Fecal calcium levels of bird nestlings as a potential indicator of species-specific metal sensitivity.

Sensitivity of bird species to environmental metal pollution varies but there is currently no general framework to predict species-specific sensitivity. Such information would be valuable from a conservation point-of-view. Calcium (Ca) has antagonistic effects on metal toxicity and studies with some common model species show that low dietary and circulating calcium (Ca) levels indicate higher sensitivity to harmful effects of toxic metals. Here we measured fecal Ca and five other macroelement (potassium K, magnesium Mg, sodium Na, phosphorus P, sulphur S) concentrations as proxies for dietary levels in 66 bird species to better understand their interspecific variation and potential use as an indicator of metal sensitivity in a wider range of species (the main analyses include 39 species). We found marked interspecific differences in fecal Ca concentration, which correlated positively with Mg and negatively with Na, P and S levels. Lowest Ca concentrations were found in insectivorous species and especially aerial foragers, such as swifts (Apodidae) and swallows (Hirundinidae). Instead, ground foraging species like starlings (Sturnidae), sparrows (Passeridae), cranes (Gruidae) and larks (Alaudidae) showed relatively high fecal Ca levels. Independent of phylogeny, insectivorous diet and aerial foraging seem to indicate low Ca levels and potential sensitivity to toxic metals. Our results, together with information published on fecal Ca levels and toxic metal impacts, suggest that fecal Ca levels are a promising new tool to evaluate potential metal-sensitivity of birds, and we encourage gathering such information in other bird species. Information on the effects of metals on breeding parameters in a wider range of bird species would also help in ranking species by their sensitivity to metal pollution.

Population divergence in maternal investment and embryo energy use and allocation suggests adaptive responses to cool climates.

The thermal sensitivity of early life stages can play a fundamental role in constraining species distributions. For egg-laying ectotherms, cool temperatures often extend development time and exacerbate developmental energy cost. Despite these costs, egg laying is still observed at high latitudes and altitudes. How embryos overcome the developmental constraints posed by cool climates is crucial knowledge for explaining the persistence of oviparous species in such environments and for understanding thermal adaptation more broadly. Here, we studied maternal investment and embryo energy use and allocation in wall lizards spanning altitudinal regions, as potential mechanisms that enable successful development to hatching in cool climates. Specifically, we compared population-level differences in (1) investment from mothers (egg mass, embryo retention and thyroid yolk hormone concentration), (2) embryo energy expenditure during development, and (3) embryo energy allocation from yolk towards tissue. We found evidence that energy expenditure was greater under cool compared with warm incubation temperatures. Females from relatively cool regions did not compensate for this energetic cost of development by producing larger eggs or increasing thyroid hormone concentration in yolk. Instead, embryos from the high-altitude region used less energy to complete development, that is, they developed faster without a concomitant increase in metabolic rate, compared with those from the low-altitude region. Embryos from high altitudes also allocated relatively more energy towards tissue production, hatching with lower residual yolk: tissue ratios than low-altitude region embryos. These results are consistent with local adaptation to cool climate and suggest that this is underpinned by mechanisms that regulate embryonic utilisation of yolk reserves and its allocation towards tissue, rather than shifts in maternal investment of yolk content or composition.

Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors.

Maternal reproductive investment can critically influence offspring phenotype, and thus these maternal effects are expected to be under strong natural selection. Knowledge on the extent of heritable variation in the physiological mechanisms underlying maternal effects is however limited. In birds, resource allocation to eggs is a key mechanism for mothers to affect their offspring and different components of the egg may or may not be independently adjusted. We studied the heritability of egg components and their genetic and phenotypic covariation in great tits (Parus major), using captive-bred full siblings of wild origin. Egg mass, testosterone (T) and androstenedione (A4) hormone concentrations showed moderate heritability, in agreement with earlier findings. Interestingly, yolk triiodothyronine hormone (T3), but not its precursor, thyroxine hormone (T4), concentration was heritable. An immune factor, albumen lysozyme, showed moderate heritability, but yolk immunoglobulins (IgY) did not. The genetic correlation estimates were moderate but statistically nonsignificant; a trend for a positive genetic correlation was found between A4 and egg mass, T and lysozyme and IgY and lysozyme, respectively. Interestingly, phenotypic correlations were found only between A4 and T, and T4 and T3, respectively. Given that these egg components are associated with fitness-related traits in the offspring (and mother), and that we show that some components are heritable, it opens the possibility that natural selection may shape the rate and direction of phenotypic change via egg composition.

Yolk steroids in great tit Parus major eggs: variation and covariation between hormones and with environmental and parental factors.

ABSTRACT: Avian mothers can potentially alter the phenotypes of their offspring by varying the concentration of steroid hormones in their eggs. We explored variation in androstenedione (A4), testosterone (T), 5α-dihydrotestosterone (DHT), 17ß-estradiol (E2), and corticosterone (CORT) in the yolks of 12 free-living great tit Parus major clutches. We analyzed variation and covariation in greater detail than previous studies, using models for variation with laying sequence that take into account variable clutch size and comparing correlations between pairs of hormones at the within- and between-clutch levels. We also investigated relationships between hormone levels and various environmental, life history, and parental traits. For three of the five steroids, we found no significant correlates, but based on individual statistical tests (a) DHT varied between clutches with male age (1 year old vs older); (b) DHT and CORT were negatively correlated within clutches with the average temperature on the day (DHT and CORT) or 3 days (DHT only) preceding laying; and (c) DHT in the last egg of the clutch relative to the clutch mean was positively correlated with the interval between clutch completion and the onset of incubation (incubation delay). Relationships with ambient temperature and incubation delay have not previously been reported for any yolk hormone in birds. Intriguingly, the three relationships for DHT are consistent with more DHT being transferred to eggs in situations that could be more energetically challenging for the female. More research is needed to determine the generality of the patterns we found and to understand their functional significance. SIGNIFICANCE STATEMENT: The yolks of birds' eggs contain steroid hormones produced by the mother which can affect the development and behavior of the resultant chicks. We analyzed five steroid hormones in the yolks of wild great tits and show for the first time that yolk hormone levels are related to ambient temperature in the day(s) just before laying and, in the last-laid egg, with the day it is laid relative to the onset of incubation, and that the concentrations of pairs of yolk hormones can vary with each other in a different way between and within clutches. These results contribute insights into the ways in which yolk hormones may adaptively modify the chicks or may reflect physiological processes occurring in the mother.