Javier Viñuela

Testosterone increases bioavailability of carotenoids: Insights into the honesty of sexual signaling

Androgens and carotenoids play a fundamental role in the expression of secondary sex traits in animals that communicate information on individual quality. In birds, androgens regulate song, aggression, and a variety of sexual ornaments and displays, whereas carotenoids are responsible for the red, yellow, and orange colors of the integument. Parallel, but independent, research lines suggest that the evolutionary stability of each signaling system stems from tradeoffs with immune function: androgens can be immunosuppressive, and carotenoids diverted to coloration prevent their use as immunostimulants. Despite strong similarities in the patterns of sex, age and seasonal variation, social function, and proximate control, there has been little success at integrating potential links between the two signaling systems. These parallel patterns led us to hypothesize that testosterone increases the bioavailability of circulating carotenoids. To test this hypothesis, we manipulated testosterone levels of red-legged partridges Alectoris rufa while monitoring carotenoids, color, and immune function. Testosterone treatment increased the concentration of carotenoids in plasma and liver by >20%. Plasma carotenoids were in turn responsible for individual differences in coloration and immune response. Our results provide experimental evidence for a link between testosterone levels and immunoenhancing carotenoids that (i) reconciles conflicting evidence for the immunosuppressive nature of androgens, (ii) provides physiological grounds for a connection between two of the main signaling systems in animals, (iii) explains how these signaling systems can be evolutionary stable and honest, and (iv) may explain the high prevalence of sexual dimorphism in carotenoid-based coloration in animals.

Birds of prey as limiting factors of gamebird populations in Europe: a review

Whether predators can limit their prey has been a topic of scientific debate for decades. Traditionally it was believed that predators take only wounded, sick, old or otherwise low‐quality individuals, and thus have little impact on prey populations. However, there is increasing evidence that, at least under certain circumstances, vertebrate predators may indeed limit prey numbers. This potential role of predators as limiting factors of prey populations has created conflicts between predators and human hunters, because the hunters may see predators as competitors for the same resources. A particularly acute conflict has emerged over the past few decades between gamebird hunters and birds of prey in Europe. As a part of a European‐wide research project, we reviewed literature on the relationships between birds of prey and gamebirds. We start by analysing available data on the diets of 52 European raptor and owl species. There are some 32 species, mostly specialist predators feeding on small mammals, small passerine birds or insects, which never or very rarely include game animals (e.g. hares, rabbits, gamebirds) in their diet. A second group (20 species) consists of medium‐sized and large raptors which prey on game, but for which the proportion in the diet varies temporally and spatially. Only three raptor species can have rather large proportions of gamebirds in their diet, and another seven species may utilise gamebirds locally to a great extent. We point out that the percentage of a given prey species in the diet of an avian predator does not necessarily reflect the impact of that predator on densities of prey populations. Next, we summarise available data on the numerical responses of avian predators to changing gamebird numbers. In half of these studies, no numerical response was found, while in the remainder a response was detected such that either raptor density or breeding success increased with density of gamebirds. Data on the functional responses of raptors were scarce. Most studies of the interaction between raptors and gamebird populations give some estimate of the predation rate (per cent of prey population taken by predator), but less often do they evaluate the subsequent reduction in the pre‐harvest population or the potential limiting effect on breeding numbers. The few existing studies indicate that, under certain conditions, raptor predation may limit gamebird populations and reduce gamebird harvests. However, the number and extent of such studies are too modest to draw firm conclusions. Furthermore, their geographical bias to northern Europe, where predator–prey communities are typically simpler than in the south, precludes extrapolation to more diverse southern European ecosystems. There is an urgent need to develop further studies, particularly in southern Europe, to determine the functional and numerical responses of raptors to gamebird populations in species and environments other than those already evaluated in existing studies. Furthermore, additional field experiments are needed in which raptor and possibly also mammalian predator numbers are manipulated on a sufficiently large spatial and temporal scale. Other aspects that have been little studied are the role of predation by the non‐breeding part of the raptor population, or floaters, on the breeding success and survival of gamebirds, as well as the effect of intra‐guild predation. Finally there is a need for further research on practical methods to reduce raptor predation on gamebirds and thus reduce conflict between raptor conservation and gamebird management.

Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling

We investigated possible pre‐hatching mechanisms of sex‐differential investment by females that may contribute to offspring sex‐ratio adjustment enhancing the fitness return from reproductive effort in the spotless starling (Sturnus unicolor). We found a seasonal shift in sex ratio from daughters to sons as the season advances. Furthermore, the probability of breeding at 1‐year old and recruitment into the breeding population in daughters is associated with laying date but not with mass at fledging. The reverse is true for males which rarely bred at 1‐year old. We also found that eggs containing female embryos are significantly heavier than those containing males in spite of the slight sexual dimorphism in favour of males. This suggests maternal control of provisioning, favouring daughters that may balance sibling mortality and competition with their brothers. Our results on seasonal variation in sex ratio and differential egg provisioning are consistent with an adaptive tactic in which mothers increase their reproductive return by enhancing the probability that daughters survive and breed in their first year of life.

The oxidation handicap hypothesis and the carotenoid allocation trade‐off

The oxidation handicap hypothesis proposes that testosterone mediates the trade‐off between the expression of secondary sexual traits and the fight against free radicals. Coloured traits controlled by testosterone can be produced by carotenoid pigments (yellow–orange–red traits), but carotenoids also help to quench free radicals. Recently, it has been shown that testosterone increases the amount of circulating carotenoids in birds. Here, a testosterone‐mediated trade‐off in the carotenoid allocation between colour expression and the fight against oxidative stress is proposed. Male red‐legged partridges were treated with testosterone, anti‐androgens or manipulated as controls. Testosterone‐treated males maintained the highest circulating carotenoid levels, but showed the palest red traits and no evidence of oxidative damage. Increased levels of a key intracellular antioxidant (i.e. glutathione) indicated that an oxidative challenge was in fact induced but controlled. The trade‐off was apparently solved by reducing redness, allowing increased carotenoid availability, which could have contributed to buffer oxidative stress.

Nestbox provisioning in a rural population of Eurasian Kestrels: breeding performance, nest predation and parasitism

The breeding biology of the Eurasian Kestrel Falco tinnunculusin nestboxes in farmland was studied to test for differences between artificial and natural sites. We report on the direct effect of nestbox provisioning on some life-history traits and how nestbox use affects nest predation and parasitism. Five types of nest-sites were available: nestboxes on poles and trees (artificial sites), stick nests on trees, stick nests on pylons and holes in buildings (‘natural’ sites). The Kestrel population increased from 23 pairs in 1993 (prior to nestbox installation) to 55 in 1998 as nestboxes were provided. In general, pairs breeding in trees started to lay later than those nesting in nestboxes on poles or in building holes, but this difference was probably associated with habitat quality rather than nest type. Differences in clutch size were found between nest-sites in some years, and were associated with laying date and, probably, with variation in territory quality. Using only data from successful nests, pairs breeding in nestboxes produce more fledglings than those in building holes or pylons. The frequency of nest predation was higher in natural sites than in nestboxes. The number of fledglings from pairs breeding in nestboxes was higher than from those breeding in old stick nests in trees when all nests were considered. Nestbox provisioning had no effect on the occurrence of the ectoparasite Carnus hemapterus, but chicks from nestboxes showed higher intensity of infection. Our results suggest that nestbox provisioning increases reproductive success and the frequency of nest predation or intensity of parasite infestation in Kestrels.

Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa).

SUMMARY In animals yellow-orange-red sexual traits pigmented by carotenoids have been suggested to act as signals of current health. Because carotenoids have important physiological functions, individuals might trade-off allocating these pigments to self-maintenance versus coloration. Carotenoids may act as scavengers of free radicals that are released during an immune response. Here, we experimentally assessed whether a local cell-mediated immune response affects circulating carotenoids, antioxidant status, oxidative damage and the expression of a carotenoid-based trait. Male red-legged partridges (Alectoris rufa) were subcutaneously injected with phytohaemagglutinin (PHA) or with phosphate buffer solution (controls). The effect of the treatment on circulating carotenoids, total plasma antioxidant status (TAS), lipid oxidative damage in erythrocytes (TBARS) and ornamentation was assessed. Immune challenge induced a 13% decrease in circulating carotenoids within 24 h. However, this treatment did not affect TAS, TBARS or coloration. Coloration, circulating carotenoids and cell-mediated immune response were positively correlated, but these were not related to TAS or TBARS. Carotenoids were only weakly related to TAS after controlling for the effect of uric acid levels. These results suggest that carotenoid-based ornaments may honestly indicate immunocompetence but probably not antioxidant capacity in this species, and that carotenoids might be relatively weak antioxidants in the plasma. Furthermore, even a relatively harmless and locally elicited immune challenge had important effects on circulating carotenoids, but this effect did not appear to be associated with oxidative stress. Alternative mechanisms linking carotenoids to immunity (not necessarily relying on the use of these pigments as antioxidants) should be considered in future studies on birds.

Opposing selective pressures on hatching asynchrony: egg viability, brood reduction, and nestling growth

Abstract At least 19 hypotheses have been proposed to explain the evolutionary significance of avian hatching asynchrony, and hatching patterns have been suggested to be the result of several simultaneous selective pressures. Hatching asynchrony was experimentally modified in the black kite Milvus migrans by manipulating the onset of incubation during the laying period. Delayed onset of incubation reduced egg viability of first-laid eggs, especially when ambient temperature during the laying period was high. Brood reduction (nestling mortality by starvation or siblicide) was more commonly observed in asynchronous nests. The growth rate was slower in synchronous broods, probably due to stronger sibling rivalry in broods with high size symmetry. Last-hatched chicks in synchronous broods fledged at a small size/mass, while in control broods, hatching order affected growth rates, but not final size. Brood reduction, variable growth rates, and the ability to face long periods of food scarcity are probably mechanisms to adjust productivity to stochastic food availability in a highly opportunistic predator. The natural pattern of hatching asynchrony may be the consequence of opposing selective forces. Extreme hatching synchrony is associated with slow growth rates, small final size of last-hatched chicks, and low viability of first-laid eggs, while extreme hatching asynchrony is associated with high mortality rates. Females seem to facultatively manipulate the degree of hatching asynchrony according to those pressures, because hatching asynchrony of control clutches was positively correlated with temperature during laying, and negatively correlated with the rate of rabbit consumption.

Condition and androgen levels: are condition-dependent and testosterone-mediated traits two sides of the same coin?

The immunocompetence handicap hypothesis posits that androgen-mediated signals honestly indicate the responsiveness of the immune system because of the immunosuppressive effect of androgens. However, androgen levels may also be related to nutritional status, and differences in body condition could be a more parsimonious explanation for variation in the expression of the signal. We maintained captive male red-legged partridges, Alectoris rufa, under regulated food shortage until they reached 85% of their initial body mass. Controls were provided with food ad libitum. After food shortage, experimental birds had lower androgen and higher corticosterone levels than controls. The condition dependence in androgen levels suggests that androgen-mediated signals could be indicating general nutritional state rather than immune function specifically. We propose that androgen-dependent signals may act as indicators of body condition or indicators of immune system quality, depending on the nutritional status of the individual.

The effects of land use and climate on red kite distribution in the Iberian peninsula

The main breeding populations of the red kite (Milvus milvus L.), have been declining in the Iberian peninsula during the last decade. However, there is a lack of regional assessments of habitat suitability that identifies limiting ecological factors for the species and areas with conservation problems. In this work we present a regional model for the distribution and abundance of breeding red kites in the Iberian peninsula. The occurrence and estimated abundance in 100 km 2 UTM squares resulting from road censuses were modelled with broad-scale explanatory variables obtained from satellite imagery, thematic digital cartography, climatic data and spatial coordinates. The occurrence model incorporated mainly climatic variables and had a good discrimination ability, while the abundance model incorporated mainly land-use variables and had a lower explanatory power (r 2 =0.14). The predictions somewhat overestimated the results of the censuses, and this agrees with the decline of population size and range observed for this species in the Iberian peninsula. These models are relevant in the conservation of the species: first, they suggest the limiting factors for red kite in the Iberian peninsula, and, second, they generate predictive maps pointing out both areas in which conservation problems may be acute (suitable locations that are unoccupied), and areas where no data is available but the red kite is likely to be present (thus guiding further survey and research). # 2003 Elsevier Science Ltd. All rights reserved.

Adaptation vs. constraint : intraclutch egg-mass variation in birds

1. Intraclutch egg-mass variation may be determined by nutritional constraints during the laying period, or may be adaptive. These hypotheses are not mutually exclusive, and may act simultaneously on the same species. For this study, egg mass variation was analysed in the black kite, Milvus migrans (Bodd.), a mid-sized Falconiforme. 2. Egg size showed consistent patterns of variation with laying order and clutch size (2-3 eggs); egg size was larger in three-egg clutches, smaller in last-laid eggs, and relatively smaller in last-laid eggs of three-egg clutches. 3. Inexperienced breeders laid smaller eggs. There were no significant effects of year or laying date on egg size, once the confounding effect of breeder experience was removed. 4. Egg size affected hatchability only in two-egg clutches, and it affected the probability of survival of last-hatched chicks, after the confounding effects of hatching order and breeder experience were removed. There was no significant effect of egg size on growth rates or asymptotic body size. 5. The relative sizes of last-laid eggs and of first-laid eggs were not correlated with hatching asynchrony. 6. Factors reflecting the degree of nutritional constraint during laying (year, laying date, breeder experience) did not affect the degree of intraclutch egg-size asymmetry. The slight intraclutch egg-mass variation in this species (less than 0.5% of female weight) cannot impose serious energy constraints. Pairs nesting in high-quality territories laid clutches with relatively large last-laid eggs, which could be an adaptive variation of egg size to food availability. 7. Although there may be nutritional constraints on egg size at the time of laying, intraclutch egg-size variation in black kites cannot be explained exclusively by this factor. Rather, the variation may reflect distribution of resources among eggs, based on their reproductive value relative to laying order. This is determined by higher mortality of last-hatched chicks and lower hatchability of first-laid eggs in three-egg clutches. Also, it may be a component of the brood reduction strategy of raptors. 8. Relative importance of nutritional constraints or adaptation in determining intraclutch egg-size variation may depend on life history traits of each species, mainly on how the resources for laying are gathered. Adaptive patterns could exist in species storing most of the resources in the prelaying period, while nutritional constraints could hamper the appearance of any adaptive variation in species gathering those resources during the laying period.