the relationships between behavioural categories and social

RESEARCH PAPER

The Relationships between Behavioural Categories and SocialInfluences in the Gregarious Big Brown Bat (Eptesicus fuscus)R. Julia Kilgour & R. Mark Brigham

Department of Biology, University of Regina, Regina, SK, Canada

Correspondence

R. Julia Kilgour, Conservation and Science,

Lincoln Park Zoo, 2001 North Clark Street,

Chicago, IL 60614, USA.

E-mail: [email protected]

Received: October 22, 2012

Initial acceptance: November 14, 2012

Final acceptance: December 4, 2012

(L. Ebensperger)

doi: 10.1111/eth.12052

Abstract

Behavioural plasticity is a critical component of natural selection leading

to evolution. However, a surge of studies in the last two decades has dis-

covered a distinct limit to behavioural plasticity, commonly referred to as

behaviour types and behavioural syndromes. We set out to understand

the relationships across behavioural categories in wild-caught adult,

female big brown bats and how they compare between social and solitary

behaviours. Using bats sampled from four different maternity colonies, we

ran a series of behavioural assays to create a behavioural profile for each

individual. The behavioural profile encompassed exploratory, learning,

competitive and aggressive categories. We found that Big brown bats exhi-

bit a mean profile relatively unique to other well-documented species,

where aggression was linked to increased competitive ability but not to

boldness. Our results indicate that the solitary and socially directed behav-

iours of individuals are not necessarily related and that behaviours per-

taining to social interactions are linked most closely to learning abilities.

Furthermore, we found evidence that poor body condition may be a pre-

dictor of increased social interactions and that behaviours exhibited in the

presence of conspecifics are unrelated to those exhibited in solitude. These

findings indicate importance of social affiliations on individual behaviours

in this species and their uniqueness relative to other well-studied taxa.

Introduction

Plasticity and phenotypic variation in inherited traits

are the driving forces behind evolutionary change in

ecological traits. Behavioural plasticity allows organ-

isms to adapt to the surrounding environment, and

variation in behavioural traits is thus considered

adaptive given the heterogeneity of habitats (Via et al.

1995; Dingemanse et al. 2004). However, our current

understanding of individual differences implies that

animals actually exhibit a limited range of behaviour-

al variation across changing environmental contexts

(Wilson 1998; Sih et al. 2004a,b). For example,

numerous studies have reported consistency in indi-

vidual aggressive behaviour (a behavioural type)

between contexts (Huntingford 1976; Riechert &

Hedrick 1993; McGhee & Travis 2010); but see

(Coleman & Wilson 1998). Concepts such as the

aggressive spillover hypothesis suggest that juvenile

voracity and adult aggression are contextually adap-

tive but are also linked to pre-copulatory sexual can-

nibalism in female fishing spiders (Dolomedes triton)

(Johnson & Sih 2005). The intensity of the behaviour

displayed may differ among individuals, where some

individuals consistently exhibit lesser or higher

degrees of that behaviour (e.g. high explorers and low

explorers in Great Tits, Parus major (Verbeek et al.

1996)). Furthermore, the expression of consistent

individual differences has been demonstrated across a

wide range of taxa (mammals: Vervaecke et al. 1999;

Dochtermann & Jenkins 2007; birds: Verbeek et al.

1996; Dingemanse et al. 2002; fish: Harcourt et al.

2009; Bell & Sih 2007; invertebrates: Wilson et al.

2010; Sih & Watters 2005).

Despite the wealth of knowledge that has accumu-

lated on the topics of consistent individual differences,

Ethology 119 (2013) 189–198 © 2013 Blackwell Verlag GmbH 189

Ethology

the range of behaviours examined across studies

remains limited. Generally, authors have focused on

expressions of boldness and/or activity between indi-

viduals (Johnson & Sih 2005; Dochtermann & Jenkins

2007; Duckworth & Badyaev 2007; Reaney &

Backwell 2007). However, alternate selection pres-

sures imposed by differences in ecology and environ-

ments among species suggest that behaviour types

and how they correlate can be unpredictable within

and across species (Sih & Bell 2008). For example,

optimal behaviour types likely differ between solitary

and social organisms where behavioural types such as

aggression can have very different long-term impacts

on individual fitness, and therefore cannot be pre-

dicted using the same paradigm. Among cooperatively

breeding cichlids, the most effective helpers in intru-

der defence are the most aggressive individuals (Le

Vin et al. 2011). Despite this, studies examining the

social effects of individual differences have generally

focused on single aspects of social relationships such

as aggressive or agonistic interactions (Budaev 1997;

McGhee & Travis 2010; David et al. 2011; Pruitt et al.

2011) or, alternatively, on the general interaction pat-

terns among all group members (Moretz et al. 2007;

Pike et al. 2008; Croft et al. 2009; Harcourt et al.

2009). These measures provide information about just

two dimensions of a long list of complex interaction

types between conspecifics. Many animal species are

highly social, meaning there has been emphasis

placed on benefits received from iterative interactions

with group members through predator defence,

assisted breeding or information transfer (Wilson

2000). Therefore, behavioural categories such as

learning proficiency represent an important skill

among social animals, where key behaviours are

derived from exposure to experienced individuals

(Kavaliers et al. 2005). Learning ability may be pre-

dictable based on other behaviours such as explora-

tion of the environment and could also affect an

individual’s competitive nature with its groupmates.

Examination of a broad range of behavioural catego-

ries is necessary to gain a broader understanding of

how an individual’s behaviour is impacted by its

groupmates and context.

In this study, we sought to examine the relation-

ships between behaviours across a wide dimension of

behavioural categories and across different social

environments in long-lived, gregarious female big

brown bats (Eptesicus fuscus). We addressed the follow-

ing questions: (1) What, if any, is the relationship

between traits encompassing activity, learning, com-

petitiveness and aggressiveness? Activity and aggres-

siveness are behavioural categories commonly

examined in studies of behavioural correlates,

although they commonly show differential degrees of

relatedness depending on species and context (Boog-

ert et al. 2006; Biro et al. 2010; Kralj-Fiser et al.

2010; Wilson et al. 2010). Learning behaviour and

competitiveness can heavily impact an individual’s

relationship among its social partners, and yet, is

rarely examined in studies of behavioural traits and

syndromes (Wilson et al. 2010; Pruitt et al. 2011); (2)

How do behaviours exhibited in solitary treatments

compare with those exhibited in the presence of a

conspecific? While other studies have examined

behavioural syndromes and group dynamics, little is

known about the relationships between behaviours

exhibited in solitary and social contexts (Bergmuller

& Taborsky 2010).

Methods

Study Animals

We selected the big brown bat (Eptesicus fuscus) as

our study species. Big brown bats are a common

vespertilionid bat, which occurs in a wide range of

habitats across North America. During the summer,

females form maternity colonies, in which adult

males usually do not occur and exhibit strong

philopatry to specific roosting areas (Willis &

Brigham 2004 for forests; Brigham 1991 for build-

ings). Within maternity colonies of forest-dwelling

populations, females conform to a fission–fusionsocial system (Willis & Brigham 2004). The prefer-

ential associations between females in subgroups are

not based on genetic relatedness (Metheny et al.

2008), indicating that female roost-mate preferences

are mediated by other factors. Females typically

have one offspring per year, and juveniles have low

overwinter survival (O’Shea et al. 2010). Like many

small mammals, thermoregulation represents a high

energetic cost. Bats rely extensively on torpor to

save energy during daytime roosting periods

throughout the summer (Racey & Swift 1981).

However, many species adjust torpor use during

certain periods of the reproductive cycle (Audet

& Fenton 1988; Grinevitch et al. 1995; Dzal &

Brigham 2012), placing greater importance on social

thermoregulation (Willis et al. 2006; Pretzlaff et al.

2010) between members of maternity colonies dur-

ing those periods. Therefore, social associations

unique between females are likely critical to big

brown bats given the potential benefits.

We collected individuals from four different

building-roosting maternity colonies in southern

Ethology 119 (2013) 189–198 © 2013 Blackwell Verlag GmbH190

The Relationships between Behavioural Categories and Social Influences R. J. Kilgour & R. M. Brigham

Saskatchewan and south-western Alberta (hereafter

referred to colonies 1 through 4, listed in chronologi-

cal order). Individuals were either caught using mist

nets (Colonies 3 and 4) or manually removed from

building roosts by hand where feasible (Colonies 1

and 2). Trapping sessions only took place during the

early or late summer to minimize the risk of disturb-

ing parturition and lactation. During the early sum-

mer, bats were expected to be in early to mid-stages of

pregnancy. Individuals from colonies 1 (n = 8) and 2

(n = 4) were caught during the typical period of preg-

nancy (May–June). No individuals caught were detec-

tably pregnant. Individuals from colonies 3 (n = 8)

and 4 (n = 8) were trapped during the post-lactation

period and all females but two exhibited signs of lacta-

tion from that year.

Experiments were conducted at the University of

Regina Cypress Hills Field Station (49°34′N and 109°53′W) during the summer of 2009, with only one

group of bats (from a single colony) held in captivity

at a time. Bats were transported to the field station

in individual cotton bags. Each bat was injected with

a passive integrative transponder (PIT) tag for identi-

fication and given a unique combination of reflec-

tive forearm bands to allow for individual

identification during video recording. Bats were

hand fed Tenebrio molitor larvae, to monitor individ-

ual food intake and had access to water ad libitum.

Bats were group-housed indoors in a 145-l Exo

Terra flexarium (Rolf C. Hagen Inc., Montreal, Can-

ada) when not participating in trials. The seasonal

light cycle was maintained, except when conducting

experiments and lights were turned on for assays,

and room temperature was maintained at 20–24°C.All behavioural assays were conducted between

20:00 and 04:00, during the natural period of activ-

ity. Bats were held in captivity for no longer than

11 d and following the experimental sessions, they

were returned to the colony where they were

trapped. All protocols were approved by the Univer-

sity of Regina President’s Committee on Animal

Care (protocol 08-01).

To examine relationships between behavioural cat-

egories, we compared the expression of seven

behavioural variables by all individuals, three solitary

behaviours (learning ability, solitary exploration and

latency to feed in captivity) and four social behaviours

(competitive ability, social exploration, latency to

explore in social contexts and biting frequency).

We also examined the relationship between behavio-

ural variables and body condition. The methodologies

used to assess behaviours and traits measured are

described below.

Body Condition Index (BCI)

To compensate for differences in overall body form,

the body condition of each bat was calculated as the

ratio of body mass (g) divided by forearm length

(mm). Forearm length was measured as the length

of the right forearm (� 0.1 mm), and body mass

(� 0.1 g) was the initial mass measured when the

individual was caught, prior to feeding. Therefore, a

high value represents an individual with a better body

condition.

Learning Ability (Learning)

The learning ability of each bat was measured during

training sessions prior to the competitive ability

experiment. Individuals were trained to walk to a

food piece located on a plastic tray. Individuals were

placed in an unfamiliar triangular arena and trained

to feed in a series of six steps. At each step, the bat

was placed farther away from the dish with the food.

After a bat successfully acquired the food at a set dis-

tance five times in succession, the bat proceeded to

the next step, where the food tray was placed farther

away. Therefore, a bat with the highest score for

learning ability completed the training in 25 trials,

although most individuals required more trials to

effectively ‘pass’ a step. Prior to trials, food was with-

held for 20 h to increase motivation. Observers

remained in the room during trials, but out of sight

for each session. Noise was kept to a minimum. Indi-

viduals were scored between 1 and 6 for their learning

ability based on the number of training sessions nec-

essary for them to complete the prescribed training

procedure. A score of 6 represents a fast-learning indi-

vidual, and a score of 1 represents a slow-learning

individual. For further information, please see

(Table S1).

Competitive Ability (Comp)

Females were placed in dyadic food competitions with

group members to assess competitive ability. Bats

were trained to acquire a piece of Tenebrio larvae from

a food dish (see ‘learning ability’). Individuals were

then tested in dyadic combinations with all other bats

from the same colony and each trial was repeated five

times. In other words, each dyad underwent five com-

petition trials. If neither competitor consumed the

food piece after 60 s, it was considered a mistrial. The

individuals used in trials were randomized, although

no female competed twice consecutively. Therefore,

each female had a minimum rest period of 1 min


R. J. Kilgour & R. M. Brigham The Relationships between Behavioural Categories and Social Influences

between trials. When not being tested, bats were kept

in cloth holding bags. Prior to trials, food was with-

held for 20 h to increase motivation. Trials took place

over 2–3 nights to reduce the effects of satiation. After

trials were complete for a night, bats were re-tested

for their ability to consume food pieces and all suc-

cessfully acquired and consumed them, indicating

that performance was not due to a lack of training or

satiation.

Competition trials consisted of two bats placed in a

triangular arena (35 9 47 9 47 cm; walls 19 cm

high) at the same time, equidistant from food. Trials

lasted until one bat successfully ate the food (typi-

cally, <30 s). Because unequal numbers of individuals

were caught at each colony, there were unequal

numbers of trials (and thus the potential number of

wins) between individuals from different colonies.

To compensate, competitive ability was standardized

by calculating the number of wins relative to the total

number of trials per individual. Competitive ability of

individuals was not measured between groups due to

limitations in acquiring bats from maternity colonies

and the logistics of holding multiple colonies simulta-

neously within the captive environment.

Exploration of a Novel Environment in a Solitary

Context (SoloEX)

To measure exploration as an indicator of an individ-

ual’s activity levels, we placed bats in a triangular

arena (different from that used in the competitive

experiment; 40 9 50 9 48 cm; walls 42 cm high)

and measured the amount of time bats exhibited

exploratory behaviour. Two novel objects were placed

in the arena during each trial, and these were chan-

ged after 8–10 trials to prevent habituation. The novel

objects were the following: a bean bag sack, a ceramic

mug, a plastic toy gun, a large plastic cup, a rock, a set

of plastic mini-speakers, a roll of duct tape and a plas-

tic lid from a small animal cage. The bats had no expo-

sure to the arena prior to trials. To encourage

exploration, bats were not allowed any habituation

period with the objects.

Exploratory behaviour was defined as any active

movement within the arena and most often took the

form of escape behaviours (e.g. attempting to climb

over the walls of the arena) and object exploration

(e.g. where bats walked under or over objects). There-

fore, an individual’s exploration score was quantified

as the number of seconds it exhibited exploratory

behaviours over the duration of the trial. We recorded

trials with a Sony Handycam (HDR-XR200V, Sony,

Tokyo, Japan) positioned directly above the arena.

Once bats were placed in the arena, observers left the

room. Trials lasted three min, and each individual was

run in three trials daily for three nights.

Exploration of a Novel Environment in a Social Setting

(SocialEX)

Exploratory behaviour was also measured in the pres-

ence of other bats. Individuals were run in explor-

atory trials in dyadic combinations with all other

group members. Each pairwise combination was

repeated three times. The rotation of novel objects,

the duration and execution of trials and the measure-

ment of exploratory behaviour were identical to the

solitary exploration trials. Pairwise combinations were

randomized and no individual participated in two

consecutive trials. Bats were kept in cloth holding

bags between trials. This treatment was also used to

measure activity levels of individuals.

Latency of Exploration in Social Settings (SocialLat)

The latency to explore was measured as the number

of seconds from the beginning of the trial to the time

when an individual began its first exploration bout of

Social Exploration trials. If an individual did not

explore during the trial, they were given a latency

score of 300 based on the 300 s duration of the trial.

Frequency of Biting Behaviour (BiteFrq)

Biting, or attempted biting, is an aggressive behaviour

used among groupmates of many different species.

Biting behaviour was assessed as the frequency of suc-

cessful or unsuccessful attempts made by each bat to

bite the other bat during the social exploration trials.

Any biting that occurred during the competitive

experiment trials was not included, as the motivation

for aggression was unequal between the two experi-

ments. Furthermore, there was a low frequency of

observed biting attempts during competitive trials.

Bats received a score for biting behaviour based on

the frequency of biting (or attempting to bite) com-

panion animals during social exploration trials.

Latency to Feed in Captivity (LatFeed)

Bats were given a score based on their ability to feed

consistently, as another measure of a bat’s learning

ability. For the 10 d that bats were maintained in cap-

tivity, they were fed mealworms (Tenebrio larvae) by

hand which allowed us to monitor food intake by

each individual. We detected variation among bats in



how quickly they began to feed, and each bat was

given a score for their latency to feed. Bats were given

scores ranging from 1 to 5 based on the number of

Tenebio larvae consumed during the first feeding bout

and consecutive bouts. A score of 1 was given to bats

who successfully consumed six larvae on the first

feeding attempt and a minimum of six larvae at all

future feeding times. Successive increases in score

number were based on number of feeding attempts

and days passing until successfully consuming a mini-

mum of six larvae at one feeding. Bats removed from

colonies by hand were caught in the afternoon and

brought to the field station that evening, and bats

caught in mist nets in the evening as they exited from

day roosts. Thus, all bats were presumed to be hungry

upon arrival at the field station. Bats were fed 6–8mealworms in two feeding sessions each night. They

were considered to be feeding consistently once they

ate six full larvae consecutively and continued to

consume at least six mealworms per feeding bout. For

more detailed information, see (Tables S2 and S3). All

bats learned to eat consistently in captivity within

4 d.

Statistical Analysis

We used Exploratory Factor Analysis (EFA) to exam-

ine the relationships among the behavioural catego-

ries measured. EFA is useful in estimating the

relationships between variables without a priori

hypotheses. Unlike Principal Component Analysis,

EFA does not expect communality to be 1, allowing

for error variance in contributing variables. The num-

ber of factors was determined based on the Scree plots

and the Chi-square statistic, which tests the null

hypothesis that the model does not fit the data. We

used promax rotation, a type of oblique rotation,

which allows for correlations between factors. All

analyses were conducted in R, Version 2.13.0 (2009).

Results

Bats exhibited considerable variation across the seven

categories of behaviours we measured (Fig. 1). With

the data pooled across all colonies, we found that the

majority of bats learned the feeding task quickly

(mean score of 3.7 � 0.42 of 6, where a score of six

indicates that an individual passed through each level

without repetition). Bats also generally had low laten-

cies to feed in captivity, as exhibited by a low mean

score (2.03 � 0.29 of 5), demonstrating that few lev-

els had to be repeated before moving on to the next

level. Bats exhibited higher exploratory behaviour in

solitary vs. social trials (overall mean seconds explor-

ing, 124.75 � 7.16 and 39.94 � 5.0, respectively).

Further analysis of these variables in a correlation

matrix allows for greater understanding of the relat-

edness between the variables (Table 1). Statistical sig-

nificance at the a = 0.05 level was observed between

several behavioural pairings (BCI and SoloEx, Learn

and Comp, Learn and LatFeed, SoloEx and LatFeed,

SocEx and SocLat); however, significance was lost

between all pairings when Bonferoni corrections were

applied. The correlations between the variables were

generally weak, with the exception of Learning and

Competitive behaviours (r = 0.54, p < 0.05).

Multivariate results from the EFA showed three fac-

tors resulting from the eight variables included in the

analysis (Fig. 2). A Chi-square analysis testing the

hypothesis that the model does not fit significantly

worse than a model where the variables correlate

freely was rejected (v2 = 1.99, df = 7, p = 0.961)

(Table 2). Barlett’s test of sphericity supported our

previous findings of sufficient correlations between

the behavioural variables (v2 = 43.74, df = 28,

p = 0.03). Kaiser–Meyer–Olkin (KMO) tests show

that, despite our small sample size, our sampling was

adequate to support the EFA (KMO = 0.58) (Budaev

2010). KMO and Barlett’s test were run in the paf

function from Rela library in R (Chajewski 2009). The

first factor relates to the measures of learning, compe-

tition, biting frequence and latency to feed, where

bats who learned quickly to obtain a food piece in the

training arena (Learning) were also individuals who

won the highest proportion of their competitive trials

(Comp), as well as had the shortest latency to feed

from the hand when first brought into captivity

(FeedLat) and also most likely to bite a conspecific

(BiteFrq). As these four categories refer to behaviours

requiring assessment and potentially cognitive skill,

the first factor is labelled ‘Cognition’. The second fac-

tor links a high BCI to a shorter latency to explore in a

social environment (SocialLat), as well as less time

spent exploring overall in the presence of a social

companion (SocialEX). This second factor also relates

to a high biting frequency (BiteFrq) and a longer

latency to feed from the hand (FeedLat). This factor

describes the overall activity level of the individual

and is therefore labelled ‘Activity’. The final factor

contains only the variable SoloEX, describing the

average exploration exhibited by a bat without any

conspecific present.

Correlations between the factors (Table 3) indicate

that Factor 2 (Activity) is highly correlated with Fac-

tor 3 (SoloEx) (r = �0.52, p < 0.05). Considering Fac-

tor 3 consists entirely of the measure of solitary



exploration (Table 3), this indicates that solitary

exploration is uniquely linked with other aspects of

exploration in the presence of conspecifics which

encompass Factor 2. Correlations between other fac-

tors were less prominent, although Factor 1 (Cogni-

tion) and Factor 2 (Activity) were mildly correlated

(r = 0.32, p > 0.05).

Discussion

The goal of our study was to assess the relationships

between a diverse range of behavioural categories in

adult female big brown bats. To our knowledge, this is

the first study to examine behavioural categories in

this species, as well as for bats in general. We exam-

ined behaviours exhibited across multiple dimensions,

including activity, learning, competitiveness and

aggressiveness, and compared the behaviour of indi-

viduals in both social and solitary contexts. Our

results indicated that correlated behaviour in this

group may not be comparable to similar studies

conducted on other species. Differences in behaviour-

al expression in solitary and social settings indicate

the strong influence of social environment on behav-

iour. Correlations among behaviours further suggest

the importance of including a wide range of behavio-

ural categories when examining relationships in

behaviour.

Using EFA, we isolated three factors to describe

which behaviours or variables varied most similarly.

Factors 1 and 2, Cognition and Activity, consisted of

more than one variable, allowing for the assessment

Table 1: A matrix showing the correlation of the variables included in the analysis. Correlations are based on Pearson’s r

BCI Learning Comp SoloEX SocialEX SocialLat BiteFrq LatFeed

BCI 0.08 �0.03 �0.37a �0.27 �0.34 0.17 0.33

Learning 0.54a 0.14 0.08 0.06 0.35 �0.39a

Comp 0.28 0.20 0.18 0.11 �0.24

SoloEX 0.35 0.04 0.08 �0.38a

SocialEX 0.39a �0.13 �0.35

SocialLat �0.17 �0.35

BiteFrq 0.08

LatFeed

aIndicates statistical significance at a = 0.05.

00.050.10.150.20.250.30.350.40.450.5

BCI0

1

2

3

4

5

6

7

Learning0

0.2

0.4

0.6

0.8

1

1.2

Competitive020406080100120140160180200

SoloEX

0

20

40

60

80

100

120

SocialEX0

5

10

15

20

25

30

35

40

SocialLat0

1

2

3

4

5

6

7

8

9

BiteFrq0

1

2

3

4

5

6

LatFeed

Fig. 1: Boxplots displaying data ranges for

variables included in our study. Note different

scales in each variable: Competitive ability is

measured in proportions of wins: losses; learn-

ing is based on a six-point scale; exploration-

based variables are measured in seconds

(maximum 300 s); biting is the number of

observed biting attempts; latency to feed is

based on five-point scale. See text for more

details.



of relationships between these variables. Factor 1,

labelled ‘Cognition’, describes characteristics of cogni-

tion and specific aspects of social interaction. This

encompasses variables of ease of learning a new task

(Learning), ease of learning a new feeding technique

in a new environment (LatFeed), competitive ability

over conspecifics (Comp) and frequency of biting

aggression to conspecifics (BiteFrq) (Table 2). Com-

bined, these variables describe an organism that can

rapidly learn and adapt to a new environment and

out-compete others for limited resources. An individ-

ual who exhibits all of these characteristics may be

more likely to acquire access to limited resources.

Although we did not examine dominance relation-

ships in this study, dominance is often defined as an

individual’s resource holding power (Parker 1974).

Further, many aspects of a successful competitor lie in

the ability to assess the social environment prior to

competition, making behavioural plasticity crucial in

acquiring socially derived benefits (Galef & Wigmore

1983; Moscovice & Snowdon 2006). Based on our

data, body size is not a predictor of competitive ability

in female bats, which may reflect the uniqueness of

this study system.

Factor 2 considers behavioural categories of social

activity, as well as body size. We found that bats with

a high BCI also exhibited the shortest latency to

explore in the presence of a conspecific (SocialLat),

were overall less exploratory in the presence of a con-

specific (SocialEX), most frequently bit a companion

(BiteFrq) and also took the longest to learn to feed by

hand in captivity (LatFeed) (Table 2). When placed in

the novel environment with a conspecific, bats who

were not exploring spent most of the time engaged in

social activity with their companion. Therefore, we

see that bats who initiate exploration quickly in a

social environment also are mostly likely to spend the

trial period interacting with their companion. Fur-

thermore, the high BCI reflects individuals who were

of improved body condition were those who were

more often engaged in social interactions. The

increased biting frequency may be a result of

increased social interaction and increased opportunity

for aggressive encounters. Bats that are of better body

condition may be this way because they glean energy

savings through increased social interactions. Individ-

uals who are more active in the presence of compan-

ions may lose energy savings or the ability to roost

socially based on decreased interactions with group-

mates. Among shoaling Trinidadian guppies (Poecilia

reticulata), individuals who engage more in bold

behaviours (predatory inspection) were also had

fewer social connections with groupmates (Croft et al.

2009).

Comparing bats to other species, our examination

of the relationships between behaviour categories is

atypical. For example, correlations between behav-

iours are often observed in aggression and boldness,

although not always (Wilson et al. 2010). Exploratory

behaviour has often been considered a measure of

boldness and neophobia (Wilson et al. 1994). When

exploratory behaviour is measured in a completely

novel environment, the motivation underlying the

exploratory behaviour may be similar to boldness

(Hughes 1997). Our results indicate that aggression

level was not prominently related to boldness, where

Table 2: Inclusive variables listed with factor loadings. Factors were

determined based on Scree plots and non-significance of chi-square

statistics

Variable Factor 1 Factor 2 Factor 3

Learning 1.02

Competitive 0.5

Biting 0.36 0.39

Latency to Feed �0.31 0.48

Social Exploration �0.48

Body Composition Index 0.42

Latency for Social Exploration �0.83

Solitary Exploration 1.11

Cumulative Proportion of

Variance Explained

0.20 0.39 0.57

Table 3: Correlations between the factors isolated using exploratory

factor analysis. Values represent correlations as calculated using Pear-

son’s r

Factor 2 Factor 3

Factor 1 0.32 �0.12

Factor 2 �0.52a

aIndicates statistical significance at a = 0.05.

BCI

LearningComp

SoloEX

SocialEX

SocialLat

BiteFrqLatFeed

–1

–0.8

–0.6

–0.4

–0.2

0

0.2

0.4

0.6

–0.4 –0.2 0 0.2 0.4 0.6 0.8 1 1.2

Fact

or 1

Factor 2

Fig. 2: Relationships between variables across Factors 1 and 2 as

derived from exploratory factor analyses.



biting was negatively related to exploration in the

presence of a conspecific (Factor 2, Table 2) and was

positively related to learning ability and competive-

ness among bats (Factor 1, Table 2). Examination of

the correlations between variables shows a slight posi-

tive relationship between individuals who most fre-

quently bit a conspecific and those who trained to

acquire a food piece from a designated area most

quickly (Table 1). These results may suggest, how-

ever, that aggression might play a role in competitive

interactions between groupmates. In social animals,

aggression towards conspecifics is typically used as a

means of acquiring resources through dominance

relationships (Chase et al. 1994; Draud et al. 2004).

Our results imply that this may be consistent in big

brown bat maternity groups. Although bats do not

compete for food in the wild, they might compete for

roosting locations, where the individual who occupies

the warmest location in the roost is less likely to go

into deep torpor during the roosting period (McGo-

wan et al. 2006). Among females, this could lead to

greater energy savings to a developing foetus. Big

brown bats might use aggressive behaviours such as

biting to gain access to high valued roosting locations.

Therefore, unlike in other species, aggression towards

group mates was not a predictor of activity levels or

boldness. Considering other behavioural measures,

such as learning ability, bats exhibited similar rela-

tionships to starlings (Sturnus vulgaris). Measures of

learning ability in wild-caught starlings suggested that

learning ability did correlate with competitive ranks

but not to boldness (Boogert et al. 2006). Other stud-

ies that have examined the relationship between

exploratory behaviour and dominance interactions in

black-capped chickadees (Fox et al. 2009) show that

low-exploring individuals out-compete subordinate

individuals for roosting locations. Our results suggest

that neither solitary nor social exploratory behaviour

in bats is an indicator of competitive or aggressive

pairwise interactions (Tables 1 and 2). This study sup-

ports the growing body of evidence suggesting that

behavioural categories, and the relationships between

them, differ across species.

In addition to our examination of multiple behavio-

ural categories included in this analysis, we also con-

sidered behaviours exhibited in solitary and social

settings. Solitary behaviours included learning ability,

latency to feed in captivity and solitary exploration.

Variables measured when bats were in social settings

included biting frequency, competitive ability, social

exploration and social latency. Exploratory behaviour

was measured in both solitary and social settings, and

we found only a slight positive correlation between

those two variables (Table 1). However, solitary

exploration was best described as a behaviour in and

of itself, as it was the sole contributor to Factor 3. Fur-

thermore, Factor 2, which included the variables

describing exploration in the presence of a conspe-

cific, was negatively correlated with Factor 3 suggest-

ing that solitary exploration in bats is negatively

related to activity in the presence of a conspecific.

However, bats were less exploratory of their sur-

roundings when in the presence of a social compan-

ion (Table 1), implying that bats alter their behaviour

in the presence of social companions, a finding consis-

tent with other studies (Metcalfe et al. 1987; Pintor

et al. 2008; Mainwaring et al. 2011).

Our data demonstrate that correlated behavioural

categories vary across different taxa, perhaps imposed

by unique selection pressure imposed on animals

with unique ecologies. Furthermore, our findings

emphasize the importance of social context on

behavioural phenotypes. It is clear from our data that

the presence of a conspecific has the potential to alter

the behaviours exhibited by bats and that the rela-

tionships between behaviour of individuals found in

bat maternity colonies may be unique among social

animals. More study is needed to understand how

the behavioural categories we included relate to indi-

vidual behaviour, fitness consequences and social

relationships. A larger sample size as well as measur-

ing social behaviours such as competitive behaviour

across colonies would provide greater insight into

behavioural profiles compare across individuals. Our

measure of competitive ability was limited to com-

parisons only between dyads of group members,

potentially confounding the independence of the

result. To our knowledge, this is the first study to

examine correlations in behaviour in this species.

Given the differences in correlated behaviours that

we discovered when compared with other taxa, it is

clear that understanding the ecological and evolu-

tionary context of each species and population is cru-

cial when examining behavioural categories and

their relationships.

Acknowledgements

We thank M Dunbar, E Gillam, GG McNickle and J

Ratcliffe for helpful comments on the manuscript.

We also thank D Braun, A Matheson and J Poissant

for their assistance with field work and care of captive

bats. Funding was provided by the Natural Sciences

and Engineering Research Council of Canada (Discov-

ery Grant to RMB) and the American Society of

Mammalogists (Grants-in-Aid of Research, RJK).



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Supporting Information

Additional supporting information may be found in

the online version of this article:

Table S1: The protocol used to assess learning abil-

ity in bats. If a bat took longer than 3 min at any stage

in the training procedure, it was considered a “mis-

trial” and was returned to the previous step.

Table S2: Description of how bats were assigned

learning scores.

Table S3: Description of how bats were scored for

latency to feed in captivity.



the relationships between behavioural categories and social

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