Elsevier

Psychoneuroendocrinology

Volume 34, Issue 7, August 2009, Pages 1056-1064
Psychoneuroendocrinology

Testosterone responsiveness to winning and losing experiences in female soccer players

https://doi.org/10.1016/j.psyneuen.2009.02.006Get rights and content

Summary

In many animal species including humans circulating androgen levels in males respond to social challenges. This response has been interpreted as an adaptive mechanism that helps the individuals to adjust their behavior to changes in social context. According to this hypothesis socially modulated androgen levels (e.g. increased levels in dominants and decreased levels in subordinates) would influence the subsequent expression of social behavior in a status-dependent fashion. This rationale is partially based on male physiology and therefore has been rarely investigated in females. Here, we investigated if a hormonal response to a social challenge that produces changes in status is also present in human females. We have collected saliva from and administered questionnaires to female soccer players of both teams playing the final match of the Portuguese Female soccer league. Samples were collected on a neutral day and on the day of the game both before and after the match. The change in testosterone levels (i.e. post-game  pre-game values = ΔT) was positive in the winners and negative in the losers and there was a significant difference in the testosterone change (i.e. ΔT) over the game between winners and losers. Cortisol levels did not vary with contest outcome. An anticipatory rise in circulating levels of both hormones (testosterone and cortisol) was detected before the match. Paralleling the hormonal responses, changes in mood and anxiety state were also found between both teams, with more positive states being observed in winners and more negative states being observed in losers at the end of the match. These results suggest that testosterone also responds to social challenges in human females and that contest-induced mood changes may influence this response.

Introduction

In recent decades evidence has accumulated for a reciprocal relationship between androgens and behavior. The role of androgens on the regulation of aggressive behavior is well established and was the first behavioral endocrinology principle to be proposed as far back as the late 19th century (Soma, 2006). More recently, social challenges, such as fighting an opponent, have been shown to elicit an androgen response in a wide range of vertebrates including humans (Hirschenhauser and Oliveira, 2006). The accumulation of this type of data led to the proposal of two independent hypotheses that try to explain a reciprocal interaction between androgens and competitive behavior: the biosocial status hypothesis (Mazur, 1985, Mazur and Booth, 1998) and the challenge hypothesis (Wingfield et al., 1990). According to these two hypotheses changes in androgens levels driven by social competition would modify the behavior of the participants in subsequent interactions according to previous social information. Therefore, they provide a conceptual framework to explain the elevation of androgen levels in males during periods of increased social competition (Wingfield et al., 1990, Hirschenhauser et al., 2003, Archer, 2006). Several psychological variables have been proposed to mediate and moderate the hormonal response to social challenges and to competition. According to the cognitive activation theory of stress (CATS) previous social interactions produce stimulus or response outcome expectancies that would be instrumental in the subsequent responses to social stimuli (Ursin and Eriksen, 2004).

Indeed, the perception of contest outcome, winning or losing, seems to modulate the androgen responsiveness, since manipulated interactions where the animal is allowed to fight without perceiving a win or a loss of status (by fighting its own image on a mirror) fail to elicit an endocrine response (Oliveira et al., 2005). In general a victory increases (or arrests a decrease in) testosterone (T) post-competition levels whereas a defeat experience decreases circulating T, although some studies have failed to find an effect of the outcome on androgen response to competition (for reviews see Mazur and Booth, 1998, Salvador, 2005, Archer, 2006, van Anders and Watson, 2006, Salvador and Costa, 2009). This differential hormonal response to competition between winners and losers has been documented not only in contests that involve physical confrontation (e.g. tennis match, Mazur and Lamb, 1980; wrestling combat, Elias, 1981), but also in non-physical face-to-face competition such as chess and domino tournaments (Mazur et al., 1992, Wagner et al., 2002). Moreover, salivary T levels also respond to competition outcome in sports fans who are psychologically linked to the success of their teams but are not directly involved in the contest (Bernhardt et al., 1998). Together, these data suggest a cognitive activation of the endocrine response to social challenge. Concomitantly the tendency to engage in future social interactions is influenced by the outcome of a previous interaction (e.g. decreased in losers, Mehta and Josephs, 2006). These hormonal and behavioral responses to previous contest experience have been interpreted as an adaptation for individuals to express appropriate behavior to ever changing social environments, by adjusting their agonistic motivation accordingly (Mazur, 1985, Mazur and Booth, 1998, Oliveira, 2004).

The rationale for this hypothesis is based on male physiology and hence the evidence supporting it is mainly grounded on male studies. Recently there has been an emerging interest in understanding the validity of this hypothesis in females. T levels in women seem to be associated with social status and the expression of assertive behaviors (Grant and France, 2001, Cashdan, 2003, Edwards et al., 2006) and are predictors of reactions to wins and losses (Josephs et al., 2006, Mehta et al., 2008).

Moreover, dominance dependent T changes may modulate subsequent social interaction in females since T may modulate a set of psychological traits that are highly relevant for the dynamics and outcome of contest. T effects on competitive relevant traits include: increased selective attention to social threat (i.e. angry faces, van Honk et al., 1999), increased visuospatial ability (Aleman et al., 2004), fear reduction (van Honk et al., 2005, Hermans et al., 2006) and reduction of punishment sensitivity and enhancement of reward dependency (van Honk et al., 2004). T is also known to promote the activation to angry vs. happy faces in women brain areas involved in reactive aggression (e.g. amygdala and hypothalamus; Hermans et al., 2008).

On the other hand, competitive situations induced an increase in T and cortisol (C) levels in female rugby and soccer players (Bateup et al., 2002, Edwards et al., 2006) but not in women playing a video game, rowing in a ergometer sprint competition or competing on cognitive tasks (Mazur et al., 1997, Kivlighan et al., 2005, Schulteiss et al., 2005, van Anders and Watson, 2007). Interestingly, none of these studies on female competition reported differences in T levels between winners and losers (Bateup et al., 2002, Schulteiss et al., 2005, Edwards et al., 2006, van Anders and Watson, 2007). However, in both studies the researchers have followed a single team and so for the same event hormonal responsiveness data were only available for one of the two conditions (win/loss). Since the salience of different win/loss episodes may depend very markedly on its consequences for self-perceived status (e.g. winning/losing a final match that decides a championship vs. winning/losing a regular season game) data on hormonal responsiveness to the outcome of a competitive event for both parties are needed.

Here we report the hormonal responsiveness to competition both in winners and in losers of the final match of the Portuguese Female Soccer League. For this purpose we collected saliva samples from and administered questionnaires to female soccer players both before and after the final match and at the same time of the day in a neutral day (i.e. the same day of the week but without neither a game nor a training session). Since C can modulate the androgen responsiveness to competition we have also measured C levels in winners and losers.

Section snippets

Participants

Thirty-three female soccer players aged 24.24 ± 4.78 from two different teams that would play against each other the match that would decide the first place in the Feminine Portuguese Soccer League (FPSL) gave their informed consent to participate in the study. Players from both teams were sampled in a neutral day before the match and on the day of the match. Players from the winning team consequently became champions of that year's FPSL, and the players from the losing team classified in the

Psychological and hormonal trait variables

The psychological trait variables measured (i.e. anxiety, mood and aggression) did not differ between the players of the two teams (Mann–Whitney U-test – anxiety total score: NW = 15, NL = 18, U = 125.00, Z = −0.36, p = 0.72; mood total score: NW = 15, NL = 17, U = 121.00, Z = 0.24, p = 0.81; aggression total score: NW = 13, NL = 18, U = 97.50, Z = 0.78, p = 0.781).

The cortisol awakening response in a neutral day (i.e. without soccer game) did not differ between players of the two teams suggesting that there are no

Discussion

The main goal of the present study was to evaluate the hormonal responses in winners and losers of a single competitive event of high valence in terms of social status. For this purpose we have sampled players of both teams during the final match of the Portuguese Female Soccer League. Overall players of the two teams exhibited an anticipatory rise both in T and C before the game. Over the game players of the winning team experienced an increase in T levels whereas T levels decreased in losers

Role of the funding source

Funding for this study was provided by FCT (Portugal) grants POCTI/PSI/38496/2001 and 331/2001; the FCT had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Conflict of interest statement

Hereby we declare that none of us (authors) have any actual or potential conflict of interest including any financial, personal or other relationships with other people or organizations within three years of beginning the work submitted that could inappropriately influence, or be perceived to influence, the work submitted here.

Acknowledgements

We thank Pedro Almeida for promoting the access to the players, Joana Rego for helping with data collection, and constructive comments from four anonymous reviewers. This study was funded by the research grant POCTI/PSI/38496/2001 from Fundação para a Ciência e a Tecnologia (FCT), the European Commission FEDER Program and the FCT Plurianual Program (R&D unit 331/2001). During this study T.O. was being supported by a research fellowship from FCT.

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