Multiple coloured ornaments in male common kestrels: different mechanisms to convey quality

The simultaneous exhibition of more than one secondary sexual trait is a widespread phenomenon in nature, though it has rarely been explored. It has been proposed that different ornaments may convey complementary or back-up information about a single aspect of individual quality (redundancy hypothesis) or that each ornament may convey unique information (multiple-messages hypothesis). During a 5-year period, we measured several carotenoid-based (eye ring, bill cere and tarsi skin) and melanin-based (head, back, rump and tail feathers) potential ornamental colours in male common kestrels. We analysed whether multiple ornaments can convey different or related information about individual quality. We explored whether different ornaments can express different information depending on the pigment (carotenoids or melanins), the time-scale over which the ornament can change (dynamic vs. static) and the season of the year when the ornament is formed. We found that both melanin- and carotenoid- based traits correlated with indexes of quality, including body condition, body condition of their partners and laying date. However, not all ornaments correlated with the same measures of quality. In addition, some ornaments were intercorrelated within the same individuals while others were not. These results suggest that different ornaments can convey information about different qualities, as predicted by the multiple-messages hypothesis. In addition, this study suggests that the predominant pigment (e.g. carotenoid vs. melanin, eumelanin vs. pheomelanin), the time-scale over which the trait is developed (static feathers vs. dynamic skin) and the season of the year at which the ornament is produced can be potential mechanisms to convey different messages in male common kestrels.     

Condition-dependent expression of melanin-based coloration in the Eurasian kestrel

Melanin is the most common pigment in animal integuments and is responsible for some of the most striking ornaments. A central tenet of sexual selection theory states that melanin-based traits can signal absolute individual quality in any environment only if their expression is condition-dependent. Significant costs imposed by an ornament would ensure that only the highest quality individuals display the most exaggerated forms of the signal. Firm evidence that melanin-based traits can be condition-dependent is still rare in birds. In an experimental test of this central assumption, we report condition-dependent expression of a melanin-based trait in the Eurasian kestrel (Falco tinnunculus). We manipulated nestling body condition by reducing or increasing the number of nestlings soon after hatching. A few days before fledging, we measured the width of sub-terminal black bands on the tail feathers. Compared to nestlings from enlarged broods, individuals raised in reduced broods were in better condition and thereby developed larger sub-terminal bands. Furthermore, in 2?years, first-born nestlings also developed larger sub-terminal bands than their younger siblings that are in poorer condition. This demonstrates that expression of melanin-based traits can be condition-dependent.     

Melanin-based coloration covaries with ovary size in an age-specific manner in the barn owl

While the adaptive function of black eumelanin-based coloration is relatively well known, the function of reddish-brown pheomelanin-based coloration is still unclear. Only a few studies have shown or suggested that the degree of reddish-brownness is associated with predator–prey relationships, reproductive parameters, growth rate and immunity. To gain insight into the physiological correlates of melanin-based coloration, I collected barn owl (Tyto alba) cadavers and examined the covariation between this colour trait and ovary size, an organ that increases in size before reproduction. A relationship is expected because melanin-based coloration often covaries with sexual activity. The results showed that reddish-brown juveniles had larger ovaries than whiter juveniles particularly in individuals in poor condition and outside the breeding season, while in birds older than 2 years lightly coloured females had larger ovaries than reddish-brown conspecifics. As barn owls become less reddish-brown between the first and second year of age, the present study suggests that reddish-brown pheomelanic and whitish colorations are associated with juvenile- and adult-specific adaptations, respectively.     

Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.     

Ornamental comb colour predicts T-cell-mediated immunity in male red grouse <Emphasis Type="Italic">Lagopus lagopus scoticus</Emphasis>

Sexual ornaments might reliably indicate the ability to cope with parasites and diseases, and a better ability to mount a primary inflammatory response to a novel challenge. Carotenoid-based ornaments are amongst the commonest sexual signals of birds and often influence mate choice. Because carotenoids are immuno-stimulants, signallers may trade-off allocating these to ornamental colouration or using them for immune responses, so carotenoid-based ornaments might be particularly useful as honest indicators of immuno-compentence. Tetraonid birds, such as the red grouse Lagopus lagopus scoticus, exhibit supra-orbital yellow-red combs, a conspicuous ornament which functions in intra- and inter-sexual selection. The colour of combs is due to epidermal pigmentation by carotenoids, while their size is testosterone-dependent. In this study, I investigated whether comb characteristics, and in particular, comb colour, indicated immuno-competence in free-living male red grouse. I assessed T-cell-mediated immunity using a standardised challenge with phytohaemagglutinin. Red grouse combs reflect in the red and in the ultraviolet spectrum of light, which is not visible to humans but that grouse most likely see, so I measured comb colour across the whole bird visible spectrum (300-700 nm) using a reflectance spectrometer. I found that males with bigger and redder combs, but with less ultraviolet reflectance, had greater T-cell-mediated immune response. Comb colour predicted T-cell-mediated immune response better than comb size, indicating that the carotenoid-based colouration of this ornament might reliably signal this aspect of male quality.     

Female ornamentation and territorial conflicts in collared flycatchers (Ficedula albicollis)

Female ornaments in species with conventional sex roles often indicate individual quality, but the evolutionary forces maintaining them are less clear. Sexual competition for breeding opportunities may represent an important role for female signals, especially in polygynous species, but there is little experimental evidence for this. The wing patch size (WPS) of female collared flycatchers indicates age and body condition and predicts social mating patterns. We challenged nest-building females with decoy females of varying WPS and found that the aggressive response of residents increased with decoy WPS, suggesting a role for this female ornament in territorial competition. Our results explain why female WPS predicts territorial distances when mated to a polygynous male and indicate that the role of WPS in female competitive interactions is similar to that in males of the same population.     

Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health

Despite a reasonable scientific interest in sexual selection, the general principles of health signalisation via ornamental traits remain still unresolved in many aspects. This is also true for the mechanism preserving honesty of carotenoid-based signals. Although it is widely accepted that this type of ornamentation reflects an allocation trade-off between the physiological utilisation of carotenoids (mainly in antioxidative processes) and their deposition in ornaments, some recent evidence suggests more complex interactions. Here, we further develop the models currently proposed to explain the honesty of carotenoid-based signalisation of heath status by adding the handicap principle concept regulated by testosterone. We propose that under certain circumstances carotenoids may be dangerous for the organism because they easily transform into toxic cleavage products. When reserves of other protective antioxidants are insufficient, physiological trade-offs may exist between maintenance of carotenoids for ornament expression and their removal from the body. Furthermore, we suggest that testosterone which enhances ornamentation by increasing carotenoid bioavailability may also promote oxidative stress and hence lower antioxidant reserves. The presence of high levels of carotenoids required for high-quality ornament expression may therefore represent a handicap and only individuals in prime health could afford to produce elaborate colourful ornaments. Although further testing is needed, this ‘carotenoid maintenance handicap’ hypothesis may offer a new insight into the physiological aspects of the relationship between carotenoid function, immunity and ornamentation.     

The fractal dimension of a conspicuous ornament varies with mating status and shows assortative mating in wild red-legged partridges (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Complex body designs, such as plumage ornaments in birds, can be described by fractal geometry. These complex patterns could have a role as visual signals during courtship and social interactions, but an empirical validation in the wild is currently lacking. Here, we investigated whether the fractal dimension (FD) of a complex plumage pattern displayed by red-legged partridges Alectoris rufa could function as a potential sexual signal. We captured wild birds early in the breeding season and tested if mated and unmated birds differed in the FD of their conspicuous melanin-based black bib. We also tested if the FD of the black bib was correlated within the pair, looking for evidence of assortative mating based on the expression of this trait. We simultaneously assessed similar effects in other ornamental traits (black bib size, white throat patch and black flank band surface, redness of the eye rings and bill). Mated birds showed higher black bib FD values than unmated ones. Mated males, but not females, also displayed a larger black bib. Moreover, the black bib FD (but not the trait size) and the white throat patch surface showed assortative mating. Finally, females with higher black bib FD showed smaller black flank band surface, suggesting a trade-off in the expression of the two melanin-pigmented plumage traits. This provides unique and novel indication for the shape complexity of a pigmented trait, here described by its fractal dimension, to be potentially under sexual selection in a wild animal.     

A link between eumelanism and calcium physiology in the barn owl

In many animals, melanin-based coloration is strongly heritable and is largely insensitive to the environment and body condition. According to the handicap principle, such a trait may not reveal individual quality because the production of different melanin-based colorations often entails similar costs. However, a recent study showed that the production of eumelanin pigments requires relatively large amounts of calcium, potentially implying that melanin-based coloration is associated with physiological processes requiring calcium. If this is the case, eumelanism may be traded-off against other metabolic processes that require the same elements. We used a correlative approach to examine, for the first time, this proposition in the barn owl, a species in which individuals vary in the amount, size, and blackness of eumelanic spots. For this purpose, we measured calcium concentration in the left humerus of 85 dead owls. Results showed that the humeri of heavily spotted individuals had a higher concentration of calcium. This suggests either that plumage spottiness signals the ability to absorb calcium from the diet for both eumelanin production and storage in bones, or that lightly spotted individuals use more calcium for metabolic processes at the expense of calcium storage in bones. Our study supports the idea that eumelanin-based coloration is associated with a number of physiological processes requiring calcium.     

The ornament�Ccondition relationship varies with parasite abundance at population level in a female bird

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.     

Trophic specialisations in alternative heterochronic morphs

Polymorphisms are suspected of reducing competition among conspecifics in heterogeneous environments by allowing differential resource use. However the adaptive significance of alternative morphs has been poorly documented. The aim of this study is to determine food partitioning of two heterochronic morphs of the Alpine newt, Triturus alpestris, in mountain lakes. The morphs differ in the functional morphology of their feeding apparatus. Only paedomorphs are able to expel water during prey suction behind the mouth through gill slits. We observed a substantial trophic differentiation between morphs in all lakes. Paedomorphs preyed mainly on plankton, whereas metamorphs foraged on terrestrial invertebrates that fell upon the water surface. This resource partitioning may facilitate the coexistence of the alternative morphs in lakes devoid of vertebrate competitors. Food diversity may thus favour the evolutionary maintenance of facultative polymorphism in natural populations.     

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.     

Sex- and age-related differences in the timing and body condition of migrating Reed Warblers Acrocephalus scirpaceus and Sedge Warblers Acrocephalus schoenobaenus

The migration strategies of birds may vary strongly between species and also between age and/or sex groups. We studied the autumn migration and body condition of molecularly sexed Reed Warblers Acrocephalus scirpaceus and Sedge Warblers Acrocephalus schoenobaenus (211 and 208 ind., respectively) at a stopover site on Lake Druzno, Northern Poland, in 2008. Immature male Reed Warblers were caught significantly later than females (median dates 9 days later), but in the Sedge Warbler, both sexes of immatures migrated at about the same time. Adult males and females of both species did not differ in their time of migration. Adult and immature males of both species were larger (wing length and body mass) than females. In both species, fat reserves were similar in both sexes of both age classes. Adults of both sexes of Reed and Sedge Warbler were generally caught earlier than immatures. In both species, the body mass and fat reserves of immatures were generally less than in adults. The autumn protogyny of immature Reed Warblers may allow smaller females to limit competition with bigger males during migration and at the wintering grounds. In the Sedge Warbler, which tends to match its migration to peak of occurrence of superabundant food at stopover sites, both sexes gain an advantage from migrating at the same time. Since part of the measured wing length variation in both species was explained by sex differences, temporal trends in wing length recorded at stopover sites should be interpreted with caution.     

Female feeding regime and polyandry in the nuptially feeding nursery web spider, Pisaura mirabilis

We examined the influence of female feeding regime on polyandry in the nuptially feeding nursery web spider (Pisaura mirabilis). In this species, the nuptial gift, a dead prey item wrapped in the male’s silk, is physically separate from the ejaculate. We manipulated female feeding regime (starved or fed) and the presence or absence of a gift with three successive males to test direct-benefits hypotheses (nuptial gift or sperm supply) for the expression of polyandry. The presence of a gift was necessary for copulation, as no male without a gift successfully copulated. Female mating behavior most strongly supports polyandry due to the accumulation of gifted food items (“nuptial gift” direct-benefits hypothesis). Starved females that were presented with a gift accepted significantly more gifts and inseminations than fed females. Most starved females (74%) copulated two or more times, as opposed to only 3% of the fed females. Nearly all of the females that accepted a gift subsequently copulated. The nuptial gift item seems to function as male mating effort and females appear to receive multiple matings as part of a feeding strategy.     

Immune activation affects chemical sexual ornaments of male Iberian wall lizards

Many animals use chemical signals in sexual selection, but it is not clear how these sexual traits might have evolved to signal honestly male condition. It is possible that there is a trade-off between maintaining the immune system and the elaboration of ornaments. We experimentally challenged the immune system of male Iberian wall lizards, Podarcis hispanica, with a bacterial antigen (lipopolysaccharide), without pathogenic effects, to explore whether the immune activation affected chemical ornaments. Immune activation resulted in decreased proportions of a major chemical in femoral secretions (cholesta-5,7-dien-3-ol = provitamin D(3)) known to be selected in scent of males by females and which active form (vitamin D) has a variety of important effects on immune system function. This result suggests the existence of a potential trade-off between physiological regulation of the immune system and the allocation of essential nutrients (vitamins) to sexual chemical ornaments in male lizards.     

Hunting behaviour and breeding performance of northern goshawks Accipiter gentilis, in relation to resource availability, sex, age and morphology

Animal territories that differ in the availability of food resources will require (all other things being equal) different levels of effort for successful reproduction. As a consequence, breeding performance may become most strongly dependent on factors that affect individual foraging where resources are poor. We investigated potential links between foraging behaviour, reproductive performance and morphology in a goshawk Accipiter gentilis population, which experienced markedly different resource levels in two different parts of the study area (rabbit-rich vs. rabbit-poor areas). Our analyses revealed (1) that rabbit abundance positively affected male reproductive output; (2) that age, size and rabbit abundance (during winter) positively affected different components of female reproductive output; (3) that foraging movements were inversely affected by rabbit abundance for both sexes (for females, this may mainly have reflected poor provisioning by males in the rabbit-poor area); (4) that younger breeders (both in males and females) tended to move over larger distances than older individuals (which may have reflected both a lack of hunting experience and mate searching); and (5) that male body size (wing length) showed some covariation with resource conditions (suggesting possible adaptations to hunting agile avian prey in the rabbit-poor area). Although we are unable to establish firm causal relationships with our observational data set, our results provide an example of how territory quality (here, food abundance) and individual features (here, age and morphology) may combine to shape a predator's foraging behaviour and, ultimately, its breeding performance.     

Development and growth in synanthropic species: plasticity and constraints

Urbanization poses serious extinction risks, yet some species thrive in urban environments. This may be due to a pronounced developmental plasticity in these taxa, since phenotypically, plastic organisms may better adjust to unpredictable urban food resources. We studied phenotypic plasticity in Nuctenea umbratica, a common European forest and urban vegetation spider. We subjected spiderlings to low (LF), medium (MF) and high (HF) food treatments and documented their growth and developmental trajectories into adulthood. Spiders from the three treatments had comparable numbers of instars and growth ratios, but differed in developmental periods. Longest developing LF spiders (♀?=?390, ♂?=?320 days) had the smallest adults, but MF (♀?=?300, ♂?=?240 days) and HF (♀?=?240, ♂?=?210 days) spiders reached comparable adult sizes through shorter development. While males and females had comparable instar numbers, females had longer development, higher growth ratios, adult sizes and mass; and while males adjusted their moulting to food availability, female moulting depended on specific mass, not food treatment. We discussed the patterns of Nuctenea sex-specific development and compared our results with published data on two other Holarctic urban colonizers (Larinioides sclopetarius, Zygiella x-notata) exhibiting high plasticity and fast generation turn-over. We conclude that despite relatively unconstrained developmental time in the laboratory enabling Nuctenea to achieve maximal mass and size—main female fitness proxies—their relatively fixed growth ratio and long generation turn-over may explain their lower success in urban environments.     

Eisen und Eisenversorgung des Warmblüter-Organismus

An adult man contains roughly 4-5 g of iron. Nearly 70% of this amount is present in hemoglobin and myoglobin. About 11% is accounted for by iron enzymes, e.g., heme enzymes that play a decisive role in cellular metabolism. Almost 19% of the body iron are deposed in iron stores. The distribution of iron in the body to the tissues and organs is handled by transferrin, a protein that binds iron so tightly that scarcely any free, i.e., ionized and hence toxic iron can exist. Since iron can only be excreted to an insignificant extent either in the urine or bile, the metabolism of iron is balanced almost exclusively by the absorption of this metal from food. This is especially true in the case of iron deficiency, e.g., in the young and growing organism, in pregnant females, or after iron loss.     

Sex-dependent obesogenic effect of tetracycline on Drosophila melanogaster deteriorated by dysrhythmia

Antibiotics have been identified as obesogens contributing to the prevalence of obesity. Moreover, their environmental toxicity shows sex dependence, which might also explain the sex-dependent obesity observed. Yet, the direct evidence for such a connection and the underlying mechanisms remain to be explored. In this study, the effects of tetracycline, which is a representative antibiotic found in both environmental and food samples, on Drosophila melanogaster were studied with consideration of both sex and circadian rhythms (represented by the eclosion rhythm). Results showed that in morning-eclosed adults, tetracycline significantly stimulated the body weight of females (AM females) at 0.1, 1.0, 10.0 and 100.0 µg/L, while tetracycline only stimulated the body weight of males (AM males) at 1.0 µg/L. In the afternoon-eclosed adults, tetracycline significantly stimulated the body weight of females (PM females) at 0.1, 1.0 and 100.0 µg/L, while it showed more significant stimulation in males (PM males) at all concentrations. Notably, the stimulation levels were the greatest in PM males among all the adults. The results showed the clear sex dependence of the obesogenic effects, which was diminished by dysrhythmia. Further biochemical assays and clustering analysis suggested that the sex- and rhythm-dependent obesogenic effects resulted from the bias toward lipogenesis against lipolysis. Moreover, they were closely related to the preference for the energy storage forms of lactate and glucose and also to the presence of excessive insulin, with the involvement of glucolipid metabolism. Such relationships indicated potential bridges between the obesogenic effects of pollutants and other diseases, e.g., cancer and diabetes.