Demographic drivers of reproductive failure in a threatened bird: Insights from a decade of data

Abstract

Hatching failure affects up to 77% of eggs laid by threatened bird species, yet the true prevalence and drivers of egg fertilization failure versus embryo mortality as underlying mechanisms of hatching failure are unknown. Here, using ten years of data comprising 4,371 eggs laid by a population of a threatened bird, the hihi (Notiomystis cincta), we investigate the relative importance of infertility and embryo death as drivers of hatching failure and explore population-level factors associated with them. We show that of the 1,438 eggs that failed to hatch (33% of laid eggs) between 2010 and 2020, 83% failed due to embryo mortality, with the majority failing in the early stages of embryonic development. In the most comprehensive estimates of infertility rates in a wild bird population to date, we find that fertilization failure accounts for around 17% of hatching failure overall and is more prevalent in years where the population is smaller and more male biased. Male embryos are more likely to die during early development than females, but we find no overall effect of sex on the successful development of embryos. Offspring fathered by within-pair males have significantly higher inbreeding levels than extra-pair offspring; however, we find no effect of inbreeding nor extra-pair paternity on embryo mortality. Accurately distinguishing between infertility and embryo mortality in this study provides unique insight into the underlying causes of reproductive failure over a long-term scale and reveals the complex risks of small population sizes to the reproduction of threatened species.

Keywords: embryo mortality; inbreeding; infertility; population demographics; sex ratio.

Fig. 1.

How egg outcomes vary with population demographics in the Tiritiri Matangi population of hihi across 10 y. (A) The total number of eggs which failed to hatch after the full incubation period for every year, compared to the count of eggs previously assumed to be unfertilized/with unknown fertilization status using macroscopic techniques, and the proportion determined to be truly unfertilized through microscopic analysis. (B) The outcome of every egg laid in the population across every year (as proportions of the total number of eggs laid), highlighting early embryo morality as the main cause of hatching failure in this population. (C) The sex ratio and size of the population of hihi on Tiritiri Matangi across 10 y.

Fig. 2.

The probability of an egg being unfertilized is significantly increased in years when the sex ratio of males to females is more biased; however, this does not significantly affect overall hatching failure, which is mostly due to embryo mortality. Embryo mortality, at any stage of development, does not seem to be influenced by sex, paternity of inbreeding level of the embryo. (A) The proportion of males and females that died at the different stages of development compared to those that hatched. (B) the inbreeding coefficients of males and females that died at different stages of development compared to those that hatched. (C) the proportion of extra-pair paternity (EPP) and within-pair paternity (WPP) of individuals that died at different stages of development compared to those which hatched. (D) The density distribution of the probability that a hihi egg will be unfertilized/infertile, unhatched, or hatched, given the dynamic sex ratio of the population of hihi on Tiritiri Matangi. The sex ratio and size of this population are significantly correlated, making it impossible to separate their respective effects on the infertility rate of eggs. (E) Mean (point) and SE (bars) of the inbreeding coefficients of extra-pair (n = 2,029) and within-pair (1,250) hihi offspring from the years 2010 to 2020 (excluding 2012), including failed embryos and hatched individuals. Plotted sample sizes are: a) Sex: Early EM = 115, Mid EM =103, Late EM = 218, Hatched = 2,856; b) Inbreeding*Sex: Early EM = 11, Mid EM = 74, Late EM = 164, Hatched = 1,618); c) Paternity: Early EM = 68, Mid EM = 107, Late EM = 220, Hatched = 2,833; and d) Inbreeding*Paternity: EPP = 1,396, WPP =888.