Leucocarbo stewarti

Nicolas J. Rawlence, R. Paul Scofield, Hamish G. Spencer, Chris Lalas, Luke J. Easton, Alan J. D. Tennyson, Mark Adams, Eric Pasquet, Cody Fraser, Jonathan M. Waters & Martyn Kennedy, 2016, Genetic and morphological evidence for two species of Leucocarbo shag (Aves, Pelecaniformes, Phalacrocoracidae) from southern South Island of New Zealand, Zoological Journal of the Linnean Society 177, pp. 676-694 : 687-689

LEUCOCARBO STEWARTI FOVEAUX SHAG

PHALACROCORAX STEWARTI OGILVIE-GRANT, 1898

Diagnosis. A species of Leucocarbo most closely related to L. chalconotus and L. onslowi but distinguished from these species by the plumage characters and allometries outlined in Table 1 .

Distribution. Restricted to Foveaux Strait and Stewart (based on historical museum skins and modern specimens). Leucocarbo stewarti bones have been recorded from Late Quaternary and archaeological deposits from this region (e.g., Worthy, 1998b). Rare archaeological and modern beach wrecks in Otago ( Rawlence et al., 2014, 2015).

TYPE LOCALITIES

The type locality of Gracalus chalconotus G. R. Gray, 1845 is currently considered to be Otago Province. However, the Otago Province included Southland and Foveaux Strait until 1861. We consider that the likely type locality is in fact Karitane, where the type specimen was likely collected by Percy Earl in 1843 ( Scofield et al., 2012). Although Earl spent the majority of his time at Karitane, Earl only travelled as far south as the Clutha River, which is still within the range of the Otago lineage, but may have had Maori ‾ collect for him elsewhere ( Scofield et al., 2012). The type locality of Phalacrocorax stewarti Ogilvie-Grant, 1898 is Bluff (a town in Southland), where specimens were collected by Baron A. von Hugel on 13 February 1875 ( Ogilvie-Grant, 1898 contra Stewart, Gill et al., 2010). Ogilvie-Grant (1898) designated three syntypes ( NHMUK 1880.5.3.1, 1880.5.3.2, and 1880.5.3.6), all pied morphs. Warren (1966) only segregated and listed the syntype 1880.5.3.6 for inclusion in the NHMUK type collection, but this action does not affect the status of the remaining unselected syntypes. NHMUK 1880.5.3.1 and 1880.5.3.2 are currently labelled as Phalacrocorax campbelli huttoni (reflecting a previous taxonomic treatment) and we did not attempt to obtain DNA from them. As all three syntypes were collected from the same locality at the same time, and 1880.5.3.6 clusters with individuals from Foveaux Strait ( Figs. 4 , 6 , Appendix 1), we refer 1880.5.3.1 and 1880.5.3.2 to L. stewarti .

PLUMAGE EVOLUTION AND PHYLOGEOGRAPHICAL

CONSIDERATIONS

Phylogenetic relationships amongst the Otago, Foveaux, and Chatham shags suggest a geologically recent colonization of the Chatham Islands from a mainland South source population, consistent with numerous phylogeographical studies from the region ( Goldberg, Trewick & Paterson, 2008; Mitchell et al., 2014; Wood et al., 2014). All New Zealand /sub-Antarctic Leucocarbo shags have subtle differences in plumage patterns (e.g. scapulars, prenuptial head crest; Marchant & Higgins, 1990). However, the Otago and Foveaux shags are the only Leucocarbo species with adult dimorphic plumage patterns – pied (black and white) and bronze (wholly dark) ( Figs 1 , 2 ). Given our phylogeny ( Fig. 4 ), we can hypothesize that the common ancestor of L. chalconotus , L. onslowi , and L. stewarti evolved dimorphic plumage. Divergence between L. chalconotus and L. stewarti is probably a result of isolation in refugia during the Pleistocene glacial cycles, when the majority of offshore islands and rock stacks in Foveaux Strait and around Stewart favoured by L. stewarti were landlocked because of lower sea levels. The Chatham Islands were colonized by progenitors of L. chalconotus , which evolved into L. onslowi . Colonization was either by pied L. chalconotus individuals or a mixture of pied and bronze individuals, with subsequent genetic drift resulting in the loss of the bronze morph. Given the lack of well-supported structure within the Otago shag we cannot definitively test evolutionary scenarios for the bronze morph, but it seems much simpler to assume that the bronze morph evolved once and was subsequently lost in L. onslowi than that it evolved independently twice (in the Otago shag and in the Foveaux shag).

CONSERVATION IMPLICATIONS

Prior to our splitting of the Stewart shag into two distinct taxa, the International Union for Conservation of Nature Red List categorized this species as Vulnerable with population estimates varying between 1600 and 1800 pairs to fewer than 5000 birds and threats including fisheries interactions and nest disturbance ( Birdlife International, 2012). Given their revised status, Otago and Foveaux shags should be managed separately, with further population-genetic research to determine levels of genetic variation at faster-evolving nuclear loci and potential inbreeding (e.g. Calderon et al., 2014). The Foveaux shag has been characterized by population and range stability, in contrast to the Otago shag that has undergone a pronounced population bottleneck and range contraction ( Rawlence et al., 2015). Although the Otago shag has recolonized part of its former distribution since the European era, its population size continues to decline ( Lalas & Perriman, 2009).

Figures

Figure 1. Distributional and morphological data for Otago, Foveaux, and Chatham Island shags. A, map of New Zeal- and showing the location of the Chatham Islands and Otago / Foveaux Strait study sites. Blue circles represent the prehistoric distribution of Otago shag outside the study area. B, distribution of Chatham Island shag breeding colonies and roosting sites (green circles). The Chatham Island shag exhibits pied plumage only (white pie chart) with pronounced bright orange caruncles in breeding plumage (orange pie chart). C, distribution of Otago (blue circles) and Foveaux (red circles) shag breeding colonies and roosting sites. Otago shag populations have 20 – 30 % pied morphs (pie charts; black: dark-bronze; white: pied) and 50: 50 % small bright orange caruncles: dark orange scattered papillae in prenuptial breeding plumage (pie charts; yellow: small bright orange caruncles; grey: dark orange scattered papillae) compared with 50 – 60 % pied morph and dark orange scattered papillae in prenuptial breeding plumage in the Foveaux shag. In (C), multiple breeding colonies and roosting sites are represented at the following locations (from north to south): Otago Peninsula including Long Beach, Aramoana, Otago Harbour, Taiaroa Head, Boulder Beach, Papanui Beach, Allans Beach, Wharekakahu Island, and Gull Rocks; Seal Rocks and Ruapuke Island; Easy Harbour and Shag Rock. In (C), the Leucocarbo shag species illustrating plumage characters are: pied morph (Otago shag), bronze morph (Foveaux shag), small caruncles (Otago shag), and scattered papillae (Foveaux shag). Figure adapted from Rawlence et al. (2014).

Figure 2. Carunculation and gular pouch colour in pied morphs of Chatham Island, Otago, and Foveaux shags. The Chatham Island shag (left) has pronounced bright orange facial caruncles and gular pouch; the Otago shag (centre) has equal frequencies of small bright orange facial caruncles (shown) and dark orange scattered papillae (not shown), and bright to dark orange (shown) or purple (not shown) gular pouch; the Foveaux shag (right) has scattered dark orange papillae (shown) and bright to dark orange (shown) gular pouch. Photos (not to scale) courtesy of New Zealand Birds Online (John Kendrick, left and Brian Bell, right) and Hiltrun Ratz (centre).

Figure 4. The Bayesian phylogram of Leucocarbo shags from an analysis with a single individual of each haplotype (from BEAST v. 1.7.4). Apart from the two outgroup taxa, the labels show the species (Leucocarbo chalconotus, Leucocarbo onslowi, and Leucocarbo stewarti) with the haplotype in parentheses (for haplotype designation see Table S 5). The

Figure 6. Principal component analysis (PCA) of pooled measurements from museum skins for 21 Otago shags (blue squares), 34 Foveaux shags (red triangles), and seven Chatham Island shags (green diamonds). Type specimens for Otago shag (Gracalus chalconotus, Graculus glaucus, and Phalacrocorax huttoni) and Foveaux shag (Phalacrocorax stewarti) are shown with labelled black circles. PC 1 loadings> 0.5 / <- 0.5, PC 2 loading Phal 0.82.

Tables

Table 1. Species diagnoses for the Otago shag Leucocarbo chalconotus (G. R. Gray, 1845), Foveaux shag Leucocarbo stewarti (Ogilvie-Grant, 1898), and Chatham Island shag Leucocarbo onslowi (Forbes, 1893)

	Chatham Island shag
Feature	( L. onslowi )	Otago shag ( L. chalconotus )	Foveaux shag ( L. stewarti )	References
Prehistoric distribution	Chatham Islands	Eastern South Island	Foveaux Strait	Rawlence et al. (2015)
Modern distribution	Chatham Islands	Otago	Foveaux Strait	Lalas (1983), Lalas &
				Perriman (2009),
				Rawlence et al. (2014)
DNA [fixed mtDNA control	Monophyletic clade ‘daughter’	Monophyletic clade,	Monophyletic clade basal to	Rawlence et al. (2014,
region 1 (CR1) differences,	to L. chalconotus .	distinguished from	L. chalconotus / L. onslowi .	2015)
248 bp; full CR, 1040 bp.	Distinguished from	L. stewarti by C-T (92), G-A	Distinguished from L. chalconotus
Numbers in parentheses	L. chalconotus by C-T (40),	(110), C-T (148), T-C (229),	by T-C (92), A-G (110), T-C (148),
represent the base pair	T-C (50), and C-T (105).	G-A (493), and T-C (628).	C-T (229), A-G (493), and C-T
position (e.g. 40) in the	Distinguished from	Distinguished from	(628). Distinguished from
CR1 sequence where the	L. stewarti by T-C (24), C-T	L. onslowi by T-C (40), C-T	L. onslowi by C-T (24), T-C (40),
fixed difference (e.g. C-T)	(40), C-T (92), C-T (105),	(50), and T-C (105)	T-C (92), T-C (105), A-G (110), C-T
occurs.	G-A (110), T-C (117),		(117), T-C (148), C-T (229), A-G
	C-T (148), T-C (229), G-A		(493), and C-T (628).
	(493), and T-C (628).
Plumage morphs	Pied (black and white)	Pied (black and white),	Pied (black and white), bronze	Lalas (1983); Marchant
		bronze (wholly dark)	(wholly dark)	& Higgins (1990);
				Rawlence et al. (2014)
Plumage morph	100% pied	~20–30% pied	~50–60% pied	Lalas (1983); Rawlence
percentages				et al. (2014)
Carunculation (breeding	Pronounced bright orange	Equal frequencies of small,	Scattered dark orange papillae	Lalas (1983); Rawlence
plumage)	facial caruncles	bright orange facial		et al. (2014)
		caruncles and dark orange
		scattered papillae
Gular pouch (breeding	Bright orange	Bright to dark orange or	Bright to dark orange	Lalas (1983); Rawlence
plumage)		purple		et al. (2014)
Morphometics/allometries	Smaller on average than both	Larger on average than both	Smaller on average than	Lalas (1983); Rawlence
	L. chalconotus and	L. stewarti and L. onslowi	L. chalconotus , and similar in size	et al. (2014); this study
	L. stewarti		to L. onslowi
Osteology	The foramen vasculare	The foramen vasculare	The foramen vasculare distale on	Worthy (2011); this
	distale on the distal	distale on the distal	the distal tarsometatarsus is small	study
	tarsometatarsus is small	tarsometatarsus varies in
		size
Onset of breeding season	September–February	May–September	September onwards	Lalas (1983)