Exposure to Dietary Methyl-Mercury Solely during Embryonic and Juvenile Development Halves Subsequent Reproductive Success in Adult Zebra Finches

Long-term exposure to methyl-mercury has deleterious effects on avian reproduction. However, little is known about whether exposure to mercury solely during embryonic and juvenile development can have long-lasting effects on subsequent reproductive performance as adults. Birds that hatch on contaminated sites but disperse elsewhere will be exposed only during development. Hence, it is important to understand the reproductive consequences of avian exposure to methyl-mercury during early life. Accordingly, in this experiment, domesticated zebra finches (<i>Taeniopygia guttata</i>) were exposed to dietary methyl-mercury (1.20 μg/g wet weight) from conception through independence (50 days post-hatching). Following maturity, developmentally exposed and control finches were paired within treatment groups and allowed to breed repeatedly for 8 months. Developmentally exposed pairs hatched 32% fewer eggs and produced 50% fewer independent juveniles despite transferring only traces of mercury into their offspring. This is the first example of mercury-related reproductive declines in birds not exposed to mercury during breeding. The magnitude of reproductive decline was similar to that of zebra finches exposed to methyl-mercury during the breeding process. Bird populations breeding in contaminated habitats may suffer from a 2-fold fitness cost of mercury exposure; adult exposure compromises parents’ reproduction, while offspring exposure results in reduced reproduction in the next generation

Effects of dietary mercury on zebra finch reproduction.

<p>All points are model averages from the generalized linear mixed models. Bars are one S.E. A) The average total number of independent offspring produced per pair in one year of reproduction. B) The average clutch size. C) The proportion of eggs laid that hatched. D) The proportion of hatched chicks that survived to leave the nest. E) The number of days between removal of the first clutch of eggs and laying of the second clutch. F) The probability that both members of the pair survived for one year.</p

Average blood mercury values for each dietary dose of adult-exposed and lifetime-exposed zebra finches.

<p>Adult-exposed averages are represented by filled circles and solid lines; lifetime-exposed averages are represented by hollow circles and dashed lines. Values are means and bars are one S.E.</p

Differences in the effects of mercury on reproduction between adult-exposed and lifetime-exposed zebra finches.

<p>Adult-exposed averages are represented by filled circles and solid lines; lifetime-exposed averages are represented by hollow circles and dashed lines. All points are model averages from the generalized linear mixed models. Bars are one S.E. A) The average total number of independent offspring produced per pair in one year of reproduction. B) The average clutch size. C) The proportion of eggs laid that hatched. D) The proportion of hatched chicks that survived to leave the nest. E) The number of days between removal of the first clutch of eggs and laying of the second clutch. F) The probability that both members of the pair survived for one year.</p

Results of Generalized Linear Mixed Models.

<p>Results of Generalized Linear Mixed Models.</p

Blood mercury accumulation for each dietary dose of zebra finches.

<p>Parental generation values are depicted in clear bars to the left within each treatment group and offspring generation values are shown by the filled bars to the right of each pair in a treatment group.</p

Variance estimates when the permanent environment effect was included or not included in models.

<p>Variance estimates when the permanent environment effect was included or not included in models.</p

Evolutionary (evol) and static (sta) allometry of the variables representing size in the hemipenis and valve area, used as a proxy for body size.

<p>The basal capsule is represented by the Basal Capsule dorsal chitinous support length (HemiBCd L, upper panel); the terminal extension is represented by the Copulatory process length (Hemi TE L, middle panel), and the Terminal extension area (HemiTE A, lower panel). Abbreviations follow <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177791#pone.0177791.t001" target="_blank">Table 1</a>.</p

Valve shape by size sexual dimorphism.

<p>Valve shape (log[L/H]) and size (log[area]), expressed as deviations from the mean of each species female population. Deviations from the origin in the horizontal and vertical direction represent magnitudes of size and shape dimorphism, respectively. Black boxes indicate four extreme specimens of <i>C</i>. <i>torosa</i> shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177791#pone.0177791.g004" target="_blank">Fig 4</a>. M = male specimen, F = female specimen.</p

Mean (m, in μm for linear dimensions, μm² for area), coefficient of variation (CV) and sample size (N) of the size of male primary sexual trait and directional asymmetry (L-R), with 95% confidence intervals (CI), and directional asymmetry (DA) of the 1WL with 95% confidence intervals in male <i>Cyprideis</i>.

<p>The length of the Basal capsule distal chitinized support (HemiBCd L) and Copulatory process (HemiTE L), and area of the Terminal extension section (HemiTE A) for the left (L) side are reported. Bilateral dimorphism of the 1WL length (WL1 L; calculated as L-R) and width (WL1 W, calculated by subtracting L (Length curve—length straight line) from R (Length curve—length straight line)) is indicated to best illustrate degree of sexual dimorphism in the secondary sexual character. Abbreviations follow <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177791#pone.0177791.t001" target="_blank">Table 1</a>; entries with <i>p</i> < 0.05 indicated in bold.</p