Genetic relatedness reveals total population size of white sharks in eastern Australia and New Zealand

Abstract

Conservation concerns exist for many sharks but robust estimates of abundance are often lacking. Improving population status is a performance measure for species under conservation or recovery plans, yet the lack of data permitting estimation of population size means the efficacy of management actions can be difficult to assess, and achieving the goal of removing species from conservation listing challenging. For potentially dangerous species, like the white shark, balancing conservation and public safety demands is politically and socially complex, often leading to vigorous debate about their population status. This increases the need for robust information to inform policy decisions. We developed a novel method for estimating the total abundance of white sharks in eastern Australia and New Zealand using the genetic-relatedness of juveniles and applying a close-kin mark-recapture framework and demographic model. Estimated numbers of adults are small (ca. 280-650), as is total population size (ca. 2,500-6,750). However, estimates of survival probability are high for adults (over 90%), and fairly high for juveniles (around 73%). This represents the first direct estimate of total white shark abundance and survival calculated from data across both the spatial and temporal life-history of the animal and provides a pathway to estimate population trend.Top-order predators retain a very visible presence in human society due to their size, power, dramatic interactions with prey and infrequent, but high profile, interactions with humans that sometimes result in tragic outcomes. The latter generates considerable public and political debate, particularly for protected species, requiring a delicate balance between maintaining public safety and population recovery 1 . The white shark (Carcharodon carcharias) is emblematic of this duality. It is globally distributed, long lived (>50 yrs), attains up to 6.5 m, and has low reproductive potential making populations vulnerable to decline from human impacts 2,3 . It has gained notoriety from attacks on humans and through its prominence in popular culture 4 . White sharks are listed under international conventions restricting global trade and coordinating conservation measures. They are listed as Vulnerable by the International Union for the Conservation of Nature (IUCN), on Appendix II of the Convention on International Trade in Endangered Species (CITES) and on both Appendices II and III of the Convention on the Conservation of Migratory Species (CMS) 5 . They are protected in the national waters of several countries due to documented or perceived population declines and vulnerabilities given its life history 2 . White sharks are protected in Australia, listed as both Vulnerable and Migratory under the Federal Environment Protection and Biodiversity Conservation Act 1999, protected under various State legislation and subject to a national recovery plan to arrest decline and improve population status 6 . Despite global progress on identifying movement patterns, habitat and populat...

Nearly unbiased estimator of contemporary effective population size using within-cohort sibling pairs incorporating parental and non-parental reproductive variations

“…The latter limitation may be overcome to some extent with the use of a hypervariable region in the mitochondrial genome and/or sex-linked markers. It should be noted that genetic differentiation between maternal and paternal relatives is a general problem with pedigree reconstruction (Huisman, 2017;Hillary et al, 2018). Therefore, incorporating the uncertainty of differentiation or modifying the theory with the use of HS (not MHS) remains a task for future research.…”

“…As a result, a more accurate estimation of contemporary effective population size can be obtained by, for example, more accurately assigned kinships (Wang et al, 2016). In addition, the recently developed theory of estimation of absolute adult number, which is based on sampled kinship pairs and known as the close-kin mark-recapture (CKMR) method (Bravington et al, 2016a,b;Skaug, 2017;Hillary et al, 2018), makes it possible to use a full-sibling (FS) or half-sibling (HS) pair; this involves many more DNA markers for detection than a parent-offspring pair. It should be noted that the CKMR method is designed to minimize the effect of reproductive variance originating from unmodeled covariates, such as avoiding the use of sibling pairs sampled from the same cohorts; meanwhile, reproductive variance strongly affects the estimation of contemporary effective population size.…”

Nearly unbiased estimator of adult population size based on within-cohort half-sibling pairs incorporating flexible reproductive variation

“…The method proposed here provides information pertaining to both the number of mothers and the effect of overdispersed reproduction from the number of within-cohort MHS pairs. A previous study of the HSP-based CKMR method avoided using within-cohort HSPs, as these may lead to a biased estimation due to the effect of within-age variation (Bravington et al 2016b;CCSBT 2017;Hillary et al 2018). Our method overcame this limitation by directly incorporating this effect into the probability that two offspring pairs share an MHS relationship (π).…”

“…Close-kin mark-recapture (CKMR) is a recently developed method that uses information about relatedness in a sample, made possible by recent advances in genetic methods for kinship determination (Bravington et al 2016a,b;Skaug 2017;Hillary et al 2018), although similar ideas have been proposed in the beginning of the 21st century (Nielsen et al 2001;Pearse et al 2001;Skaug 2001). The rationale is that the presence of a kinship pair in the sample is analogous to the recapture of a marked individual in MR. Kinship pairs in the sample are less likely to be found in larger populations; thus, the number of kinship pairs may reflect adult abundance.…”

Nearly unbiased estimator ofNe/Nbased on kinship relationships

“…Close-kin mark-recapture (CKMR) is a recently developed method for estimating N that utilizes the information about kinship in a sample. This was possible owing to the recent advances in genetic methods for kinship determination (Bravington, Grewe, & Davies, 2016;Bravington, Skaug, & Anderson, 2016;Hillary et al, 2018;Skaug, 2017) although similar methods have been proposed in the beginning of the 21st century (Nielsen, Mattila, Clapham, & Palsbøll, 2001;Pearse, Eckerman, Janzen, & Avise, 2001;Skaug, 2001). Besides, the rationale is that the presence of a kinship pair in the sample is analogous to the recapture of a marked individual in mark-recapture.…”