Invasion Risks and Social Interest of Non-native Woody Plants in Urban Parks of Mainland Spain

Anales del Jardín Botánico de Madrid 79 (1): e121 https://doi.org/10.3989/ajbm.2623 ISSN-L: 0211-1322 Abstract. Urban parks and gardens are one of the most important pathways for the deliberate introduction of non-native plant species, some of which cause environmental and socioeconomic impacts. We conducted a risk assessment on 388 non-native woody plant species from 46 urban parks of mainland Spain to classify them in lists based on their invasion status, being invasive elsewhere, climate matching with the area of origin, and potential to cause negative impacts. Only Ficus benjamina has no potential to invade (Green list). Four species are invasive and regulated (Priority list); 47 invasive or potentially invasive species can cause more impact types than the median value (Attention list), while 12 can cause less impacts than the median (Watch list). There is no park without any invasive or potentially invasive species. The most common potential impacts could be competition with native species (80% species) and the physical modification of the habitats (71%). We also identified 31 species with potential to cause human health impacts. Some species could cause several impact types. The most correlated potential impacts are among competition, toxicity, and alteration of natural succession and habitat structure. The most frequently planted invasive and potentially invasive species are the ones with the largest standard trending value from Google Trends, and therefore the ones with more societal interest. Keywords: Google trends, impact assessment, invasive species, ornamental plants, WRA. Resumen. Los parques y jardines urbanos son una de las vías más importantes de la introducción deliberada de especies de plantas no nativas, algunas de las cuales causan impactos ambientales y socioeconómicos. Realizamos un análisis de riesgo de 388 especies de plantas leñosas no nativas de 46 parques urbanos de España peninsular para clasificarlas en listas basadas en su categoría de invasión en España, la capacidad de ser invasora en otros lugares, la coincidencia climática en su área de origen y el potencial de causar impactos negativos. Solo Ficus benjamina no posee potencial invasor (Lista verde). Cuatro especies son invasoras y están reguladas (Lista de prioridad); 47 especies invasoras o potencialmente invasoras pueden causar más impactos que la mediana (Lista de atención), mientras que 12 especies pueden causar menos impactos que la mediana (Lista de observación). No hay parques sin especies invasoras o potencialmente invasoras. Los impactos potenciales más comunes podrían ser la competencia con especies nativas (80%) y la modificación física de los hábitats (71%). Además, identificamos 31 especies con potencial de causar impactos en la salud humana. Algunas especies pueden causar varios tipos de impacto. Los impactos potenciales más correlacionados serían entre competencia, toxicidad, alteración de la sucesión natural y estructura del hábitat. Las especies que se plantan con más frecuencia son las que tienen el mayor valor de tendencia estándar de Google Trends, y por tanto las que poseen un mayor interés social. Palabras clave: especies invasoras, evaluación de impacto, plantas ornamentales, tendencias de Google, WRA. How to cite this article: Bayón A., Godoy O., Vilà M. 2022. Invasion risks and social interest of non-native woody plants in urban parks of mainland Spain. Anales del Jardín Botánico de Madrid 79: e121. https://doi.org/10.3989/ajbm.2623 Title in Spanish: Riesgos de invasión e interés social de las plantas leñosas alóctonas en parques urbanos de la España peninsular. Associate Editor: Inés Álvarez. Received: 2 October 2021; accepted: 23 March 2022; published online: 2 September 2022 Copyright: © 2022 CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License. Invasion risks and social interest of non-native woody plants in urban parks of mainland Spain Álvaro BAYÓN1, Oscar GODOY2, Montserrat VILÀ3* ¹Universidad Isabel I, c/Ferrán González 76, 09003, Burgos, Spain 2Department of Biology, Instituto Universitario de Investigación Marina (INMAR), University of Cádiz, Spain 3Estación Biológica de Doñana (EBD), CSIC, Av. Américo Vespucio 26, 41092, Sevilla, Spain 3Department of Plant Biology and Ecology, University of Sevilla, Sevilla, Spain *Correspondence: [email protected] 1https://orcid.org/0000-0003-4284-8889, 2https://orcid.org/0000-0003-4988-6626 3https://orcid.org/0000-0003-3171-8261 Bayón & al. 2 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 INTRODUCTION Biological invasions by the establishment and spread of introduced non-native species cause many negative environmental and socioeconomic impacts (Blackburn & al. 2019). Because the establishment of non-native species has increased exponentially during the last decades by the amplified connection of infrastructures and global commerce (Seebens & al. 2017), it is of paramount importance to identify those with the potential to become invasive and cause harm. The introduction of non-native species may be accidental or deliberate. Deliberated introductions of ornamental plants in urban parks and gardens is one of the most important introduction pathways of non-native plants around the globe (Mayer & al. 2017; Haeuser & al. 2018). Despite that ornamental plants provide cultural and aesthetic services to people (Bolund & Hunhammar 1999; Kendal & al. 2012; Vaz & al. 2018), many ornamental introduced species have established (i.e., naturalized) in the wild, causing impacts to biodiversity and ecosystems (Hulme 2007). The most effective way to manage the impacts of non-native species is prevention through early warning techniques, as well as to perform invasion risk assessments (Convention on Biological Diversity 2010). Development of risk assessment protocols has progressed considerably in the last decades proving to be an essential tool to identify and predict potential invasions (Andreu & Vilà 2010; Roy & al. 2014). Most risk assessment protocols consider being invasive elsewhere, having the potential to be established in the wild, climate matching with the area of origin, and potential to cause impacts as the main characteristics to classify a non-native plant species with high potential to invade a region (Weber & Gut 2004; Otfinowski & al. 2007; Roy & al. 2019). Some classic examples such as the Australian weed risk assessment (WRA) (Pheloung & al. 1999) have been widely used to accurately predict potential invaders in many different regions including Spain (Gordon & al. 2008; Andreu & Vilà 2010; Gassó & al. 2010). However, when focusing on the specific case of non-native plant species introduced for aesthetic purposes, it is likely that additional factors, such as the socioeconomic interest or their planting prevalence, might affect their invasion risk. The Google Trends tool offers good proxies of the societal interest that the people have on particular items. The Google Trends tool has been used to evaluate the level of interest and queries of the population on conservation topics (Żmihorski & al. 2013; Davies & al. 2018; Schuetz & Johnston 2019) and epidemiology (Seo & Shin 2017). Recently, it has been applied to the study of biological invasions. For example, in Japan, the Google search of 31 major invasive species is a good predictor of their spatial distribution (Fukano & Soga 2019). Likewise the Google Trends has been previously used in Spain to rank non-native plants sold in nurseries (Bayón & Vilà 2019). In this paper, we will use Google Trends to rank ornamental woody plants in urban parks. Impacts of non-native species are of major concern to prioritize their management (Kumschick & al. 2015; Novoa & al. 2020). Moreover, an understanding about how the impacts interact with each other may provide knowledge on the association between impacts on the environment and on socioeconomic activities (Vilà & al. 2010). Similarly, because plants are deliberately introduced into urban parks, it is important to identify which are the most common and frequent impacts they can cause, both at the species level and at the park (‘assemblage’) level. Therefore, an analysis of the proportion of species with the potential to cause each impact type and the species occurrence in the parks allows for defining the potential non-native impact profile of a particular park. To our knowledge, this analysis has not been conducted despite its paramount importance to guide best practices for avoiding their threat to local biodiversity and causing disservices. In this paper, we performed a risk analysis to classify 486 non-native woody species planted in 46 major urban parks from 23 cities across mainland Spain in various lists. Furthermore, for all the invasive and potentially invasive species, we answered the following questions: 1) How frequent are these species across parks? 2) Is species occurrence (i.e., number of parks where present) associated with their interest to society, and with the magnitude of their risk to invade? 3) Which are the most common potential impacts of these species? 4) How frequent are the species with potential to cause impacts in urban parks? and, finally, 5) Which impacts might show higher correlations? MATERIAL AND METHODS Urban parks dataset From the database provided by the Spanish Association of Public Parks and Gardens (AEPJP 2010; see Appendix 1), we compiled the complete species list of woody and arboreal-like plant (i.e., trees, shrubs, arboreal cacti and palm trees) present in 46 parks from 23 peninsular Spanish cities. We used the Taxon stand package of R (Cayuela & al. 2019) to select all the accepted scientific names (consulted 22 May 2020), excluding species with invalid names. The species were classified as native or non-native. Archaeophytes (i.e., species introduced before 1500 AD) were not included in the analysis because they are poorly recorded and, for many species, their non-native status is under discussion (Pyšek & al. 2004). Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Interest and risks of non-native ornamental plants 3 We checked for the invasion status of these non-na- tive species in Spain (Sanz Elorza & al. 2004; BOE 2019; CABI 2020) following Richardson & al. (2000). Based on that, species were classified as: invasive, established, casual, and not present in the wild. We also consulted their regulatory status by the Spanish Catalogue of Non-native Invasive Species (BOE 2019) and the List of Invasive Alien Species of Union Concern (European Commission 2019). These regulations involve the ban of possession, transport and commerce of living beings and their propagules. Once we had the five groups of species according to its invasion status in Spain, we proceeded to classify the species into 6 lists following Bayón & Vilà (2019) methodology (Fig. 1): · Priority list: regulated (by Spain or the EU) invasive non-native species present in urban parks. · Attention list: invasive (not regulated) and potentially invasive species (i.e., climatically suitable and invasive elsewhere) with more potential impacts than the median of all species. · Watch list: invasive (not regulated) and potentially invasive species with none or fewer potential impacts than the median of all species. · Green list: non-invasive nor potentially invasive species with no climatic suitability and probably no potential to be invasive in Spain, and safe for socioeconomics and the environment. · Uncertainty list: non-invasive species with probably no potential to be invasive and that do not meet the requirements to be included in the Green List. It also includes species with known invasion status but with insufficient information on climatic suitability or being invasives elsewhere. · Data Deficient list: species without enough information about its invasion status, nor climatic suitability, nor invasive elsewhere. Therefore, they cannot be classified in any other list. Information on being invasive elsewhere was consulted in the CABI datasheets (CABI 2020) and the database of the Invasive Species Specialist Group (2015). The climatic suitability was defined as the tolerance to both, the highest historical absolute minimum temperature in Spain which was 0.2°C in Almería (9 February 1935), and the highest mean minimum temperature in the coldest month in Spain which is 10.8°C in January in Tarifa (mean recorded from data between 1981 to 2010) (AEMET 2019). These tolerances were consulted in the CABI Invasive Species Compendium (CABI 2020). Fig.1. Flow diagram of the risk assessment of ornamental non-native woody species in urban parks and gardens in Spain and their classification into respective lists following Bayón & Vilà (2019). Bayón & al. 4 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Impact assessment of invasive and potentially invasive species For the invasive and potentially invasive species, we assigned binary scores (yes/no) to a total of 14 potential impact types, following Blackburn et al (2014). We considered six potential impacts on native species: (1) competition, (2) hybridization, (3) disease transmission, (4) parasitism, (5) poisoning, toxicity and allelopathy, and (6) interaction with other invasive non-native species; and four impacts on ecosystems: (7) nutrient cycling, (8) physical modification of the habitat, (9) modification of natural succession and (10) disruption to food webs. We also assessed potential socioeconomic impacts, including on (11) human health (such as allergenic pollen), (12) infrastructures, (13) agriculture and forestry and (14) to other sectors (e.g., livestock, domestic animals, and fish farming). Information on impacts was consulted in the CABI Invasive Species Compendium (CABI 2020) and the database of the Invasive Species Specialist Group (2015). Information about pollen allergenicity was found in the Allergome database (Mari & al. 2009). For each species, we calculated the number of potential environmental (0–10) and socioeconomic (0–4) impacts. The threshold for the classification between species with a high and low number of impacts was the median value for both environmental and socioeconomic impacts. The Attention list was composed by invasive and potentially invasive species in Spain with environmental or socioeconomic impacts at or above the threshold. Meanwhile species with both environmental and socioeconomic impacts below the threshold formed the Watch List. Society interest analysis of invasive and potentially invasive species The Google Trends tool provides monthly data of up to five keywords, in a predefined geographic and temporal range. The output values of Google Trends are always relative to the maximum absolute value of all the keywords imputed, which is set as 100. To standardize the relative values of Google trends, we used the R pack “gtrendsR” v. 1.4.2 (Massicotte & Eddelbuettel 2020), carrying out a paired systematic consultation between each species and Robinia pseudoacacia L. as the control species for Spain as the geographic region, from the 1st of January of 2004 to the 31st of December of 2019. Robinia pseudoacacia was selected as the control species because it was the one with the highest Google Trends value. Invasion risk assessment of invasive and potentially invasive species We used an adaptation of the invasion risk assessment (WRA) protocol for Spain (Pheloung & al. 1999; Gassó & al. 2010) on all the invasive and potentially invasive species. The WRA scores range from –14 (benign species) to 29 (maximum risk). WRA assess species as ‘rejected’ for those species likely to be of high risk (score > 6); as ‘accepted’ those with a low score (< 1); and as ‘need further evaluation’, those with intermediate scores (1–6). Some of the WRA values were obtained from several previous studies (Gassó & al. 2010; Pino & al. 2015; Álvarez & al. 2016; Bayón & Vilà 2019). For the species for which WRA had not been performed before, it was calculated ‘de novo’. Most of the scientific information to calculate the WRA came from the Invasive Species Specialist Group (2015) and CABI (2020). Priority Index of invasive and potentially invasive species For each species in the Attention list, we calculated a Priority Index (PIi) based on Bayón & Vilà (2019) according to the following equation: Where: PIi = Priority Index for species i; Ei = number of environmental impacts for species i; Si = number of socioeconomic impacts for species i; WRAi = Weed Risk Assessment score for species i; STVi = Standard trending value for species i. The number of potential environmental impacts was set to 11 and not to 10 to be consistent with the Priority Index applied for the first time to nursery species that also included impacts on biofouling (Bayón & Vilà 2019). Statistical analyses To test if invasive and potentially invasive species occurrence (i.e., number of parks present) is related to the STV and the WRA, we calculated the Pearson’s correlation coefficient, and performed dispersion dot plots by the R ggplot2 package (Wickham 2016); smooth line was performed by ‘lm’ method. For the non-native species included in the categories of invasive or potentially invasive species, we seek to describe the occurrence of each potential impact, as well as the associations among impacts and their relative statistical weight. To answer how frequently species with potential impacts were found in parks, we related how many species were causing each type of impact with their occurrence (mean ± SE) across urban parks. These pairs of values were represented in a scatter plot, including the average values for each variable as reference dash lines. Data Resources The complete species database underpinning the analysis, with their potential impacts, reported in this paper, are deposited in the Zenodo repository at https://doi. org/10.5281/zenodo.4295845 (Bayón & al. 2020). RESULTS Non-native species lists From the 486 plants of the database, eight were not at the species level, or had not valid names. Of the remaining, there were 84 native species, 6 archaeophytes and 388 non-native Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Interest and risks of non-native ornamental plants 5 species. From the non-native species, 16 were invasive; four are regulated by the Spanish catalogue (BOE 2019), conforming the Priority List: Acacia dealbata Link, present in four parks (8.7%); Buddleja davidii Franch., present in two parks (4.3%); Opuntia ficus-indica (L.) Mill., present in two parks (4.3%); and Ailanthus altissima (Mill.) Swingle, present in 20 parks (43.5%). This last species is also regulated by the European list (European Commission 2019). Only one species, Ficus benjamina L., was classified in the Green list. From the rest of species, 39 were established, 72 were casual, and 33 were not found in the wild. We found information of potential impacts for only 59 invasive and potentially invasive species. The median number for environmental impacts was four and the median for socioeconomic impacts was one. Forty-seven species (12.1% of total non-native and 79.7% of the invasive and potentially invasive species) had potential impacts at or above these threshold number of potential impacts, conforming the Attention list (Table 1) and 12 species (3.1% of the total non-native and 20.3% of the invasive and potentially invasive species) did not reach the threshold of impacts, and thus conformed the Watch list (Table 2). Finally, the Uncertainty list (Appendix 2) has 96 species (24.7% of total non-native species). Unfortunately, we could not find information on the 228 remaining species (58.8%), and thus, they were classified in the Data Deficient list (Appendix 3). Invasive and potentially invasive species occurrence There are 21 parks (46%) with some regulated species. On average, parks have 0.57 ± 0.11 (mean ± SE) invasive regulated species from the Priority List; more concretely, two parks have three regulated species, one park has two regulated species, and 18 parks (39%) have one regulated species. In addition, parks have 8.65 ± 0.97 invasive or potentially invasive species (i.e., species listed in the Attention and Watch Lists) from which 3.15 ± 0.39 are casual, 1.98 ± 0.24 are established, and 2.09 ± 0.27 non-regulated invasive in Spain. A very relevant finding is that we did not find a park without any invasive or potentially invasive species. There is a significant positive correlation between the occurrence of these 59 invasive and potentially invasive species with the Standard Trending Value (Pearson’s R = 0.52; p-val- ue < 0.001). However, the correlation between species occurrence and their WRA score was not significant (Pearson’s R = -0.23; p-value = 0.085) (Fig. 2). Potential impacts of invasive and potentially invasive species Almost the 80% of the 59 invasive and potentially invasive species have the potential to compete with native species. At the ecosystem level, the most relevant potential impact is the physical modification of the habitat (71% species), followed by impacts on natural succession (56%). The most common potential socioeconomic impact is on human health, with 53% species. The least represented potential impacts are disruption of the food webs (15%), impacts on infrastructures (15%), parasitism (10%) and hybridization with native species (10%) (Fig. 3). On average, 19.21 ± 3.59 species can cause impacts, and species with potential to cause impact are present in 6.02 ± 1.59 parks. By relating the number of species causing each impact type with their occurrence, according to their average values, we found the following patterns. First, there are three impacts (i.e., human health, physical modification of habitats and competition) that are caused by more species than average. The most frequent impact is on human health, with species causing this impact present in 7.29 ± 1.26 parks. Second, there is one impact (i.e., natural succession) caused by more species than average (33), but they are present in less parks than average (5.58 ± 0.94). Third, there are five impacts (i.e., disease transmission, interaction with other invasive species, and disruption of food webs, on nutrient cycling and on agriculture) that are also caused by less species than average, but they are present in more parks than average. Finally, five impacts (i.e., hybridization, parasitism, poisoning, toxicity and allelopathy, impacts on infrastructures and other socioeconomic impacts) are caused by less species than average and are present in less parks than average (Fig. 4). There was no negative correlation between any pair of impacts but 18 with significant positive correlations (Fig. 5). The highest correlation was between poisoning, allelopathy and toxicity and impacts on agriculture (Pearson’s R = 0.52); toxicity is also highly related to human health (R = 0.30) and other socio-economic impacts (R=0.37). There were also high correlations, between competition, the different types of toxicity, the alteration of natural succession and the modification of the structure of the habitat, with Pearson’s coefficients between R = 0.34 and R = 0.42. In general terms, there were positive correlations not only between impacts within the same category (i.e., on native species, on ecosystems, and on socioeconomics), but also among impacts across categories. DISCUSSION Species lists The introduction of plants for ornamental purposes is the main deliberate pathway for plant invasions (van Kleunen & al. 2018). Unfortunately, this path includes some of the most harmful invasive plant species (Hulme 2007). In Spain, no park is free of planted invasive or potentially invasive species. One striking result is that almost half of the parks studied have at least one regulated invasive species (Priority List). In the parks analyzed, there are four invasive species (Ailanthus altissima, Acacia dealbata, Buddleja davidii and Opuntia ficus-indica) that are regulated and thus their plantation is forbidden (Fifth Bayón & al. 6 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Table 1. Attention list: 47 invasive (not regulated) and potentially invasive species with ≥ 4 potential environmental (Env.) impacts or ≥ 1 socioeconomic (Soc.) potential impacts. Status: I = invasive, E = established, C = casual, NW = not in the wild; Climatic confidence suitability: H = high, M = medium; Environmental impacts on Spp. (species); Ecos. (ecosystems); WRA (Weed Risk Assessment): scores < 1 indicate that the species is accepted, scores 1–6 indicate that the species needs further evaluation, scores > 6 indicate that the species is rejected; STV (Standard Trending Value) ranges from 0 to 100; Source: a = Bayón & Vilà 2019, b = Gassó & al. 2010, c = de novo, d = Pino & al. 2015, e = Álvarez & al. 2016, PI (Priority Index). All species are invasive elsewhere except Schinus molle L. for which we could not find information. Species Family Status Climate confidence suitability Impacts on No. parks STV WRA PI Env. Soc. Value Source Spp. Ecos. Acacia longifolia Paxton Leguminosae I H 1 3 3 1 0 23 a 48 Acer negundo L. Sapindaceae I H 0 1 1 22 52 13 b 33 Berberis thunbergii DC. Berberidaceae NW H 3 1 1 7 41 15 a 39 Broussonetia papyrifera (L.) L’Hér. ex Vent. Moraceae E H 2 3 2 6 41 2 a 36 Brugmansia suaveolens (Willd.) Sweet Solanaceae E M 2 2 2 1 0 13 c 33 Buddleja madagascariensis Lam. Scrophulariaceae NW M 3 2 2 1 0 11 d 33 Casuarina cunninghamiana Miq. Casuarinaceae C H 1 1 2 4 45 15 b 41 Casuarina equisetifolia L. Casuarinaceae C H 2 3 2 8 32 7 a 38 Cestrum nocturnum Lam. Solanaceae C H 2 2 2 4 90 9 a 52 Cinnamomum camphora (L.) J.Presl Lauraceae NW H 3 1 2 2 52 17 a 49 Cornus sericea L. Cornaceae NW H 1 3 1 1 0 22 a 34 Cotoneaster horizontalis Decne. Rosaceae NW H 1 2 1 7 28 26 a 42 Cupressus arizonica Greene Cupressaceae C H 0 0 1 20 53 2 c 21 Elaeagnus angustifolia L. Elaeagnaceae I H 2 4 1 2 28 21 a 45 Elaeagnus pungens Thunb. Elaeagnaceae NW H 1 3 0 4 0 9 c 17 Eriobotrya japonica (Thunb.) Lindl. Rosaceae E H 0 0 1 10 33 7 e 21 Eucalyptus camaldulensis Dehnh. Myrtaceae I H 0 1 1 6 52 17 b 36 Eucalyptus globulus Labill. Myrtaceae I H 3 1 3 4 45 21 a, b 57 Eugenia uniflora L. Myrtaceae C M 3 2 0 1 0 18 a 27 Euonymus fortunei (Turcz.) Hand.-Mazz. Celastraceae NW H 1 3 0 3 0 7 a 15 Ficus rubiginosa Desf. ex Vent. Moraceae E H 3 3 1 1 20 7 a 31 Fraxinus americana L. Oleaceae NW H 0 0 1 1 0 2 c 8 Fraxinus pennsylvanica Marshall Oleaceae NW M 1 0 1 4 0 2 c 10 Gleditsia triacanthos L. Leguminosae I H 2 2 0 10 42 10 a, b 28 Grevillea robusta A.Cunn. ex R.Br. Proteaceae C H 4 3 1 6 53 2 a 37 Lonicera japonica Thunb. Caprifoliaceae I H 1 2 1 6 40 14 a, b 35 Melia azedarach L. Meliaceae E H 2 2 1 10 65 12 a 42 Morus alba L. Moraceae C H 1 2 1 18 78 2 e 34 Nandina domestica Thunb. Berberidaceae C M 3 2 2 7 96 9 a 56 Parkinsonia aculeata L. Leguminosae I H 1 0 2 6 52 15 b 41 Parthenocissus quinquefolia (L.) Planch. Vitaceae E H 2 2 1 6 20 12 c 31 Paulownia tomentosa Lam. Paulowniaceae C H 2 2 1 8 39 19 a 41 Phoenix canariensis Chabaud Arecaceae E H 3 1 2 23 93 6 a 50 Pinus radiata D.Don Pinaceae C H 2 1 2 5 52 12 a 43 Pittosporum undulatum Vent. Pittosporaceae E H 5 4 1 2 0 19 c 43 Rhus typhina L. Anacardiaceae E H 2 3 4 6 0 15 a 49 Ricinus communis L. Euphorbiaceae I H 3 3 3 1 64 20 c 66 Robinia pseudoacacia L. Leguminosae I H 3 4 3 26 100 15 a, b 73 Salix babylonica L. Salicaceae C H 0 2 1 16 52 3 c 26 Schinus molle L. Anacardiaceae I H 0 0 1 4 66 4 b 26 Schinus terebinthifolia Raddi Anacardiaceae E H 4 2 3 2 0 22 c 51 Spiraea japonica L.f. Rosaceae C H 3 1 0 4 40 11 a 29 Tecoma stans (L.) Juss. ex Kunth Bignoniaceae C M 2 2 1 1 0 11 a 25 Thunbergia grandiflora (Roxb. ex Rottl.) Roxb. Acanthaceae NW H 1 1 2 1 0 9 c 25 Wisteria sinensis (Sims) Sweet Leguminosae C H 5 3 2 5 64 9 a 54 Yucca aloifolia L. Asparagaceae C M 2 1 1 6 24 4 a, b 23 Ziziphus jujuba Mill. Rhamnaceae E H 3 2 1 4 23 17 a 38 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Interest and risks of non-native ornamental plants 7 Table 2. Watch list: 12 invasive (not regulated) and potentially invasive species with < 4 potential environmental (Env.) impacts and no socioeconomic (Soc.) potential impacts in urban parks and gardens in Spain. Status: I = invasive, E = established, C = casual, NW = not in the wild. Climatic confidence suitability : H = high, M = medium; Spp. (species); Ecos. (ecosystems); WRA (Weed Risk Assessment): scores < 1 indicate that the species is accepted, scores 1–6 indicate that the species needs further evaluation, scores > 6 indicate that the species is rejected; STV (Standard Trending Value) ranges from 0 to 100; Source: a = Bayón & Vilà 2019, b = Gassó & al. 2010, c = de novo; PI (Priority Index). Species Family Status Climatic confidence suitability Impacts on No. parks STV WRA PI Env. Soc. Value Source Spp. Ecos. Acer platanoides L. Sapindaceae E H 0 3 0 13 52 16 c 31 Albizia julibrissin Durazz. Leguminosae E H 1 1 0 9 53 14 a 32 Berberis aquifolium Pursh Berberidaceae NW H 1 1 0 6 0 -2 c 3 Ficus elastica Roxb. ex Hornem. Moraceae NW H 2 3 0 6 66 6 c 26 Jacaranda mimosifolia D.Don Bignoniaceae C M 1 2 0 10 52 -1 b 17 Lagerstroemia indica L. Lythraceae NW M 2 2 0 15 105 10 c 39 Morus nigra L. Moraceae C H 1 1 0 1 53 4 a 24 Phormium tenax J.R. Forst. & G.Forst. Xanthorrhoeaceae I H 1 3 0 8 53 10 a 29 Pinus patula Schiede ex Schltdl. & Cham. Pinaceae NW M 0 2 0 1 0 0 c 0 Pyrus calleryana Decne. Rosaceae NW H 1 1 0 4 28 1 c 12 Trachycarpus fortunei (Hook.) H.Wendl. Arecaceae C H 1 1 0 21 41 -3 c 10 Zelkova serrata (Thunb.) Makino Ulmaceae NW H 0 2 0 4 0 -4 c -3 Fig. 2. Correlation between occurrence of invasive and potentially invasive woody species in Spanish urban parks and: A) their Standard Trending Value; (Pearson’s R = 0.59, p-value < 0.001; B) their Weed Risk Assessment score (Pearson’s R = -0.22, p-value = 0.085). Reference smooth lines performed by ‘lm’. Transitory Provision, BOE 2013). Moreover, A. altissima, present in 43.5% of the parks studied, is also listed as invasive by the European Regulation (European Commission 2019). These species shall not be kept, bred or permitted to reproduce or grown, unless it is done in contained holding, where are physically isolated and cannot escape or spread by unauthorized persons (European Commission 2014). Therefore, these species should be removed from the Spanish urban parks. On the other hand, our analysis identified only one species with no risk to be invasive. Ficus benjamina is the only species in our Green list. Based on the consulted scientific evidence (CABI 2020), this species can be planted safely. However, the criteria to classify a species in the Green list is that they are not established in Spain, not invasive anywhere and the climate in mainland Spain is not suitable. The propagule pressure is an important factor determining invasion (Lockwood & al. 2005, 2009), so it is worth considering that planting species in large quantities and in many locations can change this scenario. There are possibly many species in the Data Deficient list that could be moved to the Green list but our methodology is conservative and based on the precautionary principle. We cannot encourage planting non-native species for which there is not enough information on their invasion potential. One of the highest interests for management are the species belonging to the Attention and the Watch lists. These are invasive and potentially invasive species in which we performed a detailed analysis of the impacts they can cause according to the mechanisms proposed in Blackburn & al. (2014). We recommend that species in the Attention Bayón & al. 8 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Fig. 3. Potential impacts of 59 invasive and potentially invasive woody species in Spanish urban parks. Impacts are shown from higher to lower percentage of species within each type of impacts: on native species, on ecosystems and on socioeconomic activities. Impacts on species (coral red): Compet = competition; Poison = poisoning, toxicity and allelopathic; Dis.Tr = Disease transmission; Int.IAS = interaction with other invasive non-native species; Hybrid = hybridization with native species; Paras = parasitism. Impacts on ecosystems (green): Phys.mod = physical modification of the habitats; Nat.succ = on natural succession; Nut.cycl = on nutrient cycling; Disr.food = disruption of the food webs. Socioeconomic impacts (blue): Health = on human health including allergenic pollen; Other = other socioeconomic impacts (e.g., livestock, domestic animals, and fish farming); Agric = on agriculture and forestry; Infrast = on infrastructures. Fig. 4. Number of invasive and potentially invasive woody species per park with the potential to cause each impact type, versus their occurrence (mean ± SE) across parks. Reference dashed lines show the mean value for each axis (x = 19.21 ± 3.59 species with the potential to cause the impact; y = 6.02 ± 1.59 parks in which each species are present). See abbreviations in the caption of Figure 3. Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Interest and risks of non-native ornamental plants 9 list should be considered for regulation, especially all the species with high Priority Indexes such as Ricinus communis L. (PI = 73), Robinia pseudoacacia (PI = 73), Parkinsonia aculeata L. (PI = 67) and Eucalyptus globulus Labill. (PI = 65). The remaining species of the Attention list should be at least part of a monitoring program to prevent their spread in natural areas adjacent to parks. Moreover, the 12 species in the Watch list should also be included in early warning and active surveillance programs such as the lists of non-native species potentially capable of competing with native species, altering their genetic purity or ecological balances, set out by the Ministry of Ecological Transition of Spain (BOE 2020). Because our method is reproducible, new available information has served to provide here some updates compared to a previous risk analysis on nursery plants (Bayón & Vilà 2019). Specifically the species Cupressus arizonica Greene and Jacaranda mimosifolia D.Don., that were in the Uncertainty list are now classified in the Watch list because the low number of impacts according to CABI (2020). However, there are still many species (96) in the Uncertainty list and up to 228 species (more than the half non-native species of the whole dataset) in the Data Deficient list, with no data available at all. This is a recurring problem that deserves to be addressed as soon as possible (Bayón & Vilà 2019). We think that periodic updates of species listing are needed, as new information is available (Gallardo & al. 2016), a task that requires a collective effort of a larger team of experts (González-Moreno & al. 2014; Roy & al. 2019). Society interest on invasive and potentially invasive species We found a positive correlation between the standard trending values (STV) of the species and their occurrence in the parks. This result reinforces the notion that a greater prevalence of species at urban parks generates greater interest in people. This can cause a fashion-creating effect that can act as a snowball process influencing in turn the interest on some particular species to be planted for instance in private Fig. 5. Correlation matrix (Pearson’s R) between potential impacts of invasive and potentially invasive woody species in Spanish urban parks. Impacts on species: Compet = competition; Poison = poisoning, toxicity and allelopathic; Dis.Tr = Disease transmission; Int.IAS = Interaction with other invasive non-native species; Hybrid = hybridization with native species; Paras = parasitism. Impats on ecosystems (green): Phys.mod = Physical modification of the habitats; Nat.succ = on natural succession; Nut.cycl = on nutrient cycling; Disr.food = disruption of the food webs. Socioeconomic impacts (blue): Health = on human health including allergenic pollen; Other = other socioeconomic impacts (e.g., livestock, domestic animals, and fish farming); Agric = on agriculture and forestry; Infrast = on infrastructures. Bayón & al. 16 Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Species Family Abelia triflora R.Br. ex Wall. Caprifoliaceae Abies cephalonica Loudon Pinaceae Abies concolor (Gordon & Glend.) Lindl. ex Hildebr. Pinaceae Abies nordmanniana (Steven) Spach Pinaceae Abies procera Rehder Pinaceae Abutilon pictum (Gillies ex Hook.) Walp. Malvaceae Acca sellowiana (O.Berg) Burret Myrtaceae Acer buergerianum Miq. Sapindaceae Acer cappadocicum Gled. Sapindaceae Acer davidii Franch. Sapindaceae Acer palmatum Raf. Sapindaceae Acer rubrum L. Sapindaceae Acer saccharinum L. Sapindaceae Acer tataricum L. Sapindaceae Alnus incana (L.) Moench Betulaceae Amelanchier ovalis (Willd.) Borkh Rosaceae Amomyrtus luma (Molina) D.Legrand & Kausel Myrtaceae Araucaria angustifolia (Bertol.) Kuntze Araucariaceae Araucaria araucana (Molina) K.Koch Araucariaceae Araucaria bidwillii Hook. Araucariaceae Araucaria columnaris (G.Forst.) Hook. Araucariaceae Araucaria cunninghamii Mudie Araucariaceae Araucaria heterophylla (Salisb.) Franco Araucariaceae Archontophoenix alexandrae (F.Muell.) H.Wendl. & Drude Arecaceae Arenga engleri Becc. Arecaceae Atriplex halimus L. Amaranthaceae Aucuba japonica Thunb. Garryaceae Bauhinia forficata Link Leguminosae Bauhinia variegata L. Leguminosae Berberis candidula (C.K.Schneid.) C.K.Schneid. Berberidaceae Berberis julianae C.K.Schneid. Berberidaceae Berberis wilsoniae Hemsl. Berberidaceae Betula papyrifera Marshall Betulaceae Betula pendula Roth Betulaceae Betula utilis D.Don Betulaceae Bougainvillea spectabilis Willd. Nyctaginaceae Brachychiton acerifolius (A.Cunn. ex G.Don) F.Muell. Malvaceae Brachychiton discolor F.Muell. Malvaceae Brugmansia arborea (L.) Sweet Solanaceae Butia yatay (Mart.) Becc. Arecaceae Buxus microphylla Siebold & Zucc. Buxaceae Callistemon lanceolatus (Sm.) Sweet Myrtaceae Callistemon speciosus (Sims) Sweet Myrtaceae Camellia japonica L. Theaceae Carissa macrocarpa (Eckl.) A.DC. Apocynaceae Carya illinoinensis (Wangenh.) K.Koch Juglandaceae Carya laciniosa (F.Michx.) G.Don Juglandaceae Caryota urens L. Arecaceae Castanea dentata (Marshall) Borkh. Fagaceae Catalpa bungei C.A.Mey. Bignoniaceae Ceiba speciosa (A.St.-Hil.) Ravenna Malvaceae Celtis occidentalis L. Cannabaceae Cephalotaxus fortunei Hook. Taxaceae Cercis chinensis Bunge Leguminosae Cestrum aurantiacum Lindl. Solanaceae Cestrum elegans (Brongn. ex Neumann) Schldtl. Solanaceae Appendix 3. Data Deficient list. It includes 228 species for which we did not have found sufficient data for analysis. Species Family Chaenomeles japonica (Thunb) Lindl. ex Spach Rosaceae Chamaecyparis obtusa (Siebold & Zucc.) Endl. Cupressaceae Choisya ternata Kunth Rutaceae Citrus maxima (Burm.) Merr. Rutaceae Citrus medica L. Rutaceae Coprosma repens A.Rich Rubiaceae Cordyline indivisa (G.Forst.) Endl. Asparagaceae Cordyline rubra Otto & A.Dietr. Asparagaceae Cornus florida L. Cornaceae Corylus colurna L. Betulaceae Cotoneaster franchetii Bois Rosaceae Cotoneaster pannosus Franch. Rosaceae Cotoneaster salicifolius Franch. Rosaceae Crataegus crus-galli L. Rosaceae Cryptomeria japonica (Thunb. ex L.f.) D.Don Cupressaceae Cupressus cashmeriana Royle ex Carrière Cupressaceae Cupressus funebris Endl. Cupressaceae Cupressus nootkatensis D.Don Cupressaceae Cycas circinalis L. Cycadaceae Dasylirion acrotrichum (Schiede) Zucc. Asparagaceae Deutzia scabra Thunb. Hydrangeaceae Diosma hirsuta L. Rutaceae Dodonaea viscosa Jacq. Sapindaceae Dolichandra unguis-cati (L.) L.G.Lohmann Bignoniaceae Dracaena draco (L.) L. Asparagaceae Echinocactus grusonii Hildm. Cactaceae Erythrina caffra Thunb. Leguminosae Erythrina crista-galli L. Leguminosae Escallonia paniculata Phil. Escalloniaceae Escallonia rosea Griseb. Escalloniaceae Eucalyptus cinerea F.Muell. ex Benth. Myrtaceae Eucalyptus diversicolor F.Muell. Myrtaceae Eucalyptus pauciflora Sieber ex Spreng. Myrtaceae Euonymus europaeus L. Celastraceae Fatsia japonica (Thunb.) Decne. & Planch. Araliaceae Ficus binnendijkii Miq. Moraceae Ficus craterostoma Warb. ex Mildbr. & Burret Moraceae Ficus drupacea Thunb. Moraceae Ficus macrophylla Pers, Moraceae Firmiana simplex (L.) W.Wight Malvaceae Ginkgo biloba L. Ginkgoaceae Gymnosporia heterophylla (Eckl. & Zeyh.) Loes. Celastraceae Hamamelis mollis Oliv. Hamamelidaceae Harpephyllum caffrum Bernh. Anacardiaceae Howea forsteriana (F.Muell.) Becc. Arecaceae Ilex cornuta Lindl. & Paxton Aquifoliaceae Iochroma cyaneum (Lindl.) M.L.Green Solanaceae Jasminum azoricum L. Oleaceae Jasminum fruticans L. Oleaceae Jasminum grandiflorum L. Oleaceae Jasminum humile L. Oleaceae Jubaea chilensis (Molina) Baill. Arecaceae Juglans nigra L. Juglandaceae Juniperus chinensis L. Cupressaceae Juniperus horizontalis Moench Cupressaceae Juniperus virginiana L. Cupressaceae Justicia adhatoda L. Acanthaceae Justicia brandegeeana Wassh. & L.B.Sm. Acanthaceae Anales del Jardín Botánico de Madrid 79 (1): e121. https://doi.org/10.3989/ajbm.2623 Interest and risks of non-native ornamental plants 17 Appendix 3. Contd. Species Family Justicia carnea Lindl. Acanthaceae Justicia floribunda (C.Koch) Wassh. Acanthaceae Kennedia rubicunda Vent. Leguminosae Kerria japónica (L.) DC. Rosaceae Kolkwitzia amabilis Graebn. Caprifoliaceae Ligustrum japonicum Thunb. Oleaceae Liquidambar styraciflua L. Altingiaceae Liriodendron tulipifera L. Magnoliaceae Livistona australis (R.Br.) Mart. Arecaceae Livistona decora (W.Bull) Dowe Arecaceae Lonicera caprifolium L. Caprifoliaceae Lonicera fragrantissima Lindl. & J.Paxton Caprifoliaceae Lonicera implexa Aiton Caprifoliaceae Lonicera ligustrina Wall. Caprifoliaceae Lonicera sempervirens L. Caprifoliaceae Magnolia grandiflora L. Magnoliaceae Magnolia virginiana L. Magnoliaceae Mahonia bealei (Fortune) Pynaert Berberidaceae Mahonia japónica (Thunb.) DC. Berberidaceae Malus floribunda Siebold ex Van Houtte Rosaceae Malvaviscus penduliflorus Moc. & Sessé ex DC. Malvaceae Metasequoia glyptostroboides Hu & W.C.Cheng Cupressaceae Metrosideros excelsa Sol. ex Gaertn. Myrtaceae Morus australis Poir. Moraceae Myrsine africana L. Primulaceae Nannorrhops ritchieana (Griff.) Aitch. Arecaceae Nothofagus menziesii (Hook.f.) Oerst. Nothofagaceae Nyssa sylvatica Marshall Cornaceae Osmanthus fragrans (Oackley) Archila Oleaceae Osmanthus heterophyllus (G.Don) P.S.Green Oleaceae Ostrya carpinifolia Scop. Betulaceae Ostrya virginiana (Mill.) K.Koch Betulaceae Parajubaea cocoides Burret Arecaceae Parajubaea torallyi (Mart.) Burret Arecaceae Peltophorum dubium (Spreng.) Taub. Leguminosae Persea indica (L.) Spreng. Lauraceae Philadelphus coronarius L. Hydrangeaceae Phoenix reclinata Jacq. Arecaceae Phoenix roebelenii O’Brien Arecaceae Phoenix sylvestris (L.) Roxb. Arecaceae Photinia glabra (Thunb) Maxim. Rosaceae Phymosia umbellata (Cav.) Kearney Malvaceae Picea glauca (Moench) Voss Pinaceae Picea pungens Engelm. Pinaceae Pinus nigra J.F.Arnold Pinaceae Pinus pumila (Pall.) Regel Pinaceae Pinus roxburghii Sarg. Pinaceae Pittosporum coriaceum Aiton Pittosporaceae Pittosporum crassifolium Banks & Sol. ex A.Cunn. Pittosporaceae Pittosporum truncatum E.pritz. Pittosporaceae Platanus orientalis L. Platanaceae Podocarpus macrophyllus (Thunb.) Sweet Podocarpaceae Podocarpus neriifolius D.Don Podocarpaceae Podranea ricasoliana (Tanfani) Sprague Bignoniaceae Populus yunnanensis Dode Salicaceae Prunus fruticosa Pall. Rosaceae Prunus maackii Rupr. Rosaceae Prunus sargentii Rehder Rosaceae Species Family Prunus serrulata Lindl. Rosaceae Prunus subhirtella Miq. Rosaceae Prunus virginiana L. Rosaceae Pyrus salicifolia Pall. Rosaceae Quercus castaneifolia C.A.Mey. Fagaceae Quercus macrocarpa Michx. Fagaceae Quercus palustris Münchh. Fagaceae Quercus polymorpha Schltdl. & Cham. Fagaceae Quercus rysophylla Weath. Fagaceae Rhaphiolepis indica (L.) Lindl. Rosaceae Rhapis excelsa (Thunb.) Henry Arecaceae Rhapis humilis Blume Arecaceae Rhododendron indicum (L.) Sweet Ericaceae Rhus copallinum L. Anacardiaceae Ribes sanguineum Pursh Grossulariaceae Roldana petasitis (Sims) H.Rob. & Brettell Compositae Ruscus aculeatus L. Asparagaceae Ruscus hypophyllum L. Asparagaceae Sabal bermudana L.H.Bailey Arecaceae Sabal mexicana Mart. Arecaceae Sabal minor (Jacq.) Pers. Arecaceae Sabal palmetto (Walter) Lodd. ex Schult. & Schult.f Arecaceae Salix daphnoides Vill. Salicaceae Salix humboldtiana Willd. Salicaceae Salix nigra Marshall Salicaceae Sambucus ebulus L. Adoxaceae Sequoia sempervirens (D.Don) Endl. Cupressaceae Skimmia japónica Thunb. Rutaceae Sorbus intermedia (Ehrh.) Pers. Rosaceae Sorbus torminalis (L.) Crantz Rosaceae Sparrmannia africana L.f. Malvaceae Spiraea crenata L. Rosaceae Spiraea hypericifolia L. Rosaceae Syagrus coronata (Mart.) Becc. Arecaceae Syagrus romanzoffiana (Cham.) Glassman Arecaceae Symphoricarpos orbiculatus Moench Caprifoliaceae Tamarindus indica L. Leguminosae Tamarix chinensis Lour. Tamaricaceae Taxodium distichum (L.) Rich. Cupressaceae Tecoma capensis (Thumb.) Lindl. Bignoniaceae Teucrium fruticans L. Lamiaceae Thuja occidentalis L. Cupressaceae Thuja plicata Donn ex D.Don Cupressaceae Tilia americana L. Malvaceae Tilia tomentosa Moench Malvaceae Trithrinax campestris (Burmeist.) Drude & Griseb. Arecaceae Tsuga canadensis (L.) Carrière Pinaceae Ulex parviflorus Pourr. Leguminosae Ulmus americana L. Ulmaceae Ulmus glabra Huds. Ulmaceae Vesalea floribunda M.Martens & Galeotti Caprifoliaceae Viburnum odoratissimum Ker Gawl. Adoxaceae Viburnum rhytidophyllum Hemsl. Adoxaceae Weigela florida (Bunge) A.DC. Caprifoliaceae Yucca gigantea Lem. Asparagaceae Zelkova carpinifolia (Pall.) K.Koch Ulmaceae