Hidden impacts of conservation management on fertility of the critically endangered kākāpō

PeerJ. 2023 Feb 3:11:e14675. doi: 10.7717/peerj.14675. eCollection 2023.

Abstract

Background: Animal conservation often requires intensive management actions to improve reproductive output, yet any adverse effects of these may not be immediately apparent, particularly in threatened species with small populations and long lifespans. Hand-rearing is an example of a conservation management strategy which, while boosting populations, can cause long-term demographic and behavioural problems. It is used in the recovery of the critically endangered kākāpō (Strigops habroptilus), a flightless parrot endemic to New Zealand, to improve the slow population growth that is due to infrequent breeding, low fertility and low hatching success.

Methods: We applied Bayesian mixed models to examine whether hand-rearing and other factors were associated with clutch fertility in kākāpō. We used projection predictive variable selection to compare the relative contributions to fertility from the parents' rearing environment, their age and previous copulation experience, the parental kinship, and the number of mates and copulations for each clutch. We also explored how the incidence of repeated copulations and multiple mates varied with kākāpō density.

Results: The rearing status of the clutch father and the number of mates and copulations of the clutch mother were the dominant factors in predicting fertility. Clutches were less likely to be fertile if the father was hand-reared compared to wild-reared, but there was no similar effect for mothers. Clutches produced by females copulating with different males were more likely to be fertile than those from repeated copulations with one male, which in turn had a higher probability of fertility than those from a single copulation. The likelihood of multiple copulations and mates increased with female:male adult sex ratio, perhaps as a result of mate guarding by females. Parental kinship, copulation experience and age all had negligible associations with clutch fertility.

Conclusions: These results provide a rare assessment of factors affecting fertility in a wild threatened bird species, with implications for conservation management. The increased fertility due to multiple mates and copulations, combined with the evidence for mate guarding and previous results of kākāpō sperm morphology, suggests that an evolutionary mechanism exists to optimise fertility through sperm competition in kākāpō. The high frequency of clutches produced from single copulations in the contemporary population may therefore represent an unnatural state, perhaps due to too few females. This suggests that opportunity for sperm competition should be maximised by increasing population densities, optimising sex ratios, and using artificial insemination. The lower fertility of hand-reared males may result from behavioural defects due to lack of exposure to conspecifics at critical development stages, as seen in other taxa. This potential negative impact of hand-rearing must be balanced against the short-term benefits it provides.

Keywords: Animal behaviour; Conservation biology; Conservation management; Fertility; Genetics; Kākāpō; Reproduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bayes Theorem
  • Endangered Species
  • Female
  • Fertility
  • Male
  • Parrots*
  • Reproduction
  • Semen*

Grants and funding

Andrew Digby, Daryl Eason, Deidre Vercoe, Michael Lierz, Tineke Joustra and Caroline Lees were supported by the Kākāpō Recovery Programme, which is funded by the New Zealand government, public donations and commercial partners. Michael Lierz was also supported by the European Association of Avian Veterinarians. Alejandro Catalina was funded by the Finnish Center for Artificial Intelligence (FCAI) and supported by Aalto-Science IT project. Stephanie Galla and Tammy E. Steeves were funded by the Ministry of Business, Innovation and Employment (MBIE) Endeavour Fund (UOCX1602, awarded to Tammy E. Steeves). Stephanie Galla was also supported by a National Science Foundation Track 2 EPSCoR Program under award number OIA-1826801. Lara Urban was funded by a Feodor Lynen Research Fellowship provided by the Alexander von Humboldt Foundation. Marissa F. Le Lec was also supported by a University of Otago doctoral scholarship. Joseph Guhlin, Marissa F. Le Lec, Lara Urban, Tammy E. Steeves and Peter K. Dearden were supported by Genomics Aotearoa through their High-Quality Genomes and Population Genomics project. Tane Davis was supported by Te Rūnanga o Ngāi Tahu. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.