Low hatching success in the critically endangered kākāpō is driven by early embryo mortality not infertility

Savage, James L.; Crane, Jodie M. S.; Hemmings, Nicola

doi:10.1111/acv.12746

Cited by 15 publications

(19 citation statements)

References 39 publications

(47 reference statements)

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“…This was conducted either in the nest or in an incubation facility, and was sufficient for detecting development from approximately four days after laying. Microscopic methods can detect earlier development ( Savage et al, 2021 ), but these have only been conducted for a single breeding season for kākāpō, and so could not be used in the current study which spans multiple years. As a result of using ‘apparent’ rather than true fertility in our analyses, approximately a quarter of the eggs in which embryos died at a very young age (before four days) will have instead been classed as infertile ( Savage et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

“…A primary reason for low productivity in kākāpō is the high rate of infertility. Approximately 40% of kākāpō eggs are considered infertile from visual inspection (‘candling’), although a recent fluorescence microscope study showed that 72% of these ‘apparently infertile’ kākāpō eggs were actually fertile, and instead failed due to very early embryo death ( Savage et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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

Digby¹,

Eason²,

Catalina

et al. 2023

PeerJ

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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.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Digby¹,

Eason²,

Catalina

et al. 2023

PeerJ

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“…In some contexts, exposing extremely rare threatened species to invasive predators would be too risky, and full control/eradication/exclusion of invasive predators should remain the goal. For example, the entire population of k ak ap o (Strigops habroptilus), a large, flightless, nocturnal parrot formerly common in New Zealand (Savage et al, 2021), consists of only 199 individuals (May 2022, NZ DOC, 2022). Increasing the k ak ap o's population has been a considerable challenge due to its irregular and distinctive breeding patterns and high level of reproductive failure (Elliott et al, 2001;Savage et al, 2021).…”

Section: Long-term Thinkingmentioning

confidence: 99%

“…For example, the entire population of k ak ap o (Strigops habroptilus), a large, flightless, nocturnal parrot formerly common in New Zealand (Savage et al, 2021), consists of only 199 individuals (May 2022, NZ DOC, 2022). Increasing the k ak ap o's population has been a considerable challenge due to its irregular and distinctive breeding patterns and high level of reproductive failure (Elliott et al, 2001;Savage et al, 2021). Exposing this species to predation, with its population size at such critical levels, would obviously be irresponsible.…”

Section: Long-term Thinkingmentioning

confidence: 99%

Coexistence conservation: Reconciling threatened species and invasive predators through adaptive ecological and evolutionary approaches

Evans

Weeks

Scheele

et al. 2022

Conservat Sci and Prac

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Invasive predators are responsible for declines in many animal species across the globe. To redress these declines, conservationists have undertaken substantial work to remove invasive predators or mitigate their effects. Yet, the challenges associated with removal of invasive predators mean that most successful conservation programs have been restricted to small islands, enclosures (“safe havens”), or refuge habitats where threatened species can persist. While these approaches have been, and will continue to be, crucial for the survival of many species, in some contexts they may eventually lock in a baseline where native species vulnerable to invasive predators are accepted as permanently absent from the wild (shifting baseline syndrome). We propose an explicit theme in conservation biology termed “coexistence conservation,” that is distinguished by its pursuit of innovative solutions that drive or enable adaptive evolution of threatened species and invasive predators to occur over the long term. We argue evolution has a large role to play but using it to adapt native species to a new environmental order requires a shift in mindset from small, isolated, and short‐term leaps to deliberate, staged steps within a long‐term strategy. A key principle of coexistence conservation is that predation is treated as the threat, rather than the predator, driving a focus on the outcome rather than the agent. Without a long‐term strategy, we face the permanent loss of many species in the wild. Coexistence conservation is a complementary approach to current practice and will play an important role in shifting our current trajectory from continued and rapid invasive predator‐driven defaunation to a world where invasive predators and native prey can coexist.

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“…Having undergone severe population bottlenecks, kākāpō are now highly inbred and suffer from low reproductive success, which is further compounded by their sporadic breeding which only occurs during heavy podocarp mast seasons (approx. every 2 - 4 years) [Merton et al 1984; Powlesland et al 1992; Elliott et al 2001; Eason et al 2006; Savage et al 2021]. However, recent findings suggest that despite their long-term small population size, kākāpō have a reduced number of harmful mutations than expected [Dussex et al 2021].…”

Section: Introductionmentioning

confidence: 99%

Capturing species-wide diversity of the gut microbiota and its relationship with genomic variation in the critically endangered kākāpō

West

Digby²,

Santure

et al. 2022

Preprint

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The gut microbiota plays an essential role in host health that has important implications for the conservation management of threatened wildlife. While factors such as diet, medication, and habitat are known to shape the microbiota, our understanding of the entirety of factors, including the complex role of the host genomic background, remains incomplete. Our research on the gut microbiota of the critically endangered kākāpō (Strigops habroptilus), a flightless parrot species endemic to Aotearoa New Zealand, represents, to our knowledge, the first study to describe the gastrointestinal bacterial diversity for virtually an entire species and to assess the relationship between gut microbiota and host genomic diversity in a highly threatened population. Here we report a 16S rRNA gene–based analysis of kākāpō faecal samples representing the gut microbiota for 84% of kākāpō (n = 133). This survey was then leveraged with exceptional metadata to tease apart the impact of host genomic diversity and factors such as sex, diet, antibiotic treatment, disease status, habitat, and time of sampling on the kākāpō gut microbiota, with sex being the only covariate significantly associated with gut microbiota diversity. We find evidence of a highly polygenic genomic architecture of the gut microbiota and further identify putative associations between gut bacterial diversity and functional biological pathways related to intestinal homeostasis, inflammation, immune response and metabolism. This improved understanding of the kākāpō gut microbiota – and its relationship with host genomics – can directly benefit kākāpō management and conservation by providing new insights into the role of the gut microbiome in kākāpō health and disease mitigation. Overall, we anticipate that an integration of microbiome studies in conservation research and management will improve our understanding of how the concept of One Health with its implications for human, animal and environmental welfare can be achieved.

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Low hatching success in the critically endangered kākāpō is driven by early embryo mortality not infertility

Cited by 15 publications

References 39 publications

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

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

Coexistence conservation: Reconciling threatened species and invasive predators through adaptive ecological and evolutionary approaches

Capturing species-wide diversity of the gut microbiota and its relationship with genomic variation in the critically endangered kākāpō

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