A botanical mystery solved by phylogenetic analysis of botanical garden collections: the rediscovery of the presumed-extinct Dracaena umbraculifera
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A botanical mystery solved by phylogenetic analysis
of botanical garden collections: the rediscovery of
the presumed-extinct Dracaena umbraculifera
CHRISTINE E. EDWARDS, BURGUND BASSÜNER, CHRIS BIRKINSHAW
CHRISTIAN CAMARA, ADOLPHE LEHAVANA, PORTER P. LOWRY II, JAMES S. MILLER
A N D R E W W Y A T T and P E T E R W Y S E J A C K S O N
Abstract Extinction is the complete loss of a species, but the discoveries and the importance of documenting and con-
accuracy of that status depends on the overall information serving the flora of Madagascar.
about the species. Dracaena umbraculifera was described
Keywords Botanical garden, Dracaena reflexa, Dracaena
in from a cultivated plant attributed to Mauritius, but
umbraculifera, extinction, living collections, Madagascar,
repeated surveys failed to relocate it and it was categorized as
Mauritius, phylogeny reconstruction
Extinct on the IUCN Red List. However, several individuals
labelled as D. umbraculifera grow in botanical gardens, sug-
gesting that the species’ IUCN status may be inaccurate. The
goal of this study was to understand () where D. umbracu- Introduction
lifera originated, () which species are its close relatives, ()
whether it is extinct, and () the identity of the botanical
garden accessions and whether they have conservation
value. We sequenced a cpDNA region of Dracaena from
E xtinction is the complete and total loss of all individuals
of a species. In practice, extinction can be defined as ‘the
permanent absence of current and future records of a spe-
Mauritius, botanical garden accessions labelled as D. um- cies’ (Ladle et al., ). Although this is a relatively straight-
braculifera, and individuals confirmed to be D. umbraculi- forward concept, accurately determining and proving that a
fera based on morphology, one of which is a living plant in a species is extinct is far from straightforward. Many species
private garden. We included GenBank accessions of may be presumed to be extinct, but whether this is actually
Dracaena from Madagascar and other locations and recon- the case may depend on factors such as the amount and ac-
structed the phylogeny using Bayesian and parsimony ap- curacy of historical data on a species’ distribution; the size of
proaches. Phylogenies indicated that D. umbraculifera is its range and the density of its populations; how its range has
more closely related to Dracaena reflexa from Madagascar changed over time; the ease with which it can be observed in
than to Mauritian Dracaena. As anecdotal information in- the field; and the number of knowledgeable scientists
dicated that the living D. umbraculifera originated from searching for it, the effort they expend in searching for it,
Madagascar, we conducted field expeditions there and lo- and their overall knowledge of the biota of a region (Ladle
cated five wild populations; the species’ IUCN status should et al., ; Lee et al., ). The most convincing evidence
therefore be Critically Endangered because , wild indi- for extinction involves species that were once widespread
viduals remain. Although the identity of many botanical and well known but then experienced an observable decline
garden samples remains unresolved, this study highlights in range and population size, and cannot now be relocated
the importance of living collections for facilitating new despite a relatively complete knowledge of the biota of the
region and extensive, repeated surveys by qualified biolo-
gists. If there is robust evidence for the extinction of a spe-
cies, IUCN Red List working groups may determine it to be
Extinct or Extinct in the Wild. A considerable number of
CHRISTINE E. EDWARDS (Corresponding author), BURGUND BASSÜNER, PORTER
P. LOWRY II*, JAMES S. MILLER, ANDREW WYATT and PETER WYSE JACKSON plant species are known to be Extinct in the Wild but still
Missouri Botanical Garden, P. O. Box 299, St. Louis, MO 63166, USA persist in cultivation, mainly in botanical gardens.
E-mail christine.edwards@mobot.org
Dracaena umbraculifera (Asparagaceae sensu lato, Byng
CHRIS BIRKINSHAW, CHRISTIAN CAMARA and ADOLPHE LEHAVANA, Missouri Botanical et al., ) is an example of a plant species that is currently
Garden, Madagascar Research and Conservation Program, Antananarivo,
Madagascar categorized as Extinct on the IUCN Red List (Strahm, ).
*Also at: Institut de systématique, évolution, et biodiversité, Unité mixte de To our knowledge it has never been observed by botanists in
Recherche 7205 (Centre national de la Recherche scientifique/Muséum national the wild and as a consequence has remained a mystery for
d’Histoire naturelle/École pratique des Hautes études, Université Pierre et Marie several centuries. Described in by Nicolaus Joseph von
Curie), Muséum national d’Histoire Naturelle, Sorbonne Universités, Paris,
France Jacquin based on a plant cultivated in the greenhouses of the
Received June . Revision requested September . botanical garden at Schönbrunn in Vienna (see Plate a for
Accepted October . First published online January . original illustration, Jacquin, ), this species has a
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570
428 C. E. Edwards et al.
PLATE 1 (a) The original
illustration of Dracaena
umbraculifera from Jacquin
(), (b) a paniculate
inflorescence of Dracaena
reflexa in Madagascar
(photograph by
P. Antilahimena, collection
number ), (c) a diffuse
paniculate infructescence of
Dracaena floribunda in
Mauritius (photograph by
C. Edwards), (d) a young
inflorescence of D.
umbraculifera in Ile
Sainte-Marie (photograph by
Rova Malala Rakotoarivelo),
(e) an inflorescence of D.
umbraculifera in Ile
Sainte-Marie in full flower
(photograph by A. Lehavana),
and (f) a vegetative individual
of D. umbraculifera
(photograph by P. Lowry).
distinctive morphology, with tightly clustered flowers in a present in the current collections of the Pamplemousses
nearly umbellate inflorescence in the centre of the leaves Botanical Garden (now the Sir Seewoosagur Ramgoolam
(Plate a), differing from the diffuse, paniculate inflores- Botanical Garden).
cences that characterize all other Dracaena (Plate b). Dracaena umbraculifera was subsequently included in a
Although Jacquin indicated that the cultivated plant on list of plants of Mauritius (Bojer, ) and described as
which he based his description came from the island of growing in the thick forests in the centre of the island and
Mauritius (Jacquin, ), its origin is unclear. It may have flowering very rarely. It was also listed as a Mauritian species
been collected during a voyage made by Franz Boos and in the Flora of Mauritius and the Seychelles (Baker, ). In
Georg Scholl, who sailed to South Africa and Mauritius dur- the more recent Flore des Mascareignes (Marais & Coode,
ing – and sent back cases of plants, assembled ), doubt was expressed about whether D. umbraculifera
by M. Céré of the Pamplemousses Botanical Garden in was native to Mauritius, as the main evidence that it existed
Mauritius. However, there is no surviving documentation of in Mauritius was Bojer’s description. It was suggested that
the plants contained in this shipment nor is it known whether Bojer may have confused D. umbraculifera with Dracaena
they were all Mauritian natives. Dracaena umbraculifera is not floribunda, which still occurs in central Mauritius, and
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570Rediscovery of Dracaena umbraculifera 429
that if D. umbraculifera was indeed Mauritian it must be ex- from botanical gardens in seven countries (Table ), as
tinct. Following unsuccessful efforts over the previous cen- well as one cultivated accession of Dracaena reflexa from
tury to locate living plants in the wild, the species was Missouri Botanical Garden. Individuals from botanical gar-
categorized as Extinct in (Strahm, ). dens identified as D. umbraculifera but that are not con-
Despite the fact that no natural population of D. umbra- firmed by a flowering specimen are hereafter indicated in
culifera has been documented in the wild in Mauritius, it quotes (i.e. ‘D. umbraculifera’). Although other gardens re-
may not be extinct, as living plants labelled as D. umbracu- ported having individuals of D. umbraculifera, several flow-
lifera have long been grown in botanical gardens around the ered recently and had diffuse-paniculate inflorescences,
world. One such plant is growing at the Missouri Botanical confirming that they were incorrectly identified, and were
Garden. This stimulated an interest in the true status of this not included in the study. Leaf material of a correctly iden-
presumably extinct species and led us to initiate a study to tified, pressed specimen of D. umbraculifera was obtained
try to elucidate its origins. The individual at Missouri from the University of Vienna herbarium (WU ;
Botanical Garden was obtained in from an unknown Table ). It was prepared in from a plant cultivated in
source and, if correctly identified, the IUCN status of the Hortus Botanicus Vindobonensis (now known as the
D. umbraculifera should be updated to Extinct in the Botanical Garden of the University of Vienna), and has
Wild (IUCN, ). Further research in the database of cul- the distinctive inflorescence of D. umbraculifera. Given
tivated plants maintained by Botanic Gardens Conservation that Jacquin, who described D. umbraculifera, was the first
International (BGCI, ) found other gardens with living director of Hortus Botanicus Vindobonensis, we speculate
individuals identified as D. umbraculifera. Communications that this specimen may have originated from the same
with staff at these gardens indicated that most of these plants plant on which Jacquin based his description.
have been in their collections for decades and their origins We also conducted fieldwork in Mauritius in January
are unknown (other than in some cases in which they to collect leaf tissue of all Dracaena species currently
were obtained from other botanical gardens). As unequivo- known to be native to the island (Table ), including D. flori-
cal morphological identification of these plants relies on the bunda, D. concinna and D. reflexa (including two of the
presence of an inflorescence, yet they rarely, if ever, flower in three varieties of D. reflexa in Mauritius, var. reflexa and
cultivation (the plant in Missouri Botanical Garden has not var. angustifolia). The collected tissue was preserved in silica
been observed in flower for decades), the identity of these gel. During this trip, staff at Mauritius Herbarium informed
specimens remains uncertain. It is important to determine us of an individual of D. umbraculifera growing in a private
their identity because they may be the only remaining garden on the island. This plant had flowered recently and
individuals of a species that is otherwise extinct. its identification was confirmed based on its distinctive,
Our goal was to unravel the mystery of D. umbraculifera umbel-like inflorescence. The herbarium staff provided
and, in particular, to understand where it originated, which leaf tissue in silica gel, which was used as a reference for
species it is related to, whether it is indeed extinct in the comparison with the samples obtained from botanical gar-
wild, whether the living plants in botanical gardens are cor- dens. Although the wild origin of the plant was not indicated
rectly identified and whether they are of conservation value. on the herbarium specimen, a web search found an online
We gathered samples from living individuals labelled as D. posting by the plant’s owner indicating that ‘it grows in
umbraculifera from botanical gardens throughout the world, N-East of Madagascar in an island called Ste Marie, Illes
travelled to Mauritius to collect specimens of the extant spe- Aux Nattes’ (Dave’s Garden, ). This information as
cies of Dracaena, and investigated phylogenetic relationships well as the results from preliminary phylogenetic analyses
using this material, as well as GenBank accessions from spe- prompted us to visit Ile Sainte-Marie and its small outlier
cies from other islands of the Western Indian Ocean. As our Ile aux Nattes, off the east coast of Madagascar, in
initial phylogenetic reconstruction based on DNA sequence October , where three samples of two native Dracaena
data indicated that living plants identified as D. umbraculifera species were collected (Table ).
were more closely related to species in Madagascar than to DNA was extracted from the leaf tissue samples using a
those in Mauritius, we conducted fieldwork in Madagascar modified Cetyl trimethylammonium bromide (CTAB) ap-
in an attempt to collect additional possible relatives and per- proach (Doyle & Doyle, ). As a recent molecular phylo-
haps also locate the presumed-extinct D. umbraculifera. genetic study that investigated relationships in Malagasy D.
reflexa (Buerki et al., ) employed a plastid marker span-
Methods ning the trnL gene and trnL-F spacer, we selected this mark-
er for our study to make use of previously generated DNA
Sample collection and molecular methods sequence data. We conducted polymerase chain reactions
(PCR) using the primers C and F (Taberlet et al., )
We obtained leaf samples preserved in silica gel from living and previously published amplification protocols (Shaw
collections of accessions identified as D. umbraculifera et al., ). PCR products were cleaned with ExoSAP
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570430 C. E. Edwards et al.
TABLE 1 Cultivated accessions of Dracaena umbraculifera and Dracaena reflexa used in phylogenetic analysis of Dracaena species.
GenBank
Type of ID confirmed by accession
Label Location Accession number collection inflorescence? Source number
D. umbraculifera Vienna University WU0077694 (1895) Herbarium Yes Plant grown in MG020508
Herbarium, Vienna botanical gar-
Austria den in Vienna
(1895)
D. umbraculifera Personal garden of Voucher deposited in Living Yes Unknown MG020494
I. Vencapah, Mont the Herbarium of the
Choisy, Mauritius Missouri Botanical
Garden: Vencapah
26071
‘D. umbraculifera’ Wairere Nursery, Living No Chiltern Seeds MG020491
Auckland, New
Zealand
D. umbraculifera Dunedin Botanic Living No Chiltern Seeds MG020492
Garden, Dunedin,
New Zealand
‘D. umbraculifera’ Toronto Zoo, Living No Unknown MG020497
Toronto, Canada
‘D. umbraculifera’ Botanic Garden of 6360PA Living No Unknown MG020493
Smith College
Northampton, USA
‘D. umbraculifera’ Conservatoire 80-0330 Living No Jardin MG020505
Botanique National Botanique
de Brest, France Genève
‘D. umbraculifera’ Moscow Main New & old greenhouses Living No Grown from MG020496
Botanic Garden, seed (1968)
Moscow, Russia
‘D. umbraculifera’ Komarov Botanical Living No Pre 1917 MG020504
Institute,
St. Petersburg,
Russia
‘D. umbraculifera’ Missouri Botanical 1980-1301 Living No Unknown MG020495
Garden, St. Louis, (1904)
USA
‘D. umbraculifera’ Jardin Botanique 1989.3.056, 1990.3.194 Living No Jardin MG020506
Nancy, France Botanique
Genève
‘D. umbraculifera’ Muséum national 7460, 58406, 71595 Living No Unknown MG020507
d’Histoire naturelle,
Paris, France
D. reflexa Missouri Botanical 1989-4416 Living Joseph Hill Co MG020498
Garden, St. Louis, Tropical
USA Foliage, Miami
(1989)
(USB Corporation, Cleveland, USA) and sequenced in both ‘D. umbraculifera’ from a cultivated specimen at the Waimea
directions using BigDye Chemistry (Applied Biosystems Arboretum and Botanical Garden, Haleiwa, USA (JQ,
(ABI), Foster City, USA) on an ABI xl DNA Genetic Lu & Morden, ); three sequences of Dracaena from Asia
Analyzer at the DNA analysis facility at Science Hill at and the Canary Islands, D. draco (KC), D. cambodiana
Yale University, New Haven, USA. Forward and reverse se- (KC), and D. cochinchinensis (KC); multiple
quences were assembled and edited in Geneious R (Kearse Asparagaceae s.l. outgroups, including Convallaria majalis
et al., ). (EU), Maianthemum gongshanensis (EU),
The new sequences generated in this study were aligned Disporopsis aspersa (EU), Polygonatum cyrtonema
with the following sequences from GenBank: Dracaena (EU), and Cordyline cannifolia (KC); and one
from Madagascar (EU-EU, Buerki et al., ); additional outgroup from another family of Asparagales,
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570Rediscovery of Dracaena umbraculifera 431
TABLE 2 Wild accessions of Dracaena species used in phylogenetic analysis. All voucher specimens are deposited in the Herbarium of the
Missouri Botanical Garden.
GenBank accession
Species Location Voucher number
D. floribunda On the west banks of the Papaya River, Henrietta, Mauritius Edwards 299 MG020499
D. reflexa var. reflexa Brise Fer Conservation Management Area, Mauritius Edwards 296 MG020500
D. reflexa var. reflexa Mondrain Reserve, Mauritius Edwards 300 MG020501
D. concinna St. Martin cemetery, Baie du Cap, Mauritius Edwards 301 MG020503
D. reflexa var. angustifolia Black River Gorges National Park, Mauritius Edwards 297 MG020502
D. umbraculifera Kalalao Forest, Ile Sainte-Marie, Madagascar Miller 10775 MG020509
D. umbraculifera Kalalao Forest, Ile Sainte-Marie, Madagascar Miller 10776 MG020511
D. xiphophylla Kalalao Forest, Ile Sainte-Marie, Madagascar Miller 10778 MG020510
Crinum oliganthum (AY; Amaryllidaceae), which was from the wild in Mauritius and Madagascar (Table ). The
used to root the trees. Alignments were conducted using the aligned length of the trnL-F data matrix was characters,
default settings in Muscle (Edgar, ) and were adjusted of which characters were constant, were variable but
manually in Geneious. parsimony-uninformative and were parsimony-informative.
Parsimony searches recovered , most-parsimonious
trees with a length of steps. Because the topologies of
Data analysis the trees obtained from Bayesian and parsimony phylogeny
reconstruction were almost identical, we present only the
Phylogenetic analyses were carried out using parsimony and
Bayesian tree, with Bayesian posterior probabilities (PP)
Bayesian approaches. Parsimony analysis was implemented
and parsimony bootstrap support (BS) indicated on branches
in PAUP* .a (Swofford, ) using heuristic searches,
(Fig. ).
tree bisection–reconnection branch swapping and ,
Using Crinum as the outgroup, the remaining samples
random addition replicates, saving trees per replicate.
were clustered into two well-supported clades (both with
Bootstrap analyses (Felsenstein, ) with , replicates
PP = ., BS = %), one comprising two cultivated sam-
were employed to assess branch support, using a heuristic
ples of ‘D. umbraculifera’ from New Zealand plus a sample
search with tree bisection–reconnection branch swapping,
of Cordyline, and the other containing all of the remaining
with one random addition per replicate and saving no
taxa. Within the latter clade the accession of ‘D. umbraculi-
more than one tree per replicate. Bayesian phylogenetic ana-
fera’ from the Botanic Garden of Smith College,
lysis was conducted using MrBayes . (Ronquist et al.,
Northampton, USA, and the samples of M. gongshanensis,
). The optimal model of evolution for the data was se-
C. majalis and D. aspersa + P. cyrtonema were weakly sup-
lected using the Akaike Information Criterion in jmodeltest
ported, successive sisters to a well-supported clade (PP = .,
(Darriba et al., ). We ran two analyses, using four chains
BS = %) containing all remaining Dracaena accessions
each, three hot and one cold, the temperature set to the de-
(Fig. ). This main Dracaena clade formed an unresolved
fault of ., flat priors, and the GTR + G model of evolution
polytomy comprising seven lineages: () a single GenBank
as selected by jmodeltest. Analyses were run for million
accession of D. reflexa var. linearifolia, () a GenBank acces-
generations, sampling a tree every , generations. To de-
sion of ‘D. umbraculifera’ from the Waimea Arboretum and
termine the burn-in value, we used Tracer v. . (Rambaut
Botanical Garden, () a clade with PP = . and BS = %
et al., ) to examine the stabilization of the run para-
containing three GenBank accessions of Dracaena from
meters and discarded trees saved before the stabilization
Asia and the Canary Islands, () a clade with PP = .
of the scores. Posterior probabilities were calculated using
and BS = % that included one GenBank accession of
the sumt command in MrBayes. Trees were visualized by
Dracaena xiphophylla and two of D. reflexa var. angustifolia
constructing a majority-rule consensus of trees in the pos-
from northern Madagascar (i.e. clade C of Buerki et al.,
terior distribution using PAUP*.
), () a large clade with PP = . and BS = % con-
taining samples of D. reflexa from the far northern
Results Madagascar (i.e. clade A of Buerki et al., ), () a clade
with PP = . and BS = % containing all six Dracaena ac-
The final data set contained sequences: GenBank ac- cessions from Mauritius, and () a clade with PP = . and
cessions and sequences newly generated for this study, BS , % containing one single sample of D. xiphophylla
of which were obtained from cultivated individuals from Ile Sainte-Marie placed as the sister group to a clade
(Table ) and eight of which were from plants collected with PP = . and BS , % containing an unresolved
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570432 C. E. Edwards et al.
FIG. 1 Bayesian phylogeny of wild and cultivated Indian Ocean Dracaena spp., with Bayesian posterior probabilities/parsimony
support values indicated on the branches. Plants from Madagascar are in black font; plants from Mauritius are in turquoise; cultivated
plants are in green, with the name of the garden; Dracaena from elsewhere (outgroups) are in yellow; and outgroups are in grey. D.
umbraculifera individuals whose identification has not been confirmed by reproductive material are indicated by quotation marks.
FIG. 2 Locations of D. umbraculifera populations in Madagascar from which samples were collected for phylogenetic analysis.
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570Rediscovery of Dracaena umbraculifera 433
polytomy of the two positively identified samples of D. um- umbraculifera and the overall phylogenetic placement of
braculifera (from Mauritius and Vienna, respectively), two the species. The most likely reason that this species has re-
samples from Ile Sainte-Marie, seven ‘D. umbraculifera’ ac- mained a mystery to botanists for centuries and has long
cessions from botanical gardens (from Missouri, Moscow, been considered to be extinct is that it was attributed incor-
Toronto, St. Petersburg, Paris, Brest and Nancy) and eight rectly to Mauritius. Records accompanying th century
samples of D. reflexa from coastal north-eastern and north- material from the western Indian Ocean were often scanty
central Madagascar (i.e. clade B of Buerki et al., ). at best, and it is likely that the original plant on which
Jacquin based his description was obtained in a shipment
of plants from the Pamplemousses Garden in Mauritius,
Discussion leading to its misattribution to that island. That the species
was never detected in Madagascar is not particularly sur-
The origin and closest relatives of Dracaena prising given the country’s extensive botanical diversity
umbraculifera and endemism, the high vegetative similarity and taxonomic
uncertainty of Malagasy Dracaena, and the lack of compre-
The phylogenetic analyses presented here indicate that all hensive, expert knowledge of the Dracaena of the region.
species of Dracaena currently occurring in Mauritius form Although it is possible that D. umbraculifera once occurred
a well-supported clade, whereas the two samples positively in the wild in Mauritius and went extinct, the phylogenetic
identified as D. umbraculifera (i.e. the herbarium sample analysis indicates that D. umbraculifera probably originated
from Vienna and the living plant in the private garden, in Madagascar, which would require a relatively recent col-
with an umbel-like inflorescence) are more closely related onization event by D. umbraculifera from Madagascar to
to a clade comprising multiple samples of D. reflexa from Mauritius, followed by its extinction in Mauritius, which
Madagascar (i.e. clade B of Buerki et al., ), suggesting is a less parsimonious explanation.
that D. umbraculifera may not be a Mauritian species.
Previous phylogenetic analysis of D. reflexa in Madagascar
recovered three clades that were generally distributed ac- Current status of Dracaena umbraculifera
cording to geography, two that included samples from far
northern Madagascar (i.e. clades A and C of Buerki et al., Surveys conducted during two field trips in and
) and one (i.e. clade B of Buerki et al., ) containing located a total of five wild populations of D. umbraculifera
accessions from coastal north-eastern and north-central (Fig. ), all of which occur in low-elevation evergreen forest
Madagascar, along with a few accessions from the southern on laterite and sandy soils. Three closely spaced populations
portion of the country. Our analysis also showed that D. um- occur in partially degraded forest at Pointe à Larrée on
braculifera formed a clade with individuals of D. reflexa be- mainland Madagascar (Fig. ), one inside the recently estab-
longing to clade B (Buerki et al., ), which provided lished (in April ) protected area being managed jointly
some indication of its likely geographical origin (i.e. coastal by the local community and Missouri Botanical Garden,
north-eastern and north-central Madagascar). The inter- and two that are unprotected. A fourth population occurs
pretation that D. umbraculifera may be of Malagasy origin in Ile aux Nattes (Fig. ), on private land in highly disturbed
was consistent with the information provided by the owner secondary vegetation. The fifth population is located in
of the positively identified plant in a private garden in largely intact, closed-canopy evergreen forest at Kalalao on
Mauritius, which prior to this study was the only known liv- Ile Sainte-Marie (Fig. ). A few additional, apparently
ing individual unambiguously attributable to the species. planted individuals occur on Sainte-Marie in private
Fieldwork in Madagascar in and led to the discov- gardens.
ery of several wild populations in Ile Sainte-Marie and Ile Although our findings demonstrate that D. umbraculi-
aux Nattes, and further searches at Pointe à Larrée on the fera is clearly not extinct, it is nevertheless rare and faces
mainland, directly across from Ile Sainte-Marie, found add- many threats. Despite being known from five populations
itional wild populations (Fig. ). on Ile Sainte-Marie and mainland Madagascar, we estimate
Although D. umbraculifera has always been considered that no more than mature individuals of D. umbraculifera
to be a Mauritian species, the geographical distribution of remain in the wild, all of which face threats from habitat
the wild populations indicate that it is native to degradation, land clearing for agriculture and development,
Madagascar. Phylogenies also suggest that it is more closely fires, and cyclones. The total number of individuals is below
related to Malagasy species than Mauritian species, indicat- the threshold for Critically Endangered status under IUCN
ing that D. umbraculifera most likely originated in Red List Criterion D (IUCN, ). The species has an
Madagascar. Because we included the herbarium sample Extent of Occurrence of km and an Area of
from Vienna, which is probably derived from the type spe- Occupancy of km, and is facing continued decline in
cimen, we can be certain about the identification of D. the quality of its habitat and the number of mature
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570434 C. E. Edwards et al.
individuals. As with many threatened species in Madagascar, from New Zealand, which were placed among other
efforts to conserve D. umbraculifera should focus on protect- Asparagaceae outgroups outside Dracaena in the phylogen-
ing and restoring the forest fragments that harbour the wild etic tree. Our phylogenetic analyses did not, however, pro-
populations. Establishing back-up collections of the species in vide adequate resolution to confirm the identification of the
ex situ facilities should also be carried out to contribute to its remaining botanical garden accessions; their conservation
long-term conservation. importance thus remains unresolved. Despite the fact that
several botanical garden samples (from Missouri Botanical
Garden, France, Russia and Toronto) were placed in the
Taxonomic implications clade that contained individuals confirmed to be D. umbra-
culifera, this group also included accessions that belong to
Our results indicate that D. reflexa, as currently circum-
the D. reflexa clade B (Buerki et al., ), and we were un-
scribed, is not monophyletic. Material from Mauritius as-
able to determine to which group the botanical garden sam-
signed to this species forms a clade with the two other
ples belong. In the absence of flowering material, future
Mauritian natives D. floribunda and D. concinna, indicating
research using additional sampling and more informative
that ‘D. reflexa’ in Mauritius is evolutionarily distinct from
molecular markers (i.e. collected using next-generation
populations in Madagascar and therefore should be referred
DNA sequencing approaches) will be necessary to confirm
to under a different name. Our results also show that D. re-
the identity of these botanical garden samples as well as to
flexa clade B of Buerki et al. () is more closely related to
assess their genetic diversity and their value for conservation
D. umbraculifera, which occurs in the same geographical
or reintroduction.
area, than to other populations from northern Madagascar
This study highlights the value and importance of the liv-
also assigned to D. reflexa, indicating that D. reflexa in
ing collections maintained in botanical gardens, even those
Madagascar is also not monophyletic. As currently circum-
that are over a century old and lack information about their
scribed, D. reflexa occurs throughout the islands of the
origin. Genetic analysis of living collections can play an im-
Western Indian Ocean region, including Madagascar,
portant role in gaining a better understanding of poorly
Mauritius, Rodrigues, Réunion and the Seychelles archipel-
known species and making new discoveries of interest for
ago, and also in Mozambique in continental Africa (Wright,
biodiversity and conservation. In the past, plants of un-
; eMonocot, ). Given the geographical structuring
known origin have often been regarded as being of little
of lineages observed in Mauritius and Madagascar, it is pos-
or no value for conservation purposes. However, this re-
sible that populations currently assigned to ‘D. reflexa’ oc-
search would never have been undertaken and D. umbracu-
curring in these geographically isolated regions represent
lifera would probably not have been rediscovered in
distinct lineages and thus belong to more than one species.
Madagascar if we had not used genetic analysis to elucidate
It is also possible that some of these lineages occurring in
the true identity of the living collections of ‘D. umbraculi-
islands in the western Indian Ocean could be close relatives
fera.’ Genetic analysis of living collections will unquestion-
of D. umbraculifera. However, this study included only a
ably bring new value to undocumented living collections in
small portion of the diversity present in Madagascar and
botanical gardens and facilitate their use for conservation
Mauritius, did not include Dracaena from other locations
purposes, such as for reintroductions and augmentations
in the Indian Ocean region, and lacked the phylogenetic
of depleted gene pools of wild populations of some
resolution needed to elucidate phylogenetic relationships
Critically Endangered species.
fully. A future study employing more informative molecular
Our findings also highlight the need for additional work
markers (i.e. those generated using next-generation DNA
in Madagascar and other islands of the western Indian
sequencing approaches, such as RAD-seq or whole chloro-
Ocean. Madagascar contains an estimated , vascular
plast genomes) and more comprehensive taxon sampling of
plant species, of which nearly % are thought to be endem-
Dracaena in Madagascar, Eastern Africa and the islands of
ic (Callmander et al., ; Madagascar Catalogue, ), and
the Western Indian Ocean is needed to clarify species
many are threatened as a result of extensive and ongoing de-
boundaries, evolutionary relationships and patterns of di-
forestation. Although Madagascar has been the focus of
versity, and identify species in need of conservation.
plant taxonomic work for over centuries, comprehensive,
expert knowledge of many taxa in the region is lacking, and
Status of the botanical garden collections many endemic species are poorly known. As previously sta-
ted, D. umbraculifera was overlooked by botanists in
The phylogenetic analyses presented here have helped to re- Madagascar because of the extensive botanical diversity
solve the identification of some of the sampled individuals and endemism there, the high vegetative similarity and
identified as ‘D. umbraculifera’ in botanical gardens. Several taxonomic uncertainty of Malagasy Dracaena, and the
are clearly misidentified, including those growing in the lack of comprehensive, expert knowledge of the Dracaena
Botanical Garden at Smith College and the accessions of the region. An accurate understanding of the status of a
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
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https://doi.org/10.1017/S0030605317001570Rediscovery of Dracaena umbraculifera 435
species is necessary to devise effective conservation strat- BGCI (B O TA N I C G A R D E N S C O N S E R VAT I O N I N T E R N A T I O N A L ) ()
egies, and therefore we emphasize the urgent need to docu- PlantSearch. Https://www.bgci.org/plant_search.php [accessed
September ].
ment and conserve the biodiversity of this region,
B O J E R , W. () Hortus Mauritianus. Aimé Mamarot et Compagnie,
particularly in poorly understood groups such as Dracaena. Mauritius.
B U E R K I , S., C A L L M A N D E R , M.W., S C H Ü P F E R , F., R AV O K A T R A , M.,
K Ü P F E R , P. & A LVA R E Z , N. () Malagasy Dracaena Vand. ex
Acknowledgements L. (Ruscaceae): an investigation of discrepancies between
morphological features and spatial genetic structure at a small
We are grateful to Imran Vencapah (Mauritius) for sharing evolutionary scale. Plant Systematics and Evolution, , –.
B Y N G , J.W., C H A S E , M.W., C H R I S T E N H U S Z , M.J.M., F AY , M.F., J U D D ,
his discovery of Dracaena umbraculifera in Madagascar;
W.S., M A B B E R L E Y , D.J. et al. () An update of the Angiosperm
and Michael Kiehn and Walter Till (Vienna University Phylogeny Group classification for the orders and families of
Herbarium), Rob Nicholson (Smith College), Tom Myers flowering plants: APG IV. Botanical Journal of the Linnean Society,
(Dunedin Botanic Garden), Jody Lusk (Wairere Nursery), , –.
Elizabeth Miller (National Forestry Herbarium, New C A L L M A N D E R , M.W., P H I L L I P S O N , P.B., S C H AT Z , G.E.,
A N D R I A M B O LO LO N E R A , S., R A B A R I M A N A R I V O , M.,
Zealand), Dmitry Geltman (Botanical Institute of
R A KOT O N I R I N A , N. et al. () The endemic and non-endemic
St. Petersburg), Pete Phillipson (Missouri Botanical vascular flora of Madagascar updated. Plant Ecology and Evolution,
Garden), Aleksander Demidov (Moscow Main Botanic , –.
Garden), Claudia Baider (Mauritius Herbarium), Pei-Luen D A R R I B A , D., T A B O A D A , G.L., D O A L LO , R. & P O S A D A , D. ()
Lu (University of Hawaii at Manoa), Chad Husby (Fairchild jModelTest : more models, new heuristics and parallel computing.
Tropical Garden), Günter Gerlach (Munich Botanical Nature Methods, , .
D AV E ’ S G A R D E N () Dracaena or Yucca? Http://davesgarden.com/
Garden), Martin Callmander (Conservatoire et Jardin community/forums/t//#b [accessed October ].
Botaniques de la Ville de Genève), Sven Buerki (Natural D OY L E , J.J. & D O Y L E , J.L. () A rapid isolation procedure for small
History Museum, London), Fanch Le Hir (Conservatoire quantities of fresh leaf tissue. Phytochemical Bulletin, , –.
Botanique National de Brest), and staff at the Toronto E D G A R , R.C. () MUSCLE: a multiple sequence alignment method
Zoo and the botanical gardens in Nancy for providing sam- with reduced time and space complexity. BMC Bioinformatics, , –
.
ples. We also thank Jean-Claude Sevathian, Vikash Tatayah, E M O N O C O T () Dracaena reflexa Lam. Http://e-monocot.org/
Debby de Chazal, Carl Jones and Gabriel d’Argent taxon/urn:kew.org:wcs:taxon: [accessed September ].
(Mauritian Wildlife Foundation) for helping obtain permits F E L S E N S T E I N , J. () Confidence limits on phylogenies: an approach
and locating specimens in Mauritius; Mario Allet, Arveen using the bootstrap. Evolution, , –.
Gungadurdoss and Dharma Beetun of the National Parks IUCN () IUCN Red List Categories and Criteria: Version .. nd
edition. IUCN, Gland, Switzerland, and Cambridge, UK.
and Conservation Service of Mauritius for assisting with
J AC Q U I N , N.J. () Plantarum Rariorum Horti Caesarei
field work in Mauritius; Rova Malala Rakotoarivelo for Schoenbrunnensis.
use of her photograph of D. umbraculifera; Theo Damen K E A R S E , M., M O I R , R., W I L S O N , A., S T O N E S -H AVA S , S., C H E U N G , M.,
(Naturalis Biodiversity Centre, Netherlands) for discussions S T U R R O C K , S. et al. () Geneious Basic: an integrated and
about D. umbraculifera; and Peter Hoch (Missouri extendable desktop software platform for the organization and
analysis of sequence data. Bioinformatics, , –.
Botanical Garden) for overall assistance obtaining samples.
L A D L E , R.J., J E P S O N , P., M A L H A D O , A.C.M., J E N N I N G S , S. & B A R U A ,
M. () The causes and biogeographical significance of species
rediscovery. Frontiers of Biogeography, , –.
Author contributions L E E , T.E., F I S H E R , D.O., B LO M B E R G , S.P. & W I N T L E , B.A. ()
Extinct or still out there? Disentangling influences on extinction and
CEE, JSM, AW and PWJ conceived the study. CEE, JSM, rediscovery helps to clarify the fate of species on the edge. Global
AW, CB and PWJ conducted fieldwork in Mauritius. AW Change Biology, , –.
L U , P.L. & M O R D E N , C.W. () Phylogenetic relationships among
and PWJ coordinated collection of material in botanical gar-
Dracaenoid genera (Asparagaceae: Nolinoideae) inferred from
dens. JSM, AL, PPL, CB and CC coordinated and conducted chloroplast DNA loci. Systematic Botany, , –.
fieldwork in Madagascar. CEE and BB conducted the mo- M A D A G A S C A R C AT A LO G U E () A Catalogue of the Vascular Plants
lecular work. CEE analysed the data. CEE and JSM wrote of Madagascar. Missouri Botanical Garden, St. Louis, USA.
the article, and all authors edited and approved the final M A R A I S , W. & C O O D E , M.J.E. () . Lilacees. In Flore des
version. Mascareignes (eds J. Bosser, T. Cadet, H.R. Julien & W. Marais),
p. . Mauritius Sugar Industry Research Institute, Mauritius, and
Royal Botanic Gardens (Kew), London, UK.
R A M B A U T , A., S U C H A R D , M.A., X I E , D. & D R U M M O N D , A.J. ().
References Tracer v. .. Http://tree.bio.ed.ac.uk/software/tracer/ [accessed
October ].
B A K E R , J.G. () Flora of Mauritius and the Seychelles. Reeve & Co., R O N Q U I S T , F., T E S L E N KO , M., VA N D E R M A R K , P., A Y R E S , D.L.,
London, UK. D A R L I N G , A., H Ö H N A , S. et al. () MrBayes .: efficient Bayesian
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 21 Nov 2021 at 12:17:41, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001570436 C. E. Edwards et al.
phylogenetic inference and model choice across a large model space. W R I G H T , H. () Observations on Dracaena reflexa Lam. Annals of
Systematic Biology, , –. the Royal Botanical Garden, Peradenia, , –.
S H AW , J., L I C K E Y , E.B., B E C K , J.T., F A R M E R , S.B., L I U , W.S., M I L L E R , J.
et al. () The tortoise and the hare II: relative utility of
noncoding chloroplast DNA sequences for phylogenetic analysis.
American Journal of Botany, , –. Biographical sketches
S T R A H M , W. () Dracaena umbraculifera. In The IUCN Red List of
Threatened Species : e.TA. Http://dx.doi.org/. C H R I S T I N E E D W A R D S and B U R G U N D B A S S Ü N E R are interested in
/IUCN.UK..RLTS.TA.en [accessed using conservation genetics to ensure the effectiveness of conservation
October ]. efforts for rare plant species. C H R I S B I R K I N S H A W , C H R I S T I A N
S WO F F O R D , D.L. () PAUP*. Phylogenetic Analysis Using C A M A R A , A D O L P H E L E H A V A N A , P O R T E R P. L O W R Y II and
Parsimony (*and Other Methods). . beta . Sinauer Associates, J A M E S M I L L E R are interested in taxonomy and conservation of the
Sunderland, USA. flora of Madagascar and Africa. A N D R E W W Y A T T and P E T E R
T A B E R L E T , P., G I E L LY , L., P A U T O U , G. & B O U V E T , J. () Universal W Y S E J A C K S O N are broadly interested in conservation activities in
primers for amplification of three non-coding regions of chloroplast botanical gardens, and using botanical garden living collections for
DNA. Plant Molecular Biology, , –. ex situ conservation of rare plant species.
Oryx, 2018, 52(3), 427–436 © 2018 Fauna & Flora International doi:10.1017/S0030605317001570
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 21 Nov 2021 at 12:17:41, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
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