Contributed Paper
Resolving whether botanic gardens are on the road to conservation or a pathway for plant invasions Philip E. Hulme The Bio-Protection Research Centre, Lincoln University, P.O. Box 84850, Christchurch, New Zealand
Abstract: A global conservation goal is to understand the pathways through which invasive species are introduced into new regions. Botanic gardens are a pathway for the introduction of invasive non-native plants, but a quantitative assessment of the risks they pose has not been performed. I analyzed data on the living collections of over 3000 botanic gardens worldwide to quantify the temporal trend in the representation of non-native species; the relative composition of threatened, ornamental, or invasive non-native plant species; and the frequency with which botanic gardens implement procedures to address invasive species. While almost all of the world’s worst invasive non-native plants occurred in one or more living collections (99%), less than one-quarter of red-listed threatened species were cultivated (23%). Even when cultivated, individual threatened species occurred in few living collections (7.3), while non-native species were on average grown in 6 times as many botanic gardens (44.3). As a result, a botanic garden could, on average, cultivate four times as many invasive non-native species (20) as red-listed threatened species (5). Although the risk posed by a single living collection is small, the probability of invasion increases with the number of botanic gardens within a region. Thus, while both the size of living collections and the proportion of non-native species cultivated have declined during the 20th century, this reduction in risk is offset by the 10-fold increase in the number of botanic gardens established worldwide. Unfortunately, botanic gardens rarely implement regional codes of conduct to prevent plant invasions, few have an invasive species policy, and there is limited monitoring of garden escapes. This lack of preparedness is of particular concern given the rapid increase in living collections worldwide since 1950, particularly in South America and Asia, and highlights past patterns of introduction will be a poor guide to determining future invasion risks. Keywords: alien, biological invasions, exotic, naturalization, ornamental, plant conservation, propagule pressure, red list, risk assessment, weeds Resolver Si los Jardines Bot´anicos Est´an Encaminados a la Conservaci´ on o Si Son una V´ıa para la Invasi´ on de Plantas
Resumen: Un objetivo global de la conservaci´on es entender los medios por los cuales las especies invasoras son introducidas a regiones nuevas. Los jardines bot´ anicos son una v´ıa para la introducci´ on de plantas invasoras no-nativas, pero no se ha realizado una evaluaci´ on cuantitativa de los riesgos que presentan. Analic´e datos de las colecciones vivientes de m´ as de 3000 jardines bot´ anicos a nivel mundial para cuantificar la tendencia temporal de representaci´ on de especies no-nativas, la composici´ on relativa de las especies de plantas amenazadas, ornamentales o invasoras, y la frecuencia con la que los jardines bot´ anicos implementan procedimientos para lidiar con especies invasoras. Mientras que casi todas las especies no-nativas de plantas invasoras a nivel global se encuentran en una o m´ as colecciones vivientes (99%), menos de un cuarto de las especies amenazadas que aparecen en la lista roja son cultivadas (23%). Incluso cuando son cultivadas, las especies amenazadas individuales se encuentran en pocas colecciones vivientes (7.3), mientras que las especies no-nativas se cultivan en promedio en seis veces m´ as jardines bot´ anicos (44.3). Como resultado, un jard´ın bot´ anico podr´ıa, en promedio, cultivar cuatro veces el numero de especies no-nativas invasoras (20) que de especies amenazadas que aparecen en la lista roja (5). Aunque el riesgo que presenta una sola colecci´ on viviente es peque˜ no, la probabilidad de invasi´ on incrementa con el n´ umero de jardines bot´ anicos dentro de una regi´ on. As´ı, mientras el tama˜ no de las colecciones vivientes y la proporci´ on de especies no-nativas que son
email [email protected] Paper submitted May 30, 2014; revised manuscript accepted August 18, 2014.
1 Conservation Biology, Volume 00, No. 0, 1–9 C 2014 Society for Conservation Biology DOI: 10.1111/cobi.12426
Botanic Garden Collections and Plant Invasions
2
cultivadas han declinado a lo largo del siglo XX, la reducci´ on en el riesgo no se presenta debido al incremento diez veces mayor en el n´ umero de jardines bot´ anicos que se establecen a nivel mundial. Desafortunadamente, los jardines bot´ anicos rara vez implementan c´ odigos de conducta regionales para prevenir la invasi´ on de plantas, pocos tienen una pol´ıtica de especies invasoras y hay un monitoreo limitado de escapes del jard´ın. Esta falta de preparaci´ on es de preocupaci´ on particular dado el r´ apido incremento de colecciones vivientes en el mundo desde 1950, particularmente en Am´erica del Sur y Asia, y resaltar los patrones anteriores de introducci´ on ser´ a un m´etodo pobre para determinar riesgos futuros de invasi´ on.
Palabras Clave: conservaci´on de plantas, evaluaci´on de riesgo, ex´otico, extranjero, invasiones biol´ogicas, lista roja, maleza, naturalizaci´ on, ornamental, presi´ on de prop´agulo
Introduction A global conservation goal is to understand the pathways through which invasive non-native species are introduced into new regions and to ensure measures are in place to prevent the introduction and establishment of invasive non-native species (UNEP 2011). To date, most analyses of invasion pathways have been simple catalogs of the mechanisms by which non-native species are introduced into a region, and they offer little insight into the risk they pose (Hulme et al. 2008). However, if pathways are to be actively prioritized and managed it is essential to understand the likelihood that invasive non-native species might be introduced via a particular pathway, how the likelihood may be changing over time, and what scope exists for effective interventions. As yet, such an assessment has not been undertaken for a single invasion pathway and remains a major obstacle to delivering by 2020 the Aichi biodiversity target addressing invasive non-native species (UNEP 2011). Furthermore, a quantitative approach is essential where opposing views exist as to the risks posed by a particular pathway, especially where these involve the intentional introduction of non-native species for research or commercial gain. One such conflict has recently arisen from different perspectives regarding the conservation benefits of botanic garden living collections and the costs they may pose through the possible dissemination of invasive non-native plants worldwide (Hulme 2011a). Several lines of evidence point to the role botanic gardens have played in the dissemination of non-native plants into the natural areas of many parts of the world (e.g., Galera & Sudnik–Wojcikowska 2010; Dawson et al. 2011; Parolin et al. 2012; Kannan et al. 2013). However, many widely known plant invasions attributed to botanic gardens occurred over a century ago, which might imply that such risks are no longer present. Botanic gardens have shifted their philosophy greatly and today place ever more emphasis on conservation (Powledge 2011). Furthermore, awareness of the problems of invasive nonnative plant species has increased. Several botanic gardens now follow voluntary codes of conduct to ensure that living collections do not contain or contribute to dissemination or distribution of potentially invasive
Conservation Biology Volume 00, No. 0, 2014
plant species, and some have even assessed their living collections in terms of potential invasion risk (Heywood & Sharrock 2013). This greater emphasis on conservation priorities and awareness of plant invasions may result in living collections posing a negligible risk to the environment (Sharrock et al. 2011). But is this the case? Resolving this conflict requires a quantitative approach which examines the relative representation of non-native plants within the living collections of botanic gardens worldwide and how this has changed over time. The outcome of such an analysis should indicate whether the potential magnitude of risks from plant invasions merits a more considered approach than currently adopted by these institutions or whether the conservation benefits of living collections significantly outweigh any risk of plant invasions. To address this issue, I conducted a detailed quantitative analysis of the temporal and regional trends in the number and species composition of living collections that included an assessment of the frequency with which botanic gardens implement procedures to address invasive species. I sought to answer three questions: What is the relative contribution of species of conservation concern, ornamental taxa and documented invasive non-native plants in living collections? This was determined in terms of the proportion of the global pool found in living collections and in the number of botanic gardens that cultivate the species. Has the risk of botanic gardens introducing invasive plant species diminished over time both in terms of the scale of the pathway and the proportion of non-native species in cultivation in living collections? How active are botanic gardens in addressing the threat of invasive non-native plant species through their garden policies, monitoring of their collections, and research into the problem?
Methods PlantSearch Database The PlantSearch database (BGCI 2012) provides the most comprehensive information available on living collections worldwide (Sharrock & Jones 2011). The database has been substantially updated since the analyses
Hulme
undertaken by Hulme (2011b) and now includes over 1 million records (575,000 in 2010) that relate to taxa in cultivation in 3082 (2680 in 2010) botanic gardens around the world. Although language barriers and a lack of digital plant lists may limit participation in PlantSearch, it likely covers botanic gardens that are more conservation minded, particularly those that are members of Botanic Gardens Conservation International (BGCI), an international network addressing plant conservation (Kramer et al. 2011; Sharrock & Jones 2011). PlantSearch is the primary means by which botanic gardens report on the Global Strategy for Plant Conservation (UNEP 2008). PlantSearch was used to provide records as to which species (red listed, ornamental, and invasive non-native plants) occurred in living collections around the world. A limitation is that BGCI ensures that the precise locations of species in living collections cannot be identified from PlantSearch so that botanic gardens do not face any security issues regarding rare or valuable plants. As a result, while records of red-listed species appear reliable because botanic gardens can provide details without fear of theft, PlantSearch only provides information on the number of living collections in which a species is cultivated and not the specific countries where it is found. Thus, it is not possible to state with certainty if the species is nonnative in the region where the botanic garden is located. More detailed regional studies have required access to additional data sources (often unpublished) to provide a more comprehensive picture of living collections at a regional level such as in the cases of recent North American (Kramer et al. 2011) and European (Sharrock & Jones 2011) assessments. IUCN Red List While several different classification schemes are used around the world to identify the threat status of plant species, the International Union for the Conservation of Nature (IUCN) Red List is the most comprehensive resource detailing the global conservation status of plants and the de facto baseline reference for many conservation decisions (Rodrigues et al. 2006). However, the IUCN Red List is incomplete; 52% of countries having completed some form of red-list assessment (UNEP 2008). Although this may cover 28% of the world’s flora, such data suffer from geographical biases (Schatz 2009). Bearing these important limitations in mind, plant species listed in the living collections represented in PlantSearch were cross referenced against the most recent IUCN Red List (IUCN 2010) and scored against the standard threat categories. As of 2010, the IUCN Red List included 13,383 vascular plant taxa, 9418 of which are listed as threatened (comprising the three categories: critically endangered, endangered, and vulnerable). PlantSearch records have previously been cross-referenced with the IUCN Red List to assess the worldwide status of threatened trees in living collections (Oldfield 2009) as well as in more
3
detailed global assessments of the following individual tree genera: Quercus (Oldfield & Eastwood 2007), Magnolia (BGCI 2008), Acer (Gibbs & Chen 2009), and Rhododendron (Gibbs et al. 2011). My approach is thus consistent with that used previously by BGCI. Ornamental and Non-Native Weeds In contrast to the IUCN Red List, there is no equivalent global standardized list of invasive non-native plants. Thus, I adopted a different approach to assess the potential contribution of non-native weeds to living collections. Given that a significant proportion of plants in living collections are ornamentals, an assessment of the frequency with which invasive non-native plants were found among a representative sample of ornamental species was undertaken. Following Hulme (2011b), a random sample of 574 species (excluding cultivars or varieties), which had obtained the Award of Garden Merit (AGM) from the Royal Horticultural Society (Brickell 1999), were cross referenced against the Global Compendium of Weeds (Randall 2002) and PlantSearch to assess the prevalence in living collections of species with a history of becoming invasive non-native species. Additionally, the AGM list was also cross-referenced with the IUCN Red List to evaluate the likely proportion of ornamental plants that have threatened status and estimate the representation of these threatened ornamentals in living collections. The AGM plants are indicative of popular and commercially important ornamental species widely promoted by the horticultural trade and total approximately 3000 species (excluding cultivars or varieties). To assess the representation of invasive non-native plants, species drawn from a compendium of 450 of the world’s worst invasive non-native plants that pose an environmental threat (Weber 2003) were also crossreferenced in PlantSearch to identify the extent to which such species were found in living collections. Weber’s (2003) list of invasive non-native plants is not exhaustive and covers only a fraction of all invasive plant species globally. Nevertheless, it represents species that have significant negative effects on the native fauna and flora of the regions they have invaded (Hulme et al. 2013). I calculated the frequency with which each of the 450 non-native environmental weeds was recorded as invasive across nine biogeographic regions and 32 subregions from Weber (2003). A positive correlation between the frequency of invasive status and the number of living collections in which a species was found would be consistent of a link between botanic gardens and plant invasions. GardenSearch Database The GardenSearch database (BGCI 2013) provides descriptions of over 3000 botanic gardens, including attributes of the garden (e.g., date of establishment, Conservation Biology Volume 00, No. 0, 2014
Botanic Garden Collections and Plant Invasions
4
Table 1. Species in living collections in botanic gardens classified by the International Union for the Conservation of Nature (IUCN) Red List criteria, Award of Garden Merit (AMG)a , and known invasive plant status.
IUCN Red List category Extinct in the wild Critically endangered Endangered vulnerable Near threatened Least concern Data deficient AGM ornamentals IUCN listed Not known as invasive Known as invasive Invasive non-native plants
Species in living collections
Percentage of global number of plant species
Mean number of collections (SE)b
21
67.7
9.6 (4.0)
527 575 1058 499 887 145
30.8 23.1 20.7 34.0 51.7 18.5
6.4 (0.7) 7.1 (0.7) 7.9 (0.5) 13.5 (1.2) 20.4 (1.1) 9.4 (1.5)
36 249 325 448
6.3 43.4 56.6 99.6
89.7 (8.0) 46.0 (2.2) 73.2 (1.9) 44.3 (1.8)
a Ornamental b Mean
plants that received a mark of quality awarded by the British Royal Horticultural Society. number of collections that contain species. Results from PlantSearch (www.bgci.org; December 2012).
cultivated area, etc.), details of the plant collection (e.g., number of cultivated taxa, percentage of native species), and evidence of any research, education, and conservation programs. The level of detail contributed by botanic gardens varies considerably and thus additional data were sought from individual botanic garden websites. To understand whether botanic gardens pose less of a risk today than they may have in the past, it is essential to know how numbers of botanic gardens and the representation of non-native species in their living collections have changed over time. GardenSearch and associated web data were therefore used to explore the temporal dynamics in the establishment and composition of botanic gardens. In addition, data were extracted regarding the involvement of botanic gardens in conservation, horticulture, and invasive species research as well as the existence of invasive species policies and active monitoring of collections for invasions. Not all botanic gardens provide additional information; therefore, following Hardwick et al. (2011), the calculation of percentage of gardens undertaking these activities was based on a subset that had completed details regarding their general facilities (e.g., open to general public, retail outlet, visitor center). These figures give only an approximate indication of the relative importance of different activities and should be regarded as upper estimates of the overall percentage. Integration To estimate the approximate composition of the average living collection, the total number of collections in which IUCN red listed, AGM ornamental, or invasive species were found were divided by the total number of botanic gardens in the database to yield the average number of taxa in each category per living collection. I assumed that the sample of AGM ornamental species I chose randomly were representative of the 3000 AGM ornamental
Conservation Biology Volume 00, No. 0, 2014
species (excluding cultivars and varieties) listed by the British Royal Horticultural Society (www.rhs.org.uk) in terms of their occurrence in living collections and the proportion that are invasive species. Data on the temporal trend in the number of taxa in living collections, the total number of living collections worldwide, and the proportion comprising non-native species were integrated to provide an estimate of how the relative risk might have changed over time. For example, a shift toward more native species in living collections may be offset by a marked increase in the total number of living collections established over time.
Results Representation of Threatened, Invasive, and Ornamental Species Living collections housed 3712 (28%) of known redlisted plant taxa (Table 1). Two-thirds of species that are extinct in the wild were under cultivation in botanic gardens; species of lower risk status were more frequently cultivated than more imperiled taxa (χ 2 [1,7] = 374.58, p < 0.001, Table 1). Near threatened, least concern, and data deficient species were more frequently represented (one-way analysis of variance [ANOVA] F(7, 3709) = 30.65, p < 0.001) (Table 1), whereas threatened species were rarely found in >10 living collections. Almost all (99%) of the major invasive plant species were found in botanic gardens, with 2 exceptions: wetland nightshade (Solanum tampicense) and purple pampas grass (Cortaderia jubata). Major invasive non-native plants were 2–5 times better represented in living collections than red-listed species (oneway ANOVA F(8, 4154) = 112.21, p < 0.001, Table 1). A significant correlation was found between the number of living collections in which a species was found worldwide and both the frequency
Hulme
Temporal Trends in the Number, Size, and Composition The number of botanic gardens worldwide has increased more than 10-fold since 1900 (Fig. 1a), with the most dramatic increases in South America (29.8-fold increase) and Asia (19.0-fold increase) and the least increase in Europe (8.3-fold increase). On average, 70% of this increase has occurred since 1950 and is especially striking for South America (90.2%) and Oceania (83.3%) and more modest for Europe (65.9%). A significant positive
(a) Cumulative number of botanic gardens
600
Africa 500 400 300
N America S America Asia Europe Oceania
200 100 0 1500
1600
1700
1800
1900
2000
Year of botanic garden establishment
(b) 100
Native species in living collection (%)
with which a species was recorded as being invasive across 9 biogeographic regions (Spearman r = 0.141, df 448, p
Resolving whether botanic gardens are on the road to conservation or a pathway for plant invasions Philip E. Hulme The Bio-Protection Research Centre, Lincoln University, P.O. Box 84850, Christchurch, New Zealand
Abstract: A global conservation goal is to understand the pathways through which invasive species are introduced into new regions. Botanic gardens are a pathway for the introduction of invasive non-native plants, but a quantitative assessment of the risks they pose has not been performed. I analyzed data on the living collections of over 3000 botanic gardens worldwide to quantify the temporal trend in the representation of non-native species; the relative composition of threatened, ornamental, or invasive non-native plant species; and the frequency with which botanic gardens implement procedures to address invasive species. While almost all of the world’s worst invasive non-native plants occurred in one or more living collections (99%), less than one-quarter of red-listed threatened species were cultivated (23%). Even when cultivated, individual threatened species occurred in few living collections (7.3), while non-native species were on average grown in 6 times as many botanic gardens (44.3). As a result, a botanic garden could, on average, cultivate four times as many invasive non-native species (20) as red-listed threatened species (5). Although the risk posed by a single living collection is small, the probability of invasion increases with the number of botanic gardens within a region. Thus, while both the size of living collections and the proportion of non-native species cultivated have declined during the 20th century, this reduction in risk is offset by the 10-fold increase in the number of botanic gardens established worldwide. Unfortunately, botanic gardens rarely implement regional codes of conduct to prevent plant invasions, few have an invasive species policy, and there is limited monitoring of garden escapes. This lack of preparedness is of particular concern given the rapid increase in living collections worldwide since 1950, particularly in South America and Asia, and highlights past patterns of introduction will be a poor guide to determining future invasion risks. Keywords: alien, biological invasions, exotic, naturalization, ornamental, plant conservation, propagule pressure, red list, risk assessment, weeds Resolver Si los Jardines Bot´anicos Est´an Encaminados a la Conservaci´ on o Si Son una V´ıa para la Invasi´ on de Plantas
Resumen: Un objetivo global de la conservaci´on es entender los medios por los cuales las especies invasoras son introducidas a regiones nuevas. Los jardines bot´ anicos son una v´ıa para la introducci´ on de plantas invasoras no-nativas, pero no se ha realizado una evaluaci´ on cuantitativa de los riesgos que presentan. Analic´e datos de las colecciones vivientes de m´ as de 3000 jardines bot´ anicos a nivel mundial para cuantificar la tendencia temporal de representaci´ on de especies no-nativas, la composici´ on relativa de las especies de plantas amenazadas, ornamentales o invasoras, y la frecuencia con la que los jardines bot´ anicos implementan procedimientos para lidiar con especies invasoras. Mientras que casi todas las especies no-nativas de plantas invasoras a nivel global se encuentran en una o m´ as colecciones vivientes (99%), menos de un cuarto de las especies amenazadas que aparecen en la lista roja son cultivadas (23%). Incluso cuando son cultivadas, las especies amenazadas individuales se encuentran en pocas colecciones vivientes (7.3), mientras que las especies no-nativas se cultivan en promedio en seis veces m´ as jardines bot´ anicos (44.3). Como resultado, un jard´ın bot´ anico podr´ıa, en promedio, cultivar cuatro veces el numero de especies no-nativas invasoras (20) que de especies amenazadas que aparecen en la lista roja (5). Aunque el riesgo que presenta una sola colecci´ on viviente es peque˜ no, la probabilidad de invasi´ on incrementa con el n´ umero de jardines bot´ anicos dentro de una regi´ on. As´ı, mientras el tama˜ no de las colecciones vivientes y la proporci´ on de especies no-nativas que son
email [email protected] Paper submitted May 30, 2014; revised manuscript accepted August 18, 2014.
1 Conservation Biology, Volume 00, No. 0, 1–9 C 2014 Society for Conservation Biology DOI: 10.1111/cobi.12426
Botanic Garden Collections and Plant Invasions
2
cultivadas han declinado a lo largo del siglo XX, la reducci´ on en el riesgo no se presenta debido al incremento diez veces mayor en el n´ umero de jardines bot´ anicos que se establecen a nivel mundial. Desafortunadamente, los jardines bot´ anicos rara vez implementan c´ odigos de conducta regionales para prevenir la invasi´ on de plantas, pocos tienen una pol´ıtica de especies invasoras y hay un monitoreo limitado de escapes del jard´ın. Esta falta de preparaci´ on es de preocupaci´ on particular dado el r´ apido incremento de colecciones vivientes en el mundo desde 1950, particularmente en Am´erica del Sur y Asia, y resaltar los patrones anteriores de introducci´ on ser´ a un m´etodo pobre para determinar riesgos futuros de invasi´ on.
Palabras Clave: conservaci´on de plantas, evaluaci´on de riesgo, ex´otico, extranjero, invasiones biol´ogicas, lista roja, maleza, naturalizaci´ on, ornamental, presi´ on de prop´agulo
Introduction A global conservation goal is to understand the pathways through which invasive non-native species are introduced into new regions and to ensure measures are in place to prevent the introduction and establishment of invasive non-native species (UNEP 2011). To date, most analyses of invasion pathways have been simple catalogs of the mechanisms by which non-native species are introduced into a region, and they offer little insight into the risk they pose (Hulme et al. 2008). However, if pathways are to be actively prioritized and managed it is essential to understand the likelihood that invasive non-native species might be introduced via a particular pathway, how the likelihood may be changing over time, and what scope exists for effective interventions. As yet, such an assessment has not been undertaken for a single invasion pathway and remains a major obstacle to delivering by 2020 the Aichi biodiversity target addressing invasive non-native species (UNEP 2011). Furthermore, a quantitative approach is essential where opposing views exist as to the risks posed by a particular pathway, especially where these involve the intentional introduction of non-native species for research or commercial gain. One such conflict has recently arisen from different perspectives regarding the conservation benefits of botanic garden living collections and the costs they may pose through the possible dissemination of invasive non-native plants worldwide (Hulme 2011a). Several lines of evidence point to the role botanic gardens have played in the dissemination of non-native plants into the natural areas of many parts of the world (e.g., Galera & Sudnik–Wojcikowska 2010; Dawson et al. 2011; Parolin et al. 2012; Kannan et al. 2013). However, many widely known plant invasions attributed to botanic gardens occurred over a century ago, which might imply that such risks are no longer present. Botanic gardens have shifted their philosophy greatly and today place ever more emphasis on conservation (Powledge 2011). Furthermore, awareness of the problems of invasive nonnative plant species has increased. Several botanic gardens now follow voluntary codes of conduct to ensure that living collections do not contain or contribute to dissemination or distribution of potentially invasive
Conservation Biology Volume 00, No. 0, 2014
plant species, and some have even assessed their living collections in terms of potential invasion risk (Heywood & Sharrock 2013). This greater emphasis on conservation priorities and awareness of plant invasions may result in living collections posing a negligible risk to the environment (Sharrock et al. 2011). But is this the case? Resolving this conflict requires a quantitative approach which examines the relative representation of non-native plants within the living collections of botanic gardens worldwide and how this has changed over time. The outcome of such an analysis should indicate whether the potential magnitude of risks from plant invasions merits a more considered approach than currently adopted by these institutions or whether the conservation benefits of living collections significantly outweigh any risk of plant invasions. To address this issue, I conducted a detailed quantitative analysis of the temporal and regional trends in the number and species composition of living collections that included an assessment of the frequency with which botanic gardens implement procedures to address invasive species. I sought to answer three questions: What is the relative contribution of species of conservation concern, ornamental taxa and documented invasive non-native plants in living collections? This was determined in terms of the proportion of the global pool found in living collections and in the number of botanic gardens that cultivate the species. Has the risk of botanic gardens introducing invasive plant species diminished over time both in terms of the scale of the pathway and the proportion of non-native species in cultivation in living collections? How active are botanic gardens in addressing the threat of invasive non-native plant species through their garden policies, monitoring of their collections, and research into the problem?
Methods PlantSearch Database The PlantSearch database (BGCI 2012) provides the most comprehensive information available on living collections worldwide (Sharrock & Jones 2011). The database has been substantially updated since the analyses
Hulme
undertaken by Hulme (2011b) and now includes over 1 million records (575,000 in 2010) that relate to taxa in cultivation in 3082 (2680 in 2010) botanic gardens around the world. Although language barriers and a lack of digital plant lists may limit participation in PlantSearch, it likely covers botanic gardens that are more conservation minded, particularly those that are members of Botanic Gardens Conservation International (BGCI), an international network addressing plant conservation (Kramer et al. 2011; Sharrock & Jones 2011). PlantSearch is the primary means by which botanic gardens report on the Global Strategy for Plant Conservation (UNEP 2008). PlantSearch was used to provide records as to which species (red listed, ornamental, and invasive non-native plants) occurred in living collections around the world. A limitation is that BGCI ensures that the precise locations of species in living collections cannot be identified from PlantSearch so that botanic gardens do not face any security issues regarding rare or valuable plants. As a result, while records of red-listed species appear reliable because botanic gardens can provide details without fear of theft, PlantSearch only provides information on the number of living collections in which a species is cultivated and not the specific countries where it is found. Thus, it is not possible to state with certainty if the species is nonnative in the region where the botanic garden is located. More detailed regional studies have required access to additional data sources (often unpublished) to provide a more comprehensive picture of living collections at a regional level such as in the cases of recent North American (Kramer et al. 2011) and European (Sharrock & Jones 2011) assessments. IUCN Red List While several different classification schemes are used around the world to identify the threat status of plant species, the International Union for the Conservation of Nature (IUCN) Red List is the most comprehensive resource detailing the global conservation status of plants and the de facto baseline reference for many conservation decisions (Rodrigues et al. 2006). However, the IUCN Red List is incomplete; 52% of countries having completed some form of red-list assessment (UNEP 2008). Although this may cover 28% of the world’s flora, such data suffer from geographical biases (Schatz 2009). Bearing these important limitations in mind, plant species listed in the living collections represented in PlantSearch were cross referenced against the most recent IUCN Red List (IUCN 2010) and scored against the standard threat categories. As of 2010, the IUCN Red List included 13,383 vascular plant taxa, 9418 of which are listed as threatened (comprising the three categories: critically endangered, endangered, and vulnerable). PlantSearch records have previously been cross-referenced with the IUCN Red List to assess the worldwide status of threatened trees in living collections (Oldfield 2009) as well as in more
3
detailed global assessments of the following individual tree genera: Quercus (Oldfield & Eastwood 2007), Magnolia (BGCI 2008), Acer (Gibbs & Chen 2009), and Rhododendron (Gibbs et al. 2011). My approach is thus consistent with that used previously by BGCI. Ornamental and Non-Native Weeds In contrast to the IUCN Red List, there is no equivalent global standardized list of invasive non-native plants. Thus, I adopted a different approach to assess the potential contribution of non-native weeds to living collections. Given that a significant proportion of plants in living collections are ornamentals, an assessment of the frequency with which invasive non-native plants were found among a representative sample of ornamental species was undertaken. Following Hulme (2011b), a random sample of 574 species (excluding cultivars or varieties), which had obtained the Award of Garden Merit (AGM) from the Royal Horticultural Society (Brickell 1999), were cross referenced against the Global Compendium of Weeds (Randall 2002) and PlantSearch to assess the prevalence in living collections of species with a history of becoming invasive non-native species. Additionally, the AGM list was also cross-referenced with the IUCN Red List to evaluate the likely proportion of ornamental plants that have threatened status and estimate the representation of these threatened ornamentals in living collections. The AGM plants are indicative of popular and commercially important ornamental species widely promoted by the horticultural trade and total approximately 3000 species (excluding cultivars or varieties). To assess the representation of invasive non-native plants, species drawn from a compendium of 450 of the world’s worst invasive non-native plants that pose an environmental threat (Weber 2003) were also crossreferenced in PlantSearch to identify the extent to which such species were found in living collections. Weber’s (2003) list of invasive non-native plants is not exhaustive and covers only a fraction of all invasive plant species globally. Nevertheless, it represents species that have significant negative effects on the native fauna and flora of the regions they have invaded (Hulme et al. 2013). I calculated the frequency with which each of the 450 non-native environmental weeds was recorded as invasive across nine biogeographic regions and 32 subregions from Weber (2003). A positive correlation between the frequency of invasive status and the number of living collections in which a species was found would be consistent of a link between botanic gardens and plant invasions. GardenSearch Database The GardenSearch database (BGCI 2013) provides descriptions of over 3000 botanic gardens, including attributes of the garden (e.g., date of establishment, Conservation Biology Volume 00, No. 0, 2014
Botanic Garden Collections and Plant Invasions
4
Table 1. Species in living collections in botanic gardens classified by the International Union for the Conservation of Nature (IUCN) Red List criteria, Award of Garden Merit (AMG)a , and known invasive plant status.
IUCN Red List category Extinct in the wild Critically endangered Endangered vulnerable Near threatened Least concern Data deficient AGM ornamentals IUCN listed Not known as invasive Known as invasive Invasive non-native plants
Species in living collections
Percentage of global number of plant species
Mean number of collections (SE)b
21
67.7
9.6 (4.0)
527 575 1058 499 887 145
30.8 23.1 20.7 34.0 51.7 18.5
6.4 (0.7) 7.1 (0.7) 7.9 (0.5) 13.5 (1.2) 20.4 (1.1) 9.4 (1.5)
36 249 325 448
6.3 43.4 56.6 99.6
89.7 (8.0) 46.0 (2.2) 73.2 (1.9) 44.3 (1.8)
a Ornamental b Mean
plants that received a mark of quality awarded by the British Royal Horticultural Society. number of collections that contain species. Results from PlantSearch (www.bgci.org; December 2012).
cultivated area, etc.), details of the plant collection (e.g., number of cultivated taxa, percentage of native species), and evidence of any research, education, and conservation programs. The level of detail contributed by botanic gardens varies considerably and thus additional data were sought from individual botanic garden websites. To understand whether botanic gardens pose less of a risk today than they may have in the past, it is essential to know how numbers of botanic gardens and the representation of non-native species in their living collections have changed over time. GardenSearch and associated web data were therefore used to explore the temporal dynamics in the establishment and composition of botanic gardens. In addition, data were extracted regarding the involvement of botanic gardens in conservation, horticulture, and invasive species research as well as the existence of invasive species policies and active monitoring of collections for invasions. Not all botanic gardens provide additional information; therefore, following Hardwick et al. (2011), the calculation of percentage of gardens undertaking these activities was based on a subset that had completed details regarding their general facilities (e.g., open to general public, retail outlet, visitor center). These figures give only an approximate indication of the relative importance of different activities and should be regarded as upper estimates of the overall percentage. Integration To estimate the approximate composition of the average living collection, the total number of collections in which IUCN red listed, AGM ornamental, or invasive species were found were divided by the total number of botanic gardens in the database to yield the average number of taxa in each category per living collection. I assumed that the sample of AGM ornamental species I chose randomly were representative of the 3000 AGM ornamental
Conservation Biology Volume 00, No. 0, 2014
species (excluding cultivars and varieties) listed by the British Royal Horticultural Society (www.rhs.org.uk) in terms of their occurrence in living collections and the proportion that are invasive species. Data on the temporal trend in the number of taxa in living collections, the total number of living collections worldwide, and the proportion comprising non-native species were integrated to provide an estimate of how the relative risk might have changed over time. For example, a shift toward more native species in living collections may be offset by a marked increase in the total number of living collections established over time.
Results Representation of Threatened, Invasive, and Ornamental Species Living collections housed 3712 (28%) of known redlisted plant taxa (Table 1). Two-thirds of species that are extinct in the wild were under cultivation in botanic gardens; species of lower risk status were more frequently cultivated than more imperiled taxa (χ 2 [1,7] = 374.58, p < 0.001, Table 1). Near threatened, least concern, and data deficient species were more frequently represented (one-way analysis of variance [ANOVA] F(7, 3709) = 30.65, p < 0.001) (Table 1), whereas threatened species were rarely found in >10 living collections. Almost all (99%) of the major invasive plant species were found in botanic gardens, with 2 exceptions: wetland nightshade (Solanum tampicense) and purple pampas grass (Cortaderia jubata). Major invasive non-native plants were 2–5 times better represented in living collections than red-listed species (oneway ANOVA F(8, 4154) = 112.21, p < 0.001, Table 1). A significant correlation was found between the number of living collections in which a species was found worldwide and both the frequency
Hulme
Temporal Trends in the Number, Size, and Composition The number of botanic gardens worldwide has increased more than 10-fold since 1900 (Fig. 1a), with the most dramatic increases in South America (29.8-fold increase) and Asia (19.0-fold increase) and the least increase in Europe (8.3-fold increase). On average, 70% of this increase has occurred since 1950 and is especially striking for South America (90.2%) and Oceania (83.3%) and more modest for Europe (65.9%). A significant positive
(a) Cumulative number of botanic gardens
600
Africa 500 400 300
N America S America Asia Europe Oceania
200 100 0 1500
1600
1700
1800
1900
2000
Year of botanic garden establishment
(b) 100
Native species in living collection (%)
with which a species was recorded as being invasive across 9 biogeographic regions (Spearman r = 0.141, df 448, p
