The role of androgens in the trade-off between territorial and parental behavior in the Azorean rock-pool blenny, Parablennius parvicornis
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
References (43)
Androgens in teleost fishes
Comp. Biochem. Physiol., C: Comp. Pharmacol
(1994)- et al.
Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis
Anim. Behav
(1994) - et al.
Comparative analyses of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation
Horm. Behav
(2003) - et al.
Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta
Gen. Comp. Endocrinol
(1982) - et al.
Serum 11-ketotestosterone and testosterone concentrations associated with reproduction in male bluegill (Lepomis macrochirus: Centrarchidae)
Gen. Comp. Endocrinol
(1989) - et al.
The effects of exogenous 11-ketotestosterone, testosterone, and cyproterone acetate on prespawning and parental care behaviors of male bluegill
Horm. Behav
(1991) - et al.
Hormones, pheromones, and reproductive behavior in fish
- et al.
The influence of testosterone on territorial defence and parental behavior in male free-living rufous whistlers, Pachycephala rufiventris
Horm. Behav
(2001) - et al.
Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae)
Horm. Behav
(2001) - et al.
Endocrine correlates of male polymorphism and alternative reproductive tactics in the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis
Gen. Comp. Endocrinol
(2001)
Effects of androgens on social behavior and morphology of alternative reproductive males of the Azorean rock-pool blenny
Horm. Behav
Social modulation of androgen levels in male teleost fish
Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol
Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus: I. Changes in 11-ketotestosterone levels during the nesting cycle
Horm. Behav
Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus: II. Castration and 11-ketoandostenedione effects on courtship and parental care during the nesting cycle
Horm. Behav
Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis
Horm. Behav
Effects of long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca, during the breeding period
Anim. Behav
Mouthbrooding in the black-chinned tilapia, Sarotherodon melanotheron (Pisces: Cichlidae): the presence of eggs reduces androgen and estradiol levels during paternal and maternal parental behavior
Horm. Behav
Plasma androgen levels during male parental care in a tropical frog (Eleutherodactylus)
Horm. Behav
The lack of influence of exogenous testosterone on male parental behavior in a Neotropical frog (Eleutherodactylus): a field experiment
Horm. Behav
Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus)
Horm. Behav
Effects of testosterone of song, aggression and nestling feeding behavior in male great tits, Parus major
Horm. Behav
Cited by (66)
Parental care behaviour in response to perceived paternity is not mediated by 11-ketotestosterone in bluegill sunfish
2023, General and Comparative EndocrinologyAnimal Behavior
2021, Animal BehaviorThe endocrine disruptor, 17Α-ethinyl estradiol, alters male mate choice in a freshwater fish
2019, Aquatic ToxicologyParental behavior in fish
2018, Encyclopedia of Reproduction