Alien Plant Species Richness in Urban Protected Biodiversity Areas: A Case Study of Tshwane Metropolitan Municipality, South Africa

Abstract

Urban protected biodiversity areas conserve some of the world’s critically endangered and isolated biodiversity while providing essential ecosystem services. However, these urban habitats are threatened by the presence of alien and invasive plants. We studied alien plant species richness and identified the potential predictors in urban protected biodiversity areas in Tshwane Metropolitan Municipality, South Africa. Data on alien plant species were collected through surveys and consultations with protected area managers. We determined the relationship between the observed species richness and potential alien plant species predictors, such as area size, number of visitors, proximity to residential areas, and the year the reserve was proclaimed. We documented 574 records of 189 alien plant species from 60 families across 14 protected areas. Phanerophytes were the most common (46.5%), with many species native to South America, North America, and Africa. Most species have formed naturalised populations (67.7%), followed by invasive populations (20.6%) and casual populations (12%), posing future invasion threats. Most species (55.5%) were introduced as ornamental plants, with many of these species forming invasive populations. Half the recorded species were listed under the NEM:BA A&IS regulations, mostly categorized as 1b. Our findings indicate that the annual number of visitors strongly predicted alien plant species richness in urban protected areas. Additionally, a significant negative correlation was observed between species richness and the proximity to residential areas and years since the proclamation. Understanding the distribution patterns and predictors of species richness is crucial in monitoring invasive alien species and conserving biodiversity in urban environments.

1. Introduction

Globally, urban areas are home to critically endangered and isolated biodiverse flora, providing essential ecosystem services [1,2]. However, these environments face threats from anthropogenic factors such as agriculture, forestry, human settlement, and urbanization, leading to habitat transformation, fragmentation, and global change [3,4]. These changes result in the loss and isolation of rare and endangered native species which are essential for ecosystem services and are priorities for conservation [5]. Understanding the drivers or predictors of biological invasions across various taxa and regions is crucial for developing tailored management strategies to mitigate their impact [6]. This holistic understanding helps conservationists and policymakers in developing measures to safeguard native biodiversity for future generations and promote ecosystem services.

Conserving urban biodiversity has become a priority [7]. Protected areas (PAs) serve as crucial refuges for native species and play a pivotal role in biodiversity conservation and improving human well-being, even in urban settings [8]. Despite efforts to conserve native biodiversity within and outside PAs globally, biodiversity loss continues at an alarming rate [9]. Invasive alien species have been identified as drivers of environmental change, a leading cause of extinction and biodiversity loss [10,11,12,13], and their importance as drivers of change in PAs has been noted since the 1980s [14]. Alien species are defined as “taxa in a given area whose presence there is due to intentional or accidental introduction as a result of human activity”. In contrast, invasive species are “taxa with naturalized populations that produce reproductive offspring, often in very large numbers, at considerable distances from parent plants (approximate scales: >100 m; <50 years for taxa spreading by seeds and other propagules over 6 m within 3 years for taxa spreading by roots, rhizomes, stolon, or creeping stems), and thus have the potential to spread over a considerable area” [15]. The increasing number of studies on biological invasions in PAs highlights the need to understand various invasion dynamics beyond the extent of establishment extent [14,16,17,18].

While many studies on invasive alien plants in PAs exist, most focus on the establishment extent in large remote PAs [19], leaving other invasion dynamics underexplored. For example, 37% of studies on invasive alien plants’ impacts that have been conducted in PAs show a geographic bias towards the Americas and Pacific islands rather than Europe, Asia, and Africa [20]. Managers of PAs worldwide have raised concerns that much research focuses on the ecology of invasive plants rather than management issues [21]. In Africa, most studies focus on large, remote PAs such as oceans and national parks [18]. For instance, research predominantly targets Kruger National Park or other large national parks, with few studies on nature reserves, especially those centralized in urban areas [17,19,22,23]. In Europe, nature reserves located in urban areas are projected to face a high risk of invasive plant invasions in the future [24]. Monitoring biodiversity and identifying threats in urban conservation areas are necessary and could be achieved by developing inventories of alien plants within and around urban PAs, therefore aiding strategic management [25].

Surveillance, including rapid response, monitoring, and early detection, has proven effective in the early detection of alien species [26,27]. Such measures have successfully helped in detecting species escaping from gardens into natural urban areas in Tshwane, identifying species that require management intervention [28]; they have also aided in the detection of several emerging invaders in Limpopo province, such as Leucanthemum vulgare in Woodbush Granite grassland, a protected area and Ipomoea hederifolia in Vhembe Biosphere Reserve [29,30]. Proactive measures are crucial given invasive plant species’ potential ecological and economic consequences. Implementing early detection and rapid response can curb the spread and establishment of invasive species, reducing management costs and challenges, especially for resource-stretched South African municipalities [31,32,33]. As a signatory of the Convention on Biological Diversity (CBD), South Africa must meet international biodiversity targets, including Target 6 of the Kunming–Montreal Global Biodiversity Framework [13]. The National Environmental Management: Biodiversity Act (NEM:BA, Act 10 of 2004), Alien & Invasive Species regulation (NEM:BA A&IS), as amended, requires landowners such as municipalities to identify and control invasive species, aiding compliance with CBD targets [13].

The lack of reliable data often hinders our understanding of biological invasions in urban areas. This is often caused by a lack of systematic monitoring of alien species and tracking of biological invasions [6]. This issue can be addressed by integrating surveillance and systematic monitoring efforts, using standardised data from diverse sources, such as management plans, expert opinion, and traditional survey methods [34,35]. Utilizing multiple data sources enhances our understanding of alien species distribution dynamics, providing a comprehensive view of their richness in urban settings and the baseline data needed for developing management strategies [6].

Urban areas are hotspots for biological invasions, as alien plants are often introduced as ornamentals before escaping into the wild [36,37,38]. Tshwane, the capital city of South Africa, covers 6298 km² (629,800 hectares (ha)), has an estimated human population of 3 million [39] and hosts significant diversity of river and wetland ecosystems [40] and grassland–savanna biomes, including the critically endangered vegetation such as Rietvlei River Highveld Grassland and Bronberg Mountain Bushveld [41]. Additionally, the area includes vulnerable vegetation such as Marikana Thornveld and Critical Biodiversity Areas (CBA 1). Tshwane Metropolitan Municipality conserves over 30 isolated natural patches of significant conservation value. Among these, 15 are managed by Tshwane Municipality, covering 9847.59 ha, while the remaining patches, covering 12,493 ha, are private- and state-owned (Figure 1). Nelufule et al. [28] identified 94 alien plant species threatening natural biodiversity in natural areas within urban spaces in Tshwane. However, diversity, species distribution, pathways of introduction, invasion status, and factors influencing alien plant richness in protected areas are unknown. This information is crucial for developing management strategies for biological invasions [33] as it provides useful invasive alien species data for monitoring biological invasions at a national and global scale [34]. This, in turn, helps in achieving international biodiversity targets.

This study aimed to achieve the following goals: (1) collate and document the diversity and abundance of alien plant species within Tshwane Metropolitan Municipality PAs; (2) determine species by life forms and continent of origin; (3) classify their invasion statuses; (4) determine the reason of introduction (pathway of introduction) and the NEM:BA-A&IS regulations categories; (4) evaluate the potential factors driving the observed trends. This study presents the first inventory of alien and invasive plant species in Tshwane’s Metropolitan PAs and assesses invasion risks for urban biodiversity conservation. The focus is on PAs managed by the Tshwane municipality to provide a representative sample of urban biodiversity management practices and contribute data toward meeting biodiversity targets.

2. Materials and Methods

2.1. Methods

2.1.1. Compiling an Inventory of Alien Plant Species in Tshwane PA’s

To compile data on alien plant species within protected areas of Tshwane Metropolitan Municipality, we requested management plans from the managers of 14 selected areas (see Table 1). Tshwane Metropolitan Municipality oversees 12 nature reserves (NRs) and three nature areas (NAs). For this study, we focused on these 14 PAs accessible during the study period. Nature reserves are designated to conserve flora, wildlife, and natural habitats. In contrast, nature areas are preserved primarily for their natural features (e.g., ecosystems, landscapes) and provide ecosystem services such as aesthetics and outdoor activities for residents, though these are not officially classified as nature reserves. We extracted lists of alien plant species from each obtained management plan. In cases where management plans lacked inventories of alien plant species (e.g., Faerie Glen NR and Moreleta Kloof NR), we contacted nature conservators or PA managers via email to confirm the availability of omitted inventories in their archives, subsequently requesting such lists (e.g., Struben Dam Bird Sanctuary NA).

We observed that some protected areas listed fewer alien plant species (i.e., four or five species) in their management plans than expected. To augment these data, we conducted a rapid roadside survey following the methodology outlined by Baard and Kraaij [44]. This survey aimed to identify additional alien plant species not listed in the management plans and confirm each recorded species’ invasion status.

Due to restricted access, we could not conduct roadside surveys inside Moreleta Kloof Nature Reserve (NR), Faerie Glen NR, and Struben Dam Nature Area (NA). Instead, we conducted traditional surveys by walking through various trails and roads within these areas, documenting and identifying alien plant species. Species previously identified in the management plans were confirmed during field surveys and verified through consultations with experts for accurate identification.

2.1.2. Species Verification

We identified and verified specimens and species names using field guidebooks by Henderson [45] and Bromilow [46]. To verify whether a species was native to South Africa and Tshwane, different sources were used for plant identification, namely, van Wyk and van Wyk [47] and Pooley [48]. Photographs were also taken with geolocations during surveys for later identification. Species names were authenticated and assigned in accordance with the Plants of the World Online (POWO: http://www.plantsoftheworldonline.org/, accessed on 15 May 2024) and the Global Biodiversity Information Facility Backbone Taxonomy (GBIF: https://doi.org/10.15468/39omei, accessed on 15 May 2024). We additionally incorporated specimens that could not be identified at the species level because they lacked characteristic features such as fruits or flowers; identification was only possible at the genus level. These data are essential for precisely estimating the richness of alien species.

2.1.3. Species Classification

We quantified the abundance of alien plant species that occurred in Tshwane Metropolitan Municipality PAs by tallying the occurrences of each species within the protected area. This was performed by calculating the number of times a species was recorded in each protected area, using data sourced from the survey and management plan using an aggregate function in R (version 3.4.4i). We also calculated the number of species within each plant family. Additionally, we categorized species based on their life forms, continent of origin, invasion status, reason of introduction, and according to NEM:BA A&IS regulations. This information is crucial because it allows for the standardization of alien species data needed to make decisions on managing biological invasions at larger spatial scales [34].

2.1.4. Life Forms

Following the criteria outlined by Midolo et al. [49], each plant species underwent classification based on six Raunkiær’s life forms, including chamaephytes, geophytes, hemicryptophytes, hydrophytes, phanerophytes, and therophytes, [50]. This information was included because it may provide valuable information for predicting potential impacts [51].

2.1.5. Continent of Origin

Understanding and addressing the pathways of alien species introduction requires determining the native range for each species, which is crucial in constructing effective management strategies [52]. During invasion risk assessment, species native range plays an important role during climate matching in the recipient environment [53]. Although we identified the exact country of native range, we classified different species according to seven biogeographically regions of the Taxonomic Databases Working Group [54], namely: Africa, Australasia, Europe, North America (including Mexico), South America (including Central America), and Temperate and Tropical Asia. When a species has multiple native ranges spanning more than one continent, all regions are considered native, assuming that the species were introduced to South Africa directly from their native continent of origin [55].

2.1.6. Reason for Introduction

Each species underwent classification based on its likelihood of introduction, serving as a proxy for the introduction pathway, as outlined by Baard et al. [22]. The classifications were as follows: agriculture; edible plant; forestry (including for stabilizing sand); grazing; horticulture; medicinal use; weed (where other modes do not fit).

2.1.7. NEM:BA A&IS Status

We classified each species according to the South African invasive species legislation (NEM:BA A&IS Regulations of 2021 as amended), assigning them to either Category 1a, 1b, 2, or 3 invasive species for Gauteng province, selecting the highest applicable category. While the NEM:BA A&IS Regulations were promulgated in 2014, we utilized the updated A&IS list of September 2021 for the current study [56].

2.1.8. Invasion Status

For each recorded species, we used the number of times a species was recorded and the size of the populations to classify species as casual alien, naturalised, or invasive following a standardised classification [15,57]. If different invasion stages were attained in various PAs, then the highest level was assigned [15,57]. South African species that did not historically occur in Gauteng province and were recorded in one of these protected areas were classified as native–alien populations following a protocol developed by Nelufule et al. [58]. We described the invasion status as follows: (1) casual alien species—plants that can thrive temporarily and sometimes reproduce but do not establish self-sustaining populations and may require repeated introductions to persist; (2) naturalized species—plants that form self-sustaining populations without direct human assistance recruiting offspring’s closer to adult plants; (3) invasive species—belongs to a subgroup of naturalized species capable of producing numerous offspring at significant distances from their parents or the original introduction site, with the potential to spread extensively over long distances [15].

2.2. Potential Predictors of Alien Plants Richness in Tshwane Metropolitan Municipality PA’s

We used the species abundance as quantified above to assess the potential predictors influencing alien plant richness in Tshwane PAs. We selected four potential predictors: the size of the protected areas, the number of years since their proclamation, visitor numbers, and proximity to residential areas. These predictors were chosen due to available data and their previous use in studies on biological invasions, which are particularly relevant as these protected areas are located in densely populated urban areas [17]. Information regarding the size of the protected area and the year of the management plan’s development was extracted from the management plan. In contrast, managers and the city of Tshwane website gathered details such as the annual number of visitors to each area and the proximity of each protected area to residential zones (https://www.tshwane.gov.za/, accessed 20 May 2024). The collected data were then used to analyse the correlation between the species count within each protected area and various potential predictors.

2.3. Statistical Analysis

We used the aggregate function to count the number of species classified under different categories of life forms, invasion status, continent of origin, NEM:BA categories, and reason for introduction. A chi-square test (χ²) was used to compare the number of species in different categories of life forms, reason of introduction, continent of origin, and invasion status. All statistical analyses were conducted using R software version 3.4.4i [59]. Generalized linear models with a Poisson error distribution and log link function were employed to investigate the relationships between (a) the number of alien plant species and the size of the protected area; (b) the number of alien plant species and the proximity to residential areas; (c) the number of alien plant species and the year of proclamation for a protected area; (d) the number of alien plant species and annual number of visitors per protected area. Count data of a number of alien plant species in each Tshwane Metropolitan Municipality PA were used as response variables. In contrast, the size of the protected area, proximity to residential areas, the year of proclamation, and the annual number of visitors per protected area were used as explanatory variables.

3. Results

3.1. Alien Plant Species Richness and Abundance

We found a total of 574 alien plant species records containing 189 alien plant species from 60 different families distributed across 14 Tshwane protected areas (Figure 2). The number of alien plant species recorded during the survey was significantly higher than those obtained from management plans (χ² = 62.848, df = 1, p = 2.232 × 10⁻¹⁵).

3.2. Distribution

Struben Dam Bird Sanctuary NR had the highest number of alien plant species (n = 64), followed by Moreleta Kloof NA with 60, and Groenkoof NR with 57 species (Figure 2). In contrast, Rooihuskraal Bird Sanctuary NA had the fewest recorded alien plants, with only 17 alien plant species. Statistical analyses revealed no significant differences in alien plant species between Struben Dam Sanctuary NR and Moreleta Kloof (χ² = 0.043356, df = 1, p = 0.8351), Faerie Glen NR (χ² = 1.0876, df = 1, p = 0.297), Colbyn Wetland NR (χ² = 1.2801, df = 1, p = 0.2579), Groenkloof NR (χ² = 1.72, df = 1, p = 0.1897), Toloane NR (χ² = 2.5265, df = 1, p = 0.112), and Rietvlei NR (χ² = 3.1696, df = 1, p = 0.07502). However, there was a significant difference between Struben Dam NR and Bishop Bird NR (χ² = 5.1903, df = 1, p = 0.02271), as well as other protected areas (p < 0.05). The most-recorded alien plant species were Salvia tilifolia, occurring in 14 protected areas, Zinnia peruviana (n = 13), Ipomoea purpurea, and Lantana camara (n = 12) (Appendix A).

3.3. Families

The most dominant plant families were the following: Fabaceae, with 24 species; Asteraceae, with 20 species; Solanaceae, with 15 species; and Rosaceae, with 11 species (Appendix A). However, there was no statistical difference between the number of Fabaceae and Asteraceae (χ² = 0.16929, df = 1, p = 0.6807) or Solanaceae (χ² = 1.4501, df = 1, p = 0.2285). In contrast, statistically significant differences were observed between Fabaceae and Rosaceae (χ² = 3.7114, df = 1, p = 0.05404), Amaranthaceae (χ² = 6.4193, df = 1, p = 0.01129), and other families (p < 0.05). Among the recorded alien plants, 10 species are native to South Africa but have formed established native–alien populations in Gauteng province (Appendix A).

3.4. Life Forms and Origin

The most-presented life forms were phanerophytes (n = 88; 46.5%), therophytes (28.5%), and hemicryptophytes (17.4%). Significant differences were found between the number of phanerophytes and therophytes (χ² = 5.472, df = 1, p = 0.01932), hemicryptophytes (χ² = 18.761, df = 1, p = 1.482 × 10⁻⁵), and other life forms (p < 0.001). In addition, chamerophytes and geophytes were the least presented life forms in Tshwane protected areas (Figure 3a).

The largest numbers of alien plant species originated from South America (n = 79, 27.3%), North America (n = 62, 21.4%), Asia (19.3%; temperate, n = 38; tropical, n = 18 species) and Africa (14.5%) with majority of these species being phanerophytes (i.e., woody and shrubs) and therophytes (annual and perennial herbs) (Figure 3b). However, the number of species introduced from South America was not significantly different from those introduced from North America (χ² = 1.2628, df = 1, p = 0.2611), but it differed significantly from the number of species introduced from Africa and Temperate Asia (χ² = 8.014, df = 1, p = 0.004642) and from the rest of the continents combined (p < 0.001) (Figure 3b).

3.5. Invasion Status

A significantly large proportion of alien plant species (n = 128; 67.7%) have established naturalised populations upon introduction to Tshwane protected areas, in comparison to those forming invasive populations (n = 39; χ² = 32.712, df = 1, p = 1.069 × 10⁻⁸) and casual populations (n = 23; χ² = 52.874, df = 1, p = 3.557 × 10⁻¹³); also, we note that invasive populations fall within the naturalised populations category (Appendix A). However, species forming casual populations were not significantly different from those forming invasive populations (χ² = 2.7064, df = 1, p = 0.09995).

3.6. Invasion Status and Reason of Introduction

Most of the naturalised alien plant species recorded in this study (n = 105; 55.5%) were introduced for horticulture (Figure 4). In addition, most species that have formed invasive populations were also introduced for horticulture (Figure 4). A significantly higher number of alien plant species were introduced for horticulture compared to those introduced for medicinal purposes (χ² = 25.007, df = 1, p = 5.712 × 10⁻⁷), for food (χ² = 48.044, df = 1, p = 4.168 × 10⁻¹²) and for other uses (p < 0.001) (Figure 4). A few species were introduced for forestry, including Eucalyptus species (Figure 4).

3.7. NEM:BA A&IS Categories and Invasion Status

Most of the naturalised alien plant species (n = 103; 54.4%) recorded in Tshwane Metropolitan Municipality PA’s areas were not listed in the NEM:BA A&IS Regulations list (Figure 5). Only 45% of the species were listed—32.7% as Category 1b, 6.9% as Category 3, and 4.3% as Category 2 invaders (Figure 5). Statistical analyses revealed significant differences between alien plants not listed in NEM:BA&IS categories and Category 1b species (χ² = 7.3344, df = 1, p = 0.006765), as well as species listed under other categories (p < 0.001). Significant differences were also observed between Category 1b species and Category 3 species (χ² = 25.039, df = 1, p = 5.618 × 10⁻⁷), Category 2 species (χ² = 33.376, df = 1, p = 7.595 × 10⁻⁹), and Category 1a species (χ² = 43.914, df = 1, p = 3.432 × 10⁻¹¹). However, no statistical difference was found between Category 2 and Category 3 species (χ² = 0.702, df = 1, p = 0.4021). Invasive alien plants were shared across all NEM:BA categories but species listed as Category 1b had the highest number of species that had formed invasive populations (Figure 5). Only two species, Iris pseudacorus and Harrisia pomanensis, were listed in Category 1a with I. pseudacorus forming invasive population in Moreleta Kloof and naturalised population in Struben Dam Bird Sanctuary NA. In contrast, the established populations of H. pomanensis was recorded in Wonderboom NR.

3.8. Predictors of the Alien Plants Species Richness

We found no significant relationship between the size of the protected area and alien plant species richness (R = 68.943, df = 12, p = 0.983; Figure 6a). However, the number of alien plant species in Tshwane Metropolitan Municipality protected areas significantly increased with more visitors (R = 64.82, df = 12, p = 0.0376; Figure 6b). In contrast, we observed statistically significant negative correlations between alien plant richness and proximity to residential areas (p < 0.001) and the year of proclamation for protected areas (p < 0.00949) (Figure 6c,d).

4. Discussion

Our study identified 189 alien plant species from 60 families, providing the first comprehensive inventory of alien plants in protected areas managed by Tshwane Metropolitan Municipality in Gauteng province, South Africa. These data were collected through ecological management plans and confirmed through surveys. Our study is crucial because it provides important data that help with the detection of new incursions, reducing invasive species impacts and contributes valuable regional [23,33,60] and global [61,62] data for monitoring biological invasions at different spatial scales [34].

Our analysis indicates an increase in alien plant species within protected areas in South Africa, reflecting a global trend that threatens the conservation of biological diversity in Tshwane’s protected areas, whether managed by the state or privately [14,63,64,65,66]. This study aligns with research by Jarošík et al. [24], who documented 155 alien plant species, including 46 invasive species, across 48 nature reserves in Prague, Czech Republic. Similarly, Spear et al. [17] reported 291 alien plant species, including 101 invasive species, in urban protected areas in Cape Town, South Africa. In contrast, 136 alien plants were recorded in the Woodbush Granite Grassland (WGG) in Limpopo province, South Africa [29]. Our study contributes valuable insights into the distribution and invasion patterns in protected areas [67], essential for improving control measures and mitigating the spread of invasive alien plants. This addresses a research gap by focusing on urban protected areas [19,68,69].

4.1. Species Richness and Abundance Across Protected Areas

Species richness and abundance varied significantly across the 14 studied protected areas. Struben Dam Bird Sanctuary NR exhibited the highest number of alien species, followed by Groenkloof and Faerie Glen NR (see Figure 2). The high number of species in these reserves can be attributed to their popularity among visitors and their proximity to residential areas, which likely facilitated the accidental introduction of horticultural plants into these protected areas (see Table 1; Supplementary Figure S1).

Salvia tilifolia was the most widely distributed alien plant recorded in all protected areas and has been noted for its competitive impact on native plant communities. Of particular concern are the widespread invasive populations of species such as Lantana camara, listed among the 100 worst alien invasive species worldwide [70], as well as Robinia pseudoacacia and Ailanthus altissima, recognized as significant invaders in European protected areas [17]. These findings highlight significant invasion threats to vulnerable vegetation communities like the Marikana Thornveld [2] and critically endangered vegetation such as Magaliesberg Pretoria Mountain Bushveld (see Table 1). These observations are worrying given that protected areas within Tshwane Metropolitan Municipality conserve only a small portion of the region’s biodiversity of conservation importance [Figure 1].

4.2. Native–Alien Populations

Of particular concern is the presence of 24% of species originating from Africa, with native ranges in South Africa, forming native–alien populations in Gauteng province. This indicates an increasing trend of human-mediated introductions of native species beyond their historic native ranges within the country [38]. This trend is alarming, especially considering that 20 native–alien plant populations, including invasive forms of Tecoma capensis, have already been documented as native–alien populations in South Africa, some within urban national parks [17,22,71]. These species are known to cause negative impacts such as biotic homogenization, posing threats to native biodiversity in protected areas if left unmanaged [72]. Introducing these species for various purposes further complicates their management in Tshwane’s protected areas (see Appendix A).

4.3. Families

Fabaceae emerged as the most prominent among the identified plant families, comprising 24 distinct species, followed by Asteraceae with 10%. This observation aligns with previous studies indicating that these families contribute significantly to the presence of alien plants in natural areas within Tshwane Metropolitan Municipality [28]. The widespread distribution of Fabaceae species in Tshwane’s PAs is concerning, as many species in this family are woody and known to have a negative impact on biodiversity elsewhere, including their ability to persist under harsh conditions as seeds [73].

Other inventories of alien plant species have noted the dominance of Fabaceae and Asteraceae, such as those conducted in Kruger National Park, South Africa [18], and Mizoram, India [74]. Similar trends are also reported globally [75,76,77,78] and in studies of alien plant species in protected areas [19,79,80]. This prominence can be attributed to these families being among the most species-rich worldwide, indicating the importance of prioritizing management efforts for species within these families to control invasive spread.

4.4. Invasion Status, Life Forms, and Native Range

Most recorded alien plant species in Tshwane’s PAs (n = 167) have formed naturalised populations, with invasive species included (see Figure 3a). Regarding life forms, phanerophytes and therophytes are most represented across different PAs, with many of these species having formed naturalised populations originating from South America and North America (see Figure 3b). Notably, most species that have formed invasive populations are therophytes (7.9%) and phanerophytes (7.4%). This highlights that invasive species in Tshwane’s PAs are causing negative impacts on native biodiversity and ecosystem functioning, consistent with global trends where trees and shrubs are identified as the most problematic invasive plants in protected areas worldwide, followed by annual herbs [19,24,81,82].

The prevalence of therophytes can be attributed to their ability to establish populations quickly during favourable conditions [28], their rapid seed production, the endurance of harsh conditions, and their short life span [83], coupled with suitable climatic conditions. These species potentially threaten native plant species by outcompeting them under harsh conditions. For example, Dumalisile and Somers [84] found a higher diversity and abundance of large mammals in uninvaded sites compared to sites invaded by Chromolaena odorata in Hluhluwe-iMfolozi Park, indicating the alteration of natural vegetation by invasive species. Additionally, therophytes have been reported to intensify fire intensity, leading to the death of native trees in the savannas of eastern South Africa [85].

Our findings are consistent with studies by Foxcroft et al. [18], which reported an overrepresentation of approximately 60 alien herbaceous plant species in Kruger National Park, with 46% naturalized and 13% invasive populations. Foxcroft et al. [19] also noted that trees comprised the highest proportion (32%) of alien plant species in 135 protected areas globally, followed by shrubs. Alien tree species can also disrupt fire regimes in protected areas, altering plant community structures and ecosystem dynamics [85,86]. The widespread distribution of naturalized alien phanerophytes, including invasive populations, threatens biodiversity and ecosystem services in PAs such as Colbyn Wetland NR and Rietvlei NR, which are vital for conserving peatlands in South Africa [40]. Additionally, these threats also endanger vegetation types such as Marikana Thornveld and Rand Highveld Grassland, of which only a small proportion is conserved in the Tshwane Metropolitan Area, as well as the vulnerable Carletonville Dolomite Grassland (Figure 1). Invasive plants have similarly impacted large wetlands globally, including those in the Lower Mekong Basin, the Greater Everglades, and Kafue Flats [87].

4.5. Native Range

Tshwane Metropolitan Municipality hosts alien plant species originating from all continents [28]. However, the majority identified in Tshwane’s protected areas are native to South America, North America, and Temperate Asia. Similar trends have been observed in Kruger National Park [18] and across 13 South African National Botanical Gardens [35], where many species also originate from South America. The overrepresentation of plants from the Americas is largely attributed to their widespread use as ornamentals (see Figure 4), introduced via online trade from North America [88], often escaping detection until reaching South Africa.

The presence of numerous species from Asia, both temperate and tropical, is linked to their adaptability to various environmental and habitat conditions [89]. For instance, invasive alien species such as Ailanthus altissima, Fallopia japonica, and Impatiens glandulifera, known to impact biodiversity in Romanian protected areas negatively, originated from Asia [90]. Our study aligns with previous and current studies, indicating that many alien plants in protected areas worldwide originate from South America, Asia, and North America [22,35]. Thus, assessing the potential risks associated with species introduced from these regions before their use in horticulture is critical.

4.6. Reason of Introduction

Data on the pathways of introduction are crucial for managing pathways and developing biosecurity strategies. Most naturalized alien plant species introduced to Tshwane PAs entered through various pathways, with a significant proportion (55.5%) introduced via the horticulture trade as ornamental plants (see Figure 4). Alarmingly, species introduced for ornamental purposes also constitute the largest group forming invasive populations in Tshwane PAs (see Figure 4). This trend corresponds with findings from other protected areas, such as Kruger National Park, where many invasive alien plants were initially introduced for ornamental use before escaping into natural habitats and becoming invasive [91]. Ornamental alien plants have been implicated in negative impacts within 19 South African National Parks, where they compete with native species and alter habitat structures [92], posing future invasion threats to urban protected areas.

Our study revealed that some of the naturalized alien plants recorded in Tshwane PAs have medicinal uses, while others were introduced as food sources (see Figure 4). Some species may have been introduced accidentally, carried as seeds by wind or dispersed by birds [93]. Additionally, rivers passing through these protected areas likely introduced alien plants from nearby residential areas (see Supplementary Figure S2; Table 1). For instance, a significant number of alien plants were recorded along the river in Toloane NR. Only 8.9% of species were introduced accidentally in Tshwane protected areas, including globally recognized invasive weeds such as Tagetes minuta, Xanthium strumarium, and Datura ferox. Although these species were not highly numerous, they require monitoring due to their established invasive populations in protected areas, negatively impacting local ecosystems and human well-being [94]. There is an urgent need to engage urban residents living near protected areas about the threats posed by ornamental plants. This awareness can help reduce the number of species escaping from gardens into protected areas.

4.7. NEM:BA A&IS Regulations

Forty-four per cent of the recorded species were listed under various categories of the NEM:BA A&IS regulations, with the majority (32%) classified under Category 1b. This classification mandates their control within protected areas under the South African National Biodiversity Act. Only two species, Iris pseudocorus and Harrisia pomanensis, were classified as Category 1a invaders, highlighting the urgent need for their removal as per the legislation. The presence of species categorized as 1a and 1b within these protected areas carries significant ecological and conservation implications, including competition with native species for resources (see Figure 7), alteration of ecosystem dynamics, and disruption of ecological processes.

Therefore, urgent control measures are necessary, particularly since most species classified under Category 1b have established invasive populations (see Figure 5). Managing these invasions will mitigate the negative impacts on native plants and ecosystem function (see Figure 7), thereby preserving biodiversity and ensuring ecosystem integrity. Additionally, 55% of the recorded species were not listed in the NEM:BA A&IS regulations, despite some forming invasive populations (see Figure 5), suggesting a need for close monitoring. Furthermore, most species listed under Category 3 have also formed invasive populations, indicating their widespread distribution in urban settings and reflecting non-compliance with permit requirements governing the use of such species in South Africa [21].

4.8. Potential Predictors

Understanding factors influencing alien species richness is a crucial first step towards preventing their naturalization. Our findings indicate that the annual number of visitors was the strongest predictor of alien plant richness in Tshwane Metropolitan Municipality’s protected areas compared to other predictors used in this study (Figure 6; Table 1).

We observed a significant positive relationship between alien species richness and the number of visitors. As visitor numbers increase, so does the number of alien plant species in protected areas [95]. Furthermore, alien plant species richness significantly decreased in protected areas located far away from residential areas, indicating that many naturalized ornamental plants, as depicted in Figure 4, were introduced from nearby residential gardens (i.e., as escapes) and formed naturalized populations in Tshwane’s protected areas [38]. Our study also revealed that alien plant species richness significantly decreases in newly proclaimed nature reserves compared to older protected areas, suggesting that alien plant species have accumulated over time in older reserves due to historical gaps in invasive species management, potentially influenced by the historical lack of motivation for urban biodiversity conservation and legacies of colonization involving deliberate or accidental alien plants introductions, lack of adequate resources to manage invasive species, and establishments of alien species across metropolitan areas [96,97,98].

The weak correlation between species richness and the size of protected areas in Tshwane is attributed to the widespread dispersal of alien plants across all these areas (Figure 2). Our findings align with Lonsdale’s study [99], which highlighted tourism as a strong predictor of alien species numbers in protected areas globally, contrasting with McKinney’s findings [100], where visitation rates did not influence species richness. In South Africa, the density of the human population surrounding parks emerged as the strongest predictor of alien and invasive plant and animal species in 19 protected areas. This finding explains Tshwane’s lack of correlation between size and species richness. Other predictors, such as road numbers, years since park proclamation, park area, and river numbers, were found to be less influential [17].

Using multiple predictor variables is crucial for understanding the comprehensive drivers of biological invasions. Future research should consider additional potential predictors not covered in this study to better understand factors contributing to alien plant invasions in urban protected areas worldwide, as these areas face increasing threats from biological invasions.

5. Recommendations

The present study did not assess the NR and varying levels of visitor access and different types of visitor activities to determine the most effective management practices to prevent IAS introduction; hence, we recommend that future studies consider this aspect. It is recommended that future studies should assess the effectiveness of current regulations and practices related to the introduction and management of ornamental plants, particularly those listed under the NEM:BA. The research could focus on evaluating compliance levels, enforcement challenges, and the potential need for stricter regulations or alternative landscaping practices. Furthermore, the studies should also examine how different urban development patterns, such as residential density, proximity to protected areas, and green space connectivity, influence the spread and establishment of alien plant species.

6. Conclusions

Our study revealed that alien and invasive plant species threaten native biodiversity in Tshwane urban protected areas. Many naturalized phanerophytes and therophytes from the Asteraceae and Fabaceae families, predominantly from South America, North America, and Africa, were notably prevalent. More than half of these alien plants were initially introduced as ornamental species, subsequently escaping from nearby residential areas into the protected areas. Approximately 20.6% of these species have formed invasive populations, posing substantial threats to native biodiversity and ecosystem services within these protected areas. Many species that have formed naturalized populations are categorized as 1b under NEM:BA A&IS regulations, and some comprise a significant proportion of invasive populations requiring urgent management intervention. The species richness across various urban protected areas is influenced by multiple factors associated with human activities, with visitors strongly predicting their richness. This study provided important information for monitoring biological invasions and influencing decision-making regarding the allocation of management efforts. These efforts are essential for safeguarding the integrity of protected areas and mitigating threats from invasive species crucial for effective biodiversity conservation.

Author Contributions

Conceptualization, T.N.; Methodology, T.N.; Formal Analysis, T.N.; Investigation, T.N. and T.C.T.; Data Curation, T.N.; Writing—Original Draft Preparation, T.N.; Review and Editing, T.N., T.C.S., M.C.M., N.S., N.S.-P., T.C.T. and T.C.N.; Visualization, T.N. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are available on request.

Acknowledgments

We thank Khanyisile Malete and Nomcebo Magagula for assistance with data collection and surveys. Adelene Marais is enormously thanked for contributing alien plants data. Milingoni Ratshikhopha and Kemmone Mofela are thanked for their assistance with the maps. We are most grateful to all four anonymous reviewers who provided constructive comments that helped improve our manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Figures and Table

Figure 1. A map showing (a) South Africa, highlighting the study area within (b) Gauteng province and (c) Tshwane Metropolitan Municipality with different vegetation types classified according to Mucina and Rutherford [42] and Acocks [43]. Protected areas are distinguished by blue and white, with the 14 sampled protected areas (PAs) indicated by blue circles. TL = Toloane NR; MG = Magaliesberg NR; WB = Wonderboom NR; CW = Colbyn Wetland NR; VT = Vootrekker Monument NR; AR = Austin Roberts Bird NR; KK = Fort Klapperkop NR; GK = Groenkloof NR; SD = Struben Dam Bird Sanctuary NA; FG = Faerie Glen NR; MK = Moreleta Kloof NR; BB = Bishop Bird NR; NA; RH = Bird Sanctuary NA and RV = Rietvlei NR; NR = nature reserve; NA = nature area.

Figure 2. Number of alien plant species per protected area managed by Tshwane Metropolitan Municipality, categorized by data sources: management plans (grey) and surveys (white). NR = nature reserve; NA = nature area.

Figure 3. Stacked plot showing (a) the number of alien plant species recorded in Tshwane Metropolitan Municipality protected areas by life forms and invasion status, and (b) continent of origin by life forms. N_America = North America; S_America = South America; Asia.tropics. = Tropical Asia; Asia.temperate. = Temperate Asia as per Brummit (2001).

Figure 4. A bar graph showing the number of recorded alien plant species in Tshwane Metropolitan protected areas by reason of introduction and invasion status.

Figure 5. A bar graph showing the number of recorded alien plant species recorded in Tshwane Metropolitan protected areas by NEM:BA categories and invasion status.

Figure 6. Relationships between the number of alien plant species richness with (a) size of the protected area, (b) annual number of visitors, (c) proximity to residential areas, and (d) date of proclamation predictors.

Figure 7. (a) Invasive population of Agave sisalana in Voortrekker Monument NR, (b) invasive population of Acacia mearnsii in Fort Klapperkop NR, and (c) invasive population of Solanum pseudocapsicum in Moreleta Kloof NR (© Takalani Nelufule, Khanyisile Malete, Tshifhiwa Thenga).

Table 1

Protected areas in the Tshwane Metropolitan Municipality are organized by size, proclamation date, vegetation types conserved, annual visitor numbers, proximity to residential areas, and recorded number of alien plant species in each protected area. NR = nature reserve; NA = nature area. Vegetation types are classified according to Mucina and Rutherford [42] and Acocks [43].

Protected Areas	Area Size (ha)	Date of Proclamation	Vegetation Types Conserved	Number of Visitors	Proximity to Residential Area (Meters)
Austin Roberts Bird NR	11.76 ha	1956	Marikana Thornveld	150	10 m
Bishop Bird NR	16 ha	1992	Egoli Granite Grassland and Bakenveld	6960	0–15 m
Faerie Glen NR	124 ha	1984	Gold Reef Mountain Bushveld and Marikana Thornveld	30,150	0 m
Moreleta Kloof NR	100 ha	1877	Gauteng Shale Mountain Bushveld and Marikana Thornveld	42,740	0–10 m
Rooihuiskraal Bird Sanctuary NA	17.5 ha	2000	Carletonville Dolomite Grassland	19,940	12 m
Magaliesberg NR	~300,000 ha	1977	Gold Reef Mountain Bushveld and Marikana Thornveld	500	0 m
Colbyn Wetland NR	66 ha	2014	Mosaic Highveld Grassland and Marikana Thornveld	100	0–15 m
Rietvlei NR	3870 ha	1929	Rand Highveld Grassland	85,715	20 m
Groenkloof NR	668.2 ha	1990	Gauteng Shale Mountain Bushveld	28,000	0 m
Fort Klapperkop NR	239.5 ha	2000	Gauteng Shale Mountain Bushveld and Mesic Highveld Grassland	350	0 m
Voortrekker Monument NR	237.3 ha	1992	Gauteng Shale Mountain Bushveld and Mesic Highveld Grassland	8000	20 m
Struben dam Bird Sanctuary NA	11 ha	1984	Marikana Thornveld and Andesite Mountain Bushveld	9808	0 m
Toloane NR	201 ha	2011	Marikana Thornveld	0	7 m
Wonderboom NR	126 ha	1988	Gold Reef Mountain and Marikana Thornveld	12,859	15 m

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16080461/s1, Figure S1: Alien plant species in Tshwane protected areas classified according to the reason of introduction. Figure S2: Ornamental alien plants (a) Hypoestes aristate and (b) Callistemon viminalis identified along the water canal flowing into Faerie Glen NR from the nearby suburb.

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