Speciation, range contraction and extinction in the endemic New Zealand King Shag complex
Graphical abstract
Introduction
Prehistoric anthropogenic processes are thought to underlie the extinction of numerous vertebrate species worldwide (Sandom et al., 2014). While the majority of studies addressing human impacts have focused on terrestrial species (Lorenzen et al., 2011), recent ancient DNA (aDNA) analyses have detected similar extinctions and declines in prehistoric coastal vertebrate taxa (Boessenkool et al., 2009, Collins et al., 2014, Rawlence et al., 2015a, Rawlence et al., 2015b, Rawlence et al., 2016b, Grosser et al., 2016, Salis et al., 2016, Waters et al., 2017).
New Zealand has an exceptionally rich seabird and marine mammal fauna, including numerous endemic seabird taxa (Gill et al., 2010, Smith, 2013). Archaeological and palaeontological (from natural pre-human Holocene fossil sites) data suggest that many of these species may have experienced major range contractions and extinctions associated with human impacts (e.g. over-hunting, habitat destruction, predation from introduced rats and dogs) at a time of relative climatic stability (Holdaway et al., 2001, Smith, 2013). Indeed, the climate in New Zealand has been relatively stable for much of the late Holocene, with any minor climatic fluctuations unlikely to cause range contractions and extinctions (Wanner et al., 2008, Rawlence et al., 2015a, Rawlence et al., 2015b, Rawlence et al., 2016b). The Otago Shag (Leucocarbo chalconotus), for example, suffered pronounced regional extinctions and losses of genetic diversity shortly after human settlement (Rawlence et al., 2015a, Rawlence et al., 2016a) (Fig. 1). This species suffered an extreme range contraction, losing >99% of its population size and corresponding genetic diversity within a century of Polynesian arrival. Similar patterns have been observed in New Zealand Fur Seal (Arctocephalus forsteri; Salis et al., 2016). The Waitaha Penguin (Megadyptes waitaha) and prehistoric New Zealand Sea Lion (Phocarctos hookeri ‘NZ’) became extinct shortly after human contact, only to be replaced by the previously subantarctic-limited Yellow-eyed Penguin (Megadyptes antipodes) and Hooker’s Sea Lion (P. hookeri ‘sub-antarctic’), respectively, within a few decades (Boessenkool et al., 2009, Collins et al., 2014, Waters et al., 2017 - see also Grosser et al., 2016).
Here we assess additional impacts on mainland New Zealand’s seabirds, specifically endemic blue-eyed shag (Leucocarbo spp.) diversity. First documented by J. R. Forster on James Cook’s second voyage in 1773, the New Zealand King Shag (L. carunculatus) is an endemic species that has been restricted to a narrow portion of northeastern South Island (Marlborough Sounds; Fig. 1) for at least the past 240 years (Buller, 1888, Bell, 2010). Historical accounts from European naturalists and museum records indicate that the King Shag has only been observed in Marlborough Sounds (Buller, 1888, Bell, 2010). The King Shag is currently listed as ‘threatened’ under both the IUCN and New Zealand threat classification systems (Townsend et al., 2008, IUCN, 2015). With a population size of just over 800 birds, the King Shag is now restricted to just eight isolated breeding colonies situated on rocky islets, with 85% of the population located at five sites (Schuckard et al., 2015). Notwithstanding many morphological similarities with other Leucocarbo taxa (Rawlence et al., 2016a), genetic data confirm that the King Shag is a separate species from all other New Zealand blue-eyed shags (Kennedy and Spencer, 2014), not, as previously thought conspecific with the Otago Shag (L. chalconotus; Worthy, 1996, Holdaway et al., 2001, Worthy and Holdaway, 2002). Conservation management of the King Shag has been hampered by this previous taxonomic uncertainty, as well as the uncharismatic status of shags in general (Williams, 1945) and the illegal culling of individuals to protect fisheries stocks (Marchant and Higgins, 1990).
Despite the narrow modern range of the King Shag, a previous morphological analysis (Worthy, 1996, Worthy and Holdaway, 2002) tentatively attributed prehistoric Leucocarbo remains from northern New Zealand and southern North Island (McFadgen, 2003) to this now localised taxon based on geographic proximity to the nearest other Leucocarbo colony – albeit up to ca. 1000 km distant. Here we test the hypothesis that the contemporary King Shag population represents a ‘relict’ of a formerly widespread endemic. Alternatively, these extinct northern mainland populations could represent a distinct taxon (cf. L. chalconotus, stewarti and onslowi; Rawlence et al., 2016a). Leucocarbo are highly sedentary seabirds in contrast to pelagic seabirds, and as such, the phylogeographic structure of Leucocarbo is more akin to some terrestrial flightless birds (e.g. moa [Bunce et al., 2009, Rawlence et al., 2012] and kiwi [Weir et al., 2016]). Indeed, on the New Zealand mainland, there are currently three recognised species of Leucocarbo (Kennedy and Spencer, 2014, Rawlence et al., 2016a). Here we use aDNA, morphometric and osteological analyses to assess the affinities of prehistoric Leucocarbo specimens from coastal New Zealand, and infer the recent biogeographic history of the genus in this part of New Zealand.
Section snippets
Source of specimens
Modern King Shag tissue and feather samples, sourced from dead beach wrecked birds and breeding colonies, respectively, across the species’ contemporary range, were obtained from a variety of locations (n = 9; Table S1). Due to the isolated nature of the breeding colonies and high probability of nest disturbance from sampling efforts, larger sample sizes were not obtainable. Prehistoric (ca. 4500 years ago to 1450 CE based on associated radiocarbon dates; Millener, 1981, Millener, 1990) bones,
Phylogenetic analysis
DNA sequence data were obtained for CR1 for all nine modern King Shag samples (sourced from the northern South Island), covering the majority of the contemporary breeding colonies. The full 248 bp fragment was obtained for two prehistoric Leucocarbo specimens from northern South Island and northern New Zealand, while the smaller 156 bp (BESCR1 F1-R1) and 75 bp (BESCR1 F2-R1) fragments were obtained for a further one (northern New Zealand) and four (northern New Zealand and northern South Island)
Discussion
Phylogenetic, morphometric and osteological analysis of prehistoric Leucocarbo material from mainland New Zealand has shown that the species complex that includes the threatened New Zealand King Shag was once distributed around coastal North Island, up to 1000 km outside its current distribution (Fig. 1), and contains two genetically and morphologically distinct lineages that, although tentatively currently recognised as a single taxon, we argue belong to discrete species. The discovery of a new
Acknowledgements
We thank Auckland Museum (Jason Froggatt, Brian Gill), Museum of New Zealand Te Papa Tongarewa, and Canterbury Museum for access to specimens and supplying samples. Thank you to Jean-Claude Stahl (Te Papa) for photography, Mennobart van Eerden for the King Shag photograph in Fig. 1; and Felix Marx and Ken Miller for help with figure construction. We thank Trevor Worthy and one anonymous reviewer whose comments help improve this manuscript. We also thank Ngati Kuri for providing the common name
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