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Article

The Diversity of Alien Plant Species in South Africa’s National Botanical and Zoological Gardens

by
Thabiso M. Mokotjomela
1,2,*,
Sebataolo J. Rahlao
1,
Loyd R. Vukeya
3,
Christophe Baltzinger
4,
Lindokuhle V. Mangane
1,
Christopher K. Willis
5 and
Thompson M. Mutshinyalo
5
1
South Africa National Biodiversity Institute (SANBI) Directorate on Biodiversity Evidence, Free State National Botanical Garden, Raytton, Dan Pienaar, P.O. Box 29036, Danhof 9310, South Africa
2
School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg 3200, South Africa
3
Free State National Botanical Garden, Raytton, Dan Pienaar, P.O. Box 29036, Danhof 9310, South Africa
4
INRAE, UR EFNO, 45290 Nogent-sur-Vernisson, France
5
South African National Biodiversity Institute National Botanical Gardens, Pretoria National Botanical Garden, Pretoria 0184, South Africa
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(3), 407; https://doi.org/10.3390/d15030407
Submission received: 30 January 2023 / Revised: 21 February 2023 / Accepted: 21 February 2023 / Published: 10 March 2023

Abstract

:
The management of biological invasions, which pose a growing threat to natural resources and human well-being, is critical for reducing associated negative impacts. As part of the process of developing a strategy for the management of biological invasions in the South African National Biodiversity Institute’s (SANBI) gardens, we collated a list of alien plant species from 13 gardens as part of a situational analysis. We requested lists of alien plant species recorded in each of the SANBI’s gardens. A total of 380 records included 225 alien plant species belonging to 73 families. A significant number of species were intentionally introduced through horticultural trade as ornamentals (49%; n = 225), while 20.9% were consumed as either food or medicine by humans. Plant life forms included woody and herbaceous plants, graminoids, succulents and ferns. Herbaceous (42.7%; n = 225) and woody plants (3.8%) were the dominant life forms. The Walter Sisulu National Botanical Garden had the highest number of alien species (88 species), followed by Kirstenbosch (61 species) and Pretoria (46 species) National Botanical Gardens, with herbaceous species constituting the largest number in all gardens (i.e., 47, 19, and 27 species, respectively). The number of species that we recorded that were listed in the National Environmental Management: Biodiversity Act (NEM: BA) (Act No. 10 of 2004): Alien and Invasive Species Regulations’ categories were not notably different from the number of unlisted species (58.2% vs. 42.8%). The number of species listed in the different categories varied significantly across the different gardens, with a significantly higher number of unlisted species and of Category 1b species in the Walter Sisulu, Kirstenbosch and Pretoria National Botanical Gardens than in other gardens. That a significantly larger number of alien species originated from South America points to the need to improve biosecurity controls on existing relations. The results of this study provided a baseline database to help comparison between successive surveys in future.

1. Introduction

Botanical gardens represent the largest plant conservation network in the world [1], with diverse interconnected functions ranging from environmental education and scientific research to recreation [2,3]. Krishnan and Novy [4] reviewed different definitions of botanical gardens, and these definitions mainly emphasise the functions that gardens perform. For example, they were considered primarily as outdoor collections of labelled living plants in aesthetic landscapes, playing passive roles in their communities, as well as historical heritage sites. Presently, botanical gardens have evolved to include expanded programmes, such as the conservation of plant biodiversity, by serving as repositories of plant germplasm for the long-term preservation of species, scientific research, and creation of urban refuges for wildlife and humans [5]. In addition, Botanic Gardens Conservation International (BGCI) [6] defines botanical gardens as permanent institutions holding documented collections of living plants for the purposes of display and for education of the public. Although botanical gardens have focused strongly on plant conservation, a recent transition was noted whereby botanical gardens are valued as sentinel sites to identify pests and pathogen risks in biosecurity research for the early detection and eradication of alien pests, pathogens and plants’ screening prior to authorisation of their release to horticultural markets [7,8,9,10].
According to BGCI, one of the typical characteristics of botanical gardens should be the ability for an “Exchange of seed or other materials with other botanic gardens, arboreta or research institutions”. Consequently, botanical gardens have also been key in supporting economic botany during the 17th to 19th centuries, and this entailed the movement and introduction of new economically important plant species across the world [4]. Consistently, during the European expansion and exploration of Asia, South America and Africa, some European botanical gardens were engaged in economic botany and the cultivation of attractive plants [4,11]. The Europeans were actively involved in the collection and study, introduction and acclimatisation, cultivation, propagation and dissemination of newly discovered and tropical crops to colonial countries [4,12]. Similarly, botanical gardens play a major role in supporting the cultivation and distribution of alien plants that are used as ornamentals [12], with most of these alien species listed as the worst invasive species in the world, such as Lantana camara and Acacia mearnsii [8,13,14,15]. The World Resources Institute estimated that 150 million persons visited some 1500 botanical gardens around the world in 1989 [16]. Thus, it is also possible that with increased international tourist visitation to botanical gardens in the 17th and 18th centuries, alien species from different parts of the world were accidentally spread to different areas [1,17].
In South Africa, botanical gardens perform a range of diverse functions intertwined with the conservation of flora and fauna, in alignment with international conservation treaties (e.g., the Convention for Biological Diversity), research, environmental education, horticulture and nature-based tourism [2,18,19,20]. The 11 botanical gardens of the South African National Biodiversity Institute (SANBI) (i.e., Free State, Harold Porter, Karoo Desert, Hantam, Kirstenbosch, KwaZulu-Natal, Kwelera, Lowveld, Pretoria, Walter Sisulu, and Thohoyandou; see [21]) are classified as conservation gardens that, according to the BGCI’s definition (see [2,3]), contain natural vegetation that is a national conservation priority (i.e., Critical Biodiversity Areas—CBAs) in addition to their cultivated collections [20,21,22,23].
A globally distinguishing attribute of the SANBI gardens is that they conserve representative biodiversity of seven of South Africa’s nine biomes, except the Desert Biome and Indian Ocean Coastal Belt [18,21,22]. In addition, the Pretoria National Zoological Garden preserves a variety of animal species, both native and alien, for public display, and the Mokopane Biodiversity Conservation Centre has overlapping functions with both botanical gardens and zoological gardens [21]. South African National Botanical Gardens are associated with conservation priority biodiversity areas [21,23], and therefore warrant heightened protection from the escalating impacts of biological invasions.
To date, South Africa has recorded approximately 1880 alien species that have established within the country, some of which have become invasive (215 species, as indicated in Zengeya & Wilson [24]), and resulted in severe negative impacts on the recipient environment [23,24]. Biological invasions reduce biodiversity [25,26], which can threaten human well-being, especially for communities that rely on ecosystem goods and services in South Africa [26]. The impacts of biological invasions include the altering of habitat structures, hampering the proper functioning of ecosystems and limiting the availability of essential natural resources [26,27]. Subsequently, one of the strategic responses to the effective management of biological invasions in South Africa has entailed the development and enactment of legislative control via the National Environmental Management: Biodiversity Act (NEM: BA) (Act No. 10 of 2004) and the Alien and Invasive Species Regulations, hereafter called NEM:BA-A&IS Regulations [28], which are complemented by the updated 2021 NEM:BA-A&IS Regulations. It is required that SANBI must submit a report on the status of listed invasive species to the Minister of the Department of Forestry, Fisheries and the Environment (DFFE) every three years. Indeed, Zengeya and Wilson [24] pointed to the patchiness of species information as one of the main factors slowing the effective management of biological invasions in South Africa. The knowledge of alien species’ records in the SANBI gardens constitutes critical indicators for monitoring biological invasions at the national level across South Africa [29,30], which may enhance the effective management of the impacts of such species in SANBI’s gardens.
Despite the known and increasing negative impacts of biological invasions reported in the two national status reports produced thus far [24,26,30], the effective management of biological invasions in South Africa has been difficult because of several challenges. For instance, there is no overarching national management strategy for guiding different role players in safeguarding the national biodiversity and SANBI’s national gardens from the negative impacts of biological invasions in South Africa. Above all, there is a paucity in the knowledge of the numbers of alien and invasive species, and their associated negative impacts are a nationwide problem that include SANBI’s national gardens. Zengeya et al. [31] raised the issue of low reliability of current existing estimates of the numbers of species in different contexts. In addition, the lack of human capacity and limited resources hampers the success of containing the problem of biological invasions in different contexts, such as within local municipalities [32,33] and SANBI gardens. Although the NEM:BA-A&IS Regulations [28] emphasized the development of management plans for alien species occurring on state and private land, there has generally been limited compliance, partly due to the scarcity of scientific skills in invasion biology [29].
In view of the above arguments, the aims of this study were to: (1) document the diversity of alien and invasive plant species occurring in SANBI’s gardens with the purpose of informing the development of a management strategy; and (2) classify different alien plant species recorded in different gardens based on continental origin, life form and their status as per the NEM:BA-A&IS regulations, to guide prioritisation in resources’ allocation for management interventions. This is the first study to start screening and assessing the invasion risk for biodiversity conservation in South Africa’s gardens (see a case study in China: Ni & Hulme [15]).

2. Methods and Materials

2.1. Study Area

The study was conducted in South Africa in 11 SANBI botanical gardens, 1 zoological garden and the Mokopane Biodiversity Conservation Centre, which are situated in 8 provinces and 7 South African biomes (Figure 1). The SANBI national botanical gardens are located in eight of South Africa’s nine provinces, where there are unique vegetation types targeted for conservation (Table 1 [21]). These study sites were selected because they are all managed by SANBI and have a common function of biodiversity conservation.

2.2. Data Collection

The species data were obtained by requesting lists of alien species for each of the 13 SANBI gardens from the curators and garden estate managers.
Several key sources were used for plant species identification, including field guides by Bromilow [34,35] and Henderson [36], the Invasive Species South African Database [37] and herbarium specimen collections. Due to limited evidence, some species were identified only up to the genus level.
Species names were verified using the national resource: “The Status of Biological Invasions and their Management in South Africa” [24,26].
Following the criterion described in Mokotjomela et al. [33], plant species were classified by life form as follows: herbs, graminoids, succulents, woody for the shrubs and trees and ferns using the Botanical Database of Southern Africa (BODATSA) [38] and the Integrated Taxonomic Information System (Table A1, [39]). Pyšek et al. [40] showed that some species’ traits, especially life form, stature and pollination syndrome, may provide a method of predicting impact, regardless of the habitat and geographical region invaded. In addition, the region of origin is critical for understanding and managing the pathway of introduction for alien species (see also [41]). The data collected for each species included the gardens and their provincial locations where the species was recorded in South Africa, the reason for introduction as a proxy for the pathway pattern, and the continental origin of each species. Since the native range of the species is important for climate matching with the recipient environment during invasion risk assessment [42], we made an assumption that the species were introduced directly to South Africa from their native continent. Inasmuch as the exact country of origin of each species was identified (after [12,33]), for this study we used the continental and/or broad region to classify the recorded species as specified in the Centre for Agriculture and Bioscience International (CABI) and Global Invasive Species Database. Species were also categorised following the NEM:BA-A&IS Regulations, 2021. There are four categories—1a, 1b, 2, and 3—depending on what is permitted and the overall management goal [43,44], and the “Not listed species” (denoted by NL; 33; Table 2 and Table A1).
Depending on the risk assessment outcome of each alien species in South Africa and their differential occurrence and impacts in different provinces (Kumschick et al. [42]), some species tend to have more than one listing category based on the context in which a risk assessment was carried out. To avoid allocating one species into more than one category, the most common category and/or where a species is a priority for management was considered to be the correct category in this study [33]. Additionally, the newly adopted risk assessment framework for South Africa classified species based on risk assessment for the whole country [42] instead of the contexts in each province as shown for different categories presented in the national status report and the national regulations [26].

2.3. Data Analyses

2.3.1. Species and Families

From the total records of alien species obtained from different gardens (Table 1), we identified the gardens that have the highest number of alien species, the dominant plant families and the most common species across the gardens. We also determined if there was an overlap among the gardens in the alien plant species that occur in each.

2.3.2. Species Classification: Continental Origin, Life Forms, and NEM:BA-A&IS Categories

To compare the numbers of alien species in different classification categories (i.e., life form, NEM:BA-A&IS Regulations’ categories, species’ continental origin and reason for plant species introduction (pathway)), species count data were analysed using a Generalised Linear Models (GLM), with a Poisson error distribution and log link in SPSS software, version 20. The counts of alien plant species were generated from total records obtained from different gardens, and they were specified as the dependent variable. Different species classification categories were treated as predictor variables.

3. Results

3.1. Identification of Alien Plant Species and Families

In total, there were 380 alien species records from in 13 SANBI gardens, representing 225 unique alien plant species belonging to 73 families. Different life forms included herbs (42.7%; n = 225), woody plants (37.8%), graminoids (10.7%), succulents (6.7%) and ferns (2.2%). The most common species, occurring in more than six gardens, were: Solanum mauritianum (11 gardens), Lantana camara (10), Melia azedarach (10) and Acacia mearnsii, Jacaranda mimosifolia, Opuntia ficus-indica and Ricinus communis (6 each). Among the reported plant species, a significant number (49%; n = 225) were introduced through horticultural trade as ornamental plant species (Wald χ2 = 27.3; df = 6; p < 0.001), followed by plant species used for human consumption—medicine and food (Wald χ2 = 5.2; df = 1; p = 0.023) being more dominant.
The most represented families in the records were Fabaceae (29 species) (mainly Acacia), Asteraceae (24 species), Poaceae (23 species), Solanaceae (14 species) (mainly Solanum), Myrtaceae (11 species) (mainly Eucalyptus) and Cactaceae (11 species) (mainly Opuntia).
Walter Sisulu NBG had the highest number of alien species records (88 species), followed by Kirstenbosch NBG (61 species) and Pretoria NBG (46 species) (Figure 2).

3.2. Comparing Continental Origin of Different Alien Species, Life Forms and NEM:BA-A&IS Regulations’ Categories

There was a statistically significant relationship between the number of alien species recorded across SANBI gardens and different continental regions of the world (Pearson χ2 = 199.2; df = 48; p < 0.001; Figure 3). Overall, most plant species were from the North and South Americas together (50 + 66 = 106 species). A significantly greater number of species were introduced from South America than from Asia (Wald χ2 = 7.5; df = 1; p = 0.006) and Australia (Wald χ2 = 49.9; df = 1; p < 0.001). However, the number of species from South America was not significantly different from the number of species from Europe (Wald χ2 = 0.1; df = 1; p = 0.776) and North America (Wald χ2 = 1.0; df = 1; p = 0.326).
There was a statistically significant relationship between the number of alien species recorded in SANBI gardens and life forms (Pearson χ2 = 353.5; df = 60; p < 0.001; Figure 4; Table A1). Herbaceous and woody alien species were dominant in the records. There was a significantly greater number of woody species than succulents (Wald χ2 = 7.9; df = 1; p = 0.005) and graminoids (Wald χ2 = 3.8; df = 1; p = 0.052). However, the number of woody species was not significantly different than the number of herbs (Wald χ2 = 2.1; df = 1; p = 0.258), and ferns (Wald χ2 = 1.3; df = 1; p = 0.258). It was noteworthy that the herbaceous species accounted for the largest number of species (i.e., 40 out of 88 species) in Walter Sisulu NBG (Figure 4; Table A1).
Finally, there were no statistically significant differences between the number of alien species listed in different NEM:BA-A&IS Regulations’ categories and the number of unlisted species (χ2 = 8.9; df = 4; p = 0.317: 58.2% vs 42.8%). We noted significant differences in the number of alien species representing each NEM:BA-A&IS Regulations’ category in three gardens; namely, Walter Sisulu NBG, Kirstenbosch NBG and Pretoria NBG (Pearson χ2 = 151.0; df = 48; p < 0.001; Figure 5). Walter Sisulu NBG had the highest number of unlisted (38 species) species and category 1b species (39), followed by Kirstenbosch NBG (32, 24) and Pretoria NBG (25, 18), respectively.

4. Discussions

We recorded a total of 225 alien plant species occurring in SANBI botanical gardens, and this can be partly attributed to deliberate introductions of species to these gardens for economic botany and ornamental and conservation research purposes [12,41,45]. Deliberate introduction of alien species for biosecurity screening in different parts of the world was previously reported [10,15,16,41], while the accidental introduction of some species as contaminants is common in many areas, including South Africa [12,46]. In the SANBI gardens, we found a large number of plant species (49%; n = 225) that were introduced through horticultural trade as ornamentals [intentional introductions, 41] in South Africa and that evidently escaped [34]. Unintentional introductions of alien species could also be accelerated by the fact that botanical gardens attract large numbers of visitors from different parts of the world performing different activities, including grilling meat with firewood from unknown sources [16], and this may account for the proportion of our records that had no specific known use (10.7 %, n = 225) in South Africa. We also suggest that, in part, the large diversity of alien plant species reported in this study is a likely result of their diverse uses [10,33,46] in the multi-racial South African society [46,47,48].
Other alien species are likely to have invaded the gardens by natural spread, such as through the dispersal of fleshy-fruited species by birds [48,49,50,51], roadways connecting the gardens with different potential alien propagule sources, such as urban home gardens [33,52,53] and river systems that traverse most of the gardens [20,54]. Indeed, van Kleunen et al. [12] have shown that horticultural alien species tend to have spread more than many other alien species, and that they naturalise much better, which is essential for invasion [55]. Apart from this, many SANBI gardens are situated near urbanised areas, thus making them vulnerable to high alien plant propagule pressure that promotes invasion [56]. The fragmentation of habitats, especially in urban areas, shifts the ecological balance away from native species and towards favouring the human-associated alien species [45,57]. However, since SANBI gardens are protected and experience low biophysical disturbance (e.g., [20,21]), they may have some natural resistance to invasion by alien species [58].
It has been shown that over 100 alien species have attained invasive status, with considerable direct and indirect negative impacts on the rich biotas of South Africa [59]. The fact that we recorded some of the most abundant and damaging alien woody plant species (i.e., Lantana camara and Solanum mauritianum; [26]) and Melia azedarach in the majority of the SANBI gardens (10–11) points to the possibility of undocumented impacts of these species. Above all, L. camara and Acacia mearnsii are among the worst alien invasive species in the world [13], and were recorded in some of the SANBI gardens. Additionally, the negative impacts of woody alien species (i.e., including trees and shrubs) have been documented [24,26], as well as their increasing numbers in South Africa [25,60]. In South Africa, the local biodiversity is threatened by, among others, the 141 Australian Acacia species (wattles), of which 13 are highly invasive and growing prolifically both in cultivation and outside [44,61]. While M. azedarach does not have major or severe known negative impacts in South Africa [24], we argue that its abundance suggests a possible effective long-distance dispersal mediated by local vertebrates which could compromise the dispersal of native species [62]. A plausible explanation of the finding is an absence of dedicated management plans (limited compliance) and limited capacity to implement control measures [20,33]. Since the impacts of alien species have not been investigated in SANBI gardens, this study provides bases for the urgent planning and prioritisation of efforts to manage the affected gardens.
Knowledge of the life forms and life cycles of different alien plant species and their native range can guide the prediction of invasion risk and support invasion scenario planning for management [40,63]. Our finding of a large number of herbaceous and woody species in the SANBI gardens is possibly due to the predominance of agricultural introductions for fodder in the neighbourhood farms, horticultural elements [46] and the use of graminoids for biofuel production in neighbouring farms [64]. Alien herbs and grasses are notorious in the farming sector, where they outcompete and reduce the numbers of palatable species in the pastures [65]. Nevertheless, there has been limited research on the negative impacts of herbs and grasses in South Africa [64], and specifically on the preserved vegetation in SANBI gardens as a unique land-use type (see [20]). We suggest that Walter Sisulu NBG may have the highest number of herbaceous species and other life forms because of high propagule pressure created by a water stream emerging from a catchment embedded in urbanised human settlements [66,67]. Although we could not distinguish between the intentional and unintentional species introductions, we also speculate that, in part, a high influx of international tourists in Gauteng (to Walter Sisulu & Pretoria NBGs) and the Western Cape (Kirstenbosch NBG) provinces, particularly from the Americas and Europe, are some of the unintentional sources of most species in this study. Above all, these gardens are located in the economic hubs of South Africa where there are numerous activities that facilitate alien species’ spread [33], as well as a large local human population, as asserted in Pyšek et al. [68].
Biological invasions are reported to be one of the major drivers of ecological degradation in the grassland and fynbos biomes of South Africa [45,69,70], and, consistently, the gardens located in the fynbos and grassland biomes had a high number of alien species [20]. Most SANBI gardens have either wetlands or river systems, and indeed we recorded some of the species that have been specified as common in such environments by Richardson et al. [45]. Although Prosopis glandulosa is common in arid areas [45], it was not reported as present in the arid Hantum and Karoo National Botanical Garden, possibly due to effective garden management in place. In general, we recorded many similar species to those identified in different main habitats by Richardson et al. [45], and even some alien plant species that were not known in the national regulations. Consequently, we assert that systematic sampling of alien species in SANBI gardens will be critical to improving the list we presented in this study.
While the abundance of the recorded species was not measured, the management of the existing populations is important to mitigate negative impacts. Listing the alien species in the national regulations facilitates understanding the species’ impacts and their management needs [33,42,63], and thus prioritisation of limited resources. Alien species categorised as “1b” in the national regulations are targets for containment and, consequently, their occurrence in large numbers in SANBI gardens is possibly due to the absence of management actions. It is also possible that a large number (41.8%; n = 225) of the species were not listed in the national regulations due to limited capacity in performing the alien taxa risk assessment and profiling [see the framework, 42]. A large number of unlisted alien plant species corroborates the recent reports that there are many alien species that have not been documented [12,24,26,33,63], with actual numbers of invasive species increasing in South Africa [25]. In addition, this finding highlights the absence or limited scientific research needed to support the science-based management of biological invasions which could partly thwart management success in South Africa [33]. The results of this study are key to improving the development and implementation of integrated management plans to protect the integrity and sustainable conservation of the gardens’ ecosystems from future impacts on botanical gardens as an important conservation strategy for the world’s flora [2]. On the other hand, the horticultural plant propagations in botanical gardens can be pivotal for vegetation rehabilitation/restoration through reintroducing native species in degraded landscapes [2,4,70,71,72]).

5. Concluding Remarks

In this study, we have presented a list of alien and invasive plant species occurring in SANBI gardens located in different parts of South Africa, which may guide the safeguarding of biodiversity conservation gardens from the threats posed by biological invasions [2]. Indeed, compiling species lists and regular monitoring of high-risk sites, including the botanical gardens, can strengthen their management if public awareness campaigns are conducted timeously and the escape of various alien species from different points of introduction is reduced. We also recognise the complexity of the relationship between human socio-economic needs and alien species, and thus advocate for increased awareness of negative impacts as a potential strategy for mitigation. The findings in this study constitute progress toward reducing the reported uncertainty of the existing alien species data sets that restrict planning management of biological invasions in South Africa [63].
While this is the first study to collate this information, it is apparent that even the invasion status of unlisted species and potential negative impacts have not been investigated in SANBI gardens; a gap that Foxcroft et al. [32] identified as a major obstacle to effective science-based management of biological invasions in South Africa. The potentially impactful species populations will need to undergo clearing that is coupled with restoration using native plant species [72]. The finding that many plant species were not listed in the national regulations highlights the important knowledge gap in the negative impacts of the alien species in question and/or capacity constraints for compilation of the risk assessment. Further systematic surveys for alien and invasive species are required to improve the knowledge of invasion risk in biodiversity conservation gardens around the world. Considering the prominence of the role of botanical gardens in the dissemination of alien plants, the eight key research questions listed by van Kleunen et al. [12] should be explored in SANBI botanical gardens as a way of improving the current data sets and improving the management of negative impacts of the biological invasions in the preserved biodiversity as a natural asset in SANBI gardens.

Author Contributions

T.M.M. (Thabiso M. Mokotjomelaand), S.J.R. and L.V.M. conceptualized the study during the development of the strategy for management of biological invasions in SANBI Botanical and Zoological Gardens and collected field data for situational analysis. T.M.M. (Thabiso M. Mokotjomelaand), L.R.V. and C.B. verified the alien species’ records, statistically analysed field data and wrote the paper. C.K.W., T.M.M. (Thompson M. Mutshinyalo) and C.B. commented on the MS. C.B. provided reviews of the study. All authors have read and agreed to the published version of the manuscript.

Funding

Funding support for this study was provided by the South African National Biodiversity Institute (SANBI). The South African Department of Forestry, Fisheries and the Environment (DFFE) are also thanked for partial funding, noting that this publication does not necessarily represent the views or opinions of DFFE or its employees.

Institution Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available on request.

Acknowledgments

Different SANBI gardens’ managers provided valuable information on the state of management of biological invasions. Anish Dayaram provided information on the biomes of South Africa. Mbali Mkhize and Hannelie Snyman provided important species’ information from the South African Plant Invader Atlas database and Herbarium records.

Conflicts of Interest

The authors declare that there are no conflict of interest.

Appendix A

Table A1. List of alien plant taxa recorded in different SANBI botanical and zoological gardens (following SANBI 2016: BODATSA 2016, and it is: https://www.itis.gov/servlet/SingleRpt/SingleRpt#null, accessed on 15 February 2023). Each plant species was classified according to family, life form, NEM:BA-AIS Regulations’ categories and invasion status defined by Blackburn et al. [73].
Table A1. List of alien plant taxa recorded in different SANBI botanical and zoological gardens (following SANBI 2016: BODATSA 2016, and it is: https://www.itis.gov/servlet/SingleRpt/SingleRpt#null, accessed on 15 February 2023). Each plant species was classified according to family, life form, NEM:BA-AIS Regulations’ categories and invasion status defined by Blackburn et al. [73].
FamilyGenus, Species and Lower TaxaLife FormNEM:BA-AIS Regs. CatAlien Status 73
AdoxaceaeViburnum tinus L.WoodyNL-
AlismataceaeSagittaria latifolia Willd.HerbNLInvasive
AmaranthaceaeAmaranthus hybridus L.HerbNLInvasive
Atriplex inflata F.Muell.Herb1bInvasive
Chenopodium album L.HerbNLInvasive
Dysphania sect. botryoides (L.) Mosyakin & ClemantsHerbNL-
Salsola kali L.Herb1bInvasive
AnacardiaceaeSchinus molle L.WoodyNLInvasive
ApiaceaeFoeniculum vulgare A.W.HillHerbNLInvasive
Cyclospermum leptophyllum (Pers.)HerbNL-
ApocynaceaeAraujia sericifera Brot.Herb1bInvasive
Thevetia peruviana (Pers.) K. Schum.Woody1bInvasive
Vinca major L.Herb1bInvasive
AristolochiaceaeAristolochia elegans Mast.Woody1bInvasive
AsparagaceaeAgave americana L. var. americanaSucculentNLInvasive
Agave sisalana PerrineSucculent2Invasive
Furcraea foetida L.Succulent1aInvasive
Yucca sp.SucculentNL-
AsteraceaeAgeratum conyzoides (Mill.) M.SharmaHerb1bInvasive
Ageratina adenophora (Spreng.) R.M.King & H.Rob.Herb1bInvasive
Bidens bipinnata L.HerbNLInvasive
Bidens pilosa L.HerbNLInvasive
Campuloclinium macrocephalum (Less.) DC.Herb1bInvasive
Chromolaena odorata (L.) R.M.King & H.Rob.Herb1bInvasive
Cirsium vulgare (Savi) Ten.Herb1bInvasive
Conyza sumatrensis (Retz.) E.WalkerHerbNLInvasive
Cosmos bipinnatus Cav.Herb NLInvasive
Flaveria bidentis (L) KuntzeHerb1bInvasive
Galinsoga ciliata (Raf.) BlakeHerbNL-
Hypochaeris microcephala (Sch.Bip.) CabreraHerbNL-
Hypochaeris radicata L.HerbNLInvasive
Lactuca indica L.HerbNL-
Schkuhria pinnata (Lam.) Kuntze ex Thell.HerbNLInvasive
Sonchus oleraceus L.HerbNLInvasive
Sphagneticola trilobata (L.) PruskiHerb1bInvasive
Tagetes minuta L.HerbNLInvasive
Tithonia diversifolia (Hemsl.) A.GrayHerb1bInvasive
Tithonia rotundifolia S.F.Blake (Mill.)Herb1bInvasive
Zinnia peruviana L.HerbNLInvasive
BasellaceaeAnredera cordifolia (Ten.) SteenisHerb1bInvasive
BignoniaceaeDolichandra unguis-cati L. (A.Gentry)Woody1bInvasive
Jacaranda mimosifolia D.DonWoody1bInvasive
Tecoma stans (L.) Juss. ex KunthWoody1bInvasive
BoraginaceaeAmsinckia menziesii var. retrorsa (Lehm.) A.Nelson & J.F.Macbr.HerbNLInvasive
Echium plantagineum L.Herb1bInvasive
Heliotropium amplexicaule VahlHerbNLInvasive
Heliotropium europaeum L.HerbNLInvasive
BrassicaceaeBrassica juncea (L.) Czern.HerbNL-
Capsella bursa-pastoris (L.) Medik.HerbNLIntroduced but not naturalized
Nasturtium officinale R.Br.Herb2Invasive
Raphanus raphanistrum L.HerbNLInvasive
CactaceaeCereus jamacaru DC.Succulent1bInvasive
Cylindropuntia imbricata (Haw.) F.M.KnuthSucculent1bInvasive
Trichocereus spachianus (Lem.) RiccobSucculent1bInvasive
Opuntia aurantiaca Lindl.Succulent1bInvasive
Opuntia engelmannii Salm-Dyck ex Engelm.Succulent1bInvasive
Opuntia ficus-indica (L.) Mill.Succulent1bInvasive
Opuntia leucotricha DC.Succulent1bInvasive
Opuntia microdasys (Lehm.) Pfeiff.Succulent1bInvasive
Opuntia pubescens J.C.Wendl. ex Pfeiff.Succulent1aIntroduced but not naturalized
Opuntia stricta (Haw.) Haw.Succulent1bInvasive
CannabaceaeCeltis australis L.Woody3Introduced but not naturalized
CannaceaeCanna indica L.Herb1bInvasive
CaprifoliaceaeCentranthus ruber (L.) DC.Herb1bInvasive
Lonicera japonica Thunb.’Halliana’Woody3Invasive
CaryophyllaceaeSilene gallica L.Herb NL-
CistaceaeCistus ladanifer L.WoodyNLInvasive
CommelinaceaeTradescantia fluminensis Vell.Herb1bInvasive
ConvolvulaceaeConvolvulus arvensis L.Herb1bIntroduced but not naturalized
Cuscuta campestris Yunck.Herb1bInvasive
Ipomoea purpurea (L.) RothHerb1bInvasive
CrassulaceaeBryophyllum delagoense (Eckl. & Zeyh.) SchinzSucculent1bInvasive
CucurbitaceaeDiplocyclos palmatus L.Woody1aInvasive
CyatheaceaeSphaeropteris excelsa (Endl.) R.M.TryonFernNLInvasive
CyperaceaeCyperus eragrostis Lam.GraminoidsNL-
EuphorbiaceaeEuphorbia heterophylla L.HerbNL-
Euphorbia peplus L.HerbNL-
Homalanthus populifolius Graham.Woody1bInvasive
Mercurialis annua L.HerbNL-
Ricinus communis L.Woody2Invasive
FabaceaeAcacia cyclops A.Cunn. ex G.DonWoody1bInvasive
Acacia dealbata LinkWoody2Invasive
Acacia elata A.Cunn. ex Benth.Woody1bInvasive
Acacia longifolia (Andrews) Willd.Woody1bInvasive
Acacia mearnsii De Wild.Woody2Invasive
Acacia melanoxylon R.Br.Woody2Invasive
Acacia podalyriifolia A.Cunn. ex G.DonWoody1bInvasive
Acacia saligna (Labill.) H.L.Wendl.Woody1bInvasive
Caesalpinia decapetala (Roth) AlstonWoody1bInvasive
Caesalpinia gilliesii Wall. ex. Hook.Woody1bInvasive
Crotalaria agatiflora Schweinf.Woody1bInvasive
Cytisus palmensis (Christ) Hutch.WoodyNL-
Desmodium sp.WoodyNL-
Gleditsia triacanthos L.Woody1bInvasive
Medicago lupulina L.HerbNL-
Medicago polymorpha L. var. brevispina (Benth.) HeynHerbNL-
Paraserianthes lophantha (Willd.) I.C.NielsenWoody1bInvasive
Prosopis glandulosa var. torreyana (L.D.Benson) M.C.Johnst.Woody1bInvasive
Robinia pseudoacacia L.Woody1bInvasive
Senna bicapsularis (L.) Roxb.Woody1bInvasive
Senna septemtrionalis (Viv.) H.S.Irwin & Barneby Woody1bInvasive
Senna sp.Woody1b-
Sesbania bispinosa
(Jacq.) W.Wight
WoodyNL-
Sesbania punicea (Cav.) Benth.Woody1bInvasive
Spartium junceum L.Woody1bInvasive
Tipuana tipu (Benth.) KuntzeWoody3Invasive
Vicia atropurpurea L.HerbNL-
Vicia sativa L.HerbNL-
FagaceaeQuercus robur L.WoodyNLInvasive
HypericaceaeHypericum canariense L.WoodyNL-
IridaceaeIris pseudacorus L.Herb1aInvasive
Sisyrynchium sp.HerbNL-
JuncaceaeJuncus bufonius L. aggregateHerbNL-
LamiaceaeSalvia tiliifolia Vahl.Herb1bInvasive
LauraceaeCinnamomum camphora (L.) J.PreslWoody1bInvasive
LiliaceaeLilium formosanum WallaceHerb1aInvasive
MalvaceaeHibiscus trionum L.HerbNLInvasive
MeliaceaeMelia azedarach L.Woody1bInvasive
MoraceaeMorus alba L.Woody3Invasive
Morus nigra L.WoodyNL-
MyrtaceaeEucalyptus camaldulensis Dehnh.Woody1bInvasive
Eucalyptus grandis W.Hill ex MaidenWoody1bInvasive
Eucalyptus paniculata Sm.WoodyNLIntroduced but not naturalized
Eucalyptus saligna Sm.WoodyNL-
Leptospermum laevigatum (Gaertn.) F.Muell.Woody1bInvasive
Callistemon rigidus R.Br..Woody1bInvasive
Metrosideros excelsa Sol. ex Gaertn.Woody1aInvasive
Myrtus communis L.WoodyNL-
Psidium guajava L.Woody2Invasive
Syzygium paniculatum Gaertn.WoodyNLInvasive
NyctaginaceaeMirabilis jalapa L.Herb1bInvasive
NymphaeaceaeNymphaea mexicana ZuccHerb1bInvasive
OleaceaeLigustrum japonicum Thun.Woody1bInvasive
Ligustrum lucidum W.T. AitonWoody1bInvasive
Ligustrum vulgare L.Woody1bInvasive
Syringa vulgaris L.Woody NL-
OnagraceaeOenothera rosea L’Herit. ex AitonHerbNLInvasive
Oenothera stricta Ledeb. ex LinkHerbNLInvasive
Oenothera tetraptera Cav.HerbNLIntroduced but not naturalized
OxalidaceaeOxalis corniculata L.HerbNLInvasive
Oxalis latifolia KunthHerbNLInvasive
PapaveraceaeArgemone ochroleuca SweetHerb1bInvasive
Fumaria muralis Sond. ex KochHerbNLIntroduced but not naturalized
Papaver rhoeas L.HerbNLInvasive
PassifloraceaePassiflora caerulea L.Herb1bInvasive
Passiflora edulis Sims.Herb2Invasive
Passiflora ligularis Juss.HerbNL-
Passiflora subpeltata Ortega.Herb1bInvasive
PhytolaccaceaePhytolacca americana L.Herb1bInvasive
Phytolacca dioica L.Woody3Invasive
Phytolacca octandra L.Herb1bInvasive
PinaceaePinus patula Schiede ex Schltdl. & Cham.Woody2Invasive
Pinus pinaster AitonWoody1bInvasive
PittosporaceaePittosporum undulatum Vent.Woody1bInvasive
PlantaginaceaePlantago lanceolata L.HerbNLInvasive
Plantago major L.HerbNLInvasive
PoaceaeArundo donax L. 1753Graminoids1bInvasive
Avena barbata Pott ex LinkGraminoidsNLIntroduced but not naturalized
Avena fatua L.GraminoidsNLInvasive
Brachypodium distachyon (L.) P.Beauv.GraminoidsNL-
Briza maxima L.GraminoidsNLIntroduced but not naturalized
Bromus diandrus RothGraminoidsNLIntroduced but not naturalized
Bromus pectinatus Thunb.GraminoidsNLIntroduced but not naturalized
Bromus rigidus Roth.GraminoidsNL-
Calamagrostis acutiflora (Schrad.) Rchb.GraminoidsNLNA
Cortaderia jubata (Lemoine) Stapf.Graminoids1b-
Digitaria debilis (Desf.) Willd.GraminoidsNL-
Eragrostis mexicana (Hornem.) LinkGraminoidsNL-
Hordeum murinum L.GraminoidsNLInvasive
Imperata cylindrica (L.) RaeuschGraminoidsNL-
Lolium rigidum GaudinGraminoidsNLIntroduced
Nassella trichotoma (Nees) Hack. ex Arechav.Graminoids1b invasive
Paspalum dilatatum Poir.GraminoidsNLInvasive
Paspalum urvillei Steud.GraminoidsNLInvasive
Pennisetum clandestinum Hochst. ex Chiov.Graminoids1bInvasive
Pennisetum setaceum (Forssk.) Chiov.Graminoids1bInvasive
Pennisetum villosum
R.Br. ex Fresen.
Graminoids1b-
Phalaris minor Retz. (1783)GraminoidsNL-
Stipa capensis Thunb.GraminoidsNLIntroduced
Vulpia myuros (L.) C.C. Gmel.GraminoidsNL-
PontederiaceaePontederia crassipes (Mart.) SolmsHerb1bInvasive
PolypodiaceaeNephrolepis cordifolia L.Fern1bInvasive
Nephrolepis exaltata (L.) SchottFern1bInvasive
PrimulaceaeArdisia crenata SimsWoody1bInvasive
Lysimachia arvensis L.HerbNLIntroduced but not naturalized
PteridaceaeAdiantum raddianum PreslFernNLIntroduced but not naturalized
RosaceaeCotoneaster franchetii BoisWoody 1bInvasive
Cotoneaster pannosus Franch.Woody1bInvasive
Potentilla indica (Jacks.) FockeHerbNLInvasive
Prunus persica (L.) BatschWoodyNLInvasive
Pyracantha angustifolia (Franch.) C.K.Schneid.Woody1bInvasive
Pyracantha coccinea M.Roem.Woody1bInvasive
Rosa rubiginosa L.Woody1bInvasive
Rubus cuneifolius Pursh.Woody1bInvasive
Rubus fruticosus Lour.Woody2Invasive
Rubus odoratus L.Woody NL-
RubiaceaeRichardia brasiliensis GomesHerbNLInvasive
SalicaceaePopulus canescens (Aiton) Sm.Woody2Invasive
SalviniaceaeAzolla filiculoides Lam.Fern1bInvasive
SapindaceaeCardiospermum grandiflorum SwartzWoody1bInvasive
ScrophulariaceaeVerbascum chaixii Vill.HerbNL-
SimaroubaceaeAilanthus altissima (Mill.) SwingleWoody1bInvasive
SolanaceaeCestrum aurantiacum Lindl.Woody1bInvasive
Cestrum laevigatum Schltdl.Woody1bInvasive
Cestrum parqui L’Her.Woody1bInvasive
Datura ferox L.Herb1bInvasive
Datura innoxia Mill.Herb1bInvasive
Datura stramonium L.Herb1bInvasive
Physalis angulata L.HerbNLIntroduced but not naturalized
Physalis peruviana L.HerbNLInvasive
Physalis viscosa L.HerbNLInvasive
Solanum elaeagnifolium Cav.Woody1bInvasive
Solanum mauritianum Scop.Woody1bInvasive
Solanum nigrum L.HerbNL-
Solanum pseudocapsicum L.Herb1bInvasive
Solanum seaforthianum AndrewsWoody1bInvasive
Solanum sisymbriifolium Lam.Herb1bInvasive
TropaeolaceaeTropaeolum majus L.HerbNLInvasive
Tropaeolum speciosum Poepp. & Endl.Herb3NA
VerbenaceaeLantana camara L.Woody1bInvasive
Phyla nodiflora (L.) GreeneHerbNL-
Verbena aristigera S.MooreHerbNL-
Verbena bonariensis L.Herb1bInvasive
ZingiberaceaeHedychium coronarium J.Koenig.Herb1bInvasive
Hedychium flavescens Carey ex Roscoe.Herb1bInvasive

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Figure 1. The locations of the SANBI botanical and zoological gardens overlayed on the national vegetation map of South Africa (i.e., vegetation layers from Mucina and Rutherford [22]).
Figure 1. The locations of the SANBI botanical and zoological gardens overlayed on the national vegetation map of South Africa (i.e., vegetation layers from Mucina and Rutherford [22]).
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Figure 2. The number of alien plant species recorded in SANBI gardens.
Figure 2. The number of alien plant species recorded in SANBI gardens.
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Figure 3. Number of records of different alien species from different continental space (%; n = 380; (A)) and their occurrence in different SANBI gardens (B).
Figure 3. Number of records of different alien species from different continental space (%; n = 380; (A)) and their occurrence in different SANBI gardens (B).
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Figure 4. Number of records of different alien plant species in each life form (%; n = 380; (A)) and their occurrence in different SANBI gardens (B).
Figure 4. Number of records of different alien plant species in each life form (%; n = 380; (A)) and their occurrence in different SANBI gardens (B).
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Figure 5. Numbers of alien species’ records (%; n = 380) in different NEM:BA-AIS Regulations’ categories for species (A) and their occurrence in different SANBI Gardens (B). Cat. = Category. Category 1a: Species that are targets for eradication. Category 1b: Species that are control targets and need a national management plan. Category 2: Species requiring a permit for restricted activities. Category 3: Species that are subject to exemptions. “Not Listed” (NL): Unlisted species: alien species that are not listed in the NEM:BA-A&IS Regulations but have been reported as present in natural or semi-natural ecosystems in South Africa or on offshore islands.
Figure 5. Numbers of alien species’ records (%; n = 380) in different NEM:BA-AIS Regulations’ categories for species (A) and their occurrence in different SANBI Gardens (B). Cat. = Category. Category 1a: Species that are targets for eradication. Category 1b: Species that are control targets and need a national management plan. Category 2: Species requiring a permit for restricted activities. Category 3: Species that are subject to exemptions. “Not Listed” (NL): Unlisted species: alien species that are not listed in the NEM:BA-A&IS Regulations but have been reported as present in natural or semi-natural ecosystems in South Africa or on offshore islands.
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Table 1. SANBI botanical and zoological gardens’ features: area, the first date of current land use/proclaimed, biomes and preserved vegetation types.
Table 1. SANBI botanical and zoological gardens’ features: area, the first date of current land use/proclaimed, biomes and preserved vegetation types.
National Botanical/Zoological GardenArea (ha)First Date of Current Land Use/ProclaimedSA Province (Town)Biome Represented (Bioregion) (Mucina & Rutherford, 2006)Vegetation Types Represented
(Mucina & Rutherford, 2006)
Free State NBG671967Free State Province (Bloemfontein)Grassland (Dry Highveld Grassland)
Azonal Vegetation (Alluvial Vegetation)
Gh 7 Winburg Grassy Shrubland
Gh 8 Bloemfontein Karroid Shrubland
Gh 5 Bloemfontein Dry Grassland
AZa 5 Highveld Alluvial Vegetation
Hantam NBG62302008Northern Cape (Nieuwoudtville)Succulent Karoo (Trans-Escarpment Succulent Karoo)
Fynbos (Shale Renosterveld, and Granite and Dolerite Renosterveld)
FRd 1 Nieuwoudtville-Roggeveld Dolerite Renosterveld
FRs 2 Nieuwoudtville Shale Renosterveld
SKt 2 Hantam Karoo
Harold Porter NBG2011959Western Cape (Betty’s Bay)Fynbos (Sand Fynbos, Western Strandveld and Sandstone Fynbos)
Forest (Zonal & Intrazonal)
FFd 6 Hangklip Sand Fynbos
FFs 11 Kogelberg Sandstone Fynbos
FOz 1 Southern Afrotemperate Forest
FS 7 Overberg Dune Strandveld
Freshwater (rivers)
Marine biodiversity
Karoo Desert NBG1541921Western Cape (Worcester)Succulent Karoo (Rainshadow Valley Karoo)
Fynbos (Shale Fynbos and Shale Renosterveld)
FFh 4 Breede Shale Fynbos
FRs 8 Breede Shale Renosterveld
SKv 7 Robertson Karoo
Kirstenbosch NBG1991913Western Cape (Cape Town)Fynbos (Granite Fynbos, Sandstone Fynbos, and Shale Fynbos)
Forest (Zonal and Intrazonal)
FFg 3 Peninsula Granite Fynbos
FFh 5 Cape Winelands Shale Fynbos
FFs 9 Peninsula Sandstone Fynbos
FOz 1 Southern Afrotemperate Forest
Freshwater (rivers)
KwaZulu-Natal NBG481874/1969KwaZulu-Natal (Pietermaritzburg)Savanna (Sub-Escarpment Savanna)SVs 4 Ngongoni Veld
Freshwater (river)
Kwelera NBG1702014Eastern Cape (East London)Forest (Zonal and Intrazonal)
Azonal Vegetation (Eastern Strandveld)
Albany Thicket
AT 9 Albany Coastal Belt
FOz 6 Southern Coastal Forest
AZs 2 Albany Dune Strandveld
AT 12Buffels Thicket
Marine biodiversity
Lowveld NBG1641969Mpumalanga (Nelspruit)Savanna (Lowveld)SVl 9 Legogote Sour Bushveld
SVl 10 Pretoriuskop Sour Bushveld
Freshwater (river)
Pretoria NBG701958Gauteng (Pretoria)Savanna (Central Bushveld)SVcb 6 Marikana Thornveld
Thohoyandou NBG891986Limpopo (Thohoyandou)Savanna (Central Bushveld)SVcb21 Soutpansberg Mountain
Bushveld
Pretoria NZG 801899Gauteng (Pretoria)Savanna (Central Bushveld)SVcb 6 Marikana Thornveld
Mokopane Biodiversity Conservation Centre13981979Limpopo (Mokopane)Savanna (Central Bushveld)SVcd 20 Makhado Sweet Bushveld
SVcb 23 Polokwane Plateau Bushveld
Walter Sisulu NBG2761982Gauteng (Roodepoort/Mogale City)Savanna (Central Bushveld)
Grassland (Mesic Highveld Grassland)
SVcb 9 Gold Reef Mountain Bushveld
Gm 10 Egoli Granite Grassland
Freshwater (river)
Table 2. Different categories of alien and invasive species following the NEM:BA-A&IS Regulations, 2021.
Table 2. Different categories of alien and invasive species following the NEM:BA-A&IS Regulations, 2021.
CategoryNEM:BA-A&IS Description
Category 1(a)Species that must be combatted and are targets for eradication
Category 1(b)Species that are control targets and need a national management plan
Category 2Species requiring a permit for restricted activities
Category 3Species that are subject to exemptions
“Not Listed”Unlisted species: Alien species that are not listed in the
NEM:BA-A&IS Regulations but have been reported as present
in natural or semi-natural ecosystems in South Africa or on offshore islands
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Mokotjomela, T.M.; Rahlao, S.J.; Vukeya, L.R.; Baltzinger, C.; Mangane, L.V.; Willis, C.K.; Mutshinyalo, T.M. The Diversity of Alien Plant Species in South Africa’s National Botanical and Zoological Gardens. Diversity 2023, 15, 407. https://doi.org/10.3390/d15030407

AMA Style

Mokotjomela TM, Rahlao SJ, Vukeya LR, Baltzinger C, Mangane LV, Willis CK, Mutshinyalo TM. The Diversity of Alien Plant Species in South Africa’s National Botanical and Zoological Gardens. Diversity. 2023; 15(3):407. https://doi.org/10.3390/d15030407

Chicago/Turabian Style

Mokotjomela, Thabiso M., Sebataolo J. Rahlao, Loyd R. Vukeya, Christophe Baltzinger, Lindokuhle V. Mangane, Christopher K. Willis, and Thompson M. Mutshinyalo. 2023. "The Diversity of Alien Plant Species in South Africa’s National Botanical and Zoological Gardens" Diversity 15, no. 3: 407. https://doi.org/10.3390/d15030407

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