(1), 1–16.
https://doi.org/10.1016/j.cvex.2020.08.002
Gaalema, D. E. (2013). Sexual conditioning in the dyeing
poison dart frog (Dendrobates tinctorius). International
Journal of Comparative Psychology, 26(1), 5–18.
Gaalema, D. E., Perdue, B. M., & Kelling, A. S. (2011).
Food preference, keeper ratings, and reinforcer effectiveness in exotic animals: The value of systematic
testing. Journal of Applied Animal Welfare Science, 14,
https://doi.org/10.1080/10888705.2011.
33–41.
527602
Galbicka, G. (1994). Shaping in the 21st century: Moving
percentile schedules into applied settings. Journal of
Applied Behavior Analysis, 27(4), 739–760. https://
doi.org/10.1901/jaba.1994.27-739
Gilchrist, R. J., Gunter, L. M., Anderson, S. F., &
Wynne, C. D. (2021). The click is not the trick: The
efficacy of clickers and other reinforcement methods
in training naïve dogs to perform new tasks. PeerJ, 9,
e10881. https://doi.org/10.7717/peerj.10881
Godinez, A. M., & Fernandez, E. J. (2019). What is the
zoo experience? How zoos impact a visitor’s behaviors, perceptions, and conservation efforts. Frontiers
in Psychology, 10, 1746. https://doi.org/10.3389/
fpsyg.2019.01746
Grandin, T., Rooney, M. B., Phillips, M.,
Cambre, R. C., Irlbeck, N. A., & Graffam, W.
(1995). Conditioning of nyala (Tragelaphus angasi) to
blood sampling in a crate with positive reinforcement. Zoo Biology, 14(3), 261–273. https://doi.org/
10.1002/zoo.1430140307
Gray, J. M., & Diller, J. W. (2017). Evaluating the work
of applied animal behaviorists as applied behavior
21
analysis. Behavior Analysis: Research and Practice,
17(1), 33–41. https://doi.org/10.1037/bar0000041
Green, C. W., Reid, D. H., White, L. K., Halford, R. C.,
Brittain, D. P., & Gardner, S. M. (1988). Identifying
reinforcers for persons with profound handicaps: Staff
opinion versus systematic assessment of preferences.
Journal of Applied Behavior Analysis, 21(1), 31–43.
https://doi.org/10.1901/jaba.1988.21-31
Hall, N. J., Protopopova, A., & Wynne, C. D. (2015).
The role of environmental and owner-provided consequences in canine stereotypy and compulsive behavior. Journal of Veterinary Behavior, 10(1), 24–35.
https://doi.org/10.1016/j.jveb.2014.10.005
Hall, S. S., Maynes, N. P., & Reiss, A. L. (2009). Using
percentile schedules to increase eye contact in children with fragile X syndrome. Journal of Applied
Behavior Analysis, 42(1), 171–176. https://doi.org/10.
1901/jaba.2009.42-171
Hancocks, D. (1980). Bringing nature into the zoo: Inexpensive solutions for zoo environments. International
Journal for the Study of Animal Problems, 1(3), 170–
177. https://www.wellbeingintlstudiesrepository.org/
ijsap/vol1/iss3/7
Hanley, G. P., Iwata, B. A., & McCord, B. E. (2003).
Functional analysis of problem behavior: A review.
Journal of Applied Behavior Analysis, 36(2), 147–185.
https://doi.org/10.1901/jaba.2003.36-147
Hediger, H. (1950). Wild animals in captivity. Butterworths Scientific Publications.
Hediger, H. (1955). Studies of the psychology and behavior
of captive animals in zoos and circuses. Butterworths
Scientific Publications.
Herrnstein, R. J. (1977). The evolution of behaviorism.
American Psychologist, 32(8), 593–603. https://doi.
org/10.1037/0003-066X.32.8.593
Hollis, K. L., Pharr, V. L., Dumas, M. J.,
Britton, G. B., & Field, J. (1997). Classical conditioning provides paternity advantage for territorial
male blue gouramis (Trichogaster trichopterus). Journal
of Comparative Psychology, 111(3), 219–225. https://
doi.org/10.1037/0735-7036.111.3.219
Hopper, L. M., Egelkamp, C. L., Fidino, M., &
Ross, S. R. (2019). An assessment of touchscreens for
testing primate food preferences and valuations.
Behavior Research Methods, 51(2), 639–650. https://
doi.org/10.3758/s13428-018-1065-0
Hosey, G. R. (2000). Zoo animals and their human audiences: What is the visitor effect? Animal Welfare,
9(4), 343–357.
Hosey, G., Birke, L., Shaw, W. S., & Melfi, V. (2018).
Measuring the strength of human–animal bonds in
zoos. Anthrozoös, 31(3), 273–281. https://doi.org/10.
1080/08927936.2018.1455448
*Huskisson, S. M., Egelkamp, C. L., Jacobson, S. L.,
Ross, S. R., & Hopper, L. M. (2021). Primates’ food
preferences predict their food choices even under
uncertain conditions. Animal Behavior and Cognition,
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
8(1), 69–96. https://doi.org/10.26451/abc.08.01.06.
2021
*Huskisson, S. M., Jacobson, S. L., Egelkamp, C. L.,
Ross, S. R., & Hopper, L. M. (2020). Using a
touchscreen paradigm to evaluate food preferences
and response to novel photographic stimuli of food
in three primate species (Gorilla gorilla gorilla, Pan
troglodytes, and Macaca fuscata). International Journal
of Primatology, 41(1), 5–23. https://doi.org/10.1007/
s10764-020-00131-0
Hutchins, M. (2006). Variation in nature: Its implications
for zoo elephant management. Zoo Biology, 25(3),
161–171. https://doi.org/10.1002/zoo.20087
Hutchins, M., Hancocks, D., & Crockett, C. (1984).
Naturalistic solutions to the behavioral problems of
captive animals. Der Zoologische Garten, 54, 28–42.
Inglis, I. R., Forkman, B., & Lazarus, J. (1997). Free food
or earned food? A review and fuzzy model of contrafreeloading. Animal Behaviour, 53(6), 1171–1191.
https://doi.org/10.1006/anbe.1996.0320
Iwata, B. A., Dorsey, M. F., Slifer, K. J.,
Bauman, K. E., & Richman, G. S. (1994). Toward a
functional analysis of self-injury. Journal of Applied
Behavior Analysis, 27(2), 197–209. (Reprinted from
Analysis and Intervention in Developmental Disabilities,
2, 3–20, 1982) https://doi.org/10.1901/jaba.1994.
27-197
Jensen, G. D. (1963). Preference for bar pressing over
“freeloading” as a function of number of rewarded
presses. Journal of Experimental Psychology, 65(5),
451. https://doi.org/10.1037/h0049174
Johnston, J. M., & Pennypacker, H. S. (2010). Strategies
and tactics of behavioral research. Routledge.
Kazdin, A. E. (2021). Single-case experimental designs:
Characteristics, changes, and challenges. Journal of the
Experimental Analysis of Behavior, 115(1), 56–85.
https://doi.org/10.1002/jeab.638
Kelleher, R. T., & Gollub, L. R. (1962). A review of positive conditioned reinforcement. Journal of the Experimental Analysis of Behavior, 5(S4), 543–597. https://
doi.org/10.1901/jeab.1962.5-s543
Killeen, P. R. (2019). Timberlake’s theories dissolve
anomalies. Behavioural Processes, 166, 103894.
https://doi.org/10.1016/j.beproc.2019.103894
Kleiman, D. G., Beck, B. B., Dietz, J. M., Dietz, L. A.,
Ballou, J. D., & Coimbra-Filho, A. F. (1986). Conservation program for the golden lion tamarin. In K.
Benirschke (Ed.), Primates: The road to self-sustaining
populations (pp. 959–979). Springer-Verlag.
Kreger, M. D., & Mench, J. A. (1995). Visitor-animal
interactions at the zoo. Anthrozoös, 8(3), 143–158.
https://doi.org/10.2752/089279395787156301
Kyngdon, D. J., Minot, E. O., & Stafford, K. J. (2003).
Behavioural responses of captive common dolphins
Delphinus delphis to a ‘Swim-with-Dolphin’ programme. Applied Animal Behaviour Science, 81(2),
163–170. https://doi.org/10.1016/S0168-1591(02)
00255-1
Lasky, M., Campbell, J., Osborne, J. A., Ivory, E. L.,
Lasky, J., & Kendall, C. J. (2021). Increasing browse
and social complexity can improve zoo elephant welfare. Zoo Biology, 40(1), 9–19. https://doi.org/10.
1002/zoo.21575
Lattal, K. A., & Fernandez, E. J. (2022). Grounding
applied animal behavior practices in the experimental
analysis of behavior. Journal of the Experimental Analysis of Behavior, 118(2), 186–207. https://doi.org/10.
1002/jeab.789
Lauderdale, L., Samuelson, M., & Xitco, M. (2021).
Modern applications of operant conditioning through
the training of a beaching behaviour with bottlenose
dolphins (Tursiops truncatus). Journal of Zoo and
Aquarium Research, 9(2), 81–87. https://doi.org/10.
19227/jzar.v9i2.519
Learmonth, M. J., Chiew, S. J., Godinez, A., &
Fernandez, E. J. (2021). Animal-visitor interactions
and the visitor experience: Visitor behaviors, attitudes, perceptions, and learning in the modern zoo.
Animal Behavior and Cognition, 8, 632–649. https://
doi.org/10.26451/abc.08.04.13.2021
Lee, M. S., Yu, C. T., Martin, T. L., & Martin, G. L.
(2010). On the relation between reinforcer efficacy
and preference. Journal of Applied Behavior Analysis,
43(1), 95–100. https://doi.org/10.1901/jaba.2010.
43-95
Lukas, K. E., Marr, M. J., & Maple, T. L. (1998). Teaching operant conditioning at the zoo. Teaching of Psychology, 25(2), 112–116. https://doi.org/10.1207/
s15328023top2502_7
Maple, T. L. (2007). Toward a science of welfare for animals in the zoo. Journal of Applied Animal Welfare
Science, 10(1), 63–70. https://doi.org/10.1080/
10888700701277659
Maple, T. L. (2008). Empirical zoo: Opportunities and
challenges to a scientific zoo biology. Zoo Biology,
27(6), 431–435. https://doi.org/10.1002/zoo.20214
Maple, T. L. (2016). The rise and fall of animal behavior
labs: The future of comparative psychology. Animal
Behavior and Cognition, 3(3), 131–143. https://doi.
org/10.12966/abc.02.08.2016
Maple, T. (2017). Professor in the zoo: Designing the future
for wildlife in human care. Red Leaf Press.
Maple, T. L. (2021). The practice of management: The
ascent of women as scholars and leaders in the field
of zoo biology. The Psychologist-Manager Journal,
24(2), 97–114. https://doi.org/10.1037/mgr0000114
Maple, T. L., & Perdue, B. M. (2013). Behavior analysis
and training. In T. L. Maple & B. M. Perdue (Eds.),
Zoo animal welfare (pp. 119–137). Springer.
Maple, T. L., & Segura, V. D. (2015). Advancing behavior analysis in zoos and aquariums. The Behavior Analyst, 38(1), 77–91. https://doi.org/10.1007/s40614014-0018-x
Markowitz, H. (1978). Engineering environments for
behavioral opportunities in the zoo. The Behavior
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
22
Analyst, 1(1), 34–47. https://doi.org/10.1007/
BF03392371
Markowitz, H. (1982). Behavioral enrichment in the zoo.
Van Nostrand Reinhold.
Markowitz, H., & LaForse, S. (1987). Artificial prey as
behavioral enrichment devices for felines. Applied
Animal Behaviour Science, 18, 31–43. https://doi.org/
10.1016/0168-1591(87)90252-8
Markowitz, H., Schmidt, M. J., & Moody, A. (1978).
Behavioural engineering and animal health in the
zoo. International Zoo Yearbook, 18(1), 190–194.
https://doi.org/10.1111/j.1748-1090.1978.tb00256.x
Martin, A. L. (2017). The primatologist as a behavioral
engineer. American Journal of Primatology, 79(1),
e22500. https://doi.org/10.1002/ajp.22500
Martin, A. L., Bloomsmith, M. A., Kelley, M. E.,
Marr, M. J., & Maple, T. L. (2011). Functional analysis and treatment of human-directed undesirable
behavior exhibited by a captive chimpanzee (Pan troglodytes). Journal of Applied Behavior Analysis, 44(1),
139–143. https://doi.org/10.1901/jaba.2011.44-139
Martin, A. L., Franklin, A. N., Perlman, J. E., &
Bloomsmith, M. A. (2018). Systematic assessment of
food item preference and reinforcer effectiveness:
Enhancements in training laboratory-housed rhesus
macaques. Behavioural Processes, 157, 445–452.
https://doi.org/10.1016/j.beproc.2018.07.002
McGowan, R. T., Robbins, C. T., Alldredge, J. R., &
Newberry, R. C. (2010). Contrafreeloading in grizzly
bears: Implications for captive foraging enrichment.
Zoo Biology, 29(4), 484–502. https://doi.org/10.
1002/zoo.20282
McPhee, M. E. (2003). Effects of captivity on response to
a novel environment in the Oldfield mouse
(Peromyscus polionotus subgriseus). International Journal of Comparative Psychology, 16(2), 85–94. https://
doi.org/10.46867/C45C7H
Mehrkam, L. R., & Dorey, N. R. (2014). Is preference a
predictor of enrichment efficacy in Galapagos tortoises (Chelonoidis nigra)? Zoo Biology, 33(4), 275–
284. https://doi.org/10.1002/zoo.21151
Mehrkam, L. R., & Dorey, N. R. (2015). Preference
assessments in the zoo: Keeper and staff predictions
of enrichment preferences across species. Zoo Biology,
34(5), 418–430. https://doi.org/10.1002/zoo.21227
Mehrkam, L. R., Perez, B. C., Self, V. N.,
Vollmer, T. R., & Dorey, N. R. (2020). Functional
analysis and operant treatment of food guarding in a
pet dog. Journal of Applied Behavior Analysis, 53(4),
2139–2150. https://doi.org/10.1002/jaba.720
Melfi, V. A., & Ward, S. J. (2020). Welfare implications
of zoo animal training. In V. A. Melfi, N. R.
Dorey, & S. J. Ward (Eds.), Zoo animal learning and
training (pp. 271–288). John Wiley & Sons Ltd.
https://doi.org/10.1002/9781118968543.ch11
Miller, B., Biggins, D., Vargas, A., Hutchins, M.,
Hanebury, L., Godbey, J., Anderson, S.,
Wemmer, C., & Oldemeier, J. (1998). The captive
23
environment and reintroduction: The black-footed
ferret as a case study with comments on other taxa.
In D. J. Shepherdson, J. D. Mellen, & M. Hutchins
(Eds.), Second nature: Environmental enrichment for
captive animals (pp. 97–112). Smithsonian Press.
Morgan, D. R. (1990). Behavioral-response of brushtail
possums, Trichosurus-vulpecula, to baits used in pestcontrol. Australian Wildlife Research, 17(6), 601–613.
https://doi.org/10.1071/WR9900601
Morris, D. (1964). The response of animals to a restricted
environment. Symposia of the Zoological Society of
London, 13, 99–118.
Morris, E. K., Lazo, J. F., & Smith, N. G. (2004).
Whether, when, and why Skinner published on biological participation in behavior. The Behavior Analyst, 27(2), 153–169. https://doi.org/10.1007/
BF03393176
Morris, K. L., & Slocum, S. K. (2019). Functional analysis and treatment of self-injurious feather plucking in
a black vulture (Coragyps atratus). Journal of Applied
Behavior Analysis, 52(4), 918–927. https://doi.org/10.
1002/jaba.639
Mueller, M. M., Piazza, C. C., Patel, M. R.,
Kelley, M. E., & Pruett, A. (2004). Increasing variety
of foods consumed by blending nonpreferred foods
into preferred foods. Journal of Applied Behavior Analysis, 37(2), 159–170. https://doi.org/10.1901/jaba.
2004.37-159
Neuringer, A. J. (1969). Animals respond for food in the
presence of free food. Science, 166(3903), 399–401.
https://doi.org/10.1126/science.166.3903.399
Newberry, R. C. (1995). Environmental enrichment:
Increasing the biological relevance of captive environments. Applied Animal Behaviour Science, 44(2–4),
https://doi.org/10.1016/0168-1591(95)
229–243.
00616-Z
*Ogura, T., & Matsuzawa, T. (2012). Video preference
assessment and behavioral management of singlecaged Japanese macaques (Macaca fuscata) by movie
presentation. Journal of Applied Animal Welfare Science, 15(2), 101–112. https://doi.org/10.1080/
10888705.2012.624887
Owen, M. A., Swaisgood, R. R., Czekala, N. M., &
Lindburg, D. G. (2005). Enclosure choice and wellbeing in giant pandas: Is it all about control? Zoo
Biology, 24(5), 475–481. https://doi.org/10.1002/
zoo.20064
Pace, G. M., Ivancic, M. T., Edwards, G. L.,
Iwata, B. A., & Page, T. J. (1985). Assessment of
stimulus preference and reinforcer value with profoundly retarded individuals. Journal of Applied
Behavior Analysis, 18(3), 249–255. https://doi.org/10.
1901/jaba.1985.18-249
Padrell, M., Amici, F., Cordoba, M. P., Giberga, A.,
Broekman, A., Almagro, S., & Llorente, M. (2021).
Artificial termite-fishing tasks as enrichment for
sanctuary-housed chimpanzees: Behavioral effects and
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
impact on welfare. Animals, 11(10), 2941. https://
doi.org/10.3390/ani11102941
*Passos, L. F., Mello, H. E. S., & Young, R. J. (2014).
Enriching tortoises: Assessing color preference. Journal of Applied Animal Welfare Science, 17(3), 274–
https://doi.org/10.1080/10888705.2014.
281.
917556
Patterson-Kane, E. G., Pittman, M., & Pajor, E. A.
(2008). Operant animal welfare: Productive
approaches and persistent difficulties. Animal Welfare,
17(2), 139–148.
Perdue, B. M., Evans, T. A., Washburn, D. A.,
Rumbaugh, D. M., & Beran, M. J. (2014). Do monkeys choose to choose? Learning & Behavior, 42,
https://doi.org/10.3758/s13420-014164–175.
0135-0
Pfaller-Sadovsky, N., Arnott, G., & Hurtado-Parrado, C.
(2019). Using principles from applied behaviour analysis to address an undesired behaviour: Functional
analysis and treatment of jumping up in companion
dogs. Animals, 9(12), 1091. https://doi.org/10.3390/
ani9121091
Pfaller-Sadovsky, N., Hurtado-Parrado, C., Cardillo, D.,
Medina, L. G., & Friedman, S. G. (2020). What’s in
a click? The efficacy of conditioned reinforcement in
applied animal training: A systematic review and
meta-analysis. Animals, 10(10), 1757. https://doi.org/
10.3390/ani10101757
Phillips, M., Grandin, T., Graffam, W., Irlbeck, N. A., &
Cambre, R. C. (1998). Crate conditioning of bongo
(Tragelaphus eurycerus) for veterinary and husbandry
procedures at the Denver Zoological Gardens. Zoo
Biology, 17(1), 25–32. https://doi.org/10.1002/(SICI)
1098-2361(1998)17:1%3C25::AID-ZOO3%3E3.0.
CO;2-C
Piazza, C. C., Fisher, W. W., Hagopian, L. P.,
Bowman, L. G., & Toole, L. (1996). Using a choice
assessment to predict reinforcer effectiveness. Journal
of Applied Behavior Analysis, 29(1), 1–9. https://doi.
org/10.1901/jaba.1996.29-1
Pierce, W. D., & Cheney, C. D. (2013). Behavior analysis
and learning. Psychology Press.
Price, E. C., Wormell, D., Brayshaw, M., Furrer, S.,
Heer, T., & Steinmetz, H. W. (2012). Managing
free-ranging callitrichids in zoos. International Zoo
Yearbook, 46(1), 123–136. https://doi.org/10.1111/j.
1748-1090.2012.00167.x
Pryor, K. (1984). Don’t shoot the dog:The new art of teaching and training. Bantam Books.
*Remis, M. J. (2002). Food preferences among captive
Western gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). International Journal of Primatology, 23(2), 231–249. https://doi.org/10.1023/A:
1013837426426
Ritzler, C. P., Lukas, K. E., Bernstein-Kurtycz, L. M., &
Koester, D. C. (2021). The effects of choice-based
design and management on the behavior and space
use of zoo-housed amur tigers (Panthera tigris altaica).
Journal of Applied Animal Welfare Science, 6, 1-14.
https://doi.org/10.1080/10888705.2021.1958684
Rose, N. A., & Parsons, E. C. M. (2019). The case against
marine mammals in captivity (5th ed.). Animal Welfare Institute and World Animal Protection.
Rowden, J. (2001). Behavior of captive Bulwer’s wattled
pheasants,
Lophura
bulweri
(Galliformes:
Phasianidae). Zoo Biology, 20(1), 15–25. https://doi.
org/10.1002/zoo.1002
Ruiz-Miranda, C. R., de Morais Jr, M. M., Dietz, L. A.,
Rocha Alexandre, B., Martins, A. F., Ferraz, L. P.,
Mickelberg, J., Hankerson, S. J., & Dietz, J. M.
(2019). Estimating population sizes to evaluate progress in conservation of endangered golden lion tamarins (Leontopithecus rosalia). Plos One, 14(6),
https://doi.org/10.1371/journal.pone.
e0216664.
0216664
Saini, V., Retzlaff, B., Roane, H. S., & Piazza, C. C.
(2021). Identifying and enhancing the effectiveness
of positive reinforcement. In W. W. Fisher, C. C.
Piazza, & H. S. Roane (Eds.) Handbook of applied
behavior analysis (2nd ed., pp. 175–192). Guilford
Publications.
Salmeron, M. C., Payne, S. W., & Hegr, A. B. (2021).
Functional analysis and treatment of feline aggression
in an animal shelter. Behavior Analysis: Research and
Practice, 21(2), 128–139. https://doi.org/10.1037/
bar0000185
Sanders, K., & Fernandez, E. J. (2020). Behavioral implications of enrichment for golden lion tamarins: A
tool for ex situ conservation. Journal of Applied Animal Welfare Science, 25(3), 214–223. https://doi.org/
10.1080/10888705.2020.1809413
Sasson-Yenor, J., & Powell, D. M. (2019). Assessment of
contrafreeloading preferences in giraffe (Giraffa camelopardalis). Zoo Biology, 38(5), 414–423. https://doi.
org/10.1002/zoo.21513
Saudargas, R. A., & Drummer, L. C. (1996). Single subject (small N) research designs and zoo research. Zoo
Biology, 15(2), 173–181. https://doi.org/10.1002/(
SICI)1098-2361(1996)15:2<173::AID-ZOO7>3.0.
CO;2-8
Savastano, G., Hanson, A., & McCann, C. (2003). The
development of an operant conditioning training program for New World primates at the Bronx Zoo.
Journal of Applied Animal Welfare Science, 6(3), 247–
https://doi.org/10.1207/
261.
S15327604JAWS0603_09
Schmid, J., Heistermann, M., Gansloßer, U., &
Hodges, J. K. (2001). Introduction of foreign female
Asian elephants (Elephas maximus) into an existing
group: Behavioural reactions and changes in cortisol
levels. Animal Welfare, 10(4), 357–372.
Schwartz, L. P., Silberberg, A., Casey, A. H.,
Paukner, A., & Suomi, S. J. (2016). Scaling reward
value with demand curves versus preference tests.
Animal Cognition, 19(3), 631–641. https://doi.org/
10.1007/s10071-016-0967-4
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
24
Shepherdson, D. J., Carlstead, K., Mellen, J. D., &
Seidensticker, J. (1993). The influence of food presentation on the behavior of small cats in confined
environments. Zoo Biology, 12(2), 203–216. https://
doi.org/10.1002/zoo.1430120206
Sherwen, S. L., & Hemsworth, P. H. (2019). The visitor
effect on zoo animals: Implications and opportunities
for zoo animal welfare. Animals, 9(6), 366. https://
doi.org/10.3390/ani9060366
Shettleworth, S. J. (1993). Varieties of learning and memory in animals. Journal of Experimental Psychology:
Animal Behavior Processes, 19, 5–14. https://doi.org/
10.1037/0097-7403.19.1.5
Shyne, A. (2006). Meta-analytic review of the effects of
enrichment on stereotypic behavior in zoo mammals.
Zoo Biology, 25(4), 317–337. https://doi.org/10.
1002/zoo.20091
Siciliano-Martina, L., & Martina, J. P. (2018). Stress and
social behaviors of maternally deprived captive giraffes
(Giraffa camelopardalis). Zoo Biology, 37(2), 80–89.
https://doi.org/10.1002/zoo.21405
Skinner, B. F. (1938). The behavior of organisms. Appleton-Century-Crofts.
Skinner, B. F. (1951). How to teach animals. Scientific
American, 185(6), 26–29. https://www.jstor.org/
stable/24950550#metadata_info_tab_contents::
text=StableURL-,https://www.jstor.org/stable/
24950550,-RemoteAccessURL
Skinner, B. F. (1953). Science and human behavior. The
Free Press.
Skinner, B. F. (1957). The experimental analysis of
behavior. American Scientist, 45(4), 343–371. https://
www.jstor.org/stable/27826953
Skinner, B. F. (1966a). The phylogeny and ontogeny of
behavior: Contingencies of reinforcement throw light
on contingencies of survival in the evolution of
behavior. Science, 153(3741), 1205–1213. https://
doi.org/10.1126/science.153.3741.1205
Skinner, B. F. (1966b). What is the experimental analysis
of behavior? Journal of the Experimental Analysis of
Behavior, 9(3), 213–218. https://doi.org/10.1901/
jeab.1966.9-213
Skinner, B. (1984). Selection by consequences. Behavioral
and Brain Sciences, 7(4), 477–481. doi:https://doi.
org/10.1017/S0140525X0002673X
*Slocum, S. K., & Morris, K. L. (2022). Assessing preference in a paired-stimulus arrangement with captive
vultures (Aegypius monachus). Journal of Applied Animal Welfare Science, 25(4), 362–367. https://doi.org/
10.1080/10888705.2020.1857253
Stoinski, T. S., Beck, B. B., Bloomsmith, M. A., &
Maple, T. L. (2003). A behavioral comparison of
captive-born, reintroduced golden lion tamarins and
their wild-born offspring. Behaviour, 140(2), 137–
160. http://www.jstor.org/stable/4536018
Stoinski, T. S., Beck, B. B., Bowman, M., &
Lehnhardt, J. (1997). The gateway zoo program: A
recent initiative in golden lion tamarin zoo
25
introductions. In J. Wallis (Ed.), Primate conservation:
The role of zoological parks (pp. 113–129). American
Society of Primatologists.
Sullivan, M., Lawrence, C., & Blache, D. (2016). Why
did the fish cross the tank? Objectively measuring the
value of enrichment for captive fish. Applied Animal
Behaviour Science, 174, 181–188. https://doi.org/10.
1016/j.applanim.2015.10.011
Swaisgood, R. R., & Shepherdson, D. J. (2005). Scientific
approaches to enrichment and stereotypies in zoo animals: What’s been done and where should we go
next? Zoo Biology, 24(6), 499–518. https://doi.org/
10.1002/zoo.20066
Timberlake, W. (1984). A temporal limit on the effect of
future food on current performance in an analogue of
foraging and welfare. Journal of the Experimental
Analysis of Behavior, 41(2), 117–124. https://doi.org/
10.1901/jeab.1984.41-117
Timberlake, W. (1993). Behavior systems and reinforcement: An integrative approach. Journal of the Experimental Analysis of Behavior, 60(1), 105–128. https://
doi.org/10.1901/jeab.1993.60-105
Timberlake, W. (2004). Is the operant contingency
enough for a science of purposive behavior? Behavior
and Philosophy, 197–229. https://www.jstor.org/
stable/27759478
Timberlake, W., & Lucas, G. A. (1989). Behavior systems
and learning: From misbehavior to general principles
In S. B. Klein & R. R. Mowrer (Eds.), Contemporary
learning theories: Instrumental conditioning theory and
the impact of biological constraints on learning
(pp. 237–275). Lawrence Erlbaum Associates.
Trone, M., Kuczaj, S., & Solangi, M. (2005). Does participation in Dolphin–Human Interaction Programs
affect bottlenose dolphin behaviour? Applied Animal
Behaviour Science, 93(3–4), 363–374. https://doi.org/
10.1016/j.applanim.2005.01.003
Troxell-Smith, S. M., Whelani, C. J., Magle, S. B., &
Brown, S. (2017). Zoo foraging ecology: Development and assessment of a welfare tool for captive animals. Animal Welfare, 26(3), 265–275. https://doi.
org/10.7120/09627286.26.3.265
*Truax, J., & Vonk, J. (2021). Silence is golden: Auditory
preferences in zoo-housed gorillas. Journal of Applied
Animal Welfare Science, 1–16. Advance online publihttps://doi.org/10.1080/10888705.2021.
cation.
1968400
Vasconcellos, A. da S., Adania, C. H., & Ades, C.
(2012). Contrafreeloading in maned wolves: Implications for their management and welfare. Applied Animal Behaviour Science, 140(1-2), 85–91. https://doi.
org/10.1016/j.applanim.2012.04.012
Vaz, P. C. M., Piazza, C. C., Stewart, V., Volkert, V. M.,
Groff, R. A., & Patel, M. R. (2012). Using a chaser
to decrease packing in children with feeding disorders. Journal of Applied Behavior Analysis, 45(1), 97–
105. https://doi.org/10.1901/jaba.2012.45-97
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Applied Behavior Analysis and the Zoo
Eduardo J. Fernandez and Allison L. Martin
Veeder, C. L., Bloomsmith, M. A., McMillan, J. L.,
Perlman, J. E., & Martin, A. L. (2009). Positive reinforcement training to enhance the voluntary movement of group-housed sooty mangabeys (Cercocebus
atys atys). Journal of the American Association for Laboratory Animal Science, 48(2), 192–195.
Vonk, J., Truax, J., & McGuire, M. C. (2022). A food
for all seasons: Stability of food preferences in gorillas
across testing methods and seasons. Animals, 12(6),
685. https://doi.org/10.3390/ani12060685
Wagman, J. D., Lukas, K. E., Dennis, P. M.,
Willis, M. A., Carroscia, J., Gindlesperger, C., &
Schook, M. W. (2018). A work-for-food enrichment
program increases exploration and decreases stereotypies in four species of bears. Zoo Biology, 37(1), 3–
15. https://doi.org/10.1002/zoo.21391
Walker, S. G., & Carr, J. E. (2021). Generality of findings from single-case designs: It’s not all about the
“N.” Behavior Analysis in Practice, 14(4), 991–995.
https://doi.org/10.1007/s40617-020-00547-3
Ward, S. J., & Melfi, V. (2015). Keeper-animal interactions: Differences between the behaviour of zoo animals affect stockmanship. PloS One, 10(10),
https://doi.org/10.1371/journal.pone.
e0140237.
0140237
Wheaton, C. J., Alligood, C., Pearson, M.,
Gleeson, T., & Savage, A. (2013). First report of
alloparental care in the Key Largo woodrat (Neotoma
floridana smalli). Journal of Ethology, 31(3), 331–334.
https://doi.org/10.1007/s10164-013-0378-9
Wickins-Drazilova, D. (2006). Zoo animal welfare. Journal of Agricultural and Environmental Ethics, 19(1),
27–36. https://doi.org/10.1007/s10806-005-4380-2
Williams, B. A. (1994). Conditioned reinforcement:
Experimental and theoretical issues. The Behavior
Analyst, 17(2), 261–285. https://doi.org/10.1007/
BF03392675
Williams, D. R., & Williams, H. (1969). Automaintenance in the pigeon: Sustained pecking despite
contingent non-reinforcement. Journal of the Experimental Analysis of Behavior, 12(4), 511–520. https://
doi.org/10.1901/jeab.1969.12-511
Wilson, M. L., Perdue, B. M., Bloomsmith, M. A., &
Maple, T. L. (2015). Rates of reinforcement and
measures of compliance in free and protected contact
elephant management systems. Zoo Biology, 34(5),
431–437. https://doi.org/10.1002/zoo.21229
Winslow, T., Payne, S. W., & Massoudi, K. A. (2018).
Functional analysis and treatment of problem behavior in 3 animal shelter dogs. Journal of Veterinary
Behavior, 26, 27–37. https://doi.org/10.1016/j.jveb.
2018.04.004
Woods, J. M., Lane, E. K., & Miller, L. J. (2020). Preference assessments as a tool to evaluate environmental
enrichment. Zoo Biology, 39(6), 382–390. https://doi.
org/10.1002/zoo.21566
Yerkes, R. M. (1925). Almost human. Century.
Zhang, Z., Gao, L., & Zhang, X. (2022). Environmental
enrichment increases aquatic animal welfare: A systematic review and meta-analysis. Reviews in Aquaculture, 14(3), 1120-1135. https://doi.org/10.1111/raq.
12641
Received May 18, 2022
Final acceptance November 27, 2022
Associate Editor, Valerie Volkert
19383703, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jaba.969 by Eduardo Fernandez - University of Adelaide Alumni , Wiley Online Library on [23/12/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
26