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Hormones and Behavior

Social cues and hormone levels in male Octodon degus (Rodentia): a field

test of the Challenge Hypothesis

Mauricio Soto-Gamboaa,*, Manuel Villalonb, Francisco Bozinovicc

aInstituto de Zoologıa, Facultad de Ciencias, Universidad Austral de Chile, Casilla (Box) 567, Valdivia, ChilebUnidad de Reproduccion y Desarrollo, Departamento de Ciencias Fisiologicas, Facultad de Ciencias Biologicas,

Pontificia Universidad Catolica de Chile, ChilecCenter for Advanced Studies in Ecology and Biodiversity and Departamento de Ecologıa, Facultad de Ciencias Biologicas,

Pontificia Universidad Catolica de Chile, Chile

Received 21 March 2004; revised 28 October 2004; accepted 1 November 2004

Available online 16 January 2005

Abstract

Social interactions are important factors determining and regulating individual behaviors. Testosterone has been related to agonistic

interactions, while glucocorticoids have been related to social stress, especially during interactions of dominance. We compared testosterone

and cortisol concentrations in male degus (Octodon degus, Rodentia) under laboratory conditions without male social interactions, with data

from wild males in nature. Under natural conditions, males should present higher levels of testosterone during the breeding season due to

social interactions (Challenge Hypothesis). Alternatively, intense social instability could act as a stressing environment, raising

glucocorticoids, which inhibit testosterone concentrations. Our results show a significant increase in agonistic interactions between males

during the breeding season, and disappearance of non-agonistic male interactions during this period. Hormone levels in breeding season show

nonsignificant differences between laboratory groups, but testosterone concentrations in field males were significantly higher than in

laboratory males. Testosterone levels were similar among pre-breeding and breeding periods, but in field animals the concentration was ~30%

higher than in laboratory degus. In field animals, we found two different mating strategies: resident males, with territorial behavior, and

transient males, displayed an opportunistic approach to females. Finally, cortisol presents a similar pattern in both laboratory and field

animals; pre-breeding values of cortisol are higher than during the breeding season. This suggests that social interactions in O. degus activate

a rise in testosterone, supporting the Challenge Hypothesis, and could be considered as partial support of the Social Stress Hypothesis.

D 2004 Elsevier Inc. All rights reserved.

Keywords: Testosterone; Cortisol; Social interaction; Social stress; Social instability; Challenge Hypothesis; Octodon degus; Degu

Introduction

Social interactions are an important factor determining

and modulating individual behavior and performance. In

many cases, individual behavior is directly dependent on

relationships with other individuals that live together or in

the neighborhood (Clutton-Brock et al., 2001; Conradt and

Roper, 2000; Kappeler, 1999). These interactions include

agonistic and non-agonistic behaviors that may determine

0018-506X/$ - see front matter D 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.yhbeh.2004.11.010

* Corresponding author. Fax: +56 63 221315.

E-mail address: mrsoto@uach.cl (M. Soto-Gamboa).

social position, dominance, and hierarchy relations between

individuals within social groups (Clarke and Faulkes, 2001;

Cote, 2000; Smale and Holekamp, 1997), and in extreme

social situations may affect individual reproductive success

(Clarke and Bennett, 2001; Clutton-Brock et al., 2001;

Raouf et al., 1997; Sherman et al., 1995; Stoehr and Hill,

2000; Zielinski and Vandenbergh, 1993). Nevertheless,

individual behavior also has an important physiological

component, especially hormonal regulation, which can

determine the successful acquisition of a social position in

the hierarchy or access to reproductive females (Alberts et

al., 1992; Buck and Barnes, 2003; Clarke and Faulkes,

1998; Crews, 1997; Randall and Bromage, 1998; Raouf et

47 (2005) 311–318

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318312

al., 1997). In this sense, social interactions and hormonal

regulation are narrowly related and determine behavioral

patterns of the individual (Crews, 1997).

Among vertebrates, testosterone has several principal

functions in the physiology of an organism. It is

responsible for spermatogenesis and some secondary sex

characters as well as the activation of male sexual

behaviors (Blottner et al., 2000; Nelson, 2000; Wingfield

et al., 1997). During the reproductive period, testosterone

has direct effects on mating behaviors including attractive-

ness to females and on males’ interactions for access to

females (Cavigelli and Pareira, 2000; Dunlap et al., 2002;

Emerson, 1997; Goodson and Bass, 2001; Sinervo et al.,

2000; Wingfield et al., 1990, 1994). The Challenge

Hypothesis was originally proposed for bird species

(Wingfield et al., 1990), and predicts that androgen levels

and aggression are positively related, and are closely

associated with social context. An increase in male

interactions activates testosterone secretion and, conse-

quently, increases aggressive behaviors (Wingfield et al.,

1997). The degree of increase in testosterone levels and the

magnitude of agonistic response depend on the degree of

social stimulus (Cavigelli and Pareira, 2000; Wingfield et

al., 1990). Among mammals, male interactions and

testosterone regulation of aggressive behavior have

recently been studied (Cavigelli and Pareira, 2000; Lynch

et al., 2002; Muller and Wrangham, 2004; Ostner and

Kappeler, 2002). In these cases, there is a positive

correlation between male aggression and testosterone

levels during the reproductive period. In rodents, testoster-

one levels have been associated with territory defense,

reproductive group formation, social dominance, and

hierarchy formation (Cavigelli and Pareira, 2000; Clarke

and Faulkes, 1998; Faulkes and Abbott, 1997; Rogovin et

al., 2003; Wolff, 1994; Zielinski and Vandenbergh, 1993).

In contrast, social interactions can also act as important

stressing agent (Rogovin et al., 2003). The physiological

cost of reproduction associated with the cost of dominance

behavior often results in a stressing situation (Ketterson and

Nolan, 1999; Sapolsky, 2002). During the breeding season,

males compete for access to females and continually express

intense aggressive or agonistic interactions. These inter-

actions determine social status and, consequently, the

reproductive success of animals. Finally, these relationships

directly increase energetic demand and glucocorticoid levels

(Goymann and Wingfield, 2004). As a consequence of these

behavioral interactions, individuals reach high levels of

glucocorticoids, via the activation of the hypothalamic–

pituitary–adrenal axis (HPA). In extreme cases (chronic

stress), glucocorticoids can produce a decrease in testoster-

one secretion by the hypothalamic–pituitary–gonadal (HPG)

axis inhibition, thus affecting an individual’s social status in

the group (Blanchard et al., 2001; Knapp and Moore, 1997).

In this sense, social interactions can produce two different

types of hormonal outcomes: (1) enhancement of testoster-

one concentrations and consequent aggressive displays, and

(2) an increase in glucocorticoids via HPA axis suppressing

the HPG axis, and diminished testosterone levels. The

objective of this work is to evaluate how social interaction

levels affect hormonal levels of males, and how these have

direct repercussions on the behavioral patterns in male

degus.

The degu, Octodon degus, is a social caviomorph rodent

endemic to central Chile. This semi-fossorial, diurnal, and

herbivorous rodent (~180 g), lives in groups, but only

presents a structured social system during the breeding

season (Soto-Gamboa, unpublished data; Vasquez, 1997).

During this period, O. degus have been observed to form

polygynous groups consisting in one male and one to three

females (Ebensperger et al., 2004; Fulk, 1976). Previous

laboratory work reported a direct relationship between

male’s aggression and testosterone levels only during the

breeding period (Farfan et al., 2001). In this study, we

compare variation of testosterone and cortisol levels in

captive males without and with low social interactions with

field animals in the pre-breeding and breeding seasons. We

hypothesized that social interactions have positive effect on

testosterone levels enhancing aggressive behavior during the

breeding season, i.e., the Challenge Hypothesis. Alterna-

tively, intense social instability could be a stressing environ-

ment, raising glucocorticoids, which ultimately inhibit

testosterone concentrations, i.e., social stress hypothesis.

These hypotheses are not mutually exclusive, but the

relative importance of variation in hormonal changes

depends on the magnitude of social interactions.

Methods

To test social interactions, we divided the experimen-

tal design into two different approaches. The field Study

includes behavioral patterns of activity and testosterone

and cortisol levels. These data were compared with

laboratory animals separated into virgin (without social

interaction) and reproductive males (only with female

social interaction).

Field study

We studied a natural population of O. degus in

Rinconada de Maipu (33831VS, 70850VW), a field station

of the Universidad de Chile, located near Santiago, in

Central Chile. In April and June–July of 2002, we captured

animals using a capture effort of 100 Sherman live traps

during 5 days. All captured animals were sexed, weighed,

and marked with a uniquely colored collar ring. For later

hormone analysis (see below), we took blood samples from

all captured males (approximately 700 Al from the

suborbital sinus with a heparinized glass pipette). To avoid

manipulation effects, the traps were checked every half

hour, following Place and Kenagy (2000), and based on

preliminary data that degus do not present significant

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318 313

variation in testosterone and glucocorticoid levels when

animals were maintained between 0 and 2 h inside the traps

(K.S. Matt and F. Bozinovic, unpublished data). The

handling time for blood sampling was never over 30 s,

and was obtained immediately after animals were removed

from the traps. In total, we got blood samples from 9 males

in April and from 12 males in June–July.

During the 5 days after capture, we recorded behavioral

data through direct observations, consisting of 15 min of

focused male observation, registering all interactions with

other animals. In total, we registered 20 focal observations

per period, during which we identified all animals interact-

ing with the focal animal. The interaction rate was classified

using four different classes based on behavioral repertoires

previously described by Fulk (1976): (1) agonistic inter-

actions between males, including chases, mounting and

foreleg pushing; (2) non-agonistic interactions between

males, including allogrooming, nose contact (olfaction),

and group foraging; (3) agonistic interactions of males

towards females, including chases and foreleg pushing; and

(4) non-agonistic interactions of males towards females,

including allogrooming, nose contact (olfaction), and group

foraging. Rates of interaction were calculated for individual

animals and represent a percentage of the total interactions

for a particular male.

Finally, we classified males as resident or transient in

function of their capacity to defend territories and monop-

olize females. This differentiation was made in order to

compare hormone levels of animals with high (resident) and

low (transient) rates of social interactions. During breeding

period, we recognized a total of five resident males and

seven transient male (in total 12 animals).

Laboratory study

For our experimental study, we used males born in the

laboratory by parents from a native population from Lampa

(33817VS, 70853VW), near Santiago, in Central Chile.

Animals were separated from their mother at 2 months of

age (weaning), and were maintained in individual cages.

Photoperiod was maintained on a D:L 12:12-h cycle with

controlled temperature between 15 and 258C following the

night–day cycle. Rabbit food (ChampionR) pellets and

water were offered ad libitum.

Males were randomly separated into two different

groups: virgin males and reproductive males. Animals in

the first group were constantly maintained in individual

cages, while in the second group, males were enclosed with

two or three females to establish reproductive families

during the breeding period. Reproductive groups were

utilized to evaluate the effect of male–female interactions

on circulating testosterone levels. In this group, all males

were effective as reproductive animals and in most families

at least one female was pregnant. We obtained blood

samples from a total of 30 individuals: 10 virgin males in

the pre-breeding period (April 2003), 10 virgin males in the

breeding period, and 10 reproductive males with females

during the breeding period (June–July 2003). Similar to

wild animals, for blood sampling, handling time was never

over 30 s. This protocol was used to compare non-

reproductive and reproductive values of hormones in virgin

(single) males, and in males interacting with females and to

compare hormone results between wild and laboratory

animals. In this way, we designed different levels of social

interactions: virgin (without social interactions), reproduc-

tive males (only with females interactions), wild transients

males (with low male–male interactions), and resident males

(with highest levels of social interaction, including female

and male interactions).

Steroid assays

Blood samples were transported to the laboratory in a

refrigerated cooler (not more than 8 h after being taken) and

centrifuged at 7000 rpm for 10 min. Plasma was separated

from blood cells and stored at �208C for latter hormone

assays. Testosterone and cortisol concentrations were

measured by enzyme immunoassay with reagents supplied

by the World Health Organization program for the Provision

of Matched Reagents for RIA of Hormone in Reproductive

Physiology, and following their recommended procedures

(Sufi et al., 1998). For testosterone determination, we

extracted the hormone with diethyl-ether, evaporating 50

Al of plasma, and resuspending in RIA assay buffer. For

cortisol determination, we diluted 25 Al of plasma sample in

500 Al of RIA buffer solution, and took 20 Al of this solutionfor protein denaturation to 608C. These methods had

resolution limits for testosterone of 0.12 ng/ml and 17.8

ng/ml for cortisol. Finally, all samples were analyzed in

duplicate, and the precision of the assay was evaluated by

determining the intra- and interassay coefficient of variation

(CV). Intra- and interassay CV for testosterone were 5.3%

and 9.3%, and for cortisol, 8.3% and 11.7%, respectively.

Statistical analyses

Statistical analyses were performed using parametric and

non-parametric statistical tests. To analyze behavioral

relationships, we used interaction rates expressed as a

percentage of total interactions displayed by an individual

male. We utilized a Mann–Whitney U test to evaluate

significant differences between breeding periods for each

interaction type at P b 0.05. For hormonal comparisons, we

utilized ANOVA. Normality of the data was evaluated using

the Kolmogorov–Smirnov test and homogeneity of variance

was evaluated with Levene’s test. In the seasonal compar-

ison, we utilized two-way ANOVA, using as factors

seasonality (pre-breeding and breeding) and treatment

(laboratory and field animals). During breeding season,

one-way ANOVA was performed to compare the different

classes of males. In the case of the testosterone data set, we

performed a log-transformation to meet assumptions (Zar,

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318314

1996). An unequal Tukey Test was utilized for post hoc

analysis. All statistical analyses were performed using

Statistica 6.0 software (StatSoft, 2001). Results are pre-

sented as means F 1 standard error (SEM).

Ethical note

All experimental procedures in this work were carried

out under the approval of Pontificia Universidad Catolica de

Chile ethical committee and according to the current

Chilean law, under permit number SAG-698 of the Servicio

Agrıcola y Ganadero.

Fig. 2. Seasonal patterns of hormonal variation between pre-breeding and

breeding periods. Panel (a) exhibits testosterone levels for laboratory and

field animals, and panel (b) presents variation in cortisol levels between

animal groups. Groups size were n = 9 field pre-breeding males, n = 12

field breeding males, n = 20 laboratory pre-breeding animals, and n = 20

breeding animals. An asterisk (*) indicates significant differences at P b

0.05 using an Unequal Tukey post hoc test. Data are presented as mean F

Results

Field behavioral analysis

Interaction rates of male behavior varied throughout the

reproductive cycle. During the breeding period, males

showed a significant increase in aggressive interactions

with other males [Mann–Whitney test: U(20,20) = 92, P =

0.03]. Non-agonistic behaviors between males were not

observed during this period (Fig. 1). The most frequently

observed agonistic behavior during this period was chases

of transient males by resident males. Resident males

actively defended territories and females, and were the

winner in more than 90% of agonistic interactions. This

result contrasts with the pre-breeding period, where we

observed frequent male non-agonistic behavior, particularly

in foraging groups. When we analyzed interactions

between males and females, we did not observe agonistic

Fig. 1. Seasonal changes in behavioral patterns of interactions in wild male

animals from the field. Data represent percentages of total interactions

destined to agonistic and non-agonistic encounters separated by sex (n = 20

focal observations per period). An asterisk (*) indicates significant

differences at P b 0.05 using the Mann–Whitney U test. Data are expressed

as mean F standard error.

standard error.

behavioral displays in either period (Fig. 1). Furthermore,

we did not find significant differences in non-agonistic

behaviors displayed by males towards females between the

pre-breeding and breeding period [Mann–Whitney test:

U(20,20) = 169, P = 0.41], thus accounting for approx-

imately 50–60% of total interactions of males in both

periods (Fig. 1).

Hormonal variation between pre-breeding and breeding

seasons

To evaluate the effect of male social interactions on

hormone levels, we compared data for pre-breeding and

breeding seasons between field animals and laboratory

animals that never experienced social stimuli (i.e., virgins).

In Fig. 2a, we present variation in testosterone concen-

trations between reproductive periods, and between wild

and laboratory animals. We found significant differences

between pre-breeding and breeding periods, with animals

in the breeding period showing the highest levels of

testosterone [two-way ANOVA: F(1,37) = 10.52, P =

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318 315

0.003]. On the other hand, there were no significant

differences between animal groups [two-way ANOVA:

F(1,37) = 2.79, P = 0.103] or significant interactions, i.e.,

both animal groups (field and lab) presented the same

pattern of variation in testosterone concentrations between

pre-breeding and breeding periods [two-way ANOVA:

F(1.37) = 0.501, P = 0.48]. Cortisol concentrations varied

only between pre-breeding and breeding periods (Fig. 2b),

where the pre-breeding period presented the highest

concentrations [two-way ANOVA: F(1.37) = 18.150, P =

0.0001], and there were no significant differences between

field and lab animals [two-way ANOVA: F(1,37) = 0.0852,

P = 0.772]. These results indicate that field animals have

the same cortisol concentrations patterns as laboratory

animals.

Hormone relationships during the breeding season

During the breeding season, field males are exposed to

intense social instability caused by interactions with other

males (Fig. 1), while laboratory animals never were

exposed to male interactions. Comparing the four different

classes of males, i.e., virgin laboratory males, reproductive

laboratory males, transient males, and resident males, we

Fig. 3. Hormonal levels of male degus during the breeding season. We

compare field animals separated in resident (n = 5) and transient (n = 7)

males with virgin (n = 10) and reproductive laboratory (n = 10) males.

Panel (a) presents variation in testosterone levels between groups, and panel

(b) presents variation in cortisol between groups. An asterisk (*) indicates

significant differences at P b 0.05 using ANOVA. Data are expressed as

mean F standard error.

found significant differences in testosterone levels [one-

way ANOVA F(3,38) = 5.96 P = 0.003]. Tukey post hoc

test showed that resident males had significantly higher

levels of testosterone than the other groups, and transient

males were not significantly difference than either

laboratory animal groups (Fig. 3a). Cortisol levels present

the same pattern. Exist significant differences between

male groups [one-way ANOVA F(3,28) = 3.92 P = 0.019].

Tukey post hoc test showed that resident males present

significant highest hormonal level than the other groups

(Fig. 3b).

Discussion

In this study, we experimentally manipulated the

social interactions in laboratory male degus and com-

pared their hormone levels with two different classes of

wild males (resident and transient). We found that both

groups of animals, laboratory and field males, have a

seasonal variation in hormonal levels. During the pre-

breeding season, animals show high levels of cortisol but

this diminished during breeding season. Contrary, testos-

terone levels show low values during pre-breeding

season, but increase significantly during breeding season.

Previous studies have not found seasonal variation in

testosterone levels of wild males (Kenagy et al., 1999).

These authors reported very low values of testosterone,

and few animals had detectable testosterone levels. This

makes interpretation of their results difficult. There is an

obvious contradiction between results from Kenagy et al.

(1999) and our data, which show a very clear pattern of

testosterone variation between pre-reproductive and

reproductive period, but the reason for this discrepancy

remains unexplained. Probably the very low levels of

testosterone observed by Kenagy and collaborators were

nearby the limit of detection.

The high levels of testosterone found during repro-

ductive periods among field males indicate that, under

natural conditions, there exist environmental factors that

directly affect testosterone levels. We found that social

agonistic interactions between males during this period

increase testosterone, concordantly with Challenge

Hypothesis. Particularly, resident males that are more

exposed to social interaction and present the highest

levels of testosterone, but have highest levels of cortisol

too. These results propose that resident males have two

different responses to social stimuli. First, increases in

testosterone by male–male interaction, increasing behav-

ioral agonistic displays, and second, increases in cortisol

levels in response to the social stress of defending the

territory and/or females. These increases of the levels of

cortisol also might be only an effect of the increase of

the energetic demands associated with the cost of the

defense of territory and/or females (Moore and Jessop,

2003).

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318316

The Challenge Hypothesis

The Challenge Hypothesis claims a direct relationship

between temporal patterns of male testosterone levels and

mating system strategies (Wingfield et al., 1990). In

particular, testosterone secretion in polygynous species is

postulated to be directly related to male–male interactions

(Wingfield, 1984). Moreover, it is possible to distinguish

between baseline testosterone concentrations in the non-

reproductive season (i.e., the non-breeding baseline), the

reproductive season (i.e., the reproductive baseline), and the

transient surges of testosterone secretions induced by male–

male interactions (Muller and Wrangham, 2004; Wingfield

et al., 1990). Our results represent a complete synthesis of

this pattern. O. degus are polygynous social rodents where

males compete for female access to form reproductive

groups (Fulk, 1976). Our laboratory results represent the

physiological baseline during the pre-breeding season and

the reproductive baseline during the breeding season. It is

very interesting that testosterone levels in the pre-breeding

season are not different between laboratory and field males.

This suggests that both laboratory and field degus show a

similar endogenous pattern of their reproductive cycle, and

the same non-reproductive baseline of testosterone secre-

tions. In contrast, during the reproductive period, laboratory

animals represent the reproductive baseline of testosterone

levels, and have significantly higher testosterone levels than

animals observed in the pre-breeding period. The higher

testosterone levels observed in field reproductive males

could indicate that testosterone levels that are near their

maximum physiological levels could be due to the effects of

social interactions.

We were able to differentiate between two different

classes of field males: resident males with a defensible

female group, and transient males with reduced presence in

the study area (Clutton-Brock, 1989). It is very striking that

only resident males exhibited high levels of testosterone,

and they were also the animals that most frequently

presented agonistic behaviors during the breeding season,

while transient males exhibited the basal reproductive level,

thus maintaining their potential to breed. These results may

represent two different male reproductive strategies. First, at

the beginning of the breeding season, males actively

compete to monopolize females, and then quickly form

reproductive groups. This period of social instability

induces elevated testosterone levels in group-forming males

(i.e., resident males), while the males that are not able to

form groups lose their chance to breed in this season (i.e.,

transient males). Alternatively, transient males may use an

opportunistic strategy for female accessibility at low

physiological cost. Clearly, the defensible harem has high

physiological costs associated with it, to maintain the

exclusivity of females, this includes the increased metabolic

cost of maintaining high levels of testosterone (Ketterson

and Nolan, 1999; Ketterson et al., 1996; Wingfield et al.,

1997) and possible effects on immune system suppression

(Braude et al., 1999; Casto et al., 2001; Folstad and Karter,

1992; Wedekind and Folstad, 1994). To differentiate

between these alternatives, it is necessary to take a new

approach towards the study of mating systems in degus to

determine the real reproductive output of resident versus

transient males.

Finally, hormonal differences in male mating strategies

could be associated with other factors more than social

stimuli. Age, experience, energy storage, and health are

important factors than can affect directly hormonal levels

and reproductive success (Wingfield, 1994). In O. degus, it

has been demonstrated that the testosterone levels and

testicular development decrease in function of age and older

animal increase body mass (Bustos-Obregon and Ramirez,

1997). In our results, we did not find a significant difference

in body mass between different classes of males during

breeding season and all laboratory animals were of same age

(proximate 10 months). We cannot estimate the age of wild

males, and most probably, we include different cohorts in

our analysis.

Social stress

Our results indicate that male degus presented a similar

seasonal pattern of cortisol concentrations in both laboratory

and wild groups. During the pre-breeding season, cortisol

levels were higher than during the breeding season,

presumably following an endogenous rhythm. This affirma-

tion is supported by the fact that laboratory animals lack

environmental factors that may modulate cortisol variations.

Seasonal variations of glucocorticoids have been reported

for a variety of vertebrate taxa, but remain unclear for most

mammals (Romero, 2002). However, rodents exhibiting

clear patterns of seasonal variation have been reported (see

Boswell et al., 1994; Kenagy and Place, 2000; Place and

Kenagy, 2000), particularly degus (Kenagy et al., 1999). In

all of these cases, glucocorticoids decline during mating

season. What is the cause of this variation is unknown, but

the most likely explanation is that during the pre-breeding

season, food is scarce and animals must allocate more time

to feeding and storing energetic reserves for the breeding

period. This could be strictly associated with an increase of

glucocorticoids, thus stimulating foraging behavior and

energy mobilization for storage (Boswell et al., 1994; Green

et al., 1992; Romero, 2002; Sapolsky et al., 2000; Wingfield

and Kitaysky, 2002).

Field resident male degus showed different cortisol levels

in comparison to transient and laboratory groups of males.

While resident males presented the highest levels of

testosterone and cortisol, the others groups have low levels.

It is clear that social and physical stressors can cause an

increase in glucocorticoids, which can suppress male

reproduction (Boonstra and McColl, 2000), but in our

study, males exposed to increased social interactions (i.e.,

resident males) did not show hormonal signals of repro-

ductive suppression. Our results represent a transitional

M. Soto-Gamboa et al. / Hormones and Behavior 47 (2005) 311–318 317

situation in which resident males have intermediate levels of

stress, increased cortisol levels but not sufficient to inhibit

testosterone secretion. Recent studies of cooperative

breeders in the field show that dominant males can have

high levels of glucocorticoids as a result of the increased

cost of maintaining their dominance status and hierarchical

position (Boonstra and McColl, 2000; Creel, 2001; Creel et

al., 1996, 1997). Our results suggest that male degus have a

similar pattern, in which resident males experience a high

cost in terms of territorial defense and challenges with

transient animals. Finally, it is unclear what factors

determine resident or transient males, but they are affected

by age, body condition, health, or sensitivity to environ-

mental condition. These possibilities could be considered

for future approach to this problem.

In summary, our study of captive and free living male

degus has contributed new information regarding hormonal

regulation of behavior in group-living animals. In particular,

we found evidence to support the fundamental premises of

the Challenge Hypothesis, indicating that male degus are

directly affected by social interactions with other males.

However, in wild males, we observed two different

strategies (i.e., resident versus transient) for breeding males.

Both classes of males presented significant hormonal

differences possibly associated with behavioral strategies

of mate formation. These data could be partially supported

by the Social Stress Hypothesis since the high level of

cortisol in resident males did not have an effect on their

reproductive performance and testosterone levels.

Acknowledgments

We are grateful to Luis Ebensperger, Diego Urrejola, and

Marıa Jose Hurtado for field assistance. Special thanks to

John C. Wingfield and James G. Kenagy for critical

comments on the manuscript. Thanks are due to the

Universidad de Chile and Jose Daniel Garcıa (Field Station

Administrator) for access to the study area. This research

was funded by a CONICYT Doctoral Thesis Fellowship to

M. Soto-Gamboa and by FONDAP Grant 1501-001

program 1 to F. Bozinovic.

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