Conservation assessment of Pinus cernua (Pinaceae)

The paper presents results of completed conservation assessment of the strict Laos-Vietnamese endemic, Pinus cernua, based on survey of all previous publications and data obtained from extensive fieldworks during September–October 2016, supported by Mohamed bin Zayed Species Conservation Fund, Komarov Botanical Institute of the Russian Academy of Sciences, Russian Foundation for Fundamental Investigations (RFFI) and the Center for Plant Conservation of the Vietnam Union of Science and Technology Associations. Present review verified 23 locations of the species in Pha Luong Mountains situated on the state boundary of Laos (Houaphan province) and Vietnam (Son La province). Among available localities, 6 were found at first, the species extinction was detected in 1 locality. The area of the species distribution (EOO) decreased during last 3–5 years on 25–30 % from about 20 to 15 km2, with total occupancy area (AOO) becoming less than 3 km2, therefore species conservation status is assessed as globally critically endangered (CR) following to accepted IUCN Red List Categories and Criteria: B1a, b (i-v), B2a, b (i-v). Report also provides basic data on geography, geomorphology and climate of Pha Luong Mountains, as well as detailed descriptions of P. cernua ecology, habitats, vegetation, biology, population structure and taxonomy. All field data and descriptions are based on collected voucher herbaria, which belong to 99 families, 180 genera and 550 species. Among collected plants, 6 species are new for the flora of Laos and Vietnam, 30 species are local threatened endemics needed protection and 12 species are new for science. The main factors of P. cernua extinction are formulated and the recommendations for its effective protection are proposed.


Introduction
Uplifted landmasses in eastern Indochina form a series of more or less high ridges known today as the Truong Son or Annamese Range. These highlands stretch as a southeastern extension of the Himalayas for more than 1000 km from the mountainous areas of Yunnan across the entire peninsular territory to the seashore of southern Cambodia. During the long and complicated geological history, these mountain chains, running in a longitudinal direction, created a corridor for repeated plant movements from subtropical and temperate Asia to tropical highlands of eastern Indochina. Ancient species migrations and species isolation within many mountain systems resulted in active processes of the species formation in this area (Averyanov et al., 2003). Isolation of representatives of a number of temperate Asian or Holarctic genera led to the creation of numerous endemic and sub-endemic taxa within highest mountain systems of eastern Indochina. Diversity and distribution patterns of pine species (Pinus L.) within eastern Indochina is an evident example of such migrations and subsequent isolation within a number of more or less isolated mountain massifs. As a result, eastern Indochina may constitute the region of the world with the highest pine diversity (Hiep, Vidal, 1996;Farjon, 2001;Hiep et al., 2004;Phan Ke Loc et al., 2013;Averyanov et al., 2015a).
At least 12 native Pinus species and varieties were inventoried within this territory during recent explorations, observations and taxonomic studies (Businsky, 2013(Businsky, , 2016Phan Ke Loc et al., 2013;Averyanov et al., 2015a). Additionally, the high-lands of southern Vietnam in limits of Lam Dong, Dac Lac and Khanh Hoa provinces provide a home to Ducampopinus krempfii (Lecomte) A. Chev., a unique relictual endemic of Chu Yang Sin and Bi Dup Mountains. This peculiar primitive pine is possibly allies to ancestral complex of all modern pines (Orlova, Averyanov, 2004). Four well defined allopatric varieties of the endemic Pinus dalatensis Ferré -P. dalatensis var. dalatensis, var. anemophila (Businsky) Aver., var. bidoupensis Businsky and var. procera (Businsky) Aver. inhabit isolated mountain areas within southern and central Vietnam and in Laos. A number of isolated massifs of rocky karstic limestone in northern Vietnam and in adjacent regions of China represent the area of distribution of the subendemic P. henryi Masters subsp. averyanovii Businsky and four calcium-dependent endemic races of P. wangii Hu et W. C. Cheng -P. wangii var. wangii, var. kwangtungensis (Tsiang) Silba, var. varifolia (Nan Li et Y. C. Zhang) Aver. and var. eremitana (Businsky) Aver. Two widespread species, Pinus kesiya Gordon and P. latteri Mason, occasionally form scattered mixed and coniferous forests throughout Indochina. Meanwhile, many mountainous areas of eastern Indochina, particularly regions along the border with Vietnam remain insufficiently explored because they are often inaccessible for botanists. Such areas certainly contain the potential for the discovery of numerous local endemic plants during future scientific explorations including pine species.
Ancient table-shaped sandstone formations occurring sporadically in northern and central Vietnam and Laos represent particular interest for pine geo-graphic investigation. These formations resulted in ancient tectonic breaks of sediment sandstone plates and represent faults, which presently have form of more or less continuous table-shaped formations uplifted to 600-1800 m a. s. l. Commonly such formations in eastern Indochina are oriented in more or less longitudinal direction and have cliffy to almost vertical margin at least from one side (commonly on north faced slope). Summits of such formations are often almost flat. However, in some cases uplifted plateaus are dissected by deep rifts or even eroded into a peneplain with numerous rocky mesas in its peripheral zone. Thin sandy, poor, well-drained soils rich in quartzite are favorable for conifers and provide suitable conditions for pine species, which often form here mixed and true monodominant coniferous zonal primary forests. Earlier floristic studies detected such primary indigenous coniferous forests on sandstone with endemic varieties of Pinus dalatensis in Quang Binh (Minh Hoa district, voucher herbarium specimens -HAL 11783, year 2008, d-EXSICCATES OF VIETNAMESE FLORA 0121/ HAL 11783) and Quang Nam (Dai Loc district, voucher herbarium specimen -CPC 3575, year 2011) provinces in central Vietnam and Laos (Businsky, 2010). However, highest sandstone formation of mentioned type known as Pha Luong Mountains situated on Laos-Vietnamese border between Houaphan and Son La provinces a long time remains insufficiently investigated. Meanwhile, new endemic pine species -Pinus cernua was reported from this area recently as an important co-dominant of indigenous coniferous forests (Averyanov et al., , 2015a. Detailed assessment of this strictly endemic species was undertaken in the present study.

Geographical position and landforms
of Pha Luong Mountains Pha Luong mountain system occupies territory roughly estimated as approximately 40-45 km 2 , which extends on 4-5 km from the S to the N (between N20°40´00″ and N20°42´50″) and on about 10 km from the W to the E (between E104°36´30″ and E104°41´40″E). Administratively Pha Luong Mountains in their main territory belong to Son La province, Moc Chau district, Chieng Son commune (municipality) and Van Ho district, Tan Xuan commune of Vietnam. Southern mountain system slopes in smallest part belong to Houaphan province, Xam Neua district (Lao PDR). Eastern part of Pha Luong Mountains is included presently into main and buffer zones of Xuan Nha nature reserve (Vietnam).
On their geomorphology, Pha Luong Mountains represent uplifted well-developed peneplain with many picturesque exposed rocky peaks, deep rifts with vertical cliffs, rocky outcrops and numerous crowded mesas composed with red-brown highly eroded sandstone. Main summit of mountain massif has appearance of uplifted table-shaped plateau with highest point at SW margin elevated to 1869 m a. s. l. (Fig. 1A, B). Sandstone plateau is dissected by numerous rifts on its margin and composed on periphery with eroded mesas, rocky peaks and impressively exposed cliffs (Fig. 1C, D). Tall open vertical cliffs with many lithophytic plant species are very typical landforms in any part of mountains. Almost all mountain body are composed by solid red-brown highly eroded sandstone with many giant roller boulders, caves and overhanging eroded platforms. Few karstic limestone rocks also occasionally are observed in this area, but lime outcrops here are rather rare.

Climate of Pha Luong Mountains
Climate in the area of Pha Luong Mountains is classified in national climatology as "monsoon tropical climate with cold winter and summer rain season" (Nguyen Khanh Van et al., 2000). Mean annual precipitation is about 1560 mm and mean annual temperature is 18.5 °C, with five cold and dry winter months (from November to March). Detailed climate data recorded in nearest meteorology station in Moc Chau town at elevation 958 m a. s. l. -may be found in monograph of Nguyen Khanh Van et al. (2000, page 71, diagram 55). Basic data on mean month temperatures and precipitation recorded in this monograph are presented in Table 1. Absolute temperature maximum recorded here is +35 °C, and absolute minimum -1.5 °C. Cloudy fogs and mists are very common at high elevations in Pha Luong Mountains that provide almost permanent high humidity favorable for rich epiphytic and lithophytic vegetation observed near mountaintop. This kind of the forest spreads in Pha Luong area at elevations of (500)600-1750(1800) m on slopes of any exposition inclined commonly to 0-40(50)°. The parental soil material in all area is solid redbrown sandstone. The leaf litter usually 0-5 cm thick with projective coverage to 100 %. Soils rather thin and poor, well drained, with brown humuscontaining horizon about (20)30-40(50) cm. Forest structure includes commonly 5 strata with rich non strata vegetation.
The rocky outcrops become dominant in soil cover on very steep cliffy slopes near mountaintops and on summits. In such conditions project coverage of all tree forest strata decrease, but lithophytes become abundant in species diversity and ground coverage.
Mixed forest in Pha Luong Mountains occurs at elevations (800)900-1500(1550) m on slopes of any exposition with inclination commonly 0-70(80)°. In all observed localities, soils of forest habitats are derived from solid red-brown sandstone. Leaf litter here is 0-3 cm thick with projected coverage from 0 to 100 % in small depressions. Soils are thin, poor, well drained, with brown humus-containing horizon (5)10-20(30) cm.
Fifth stratum includes indeterminable mixture of juvenile mosses and lichens (0.1)0.5-3 cm tall with coverage 10-80 (100)  Among plants of specific living forms, woody and semi-woody lianas like Actinidia sp., Dioscorea sp., Smilax sp., and Tetrastigma sp. should be mentioned. All they in primary intact forest are rather uncommon.
Fragments of true mono-or oligodominant coniferous forest in Pha Luong Mountains cover very small highly fragmented, mosaic rocky areas at elevations of (800)900-1500(1550) m. Commonly they cover very steep to almost vertical cliffs with inclination of 70-90° and rocky tops of remnant mesas composed exclusively red-brown sandstone ( Fig. 1G, 2E-I). Leaf litter here may be 0-3 cm thick with projected coverage 0-100 %. Soil is very thin, well drained, with brown humus-containing horizon (5)10-20(30) cm.
Stratum of mosses and lichens (fifth forest stratum) of (0.1)0.5-3 cm tall covers ground on (10)30-80 (100)  Evergreen broad-leaved tropical montane cloud forest covers mountain tops and main summit of Pha Luong Mountains (Fig. 1H). Its fragments also may be seen on steep humid slopes and upper rocky cliffs of any exposition at elevations (1500)1700-1860 m a. s. l. with inclination up to 90°. They grow on very thin, poor, well drained soils having brown, humuscontaining horizon (0)5-10(15) cm derived from solid red-brown sandstone bedrocks. Leaf litter commonly 0-3 cm thick, with projected coverage from 0 to 100 % observed in small local depression. Vertical forest structure is simple and consists of only three strata.
Ericaceous montane scrub covers highest rocky peaks of Pha Luong Mountains. These dense thickets are observed on windy places of summits, on steep slopes and exposed cliffs at elevations (1500)1700-1860 m a. s. l. on any slope exposition at inclination 0-70(90)°. Bedrocks in these habitats are exclusively solid red-brown sandstone. Soils here are very thin, poor, well drained, with brown humus-containing horizon (0)1-3(5) cm thick. Ground surface is covered by leaf litter 0-3 cm thick with projected coverage 0-100 %. Vertical structure is very simple including actually only three strata.
Among climbers and lianas, Dioscorea sp., Smilax sp. and Tetrastigma sp. occasionally found in rather open rocky places and cliffs may be mentioned.
Bamboo montane thickets are azonal plant community, which represents early successive stage of forest regeneration after forest fire. Meanwhile, this plant community remains more or less stable a long time on windy places, particularly on steep cliffy rocky outcrops or mountain tops (Fig. 2B). In Pha Luong Mountains bamboo montane thickets are common at elevation (1500)1700-1860 m on slopes of any exposition with inclination 0-70(90)°. They commonly cover mountain tops composed with red-brown sandstone. Leaf litter here is 0-3 cm thick with projected coverage 0-100 %. Soils are very thin, poor, well drained with brown humuscontaining horizon commonly less than 5 cm thick. Structure of bamboo montane thickets in Pha Luong Mountains is very simple including three strata.
Mosses and lichens form stratum (0.1)0.5-3 cm tall with ground coverage (10) Montane grassy vegetation in Pha Luong Mountains is azonal plant community, which represents first initial successive stage of plant cover regeneration after forest fire. Mossy grasslands are well presented in main almost flat summit of Pha Luong Mountains at elevation 1800-1820 m a. s. l. Here this meadow-like plant community demonstrates certain stability in its structure and specific species composition on open sandstone rocky surface almost lacking of soil deposits. Only two strata may be recognized in this plant community.
Some climbers and lianas are more or less common here in open rocky outcrops and cliffs. Among such plants are species of such genera as Ampelopsis, Crawfurdia, Dioscorea, Smilax, and Tetrastigma.

Non strata vegetation of Pha Luong Mountains
Epiphytic and lithophytic plants form specific extra-strata plant communities, which belong to socalled non strata vegetation. Species composition of non-strata vegetation in Pha Luong Mountains is very rich due to relatively high humidity and numerous rocky outcrops, particularly in upper part of slopes.
Epiphytic plants are common in plant communities of Pha Luong Mountains at any elevations. Epiphytes here belong to many families, but ferns and orchids dominate in all habitats. Epiphytic species and their families are listed below.

History of discovery and taxonomy
of Pinus cernua The history of Pinus cernua discovery was reported in details in earlier publications (Averyanov et al., , 2015aPhan Ke Loc et al., 2014a, b). The species was first recognized by Vietnamese geologists at the end of 2011 within the steep cliffs located in the peripheral zone of Pha Luong Mountains near Laos -Vietnam state boundary between Houaphan and Son La provinces. This discovery was announced in the January issue of the People's Army Newspaper (Luong Tu Chan, 2012) and was also shortly noted in Vietnam Environment Administration Magazine (Le Tran Chan et al., 2012). In middle 2012 the discovery of the new species was confirmed by collected of voucher herbarium specimens Phan Van Thang et al., 2013). These initial assessments and attempts to understand newly discovered pine species resulted in its tentative Conservation assessment of Pinus cernua identification as "Pinus aff. armandii Franchet" Phan Ke Loc et al., 2013). Meanwhile, authors indicated certain morphological differences found in the Vietnamese pine from true P. armandii (Phan Ke Loc et al., 2013). Almost simultaneously, the identification of the discovered plant as P. fenzeliana Hand.-Mazz., was proposed based on speculative studies of plant images entering to the Internet (Businsky, 2013). Further field and laboratory studies confirmed the obvious differences between the discovered plant from both P. armandii and P. fenzeliana, the latter known from isolated locations in southern China. Given the clear distinction of the discovered tree and its morphological differences from all known species of the genus, it was described as a new species under the name Pinus cernua L. K. Phan ex Aver., K.S. Nguyen et T. H. Nguyen in Averyanov et al. (2014, 2015a. Other scientists also accepted the segregation of new taxon, but in subspecies rank. It resulted in description of the same pine under the name Pinus armandii Franchet subsp. xuannhaensis L.K. Phan (Phan Ke Loc et al., 2014a, b). This study based on extensive field investigations of many newly discovered subpopulations revealed fairly uniform morphology and very low genetic variability of new taxon (Nguyen Minh Tam et al., 2015). At the same time, the another study based on observation of single marginal subpopulation of Pinus cernua (mixed with P. latteri) deny any differences of Pha Luong pine from internet-available herbarium specimens of P. fenzeliana originated from mainland SE China and Hainan (Businsky, 2016). New field investigation and species assessment was undertaken throughout all area of Pha Luong Mountains in September -October 2016. It resulted in discovery of 6 new subpopulations of Pinus cernua in addition to already verified 16 earlier known localities. Extinction of one subpopulation due to forest burning is detected in south-west corner of the pine distribution area.
Taxonomical notes. The discovered species probably has some relation to the variable complex of Pinus fenzeliana. However, our plant distinctly differs from representatives of this complex in having narrow, slender needles more than twice as long as the ripe seed cones (Fig. 4-5), ovoid small persistent seed cones clustering regularly in whorls of 2-6, smaller seed scales with deltoid apophysis recurved and thickened at the apex in the form of a transverse, finely-grooved cushion without a distinct mucro and in seeds with a rudimentary, scarious, early-disintegrating wing. These characteristic features have already been emphasized during the initial studies of the first discovered subpopulations Phan Ke Loc et al., 2013) and in later studies (Phan Ke Loc et al., 2014a, b) resulted in description of Pinus armandii subsp. xuannhaensis. Specimens from Hainan selected as a neotype for P. fenzeliana do not agree with the species protologue (Businsky, 2004(Businsky, , 2011. They resemble Vietnamese plants and may be close to our species described here. At the same time according to its original description, P. fenzeliana has a distinct morphologic resemblance with the previously described P. kwangtungensis Chun ex Tsiang, or it may belong to a hybrid of uncertain origin. Some comments and individual opinions on P. cernua taxonomy may be additionally found in some relevant publication (Phan Ke Loc et al., 2014a;Businsky, 2016).
The name of the assessed pine, P. cernua, refers to the long slender weeping needles, which represent bright diagnostic feature easy distinguishing Pha Luong pine from more or less related species.

Distribution, ecology and population structure of Pinus cernua
Pinus cernua in Pha Luong Mountains is an integral element of evergreen mixed and coniferous tropical forests at elevation (800)850-1500(1550) m a. s. l. (Fig. 1G, 2E-I; Averyanov et al., 2016b, Appendix 1-3). It is rather thermopile, warm-growing element in comparison with its more or less com-mon coniferous associates like Amentotaxus argotaenia, A. yunnanensis, Cephalotaxus mannii, Cunninghamia konishii, Dacrycarpus imbricatus, Fokienia hodginsii, and Podocarpus neriifolius, which are occasionally observed at any elevations of Pha Luong mountain system Nguyen Minh Tam et al., 2015). Elevational distribution of Pinus cernua in studied mountains is strongly limited by 1500 (1550) m a. s. l. In most localities, Pinus cernua is observed as a co-dominant or occasional associate in mixed forests with high percentage of broad-leaved trees. True mono-and oligodominant coniferous forests with Pinus cernua are rather rare and confined to a very limited territory. At elevations of 1200-1550 m a. s. l. coniferous forests with Pinus cernua are often mixed with Fokienia hodginsii. On lower elevations, at (800)850-1200 m a. s. l. Pinus cernua forms monodominant coniferous forests, or sometimes sporadically mixed with scattered trees of Pinus latteri (Nguyen Minh Tam et al., 2015;Businsky, 2016). Such species assemblage in its typical form was observed on few narrow highly dissected ridges of northern slopes in peripheral zone of Pha Luong mountains allied to agricultural fields (Businsky, 2016).
According to the present knowledge, Pinus cernua is a local endemic of Pha Luong Mountains occurring on the Laos-Vietnamese state boundary between Houaphan and Son La provinces. Deep erosion of the solid red-brown sandstones forms here unique picturesque landforms with numerous rocky ridges, very steep cliff slopes and rocky outcrops on the tops of remnant mesas (Fig. 1A, C, D, F, and 2 E-G). The species almost exclusively inhabits steep rocky slopes and cliffs composed with sandstone ( Fig. 2E-H) at elevation (800)850-1500(1550) m a. s. l. It was not found anywhere in Vietnam despite special extensive field searches.
Locations of all 22 presently extant and one extinct subpopulations are indicated (by appropriate numbers) on Pinus cernua distribution map (Fig. 3). Localities 1-12 discovered during 2011-2013 listed also in Table 2 were reported in earlier publications Averyanov et al., 2014Averyanov et al., , 2015a.
Locations of 6 extant and 1 extinct subpopulations (numbered respectively as 13-18 and 19) discovered in September -October 2016 are listed in Table 3 and indicated on Fig. 3.
Locations of 4 extant subpopulations (numbered respectively as 20-23) discovered in 2015-2016 by other research groups and individuals (Nguyen Minh Tam et al., 2015;Businsky, 2016) are listed in Table 4 and indicated on Fig. 3.

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Turczaninowia 20 (4): 159-184 (2017)   Actually, all discovered extant and extinct Pinus cernua subpopulations occupy total area less than 15 km 2 that spreads on 7.5 km from W to E (E104°36′50 -E104°41′03) and on 4.5 km from N to the S (N20°40′27″ -N20°42′43″). At the same time, all locations are within 2 km of each other or less. Therefore, they may be reasonably regarded as lone population according to IUCN Red List criteria (IUCN Red List Categories and Criteria, 2001).
Mono-and oligodominant stands of Pinus cernua with more than 50-100 trees within locality are observed only in north-eastern part of distribution area (locations 1-8, 20, 21). Very few saplings and young immature trees (less than 1 %) were observed in these subpopulations. Only 1 to 25 mature trees commonly scattered in broad-leaved forests were recorded in all other locations (9-18, 22, 23). One recently extinct subpopulation (19) was detected in south-western corner of the distribution area (Fig. 3). Seedlings were not found in all observed locations. Burned, human-cut and naturally felled trunks have been seen in some locations.
Newly found locations of Pinus cernua (numbered on figure 3 as 13-18) discovered during fieldwork in September -October 2016 expand known distribution area essentially (Fig. 3).
Discovered location 17 outlines south-eastern corner of Pinus cernua distribution at point N20°40′58.4′′, E104°41′02.8′′ (Fig. 2F-H). This subpopulation includes 20 mature trees 10-15 m tall growing on rocky outcrops at elevation 1500-1550 m a. s. l. (Table 3). This is highest elevation of known Pinus cernua habitats. Trees here inhabit upper parts of humid cliffy slopes of narrow ravines and canyons, as well as tops of remnant eroded mountaintops and mesas. Fokienia hodginsii is another common conifer at this location. No seedlings and saplings were observed here. Squirrels damaged many ripening cones in some trees in this location.
Newly found location 18 defines southern border of Pinus cernua distribution. It situated in point N20°40′46.2′′, E104°39′49.6′′ at elevation 1500 m a. s. l. (Fig. 3). Only 3 old trees 15-20 m tall and 70-80 cm DBH, as well as few naturally fallen trunks were located in this subpopulation. Surviving Pinus cernua trees were observed here mostly on tops of remnant hills in association with Fokienia hodginsii. No young trees or seedlings were found in this locality.
The location of extinct subpopulation destroyed by forest fire 3-5 years ago was detected on the base of timber remnant and information obtained from local people. This locality is situated on Laos -Vietnam state border at elevation about 1500 m around point N20°40′27′′, E104°36′50′′ (Fig. 3). Wide forest burning around this locality, as well as on all southern slopes of Pha Luong main summit (Fig. 1B) leaded to probably full extinction of Pinus cernua on Laos territory. The extinction of Pinus cernua due to extensive uncontrolled forest fires decreased its distribution area on at least 25 % during last 5-15 years.
Pinus cernua forms primary humid coniferous and mixed forests on steep slopes, cliffs and rocky outcrops of remnant, highly-eroded solid red-brown sandstone at elevations (800)8500-1500(1550) m a. s. l. Often it was observed also as a scattered tree in closed evergreen, broad-leaved forests. Its occasional gymnosperm associates are Amentotaxus argotaenia, A. yunnanensis, Cephalotaxus mannii, Cunninghamia konishii, Dacrycarpus imbricatus, Fokienia hodginsii and Podocarpus neriifolius. Habitat character, plant community structure and common associates are described above under characteristics of evergreen mixed tropical submontane forest (Averyanov et al., 2016b, Appendix 1, 2) and evergreen coniferous tropical submontane forest (Averyanov et al., 2016b, Appendix 1, 3) listed in commonly accepted classification as II.A.2a formation -Evergreen needle-leaves woodland composed of trees at least 15 m tall with crown coverage more than 40 % (International classification …, 1973).
The seed cones in most subpopulations develop high percentage of mutilated abnormal or abortive seeds ( Fig. 4-6), or no seed at all. At the same time, squirrels and other rodents eat almost all normally developed seeds in ripening cones. This is serious factor preventing successful natural seed germination. Seed fertility of P. cernua varies between 50-60 % according to observations on germination of seeds collected during autumn of 2013 and 2016 (Averyanov et al., 2015a). It was observed that most seedlings in nature die soon after germination (Phan Ke Loc et al., 2013). Meanwhile, seedlings demonstrate good growth and development under cultivation ex situ at least during first and second year age (Averyanov et al., 2015a).
Very few saplings are found on open rocky slopes and cliff shelves only in several locations in south-east corner of Pinus cernua distribution area. In shady forests on mountain summits regeneration is very poor or absent. Data are available regarding the successful cultivation by seeds and cuttings Phan Van Thang et al., 2013;Averyanov et al., 2015a). In natural habitats trees grow rather slow. Winter buds form new leaves in March-April. Male strobili spread pollen for pollination in February -early April. Seeds ripening in 20-22 months later, in October-December (Phan Ke Loc et al., 2014a, b). Annual growth of individual trees of P. cernua in observed populations is very variable and depends on habitat conditions. Timber of plants found on relatively dry open rocky summits exhibits annual rings (0.3)0.5-1(1.5) mm wide, which indirectly estimates the age of the oldest observed trees between 150-200 years.
The review of all earlier data and results of present field studies confirm current global status of Pinus cernua as a critically endangered species according to The IUCN Red List Categories and Criteria, version 3.1 (IUCN 2001).

A. Population reduction
Actual present day data: reduction of species distribution area on 25-30 % during last 3-5 years approximately from 20 to 15 km 2 (Fig. 3) and on at about ≥ 30 % during 5-15 past years.
Present actual species conditions match with following criteria: A2. Population reduction observed, estimated, inferred, or suspected in the past where the causes of reduction may not have ceased OR may not be understood OR may not be reversible: -≥ 30 % (a) direct observation (c) a decline in area of occupancy (AOO), extent of occurrence (EOO) and/or habitat quality (d) actual or potential levels of exploitation A3. Population reduction projected or suspected to be met in the future (up to a maximum of 100 years): -≥ 30 % (c) a decline in area of occupancy (AOO), extent of occurrence (EOO) and/or habitat quality Conservation assessment of Pinus cernua (d) actual or potential levels of exploitation A4. An observed, estimated, inferred, projected or suspected population reduction (up to a maximum of 100 years) where the time period must include both the past and the future, and where the causes of reduction may not have ceased OR may not be understood OR may not be reversible: -≥ 30 % (c) a decline in area of occupancy (AOO), extent of occurrence (EOO) and/or habitat quality (d) actual or potential levels of exploitation Status according to formal criteria A: A2a, c, d; A3c, d; A4c, d = VU B. Geographic range Actual present day data: present species distribution area (extent of occurrence -EOO) is less than 15 km 2 (Fig. 3); present species occupancy area (AOO) is less than 3 km 2 ; 22 localities are currently known but these are within 2-3 km of each other and may be regarded as a single known population with close species locations.
Present actual species conditions match with following criteria: B1. Extent of occurrence (EOO): -< 100 km² (a) Severely fragmented, (b) Continuing decline in any of: (i) extent of occurrence; (ii) area of occupancy; (iii) area, extent and/or quality of habitat; (iv) number of locations or subpopulations; (v) number of mature individuals.
B2. Area of occupancy (AOO): -< 10 km² (a) Severely fragmented, (b) Continuing decline in any of: (i) extent of occurrence; (ii) area of occupancy; (iii) area, extent and/or quality of habitat; (iv) number of locations or subpopulations; (v) number of mature individuals.
Status according to formal criteria B: B1a, b (iv); B2a, b (i-v) = CR C. Small population size and decline Actual present day data: number of mature individuals more than 250, but less than 2500, affected undoubtedly by decreasing on 20 % during 2 generations; 1 population is known, consisting of about 95 % mature individuals.
Present actual species conditions match with following criteria: Number of mature individuals -< 2,500 C1. An estimated continuing decline of at least -

% in 2 generations
C2. An observed, estimated, projected or inferred continuing decline AND at least 1 of the following 3 conditions: a i -number of mature individuals in each subpopulation ≤ 250; a ii -% of mature individuals in one subpopulation = 95-100 % Status according to formal criteria C: C1; C2a (i, ii) = EN D. Very small or restricted population Actual present day data: AOO less than 3 km 2 . Present actual species conditions match with following criteria: D2. Restricted area of occupancy or number of locations with a plausible future threat that could drive the taxon to CR or EX in a very short time, -AOO < 20 km² Status according to formal criteria D: D2 = VU E. Quantitative Analysis Actual present day data: AOO less than 3 km 2 . Present actual species conditions match with following criteria: Indicating the probability of extinction in the wild to be: -≥ 20 % in 20 years or 5 generations (100 years max.) Status according to formal criteria EC: E = EN The status of Pinus cernua based on assessment summarized data according to various formal IUCN Red List criteria (A-E) are follow: A2a, c, d; A3c, d; A4c, d -VU B1a, b (i-v); B2a, b (i-v) -CR C1; C2a (i, ii) -EN D2 -VU E -EN Following to the highest rank of the accepted status category of Pinus cernua should be respectively assessed as globally critically endangered species B1a, b (i-v) and B2a, b (i-v) according to IUCN Red List criteria and categories (IUCN Red List Categories and Criteria, 2001).
The habitat loss caused by occasional uncontrolled forest fires connected with primitive agriculture is the main fatal factor of Pinus cernua extinction. Additional, but also important damage factors are deforestation caused by forest logging, selected felling for fragrant soft pine timber, overexploitation by local people and forestry enterprises, clearing forest for agriculture fields, as well as miserable area of actual occupancy, seed mutilation and very poor regeneration. Anthropogenic pressure over many years has resulted in a great fragmentation of surviving coniferous forests with Pinus cernua and lead to their deep degradation in most of habitats. Presently Pinus cernua often survives only in small patches of secondary forests surrounded by agricultural fields. Some discovered subpopulations Conservation assessment of Pinus cernua are situated outside Xuan Nha nature reserve on lands having no any protected status.
Protection and monitoring of all known subpopulations of Pinus cernua located within and outside the Xuan Nha nature reserve may be critically important action for the species effective conservation. The including of newly discovered locations into proper Xuan Nha nature reserve territory or into its buffer zone may well be a step on this way. The studies of seed biology and germination, as well as artificial seed propagation, plantation and reforestation may seriously support species conservation. The attempts of the initiation of a community based conservation programme that involves seed collecting, cultivation and reintroduction for the reinforcement of existing stands may be very fruitful initiative Nguyen Duc To Luu, 2014;Averyanov et al., 2015a). Mature samples of Pinus cernua form nodding shoots with long slender weeping needles. The species is therefore highly desirable for cultivation as ornamental tree, particularly in rock gardens of the Asian style. Exsitu propagation and introduction into cultivation of this species as an ornamental plant may be additional effective measures to its conservation. More surveys on mountainous boundary areas in Vietnam and particularly in the Lao PDR should be undertaken as soon as possible for searches of more possibly surviving populations.

Plant diversity and flora of Pha Luong Mountains
Flora of Pha Luong Mountains belongs to typical tropical floras of North Indochinese floristic province of Indochinese floristic region belonging to Indomalesian subkingdom of Holarctic (Averyanov et al., 2003). It contains many representatives of true tropical families such as Acanthaceae, Anacardiaceae, Annonaceae, Apocynaceae, Balanophoraceae, Begoniaceae, Burmanniaceae, Gesneriaceae, Melastomataceae, Meliaceae, Rubiaceae, Sapindaceae, Sapotaceae, Simaroubaceae and Zingiberaceae. The largest family here like in all other tropical floras is orchids -Orchidaceae. Meanwhile, subtropical Holarctic plant representatives participate and even dominate in plant communities at elevation higher than 1200-1500 m. These are representatives of families like Aceraceae, Betulaceae, Cornaceae, Cupressaceae, Cyperaceae, Ericaceae, Fagaceae, Hamamelidaceae, Magnoliaceae, Pinaceae, Polygonaceae, Primulaceae, Ranunculaceae, Rosaceae and Taxaceae, as well as subtropical ferns and ferns of moderate climate (Adiantum, Asplenium, Diplazium, Polystichum, Thelypteris etc.). The combination of different geographic elements makes diversity and richness of the flora of Pha Luong Mountains particularly high and diverse.
At least 1131 plant species belonging to 650 genera and 189 families were reported recently in Xuan Nha nature reserve including western part of Pha Luong Mountains (Tran Huy Thai, 2012). Among them there are 33 rare threatened species recorded in the Red Data Book of Vietnam, 356 woody species, 400 medicinal and 90 essential oil plants, as well as 180 other species used in national economy including oleiferous, tannin-bearing, fibre, edible and ornamental plants.
During fieldwork for conservation assessment of Pinus cernua, about 550 species of vascular plants belonging to 180 genera and 99 families were additionally collected which are listed in Appendix 2 of technical project report for Mohamed bin Zayed Species conservation fund (Averyanov et al., 2016b). For all these species, voucher herbarium specimens as a scientific base for habitat and plant communities descriptions (Averyanov et al.,  At least 30 species detected here and confirmed by voucher herbaria are threatened local endemics desirable for special protection on the national level. They are: