Camille Duval

Maternal investment of female mallards is influenced by male carotenoid-based coloration

The differential allocation hypothesis predicts that females modify their investment in a breeding attempt according to its reproductive value. One prediction of this hypothesis is that females will increase reproductive investment when mated to high-quality males. In birds, it was shown that females can modulate pre-hatch reproductive investment by manipulating egg and clutch sizes and/or the concentrations of egg internal compounds according to paternal attractiveness. However, the differential allocation of immune factors has seldom been considered, particularly with an experimental approach. The carotenoid-based ornaments can function as reliable signals of quality, indicating better immunity or ability to resist parasites. Thus, numerous studies show that females use the expression of carotenoid-based colour when choosing mates; but the influence of this paternal coloration on maternal investment decisions has seldom been considered and has only been experimentally studied with artificial manipulation of male coloration. Here, we used dietary carotenoid provisioning to manipulate male mallard (Anas platyrhynchos) bill coloration, a sexually selected trait, and followed female investment. We show that an increase of male bill coloration positively influenced egg mass and albumen lysozyme concentration. By contrast, yolk carotenoid concentration was not affected by paternal ornamentation. Maternal decisions highlighted in this study may influence chick survival and compel males to maintain carotenoid-based coloration from the mate-choice period until egg-laying has been finished.

Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens

Studies of avian eggshell coloration have been a long-standing research focus in behavioral evolutionary ecology. Museum collections have provided a widely used resource because they allow efficient sampling across broad temporal, geographical, and taxonomic ranges, even for species that are rare and for which sampling in the wild is ethically or practically unwarranted. We used reflectance spectrophotometry across the avian visual spectrum to compare eggshell color of specimens of the song thrush (Turdus philomelos) in two museums (Natural History Museum, UK and Auckland Museum, New Zealand) with each other and with eggshells collected fresh in New Zealand. These data enabled us to test the effects of source and storage in different museums, as well as time since collection, across four metrics of eggshell coloration: blue-green and ultraviolet chroma, overall brightness, and the spectral coefficient of variation. Variation within an egg, within a clutch, and among clutches, was similar between the two museum datasets but different from those of fresh eggs. We found significant differences in all four metrics between the collections, and that fresh eggshells reflected stronger in the blue-green wavelength than in museum eggs. This difference is most likely due to different preservation techniques and storage histories. Furthermore, an effect of time since collection was only apparent in the blue-green chroma and was higher in more recent museum eggshell samples. Our results support the use of historic museum samples in intraspecific studies of shell coloration providing that efforts are made to compare specimens, which were collected during similar periods.

Condition-dependent strategies of eggshell pigmentation: an experimental study of Japanese quail ( Coturnix coturnix japonica )

SUMMARY A relationship has been suggested between eggshell colour and female body condition based on the opposing antioxidant properties of the two main eggshell pigments: the antioxidant biliverdin (blue–green) and the pro-oxidant protoporphyrin (brown). We hypothesized that experimentally food-restricted females with low antioxidant capacity would deposit more protoporphyrin and less biliverdin in their eggshells, resulting in eggshells of reduced brightness but increased colour intensity. Two eggs were collected at the beginning and two at the end of a 2 week period from each of 24 female Japanese quails that were either food restricted or receiving ad libitum food (i.e. controls) during that time. Reflectance spectra were recorded and analysed using spectral shape descriptors, chromatic and achromatic contrasts were computed accounting for avian visual sensitivities, and eggshell pigments were quantified. We examined both spot and background pigmentation and found no significant effect of food restriction on eggshell reflectance. However, food-restricted females in lower body condition increased the deposition of protoporphyrin and decreased the amount of biliverdin invested in their eggshells. We hypothesize that in species laying brown-spotted eggshells, females modulate eggshell pigment investment in response to their body condition. According to this hypothesis, we predict that females maintain eggshell colour to limit visible changes that could be detected by predators and thereby conceal their eggs, although this work has yet to be conducted. We suggest that further experimental work on egg camouflage under different environmental conditions will elaborate on the process of pigment deposition and the physiological costs to females of laying heavily pigmented eggshells.

Effect of preen oil on plumage bacteria: An experimental test with the mallard

Feathers are essential for avian thermoregulation, communication or flight and a reduction of plumage condition may alter these functions and reduce individual fitness. Recently, descriptive studies provided evidence that birds carry feather-degrading bacteria on their plumage that have the ability to degrade feathers rapidly under laboratory conditions. If such bacteria reduce avian fitness, natural selection should favour the evolution of anti-bacterial defences to limit the effects of these detrimental microorganisms. Preening behaviour and associated preen gland secretions have been proposed as the main factor used by birds to limit feather-degrading bacterial growth and some recent in vitro studies provided evidence that uropygial oil inhibited the growth of some keratinolytic strains in passerines. However, preen oil antimicrobial properties remained to be experimentally tested in vivo. We conducted an experiment with mallards (Anas platyrhynchos) onto which we fixed a removable mechanism that blocked access to the uropygial gland in a first group of mallards, whilst birds in a second group had the same removable mechanism but access to their gland and a third group of birds had normal access to their gland. We found no significant effect of our treatment on total and feather-degrading bacterial loads. Three hypotheses may explain the discrepancy between our results and previous in vitro studies. First, in vitro studies may have over-estimated the bactericidal properties of the preen oil. Second, preen gland deprivation may have affected only a small portion of the feather-degrading bacterial community. Third, ducks and passerine oils might have different bactericidal properties.

Effect of Restricted Preen-Gland Access on Maternal Self Maintenance and Reproductive Investment in Mallards

Background As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg. Methodology/Principal Findings Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access. Conclusion/Significance Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.

Peri-pubertal exposure to testicular hormones organizes response to novel environments and social behaviour in adult male rats

Previous research has shown that exposure to testicular hormones during the peri-pubertal period of life has long-term, organizational effects on adult sexual behaviour and underlying neural mechanisms in laboratory rodents. However, the organizational effects of peri-pubertal testicular hormones on other aspects of behaviour and brain function are less well understood. Here, we investigated the effects of manipulating peri-pubertal testicular hormone exposure on later behavioural responses to novel environments and on hormone receptors in various brain regions that are involved in response to novelty. Male rodents generally spend less time in the exposed areas of novel environments than females, and this sex difference emerges during the peri-pubertal period. Male Lister-hooded rats (Rattus norvegicus) were castrated either before puberty or after puberty, then tested in three novel environments (elevated plus-maze, light–dark box, open field) and in an object/social novelty task in adulthood. Androgen receptor (AR), oestrogen receptor (ER1) and corticotropin-releasing factor receptor (CRF-R2) mRNA expression were quantified in the hypothalamus, hippocampus and medial amygdala. The results showed that pre-pubertally castrated males spent more time in the exposed areas of the elevated-plus maze and light–dark box than post-pubertally castrated males, and also confirmed that peri-pubertal hormone exposure influences later response to an opposite-sex conspecific. Hormone receptor gene expression levels did not differ between pre-pubertally and post-pubertally castrated males in any of the brain regions examined. This study therefore demonstrates that testicular hormone exposure during the peri-pubertal period masculinizes later response to novel environments, although the neural mechanisms remain to be fully elucidated.

An experimental test in Mallards (Anas platyrhynchos) of the effect of incubation and maternal preen oil on eggshell microbial load

Abstract Microbial infection is one of the main factors reducing survival in the first stages of life in oviparous species, and recent studies have shown that the avian eggshell harbors an important variety of microorganisms that can rapidly multiply and penetrate the shell, leading to a decrease in hatchability. Here, we report the results of an experiment in which we examined how incubation and maternal preen oil affect the growth of avian eggshell microbes, using the Mallard (Anas platyrhynchos) as a model species. We compared the bacterial and fungal loads on the shell of non-incubated eggs and eggs incubated by females having free or blocked access to their preen gland. An increase of eggshell bacterial loads was observed in all conditions, but bacterial growth was higher on the shell of incubated eggs than on non-incubated eggs. We did not find any significant difference in eggshell bacterial growth for eggs incubated by females with free or blocked access to their preen gland. In addition, fungal growth during our experiment was not affected by incubation or the mother’s preen oil. Our findings are in contrast with those of previous studies which showed that incubation limited or had no effect on eggshell bacterial growth. Differences in environmental conditions and/or species ecology may explain the difference between the results of our experiment and those of previous studies. Our study provides the first data on the effect of maternal preen oil on eggshell microorganisms, showing that preen oil does not limit eggshell microbial growth.ZusammenfassungEin experimenteller Test an Stockenten (Anas platyrhynchos) zum Effekt von Bebrütung und mütterlichem Bürzeldrüsenfett auf die Mikrobenbelastung von Eierschalen Mikrobielle Infektionen sind ein Hauptfaktor für reduzierte Überlebensraten der ersten Lebensstadien bei oviparen Arten. Aktuelle Studien belegen, dass bei Vögeln die Eierschale eine erhebliche Vielfalt an Mikroorganismen beherbergt, die sich schnell vermehren und in die Schale eindringen können. Dies führt zu einer verringerten Schlupfrate. Hier stellen wir die Ergebnisse eines Experimentes vor, bei dem wir untersucht haben, wie Bebrütung und mütterliches Bürzeldrüsenfett das Wachstum von Mikroben auf Eierschalen von Vögeln beeinflussen. Als Modellart diente die Stockente (Anas platyrhynchos). Wir verglichen den Bakterien- und Pilzbefall der Schalen bebrüteter und nicht-bebrüteter Eier mittels Weibchen, die einen freien oder blockierten Zugriff auf ihre Bürzeldrüse hatten. Bei allen Eierschalen wurde ein Anstieg der Bakterienbelastung beobachtet, wobei das Bakterienwachstum auf Schalen bebrüteter Eier höher war als auf den Schalen unbebrüteter Eier. Hinsichtlich der Weibchen mit freiem oder blockiertem Zugriff auf ihre Bürzeldrüse konnte kein signifikanter Unterschied im Bakterienwachstum auf den Eierschalen festgestellt werden. Darüber hinaus war das Pilzwachstum während des Experimentes nicht beeinflusst durch die Bebrütung oder das Bürzeldrüsensekret des Weibchens. Unsere Ergebnisse stehen im Gegensatz zu früheren Studien, die gezeigt haben, dass die Bebrütung entweder einen limitierten oder gar keinen Effekt auf das Bakterienwachstum auf Eierschalen hatte. Unterschiede in den Umweltbedingungen und/oder der Ökologie der Arten könnten den Unterschied zwischen diesem Experiment und vorherigen Studien erklären. Die vorliegende Studie liefert die ersten Daten zum Einfluss von mütterlichem Bürzeldrüsensekret auf Mikroorganismen von Eierschalen, die zudem zeigen, dass das Bürzeldrüsensekret das mikrobielle Wachstum auf Eierschalen nicht begrenzt.

Eggshell appearance does not signal maternal corticosterone exposure in Japanese quail: an experimental study with brown-spotted eggs.

Reproduction is a critical period for birds as they have to cope with many stressful events. One consequence of an acute exposure to stress is the release of corticosterone, the avian stress hormone. Prolonged stress can have negative impacts on the immune system, resulting in, for example, increased oxidative stress. Through maternal effects, females are known to modulate their investment in eggs content according to their own physiological condition. Less is known about maternal investment in eggshells, especially in pigments. The two main eggshell pigments may possess opposite antioxidant properties: protoporphyrin (brown) is a pro-oxidant, whereas biliverdin (blue-green) is an antioxidant. In Japanese quail, we know that the deposition of both pigments is related to female body condition. Thus, a chronic stress response may be reflected in eggshell coloration. Using female Japanese quails that lay brown-spotted eggs, we explored whether physiological exposure to corticosterone induces a change in female basal stress and antioxidant factors, and eggshell pigment concentration, spectrophotometric reflectance, and maculation coverage. We supplemented adult females over a 2 week period with either peanut oil (control) or corticosterone (treatment). We collected pre- and post-supplementation eggs and analysed the effect of corticosterone treatment on female physiology and eggshell appearance parameters. Except for corticosterone-fed birds which laid eggs with brighter spots, supplementation had no significant effect on female physiology or eggshell pigment concentration, reflectance and maculation. The change in eggshell spot brightness was not detected by a photoreceptor noise-limited color opponent model of avian visual perception. Our data confirms that eggshell reflectance in spotted eggs varies over the laying sequence, and spot reflectance may be a key factor that is affected by females CORT exposure, even if the changes are not detected by an avian visual model.

Maternal influence on eggshell maculation: implications for cryptic camouflaged eggs

AbstractEgg camouflage may explain the adaptive significance of avian eggshell pigmentation in ground-nesting species. Eggshell maculation (spots) is predominantly due to protoporphyrin, but both biliverdin (antioxidant) and protoporphyrin (pro-oxidant) may be present in spotted eggshells. Because of their role in oxidative stress, the deposition of eggshell pigments might be condition-dependent. However, because of the fitness benefits of eggshell coloration, cryptic eggshell appearance should be strongly conserved in ground-nesting species regardless of female condition and eggshell pigment concentrations. We investigated whether Japanese quails (Coturnix coturnix japonica) maintained eggshell maculation under food restriction. We quantified eggshell maculation (i.e., percentage of spot coverage) using digital photography, and both protoporphyrin and biliverdin concentrations of eggs laid by females either on a food-restricted or an ad libitum diet. Females on a high quality diet, which are known to decrease the deposition of eggshell protoporphyrin, decreased eggshell maculation compared with food-restricted females that maintained it. For the first time, we propose an experimental study which suggests that eggshell maculation depends on female body condition and that manipulating eggshell maculation may be the strategy used by females to potentially optimize egg camouflage.ZusammenfassungMaternaler Einfluss auf die Befleckung der Eierschale: Folgen für kryptische getarnte Eier Die Tarnung von Eiern könnte die adaptive Bedeutung der Pigmentierung der Eierschale bodenbrütender Vögel erklären. Die Befleckung der Eierschale ist hauptsächlich auf Protoporphyrin zurückzuführen, aber sowohl Biliverdin (ein Antioxidant) als auch Protoporphyrin (ein Prooxidant) können in gefleckten Eierschalen enthalten sein. Aufgrund der Rolle von Eierschalenpigmenten bei oxidativem Stress könnte ihre Einlagerung in die Eierschale konditionsabhängig sein. Aufgrund der Fitnessvorteile einer Färbung der Eierschale sollte ein kryptisches Aussehen der Eier bei Bodenbrütern jedoch hochkonserviert sein, unabhängig von der Kondition der Weibchen und der Konzentration der Eierschalenpigmente. Wir haben untersucht, ob Japanwachteln (Coturnix coturnix japonica) die Befleckung ihrer Eierschale bei Futterknappheit beibehielten. Wir haben die Eierschalenbefleckung (d.h. den Anteil der Abdeckung mit Flecken) mit Hilfe digitaler Fotografie quantifiziert sowie die Protoporphyrin- und Biliverdin-Konzentrationen der Eier von Weibchen ermittelt, die entweder eingeschränkt oder ad libitum Futter erhielten. Weibchen mit hochwertiger Kost, die bekannterweise die Einlagerung von Protoporphyrin in die Eierschale reduzieren, reduzierten die Befleckung der Eierschale im Vergleich zu Weibchen mit eingeschränkter Kost, welche sie beibehielten. Zum ersten Mal liefern wir eine experimentelle Studie ab, die darauf hindeutet, dass die Befleckung der Eierschale von der Kondition des Weibchens abhängt und dass Weibchen die Befleckung der Eierschale beeinflussen könnten, als Strategie, um die Tarnung der Eier potenziell zu optimieren.

On the use of commercial quails as study organisms: lessons about food intake from individual variation in body mass

We analysed inter-individual body mass variation of Japanese quail (Coturnix coturnix japonica) in an examination of the effectiveness of regulations governing daily food requirements. We measured the daily food intake of 26 adult female quail during a feeding trial over four consecutive days. Non-ingested food was weighed every morning and 70 g of food was provided to each bird for every day of the trial. This represented more than three times the theoretical recommended daily amount of food required by Japanese quail, as described in the literature. We then calculated a female-specific mean daily food requirement and found highly significant variation among individuals. Daily food intake was significantly repeatable within-female over the trial and mean food intake was highly correlated with female body mass. We suggest that using daily requirements for individuals based upon ‘population’ means, whilst ignoring differences in body mass among individuals might have severe consequences for the welfare of birds. Furthermore, these results have significant implications for studies where the aim is to perform identical experimental manipulations (as some studies intend and suggest), resulting in the drawing of unsubstantiated conclusions.