Egg antimicrobials, embryo sex and chick phenotype in the yellow-legged gull

Maternal effects through albumen quality are largely unexplored, despite the fundamental role that albumen exerts as source of proteins and water, as well as for antimicrobial defence of the embryo. We analysed the variation of two major albumen antimicrobials, avidin and lysozyme, by extracting samples from freshly laid eggs of the yellow-legged gull (Larus michahellis) and by correlating their levels to egg features. Lysozyme concentration increased along the laying sequence, while avidin concentration decreased. Both antimicrobials declined during the season. In addition, avidin concentration declined from first- to last-laid male eggs, whereas the opposite was true among the female eggs. We also analysed chick body mass and size and immune response, in relation to albumen antimicrobial levels in their original egg while controlling for potential covariation between egg quality and rearing conditions by cross-fostering eggs between nests. Tarsus length decreased with avidin concentration, particularly early in the season. Avidin concentration negatively predicted tarsus length of chicks and the phytohaemagglutinin response of females, but not males. However, chick phenotype did not covary with lysozyme albumen concentration. This is the first study where maternal effects mediated by albumen antimicrobials are investigated in relation to both sex and egg features in any wild bird species. Whether the observed patterns of variation in antimicrobial concentration are the by-product of maternal physiological constraints, or reflect adaptive allocation strategies, cannot be ascertained. The covariation between chick cell-mediated immunity and albumen avidin concentration might be causal, according to the documented effects of albumen proteins on immunity in other species.     

Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus)

Egg composition, which is under maternal control, can have a profound effect on offspring fitness. The presence of maternal testosterone and carotenoids in avian egg yolk, for example, is thought to enhance the development and competitive ability of the offspring and protect the hatching and growing chick against oxidative stress. Egg quality often differs between females and such variation can be due to differences in maternal social environment, e.g. breeding density. However, this is confounded by the possibility that the quality of individuals breeding in high- or low-density areas may vary. We tested if maternal social environment influences egg composition in a colonial seabird, the lesser black-backed gull (Larus fuscus). To control for confounding effects of female quality, we experimentally manipulated maternal social environment during egg formation. We increased the frequency of intra-specific interactions (i.e. aggressive encounters with conspecifics other than nest mates) in which the females were involved, by placing an elevated platform in their territory. Females that took part in more intra-specific interactions produced a heavier last egg, but the yolk testosterone concentration in eggs laid by control and experimental females did not differ. Differences in yolk testosterone concentration in relation to embryo sex were found neither in the control nor in the experimental group. In contrast, within the control group, eggs with a male embryo contained more carotenoids than eggs with a female embryo. Moreover, experimental females that had been involved in more intra-specific interactions produced female eggs with higher carotenoid levels compared to female eggs of control birds. An experimental increase in carotenoid levels was not observed in eggs containing a male embryo. Our results suggest that intra-specific interactions experienced by female birds during egg formation can influence conditions for embryonic development.Communicated by J. Graves     

Experimentally manipulated brood sex ratios: growth and survival in the black-headed gull (Larus ridibundus), a sexually dimorphic species

In sexually size dimorphic species, individuals of the larger sex often suffer from enhanced mortality during the nestling period. This has been attributed to higher nutritional requirements of the larger sex, which may render this sex more vulnerable to adverse food conditions. However, sex-biased mortality might not exclusively depend on the differences in food demand but also on other phenotypic differences, e.g., in competitiveness. Interference competition between the sexes and position in the laying sequence in particular may be essential components contributing to biased mortality.By creating synchronously-hatched unisex broods in the sexually size dimorphic black-headed gull, we specifically tested the effect of sex-specific food demand by excluding interference competition between the sexes as well as hatching asynchrony. To test the effect of egg quality, which varies with the position in the laying sequence, we composed each nest of chicks from eggs of all different positions in the laying sequence.All-male nests showed significantly enhanced mortality compared to all-female nests from the beginning of the development of the sexual size dimorphism onwards. This underlines the role of a higher food demand in biased mortality of the larger sex.In males but not females, asymptotic body mass and skeletal size were negatively associated with position in the laying sequence, while survival was not affected by position. As a consequence, sexual size dimorphism at the end of the nestling period was less pronounced compared to the natural situation. These data show that, although male growth is more sensitive to a decrease in egg quality, the higher mortality of last hatched chicks in natural nests is mainly due to hatching asynchrony and egg size but not egg content.     

Temporal and geographical variations of mercury and selenium in eggs of Larus michahellis and Larus audouinii from central Mediterranean islands

In this study, we determined mercury and selenium levels in abandoned unhatched eggs of the yellow-legged gull (Larus michahellis) and Audouin’s gull (Larus audouinii) collected during 2004–2005 from the Tuscan archipelago and Sardinia (Italy). The different feeding habits of the two species probably determine the different uptakes of trace elements, as the study shows highly significant differences for selenium and mercury levels as well as shell thickness and Hg:Se molar ratio values. Audouin’s gulls nesting on the coasts of the Tuscan archipelago showed significantly higher selenium levels than did gulls from colonies from the islands around Sardinia. Comparisons with a similar investigation previously conducted in the same area suggested that mercury and selenium concentrations, although in line with reports in the literature, were significantly lower than levels encountered in gulls in the early 1980s. Mercury (mg/kg d.w.) dropped from 8.631 to 5.030 in Audouin’s gulls and from 2.509 to 0.828 in yellow-legged gulls. The regional decline in mercury levels following reduced use of the metal in industry and the probable food depletion effects linked to the overfishing of fish prey of these two gull species are discussed as hypotheses that could explain the decrease in mercury levels found in eggs.     

A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain

The widespread omnivory of consumers and the trophic complexity of marine ecosystems make it difficult to infer the feeding ecology of species. The use of stable isotopic analysis plays a crucial role in elucidating trophic interactions. Here we analysed δ¹⁵N, δ¹³C and δ³⁴S in chick feathers, and we used a Bayesian triple-isotope mixing model to reconstruct the diet of a generalist predator, the yellow-legged gull (Larus michahellis) that breeds in the coastal upwelling area off northwest mainland Spain. The mixing model indicated that although chicks from all colonies were fed with a high percentage of fish, there are geographical differences in their diets. While chicks from northern colonies consume higher percentages of earthworms, refuse constitutes a more important source in the diet of chicks from western colonies. The three-isotope mixing model revealed a heterogeneity in foraging habitats that would not have been apparent if only two stable isotopes had been analysed. Moreover, our work highlights the potential of adding δ³⁴S for distinguishing not only between terrestrial and marine prey, but also between different marine species such as fish, crabs and mussels.     

Certainty of paternity covaries with paternal care in birds

Summary Male investment in parental care has been hypothesized to be affected or not to be affected by their certainty of paternity, depending on the particular assumptions of theoretical models. We used data on paternal care and extra-pair paternity from 52 bird species to determine whether male parental care was related to certainity of paternity. Paternal care was measured as the relative male contribution to nest building, courtship feeding, incubation, and feeding of nestlings, respectively. Males of avian taxa did not provide less parental care during nest building, courtship feeding and incubation if the frequency of extra-pair paternity was high. However, male participation in feeding of offspring was significantly negatively related to the frequency of extra-pair paternity. This was also the case when the effects of potentially confounding variables such as developmental mode of offspring (which may result in males being freed from parental duties), extent of polygyny (which may result in less paternal care), and the frequency of multiple clutches during one breeding season (which may increase the probability of finding fertile females during the nestling period) were controlled statistically. These results suggest that the extent of paternal care has been affected by certainty of paternity, and that sex roles during the energetically most expensive parts of reproduction have been shaped by sperm competition.     

Factors influencing egg size in the gammarid amphipod Gammarus insensibilis

Developmental and seasonal changes in egg volume were examined in a population of the amphipod Gammarus insensibilis Stock occurring on the south coast of England, towards its northern limit of distribution. Results showed a marked increase in egg volume during development (2.9 times by Egg Stage V), resulting from water uptake and from the conversion of yolk reserves into structural elements. The maximum rate of increase coincides with the period of organ and limb development. At hatching, after initial rupture of the egg membrane by urosome spines, egg volume increases rapidly over a short period (15 to 20 min) by a further 30% (uptake rate 3.6×10^–5 mm³s^–1), followed by a post-hatching decrease in juvenile volume. Increase in size at hatching is the result of drinking by embryos, although changes in body-wall permeability may contribute. Females carrying eggs in an advanced stage of development exhibit egg-collecting behaviour. This is seen as an adaptation to an increased likelihood of egg loss with increase in volume of the brood as hatching approaches. Seasonal changes in Stage I (early) egg size are marked in this species, with winter eggs as much as 60% greater in volume than summer eggs. Egg size is inversely related to the temperature during oocyte development. A simple model has been derived to account for the observed seasonal pattern in egg size. The consequences of seasonal variation in egg and juvenile size are considered.     

Identification and field bioassays of the sex pheromone of the yellow-legged clearwing Synanthedon vespiformis (Lepidoptera: Sesiidae)

The yellow-legged clearwing (YLC) Synanthedon vespiformis (Lepidoptera: Sesiidae) occurs in the Mediterranean and central Europe. It is polyphagous, boring into the woody parts of broadleaf species including forest trees as well as various Rosaceae species. S. vespiformis has been reported as an economically important pest causing severe injury to stone fruit plantations. Many attractants for sesiid species were discovered by random field screening using 2,13- and 3,13-octadecadienyl alcohols, acetates and aldehydes, including one for S. vespiformis; and about 20 sex pheromones of sesiids have been identified so far. In the present study we identified the natural composition of the sex pheromone of YLC laboratory reared females as a blend of E3,Z13- and Z3,Z13-octadecadienyl acetates, at a ratio of 4:1. We developed an efficient lure for monitoring the pest. Pheromone funnel traps with rubber septa, impregnated with 1 mg pheromone blend, efficiently captured males for 10 weeks. Suspension of Shin-Etsu^? ropes containing a 2:1 blend of E3,Z13-18:Ac and Z3,Z13-18:Ac at 13.74 mg/ha/h, resulted in shutdown of trap catches in the treated plots and closely situated neighboring plots indicating that mating disruption is feasible.     

Sperm removal and ejaculate size correlate with chelae asymmetry in a freshwater crayfish species

Asymmetry in traits of sexual relevance may impair copulation behaviour and sexual performance of males, ultimately resulting in a fitness cost. Freshwater crayfish males use chelae, a sexually selected trait, to secure and position the female prior to and during mating. Thus, a relatively large chelae asymmetry, resulting from accidental loss and regeneration of one cheliped after autotomy, could have great consequences for male sexual behaviour. We studied copulatory behaviour and sperm expenditure of males paired to a mated female in Austropotamobius italicus, a freshwater crayfish species where both male and female mate multiply and where last-mating males are able to actively remove previously deposited sperm. We aimed at assessing whether male sperm removal and expenditure varied according to sperm allocated by first-mating males, and according to copulation behaviour and phenotypic traits (carapace length, chelae length and relative chelae asymmetry) of second-mating males. Second-mating males did not adjust their ejaculate size in relation to first-mating male ejaculate, nor to the first-mating male’s sperm removed. Moreover, the amount of sperm removed by second-mating males increased with increasing first-mating males ejaculate size, and first-mating male sperm remaining after removal did not correlate with the original first-mating male ejaculate size. Interestingly, the amount of sperm removed by second-mating males decreased with increasing relative chelae asymmetry, while increasing with male body size. However, second-mating (but not first-mating) asymmetric-clawed males produced larger ejaculates than symmetric-clawed ones. Importantly, the proportion of second-mating male sperm remaining after the two matings did not vary with relative chelae asymmetry nor with body size of second-mating males. Thus, small, asymmetric-clawed crayfish males appear to adopt sperm allocation tactics that allow them to fully compensate for their inferior sperm removal ability.     

Paternal care and egg survival both increase with clutch size in the fathead minnow,Pimephales promelas

Summary In some species of fishes with paternal care, females prefer to spawn with males who are already defeding eggs; moreover, in many species, paternal care increases with the number of eggs that a male is defending. If egg survival depends on the level of paternal care, and is largely independent of egg number, then egg survival should increase with clutch size. This result would provide a potential adaptive mechanism for female preference for males with eggs. I examined the effects of clutch size on paternal care and egg survival in the fathead minnow, Pimephales promelas, and found that both increased with male clutch size.     

Effect of size and sex on buoyancy in the oyster toadfish

In 1991 we examined the developmental consequences of swimbladder growth and sexual dimorphism on specific gravity (SG) and percent buoyancy (%B) in the oyster toadfish (Opsanus tau Linnaeus collected in the York River, Virginia) and tested the hypothesis that large ovaries compensate for the buoyancy conferred by a smaller swimbladder in females. Weight in water (Ww) increased as a linear function of weight in air (Wa) for both sexes, and there were no sexual differences between regressions. SG and %B did not change with Wa, indicating proportional growth of body and swimbladder. SG averaged 1.049±0.002 and %B 3.183±0.160. Removal of the gonads had no significant effect on Ww, SG or %B, indicating that the larger ovaries did not compensate for buoyancy associated with a smaller swimbladder. In fact testis and ovary SG did not differ significantly from values for intact fish. However, gonad composition changed with development: testis SG and % fat decreased with gonosomatic index, whereas overy SG and % fat increased, but % water decreased. Removal of the swimbladder significantly increased SG to 1.083 and %B to 6. Swimbladder volume increased linearly with Wa and was significantly larger in males; adjusted means were 11.40±0.83 and 8.94±0.83 ml for males and females, respectively. Variability in bladder volumes contributed to the absence of sexual differences in SG and may be permissible because negative buoyancy imparts minimal selective advantage for precise volume and buoyancy control. The absence of a relationship between fish buoyancy and sexual dimorphism in bladder size supports evidence that sexual dimorphism in the swim-bladder relates to its function in sound production.     

Queen fertility, egg marking and colony size in the ant Camponotus floridanus

In ant societies, workers do not usually reproduce but gain indirect fitness benefits from raising related offspring produced by the queen. One of the preconditions of this worker self-restraint is sufficient fertility of the queen. The queen is, therefore, expected to signal her fertility. In Camponotus floridanus, workers can recognize the presence of a highly fertile queen via her eggs, which are marked with the queen's specific hydrocarbon profile. If information on fertility is encoded in the hydrocarbon profile of eggs, we expect workers to be able to differentiate between eggs from highly and weakly fertile queens. We found that workers discriminate between these eggs solely on the basis of their hydrocarbon profiles which differ both qualitatively and quantitatively. This pattern is further supported by the similarity of the egg profiles of workers and weakly fertile queens and the similar treatment of both kinds of eggs. Profiles of queen eggs correspond to the cuticular hydrocarbon profiles of the respective queens. Changes in the cuticular profiles are associated with the size of the colony the queen originates from and her current egg-laying rate. However, partial correlation analysis indicates that only colony size predicts the cuticular profile. Colony size is a buffered indicator of queen fertility as it is a consequence of queen productivity within a certain period of time, whereas daily egg-laying rate varies due to cyclical oviposition. We conclude that surface hydrocarbons of eggs and the cuticular profiles of queens both signal queen fertility, suggesting a major role of fertility signals in the regulation of reproduction in social insects.     

Incubation start and egg size in relation to body reserves in the common eider

Avian incubation is often initiated before all eggs are laid. In altricial birds this has been proposed to facilitate brood reduction through asynchronous hatching. However, in precocial birds eggs normally hatch synchronously even if incubation has started before all eggs are laid. Patterns of incubation start may be the adaptive trait selected for both in altricial and precocial species. Several hypotheses have been proposed to explain the timing of incubation start in birds. Decreasing egg-size after incubation start may be adaptively related to an early incubation start, either to ensure synchronous hatching or to decrease fitness cost of late hatched eggs. We have measured individual body condition, egg size and start of incubation in common eider Somateria mollissima, a precocial sea-duck which does not feed during the incubation period. Females in poor body condition start to incubate earlier in the laying sequence than those in good body condition. Furthermore females in poor body condition lay smaller final eggs than females in good body condition. The laying of smaller eggs late in the sequence is therefore probably related to energetic or nutritional state. We propose that females in poor body condition start to incubate early to shorten the nest period in order to reduce their mass loss, but at the cost of reduced size and growth of the ducklings from the eggs laid after incubation start. Females in good body condition on the other hand postpone incubation start at the cost of a longer incubation period and a higher mass loss to the benefit of synchronized hatching and a higher survival of ducklings.     

Inter- and intra-sexual patterns of fluctuating asymmetry in the red-billed streamertail: should symmetry always increase with ornament size?

Recent work on fluctuating asymmetry has suggested that ornaments should have higher levels of fluctuating asymmetry than (1) non-ornaments and (2) homologous structures in the non-ornamented sex. In addition, as both ornament size and symmetry should increase with individual quality there should be a tendency for ornament symmetry to increase with ornament size. In non-ornaments, a U-shaped relationship between symmetry and size is expected, with the individuals at the extremes being more asymmetrical than individuals around the optimum. We tested these predictions in the red-billed streamertail (Trochilus polytmus), a sexually dimorphic endemic Jamaican hummingbird. The lengths of four bilaterally symmetrical traits (first and second outermost tail feathers, tarsi and wings) in 43 adult males and 42 females were measured. The second outermost tail feathers of adult males (which are elongated into streamers) were absolutely but not relatively more asymmetrical than non-ornaments (including the homologous feathers in females). When character size was controlled for, wings were shown to be relatively more symmetrical than other traits. Symmetry did not increase with increasing trait size in any of the morphological traits measured. There was a U-shaped relationship between asymmetry and trait size for four traits (adult male streamers, adult male wings and female outer tail feathers). These results do not support any of the predictions made by fluctuating asymmetry hypotheses and suggest that stabilising selection may act on ornaments as well as non-ornaments. These predictions have been supported in swallows and peafowl but not in sunbirds; this may be due to differences in female perception of tail ornaments. Perhaps male tails do not convey information about quality in some species, or there may be inter-specific differences in the relative costs of tail ornaments and the benefit of marginal increases in tail length and symmetry.     

Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (<Emphasis Type="Italic">Larus ridibundus</Emphasis>) depend on the hatching order

Hatching asynchrony in avian species leads to age and size differences between nestlings within a brood, handicapping last-hatched chicks in the sibling rivalry. Starvation due to this competitive disadvantage has been regarded as the primary cause of an increase in mortality with hatching order. However, for gulls it has also been suggested that disease is the cause of mortality for last-hatched chicks, possibly through reduced immunocompetence and thereby an enhanced susceptibility to infection. In addition, the male-biased mortality reported for several gull species may be related to a higher vulnerability to diseases in males compared to females. To determine the potential influence of the immune system on these mortality patterns, we investigated the T-cell-mediated immunity (CMI) of black-headed gull chicks in relation to hatching order and sex. We found a significant decrease in the CMI with hatching order. This result may be causally related to systematic changes in maternal yolk steroids and carotenoids within the laying sequence. For second-laid eggs, male CMI was significantly lower than female CMI. This is possibly linked to higher plasma levels of testosterone in male embryos which might have an immunosuppressive effect. If so, this effect is masked in eggs of either high (first egg) or low (last egg) quality. Chicks with low CMI showed enhanced mortality rates. Thus the differences in immune response are likely to contribute to the observed mortality patterns. However, hatching order significantly affected mortality independently of CMI, suggesting that competitive disadvantage due to hatching asynchrony is also important.Communicated by M. Webster     

Offspring sex ratio response to host size in the parasitoid wasp Spalangia endius

The host size model, an adaptive model for maternal manipulation of offspring sex ratio, was examined for the parasitoid wasp Spalangia endius. In a Florida strain, as the model predicts, daughters emerged from larger hosts than sons, but only when mothers received both small and large hosts simultaneously. The pattern appeared to result from the mother's ovipositional choice and not from differential mortality of the sexes during development. If sex ratio manipulation is adaptive in the Florida strain, it appears to be through a benefit to daughters of developing on large hosts rather than through a benefit to sons of developing on small hosts. Both female and male parasitoids were larger when they developed on larger hosts. For females, developing on a larger host (1) increased offspring production, except for the largest hosts, (2) increased longevity, (3) lengthened development, and (4) had no effect on wing loading. For males, development on a larger host had no effect on any measure of male fitness – mating success, longevity, development duration, or wing loading. In contrast, a strain from India showed no difference in the size of hosts from which daughters versus sons emerged, although both female and male parasitoids were larger when they developed on larger hosts. These results together with previous studies of Spalangia reveal no consistent connection between host-size-dependent sex ratio and host-size-dependent parasitoid size among strains of S. endius or among species of Spalangia. Received: 28 October 1998 / Received in revised form: 20 May 1999 / Accepted: 30 May 1999     

Removal process estimation of population size for a population with a known sex ratio

A removal model for estimating population size which uses the known population sex ratio is studied. A maximum likelihood estimate and an optimal martingale estimate of the population size are proposed. Their standard errors and large sample properties are obtained. Simulation studies are reported, and the performance of the proposed estimators are compared with the standard maximum likelihood estimator which ignores the sex ratio information. An example on a capture study of deer mice is given.