The role of androgens in the trade-off between territorial and parental behavior in the Azorean rock-pool blenny, Parablennius parvicornis

doi:10.1016/j.yhbeh.2004.04.007

Hormones and Behavior

Volume 46, Issue 4, November 2004, Pages 491-497

https://doi.org/10.1016/j.yhbeh.2004.04.007 Get rights and content

Abstract

Androgen hormones have been shown to facilitate competitive ability in courtship and territorial behavior, while suppressing paternal behavior. The rock-pool blenny, Parablennius parvicornis, provides an excellent model to study the proximate regulation of such a trade-off between territorial and parental behavior, because nest-holder males of this species display these behaviors simultaneously. A field study was carried out in which territorial nest holder males were either treated with long-lasting implants filled with 11-ketotestosterone (11-KT) or with control implants. Males treated with 11-KT showed a higher frequency of aggressive behavior, were more responsive to aggressive challenges, and were more persistent in aggressive behavior than control males. In addition, territories were larger in males treated with 11-KT than in controls. We found evidence for incompatibility between defense of a large territory and high levels of parental behavior. However, contrary to expectation, 11-KT did not suppress parental behavior. We suggest that trade-offs between territorial and parental behavior may not be regulated by androgen hormones but may result from a time constraint in the individual's activity budget.

Introduction

Androgen levels of males are thought to be adjusted to the social environment the animal is living in and have been proposed to promote the success in aggressive competition Oliveira et al., 2001d, Wingfield et al., 1990. Studies that were carried out to test this hypothesis by increasing levels of androgens experimentally, found an increase in male–male competition, the territory size, and the number of extra-pair copulations (e.g., Ketterson et al., 1996). Although these effects are likely to enhance fitness, not all male individuals of a particular population raise their androgen levels to the physiological maximum during the reproductive season. Therefore, it has been proposed that high levels of testosterone are costly to maintain. Folstad and Karter (1992) suggested that only animals of good quality might be able to maintain high levels of androgens since chronic allocation of resources towards androgen-mediated aggressive behavior will compromise other traits, like immunocompetence. Otherwise, Wingfield et al. (1990) proposed that androgens suppress parental care, which will constrain the expression of high levels of androgens during the breeding season in species in which males provide parental care.

Many vertebrate taxa show a negative relationship between levels of testosterone and paternal effort (e.g., Ziegler, 2000; but see Trainor and Marler, 2001). In avian species, polygynous males maintain high levels of testosterone throughout the breeding season and typically show little parental care. In monogamous parental males, levels of testosterone are high during territory establishment and mate choice but decrease at the start of the period of parental care (Wingfield et al., 1990). Likewise, in parental males of several teleost species, 11-ketotestoterone (11-KT) decreases from the mating to the parental phase (Oliveira et al., 2002).

The goal of this study was to test the effect of androgens on aggression and parental care in the Azorean rock pool blenny, Parablennius parvicornis, a teleost that shows alternative reproductive tactics (Santos et al., 1996). Nest-holder males have overlapping courtship, parental and territorial behaviors, and are therefore particularly appropriate to study the interrelation between androgens, territorial behavior and parental behavior. Oliveira et al. (2001b) showed in a natural population that parental males have higher levels of 11-KT than nonparental satellite males. Furthermore, within males of the bourgeois tactic, 11-KT levels did not differ between nonparental and parental males. Although these data show that in nest-holder males hormonal levels are relatively high, 11-KT levels showed a negative correlation with egg fanning, which is the main male parental behavior. This suggests that 11-KT is modulating a trade-off between parental care and territorial behavior. To investigate the underlying mechanism of this trade-off, nest holder males of the rock-pool blenny were treated in the field with slow-release 11-KT implants and compared to non-hormone-treated males in respect to their territorial and parental behaviors, and in their attractiveness to females.

Section snippets

Study site and experimental procedure

The field study was conducted from May to the end of July 2002 in intertidal rock pools on a flat basaltic platform at Feteira on the south coast of Faial Island, Azores (38°31′N; 28°27′W; for a description of the area, see Santos and Barreiros, 1993).

During an initial survey, visible male territories were mapped to select the best sites for behavioral observations and hormonal manipulation. To facilitate identification, nest-holder males were hand-netted, tagged in the dorsal muscle close to

Effects of 11-KT on social behavior and territoriality

11-KT treatment increased the frequency of intraspecific aggression and of excursions (Fig. 1; Mann–Whitney U tests: intraspecific aggression, U = 26.5, P < 0.05, excursions, U = 24.5, P < 0.01), while no effect was found on interspecific aggression (Fig. 1). Treatment with 11-KT did not affect sexual behavior of the nest-holders (Fig. 1) and had no effect neither on the frequency of sexual behavior received from females, nor on the number of females that entered the nest of the focal male.

Discussion

The aim of our experiment was to investigate whether 11-KT regulates the trade-off between territorial and parental behaviors in teleost species that show these behaviors simultaneously. Based on the challenge hypothesis, we expected that androgens would suppress parental behavior (Wingfield et al., 1990; for a recent review, see Hirschenhauser et al., 2003). In a field study, nest-holder males of the Azorean rock-pool blenny, P. parvicornis, were treated with long-lasting implants of 11-KT,

Acknowledgements

We are very grateful to Elsa Couto for running the radioimmunoassay. During this study, AFHR was being supported by a postdoctoral fellowship from the Portuguese Foundation for Science and Technology (FCT) (SFRH / BPD / 7143 / 2001). RFO's and AFHR's research is supported by FCT's Plurianual Program (R and D Unit 331/94). The procedures used in this study comply with the “Principles of animal care,” publication No. 86-23, revised 1985, of the National Institutes of Health, USA, and with the

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The role of androgens in the trade-off between territorial and parental behavior in the Azorean rock-pool blenny, Parablennius parvicornis

Abstract

Introduction

Section snippets

Study site and experimental procedure

Effects of 11-KT on social behavior and territoriality

Discussion

Acknowledgements

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