A new species in the tree genus Polyceratocarpus (Annonaceae) from the Udzungwa Mountains of Tanzania

Abstract Polyceratocarpus askhambryan-iringae, an endemic tree species of Annonaceae from the Udzungwa Mountains of Tanzania, is described and illustrated. The new species is identified as a member of the genus Polyceratocarpus by the combination of staminate and bisexual flowers, axillary inflorescences, subequal outer and inner petals, and multi-seeded monocarps with pitted seeds. From Polyceratocarpus scheffleri, with which it has previously been confused, it differs in the longer pedicels, smaller and thinner petals, shorter bracts, and by generally smaller, less curved monocarps that have a clear stipe and usually have fewer seeds. Because Polyceratocarpus askhambryan-iringae has a restricted extent of occurrence, area of occupancy, and ongoing degradation of its forest habitat, we recommend classification of it as Endangered (EN) on the IUCN Red List.


Introduction
Th e Eastern Arc Mountains of Kenya and Tanzania are well known for their high levels of biodiversity and endemism across many plant and animal groups (Lovett and Wasser 1993, Myers et al. 2000, Newmark 2002, Dawson and Gereau 2010. Th e 13 mountain blocs making up the chain are somewhat isolated from one another, and each block exhibits its own unique suite of species. Many of the forests occupying these mountains are under threat from expanding agriculture and human population increase: an estimated 2.79 Mha of forest was lost between 1908 and 2000 (Willcock et al. 2016), with just 10% of the Eastern Arc Mountains still forested (Platts et al. 2011). Th ese development pressures have added urgency to the inventory of the unique biota of this region.
Within the Eastern Arc chain, the 19,375 km 2 Udzungwa Mountains form the largest mountain bloc (Platts et al. 2011) and comprise the largest area of forest in the Eastern Arc Mountains, totaling around 1,600 km 2 . Th e Udzungwa Mountains have enormous biodiversity value, with the highest plant species richness, the highest endemic vertebrate species richness, and the second highest endemic plant species richness of all mountain blocs in the region Rovero et al. 2014). Th e distinctive character of Udzungwa biodiversity has been recently highlighted by high-profi le mammal species discoveries including the kipunji monkey (Rungwecebus kipunji; Davenport et al. 2006) and Udzungwa elephant shrew (Rhynchocyon udzungwensis; Rovero et al. 2008).
Species of the fl owering plant family Annonaceae are prominent among the understory trees and woody climbers of the Eastern Arc Mountains. In these mountains, there are 50 known Annonaceae species, 16 of which are endemic, including 12 out of 127 reported endemic tree species (R.E. Gereau, unpubl. data).
Th e genus Polyceratocarpus Engl. & Diels (Annonaceae subfamily Malmeoideae, tribe Piptostigmateae, Chatrou et al. 2012) is distinguishable from other African genera of the family by the combination of a tree habit, percurrent tertiary veins of the leaves, axillary (sometimes caulifl orous) infl orescences, occurrence of both staminate and bisexual fl owers, petals of the outer and inner whorls roughly equal in size and shape, numerous monocarps with multiple seeds arranged in a single row, and pitted seeds with spiniform ruminations ). Engler and Diels (1900) published the genus based on P. scheffl eri Engler & Diels, collected in the Usambara Mountains. Since that time seven additional species have been added to the genus, all from western and central Africa.

Polyceratocarpus askhambryan-iringae
Distribution. Polyceratocarpus askhambryan-iringae is endemic to the Udzungwa Mountains of Tanzania. It is known from Mwanihana Forest in the Udzungwa Mountains National Park, Ndundulu Forest in the Kilombero Nature Reserve, and the Uzungwa Scarp Forest Reserve (Fig. 1).
Habitat and ecology. Inhabits montane forest on brown sandy loam soils (pH range 4-5 measured in Ndundulu Forest). Mean annual rainfall of collection localities approximately 1500-2000 mm/yr (Marshall, Ndangalasi, unpubl. data). Th irty-eight mature individuals were found mostly on slopes or ridge-tops at elevations 1090-1540m. Mature fl owers were collected in May, November, and December, fruits in February and May-October.
Associated taxa recorded with Polyceratocarpus askhambryan-iringae include the following: (1) Ndundulu Forest: Allanblackia ulugurensis Engl., Alsodeiopsis schumannii Engl.; Anisotes pubinervius (T.Anderson) Heine, Anthocleista grandifl ora Gilg,     Additional fi eld notes. Slash dry, slightly stringy, pale yellow (to pale peach), occasionally streaked yellow-brown, dark brown at outer edge formed by the colour of the inner bark, potpourri aroma. Leaf lamina dark green above, mid-green with greyish tinge below, turning greenish-grey when dried, new fl ush pinkish; petiole initially pale green in vivo, becoming roughened grey-brown with age; midrib yellow-green above and below in vivo. Flower buds broadly ovoid, green or pale brown-yellow with occasional pink tinge at apex in vivo; sepals yellowish-green in vivo.
Etymology. Th is new species of Polyceratocarpus was named by Askham Bryan College and Iringa International School as part of a rainforest education program.
Conservation status. Our IUCN Red List assessment for P. askhambryan-iringae was based on "area of occupancy" (AOO), "extent of occurrence" (EOO; IUCN 2012) and the level of threat. Th e 38 observed mature P. askhambryan-iringae stems were found at four collection localities, with only 112 km between the most distant individuals. Th e four collection localities represented three diff erent levels of governmental protection, including Forest Reserve (Uzungwa Scarp), Nature Reserve (Kilombero, KNR; and also Uzungwa Scarp proposed status) and National Park (Udzungwa Mountains; UMNP), with only UMNP having the maximum level of protection under Tanzanian law (IUCN category II; Dudley 2008). At the time of survey, the greatest threat to P. askhambryan-iringae was widespread timber-felling observed in Uzungwa Scarp Forest Reserve. Conversely, threats to P. askhambryan-iringae in KNR and UMNP were much lower, both comprising only very occasional removal of polesized trees by villagers, and potential damage from an increasing elephant population (Marshall et al. 2012). KNR was further threatened by a lack of formal ranger patrols and rapid population expansion in the nearest villages. Given that the sources of threat were closely associated with the three protected areas, for the purpose of Red List assessment we considered three rather than four threat-defi ned "locations" (IUCN 2012). In calculating AOO, we used 10 km 2 grid cells so that the projected area was not extrapolated far beyond the expected habitat tolerance of the species. We estimated an AOO of 300 km 2 and an EOO of 1,410 km 2 , with EOO, AOO, habitat quality and the number of mature individuals, all presumed declining as a result of timber-felling in USFR. Given this continuing decline, plus an EOO of less than 5,000 km 2 , an AOO of less than 500 km 2 , and a population at no more than fi ve locations, the species qualifi ed fi rmly as endangered on the IUCN Red List (IUCN 2012), EN B1ab(i, ii,iii,v)+2ab(i,ii,iii,v). Within the Udzungwa Mountains, closed-canopy forest was not extensive at elevations suitable for P. askhambryan-iringae, and hence we expect that future expeditions will not expand the AOO or EOO of P. askhambryan-iringae above the IUCN endangered threshold. However, the Rubeho and Mahenge mountain blocs adjacent to Udzungwa were more poorly known, and may contain suitable habitat in which this species might also be found.

A) Systematics
Polyceratocarpus askhambryan-iringae is similar to P. scheffl eri and has previously been confused with it. As far as is known, however, P. scheffl eri is confi ned to the Usambara Mountains and P. askhambryan-iringae to the Udzungwa Mountains; previous reports of P. scheffl eri from the Udzungwa Mountains (e. g. Lovett et al. 1988, Couvreur et al. 2006 Lamina rounded and minutely subcordate at base, with tertiary veins reticulate to weakly scalariform; pedicel 15-29 mm long, bearing a bract 0.8-1 mm long; sepals connate only at base, distinct, crescent-shaped; petals 10-17 mm long; monocarps up to 18 per fruit, (1.9-) 6-8.6 cm long, weakly recurvedfalciform, short-stipitate ( Th e genus Polyceratocarpus outside East Africa has a Guineo-Congolean distribution, with the other seven species scattered from Côte d'Ivoire to northern Angola and the Democratic Republic of the Congo. Polyceratocarpus askhambryan-iringae and P. scheffl eri both diff er from most of the more western species in having larger numbers of carpels and large strongly torulose monocarps. Th e only other species with such a high number of carpels (18 to 20) is Polyceratocarpus laurifolius Paiva from northern Angola, but that species diff ers from P. askhambryan-iringae in having densely pubescent twigs, a distinctly cuneate base to the leaf, a larger bract on the pedicel, and larger sepals. Polyceratocarpus laurifolius also diff ers from P. askhambryan-iringae in having larger petals of the staminate fl owers than of the bisexual ones (Paiva 1966); in P. askhambryan-iringae no petal dimorphism between staminate and bisexual fl owers was seen.
Polyceratocarpus askhambryan-iringae (as "Polyceratocarpus sp.") was one of four Polyceratocarpus species included in the phylogenetic analysis of Couvreur et al. (2009) focused on the phylogeny of several closely related African genera of Annonaceae. In this analysis P. askhambryan-iringae appeared as sister to the other three species of Polyceratocarpus sampled (P. microtrichus (Engl. & Diels) Ghesq. & Pellegr., P. parvifl orus (Baker f.) Ghesq., and P. pellegrinii Le Th omas) forming a monophyletic group with strong bootstrap and posterior probability support. Th e other fi ve species remain to be sampled. Th e genus itself, however, was nested within the western and central African genus Piptostigma Oliv., to which it is morphologically dissimilar, so additional sampling is needed.

B) Regional endemism and biodiversity
East Africa is an area of both high endemism and high diversity for Annonaceae, with 28 genera and 85 species known from Tanzania alone (Couvreur et al. 2006). In particular, the Eastern Arc Mountains form an area of high species endemism for East African Annonaceae. Furthermore, many Annonaceae genera represented in these mountains have main areas of diversity in the Guineo-Congolean region and are represented in the Eastern Arc Mountains by endemic taxa. In addition to Polyceratocarpus, the genera Annickia Setten & Maas, Greenwayodendron Verdc., Isolona Engl., Monodora Dunal, Uvariodendron (Engl. & Diels) R.E. FR., and Uvariopsis Engl. all follow this pattern (Verdcourt 1971, 1986, Couvreur et al. 2006, Couvreur 2009, Couvreur and Luke 2010. Polyceratocarpus askhambryan-iringae also adds to the growing list of species unique to the Udzungwa bloc, including various recently discovered plants (e.g. Luke and Beentje 2003;Knox et al. 2004). Th ere are now 71 known endemic plant species from the Udzungwa Mountains (comprising 15 trees, including P. askhambryan-iringae); among the Eastern Arc Mountains this is second only to the Uluguru Mountains (86 endemic species [14 trees]; R.E. Gereau, unpubl. data). P. askhambryan-iringae is the second large tree (≥20m) and the third endemic Annonaceae species to be described from the Udzungwa Mountains over the last 20 years, following the respective discoveries of Omphalocarpum strombocarpum Y.B.Harv. & Lovett (Harvey and Lovett 1998), Toussaintia patriciae Q. Luke & Deroin (Deroin and Luke 2005) and Monodora globifl ora Couvreur (Couvreur et al. 2006). Given further new species descriptions in preparation and the larger size of the Udzungwa Mountains, it is likely to be the most important Eastern Arc Mountain bloc for tree species endemism. More plant species are known from the Udzungwa Mountains than other Eastern Arc Mountain blocs, and while this is partly due to increased survey eff ort over other blocs, recent projections by distribution models estimate that the number of endemic/threatened plant taxa will not be superseded following increased exploration of other blocs .
Th e four P. askhambryan-iringae localities are coextensive with other recent discoveries of rare and endemic Eastern Arc animals, e.g. the Critically Endangered endemic Sanje mangabey (Cercocebus sanjei; Mwanihana and Uzungwa Scarp), the Critically Endangered kipunji monkey (Rungwecebus kipunji; Ndundulu; also found on Rungwe Mountain), the endemic Udzungwa forest partridge (Xenoperdix udzungwensis; Ndundulu), the endemic rufous-winged sunbird (Nectarinia rufi pennis; Mwanihana, Ndundulu and Uzungwa Scarp), the endemic Udzungwa elephant shrew (Rhynchocyon udzungwensis; Ndundulu and Mwanihana), further emphasizing the exceptional local biodiversity value. Th e exceptional biodiversity of these areas led to the incorporation of Mwanihana forest into the Udzungwa Mountains National Park in 1991, and later incorporation of Ndundulu forest into the Kilombero Nature Reserve in 2007 (Marshall et al. 2007).
Th e discovery of P. askhambryan-iringae further highlights the need for improved conservation of Uzungwa Scarp Forest Reserve, one of the most important forests in the region for primates and birds (Dinesen et al. 2001), where herpetofauna endemism has been estimated at eight times that of the Eastern Arc as a whole (Menegon, unpublished data). Uzungwa Scarp FR is home to the Kihansi spray toad (Nectophrynoides asperginis), which was extinct in the wild, but was successfully reintroduced in October 2012 following zoo conservation breeding (Channing et al. 2009;Gereau et al. 2014). We hope that our discovery of yet another new endemic will add weight to ongoing proposals for gazettement of Uzungwa Scarp Forest Reserve as a Nature Reserve, the highest designation of protected area possible under the Tanzania Forestry Service.

Acknowledgements
Th anks to COSTECH and TAWIRI for permits. Th e collection expedition to Ndundulu Forest was primarily funded by Flamingo Land Ltd., through the Udzungwa Forest Project. Preliminary surveys of Ndundulu were funded by HMJ Design and Mazuri Foods Ltd., through the British and Irish Association of Zoos and Aquaria Mammal Working Group, and by the Wildlife Conservation Society. Collections from the Uzungwa Scarp Forest Reserve were funded by Danish International Development Agency (DANIDA) through the ENRECA Project at the Department of Botany, University of Dar es Salaam. Th anks to National Museums of Kenya staff especially John Kimeu, for herbarium support. Roy Gereau (Missouri Botanical Garden) is thanked for comments on the manuscript. Nancy Murray (Ohio Wesleyan University) for helpful comments on the manuscript. Phil Roberts (University of York) is thanked for administrating the production of illustrations, and Andrew Brown for producing two of the sketches. We also thank the many fi eld assistants who helped with collections, and with expedition logistics, especially Richard Mgata from Udekwa village, who climbed tall trees in pursuit of vital material for this description. TLPC thanks the Netherlands Organization for Scientifi c Research (NWO), Hugo de Vries Fonds and Air France-KLM for fi nancial help in Tanzania in 2006. Frank Mbago is thanked for assistance while in the fi eld with TLPC. We also thank the United Bank of Carbon for funding to develop a schools' rainforest education program around this species, which led to the chosen species name.