NEWS AND PERSPECTIVES

Are shy individuals less behaviorally variable? Insightsfrom a captive population of mouse lemurs

Jennifer L. Verdolin • John Harper

Received: 20 December 2012 / Accepted: 10 May 2013

� Japan Monkey Centre and Springer Japan 2013

Abstract Increasingly, individual variation in personality

has become a focus of behavioral research in animal sys-

tems. Boldness and shyness, often quantified as the ten-

dency to explore novel situations, are seen as personality

traits important to the fitness landscape of individuals. Here

we tested for individual differences within and across

contexts in behavioral responses of captive mouse lemurs

(Microcebus murinus) to novel objects, novel foods, and

handling. We report consistent differences in behavioral

responses for objects and handling. We also found that the

responses to handling and novel objects were correlated

and repeatable. Lastly, we show that shyer individuals may

show less variability in their behavioral responses. This

study provides new information on the potential for

behavioral syndromes in this species and highlights

differences in the degree to which behavioral types (e.g.,

shy/bold) vary in their behavioral responses.

Keywords Boldness � Novel object � Personality �Behavioral repeatability � Temperament

Introduction

Individual variation is the ‘grist’ of natural selection and

has implications for social dynamics, population structure,

and disease transmission (Drea and Wallen 1999; Reale

et al. 2000; Dingemanse and Reale 2005; Wilson 2007;

Hamede et al. 2009; Pinter-Wollman 2012). Despite this,

behavioral ecologists have traditionally considered indi-

vidual variation along a behavioral axis as statistical

noise. Recently, however, empirical evidence from a

broad range of taxa, including invertebrates and verte-

brates, has revealed that individuals may show consistent

differences that are correlated across different contexts

(Gosling 2001; Sih et al. 2004a, b; Bell 2005; Quinn and

Cresswell 2005; Powell and Gartner 2011), often referred

to as behavioral syndromes or personality (Gosling and

John 1999; Gosling 2001; Sih et al. 2004a, b; Wilson and

Godin 2009). As a consequence of fitness differences,

selection can and will sustain individual variation in a

population (Wilson 1998; Sih et al. 2004a), resulting in

polymorphic populations differing in life history traits

(Biro and Stamps 2008). Alternatively, differing life his-

tory strategies can produce variation in risk-taking

behavior among individuals within a population, thereby

promoting the evolution of personality (Wolf et al. 2007;

Dammhahn 2012).

Generally, individuals that approach novel objects and

food sooner, reflecting a willingness to explore, are con-

sidered bolder relative to others (Wilson et al. 1994; Bell

and Stamps 2004; Sih et al. 2004a, b). Although aggression

has also been correlated with boldness in a variety of

species (Wilson et al. 1994; Bell and Stamps 2004; Sih

et al. 2004a, b; Moretz et al. 2007; Pintor et al. 2008), it is

typically measured as conspecific aggression (but see Reale

et al. 2000). In contrast, the relationship between

J. L. Verdolin and J. Harper are co-first authors.

J. L. Verdolin (&)

National Evolutionary Synthesis Center (NESCent),

2024 W. Main Street, Durham, NC 27705, USA

e-mail: verdolin@nescent.org

J. Harper

Department of Biological Sciences, North Carolina State

University, Raleigh, NC 27695, USA

J. Harper

Department of Biological Sciences, University of Leeds,

Leeds LS2 9JT, UK

123

Primates

DOI 10.1007/s10329-013-0360-8

aggression and boldness, in the context of animal handling

by humans, may be more variable depending on the spe-

cies. For example, response to human handling may indi-

cate a fear response rather than conspecific aggression,

while a lack of response may indicate greater risk-taking,

or boldness (e.g., Moeller and Garamszegi 2012). There-

fore, responses to handling, or approach by humans,

reflects one important potential measure contributing to

behavioral syndromes (Reale et al. 2000; Moeller and

Nielson 2010; Moeller and Garamszegi 2012).

We investigated personality and variability in a captive

population of gray mouse lemurs (Microcebus murinus).

Gray mouse lemurs are small, arboreal, nocturnal pri-

mates found in the western and southwestern regions of

Madagascar (Martin 1972; Mittermeier et al. 1994;

Radespiel 2000). Strepsirrhine primates, such as the gray

mouse lemur, represent a primitive group and evidence of

behavioral syndromes in this group may suggest con-

vergence on this trait with other basal primate groups.

Recent experimental tests of wild populations demon-

strate consistent interindividual differences that were

correlated across exploratory behavior, foraging behavior,

and across differing fitness potentials (Dammhahn 2012;

Dammhahn and Almeling 2012). Here, we explored

whether captive gray mouse lemurs showed individual

variation in behavioral responses towards novel objects,

novel foods, and human handling. We then determined if

behavioral syndromes were present by assessing whether

responses were correlated across these contexts. First, we

predicted that we would detect individual variability.

Second, if behavioral syndromes exist in this species

using the behavioral axes we quantified, we predicted that

responses would be consistent within individuals across

contexts. Last, we predicted that there would be a dif-

ference in the degree of variation exhibited by bold and

shy individuals.

Methods

This study was conducted on a population of gray mouse

lemurs housed at the Duke Lemur Center (DLC) in

Durham, NC. A total of 14 individuals were sampled,

ranging in age from 1 to 8 years old. Age classes were

assigned as follows: Class 1 ([1 and \3 years;nmales = 4, nfemales = 4), Class 2 ([3 and \7 years;nmales = 1, nfemales = 1), Class 3 ([7 years;nmales = 2, nfemales = 2). All object and food trials

were recorded using a Digital8 video camera (Sony DCR-

TRV280) and lemur behavioral responses to trials were

quantified from the tapes by JLV. A data table containing

information on individuals and responses is available in

Dryad, http://dx.doi.org/10.5061/dryad.5m083.

Behavioral experiments

Novel object assessment

Individual were tested for their willingness to explore a novel

object. Each individual was tested alone in his or her own

enclosure. Individuals were tested for their responses to both

control and novel objects. Control objects were chosen from

items the DLC staff uses for enrichment, thus representing

objects individuals were familiar with (e.g. tissue box, yogurt

container, toilet paper roll). Novel objects were chosen that

contained a shape, color, or texture feature the animals were

unfamiliar with. Items used included a miniature wooden

chair, a wooden heart, a wooden ladybug, plastic keys, an egg

carton, an orange ball, or a stuffed toy frog. All novel objects

were confirmed as novel by DLC staff (Dr. Sarah Zehr,

personal communication) and approved for use by a DLC

veterinarian to ensure animal safety. Each trial consisted of

four parts as follows: (1) a 5-min observation period with the

observer in the room, (2) presentation of either a control

object or novel object in the center of the enclosure, (3) a

5-min observation period, and (4) the presentation of either a

control or novel object in the center of the enclosure. Control

and novel objects were selected prior to the start of each trial

using a random number generator and were presented in

random order by flipping a coin. Each mouse lemur was

given 5 min to explore the object. The individual measures

of boldness we quantified were (a) latency to approach the

object, (b) how many times the object was approached,

(c) how many times it was touched, (d) how many times the

object was handled, and (e) the total time spent near or

handling the object. ‘Approached’ was defined as being close

enough to the object to touch it. After 5 min, the object was

removed and following a 5-min observation period, the

second object was placed in the enclosure for 5 min. Mouse

lemurs that did not approach an object, whether control or

novel, during the 5-min experimental period were assigned a

score of 5 min. A second trial was repeated 1 week later.

Novel food assessment

At least 1 week after both novel item trials were com-

pleted, the mouse lemurs were tested in their enclosures for

their inclination to consume a control and novel food item.

Following the same procedure detailed above, individuals

were presented with a control or novel food item for 5 min.

Food was presented in a stainless steel food dish prior to

the mouse lemurs receiving their afternoon meal. Control

food items were apples or bananas and the novel foods,

after being deemed safe by the DLC veterinarian, were

mango and papaya. The novel fruits were chosen based on

recommendations from DLC staff as having a high prob-

ability of being perceived as novel (Dr. Sarah Zehr,

Primates

123

personal communication). The individual measure of

boldness we quantified was the latency to grab and con-

sume the food item. All individuals that grabbed the food

consumed it. If the food was not touched during the

experiment, individuals were given scores of 5 min. A

second trial was repeated 1 week later.

Response to handling

DLC staff regularly caught and handled most individual

mouse lemurs in this study on a weekly basis for the pur-

poses of cleaning enclosures, routine weighing, or taking

breeding season measurements. An agitation score was

given to each mouse lemur based on behavior during

handling. DLC staff recorded the behaviors of individuals

on a check sheet with defined categories, provided by JLV.

We attributed 0 points if the mouse lemur was willingly

handled, 1 point if he/she vocalized, 1 point for urination, 1

point for defecation, 2 points for struggling, and 3 points

for biting. Therefore, we used an agitation index where an

individual could score a minimum of 0 (no agitation) and a

maximum of 8 (high agitation). Between 1 and 18 inde-

pendently collected scores were obtained for each indi-

vidual ( �X ± SE = 9.43 ± 1.69; N = 14). Because some

individuals were handled more frequently and males may

have been handled more than females for the collection of

breeding season measurements, we tested for any bias due

to sex, age-class, and the number of times that an indi-

vidual was handled. There was no relationship an indi-

vidual’s agitation index and sampling effort, sex, age class,

or sex-age class interaction (F4,9 = 1.21, P = 0.37).

Statistical analyses

We performed principal component analysis (PCA) on the

novel object behavioral measures to see if we could reduce

these variables and we also determined whether there were

any correlations among the variables (Table 1). Next, we

compared individual behavioral responses across experi-

ments and agitation indices to assess individual consistency

across the different measures. Across-context correlations

were calculated using the nonparametric Spearman’s rank

correlation test. Only individuals for whom data were

available were used in each comparison. One individual died

and one individual could not be tested due to logistical issues

prior to completion of the object and food trials, and one

individual was only handled once and was excluded from

tests involving handling (see Dryad, http://dx.doi.org/10.50

61/dryad.5m083).

We were also interested in quantifying behavioral

repeatability (r) in the mouse lemurs. To do so, we cal-

culated repeatability scores to determine how consistent

individuals were within each behavioral measure by fol-

lowing the protocol described in Lessells and Boag (1987),

where (r) represents the within-class correlation coeffi-

cient. Where necessary, data were normalized by log

transformation. We corrected for unequal sample sizes

when calculating the repeatability of handling by using the

weighted average number of observations (Gelman and

Hill 2007). We determined significance of repeatability by

calculating the 95 % confidence intervals (CIs) for each

measure as outlined in Nakagawa and Schielzeth (2010),

where significance was based on whether the 95 % CIs

overlapped 0. Lastly, because individuals were handled

multiple times and agitation indices were normally dis-

tributed, we used generalized linear models (GLM) to

determine whether individuals with higher agitation scores

showed less variation in their behavioral response using the

coefficient of variation (CV) as the dependent variable.

Sample sizes were relatively small and although multiple

tests were performed, we did not make Bonferroni cor-

rections due to the inherent low statistical power (see

Nakagawa 2004).

Results

Following PCA, in the novel object test only the first

component had an eigenvalue greater than 1, which

explained 63 % of the total variance (Table 1). Given the

strong correlation among the measures and the similar

results whether we used only the latency to approach or

PC1, we decided to use only the latency to approach in

further analyses. As expected, the small population of

captive mouse lemurs showed variation in mean (±SE)

agitation index per individual, suggesting behavioral

response differences among individuals (see Dryad,

http://dx.doi.org/10.5061/dryad.5m083). The Spearman’s

rank correlation between agitation index and the latency to

Table 1 Correlation matrix of novel object variables measured

where V1 latency to approach the object, V2 number of times the

object was approached, V3 number of times the object was touched,

V4 number of times the object was handled, and V5 total time spent

near or handling the object

Novel object

variables

V1 V2 V3 V4 V5 PC1 Eigen

value

V1 1.0 – – – 0.63 3.08

V2 -0.79 1.0 – –

V3 -0.49 0.69 1.0 –

V4 -0.36 0.17 -0.19 1.0 –

V5 -0.54 0.90 0.70 -0.21 1.0

PC1 reflects the only PCA loading for novel objects that had an

eigenvalue greater than 1

Primates

123

approach a novel object was positively correlated

(rs = 0.63, P = 0.03; Fig. 1). A similar result was found

when examining the relationship between agitation index

and the latency to approach a control object (rs = 0.74,

P = 0.0006), suggesting that individuals showing greater

agitation during handling took longer to explore any object

placed in a novel location in their enclosure. However,

neither agitation index nor latency to approach a novel

object was significantly correlated with the latency to

consume a novel food (handling score: rs = 0.13,

P = 0.71; object: rs = 0.36, P \ 0.29). Agitation index

was also not significantly correlated with the latency to

consume a control food (rs = 0.06, P = 0.85). In addition,

the latency to approach a novel object was not significantly

correlated with the latency to consume a control food

(rs = 0.27, P = 0.43), nor was the latency to approach a

control object and consume a novel food (rs = 0.47,

P = 0.15).

We measured repeatability for agitation index, latency

to approach the novel object, and latency to consume the

novel food. Of these three behavioral traits, both the agi-

tation index (r = 0.73, 95 % CI 0.57–0.89) and latency to

approach the novel object (r = 0.36, 95 % CI 0.20–0.52)

were repeatable, but the latency to consume the novel food

was not significantly repeatable (r = 0.22, 95 % CI -0.10

to 0.54). Lastly, higher agitation index was negatively

correlated with the coefficient of variation in agitation

index (r2 = 0.77, F1,11 = 37.85, P = 0.001), suggesting

these individuals showed less variation in their response

(Fig. 2).

Discussion

We tested the hypotheses that individuals varied in their

responses to behavioral tests, that individuals were con-

sistent in their responses, and that there were correlations

among responses to the different tests. Results reveal

considerable and repeatable between-individual variation

in two of the three behavioral tests we administered.

Individuals showed consistent differences in their response

to handling and exploratory behavior (control and novel

object). Although individuals with higher agitation scores

also were less exploratory, these patterns were not con-

sistent with the novel food item test. The relationship

between handling and investigation of objects was signif-

icant, regardless of whether the object was novel or

familiar. This suggests that the novelty of placement in the

enclosure may be the stimulus individuals were responding

to. Regardless of whether a control object is used or not,

one cannot decouple the object from novel placement.

Therefore, we suggest that individuals varied in their

willingness to explore objects placed in novel locations in

their enclosures. This variation was correlated with han-

dling such that individuals with a decreased latency to

explore objects were also less agitated when being handled.

These findings are consistent with what has been charac-

terized as boldness in other species (Wilson and Godin

2009). Although a general relationship has been reported

between conspecific aggression and boldness, our results

suggest that agitation during human handling may reflect

shyness, or anxiety as suggested by Carter et al. (2012).

This is in contrast to results reported by Reale et al. (2000),

where aggression in response to human handling was

correlated with measures of boldness in bighorn ewes, Ovis

Canadensis. This difference may reveal important species

variability in behavioral responses that should be

considered.

Despite the lack of correlation between the novel food

test and the other measures, we do not characterize this as a

lack of behavioral syndromes per se in mouse lemurs.

Rather, there are two possibilities. First, perhaps the food

items chosen as novel may not necessarily have been

Mean agitation index

0

75

150

225

300

0 1 2 3 4 5 6 7 8

Mea

n la

tenc

y to

app

roac

h (s

ec)

Fig. 1 Relationship between response to handling and the latency to

approach a novel object for mouse lemurs. The relationship was tested

using the nonparametric Spearman’s correlation: rs = 0.63,

P = 0.03, N = 12

0

0.5

1

1.5

2

0 2 4 6 8

CV

Agitation index

Fig. 2 Relationship between response to handling (agitation index)

and the log coefficient of variation of the agitation index (GLM:

r2 = 0.77, F1,11 = 37.85, P = 0.001)

Primates

123

perceived as such by individuals. While individuals were

not fed those particular fruits prior to these experiments, it

is possible that there was some feature familiar to the

mouse lemurs (e.g., smell, consistency, presentation in

familiar food dish). Second, recent studies of wild baboons,

Papio ursinus, revealed a lack of correlation among novel

food and an individual’s threat response (Carter et al.

2012). Such findings have also been reported for other

species (e.g., pumpkinseed sunfish, Lipomis gibbosus;

Coleman and Wilson 1998).

This study also addresses two key areas of current ani-

mal personality research: repeatability and flexibility. In

addition to the correlation between handling and novel

object, we found significant repeatability within individuals

across those two contexts. This strengthens the evidence

for behavioral correlations in mouse lemurs reported

for wild populations (Dammhahn 2012; Dammhahn and

Almeling 2012). The lack of repeatability in the novel food

test is also consistent with its lack of relationship with the

other two experiments and supports our suspicion that we

were unable to account for how the animals may have

actually perceived the food items or that novel foods

generally do not provide a good assay for personality tests

(see Carter et al. 2012).

In addition, the finding that individuals who were more

agitated in response to handling exhibited less variation in

that response may have implications for how flexible dif-

ferent personality types are in their behavioral responses. If

we assume that greater agitation and a lower willingness to

explore a novel object reflects a shy personality, then it is

possible that, in mouse lemurs, shyer individuals are also

less variable in their behavioral responses. This can have

important ecological and evolutionary consequences. For

example, shyer individuals may be less able to decouple

behavioral traits across contexts, constraining their ability

to adapt to uncertain or changing environmental conditions

(Dall et al. 2004; Sih et al. 2004a; Wilson and Godin 2009).

Alternatively, it has been suggested that bold individuals

exhibit less variation in behavioral traits across a bold-shy

axis (decreased behavioral plasticity) in comparison to

shyer individuals (Dochtermann and Jenkins 2007). Such

decreased variation has been observed in behaviors such as

neophobia and the likelihood of forming routines (Sih et al.

2004a; Dochtermann and Jenkins 2007). However, consis-

tent with other species, here the opposite pattern was

observed, with bolder individuals showing greater variation

or flexibility in behavioral responses than shyer individuals

(Rodriguez-Prieto et al. 2011; Dingemanse et al. 2012). This

suggests important species-specific differences that warrant

further study. As behavioral syndrome studies are emerging

as a vital part of behavioral ecology, results of such studies

have important implications for animal welfare and conser-

vation practices. A better understanding of individual

variation in behavior can be used to improve conditions for

captive animals and potentially improve the success of ani-

mal reintroduction back into the wild (Bremner-Harrison

et al. 2004; Powell and Svoke 2008; Powell 2010; Powell and

Gartner 2011). However, the effect of behavioral syndromes

and plasticity for different behavioral types, which have

implications for how well individuals cope with changing

conditions, remain unclear.

Acknowledgments Our study was approved by the institutional

Animal Care Committee at Duke University (A-227-09-08) and

adheres to the guidelines of the American Society of Primatologists’

Principles for the Ethical Treatment of Non-Human Primates. We

thank the DLC staff for their assistance with handling data collection

and other logistical support. We thank Dr. Sarah Zehr and two

anonymous reviewers for comments that greatly improved this

manuscript.

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