Alpine Botany
https://doi.org/10.1007/s00035-018-0208-3
SHORT COMMUNICATION
The highest vascular plants on Earth
Cédric Dentant1
Received: 12 January 2018 / Accepted: 12 July 2018
© Swiss Botanical Society 2018
Abstract
Mountaineering, since the beginning of its history, has played an inconspicuous but key role in the collection of species
samples at the highest elevations. During two historical expeditions undertaken to reach the summit of Mount Everest in 1935
and 1952, mountaineers collected five species of vascular plants from both the north and south sides of the mountain, at ca.
6400 m a.s.l. Only one of these specimens was determined immediately following the expedition (Saussurea gnaphalodes),
and the remaining four were not identified until quite recently. In 2000, the second specimen from the 1935 expedition was
described as a new species for science (Lepidostemon everestianus), endemic to Tibet. In this paper, the remaining three
specimens from the 1952 Everest expedition are reviewed and analysed, bringing the number of species sharing the title of
“highest known vascular plant” from two to five. I identify one of the 1952 specimens as Arenaria bryophylla, and describe
two novel taxa based on analysis of the herbarium records: Saxifraga lychnitis var. everestianus and Androsace khumbuensis. Although elevation records on their own do not inform us about the ecological conditions and physiological capacity of
plants at the upper limit of their distribution, this taxonomic investigation contributes to our knowledge of the biogeography
of Himalayan flora and opens the way for future field-based investigations of mechanisms limiting plant growth on the roof
of the world.
Keywords Vascular plants · Lepidostemon everestianus · Androsace khumbuensis · Mountaineering · High elevation ·
Everest · Himalaya
Introduction
Mountaineers have a long tradition of contributing to
biological knowledge at the upper limits of life. In 1787,
during his ascent of Mont Blanc, De Saussure (1796)
noted the presence of Silene acaulis subsp. bryoides at
an altitude of ca. 3600 m a.s.l., which is probably the
first scientific record of a high-mountain plant. In 1802,
Humboldt and Bonpland made famous and complete
records of plant species they encountered while climbing Mount Chimborazo (Andes, Ecuador). Despite failing
to reach the summit (6263 m a.s.l.), they climbed up to
ca. 5880 m a.s.l. (record for scientists at the time) and
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s00035-018-0208-3) contains
supplementary material, which is available to authorized users.
* Cédric Dentant
[email protected]
1
Ecrins National Park, Domaine de Charance, 05000 Gap,
France
noted the upper limit of vascular plants at 4600 m a.s.l.
(von Humboldt and Bonpland 1805). In 1835, during the
first ascent of Piz Linard in the eastern Swiss Alps, Heer
precisely noted every species he encountered along an
elevation gradient. These botanical pioneers established
the first links between mountaineering and alpine botany,
and paved the way for future scientific monitoring at high
elevations (Wipf et al. 2013; Morueta-Holme et al. 2015).
During the so-called “Golden Age” of mountaineering in
the European Alps (1860–1865), interest in these highest
climbing species had increased through years, questioning what renders life possible at such elevations. Between
1861 and 1864, Whymper (1871) recorded several species
occurrences during his attempts to reach the summit of
the Matterhorn by the south ridge, and noted his fascination with what he called “atoms of life in a world of
desolation”. Ball (1860), botanist and first president of the
Alpine Club of London, published guidelines encouraging
mountaineers to participate to Natural History knowledge
in recording plants encountered during their tours in upper
altitudes. Carret (1880) after examining plants sampled
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Alpine Botany
during the third ascent of La Meije—one of the last major
summits in the Alps to be climbed—declared mountaineering as a new means of extending the study of Natural
History to mountain environments, and placed particular
emphasis on botany.
For botanists, mountaineering, therefore, became a necessary means of collecting high-elevation biological data for
scientific purposes. A striking example of this approach is
the first British Reconnaissance Expedition to Mount Everest (1921), during which Wollaston collected what turned
out to be at the time the highest vascular plant ever encountered: Arenaria bryophylla, sampled between 6100 and
6200 m a.s.l. (Miehe 1991). During the same expedition, he
also found a primrose new to science: Primula wollastonii.
In 1963, members of the American Mount Everest Expedition sampled granular soil near the summit, at 8400 m (Swan
1992). Researchers found several bacteria within the sample,
including a new taxa: Geodermatophilus obscurus subsp.
everesti. This discovery prompted scientists to consider the
possibility of life on Mars for the first time. The altitude
record for visible organisms is 7400 m, on the south face of
Makalu, where Aleš Kunaver [cited “T. Kunavar” in Miehe
(1991) or “Kunvar” in Miehe (1988) and Körner (2003)],
leader of the fourth Yugoslavian Makalu Climbing Expedition, collected two lichens in 1972: Lecidea vorticosa and
Lecanora polytropa—the latter species also contained the
lichenicole fungus Cercidospora epipolytropa (Miehe 1991).
Collectively, these examples illustrate the potential of mountaineering to contribute to our understanding of the upper
limits of life in mountain environments.
Fig. 1 Satellite images of the
Mount Everest region with
locations of both expeditions
samples. Image: ©2018 DigitalGlobe, CNES/Airbus. Map
data: ©2018 Google
13
As the highest mountain on Earth and with rock surfaces
present all the way to its summit, Mount Everest (8848 m
a.s.l.) provides exceptional potential for establishing elevation records for the occurrence of organisms. Two historical
Himalayan expeditions were especially significant for the
collection of botanical data, in addition to their climbing
achievements: the 1935 British expedition, led by Eric E
Shipton, and the 1952 Swiss expedition, led by Edouard
Wyss-Dunant. The first expedition took place in Tibet, and
accessed the base of Mount Everest by way of the East Rongbuk Glacier. Shipton and his colleagues were able to collect
two vascular plant specimens at ca. 6400 m a.s.l., before
being forced to turn around below 7100 m a.s.l. due to a
snow storm. The Swiss expedition was the second European
expedition to Nepal, accessing Mount Everest from the south
along the Khumbu Glacier. During the attempt, scientific
members of the expedition collected three vascular plant
specimens at ca. 6350 m a.s.l. (Fig. 1). The party reached the
remarkable altitude of 8600 m a.s.l., and paved the way for
the successful British expedition the following year, when
Tenzing Norgay and Edmund Hillary reached the summit.
Although the members of the 1935 and 1952 expeditions
were unable to identify the species they encountered, they
collected samples which they brought back to scientific institutions in Europe. One of the samples collected in 1935, at
6400 m a.s.l., was later identified as Saussurea gnaphalodes (Royle ex DC.) Sch.Bip.; it is often cited as the highest vascular plant on Earth (Miehe 1991; Bajracharya 1996;
Körner 2003). The other sample from 1935 was described
as a new species, Lepidostemon everestianus Al-Shehbaz,
Alpine Botany
in the recent past (Al-Shehbaz 2000). In contrast, the samples from 1952 were never studied nor identified. To my
knowledge, mountaineers on Mount Everest have made no
further records of vascular plant life at equivalent or higher
elevations since the 1935 and 1952 expeditions.
Herbarium records, such as the samples collected during
the 1935 and 1952 Everest expeditions, are an under-utilized
source of information about plant occurrences in extreme
and remote mountain locations. Even years or decades after
initial collection, specimens can (1) provide insight into the
upper limits of plant distribution and (2) provide the basis
for the description of novel taxa. The aim of this paper is to
formally describe these highest climbing plants ever collected, and in so doing contribute to our knowledge of the
upper limits of vascular plant life.
Sampling sites
The British and Swiss expeditions collected a total of five
species around 6400 m a.s.l. Saussurea gnaphalodes (Royle
ex DC.) Sch.Bip. is a fairly widespread plant throughout
Nepal, Tibet, Pamir and the Hindu Kush, growing usually
between 5000 and 6000 m. These characteristics explain
why this species was the only one of the five identified soon
after the expedition. The original specimen was collected
by Shipton in 1935 in the “big scree” bordering the north
side of the East Rongbuk Glacier, at Camp III, close to the
base of the North Col. Shipton (1936) did not mention any
botanical sample in his expedition report, but the label of
the herbarium specimen, conserved in the British Museum
Herbarium (BM), is explicit and unambiguous.
However, Shipton did not only sample one species at
6400 m a.s.l., but two. The second one, totally unknown
in 1935, was archived in the BM without any name until
2000. Working on the Flora of China project (efloras.org
2008), the worldwide specialist of the Brassicaceae family,
Ihsan Al-Shehbaz, came across the sample and described it
as a new species: Lepidostemon everestianus (Al-Shehbaz
2000; Fig. 2). Despite the striking elevation, no connection
was then made at the time with the other sample collected
by Shipton, Saussurea gnaphalodes, which belonged to a
family outside the scope of his study. The discovery of Lepidostemon everestianus, a Tibetan endemic, made the genus
Lepidostemon no longer monotypic. The specimen collected
by Shipton remains the only one ever encountered for this
species.
In 1952, on the south (Nepalese) side of Everest, the botanist of the scientific Swiss expedition, Albert Zimmermann,
sampled three species on a section of moraine and cliff bordering the north side of the Khumbu Glacier (Zimmermann
1952). The recorded altitudes were 6335 m a.s.l. for the first
species, and 6350 m a.s.l. for the two others, respectively.
Fig. 2 Illustration of Lepidostemon everestianus based on the herbarium specimen (BM[000587908]) and Al-Shehbaz’ description. Drawing: C. Dentant
Zimmermann described the location in which he found the
specimens as “between Camp IV and Camp V”. However,
Camp IV was settled at 6450 m a.s.l. and Camp V at 6900 m
a.s.l. (Roch 1952)! Zimmermann maintained this location in
his report of the expedition, however, as well as on the herbarium labels. The Zimmermann’s cited location is an obvious discrepancy: Camp IV was in the middle of the Western
Cwm (upper part of the Khumbu Glacier) and Camp V in the
slope below the South Col. There is neither rock nor moraine
between them. The correct location is between Camp III and
Camp IV. Considering this discrepancy and the precision of
the tools that were available to assess altitudes in 1935 and
1952, these three altitude values (6400, 6335 and 6350 m)
can be considered as equivalent.
Taxonomic analysis
Here, I present an account of the five samples collected
from the Mount Everest in 1935 and 1952. The specimens
collected in 1935 have already been correctly identified or
described elsewhere and are included for comprehensiveness. The three samples from 1952 were studied in May
and June 2017 in G (Conservatoire et Jardin botaniques de
la Ville de Genève), where they have been stored since collection, using standard methods of herbarium taxonomy. In
addition, I relied on the Himalayan herbarium collection at
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Alpine Botany
G, digitized specimens at BM, E (Flora of Nepal project),
A and MO (Flora of China project), floristic literature and
reports based on data collected during the Swiss expedition (Zimmermann 1952; Weibel 1956; Baehni 1958).
Zimmermann’s unpublished field notebook was also
consulted. Herein, he proposed names for the collected
specimens: “Arenaria !”, “Androsace microphylla !” and
“Sedum or Saxifraga”. In the expedition report (Zimmermann 1952), he corrected his first hesitation, stating that
the third specimen appeared to be without a doubt a tiny
Saxifraga.
1. Saussurea gnaphalodes (Royle ex DC.) Sch.Bip.—Tibet
(China), East Rongbuk Glacier, big scree, 21,000 ft. (ca.
6400 m)—07/26/1935—coll.: Eric E Shipton; determin.:
s.n. BM[000803807]! (herbarium specimen in Online
Resource 1).
A complete description of the taxon can be found in Shi
and von Raab-Straube (2008).
2. Lepidostemon everestianus Al-Shehbaz—Tibet
(China), East Rongbuk Glacier, big scree, 21,000 ft.
(ca. 6400 m)—07/26/1935—coll.: Eric E Shipton;
determin.: Ihsan A Al-Shehbaz (1999). HOLOTYPE:
BM[000587908]! (herbarium specimen in Online
Resource 2).
A complete description of the taxon can be found in
Al-Shehbaz (2000).
3. Arenaria bryophylla Fernald—Nepal, Mount Everest,
Khumbu Glacier, moraine, 6335 m, between Camp IV
and Camp V—05/25/1952—coll.: Albert Zimmermann
(accompanied by E Hofstetter and Aïla sherpa); determin.: Cedric Dentant (2017). G[G00429530]! (herbarium specimen in Online Resource 3).
A complete description of the taxon can be found in
Zhengyi and Wagner (2008).
This taxon was considered for years as the highest
occurring plant in the world (Polunin and Stainton 1997),
before Miehe (1991) corrected it with Shipton’s sample
of Saussurea gnaphalodes. This plant forms dense cushions, with woody caudex. Leaves are linear, crowded and
reflexed, forming columns. Leaf margins are involute and
membranous. Above 5000 m a.s.l., two other species of
Arenaria may be encountered: A. edgeworthiana and A.
pulvinata. With no flower on the sample, the single reliable feature to distinguish A. bryophylla is the leaf margin: glabrous or sparsely ciliate for this species; hairy or
distinctly ciliate for others.
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4. Saxifraga lychnitis Hook.f. & Thomson var. everestianus Dentant, var. nov. (Fig. 3; herbarium specimen
in Online Resource 4)—HOLOTYPE designed here:
Nepal, Mount Everest, crevices on south-facing cliffs,
6350 m, between Camp IV and Camp V—05/25/1952—
coll.: Albert Zimmermann (accompanied by E Hofstetter and Aïla sherpa); determin.: Cedric Dentant (2017).
G[G0042528]!
Herbs perennial. Roots mainly primary, with scarce secondary ones. Axillary stems (or stolons?), 1–3 per rosette,
short, thick and sparsely leafy. Leaves 2–3.5 mm long, elliptical, forming lax rosettes, 2.5–4 mm in diameter. Both leaf
surfaces flat, glabrous, eglandular or brownish glandular.
Margins uneven, mostly with scarce brownish glandular hair,
sometimes only with irregular eglandular teeth. Apex fleshy,
sometimes mucronate. Stem leaves longer than rosette’s
ones, with a conspicuous central rib (absent for rosette
leaves). Flowers and fruits unknown.
In Nepal, Saxifraga contains 87 species, including 21
endemics. S. lychnitis belongs to section Ciliatae (because
of its entire leaves without chalk glands), which contains
65 species in Nepal (Akiyama et al. 2012). It also includes
Saxifraga zimmermannii, which was described in 1958 from
Zimmermann’s samples collected at other, lower localities
during the 1952 expedition (Baehni 1958).
Saxifraga lychnitis can be distinguished from closely
related species S. stella-aurea, S. llonakhensis, S. harae, and
S. viscidula, due to its elliptical, mostly brown-glandular
leaves, that have no well-defined petiole nor a crisped villous
margin, and that are not placed in rows. Var. everestianus
differs from var. lychnitis and var. oresbia in the following
characters: the presence of short, leafy axillary stems, and
smaller leaves and rosettes.
Although variation in leaf size alone would not argue for
a varietal status, the combination of its leaves, growth form
with axillary stems (which could be interpreted as stolons)
and extreme elevation demonstrates that this collection represents a separate taxon. Indeed, the axillary stems, which
are buried in the soil and absent from the other two varieties,
may represent an adaptation to the plant’s extreme habitat.
They anchor the plant in the unstable substrate and may protect the base of the stem from freezing (Dvorský et al. 2016).
The species is named after Mount Everest, the only
mountain where the variety is known to occur.
5. Androsace khumbuensis Dentant, sp. nov. (Fig. 4; herbarium specimen in Online Resource 5)—HOLOTYPE
designed here: Nepal, Mount Everest, crevices in southfacing cliffs, 6350 m, between Camp IV and Camp
V—05/25/1952—coll.: Albert Zimmermann (accompanied by E Hofstetter and Aïla sherpa); determin.: Cedric
Dentant (2017). G[G00429529]!
Alpine Botany
Fig. 3 Saxifraga lychnitis var.
everestianus. a Leaves (lf) forming rosette, with several stems
(ste) and a short and thick axillary stem (a ste); b individual
with loose rosette; c leaf with
glandular hair (gh) on the margin and brown glands (bg) on
surfaces; example of glabrous
leaf, with short whitish teeth (t).
Drawings: C. Dentant
Herbs perennial, forming a more or less dense cushion.
Roots mainly primary, with scarce secondary ones. Leaves
gathered in numerous rosettes less than 3 mm in diameter;
leaves 1–2.5 mm long, rather homomorphic despite external
ones much more curved than inner ones. Abaxial and adaxial
leaf surfaces glabrous; margins with scarce and irregular
whitish teeth, 0.1–0.4 mm long, more numerous on apex of
external leaves. Inner leaves with cartilaginous margins and
a conspicuous central rib. Corolla white.
In Nepal, Androsace contains 21 referenced taxa, including
4 infra-taxa (Shrestha and Press 2008). Miehe (1987) cited
seven Androsace species from the Everest region of Nepal.
The specimen has been compared with all of them with respect
to morphology (based on herbarium specimens) and ecological conditions, as well as to all 73 Androsace species from
China (Hu and Kelso 2008) and A. mucronifolia, the only species known from Pakistan. Although the specimen is rather
poorly preserved, it is clearly distinct from all described species. The specimen lacks reproductive features except for a
single corolla; peduncles, sepals, stamens, ovary, fruits and
seeds are unknown. Nevertheless, the delineation of A. khumbuensis from closely related species is clear due to its tiny,
glabrous, homomorphic, white-teethed leaves. Specifically,
in contrast to A. khumbuensis, (1) A. globifera has pointed
leaves with a hairy apex (long white hair); (2) A. muscoides
has flat leaves, fairly pointed, with a hairy apex (long white
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Alpine Botany
Fig. 4 Androsace khumbuensis.
a Rosette; b external leaf with
whitish teeth (t); c internal
leaf, also with whitish teeth (t).
Drawings: C. Dentant
hair); (3) A. delavayi has hairy abaxial surface of leaves; apex
hold thin, long (0.6–0.9 mm) and dense translucent trichomes;
leaf length 2–4 mm; (4) A. tapete has hairy leaves, gathered in
columns; (5) A. lehmanii has dimorphic leaves, with pink dried
corolla (white when fresh); (6) A. mucronifolia (= A. microphylla) is much bigger in all its features, including stolons
that are much longer and thicker, and it has leaf margins that
are densely setose–ciliate. [This species is cited by Zimmermann (1952) with a question mark; no specimens from Nepal
have been encountered.] More specimens would be required to
enable a better understanding of this remarkable taxon.
The species is named after the Khumbu Glacier, where the
species is described from. It is dedicated to all of the members
of the 1952 Swiss expedition for their remarkable blend of
mountaineering and science.
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Discussion
High‑elevation vascular plants
The five highest vascular species of the world belong to
five different families: Asteraceae, Brassicaceae, Caryophyllaceae, Saxifragaceae and Primulaceae. 40% of the
encountered taxa are new for science. In other recent studies carried out in the Himalayan region (Dvorský et al.
2015; Angel et al. 2016), botanists found a similar proportion of new species, recording a total of eight different
species belonging to three families at 6150 m a.s.l.: Brassicaceae (Draba alshehbazii, Draba altaica, Ladakiella
klimesii); Asteraceae (Saussurea glacialis, Saussurea
Alpine Botany
gnaphalodes, Saussurea inversa, Waldheimia tridactylites)
and Poaceae (Poa attenuata). Three out of these eight
species were also new discoveries for science and only
described very recently, after 2002 (Klimeš and German
2009; German and Al-Shehbaz 2010; von Raab-Straube
2011). Even if records of altitude tell little about life conditions, it is striking to see how little is known about this
specific diversity. Two other records known from literature can be mentioned to complete this list of vascular
plant occurrences above 6100 m a.s.l. (Table 1): Desideria
himalayensis (= Ermania himalayensis; Brassicaceae) at
6300 m a.s.l. on Kamet, and Stellaria decumbens (Caryophyllaceae), observed by Swan at 6130 m a.s.l. on Makalu
(Miehe 1991). It is notable that among these 14 different species encountered above 6100 m a.s.l., most were
found to grow in multiple-species patches: Saussurea gnaphalodes and Lepidostemon everestianus (6400 m a.s.l.);
Androsace khumbuensis and Saxifraga lychnitis var. everestianus (6350 m a.s.l.); Draba alshehbazii, Draba altaica,
Ladakiella klimesii, Saussurea gnaphalodes, Waldheimia
tridactylites and Poa attenuata (6150 m a.s.l.). These
results seem to point out favourable sites for colonization of vascular plants in highest elevations rather than
accidental occurrences (Angel et al. 2016). Both Everest
sites are worth to be investigated anew to (1) check and
to compare the species occurrences; (2) gather biological
information on encountered species and (3) investigate the
local environmental conditions.
Habitat conditions of highest plant occurrences
Information on the habitats where plant species were
collected in 1935 and 1952 is limited to succinct habitat descriptions. Despite the lack of quantitative data on
Table 1 Complete list of vascular plants ever recorded to date (above 6100 m a.s.l.)
Speciesa
Familyb
Mountain
Highest
recorded elevation (m)
Reference
Year of first
descriptionc
Androsace khumbuensis
Dentant
Arenaria bryophylla Fernald
Primulaceae
6350
this study
2018
this study
1919
Miehe (1991)
1844
Angel et al. (2016)
2008
Dvorský et al. (2015), Angel
et al. (2016)
Dvorský et al. (2015), Angel
et al. (2016)
1841
Caryophyllaceae 6335
Brassicaceae
6300
Brassicaceae
6150
Brassicaceae
6150
Brassicaceae
6150
Brassicaceae
6400
Poaceae
6150
Saussurea glacialis Herder
Asteraceae
6150
Saussurea gnaphalodes
(Royle ex Royle) Sch.Bip.
Saussurea inversa RaabStraube
Saxifraga lychnitis var. everestianus Dentant
Stellaria decumbens Edgew.
Asteraceae
6400
Asteraceae
6150
Saxifragaceae
6350
Desideria himalayensis
(Cambess.) Al-Shehbaz
Draba alshehbazii Klimeš &
D.A.German
Draba altaica (C.A.Mey.)
Bunge
Ladakiella klimesii (AlShehbaz) D.A. German &
Al-Shehbaz
Lepidostemon everestianus
Al-Shehbaz
Poa attenuata Trin.
Waldheimia tridactylites Kar.
& Kir.
a
Caryophyllaceae 6130
Asteraceae
6150
Mount Everest (Nepal, Eastern Himalayas)
Mount Everest (Nepal, Eastern Himalayas)
Kamet (Garhwal, Western
Himalayas)
Mount Shukule II (Ladakh,
Western Himalayas)
Shukule Peaks (Ladakh,
Western Himalayas)
Shukule Peaks (Ladakh,
Western Himalayas)
Mount Everest (Nepal, Eastern Himalayas)
Mount Shukule II (Ladakh,
Western Himalayas)
Shukule Peaks (Ladakh,
Western Himalayas)
Mount Everest (Nepal, Eastern Himalayas)
Shukule Peaks (Ladakh,
Western Himalayas)
Mount Everest (Nepal, Eastern Himalayas)
Makalu (Nepal, Eastern
Himalayas)
Shukule Peaks (Ladakh,
Western Himalayas)
2002
Al-Shehbaz (2000)
2000
Angel et al. (2016)
1835
Dvorský et al. (2015)
1867
Miehe (1991)
1846
Dvorský et al. (2015)
2011
this study
2018
Miehe (1991)
1846
Dvorský et al. (2015), Angel
et al. (2016)
1842
Species names based on The Plant List (theplantlist.org)
b
Family names based on APG IV (2016)
c
Basionym publication
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ecological conditions in these contexts, previous findings
from the literature enable discussion of the environmental
constraints operating at 6400 m a.s.l. on Mount Everest.
On the one hand, Saxifraga lychnitis var. everestianus and
Androsace khumbuensis were found in rock crevices, which
are, according to Miehe (1987), a more suitable substrate
for vascular plants at upper elevations on Mount Everest.
Indeed, Miehe considers that the most decisive limiting
factor for plant colonization at the highest elevations is
the daily movement of the substrate by freezing and thawing action during the growing season. Consequently, rock
crevices capable of accumulating sun warmth may favour
plant colonization, as observed for the highest climbing
plant cited in the European Alps: Saxifraga oppositifolia,
at 4504 m a.s.l. (Körner 2011). On the other hand, Saussurea gnaphalodes, Lepidostemon everestianus and Arenaria
bryophylla were encountered on scree and moraine, that is to
say unstable substrates. According to Dvorský et al. (2016),
however, the root-zone temperature is the most important
driver for plant colonization and growth, making exposure
and micro-topography crucial. This factor is less dependent
on soil properties. In both cases, at the highest elevations on
Earth, seasonal effects are not to be underestimated: unusual
freezing or snowfall can counteract plant colonization. Succession of favourable conditions during the growing season
is, therefore, required to the establishment as well as the
survival of vascular plants (Dolezal et al. 2016).
Distribution and phylogeny of the highest vascular
plants
The five uppermost taxa found on Mount Everest belong
to clades known for being very speciose in cushion plants
(Aubert et al. 2014), a life form perfectly suited to arctico-alpine environments and representing an evolutionary
convergence among angiosperms (Boucher et al. 2016).
These clades display a similar pattern of distribution in
Eurasian mountain ranges: they account for 54% of the
nival flora in the Everest region (based on data from Miehe
1987); 49% in the Hindu Kush; 46% in Caucasus (Breckle
et al. 2017); and more than 52% in the European Alps
(Aeschimann et al. 2011). The striking similarity in the
altitudinal distribution of these clades through Eurasia
can be illustrated with the late Miocene radiation of the
Androsace genus roughly 15 million years ago (Boucher
et al. 2012; Roquet et al. 2013). At this time and in this
clade, the cushion life form, including many new species,
appeared independently in two rising mountain ranges: the
European Alps and the Himalaya. This convergent evolutionary history is reflected in taxonomic outcomes such
as ongoing discovery of novel taxa in different Eurasian
mountains: “Androsace innominata” (provisional name) in
the western Alps [see Jordan (2015) and Dentant (2017)],
13
Androsace komovensis in the Balkans (Schönswetter and
Schneeweiss 2009) and now Androsace khumbuensis on
Mount Everest. These highest climbing species appear
thus to be more than records of plant life. Taxonomic novelties highlight how little we know about plant diversity
and evolution in highest elevations.
Conclusion
Vascular plant species have been documented close to the
uppermost elevations of most of the world’s great mountain
ranges: the elevation record in Africa is 5760 m a.s.l., on
Mount Kilimanjaro (5895 m a.s.l.; Grabherr et al. 1995); in
the Andes, the highest vascular plants have been observed at
5800 m a.s.l. in the tropical part of the range (Halloy 1991).
The Everest specimens collected in the 1935 and 1952
expeditions are to date the highest climbing vascular plants
observed on Earth. Nevertheless, recent descriptions of new
taxa encountered above 6100 m highlight the need for further investigation on high-elevation growing species. Scarcity of vegetation is certainly not the only factor explaining
the little amount of data from upper elevations: sampling is
extremely difficult due to the hard access and the harsh environment of high mountains, and to the little investment of
modern mountaineers compared to pioneers of the discipline
[with exceptions, see Körner (2011) and Marx et al. (2017)].
Without question, it seems timely to encourage a renewed
approach to mountaineering, one which integrates awareness of scientific issues and a culture of data collection. Climate change and its consequences on biodiversity could be
an interesting point of convergence between mountaineers
and scientists. Ongoing effects of recent climate change on
alpine plant species are well studied in the European Alps:
widespread thermophilization and upward migration of plant
species (Gottfried et al. 2012), densification of alpine communities (Carlson et al. 2017), colonization processes and
increases in species richness on mountain summits (Kammer
et al. 2007; Steinbauer et al. 2018) and predicted habitat loss
due to warming (Engler et al. 2011). While similar processes
are likely underway in the Himalaya, the general increase in
temperature pushing species upwards appears to be potentially and deeply offset by seasonal and occasional adverse
conditions, such as repeated snowfalls or freezing events
during growing season (Dolezal et al. 2016). Renewal of biological scientific expeditions to Mount Everest, following the
example of the recent Czech expeditions in Eastern Ladakh
[see Dvorský et al. (2015) and Angel et al. (2016)], would
likely allow us to improve our knowledge on diversity and
ecological limits of the uppermost taxa, and consequently
to improve our understanding of plants’ ability to colonize
and survive at the upper limits of life.
Alpine Botany
Acknowledgements I would like to acknowledge the herbarium curators who provided a decisive assistance for this study: Fred Stauffer
and Laurent Gauthier (Conservatory and Botanical Garden of Geneva,
G); Ranee Prakash (Natural History Museum of London, BM). I would
also thank Fabien Anthelme and Hannah Marx for their advice for
improving the manuscript. And finally a special thanks to Sonja Wipf
for her indefatigable support and to Brad Carlson for his invaluable
contribution in refining the manuscript.
Author contributions C. Dentant analysed herbarium records at
the Conservatory and Botanical Garden of Geneva and the British
Museum, carried out research on historical expeditions to Mount Everest and wrote the paper.
Compliance with ethical standards
Conflict of interest The author declares that he has no conflict of interest.
References
Aeschimann D, Rasolofo N, Theurillat JP (2011) Analyse de la flore
des Alpes. 1: historique et biodiversité. Candollea 66:27–55
Akiyama S, Gomall RJ, Adhikari B et al (2012) Saxifragaceae. In:
Flora of Nepal (floraofnepal.org). Royal Botanical Garden Edinburg. http://www.floraofnepal.org. Accessed 2017
APG IV (2016) [Angiosperm Phylogeny Group] An update of the
Angiosperm Phylogeny Group classification for the orders and
families of flowering plants: APG IV. Bot J Linn Soc 181:1–20.
https://doi.org/10.1046/j.1095-8339.2003.t01-1-00158.x
Al-Shehbaz IA (2000) Lepidostemon (Brassicaceae) is no longer
monotypic. Novon 10:329–333
Angel R, Conrad R, Dvorsky M et al (2016) The root-associated
microbial community of the world’s highest growing vascular
plants. Microb Ecol 72:394–406. https://doi.org/10.1007/s0024
8-016-0779-8
Aubert S, Boucher F, Lavergne S et al (2014) 1914–2014: a revised
worldwide catalogue of cushion plants 100 years after Hauri
and Schröter. Alp Bot 124:59–70. https://doi.org/10.1007/s0003
5-014-0127-x
Baehni C (1958) Résultats des expéditions scientifiques genevoises au
Népal en 1952 et 1954 (partie botanique).13. Juglandaceae, Santalaceae, Thymelaeaceae et Saxifragaceae. Candollea 16:215–227
Bajracharya DM (1996) Phyto-geography of Nepal Himalaya. Tribhuvan Univ J 19:57–76
Ball J (1860) Suggestions for Alpine Travellers. In: Ball J (ed) Peaks,
passes and glaciers, 5th edn. Longman, Green, Longman & Roberts, London
Boucher FC, Thuiller W, Roquet C et al (2012) Reconstructing the
origins of high-alpine niches and cushion life form in the genus
Androsace s.l. (Primulaceae). Evolution 66:1255–1268. https://
doi.org/10.1111/j.1558-5646.2011.01483.x
Boucher FC, Lavergne S, Basile M et al (2016) Evolution and biogeography of the cushion life form in angiosperms. Perspect Plant Ecol
Evol Syst 20:22–31. https://doi.org/10.1016/j.ppees.2016.03.002
Breckle SW, Fayvusch G, Murtazaliev R, Nakhutsrishvili G (2017)
Floristic analysis of the subnival-nival vegetation of Hindu Kush
and Caucasus. Bielef Ökologische Beitr 21:7–31
Carlson BZ, Corona MC, Dentant C et al (2017) Observed long-term
greening of alpine vegetation—a case study in the French Alps.
Environ Res Lett 12:114006. https://doi.org/10.1088/1748-9326/
aa84bd
Carret M (1880) Note sur quelques plantes trouvées au pic de la Meije.
Ann Soc Bot Lyon 7:171–176
De Saussure H-B (1779–1796). Voyage dans les Alpes. Samuel Fauche
(tome I), Geneva; Barde, Manget & Compagnie (tome II), Geneva;
Louis Fauche-Borel (tomes III and IV), Geneva
Dentant C (2017) Flora verticalis. Editions Le Naturographe, Gap
Dolezal J, Dvorsky M, Kopecky M et al (2016) Vegetation dynamics
at the upper elevational limit of vascular plants in Himalaya. Sci
Rep 6:1–13. https://doi.org/10.1038/srep24881
Dvorský M, Altman J, Kopecký M et al (2015) Vascular plants at
extreme elevations in eastern Ladakh, northwest Himalayas.
Plant Ecol Divers 8:571–584. https ://doi.org/10.1080/17550
874.2015.1018980
Dvorský M, Chlumská Z, Altman J et al (2016) Gardening in the zone
of death: an experimental assessment of the absolute elevation
limit of vascular plants. Sci Rep 6:1–10. https://doi.org/10.1038/
srep24440
efloras.org (2008) Flora of China. Missouri Botanical Garden. MO &
Harvard University Herbaria, St Louis. Cambridge, MA. http://
www.efloras.org. Accessed 2017
Engler R, Randin CF, Thuiller W et al (2011) 21st century climate
change threatens mountain flora unequally across Europe.
Glob Chang Biol 17:2330–2341. https ://doi.org/10.111
1/j.1365-2486.2010.02393.x
German DA, Al-Shehbaz IA (2010) Nomenclatural novelties in miscellaneous Asian Brassicaceae (Cruciferae). Nord J Bot 28:646–651.
https://doi.org/10.1111/j.1756-1051.2010.00983.x
Gottfried M, Pauli H, Futschik A et al (2012) Continent-wide response
of mountain vegetation to climate change. Nat Clim Chang 2:111–
115. https://doi.org/10.1038/nclimate1329
Grabherr G, Gottfried M, Gruber A, Pauli H (1995) Patterns and current changes in alpine plant diversity. In: Chapin FS, Körner Ch
(eds) Arctic and alpine biodiversity: patterns, causes and ecosystem consequences. Ecological studies, vol 113. Springer, Berlin,
Heidelberg, New York, pp 167–181
Halloy S (1991) Islands of life at 6000 m altitude—the environment of
the highest autotrophic communities on Earth (Socompa Volcano,
Andes). Arct Alp Res 23:247–262. https://doi.org/10.2307/15516
02
Hu Q, Kelso S (2008) Primulaceae. In: Flora of China (efloras.org).
Missouri Botanical Garden. MO & Harvard University Herbaria,
St Louis. Cambridge, MA. http://www.efloras.org. Accessed 2017
Jordan D (2015) Atlas de la flore rare ou menacée de Haute-Savoie.
Naturalia Publications, Turriers
Kammer PM, Schöb C, Choler P (2007) Increasing species richness
on mountain summits: Upward migration due to anthropogenic
climate change or re-colonisation? J Veg Sci 18:301–306. https://
doi.org/10.1111/j.1654-1103.2007.tb02541.x
Klimeš L, German D (2009) Draba alshehbazii (Brassicaceae), a new
species from extreme altitudes of eastern Ladakh (Jammu and
Kashmir, India). Bot J Linn Soc 158:749–754. https://doi.org/10
.1111/j.1095-8339.2008.00933.x
Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin
Körner C (2011) Coldest places on earth with angiosperm plant life.
Alp Bot 121:11–22. https://doi.org/10.1007/s00035-011-0089-1
Marx HE, Dentant C, Renaud J et al (2017) Riders in the sky (islands):
using a mega-phylogenetic approach to understand plant species
distribution and coexistence at the altitudinal limits of angiosperm
plant life. J Biogeogr 44:2618–2630. https ://doi.org/10.1111/
jbi.13073
Miehe G (1987) An annotated list of vascular plants collected in the
valleys south of Mt Everest. Bull Brit Mus Nat Hist 16:225–268
Miehe G (1988) Vegetation patterns on Mount Everest as influenced by
monsoon and föhn. Vegetatio 79:21–32. https://doi.org/10.1007/
BF00044845
13
Alpine Botany
Miehe G (1991) Der Himalaya, eine multizonale Gebirgsregion. In:
Walter H, Breckle SW (eds) Ökologie der Erde, vol 4. Fischer,
Stuttgart, pp 181–230
Morueta-Holme N, Engemann K, Sandoval-Acuña P et al (2015)
Strong upslope shifts in Chimborazo’s vegetation over two centuries since Humboldt. Proc Natl Acad Sci 112:12741–12745.
https://doi.org/10.1073/pnas.1509938112
Polunin O, Stainton A (1997) Flowers of Himalaya. Oxford University
Press, Oxford
Roch A (1952) Everest 1952. Jeheber, Geneva
Roquet C, Boucher FC, Thuiller W, Lavergne S (2013) Replicated
radiations of the alpine genus Androsace (Primulaceae) driven
by range expansion and convergent key innovations. J Biogeogr
40:1874–1886. https://doi.org/10.1111/jbi.12135
Schönswetter P, Schneeweiss GM (2009) Androsace komovensis sp.
nov., a long mistaken local endemic from the southern Balkan
Peninsula with biogeographic links to the Eastern Alps. Taxon
58:544–549
Shi Z, von Raab-Straube E (2008) Saussurea. In: Flora of China (efloras.org). Missouri Botanical Garden. MO & Harvard University
Herbaria, St Louis. Cambridge, MA. http://www.eflor as.org.
Accessed 2017
Shipton EE (1936) The Mount Everest reconnaissance, 1935. Himal J 8
Shrestha KK, Press R (2008) Annotated Checklist of the Flowering
Plants of Nepal. In: efloras.org. Missouri Botanical Garden. MO
& Harvard University Herbaria, St Louis. Cambridge, MA. http://
www.efloras.org. Accessed 2017
13
Steinbauer MJ, Grytnes J-A, Jurasinski G et al (2018) Accelerated
increase in plant species richness on mountain summits is linked
to warming. Nature. https://doi.org/10.1038/s41586-018-0005-6
Swan LW (1992) The Aeolian Biome. Ecosystems of the earth’s
extremes. Bioscience 42:262–270
von Raab-Straube E (2011) The genus Saussurea (Compositae, Cardueae) in China: taxonomic and nomenclatural notes. Willdenowia 41:83–95. https://doi.org/10.3372/wi.41.41109
von Humboldt A, Bonpland A (1805) Essai sur la géographie des plantes. Levrault, Shoell et compagnie, Paris
Weibel R (1956) Résultats des expéditions scientifiques genevoises au
Népal en 1952 et 1954 (partie botanique).4. Primulaceae. Candollea 15:157–165
Whymper E (1871) Scrambles amongst the Alps in the years 1860–
1869. John Murray, London
Wipf S, Stöckli V, Herz K, Rixen C (2013) The oldest monitoring site
of the Alps revisited: accelerated increase in plant species richness
on Piz Linard summit since 1835. Plant Ecol Divers 6:447–455.
https://doi.org/10.1080/17550874.2013.764943
Zhengyi W, Wagner WL (2008) Arenaria. In: Flora of China (efloras.org). Missouri Botanical Garden. MO & Harvard University
Herbaria, St Louis. Cambridge, MA. http://www.eflor as.org.
Accessed 2017
Zimmermann A (1952) Botanique. In: Lobsiger-Dellenbach M, Lombard A, Zimmermann A (eds) Himalaya du Népal. Expédition
scientifique genevoise. Jeheber, Geneva