Albert F. H. Ros

THE RELATION AMONG GONADAL STEROIDS, IMMUNOCOMPETENCE, BODY MASS, AND BEHAVIOR IN YOUNG BLACK-HEADED GULLS (LARUS RIDIBUNDUS )

We experimentally examined the effect of testosterone on the antibody response to a single immunization with sheep red blood cells in young black‐headed gulls. This species performs a number of testosterone‐mediated elaborate postural displays in social interactions and breeds in dense colonies in which there is a high likelihood of infectious diseases. In young chicks, only one‐third were capable of responding to immunization. In the responding chicks, testosterone enhanced antibody titers. Even when antibody responsiveness was measured >1 mo after the termination of hormonal treatment, antibody responses were enhanced in birds treated with androgen but not estrogen. At 9 mo of age, all birds responded to immunization, but there was no effect of testosterone on antibody titers. In these juveniles, frequency of display behavior was negatively related to changes in body mass, which suggests that displaying is energetically costly. Despite decreased body mass, antibody titers were highest in birds that displayed more frequently. This suggests that displaying signals immunocompetence. The results are discussed in relation to the immunocompetence handicap hypothesis and to what is known of the influence of the bursa of Fabricius and social stress on antibody production.

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

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 individuals activity budget.

Aggressive behaviour and energy metabolism in a cichlid fish, Oreochromis mossambicus

We have investigated the effect of mirror-elicited agonistic behaviour on oxygen consumption in the Mozambique tilapia, Oreochromis mossambicus (Cichlidae). Males exposed to their mirror image showed higher frequencies of both lateral display and tail-beating and escalated aggression more frequently than males exposed to a transparent glass that was used as a control for the presence of a novel object in the tank. This aggressive response was correlated with an increase in oxygen consumption. Overt aggression was highly correlated with display behaviour and with locomotor activity. Bivariate analyses showed high correlation (explaining about 64% of variation) between overt aggression, locomotor activity and metabolic rates. Weakly positive bivariate correlations between displays and metabolic rates turned spurious after partialling out aggression. The data suggest that energetic costs only emerge late during the conflict, when animals escalate their aggressive behaviour.

Tactile stimulation lowers stress in fish

In humans, physical stimulation, such as massage therapy, reduces stress and has demonstrable health benefits. Grooming in primates may have similar effects but it remains unclear whether the positive effects are due to physical contact or to its social value. Here we show that physical stimulation reduces stress in a coral reef fish, the surgeonfish Ctenochaetus striatus. These fish regularly visit cleaner wrasses Labroides dimidiatus to have ectoparasites removed. The cleanerfish influences client decisions by physically touching the surgeonfish with its pectoral and pelvic fins, a behaviour known as tactile stimulation. We simulated this behaviour by exposing surgeonfish to mechanically moving cleanerfish models. Surgeonfish had significantly lower levels of cortisol when stimulated by moving models compared with controls with access to stationary models. Our results show that physical contact alone, without a social aspect, is enough to produce fitness-enhancing benefits, a situation so far only demonstrated in humans.

Social stimuli, testosterone, and aggression in gull chicks: Support for the challenge hypothesis

We tested the challenge hypothesis for the hormonal regulation of aggression in chicks of the black-headed gull, Larus ridibundus. Chicks of this species are highly aggressive toward conspecifics, but never to peers that hatched from the same clutch (modal clutch size is three). Therefore, in the first experiment small families were housed together in large groups (challenged condition) and compared to families kept isolated (nonchallenged condition). As expected, in the challenged condition during the initial stage of territory establishment basal levels of testosterone (T) were clearly higher than those in the nonchallenged condition. In the second experiment we tested the effect of a short social challenge on short-term T-fluctuations. The design was based on an earlier experiment, showing that after temporary T-treatment chicks become very sensitive to social challenges while having low basal T-levels. We now show that these social challenges induce brief elevations in plasma T-levels. These peaks are similar to those in previously untreated chicks but untreated chicks do not respond with aggression to a challenge. Therefore, we conclude that the initial exposure to elevated T-levels increases the sensitivity to brief changes in T induced by social challenges. In this way exposure to T, that may be detrimental for development, is minimized while birds remain able to defend territories. This is the first report showing that the challenge hypothesis as established for adult birds, is also applicable for aggressive behavior in young birds outside the sexual context. Furthermore we suggest that a phase of priming with T is necessary to obtain the high behavioral responsiveness to a challenge.

Intra-sexual variation in male reproduction in teleost fish: A comparative approach

The occurrence of intra-sexual variation in reproduction is a widespread phenomenon in teleosts. One such form of variation consists in the occurrence of alternative male types: males that invest resources in mate attraction and males that exploit the investment of the former males, by trying to sneak fertilizations during spawning. These alternative reproductive tactics can be classified according to their plasticity during the life span of the individuals (i.e., fixed vs. sequential vs. reversible). Furthermore, the differences between morphs within a given species may involve a set of different traits, including reproductive behavior, the differentiation of male morphological traits, and the patterns of gonad tissue allocation and the differentiation of gonadal accessory glands. In this paper, we review the available data on four species exhibiting different types of intra-sexual plasticity in reproduction that have been studied in our lab. The data on the proximate mechanisms, androgens and forebrain arginine-vasotocin (AVT), underlying these alternative tactics suggest that between-morph differences in androgen levels, especially in 11-ketotestosterone, are especially present in species where the alternative male types have evolved morphological traits that are tactic-specific (i.e., sexual polymorphisms) and that differences in AVT appear to be related to between-morph differences in the expression of courtship behavior. Therefore, this comparative approach leads us to propose that the different endocrine systems are involved in the differentiation of different sets of traits that make up alternative phenotypes, and that the differentiation of alternative tactics is not controlled by a single endocrine system (e.g., androgens).

The hormonal control of begging and early aggressive behavior: Experiments in black-headed gull chicks

The hormonal control of begging and sibling competition is largely unknown, but recent evidence suggests a role for steroid hormones. We tested the influence of the aromatizable androgen testosterone (T), the non-aromatizable androgen 5alpha-dihydrotestosterone (DHT), and 17beta-estradiol (E) on both begging behavior and aggressive behavior in black-headed gull chicks (Larus ridibundus). Chicks of this species have a conspicuous begging display, while their frequently performed early aggressive behavior is facilitated by testosterone and important for territorial defense. Hormone treatment was applied by implants between days 6 and 16 after hatching. Behavior was tested by means of standard stimulus tests. The results were validated in a second experiment under semi-natural conditions. Begging was suppressed by T and DHT and not affected by E. Aggressive Pecking was strongly facilitated by T. The erect threat posture, characteristic for older chicks, was facilitated by T, DHT, and E and the nest-oriented threat display, typical for young chicks, only by T and DHT. Growth was suppressed in the T group. The results indicate that androgen production, needed for territorial defense, has costs in terms of a suppression of begging and growth. It is discussed to what extent older chicks may avoid these costs by converting testosterone to estrogen and why pre-natal and post-natal exposure to androgens differ in their effect on begging behavior.

Alternative male reproductive tactics and the immunocompetence handicap in the azorean rock-pool blenny, Parablennius parvicornis

In the Azorean rock-pool blenny (Parablennius parvicornis) reproductively active males display alternative morphotypes, which differ in the expression of secondary sexual characters (SSC). Males expressing SSC, the M+ morphotype, have high androgen levels and compete for crevices that will be visited by females to spawn. M+ males holding nests court females and care for the eggs. Males with low expression of SSC, the M− morphotype, have low levels of androgens and reproduce by stealing fertilizations from the M+ males. Based on the hypothesis that androgens are immunosuppressive, we expected these morphotypes to differ in immunocompetence. To test this hypothesis, we conducted a field study in which we collected repeated blood samples to monitor leukocyte populations (blood smears), and to measure the primary antibody response of males that were experimentally challenged with a foreign non-pathogenic antigen (sheep red blood cells). Circulating levels of 11-ketotestosterone and testosterone were higher in M+ males than in M− males. Neither granulocyte nor thrombocyte counts did covariate with androgens or male tactic. In contrast, lymphocyte counts and humoral antibody response were negatively correlated with body size, and as expected, both were lower in M+ than in M− males. Interestingly, in M+ males androgen levels decreased after immunization, and this was less in nest-holder males than in M+ males that were floating around in the pools. Within each morphotype we found no relationship between androgens and immunocompetence. The latter result is not supportive for androgen regulated immunosuppression in M+ males. A possible alternative is enhancement of immunity in M− males. These males had relatively high levels of injuries in comparison with M+ males. High immunity might be a consequence of high infection rate because of such injuries.

Endocrine correlates of intra-specific variation in the mating system of the St. Peter's fish (Sarotherodon galilaeus).

The Challenge Hypothesis postulates that androgen levels are a function of the social environment in which the individual is living. Thus, it is predicted that in polygynous males that engage in social interactions, androgen levels should be higher than in monogamous animals that engage in parental care. In this study, we tested this hypothesis at the intra-specific level using a teleost species, Sarotherodon galilaeus, which exhibits a wide variation in its mating system. Experimental groups of individually marked fish were formed in large ponds with different operational sex-ratios (OSR) to study the effects of partner availability on blood plasma levels of sex steroids [11-ketotestosterone (11-KT), testosterone (T), and 17,20beta-dihydroxy-4-pregnen-3-one (17,20beta-P)] and gonadosomatic index (GSI). Polygyny mostly occurred in the female biased OSR groups. 17,20beta-P and gonadosomatic index did not differ among OSR groups. However, 11-KT was high in male biased OSR and positively correlated with aggressive challenges, thereby supporting the central postulate of the Challenge Hypothesis. The results of T were the inverse of those of 11-KT, probably because 11-KT is metabolized from T. 11-KT levels of polygynous males did not differ neither from those of monogamous males, nor from those of males that participated in parental care. These results do not support the expected relationships between polygyny, parental care, and androgen levels. The differences from expectations for 11-KT may be related to the fact that in S. galilaeus, the mating and the parenting phase are not clearly separated and thus, males may still fight and court while they are brooding.

Social context may affect urinary excretion of 11-ketotestosterone in African cichlids

Summary We previously investigated the androgen responsiveness of males to simulated partner and territory intrusions in five African cichlid species (Neolamprologus pulcher, Lamprologus callipterus, Tropheus moorii, Pseudosimochromis curvifrons, Oreochromis mossambicus; Hirschenhauser et al., 2004). Here we re-analysed data on 11-ketotestosterone (11-KT) levels in holding water to compare the free (presumably from the gills) and conjugated (presumably from urine and faeces) 11-KT fractions. We sampled (i) pre-test baseline control levels from individual males in social isolation and (ii) response levels released after social interactions, either with an ovulating female or a male territory intruder. In four out of five species, conjugated metabolites contributed to the observed total 11-KT responses in water during social context, which was particularly apparent in peak responsive individuals exposed to male intruders. Thus, in water from males sampled in isolation immunoreactive 11-KT seemed to derive both from gills and urine, whereas the urinary 11-KT component apparently increased in the social context, particularly when a male was challenged by a same-sex intruder. These results suggest that (i) the social context may affect urine release patterns of males and (ii) 11KT data acquired by using fish-holding water may not simply reflect the passive transmission of steroid hormones via the gills.