Elevated spring testosterone increases parasite intensity in male red grouse

The expression of testosterone-dependent sexual traits might signal the ability of their bearers to cope with parasite infections. According to the immunocompetence handicap hypothesis (IHH), such signals would be honest because physiological costs of testosterone, such as a reduced ability to control parasite infections, would prevent cheating. We tested whether testosterone would affect the outcome of a standardized parasite challenge in red grouse, using a main parasite of the species, the nematode Trichostrongylus tenuis. We caught males in spring, removed their nematode parasites, and implanted them with testosterone or empty implants, as controls. After 1 month, they were reinfected with a standard dose of infective T. tenuis parasites. When challenged, testosterone males had relatively less globulin relative to albumin plasma proteins than control males, an indication that they had experienced increased physiological stress. Testosterone-treated males had significantly more T. tenuis parasites than controls in the next autumn and also had more coccidia and lost more weight than controls. Testosterone-treated males nevertheless benefited from their elevated spring testosterone: they had bigger sexual ornaments than controls both in spring and autumn, and they tended to have a higher pairing and breeding success than controls. Our results supported the IHH in showing that elevated testosterone impaired the ability of males to cope with a standardized challenge by a dominant parasite. Testosterone thus plays a key role in mediating trade-offs between reproductive activities and parasite defense, and testosterone-dependent comb size might honestly signal the ability of red grouse to control T. tenuis infection.

Related papers:

title: Heritable true fitness and bright birds: a role for parasites?
abstract: Combination of seven surveys of blood parasites in North American passerines reveals weak, highly significant association over species between incidence of chronic blood infections (five genera of protozoa and one nematode) and striking display (three characters: male "brightness," female "brightness," and male song). This result conforms to a model of sexual selection in which (i) coadaptational cycles of host and parasites generate consistently positive offspring-on-parent regression of fitness, and (ii) animals choose mates for genetic disease resistance by scrutiny of characters whose full expression is dependent on health and vigor.

title: Parasites and sexual selection: Current status of the Hamilton and Zuk hypothesis
abstract: Hamilton and Zuk (1982) suggested that females could continuously base their choice of mates on heritable resistance to parasites, as generated in a process of coadaptational cycles of hosts and their parasites and advertized in terms of individual differences in plumage features or displays of the chosen sex. This hypothesis was based on three assumptions: (1) the full expression of secondary sexual traits of individual hosts is dependent on their overall health and vigour; (2) hosts are coevolving with their parasites, thereby continuously generating heritable resistance to parasites; and (3) parasites have negative effects on host viability. Given these assumptions one may then make the following intra‐ and interspecific predictions: (1) females will obtain mates with few or no parasites by choosing males with fully expressed sexual ornaments, (2) males with inferior ornaments will be less desirable partners and therefore take longer to become mated, (3) assortative mating occurs with respect to parasite loads, (4) females which mate with males with poorly developed secondary sexual characters will copulate outside their pair bond with males showing more fully expressed ornaments, and (5) in species especially vulnerable to parasite invasions, sexual selection will lead to more extreme development of health‐certifying traits, allowing females to more accurately assess the parasite load of a male. Here I shall evaluate the empirical evidence for these assumptions and predictions and discuss alternative hypotheses advanced, in order to explain the importance of parasites for the sexual selection theory. An open question not yet studied satisfactorily is whether, and how often, coadaptational cycles exist, and, if they exist, how they should affect mate choice.

title: Parasitism, Host Immune Function, and Sexual Selection
abstract: Parasite-mediated sexual selection may arise as a consequence of 1) females avoiding mates with directly transmitted parasites, 2) females choosing less-parasitized males that provide parental care of superior quality, or 3) females choosing males with few parasites in order to obtain genes for parasite resistance in their offspring. Studies of specific host-parasite systems and comparative analyses have revealed both supportive and conflicting evidence for these hypotheses. A meta-analysis of the available evidence revealed a negative relationship between parasite load and the expression of male secondary sexual characters. Experimental studies yielded more strongly negative relationships than observations did, and the relationships were more strongly negative for ectoparasites than for endoparasites. There was no significant difference in the magnitude of the negative effect for species with and without male parental care, or between behavioral and morphological secondary sexual characters. There was a significant difference between studies based on host immune function and those based on parasite loads, with stronger effects for measures of immune function, suggesting that the many negative results from previous analyses of parasite-mediated sexual selection may be explained because relatively benign parasites were studied. The multivariate analyses demonstrating strong effect sizes of immune function in relation to the expression of secondary sexual characters, and for species with male parental care as compared to those without, suggest that parasite resistance may be a general determinant of parasite-mediated sexual selection.

title: The Handicap Principle: A Missing Piece of Darwin's Puzzle
abstract: Ever since Darwin, animal behaviour has intrigued and perplexed human observers. The elaborate mating rituals, lavish decorative displays, complex songs, calls, dances and many other forms of animal signalling raise fascinating questions. To what degree can animals communicate within their own species and even between species? What evolutionary purpose do such communications serve? Perhaps most importantly, what can animal signalling tell us about our own non-verbal forms of communication? In The Handicap Principle, Amotz and Ashivag Zahavi offer a unifying theory that brilliantly explains many previously baffling aspects of animal signalling and holds up a mirror in which ordinary human behaviours take on surprising new significance. The wide-ranging implications of the Zahavis' new theory make it arguably the most important advance in animal behaviour in decades. Based on 20 years of painstaking observation, the Handicap Principle illuminates an astonishing variety of signalling behaviours in animals ranging from ants and ameba to peacocks amd gazelles. Essentially, the theory asserts that for animal signals to be effective they must be reliable, and to be reliable they must impose a cost, or handicap, on the signaller. When a gazelle sights a wolf, for instance, and jumps high into the air several times before fleeing, it is signalling, in a reliable way, that it is in tip-top condition, easily able to outrun the wolf. (A human parallel occurs in children's games of tag, where faster children will often taunt their pursuer before running). By momentarily handicapping itself-expending precious time and energy in this display-the gazelle underscores the truthfulness of its signal. Such signalling, the authors suggest, serves the interests of both predator and prey, sparing each the exhaustion of a pointless chase. Similarly, the enormous cost a peacock incurs by carrying its elaborate and weighty tail-feathers, which interfere with food gathering, reliably communicates its value as a mate able to provide for its offspring. Perhaps the book's most important application of the Handicap Principle is to the evolutionary enigma of animal altruism. The authors convincingly demonstrate that when an animal acts altruistically, it handicaps itself-assumes a risk or endures a sacrifice-not primarily to benefit its kin or social group but to increase its own prestige within the group and thus signal its status as a partner or rival. Finally, the Zahavis' show how many forms of non-verbal communication among humans can also be explained by the Handicap Principle. Indeed, the authors suggest that non-verbal signals-tones of voice, facial expressions, body postures-are quite often more reliable indicators of our intentions than is language. Elegantly written, exhaustively researched, and consistently enlivened by equal measures of insight and example, The Handicap Principle illuminates virtually every kind of animal communication. It not only allows us to hear what animals are saying to each other-and to understand why they are saying it-but also to see the enormously important role non-verbal behaviour plays in human communication.

title: Parasites, Bright Males, and the Immunocompetence Handicap
abstract: It has been argued that females should be able to choose parasite-resistant mates on the basis of the quality of male secondary sexual characters and that such signals must be costly handicaps in order to evolve. To a large extent, handicap hypotheses have relied on energetic explanations for these costs. Here, we have presented a phenomenological model, operating on an intraspecific level, which views the cost of secondary sexual development from an endocrinological perspective. The primary androgenic hormone, testosterone, has a dualistic effect; it stimulates development of characteristics used in sexual selection while reducing immunocompetence. This "double-edged sword" creates a physiological trade-off that influences and is influenced by parasite burden. We propose a negative-feedback loop between signal intensity and parasite burden by suggesting that testosterone-dependent signal intensity is a plastic response. This response is modified in accordance with the competing demands of the potential costs of parasite infection versus that of increased reproductive success afforded by exaggerated signals. We clarify how this trade-off is intimately involved in the evolution of secondary sexual characteristics and how it may explain some of the equivocal empirical results that have surfaced in attempts to quantify parasite's effect on sexual selection.

title: Avoiding the ‘Costs’ of Testosterone: Ecological Bases of Hormone-Behavior Interactions
abstract: A combination of laboratory and field investigations of birds has shown that expression of behavior such as territorial aggression can occur throughout the year in many species and in different life history stages. Although it is well known that testosterone regulates territorial aggression in males during the breeding season, the correlation of plasma testosterone and aggression appears to be limited to periods of social instability when a male is challenged for his territory by another male, or when mate-guarding a sexually receptive female. How essentially identical aggression is modulated in non-breeding life history stages is not fully resolved, but despite low circulating levels of testosterone outside the breeding season, expression of territorial aggression does appear to be dependent upon aromatization of testosterone and an estrogen receptor-mediated mechanism. There is accumulating evidence that prolonged high levels of circulating testosterone may incur costs that may potentially reduce lifetime fitness. These include interference with paternal care, exposure to predators, increased risk of injury, loss of fat stores and possibly impaired immune system function and oncogenic effects. We propose six hypotheses to explain how these costs of high testosterone levels in blood may be avoided. These hypotheses are testable and may reveal many mechanisms resulting from selection to avoid the costs of testosterone. It should also be noted that the hypotheses are applicable to vertebrates in general, and may also be relevant for other hormones that have a highly specialized suite of actions in one life history stage (such as breeding), but also have a limited action in other life history stages when the full spectrum of effects would be inappropriate.

title: Testing the immunocompetence handicap hypothesis: a review of the evidence
abstract: The immunocompetence handicap hypothesis was formulated 12 years ago in an attempt to offer a proximate mechanism by which female choice of males could be explained by endocrine control of honest signalling. The hypothesis suggested that testosterone has a dual effect in males of controlling the development of sexual signals while causing immunosuppression. Our purpose in this review is to examine the empirical evidence to date that has attempted to test the hypothesis, and to conduct a meta-analysis on two of the assumptions of the hypothesis, that testosterone reduces immunocompetence and increases parasitism, to ascertain any statistical trend in the data. There is some evidence to suggest that testosterone is responsible for the magnitude of trait expression or development of sexual traits, but this is by no means conclusive. The results of many studies attempting to find evidence for the supposed immunosuppressive qualities of testosterone are difficult to interpret since they are observational rather than experimental. Of the experimental studies, the data obtained are ambiguous, and this is reflected in the result of the meta-analysis. Overall, the meta-analysis found a significant suppressive effect of testosterone on immunity, in support of the hypothesis, but this effect disappeared when we controlled for multiple studies on the same species. There was no effect of testosterone on direct measures of immunity, but it did increase ectoparasite abundance in several studies, in particular in reptiles. A funnel analysis indicated that the results were robust to a publication bias. Alternative substances that interact with testosterone, such as glucocorticoids, may be important. Ultimately, a greater understanding is required of the complex relationships that exist both within and between the endocrine and immune systems and their consequences for mate choice decision making.

title: Signaling Health versus Parasites
abstract: The Hamilton‐Zuk hypothesis, that parasite‐host coevolution can maintain heritable variation in fitness, has inspired a very successful research program on sexual selection on signals of health. The immunocompetence handicap hypothesis was developed to provide a handicapping mechanism to stabilize the correlation between signals and health. In earlier articles, I showed that handicap signaling is a special case, not a general law that we can rely on to deduce relative costs across signalers of different quality at equilibrium. The essential requirement for reliable signaling is that higher‐quality signalers are more efficient; they get greater marginal fitness returns from an incremental increase in the signal. This does not undermine the Hamilton‐Zuk hypothesis or the immunocompetence mechanism, but it does raise doubts about a widespread assumption that is commonly used to test these hypotheses: that sexual selection on signals of health implies the choice of mates with the fewest parasites. Immunity and parasites might play a fundamental role in many biological signaling systems, but viability‐indicating traits are not necessarily parasite‐load‐indicating traits. Theory allows for the possibility that high‐quality big signalers have greater health and more parasites than low‐quality small signalers (and the data suggest that in many systems they do). This means that we cannot test the Hamilton‐Zuk hypothesis or the immunocompetence handicap hypothesis by counting parasites. More generally, we cannot understand sexual selection on signals of health by focusing on the viability costs of signals.

title: Steroid Hormones and Immune Function: Experimental Studies in Wild and Captive Dark‐Eyed Juncos (Junco hyemalis)
abstract: Monogamous and polygynous male songbirds generally differ in their breeding season profiles of circulating testosterone. Testosterone level spikes early in the breeding season of monogamists and then declines, but it remains high in polygynists. Male dark‐eyed juncos (Junco hyemalis) are socially monogamous and exhibit the usual pattern, but experimental maintenance of high testosterone throughout the breeding season alters normal behavior and physiology and affects various components of annual reproductive success but not overall annual success. Because stabilizing selection predicts that alteration of naturally existing phenotypes should reduce lifetime reproductive success, we asked whether prolonged testosterone exposure might impair immune function and perhaps thereby reduce life span. We assessed immune function in captive and wild male juncos that we treated with either testosterone‐filled or empty Silastic implants. Results indicate that prolonged elevation of testosterone suppresses antibody production in captive males and cell‐mediated immunity in wild males. Together these results suggest that testosterone‐treated males may be more susceptible to disease or parasitic infection. As earlier studies have shown, levels of corticosterone as well as testosterone are higher in testosterone‐treated males, so it is unclear whether the immune suppression we observed is due to testosterone’s direct effects on immunity or testosterone’s influence on glucocorticoid production. We discuss results in the context of recent hypotheses regarding life‐history theory and potential endocrine‐immune interactions.

title: A condition dependent link between testosterone and disease resistance in the house finch
abstract: Testosterone has recently been proposed as a link between male quality and health and the expression of sexual traits. We investigated the relationship between testosterone and measures of the individual condition and health of males in a natural population of house finches (Carpodacus mexicanus). We also conducted a captive experiment in order to test for the effects of testosterone on resistance to coccidia, which is a common parasite of house finches. Free-living males in better condition had higher testosterone levels and lower corticosterone levels than free-living males in poor condition. In our captive experiment, increased testosterone accelerated the rate of coccidial infection as compared with sham-implanted or gonadectomized males. Although the differences were not significant, free-living males infected with coccidia had lower levels of testosterone and higher levels of corticosterone than males that were not infected. Thus, experimentally elevating testosterone levels in captive males resulted in a higher percentage of infected males, while free-living males with coccidial infection had low testosterone levels. This apparent discrepancy between captive and free-living males in the association of testosterone and disease may be explained by the condition dependence of testosterone. These results suggest that the testosteronedependent sexual traits reliably indicate male overall condition and health and, thus, females could benefit from assessing potential mates based on these traits.

title: Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica

abstract: The immuno-competence hypothesis predicts that the expression of secondary sex traits should be positively related to testosterone levels, but that androgens should simultaneously have negative effects on the immune defence system. Relatively high levels of circulating androgens should therefore result in elevated levels of parasite infections. Parasite load and testosterone levels will be uncorrelated, or even negatively correlated, however, if males with high testosterone levels and large secondary sexual characters are reliable advertisers of genetic resistance to parasites. In male barn swallows, testosterone concentrations peaked during the pre-laying period. Males that had high levels of testosterone (adjusted for the stage of the breeding cycle) at one stage of the breeding cycle also had relatively high levels at other stages. The length of the outermost tail feathers, which are secondary sexual characters currently involved in sexual selection, was positively related to adjusted circulating levels of testosterone, even when potentially confounding variables were controlled statistically. The prevalence (proportion of hosts infected) and intensity (number of parasites per host individual) of ecto-parasites (two species of Mallophaga, one species of Acari) infecting barn swallows were unrelated to adjusted testosterone concentrations. Intensities of ecto-parasite infections were negatively related to tail length of male barn swallows, and unmated males had higher intensities of infections than mated males. These results are consistent with the immuno-competence version of the handicap principle.

title: Testosterone and male mating success on the black grouse leks
abstract: On black grouse (Tetrao tetrix) leks females prefer dominant, viable males that have managed to acquire relatively central territories. The immunocompetence hypothesis predicts that, because high levels of testosterone are costly to the immune system, male sexual traits that are controlled by testosterone are likely to serve as reliable indicators of male health. Indeed, testosterone concentrations of black grouse males were highly variable, and strongly correlated with male mating success. This is related to the fact that males with high testosterone levels had most central territories. However, the association of testostestorone level with male mating success was not solely related to centrality. Indeed, the particularly strong correlation suggests a possibility for an important role of the immunocompetence hypothesis in this lekking bird species.

title: Effects of testosterone on breeding density, breeding success and survival of red grouse
abstract: Territorial intolerance can limit bird numbers by preventing subordinates from holding territories and breeding. We report the first controlled and replicated experiment in a natural population of territorial animals which shows that population density can be decreased by implants of testosterone inducing increased aggressiveness. Implanted territorial cocks expanded their territories at the expense of unimplanted neighbours, some of which left the study area. The probability of an unimplanted cock leaving the study area increased with his number of implanted neighbours. Implanted cocks had better breeding success but poorer subsequent survival than control cocks.

title: Testosterone, dominance signalling and immunosuppression in the house sparrow, Passer domesticus
abstract: The immunocompetence handicap hypothesis (ICHH) suggests that dominance signals are costly because their development is controlled by testosterone, which is immunosuppressive. Signal control therefore links an increased disease risk with a high quality signal. The chest bib of the house sparrow, Passer domesticus, is a signal known to be related to dominance and under control of testosterone levels. We experimentally manipulated testosterone in male sparrows during the breeding season and again independently during the post-breeding period to test whether variation in levels of testosterone could cause variation in levels of immunocompetence. There was no effect of testosterone manipulation on the cell-mediated response of birds to phytohaemagglutinin injection, nor did testosterone levels appear to affect either white blood cell ratios or red blood cell counts. In contrast, both breeding season and post-breeding season testosterone levels had significant effects upon the humoral response of the birds to sheep red blood cell injections. However, whilst testosterone during the breeding season appeared to act immunosuppressively, the role of post-breeding levels is less clear. In concordance with a previous study, there was an indication that corticosterone is involved in mediating the immunosuppressive effects of testosterone. The strength of the secondary humoral response and the cell-mediated response were negatively related suggesting the possibility of a trade-off between the different arms of the immune system. These results provide some support for the ICHH as a mechanism promoting the evolution of costly badges of status, although the results question whether the immunosuppressive cost can be mediated by testosterone at the time of badge development.

title: The effects of testosterone on a viral infection in greenfinches (Carduelis chloris): an experimental test of the immunocompetence-handicap hypothesis
abstract: The immunocompetence–handicap hypothesis suggests that the honesty of quality signals could be guaranteed if testosterone (T) suppresses immune function while enhancing male ornaments. In addition, it has been proposed that the cost of enhancing ornaments should be highest for males with small ornaments. Recently, the assertion that T causes obligate immunosuppression has been questioned. In this study, we tested whether elevated T levels would increase susceptibility to a viral infection, and whether this hypothesized effect would be most pronounced in males with small ornaments. We surgically inserted T implants into 15 male greenfinches (Carduelis chloris) and control implants into a further 15 males. All birds were then infected with a naturally occurring virus (Sindbis virus, Alphavirus genus), and each bird's daily viraemia (blood virus concentration) was measured for seven days. The specific antibody response was measured for eight weeks. T–implanted males did not exhibit increased viraemia or decreased antibody response, and males with small and large ornaments did not respond differently to T implantation. We did, however, find that T implantation decreased viraemia early in the course of the infection and increased viraemia late in the infection. Thus, our results demonstrate that T may act both to increase and to decrease viraemia.

title: Testosterone treatment is immunosuppressive in superb fairy–wrens, yet free–living males with high testosterone are more immunocompetent
abstract: The immunocompetence handicap hypothesis proposes that the immunosuppressive effect of testosterone enforces honesty of sexual signalling via a physiological trade–off between signal intensity and immuno–competence. However, evidence that testosterone is immunosuppressive is scant, particularly in birds. I studied the correlation between immunocompetence and testosterone in superb fairy–wrens (Malurus cyaneus), a species with intense intersexual selection. Males are seasonally dichromatic and testosterone increases during the moult from dull brown eclipse plumage into bright nuptial plumage. I determined the primary antibody response to immunization with sheep red blood cells (SRBCs) in (i) control and testosterone–implanted males in captivity, and (ii) a cross–section of free–living males with basal and elevated testosterone (in eclipse plumage, moulting and in nuptial plumage). Experimental treatment with testosterone decreased the likelihood of an antibody response to SRBCs in captive birds. In contrast, free–living males which had acquired the nuptial plumage and had naturally elevated testosterone were more likely to respond to SRBCs than males in eclipse plumage with basal testosterone levels. The association between higher immunocompetence and higher immunosuppressive testosterone could arise if both are positively correlated with male phenotypic quality. In addition, the association could result if males compensate for potential immunosuppression by enhancing their humoral immune responses, particularly since high testosterone is linked to other demanding activities such as moulting and courtship displays.

title: Is avian humoral immunocompetence suppressed by testosterone?
abstract: A key issue in sexual selection theory is how a correlation between male secondary sexual characters and male genetic quality can be maintained. The immunocompetence-handicap hypothesis proposes that testosterone-dependent male characters remain honest signals because of the immunosuppressive effect of elevated steroid hormone levels. The hypothesis requires that physiological levels of testosterone depress immune system function. We quantified testosterone titers and humoral immunocompetence of captive male and female red-winged blackbirds (Agelaius phoeniceus) at three points in the annual cycle (autumn, prebreeding, and breeding). We also conducted an implant experiment on the males to assess the effects of prolonged, above-normal testosterone titers on humoral immune responses. Humoral immunocompetence was measured as secondary antibody production to a non-pathogenic protein antigen, keyhole limpet hemocyanin, using an enzyme-linked immunosorbent assay we developed for A. phoeniceus. Secondary antibody responses of individuals were highly repeatable between sampling periods. Neither physiological nor above-normal levels of plasma testosterone suppressed secondary antibody production. In paired tests of the same individuals between prebreeding and breeding, and between breeding and implant, plasma testosterone increased significantly but secondary antibody responses were unaffected. We are confident in these results because with 80% power, an 11–14% difference in antibody titers would have been detected. There was no relationship between plasma testosterone levels and humoral immunocompetence in free-ranging males tested at the peak of breeding. These results cast doubt on a key assumption of the immunocompetence-handicap hypothesis.

title: The Relation Among Gonadal Steroids, Immunocompetence, Body Mass, And Behavior in Young Black‐Headed Gulls (Larus Ridibundus)
abstract: 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.

title: Social class, socially-induced loss, recruitment and breeding of red grouse
abstract: SummaryIndividually marked red grouse (Lagopus lagopus scoticus) could be distinguished as territorial or non-territorial from November till the next spring. Territorial birds survived well and many reared young, but numerous nonterritorial birds died or disappeared, and none paired up or reared young. Differences in spring sex ratio between years had already been set in the previous autumn's territorial stock. Many old birds which had been territorial in earlier seasons lost territories after an annual re-distribution of territory each October–November. Thereafter very few of them were seen alive on the area over the winter, and many were found dead, whereas nearly all old birds that kept their territories were still there in spring. The number of birds in spring and the fate of individuals over winter were predicted reasonably accurately from observations of behaviour in the previous November–December. Thus, differences of social class in autumn were critical to a bird's survival to breed in the next summer and to its chances of contesting for territory and breeding in subsequent years.

title: The energetic consequences of parasitism: effects of a developing infection of Trichostrongylus tenuis (Nematoda) on red grouse ( Lagopus lagopus scoticus ) energy balance, body weight and condition
abstract: The timing of the energetic consequences of a developing, single-dose infection of Trichostrongylus tenuis larvae was investigated in captive red grouse Lagopus lagopus scoticus . At 12 days post-infection (p.i.), infected birds had a resting metabolic rate 16% greater than controls and thenceforth lost weight at a faster rate than controls. At 16 days p.i. infected birds consumed 38% less energy and excreted 33% less energy than controls. The estimated total daily energy expenditure and energy expended on activity for infected birds at 16 days p.i. were 36% and 83% lower, respectively, than for controls. Infected birds lost condition from 16 days p.i. onwards. The period of energy imbalance at 12–16 days p.i. coincided with development of late 4th-stage larvae into adult worms and the onset of patency. After this, the effects on energy balance diminished. Synchronous development of previously arrested T. tenuis larvae in wild birds in spring probably has similar effects to those reported here and places grouse under conditions of energy imbalance. The observed effects on energy balance provide a possible mechanism by which the parasite can reduce fecundity and survival of infected grouse.

title: Regulation and stability of a free-living host-parasite system : Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments
abstract: Intensive population studies were conducted for 10 years on red grouse (Lagopus lagopus scoticus) and the parasitic nematode, Trichostrongylus tenuis, in northern England. Winter loss was the key factor determining changes in grouse numbers, although breeding losses were also important. T. tenuis had an aggregated distribution within the adult grouse population, even though the degree of aggregation was relatively low compared with other parasite systems

title: Effects of the caecal nematode Trichostrongylus tenuis on egg-laying by captive red grouse.
abstract: Captive hen red grouse infected with Trichostrongylus tenuis larvae started to lay later in spring and laid fewer eggs at a slower rate than uninfected hens. March-infected hen grouse showed greater effects than December-infected ones, probably because developing larvae were more pathogenic than adult worms. The mechanism by which parasites interfered with egg production involved reduction in food intake. Infected hens also gained less weight than controls before laying.

title: Aggressiveness and dominance in captive cock red grouse
abstract: A method for measuring the aggressiveness of captive cock red grouse is described. A cock's aggressiveness varied according to season, type of cage and social environment. A method for ranking the dominance order of cocks in a group is also described. Dominance ranks remained stable for up to two years. Correlations between the aggressiveness of isolated cocks and their dominance ranks when in a group were positive but weak. Aggressiveness and dominance should be clearly distinguished. Both aggressiveness and dominance were related to the size of cock's combs, and implants of testosterone increased all three. In situations where a cock's aggressiveness changed, comb size changed in the same direction. The aggressive behaviour of captive cocks shows several major parallels with that of wild cocks.

title: Testosterone and autumn territorial behavior in male red grouse Lagopus lagopus scoticus

abstract: In many bird species, males exhibit territorial aggression outside the breeding season, when testosterone concentrations are low and may not regulate territorial behaviors. The hormonal regulation of aggression at this time of year has only been studied in passerine birds. Here, we investigated the role of testosterone in the regulation of aggression in a non-passerine bird, the red grouse Lagopus lagopus scoticus. Male red grouse are aggressive in early spring when breeding starts, in autumn when they establish territories, and sporadically through much of the winter. We first describe seasonal variations in plasma testosterone concentrations and in the size of males' sexual ornaments, their red combs, which relates to aggressiveness. Testosterone concentrations and comb size were correlated. Both increased in autumn to a peak in October, and then increased again in spring, to a greater peak in early April. Secondly, we experimentally investigated the effects of testosterone, and of an anti-androgen (flutamide) used in combination with an aromatase inhibitor (ATD), on autumn territorial behavior. Males were treated with either empty implants, as controls (C-males), testosterone implants (T-males), or with flutamide and ATD implants (FA-males). One month after implanting, both T- and FA-males had higher concentrations of testosterone than C-males. Comb size, aggressive call rate, and response to playbacks of territorial call all significantly increased in T-males. However, the increase in testosterone in FA-males did not increase comb size or aggressive behavior. In the following spring, after the content of implants was used, FA-males had significantly lower testosterone than C-males, and had a reduced seasonal increase in comb size. The results suggest that testosterone plays a significant role in regulating red grouse aggressive behavior in autumn. However, the observation that flutamide and ATD treatment did not reduce territorial behavior, suggests that estradiol may also be involved in the regulation of non-breeding aggression.

title: Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus)
abstract: We studied pairing success in male rock ptarmigan (Lagopus mutus) in northern Alaska to learn whether males obtaining more females possessed phenotypic traits that influenced female choice directly, whether these traits permitted males to obtain territories favored by females, or whether both processes occurred. The number of females per male varied from zero to three. Several male and territory traits were significantly correlated with number of females per male. We used multiple regression to obtain a single measure of male quality and a single measure of territory quality. These measures of male and territory quality correlated with each other and with male pairing success. We used path analysis to separate direct effects of male quality on pairing success from indirect effects due to high-quality males obtaining high-quality territories. Both direct and indirect pathways had significant effects on pairing success, and direct and indirect effects of male traits on pairing success were about equal. This study illustrates an analytical approach for estimating the relative importance of direct and indirect causal relationships in natural systems.

title: Combs and sexual selection in black grouse (Tetrao tetrix)
abstract: We studied supra-orbital combs in lekking black grouse (Telrao tetrix) in relation to sexual selection at five leks in Finland 1991-1998 and four leks in Sweden 1992-1995. Comb size was estimated in two ways: by observing its natural size in the field at

title: Transmission dynamics and host-parasite interactions of Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus).
abstract: Two components of the transmission dynamics of Trichostrongylus tenuis in red grouse are examined and quantified, namely parasite transmission rate and density-dependent reductions in egg production. Age-intensity data for birds of known age suggest that the rate of parasite uptake increases during the first 6 mo of a bird's life and this increase reflects an increase in feeding rate with age and exhibits no signs of self-cure. Analysis of these age-intensity curves permits us to estimate the transmission rate of the free-living infective stages. Reinfection rates of adults treated to reduce parasite intensities were not significantly different from infection rates of naive immature grouse. Secondary infections continued to rise over a period of 18 mo and this suggests that there is no strong host-mediated response against the parasite. Any density-dependent reduction in parasite fecundity is probably very weak and would act through interspecific competition between parasites. Initial analysis of worm egg production in relation to the intensity of worm infection found weak evidence of density-dependent suppression of egg production at high worm intensities. However, a more rigorous analysis found that such a relationship suffered from Type I errors and was a consequence of the aggregated distribution of the parasites. Any density-dependent suppression of parasite egg production is too weak to be detected and would only occur at high worm intensities. The potential density-dependent reductions in fecundity on the population dynamics of T. tenuis and red grouse are examined using a mathematical model. The model suggests that the presence of density-dependent reductions in worm fecundity could produce significant reductions in the propensity of the grouse-nematode system to exhibit population cycles. The sustained cycles observed in the long-term dynamics of the grouse populations in the study area suggest that density-dependent reductions in worm fecundity and establishment are either absent or only operating at levels that are not detectable in field studies.

title: Caecal threadworms Trichostrongylus tenuis in red grouse Lagopus lagopus scoticus: effects of weather and host density upon estimated worm burdens.
abstract: Trichostrongylus tenuis eggs were counted in faeces from individually marked wild red grouse for 8 years. Egg counts varied seasonally and annually. In some years, a sudden increase in mid-April was consistent with delayed maturation of larvae which had overwintered in the birds in a hypobiotic state. A more gradual increase in summer was probably due to uninterrupted maturation of larvae ingested then. Despite 30-fold year-to-year variation in mean egg counts, relative differences in egg counts among known individuals within years tended to persist across years. Rainfall in previous summers explained much of the year-to-year variation in egg counts, probably because parasite recruitment was greatest during wet summers. Grouse density was only weakly related to worm egg counts. The data were not consistent with the hypothesis that the cyclic-type population fluctuation in red grouse numbers observed at the time of this study was caused by the parasites.

title: Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation
abstract: 1. A cornerstone concept of ecological immunology is that immune function, interacting with various aspects of individual health state, plays a central role in the life-history trade-offs between conflicting demands of survival and reproduction. In order to develop this research, more knowledge about the applicability and usefulness of different health state assays is needed.

2. Eleven, mostly hemato-serological, health state indices are described and their suitability for sensing the condition of breeding Great Tits (Parus major L.) in terms of measurement precision, constancy in time, diurnal variation, and sex- and site-related differences, is examined.

3. Measurement errors for the plasma albumin content, residual body mass, heterophile/lymphocyte ratio and total plasma protein content were relatively small compared with the total variation, suggesting these indices to be most adequate for ecological research. Measurement precision was lowest for the heterophile count and ‘buffy coat’ layer height (relative amount of leucocytes in total blood volume). Buffy coat layer height correlated weakly (r=0·21) with total leucocyte count estimated from blood smears and therefore appeared inappropriate for estimation of the leucocyte number.

4. Body mass (residual in respect to size) and intensity of Haemoproteus blood parasite infection were the least variable state indices during the nestling period (for both, the correlation between the values measured on the 8th and 15th days of the nestling period=0·71). Haematocrit, heterophile count and albumin/globulin ratio showed no individual constancy across the nestling period, while other traits revealed moderate but statistically significant correlations between 8th- and 15th-day values.

5. Leucocyte (both lymphocyte and heterophile) counts were higher among females captured at night compared with those captured during the day.

6. Females had higher intensities of Haemoproteus infection, higher heterophile counts and higher heterophile/lymphocyte ratios than males. Contrary to published information, females had higher haematocrits than males.

7. Haematocrit values in both sexes, as well as total plasma protein and albumin concentrations in males, differed significantly between Great Tits breeding in urban habitat and rural woodlands, respectively.

title: Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse
abstract: The causes of population cycles fascinate and perplex ecologist. Most work have focused on single processes, whether extrinsic or intrinsic, more rarely on how different processes might interact to cause or mould the unstable population dynamics. In red grouse (Lagopus lagopus scoticus), two causal mechanisms have been supported: territorial behaviour (changes in autumn aggressiveness) and parasites (parasite induced reduction in fecundity). Here, we report on how these two regulatory processes might interact, by testing whether the parasite suspected to cause the grouse cycles, the nematode Trichostrongylus tenuis, reduces male autumn territorial behaviour. We either treated males with an anthelmintic, to remove parasites (dosed or D-males), or challenged them with infective T. tenuis larvae, to increase parasite intensity (challenged or C-males). We first show that dosing was effective in removing T. tenuis parasites, while parasite intensities increased in challenged birds during the autumn. Because old males initially had more parasites than young males, the treatments generated greater differences in parasite intensity in old than in young males. We also show that various aspects of territorial behaviour (increase in testosterone-dependent comb size in autumn, territorial call rate, likelihood of winning territorial interactions and over-winter survival) were significantly higher in dosed than in challenged males, but in old birds only. Our data thus supported the hypothesis that parasites reduce male aggressiveness during the autumn territorial contests, and could thereby influence recruitment. Our results also highlight that the territorial behaviour of young males, which have fewer parasites, is not as limited by parasites as that of old, previously territorial males. We discuss the implications of these findings for our understanding of the processes regulating red grouse populations and causing their complex, unstable population dynamics.

title: Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus
abstract: The reliability of different egg counting methods for estimating the intensity of Trichostrongylus tenuis infections in red grouse, Lagopus lagopus scoticus, was investigated in the autumn, when grouse may harbour high parasite intensities. Possible limitations to the use of these methods were also examined. Faecal egg counts were found to accurately estimate T. tenuis worm intensities, at least up to an observed maximum of c. 8000 worms. Two egg counting methods (smear and McMaster) gave consistent results, although the exact relationship with worm intensity differed according to the method used. Faecal egg counts significantly decreased with increasing length of sample storage time, but egg counts were reliable for estimating worm intensity for three weeks. The concentration of eggs in the caecum was also found to reliably estimate worm intensity. However, egg counts from frozen gut samples cannot be used to estimate worm intensities. These results conclude that, despite some limitations, faecal and caecum egg counts provide useful and reliable ways of measuring T. tenuis intensities in red grouse.

title: Temporal variation in shedding of coccidial oocysts : implications for sexual-selection studies
abstract: Studies of the effects of parasites on the sexual ornamentation and behavior of animals are becoming increasingly common. A potential difficulty in many studies of this type is the accurate assessment of parasite prevalence within a population and of the parasite burden of individual hosts. We present data that illustrate how a simple factor such as the time of day at which samples are collected can drastically alter the results of parasite assessments. House finches (Carpodacus mexicanus) infected with coccidians of the genus Isospora shed oocysts in their feces predominantly during the late afternoon. The importance of recognizing such circumstances (e.g., diurnal periodicity) is discussed in the light of possible negative effects on studies of host-parasite relationships.

title: Effects of Time of Sampling on Oocyst Detection and Effects of Age and Experimentally Elevated Testosterone on Prevalence of Coccidia in Male Dark-eyed Juncos
abstract: The hormone testosterone (T) has been linked to enhanced expression of secondary sexual traits and acquisition of mates (Ligon et al. 1990, Alatalo et al. 1996, Raouf et al. 1997). However, high plasma levels of testosterone also have been suggested to suppress immune function (Folstad and Karter 1992, Zuk et al. 1995, Hillgarth and Wingfield 1997; but see Ros et al. 1997, Hasselquist et al. 1999). Thus, an obvious question is whether testosterone enhances reproductive success while simultaneously affecting susceptibility to disease. In the Dark-eyed Junco (Junco hyemalis), experimental maintenance of plasma testosterone levels at their natural early season peak for the entire breeding season causes males to sing more frequently, and testosterone-treated males (T-males) in captivity are more attractive to females than are control males (Cmales; Enstrom et al. 1997, Hill et al. 1999). However, T-males also have elevated plasma levels of the steroid hormone corticosterone (Ketterson et al. 1991, Klukowski et al. 1997) and show a greater response to handling stress than do C-males (Schoech et al. 1999), which can translate into suppressed immune function (Sapolsky 1992, Besedovsky and del Rey 1996, J. Casto pers. comm.). To investigate possible effects of elevated levels of plasma testosterone on the junco’s susceptibility to disease, we asked whether free-living males treated with testosterone would be more likely than controls to be infected by coccidia (Isospora spp.), a protozoan gut parasite belonging to the Eimeria complex. We also asked whether yearling juncos were more likely than older adults to be infected and whether our ability to detect infection was affected by the time of day when fecal samples were collected. Methods.—This research was conducted at the University of Virginia’s Mountain Lake Biological Station (378229N, 808329W; see Chandler et al. [1994] for description of study area). We captured male juncos in mist nets and Potter traps during the early spring of 1995 and 1996 and classified them as second year (younger) and after second year (older) based on

title: Haematology, weight and condition of captive red grouse (Lagopus lagopus scoticus) infected with caecal threadworm (Trichostrongylus tenuis).
abstract: Red grouse infected with the caecal threadworm Trichostrongylus tenuis developed a mild anaemia. Haemoglobin and albumin levels in the blood fell but there were no significant changes in the number of red blood cells or their size. In infected birds the numbers of circulating eosinophils and heterophils increase, as did the concentration of alpha, beta and gamma globulin. Body weights did not change but muscle masses shrank. Birds that subsequently died had the lowest concentration of haemoglobin and packed cell volumes and the highest counts of eosinophils. The survivors were affected little by worms and their haematology showed small deviations from normal.

title: Host-parasite evolution: general principles and avian models.
abstract: Chapter 1 - Introduction. Part I: General Principles. Chapter 2 - Parasite-mediated natural selection. Chapter 3 - Immune defence: genetic control. Chapter 4 - Behavioural defence. Chapter 5 - Parasite-mediated sexual selection: endocrine aspects. Chapter 6 - Parasitism and the evolution of host life history. Chapter 7 - Host-parasite processes and demographic consequences. Chapter 8 - The role of parasites in bird conservation. Chapter 9 - Community ecology of parasites and free-living animals. Chapter 10 - Comparative studies of host parasite communities. Chapter 11 - Host-parasite cospeciation: history, principles and prospects. Chapter 12 - Host-parasite cospeciation, host switching and missing the boat. Part II: Avian Models. Chapter 13 - Birds as habitat for parasites. Chapter 14 - Viruses, bacteria and fungi of birds. Chapter 15 - Protozoa, helminths and arthropods of birds. Chapter 16 - Avian brood parasites. Chapter 17 -  Evolution of host-parasite interactions

title: Factors affecting the establishment of the caecal threadworm Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus).
abstract: The resistance of captive reared red grouse to Trichostrongylus tenuis was measured as the proportion of ingested infective 3rd-stage larvae which failed to develop to adult worms. Individual grouse showed wide, repeatable variations in resistance. Seasonal variations may also have occurred. Red grouse acquired little or no effective immunity to reinfection after challenge with a single dose of infective larvae. In trickle-dosed grouse, however, adult worms weakly inhibited the establishment of incoming larvae in an intensity-dependent fashion. Despite this, the proportion of larvae established in trickle infections was similar to that in single-dose challenges.

title: Separating Behavioral and Physiological Mechanisms in Testosterone‐Mediated Trade‐Offs
abstract: Testosterone often mediates trade‐offs between reproduction and other life‐history traits, which are usually investigated using testosterone implants. However, this approach does not distinguish between the physiological and behavioral effects of testosterone. We studied a wild game bird, the red grouse Lagopus lagopus scoticus, and took a new approach to investigate mechanisms linking elevated testosterone to increased parasite intensity. We caught males in autumn, removed their parasites, implanted them with the antiandrogen flutamide in combination with an aromatase inhibitor (FA males) or with empty implants (control males), and challenged them with parasites. The FA treatment increased testosterone concentration and physiological stress, but without enhancing testosterone‐dependent behaviors, because testosterone receptors were blocked. FA males ended up with more parasites than the control males the following autumn, an effect similar to that of a testosterone treatment reported elsewhere. However, and unlike the testosterone treatment, the FA treatment did not affect home range, pairing, or breeding success. The results supported a physiological mechanism (increased susceptibility) linking elevated testosterone and increased parasite intensity. The FA treatment provided a new way of investigating testosterone‐mediated trade‐offs whereby testosterone concentration was increased while the effects on behavior were blocked, resulting in physiological costs without phenotypic benefits.

title: The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus)
abstract: Many bird species have patches of colour in their plumage, contrasting with their basic coloration, which are used to display and signal status to conspecifics. These are called ’badges of status’, because they are believed to be low-cost signals of social status. For a signalling system to be evolutionarily stable, cheating must be controlled. The conventional view is that there is frequent testing, which uncovers cheats. Recently, the immunocompetence handicap hypothesis (ICHH) suggested that signals may be dependent on testosterone for their development, with a cost being imposed through immune suppression. We report experiments on house sparrows (Passer domesticus) which show that testosterone significantly influences the size of the bib (a ’badge of status’). The ultimate effect of the testosterone manipulation was to impair antibody production, as predicted by the ICHH. However, testosterone manipulations also changed the levels of the ’stress hormone’ corticosterone. The level of corticosterone was also related to the degree of immunosuppression. After controlling for the effect of corticosterone, testosterone enhanced the birds’ ability to produce antibodies, counter to the ICHH. The hypothesis therefore must be modified. We suggest that testosterone has a dual effect: it leads to immunosuppression through a mechanism involving corticosterone but, conversely, leads to increased immunocompetence probably via dominance influencing access to resources.

title: Androgens and the Immunocompetence Handicap Hypothesis: Unraveling Direct and Indirect Pathways of Immunosuppression in Song Sparrows
abstract: The immunocompetence handicap hypothesis proposes that testosterone (T)‐dependent sexual signals are honest indicators of male health or genetic quality because only high‐quality males are able to withstand the obligate effects of T‐induced immunosuppression. In birds, the basic assumption that T suppresses immune function is equivocal, and the physiological mechanisms underlying T‐induced immunosuppression remain to be investigated. We explored the proximate pathways of T‐induced immunosuppression in song sparrows (Melospiza melodia) by treating captive nonbreeding males with different androgens and measuring several components of acquired immune function. Males implanted with T suppressed cell‐mediated and humoral immune responses compared to males implanted with 5∝‐dihydrotestosterone (DHT), dehydroepiandrosterone, or control (empty) implants. Furthermore, T treatment increased plasma levels of corticosterone and decreased body mass and fat stores in relation to other treatments. The failure of DHT to depress immune function suggests that T‐induced immunosuppression does not occur through a direct pathway because both T and DHT bind to androgen receptors on target cells. Instead, we outline indirect pathways that are likely responsible for suppression of the avian immune system that include stress‐induced immunosuppression, aromatization to estrogen, and alterations in energy allocation that constrain expenditures toward immune system activation.

title: Testosterone increases the transmission potential of tick-borne parasites
abstract: Using laboratory-bred natural rodent hosts that had been castrated and then implanted with either testosterone or inert oil, we have shown that testosterone causes prolonged and more intense infections of a tick-borne piroplasm, Babesia microti. This will result in more ticks becoming infected while feeding. Sexually active male rodents with high testosterone levels are also known to show increased locomotory activity and reduced innate and acquired resistance to tick feeding, so that more ticks are likely to be picked up and then fed successfully by these hosts. As a result, the transmission potential of B. microti is significantly increased via hosts with high rather than low testosterone levels. It is argued that testosterone helps to generate the observed aggregated distributions of parasites amongst their hosts, which also enhances parasite persistence.

title: Disease, Endocrine‐‐Immune Interactions, and Sexual Selection
abstract: Parasites and disease have been increasingly recognized as agents of eco- logical and evolutionary importance. Because the endocrine and immune systems are re- lated, it is also likely that hormonally controlled traits, such as secondary sexual characters, may be influenced by responses to disease. Testosterone appears to be associated with a suppressed immune system in many vertebrates, and evidence from captive Red Jungle Fowl suggests that the sexes differ in blood parameters involved in immunity and that comb length is negatively correlated with lymphocyte number in males. Immune system parameters may provide a useful gauge of condition in captive and field-caught animals.

title: Testosterone affects reproductive success by influencing extra–pair fertilizations in male dark–eyed juncos (Aves: Junco hyemalis)
abstract: Monogamous male birds typically allocate less effort to courtship and more to parental behaviour than males of polygynous species. The seasonal pattern of testosterone (T) secretion varies accordingly. Monogamous males exhibit a spring peak in plasma T followed by lower levels during the parental phase, while males of polygynous species continue to court females and maintain T at higher levels. To determine whether testosterone underlies the trade–off between mating and parental effort, we treated male dark–eyed juncos (Junco hyemalis) with exogenous T and compared the reproductive success (RS) of T–treated males (T–males) to that of controls. T–males had lower apparent annual RS than controls, probably because elevated T reduced parental care. Nevertheless, annual genetic RS of the treatment groups was similar because (i) T–males suffered fewer losses in genetic RS due to extra–pair fertilizations (EPFs), and (ii) T–males gained more genetic RS through their own EPFs. This is the first hormonal manipulation of an avian phenotype shown to have influenced male RS through EPFs. Together with other studies, it suggests that testosterone may have mediated the evolution of inter– and intraspecific differences in allocation of reproductive effort to mate attraction and parental care.

title: Territory size and polygyny in the spotless starling: resource-holding potential or social inertia?
abstract: In male birds that base their acquisition of mates on the defence of resources essential for female reproduc - tion, the size or quality of the territory decisively affects polygyny rate and breeding success. However, there is contra - dictory evidence concerning the importance of resource-holding potential (RHP) versus factors not related to individual quality on between-year consistency in territory occupancy and hence on long-term reproductive success. We manipu- lated the aggressiveness (a major determinant of RHP) of male spotless starlings (Sturnus unicolor) by means of andro- gens and antiandrogens to investigate the importance of RHP in breeding-territory acquisition and maintenance, polygyny rate, and breeding success over 3 years (1996-1998). The number of males that held a territory for the first time was high in 1996 with respect to the year before the experiment began. Most of these males still bred in the col- ony during the third study year, though new owners established territories to the detriment of the former males, espe - cially in 1998. Manipulation of testosterone activity during the first year affected the number of nest boxes defended by males and also the number of mates gained and the number of successful breeding attempts made throughout the 3 study years. The results were in the expected direction: an increase in testosterone activity led to greater success. The results suggest that RHP may be important in the acquisition of territory and mates, at least under conditions of re- cently established interindividual relationships. However, social inertia, i.e., the maintenance of dominance status irre- spective of changes in RHP, seems to be of crucial importance in the long-term maintenance of territory resources and polygyny rates.

title: The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies
abstract: A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions. Furthermore, evidence from other vertebrate taxa suggests strongly that the model is applicable to other classes

title: Spatial arrangement of kin affects recruitment success in young male red grouse
abstract: Models have shown that population cycles might be driven by time lags resulting from positive feedback between kin structure and population change, coupled with negative feedback between density and population change. One such model operates through kin favouritism facilitating the recruitment of young cock red grouse. We investigated whether recruitment by young cocks depended on the presence and spatial arrangement of elder relatives in the territorial population. We used molecular genetic estimates of relatedness, and checked for effects of covariates including natal territory size, hatching date, body size, parasite burdens and local density. Philopatric recruitment by cock red grouse led to the formation of clusters of contiguous territories owned by kin. The probability that an individual young cock would establish a territory increased with the number of kin in his father's cluster. This pattern might have been due to genetic quality determining both recruitment success and the size of the paternal cluster. If so, there should have been a positive correlation between a young cock's probability of recruitment and the number of his relatives in the population, irrespective of their spatial distribution. This did not occur and so the effect of cluster size is unlikely to have been confounded by genetic quality. The only morphological measure correlated with recruitment success was supraorbital comb size. The results are consistent with the prediction that kin tolerance affects recruitment but were at the level of the individual within years, rather than the population among years. Hence an experimental test of the kin favouritism hypothesis for population cycles, by manipulation of relatedness in populations among years, is now required.

title: Ornament size influences mating success in male rock ptarmigan
abstract: Factors influencing male mating success in a natural population of rock ptarmigan, Lagopus mutus , were examined. In the first year of study, 1984, a survey of mating patterns revealed bigamous, monogamous and bachelor males in the population. In that year, males with the largest supraorbital combs had the most mates. After males were paired in 1984, they were captured and banded with a unique sequence of coloured leg bands for future identification. The following year, returning males with combcoloured bands were more successful at obtaining mates than were males with similar comb size but without these band colours. These results suggest that among rock ptarmigan, the comb is a target of sexual selection and that a novel, non-genetic trait, when similar in colour to the target, can also influence a male's mating success.

title: Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)
abstract: In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season.

title: The effect of aggressiveness on the population dynamics of a territorial bird
abstract: A central issue in ecology lies in identifying the importance of resources, natural enemies and behaviour in the regulation of animal populations. Much of the debate on this subject has focused on animals that show cyclic fluctuations in abundance. However, there is still disagreement about the role of extrinsic (food, parasites or predators) and intrinsic (behaviour) factors in causing cycles. Recent studies have examined the impact of natural enemies, although spatial patterns resulting from restricted dispersal or recruitment are increasingly recognized as having the potential to influence unstable population dynamics. We tested the hypothesis that population cycles in a territorial bird, red grouse Lagopus lagopus scoticus, are caused by delayed density-dependent changes in the aggressiveness and spacing behaviour of males. Here we show that increasing aggressiveness experimentally for a short period in autumn reduced recruitment and subsequent breeding density by 50%, and changed population trajectories from increasing to declining. Intrinsic processes can therefore have fundamental effects on population dynamics.