Is There A Future For The Cactaceae Genera Copiapoa, Eriosyce and Eulychnia? A Status Report of A Prickly Situation

Biodivers Conserv (2014) 23:1249–1287
DOI 10.1007/s10531-014-0664-z
ORIGINAL PAPER
Is there a future for the Cactaceae genera Copiapoa,

Eriosyce and Eulychnia? A status report of a prickly
situation
Isabel Larridon • Kirsty Shaw • Mauricio A. Cisternas •

Anna Paizanni Guillén • Suzanne Sharrock • Sara Oldfield •
Paul Goetghebeur • Marie-Stéphanie Samain
Received: 3 October 2013 / Revised: 6 February 2014 / Accepted: 25 February 2014 /

Published online: 8 March 2014
Ó Springer Science+Business Media Dordrecht 2014
Abstract Many of Chile’s iconic cactus species are threatened by human activities and
global change. In order to safeguard them from extinction, both in situ and ex situ con-
servation actions are urgently needed. In this paper, an overview is given of the in situ and
ex situ conservation status of the mainly Chilean cactus genera Copiapoa, Eriosyce and
Eulychnia, including a worldwide survey of living ex situ collections of the species of
these genera. From our results, we can conclude that although the threats to Chile’s
remarkable biodiversity are now recognized as an environmental problem, and efforts are
underway to protect the threatened endemic flora, many of the most threatened species are
currently not protected in situ. Although a higher percentage of living accessions of
Copiapoa, Eriosyce and Eulychnia in ex situ collections are of known wild origin com-
pared to results of previous studies on other plant groups, the number of available
accessions is insufficient to adequately preserve the genetic diversity of the threatened
species. Prospects to upscale both in situ and ex situ conservation of the studied genera are
discussed.
Communicated by Danna J Leaman.
I. Larridon (&) P. Goetghebeur M.-S. Samain

Ghent University Research Group Spermatophytes & Botanical Garden, K.L. Ledeganckstraat 35,
9000 Ghent, Belgium
e-mail: isabel.larridon@ugent.be
K. Shaw S. Sharrock S. Oldfield

Botanic Gardens Conservation International (BGCI), 199 Kew Road, Richmond, Surrey TW9 3BW,
UK
M. A. Cisternas
Jardı́n Botánico Nacional, Camino El Olivar 305 El Salto, Viña del Mar, Chile
A. Paizanni Guillén M.-S. Samain

Centro Regional del Bajı́o, Instituto de Ecologı́a, A.C., Avenida Lázaro Cárdenas 253,
61600 Pátzcuaro, Michoacán, Mexico
123
1250 Biodivers Conserv (2014) 23:1249–1287
Keywords Argentina Botanic gardens Chile Cactaceae Copiapoa Eriosyce

Eulychnia Ex situ conservation In situ conservation Peru Threatened
plant species
Introduction
Cacti and succulent plants, like orchids, exert a powerful attraction to collectors (e.g.
Oldfield 1997; Walter 2011). As a consequence, wild populations suffer much from illegal
harvest and trade by amateur and professional collectors despite being included in
Appendix I or II of the CITES species index (UNEP-WCMC 2011). Sadly, this is only one
of the threats faced by many Cactaceae species today. In total, about one in five of the
world’s plant species are facing extinction because of, e.g. habitat destruction, the spread
of invasive alien species, pollution and climate change (GSPC 2012).
The in situ conservation of habitats containing high species richness (e.g. in national
parks and other protected areas) undoubtedly deserves top priority since conserving natural
communities and their complex relationships allows species to continue adapting and
evolving (e.g. McNaughton 1989; Glowka et al. 1994; Guerrant et al. 2004a). However, for
a number of species, in situ conservation alone may not be sufficient to safeguard them
from extinction (e.g. Cochrane 2004; Swarts and Dixon 2009; Seaton et al. 2010). This can
be due to environment alterations caused by changes in land use, road construction, mining
and energy projects, to the unwillingness of local stakeholders to actively protect biodi-
verse areas, and/or to climate change.
Many Chilean cactus species are narrow endemics and occur in regions suffering strong
environmental impacts. Their distribution area happens to be one of the world’s most richly
endowed territories in terms of copper–molybdenum porphyric deposits, amongst many
other minerals, which have been exploited by a steadily growing mining industry since the
1980s (e.g. Oyarzun and Oyarzun 2011). Between 2006 and 2011, the Chilean mining
industry accounted for 16.4 % of the country’s GDP, generated 64.3 % of total exports and
contributed 23.4 % of total tax revenue (SONAMI 2012).
Central Chile is recognised as one of the world’s biodiversity hotspots according to
Myers et al. (2000). This area, called the ‘Chilean Winter Rainfall–Valdivian Forests’, is
characterised by a high degree of endemism due to its position at the edge of the Neo-
tropical floristic region, and its extraordinary range of habitats combined with its geo-
graphic isolation from the rest of South America by the Andes and the desert in northern
Chile and southern Peru (Arroyo et al. 1996; Villagrán and Hinojosa 1997; Armesto et al.
1998). The Chilean biodiversity hotspot is home to ca. 3,900 native plant species, of which
50.3 % are restricted in distribution to the hotspot (Arroyo et al. 2004). As defined in
Arroyo et al. (2004), this hotspot extends in Chile from the Pacific coast to the peaks of the
Andes between 25° and 47°S, in addition to a narrow coastal strip between 19° and 25°S,
as well as the islands of San Félix and San Ambrosio and the Juan Fernández Islands. It
also includes a small area of forest on the western edge of Argentina. The hotspot covers
397,142 km2 and encompasses about 40 % of Chile’s land area (Conservation Interna-
tional: http://www.conservation.org/). Vegetation types in the more northerly area include
coastal fog (camanchaca) desert and the more southerly inland desierto florido. Other
vegetation types include coastal and inland matorral and savannas, deciduous forests,
coastal rainforest and high-elevation alpine vegetation (Arroyo et al. 2008).
123
Biodivers Conserv (2014) 23:1249–1287 1251
It is generally agreed that ex situ approaches should be complementary to and/or

supporting in situ conservation (e.g. Glowka et al. 1994; Guerrant et al. 2004a; Li and
Pritchard 2009). Especially for species occurring in areas that are strongly impacted by
socio-economic activities, ex situ conservation can offer valuable options (e.g. Cochrane
2004; Swarts and Dixon 2009). Botanical gardens can play a key role in conservation of
plant diversity (e.g. Swarts and Dixon 2009; Ali and Trivedi 2011), but only about 30 % of
globally threatened plant species are estimated to be held in living collections (Oldfield
2010). As stated in Target eight of the Global Strategy for Plant Conservation (GSPC
2012), by 2020, at least 75 % of threatened plant species should be present in ex situ
collections, preferably in their country of origin, and at least 20 % should be available for
recovery and restoration programmes. The ability to undertake such programmes and their
success depend on the knowledge of the wild origin of the collections as well as their
genetic representativeness (e.g. Rae 2011, Sharrock and Jones 2011). Unless they focus on
a specific plant group, the majority of botanic gardens only have one or a few accessions of
each species (Maunder et al. 2001; Kozlowski et al. 2012; Brütting et al. 2013). Besides the
usually small number of accessions available, many botanic garden collections lack suf-
ficient documentation (e.g. Maunder et al. 2001; Kozlowski et al. 2012; Brütting et al.
2013). Furthermore, although this is improving (Maunder et al. 2004), many ex situ col-
lections are still not specifically managed for conservation purposes, resulting in some
unfavourable genetic and demographic characteristics (Maunder and Culham 1997;
Maunder et al. 2004; Frankham 2008; Christie et al. 2012). This is corroborated by many
recent studies indicating that ex situ collections tend not to be genetically representative for
the species (e.g. Rucı́nska and Puchalski 2011; Hou et al. 2012; Brütting et al. 2013).
In the Status Survey and Conservation Action Plan for Cactus and Succulent Plants
(Oldfield 1997), eight priorities and strategies for future actions for successful/improved
ex situ conservation of succulents were presented. The present study focuses on the two
first priorities of this Action Plan: (1) Analyse existing ex situ collections and develop
and enhance databases to track them; and (2) Develop a strategy for the use of ex situ
collections of cacti and succulents for conservation; that is, to highlight priority species,
and then overlay these with ex situ collections enabling a clear identification of par-
ticular conservation needs. Oldfield (1997), citing Anderson et al. (1990), also rec-
ommended specific in situ conservation actions to be taken in Chile. Since then,
Chilean researchers have contributed significantly to the knowledge of Chile’s threa-
tened flora in some of the regions (e.g. Squeo et al. 2008a, b; CONAMA 2005, 2006;
SAG 2007).
This study fits in ‘A future for cacti?’, a collaborative project between Botanic Gardens
Conservation International (BGCI) and the Ghent University Botanical Garden & Research
Group Spermatophytes, and focuses on three mainly Chilean cactus genera, Copiapoa,
Eriosyce and Eulychnia of which some species are illustrated in Figs. 1 and 2. The project
is part of an initiative to measure the conservation value of ex situ collections in order to
inform and prioritize conservation action by assessing and comparing the genetic diversity
between ex situ collections and natural populations of selected taxa of three flagship plant
families, i.e. Cactaceae, Hydrangeaceae and Magnoliaceae (Samain and Cires 2012; Cires
et al. 2013).
In this paper, we aim to assemble and analyse data concerning the conservation status of
the abovementioned Cactaceae genera in Chile. These data include: (1) the conservation
status of the species of these genera, (2) the in situ and ex situ conservation measures for
these species in Argentina, Chile and Peru, and (3) a worldwide survey of living ex situ
collections of the species of these genera. This status report will inform the ongoing
123
Fig. 1 Diversity of Copiapoa and Eriosyce in Chile. a C. ahremephiana in Quebrada Botı́ja. b C. cinerea
subsp. columba-alba near Las Tórtolas. c C. cinerea subsp. haseltoniana north of Paposo. d C. krainziana in
Quebrada San Ramón. e C. fiedleriana near Totoral. f C. taltalensis subsp. taltalensis south of Taltal.
g E. aurata near Hurtado. h E. chilensis in Pichidangui. a, c, e–h Pictures taken by Isabel Larridon. b,
d Pictures taken by Marie-Stéphanie Samain
research studying the genetic diversity of living ex situ collections and natural populations
of these taxa, and forms a case study for the BGCI/IOS Cactus and Succulent Plant Survey,
a global ex situ survey of collections of all cacti and succulent taxa.
123
Fig. 2 E. breviflora east of

Totoral, Chile. Picture taken by
Isabel Larridon
Materials and methods
The classification of the genera, species and subspecies follows Hunt et al. (2006). The red
list (RL) category, distribution, estimation of extent of occurrence, threats and in situ
conservation areas for the species of Copiapoa, Eriosyce and Eulychnia occurring in
Argentina, Chile and Peru was recorded from the IUCN RL of threatened species (IUCN
2013, see also Tables 1, 2, 3). The RL categories used in this paper are according to the
IUCN (2012) criteria: critically endangered (CR), endangered (EN), vulnerable (VU), near
threatened (NT), and least concern (LC). The data from the IUCN RL of threatened species
(IUCN 2013) was supplemented by data from the ‘Species background files’ and/or
‘Species summary files’ (Fichas de antecedentes de especies or Fichas resumen de
especies) prepared by the Chilean Ministry of Environment (Ministerio del Medio Ambi-
ente (MMA), Gobierno de Chile, http://www.mma.gob.cl/clasificacionespecies/), and data
from Hoffmann and Walter (2004) and Hunt et al. (2006). Additions were made based on
observations in the field made by the authors Larridon, Samain and Cisternas in April 2013
(e.g. Fig. 3).
The specific ex situ conservation measures in Chile were extracted from the mentioned
species background/summary files prepared by the MMA, supplemented by data provided
by the Chilean co-author of this paper and through personal communication with Chilean
researchers. Information concerning the ex situ conservation of Argentinean and Peruvian
species was provided by Cactaceae specialists in these countries.
The survey of ex situ collections of all species of the genus Copiapoa, Eriosyce and
Eulychnia was undertaken by analysing data and information obtained through: (1) the
BGCI PlantSearch database (www.bgci.org/plant_search.php), and (2) direct contact with
botanic gardens holding important cactus collections. For the results presented in Tables 1,
2 and 3 and Figs. 4 and 5, a record/collection is the presence of a single living repre-
sentative of any taxon of Copiapoa, Eriosyce or Eulychnia within an institution and may
123
Table 1 Extant taxa of Copiapoa according to the classification of Hunt et al. (2006), their most common synonyms, distribution, extent of occurrence, RL category, threats
1254
for wild populations, in situ conservation (presence in protected areas in country of origin), and ex situ conservation (presence or absence in seed banks and living collections
in or outside country of origin)
123
Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation
occurrence
(estimation
in km2)
Available Available in Available in Available in
in seed seed bank living living
bank in outside collection in collection
country of country of country of outside
origin origin origin country of
origin
Copiapoa Chile, Region 82 CR Drought, collecting, herbivory None Y N Y Y

ahremephiana II (Coleoptera)
Copiapoa Chile, Region 2 CR Collecting, habitat loss and None N N Y N
angustiflora II degradation
[(re-)construction of roads],
herbivory (Coleoptera)
Copiapoa calderana Chile, Region 8,260 LC Collecting, habitat loss and None Y Y Y Y
subsp. calderana III degradation (urbanisation,
(C. lembckei) tourism, construction of
Copiapoa calderana Chile, Region industrial harbours) National Park Morro Y Y Y Y
subsp. atacamensis II Moreno; Natural
(C. boliviana) Reserve La Chimba;
Natural Monument
La Portada
Copiapoa Chile, Region 345 EN Herbivory (guanacos), National Park Pan de Y N Y Y
cinerascens III vandalism Azúcar
Table 1 continued

occurrence
(estimation
in km2)
origin
Copiapoa cinerea Chile, Region 4,550 LC Illegal collecting, habitat loss None N Y Y Y
subsp. cinerea II and degradation (off-road

(C. cinerea) vehicles, road construction)
Copiapoa cinerea Chile, Region National Park Pan de Y Y Y Y
subsp. columna- II and III Azúcar
alba
(C. melanohystrix)
Copiapoa cinerea Chile, Region None Y Y Y Y
subsp. haseltoniana II
(C. cinerea subsp.
gigantea,
C. eremophila)
Copiapoa Chile, Region 25,000 LC Drought (dam construction in National Park Fray N Y Y Y
coquimbana III and IV the Elqui and Huasco Jorge; National
(C. alticostata, Valleys), habitat loss and Reserve Pingüino de
C. pendulina, degradation (urbanisation, Humboldt
C. pepiniana, agriculture)
C. vallenarensis)
Copiapoa dealbata Chile, Region 500 LC Habitat loss and degradation National Park Llanos N Y Y Y
(C. carrizalensis, III (off-road vehicles, road de Challe
C. malletiana) construction)
Copiapoa decorticans Chile, Region 30 CR Drought, illegal collecting None N N Y N
II (young plants), habitat loss
and degradation (mining)
1255
123
Table 1 continued
1256

occurrence
123
(estimation
in km2)
origin
Copiapoa echinoides Chile, Region 2,500 NT Habitat loss and degradation National Park Llanos Y Y Y Y
(C. bridgesii, III (widening of roads) de Challe
C. cuprea, C. dura)
Copiapoa Chile, Region 35 CR Illegal collecting, herbivory National Park Pan de N N Y Y
esmeraldana II (guanacos), erosion Azúcar
(C. humilis var.
esmeraldana)
Copiapoa fiedleriana Chile, Region 800 EN Habitat loss and degradation National Park Llanos Y Y Y Y
III (urbanisation, off-road de Challe
vehicles, industry)
Copiapoa grandiflora Chile, Region 305 EN Illegal collecting (young National Park Pan de Y Y Y Y
II and III plants), habitat loss and Azúcar
degradation (road
construction)
Table 1 continued

occurrence
(estimation
in km2)
origin
Copiapoa humilis Chile, Region 24,000 NT Drought, illegal collecting, National Reserve N Y Y Y
subsp. humilis III habitat loss and degradation Paposo

(C. chaniaralensis, (mining, road construction),
C. longispina) herbivory (goats)
Copiapoa humilis Chile, Region N N Y Y
subsp. tenuissima II
subsp. tocopillana II
subsp. variispinata II
Copiapoa hypogaea Chile, Region 700 EN Illegal collecting, herbivory National Park Pan de N N Y Y
subsp. hypogaea II and III (guanacos) Azúcar
Copiapoa hypogaea Chile, Region N Y Y Y
subsp. laui II and III
Copiapoa krainziana Chile, Region 60 LC Illegal collecting None N Y Y Y
II
Copiapoa Chile, Region 192 LC Illegal collecting, habitat loss National Park Pan de Y Y Y Y
longistaminea II and degradation (road (re-) Azúcar
construction)
Copiapoa marginata Chile, Region 5,000 NT Drought (climate change), National Park Pan de N Y Y Y
(C. streptocaulon) III illegal collecting Azúcar
1257
123
Table 1 continued
1258

occurrence
123
(estimation
in km2)
origin
Copiapoa megarhiza Chile, Region 6,000 VU Drought (climate change), None Y N Y Y

subsp. megarhiza III llegal collecting, habitat loss
Copiapoa megarhiza and degradation N N N Y
subsp. echinata (urbanisation, road
(C. totoralensis) construction, industry,
landfills)
Copiapoa montana Chile, Region 1,550 LC Illegal collecting None N N Y Y
(C. mollicula) II and III
Copiapoa Chile, Region 75 EN Drought, illegal collecting, National Park Pan de N N Y Y
serpentisulcata II and III habitat loss and degradation Azúcar
(tourism)
Copiapoa solaris Chile, Region 1,550 EN Drought (climate change), None Y Y Y Y
II habitat loss and degradation
(mining)
Copiapoa taltalensis Chile, Region 700 EN Drought (climate change), None N Y Y Y
subsp. taltalensis II herbivory (guanacos),
(C. aphanes, vandalism
C. rubriflora,
C. rupestris)
Copiapoa taltalensis N N Y Y
subsp. desertorum
include multiple accessions and/or individuals. For the results presented in Figs. 6 and 7,
the data is based on separate accession information provided by the botanic gardens. All of
BGCI’s institutional members, as well as the wider botanic garden community, were
invited to contribute to the survey, which was promoted through BGCI’s website (www.
bgci.org). Records from two public Chilean botanic gardens were included in this study:
(1) the Jardı́n Botánico Nacional in Viña del Mar (data available via the PlantSearch tool,
supplemented by data provided by the garden), and (2) the Jardı́n Botánico Aguas Anto-
fagasta (garden not associated with BGCI, data gathered during own visit). Data from the
seed bank held by the Instituto de Investigaciones Agropecuarias (INIA) was provided by
A. C. Sandoval of the INIA seed bank in Vicuña, Coquimbo Region, Chile. Also, data was
included of the EXSIS Project: Ex-situ and in situ Cactaceae Conservation Project, San-
tiago, Chile (H. E. Walter pers. comm.).
The type locality or area of major abundance of each of the species studied in Chile as
well as the protected natural areas were mapped with Quantum GIS version 1.7.0 Wroclaw
(QGIS Development Team 2010) with the projection WGS84/Pseudo Mercator, using the
Google Physical 2013 base map (Fig. 8). Type localities from rare species were retrieved
from protologues or other publications and subsequently georeferenced, whereas areas of
major abundance for more common species were derived from a data set of collection
localities and the mentioned species background/summary files prepared by the MMA. The
polygons of the protected areas were taken from the maps of the project GEF ‘‘Creación de
un Sistema Nacional Integral de Áreas Protegidas para Chile: estructura financiera y op-
eracional’’ or GEF-SNAP (http://www.proyectogefareasprotegidas.cl/recursos/mapas/).
Results
In situ and ex situ conservation status of Copiapoa
Copiapoa is endemic to Chile, and more specifically to its three most northerly regions
(Tarapacá, Antofagasta and Atacama), except one species, i.e. C. coquimbana, of which
the distribution range extends southwards into the north of Región IV (Coquimbo)
(Table 1). The genus is particularly species rich in the area around Paposo and Taltal
(between ca. 24° and 25°S), and in and around the national parks of Pan de Azúcar and
Llanos de Challe. Except at the time of the desierto florido, populations of Copiapoa are
often the only obvious plants seen in these areas. Hunt et al. (2006) recognised 21
Copiapoa species encompassing a total of 30 separate taxa (Table 1). In 2006, one addi-
tional species was described, i.e. Copiapoa angustiflora (Walter and Mächler 2006). The
species are either solitary (Fig. 1b, f) or form (large) clusters (Fig. 1a, d, e) and usually
have yellow flowers (Fig. 1a, c). A molecular study focusing on species delimitation and
phylogenetic relationships in Copiapoa is ongoing at the Ghent University Research Group
Spermatophytes.
Of the 22 Copiapoa species (Table 1), four are listed as CR, seven as EN, one as VU,
three as NT, and seven as LC. Threats to the continued survival of the natural populations
of Copiapoa include: drought; illegal collecting; habitat loss and degradation due to
agriculture, urbanisation, road construction and reconstruction, mining and industry; her-
bivory by invertebrates, guanacos and livestock; and vandalism.
Thirteen Copiapoa species have populations that occur in national parks, national
reserves, and/or natural monuments, while eight species are not protected in situ. A last
species, C. humilis is listed as occurring in the ‘‘Paposo National Reserve’’ (Guerrero et al.
123
Table 2 Extant taxa of Eriosyce according to the classification of Hunt et al. (2006), their most common synonyms, distribution, extent of occurrence, RL category, threats
1260
123
occurrence
(estimation
in km2)
Available Available Available Available
in seed in seed in living in living
bank in bank collection collection
country of outside in country outside
origin country of of origin country of
origin origin
Eriosyce aspillagae Chile, Region 3,000 EN Illegal collecting, None Y Y Y Y

VI and VII habitat loss and
degradation
(urbanisation,
road
construction,
livestock
ranching)
Eriosyce aurata Chile, Region Very wide LC Illegal collecting, National Park Fray Jorge; Y Y Y Y
(E. ceratistes, III–V and range vandalism National Reserve Las
E. ihotzkyanae, Metropolitana Chinchillas; Nature
E. lapampaensis, Sactuary Serranı́a el Ciprés,
E. sandillon, Compañı́a de Tabaco
E. spinibarbis)
Eriosyce bulbocalyx Argentina, La ? LC None National Park Sierra de las N Y Y Y
Rioja, San Quijadas; Provincial Park
Juan and San Valle Fértil
Luis
Provinces
Eriosyce calderana Chile, Region 1,400 EN Illegal collecting None N Y Y Y
III
Table 2 continued

occurrence
(estimation
in km2)
origin origin
Eriosyce chilensis Chile, Region 45 CR Illegal collecting None Y Y Y Y

IV and V
Eriosyce confinis Chile, Region 2,500 VU Drought (climate None N Y Y N
III change), illegal
collecting
Eriosyce crispa subsp. Chile, Region 2,400 EN Illegal collecting, National Park Llanos de Y Y Y Y
crispa III habitat loss and Challe
Eriosyce crispa subsp. degradation N N Y Y
totoralensis (agro-industry,
mining,
urbanisation)
Eriosyce curvispina Chile, Region Wide range LC Illegal collecting, National Park Fray Y Y Y Y
subsp. curvispina IV, V and habitat loss and Jorge, La Campana, Roblerı́a
(E. curvispina var. Metropolitana degradation de Loncha; National
tuberisulcata) (agriculture, Reserve Las Chinchillas,
Eriosyce curvispina Chile, Region mining, Lago Peñuelas, Rı́o Y Y Y Y
subsp. armata VI arbanisation, Clarillo; Nature Sactuary
(E. limariensis) desertification) Yerba Loca; Natural
Monument
Eriosyce curvispina Chile, Region El Morado N N Y Y
subsp. marksiana V–VII
Eriosyce engleri Chile, Region 1,000 LC None None Y Y Y Y
Metropolitana
1261
123
Table 2 continued
1262

occurrence
123
(estimation
in km2)
origin origin
Eriosyce eriosyzoides Chile, Region Wide range LC Illegal collecting National Park Llanos de Y Y Y Y
subsp. eriosyzoides III and IV Challe
(E. kunzei)
Eriosyce eriosyzoides Chile, Region Y Y Y Y
subsp. atroviridis III
Eriosyce esmeraldana Chile, Region \100 EN Illegal collecting, National Park Pan de Azúcar N Y Y Y
II habitat loss and
degradation
(road
construction),
herbivory
(guanacos)
Eriosyce garaventae Chile, Region 20 LC None National Park La Campana Y Y Y Y
V
Eriosyce heinrichiana Chile, Region 16,000 LC Illegal collecting, National Park Fray Jorge Y Y Y Y
III and IV habitat loss and
degradation
(mining,
agriculture)
Eriosyce iquiquensis Chile, Region I 3,000 EN Drought (climate None N N Y Y
change), illegal
collecting
Table 2 continued

occurrence
(estimation
in km2)
origin origin
Eriosyce islayensis subsp. Chile, Region I; Chile: NT Drought (climate Reservation Zone San N Y Y (Chile, N
islayensis Peru, Ica, extinct? change), habitat Fernando (Peru) Peru)

Eriosyce islayensis subsp. Arequipa, Peru: ? loss and N N N N
grandis Moquegua degredation
and Tacna (urbanisation,
Eriosyce islayensis subsp. Provinces recreational N N N Y
omasensis areas)
Eriosyce laui Chile, Region \100 CR Illegal collecting, None N N Y Y
II habitat loss and
degradation
(future mining)
Eriosyce megliolii Argentina, San Small range LC None Provincial Park Valle Fértil N N Y N
Juan Province
1263
123
Table 2 continued
1264

occurrence
123
(estimation
in km2)
origin origin
Eriosyce napina subsp. Chile, Region \10,000 VU Illegal collecting, National Park Llanos de Y Y Y Y
napina III herbivory Challe
Eriosyce napina subsp. (guanacos) N Y Y Y
aerocarpa
Eriosyce napina subsp. N Y Y Y
glabrescens
Eriosyce napina subsp. Y Y Y Y
lembckei (E. napina
subsp. duripulpa)
Eriosyce napina subsp. N Y Y Y
tenebrica
Eriosyce occulta Chile, Region 190 EN Illegal collecting, None Y Y Y Y
II habitat loss and
degradation
(road (re-)
construction)
Eriosyce odieri subsp. Chile, Region \10,000 VU Illegal collecting National Park Pan de Azúcar Y Y Y Y
odieri III
Eriosyce odieri subsp. Y Y Y Y
krausii
Table 2 continued

occurrence
(estimation
in km2)
origin origin
Eriosyce paucicostata Chile, Region 11,000 LC None None N Y Y Y

subsp. paucicostata II
Ferryman
Eriosyce paucicostata N Y Y Y
subsp. echinus
Eriosyce paucicostata N N Y Y
subsp. floccosa
Eriosyce recondita Chile, Region Known VU Illegal collecting National Park Morro Moreno; N Y Y Y
II from 2 Natural Reserve La Chimba
localities
Eriosyce rodentiophila Chile, Region 5,000 VU Illegal collecting National Park Pan de Azúcar N Y Y Y
(E. megacarpa) II and III (mature plants,
seeds)
Eriosyce senilis subsp. Chile, Region 16,000 VU Illegal collecting, National Reserve Las Y Y Y Y
senilis IV habitat loss and Chinchillas
Eriosyce senilis subsp. Chile, Region degradation Y Y Y Y
coimasensis IV, V and (agriculture,
Metropolitana urbanisation)
Eriosyce simulans Chile, Region 74 EN Illegal collecting, None Y Y Y Y
IV habitat loss and
degradation
(mining)
1265
123
Table 2 continued
1266

occurrence
123
(estimation
in km2)
origin origin
Eriosyce sociabilis Chile, Region ? EN Drought (climate None Y Y Y Y

III change), illegal
collecting
Eriosyce strausiana Argentina, La Wide range LC Habitat loss and Provincial Reserve N Y Y Y
subsp. strausiana Pampa, degradation Divisadero Largo,
Mendoza, (agriculture) Villavicencio, Payunia
Neuquen and
Rı́o Negro
Provinces
Eriosyce strausiana Argentina, N N N Y
subsp. pachacoensis Mendoza and
San Juan
Provinces
Table 2 continued

occurrence
(estimation
in km2)
origin origin
Eriosyce subgibbosa Chile, Region Wide range LC Illegal collecting, National Park Fray Jorge Y Y Y Y
subsp. subgibbosa IV–VIII habitat loss and

(E. subgibbosa subsp. degradation
nigrihorrida, (urbanisation in
E. subgibbosa var. tourism areas)
castanea, E. subgibbosa
var. litoralis
Eriosyce subgibbosa Chile, Region Y Y Y Y
subsp. clavata IV
subsp. vallenarensis III
subsp. wagenknechtii IV
Eriosyce taltalensis subsp. Chile, Region Wide range VU Illegal collecting National Park Pan de Azúcar N Y Y Y
taltalensis II
Eriosyce taltalensis subsp. Chile, Region N Y Y Y
pygmaea III
Eriosyce umadeave Argentina, 1,300 EN Illegal collecting None N N N Y
Salta and
Jujuy
Provinces
1267
123
Table 2 continued
1268

occurrence
123
(estimation
in km2)
origin origin
Eriosyce villicumensis Argentina, San 500 LC Localised habitat None N Y N Y

Juan Province loss and
degradation
(quarrying)
Eriosyce villosa Chile, Region 5,000 LC Illegal collecting, National Park Llanos de Y Y Y Y
III habitat loss and Challe
degradation
(industry)
Taxa endemic to Argentina and Peru are indicated in underlined font. Remark Eriosyce islayensis subsp. islayensis occurs both in Chile and Peru
Table 3 Extant taxa of Eulychnia according to the classification of Hunt et al. (2006), their most common synonyms, distribution, extent of occurrence, RL category, threats
occurrence
(estimation
in km2)
Available in Available in Available in Available in
seed bank in seed bank living living
country of outside collection in collection
origin country of country of outside country
origin origin of origin
Eulychnia acida Chile, Wide range LC Habitat loss and National Park Fray Y Y Y Y
Region degradation (agro- Jorge; National
III and IV industry), Reserve Las
herbivory (goats) Chinchillas
Eulychnia breviflora Chile, 25,000 LC No major threats National Park Llanos Y Y Y Y
(E. longispina, Region de Challe
E. saint-pieana) III and IV
Eulychnia castanea Chile, 5,000 LC Habitat loss National Park Fray Y Y Y Y
Region (urbanisation in Jorge
IV and V tourism areas,
eolic parks)
Eulychnia iquiquensis Chile, 2,000 LC High mortality rates National Park Morro N Y Y Y
subsp. iquiquensis Region I– north of Moreno, Pan de
(E. aricensis, III Antofagasta Azúcar; Natural
E. morromorenoensis) fragment the Reserve La
subpopulations. Chimba
Eulychnia iquiquensis Peru, LC Drought None N N N Y
subsp. ritteri Arequipa
Province
The taxon from Peru is indicated in underlined font
1269
123
2013c). As part of a project to conserve the genetic diversity of the threatened endemic
Chilean flora focussing on the desert and Mediterranean zones, seeds of 11 taxa were
collected and stored by the INIA in Chile (León-Lobos et al. 2008; A. C. Sandoval pers.
comm.). From all but three of these 11 taxa (i.e. C. ahremephiana, C. cinerascens,
C. megarhiza subsp. megarhiza), seeds are also available in one or more seeds banks
outside Chile (BGCI, PlantSearch database 2013). In these foreign seed banks, seeds of a
further seven taxa are present as well (Table 1).
The survey of botanic garden collections shows that all Copiapoa taxa are currently held
in living collections by botanic gardens. In total, 992 records from 98 institutions in 31
countries were identified (BGCI, PlantSearch database 2013). Figure 4a reveals that the
United States of America, Germany and the United Kingdom are the countries with the
highest percentage of botanic gardens holding ex situ collections of the genus Copiapoa.
These three nations contain almost 50 % of all botanic gardens with living Copiapoa
collections, and over 50 % of all Copiapoa ex situ collections worldwide (Fig. 5a). Other
countries with sizable ex situ collections are Chile, France, the Netherlands, Slovakia and
Switzerland.
Thirty of the 31 accepted Copiapoa taxa are present in living collections in Chile
(Fig. 6a), whereas C. megarhiza subsp. echinata is not. Two of the four CR Copiapoa
species (IUCN 2013) are only represented in the EXSIS project collection (H. E. Walter
pers. comm.).
In situ and ex situ conservation status of Eriosyce
Hunt et al. (2006) recognised 51 separate taxa representing 32 species in Eriosyce

(Table 2). Most species of the genus are endemic to central and northern Chile (27 spe-
cies), with five species occurring in neighbouring Argentina and one species in both
northern Chile and southern Peru (Table 2). The plants are usually (sub)globose and often
solitary (Fig. 1g), more seldom forming small clusters (Fig. 1h), with yellow to red,
sometimes pink or whitish flowers. They tend to prefer more rocky and shaded habitats
than most Copiapoa species.
In Argentina, researchers use a different classification for the taxa included in Eriosyce
by authors as Kattermann (1994), Anderson (2001), Hoffmann and Walter (2004) and Hunt
et al. (2006). In the Catálogo de las Plantas Vasculares del Cono Sur (1997–2013), only
Eriosyce aurata and E. rodentiophila are recognised in Eriosyce. This while most other
species, including the Argentinean species, are placed in Pyrrhocactus since they are
morphologically very different from the type species of Eriosyce, i.e. E. sandillon
(accepted name E. aurata) (R. Kiesling pers. comm.). The genus Islaya is also recognised.
Additionally, some confusion exists in the information provided by the Chilean Ministry
of Environment (see Materials and methods), where some of the species were included into
Islaya, Neoporteria and Pyrrhocactus, but with ambiguous generic boundaries. Clearly, there
is no consensus about the generic circumscription of Eriosyce indicating the need for a
classification based on molecular phylogenetic data. A preliminary study based on chloro-
plast DNA including species of Eriosyce section Neoporteria was published recently
(Guerrero et al. 2011). However, further research is needed encompassing all species in this
group, and preferably also with a wide sampling of the related genera. A molecular phylo-
genetic hypothesis of Eriosyce is in preparation at the Universidad de Chile, Santiago (Chile).
Two Eriosyce species are categorised as CR, nine as EN, seven as VU, one as NT, and
thirteen as LC (Table 2). Also, E. islayensis subsp. islayensis is believed to be extinct in
the wild in Chile (Cáceres et al. 2013a; H. E. Walter pers. comm.). As with Copiapoa,
123
Fig. 3 C. solaris near El Cobre, Chile. a Picture taken by Isabel Larridon. b, c Pictures taken by Marie-
Stéphanie Samain
123
Fig. 4 Worldwide distribution of the botanic gardens surveyed holding Copiapoa, Eriosyce and Eulychnia c
ex situ collections. a Percentage of botanic gardens per country possessing living Copiapoa ex situ
collection(s). b Percentage of botanic gardens per country possessing living Eriosyce ex situ collection(s).
c Percentage of botanic gardens per country possessing living Eulychnia ex situ collection(s). Countries of
origin are in bold
threats to the continued survival of the natural populations of Eriosyce include drought,
illegal collecting, habitat loss and degradation due to human impacts. Some species also
suffer from herbivory by guanacos and/or livestock.
Of the 27 species occurring in Chile, fifteen have populations that occur in protected
areas. Three of the five Argentinean Eriosyce species occur in protected areas. E. islay-
ensis, a species found both in Chile and Peru, occurs in a protected area in Peru. Seeds of
25 Chilean Eriosyce taxa were collected and stored in the INIA seed bank (A. C. Sandoval
pers. comm.). Seed banks outside the countries of origin store a total of 41 of the 51
recognised Eriosyce taxa (BGCI, PlantSearch database 2013) (Table 2). These 41 taxa
represent the 25 Chilean taxa also present in the INIA seed bank, and a further 13 Chilean
and three Argentinean taxa.
All Eriosyce species are currently held in living collections by botanic gardens. In total,
510 records from 52 institutions in 24 countries were identified (BGCI, PlantSearch
database 2013). Figure 4b reveals that the United States of America, Germany and Chile
are the countries with the most botanic gardens holding living ex situ collections of the
genus Eriosyce. These three nations contain 40 % of all botanic gardens with living
Eriosyce collections. The distribution of the number of collections held is slightly different,
with most collections present in the United States of America, the United Kingdom and
Chile. These four countries hold just under 60 % of all living Eriosyce collections
worldwide (Fig. 5b).
Forty-two of the 51 Eriosyce taxa recognised by Hunt et al. (2006) are present in living
ex situ collections in Chile (Fig. 6b). They represent all Chilean taxa (Table 2). Most of
these taxa are only present in the EXSIS project collection (H. E. Walter pers. comm.).
There are no Argentinean gardens that have provided collection information to BGCI’s
PlantSearch database and through personal communication with the gardens it has been
ascertained that most of these gardens do not hold the native Eriosyce species in their
collections. The largest cactus collection in Argentina is the privately held Ferrari col-
lection in Buenos Aires (http://www.cactusferrari.com.ar/), which includes many Argen-
tinean cactus species. Concerning the studied genera, this collection holds C. humilis
subsp. humilis and subsp. tenuissima, C. hypogaea subsp. hypogaea and C. montana, as
well as E. bulbocalyx, E. napina subsp. napina and E. occulta. At least two other species
are present in living ex situ collections in Argentina, i.e. E. megliolii and E. strausiana (R.
Kiesling pers. comm.).
Eriosyce islayensis subsp. islayensis is available in living collections in both its
countries of origin (Chile and Peru). E. islayensis subsp. omasensis is also present in a
living collection in Peru (G. Pino Infante pers. comm.). Concerning the occurrence in
living collections of the third subspecies of E. islayensis (i.e. subspecies grandis), no
information is available.
In situ and ex situ conservation status of Eulychnia
Eulychnia species fit the iconic image of large tree-like cacti (Fig. 2). They occur mostly in
the coastal zones of Chile’s northern deserts that are influenced by camanchaca. Their
123
123
123
b Fig. 5 Worldwide distribution of living Copiapoa, Eriosyce and Eulychnia ex situ collections surveyed.
a Percentage of living Copiapoa ex situ collections per country. b Percentage of living Eriosyce ex situ
collections per country. c Percentage of living Eulychnia ex situ collections per country. Countries of origin
are in bold
flowers are white to pinkish. Hunt et al. (2006) recognised four Eulychnia species with a
total of five separate taxa (Table 3). In Chile, they are found from Region I to V. Only one
taxon occurs outside Chile (i.e. E. iquiquensis subsp. ritteri in southern Peru). Since the
publication of Hunt et al. (2006), three Eulychnia taxa have been recognised at species
level, i.e. E. chorosensis and E. taltalensis by Hoxey and Klaassen in 2011, and Charles
et al. in 2013 recognised the Peruvian subspecies as a separate species (E. ritteri). How-
ever, conservation assessments are not yet available for these recently recognised species.
Also, to date, a molecular phylogenetic hypothesis of Eulychnia is lacking. As a conse-
quence, species delimitation and relationships in Eulychnia are still under discussion.
All four Eulychnia species are assessed as of LC (IUCN 2013), although Eulychnia
iquiquensis shows a high level of largely unexplained mortality (e.g. Pinto 2007). Popu-
lations of all four Chilean Eulychnia taxa occur in protected areas (Table 3). The INIA
seed bank stores seeds of three of the four Chilean Eulychnia species (A. C. Sandoval pers.
comm.), and seeds of all Chilean taxa are stored in seed banks outside the country of origin
(BGCI, PlantSearch database 2013) (Table 3). The Peruvian species is not protected
in situ, nor is it present in a seed bank.
All Eulychnia taxa are currently held in living collections by botanic gardens (Table 3).
In total, 148 records from 54 institutions in 18 countries were identified (BGCI, Plant-
Search database 2013). Figure 4c reveals that Germany, the United States of America and
the United Kingdom are the countries with the highest percentage of botanic gardens
holding ex situ collections of the genus Eulychnia. These three nations contain more than
50 % of all botanic gardens with living Eulychnia collections, and 55 % of all Eulychnia
ex situ collections worldwide (Fig. 5c). Other countries with sizable living collections of
Eulychnia are Chile, Belgium, France and Switzerland. The four endemic Eulychnia
species recognised in Hunt et al. (2006) are present in living collections in Chile (Fig. 6c).
No records of the endemic Peruvian Eulychnia species were found in Peruvian botanic
gardens (G. Pino Infante pers. comm.).
Botanic garden accessions: quantity and quality
For the data of the Chilean botanic gardens, one collection corresponds to one accession.
Most taxa are represented by a small number of individuals (generally ca. 10 accessions,
Fig. 6). Little information is available about ex situ collections of E. bulbocalyx,
E. megliolii, E. strausiana, E. umadeave and E. villicumensis in Argentina, and of the
E. islayensis taxa as well as Eulychnia (iquiquensis subsp.) ritteri in Peru, although cer-
tainly none of these species is well-represented in botanical gardens in the country of origin
(G. Pino Infante pers. comm.)
Although the proportion of well-documented collections (detailed collecting data: e.g.
collector, collector’s number, detailed locality information, coordinates and elevation) is
relatively low, a sizable amount of the collections is of a known wild provenance (see
further). This information is not included in the PlantSearch database and was obtained
through direct contact with the botanic gardens. The response to our inquiry was relatively
good. We managed to obtain detailed information about the separate accessions from 54 %
of all Copiapoa collections, 66 % of all Eriosyce collections, and 64 % of all Eulychnia
123
Fig. 6 Number of living ex situ collections held in Chile. a Copiapoa, b Eriosyce, c Eulychnia
collections included in this study. A total of 1,353 accessions of Copiapoa, 887 accessions
of Eriosyce and 193 accessions of Eulychnia were included. For Copiapoa, the ratio of
known wild origin/horticultural or unknown origin is ca. 1/1, for Eriosyce this ratio is 3/1,
and for Eulychnia it is 3/2. Figure 7 shows the number of accessions according to their
origin.
123
Fig. 7 Number of ex situ collections by source of material. Dark grey collections of known wild origin.
Light grey collections of horticultural or unknown origin. a Copiapoa, b Eriosyce, c Eulychnia
Discussion
In situ and ex situ conservation of Copiapoa in Chile
About two thirds of the Copiapoa species (Table 1) have populations that occur in pro-
tected areas. In addition, two-thirds of the taxa are represented in seed banks in Chile
123
Fig. 8 Map indicating the protected natural areas and the type locality or area of major abundance of each
of the species studied in Chile
123
and/or abroad. Eleven species occur both in in situ protected areas, and are present in seed
banks and in living collections (i.e. C. calderana, C. cinerascens, C. cinerea, C. coquim-
bana, C. dealbata, C. echinoides, C. fiedleriana, C. grandiflora, C. hypogaea, C. longi-
staminea, and C. marginata). These 11 species can be seen as the currently best-protected
taxa. Two species occur in protected areas and are held in living collections (C. esmeral-
dana and C. serpentisulcata). Another six species lacking in situ protection are present in
both living collections and seed banks [C. ahremephiana (Fig. 1a), C. humilis, C. kra-
inziana (Fig. 1d), C. megarhiza, C. solaris (Fig. 3) and C. taltalensis (Fig. 1f)]. According
to Guerrero et al. (2013c), C. humilis is present in the ‘‘Paposo National Reserve’’.
However, although this area of high endemism including several Copiapoa, Eriosyce and
Eulychnia species is meant to become a national reserve (e.g. CONAMA 2005, 2006; SAG
2007), it is currently not effectively protected. Of the three remaining Copiapoa species,
two are only present in living collections inside Chile, and one is present in living col-
lections both in and outside its country of origin. Although conservation efforts should be
focussed on the taxa that are most at risk of extinction (e.g. Guerrant et al. 2004b; BGCI
2008; IUCN 2012, 2013), currently this is not the case for Copiapoa. For example, of the
11 species conserved both in situ and ex situ, only C. cinerascens, C. fiedleriana,
C. grandiflora and C. hypogaea are EN, the other seven species are categorised as NT or
LC (IUCN 2013). In contrast, of the four CR species, C. ahremephiana (Fig. 1a), C. an-
gustiflora, C. decorticans, and C. esmeraldana, only one is protected both in situ and ex
situ, one is present in a seed bank and in living collections both in and outside Chile, and
two are only held in the EXSIS project collection (H. E. Walter pers. comm.). Also, two of
the EN species are not present in in situ conservation areas (see Table 1 for details).
Recently, the new RL assessments were published for the Chilean cacti species (IUCN
2013). As is the case in this paper, the IUCN RL assessments are based on the classification of
Hunt et al. (2006). However, while we also treat the taxa that Hunt et al. (2006) placed at
subspecies level separately, this is not the case with the RL assessments. Because of this,
many taxa previously assessed as threatened (in e.g. Hoffmann and Walter 2004, as well as in
the assessments of the Chilean MMA) are lumped at species level resulting in the loss of
important information. Furthermore, based on recent field observations, the IUCN (2013) RL
assessments of a few species appear somewhat counterintuitive. This is the case for two
Copiapoa species, C. krainziana (Fig. 1d) and C. solaris (Fig. 3). C. krainziana is categorised
as LC (Saldivia et al. 2013), but this narrow endemic only has a very restricted area of natural
distribution in the cerros of the Quebrada San Ramón north of Taltal (ca. 60 km2, Saldivia
et al. 2013). Contrarily, other species with similar areas of distribution are categorised as
either CR or EN (Table 1). It is true that, in contrast to most other narrowly endemic species,
C. krainziana is abundantly present in its distribution area. However, the species is not
currently protected in situ and has high ornamental value for collectors. Moreover, its dis-
tribution area is well known, not at all inaccessible (in contrast to what is stated by Saldivia
et al. 2013), and close to an urbanised area undergoing both touristic and industrial devel-
opment. Therefore, although a species, which is abundant and not currently declining, cannot
be categorised as threatened according to the IUCN RL criteria, we suggest reassessing the
RL category of this species at regular intervals in order to ensure that any changes in its status
are noticed in time to prevent grave consequences. In earlier assessments, the species was
categorised as VU by Hoffmann and Walter (2004), and as CR by Guerrero et al. (2010).
In the IUCN (2013) RL assessments, C. solaris has been categorised as EN (Walter
et al. 2013). However, Muñoz and Serra (2006) provide reasons to class it as CR. Having
recently studied this species in situ, we would tend to agree with this higher category
assessment as nearly all individuals of this species in its entire distribution area are dying
123
because of desiccation caused by drought brought on by environmental alterations due to

mining and/or as a consequence of climate change (Fig. 3). Furthermore, a possible
phytopathological cause of the decreasing viability of this species is currently being
investigated in collaboration with the Universidad Católica de Valparaı́so in Quillota,
Chile. Again, this species is not protected in situ.
In situ and ex situ conservation of Eriosyce in Chile
A little over half of the Chilean Eriosyce species (Table 2) have populations that occur in
protected areas (E. aurata, E. crispa, E. curvispina, E. eriosyzoides, E. esmeraldana,
E. garaventae, E. heinrichiana, E. napina, E. odieri, E. recondita, E. rodentiophila,
E. senilis, E. subgibbosa, E. taltalensis, and E. villosa). These species are also present in
seed banks and present in living collections. Another species, E. aspillagae, could be added
to this list since it is more or less protected in situ because it occurs on the grounds of the
Hacienda Tanumé, a CONAF (Corporación Nacional Forestal of Chile ‘National Forestry
Cooperation’, Guerrero and León-Lobos 2010) forestry research centre, and is present in
seed banks and botanic garden collections. Another nine Chilean Eriosyce species are
included in both seed banks and garden collections, but do not occur in protected areas.
Two Chilean species only occur in living collections (E. iquiquensis and E. laui). As with
the Copiapoa species, the in situ and ex situ conservation efforts are not clearly focussed
on priority taxa for conservation based on the RL assessments. For example, E. laui one of
the species only occurring in living collections is categorised as CR. The other Eriosyce
species given CR status, i.e. E. chilensis, does occur in both seed banks and living col-
lections, but is not protected in situ despite being overcollected (Faundez et al. 2013) (see
Table 2 for details).
In situ and ex situ conservation of Eriosyce in Argentina
Of the five Argentinean Eriosyce species, two are present in in situ protected areas as well
as in seed banks and living collections; one is protected in situ and available in a living
collection in Argentina. The two other species only occur either in a seed bank or in living
collections outside its country of origin. Again, for the Argentinean species the conser-
vation efforts are not focussed on the most threatened taxa (see Table 2 for details), with
E. umadeave, the most threatened one (EN), being the species only available in living
collections outside Argentina.
In situ and ex situ conservation of Eriosyce in Peru
One species encompassing three subspecies occurs in Peru, i.e. E. islayensis subsp. is-
layensis, subsp. grandis and subsp. omasensis (see Table 2 for details). According to
Cáceres et al. (2013a), this species is present in the protected area of San Fernando in the
Ica Province. However, it is unclear which subspecies occurs in that area since this dis-
tribution does not concur with the distribution data of the subspecies as given by Hunt et al.
(2006). Also, the distribution area of E. islayensis subsp. omasensis (Lima Province) is not
listed in the IUCN RL assessment (Cáceres et al. 2013a). More detailed information on
these Peruvian taxa is needed.
123
In situ and ex situ conservation of Eulychnia in Chile and Peru
All Chilean Eulychnia taxa are included in both in situ and ex situ conservation. The
Peruvian taxon, Eulychnia (iquiquensis subsp.) ritteri (of which no separate IUCN status
assessment is available), is not present in any in situ conservation areas, and it is unclear
whether it is available in living collections in Peruvian botanic gardens. However, it is
present in living collections outside the country of origin (see Table 3 for details). Con-
sidered as a separate species, E. ritteri would probably receive in a higher RL classification
(Cáceres et al. 2013b).
Ex situ collections survey
For Copiapoa, Eriosyce and Eulychnia combined, nearly 50 % of all botanic gardens with
living collections, and nearly 55 % of all ex situ collections worldwide are held in the
United States of America, Germany and the United Kingdom. When looking at the pre-
sence of taxa in living collections, clear differences are noticeable between the three
genera. Copiapoa is better represented in botanic gardens, while a more limited number of
botanic gardens hold (smaller) collections of Eriosyce. Eulychnia, a genus of only four
species, is relatively well-represented in botanic gardens, although with generally only
very few individuals as they are quite large plants. The same pattern exists in the living
collections of these genera in the two public botanic gardens in Chile, where most
Copiapoa taxa and all Chilean Eulychnia taxa are present, compared to only 10 of the 27
Chilean Eriosyce species. However, in the EXSIS project collection, most endemic
Copiapoa taxa as well as all endemic Eriosyce and Eulychnia taxa are represented (H.E.
Walter pers. comm.). In general, the number of accessions in living collections, even of the
most commonly cultivated taxa, is too low to allow effective ex situ conservation of the
genetic diversity of these taxa. To conserve genetic diversity, ex situ collections should
consist of many different individuals from several populations (e.g. Walters 2004). Per
species, up to 50 individuals of up to 50 populations should be collected to capture
sufficient genetic variation (Brown and Marshall 1995; Guerrant et al. 2004b). Despite
other opinions (e.g., 15 individuals, Namoff et al. 2010), even of the most commonly
cultivated taxa included in this study, generally, an insufficient number of accessions of
known wild origin are available.
The ratios of known wild origin/horticultural or unknown origin are much higher for the
studied cactus genera than expected from the results of Kozlowski et al. (2012), where
generally only 20 % of collections of the tree genus Zelkova were of a known wild
provenance. This difference might be explained by the relatively high number of (amateur)
cactus enthusiasts travelling to South America who brought back collections that (even-
tually) ended up in botanic gardens, compared to the lower number of introductions of rare
tree species. The latter were often the result of a single individual or a handful of plants
brought to Europe by (professional) plant hunters.
Upscaling in situ conservation of Copiapoa, Eriosyce and Eulychnia in Chile
In Chile, the threats to this country’s remarkable biodiversity are currently recognized as
an environmental problem, and efforts are underway to protect more of the threatened
endemic flora. For example, Squeo et al. (2008a) focussed on the flora of the Atacama
Region and described clear priority sites for conservation in which 96 % of the threatened
and 82.5 % of all native species of that region would be protected. Similarly, for the
123
Paposo area in the Antofagasta Region, research was carried out at the Universidad de
Chile to study its fauna and flora, the threats they are exposed to, the possibilities of
protecting this zone and its management (CONAMA 2005, 2006; SAG 2007). However, to
this day only 1.8 % of the area of the Atacama Region is protected in national parks and
reserves, retaining only 51 % of the EN and VU species (Squeo et al. 2008b), and the
Paposo area was not yet included in the ‘National System of Protected Areas of the State’
(Sistema Nacional de Áreas Silvestres Protegidas del Estado—SNASPE, Fig. 8) as pro-
posed by conservation action plans such as Anderson et al. (1990), Oldfield (1997) and
Squeo et al. (1998). Figure 8 shows the protected areas in Chile. Here the type locality or
the area of major abundance of each of the Copiapoa, Eriosyce and Eulychnia species
occurring in Chile was mapped. The figure shows that although the protected areas are
defined to include as many species as possible, for most species their area of major
abundance is not inside a protected area. Also, many of the (critically) EN species do not
occur near/inside one of the protected areas.
Besides the fact that quite a number of (sub)species are not yet protected in situ, several
Eriosyce species have very low population estimates (i.e. E. calderana: 2,500 mature
individuals, E. occulta: \1,000 individuals and largest subpopulation with only 50 mature
plants, E. sociabilis: \250 mature individuals (Faundez et al. 2013); E. recondita: 1,000
individuals (Guerrero et al. 2013a); and E. taltalensis: ca. 700 mature individuals (Guerrero
et al. 2013b). More efforts should be taken to protect these taxa in situ, and include them
with priority in seed banks and possibly cultivation and restoration projects. Urgent
investigations are needed to confirm whether E. islayensis is indeed extinct in Chile as was
suggested (Cáceres et al. 2013a, H. E. Walter pers. comm.). If some individuals remain,
these should be protected, their genetic diversity secured and included in conservation and
recovery projects. For this action to be successful, more information is needed concerning
the remaining populations, and the genetic diversity and ecology of this species. Moreover,
for taxa like C. solaris and E. iquiquensis that show a high level of largely unexplained
mortality (e.g. this study, Pinto 2007), additional research is urgently needed in order to
stop populations from further decline.
Other species could also become threatened in the near future. Species with small
distribution areas (see Tables 1, 2, 3) like C. krainziana are especially VU to human impact
and climate change. As mentioned before, mining is economically very important for
Chile, and has an impact on large parts of the distribution area of the three studied genera.
Some legal instruments are already in place to limit the negative effects of mining and
other activities, e.g. like performing mandatory environmental impact studies prior to
starting the activities (Campos-Ortega and Jorquera-Jaramillo 2008). However, conflicts
still occur between ecological and economic interests. For example, according to Faundez
et al. (2013) there is a mining project planned in the near future that will affect the habitat
quality and quantity of 50 % of the population E. simulans, a species which has an
estimated extent of occurrence of only 74 km2. Furthermore, one of the most common
threats to the continued survival of the natural populations of cacti in the north of Chile is
drought. Desiccation of plants seems to results from droughts influenced by climate
change, but is aggravated by mining operations in the area since this industry uses a lot of
water in order to extract minerals from the bedrock (e.g. Acosta 2005; Dixon 2013).
Seawater desalination has recently been suggested as a less devastating supply of water for
the mining industry (Dixon 2013; Knops et al. 2013). Besides enforcing existing legal
instruments to ensure the protection of the threatened species, more compensation could be
sought from mining companies in particular to support conservation and recovery pro-
grammes in the areas that they affect. In addition, using the iconic endemic cacti as
123
flagship species for conservation in Chile could help engage the broader public for con-
servation actions. Without a strong conservation message, the mining companies may not
take in situ conservation and species protection seriously.
In general, the current areas for in situ conservation are insufficient to protect all taxa or
even the most threatened taxa (e.g. Squeo et al. 2008a; Fig. 8). The feasibility of in situ
conservation should be further investigated. The achievability of expanding the currently
protected areas, the potential of local research institutions, the balancing of various
interests in these areas, and the willingness of the government and local policy makers are
aspects that certainly will play a role. If expanding boundaries of current nature reserves is
not possible, an option could be managed relocation of populations of threatened species to
protected areas and reintroduction of species into restored habitats where the species
previously occurred. In Mexico, some research has been performed concerning reintro-
duction of Mammillaria (Peters et al. 2008; Garcı́a-Rubio and Malda-Barrera 2010). In
order to allow successful population recovery and reintroductions in the future, information
on the genetic diversity (both phylogenetic data to assess species limits and allow iden-
tification by barcoding, and population genetic studies to inform conservation actions) and
ecology of the concerned species is urgently needed.
Upscaling ex situ conservation of Copiapoa, Eriosyce and Eulychnia
Although the statement of Guerrant et al. (2004a) ‘‘An effective ex situ conservation project
begins with the collection of a genetically appropriate and representative sample. Ulti-
mately, the conservation value of these samples will be realized, or not, in their natural
habitats. Ex situ samples are a means to an end, a tool for enhanced survival prospects in
the wild.’’ is definitely accurate in an ideal situation, there is a growing feeling that
returning species to the ‘wild’ may not always be possible and that the traditional
approaches to ex situ and in situ conservation are no longer valid (Volis and Blecher 2010,
S. Sharrock pers. comm.). Ex situ conservation may be more valuable in cases where the
‘natural’ areas for the species no longer occur. Whatever value is placed on ex situ
conservation compared to in situ conservation, given the limited size of the established ex
situ collections, additional efforts are needed to expand both the living and seed bank
collections. Therefore, well-documented accessions of wild origin should be brought
together in collections that are managed specifically with ex situ (and possible future
in situ) conservation in mind, preferably in Chile in the region of origin of the species in
localities like Arica or Iquique for the northern species, Antofagasta (e.g. in the Jardı́n
Botánico Aguas Antofagasta), Paposo or Taltal for the species occurring in this very
diverse sector, in national parks like Pan de Azúcar (e.g. at the CONAF office where now a
small cactus and succulent garden is maintained providing information to visitors) and
Llanos de Challe, and/or in the Jardı́n Botánico Nacional in Viña del Mar.
As is the case for in situ conservation, there is a need for public engagement. Botanic
gardens provide an ideal opportunity to reach out to the public through education and
awareness raising campaigns. Another conservation action where botanic gardens can play
a key role is propagation of rare plants to satisfy the demands of plant collectors. An
example can be found in International Succulent Introductions (ISI), a plant distribution
program of the Huntington Botanical Gardens, California (USA) which aims to propagate
and distribute new or rare succulents to collectors, nurseries and institutions in keeping
with conservation practices without causing harm to wild populations. Similar programs
exist in the Botanical Garden of the National Autonomous University of Mexico (UNAM)
where not only rare cacti are being propagated and sold with a certificate to garden visitors,
123
but staff members are also involved in in situ conservation of several species in cooper-
ation with indigenous people near the threatened localities, e.g. Mammillaria hernandezii
(J. Reyes Santiago, pers. comm.). Also, attention should be given to private collections that
sometimes hold a large amount of well curated and documented plants of known wild
origin. Independent of their sometimes dubious legality, the already existing collections
should be preserved. Where possible, they should be integrated into a recognised botanic
garden so they can be managed according to international regulations and provide a source
of information and plant material for future conservation actions.
Integrating in situ and ex situ conservation of Copiapoa, Eriosyce and Eulychnia
The currently existing in situ protected areas and the ex situ collections are for long-term
preservation of the (genetic) diversity of the species of Copiapoa, Eriosyce and Eulychnia.
Further local and international efforts are needed to protect the plants in situ against further
habitat loss, and to build up ex situ collections (both living and seed bank collections) that
conserve a sufficient amount of genetic diversity. Additional research is needed in order to
come to an integrated approach that efficiently uses both in situ and ex situ conservation
actions to safeguard the species of Copiapoa, Eriosyce and Eulychnia. Currently, within
the research project ‘A future for cacti?’ mentioned above, the genetic diversity present in
living ex situ collections and wild populations of ca. 10 species of Copiapoa, Eriosyce and
Eulychnia is being assessed and compared using different molecular techniques (e.g. DNA
barcoding, microsatellites, RAD-sequencing) to guide both in situ and ex situ conservation
actions. Also, additional efforts should be undertaken to disseminate horticultural expertise
available in botanic gardens and private ex situ collections that have been cultivating
Copiapoa, Eriosyce and Eulychnia species for decades to support in situ conservation
project including reintroduction efforts.
Acknowledgments We are grateful to H. E. Walter, P. C. Guerrero and A. C. Sandoval (Chile), G. Pino

Infante, C. Ostolaza and F. Cáceres Huamani (Peru), as well as R. Kiesling (Argentina) for information
about Copiapoa, Eriosyce and Eulychnia species in their countries. We would also like to acknowledge J.
Reyes Santiago for providing information concerning cactus conservation at the Botanical Garden of the
Biology Institute of the National Autonomous University of Mexico. This work was supported by research
grants of the Special Research Fund (‘A future for cacti?’ postdoctoral research Grant no. B/13089/19, BOF,
Ghent University, Belgium) and the Department of Biology, Ghent University, Belgium. The field expe-
dition was financed by travel Grants of the Research Foundation—Flanders (FWO) and the Leopold III-
Fund and with support of the Department of Biology, Ghent University, Belgium. This study is part of the
project ‘‘PLAN(E)T, Plants for the future—A future for our planet’’ funded by the Fondation Franklinia
(Ghent University project number E/01394/01).
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Biodivers Conserv (2014) 23:1249–1287

Is there a future for the Cactaceae genera Copiapoa,

Isabel Larridon • Kirsty Shaw • Mauricio A. Cisternas •

Paul Goetghebeur • Marie-Stéphanie Samain

Received: 3 October 2013 / Revised: 6 February 2014 / Accepted: 25 February 2014 /

Communicated by Danna J Leaman.

I. Larridon (&) P. Goetghebeur M.-S. Samain

K. Shaw S. Sharrock S. Oldfield

A. Paizanni Guillén M.-S. Samain

Keywords Argentina Botanic gardens Chile Cactaceae Copiapoa Eriosyce

It is generally agreed that ex situ approaches should be complementary to and/or

Fig. 2 E. breviflora east of

Materials and methods

Copiapoa Chile, Region 82 CR Drought, collecting, herbivory None Y N Y Y

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

subsp. cinerea II and degradation (off-road

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

subsp. humilis III habitat loss and degradation Paposo

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Copiapoa megarhiza Chile, Region 6,000 VU Drought (climate change), None Y N Y Y

In situ and ex situ conservation status of Copiapoa

Eriosyce aspillagae Chile, Region 3,000 EN Illegal collecting, None Y Y Y Y

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Eriosyce chilensis Chile, Region 45 CR Illegal collecting None Y Y Y Y

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

islayensis Peru, Ica, extinct? change), habitat Fernando (Peru) Peru)

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Eriosyce paucicostata Chile, Region 11,000 LC None None N Y Y Y

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Eriosyce sociabilis Chile, Region ? EN Drought (climate None Y Y Y Y

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

subsp. subgibbosa IV–VIII habitat loss and

Taxon Distribution Extent of RL Threats In situ conservation Ex situ conservation

Eriosyce villicumensis Argentina, San 500 LC Localised habitat None N Y N Y

In situ and ex situ conservation status of Eriosyce

Hunt et al. (2006) recognised 51 separate taxa representing 32 species in Eriosyce

In situ and ex situ conservation status of Eulychnia

Botanic garden accessions: quantity and quality

In situ and ex situ conservation of Copiapoa in Chile

because of desiccation caused by drought brought on by environmental alterations due to

In situ and ex situ conservation of Eriosyce in Chile

In situ and ex situ conservation of Eriosyce in Argentina

In situ and ex situ conservation of Eriosyce in Peru

In situ and ex situ conservation of Eulychnia in Chile and Peru

Ex situ collections survey

Upscaling in situ conservation of Copiapoa, Eriosyce and Eulychnia in Chile

Upscaling ex situ conservation of Copiapoa, Eriosyce and Eulychnia

Integrating in situ and ex situ conservation of Copiapoa, Eriosyce and Eulychnia

Acknowledgments We are grateful to H. E. Walter, P. C. Guerrero and A. C. Sandoval (Chile), G. Pino

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