The commercial trade of propagated listed plants is a common but controversial ex situ conservation approach for rare plant species. We investigated the Internet trade of plants protected under the U.S. Endangered Species Act to determine their availability for interstate (i.e., regulated) commerce. We identified 49 listed plant species that were available via the Internet, with less than 10% of vendors having obtained the required federal permit. The lack of permits among vendors suggests that sellers are unaware or ignore regulations. Illegal trade undermines both the permitting process and conservation efforts of the U.S. Fish and Wildlife Service to ensure that commercial propagation aids the long-term survival of listed species. Furthermore, in addition to supplying a demand for plant collections and landscaping, commercial trade could provide a source of plants for deliberate species introductions, including assisted colonization—a debated conservation strategy that involves moving species to new environments to mitigate for habitat loss and climate change. Given the potential costs and benefits associated with trade, the challenges suggest that a collaborative approach between agencies, nurseries, and plant collectors is needed to regulate the trade of listed plants. In regulating commercial trade, policymakers and conservation biologists may want to consider potential risks and benefits of private efforts to recover species.
Worldwide, thousands of plants are threatened or endangered for reasons including habitat loss, population fragmentation, taking due to collection, vandalism, or harvest, and introduction of nonnative species (McMahan 1980; Falk & Holsinger 1991; Falk & Olwell 1992; Given 1994). Several strategies have been used to conserve these plants, including legal and physical protection (i.e., in situ conservation; Maxted et al. 1997), seed banking (Guerrant et al. 2004), and propagation (i.e., ex situ conservation; Hawkes et al. 2000; Havens et al. 2006). In addition to these strategies, controversial ex situ approaches for conserving rare plant species include commercial propagation and trade (Affolter 1997), landscaping with rare species for collection or expressed conservation (Reinartz 1995), and assisted colonization (Vitt et al. 2010).
Plants are introduced by the commercial trade because they can provide food, fiber, or forage; have attractive features, or offer medicinal properties (Winter & Botha 1994; Affolter 1997; Kennedy 2008). In contrast, some species lack commercial potential because they have none of these attributes or are difficult to propagate. For threatened or endangered plants that are marketable, legitimate conservation arguments can be made for and against their commercial trade (Table 1). These potential benefits and risks of commercial trade make decisions concerning regulation particularly challenging, demonstrating why commercial activity involving listed plant species is not outlawed, but highlighting why it is regulated.
Table 1. Benefits and risks associated with the commercial trade of endangered plants
Reasons for allowing the commercial trade of endangered plants
Some endangered plants have been conserved by propagation and distribution (Affolter 1997)
The Franklin tree is extinct in the wild, but exists in cultivation (Evans & Bohn 1986; Falk & McMahan 1988; Jenkins & Oldfield 1992)
Propagation can reduce collecting pressure on wild populations by providing an alternate source of plants (Read 1989; Winter & Botha 1994; Affolter 1997; Entwistle et al. 2002; Kay et al. 2011)
The Tennessee coneflower was delisted because 20 new colonies were established in the species’ historic range; cultivation in botanical gardens and native plant nurseries provided a source of plants for reestablishing the 20 wild colonies required for delisting the species while also providing a commercial source of plants to reduce likelihood of collecting from the wild (76 FR 46632)
Promotes “backyard” conservation efforts and endangered species education (Reinartz 1995)
FWS encouraged propagation and distribution of Virginia round-leaf birch due to decline in the wild from habitat loss, vandalism, and collecting (59 FR 59173)
Provide a novel source of funding to supplement endangered plant conservation (e.g., botanical garden sales)
Fewer than 100 mature trees of Wollemi pine exist in the wild, but an extensive effort from a public–private partnership resulted in the plant being propagated and distributed around the world; royalties from these sales support conservation of the wild population (www.wollemipine.com; Offord & Meagher 2006; Trueman et al. 2007)
Reasons for regulating the commercial trade of endangered plants
Encourages the over-exploitation of wild populations by encouraging harvest of plants or seeds for sale or propagation (McMahan 1980; Coggins & Harris 1987; Read 1989; Jenkins & Oldfield 1992; Luken 2005)
In Hawaii, the lack of law enforcement preventing illegal seed and tree collection contributed to the continued decline of this rare lo'ulu palm (Burney & Burney 2007). Most species of lo'ulu are sold in commercial trade (Chapin et al. 2004).
Cacti are vulnerable to wild collection due to hobbyists (wild plants are older and have larger flowers) and the increased interest in drought-tolerant plants for landscaping (xeriscaping); the increased demand resulted in increased collection and export of wild plants from Texas and Mexico to Arizona (Robbins 2003).
Could adversely impact the gene pool of species through either cultivation of limited numbers of individuals from the wild population (i.e., founder effect) or anthropogenic hybridization (i.e., gene transfer) (Maunder 1992; Rhymer & Simberloff 1996; Whitham & Maschinski 1996; Ricciardi & Simberloff 2009)
In Hawaii, two endangered species of Hibiscadelphus that had natural allopatric distributions were brought together in Hawaii Volcanoes National Park to help preserve each species. Cross-fertilization created a vigorous hybrid population that was eliminated in addition to eliminating the introduced H. hualalaiensis to protect remaining H. giffardianus trees (Baker & Allen 1977)
Introduction of cultivated species to new locations where they can naturalize and may inadvertently become pests (Reichard & White 2001; Ricciardi & Simberloff 2009; Bradley et al. 2012); though the probability of intra-continental transfers or rare plants becoming invasive is low (Gordon & Gantz 2008; Mueller & Hellmann 2008), risk should be evaluated (Reichard et al. 2012)
Swollen bladderwort is an aquatic, carnivorous plant that is traded by aquatic gardeners and carnivorous plant enthusiasts because of its showy yellow flowers and bladders that trap invertebrates. It is rare in portions of its native range and protected as endangered in Maryland and as a species of special concern in Tennessee. In Washington state where it has been introduced, the swollen bladderwort has recently been listed as a noxious weed (USDA plants profile database, http://plants.usda.gov)
On the Hawaiian Islands, the ohai or riverhemp is an endangered plant threatened by habitat destruction and nonnative species, including hybridization with introduced species of Sesbania. However, in Puerto Rico where there is a native Sesbania species, the introduced S. tomentosa has become naturalized in at least two locations (www.centerforplantconservation.org)
Transporting and introducing pests and pathogens (Read 1989; Maunder 1992; Brasier 2008; Garbelotto & Pautasso 2012)
Undescribed water mold and fungal pathogen species spread through the ornamental plant trade could pose a threat to wild populations because the ecology of many plants and their pathogens is relatively unknown (Moralejo et al. 2009). The combination of human and natural spread of pathogens makes prediction challenging. Therefore, risk should be taken into account when moving plants and planning reintroduction and assisted colonization efforts (Garbelotto & Pautasso 2012).
Regulation of activities associated with the plant trade is an important and emerging topic for conservation efforts at local (wild collection of state-listed plants; Luken 2005), regional (wild-dug plants from Texas to fulfill xeriscaping demand in Arizona; Robbins 2003), and international scales (wild-dug plants sold at border markets, Phelps et al. 2010; global trade and plant invasions, Bradley et al. 2012). While examining the movement of endangered species outside their historical range as examples of assisted colonization in the United States (Shirey & Lamberti 2010), we noted that some plants listed as threatened or endangered (hereinafter listed) under the U.S. Endangered Species Act were being offered for sale across states via the Internet without the required permit. We then called for increased attention to the trade of listed plants, the unregulated, purposeful creation of hybrids from listed plants, and the uncoordinated rare plant distribution through commercial trade and citizen-initiated assisted colonization (Shirey & Lamberti 2011). We are following that comment with details in this manuscript, first reviewing the U.S. federal laws that apply to commercial trade of listed plants. We then investigate the species of plants being sold via the Internet by asking: if someone wants to purchase a listed plant, how many such species are being sold or advertised online for interstate commerce in the United States? Furthermore, are the vendors of such species obtaining the proper permits needed to sell such species in interstate commerce? Finally, we suggest options for the federal government and private entities to cooperate to maximize benefits and minimize risks of commercial trade in listed plants.
U.S. regulations of endangered plant commerce
The U.S. Endangered Species Act (ESA; 16 USC §1531 et seq.) does not prohibit intrastate commercial sales of listed plants, the transport and transplant of privately owned listed plants or destroying listed plants in areas not under Federal jurisdiction (McMahan 1980; Campbell 1988; Falk & Olwell 1992; McDonald 1996). In other words, a listed plant could be purchased in one state and then transported to another state without violating the ESA, so long as the plant was taken from and planted on property not under Federal jurisdiction, such as private property. Furthermore, the ESA does not prohibit an individual from giving listed plants as a gift to someone in another state so long as a change in plant ownership is not in the pursuit of gain or profit. However, any violation of a state law in the process of purchasing, transporting, or transplanting plants would trigger additional violations of the ESA and Lacey Act (16 USC §§3371–3378).
Federal law does regulate interstate commerce of both cultivated and wild-collected listed plants—a permit is required before selling a cultivated plant in interstate commerce. Offering a listed plant for sale in interstate commerce also requires this permit, but an exception is provided: advertising a plant for sale in interstate commerce without a permit is permissible and not considered an offer for sale providing a warning is given that “no sale may be consummated until a permit has been obtained” from FWS (50 CFR §17.61 for endangered plants & §17.71 for threatened plants); though “seeds of cultivated specimens of species treated as threatened shall be exempt from all the provisions of §17.61, provided that a statement that the seeds are of ‘cultivated origin’ accompanies the seeds” (50 CFR §17.71). In 1977, the U.S. Fish and Wildlife Service (FWS) published an extensive statement in the U.S. Federal Register explaining the regulations, which were a compromise between a full ban on commercial trade and no regulation, summarized as follows:
The Service recognizes the beneficial and educational aspects of activities with seeds and cultivated plants, which generally enhance the propagation of the species, and therefore would satisfy permit requirements under the Act. The Service intends to monitor the interstate and foreign commerce and import and export of endangered and threatened plants in a manner which will not inhibit such activities, providing that the activities do not represent a threat to the survival of species in the wild (USFWS 1977).
Though the primary threat to listed plants is habitat destruction, such threats to wild populations from commercial trade might include overexploitation, genetic effects, or hybridization (Box 1), risk of invasiveness in new environments, and introduction of pests or pathogens (Table 1). The FWS recognized the potential benefits of commercial trade, including reducing collecting pressure on wild populations, creating reservoirs for reintroduction and restoration, and encouraging the survival of species germplasm in cultivation (USFWS 1977). Thus, federal regulations do not prohibit commercial trade, but do require that sellers of cultivated listed plants and seeds from endangered plants apply for a $100 permit from the FWS (50 CFR §17.62 & §17.72; www.fws.gov/forms/3–200–55.pdf). The permit requirement helps to ensure that interstate commerce contributes to the species’ recovery by enhancing propagation or survival (50 CFR §17.62 & §17.72), which can be as active as providing plants for restoration, or as passive as promoting appreciation of the species through consumer education (USFWS 1977). The FWS implemented these restrictions because collection and trade have contributed to the decline of some wild plant populations despite laws protecting plants (McMahan 1980; Coggin & Harris 1987), in part because of the enforcement challenge even when plants are growing in protected areas (e.g., the illegal collection of state-listed Venus fly trap; Luken 2005). In addition, there are practical challenges distinguishing listed from unlisted species (McMahan 1980) and wild from cultivated plants.
Box 1: Listed species and hybridization: issues for conservation policy
Hybridization has been important (1) for the ecology and evolution of plants, (2) as a source of economically important plants (e.g., crops and ornamentals), (3) for biodiversity and unique community interactions, and (4) as a catalyst for speciation in other organisms; conversely, hybridization also poses risks to rare plant species including (1) introgression that reduces genetic diversity, (2) reductions in fitness due to outbreeding depression, (3) contaminating ex situ gene pools for future reintroduction or restoration, and (4) reduced legal protection (Whitham & Maschinski 1996; Soltis & Gitzendanner 1999; Allendorf et al. 2001; Guerrant et al. 2004). Generally, the conservation value of hybrids increases as a function of time since the hybridization event (Travis et al. 2008). Both in situ and ex situ hybridization caused by commercial trade and assisted species movements contributes to conservation concerns about unintentional or intentional introgression (Baker & Allen 1977; Rhymer & Simberloff 1996; Guerrant et al. 2004; Carlson & Meinke 2008; Weeks et al. 2011). For example, some endangered Pritchardia species are being cultivated, offered in commercial trade, and planted outside their historic range near other endangered Pritchardia species, increasing the risk of unintentional ex situ hybridization resulting from artificial sympatry (Chapin et al. 2004).
In the United States, interstate commerce and trade involving natural or anthropogenic hybrids of listed plant species is unregulated. As a matter of policy, the FWS considers the intentional hybridization of listed species to be contrary to the purposes of the ESA unless necessary to preserve genetically viable populations (library.fws.gov/IA_Pubs/esa_permits.pdf), though there are no restrictions in the ESA or FWS regulations to discourage the creation of hybrids to avoid compliance with the permit requirements for interstate commerce. For example, Tennessee coneflower can hybridize with other Echinacea species (Ault 2006); in 2003, a seed company introduced a cultivated commercial hybrid to the nursery trade. Cultivated hybrid coneflowers are known to cross-pollinate with natural populations if hybrid plants are grown within pollinating distance (van Gaal et al. 1998; Walck et al. 2002), termed “genetic pollution” (Ault 2006). The FWS does not view cultivated hybrids as a threat to wild Tennessee coneflower “because planting of (hybrid) individuals is not allowed on public and state owned property where wild populations occur” (76 FR 46646). However, one protected Tennessee coneflower population lies within fragmented habitat bordered by private property, including housing developments in an area where the hybrid is sold (Figure 2). Any private planting of hybrid plants believed to be Tennessee coneflower within pollinating distance of wild populations could pose a risk of cross-pollination.
In addition to concerns over unintentional and intentional ex situ introgression, naturally occurring rare hybrids under threat of commercial trade, such as Lloyd's hedgehog cactus (Echinocereus × roetteri), could benefit by being protected under the ESA (Allendorf et al. 2001). The FWS proposed an official hybrid policy in the 1990s that was not completely adopted, in part because of controversy over protecting hybrids and the challenge of making the policy flexible enough to include the risks and benefits of hybridization (Allendorf et al. 2001; Ellstrand et al. 2010).
Citizen-initiated assisted colonization
The commercial trade of listed plants also increases the potential for individuals and citizen groups to move listed plant species for collections, landscaping, or conservation purposes, such as assisted colonization. Assisted colonization is the intentional movement of a species or genotype to a location outside of its documented native range where the species could survive under current or future climate and land-use scenarios (Hunter 2007); assisted colonization has also been referred to as assisted migration (McLachlan et al. 2007) and managed relocation, with variations and definitions discussed by Schwartz et al. (2012). Translocation and reintroduction have been performed in the past for listed plant conservation and scientific research (Falk & McMahan 1988; Gordon 1994; Gordon 1996; Wendelberger et al. 2008). However, assisted colonization has been proposed as a specific management option to move species with poor dispersal abilities to disconnected habitats, subject to changing climate, and land use (Hoegh-Guldberg et al. 2008; Richardson et al. 2009).
Although most efforts remain in the proposal stage for a variety of plants (e.g., Vitt et al. 2010), assisted colonization has been carried out by (1) governments and scientists as a last resort for species preservation [e.g., Virginia round-leaf birch (Betula uber) planted on public land and distributed commercially for landscaping in the United States (Shirey & Lamberti 2010)]; (2) by scientists during climate change adaptation experiments [e.g., understory forest herbs purchased from southern France and planted in Belgium (Van der Veken et al. 2012)]; and (3) by private citizen groups [e.g., Torreya Guardians]. In the United States, the structure of the Endangered Species Act, coupled with inadequate funding for endangered plant conservation, has encouraged citizens to undertake plant conservation, especially for charismatic plants threatened by climate change. For example, the Torreya Guardians have obtained plants and seeds of Florida torreya (Torreya taxifolia), and moved seedlings and saplings to the southern Appalachian Mountains, outside of the species’ historic range (McLachlan et al. 2007; www.torreyaguardians.org). The population of T. taxifolia declined by 98% during the last century due to disease and poor recruitment, making restoration in its historic range difficult (Schwartz et al. 2000). The Torreya Guardians argued for moving T. taxifolia northward where it may have thrived during the last peak interglacial because its current range is restricted by human-caused extinctions of seed dispersers (Barlow 2009). Establishing experimental populations of T. taxifolia through assisted colonization was discussed by conservation biologists over 20 years ago (Falk 1990), but never materialized. However, public and private organizations took measures to conserve T. taxifolia and study why it was declining in the wild (Affolter 1997). Specifically, the Center for Plant Conservation (http://www.centerforplantconservation.org) led an extensive effort to document locations of all known plants and coordinate ex situ conservation in botanical gardens to ensure survival of the species (USFWS 2010b). In contrast to accepted ex situ conservation practices (Haskins & Keel 2012), the Torreya Guardians established private experimental populations on the property of cooperative landowners to help preserve the species outside of its historic range because of its decline, lack of federal funding, and the availability of privately owned and commercially available plants and seeds.
While no other groups or individuals have announced projects similar in scope, this disconnect between accepted conservation practice and what the law allows creates a loophole wherein individuals involved in such projects are not required to consider the potential negative impacts of plant movement (Box 2; Figure 1). Whether through coordinated projects or uncoordinated distribution, commercial trade of listed plants adds risks and challenges for plant conservation (Table 1). In fact, commercial nurseries around the world have expanded their plant distribution, giving marketable species a potential head start on climate change (Van der Veken et al. 2008), but also increasing the risks of unintended consequences for conservation. Therefore, establishing which species are available in commercial trade could aid conservation management and education efforts (Bradley et al. 2012).
Box 2: Potential conservation issues associated with assisted colonization
The strategy of using assisted colonization for conservation is replete with scientific and legal issues (Hewitt et al. 2011). First, because establishing populations can be notoriously challenging for rare species, even in recently occupied habitat (Falk et al. 1996; Guerrant & Kaye 2007), this approach is likely restricted to species that are easier to propagate (i.e., commercially or by botanical gardens; Reinartz 1995). Second, assisted colonization may detract from efforts to conserve plants in their existing habitats (Falk & Olwell 1992; Allen 1994) and divert resources from other conservation projects (Haskins & Keel 2012). For example, rare and endangered orchids in southwestern China were moved to a higher elevation outside of their range, but less than 30 km from the source population, to avoid flooding by a hydroelectric project on the Hongshui River (Liu et al. 2012); while imminent development may force rescue of endangered plants, such projects could encourage moving species in the name of climate change to mitigate for development and mislead the public and policymakers into thinking that mitigation can always replace in situ conservation (Falk & Olwell 1992; Allen 1994; Haskins & Keel 2012). Third, assisted colonization may conflict with laws when organisms are transported across political borders. For example, state-level endangered species laws in the United States differ in protecting of endangered plants and regulating commercial trade with some providing little or no protection and others strictly regulating commerce and plant movement (McMahan 1980; Goble et al. 1999). In addition, even though state laws apply in some instances, few states extend legal protection to all plants listed under the federal ESA (McMahan 1980). Finally, under U.S. federal law, citizens who move a listed plant are not constrained by the same assessment process as the federal government—their actions are legal under the ESA without a review of their plans (Figure 1; McDonald 1996).
Quantifying commercial availability
From October 2009 to January 2011 we used Google's search engine (www.google.com; Wilson et al. 2007) to quantify the number of federally listed threatened and endangered plant species being offered for sale online. We searched for the 753 plant species listed under the ESA in October 2009 (http://www.fws.gov/endangered/) using both common name and scientific name with the phrases “plants for sale,” “seeds for sale,” and “add to cart,” restricting searches to the top 50 page hits. We also performed automatic searches of online auction listings (i.e., eBay.com). Synonyms of scientific and common names were included in our search, given that some species, especially cacti, have had multiple taxonomic names. Because we found some evidence for misspellings of species names, these were also included in our searches. To determine whether sellers obtained the proper permit, we compared species being offered for sale in interstate commerce with permit notices for species in the U.S. Federal Register by searching the U.S. Government Printing Office database (www.gpo.gov). Because our survey is limited to Internet availability of listed species, we are likely underestimating the species available commercially, since sales would likely be augmented by local and international sales from collectors, botanic gardens, and nurseries (Robbins 2003). In addition, we have not surveyed over 2,000 critically imperiled (G1) or imperiled (G2) rare plant taxa in the United States that are potentially more vulnerable to the risks of commercial trade (McMahan 1980) because they are not legally protected under the ESA (Schwartz 2008). We have also not surveyed the number of actual sales of listed plants, the number of individual plants or seeds involved in sales, or whether the sales of listed plants are having a detrimental impact on the status and conservation of wild populations of the species involved.
In our survey of listed plants, we assumed an offer to sell a plant was potentially interstate if (1) the plant could be added to an online “cart,” (2) the plant is offered on an auction website without restricting to local pickup, or (3) the seller ships interstate and does not specify either that the listed plant cannot be sold interstate, or that the offer for sale is contingent on receiving a permit from FWS. We found that plants and seeds of 49 federally listed species and seven hybrids were being offered online through interstate commerce (Tables 2 and 3), often by multiple sellers. Of the 49 species, 29 were offered for sale on eBay and 41 were offered for sale from states outside of their native range (Tables 2 and 3). Only 26% of listings described the plant as listed (threatened or endangered), with some sellers instead describing plants as “rare” or “very rare.” In addition to interstate sales, a further 52 species were offered for intrastrate sale (not federally regulated), either advertised online for in-store purchase or available for online purchase to individuals with an in-state address; the vast majority of species offered for intrastate sale were in California or Hawaii. Of those offered intrastate, some were through botanical gardens to promote education on endangered native species conservation and raise money for conservation efforts; others were offered for sale by nurseries that explained that they could not sell federally listed plants interstate because they did not have a permit to ship interstate (see Affolter 1997). We also found that 18 species were offered online from points of origin outside of the United States with 10 listed under the Convention on International Trade in Endangered Species (CITES; http://www.cites.org/). Of the species offered for sale in interstate commerce, some have been commercially propagated and available for decades, including swamp pink (Helonias bullata), Chapman's rhododendron (Rhododendron chapmanii), and star cactus (Astrophytum asterias) (McMahan 1987). However, many of the taxa that were available for purchase have also been threatened by over-collecting in addition to the primary threat of habitat loss (McMahan 1980, 1987; Robbins 2003). Sellers varied in size from individuals propagating or collecting plants and seeds to large nurseries capable of producing thousands of plants for some species. Only 4 U.S. sellers out of more than 50 evaluated had obtained the proper interstate commerce permits (Box 3), making the majority of interstate offers for sale illegal (>90% of vendors).
Table 2. Endangered species listed under the U.S. Endangered Species Act being offered for sale in interstate commerce. While some sellers only offer these species intrastate, at least one seller offered plant material in interstate commerce
Species common name
Approx. number remaining
Average annual funding
*Offered for sale only with an interstate commerce permit; D = Delisted; P = plants; S = seeds; H = hybrid; average annual funding is over the previous 10 years reported (Fiscal Year 2001–2010), including state and federal expenditures, but not land acquisition costs; list of state abbreviations: http://en.wikipedia.org/wiki/List_of_U.S._state_abbreviations; hybrid seeds of Lilium occidentale were also sold interstate.
Table 3. Threatened species listed under the U.S. Endangered Species Act being offered for sale in interstate commerce
Species common name
Approx. number remaining
Average annual funding
*Offered for sale only with an interstate commerce permit; D = Delisted; P = plants; S = seeds; H = hybrid; average annual funding is over the previous 10 years reported (Fiscal Year 2001–2010), including state and federal expenditures, but not land acquisition costs.
The general lack of permits among vendors suggests that interstate commerce regulations are not being enforced, or those sellers are unaware or ignore regulations. All of these potential reasons have important implications for conservation. While in this study we did not survey the sellers, surveys of commercial seed collectors and growers of rare plants in Canada suggested that plants and seeds are obtained by both legal and illegal collecting (Morris 2010). The conservation challenges suggest that a collaborative approach between agencies, the nursery industry, and plant collectors is needed to regulate the trade of listed plants. Furthermore, public education is needed to address the plight of listed species (McMahan 1980), and the risks and challenges of cultivation, sale, purchase, and movement of listed plants by private citizens, similar to concerns raised for state-listed species (Reinartz 1995).
Commercial propagation and species conservation
Partnership with the nursery industry is important for ex situ plant conservation to ensure that the propagation and trade of listed species benefits the long-term survival of the species without harming wild populations or their habitats (Evans & Bohn 1986; Reinartz 1995; Affolter 1997; Trueman et al. 2007). Nurseries wanting to sell plants through interstate commerce are required to obtain a permit from the FWS. We speculate that the $100 fee plus the paperwork and risk of being declined may stop individuals and small nurseries from applying. The FWS could reward compliant nurseries by (1) offering an electronic application as an option to facilitate the permitting process, (2) working with nurseries to help satisfy the requirements to obtain a permit, (3) providing them with business if propagated plants are needed for restoring wild populations, or otherwise certifying nurseries that comply with agency requirements as a plant source for restoration efforts outside of federal jurisdiction (Robbins 2003), and (4) deciding whether to enforce the permit requirements for noncompliant market participants, such as when there exists indication of concurrent collecting of plants in wild populations (e.g., Key tree-cactus Pilosocereus robinii sold on eBay in 2006, USFWS 2010a; illegal harvest and sale of Pritchardia viscosa seeds from the wild population, Burney & Burney 2007).
When submitting the permit application (FWS permit form 3–200–55), applicants can help the FWS and plant conservation by participating in a voluntary, cooperative propagation program where they contribute data and specimens to species recovery efforts. Indeed, nurseries and nonprofit propagation efforts that comply with the ESA permit requirements have worked with conservation biologists in government and nonprofit organizations to inform recovery efforts and supply propagated plants for population restoration (Box 3). Applicants planning large-scale propagation may also want to voluntarily contribute a portion of profits from sales of listed plants to conservation of species in the wild as good will; though there is no regulatory requirement or structure under the ESA, in Australia the royalties from sales of Wollemi pine (Wollemia nobilis), propagated by a commercial forest grower under a public–private agreement, contribute to funding conservation of the wild population and other endangered plants (Offord & Meagher 2006; Trueman et al. 2007). While this ex situ conservation approach was, in part, to discourage potential illegal seed and plant collecting, the propagation of Wollemi pine was a thoroughly planned, decade-long, collaborative scientific process that considered genetic diversity, researched propagation techniques, and evaluated the associated pests and pathogens (Trueman et al. 2007). This approach required significant investment in infrastructure and research that delayed revenue, but it also helped establish an ex situ collection that returns benefits to the in situ population. These examples of cooperative conservation through public–private partnerships show that (1) legal commercial propagation and distribution of listed plant species is possible under endangered species laws, and (2) private, commercial interests can contribute to species conservation efforts when conservation and legal guidelines are followed (Box 3; Evans & Bohn 1986; Reinartz 1995; Robbins 2000; Entwistle et al. 2002).
Entities that propagate plants, including small nurseries and individuals, can have an important role to play in the ex situ conservation of rare species (Falk & McMahan 1988; Morris 2010), and therefore assume a great responsibility in species survival (Evans & Bohn 1986). These caretakers of cultivated plants can help support future conservation of wild populations and genotypes as the genetic diversity and numbers of cultivated populations of some species now exceed wild populations (Koontz et al. 2001; Chapin et al. 2004; Asmussen-Lange et al. 2011). Propagators can manage this responsibility by following propagation standards developed for ex situ conservation by government agencies (e.g., USFWS, USDA, U.S. Bureau of Land Management Native Plant Materials Development Program & Seeds of Success), the Center for Plant Conservation, botanical gardens, and restoration nurseries. For example, one of the recommended standards is to maintain provenance (geographic locality) records of plant origin by geo-referencing original plant sources and indexing this information (Falk et al. 1996; Guerrant et al. 2004; Vitt et al. 2010; Maschinski & Haskins 2012). Provenance records are critical when species are rare in the wild, because species purity is important to preserve in cultivation, and genotypic diversity could act as biological insurance against environmental fluctuations (Pavlik et al. 1993; Gordon 1994; Bischoff et al. 2010). This controlled propagation approach is especially important if reintroduction is deemed necessary to perpetuate wild populations, because (1) care must be taken to avoid introgression and hybridization from artificial sympatry (Evans & Bohn 1986; Koontz et al. 2001; Box 1); (2) using cultivated stock is almost always preferable to transplanting wild populations (Falk et al. 1996), and (3) these entities can produce large numbers of seedlings (Maunder 1992).
Box 3: Collaboration contributing to conservation
Of over 50 sellers offering listed plants in interstate commerce, the 4 permit holders included two conservation organizations that grow carnivorous plants to help propagate species and assist conservation efforts (International Carnivorous Plant Society; Meadowview Biological Research Station), a native-plant nursery that grew thousands of Tennessee coneflower plants to help re-establish populations at monitored sites in the species’ native range (Sunlight Gardens), and a cactus grower who has worked with government agencies since 1985 (Mesa Garden). The delisting of Tennessee coneflower by the FWS on September 2, 2011, highlights an example of coordinated efforts by conservation biologists, government agencies, nonprofit organizations, and commercial nurseries to undertake research, protect land, propagate plants, and restore populations over a period of 30 years (76 FR 46632; Bowen 2011). The Tennessee coneflower is a naturally rare species that was listed as endangered in 1979, and is limited in its ability to colonize new cedar glades or limestone barrens (Walck et al. 2002). The cultivation of Tennessee coneflower in botanical gardens and native plant nurseries like Sunlight Gardens provided a source of plants for establishing the 20 additional wild colonies required for delisting the species while also providing a commercial source of plants to reduce the likelihood of collecting from the wild. Similarly, the owner of Mesa Garden has worked with the FWS to propagate rare cacti to restore populations, such as Knowlton's cactus (Olwell et al. 1986), while also providing collectors with a source of propagated plants and seeds (Anderson 2001). In cooperating with the FWS, Mesa Garden has provided government agencies and nonprofit organizations with vital resources for restoring wild populations, including propagated cacti, location data, germination requirements, and disease risks (Olwell et al. 1986; Falk & McMahan 1988).
Regulatory and management implications
Policymakers may want to evaluate endangered species regulation and education in light of what constitutes a potentially challenging set of circumstances: (1) the flexible laws that enable potentially risky citizen-initiated projects (Figure 1), (2) the legal and illegal Internet trade (Tables 2 and 3), (3) the creation of hybrids from listed species (Box 1), which could be used to evade laws for listed species, and (4) the uncoordinated distribution of listed species and their hybrids (Figure 2). The outcome of such trade and distribution for listed plants could be positive for conservation efforts in some instances, but cooperation, appropriate conservation guidelines, and regulation are still needed because of the risks (Table 1). Questions remain regarding whether (1) the illegal interstate trade of listed plants could undermine the efforts of nurseries that obtain proper permits and work with the FWS to propagate species and restore wild populations; (2) to revisit previous discussions on proposals to regulate natural and human-produced hybrids that have not been completely adopted; and (3) the trade in rare plants could lead to unintended consequences from unmonitored and haphazard introductions of species, such as transport of pathogens. If conservation guidelines are followed to minimize risks, the conservation community may be able to maximize benefits of commercial propagation for threatened or endangered plants (Reinartz 1995; Trueman et al. 2007; Kay et al. 2011): (1) propagation, legal commercial trade, and distribution of listed plants could help inform conservation and recovery of populations if monitored and documented by a central authority such as the FWS, and (2) private efforts to propagate listed plants could have positive outcomes, especially if wild populations are already extirpated.
Other researchers have suggested that if existing national and international laws on plant commerce are enforced, voluntary compliance that is reinforced through public education and commercial partnership may be more practical than new restrictions on commercial trade (Reinartz 1995; Robbins 2000; Burkhart et al. 2012). However, participants in commercial trade of listed plants are required by law to abide by existing regulations, not only vendors and consumers, but also the shipping companies that transport plants and the websites that facilitate the sales of plants. For example, online marketplace and auction websites that profit from such sales may want to require vendors to provide digital scans of appropriate permits and phytosanitary certificates if they allow sales of such listed species. Such permits include those needed for local (state agencies), interstate (FWS or USDA in United States), or international trade (CITES).
The lack of authority within the ESA to regulate intrastate sales of listed plants (16 USC §1531 et seq.; USFWS 1997) and the lack of restrictions on noncommercial interstate movement of species (50 CFR §17.61 & §17.71) create a loophole for citizen-initiated assisted colonization that may need to be evaluated, because individuals can and do legally and illegally move listed plant species (Figure 2). While in the U.S. individual state laws also apply to plant movement in some instances (Goble et al. 1999), the challenges facing the regulation of plant movement by state government is daunting and likely unenforceable beyond plant sales. In addition, conservation biologists and agencies are not adequately prepared to assess citizen-initiated assisted colonization (Kennedy et al. 2012). State agencies may want to consider the regulatory context and policies for working with nurseries, managing commercial trade, and addressing the complex issues surrounding assisted colonization.
While introduced populations originating from cultivated plants may benefit conservation efforts in some instances (e.g., Delphinium luteum; Koontz et al. 2001), the practical contributions to species recovery efforts of landscaping with listed plants are limited because of unknown failure rates, and a lack of coordination, monitoring, and reporting. This is not to suggest that citizens have no role to play in plant conservation and management of biodiversity (Table 4). As a profession, conservation scientists can first encourage the use of propagated common native plants produced with local germplasm in gardening and landscaping (Tallamy 2009), which has the added benefit of increasing the biodiversity of other taxa, including insects and birds (Burghardt et al. 2009, 2010; Tallamy & Shropshire 2009).
Table 4. Options for capturing the enthusiasm of individuals and groups that care about threatened and endangered species
Citizen science—Anecdotal evidence from Internet forums suggests that a strong desire to conserve endangered plants exists among the buyers of listed plants. Research on the culture of such enthusiasts determined that key individuals who collect, grow, and distribute rare plants, could represent a wealth of information on rare species (Morris 2010).
Conservation biologists can put this enthusiasm to good use by involving the public in endangered plant conservation. Examples include the active training of citizen scientists to monitor rare plant populations at the Lady Bird Johnson Wildflower Center at the University of Texas and the Plants of Concern program at the Chicago Botanic Garden (Havens et al. 2012).
Private land conservation—The U.S. Endangered Species Act provides flexibility for working with landowners to identify habitat for listed plant species when landowners are approached respectfully and educated on how the ESA applies to plants (Janssen & Williamson 1996). In a recent survey in Oregon, only 53% of rural landowners knew that federally listed plants are not protected on private lands; this survey also suggested that many rural landowners are willing to provide habitat for listed species (Kaye et al. 2011).
Some private landowners have taken the initiative to restore populations of listed species. As an example, Texas landowner J. David Bamberger has dedicated resources to restore Texas snowbells in its historic range, spending his own money and receiving a grant to survey private land, propagate snowbells, and restore populations. While initially skeptical of planting endangered species on their property, 24 landowners have joined efforts to voluntarily manage Texas snowbells, in part because of the legal flexibility (Best 2011).
Digital repositories—Collecting and sharing information on localities where commercially propagated listed plants have been legally obtained, transplanted, and survived within and outside historic ranges could help to identify locations for potential introductions. However, there are no requirements, policy guidelines, or mechanisms under the ESA for the Fish and Wildlife Service to track private propagation, reintroduction, and augmentation efforts (McDonald 1996). The expansion and availability of the Internet makes this approach possible, but a coordinated approach is needed to inform conservation.
Reinhartz (1995) suggested developing a species database that would allow reporting of planting sites of commercially traded species and encouraging cooperation among agencies, commercial growers with permits, and landowners who purchase and plant listed species. For larger, coordinated introduction efforts by conservation biologists, the Center for Plant Conservation maintains an online Reintroduction Registry for rare plant species to catalog past reintroductions and inform future conservation efforts; to protect wild plants and respect landowner confidentiality, detailed plant location information is not disclosed.
Globally, scientists have just recently started to assess the potential for assisted colonization to mitigate for climate change by conducting experiments with plants (Liu et al. 2012; Moir et al. 2012; Roncal et al. 2012), including plants propagated in commercial nurseries (Van der Veken et al. 2012). While these experiments have shown some potential for conservation, similar reintroduction efforts for rare plants that failed many years after initial indications of success (e.g., Allen 1994) underscore the need for thoughtful discourse on approaches for commercial propagation, the Internet trade of listed plants, and the implications of assisted colonization, especially citizen-initiated translocations or reintroductions of species; this discourse is also imperative so that broader conservation efforts are not subverted by well-intentioned but risky individual projects (Maschinski & Haskins 2012). The National Fish, Wildlife and Plants Climate Adaptation Strategy (National Fish, Wildlife and Plants Climate Adaptation Partnership 2012) and the Center for Plant Conservation Best Reintroduction Practice Guidelines (Maschinski et al. 2012) provide a starting point for further policy discussion.
Scientific input and careful planning are critical when propagating listed species and moving them within and outside of their native range. Significant issues include (1) the challenge of propagating plants while maintaining species identity, (2) the potential for unintended consequences such as the movement of pests and pathogens, (3) adverse interactions with endemic biota, and (4) genetic exchange with wild populations. However, declining populations, especially due to climate change, may eventually necessitate unconventional, directed efforts such as commercial propagation (Winter & Botha 1994; Affolter 1997) and assisted colonization of propagated plants (Vitt et al. 2010) in coordination with other means to perpetuate species (Kostyack et al. 2011; Maschinski et al. 2011; Goodman et al. 2012). If listed species need to be propagated to be reintroduced or moved to mitigate for climate change, examples of previous introductions highlight the need for collaborative, monitored studies coordinated by government agencies such as the FWS that (1) consider genetic diversity, (2) take an experimental approach to address ecological questions, such as using common garden experiments in multiple locations, and (3) minimize potential adverse impacts by conducting risk assessment and screening plants for pests and pathogens (Pavlik et al. 1993; Gordon 1994; Reinartz 1995; Falk et al. 1996; Gordon 1996; Pavlik 1997; Guerrant & Kaye 2007; Wendelberger et al. 2008; Weeks et al. 2011; Maschinski & Haskins 2012). Some major impediments to cooperation include laws that do not require consultation with scientists and agencies for citizen-initiated projects (McDonald 1996), and the fact that long-term commitment is required, especially when efforts begin at a grassroots level (Falk et al. 1996). If society wishes to minimize risks associated with propagating and moving species while maximizing potential benefits to species recovery, then these entities should foster efforts to work collaboratively on the planning, implementation, and monitoring of plant propagation, commercial trade, and distribution.
PDS was supported by a fellowship from the NSF IGERT grant award #0504495 to the GLOBES graduate training program at the UND, the UND Center for Aquatic Conservation, a UND CEST Bayer Predoctoral Research Fellowship, and a George Melendez Wright Climate Change Fellowship from the National Park Service. BNK was supported by the UND College of Science and a UND GLOBES NSF-IGERT REU. We thank N. Green, E.L. McWilliams, J.R. Wilson, and anonymous reviewers for providing comments on a previous draft and R.D. Brubaker, C. Hamlin, R.A. Hellenthal, D.M. Lodge, J.C. Nagle, and attendees at the 2012 Ecological Society of America Emerging Issues Conference for providing valuable feedback on this research.