Abstract: Handicap models link the evolution of secondary sexual ornaments to physiological costs and thus provide a mechanistic explanation for signal honesty in sexual selection. Two commonly invoked models, the immunocompetence handicap hypothesis (ICHH) and the oxidative stress handicap hypothesis (OSHH), propose suppression of immunocompetence or increase of oxidative stress by testosterone, but empirical evidence for both models is controversial and based on morphological and physiological assays. Here, we investigated these two models on the gene transcription level using microarrays to quantify the transcriptomic response of red grouse (Lagopus lagopus scoticus) caecal, spleen and liver tissues to experimental manipulation of testosterone levels. We used a geneontology framework to identify genes related to immune function and response to reactive oxygen species and examined how transcription levels changed under experimentally increased testosterone levels in birds with parasites present or absent. Contrary to our expectations, testosterone had virtually no effect on gene transcription in spleen and liver. A small number of genes were significantly differentially regulated in caecum, and while their functions and transcription changes are consistent with the ICHH, we found little support for the OSHH. More genes responded to testosterone in the presence rather than absence of parasites, suggesting that handicap mechanisms may be context dependent and more pronounced in the presence of adverse environmental conditions. These findings illustrate the utility of transcriptomics to investigating handicap models, suggest that classic models may not underlie the handicap mechanism, and indicate that novel emerging models involving different mediators and physiological systems should be examined.
Abstract: Sexually mature young males of many dichromatic species begin breeding while expressing female-like or incomplete adult phenotypes, which contradicts sexual selection theory. It is thought that by delaying the acquisition of adult appearance, young males may avoid aggression from other males, but reduce mating opportunities, resulting in trade-offs between these 2 life-history traits. Thus, an optimal young male phenotype should allow mating while reducing aggressiveness. Differential character maturation (i.e., the acquisition of adult appearance does not occur in all traits at the same time) has been described in bird species, but has largely been neglected in the study of delayed plumage maturation. Using the common kestrel Falco tinnunculvs, we tested the prediction that maturation of different adult traits depends on the aggressiveness elicited by both male and female individuals and that young male phenotypes should be a combination of traits triggering low levels of aggressiveness while still revealing sex. We explored the pattern of delayed plumage maturation observed in 4 different adult male traits (head, rump, tail, and back plumages) in young breeding males captured over 8 years. We then analyzed the intensity of agonistic responses against these traits in breeding males and females by presenting young male decoys showing these mature characters. We found that those characters eliciting high aggressiveness in males (head and rump) were partly expressed in young males and only 1 (tail) of the 2 traits (tail and back) eliciting high aggressiveness in females was poorly expressed. Our study suggests that conspecific aggressiveness of both males and females can play a significant role in determining patterns of delayed plumage maturation.
Abstract: Numerous studies have shown positive associations between ornaments and condition, as predicted by indicator models of sexual selection. However, this idea is continuously challenged by opposite results, which reveal our lack of full understanding of how sexual selection works. Environmental heterogeneity may explain such inconsistencies, but valid field tests of this idea are currently lacking. We first analysed the relationship between condition and ornament expression from nine populations over 7 years in a wild bird, the red grouse Lagopus lagopus scoticus. We then manipulated male aggressiveness at the population level by means of testosterone implants in a replicated field experiment. We found that the relationship between condition and ornamentation varied greatly between environments and became stronger when environmental conditions (ECs) were worse or when aggressiveness in the population was experimentally increased. Some ornaments may therefore reliably advertise a better condition only in adverse ECs. Considering environmental heterogeneity can help reconcile conflicting findings regarding the reliability of ornaments as indicators of condition and will help our understanding of sexual selection processes.
Abstract: Indicator models of sexual selection predict that the expression of sexual ornaments should be condition dependent. This is only partly supported by data, as many studies do not find positive associations between ornaments and condition. The reason for this inconsistency remains poorly understood. It has been hypothesized that environmental context may explain variation in the condition dependence of sexual traits, with stronger relationships between ornaments and condition expected in harsher environments. However, field tests of this idea are scarce. We studied 9 populations of wild red grouse Lagopus lagopus scoticus over 11 years, and compared the relationship between ornamentation and body mass (an index of body condition) in relation to environmental variability. We used the abundance of a key parasite in this system, Trichostrongylus tenuis, as an index of environmental conditions. We found that both ornament expression and body mass negatively correlated with parasite infection at both population and individual levels. More interestingly, we found that the relationship between ornamentation and body mass was stronger in populations with high parasite infection levels. Our findings support the idea that the condition dependence of secondary sexual ornaments varies in relation to environmental context. In sites and years when parasites are abundant, sexual ornaments provide better signals of condition.
Abstract: Individuals can gain fitness benefits and costs through their mates. However, studies on sexual selection have tended to focus on genetic benefits. A potentially widespread cost of pairing with a parasitized mate is that doing so will increase an individual's parasite abundance. Such a cost has been overlooked in systems in which parasites are indirectly transmitted. We manipulated the abundance of the nematode parasite Trichostrongylus tenuis, an indirectly transmitted parasite, within pairs of wild red grouse Lagopus lagopus scoticus in spring. Parasite levels were correlated within pairs before the experiment. We removed parasites from males, females, or both members of the pair and evaluated individual parasite uptake over the subsequent breeding period. At the end of the breeding season, an individual's parasite abundance was greater when its mate had not been initially purged of parasites. This cost appeared to be greater for males. We discuss the implications of our results in relation to the costs that parasites may have on sexual selection processes.
Abstract: Theory suggests that condition-dependent sexual displays should be more weakly expressed under adverse conditions than under more favourable ones. Here, we tested this hypothesis in wild red grouse Lagopus lagopus scoticus using a data set of nearly 1500 individuals from nine populations over 8 years, covering varying environmental conditions. We analysed whether male and female ornament expression (i.e. comb size) in a given site and year varied with various indices of environmental conditions: population density, Trichostrongylus tenuis nematode infection at the population level, and climate conditions [measured as winter North Atlantic oscillation (NAO) index]. We found that average comb size in males, but not in females, negatively correlated with population density, parasite infection levels, and winter NAO index. Furthermore, the coefficient of variation (CV) of comb size was higher in females than in males. CVs in both males and females were not clearly associated with the studied environmental variables. Our results support the idea that the expression of condition-dependent sexual traits should be lower under more stressful environmental conditions, but only in males. We discuss the potential reasons behind the effect of environmental conditions on secondary sexual traits, and why these effects differ between sexes. (C) 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, , .
Abstract: In order to maximise fitness individuals should adjust their level of signalling according to their surrounding social environment. However, field experiments showing such adjustment of current signalling associated to changes in social context are lacking. Here, we manipulated levels of male aggressive- and dominance-related displays in a wild bird in our treated area by increasing testosterone levels using implants in a subset of males. We then compared the expression of sexual signals (i.e. comb size) between non-treated red grouse Lagopus lagopus scoticus males from control and treatment areas. We further explored the potential endocrinological mechanism linking social environment and signal expression by analysing testosterone levels in all males. Our treatment successfully increased overall aggressive- and dominance-related behaviours in the treatment area. Furthermore, testosterone-implanted birds increased their comb size as repeatedly shown in previous studies in male red grouse. Interestingly, untreated males living in the treatment area decreased their comb size, whilst increasing testosterone levels. Since comb size is a signal of dominance, untreated males from the treatment area may have perceived themselves as subordinate individuals and decreased their signalling levels to avoid confrontations with testosterone-treated, dominant individuals. In conclusion, our findings show that social context has the potential to regulate sexual signalling and testosterone levels. Our results highlight the role of social context when exploring the link between testosterone and behaviour, as it may reverse the relationship between both traits. Our results suggest that social context affects signalling and testosterone independently. (C) 2012 Elsevier Inc. All rights reserved.
Abstract: The identification of genes involved in a host's response to parasite infection provides both a means for understanding the pathways involved in immune defence and a target for examining host-parasite co-evolution. Most studies rely on a candidate gene approach derived from model systems to identify gene targets of interest, and there have been a dearth of studies geared towards providing a holistic overview of immune response from natural populations. We carried out an experiment in a natural population of red grouse (Lagopus lagopus scoticus) to manipulate levels of Trichostrongylus tenuis parasite infection. The transcriptomic response of individuals was examined from standard cDNA and suppressive subtractive hybridization (SSH) libraries produced from gut, liver and spleen, enriching for genes expressed in response to T. tenuis infection. A total of 2209 and 3716 unique transcript sequences were identified from the cDNA and SSH libraries, respectively. Forty-five of these had Gene Ontology annotation associated with immune response. Some of these genes have previously been reported from laboratory-based studies of model species as important in immune response to gastrointestinal parasite infection; however, multiple novel genes were also identified. These may reveal novel pathways involved in the host response of grouse to T. tenuis and provide a resource that can be utilized as candidate genes in other species.
Abstract: In many species, females display brightly coloured and elaborate traits similar to those that males use in intra-and inter-sexual selection processes. These female characters are sometimes related to fitness, and might function as secondary sexual characteristics that have evolved through sexual selection. Here, we used descriptive data from 674 females in 10 populations and an experimental removal of Trichostrongylus tenuis parasites in four populations, to examine the effects of season, age, condition, and parasites on the size of supra-orbital combs displayed by female red grouse Lagopus lagopus scoticus. We found that comb size (i) was greater during the breeding than the non-breeding season, (ii) was greater in adult than in young females, (iii) was positively correlated with body condition, and (iv) negatively correlated with parasite abundance. Experimentally, we showed that comb size increased proportionally to the number of worms removed after parasite dosing. Our findings provide a better understanding of proximate mechanisms behind the expression of a male-like trait in females, and we discuss its possible function as a female ornament.
Abstract: A central issue in ecology is in understanding the relative influences of intrinsic and extrinsic effects on population regulation. Previous studies on the cyclic population dynamics of red grouse (Lagopus lagopus scoticus) have emphasized the destabilizing effects of either nematode parasites or territorial behaviour and aggression. The potential interacting effects of these processes, mediated through density-dependent, environmentally induced alterations of host immunocompetence influencing susceptibility to parasites have not been considered. Male red grouse at high density are more aggressive, associated with increased testosterone, which potentially could lead to reduced immunocompetence at a stage when parasites are most prevalent. This could depress individual condition, breeding performance and survival and thus drive or contribute to overall reductions in population size. Here, we characterize the transcriptomic response of grouse to nematode parasite infection and investigate how this is subsequently affected by testosterone, using a microarray approach contrasting red grouse with high and low parasite load at both high and low testosterone titre. A suite of 52 transcripts showed a significant level of up-regulation to either chronic parasite load or experimental parasite infection. Of these, 51 (98%) showed a reduced level of expression under conditions of high parasite load and high testosterone. The genes up-regulated by parasites and then down-regulated at high testosterone titre were not necessarily associated with immune response, as might be intuitively expected. The results are discussed in relation to the fitness and condition of individual red grouse and factors influencing the regulation of abundance in natural populations.
Abstract: The onset of incubation before the end of laying imposes asynchrony at hatching and, therefore, a size hierarchy in the brood. It has been argued that hatching asynchrony might be a strategy to improve reproductive output in terms of quality or quantity of offspring. However, little is known about the mediating effect of hatching asynchrony on offspring quality when brood reduction occurs. Here, we investigate the relationship between phenotypic quality and hatching asynchrony in Common Kestrel Falco tinnunculus nestlings in Spain. Hatching asynchrony did not increase breeding success or nestling quality. Furthermore, hatching asynchrony and brood reduction had different effects on nestlings' phytohaematogglutinin (PHA)-mediated immune response and nestling growth. In asynchronous and reduced broods (in which at least one nestling died), nestlings showed a stronger PHA-mediated immune response and tended to have a smaller body size compared with nestlings raised in synchronous and reduced broods. When brood reduction occurred in broods hatched synchronously, there was no effect on nestling size, but nestlings had a relatively poor PHA-mediated immune response compared with nestlings raised in asynchronous and reduced broods. We suggest that resources for growth can be directed to immune function only in asynchronously hatched broods, resulting in improved nestling quality, as suggested by their immune response. We also found that males produced a greater PHA-mediated immune response than females only in brood-reduced nests without any effect on nestling size or condition, suggesting that females may trade off immune activities and body condition, size or weight. Overall, our results suggest that hatching pattern and brood reduction may mediate resource allocation to different fitness traits. They also highlight that the resolution of immune-related trade-offs when brood reduction occurs may differ between male and female nestlings.
Abstract: Environmental heterogeneity is expected to create variation in the ornament-condition relationship. This topic has been studied in males with less attention being given to females. Here, we explore inter-population variation in the relationship between the size of a male-like trait, supra-orbital combs, and body mass in female red grouse Lagopus lagopus scoticus. We used the abundance of the nematode Trichostrongylus tenuis, a parasite with strong negative effects on this species, as a proxy of environmental conditions. We studied six populations over 5 years and showed that the comb size-body mass relationship varied with mean parasite abundance, with stronger ornament-condition relationships in populations with higher parasite infection levels. Our study supports the idea that environmental conditions, and in particular parasite infection levels, may affect the reliability of female ornaments as condition indicators.
Abstract: Vertebrates commonly use carotenoid-based traits as social signals. These can reliably advertise current nutritional status and health because carotenoids must be acquired through the diet and their allocation to ornaments is traded-off against other self-maintenance needs. We propose that the coloration more generally reveals an individual's ability to cope with stressful conditions. We tested this idea by manipulating the nematode parasite infection in free-living red grouse (Lagopus lagopus scoticus) and examining the effects on body mass, carotenoid-based coloration of a main social signal and the amount of corticosterone deposited in feathers grown during the experiment. We show that parasites increase stress and reduce carotenoid-based coloration, and that the impact of parasites on coloration was associated with changes in corticosterone, more than changes in body mass. Carotenoid-based coloration appears linked to physiological stress and could therefore reveal an individual's ability to cope with stressors.
Abstract: Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.
Abstract: How colouration provides information about individuals in birds has been a central issue in recent decades. Although much information has been derived, little is known about the adaptive significance of egg colouration in birds. A recent idea suggests that biliverdin-and porphyrin-pigmented eggs may act as a post-mating sexual signal for males to assess female quality. In birds, it is common for males to influence prelaying female condition by courtship feeding. Using Eurasian kestrels, a species that lays protoporphyrin-pigmented eggs, we descriptively assessed the influence of male feeding on egg pigmentation by considering female phenotype, condition, breeding parameters and male body condition. We found that older females and females with greyer tails (an index of individual quality) produce highly pigmented eggs. However, male body condition was the only variable that explained egg colouration when considered together with the female-related variables. Therefore, females that mated with males in better condition laid highly pigmented eggs. With the same species, we also explored the cost of producing protoporphyrin-pigmented eggs using a food-supply experiment before the laying period. Food supplementation did not increase egg pigmentation, but hatching success and egg mass were positively related to egg colouration only in food supplied pairs. We suggest that egg colouration might be costly to produce and probably suggests egg quality. However, this cost cannot be explained by female quality, but by male condition instead. In general, our results do not support the theory that egg colouration is a post-mating sexual signal in species where males determine female condition at the time of laying.
Abstract: Testosterone underlies the expression of most secondary sexual traits, playing a key role in sexual selection. However, high levels might be associated with physiological costs, such as immunosuppression. Immunostimulant carotenoids underpin the expression of many red-yellow ornaments, but are regulated by testosterone and constrained by parasites. We manipulated testosterone and nematode burdens in red grouse (Lagopus lagopus scoticus) in two populations to tease apart their effects on carotenoid levels, ornament size and colouration in three time-step periods. We found no evidence for interactive effects of testosterone and parasites on ornament size and colouration. We showed that ornament colouration was testosterone-driven. However, parasites decreased comb size with a time delay and testosterone increased carotenoid levels in one of the populations. This suggests that environmental context plays a key role in determining how individuals resolve the trade-off between allocating carotenoids for ornamental coloration or for self-maintenance needs. Our study advocates that adequately testing the mechanisms behind the production or maintenance of secondary sexual characters has to take into account the dynamics of sexual trait expression and their environmental context.
Abstract: The duration of the postfledging dependence period (PFDP) is supposed to be modulated by the parent offspring conflict: Offspring should extract the highest levels of parental investment, although parents may respond by setting fixed limits to the level of investment or by raising the costs of attempts to extract additional investment. In this context, longer PFDPs are expected in nests tended by higher quality parents and in dominant siblings. We explored these hypotheses with a combination of experimental and correlative results. First, we food supplemented offspring during the PFDP to study whether food supply during fledging, an indicator of parental quality, has an effect on the PRO duration in the Eurasian kestrel. We found that the PFDP was longer in food-supplemented nests. Second, we measured the duration of the PFDP over 3 years under different environmental conditions to explore whether the quality of parents and nestling phenotype were correlated with the duration of PFDP. Correlative results suggest that fledglings raised by higher quality parents and in the year with poorer food conditions showed longer PFDP. Furthermore, male fledglings showing grayer coloration in the rump (an index of competitive capacity) have longer PFDPs than browner males. Overall, our results suggest that parent, rather than offspring characteristics, can modulate the PFDP duration mediated by food conditions, although more colored nestlings stay in the nest territory for longer periods.
Abstract: Background: Most hypotheses on population limitation of small mammals and their predators come from studies carried out in northern latitudes, mainly in boreal ecosystems. In such regions, many predators specialize on voles and predator-prey systems are simpler compared to southern ecosystems where predator communities are made up mostly of generalists and predator-prey systems are more complex. Determining food limitation in generalist predators is difficult due to their capacity to switch to alternative prey when the basic prey becomes scarce. Methodology: We monitored the population density of a generalist raptor, the Eurasian kestrel Falco tinnunculus over 15 years in a mountainous Mediterranean area. In addition, we have recorded over 11 years the inter-annual variation in the abundance of two main prey species of kestrels, the common vole Microtus arvalis and the eyed lizard Lacerta lepida and a third species scarcely represented in kestrel diet, the great white-toothed shrew Crocidura russula. We estimated the per capita growth rate (PCGR) to analyse population dynamics of kestrel and predator species. Principal Findings: Multimodel inference determined that the PCGR of kestrels was better explained by a model containing the population density of only one prey species (the common vole) than a model using a combination of the densities of the three prey species. The PCGR of voles was explained by kestrel abundance in combination with annual rainfall and mean annual temperature. In the case of shrews, growth rate was also affected by kestrel abundance and temperature. Finally, we did not find any correlation between kestrel and lizard abundances. Significance: Our study showed for the first time vertebrate predator-prey relationships at southern latitudes and determined that only one prey species has the capacity to modulate population dynamics of generalist predators and reveals the importance of climatic factors in the dynamics of micromammal species and lizards in the Mediterranean region.
Abstract: Extravagant ornaments evolved to advertise their bearers' quality, the honesty of the signal being ensured by the cost paid to produce or maintain it. The oxidation handicap hypothesis (OHH) proposes that a main cost of testosterone-dependent ornamentation is oxidative stress, a condition whereby the production of reactive oxygen and nitrogen species (ROS/RNS) overwhelms the capacity of antioxidant defences. ROS/RNS are unstable, very reactive by-products of normal metabolic processes that can cause extensive damage to key biomolecules (cellular proteins, lipids and DNA). Oxidative stress has been implicated in the aetiology of many diseases and could link ornamentation and genetic variation in fitness-related traits. We tested the OHH in a free-living bird, the red grouse. We show that elevated testosterone enhanced ornamentation and increased circulating antioxidant levels, but caused oxidative damage. Males with smaller ornaments suffered more oxidative damage than those with larger ornaments when forced to increase testosterone levels, consistent with a handicap mechanism. Parasites depleted antioxidant defences, caused oxidative damage and reduced ornament expression. Oxidative damage extent and the ability of males to increase antioxidant defences also explained the impacts of testosterone and parasites on ornamentation within treatment groups. Because oxidative stress is intimately linked to immune function, parasite resistance and fitness, it provides a reliable currency in the trade-off between individual health and ornamentation. The costs induced by oxidative stress can apply to a wide range of signals, which are testosterone-dependent or coloured by pigments with antioxidant properties.
Abstract: Competition for resources (e.g. mates or food) is the main evolutionary explanation for conspicuous ornaments in males, although this idea is not generalized in females. Whether or not the expression of melanic coloration is dependent on environmental conditions remains controversial. We studied three different melanin-based female traits in the Eurasian kestrel Falco tinnunculus, a sexually dichromatic species, for a period of 10 years: grey coloration in rump and tail and the width of the black subterminal tail band. We analysed these traits for within-individual variation among years, as well as their possible link with indices of quality, such as age, body size, and breeding performance. The results obtained demonstrate that female melanin-based coloration increased from yearlings to adults. In addition, the expression of female rump coloration covaried positively with the environmental conditions in the previous year (i.e. measured as clutch size at population level). Finally, we found a positive correlation between grey rump coloration and clutch size. These results suggest that the expression of rump coloration, a melanin-based trait, is environmentally constrained, and we propose that this character could function as an indicator of individual quality in female Eurasian kestrels. (C) 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 781-790.
Abstract: Background: Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals. Methodology/Principal Findings: We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation. Conclusions/Significance: With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.
Abstract: Ticks are important arthropod vectors of diseases of human, livestock, and wildlife hosts. In the United Kingdom, the sheep tick (Ixodes ricinus) is increasingly recognized as a main limiting factor of red grouse (Lagopus lagopus) populations, a game bird of high economic value. We evaluated the effectiveness of a new practical technique that could help managers reduce negative impacts of ticks on young grouse. In a replicated field experiment, we treated breeding females with leg bands impregnated with permethrin, a slow-releasing potent acaracide. We found that treatment reduced tick burdens on young chicks. Because this treatment is easily applied, it offers a new practical management tool to tackle problems caused by ticks in game bird populations.
Abstract: Predation has received considerable theoretical and empirical support in population regulation. The effect of predators, however, could be achieved in direct (killing) or indirect effects (such as displacement). In this paper, we explored the relationship between Eurasian kestrels Falco tinnunculus and skylarks Alauda arvensis in Mediterranean grasslands. First, we analysed the presence of skylarks in the kestrel diet over 9 years. We also compared a grassland area of experimentally increased kestrel density and a second grassland as control area to evaluate the direct or indirect effect on skylark abundance. We also considered two different habitats, grazed and ungrazed plots. If skylark abundance decreased as the kestrel breeding season progressed in high-density kestrel area compared with the control area, it would suggest a direct effect (predator hypothesis). If skylark abundance remains constant in both areas of contrasting kestrel density, it would suggest that skylarks avoid kestrels (avoidance hypothesis). We found that skylark abundance decreased in the kestrel area from the beginning of kestrel nest-box installation to recent years. The rate of skylark consumption decreased in a 9-year period as kestrel abundance increased, although the total amount skylark consumption did not show a decreasing trend. In addition, skylarks were more abundant in the kestrel-free area than in the kestrel area. Finally, we found that skylark abundance did not change through the kestrel breeding period in relation to grazing. We suggest that an increased breeding density of kestrels during their breeding period may force the skylarks to breed in other areas, which may explain the decline of their abundance.
Abstract: Abundance and diversity of small mammals are usually affected strongly by grazing either due to decreased food availability or quality, decreased suitability of soil for building burrow systems due to trampling and/or due to increased predation risk in the structurally simpler grazed areas. We estimated the effects of grazing-induced changes in vegetation and soil and of increased predation on small mammals in a Mediterranean grassland landscape. We measured vegetation structure, soil compaction and small mammal abundance and species composition in 22 plots of 8 Sherman live traps each, arranged according to an unbalanced two-way ANOVA design with two grazing levels (grazed areas and cattle exclosures) and two predator abundance levels (increased densities of Eurasian kestrets Falco tinnunculus by means of nest boxes and control). Plots were sampled during 2 consecutive years in early summer and earty fall. Exclosure from cattle increased significantly vegetation height and volume and decreased soil compaction. Grazing-induced changes in vegetation height and volume and in soil compaction produced strong effects on small mammal abundance and species richness. Increased kestrel. densities did not have significant additive or interactive effects, with the effects of grazing-induced vegetation and soil gradients on abundance or richness of small mammals. Our results suggest that the effects of grazing on small mammal communities in Mediterranean montane grasslands were mainly due to reduced food availability and by negative effects of trampling on the suitability of soils for building burrow systems. Decreased food quality and increased predation in grazed areas seemed to play a minor rote, if any. Reductions in stock densities would then favor generalist predator populations in Mediterranean grasslands through the expected positive effects of such reductions on the availability of food and burrows for small mammals. (C) 2006 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.
Abstract: Sex differences in testosterone levels and sex-biased sensitivity to testosterone are the basis of some ideas postulated to account for sex-linked environmental vulnerability during early life. However, sex variation in circulating testosterone levels has been scarcely explored and never manipulated at post-natal stages of birds in the wild. We measured and experimentally increased circulating testosterone levels in nestling Eurasian kestrels Falco tinnunculus. We investigated, possible sexual differences in testosterone levels and the effect of this hormone on growth (body mass and tarsus length) and cell-mediated immunity in males and females. We also explored testosterone effects on rump coloration, a highly variable melanin-based trait in male nestlings. We analysed data on circulating testosterone levels of nestlings in 15 additional bird species. Increased levels of testosterone tended to negatively affect body condition, reduced cell-mediated immune responses in male and female nestlings and also diminished the expression of grey rump coloration in male nestlings. No sex differences were observed in testosterone levels in either control or increased testosterone group nestlings, and no interactions were found between sex and treatment. However, male nestlings showed a lower cell-mediated immune response than females in both groups. Our results indicate first, that a high level of testosterone in all nestlings in a brood entails costs, at least in terms of immunity, coloration and probably growth. Secondly, sex differences in post-natal cell-mediated immunity, and consequently in the capacity to prevent diseases, cannot be explained by sex differences in circulating testosterone levels. Finally, by comparing published data at an interspecific level, contradictory sex patterns in circulating testosterone levels have been found, supporting the idea that circulating testosterone might not be a proximate factor causing sex-dependent vulnerability in bird species.
Abstract: Among the most familiar sexual signals are red, yellow, and orange sexual traits pigmented by carotenoids. Many birds can detect near-ultraviolet (UV) light, and UV signals can play key roles in mate choice. Grouse (Tetraonidae) exhibit bright carotenoid-dependent sexual ornaments, their supra-orbital combs, which to humans appear orange-red. Combs also reflect in the UV, which is not visible to humans but is likely to be visible to grouse. In male red grouse Lagopus lagopus scoticus, we show that comb UV reflectance decreases with increasing comb size and redness. By removing the epidermis of combs, where carotenoid pigments are, we show that the UV reflectance is a property of the dermis, underneath the red pigmented epidermis. Carotenoid pigmentation of combs acted as a mask to reduce reflectance by the dermis in the range 400-550 nm and in the UV, 300-400 nm. Patagium skin (non-ornamental skin under the wing) also reflects in the UV, but epidermis removal on this bare part tended to reduce UV reflectance, whereas removal of the red epidermis of combs increased UV reflectance. Males in better condition (greater body mass relative to size) had bigger and redder combs, but with less UV. Thus, carotenoid pigments of grouse combs are deposited on a white background with significant UV reflectance, which can influence how the signal is perceived by conspecifics. Carotenoid-based traits exhibit UV reflectance in a number of species, but how UV reflectance and carotenoid pigmentation influence colour remains little known for integumentary ornaments compared to plumage traits. UV vision is not uncommon in birds and other animals, so future studies should investigate how UV reflectance influences the perception of carotenoid-based signals of quality.
Abstract: Carotenoids determine the yellow-red colours of many ornaments, which often function as signals of quality. Carotenoid-based signalling may reliably advertise health and should be particularly sensitive to parasite infections. Nematodes are among the commonest parasites of vertebrates, with well-documented negative effects on their hosts. However, to date, little is known about the effects that these parasites may have on carotenoid-based signalling. Tetraonid birds (grouse) exhibit supra-orbital combs, which are bright integumentary ornaments pigmented by carotenoids. We tested the effect of the nematode parasite Trichostrongylus tenuis on signalling in free-living male red grouse Lagopus lagopus scoticus. We show that experimentally reduced nematode infection increases plasma carotenoid concentration and comb redness, demonstrating for the first time that nematodes can influence carotenoid-based signals.
Abstract: Among the commonest sexual signals of birds are the red-yellow traits pigmented by carotenoids, but how they reliably advertise individual quality remain poorly understood. Here we tested the hypothesis that carotenoid-based signalling is enhanced by testosterone but reduced by parasites, and that the dual action of testosterone on ornament expression and parasite resistance ensures reliable signalling. Tetraonid birds such as the red grouse Lagopus lagopus scoticus have bright red combs pigmented by carotenoids, which function in intra- and inter-sexual selection. In separate experiments, we manipulated a main nematode parasite, Trichostrongylus tenuis (using deparasitation and re-infection) and testosterone (using testosterone or combined Flutamide/ATD treatments) in free-living males and investigated effects on plasma carotenoids and comb colour. In untreated males, comb redness positively correlated with plasma carotenoids, testosterone concentration and condition. Plasma carotenoids and comb redness both negatively correlated with T. tenuis abundance. Plasma carotenoids decreased in response to a challenge from T. tenuis, but increased when parasites were reduced. Testosterone enhanced comb redness, but tended to deplete plasma carotenoids. Combined Flutamide and ATD treatment had no significant effects on comb colour or plasma carotenoids, indicating that testosterone effects might be direct. Our experiments show contrasted effects of testosterone and nematode parasites on carotenoid-based ornamentation. Testosterone and parasites have well documented interactions in the study model. These, together with the opposite effects that testosterone and parasites have on carotenoid availability and use, would shape optimal levels of signalling, depending on individual quality, and might ensure reliable signalling. Carotenoid-based and testosterone-dependent traits have rarely been linked. Our study provides such a connection and shows that investigating how parasites, testosterone and carotenoids interact helps in the understanding of the evolution and maintenance of honest carotenoid-based signals of health.
Abstract: The theory of sex allocation suggests that if the reproductive value and the cost of producing/rearing offspring differ between male and female offspring, parents should invest differently in sexes depending on environmental conditions. Female parents could allocate more resources to eggs of one sex to compensate potential sex-dependent constraints later during the nestling period. In this study, we tested the influence of environmental conditions on sexual dimorphism in eggs of Eurasian kestrels (Falco tinnunculus) by experimentally manipulating food availability before laying. We found that an increase in food abundance before laying did not increase egg mass but changed sex-dependent resource distribution in eggs. In food-supplemented pairs, but not in control pairs, egg mass and hatchling mass were similar between males and females. In addition, we found, in the food-supplemented group, that the latest hatched females showed shorter hatching times than in the control group. In control pairs, female eggs, hatchlings and nestlings were heavier than males. In addition, male fledglings in the food-supplemented group gained less mass than those in the control group. As that food abundance was only increased until the onset of laying, female kestrels were expected to invest in eggs taking food abundance before egg formation as a predictor of future conditions during brood rearing. Our study shows that environmental conditions before laying promote a subtle adjustment of the resources invested in both sexes of offspring rather than in other breeding parameters. This adjustment resulted in a shortening of hatching time of the last hatched females that possibly gives them advantages in their competitive capacity with respect to male nest-mates.
Abstract: Theoretical models of parental care predict differential allocation in relation to the expected fitness of the offspring. As birds must allocate all the resources required for embryonic development in self-contained packages, maternal egg allocation takes a central role in avian life histories. It is predicted that mothers can influence offspring performance by varying the size or composition of their eggs. In this context, T cell-mediated immune response has been revealed as a valuable tool to evaluate fledgling fitness. However, little is known about its relationships to egg mass. I describe a negative association between egg mass and cellular immune response in Eurasian kestrel nestlings (Falco tinnunculus) throughout 3 years. To explore how environmental conditions could mediate this relationship, I experimentally supplied food to females before egg formation in the third study year. I found that this relationship turned to positive in food-supplied females without any effect on egg size. This result shows that environmental conditions before egg formation mediate the relationship between egg mass and future immune response of the nestlings. I suggest that females may be constrained in improving the future immune response of their offspring due to resource allocation trade-offs determined by their pre-laying condition.
Abstract: Host-parasite interactions are central in evolutionary and behavioural ecology. In the last few years, skin injections of the mitogen Phytohaemagglutinin (PHA) have become one of the most important and widely used in-vivo assays of immune function in birds. However, there are no studies of the circadian variation suggesting that care should be taken interpreting results when using this technique. This 3-year study assessed PHA responses as a function of daylight time in 310 Eurasian kestrel Falco tinnunculus nestlings at 24 days of age in Central Spain. I found that T-cell-mediated immunity was positively related to nestling mass and varied among years. Controlling for these variables, I also found that T-cell-mediated immunity decreased with the hour of sampling, and that this pattern was consistent between years. In addition, I found that at the end of the day only, T-cell-mediated immunity decreased with brood size. Parasites seem not to be behind this pattern, but I suggest that the cumulative effect of sibling competition during the day might explain the decrease of cellular immunity with the hour of sampling. Thus, I strongly recommend that future studies of cellular immunity should control for this potential source of variation when nestling self-maintenance is evaluated by the PHA-induced skin-swelling response.
Abstract: We describe the blood and intestinal parasites in the Ocellated lizard, Lacerta lepida, examining the factors that determine the prevalence and intensity of infection of haemogregarines, and the prevalence of coccidia and nematodes. In relation to haemogregarines, no juveniles were detected as being infected, whereas 71.7 % of adults were infected. The prevalence of infection was positively related to the size of the adults. There were no differences between seasons or sexes in the prevalence or intensity of infection in adults. There were no significant differences in the prevalence of infection by nematodes between ages or sexes, nor in relation to the size of adult lizards, but adult lizards excreting coccidian oocysts tend to be smaller. During the mating period, reproductive activities lead to a decrease in the body condition. However, neither the intensity of haemogregarine's infection nor the prevalence of intestinal parasites was related to the lizards' body condition.
Abstract: 1. Brood hierarchies established through hatching asynchrony are supposed to be costly for small chicks because of impaired growth and survival. An additional cost that has remained unexplored is the stress imposed by competition for resources in the nest. 2. In the present study of broods of Eurasian kestrels, we have used the level of heat shock proteins such as Hsp60 and Hsp70 in peripheral blood as well as the heterophile/lymphocyte ratio to detect stress in nestlings. The sex of nestlings and their Caryospora sp. oocyst excretion were included in analyses. 3. Nestlings showing a large size difference with respect to their largest sibling had higher levels of both stress proteins, and this effect was stronger for female chicks as indicated by a significant interaction sex x size difference, presumably because of their higher food requirements for growth. Nestlings for which the largest sibling was a female had higher levels of Hsp60 than when it was a male. The heterophile/lymphocyte index was a much poorer predictor of competitive stress. 4. Stress proteins are effective estimators of competitive, nutritional and parasite-mediated stress of nestlings in the wild. The cost of sustained stress has to be included in future analyses of the fitness repercussions of dominance hierarchies in avian broods.
Abstract: 1. In birds, the potential maternal ability to adjust resource allocation to different eggs in the clutch might have a major effect on the survival expectancies of particular nestlings or entire broods. We assessed whether sexually size-dimorphic Eurasian kestrels Falco tinnunculus (Linnaeus) are able to adjust their reproductive effort by adopting different strategies of egg mass provisioning according to egg sex and laying order. 2. Initial eggs bearing male embryos were heavier than initial eggs bearing female embryos, but no differences in egg mass associated to sex were detected for eggs laid subsequently. Furthermore, in clutches started with a male egg, egg mass declined in subsequent eggs, while in clutches started by a female egg the opposite trend in within-clutch egg-mass variation was found. This suggests differential deposition of resources invested in initial eggs of different sex leading to saved or depleted resources for subsequent eggs. 3. Daughters from initial eggs hatched earlier than sons from initial eggs, which may enhance survival of smaller siblings hatched later. These contrasting strategies of egg provisioning and hatching patterns depending on the sex of the first-laid egg were associated, respectively, with marked mass hierarchies and a lack of mass hierarchies at fledgling in broods initiated with eggs bearing sons and daughters. 4. Parental kestrels may allocate reproductive effort by promoting favouritism towards early hatched chicks or by avoiding any favouritism by producing siblings of each sex with similar mass. This may be achieved depending on the female ability both to identify egg sex and to partially reabsorb or differentially allocate resources to eggs accordingly to adjust reproductive investment. This may be a key mechanism to control sibling competition in birds with sexual dimorphism in mass.
Abstract: Parental favoritism in birds would be enhanced if parents can control any egg feature influencing the ontogeny of the embryo during incubation. Egg size and composition may influence the duration of incubation and hatching periods, and eggs bearing embryos of different sex may differ in size and composition. Therefore, the sex of the embryo could also influence its ontogeny before hatching. We tested this prediction by investigating the duration of the embryonic period of different-sex embryos in the Eurasian kestrel (Falco tinnunculus), a sexually dimorphic raptor in which adult females are approximately 20% heavier than are adult males. We found the first evidence of sex differences in the duration of the embryonic period in avian eggs. Female embryos had a shorter embryonic period than did male embryos, which allowed females to hatch earlier in the hatching sequence and assume a higher rank than that of males in the intrabrood size hierarchy. Embryos with a fast growth and development resulted in hatchlings with greater residual reserves and thus larger mass, which suggests that a shorter embryonic period requires less maintenance metabolism relative to growth. Our results also indicated that early hatching may be advantageous to gain a high rank in the size hierarchy within the brood independently of the effect of sex on fledgling mass. Sex differences in avian egg ontogeny may therefore be a factor shaping life-history traits associated with parental control of sibling competition, which should be addressed in any future work on optimal reproductive investment.
