Rita Hargitai

Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts

Common cuckoo (Cuculus canorus) parasitism drastically reduces the reproductive success of their hosts and selects for host discrimination of cuckoo eggs. In a second stage of anti-parasite adaptation, once cuckoos can lay eggs that mimic those of their hosts, a high uniformity of host egg appearance within a clutch may favour cuckoo egg discrimination. Comparative evidence provides indirect support for this hypothesis although experimental support is currently lacking. Here, we studied the effect of experimentally decreased uniformity of host egg appearance on cuckoo egg discrimination by great reed warbler (Acrocephalus arundinaceus) hosts in a population in which long-term cuckoo parasitism has led to high levels of cuckoo–host egg mimesis. We manipulated host clutch uniformity by adding extra spots to fresh host eggs just after they were laid. Rejection of non-mimetic experimental eggs added to these nests was compared with those in control nests in which uniformity was not altered. Previously, by over-painting real spots in a control group of nests, we showed a negligible effect of our paints on hosts’ perception of their eggs. We show that for the great reed warbler, non-mimetic experimental eggs were relatively more tolerated in experimental nests, i.e. with lower uniformity (40%) than in control nests (5%). This is the first experimental study, to our knowledge, which demonstrates a reduced discrimination of foreign eggs as a consequence of an increase of egg phenotypes variation perception in a cuckoo host.

Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order

Birds may influence the fitness of their offspring by transmission of different amounts of carotenoids to their eggs. Carotenoids play crucial roles in antioxidant protection and immune defence mechanisms, but they may be available to females in limiting amounts. Therefore, their allocation to the eggs may be influenced by the female’s condition, age and environmental circumstances. Furthermore, the quality of the male parent, which affects the reproductive value of the offspring, may also influence this investment. In this correlational study, we investigated proximate and ultimate factors that may lead to variation in yolk lutein, zeaxanthin and β-carotene concentrations among and within clutches of a wild passerine, the collared flycatcher (Ficedula albicollis). We found that carotenoid concentration was positively associated with caterpillar supply at the time of egg formation, which suggests a proximate constraint of carotenoid availability on yolk composition. Neither female condition, body size, age, nor male plumage ornamentation, age and body size correlated with carotenoid deposition. Yolk β-carotene concentration was found to be positively linked to yolk testosterone concentration. We suggest that females allocated more β-carotene to their eggs to mitigate the potentially detrimental effects of elevated steroid concentration. We found that concentration of β-carotene increased with laying order. The possible function of this pattern may be to enhance the resistance to oxidative stress and pathogens of the disadvantaged last-hatching nestling, suggesting that collared flycatchers pursue a compensatory, “brood survival” strategy.

EFFECTS OF ENVIRONMENTAL CONDITIONS AND PARENTAL QUALITY ON INTER- AND INTRACLUTCH EGG-SIZE VARIATION IN THE COLLARED FLYCATCHER (FICEDULA ALBICOLLIS)

Abstract Egg size is a particularly important life-history trait mediating maternal influences on offspring phenotype. Females can vary their egg-size investment in relation to environmental circumstances, their own breeding condition, and the quality of their mate. Here we analyzed inter- and intraclutch variation in egg size in the Collared Flycatcher (Ficedula albicollis) on the basis of eight years of data. According to our results, mean egg size increased with female condition, but did not differ among young, middle-aged, and old females. The male’s age, body size, and forehead patch size did not influence egg size; thus, we found no evidence for differential investment in egg size in relation to male quality. We found no effect of laying date on egg size when controlling for ambient temperature during the egg formation period, yet temperature had a significant effect on egg size. That result indicates proximate constraints on egg formation. Furthermore, we report on annual differences in intraclutch egg-size variation. Egg size increased within clutches in years with a warm prelaying period; whereas in years when the weather during that period was cold, there was no significant intraclutch trend. Proximate considerations seem to explain the observed patterns of intraclutch egg-size variation; however, we cannot reject the adaptive explanation. Mean egg size and intraclutch egg-size variation were unrelated to clutch size. Therefore, we found no evidence for a trade-off between size and number of eggs within a clutch.

Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher

Offspring survival can be influenced by resources allocated to eggs, which in turn may be affected by the environmental factors the mother experiences during egg formation. In this study, we investigated whether experimentally elevated social interactions and number of neighbouring pairs influence yolk composition of collared flycatchers (Ficedula albicollis). Social challenge was simulated by presentation of a conspecific female. Experimental females spent more time near the cage and produced eggs with higher androgen concentration, but local breeding density did not affect yolk androgen level. Moreover, we found that females exposed to more intra-specific interactions and those that bred at higher density produced eggs with smaller yolk. These females may be more constrained in foraging time due to more frequent social encounters, and there might be increased competition for food at areas of higher density. In contrast, the present study did not reveal any evidence for the effect of social environment on yolk antioxidant and immunoglobulin levels. However, we found that yolk lutein and immunoglobulin concentrations were related to the female’s H/L ratio. Also, yolk lutein and α-tocopherol levels showed a seasonal increase and were positively related to the female’s plasma carotenoid level. Mothers may incur significant costs by transferring these compounds into the eggs, thus only females in good physiological condition and those that lay eggs later, when food is probably more abundant, could allocate higher amounts to the eggs without compromising their defence mechanisms. Our results suggest that environmental circumstances during egg formation can influence conditions for embryonic development.

Phenotypic plasticity in a conspicuous female plumage trait: information content and mating patterns

Explaining sexual ornamentation in the limiting sex, usually females, requires information on the proximate background of ornaments and their consequences for sexual selection. Phenotypic variation within individuals has received little attention in either of these research directions. We used 6 years of data to examine the information content and potential role of white wing patch size in female collared flycatchers, Ficedula albicollis. Female wing patch size differed among years. Yearling females had smaller wing patches than older females. The negative effect of original patch size on intraindividual patch size change was stronger in yearling than in older birds, which may reflect an age-dependent trade-off. Change in wing patch size was strongly positively related to the summer North Atlantic Oscillation (NAO) index. Clutch size laid in the previous breeding season had a negative effect on patch size change, but only in high-NAO years. Thus, the immediate effect of poor climate during moult apparently overrode the more indirect influence of reproductive effort. Two sexually selected ornaments of mates were unrelated to female wing patch size at the population level, but intraindividual changes of female wing patch size significantly predicted differences in wing patch size between mates obtained in the 2 years. Our data suggest that significant mating advantages to more ornamented females may not be detected from population-level mating patterns. Research on potential female ornaments should also pay more attention to age-dependent phenotypic plasticity, the trade-off between current and future ornament size and the costs of reproduction to apparent future attractiveness.

Shell thickness and pore density in relation to shell colouration, female characteristics, and environmental factors in the Collared Flycatcher Ficedula albicollis

Avian eggshell structure may have important consequences for embryonic growth and development, but relatively little is known about the factors responsible for variation in eggshell characteristics of wild birds. In this paper, we explored potential causes of variation in eggshell colour and structure (shell thickness and porosity) in the Collared Flycatcher (Ficedula albicollis). We analysed if eggshell colour is affected by shell structure or pigment level, and whether female traits, laying date, local breeding density, and clutch size affect shell thickness and pore density. We found that eggshell blue-green and UV colours were unrelated to shell thickness, pore density and egg size. Eggs with higher concentration of biliverdin showed lower UV reflection and higher reflection in the blue-green part of the spectrum. We found that females in better nutritional condition, indicated by their higher mass controlled for tarsus length, laid eggs with thicker shells. It is possible that females in better condition have more time available for searching calcium-rich food, and thus could produce eggs with stronger shells. However, female physical characteristics had no significant relationships with shell porosity. In contrast to our expectation, shell thickness and pore density were unrelated to local breeding density and laying date, though very late and repeat clutches were not sampled in our study. However, we found that eggs in larger clutches had lower pore density than eggs in smaller clutches, which may be expected if the rate of water loss and nest humidity are to remain constant in clutches of different egg numbers.ZusammenfassungDie Struktur der Eischale von Vögeln kann wichtige Folgen für das Wachstum und die Entwicklung der Embryonen haben, doch über die Faktoren, die für Variation in den Eigenschaften der Eischale bei freilebenden Vögeln verantwortlich sind, ist relativ wenig bekannt. In diesem Artikel haben wir mögliche Gründe für die Variation in Eischalenfarbe und -struktur (Schalendicke und Porosität) beim Halsbandschnäpper (Ficedula albicollis) untersucht. Wir haben analysiert, ob die Eischalenfarbe von der Schalenstruktur oder dem Pigmentgehalt beeinflusst wird und ob Weibchenmerkmale, Legedatum, lokale Brutpaardichte und Gelegegröße die Schalendicke und Porendichte beeinflussen. Wir fanden, dass blaugrüne und ultraviolette Farben der Eischale nicht mit der Schalendicke, Porendichte und Eigröße zusammenhingen. Eier mit einer höheren Biliverdinkonzentration zeigten eine geringere UV-Reflexion und stärkere Reflexion im blaugrünen Bereich des Spektrums. Wir fanden, dass Weibchen in besserem Ernährungszustand, angezeigt durch ihre höhere Körpermasse korrigiert für Tarsuslänge, Eier mit dickerer Schale legten. Es ist möglich, dass Weibchen in besserer Kondition mehr Zeit haben, kalziumreiche Nahrung zu suchen, und daher Eier mit stärkerer Schale produzieren. Die Körpermerkmale der Weibchen standen jedoch in keiner signifikanten Beziehung zu der Schalenporosität. Entgegen unserer Erwartung standen Schalendicke und Porendichte nicht mit der lokalen Brutpaardichte und dem Legedatum in Zusammenhang, obwohl sehr späte Gelege und Nachgelege in unserer Studie nicht beprobt wurden. Wir fanden jedoch, dass Eier in größeren Gelegen eine geringere Porendichte hatten als Eier in kleineren Gelegen, was zu erwarten wäre, wenn die Wasserverlustrate und die Nestfeuchte in Gelegen mit unterschiedlicher Eizahl konstant blieben.

Effects of breeding habitat (woodland versus urban) and metal pollution on the egg characteristics of great tits (Parus major)

In an urban environment, birds are exposed to metals, which may accumulate in their tissues and cause oxidative stress. Female birds may eliminate these pollutants through depositing them into eggs, thus eggs become suitable bioindicators of pollution. In this study, we aimed to analyse whether eggshell spotting pattern, egg volume, eggshell thickness and egg yolk antioxidant (lutein, tocopherol, retinol and selenium) levels were related to the breeding area (woodland versus urban) and the metal levels in the eggshell of a small passerine species, the great tit (Parus major). In the urban habitat, soil and eggshells contained higher concentrations of metals, and soil calcium level was also higher than that in the woodland. Eggshell spotting intensity and egg volume did not differ between eggs laid in the woodland and the urban park, and these traits were not related to the metal levels of the eggshell, suggesting that these egg characteristics are not sensitive indicators of metal pollution. A more aggregated eggshell spotting distribution indicated a higher Cu concentration of the eggshell. We found that eggshells were thinner in the less polluted woodland habitat, which is likely due to the limited Ca availability of the woodland area. Great tit eggs laid in the urban environment had lower yolk lutein, retinol and selenium concentrations, however, as a possible compensation for these lower antioxidant levels, urban females deposited more tocopherol into the egg yolk. It appears that females from different breeding habitats may provide similar antioxidant protection for their offspring against oxidative damage by depositing different specific dietary antioxidants. Egg yolk lutein and retinol levels showed a negative relationship with lead concentration of the eggshell, which may suggest that lead had a negative impact on the amount of antioxidants available for embryos during development in great tits.

Darker eggshell spotting indicates lower yolk antioxidant level and poorer female quality in the Eurasian Great Tit (Parus major)

ABSTRACT Protoporphyrin pigment causes the red-brown eggshell colors; however, for many species, the function of this pigment is unknown. It has been proposed that eggshell pigmentation may strengthen the shell or that it may be a sexually selected signal, which advertises the quality of the female and that of her offspring to the male parent. In this study, we aimed to discover whether protoporphyrin-based eggshell pigmentation patterns of Eurasian Great Tits (Parus major) were related to female or egg quality. Additionally, we tested whether different methods of eggshell pigmentation estimation could be reliable predictors of eggshell protoporphyrin levels. We found that spot intensity, spot size, spotting coverage, and brown spot chroma indicated the protoporphyrin pigment concentration of the eggshell. Our results revealed that Eurasian Great Tit females that laid eggs with darker pigmentation had more lymphocytes in their circulation and had paler yellow breast and lower UV plumage reflectance, possibly indicating poorer health and individual quality. However, we did not find evidence that eggshell pigmentation patterns indicated the body condition, body size, or plasma oxidative status of females. Furthermore, we found that eggs with darker spots contained lower concentrations of antioxidants in the yolk. High protoporphyrin levels may be detrimental to females as they may cause oxidative damage, and this may be why birds that laid eggs with darker spots deposited lower amounts of antioxidants into the egg yolk. Shell spot darkness may also indicate territory quality, as females that laid smaller clutches also laid eggs with higher eggshell pigmentation levels. Thus, our results suggest that shell spot darkness may indicate the state of health of the female, egg yolk antioxidant level, and possibly also the quality of the territory.

Effects of environmental conditions on the egg mass, yolk antioxidant level, eggshell thickness and eggshell spotting patterns of Great Tits (Parus major)

AbstractAvian mothers can influence the fitness of their offspring by resource investment into the egg. Allocation of macro- and micronutrients into the eggs may be costly for the female, therefore, we expect that resource investment may be affected by the environmental and social conditions the mother experiences during egg formation. Here, we investigated whether environmental circumstances experienced by the reproducing female exert an influence on egg mass, yolk antioxidant (lutein and tocopherol) concentration, eggshell thickness, and the eggshell spotting patterns of Great Tits (Parus major). Our study showed that when caterpillars were less abundant, in colder weather and when breeding in an area of higher local breeding density, female Great Tits laid eggs of lower mass, suggesting that adverse environmental circumstances constrain the macronutrient investment into the eggs. However, we found no evidence that yolk antioxidant concentration and eggshell thickness were affected by environmental factors. Female Great Tits may use their endogenous stores or spend more time and energy in finding sufficient amounts of dietary antioxidants and calcium under unfavourable environmental conditions, which may have a cost effect on their own conditions. We found that birds that bred in the beginning of the season laid eggs with darker eggshell spots. Moreover, females laid more spotted eggs in colder weather and when breeding in higher density areas. Our results suggest that Great Tits deposit more of the potentially harmful pro-oxidant protoporphyrin pigment into the eggshell under unfavourable environmental conditions.ZusammenfassungAuswirkungen von Umweltbedingungen auf Eimasse, Antioxidantiengehalt des Dotters, Schalendicke und Fleckung der Eischale bei Kohlmeisen (Parus major) Vogelmütter können die Fitness ihrer Nachkommenschaft durch die Ressourcen beeinflussen, die sie in ein Ei investieren. Die Abgabe von Makro- und Mikronährstoffen an die Eier kann für das Weibchen kostspielig sein, daher ist zu erwarten, dass die Investition von Ressourcen durch Umweltbedingungen und soziale Faktoren beeinflusst wird, denen die Mutter während der Eibildung ausgesetzt ist. Hier untersuchten wir, inwieweit die Umweltbedingungen, denen das Weibchen während der Fortpflanzung ausgesetzt war, einen Einfluss auf die Eimasse, die Konzentration von Antioxidantien (Lutein und Tocopherol) im Dotter, die Schalendicke und die Fleckung der Eischalen von Kohlmeisen (Parusmajor) ausübten. Unsere Studie zeigte, dass Kohlmeisen-Weibchen in Zeiten geringeren Raupenangebots, bei kälterem Wetter und in Brutgebieten mit höherer lokaler Brutdichte Eier von geringerer Masse legten, was darauf hindeutet, dass ungünstige Umweltbedingungen die Investition von Makronährstoffen in die Eier beschränken können. Allerdings fanden wir keine Hinweise darauf, dass die Konzentration von Antioxidantien im Dotter und die Schalendicke durch Umweltfaktoren beeinflusst wurden. Unter ungünstigen Umweltbedingungen können Kohlmeisen-Weibchen körpereigene Reserven angreifen oder mehr Zeit und Energie auf die Suche nach ausreichenden Mengen nahrungsgebundener Antioxidantien und Kalzium aufwenden, was zu Lasten ihrer eigenen Kondition gehen kann. Wir stellten fest, dass früh in der Saison brütende Vögel Eier mit dunklerer Schalenfleckung legten. Außerdem legten die Weibchen bei kälterem Wetter und in dichter besetzten Brutgebieten mehr gefleckte Eier. Unsere Ergebnisse deuten an, dass Kohlmeisen unter ungünstigen Umweltbedingungen mehr des potenziell schädlichen prooxidativen Pigments Protoporphyrin in der Eischale ablagern.

Biliverdin- and protoporphyrin-based eggshell pigmentation in relation to antioxidant supplementation, female characteristics and egg traits in the canary (Serinus canaria)

Avian eggs exhibit a large variability in coloration and patterns, which are produced by blue-green biliverdin and red-brown protoporphyrin pigments. Several hypotheses have been proposed to explain the function of eggshell coloration. In this experimental study, we tested two hypotheses (signalling-function hypothesis and structural-function hypothesis) on both eggshell pigment types in an open-nesting songbird, the canary (Serinus canaria). Also, we aimed to examine whether deposition of pigments into the eggshell has any cost in terms of the plasma oxidative status of the female. We found that eggshell average blue-green chroma was increased by antioxidant supplementation, although we note that there had already been a pre-existing bias in plasma antioxidant capacity between the supplemented and control groups. Eggshell average blue-green chroma was positively related to female body condition during egg laying. However, blue-green eggshell colour was not related to female oxidative status during or after the laying period, and blue-green chroma increased with laying order. Accordingly, we found some support for that eggshell blue-green colour could reflect maternal antioxidant availability and body condition, but did not find evidence that it has a cost for the female’s oxidative status. By contrast, eggshell spot brightness was positively related to body condition, suggesting that darker spotting reflected poorer nutritional condition in the canary. Eggshell blue-green pigmentation was not significantly connected to the egg volume or yolk antioxidant level, but we found that eggs with lower yolk antioxidant concentration had higher average eggshell brown chroma. In sum, our results suggest that eggshell colour reflected female antioxidant and nutrient availability. Finally, we found that eggs with thinner eggshells had a more aggregated spot distribution, supporting the view that aggregated spots may help to strengthen eggshells.Significance statementAvian eggs have a large variability in colours and patterns, which are due to two pigments: the blue-green biliverdin and the red-brown protoporphyrin. In this study, we tested whether eggshell pigmentation, measured by a spectrophotometer, could reflect female and egg quality in the canary, an open nesting songbird. We found that females supplemented with antioxidants before and during egg-laying laid more intense blue-green eggs. Females in better body condition laid eggs that had a more intense blue-green coloration, but lower intensity of brown coloration. Egg yolk antioxidant level was lower in eggs with more intense brown eggshell coloration. These results suggest that eggshell coloration could reflect the antioxidant and nutrient availability of females. Moreover, we found that eggs with thinner eggshells had a more aggregated spot distribution on the eggshell, supporting the view that aggregated brown pigment spots may help to strengthen eggshells.