Long-term Memory of a Complex Foraging Task in

Monitor Lizards (Reptilia: Squamata: Varanidae)

Authors: Cooper, Taylor L., Zabinski, Caroline L., Adams, Emily J.,
Berry, Savannah M., Pardo-Sanchez, Juanita, et al.
Source: Journal of Herpetology, 54(3) : 378-383
Published By: Society for the Study of Amphibians and Reptiles
URL: https://doi.org/10.1670/19-122

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 Journal of Herpetology, Vol. 54, No. 3, 378–383, 2020
Copyright 2020 Society for the Study of Amphibians and Reptiles

Long-term Memory of a Complex Foraging Task in Monitor Lizards (Reptilia: Squamata:

Varanidae)

TAYLOR L. COOPER,1,2 CAROLINE L. ZABINSKI,1,2 EMILY J. ADAMS,1 SAVANNAH M. BERRY,1 JUANITA PARDO-SANCHEZ,1
EMMA M. REINHARDT,1 KATHERINE M. ROBERTS,1 JULIA WATZEK,3 SARAH F. BROSNAN,2,4 ROBERT L. HILL,5 EMILY G. WEIGEL,1
1,5,6
AND JOSEPH R. MENDELSON, III

1
School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
3
Department of Psychology, Language Research Center, Georgia State University, Atlanta, Georgia, USA
4
Department of Philosophy, Neuroscience Institute, Center for Behavioural Neuroscience, Georgia State University, Atlanta, Georgia, USA
5
Zoo Atlanta, Atlanta, Georgia, USA

ABSTRACT.—Procedural memory allows animals to solve previously encountered tasks over weeks, months, or years efficiently.
Although thoroughly documented in vertebrate clades such as mammals and birds, studies of procedural memory in squamate reptiles
are lacking. Filling the gap in knowledge regarding procedural memory in squamates is important to understanding the degree to which
procedural memory is unique to birds and mammals, as it is related to their unique cognitive abilities. We tested for memory of a
problem-solving task in two species of monitor lizard (Varanus spp.) and a beaded lizard (Heloderma sp.) after a 20-mo hiatus in
exposure, representing approximately 25% of their ages at the time of testing. All the monitor lizards had lower initial latencies to solve
the task upon re-exposure posthiatus than they had as naı̈ve individuals during the prehiatus trials and reached minimum latencies in
fewer trials than when previously tested. Our results indicate procedural memory of puzzle-solving behaviors on the time scales of years.
Our results add to an emerging literature suggesting that squamate and other nonavian reptiles share a number of cognitive traits with
birds and mammals, suggesting that such traits are far more widespread across taxa than previously recognized. We also discuss a
framework for studying cognition in squamates that would allow tests of cognition across a great diversity of body forms and ecologies.

Although reptiles have quite elaborate patterns of instinc- al., 1999; Manrod et al., 2008; LaDage et al., 2012, 2017; Cooper
tive behaviour, no one could claim that they are good at et al., 2019). The taxonomic imbalance in the number of studies
adapting to unfamiliar situations, or have much ability to
learn from experience. of mammals and birds versus nonavian reptiles is problematic
—Angus Bellairs (1970:339) because, as brain anatomy underlies brain function (Rodriguez
et al., 2002; Striedter, 2015; Tosches et al., 2018), the knowledge
Cognition is best understood within the context of ecological of homologous regions in the brain among organisms underlies
and evolutionary processes; the evolutionary backdrop shaping our abilities to recognize homologous behaviors (Greene, 1994),
the framework for cognitive abilities in an organism is both or homologous abilities in cognition (e.g., Finn, 2017; Murray et
preceded by, and shaped by, the ecological obstacles an al., 2018). An appropriately comparative approach (Harvey and
organism encounters (Adams-Hunt and Jacobs, 2007). The Pagel, 1991) to evaluate homology or convergence of behaviors
intimate relationship between cognition and ecological and or cognitive abilities among species will require phylogeneti-
evolutionary processes underpins the importance of compara- cally diverse exemplars.
tive studies when evaluating behavioral cognition. Historically, Procedural memory, or the ability to store and retrieve
work in cognition has focused largely on mammals (Wilkinson information on how to perform specific skills, provides
and Huber, 2012). But substantial work on birds has shown advantages to individuals to solve previously encountered
clearly that, despite having a very different brain morphology tasks more efficiently over weeks, months, or even years, and
(Striedter, 2015), they perform comparably with mammals on has not been studied extensively in squamates. Of the few
many tests of cognition. In contrast, fewer studies have included studies of what could be considered long-term memory in
other clades such as the nonavian reptiles (Wilkinson and nonavian reptiles, most have focused on chelonians (Davis and
Huber, 2012; Burghardt, 2013), resulting in an incomplete Burghardt, 2007; Wilkinson et al., 2010; Soldati et al., 2017). In
phylogenetic perspective on the origins and evolution of this study, we tested long-term retention of a problem-solving
cognitive traits in tetrapods. The lack of inclusion of nonavian skill in two species of monitor lizards (Varanus spp.) over a
reptiles in studies of cognition may be, in part, due to a period of 20 mo; we also examined the performance on the same
persistent problem in the relevant literature regarding the task of a species of beaded lizard (Heloderma charlesbogerti) as a
inconsistent use of the taxonomic term ‘‘reptile.’’ Some studies phylogenetic outgroup. Varanids are good candidates for long-
and reviews (e.g., Striedter, 2015) embrace the fact that birds are, term memory given that they live a relatively long time,
in fact, reptiles, whereas others (e.g., Wilkinson and Huber, approximately 10–20 yr (Mendyk, 2015), and maintain large
2012; Roth et al., 2019) discuss results comparing birds to the territories in complex environments, with evidence that they
nonmonophyletic assemblage of nonavian reptiles. In any case, learn about these landscapes (Auffenberg, 1981, 1988, 1994;
there have been relatively few behavioral studies on cognition Sweet, 1999; Pianka et al., 2004; Sweet, 2007). Previous work has
in squamate reptiles, relative to birds and mammals (e.g., Day et also demonstrated learning and problem-solving abilities in the
clade (e.g., Burghardt et al., 2002; Manrod et al., 2008; Gaalema,
2 2011; Mendyk and Horn, 2011; Cooper et al., 2019). Considered
These authors contributed equally to the project and are listed
alphabetically.
together, these characteristics suggest that varanids may be
6
Corresponding Author. E-mail: [email protected] capable of developing long-term memory (sensu Snell-Rood,
DOI: 10.1670/19-122 2013) related to a problem-solving task. We had no precon-

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 MEMORY IN VARANID LIZARDS 379

capped with a rubber lid and the bottom glued onto a heavy
resin platform (10.0 · 10.0 cm) to ensure stability and to prevent
the lizards from moving the device itself. A dead mouse (the
routine food item offered to these lizards) was placed in the
cylinder and could only be accessed by opening the door.
The initial trials of Cooper et al. (2019) were concluded on 28
May 2017 and were followed by the present trials conducted
approximately twice weekly between 30 January and 23
February 2019 between 1100 and 1300 h. Because trials replaced
the subjects’ normal feeding regimen, zoo staff ensured that trial
days and times coincided with the normal daily feeding
schedule of each individual, and the mice offered were
consistent in size with the animals’ normal diet. Eight trials
were conducted with each lizard using the same procedures
FIG. 1. The puzzle-feeder device. Mertens’ Water Monitor (Varanus
mertensi) investigating puzzle feeder device, in situ in its home described by Cooper et al. (2019). A baited device was placed
enclosure. The dashed line marks the vertical plane of the device base. into the lizard’s home enclosure, situated approximately at one
Once crossed, the latency time measures were initiated. body-length distance, with the device’s door oriented towards
the lizard. The animals were not touched or moved. Trials were
ceived notions regarding Heloderma, as the only cognitive work digitally recorded by stationary human observers approximate-
with those lizards of which we are aware was by Cooper et al. ly 2 ft away from the enclosure. The time elapsed between a
(2019). lizard’s initial contact with the device and successfully gaining
Here, we report a study of long-term procedural memory in entry and grasping the food item with its mouth was recorded
two clades of squamate reptiles and discuss the results at as its measure of latency. Initial contact was defined as the
different levels of evolutionary generality. We used the foraging anterior portion of the lizard’s body crossing the vertical plane
task described by Cooper et al. (2019) to test for reconsolidation of the base of the device (Fig. 1); tongue flicks crossing this plane
of a problem-solving task. The subjects had to manipulate a were not considered to represent contact with the device. If a
puzzle device, requiring them to use their claw or snout to open lizard failed to open the device and seize the food within 30
the door of a clear, nonairtight box to access a food reward. We min, the trial was stopped, the device was removed, and the
compared problem-solving latencies in the current study to the food item was offered to the lizard. Video of a successful trial is
same individuals’ latencies in previous work performed 20 mo available (https://youtu.be/ukayoMTScXw), and full raw data
prior (Cooper et al., 2019). Specifically, we sought to determine are posted on Dryad (doi:10.5061/dryad.gm286rk).
if, after the 20-mo hiatus, the subjects would show solving To test the impact of the 20-mo hiatus, we compared
latencies similar to their performance when they were naı̈ve to posthiatus latency data from each individual to previously
the puzzle, or if their latencies would reflect memory retrieval published data from Cooper et al. (2019). Both the pre- and
and be similar to those shown after they had learned how to posthiatus data were scored by TLC. We analyzed both the
solve the puzzle (i.e., after approximately 40 trials, as reported posthiatus data set and the combined pre- and posthiatus data
by Cooper et al., 2019). To the extent that an individual is able to sets using Bayesian multilevel modeling in a repeated-measures
access the relevant procedural memory, the initial solving censored generalized linear model and specified a lognormal
latency posthiatus will be shorter than the novel exposure, distribution for the latencies. The latency data conformed to a
and the minimum latency posthiatus will be met in fewer trials lognormal distribution with a long upper tail, thus requiring the
than in the previous experiment. use of a generalized linear model (Gustavsson et al., 2014).
Bayesian modeling allowed us to include unsuccessful trials
(i.e., trials in which the problem was not solved within 30 min)
MATERIALS AND METHODS
into the data set in the form of censored data (Young and
We studied two Emerald Tree Monitors (Varanus prasinus; 1 = Crumer, 2018; see also Cooper et al., 2019). The censored data
13R077, adult female, age = 79 mo; 2 = 13R076, adult female, points in our analyses were modeled as if each latency was at
age = 67 mo), two Mertens’ Water Monitors (Varanus mertensi; 1 least 30 min, even though the actual time is unknowable. For
= 11R071 and 2 = 11R072, adults, sex undetermined, age = 91 each lizard, we estimated its initial solving latency (intercept)
mo), and one Guatemalan Beaded Lizard (Heloderma charlesbo- and the decrease in latency as trials progressed (slope).
gerti; 13R027, subadult, sex undetermined, age = 67 mo). All Statistical analyses were conducted using R software (R Core
individuals were maintained in off-exhibit enclosures at Zoo Team, 2019); the code used is available (https://www.
Atlanta, Georgia, USA, and all trials occurred in the lizards’ copeiajournal.org/ch-18-119).
home enclosures; that is, animals were not relocated to test
arenas for the trials. All procedures were approved by The
Scientific Research Committee of Zoo Atlanta. RESULTS
Individuals were exposed to a similar puzzle device as that All four varanid lizards solved the puzzle device in almost all
used by Cooper et al. (2019). The device (Fig. 1) was a clear of the eight trials; V. mertensi–2 had one unsuccessful attempt
acrylic cylinder approximately 18.0 cm tall and 11.4 cm in (Trial 1) and V. prasinus–1 did not initiate an attempt in one trial
diameter. A side-hinged (zip-tie hinges) door was cut into one (Trial 5). Latencies observed were comparable to latencies
lower side of the cylinder; the doors were flush-fitting with a recorded in the final trials of the previous data set concluded
notch cut into the lower nonhinged corner to allow the lizards to nearly 2 yr prior (Cooper et al., 2019; Fig. 2). The individual
insert a claw or snout to open the door. Thirteen equally spaced Heloderma charlesbogerti retested in this study did not success-
holes were drilled through the sides of the tube. The top was fully complete any trials, a result also consistent with the

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 380 T. L. COOPER ET AL.

FIG. 2. Latency to solve the foraging puzzle for each lizard. Each plot displays the individual’s combined latency results from both the previous
(Cooper et al. 2019) and present experiment with dotted vertical lines marking the 20-mo hiatus. Solid circles = solved trials, open circles = censored
data where the individual did not solve the foraging puzzle within the 30-min trial period, and the solid lines = the Bayesian model fit with 95%
credible intervals (shaded regions). The y intercepts estimate the initial latencies of each lizard’s naı̈ve attempt to solve the puzzle in 2017, and the
slope is the decrease in latency as trials progressed. The model fit for H. charlesbogerti is not shown because it is outside the plotted area.

previous data. For each varanid lizard, the combined data set varanid lizards, but not for the beaded lizard. For all lizards,
from both the original and posthiatus trials were well described the most likely slope value was negative, although there were
by the Bayesian model (Fig. 2). The analysis revealed that there varying degrees of uncertainty in the slope estimates. Overall,
was strong evidence of learning (negative slopes) for the the estimated slope was -0.10 with a 95% credible interval of

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 MEMORY IN VARANID LIZARDS 381

TABLE 1. Lognormal transformed regression equations for each lizard (Varanus, Heloderma) from both the previous and current experiment. A
Bayesian approach for multilevel modeling over repeated measures with censoring was used to calculate the regression equations from this
experiment.

Year Lizard Intercept 95% credible interval Slope 95% credible interval

2017 All lizards combined 6.74 [4.84, 8.84] 0.061 [-0.130, -0.002]
V. prasinus–1 7.14 [6.45, 7.89] 0.080 [-0.106, -0.055]
V. prasinus–2 5.12 [4.08, 6.07] 0.028 [-0.091, 0.047]
V. mertensi–1 6.66 [5.96, 7.39] 0.063 [-0.089, -0.038]
V. mertensi–2 6.41 [5.20, 7.80] 0.074 [-0.191, 0.023]
H. charlesbogerti 9.51 [7.89, 11.78] 0.069 [-0.178, 0.015]
2019 All lizards combined 6.30 [4.76, 8.14] -0.10 [-0.32, 0.20]
V. prasinus–1 5.31 [4.07, 6.50] -0.20 [-0.44, 0.036]
V. prasinus–2 5.17 [3.86, 6.40] -0.11 [-0.34, 0.15]
V. mertensi–1 4.84 [3.60, 6.10] -0.24 [-0.50, -0.0091]
V. mertensi–2 6.22 [4.98, 7.63] -0.26 [-0.54, -0.033]
H. charlesbogerti 9.53 [5.58, 15.15] 0.28 [-0.40, 2.00]

-0.32 to 0.20; the intercept was 6.30 (Table 1). Excluding the As these results make clear, a broader exploration of cognition
beaded lizard that failed to engage with the device in the in varanid lizards and other squamates will expand our
posthiatus trials produced essentially the same results, with an understanding of the evolution of behavioral plasticity and
estimated slope of -0.14 with a 95% credible interval of -0.32 to cognition within the megadiverse squamate clade that has been
0.10; the intercept was 5.51. largely neglected in cognitive studies (Wilkinson and Huber,
2012; Burghardt, 2013). Part of the reason for this dearth of
studies is undoubtedly practical; most cognitive studies require
DISCUSSION
controlled experiments, which typically require captive condi-
After learning a task, the memory of a learned behavior may tions. Many of these species are rarely maintained in captivity or
be consolidated into long-term memory, but over time becomes are, as in our case, available in small sample sizes. However, as
susceptible to destruction (Sweatt, 2010; Sandrini et al., 2015). work in other species in captivity (e.g., primates, cetaceans,
Our study demonstrates that the memory to solve a foraging elephants) has shown, small sample sizes can be informative
puzzle device remained intact in the included varanid lizards simply to help us to understand the extent of a species’ abilities
after a 20-mo hiatus in exposures. In long-term memory, upon (Matsuzawa, 1985a,b; Reiss and Marino, 2001; Plotnik et al.,
re-exposure, an individual can retrieve the consolidated 2006).
memory and re-establish the learned behavior (Finn, 2017). The results of Cooper et al. (2019) and the present study
Our results suggest that procedural memory was evident in the document procedural memory at two different time scales in
varanid lizards, as their initial re-exposure latencies were lower monitor lizards. In consideration of the small body of cognitive
than their original naı̈ve latencies and showed continued decline work that has been done with these lizards, we posit that the
toward a minimum latency in fewer trials than before the hiatus varanid clade can represent model organisms around which to
(Fig. 2). develop a research program on comparative cognition. For
The time frame of our study represents 22–30% of the lives of example, the group would seem ideal to study the extents of
these individual lizards at the time of the study; we consider other forms of memory (e.g., working memory or episodic
this to indicate long-term memory. For comparison, Atlantic memory). The sheer diversity of Squamata is at once both the
Bottlenose Dolphins (Tursiops truncatus) have exhibited social source of interesting comparative questions and a formidable
recognition of individual whistle communications for at least 20 diversity of challenges, but all contained in a conceptually clear
yr, encompassing approximately at least 75% and possibly an monophyletic framework. With body forms as distinct as snakes
entire lifetime (Bruck, 2013; Jaakkola and Willis, 2019). Garden or chameleons, and with sensory abilities distributed along
Warblers (Sylvia borin) returned to the ‘‘correct’’ experimental continua that include organisms who are blind (e.g., amphis-
room, which contained a food source during initial exposure, baenians), possess infrared vision (e.g., pitvipers), are heavily
after up to 1 yr after testing (Mettke-Hoffmann and Gwinner, olfactorily-oriented (e.g., beaded lizards), or are heavily reliant
2003), or about 15% of their life span (Payevsky and Shapoval, on both scent and vision (e.g., monitor lizards), one can study
2000). the evolution of behavior, cognition, and sensory modalities in a
The failure by the phylogenetic outgroup species, H. monophyletic group with widely diverse ecological, behavioral,
charlesbogerti, to learn to solve the device in both pre- and and anatomical realities. By comparison, all birds are predom-
posthiatus trials supports the suggestions by Burghardt (2013) inantly visually oriented, active foragers. All mammals are
and others that monitor lizards may have derived improved active foragers, with important differences in sensory modali-
cognitive abilities relative to other squamates. Based on reviews ties.
of studies that addressed varanid cognition and learning across As an example, our work did not necessarily demonstrate
different species and methods, Burghardt (2013) opined that lack of procedural memory in our outgroup, Heloderma, but may
‘‘these animals seem to be in a different psychological place than suggest that the different ecologies and sensory modalities of
other lizards’’ (p. 292). However, we do not suggest that our helodermatids need to be better considered in order to assess
results indicate absence of the ability to form procedural their memory and cognition. Roth et al. (2019) emphasized the
memories in beaded lizards, as this is a single task and other challenge of finding ecologically relevant means of measuring
experimental approaches may well find such abilities in these and comparing cognition across diverse animals, as well as
lizards. caution in the interpretation of negative results. Roth et al.

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 382 T. L. COOPER ET AL.

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