THE STATUS AND FUTURE OF
ORCHID CONSERVATION IN
NORTH AMERICA1
Gary A. Krupnick,2 Melissa K. McCormick,3
Thomas Mirenda,4 and Dennis F. Whigham3
ABSTRACT
The status and trends of issues related to the conservation of orchids native to the United States, Canada, and Greenland are
considered. We focus on nine of the 16 Targets of the Global Strategy for Plant Conservation (GSPC). The first two targets, which
all other targets rely upon, appear to have been adequately achieved, in addition to Target 11. Limited progress has been made
on six other GSPC targets. Three case studies of efforts to conserve the native threatened orchids, Platanthera leucophaea (Nutt.)
Lindl., Isotria medeoloides (Pursh) Raf., and Tolumnia bahamensis (Nash) Braem, are presented to demonstrate the difficulties as
well as the issues associated with effective conservation. We describe our efforts to establish an international program to
conserve all native orchids in the United States and Canada. The North American Orchid Conservation Center (NAOCC) is an
internationally focused effort that is based on public-private partnerships. The goal of NAOCC is to conserve the genetic
diversity of all native orchids through efforts to develop an international collection of seeds and orchid fungi. The NAOCC also
focuses on the cultivation of all native orchids in an international network of botanic gardens, and they partner with private and
public landowners to develop techniques to conserve and restore all native orchid species.
Key words: Endangered species, Global Strategy for Plant Conservation (GSPC), North American Orchid Conservation
Center (NAOCC), Orchidaceae, restoration.
Beautiful, diverse, and often bearing large and
showy flowers, orchids are an ancient plant family
that has evolved an amazing array of bizarre flower
types, unique pollination syndromes, and complex
symbiotic interactions with animals and fungi. In the
plant world, orchids reign supreme as about 10% of
all flowering plant species are members of the
Orchidaceae. No other plant family can match the
peculiar array of evolutionary features that orchids
collectively possess. Along with the Asteraceae, the
Orchidaceae has more species, estimated to be
between 20,000 and 35,000 taxa (Cribb et al.,
2003), than any other family of flowering plants,
and individual orchid species are often rare in nature,
occurring in restricted and specific niches and
habitats. Collectors prize orchids for their seemingly
infinite variety of showy flowers; scientists have long
been fascinated by the relationships between the
plants and their pollinators and other symbionts.
Today, orchids have taken on even greater
significance. Due to their interconnectedness with
the species around them, orchids, highly sensitive to
habitat change, are among the first casualties from
environmental degradation. Most orchid genera
contain threatened or endangered species (Swarts &
Dixon, 2009). Orchids are found throughout North
America, and many of the approximately 210 species
found north of Mexico are threatened, endangered, or
extirpated in at least part of their ranges because of
habitat loss and alteration. Most North American
orchids are terrestrial. Globally, terrestrial orchids
make up only one third of orchid species with the
other two thirds being epiphytes and lithophytes.
However, terrestrial herbaceous perennials are disproportionately represented in the extinct plant
species listed by The World Conservation Union
(IUCN, 1999). Consequently, terrestrial orchids are
likely subject to a greater extinction risk than
epiphytes, particularly in response to current climate
changes.
Much of orchids’ sensitivity to habitat change
likely can be traced to their dependence on two, often
1 We are thankful to the United States Botanic Garden and the Smithsonian Institution for financial support of the North
American Orchid Conservation Center (NAOCC) through a Smithsonian Grand Challenges Award grant. Frank Clements,
Vickie Dibella, Tony Dove, Barbara Faust, Christine Flanagan, Jim Kaufmann, John Kress, William McLaughlin, Ray
Mims, Jay O’Neill, Holly Shimizu, Teresa Vetick, and Kyle Wallick contributed substantially to discussions about the
structure and development of NAOCC. Intern Jean Linsky assisted in collecting data. Information related to the case study
description of Isotria medeoloides was obtained during a research project funded by Contract Number H399207001/
J370010018 from the National Park Service.
2 Department of Botany, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 166,
Washington, D.C. 20013-7012, U.S.A. krupnickg@si.edu.
3 Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, Maryland 21037, U.S.A. mccormickm@si.edu;
whighamd@si.edu.
4 Smithsonian Gardens, Smithsonian Institution, P.O. Box 37012, MRC 506, Washington, D.C. 20013-7012, U.S.A.
mirendat@si.edu.
doi: 10.3417/2011108
ANN. MISSOURI BOT. GARD. 99: 180–198. PUBLISHED
ON
13 DECEMBER 2013.
Volume 99, Number 2
2013
Krupnick et al.
181
Status and Future of Orchid Conservation in
North America
very specific, types of symbiotic associations.
Orchids’ relationships with specific pollinators have
been a subject of interest since before Darwin, but
more recently orchid dependence on mycorrhizal
fungi has also received substantial research attention
(Waterman & Bidartondo, 2008). Identification of the
fungi on which orchids depend requires DNA
sequencing and analysis, but it is clear at this point
that some orchids are dependent upon fungi that are
free living in the soil, while others associate with
fungi that are also connected to other plants,
especially trees. As habitats change, the fungal
community changes, and orchids may lose fungi
upon which they depend for their survival.
As popular, desirable, and charismatic subjects for
cultivation, orchids face another serious threat. Like
precious gems, the most unique and rare orchids are
sought by the most enthusiastic collectors. As word
spreads about the location of a rare orchid, more and
more demand is placed on already fragile populations. Unfortunately, without efforts to cultivate the
symbiotic fungi, most of these plants are doomed in
cultivation. Due to the combination of habitat loss
and poaching, many orchid species, which were once
widespread, are now found in small, ecologically
fragile, fragmented populations. The majority of
orchids are represented globally by tropical epiphytes, but temperate zone terrestrials make up a
significant proportion (approximately 28%; Gravendeel et al., 2004) and conservation of terrestrial
species has proven to be especially challenging (e.g.,
Stewart & Hicks, 2010). No orchid has ever been delisted, though one, Isotria medeoloides (Pursh) Raf.,
was upgraded from endangered to threatened in 1994
(U.S. Fish and Wildlife Service, 1994) after extensive
directed searching uncovered new populations. A
comprehensive holistic approach to species conservation has to be fully realized in conservation and
restoration plans.
The orchid flora of North America represents an
important scientific challenge for conservation biologists. Unlike many other plant species, where
significant efforts are often employed to cultivate
and reintroduce rare plants and to store germplasm,
the majority of organizations that identify and protect
orchids on public and private lands rely solely on
habitat conservation for management. This conservation strategy has largely been dictated by the unique
aspects of orchid biology that make them not
amenable to standard plant conservation techniques.
We propose a model of centralized but integrated
orchid conservation that can provide one-stop
shopping for agencies and organizations responsible
for and actively participating in efforts to conserve
native orchids.
We begin by identifying successes and major gaps
in conservation strategies for North American native
orchids by addressing nine of the 16 targets of the
2011–2020 Global Strategy for Plant Conservation
(GSPC) in relation to the conservation of orchid
species native to the United States, Canada, and
Greenland. GSPC targets 4, 5, 6, 9, 10, 12, and 13 do
not apply directly to native North American orchid
species. We then propose a centralized North
American Orchid Conservation Center (NAOCC) that
addresses each deficiency.
GLOBAL STRATEGY
TARGET
1,
OF
PLANT CONSERVATION TARGETS
AN ONLINE FLORA OF ALL KNOWN PLANTS
A total of 210 orchid species are native to the
United States, Canada, and Greenland (see Table 1),
including one described as recently as 2007, as
Platanthera yosemitensis Colwell, Sheviak & P. E.
Moore (Colwell et al., 2007). The novel orchid list is a
compilation of species from Kartesz (1994), the Flora
of North America (Romero-González et al., 2002),
Brown (2009), and NatureServe Explorer (NatureServe, 2011), and each name is accepted by The
Plant List (,http://www.thePlantList.org.) and the
World Checklist of Selected Plant Families (WCSP,
2011). Additionally, 135 orchid species are native to
Puerto Rico and the Virgin Islands (AcevedoRodrı́guez & Strong, 2007), but of these species only
those that extend into the mainland are treated here.
The 210 described species (Table 1) are distributed among 66 genera (Table 2), with 49 genera
(74%) represented by only one or two species and a
few genera being represented by more than three
species (e.g., Platanthera Rich. with 35 species,
Spiranthes Rich. with 23 species). While there are
always questions of whether taxa should be split or
lumped and questions about the treatment of hybrids,
relationships between most genera in the Orchidaceae are well established (e.g., Górniak et al., 2010).
Native orchid species are found in all 50 states
within the United States and all 10 provinces and
three territories of Canada. On average, there are 40
native species per state, with Hawaii having the
fewest native species (three) and Florida with the
most (106). Other species-rich areas include the
states along the East Coast associated with the
Appalachian Mountains, especially North Carolina
(67 species), Virginia (59 species), and New York (57
species). Of the Canadian provinces, Prince Edward
Island and Ontario have an especially diverse orchid
assemblage (59 and 58 species, respectively). All
NatureServe
conservation
status ranksa
Species
G3;
G5;
G4;
G2;
G4;
G4;
G5;
G3;
G4;
G4;
G2;
G3;
G4;
G5;
S3
SH, S1-S5, SNR
SX, SH, S1-S4, SNR
S1
S1*
SH
S3
SX
SX
S1-S3, SNR
SH, S1-S3
SH, S1, S2, SNR
S1-S5, SNR
SX, S1-S4, SNR
G5; SH, S1-S5, SNR
G4; S1*
G4; S1
G4; S2, S3, SNR
G4; S1-S4, SNR*
G4; SX, S1, S3, S4, SNR*
GNR; S2
G1; S1
G5; SH, S1-S4, SNR
G4; S2, S3, S5, SU, SNR
G5; SH, S1-S5, SNR
G5; SH, S1-S4, SNR
G5; S1-S5, SNR
G5; SX, SH, S1-S5, SNR
G4; S1
G4; SNR*
G4; SH*
G5; S1, S3-S5, SNR
U.S.
Endangered
Species Actc
U.S. State
conservation
listingd
Canada’s
Species At
Risk Acte
Vulnerable
1
11
0
0
0
5
17
37
0
1
0
0
2
16
Endangered
Endangered
Endangered
Endangered
Threatened
Endangered
Endangered
Endangered
Endangered
Endangered
Threatened
Endangered*
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Number of
botanic gardens
where presentf
8
5*
1
1
3*
1
0
0
12
1
2
0
2
2
2
0
4*
22
Annals of the
Missouri Botanical Garden
Anoectochilus sandvicensis Lindl.
Aplectrum hyemale (Muhl. ex Willd.) Nutt.
Arethusa bulbosa L.
Basiphyllaea corallicola (Small) Ames
Beloglottis costaricensis (Rchb. f.) Schltr.
Bletia patula Hook.
Bletia purpurea (Lam.) DC.
Brassia caudata (L.) Lindl.
Bulbophyllum pachyrachis (A. Rich.) Griseb.
Calopogon barbatus (Walter) Ames
Calopogon multiflorus Lindl.
Calopogon oklahomensis D. H. Goldman
Calopogon pallidus Chapm.
Calopogon tuberosus (L.) Britton, Sterns &
Poggenb.
Calypso bulbosa (L.) Oakes
Camaridium vestitum (Sw.) Lindl.
Campylocentrum pachyrrhizum (Rchb. f.) Rolfe
Cephalanthera austiniae (A. Gray) A. Heller
Cleistesiopsis bifaria (Fernald) Pansarin & F. Barros
Cleistesiopsis divaricata (L.) Pansarin & F. Barros
Cleistesiopsis oricamporum P. M. Br.
Corallorhiza bentleyi Freudenst.
Corallorhiza maculata (Raf.) Raf.
Corallorhiza mertensiana Bong.
Corallorhiza odontorhiza (Willd.) Nutt.
Corallorhiza striata Lindl.
Corallorhiza trifida Châtel.
Corallorhiza wisteriana Conrad
Cranichis muscosa Sw.
Cyclopogon cranichoides (Griseb.) Schltr.
Cyclopogon elatus (Sw.) Schltr.
Cypripedium acaule Aiton
IUCN 2011
Red Listb
182
Table 1. The 210 native orchid species of the United States, Canada, and Greenland, including conservation assessments, legal protections, and the number of botanic gardens holding ex situ
collections. This list is a compilation of species from Kartesz (1994), the Flora of North America (Romero-Gonza´ lez et al., 2002), Brown (2009), and NatureServe Explorer (NatureServe, 2011).
NatureServe
conservation
status ranksa
Species
G3;
G3;
G4;
G4;
G5;
G3;
G4;
G5;
G4;
G4;
G4;
G5;
G4;
G5;
SH, S1-S3
S3
SX, SH, S1-S3, SNR
S1-S3
S2, SNR
S1-S3
S1-S4, SNR
SH, S1-S4, SNR
S1-S4, SNR
SX, S1-S4, SU, SNR, SNA
SNR*
S1
S4
SX, SH, S1-S5, SNR*
G3; S2*
GU; SNR*
U.S.
Endangered
Species Actc
U.S. State
conservation
listingd
Canada’s
Species At
Risk Acte
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Number of
botanic gardens
where presentf
1
7
10
2
7
14
3
12
2
33
1
22
0
11*
7*
0
G5; SNR*
2
G4; S3, SNR*
0
G4; S1
G4; SNR
GNR; S3
Endangered
G4; SX
Endangered*
G4;
G4;
G4;
G4;
G4;
G4;
G2;
S2, S3, SNR*
S2
S3
S1
S1-S3, SU, SNR
S4
S1, S2*
Endangered
Endangered
Endangered
Endangered
Special Concern
Endangered
1
23
0
10
1*
5
4*
25
19
1
37
6
0
Krupnick et al.
183
Status and Future of Orchid Conservation in
North America
Cypripedium arietinum R. Br.
Cypripedium californicum A. Gray
Cypripedium candidum Muhl. ex Willd.
Cypripedium fasciculatum Kellogg ex S. Watson
Cypripedium guttatum Sw.
Cypripedium kentuckiense C. F. Reed
Cypripedium montanum Douglas ex Lindl.
Cypripedium parviflorum Salisb.
Cypripedium passerinum Richardson
Cypripedium reginae Walter
Cypripedium yatabeanum Makino
Cyrtopodium punctatum (L.) Lindl.
Dactylorhiza aristata (Fisch. ex Lindl.) Soó
Dactylorhiza viridis (L.) R. M. Bateman, Pridgeon
& M. W. Chase
Dendrophylax lindenii (Lindl.) Benth. ex Rolfe
Dendrophylax porrectus (Rchb. f.) Carlsward &
Whitten
Dichromanthus cinnabarinus (La Llave & Lex.)
Garay
Dichromanthus michuacanus (La Llave & Lex.)
Salazar & Soto Arenas
Eltroplectris calcarata (Sw.) Garay & H. R. Sweet
Encyclia tampensis (Lindl.) Small
Epidendrum amphistomum A. Rich.
Epidendrum anceps Jacq.
Epidendrum blancheanum Urb.
Epidendrum floridense Hágsater
Epidendrum magnoliae Muhl.
Epidendrum nocturnum Jacq.
Epidendrum rigidum Jacq.
Epidendrum strobiliferum Rchb. f.
Epipactis gigantea Douglas ex Hook.
Eulophia alta (L.) Fawc. & Rendle
Eulophia ecristata (Fernald) Ames
IUCN 2011
Red Listb
Volume 99, Number 2
2013
Table 1. Continued.
184
Table 1. Continued.
NatureServe
conservation
status ranksa
Species
G4;
G1;
G5;
G5;
G5;
G5;
G5;
SNR
S1
S1-S5, SNR
S1-S5, SNR
S1-S5, SNR
SH, S1-S5, SNR
SX, SH, S1-S5, SU, SNR
G5;
G4;
G4;
G5;
G4;
G4;
G4;
S1
SNR*
S1, SNR
S1-S3, SNR
S1-S3, SNR*
S1*
S2
G3;
G1;
G5;
G2;
G4;
G2;
G5;
G3;
G3;
G5;
G5;
G4;
G4;
G4;
G1;
G4;
G4;
G4;
G4;
S1, S3
S1, SNR
SH, S1-S4, SNR
S1, S2
S1
SX, SH, S1, S2
SX, S1-S5, SNR
SH
S3
SX, S1-S5, SNR
SX, SH, S1-S5, SNR
S2
SH
S1, S3*
SH, S1, SU
S3, S4*
SNR, SNA
SH, S1-S4, SNR*
S2, SNR
U.S.
Endangered
Species Actc
U.S. State
conservation
listingd
Canada’s
Species At
Risk Acte
0
0
4
9
27
14
3
0
1
2*
1
4
2
18*
2
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered*
Endangered
Endangered
Threatened
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered*
Endangered
Endangered
Endangered*
Number of
botanic gardens
where presentf
Endangered
Endangered
Endangered
2
0
3
0
10
1
5
1
3
4
8
10
0
0
0
0
3*
1
0
Annals of the
Missouri Botanical Garden
Galeandra beyrichii Rchb. f.
Galeandra bicarinata G. A. Romero & P. M. Br.
Galearis spectabilis (L.) Raf.
Goodyera oblongifolia Raf.
Goodyera pubescens (Willd.) R. Br.
Goodyera repens (L.) R. Br.
Goodyera tesselata Lodd.
Govenia floridana P. M. Br.
Habenaria distans Griseb.
Habenaria floribunda Lindl.
Habenaria quinqueseta (Michx.) Sw.
Habenaria repens Nutt.
Hammarbya paludosa (L.) Kuntze
Heterotaxis sessilis (Sw.) F. Barros
Hexalectris grandiflora (A. Rich. & Galeotti) L. O.
Williams
Hexalectris nitida L. O. Williams
Hexalectris revoluta Correll
Hexalectris spicata (Walter) Barnhart
Hexalectris warnockii Ames & Correll
Ionopsis utricularioides (Sw.) Lindl.
Isotria medeoloides (Pursh) Raf.
Isotria verticillata (Muehl. ex Willd.) Raf.
Lepanthopsis melanantha (Rchb. f.) Ames
Liparis hawaiensis H. Mann
Liparis liliifolia (L.) Rich. ex Lindl.
Liparis loeselii (L.) Rich.
Liparis nervosa (Thunb.) Lindl.
Macradenia lutescens R. Br.
Malaxis abieticola Salazar & Soto Arenas
Malaxis bayardii Fernald
Malaxis brachystachys (Rchb. f.) Kuntze
Malaxis macrostachya (Lex.) Kuntze
Malaxis monophyllos (L.) Sw.
Malaxis porphyrea (Ridl.) Kuntze
IUCN 2011
Red Listb
Species
IUCN 2011
Red Listb
U.S.
Endangered
Species Actc
G4; S1-S3, SNR
G5; S1-S5, SX, SNR
G2; S1
G4; S1, S2*
GNR; S1
G3; S1-S3, SNR*
G4; S1-S4, SNR*
G4; S1-S4, SNR*
G4; SH, S1-S4, SNR*
G5; S1-S4, SNR*
G5; SH, S1-S5, SNR*
G4; S1-S4*
GNR; S1
G5; S1
G1; S1*
G3; S2, S3, SNR
G3; S3
G4; S3
G5; SH, S1-S5, SU, SNR*
G4; S3, S4, SNR
G4; S3, S4, SNR
G3; S3
G4; S3, S4, SNR
G5; S1-S5, SNR
G2; S2
G5; SX, S1-S5, SU, SNR
G4; S1-S4, SNR
G4; SNR
G2; S1, SH, SNR
G3; S2-S4
G5; SX, SH, S1-S4, SNR
G5; SH, S1-S5, SU, SNR
U.S. State
conservation
listingd
Endangered
Endangered
Endangered
Endangered*
Endangered*
Endangered*
Endangered*
Endangered
Endangered*
Endangered
Endangered
Threatened
Endangered
Canada’s
Species At
Risk Acte
Number of
botanic gardens
where presentf
0
2
0
1*
0
0
4*
5*
0
0
1
0
9*
1
3*
0
0
0
5*
1
0
0
0
0
0
3
4
0
1
2
5
2
0
Krupnick et al.
185
Status and Future of Orchid Conservation in
North America
Malaxis spicata Sw.
Malaxis unifolia Michx.
Malaxis wendtii Salazar
Mesadenus lucayanus (Britton) Schltr.
Microthelys rubrocallosa (B. L. Rob. & Greenm.)
Garay
Neottia auriculata (Wiegand) Szlach.
Neottia banksiana (Lindl.) Rchb. f.
Neottia bifolia (Raf.) Baumbach
Neottia borealis (Morong) Szlach.
Neottia convallarioides (Sw.) Rich.
Neottia cordata (L.) Rich.
Neottia smallii (Wiegand) Szlach.
Oncidium ensatum Lindl.
Pelexia adnata (Sw.) Poit. ex Rich.
Peristylus holochila (Hillebr.) N. Hallé
Piperia candida Rand. Morgan & Ackerman
Piperia colemanii Rand.Morgan & Glic.
Piperia cooperi (S. Watson) Rydb.
Piperia dilatata (Pursh) Szlach. & Rutk.
Piperia elegans (Lindl.) Rydb.
Piperia elongata Rydb.
Piperia leptopetala Rydb.
Piperia transversa Suksd.
Piperia unalascensis (Spreng.) Rydb.
Piperia yadonii Rand. Morgan & Ackerman
Platanthera aquilonis Sheviak
Platanthera blephariglottis (Willd.) Lindl.
Platanthera brevifolia (Greene) Senghas
Platanthera chapmanii (Small) Luer
Platanthera chorisiana (Cham.) Rchb. f.
Platanthera ciliaris (L.) Lindl.
Platanthera clavellata (Michx.) Luer
Platanthera convallariifolia (Fisch. ex Lindl.) Lindl.
NatureServe
conservation
status ranksa
Volume 99, Number 2
2013
Table 1. Continued.
186
Table 1. Continued.
NatureServe
conservation
status ranksa
Species
G5; S1-S4, SX, SNR
G4; SX, S1-S4, SU, SNR
G5; SX, S1-S4, SNR
G4; SX, S1-S4, SH, SNR
G5; S1-S5, SU, SNR*
G5; S4
G3; S1-S3, SNR
G2; SH, S1-S3, SU
G5; S1-S5, SNR
G2; SX, SH, S1, S2
G4; S4, SNR
G5; SH, S1-S3, SNR
G5; S1-S5, SNR
G5; SX, SH, S1-S4, SNR
GNA; SU, SNA, SNR*
G5; SX, S1-S4, SNR
G3; SH, S1-S3
G5; SX, SH, S1-S5, SNR
G5;
G1;
G4;
G5;
SX, SH, S1-S5, SNR*
S1, SNR
S1, SNR
S1-S5, SNR
U.S.
Endangered
Species Actc
U.S. State
conservation
listingd
Canada’s
Species At
Risk Acte
Number of
botanic gardens
where presentf
Endangered
0
1
3
2
3
5
0
1
7
2
0
1
1
1
0
1
1
2
0
Endangered
Endangered
Endangered
Endangered
Candidate
Endangered
Endangered
Endangered
Threatened
Endangered
Endangered
Vulnerable
Endangered
Endangered
Threatened
Endangered
Endangered
Endangered
Endangered*
Endangered
G4; S2
G2; S2
1
0
0
4*
0
0
0
G2; S1, S2
0
Sensitive
G4; S1, SNR
G5; SX, SU, S1-S5, SNR
G4; S3
G3; S1
Endangered
Endangered
Endangered
0
0
17
13
1
Annals of the
Missouri Botanical Garden
Platanthera cristata (Michx.) Lindl.
Platanthera flava (L.) Lindl.
Platanthera grandiflora (Bigelow) Lindl.
Platanthera hookeri (Torr.) Lindl.
Platanthera huronensis Lindl.
Platanthera hyperborea (L.) Lindl.
Platanthera integra (Nutt.) A. Gray ex L. C. Beck
Platanthera integrilabia (Correll) Luer
Platanthera lacera (Michx.) G. Don
Platanthera leucophaea (Nutt.) Lindl.
Platanthera limosa Lindl.
Platanthera nivea (Nutt.) Luer
Platanthera obtusata (Banks ex Pursh) Lindl.
Platanthera orbiculata (Pursh) Lindl.
Platanthera pallida P. M. Br.
Platanthera peramoena A. Gray
Platanthera praeclara Sheviak & M. L. Bowles
Platanthera psycodes (L.) Lindl.
Platanthera purpurascens (Rydb.) Sheviak & W.
F. Jenn.
Platanthera rotundifolia (Banks ex Pursh) Lindl.
Platanthera shriveri P. M. Br.
Platanthera sparsiflora (S. Watson) Schltr.
Platanthera stricta Lindl.
Platanthera tescamnis Sheviak & W. F. Jenn.
Platanthera tipuloides (L. f.) Lindl.
Platanthera yosemitensis Colwell, Sheviak & P. E.
Moore
Platanthera zothecina (L. C. Higgins & S. L.
Welsh) Kartesz & Gandhi
Platythelys querceticola (Lindl.) Garay
Platythelys sagraeana (A. Rich.) Garay
Pogonia ophioglossoides (L.) Ker Gawl.
Polystachya concreta (Jacq.) Garay & H. R. Sweet
Ponthieva brittoniae Ames
IUCN 2011
Red Listb
NatureServe
conservation
status ranksa
Species
G4;
G4;
G4;
G4;
G4;
G5;
G4;
U.S.
Endangered
Species Actc
S1-S3, SNR
S1
S1*
S3*
S1*
S3, SNR*
S3*
GNR; S3, S4, SNR
G3; SNR*
G1; S1, SNR
G4; S1-S4, SNR
G5; S1-S5, SU, SNR
G1; S1
G2; S1, S2
G3; SH, S1-S3, SNR
G1; S1
G5; S1-S5, SNR
G4; S1-S4, SU, SNR
G3; SH, S1-S3, SNR
G5; SX, SH, S1-S5, SNR
G4; SX, S1-S4, SNR
G4; SH, S1-S3, S5, SNR
G5; SH, S1-S4, SU, SNR
G5; SH, S1-S5, SNR
G3; S3
G4; S1, S2, S4, SNR
G5; SH, S1-S4, SU
G5; SH, S1-S5, SU, SNR
GNR; S1
G4; S1*
G5; SH, S1-S5, SNR
G5; S1-S5, SNR
G5; S1*
G4; S1, S3-S5, SNR
U.S. State
conservation
listingd
Endangered
Endangered
Threatened*
Endangered
Threatened
Endangered
Endangered
Endangered
Vulnerable
Endangered
Endangered
Threatened
Endangered
Threatened
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Sensitive
Endangered
Endangered
Endangered
Endangered
Endangered*
Endangered
Canada’s
Species At
Risk Acte
Number of
botanic gardens
where presentf
4
1
6*
65*
9*
3
8*
0
0
0
0
0
28
1
5
0
0
5
0
0
2
2
2
15
3
2
3
1
5
0
0
4
5
3
15
Krupnick et al.
187
Status and Future of Orchid Conservation in
North America
Ponthieva racemosa (Walter) C. Mohr
Prescottia oligantha (Sw.) Lindl.
Prosthechea boothiana (Lindl.) W. E. Higgins
Prosthechea cochleata (L.) W. E. Higgins
Prosthechea pygmaea (Hook.) W. E. Higgins
Pseudorchis albida (L.) Á. Löve & D. Löve
Sacoila lanceolata (Aubl.) Garay
Sacoila squamulosa (Kunth) Garay
Schiedeella arizonica P. M. Br.
Schiedeella confusa (Garay) Espejo & López-Ferr.
Spiranthes brevilabris Lindl.
Spiranthes casei Catling & Cruise
Spiranthes cernua (L.) Rich.
Spiranthes delitescens Sheviak
Spiranthes diluvialis Sheviak
Spiranthes eatonii Ames ex P. M. Br.
Spiranthes infernalis Sheviak
Spiranthes lacera (Raf.) Raf.
Spiranthes laciniata (Small) Ames
Spiranthes longilabris Lindl.
Spiranthes lucida (H. H. Eaton) Ames
Spiranthes magnicamporum Sheviak
Spiranthes ochroleuca (Rydb.) Rydb.
Spiranthes odorata (Nutt.) Lindl.
Spiranthes ovalis Lindl.
Spiranthes parksii Correll
Spiranthes porrifolia Lindl.
Spiranthes praecox (Walter) S. Watson
Spiranthes romanzoffiana Cham.
Spiranthes sylvatica P. M. Br.
Spiranthes torta (Thunb.) Garay & H. R. Sweet
Spiranthes tuberosa Raf.
Spiranthes vernalis Engelm. & A. Gray
Stelis gelida (Lindl.) Pridgeon & M. W. Chase
Tipularia discolor (Pursh) Nutt.
IUCN 2011
Red Listb
Volume 99, Number 2
2013
Table 1. Continued.
188
Table 1. Continued.
NatureServe
conservation
status ranksa
Species
U.S.
Endangered
Species Actc
U.S. State
conservation
listingd
Canada’s
Species At
Risk Acte
Number of
botanic gardens
where presentf
G3; S1
Endangered
5
G4; S1*
Endangered*
1
Endangered
Endangered
0
0
0
G1; S1
G4; SNR
G3;
G1;
G4;
G4;
G3;
SH, S1-S3, SNR
S1
S1
S2
SNR
G3; S1
G4; S1
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
Endangered
0
0
1
7
5
1
2
8
* Listed in original publication under a synonymous name.
Conservation assessments by NatureServe correspond to Global threats: G1 ¼ Critically Imperiled, G2 ¼ Imperiled, G3 ¼ Vulnerable, G4 ¼ Apparently Secure, G5 ¼ Secure, GU ¼
Unrankable, GNR ¼ Not Yet Ranked, GNA ¼ Not Applicable. Subnational threats follow similar values (S1 to S5, etc.), but apply at the state or provincial levels. NatureServe rankings
are available through ,http://www.natureserve.org/explorer..
b
International Union for Conservation of Nature and Natural Resources (IUCN), 2011.
c
Endangered Species Act (ESA), 1973; U.S. Government Printing Office, 2012.
d
U.S. State listing is at the highest level of protection among all states listed, as reported by the USDA PLANTS Database (USDA, NRCS, 2012).
e
Species at Risk Act (SARA), 2002.
f
The number of botanic gardens where the orchid species is conserved or present, according to Botanical Gardens Conservation International (2012).
a
Annals of the
Missouri Botanical Garden
Tolumnia bahamensis (Nash ex Britton & Millsp.)
Braem
Trichocentrum undulatum (Sw.) Ackerman & M.
W. Chase
Triphora amazonica Schltr.
Triphora craigheadii Luer
Triphora gentianoides (Sw.) Nutt. ex Ames &
Schltr.
Triphora trianthophora (Sw.) Rydb.
Triphora yucatanensis Ames
Tropidia polystachya (Sw.) Ames
Vanilla barbellata Rchb. f.
Vanilla dilloniana Correll
Vanilla inodora Schiede
Vanilla mexicana Mill.
Vanilla phaeantha Rchb. f.
IUCN 2011
Red Listb
Volume 99, Number 2
2013
Krupnick et al.
189
Status and Future of Orchid Conservation in
North America
Table 2. Species distribution among listed orchid genera in
Table 1.
Genus
Species #
Percent of
total species
Platanthera Rich.
Spiranthes Rich.
Cypripedium L.
Piperia Rydb.
Malaxis Sol. ex Sw.
Epidendrum L.
Corallorhiza Gagnebin
Neottia Guett.
Calopogon R. Br.
Hexalectris Raf.
Triphora Nutt.
Vanilla Mill.
Goodyera R. Br.
Habenaria Willd.
Liparis Rich.
Cleistesiopsis Pansarin & F. Barros
Prosthechea Knowles & Westc.
Bletia Ruiz & Pav.
Cyclopogon C. Presl
Dactylorhiza Neck. ex Nevski
Dendrophylax Rchb. f.
Dichromanthus Garay
Eulophia R. Br. ex Lindl.
Galeandra Lindl.
Isotria Raf.
Platythelys Garay
Ponthieva R. Br.
Sacoila Raf.
Schiedeella Schltr.
Anoectochilus Blume
Aplectrum Blume
Arethusa L.
Basiphyllaea Schltr.
Beloglottis Schltr.
Brassia R. Br.
Bulbophyllum Thouars
Calypso Salisb.
Camaridium Lindl.
Campylocentrum Benth.
Cephalanthera Rich.
Cranichis Sw.
Cyrtopodium R. Br.
Eltroplectris Raf.
Encyclia Hook.
Epipactis Zinn
Galearis Raf.
Govenia Lindl.
Hammarbya Kuntze
Heterotaxis Lindl.
Ionopsis Kunth
Lepanthopsis Ames
Macradenia R. Br.
Mesadenus Schltr.
Microthelys Garay
Oncidium Sw.
Pelexia Poit. ex Lindl.
35
23
12
10
9
8
7
7
5
5
5
5
4
4
4
3
3
2
2
2
2
2
2
2
2
2
2
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
16.7%
11.0%
5.7%
4.8%
4.3%
3.8%
3.3%
3.3%
2.4%
2.4%
2.4%
2.4%
1.9%
1.9%
1.9%
1.4%
1.4%
1%
1%
1%
1%
1%
1%
1%
1%
1%
1%
1%
1%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
Table 2. Continued.
Genus
Species #
Percent of
total species
Peristylus Blume
Pogonia Juss.
Polystachya Hook.
Prescottia Lindl.
Pseudorchis Ség.
Stelis Sw.
Tipularia Nutt.
Tolumnia Raf.
Trichocentrum Poepp. & Endl.
Tropidia Lindl.
1
1
1
1
1
1
1
1
1
1
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
0.5%
state and provincial species numbers are according to
the NatureServe Explorer (NatureServe, 2011). Three
species are endemic to California, as Piperia
colemanii Rand. Morgan & Glic., P. yadonii Rand.
Morgan & Ackerman, and Platanthera yosemitensis,
and three to Hawaii, as Anoectochilus sandvicensis
Lindl., Liparis hawaiensis H. Mann, and Peristylus
holochila (Hillebr.) N. Hallé. Two orchid species are
endemic to Florida, Govenia floridana P. M. Br. and
Triphora craigheadii Luer; one species is endemic,
each to three states, with Spiranthes delitescens
Sheviak in Arizona, S. infernalis Sheviak in Nevada,
and S. parksii Correll in Texas.
TARGET
2, AN ASSESSMENT OF THE CONSERVATION STATUS OF
ALL KNOWN PLANT SPECIES, AS FAR AS POSSIBLE, TO GUIDE
CONSERVATION ACTION
Only two North American orchids have been
assessed by the International Union for Conservation
of Nature and Natural Resources (IUCN) and are
listed as threatened on the 2011 IUCN Red List of
Threatened Species (IUCN, 2011): Anoectochilus
sandvicensis as Vulnerable (or VU), and Platanthera
praeclara Sheviak & M. L. Bowles, as Endangered (or
EN).
The U.S. Endangered Species Act (ESA; 1973;
U.S. Government Printing Office, 2012) federally lists
the four endangered species Piperia yadonii, Peristylus holochila [[ Platanthera holochila (Hillebr.)
Kraenzl.], Spiranthes delitescens, and S. parksii, as
well as the four threatened species as Isotria
medeoloides, Platanthera leucophaea (Nutt.) Lindl.,
P. praeclara, and S. diluvialis Sheviak, and the one
candidate species, Platanthera integrilabia (Correll)
Luer. At the state level, 57% (119 species) are
protected as endangered, threatened, vulnerable, or
sensitive in at least one state (cf. Table 1).
The Canadian Species at Risk Act (SARA; 2002)
lists seven endangered orchid species, as Cypripedi-
190
Annals of the
Missouri Botanical Garden
um candidum Muhl. ex Willd., Isotria medeoloides, I.
verticillata (Muhl. ex Willd.) Raf., Liparis liliifolia
(L.) Rich. ex Lindl., Platanthera leucophaea, P.
praeclara, and Triphora trianthophora (Sw.) Rydb.
Further, one threatened species, Cephalanthera
austiniae (A. Gray) A. Heller, is included, as well
as one species that is noted of special concern for
conservation, Epipactis gigantea Douglas ex Hook.
(cf. Table 1).
All but 10 species of the 210 orchid names
included in Table 1 have been assessed by NatureServe (2011), with 24% (50 species) listed as globally
threatened. Of these 50 threatened species, 11 were
assessed at the global scale as critically imperiled
(G1), 13 are imperiled (G2), and 26 are vulnerable
(G3; cf. Table 1). For subnational assessments by
NatureServe, 14% (30 species) are presumed to be
extirpated from at least one state or province, and an
overlapping 23% (48 species) are possibly extirpated
from at least one state or province. Also at the
subnational level, 84% (176 species) are variably
threatened (ranging from S1 or critically imperiled,
S2 or imperiled, or S3 or vulnerable) in at least one
state or province. In all cases, where an orchid had
been extirpated in one or more states, it was also
threatened or endangered in at least one other state.
specialized equipment (Liu et al., 2010; Seaton et al.,
2010; Stewart & Hicks, 2010). However problematic,
this is essential for propagation and establishment of
self-sustaining populations. Few organizations have
the capacity to handle these unique aspects of orchid
biology, placing cultivation and reintroduction beyond
the abilities of nearly all conservation agencies.
Scientific research has made substantial progress in
overcoming these difficult aspects of orchid ecology,
but additional efforts are needed on all key elements of
orchid life histories that must be understood if we are
to successfully support conservation, reintroduction,
and propagation efforts for native orchids. The
techniques being developed by scientists are still,
and likely will remain, beyond the capacity of most
conservation agencies, and there exists no current
network for scientific researchers either to support
conservation program managers or to communicate
with commercial or private growers and garden
enthusiasts who would benefit from a more complete
understanding of all aspects of orchid growth,
cultivation, and conservation.
3, INFORMATION, RESEARCH AND ASSOCIATED
OUTPUTS, AND METHODS NECESSARY TO IMPLEMENT THE
TARGET
STRATEGY DEVELOPED AND SHARED
As indicated by Stewart (2008), much of the
information on conservation and reintroduction of
orchids has been published in the ‘‘gray’’ literature
and obtained from unreplicated efforts that are rarely
designed as scientific studies to obtain statistically
significant data. Academic research occasionally
addresses aspects of orchid biology, but rarely
includes the whole process from basic biology to
application for conservation or reintroduction (e.g.,
Kindlmann et al., 2002; Dixon et al., 2003).
Replicated assessment of conservation is sorely
lacking. There are three major areas of orchid biology
that urgently need additional research: (1) identification of fungi associated with nearly all orchids, (2)
understanding of how those fungi contribute to seed
germination in situ and in vitro, and (3) how to
maximize survival of cultured seedlings or plants.
Seed banking alone cannot successfully preserve
orchids, because using the seeds to eventually
cultivate and restore plants in nature requires that
appropriate mycorrhizal fungi are present, especially at
the orchid’s protocorm stage. Identifying, maintaining,
and establishing the symbiotic fungi needed for orchid
seed germination is technically difficult and requires
TARGET
7,
AT LEAST
75%
OF KNOWN THREATENED PLANT
SPECIES CONSERVED IN SITU
When considering the proportion of threatened
orchids that are conserved in situ, it is important to
distinguish between species that are considered
globally threatened and the majority of orchids that
are threatened within a portion of their ranges.
Conserved in situ means ‘‘that biologically viable
populations of these species occur in at least one
protected area or the species is effectively managed
outside the protected area network, e.g., as part of a
management plan’’ according to a recent GSPC Plant
Conservation Report (Convention on Biological
Diversity [CBD], 2009: 23–24). As previously
outlined (cf. Table 1), of the 50 globally threatened
(i.e., ranked G1, G2, or G3 by NatureServe) orchid
species, only eight are protected under the ESA and
one additional species, Triphora trianthophora, under
Canada’s SARA. An additional 22 species are
protected at the state or province level. Taken
together, a total of 62% (31 of 50 species, cf. Table
1) of native orchid species assessed as threatened are
thus conserved in situ (i.e., have legal protection),
which is far below the goal of Target 7. It is
noteworthy that six of the 10 globally imperiled or
critically imperiled species (G1 or G2) that currently
have no protection at the federal or state level have
only recently been described, suggesting that accurate identification and species delimitation have
hampered attempts at species protection.
Volume 99, Number 2
2013
Krupnick et al.
191
Status and Future of Orchid Conservation in
North America
Beyond recognition of the need to protect orchid
taxa is the degree to which protection is actually
accomplished. The level of protection provided by
state or federal protected status depends on both the
number and distribution of plants on protected land
and also on the knowledge of the species’ biology
needed to determine whether protection is adequate.
A number of protected reserves in the United States
and Canada focus to some degree on orchids or on
habitats with disproportionately many orchids. One
such example is the Bruce Peninsula National Park
in Ontario, which supports 43 of the orchid species
native to Canada that will be threatened as a result of
climate change (Suffling & Scott, 2002). The heart of
the Niagara Escarpment Biosphere Reserve includes
the Bruce Peninsula National Park, a Nature
Conservancy Preserve, and First Nations lands, all
of which share knowledge about species at risk. The
stated park goal is to maintain viable populations of
all native species in situ, and there is a program
underway to report on the condition of all SARA
species, including trends in populations and the
factors that contribute to their condition.
Attributing population trends to particular factors
highlights the importance of in-depth understanding
of species biology for accomplishing effective conservation. Most endangered orchids in North America
have had at least some investigation of population
genetic structure, and this has been used to
understand connectivity between populations and to
determine the contribution of outlying populations to
species integrity. For example, Wallace (2003) found
that Platanthera leucophaea was a predominantly
outcrossing species and that inbreeding depression,
especially in small populations, suppressed seed
viability. These results suggested that larger, more
diverse and outcrossing populations were needed to
support population genetic variability in the current
fragmented landscape. This white-fringed orchid
historically was distributed from Missouri and Iowa
to Ontario with disjunct populations in Maine, New
Jersey, and Virginia (Bowles et al., 2005). The
current distribution is, however, much reduced and
few populations are self-sustaining.
Also important to consider are critical issues of
land management. Many terrestrial orchids are
pioneer species and cannot compete with overgrown
habitat. One prime example is the Green Swamp
Preserve of southeastern North Carolina in Brunswick
and Columbus counties. Originally established to
protect the habitat of the Venus fly trap (Dionaea
muscipula J. Ellis, Droseraceae), a great variety of
orchids, including species of Calopogon R. Br.,
Platanthera, and Cleistes Rich. ex Lindl., exist in the
preserve. The reserve’s 17,424 acres are owned and
managed by The Nature Conservancy, and its
longleaf pine savannas must be periodically subjected to prescribed burns to keep the habitat prime for
the smaller, herbaceous species that would be
otherwise crowded out by succession.
In contrast, other woodland species, such as
Cypripedium acaule Aiton, C. fasciculatum Kellogg
ex S. Watson, C. montanum Douglas ex Lindl., and
C. reginae Walter, have ecological strategies and
dependencies based both on edaphic constancy and
occasional disturbance of their environments. For
example, even though C. fasciculatum and C.
montanum grow sympatrically in old growth forest,
there is evidence that C. montanum needs occasional
disturbances, such as fire or tree-felling and thinning,
to create open, sunnier areas in which they will bloom
and set seed more freely. Its sympatric relative, C.
fasciculatum, conversely seems to be inhibited by
burns and other such disturbances. Therefore, it
becomes increasingly important to investigate the
individual ecological complexities of each individual
species if comprehensive management plans are to be
created.
Understanding what factors influence population
dynamics is critical for understanding how species
will respond to warming global temperatures. With
orchids, this uncertainty may be compounded by
considering the other species on which they depend.
Some orchids may be limited by the availability of
pollinators. For example, the deceptive orchid
Cyrtopodium punctatum (L.) Lindl. depends on oilgathering Centris bees for pollination. These bees rely
on other flowering plants, especially Byrsonima
lucida (Sw.) DC. (Malpighiaceae), for the oils they
collect. This led Pemberton and Liu (2008) to suggest
that B. lucida, which is almost completely absent
from the areas where the few remaining native orchid
populations of C. punctatum persist, be planted in the
vicinity of orchids to attract and support the bees that
pollinate both taxa. Such activities may also be
needed to support the interaction between orchids
and their pollinators in the face of climate change. In
particular, Liu et al. (2010) suggested that warming
temperatures in southwestern China are differentially
affecting pollinator and orchid phenologies such that
availability of pollinators and orchid flowering may be
increasingly out of synchronization. Effects of climate
change on orchid mycorrhizal fungi are completely
unknown, reflecting that very little is known about
what factors drive the distribution and abundance of
nearly all fungi. Because of this, conservation of fungi
must be largely accomplished through habitat
conservation.
192
TARGET
Annals of the
Missouri Botanical Garden
8, AT LEAST 75% OF THREATENED PLANT SPECIES IN
EX SITU COLLECTIONS, PREFERABLY IN THE COUNTRY OF
ORIGIN, AND AT LEAST
20% AVAILABLE FOR
RECOVERY AND
RESTORATION PROGRAMS
The Botanical Gardens Conservation International’s (BGCI; 2012) Plant Search database shows that
66% (139 species) of native North American orchids
are found in ex situ collections in botanical
institutions around the world (Table 1). Each of
these species is reported from an average of six
botanic gardens, but more than 25% (36 species) are
reported from a single botanic garden only. The
species most prevalent is Prosthechea cochleata (L.)
W. E. Higgins [[ Encyclia cochleata (L.) Dressler], a
species easily propagated (Pugh-Jones, 2009), which
is reported from 65 botanic gardens. Only two of 11
species ranked G1 by NatureServe are found in any
botanic garden collection, being Peristylus holochila
at three gardens and Spiranthes delitescens at one
institution. Five of 13 species ranked G2 are
represented in botanic gardens, but only two are
reported from more than one garden (two and five
gardens, Platanthera leucophaea and S. diluvialis,
respectively). It is highly unlikely that any of these ex
situ collections represents a genetically representative sample of the species.
The major method likely to preserve species
genetic variation is seed banking, as storing many
genetically distinct orchid seeds requires very little
space. Accomplishing such genetically representative
conservation is a major goal of the project Orchid
Seed Stores for Sustainable Use (OSSSU; Seaton et al.,
2010). This project is initially focusing on hotspots of
orchid diversity but is also beginning to work with
groups within North America to organize locations and
organizations for genetically representative orchid
seed storage. The Center for Plant Conservation
(CPC; ,http://www.centerforplantconservation.org.)
maintains seed collections for eight orchid species,
two of which are ranked G1 (Peristylus holochila and
Spiranthes delitescens), three G2 (Isotria medeoloides,
Platanthera leucophaea, and S. diluvialis), and three
G3 (Cypripedium kentuckiense C. F. Reed, Platanthera praeclara, and S. parksii). These species are
specifically directed to be available for conservation
and restoration activities, so this would suggest that
seeds of 16% (eight of 50) of threatened North
American orchid species are available for conservation and restoration, though the extent to which their
collections are genetically representative is unclear.
One shortcoming of seed storage for orchids is
that all orchids are dependent on or benefit from
mycorrhizal fungi for seed germination and all
species are dependent on fungi for protocorm
growth. While fungal requirements can sometimes
be overcome under specialized conditions in the
laboratory, there is little question that under natural
conditions fungi are required for orchid recruitment
and long-term survival of populations. Many orchids
require specific fungi at all life history stages (e.g.,
McCormick et al., 2004), while other more generalist
orchids use fungi from one or a few families (e.g.,
Shefferson et al., 2010). As a result, effective ex situ
conservation of orchids will require not just seed
banking, but also maintenance of required mycorrhizal fungi. This goal is still far from being
accomplished. One of the central difficulties has
been to simply identify the needed fungi. Most
orchid mycorrhizal fungi rarely produce spores and
so were known only from the anamorphic stage for
many years. Now they can be identified largely by
DNA sequencing. This rarity of spore production,
coupled with inconspicuous and morphologically
depauperate sporulating bodies, has resulted in a
poorly defined taxonomy of these cryptic fungi (e.g.,
Swarts & Dixon, 2009); DNA sequences rarely
match the taxonomically described species. Furthermore, with few spores produced, the fungi that
an orchid needs can rarely be stored as spores and
so must be maintained as active cultures. However,
some researchers have been testing methods for
storing fungal cultures in liquid nitrogen (Batty et
al., 2001). If these methods prove successful, then
conservation of genetically representative collections of mycorrhizal fungi may become more
common.
As yet there are relatively few orchid mycorrhizal
fungi in culture. The University of Alberta Mycological Herbarium’s (UAMH; ,http://www.uamh.
devonian.ualberta.ca.) culture collection currently
maintains 113 fungal cultures obtained from 37
orchid species. The Smithsonian Environmental
Research Center (SERC) currently maintains more
than 400 fungal isolates in culture from more than 40
native orchid species (D. F. Whigham, M. K.
McCormick & J. P. O’Neill, pers. comm.). The
American Type Culture Collection (ATCC) maintains
30 isolates from 13 orchid species (,http://www.atcc.
org.). Other scattered fungal cultures exist in
laboratories around the country where orchid research is conducted, but the maintenance of these
collections is often uncertain. Most of the existing
collections focus on saprotrophic Tulasnella J.
Schröt. and Ceratobasidium D. P. Rogers fungi, while
many orchids rely on fungi that form ectomycorrhizal
associations with other plants. These fungi are often
difficult to culture and many cannot be grown without
a photosynthetic host, often a tree, making them very
Volume 99, Number 2
2013
Krupnick et al.
193
Status and Future of Orchid Conservation in
North America
difficult to establish or maintain in culture. Even
when fungi are available in culture, however, their
role in facilitating seed germination is far from
certain.
Germination requirements for seven of 11 G1ranked and five of 13 G2-ranked orchids have yet to
be studied (Stewart & Hicks, 2010). One threatened
orchid (Isotria medeoloides) has so far proven
completely recalcitrant in culture or in the field. Of
the 11 G1- and G2-ranked orchids for which some
level of germination success has been obtained, two
have had only limited asymbiotic success and only
five have been germinated symbiotically. Symbiotic
germination has not been reported for the other six of
these 11 species. Symbiotic germination is expected
to be the method that leads to seedlings best able to
survive reintroduction and also provides a method for
co-introducing needed fungi and orchids (e.g.,
Stewart, 2008).
Few well-documented orchid reintroductions exist.
Often reintroductions occur in one location at one
time and either succeed or fail without providing
information about what may have been suboptimal or
may increase success in the future (Stewart, 2008).
Two examples of reintroductions designed as studies
are outlined by Stewart (2008). Elements of another
reintroduction are described by Zettler and Piskin
(2011). All three studies were designed to assess
effectiveness of introduction into different habitats,
but only one utilized symbiotic seedlings because
fungi were not available for the other two species. In
two of the three studies, survival was highest in sites
that already had the target orchid species. In the third
study, reintroduction was only attempted in sites with
the target species so existing plants could act as
sources for mycorrhizal colonization of the transplants. This suggests that mycorrhizal colonization
may be critical for reintroduction success. No
mention of pollinator availability was made in these
three studies.
or certificates to import, export, or re-export orchid
species across international lines. However, the
smuggling of wild orchids remains a problem
(Phelps et al., 2010).
TARGET
11,
NO SPECIES OF WILD FLORA ENDANGERED BY
INTERNATIONAL TRADE
The United States and Canada are both parties to
The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES;
,http://www.cites.org.), the lead coordinating
agency for the implementation, monitoring, and
review of Target 11. All orchid species are listed in
CITES appendix II, thus preventing the endangerment of North American orchids by over-exploitation
caused by international trade. Artificially propagated plants, hybrids, plant parts, products, or
derivatives, with a few exceptions, require permits
TARGET
14,
THE IMPORTANCE OF PLANT DIVERSITY AND THE
NEED FOR ITS CONSERVATION INCORPORATED INTO
COMMUNICATION, EDUCATION, AND PUBLIC AWARENESS
PROGRAM
As environmental awareness matures and enters
the digital age, several organizations previously
limited to spreading their messages slowly though
periodicals and mailings have found much broader
and enthusiastic younger audiences. One example is
the Native Orchid Conference (,http://tech.groups.
yahoo.com/group/nativeorchidconference/.) that has
become the ‘‘go to’’ place for information about native
orchid species and access to experts, photographs,
ecology, phenology, and field information to any
interested party. It is particularly useful to the public,
who may not otherwise have access to or might be
intimidated by scientific publications.
Botanical institutions nationwide, such as the
Smithsonian Institution and the U.S. Botanic Garden
(USBG), provide a type of outreach through conservation messages that regularly appear in exhibits,
particularly annual orchid exhibits, and are viewed
by their many visitors. In addition, speakers from
these institutions regularly travel around the country
discussing conservation values to likely interested
parties at orchid societies and special events across
North America. These efforts, however, are not
sufficient. Considerably more could, and should, be
done to raise public awareness about the importance
of North American native orchid species.
TARGET
15, THE NUMBER OF TRAINED PEOPLE WORKING WITH
APPROPRIATE FACILITIES SUFFICIENT ACCORDING TO NATIONAL
NEEDS, TO ACHIEVE THE TARGETS OF THIS STRATEGY
Without a centralized organization focusing on
North American orchids, it is difficult to assess how
many trained individuals work on the in situ and ex
situ conservation of orchid species. Kramer et al.
(2010) report on a U.S. survey that revealed a major
decline in botanical courses and degree programs at
universities and colleges nationwide, as well as a
deficiency of botanists at U.S. government agencies.
With fewer college graduates entering the botanical
workforce and many government botanists retiring in
the coming years, it will be difficult to increase the
number of trained people working on orchid
taxonomy and conservation.
194
Annals of the
Missouri Botanical Garden
Figure 1. Three endangered orchid species. —A. Platanthera leucophaea (Nutt.) Lindl. (photo by Timothy Bell). —B. Isotria
medeoloides (Pursh) Raf. (photo by Melissa McCormick). —C. Tolumnia bahamensis (Nash) Braem. (photo by Matt Richards).
TARGET
16,
INSTITUTIONS, NETWORKS, AND PARTNERSHIPS
FOR PLANT CONSERVATION ESTABLISHED OR STRENGTHENED
AT NATIONAL, REGIONAL, AND INTERNATIONAL LEVELS TO
ACHIEVE THE TARGETS OF THIS STRATEGY
The CPC is a successful network of botanic
institutions dedicated to preventing the extinction of
U.S. native plants by ensuring that ex situ material is
available for restoration and recovery efforts. Orchids,
however, are unique in that effective ex situ
conservation of orchids requires not just seed
banking, but also maintenance of cultures of required
mycorrhizal fungi. A network of partnerships focusing
exclusively on the needs of orchids is necessary.
THREE CASE STUDIES
As described throughout this manuscript, effective
conservation of any orchid species is a complex
undertaking that includes a wide range of variables
from long-term storage and maintenance of collections of materials (e.g., seeds and mycorrhizal fungi)
that would be required for cultivation and propagation to the establishment and maintenance of habitats
that support the long-term success of orchid
populations. For many of the reasons described
above, we are unaware of any effort that has been
fully successful in assuring the long-term survival of
any native orchid species. There are, however, a few
examples of the efforts that are necessary to build an
information base, which can support further attempts
to conserve all native orchid species.
Effective orchid conservation must integrate the
understanding of existing and future environmental
threats, taxonomic distinctiveness, numbers of individuals in populations, reproductive biology, ex situ
propagation, and the maintenance of evolutionary
processes influencing population distribution patterns. In order to do this, conservation must combine
detailed experimentation directed at continued
survival of the species both in situ and ex situ
(Ramsay & Dixon, 2003). The integrated conservation strategy emphasizes the study of interactions
among land conservation, biological management,
research and propagation and reintroduction and
habitat restoration (Hopper, 1997).
CASE
1
Platanthera leucophaea (Fig. 1A) is currently
listed as federally threatened, under the ESA, and
has declined in the United States by more than 70%
from estimates provided by original county records.
This decline has mainly been due to habitat loss.
Most of the remaining 79 populations are small, these
with fewer than 50 plants, and only 28% have
adequate protection and management (U.S. Fish and
Wildlife Service, 2007). Investigation of the orchid’s
genetics indicates that the species is primarily
outcrossing and demonstrates significant inbreeding
depression particularly prevalent in small populations (Wallace, 2003). Despite the low number of
protected populations, the outlook for conservation of
P. leucophaea is relatively good. Well-coordinated
efforts to recover this species are currently in place
and involve a network of scientists, private landowners, and volunteers (Zettler & Piskin, 2011). Fungi
needed by P. leucophaea are known, and symbiotic
germination is regularly accomplished in laboratory
cultures, although successful transplantation of
seedlings into natural populations has met with
Volume 99, Number 2
2013
Krupnick et al.
195
Status and Future of Orchid Conservation in
North America
limited success (Zettler et al., 2005; Zettler & Piskin,
2011). Genetic surveys have found that even small
populations of P. leucophaea may retain relatively
high levels of genetic diversity (Holsinger & Wallace,
2004), potentially resulting in significant seed
production and recruitment where habitat is available. This level of information about the species and
the network of public and private agencies cooperating toward the orchid’s conservation suggest that P.
leucophaea has a strong potential for recovery.
population persistence and also the founding of new
populations. This suggests that this species, many of
whose extant populations are relatively well protected, is sufficiently poorly understood and that its
maintenance in the face of a changing climate is a
serious concern.
CASE
2
In contrast to the favorable outlook for Platanthera
leucophaea, Isotria medeoloides (Fig. 1B) is listed by
NatureServe as imperiled (G2) in 14 (78%) of the 18
states and provinces in which it is still known to
occur; the orchid is thought to be historical or
extirpated in five states. Nowhere across its distributional range in eastern North America is I.
medeoloides considered secure or common. The
primary threat to its existence is destruction of its
woodland habitat for development or forestry. The
majority of its populations number fewer than 25
plants and are thus vulnerable to local extinction
(U.S. Fish and Wildlife Service, 1994). Many of the
extant populations, including some of the largest
populations, occur on land protected by federal or
state agencies or the U.S. military, and on this basis
the plant might be considered well protected (U.S.
Fish and Wildlife Service, 1994). Its preferred
habitat conditions have also been identified (Sperduto & Congalton, 1996), and searching these habitat
types allowed researchers to locate many new
populations in the late 1990s. However, the plant’s
biology throughout much of its range is defined by
many small, ephemeral populations that make it quite
difficult to target areas to protect. Additionally, long
periods of dormancy, common in many terrestrial
orchids, are characteristic of the lifecycle of this
species, making it difficult to assess population sizes
or even plant presence (Mehrhoff, 1989).
Ongoing management experiments of Isotria medeoloides are beginning to reveal a management
technique, tree thinning, which can benefit local
populations (e.g., Brumback et al., 2011). The fungi
needed by this orchid have recently been identified
(M. K. McCormick, unpubl. data), but they have so
far been resistant to culture in the laboratory. Seed
germination, either symbiotic or asymbiotic, has
never been accomplished either in the field or in
the laboratory, yet based on population demographic
studies (Mehrhoff, 1989) and preliminary genetic
analyses (M. K. McCormick, unpubl. data), recruitment from seed is critically important to both
CASE
3
An additional case study involved returning a
semiepiphytic species, Tolumnia bahamensis (Nash
ex Britton & Millsp.) Braem (Fig. 1C), to reasonably
pristine habitat, where ostensibly all the other pieces
of the ecological puzzle remain. In this case, suitable
unspoiled, historical habitat in Jonathan Dickinson
State Park in southern Florida was assessed and the
few extant plants of T. bahamensis were crosspollinated and grown ex situ at Atlanta Botanical
Garden. With most of the host plants and presumably
mycorrhizal fungi intact in the orchid’s preferred
environment, reintroduction has initially been successful. These types of enrichment reintroductions
should be attempted whenever suitable protected
habitat is available. This underscores the need for a
holistic approach to orchid conservation in which
entire habitats and ecosystems are sought to be
preserved whenever possible (Jonathan Dickinson
State Park, 2011).
THE FUTURE
OF
ORCHID CONSERVATION
International efforts such as CITES have focused
on the illegal trade of orchids and many organizations
have been established to cultivate, market, and enjoy
orchids, but there is no one national organization that
focuses on their conservation and restoration. Neither
is there one entity devoted to educating the public
about the evolutionary and ecological importance of
orchids. Organizations (e.g., federal agencies and the
U.S. military) that are mandated to identify and
protect orchids on public lands have been involved in
research on relatively few species (see examples
above), and they rely mostly on habitat conservation
for management. While habitat management is
important, ecological attributes of orchids (e.g., the
obligatory relationships between orchids and fungi at
critical life history stages) dictate that habitat
management alone will not result in orchid conservation or restoration. Every U.S. state lists at least one
orchid species that is rare or threatened and most
states list multiple orchid species. There is, however,
little coordination among states and no one organization that can provide answers to basic questions
that would guide effective management plans. Private
land-management conservation groups (e.g., The
196
Annals of the
Missouri Botanical Garden
Nature Conservancy) face a similar dilemma. Perhaps
most important, the public has little recognition of the
diversity and importance of orchids and there is no
central organization that focuses on orchids as an
important aspect of education and outreach to the
public.
We propose a possible solution to the lack of
coordination and the pooling of resources to focus on
the more than 200 native orchids listed within the
United States and Canada. The NAOCC (http://
northamericanorchidcenter.org) is the first internationally focused public–private effort to support the
conservation, cultivation, and restoration of native
orchid species. NAOCC began as a collaborative
effort between the SERC, Smithsonian Gardens,
Department of Botany at the National Museum of
Natural History (NMNH), Exhibits and Park Management Department of the National Zoological Park
(NZP), and USBG. Other government agencies,
botanic gardens, and public and private landowners
are joining the collaboration. NAOCC launched in
2012 and the network that will support the effort will
be developed over approximately 10 years.
The NAOCC’s mission is to conserve the native
orchid heritage of the United States and Canada
through preservation, restoration, and cultivation of
native orchids and to convey the importance of
NAOCC to the public through innovative educational
programs. The goals of NAOCC are to:
roles. NAOCC administration and research are based
at the SERC, which provides research services to
private and public organizations, and collaborates
with the CPC and other affiliated organizations (e.g.,
Kew Gardens and the U.S. Bureau of Land
Management’s Seeds of Success program) to develop
a genetically diverse seed bank for all native orchids.
The seed collection will not only be used to assure
the long-term survival of the germplasm of each
species, but will also serve as a resource for material
to support efforts to grow and cultivate all native
orchids. SERC is collaborating with the partners of
NAOCC to expand its collection of orchid mycorrhizal fungi to include fungi from all native orchids.
SERC is also playing a lead role in developing a
network of laboratories that provides services for the
molecular analysis of orchid fungi. The Smithsonian’s
Department of Botany at the NMNH will focus on the
development of a well-curated and complete herbarium-based orchid collection and will develop DNA
barcodes for all North American orchids. NMNH will
also develop a digital library of all North American
orchids, including visual images of all species, and
will actively partner with SERC and NAOCC to
develop web-based technologies to provide up-to-date
public access to orchid information. Smithsonian
Gardens, the Exhibits and Park Management Department of the NZP, and the USBG will coordinate
efforts to cultivate all orchids within the Washington
ecoregion into their living collections, and they will
collaborate with partner-gardens to develop and put
into effect a plan to cultivate all 210 native orchids in
a range of gardens across the United States and
Canada. The Smithsonian and the USBG will also
include exhibits about native orchids in their
biannual orchid show.
Develop an international seed bank collection, in
collaboration with the CPC, that will be representative of the genetic diversity of all North
American orchid species.
Develop an international collection of fungi
representative of the genetic diversity of mycorrhizal fungi required by native orchids.
Develop techniques to conserve the genetic
diversity of all native orchids by cultivating them
in an international network of botanic gardens and
arboretums.
Use seed and mycorrhizal fungal banks to develop
techniques for restoring, conserving, cultivating,
and restoring orchids in native habitats.
Support efforts to conserve orchid populations
through habitat conservation and restoration.
Develop web-based materials that will provide upto-date information on the ecology, conservation
status, and techniques for the cultivation of North
American orchids.
An initial goal of the network of botanic gardens is
to grow and display all native orchids in the United
States and Canada using an ecoregional approach.
The primary partners play different yet integrated
CONCLUSION
Native orchids occur in every state in the United
States and every Canadian province, and one or more
species is listed as endangered or threatened in every
state and province. As described above, national and
international efforts have provided a degree of
protection for native orchids, and there have been
efforts to conserve and restore a small number of
species. It is our view that progress toward the
effective conservation of the numerous species that
are listed as threatened or endangered will require a
large-scale integrated effort to develop the knowledge
base required to develop effective management
strategies to assure the survival of the more than
200 species of native orchids. In establishing the
NAOCC, our goal is to develop the resource base and
integration of public and private organizations
Volume 99, Number 2
2013
Krupnick et al.
197
Status and Future of Orchid Conservation in
North America
responsible for or interested in native orchids to
ultimately assure the survival of all native orchid
species. The success of NAOCC will require longterm commitments to obtain the financial support for
the research, training, and education necessary to
reach the organization’s goal of conserving the genetic
diversity of all native orchid species.
In addition to botanic gardens, research organizations, and private and public groups devoted to
orchid conservation, the success of NAOCC will also
require the establishment of a dynamic web site and
associated web-based materials that will enlist the
public in the effort. The ultimate success of NAOCC
and its partner organizations is important for other
reasons. While the orchid family is the most diverse
family of flowering plants on earth, the number of
species in the United States and Canada is relatively
small, and conserving our native orchids would be a
success that has never been obtained. Orchids are
more than just beautiful flowers. They are an
important component of North America’s ecology,
biological richness, and heritage, and they need
greater protections than they currently receive. With
so many uncertainties in the future due to habitat
degradation, urban sprawl, and climate change, it is
incumbent on organizations with the infrastructure
necessary to guide and coordinate the efforts of the
many individuals and organizations that have a stake
in native orchid preservation. NAOCC seeks to be
this important resource for North American orchid
species and ultimately to serve as a model for similar
conservation organizations in other parts of the world.
test2/pdf/Brumback_et_all_2011.pdf., accessed 5
June 2012.
Colwell, A. E. L., C. J. Sheviak & P. E. Moore. 2007. A new
Platanthera (Orchidaceae) from Yosemite National Park,
˜ 54: 86–93.
California. Madrono
Convention on Biological Diversity (CBD). 2009. Report of
the third meeting of the liaison group on the Global
Strategy for Plant Conservation. UNEP/CBD/LG-GSPC/3/
4. Dublin, Ireland. ,http://www.cbd.int/doc/meetings/pc/
gspclg-03/official/gspclg-03-04-en.pdf., accessed 5
June 2012.
Cribb, P. J., S. P. Kell, K. W. Dixon & R. L. Barrett. 2003.
Orchid conservation: A global perspective. Pp. 1–24 in
K. W. Dixon, S. P. Kell, R. L. Barrett & P. J. Cribb
(editors), Orchid Conservation. Natural History Publications, Kota Kinabalu, Sabah.
Dixon, K. W., S. P. Kell, R. L. Barrett & P. J. Cribb
(editors). 2003. Orchid Conservation. Natural History
Publications, Kota Kinabalu, Sabah.
Endangered Species Act (ESA). 1973. Publ. Law 93–205,
87 Stat. 884, as amended; 16 U.S. Code 1531–1544.
,http://epw.senate.gov/esa73.pdf., accessed 4 June
2012.
Górniak, M., O. Paun & M. W. Chase. 2010. Phylogenetic
relationships within Orchidaceae based on a low-copy
nuclear coding gene, Xdh: Congruence with organellar
and nuclear ribosomal DNA results. Molec. Phylogen.
Evol. 56: 784–795.
Gravendeel, B., A. Smithson, F. J. W. Slik & A. Schuiteman. 2004. Epiphytism and pollinator specialization:
Drivers for orchid diversity Philos. Trans., Ser. B, 359:
1523–1535.
Holsinger, K. E. & L. E. Wallace. 2004. Bayesian
approaches for the analysis of population genetic
structure: An example from Platanthera leucophaea
(Orchidaceae). Molec. Ecol. 13: 887–894.
Hopper, S. D. 1997. An Australian perspective on plant
conservation biology in practice. Pp. 255–278 in P. L.
Fiedler & P. M. Kareiva (editors), Conservation Biology
for the Coming Decade. Chapman and Hall, New York.
IUCN. 1999. IUCN guidelines for the prevention of
biodiversity loss due to biological invasion. Species
[Newsletter of the IUCN Species Survival Commission]
31–32: 28–42 [ISSN 1016-927X].
IUCN. 2011. IUCN Red List of threatened species. Gland,
Switzerland, and Cambridge, United Kingdom. ,http://
www.iucnredlist.org/., accessed 16 November 2011.
Jonathan Dickinson State Park. 2011. Jonathan Dickinson
State Park Annual Report for Tolumnia bahamensis
Conservation Activities, FDEP Permit # 5-10-56, 4
March 2011.
Kartesz, J. T. 1994. A Synonymized Checklist of the
Vascular Flora of the United States, Canada, and
Greenland. 2nd ed., 2 Vols. Timber Press, Portland.
Kindlmann, P., J. H. Willems & D. F. Whigham. 2002.
Trends and Fluctuations and Underlying Mechanisms in
Terrestrial Orchid Populations. Backhuys Publishers,
Leiden.
Kramer, A. T., B. Zorn-Arnold & K. Havens. 2010.
Assessing botanical capacity to address grand challenges
in the United States. 64 pp., plus appendices. ,http://
www.bgci.org/files/UnitedStates/BCAP/bcap_report.pdf.,
accessed 5 June 2012.
Liu, H., C.-L. Feng, Y.-B. Luo, B.-S. Chen, Z.-S. Wang &
H.-Y. Gu. 2010. Potential challenges of climate change
Literature Cited
Acevedo-Rodrı́guez, P. & M. T. Strong. 2007. Catalogue of
seed plants of the West Indies. ,http://botany.si.edu/
Antilles/WestIndies/catalog.htm., accessed 16 November 2011.
Batty, A. L., K. W. Dixon, M. Brundrett & K. Sivasithamparam. 2001. Long-term storage of mycorrhizal fungi and
seed as a tool for the conservation of endangered Western
Australian terrestrial orchids. Austral. J. Bot. 49: 1–10.
Botanical Gardens Conservation International (BGCI).
2012. Plant search database. ,http://www.bgci.org/
plant_search.php., accessed 5 June 2012.
Bowles, M., L. Zettler, T. Bell & P. Kelsey. 2005.
Relationships between soil characteristics, distribution
and restoration potential of the federal threatened eastern
prairie fringed orchid, Platanthera leucophaea (Nutt.)
Lindl. Amer. Midl. Naturalist 154: 273–285.
Brown, P. M. 2009. Personal checklist of the wild orchids of
North America, north of Mexico. N. Amer. Native Orchid
J., Special Publication No. 4.
Brumback, W. E., S. Cairns, M. B. Sperduto & C. W. Fyler.
2011. Response of an Isotria medeoloides population to
canopy thinning. Northeastern Naturalist 18: 185–196.
,http://www.fws.gov/northeast/EcologicalServices/es_
198
Annals of the
Missouri Botanical Garden
to orchid conservation in a wild orchid hotspot in
southwestern China. Bot. Rev. 76: 174–192.
McCormick, M. K., D. F. Whigham & J. P. O’Neill. 2004.
Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytol. 163: 425–438.
Mehrhoff, L. A. 1989. Reproductive vigor and environmental factors in populations of an endangered North
American orchid, Isotria medeoloides (Pursh) Rafinesque.
Biol. Conservation 47: 281–296.
NatureServe. 2011. NatureServe Explorer: An online
encyclopedia of life, ver. 7.1. ,http://www.natureserve.
org/explorer., accessed 16 November 2011.
Pemberton, R. W. & H. Liu. 2008. Potential of invasive and
native solitary specialist bee pollinators to help restore
the rare cowhorn orchid (Cyrtopodium punctatum) in
Florida. Biol. Conservation 141: 1758–1764.
Phelps, J., E. L. Webb, D. Bickford, V. Nijman & N. S.
Sodhi. 2010. Boosting CITES. Science 330: 1752–1753.
Pugh-Jones, S. 2009. In praise of Prosthechea cochleata.
Orchid Rev. 117: 28–31.
Ramsay, M. M. & K. W. Dixon. 2003. Propagation science,
recovery and translocation of terrestrial orchids. Pp. 259–
288 in K. W. Dixon, S. P. Kell, R. L. Barrett & P. J.
Cribb (editors), Orchid Conservation. Natural History
Publications, Kota Kinabalu, Sabah.
Romero-González, G. A., G. C. Fernández-Concha, R. L.
Dressler, L. K. Magrath & G. W. Argus. 2002. Orchidaceae. Pp. 490–651 in Flora of North America Editorial
Committee, (editors), Flora of North America North of
Mexico, Vol. 26. Magnoliophyta: Liliidae: Liliales and
Orchidales. Oxford University Press, New York.
Seaton, P. T., H. Hu, H. Perner & H. W. Pritchard. 2010.
Ex situ conservation of orchids in a warming world. Bot.
Rev. 76: 193–203.
Shefferson, R. P., C. C. Cowden, M. K. McCormick, T.
Yukawa, Y. Ogura-Tsujita & T. Hashimoto. 2010.
Evolution of host breadth in broad interactions: Mycorrhizal specificity in East Asian and North American
rattlesnake plantains (Goodyera spp.) and their fungal
hosts. Molec. Ecol. 19: 3008–3017.
Species at Risk Act (SARA). 2002. Canadian Species at
Risk Public Registry. ,http://www.sararegistry.gc.ca/
approach/act/sara_e.pdf., accessed 5 June 2012.
Sperduto, M. B. & R. G. Congalton. 1996. Predicting rare
orchid (small whorled pogonia) habitat using GIS.
Photogrammetric Engineering Remote Sensing. 62:
1269–1279. ,http://www.asprs.org/a/publications/pers/
96journal/november/1996_nov_1269-1279.pdf., accessed 5 June 2012.
Stewart, S. L. 2008. Orchid reintroduction in the United
States: A mini-review. N. Amer. Native Orchid J. 14: 54–
59.
Stewart, S. L. & A. Hicks. 2010. Propagation and
conservation status of the native orchids of the United
States (including selected possessions), Canada, St.
Pierre et Miquelon, and Greenland. N. Amer. Native
Orchid J. 16: 47–66.
Suffling, R. & D. Scott. 2002. Assessment of climate change
effects on Canada’s National Park System. Environm.
Monit. Assess. 74: 117–139.
Swarts, N. D. & K. W. Dixon. 2009. Terrestrial orchid
conservation in the age of extinction. Ann. Bot. 104:
543–556.
U.S. Fish and Wildlife Service. 1994. Endangered and
Threatened Wildlife and Plants; Final Rule to Reclassify
the Plant Isotria medeoloides (Small Whorled Pogonia)
from Endangered to Threatened. Federal Register 59, No.
193 (50 CFR Part 17), 6 October 1994. ,http://www.gpo.
gov/fdsys/pkg/FR-1994-10-06/html/94-24713.htm.,
accessed 8 June 2012.
U.S. Fish and Wildlife Service. 2007. Eastern Prairie
Fringed Orchid (Platanthera leucophaea) 5-Year Review:
Summary and Evaluation. Federal Register (72 FR
41348), 27 July 2007.
U.S. Government Printing Office. 2012. Electronic Code of
Federal Regulations. Title 50—Wildlife and Fisheries,
Part 17.12. ,http://ecfr.gpoaccess.gov/cgi/t/text/text-idx?
c¼ecfr&tpl¼%2Findex.tpl., accessed 8 June 2012.
USDA, NRCS. 2012. The PLANTS Database. National
Plant Data Team, Greensboro, North Carolina. ,http://
plants.usda.gov/java/., accessed 4 June 2012.
Wallace, L. E. 2003. The cost of inbreeding in Platanthera
leucophaea (Orchidaceae). Amer. J. Bot. 90: 235–242.
Waterman, R. J. & M. I. Bidartondo. 2008. Deception
above, deception below: Linking pollination and mycorrhizal biology of orchids. J. Exp. Bot. 59: 1085–1096.
WCSP. 2011. World Checklist of Selected Plant Families.
Facilitated by the Royal Botanic Gardens, Kew. ,http://
apps.kew.org/wcsp/home.do., accessed 5 June 2012.
Zettler, L. W. & K. A. Piskin. 2011. Mycorrhizal fungi from
protocorms, seedlings and mature plants of the eastern
prairie fringed orchid, Platanthera leucophaea (Nutt.)
Lindley: A comprehensive list to augment conservation.
Amer. Midl. Naturalist 166: 29–39.
Zettler, L. W., K. A. Piskin, S. L. Stewart, J. J. Hartsock, M.
L. Bowles & T. J. Bell. 2005. Protocorm mycobionts of
the federally threatened eastern prairie fringed orchid,
Platanthera leucophaea (Nutt.) Lindley, and a technique
to prompt leaf elongation in seedlings. Stud. Mycol. 53:
163–171.
Gary Krupnick