Tomás Pérez-Contreras

Trade-off between immunocompetence and growth in magpies: an experimental study

A trade–off between immunity and growth has repeatedly been suggested, mainly based on laboratory and poultry science, but also from experiments where parasitism intensity was manipulated in field bird populations. However, as resource allocation to different activities (or organs) during growth is difficult to manipulate, this trade–off has only been experimentally tested by studying the effects of non–pathogenic antigens. By providing some nestling magpies (Pica pica) with methionine, a sulphur amino acid that specifically enhances T–cell immune response in chickens, we investigated this trade–off by directly affecting allocation of limited resources during growth. Results were in accordance with the hypothetical trade–off because nestlings fed with methionine showed a lower growth rate during the four days of methionine administration, but a larger response when fledglings were challenged with phytohaemagglutinin (a measure of the intensity of T–lymphocyte–mediated immune responsiveness) than control nestlings. Surprisingly, we found that control and experimental nestlings fledged with similar body mass, size and condition, but experimental nestlings suffered less from blood parasites (Haemoproteus) and had fewer lymphocytes (a widely used measure of health status) than control nestlings, suggesting a negative effect of blood parasites or other pathogens on nestling growth.

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

Abstract A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos.

Dark Nests and Conspicuousness in Color Patterns of Nestlings of Altricial Birds

Nests of altricial birds exhibit variable spectral properties that may affect the efficacy (conspicuousness) of the colored begging traits that a nestling displays to its parents. Here we explored whether selection for efficient perception has favored the evolution of nestling color designs that maximizes nestling detectability in variable light environments. Visual models were used to estimate how parents perceive the coloration of mouths, flanges, heads, and breasts of nestlings within their nest in 21 species of European birds. We show that the largest chromatic and achromatic contrasts against the nest background appeared for nestling mouths and flanges, respectively. Nestlings of open‐nesting species showed a larger general achromatic contrast with the nest than did nestlings of hole‐nesting species. However, nestlings of hole nesters showed a more evident achromatic contrast between flanges and other traits than did nestlings of open nesters. In addition, species with larger clutch sizes showed larger general achromatic contrasts with the nest. Gaping traits of open‐nesting species contrasting with the nest background were better perceived under rich light regimes than under poor ones. These findings are consistent with a scenario in which selection for nestling detectability in dark environments has favored the evolution of particular achromatic components of gape coloration but also nestling traits that enhance signal efficacy by maximizing color contrasts within a nestling.

Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor)

Many colourful sexually selected signals in animals are carotenoid-dependent and, because carotenoids function as antiradicals and immunostimulating molecules, carotenoid-dependent signals may honestly reflect the health state of individuals. Some others nutrients like vitamin A may also enhance health and colouration, but these have rarely been tested alongside carotenoids in colourful birds. Here, we examined whether beak colour of the spotless starling (Sturnus unicolor) reflected circulating levels of carotenoids and/or vitamin A (retinol). Spotless starlings are polygynous, sexually dimorphic birds (i.e. length of chest feathers). The tip of the beaks of male and female spotless starlings is more intensely coloured at the beginning of the breeding season and becomes dull after mating, which may suggest a sexual function. We found that females have a more intensely coloured beak and higher plasma carotenoid concentration than males during mating, and, despite the finding that carotenoid and vitamin A levels were not significantly related; colour intensity was positively correlated with plasma concentration of carotenoids and vitamin A in both sexes. However, adult beak coloration was not associated with carotenoid and vitamin A concentrations after nestlings were hatched. Therefore, beak colouration of spotless starlings provides information about circulating levels of carotenoids and vitamins during the mating season and may potentially function as a reliable signal of physiological status in the context of sexual selection.

Is the relation between colour and immune response mediated by nutritional condition in spotless starling nestlings

The hypothesis that nestling coloration is important for parenteoffspring communication, because it influences parental feeding decisions, has received strong experimental support. In European starlings, Sturnus vulgaris, and Alpine swifts, Apus melba, manipulation of ultraviolet reflectance of nestlings’ mouth and skin affected the amount of food parents provided, and skin brightness of starling nestlings predicted their T-cell-mediated immune response. Therefore, a link between nestling coloration and immunity, mediated by parental effort, was suggested. We explored this hypothesis by experimentally feeding some spotless starling, Sturnus unicolor, nestlings while leaving others in the same nest as a control. First, we found a significant effect of food supplementation on nestlings’ immune response, which is a requirement for the hypothesis. Second, we confirmed in spotless starlings the association between skin brightness and ability to raise an immune response. However, this correlation disappeared when we controlled for between-nest variation. These results suggest that parental feeding preference is not the only factor explaining nestling immunity, and that covariation between mean brood nestling coloration and parental quality, and/or intrinsic (i.e. genetic) quality of nestlings, may explain the association between immunity and coloration of nestlings. Finally, within-nest variation in nestling coloration partially explained immune responses because food supplementation had more effect on nestlings with brighter skin. We discuss these results as possible evidence of nestling coloration partially reflecting intrinsic characteristics that affect both ability to produce efficient immune responses and parental feeding preferences.

Benefits associated with escalated begging behaviour of black-billed magpie nestlings overcompensate the associated energetic costs

SUMMARY Several experimental results support the existence of costs associated with exaggerated begging behaviour, which are assumed by some theoretical models of honest signalling in parent–offspring communication. However, to understand how honest begging behaviour is evolutionarily maintained in nature, the long-term cost–benefit output associated with exaggerated signals should also be estimated. As far as we know, the net cost–benefit balance of begging display has not previously been explored. Here, we used an appetite stimulant, cyproheptadine hydrochloride, to increase the feeling of hunger in some magpie nestlings. Supporting the use of cyproheptadine to manipulate hunger level and thereby begging behaviour, we found that experimental nestlings increased the frequency of begging and received more food than their control nestmates. Contrary to the expectation that physiological costs per se counteract the associated benefits of escalated begging signals, we found that near-fledging experimental magpies showed a better physical condition than control nestlings. These findings stress the interesting question of why magpie nestlings do not show to adults an escalated level of hunger if it implies an advantage. We discuss the responsibility of inclusive fitness costs and indirect genetic effects for the maintenance of honesty in parent–offspring communication.

Male spotless starlings adjust feeding effort based on egg spots revealing ectoparasite load

Parents may vary their parental behaviour and investment in reproduction in response to parasite-induced changes in the fitness prospects of their offspring. Thus, parents may use the physical condition of their offspring, or any other trait related to parasite load, to adjust parental effort. The immaculate eggs of the spotless starling, Sturnus unicolor , often become densely spotted owing to the activity of the ectoparasite carnid fly Carnus hemapterus . Spot density anticipates the intensity of fly infestation suffered by nestlings and, therefore, may serve as a cue for parents to adjust reproductive investment. By cleaning spots produced by C. hemapterus on eggs of spotless starlings, we manipulated the parasites traces revealing its presence in broods of starlings, without modifying the level of infestation, to test whether parents use these signals to adjust reproductive effort. We found support for the hypothetical negative effect of Carnus flies since nestlings raised in nests with a higher fly load had lower body mass. The experimental egg cleaning during incubation did not change the intensity of carnid fly infestation during nestling development. However, it had a significant positive influence on paternal but not maternal effort. Our experimental results support the idea that spotless starling males adjust their effort in response to their perception of the fitness prospects of their nestlings as indirectly estimated by traces of parasites on the eggshells. As far as we know, this is the first evidence of the use of parasite traces to infer risk of parasitic infestation by animal hosts.

House sparrows selectively eject parasitic conspecific eggs and incur very low rejection costs

Most host species of obligate interspecific brood parasites are under strong selection because such parasitism, e.g., that involving evictor nestmates, is highly costly. Egg rejection is one of the most efficient host defences against avian brood parasites. Many hosts have thus evolved egg-recognition ability and rejection behaviour. However, this defensive mechanism has not evolved in most species where only intraspecific brood parasitism occurs, probably because (1) the eggs of conspecific females are very similar in appearance, making egg rejection less likely to emerge, and (2) such parasitism is frequently less costly than interspecific parasitism. Using a captive population of house sparrows (Passer domesticus) with a low breeding density, we here provide new evidence showing that this species actually has a fine capacity to discriminate conspecific eggs and to eject them (44.2% of foreign eggs ejected) while incurring very low rejection costs (4.2% of own eggs ejected). This result contradicts those previously found in high-density house sparrow populations in which very high rejection costs and very high clutch desertion rates were reported, probably as a consequence of intraspecific competition and infanticide provoked by the high breeding density. The house sparrow has only rarely been reported as the host of an interspecific brood parasite, which implies that it is a newly described example of an altricial species in which egg ejection has evolved and is maintained in response to intraspecific brood parasitism.

Spotless starlings rely on public information while visiting conspecific nests: an experiment

Animals may acquire information on potential breeding sites by prospecting, which allows future optimal selection of breeding territories. The reproductive success of conspecifics, as public information (PI), has been proposed as one of the cues that prospectors could gather and then use for future reproductive decisions. We experimentally decreased brood size in spotless starling nests to investigate whether this species gathers PI while visiting conspecific nests. We expected visiting frequency to decline with the experimental decrease in brood size because visitors are expected to prefer sites with high reproductive success and to spend more time at those sites to gain familiarity. Furthermore, the effect of the experimental manipulation was recorded at three different stages of the nestling period to establish the importance of the reliability of PI. Brood size decreased in direct relation to the manipulation and, consequently, parental feeding rates decreased too. Visiting frequency of starlings to conspecific nests was affected by the interaction between the experimental manipulation and the stage in the nestling period: visiting frequency increased from decreased to control nests at the end of the nestling period, not so strongly in the middle of that period and it was not affected by the manipulation at the beginning of it. This variation in visiting frequency seemed to be better explained by brood size than by parental provisioning rate. These results may be interpreted as spotless starlings visiting conspecific nests to gather PI, which seems to increase its informative value when its reliability does.

The cost of host egg damage caused by a brood parasite: experiments on great spotted cuckoos (Clamator glandarius) and magpies (Pica pica)

Abstract Adult great spotted cuckoos, Clamator glandarius, frequently damage one or more eggs of their magpie host, Pica pica, without removing or eating them. The presence of damaged host eggs could signal parasitism thereby increasing the probability that the parasitic egg is ejected. This hypothesis was tested by experimentally introducing a model cuckoo egg with or without damaged host eggs. Magpie responses to experimental parasitism did not differ significantly between treatments implying that damaged host eggs are not used by magpies to assess parasitism. We followed the fate of magpie eggs naturally damaged by the great spotted cuckoo or experimentally damaged by us. Host response was very similar for naturally or experimentally damaged host eggs, but varied significantly according to the type of egg damage, eggs being removed more frequently when pecked than crushed, while cracked eggs were never removed. However, the egg damage that most readily causes egg removal is albumen leakage.