Reinstatement of the Loyalty Islands Sandalwood, Santalum austrocaledonicum var. glabrum (Santalaceae), in New Caledonia

Abstract Sandalwoods encompass 19 species restricted to southeast Asia and the Pacific. The species Santalum austrocaledonicum Vieill. (Santalaceae) is endemic to New Caledonia (Grande-Terre, Isle of Pines, Loyalty Islands) and Vanuatu, where several varieties are recognized. The Loyalty Islands sandalwood variety is here reinstated as Santalum austrocaledonicum var. glabrum Hürl. emend. Butaud & P.Firmenich, mut. char. It was previously considered a synonym of the type variety; however, new morphological and genetic studies confirmed its distinctiveness. The key for New Caledonian varieties of Santalum austrocaledonicum has been updated and a short description of its essential oil composition and organoleptic quality is given.


Introduction
Sandalwoods are shrubs or small trees well known for the essential oil extracted from their fragrant heartwood and used in perfumery. Th ey belong to the genus Santalum (Santalaceae) comprising 19 species restricted to southeast Asia and the Pacifi c (Harbaugh and Baldwin 2007, Harbaugh 2007, Harbaugh et al. 2010. Th e most soughtafter species is the Indian sandalwood, Santalum album L. Santalum austrocaledonicum Vieill. is the only native sandalwood in New Caledonia and Vanuatu (Guillaumin 1925, Hallé 1988, Harbaugh and Baldwin 2007, and is endemic to these archipelagoes. It has been heavily harvested for the past 150 years (Shineberg 1967) and its wood is still exploited for the fragrance industry as its essential oil can be considered as a substitute for Indian sandalwood oil (Braun et al. 2005).
No comprehensive study of the variation of these characters is available in Vanuatu due to lack of herbarium specimens from most of sandalwood populations there.
For this reason,  intended to describe the Loyalty endemic sandalwood under the variety loyaltensis but his manuscript was never published.
More recently, molecular studies of New Caledonian sandalwood showed strong genetic diff erentiation between islands and led to the recognition of two evolutionarily signifi cant units, i.e. Grande-Terre and Isle of Pines for the fi rst, and Loyalty Islands for the second (Bottin et al. 2005(Bottin et al. , 2007. Th e New Caledonian sandalwood is subject to exploitation through harvesting and is grown in plantations to satisfy the increasing international demand of sandalwood essential oil. However, its taxonomy appears to be in need of revision to more precisely describe the variability of this New Caledonian biodiversity hotspot species (Myers et al. 2000) and to contribute to the sustainable management of this natural resource.
A fi rst step of this revision is presented here, with the recognition of an endemic sandalwood variety from the Loyalty Islands based on morphological and molecular studies as well as examination of living plants and herbarium specimens.

Nomenclature
Th e New Caledonian sandalwood, Santalum austrocaledonicum, was described by Vieillard (1861) from samples collected on the hills of Arama, in the Northern extremity of Grande-Terre (E. Vieillard 1090, holotype P00645808). Later, it was confi rmed that this species was also present on the Isle of Pines, Loyalty Islands and Vanuatu (Guillaumin 1925, Virot 1950. In 1964, Hürlimann described a new variety based on a sample collected on the island of Maré in the Loyalty Islands (Stauff er and Hürlimann 1964), Santalum austrocaledonicum var. glabrum Hürl. characterized by glabrous fl owers, diff ering from the type variety (Santalum austrocaledonicum Vieill. var. austrocaledonicum) represented erroneously by samples gathered around Nouméa (Ouen Toro, Anse Vata, Baie de l'Orphelinat) which have villous fl owers.
In 1988, the revision of the New Caledonian Santalum by Hallé recognized the three varieties mentioned in the introduction. Hallé reduced var. glabrum of Hürlimann to synonymy under the type (autonym) variety, considering it superfl uous due to confusion by Hürlimann on what was really the type of the species. Indeed, the latter described var. glabrum in comparison with what is now recognized as var. pilosulum, this one diff ering morphologically from var. austrocaledonicum. Th e true var. austrocaledonicum and var. glabrum are in fact identical relative to the morphological diff erences pointed out by Hürlimann in his diagnosis.
As the native Loyalty Islands sandalwoods are quite homogeneous, only one variety is to be recognized for the entire Loyalty archipelago, which is the one of Hürlimann. Th us, to reinstate the varietal name glabrum for the endemic Loyalty sandalwood, its description must be amended to distinguish it from the true type specimen. Diagnosis. Santalum austrocaledonicum var. glabrum is most similar to var. austrocaledonicum in its glabrous infl orescence and leaves wider than 1.5 cm, which diff erentiates them from the other New Caledonian S. austrocaledonicum varieties. Santalum austrocaledonicum var. glabrum diff ers from S. austrocaledonicum var. austrocaledonicum by the seed size, which is more than 7.5 mm wide for the former and less than 7.5 mm for the latter.
Phenology. Flowering and fruiting probably occurring throughout the year but with some peaks; herbarium samples provide the following data: fl owers from December to August, fruits from January to August.
Distribution. New Caledonia, endemic to Loyalty Islands; known only from Ouvéa, Lifou and Maré islands (Figure 1). Not recorded on the smaller islands of Beautemps-Beaupré, Tiga and Walpole.
Habitat and biology. Th is variety is restricted to the calcareous soils of uplifted atolls between 5 and 80 m elevation and is closely linked with traditional agriculture which consists of shifting cultivation. Regeneration by seeds occurs mainly in the open cultivated areas and young fallow lands. Loyalty sandalwood is therefore characteristic of fallows, shrublands and secondary forests, and rarely occurs in mature forests. It is also commonly found along roads and close to villages in open areas where it is generally protected and managed by inhabitants. Th e surrounding vegetation is often composed of trees and shrubs, such as Acacia spirorbis Labill., Acalypha spp., Acronychia laevis J.R.Forst. & G.Forst., Dodonaea viscosa (L.) Jacq., Elattostachys apetala (Labill.) Radlk., Glochidion billardierei Baill., Melochia odorata L.f., Morinda citrifolia L., Pandanus macrocarpus (Brongn.) Solms, Podonephelium homei (Seem.) Radlk., Polyscias bracteata (R.Vig.) Lowry subsp. bracteata., Psidium guajava L., and Schinus terebenthifolius Raddi. Loyalty sandalwood is a hemiparasitic tree like all Santalum species; its pollination is insect-mediated whereas its fl eshy fruits are dispersed mainly by doves and pigeons (Bottin et al. 2005).
Conservation status. Using the categories and criteria of IUCN (2001), we propose for S. austrocaledonicum var. glabrum the IUCN Red List Category Vulnerable (VU): B (1+2) ab (iii,v). Its population size is estimated at more than 10,000 mature individuals (excluding criteria C and D) with an extent of occurrence around 8,000 km² and an area of occupancy around 1,000 km². Criteria A can not be used due to lack of knowledge of generation length and magnitude of population size reduction. Th ree locations (one per island) can be distinguished without any fragmentation. A continuing decline is observed and projected in terms of habitat quality and number of mature individuals due to harvest, competition with invasive plant species (Schinus terebenthifolius Raddi, Pluchea odorata (L.) Cass., Lantana camara L.), hybridization with other S. austrocaledonicum varieties used in plantations, and changes in the traditional agricultural system (less cultivated fi elds, short fallows...). Indeed, despite provincial regulations establishing quota and exploitability criteria, illegal logging is still occurring (Butaud et al. 2013) whereas hybridization is suspected due to sandalwood interspecifi c crossability (Tamla et al. 2012).
Discussion. Santalum austrocaledonicum var. glabrum is the sole native sandalwood in the Loyalty Islands. Nevertheless, two other varieties have been introduced for plantation purposes, mainly in Maré and Lifou: var. pilosulum from Ouen Toro in Nouméa, and var. austrocaledonicum from Isle of Pines. Th ese plantations can be considered a risk for the Loyalty variety because of hybridization and subsequent introgression. Plantations with exotic varieties should be discouraged to preserve the  Loyalty sandalwood's morphological, genetic, sylvicultural and chemical specifi cities (Bottin 2006, Bottin et al. 2007, Butaud et al. 2013, Ehrhart 1998). On the other hand, the sustainable exploitation of natural stands of Loyalty Islands sandalwood is becoming increasingly diffi cult with the lack of regeneration and the increasing international demand for sandalwood essential oil. Well-managed plantations with variety glabrum could be promoted to preserve the natural stands, to develop the Loyalty sandalwood sector, and to increase the production of heartwood and essential oil (Butaud 2011, Butaud et al. 2013. Th e taxonomy of S. austrocaledonicum still needs to be further investigated. Indeed, the study of herbarium samples of var. austrocaledonicum and previous molecular and morphometric studies (Bottin 2006, Bouvet et al. 2005 showed signifi cant variability. It is expected that future work supported by increased surveys and sampling of northern Grande-Terre sandalwood could reveal one or two new varieties, including one on Isle of Pines (taxon previously described as Santalum homei Seem.). Moreover, two new endemic varieties of S. austrocaledonicum are expected based on the recent study of Millet et al. (2012) on the genetic structure of Vanuatu sandalwood, one for the northern islands and one for the southern islands.

Essential oil quality
Essential oil of Santalum austrocaledonicum was previously assessed for its composition and organoleptic properties, and was considered as a possible substitute for Indian sandalwood oil (Santalum album) but also as a promising new raw material for the fra-grance industry (Braun et al. 2005). Th ese evaluations were performed on essential oils resulting from mixtures of sandalwood varieties glabrum (Loyalty islands), pilosulum (surroundings of Nouméa) and austrocaledonicum (Isle of Pines), leaving unknown the quality of each individual variety.
Th e organoleptic evaluation showed that the Loyalty essential oil is lighter and less milky than the Indian sandalwood; the former has also a character less woody but more animal and masculine (P.-A. Blanc and S.A. Firmenich, pers. comm. 2015).
Th ese fi ndings are in accordance with Braun et al. (2005), especially for the organoleptic evaluation. Moreover, the composition of both Loyalty essential oils meets the ISO Standard for Indian sandalwood, which was not the case for the samples of the previous study. Th us, Santalum austrocaledonicum var. glabrum or Loyalty sandalwood constitutes a true substitute for Indian sandalwood in the perfume industry.

Acknowledgments
I am grateful to the Province des Iles Loyauté (PIL) which has initiated and supported recent investigations on the Loyalty Islands fl ora, to the Firmenich Charitable Foundation for supporting taxonomical studies, and to the Herbier du Centre IRD de Nouméa (NOU) for access to its Santalum collections. I thank Gildas Gâteblé (Institut Agronomique néo-Calédonien) for helpful discussions on Loyalty Islands Santalum, and, together with David Lorence (National Tropical Botanical Garden, Hawai'i), Art Whistler, and Jacques Florence (IRD), for their important comments and corrections of previous drafts of this paper. I appreciate review comments by Daniel Nickrent and an unknown reviewer.
I am indebt to Christian Vial and Pierre-Alain Blanc (Firmenich S.A.) for, respectively, gas-chromatography analysis and organoleptic analysis of S. austrocaledonicum var. glabrum essential oils, and to Annette Olsson (Conservation International) for English wording review. I am also grateful to George Kakue, Luen Iopue, Meri Th upalua (PIL) and Jean-Christophe Lefeuvre (Conservation International) for their support and interest in establishing a Flora of Loyalty Islands, and to Selma Haouet for providing the map background.