A data-set containing all promulgated legislation relevant to biological invasions in South Africa, compiled as part of this project, is available on https://zenodo.org/ record/3660175#.Xj-zbTEzaUk

# References

Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

# Chapter 19 More than a Century of Biological Control Against Invasive Alien Plants in South Africa: A Synoptic View of What Has Been Accomplished

Martin P. Hill , Vincent C. Moran , John H. Hoffmann , Stefan Neser , Helmuth G. Zimmermann , David O. Simelane , Hildegard Klein , Costas Zachariades , Alan R. Wood , Marcus J. Byrne , Iain D. Paterson , Grant D. Martin , and Julie A. Coetzee

Abstract Invasive alien plant species negatively affect agricultural production, degrade conservation areas, reduce water supplies, and increase the intensity of wild fires. Since 1913, biological control agents i.e. plant-feeding insects, mites, and fungal pathogens, have been deployed in South Africa to supplement other management practices (herbicides and mechanical controls) used against these invasive plant species. We do not describe the biological control agent species

M. P. Hill (\*) · I. D. Paterson · G. D. Martin

Centre for Biological Control, Department of Zoology and Entomology, Rhodes University, Makhanda, South Africa e-mail<EMAIL_ADDRESS>
V. C. Moran · J. H. Hoffmann Department of Biological Sciences, University of Cape Town, Cape Town, South Africa

S. Neser · H. G. Zimmermann · D. O. Simelane · H. Klein Agricultural Research Council-Plant Health and Protection, Pretoria, South Africa

C. Zachariades Agricultural Research Council-Plant Health and Protection, Cedara, South Africa

A. R. Wood Agricultural Research Council-Plant Health and Protection, Stellenbosch, South Africa

M. J. Byrne Centre for Invasion Biology, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa

Centre for Biological Control, Rhodes University, Makhanda, South Africa

J. A. Coetzee Centre for Biological Control, Department of Botany, Rhodes University, Makhanda, South Africa

© The Author(s) 2020 B. W. van Wilgen et al. (eds.), Biological Invasions in South Africa, Invading Nature - Springer Series in Invasion Ecology 14, https://doi.org/10.1007/978-3-030-32394-3\_19

that have been used, or what they do, or how they damage the target plant species. We focus instead on evaluations (informed opinions, evidence and quantifications) of what has been achieved in South Africa by using biological control to suppress populations and impacts of invasive plant species. Satisfactory long-term evaluations of outcomes are difficult and expensive, but many have been done, providing ample evidence that biological control is often highly successful. We use case studies from South Africa to support this assertion and to make the point that successes may be largely forgotten in a relatively short time. Biological control of invasive plants in South Africa is demonstrably cost effective and has become generally accepted as a preferred management strategy. However, it is not a panacea, and we discuss several issues which complicate our understanding of its effectiveness and which raise research and implementation challenges. Further studies are needed on the economic and social benefits of biological control of invasive plants to inform and involve the wider South African community.

## 19.1 Introduction

Biological control of invasive alien plants relies on suitably host-specific natural enemies (agents), mainly plant-feeding insects and mites, and fungal pathogens. The agent species are sourced from their respective countries of origin and released into the invaded range to suppress the aggressiveness of the targeted plant species. The rapid and spectacularly successful outcome of biological control against cactus species, particularly in Australia in the 1930s (Dodd 1940; Mann 1970), set an early precedent suggesting, deceptively, that biological control and the evaluation of its success is easy. This also led, ironically, to the misguided perception that other biological control projects targeting invasive plant species that had less-dramatic outcomes were relative failures. Over the years, unequivocal successes have made up a diminishing proportion of the escalating number of projects that have been initiated, and an increasing number of projects have resulted in significant levels of control, but which have been less obvious and harder to gauge (Raghu and Walton 2007).

Biological control, as a management tool, and as a supplement to physical destruction or removal of the problem plants, and to herbicidal applications, has been used in South Africa since 1913 and has accumulated an impressive number of documented successes (Moran et al. 2005, 2013; Klein 2011; Zachariades et al. 2017). Initially (from 1913 to the 1930s) invasive plants in agriculture, particularly invasive cacti, were the targets of biological control introductions (Zimmermann et al. 2009). Between the 1950s and 1980s, biological control projects were initiated on several species of plants that were invasive in the Cape Floristic Region, a 'biodiversity hotspot', including Hypericum perforatum (Clusiaceae; St. John's Wort; Gordon et al. 1986; Gordon and Kluge 1991), Hakea sericea (Proteaceae; Silky Hakea; Esler et al. 2010; Gordon and Fourie 2011), several Australian Acacia species (Fabaceae; wattles) (Impson et al. 2011), and Leptospermum laevigatum (Myrtaceae; Australian Myrtle; Gordon 2011). This era also saw projects initiated against floating, invasive aquatic plants (Coetzee et al. 2011a) and against the various hybrids in the Lantana camara L. hybrid-complex (Verbenaceae; Lantana; Urban et al. 2011). More recently, herbaceous plants, vines and various subtropical shrubs have been subjected to biological control (Moran et al. 2013).

For over a century, South Africa has been one of the five main countries conducting research on and implementation of biological control of invasive alien plants (McFadyen 1998). Since 1995, with major increases in funding from state sources (Zimmermann et al. 2004) and the consequent involvement of many more researchers, students, support staff (see also van Wilgen 2020, Chap. 2, Sect. 2.2), and implementers, there have been an increasing number of innovative and successful projects, allowing South Africa to play a leadership role in the use of biological control in the management of invasive alien plants (Moran and Hoffmann 2015; Schwarzländer et al. 2018).

All the projects and programmes on biological control of invasive plants in South Africa have been thoroughly documented in three sets of reviews (Hoffmann 1991; Olckers and Hill 1999; Moran et al. 2011), in Muniappan et al. (2009), and in a recent overview of the entire South African biological control effort (Zachariades et al. 2017). These compilations have been comprehensive in recording which agents have been sourced, tested, mass-reared, released, established and redistributed against each of the targeted, invasive plant species, and in recording their progress and the extent of damage caused on the target host-plants. However, these accounts have been less clear in summarising the overall achievements (i.e. outcomes) of biological control programmes against invasive alien plant species and consequently, that is the primary purpose of this account.

# 19.2 Evaluating the Effectiveness of Biological Control of Invasive Alien Plants

Across the world, many different approaches have been used to evaluate and express the outcomes of biological control projects against invasive plant species (e.g. Syrett et al. 2000; Morin et al. 2009). It has long been understood that the objective of biological control "... is not the eradication [of the target plant species] but the reduction of their densities to non-economic levels" (Huffaker 1964). In some instances, the success of biological control is self-evident and before-and-after photographic records (see, for example, Figs. 19.1, 19.2 and 19.3) suffice to make the general point. Evaluations of biological control accomplishments against invasive alien plant species, during the earlier eras, were mostly descriptive and subjective. Thus, an apparent understanding of the outcomes of biological control was, and often still is, based on 'proxy-studies' of the progress of the released biological control agents themselves. These studies aligned with the expertise of the scientists involved, who were overwhelmingly entomologists or, less often, pathologists, not plant ecologists. Many of these studies were appropriate for short-term funding cycles and provided excellent subject-matter for post-graduate student projects.

Fig. 19.1 Photographs taken at paired sites near Makhanda, Eastern Cape, before and after successful biological control, on hillsides covered with dense infestations of Acacia longifolia (Long-Leaved Wattle) trees in 1978 (a), subsequently replaced by native vegetation in 2013 (b). Photographs courtesy of JH Hoffmann

Fig. 19.2 Photographs taken at paired sites on Sunset Dam, Kruger National Park, Mpumalanga, before (a) and after (b) successful biological control of Pistia stratiotes (Water Lettuce). Photographs courtesy of LC Foxcroft

Fig. 19.3 Photographs taken at paired sites near Upington, Northern Cape, of flourishing populations of Cylindropuntia fulgida (Boxing-Glove Cactus) in 2012 (a) replaced by dead and dying stumps in 2015 (b) after biological control. Photographs courtesy of Travor Xivuri

But Crawley (1989), among others, has emphasised that measures of agent numbers and the levels of damage that they inflict, while useful determinants of progress, are not relevant to the population dynamics of the target plants themselves, i.e. to the outcomes of biological control. This plant-population perspective has been recognised by practitioners and has helped to change the emphasis in assessing the accomplishments of biological control of invasive alien plants.

The outcomes of biological control of invasive alien plants can be measured in many ways, including, for example, reductions in density of the invasive species, the extent of their distribution, changes in biomass, their longevity, and the numbers of seeds, or other propagules, produced and accumulated. Furthermore, as Hoffmann et al. (2019) have noted: "Each of these measures must be considered in a context of scale (e.g. in a defined locality such as a reserve or forest, in a functional habitat such as a river catchment or mountain range, or at a landscape level that might include a biome, region or country)." In the latest world catalogue of biological control of "weeds" (Winston et al. 2014), the "scale of impact" of biological control is categorised by subjective estimates as: "localized, regional, widespread throughout [the] range [of the target plant], and unknown", and descriptive notes are provided to support these opinions for each of 1555 intentional releases of "weed" biological control agents, worldwide. Thus, the impacts of biological control are invariably complex and often site-specific. For example, on Chromolaena odorata (Asteraceae; Triffid Weed), in South Africa, agent-impacts are sporadic and highly localised (Zachariades et al. 2011), and the situation is dynamic and not yet understood (Zachariades et al. 2016). Similarly, on the various taxa in the L. camara hybrid complex, agents undergo 'boom and bust' cycles, dependent on varietal types of the plants, and on altitudinal and other effects (Urban et al. 2011).

For all of these reasons, accurate quantitative measures of plant- and seedpopulation dynamics, and accompanying experimental evaluations of outcomes in biological control, are expensive and difficult, and require years or decades of study. The key here, with more recent South African programmes since the 1970s, has been sustained funding for biological control of invasive plants and the career-longcontinuity of many of the research- and support-personnel involved. This has encouraged long-term research programmes (albeit never enough) and a disproportionately high number of carefully-quantified and unambiguous evaluations. For example: the 25-year evaluation of biological control of Opuntia stricta (Cactaceae; Australian Pest Pear; see Box 19.1) (Hoffmann et al. 1998; Paterson et al. 2011); 16 years of assessment on the biological control of Sesbania punicea (Fabaceae; Red Sesbania) at 22 sites (Hoffmann and Moran 1998); ongoing observations over 28 years on a fungal-pathogen biological control agent used against Acacia saligna (Fabaceae; Port Jackson Willow) (Wood and Morris 2007); continuing country-wide surveys over the past decade on several species of invasive aquatic plants (Coetzee et al. 2011a); and finally, the assessments of the degree of biological control against L. camara, ongoing since the 1970s (Cilliers 1987; Cilliers and Neser 1991; Urban et al. 2011). In all of these cases, and for the other cases cited throughout the text, conclusions about the status of the individual biological control projects, which have not been recently or fully published, have been brought up to date (to 2019) from the personal knowledge of one or more of the contributing authors.

#### Box 19.1 Opuntia stricta (Cactaceae) (Australian Pest Pear)

Invasion by Opuntia stricta (Australian Pest Pear) in the Kruger National Park was rapid, with about 60,000 ha being infested by the turn of the century, mainly through seeds being spread by baboons and elephants. An intensive herbicide-based control programme failed to achieve its objectives and eventually biological control was adopted as a management process despite the park management's reluctance to have additional non-native species (i.e. biological control agents) brought into a conservation area. Simulation models had correctly predicted that the release of the well-known cactus moth, cactoblastis, in 1988, would result in diminished invasion. But success was mainly due to the release of a cochineal insect species (open circles), in 1997, that kills the pads/ cladodes (closed circles) and the plants. Long-term surveys over 20 years showed that there was a rapid decline in the density of the cactus plants and that the weed has now been permanently controlled well below an acceptable threshold by biological control (Figure updated from Impson et al. 2011).

A system has been used in South Africa to describe overall success, i.e. outcomes of biological control against invasive alien plants, at the plant population (demographic) level, as 'complete', 'substantial', 'negligible', or 'unknown', and which relies on long-term formal evaluations, or on expert-opinion on broad categorisations of the reduced dependency on alternative control methods (chemical or mechanical), as a result of the introduction of biological control agents. This classification system was initiated by Hoffmann (1991). It has subsequently been refined and elaborated by Hoffmann (1995), Anonymous (1999), Hoffmann and Moran (2008), Klein (2011) and Zachariades et al. (2017), and has been widely adopted internationally (McFadyen 1998). Using this 'now-traditional' descriptive system as a basis, several assessments of the outcomes of biological control of invasive plants in South Africa at the level of a plant population, have been made, including:

A feature of all these summaries is that they are based on the foundation of the 'traditional' system for describing and recording biological control achievements against invasive alien plants. Until now this has been the only way of doing so, but the descriptors and their definitions are vague, often subjective or ambiguous, and convey little or no information about details or context. An elaboration of the present system has therefore been proposed by Hoffmann et al. (2019) which is based on a conceptual framework (see Box 19.2) that categorises the outcomes of biological control, from barely perceptible (category C), to spectacularly successful (categorised as A+) where, over decades, the agents have had a considerable impact on one or more of four 'invasion parameters' of their target hosts, namely, plant population density, distribution (area), biomass and number of propagules (seeds), for different regions, habitats or circumstances (see Box 19.3). Other parameters, such as the longevity of invasive plant populations, could be accommodated if required. This system has now been adopted in South Africa, and when implemented it will allow for more nuanced, detailed, and accurate analyses and descriptions of the outcomes of biological control of invasive alien plants.

#### Box 19.2 Envisaging the Outcomes of Weed Biological Control

The sigmoid curve in the figure below (reproduced with permission from Hoffmann et al. 2019) represents the hypothetical extent and progress of an invasion by an alien plant species, commonly measured as either area invaded, density, biomass, seed production or its equivalent. Given time (usually at least 10–20 years) after the initiation of biological control, damage by the biological control agents can reduce target-plant populations and their invasiveness: (1) if the effects are only slight, the trajectory of the curve will be moderated to a greater or lesser degree within the bounds of 'control category C'; or (2) as in about 40% of the cases in South Africa, biological control can 'reverse', i.e. reduce target-plant populations and the extent of the invasion, depressing the trajectory of the curve into 'control category B'; or (3) as in about 30% of the cases in South Africa, can spectacularly reduce weed populations and the extent of the invasion to levels below a tolerable threshold, moving the curve into 'control category A'. Conceptualising biological control in this way allows for categorisations and subsequent recording of outcomes, from C (imperceptible levels of control) to A+ (the most favourable outcome), for different regions, habitats, and circumstances. Some examples that illustrate the application of this framework for viewing outcomes in weed biological control are given in Box 19.3.

#### Box 19.3 A System for Recording the Outcomes of Weed Biological Control

Since the early 1990s, 'complete', 'substantial', or 'negligible' have been accepted descriptions of achievements in weed biological control at the plant population level (i.e. outcomes). These terms are too coarse and therefore can be misleading. For example, a biological control programme might result in the near-elimination ('complete' control), of the target weed in one area or situation, but in 'negligible' control elsewhere, an outcome that would 'average out' as 'substantial' control. This is clearly unsatisfactory. Recently a more elaborate and robust system has been developed for recording outcomes that considers four different 'invasion parameters': density, area, biomass and number of propagules (seeds), for different regions and habitats (Hoffmann et al. 2019). The examples, in the table below, of three well-known South African weed species, illustrate this system. The most positive 'outcomes' are recorded as A+ through to C as the least favourable, based on categorisations as defined by Hoffmann et al. (2019) (and see Box 19.2). The categorisations that are dependent on expert opinion and observations are in light type, with those supported by quantified evidence in bold type. (1) Opuntia ficus-indica (Mission Prickly Pear), is not under satisfactory biological control in the coastal regions of the Eastern Cape, but is under excellent biological control in drylands, in all other regions, where populations are maintained well below an acceptable threshold. The biological control programme against O. ficus-indica has been ongoing for 86 years since the first agent was released against this plant in South Africa. (2) Invasions of Acacia saligna (Port Jackson Willow), in terms of density, biomass and numbers of seeds have been considerably moderated by biological control, but the distribution of the weed has remained static and is characterised by the appearance, over a wide area, of dense mats of seedlings from accumulated seed-banks after a fire or soil-disturbance. (3) Eichhornia crassipes (Water Hyacinth), is under far better biological control in the warmer, coastal areas and in clear waters, than it is in the highlands, under eutrophic conditions.

# 19.3 What Has Been Forgotten over the Passage of Time?

One of the idiosyncrasies of biological control of invasive plant species is that society tends to forget the extent and/or intensity of the specific invasions that existed before biological control was implemented and fails to recall that there was ever a problem in the first place. Examples to support this statement and to elaborate on some of the successes achieved, are briefly described below:

#### 19 Biological Control Against Invasive Alien Plants 563

the landscape, is principally due to biological control, albeit in conjunction with manual clearing operations, fires and other natural mortalities affecting the seeds. Over 30 years, biological control, and multiple fire cycles, have reversed the aggressiveness of A. longifolia which, in most situations, is now generally considered to have been rendered insignificant as an invasive species (Moran and Hoffmann 2012) (see Fig. 19.1).

both of which are currently being suppressed, over a wide area, to very low levels by biological control (Zimmermann 2017) (see Fig. 19.3).

#### Box 19.4 Myriophyllum aquaticum (Haloragaceae) (Parrot's Feather)

Myriophyllum aquaticum (Parrot's Feather) was regarded as one of South Africa's worst aquatic weeds, found in every province, where it caused a reduction in stream flow, blocked water pumps and interfered with recreational activities. Biological control was implemented in 1994 and a survey conducted in 2008 showed that the weed had been eliminated (i.e. 'clear') at 66 (63%) of the 105 sites surveyed (see lower section of 'stack' diagram). Surveys from 1995 to 2017 showed a significant reduction in the density of the weed at the other 39 sites (see lower histogram: mean number of shoots/ <sup>m</sup><sup>2</sup> SE) to levels below a tolerable threshold (Coetzee et al. 2011a)

# 19.4 Additional Considerations, Caveats and Conclusions

Since 1995, and the advent of support from the Working for Water programme (Zimmermann et al. 2004), biological control of invasive plants in South Africa has gained enormous momentum, and many of the outcomes summarised in this chapter owe their successes to this. Much has been achieved, but some additional points and caveats need to be recorded:

We conclude that even small degrees of suppression of plant fitness, or reductions in the size of populations through biological control will be compounded over the years. In most cases, biological control will reduce the costs of other interventions and will make successful management of the problem more likely and easier. If there are any doubts about what has been achieved with biological control against invasive alien plants in South Africa over the years, the fundamental counterfactual question is: 'what would be the extent of the alien plant invasions if there had been no biological controls?'

Acknowledgements Our thanks and respects are extended to past and present invasive plant biological control practitioners in South Africa. Not all of them can be recorded as authors, but their work is the foundation for many of the cases and outcomes reported here. We appreciate the valuable inputs from the reviewers and the editors. We are also grateful to the Working for Water programme of the Department of Water Affairs and Forestry, subsequently the Department of Environmental Affairs, Natural Resources Management Programmes, for their generous financial support since 1995, which has put South Africa in the forefront of endeavours in biological control against invasive alien plants worldwide.

## References

Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence and indicate if changes were made.

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# Chapter 20 Analysing the Risks Posed by Biological Invasions to South Africa

Sabrina Kumschick , Llewellyn C. Foxcroft , and John R. Wilson

Abstract Risk analysis is an important decision-support tool for the management of biological invasions. South Africa, as a signatory to international agreements, has enacted legislation requiring risk analyses to be conducted if trade is to be restricted or regulated and if alien species are to be introduced. In this chapter, we outline the various needs for risk analyses for biological invasions in South Africa, summarise the current status, and make recommendations for a way forward. In particular, we highlight the need to move away from approaches that are purely based on expert opinion or entirely reactive, and propose a new system and process which includes the use of a structured risk analysis framework with clear guidelines to avoid expert bias. We highlight the need to assess risk, consider risk management options (including benefits), and to develop clear recommendations. The proposed process also involves the review of recommendations by an independent panel. We further note that the effectiveness of such approaches will be defined by their transparency, their accuracy, how feasible they are to implement in practice, and the trust that people have in the system.

S. Kumschick (\*) · J. R. Wilson

Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

South African National Biodiversity Institute, Kirstenbosch Research Centre, Cape Town, South Africa e-mail<EMAIL_ADDRESS>
L. C. Foxcroft Conservation Services, South African National Parks, Skukuza, South Africa

Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

## 20.1 Risk Analysis for Biological Invasions

Frameworks for the management and regulation of alien species and associated processes have been developed all over the world to deal with undesirable consequences and to mitigate future impacts of species introduced outside of their native ranges. Risk analysis is a formal, evidence-based process to analyse the risk of a particular hazard to a certain area or situation. A hazard can be an event or phenomenon, like the increase of temperature globally or the pollution of a river with chemicals. A hazard can also be more specific, like the introduction of an alien species to a new area. This chapter reviews what has been done in South Africa in the context of international best practice, and outlines a proposed way forward.

In general terms, risk analysis is the combination of hazard identification, risk assessment, risk management and risk communication (Fig. 20.1). Biological invasions present various hazards that can be broadly grouped in terms of species, pathways, and areas. If the hazard is the alien species itself, risk assessment includes the likelihood of a particular species being introduced, establishing and spreading in an area, and the consequences (negative impacts) thereof; risk management focuses on management options available for the species, the ease of management more broadly, and people's perceptions and uses of the species that could lead to conflicts of interest around its control (Branquart et al. 2016). For pathway risk assessment, the likelihood and consequences of the pathway or vector bringing in harmful alien species is assessed (in this case, risk is often proportional to the number of harmful alien species introduced along a pathway, i.e. the colonisation pressure); and risk management focuses on interventions to make the pathways "cleaner" (e.g. the Ballast Water Convention; IMO 2004). Lastly, area-based risk assessments examine the suite of alien species in a certain area and the vulnerability of the area itself to

Fig. 20.1 The components of risk analysis. Hazard identification frames the problem that is being addressed (with respect to biological invasions this is often in terms of pathways, species, or areas not shown in the figure). Risk assessment focuses on the likelihood and consequences of the hazard occurring. Risk management considers ways to mitigate the risks while maintaining any benefits. Risk communication aims to ensure effective communication and sharing of relevant information between stakeholders and assessors during the process of risk assessment and management, both to improve the information available for the risk analysis and to try to ensure that everyone ultimately agrees to abide by the outcome of the process

invasion, to distinguish high from low risk areas; and risk management efforts aim both to reduce the total level of invasion in the area and to limit the potential for all pathways to bring in new species. Since alien species generally affect a wide variety of stakeholders and are socially complex rather than clearly defined scientific problems (Woodford et al. 2016), communication with stakeholders is key throughout the process. Such communication needs to be a two-way process which aims to inform people about the outcomes of the analysis (risk communication), but also ensures stakeholders' knowledge, opinions, and concerns are considered during the risk assessment and risk management planning.

Besides the assessment of different hazards, risk analyses can also focus on different stages in the invasion process (Blackburn et al. 2011). One of the most prominent distinctions is between pre- and post-border analyses. It is often much more cost-effective to prevent an invasion from happening than to mitigate the harm or try to eradicate a species once it has established—pre-border risk analyses can help to make decisions about whether or not to allow the import of a new species, based on risk to the recipient environment. For species that are already present, we need ways to assess which to regulate and manage post-border. The main distinctions between pre- and post-border analyses are therefore: (1) the need for pre-border analyses to include the likelihood of arrival and introduction into the country; and (2) the need for post-border analyses to include risk management considerations focussing on reducing the negative impacts of invasions while maintaining benefits, and reaching agreement between stakeholders that might hold opposing entrenched positions.

Risk analysis methods ideally have a few key qualities that make them useful for helping to make management decisions including that they should be transparent, accurate, realistic, evidence-based, and free of biases as far as possible. Transparency ensures that decisions are traceable and the rationale behind them is clear. Accuracy is needed so that resources are not wasted on managing benign species, or so that potentially harmful species can be prevented from becoming problematic. Risk analysis also requires resources to implement, including financial and human capital (i.e. skilled practitioners). Given the inherent biases any assessor may have (e.g. Montibeller and Von Winterfeldt 2015) it is also important that such analyses are based on sound evidence. Furthermore, group assessments and independent review panels can minimise biases by a single assessor. Explicit guidance documents and training of assessors in the principles and methods of risk analysis can further improve the process and reduce assessor bias rooted in a different understanding of the questions asked. A group of European scientists developed a minimum set of 14 standards for risk assessment to aid their implementation for the EU Regulation on invasive alien species (1143/2014) (Roy et al. 2018), many of which overlap with what is discussed in this paragraph, and a few of which are specific to the requirements of EU regulation (like the assessment of impact on ecosystem services and effects of future climate change). But these standards are also useful in a South African context and have largely been followed in what is suggested here.

## 20.1.1 Risk Assessment

Many tools have been developed to assess the risk of biological invasions, but most focus on specific species as the hazard (Kumschick and Richardson 2013). Such tools typically cover a variety of aspects related to the risks posed by a species, which includes transport, establishment, abundance, spread, and impact (Leung et al. 2012). However, there are also many tools that cover or assess only a specific part of the risk of a species and which are often mistakenly put under the umbrella of "risk assessments". For example, much effort has been put into standardising the way we quantify impacts, and many recent developments were made around impact assessment tools (e.g. Blackburn et al. 2014; Bacher et al. 2018; Zengeya et al. 2020, Chap. 17). Similarly, species distribution models and climate matching tools are improving the way we can assess and map a species' climatically suitable area in a new range (see Wilson et al. 2020, Sect. 13.5, Chap. 13). Van Wilgen et al. (2009), for example, present climate suitability matches for amphibians and reptiles that can improve the way we assess risks for this group. In combination with other tools, climate suitability models and impact assessments can improve the assessment and analysis of risks of biological invasions in a transparent, standardised, and repeatable manner. However, by definition, a risk assessment needs to cover both the likelihood of the hazard occurring (i.e. the invasion process) as well as its consequences (i.e. the negative impacts).

Despite the aspects of risk to be covered being rather straightforward, there are many ways in which these can be assessed in practice. Several approaches to risk assessment have been suggested, including the trait-scoring, statistical, decisiontree, rapid screening, mechanistic, and detailed approach (Keller and Kumschick 2017). Each of these has its own benefits and weaknesses and is based on different premises:

Trait Scoring This assumes that species with specific traits have a higher chance of becoming invasive, and of having higher impacts. In other words, the more "invasive traits" a species has, the higher the risk it poses. This is the most common approach used to date, including in the Australian Weed Risk Assessment model (AWRA; Pheloung et al. 1999), which was developed as a pre-border tool to screen alien plants to be introduced to Australia. The AWRA has been used around the world and modified for different taxonomic groups including fish and freshwater invertebrates (Copp et al. 2005; Tricarico et al. 2010; see Appendix in Kumschick and Richardson 2013). This approach of assessing risk requires information about the taxon as alien and what makes some species more successful than others. It also assumes that the main contributor to invasion success is inherent to the introduced species' traits, and it is generally limited to a taxonomic group with comparable traits.

Statistical Approach The statistical approach is very similar to trait-scoring insofar as it uses traits of species to predict the potential for invasion and causing harm (Keller and Kumschick 2017). In the trait-scoring approach (seemingly) important traits are collated and rated by experts only. In the statistical approach the list of traits is refined using statistical or machine learning algorithms. These algorithms find patterns in the data and include only those traits that contribute to invasion success, as opposed to all traits considered important by experts. For example, for alien cacti it was found that native range size is a predictor of both impact and invasiveness in South Africa (Novoa et al. 2016a). The statistical approach can take into account interactions between traits and lead to much simpler tools than trait-scoring, but the underlying methods and mechanisms are not always easily understood and therefore less likely to be supported by managers and policy-makers (Keller and Kumschick 2017). Furthermore, due to the models including a very limited number of variables, no conclusion can be reached if data for any of the few selected variables is lacking.

Decision Trees These can be a subset of the statistical approach, but also be based on traits considered as important by experts. Similar issues therefore arise in this approach, which comprises of several questions of which each answer leads either to another question or a decision regarding a species' risk. If the answer to any question is not known, no decision can be reached, or tenuous assumptions are made. For that reason, this approach has not been used extensively. However, Tucker and Richardson (1995) suggested a decision tree approach to assess risks of tree invasions to the Fynbos Biome.

Rapid Screening The rapid screening approach can use elements of the previous three approaches, with the focus on a quick assessment of often a large number of species where little information is available. Rapid screening can be used as a standalone risk assessment, to prioritise species for more detailed risk analysis or to create watch lists. Faulkner et al. (2014) applied a rapid screening tool to almost 400 species to create a watch list of alien species for South Africa. Their tool included only three aspects: (1) the invasiveness of the species elsewhere, (2) climate match, and (3) tourism and trade data as a proxy for propagule pressure.

Mechanistic Approach The mechanistic approach is not based on traits per se, but it follows a species through the invasion process and assesses the likelihood that it will cross certain barriers (e.g. those proposed by based on Blackburn et al. 2011), and whether it has the potential to have an impact. For example, if a species is unlikely to find suitable climatic conditions and habitats in a new region, it would be unlikely to establish and subsequently become invasive, which can reduce its risk despite potential impacts. Such an approach is implemented in Belgium (D'hondt et al. 2015).

Detailed Approach The detailed approach, as the name suggests, requires a substantial amount of data on the alien species' ecology, biology and behaviour, as well as the recipient environment and the interaction between all these factors. It often requires additional research to fill knowledge gaps, which may include interviews with experts. Since it also includes management considerations and stakeholder perceptions, it resembles more closely a risk analysis approach. It has been used in Canada to assess risks of the highly contentious Asian carp species (Mandrak and Cudmore 2004).

Which approach is most useful depends on the circumstances and purpose. For example, rapid screening is quick and easy. However, results of such assessments provide limited knowledge on the mechanisms of invasion and expected behaviours of a species under specific circumstances as the underlying assumptions are often not explicit. This can be problematic for species with no previous history of introduction outside of their native range (no "invasion history"). Trade-offs between the optimal investment and the optimal outcome need to be made when selecting an approach for a risk assessment tool. Furthermore, the amount of knowledge available on a taxon can limit the use of certain approaches. The statistical approach requires the input of a substantial amount of data to train the model—without adequate knowledge about the taxon and its behaviour as an invader, such models cannot be developed. Furthermore, the final model requires data on only a few variables, which increases the likelihood of this information not being available for some species. This emphasises the need for a risk assessment tool to accommodate situations where information on a species to be assessed is scarce or lacking.

Many tools approach this by applying the precautionary principle—if no data are available on a species or a certain situation, preventing informed decision-making on the risks involved, the species is by default deemed to be a high risk (e.g. Nentwig et al. 2016). This principle is common practice and also anchored in international agreements. For example, in the management of alien species, the IUCN (2000) states that "unless there is a reasonable likelihood that an introduction will be harmless, it should be treated as likely to be harmful".

## 20.1.2 Risk Management

To reach sensible and effective management decisions, risk management considerations are fundamental. Ignoring management feasibility, benefits of the taxon, or potential conflicts between stakeholders, has been shown to lead to unsuccessful and wasteful management decisions (e.g. van Wilgen and Richardson 2012). The distinction between whether, as opposed to how, to regulate and manage a species relies on estimating the risks it poses to the recipient environment and economy. For taxa that are not yet present in an area, and for which decisions on importation are required, this can be a relatively straightforward process: if the species poses a high risk its importation should not be allowed, but if it poses a low risk the species could be considered safe for import (e.g. Keller and Kumschick 2017). However, decisions regarding taxa that are already present in an area, and in use for various purposes, cannot solely rely on estimates of the risks they pose, but also depend on management options available for the species. For example, many trees were introduced into South Africa for forestry. Even though many of them threaten native biodiversity, management decisions need to take into account the costs of management, the techniques and tools available, as well as the species life-history traits (Wilson et al. 2011; Richardson et al. 2015). Further, management does not happen in isolation from the rest of society; social perceptions and benefits need to be assessed and accounted for (e.g. van Wilgen and Richardson 2012; Zengeya et al. 2017; see Shackleton et al. 2020, Chap. 24). Unlike in the risk assessment where clear answers and probabilities are often provided to determine the level of risk, the inclusion of benefits is dependent on the agendas of various role players, priorities of decision makers, and the influence of key stakeholders (e.g. Kumschick et al. 2012; Woodford et al. 2017). To keep the process transparent, provision needs to be made to outline how the inclusion of benefits influences the management decisions, and which benefits are included.

Once a risk has been identified and assessed, and the species is regarded as of concern (i.e. high risk), one needs to consider what can be done to manage the risk (Fig. 20.2). For species already present in an area this will often require a detailed evaluation of management options, the development of management plans and

Fig. 20.2 The proposed process outlining the steps to develop recommendations for the listing of alien species under national legislation in South Africa. Reproduced from Kumschick et al. (2018) with permission

financial resources, and a process of prioritisation of potential interventions, including considerations related to the funds available to put the management plan into action (Wilson et al. 2017). Such detailed assessments are generally beyond the scope of risk analyses which are mostly desktop-based (but see example of biological control release applications below). However, some basic management considerations need to be taken into account that allow for a broad classification of how to treat a certain risk.

Risk management is generally more open-ended than the risk assessment, but needs to be documented in detail to assure that decisions are transparent and can be revisited when information becomes available. Risk management can include parameters like socio-economic and environmental benefits, the feasibility of stopping future immigration of a risky species, and basic considerations regarding eradication feasibility (e.g. Panetta and Timmins 2004; Wilson et al. 2017). Renteria et al. (2017), for example, suggested a rapid scheme for prioritisation of alien species in South Africa for eradication, using information on the species' distribution and "eradication feasibility syndromes". While such simple desktop studies are useful to flag species for further evaluation, they are not sufficient to determine whether a species is a suitable eradication target. In practice, eradication feasibility depends heavily on the biological (e.g. location of individuals, detectability, availability of effective control methods) and administrative context (e.g. funds available, and a dedicated and persistent leader and team).

## 20.1.3 Risk Communication

Once the level of risk has been determined and options for management and benefits evaluated, it is crucial to clearly communicate the outcomes of the analysis to stakeholders, including the general public, policy-makers and traders of the alien species. There are two important requirements for risk communication. Firstly, stakeholders must be engaged during the risk analysis, both for assessors to obtain information on the hazard, and to gain the support of stakeholders (e.g. Novoa et al. 2015, 2016b). There are often formal regulatory processes of stakeholder engagement. For example, before the promulgation of new regulations in South Africa, they are published for public comment, whereafter the comments needed to be addressed or acknowledged. In contentious cases, an independent scientific assessment might be needed (Scholes et al. 2017), but if conflicts are to be avoided, engagement should happen from the outset of the process.

Secondly, risk communication is important for providing stakeholders with sufficient information to understand the recommendations. Stakeholders need to be in a position to know under which circumstances decisions would be altered, for example, how new information or changing practices would influence risk. Therefore, communication needs to be simple enough to ensure understanding, but simultaneously enough information needs to be provided to underpin the decision. Decisions are often only successful and implementable if stakeholders understand the risks associated with the taxon. To gain the support from the general public and financial institutions (e.g. government departments), engagement and clear communication regarding risks is crucial. In practice, part of risk communication consists of clearly documenting the hazard, the circumstances of the assessment (including the area of assessment), and the results of the assessment, in an easily understandable manner. An easy-to-digest summary sheet including the main findings of each section (risk assessment and management), including short descriptions of the hazard (e.g. the alien species), pathways, impacts, management options, and benefits can serve this purpose.

## 20.2 Risk Analysis in South Africa

Various tools have been developed for use specifically in the South African context. Tucker and Richardson (1995) were amongst the pioneers in risk assessments for biological invasions. They developed a tool to assess the risks that woody plants pose to the Fynbos Biome, which requires information on the alien species, the region of origin, and various details specific to the Fynbos Biome, for example tolerance to fires. This approach is a combination of a trait-based scoring approach and a decision tree, and allowance is made for the lack of data on some traits or aspects. Due to the very specific focus of the scheme (the Fynbos Biome) it is most likely not applicable to a wider geographic range or different habitats, and it is limited to assessing woody plants. Similarly, other studies developing or applying risk assessments and analysis

Fig. 20.3 Aspects of risk to be considered for the listing and regulation of alien species under national legislation in South Africa divided into risk assessment, risk management and risk communication based on a standard framework for risk analysis. The process suggested for risk management is shown in Fig. 20.2

in a South African context have been rather limited in scope. For example, van Wilgen et al. (2008) called for the use of risk assessments for the herpetofauna present in South Africa, mainly introduced through the pet trade. Alien fish have been extensively assessed for their risks in South Africa (Ellender and Weyl 2014; Marr et al. 2017), also necessitated by the conflicts between conservationists and recreational anglers (see Weyl et al. 2020, Chap. 6). An exception to this is the 'watch list' approach outlined above (Faulkner et al. 2014), which is applicable in any given region and can rapidly assess a wide variety of taxonomic groups. Most recently, we developed a risk analysis framework to underpin the regulation of alien taxa and aid management decisions (Kumschick et al. 2018). It is applicable to any taxonomic group and can be used pre- and post-border.

The need for risk analyses on biological invasions has been formally adopted in South African legislation (Box 20.1). The legislation outlines actions related to alien species that need risk analyses to be completed. This includes permits for the importation of new alien species into the country and to carry out restricted activities involving some listed species, the listing of alien species under national legislation (Fig. 20.3), and the introduction and subsequent release of alien species for biological control (see Hill et al. 2020, Chap. 19). For all these issues, processes are being instituted and frameworks developed in South Africa, which need to be followed to carry out the respective activities. In Table 20.1, we summarise the legislative needs for risk analysis in South Africa, how they are currently implemented, and provide recommendations for the future (for further details see the discussion below).

#### Box 20.1 Key International and South African Legislation Pertaining to the Risk Analysis of Biological Invasions

International agreements under the World Trade Organisation (WTO) require the assessment of risks before certain activities involving an alien taxon, especially trade, can be restricted, or before a new taxon should be allowed for import. These agreements recognise the standards set by the International Plant Protection Convention (IPPC; FAO 1996) and the World Organisation for Animal Health (OIE 2011). The assessment of the risk that a species poses allows for the distinction between potentially harmful and benign taxa. However, risk analysis additionally includes considerations regarding whether and how these risks can be managed (Convention on Biological Diversity 2002).

These international standards and agreements which South Africa is part of are complemented by legal obligations which need to be considered and followed where risk analysis is required. Specifically, the National Environmental Management: Biodiversity Act (NEM:BA, Act 10 of 2004) Alien and Invasive Species Regulations (in short, NEM:BA A&IS Regulations; Department of Environmental Affairs 2014) outline the necessary content of risk analyses for the application of permits, including for import and restricted activities.

## 20.2.1 Import of Alien Species

Several government departments administer import applications for alien species; on a national level those are the Department of Environment, Forestry, and Fisheries (DEFF) and the Department of Agriculture, Land Reform and Rural Development (DALRRD) mainly concerning new introductions into the country. For many other introductions of alien species and species new to a province, provincial departments are still largely responsible for the reviewing of import applications to introduce species from outside the country. They generally need to adhere to provincial legislation, but the processes followed vary significantly between provinces and taxa. Furthermore, they depend on the expertise available in the respective departments, and no consistent frameworks are followed to guide decision-making. In the following paragraphs, we mainly focus on the import of new alien species.

DALRRD (through South Africa's National Plant Protection Organisation, NPPOZA), is mandated to prevent the introduction, establishment and spread of alien pest or disease species on plants and plant products. DALRRD conducts pre-border risk analysis for agricultural species imported into South Africa. These analyses have a focus both on minimising the risks of introducing pathogens or pests on imported species and on the risks of the species themselves becoming invasive. The responsibility of DALRRD is to reduce risks of agriculture, but in the absence of other processes before the promulgation of the NEM:BA A&IS Regulations (see van Wilgen et al. 2020, Chap. 1, Box 1.1), DALRRD have issued permits for new introductions of non-agricultural alien species as well. This has not been sufficient to address all of the environmental risks associated with the introduction of new species, and the minimum standards for accepting introductions has historically been set differently for different organisms introduced for different purposes.

To address this, the NEM:BA A&IS Regulations were developed and DEFF mandated to issue permits for alien species not yet legally present in the country (i.e. new introductions) (Department of Environmental Affairs 2014). Every application for the import of a species not yet present in a country needs to be accompanied by a risk analysis according to international agreements (Box 20.1). The NEM:BA A&IS Regulations have since August 2014 outlined the information required for risk analyses accompanying import applications for the introduction of new species into South Africa (note these are currently termed "risk assessments" in the regulations, but are actually "risk analyses" as per the definitions in this chapter and in line with the international naming standards in Fig. 20.1). The requirements include information on the species to be imported, its taxonomy, biology and ecology, aspects linked to the likelihood of invasion like invasion history elsewhere, and traits linked to impact potential. This list includes several aspects that have been shown to be linked to invasion success and impact. Furthermore, it includes specific information regarding the planned activity in South Africa and measures proposed to manage the risks, which can be grouped under risk management. These risk analyses are the responsibility of applicants who wish to import new alien species, and the minimum requirements for assessors qualifications are specified in the NEM:BA A&IS Regulations, which makes the quality of analyses rather heterogeneous. Furthermore, while the regulations require detailed information on the biology and ecology of the species, the region and circumstances of its introduction and other relevant factors, they do not provide guidance on how to reach conclusions on the species' risk based on that information, or how to format the analysis (i.e. it is not actually a framework for risk analysis). Given the lack of clear guidelines on how to assess and weight each aspect, and how to reach a conclusion on the magnitude of risk, it is difficult to defend the accuracy and consistency when using this approach (Keller and Kumschick 2017). Further disadvantages of this approach are that it is time and resource-consuming.

To assist applicants for import permits to develop risk analyses and to render the decision-making process more transparent, a framework and guidelines for risk analysis have been developed—the Risk Analysis for Alien Taxa Framework (RAAT; Kumschick et al. 2018). The framework is based on international bestpractice, and the guidelines cover most aspects related to the risk of alien species as outlined in the framework provided in the NEM:BA A&IS Regulations; information on the intended activities related to the permit application would need to be outlined separately. RAAT consist of 23–29 detailed questions. Answers to questions are given as scenarios to reduce assessor bias, and calculations provided to achieve risk levels (low, medium or high). The framework includes all aspects of risk as described in Fig. 20.3. In many developing countries like South Africa, decisions need to be made with limited funds and expertise available (see also Soliman et al. 2016 for southeast Asia). Even though RAAT can take several days to complete, it is less labour-intensive than collecting all the detailed information as outlined in the NEM:BA A&IS Regulations. Furthermore, conclusions regarding risk levels are less subjective as answer levels and calculations are outlined in detail. These guidelines are, however, not currently implemented for import applications (but see below for listing of species under the NEM:BA A&IS Regulations).

To support the DEFF in making decisions concerning the risks of biological invasions, the South African Alien Species Risk Analysis Review Panel (ASRARP) was formed. ASRARP is tasked with reviewing risk analyses attached to import applications to ensure they are scientifically robust and take into account the best available evidence, as well as risk analyses underpinning the listing of species under national legislation (see below and Fig. 20.4). ASRARP is an independent body (run through the South African National Biodiversity Institute) that incorporates scientists and taxon experts. It provides recommendations as to the validity and completeness of the information provided in the analysis, as well as recommendations regarding the outcomes of the application (i.e. whether to import and/or regulate a species). Recommendations are submitted to DEFF who then decide whether to grant the import permit (Fig. 20.4).

Fig. 20.4 Procedure for development of recommendations regarding the import of an alien species not currently legally in the country, specifically focusing on the review of applications by the Alien Species Risk Analysis Review Panel (ASRARP). Acronyms: SACNASP South African Council of Natural Science Practitioners, DEFF Department of Environment, Forestry and Fisheries, NEM:BA National Environmental Management: Biodiversity Act 2004 (Act No. 10 of 2004) Alien and Invasive Species Regulations, 2014

## 20.2.2 Listing of Alien Species Under National Legislation

There are two broad types of regulatory lists in South Africa, namely the prohibited list, which consists of species not yet present in the country, and a list of species which are in the country and need to be managed to reduce their impacts. The latter puts species in categories based on the benefits and the feasibility of control, namely: Category 1a eradication targets; Category 1b—control targets needing a national management plan; Category 2—species requiring a permit for restricted activities (1b outside of permitted conditions—see next section for details); Category 3—species which can remain but need to be phased out (propagation to be prevented). The initial development of the lists of species regulated under national legislation included workshops with taxonomic experts to determine which species should be regulated and how (prohibited, or listed for control). Such workshops that include several experts can be very useful as they can reduce biases that could arise if a single expert was used (Sutherland and Burgman 2015). The inclusion of various stakeholders in these meetings was aimed at reducing conflicts and ensuring that stakeholders' voices are heard. However, in this case, decisions on which species and taxa to list were not based on a structured or transparent process, as no consistent framework for risk analysis was available. Each taxon-specific working group took a slightly different approach to develop recommendations on which species to regulate and how. The final decisions were, of course, taken by policy makers, but it is not clear why (and in some cases how) these decisions differed from the recommendations, as neither process was made publicly available.

Given the lack of transparency of the process leading to the regulation of certain alien taxa in South Africa, stakeholders have raised queries about the species that are regulated. As a result, various retrospective assessments and analyses have been carried out as emergency measures to respond to the criticisms, but none of those followed a framework specifically developed for South African conditions. A framework for decision-making related to the regulation of species needs to consider all aspects of risk and be explicit enough to transparently show the decision-making process and the evidence underpinning it (Roy et al. 2018). The Risk Analysis for Alien Taxa Framework—as described in the previous section—has been developed to this end (Kumschick et al. 2018). Besides the need to assess whether a species is of high risk, management feasibility and benefits of the species need to be assessed to underpin decisions regarding the listing category (Fig. 20.2). The benefits of using such a framework, as opposed to expert opinion alone, are that it leads to more transparent policy which is evidence-based and therefore more defendable. Furthermore, it provides stakeholders with reasons for management implications which should prevent queries from being raised.

## 20.2.3 Permits for Restricted Activities

Restricted activities, as defined in the NEM:BA A&IS Regulations, include, amongst others, possession, breeding, propagating or trading of listed alien species. Some alien species can be extremely harmful to the recipient environment, but at the same time have large benefits for some stakeholders. Such species are generally termed "conflict species" as they often lead to disputes around their management and control (Zengeya et al. 2017). On the one hand, once there is a large enough market for a species it is often difficult to enforce control. On the other hand, in many cases some of the impacts can be avoided and risks mitigated with risk management strategies. For example, keeping pets in escape-safe cages can ensure they do not get introduced into natural areas and cause harm to native species. Similarly, importing only males of certain species can (in most cases) prevent propagation and therefore the establishment of the species in the new area, even should some individuals escape. This issue is tackled with the requirement of permits for certain species (Category 2 listed species under the NEM:BA A&IS Regulations in South Africa; although permits to conduct research or biological control tests can be issued for work on taxa listed in other categories) and the development of permit conditions that mitigate the risks of the species. Each species regulated under national legislation would have gone through a thorough risk analysis process in order to be listed (see above). Therefore permit applications for restricted activities for some species mainly focus on risk management aspects including, for example, the nature and location of the planned activity and the number and sex of individuals to be used. This is similar to requirements for import permits for new alien species (see above). These considerations should be detailed enough to cover risk related to any of the activities involved, including for example transport from breeding facilities elsewhere. Permits already issued and refused for species listed as Category 2 under the NEM:BA A&IS Regulations in South Africa are listed in Table 20.2.

## 20.2.4 Non-regulated Alien Species

Various other activities would benefit from having frameworks and processes in place to prevent unintended negative consequences. This includes for example the commercialisation of alien species present in the country but not (yet) regulated under national legislation. At present, such species can be cultivated and traded without restrictions under the NEM:BA A&IS Regulations (although they are subject to other regulations like the Convention on International Trade in Endangered Species of Wild Fauna and Flora, CITES). Given that propagule pressure plays an important role in the establishment success of species, certain uses could enhance the chances of some species becoming invasive and causing harm (e.g. Kumschick et al. 2016). An example in South Africa to illustrate the potential issue is the "giant flag" project (www.giantflag.co.za), to build a South African flag consisting of colourful desert plants (including alien cacti). The alien cacti initially proposed to be used for this project were not considered as a particularly high risk in South Africa by the project co-ordinator, partly because of their main use as horticultural species and the low propagule pressure related to their use. However, the proposed project involves the planting of millions of cacti in their preferred habitat in South Africa, which changes the risk of these species becoming invasive due to the sheer number of individuals planted (Colautti et al. 2006).

20 Analysing the Risks Posed by Biological Invasions to South Africa 589

Table 20.2 (continued)

## 20.2.5 Release Applications for Biological Control Agents

A separate process to ensure that the introduction and release of classical biological agents for alien plants poses an acceptable environmental risk has been highly efficient (Moran et al. 2005). The levels of risk and protocols followed are based on international best practice, and largely determined by the research community itself. As a result, the process for assessing risks of the deliberate release of biological control agents against various invasive alien plants is very sophisticated and includes the collection of new data and conducting of experiments under quarantine over several years (Klein et al. 2011; for more information on biological control, see Hill et al. 2020, Chap. 19). These experiments include host-specificity tests to make sure the agent only feeds on or attacks the target species to be controlled and no other, closely related native plants and crops. All these experiments take place in secure quarantine facilities which reduces the risk of unintentional release of the species under investigation and allows for the screening of parasites and pathogens on the potential agent. Permit applications for the release of biological control agents, including an estimate of the likelihood and consequences of non-target effects and an assessment on the potential benefits of the introduction, are compiled by a dedicated team of scientists and submitted to the decision making body (in this case chaired by DALRRD). The applications including the risk assessments are then reviewed by an independent panel of experts similar to ASRARP, namely the National Biological Control Release Application Review Committee (Zachariades et al. 2017), and sent for review to international experts. The record of safety is enviable. Despite South Africa being among the top five countries globally with regard to the use of weed biological control, no direct significant non-target effects of weed biological control agents in South Africa have been detected over the past century (Moran et al. 2005).

## 20.3 Conclusions

South Africa's environment and biodiversity need to be protected from the negative impacts of biological invasions (see Le Maitre et al. 2020, Chap. 15; O'Connor and van Wilgen 2020, Chap. 16; Zengeya et al. 2020, Chap. 17). Risk analysis can aid towards reaching this goal insofar as it can help us distinguish the "good" from the "bad" alien species. Furthermore, there are clear economic benefits that come about by using risk analyses to underpin management decisions on alien species (e.g. Keller et al. 2007). This chapter provides guidelines on how to optimise the use of risk analysis to regulate imports and permitting of alien species and to underpin decisions regarding their management.

However, risk analyses have limitations. They can provide important information to prioritise species for management, but risk analyses are not, by themselves, prioritisation tools. Decisions as to which species to manage, and how, depend on the funds available, the costs of management, and many other factors that are not addressed in most risk analyses. Risk analyses are also not equivalent to, and cannot replace, management plans. While risk analyses compile much useful information for the management of a species, pathway, or area, additional information is needed and SMART (Specific, Measurable, Achievable, Realistic, and Timely) goals need to be set for management. Furthermore, as mentioned earlier, desktop-based risk analyses cannot replace detailed assessments of the feasibility of eradication (e.g. Kaplan et al. 2012; Jacobs et al. 2014), but they can provide useful information to aid prioritisation of potential eradication targets. South Africa has historically taken a pragmatic or reactive approach to the issue, but we believe that the solutions provided here offer an opportunity for more transparent and evidence-based decision-making.

Acknowledgements We thank Reuben Keller for his work on approaches to risk assessments, Kim Canavan for advice with biological control risk assessments, and Craig Whittington-Jones for a report on provincial processes related to import applications. We also thank the reviewers for helpful comments. The South African Department of Environment, Forestry, and Fisheries (DEFF) are thanked for funding the South African National Biodiversity Institute noting that this publication does not necessarily represent the views or opinions of DEFF or its employees.

## References

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# Chapter 21 The Extent and Effectiveness of Alien Plant Control Projects in South Africa

Brian W. van Wilgen , John R. Wilson , Andrew Wannenburgh , and Llewellyn C. Foxcroft

Abstract Since 1995, the South African government has spent at least ZAR 15 billion (unadjusted for inflation; approximately USD1 billion) on alien plant control operations across South Africa. The amount spent per year has risen exponentially since 2010, and in 2019 annual spending is around ZAR 2 billion per year. Based on a small (but growing) number of case studies that have assessed management effectiveness, it is clear that the cover of invasive alien plants has been reduced in some localised areas, but continues to grow in others. A number of factors contribute to success, but the effort and resources required for successful control appear to be routinely under-estimated, with actual costs between 1.5 and 8.6 times higher than initial budget estimates. Currently, therefore, control measures (other than biological control) have largely failed to check invasions at a national scale, and there have been no documented eradications of plant invasions from continental South Africa. We argue that control can be considerably improved by effective prioritisation, goal-setting and planning; monitoring of outcomes rather than of inputs;

J. R. Wilson

L. C. Foxcroft

Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

Conservation Services, South African National Parks, Skukuza, South Africa

B. W. van Wilgen (\*)

Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa e-mail<EMAIL_ADDRESS>
Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

South African National Biodiversity Institute, Kirstenbosch Research Centre, Cape Town, South Africa

A. Wannenburgh Department of Environment, Forestry and Fisheries, Cape Town, South Africa

ensuring that the existence of multiple goals does not lead to confusion over priorities; developing methods to reduce the under-estimation of the costs of control; adherence to best practices and standards; simplifying the currently complex contracting and employment models; and using a variety of methods to resolve or reduce conflicts over species that have commercial or other value, but cause significant environmental damage. Addressing these challenges will be difficult, but would be essential if plant invasions in South Africa are to be brought under control.

## 21.1 Introduction

Attempts to control invasive alien plants have a long history in South Africa. While we do not have detailed knowledge of early control efforts, regulations relating to invasive plant management date back to 1861 (see Lukey and Hall 2020, Chap. 18). The first biological control agents were introduced over 100 years ago (Moran et al. 2013). The government made attempts to control pines (Pinus species), gums (Eucalyptus species) and hakeas (Hakea species) in grassland and fynbos areas near Makhanda (Grahamstown) as early as the 1930s (Macdonald 2004). In 1943, operations were introduced to control invasive alien pines, wattles (Australian Acacia species) and gums in the Cape of Good Hope Nature Reserve on the Cape Peninsula (Macdonald et al. 1989). Attempts to control invasive alien plants in the Kruger National Park began in the 1950s (Foxcroft and Freitag-Ronaldson 2007). In 1968, legislation was enacted and an eradication programme initiated against Solanum elaeagnifolium (Satansbos), although eradication was never achieved (Wilson et al. 2013). In 1976, the Department of Forestry scaled up its efforts to control invasive alien plants in the mountain catchment areas in the Western Cape (Fugler 1983; Fenn 1980), but after a decade the programme fell behind schedule, and essentially came to a halt when the responsibility for managing catchment areas was transferred to the provinces in the late 1980s (van Wilgen and Wannenburgh 2016). In 1995, efforts to control invasive alien plants across the whole country were started afresh under the auspices of the Working for Water (WfW) Programme. This public works programme has the dual goals of controlling invasive alien plants while at the same time creating employment and development opportunities for disadvantaged people in rural areas (van Wilgen and Wannenburgh 2016). This chapter reviews the extent to which projects dealing with terrestrial plant invaders have been implemented across the country, and their costs and effectiveness. Chapter 4 (Hill et al. 2020a) discusses progress and challenges relating to the management of aquatic plant invaders.

## 21.2 Alien Plant Control Projects

Many conservation agencies at national and provincial level, private landowners, volunteer "hack" groups, and NGOs have implemented alien plant control projects (Fenn 1980; Attwell 1985; Macdonald et al. 1985; van Wilgen et al. 2017; van Rensburg et al. 2017). However, monitoring data for these efforts were either not available to us, or were never collected in the first place. This section therefore provides a brief summary of the extent of alien plant control projects funded by the WfW programme between 1995 and 2017, both because data are available, and because WfW has provided the bulk of funding for alien plant control projects over the past two decades.

Since 1995, WfW has spent ZAR 15 billion (unadjusted for inflation) on alien plant control operations across South Africa. The amount spent per year has risen exponentially since 2010, reaching around ZAR 2 billion per year in 2017 (Fig. 21.1a). During this time, WfW has cleared an average of about 200,000 condensed ha (Fig. 21.1c) per year, and conducted follow-up operations on about 600,000 ha per year (cleared areas are subjected to an average of three follow-up operations over time). The apparent decrease in area treated since 2014 is due to a relaxation of the requirement to record areas treated. This essentially means that recent figures are underestimates. In terms of the species targeted, wattles received more than three times the funding (ZAR 3.5 billion) than any other taxon (Table 21.1). The other groups on which large amounts have been spent include Lantana camara (Lantana), trees in the genera Prosopis and Eucalyptus, and Chromolaena odorata (Triffid Weed) (Table 21.1). WfW has dual goals, which require it to create employment and to clear invasive alien plants (van Wilgen and Wannenburgh 2016); the programme has created between 2000 and 23,000 fulltime equivalent jobs per year.

Alien plant control operations funded by WfW are carried out by implementing agents who often operate on adjacent land parcels owned or managed by different agencies. Plant invasions, however, do not respect jurisdictional boundaries. To gain control over invasions in any given area, it would therefore be necessary for neighbouring landowners to collaborate closely with each other, and to co-ordinate control efforts, which brings additional challenges. Box 21.1 profiles case studies where alien plants are managed in large areas across several jurisdictions to illustrate challenges and achievements.

Fig. 21.1 The contribution of the Working for Water programme to alien plant control in South African in terms of: (a) the amount of money invested (ZAR unadjusted for inflation); (b) the number of full-time equivalent jobs created. This number only includes jobs created for previously unemployed people as part of poverty alleviation efforts; (c) the area treated per annum in condensed ha (see Table 21.1 for a definition of condensed ha). Note that the apparent decrease in area treated between 2013 and 2014 is due to a relaxation of the requirement to record areas treated. Data sourced from Working for Water Information Management System

21 The Extent and Effectiveness of Alien Plant Control Projects in South Africa 601

100 ha ¼ 50 condensed ha), based on data from cVersfeld et al. (1998) and dKotze et al. (2010) except where otherwise specified. Note that the survey by Kotze et al. (2010) excluded most of the arid parts of South Africa (i.e. the Karoo, Grassland and arid Savanna Biomes in the west of the country).

bQDGCs quarter degree grid cells; QDGC data are from Henderson and Wilson (2017)

1Acacia mearnsii; 2Acacia saligna; 3Acacia cyclops; 4Acacia dealbata; 5Acacia decurrens; 6Cylindropuntia fulgida; 7Cylindropuntia imbricata; 8Opuntia engelmannii; 9Opuntia ficus-indica; 10Opuntia humifusa; 11Eucalyptus camaldulensis; 12Pinus pinaster; 13Pinus radiata; 14Populus alba/canescens; 15Populus deltoids; 16Prosopis glandulosa; 17Prosopis hybrids

#### Box 21.1 Co-ordinating Alien Plant Control Across Jurisdictions: Three examples from Biosphere Reserves in South Africa

Implementing effective alien plant control projects is difficult enough on individual protected areas or farms, but the complexity increases exponentially when an invasion occurs across multiple land parcels, owned or managed by different individuals or organisations, each with different purposes and levels of capacity. For the management of invasive alien plants to be effective, collaboration across different land parcels is needed. Biosphere reserves are a good model for how this can be achieved. Biosphere reserves are areas of terrestrial and coastal ecosystems that are internationally recognised within the framework of the United Nations Education, Scientific and Cultural Organisation's (UNESCO's) Man and Biosphere programme. Biosphere Reserves have core, buffer and transition zones that cater for strict conservation, limited sound ecological use, and ecologically-friendly development respectively. South Africa has eight Biosphere Reserves, and within some of these there have been attempts to co-ordinate alien plant control projects. An examination of three of these Biosphere Reserves (table below) reveals some common features:

## 21.3 Alien Plant Eradication Projects

The Working for Water programme (WfW) explicitly took an area-based, as opposed to a species-based, approach to management (see Faulkner et al. 2020, Chap. 12, for a discussion on pathway-based approaches). Invaded areas were demarcated, estimates of the overall density of all alien plants in those areas were made, and contracts issued to clear all the alien plants in the specified areas. Classical biological control aside, individual species were not explicitly targeted. To address this gap, in 2008, the South African National Biodiversity Institute (SANBI) was contracted by WfW to develop species-specific control programmes focusing on alien plant species that were not yet widespread invaders (Wilson et al. 2013). Over time, this mandate has narrowed so that the focus of control efforts is on species where the possibility of national-scale eradication has not been ruled out (see Sect. 21.6 for a discussion of species-specific management programmes where the goal is not eradication).

There have been several documented plant eradication attempts in continental South Africa, all initiated by the government, but none of which succeeded (cf. work on the sub-Antarctic Islands, Greve et al. 2020, Chap. 8). Intensive programmes were initiated in the early 1960s to remove Alhagi camelorum (Camel Thorn) from irrigation schemes. However, the systemic herbicides available at the time were ineffective for dealing with the extensive underground root systems (Erasmus and Viljoen 1993; Jooste 1965). In 1968 an eradication programme was initiated against Solanum elaeagnifolium (Satansbos) (Wasermann et al. 1988). Despite some local successes, by 1972 the eradication campaign was cancelled; failure was ascribed to inadequate biological knowledge, ineffective herbicides and application techniques, and a lack of cooperation from many farmers. The most extensive eradication campaign in South Africa was against Opuntia aurantiaca (Jointed Cactus) (Moran and Annecke 1979), but despite significant governmental support, apparently not a single farm was fully cleared.

These efforts focussed on alien plants that were already widespread in the country, and basic requirements to achieve eradication were not always in place, e.g. no new immigration of propagules, all populations delimited, sufficient resources available to complete eradication, and adequate monitoring and evaluation in place (Wilson et al. 2017).

There are 42 alien plant species listed as Category 1a in South Africa's Alien & Invasive Species Regulations, published in 2014 under the National Environmental: Biodiversity Act (NEM:BA, Act 10 of 2004) (i.e. deemed as nation-wide eradication targets). On investigation, several of these species have been found to be present at many sites across the country (e.g. Iris pseudacorus (Yellow Flag) (Jaca and Mkhize 2015), and Furcraea foetida (Mauritian Hemp), although the formal process of documenting the evidence and transfer of these species to more appropriate management categories has not been completed yet (see Chap. 20; Kumschick et al. 2020). Several of the Category 1a species [Cabomba caroliniana, (Cabomba) and Euphorbia esula (Leafy Spurge)] have not been found again, and might simply not be in the country, while others are not known to have become invasive and were listed for precautionary purposes (Henderson and Wilson 2017). Several of the species are found in private gardens [e.g. Triplaris americana (Ant Tree)]. While this does not preclude eventual eradication, it complicates both control efforts and our ability to declare a species eradicated. A few Cactaceae species have (or will likely in future have) effective biocontrol agents, such that nation-wide eradication would probably not be required for adequate control to be effected. Consequently, only around a third of the species listed in Category 1a are still the focus of on-going eradication efforts. By contrast, many other taxa that are not yet listed in the regulations have been identified as eradication targets and are subject to control efforts [e.g. Acacia viscidula (Sticky Wattle), and Melaleuca parvistaminea (Rough-barked Honey Myrtle) (Magona et al. 2018; Jacobs et al. 2014)].

The mismatch between legal status and feasibility of eradication discussed above highlights the need to set eradication as the management goal only once a formal detailed assessment of eradication feasibility has been conducted. Such assessments require investment in delimitation and pilot control measures (Wilson et al. 2017). It is also clear that there is a substantial invasion debt in the country (Rouget et al. 2016)—many alien plants have only naturalised or invaded a few sites, and there are likely to be many that are still to be detected.

In the decade that the SANBI programme has been active, no alien plant species had been formally declared as eradicated. The project closest to achieving eradication is probably that against Spartina alterniflora (Smooth Cordgrass), a grass invading the Knysna estuary in the Western Cape. However, the conditions under which eradication can be declared have not been specified, nor is it clear why the plant was introduced in the first place, so the possibility of reintroduction has not been ruled out (Riddin et al. 2016). Detailed point patterns have been produced for a number of species (Wilson et al. 2013), and insights have been gained in terms of efforts to delimit populations (Jacobs et al. 2014), produce risk maps (Kaplan et al. 2014), estimate the costs of eradication (Moore et al. 2011), and the continuing need for morphological and molecular taxonomy (Magona et al. 2018; Jacobs et al. 2017).

The SANBI programme has funded postgraduate students to work on particular species or taxa, and produced an increasing number of published analyses of risk analyses, impact assessments, and estimates of eradication feasibility (Kumschick et al. 2020). However, the programme has suffered from similar issues to other projects funded under the WfW umbrella. The onus has been to report on input indicators (e.g. person days of employment), and few or no data are routinely collected on output indicators (e.g. the number of plants present). When assessed against the requirements set by the National Status Report on Biological Invasions (van Wilgen and Wilson 2018), the project planning was evaluated as being inadequate across the board. These are solvable issues, but will require a shift in approach to ensure that dedicated teams focus on specific targets year on year, that data are collected, and that monitoring data feed back into decision-making both at a project level and as input to the regulatory changes. If the global best practices regarding alien plant incursion response are applied (e.g. Wilson et al. 2017), then we can expect to see an increasing number of declared alien plant eradications in the next decade. For some taxa, particularly those with long-lived seed-banks (Zenni et al. 2009; Wilson et al. 2011), eradication might only be achieved far in the future, but it is feasible given persistence and effective monitoring.

## 21.4 Management Plans for Invasive Species

South Africa's National Environmental Management: Biodiversity Act (NEM:BA), Alien & Invasive Species (A&IS) Regulations, published in 2014, state that "if an Invasive Species Management Programme has been developed in terms of section 75 (4) of the Act, a person must control the listed invasive species in accordance with such programme". In many cases, the need for species-specific management programmes is clear, even for species where eradication is not feasible, but neither the Act nor the Regulations, provide guidance on which of the listed invasive species should be the subject of such a programme. The development of national-level, species-specific programmes for all listed species would be extremely onerous, but there has been little to no progress even on priority species. Species-specific strategies have been developed only for Parthenium hysterophorus (Parthenium Weed), and Campuloclinium macrocephalum (Pompom Weed) (Le Maitre et al. 2015; Terblanche et al. 2016; see also Table 21.1). These strategies recommended different management approaches for different administrative areas depending on the stage of invasion. In addition, two genus-level strategies [for Australian Acacia species and Prosopis (van Wilgen et al. 2011; Shackleton et al. 2017)], and one family-level strategy (for Cactaceae, Kaplan et al. 2017) have been developed.

None of these strategies has been formally adopted to date, and no entities have been established, as provided for in law, to co-ordinate and implement them (though the aim of the National Cactus Working Group is to facilitate the implementation of the Cactaceae strategy; Kaplan et al. 2017).

## 21.5 Management Plans for Invaded Areas

The successful implementation of invasive alien plant control projects relies on, among other things, careful planning that sets realistic goals, monitoring of progress towards those goals, and adapting management as new information comes to light. In South Africa, there are a number of statutory requirements to develop such plans. The management authorities of protected areas, and all other organs of state in all spheres of government are required in terms of the NEM:BA A&IS Regulations to prepare invasive alien species control plans; and in terms of the National Environmental Management: Protected Areas Act (Act 57 of 2003, NEM:PAA), the management authorities of all protected areas must submit a management plan for the protected area for ministerial approval. In turn, plans require accurate information on the extent and abundance of invasive species, so that the resources required to control them can be reliably estimated. These requirements have not been adhered to in practice, however. In terms of the NEM:BA requirement, submitted control plans covered only about 4% of the country, mainly in the Western Cape, and almost all of the plans failed to meet the required criteria (van Wilgen and Wilson 2018). Both the relatively small number of plans, and the inadequacy of many plans, was attributed to a lack of capacity or expertise within many organs of state (van Wilgen and Wilson 2018). Furthermore, while most protected areas have prepared management plans as required by NEM: PAA, the sections of these plans that deal with alien plant control are typically highlevel, long-term statements of intent, and these have not been effectively carried forward into the more detailed medium to short-term plans that would be necessary for guiding control operations (van Wilgen et al. 2017).

Creating accurate maps of the distribution and abundance of alien plant invasions as a basis for realistic planning has also proved challenging up to now (Richardson et al. 2020, Chap. 3). At a national scale, there have been at least three attempts to map the extent of the problem. In 1993, the Council for Scientific and Industrial Research mapped invasive alien plants in South Africa, with the goal of estimating their impact at a national scale (Le Maitre et al. 2000). The mapping techniques used were coarse due to the paucity of reliable data, but a map at a 1:250,000 scale was produced, based primarily on the local knowledge of natural resource experts from across South Africa. The project estimated that invasive plants occupied 10.1 million ha (6.82% of South Africa and Lesotho). The longest-running project aimed at recording information on the national extent of alien plants is the Southern African Plant Invaders Atlas (SAPIA), which was initiated in 1994 (Henderson 2007). As of May 2016, SAPIA had over 87,000 geo-referenced records for 773 alien plant taxa that are present outside of cultivation in southern Africa, making it the most extensive source of information on the distribution of invasive plants in the region (see Richardson et al. 2020). In 2008, the Department of Environmental Affairs commissioned the Agricultural Research Council to develop and implement a repeatable sampling protocol to track trends in alien plant distribution and density across half of the country. This project has run for more than a decade, and has mapped the distribution of 27 alien plant taxa (species in the genera Pinus, Eucalyptus and some Australian Acacia species were mapped collectively). The project is ongoing, but no adequate description of the sampling methodology has been published to date, nor have any peer-reviewed papers that present the findings been published.

At finer scales, relatively detailed maps of the extent of invasion have been developed for some areas, mostly protected areas [e.g. Foxcroft et al. (2004, 2009) for Kruger National Park; Cheney et al. (2018) for Table Mountain National Park; and van Wilgen et al. (2016) for protected areas in the Cape Floristic region]. Cheney et al. (2018) compiled a map of invasive alien plants derived from fine-scale systematic sampling of the entire Table Mountain National Park (26,500 ha), and compared this to two other datasets in use for planning and management. They found that management datasets overestimated species cover by orders of magnitude, and that this resulted in questionable allocations of funding. They concluded that "contrary to perception, fine-scale surveys are a cost-effective way to inform long-term monitoring programmes and improve programme effectiveness". In addition, where plans are developed, they are not always followed (Kraaij et al. 2017). It appears, thus, that the level of planning for alien plant control in South Africa falls substantially short both of what is required by law and what is necessary for management to be effective.

# 21.6 National-Scale or Species-Specific Assessments of Management Effectiveness

The most comprehensive national-scale assessment of management efficacy at a species level to date (Henderson and Wilson 2017) was based on the Southern African Plant Invaders Atlas (SAPIA). The 773 alien plant taxa recorded in SAPIA was an increase of 172 taxa over the last assessment in 2006 (Henderson and Wilson 2017). Between 2000 and 2016 there was also an approximately 50% increase in the broad-scale documented range of alien plants in SAPIA. Several species (Campuloclinium macrocephalum, Parthenium hysterophorus, Opuntia engelmannii, Cryptostegia grandiflora, Pennisetum setaceum, Tecoma stans, Sagittaria platyphylla, Gleditsia triacanthos, and Trichocereus spachianus) were considered to be of particular concern as they had increased substantially in distribution over the past decade. Henderson and Wilson (2017) reported further that approximately 126 taxa were targeted for clearing by the Department of Environmental Affairs' Natural Resource Management (NRM) programmes (formerly "Working for Water") between 2000 and 2012, although most effort was focussed on a relatively small number of widespread taxa (Table 21.1). Examination of the data suggested that whether a species was targeted for control or not made little difference, as both targeted and neglected species continued to spread at comparable rates. Henderson and Wilson (2017) concluded that this outcome was perhaps not surprising, given the lack of evidence of a general strategic approach to NRM's activities, and the absence of dedicated strategic efforts to contain specific invasive plants, or to reduce the rate at which they invade particular areas. By contrast, they found a clear signal that biological control had reduced rates of spread of several important invasive alien plant species. Notably, however, SAPIA was not designed as a tool to monitor management effectiveness, but rather as a means of collating information on alien plant distributions and how that distribution has changed over time. For reliable assessments of management efficacy over time, SAPIA would need to be augmented by monitoring specifically designed for this purpose. There have been few examples of such monitoring to date.

A species-specific study on the integrated control of Hakea sericea (Sweet Hakea) was conducted in the Western Cape by Esler et al. (2010). The control included a combination of felling and burning, augmented by biological control (van Wilgen et al. 1992). Data from two surveys, 22 years apart, suggested that the distribution of the species was reduced by 64%, from ~530,000 to ~190,000 ha between 1979 and 2001. The species either decreased in density, or was eliminated from 492,113 ha, while it increased in density, or colonised 107,192 ha. It was concluded that the initial mechanical clearing, integrated with the judicious use of prescribed burning, in the 1970s and 1980s by the then Department of Forestry (van Wilgen et al. 1992) was responsible for reducing the density and extent of infestations, and that biological control was largely responsible for the failure of the species to re-colonise cleared sites, or to spread to new areas following unplanned wildfires (Hill et al. 2020b, Chap. 19, Sect. 19.3). Between 2000 and 2015, H. sericea increased its occurrence in quarter degree grid cells from 77 to 85, an increase of 10% (Henderson and Wilson 2017). During the same period, the ecologically similar pine trees [Pinus pinaster (Cluster Pine) and P. radiata (Monterey Pine), for which no biological control is available] increased from 85 to 108, and from 70 to 95 QDGCs, or 27% and 21% respectively.

Marais et al. (2004) reported that good progress had been made with clearing certain species (at a cost of ~ZAR 2.3 billion between 1996 and 2004, costs unadjusted for inflation), but also that at current estimated rates of clearing, many of the targeted species would not be brought under control within the next half century. They stressed that their estimates were preliminary, given the incomplete data on the project management system. In 2012, van Wilgen et al. (2012) reported that control operations were in many cases only applied to a relatively small portion of the estimated invaded area (2–5% depending on the species), despite substantial spending (ZAR 3.2 billion in 2012 values).

## 21.7 The Effectiveness of Management in Selected Areas

## 21.7.1 Monitoring of Control Effectiveness

The effectiveness of control measures in a particular area (for example a protected area, a catchment area, a farm, or a stretch of river) needs to be assessed against the goal of the management, with such assessments based on regular monitoring of outcomes. However, while almost all alien plant control projects in South Africa have an implicit goal of reaching a "maintenance level", this goal is seldom stated explicitly in terms of the desired final extent or density of invasion (van Wilgen et al. 2016; Fill et al. 2017). The concept of a maintenance level recognises that, for most invasions, eradication is infeasible, but that invasions can be reduced to a level where the negative impacts are negligible and control costs are relatively low in perpetuity. In the vast majority of South Africa's government-funded alien plant control projects, the indicators used to monitor progress and set targets include the amounts of money to be spent, the number of people to be employed, and the areas to be treated. These are input or output indicators, rather than outcomes in terms of changes in the levels of plant invasions (Wilson et al. 2018). In the absence of a monitoring programme that is focussed on outcomes, it is difficult to assess effectiveness objectively. However, several studies have been conducted, particularly over the past decade, in which the effectiveness of management has been assessed, and these are summarised here. These studies provide a limited basis from which to derive broad conclusions about the effectiveness of control measures.

# 21.7.2 Alien Plant Control Projects in the Cape Floristic Region

Most studies addressing the effectiveness of alien plant control measures in South Africa have been carried out in the Cape Floristic Region (CFR) in the Western and Eastern Cape provinces. The natural vegetation of the CFR comprises fynbos shrublands, and the most prominent invasive species are trees and shrubs (Australian Acacia, Hakea, and Pinus species in particular). Historical costs for control in CFR protected areas between 1996 and 2015 amounted to ZAR 564 million (2015 values; van Wilgen et al. 2016), additional amounts spent outside of formally protected areas. When assessed at the scale of individual projects, there is clear evidence that progress has been made. Macdonald et al. (1989) recorded marked declines in cover of all alien species in the Cape of Good Hope Nature Reserve following the implementation of a systematic clearing plan in the 1970s. Similar declines were recorded in the Berg River catchment (Fill et al. 2017; Fig. 21.2), the Vergelegen Estate (van Rensburg et al. 2017; Fig. 21.3), and along the Rondegat River (Fill et al. 2018, see Sect. 21.9). In the Hawequas mountains, where control focussed on the removal of abandoned pine plantations, McConnachie et al. (2016) estimated that the cover of invasive trees would have been almost 50% higher had there been no control. They also concluded that control might have prevented a larger area from being invaded if it had focussed all of its effort on untransformed land, and not on abandoned plantations. However, the costs associated with many of these projects were much higher than originally estimated. McConnachie et al. (2012) concluded that the cost to clear the Krom and Kouga

Fig. 21.2 Area occupied by alien Pinus and Acacia trees at different levels of cover in the upper Berg River catchment at the initiation of a control project in 2001, and after 13 years of treatments in 2014. Cover levels are dense (>50% cover), medium (26–50% cover), low (6–25% cover) and scattered (0.5–5% cover). Figure redrawn from Fill et al. (2017) with permission

Fig. 21.3 Area occupied by invasive plants in six cover classes at Vergelegen Wine Estates in 2004 and 2015. The classes are occasional (<1% cover); very scattered (1–5% cover); scattered (5–25% cover); medium (25–50% cover); dense (50–75% cover); and closed (>75% cover). Figure redrawn from van Rensburg et al. (2017) with permission

catchments in the Eastern Cape was 2.4 times higher than the highest equivalent estimate made elsewhere in South Africa at the time. The cost to clear the Berg River catchment was estimated at ZAR 6 million in 1996 (2016 ZAR values; van Wilgen et al. 1997), but by 2016 the actual cost had reached ZAR 50 million (2016 ZAR values), 8.3 times the original estimate, without having reached a maintenance phase (Fill et al. 2017). Similarly, on privately-owned land at Vergelegen Estate, operations cost 3.6 times more than was originally estimated (ZAR 43.6 vs. 12.19 million respectively; van Rensburg et al. 2017). Much of this problem can be attributed to regular unplanned wildfires which necessitate large amounts of follow-up to clear seedlings that appear in dense stands after wildfires. However, in some cases, the additional costs may well be due to management inefficiencies. For example, McConnachie et al. (2012) found significant inefficiencies in the Krom and Kouga catchments, in the form of inaccurate records, where 25% of the areas recorded as having been cleared had in fact not been cleared; and Kraaij et al. (2017) found that the quality of many treatments in the Garden Route National Park was inadequate, with work done to standard in only 23% of the assessed area. The prognosis for gaining control of alien plant invasions in the CFR's protected area network was investigated by van Wilgen et al. (2016). The study concluded that, for scenarios in which control measures continued against all invasive plant species, the estimated required funding to achieve the goal of reducing invasions to a manageable level was up to 4.6 times greater than the amount spent over the past 20 years. Under many plausible future scenarios (for example 8% spread and current or reduced funding) the invaded area would continue to grow.

# 21.7.3 Management of Prosopis Species in the Northern Cape

Trees in the genus Prosopis (Mesquite) were introduced to provide a source of fodder for livestock in the arid areas of South Africa, and subsequently became invasive. Historical estimates for the rate of spread of Prosopis trees in South Africa ranged from 3.5 to 18% per year (van den Berg 2010; Wise et al. 2012), which implied that the invaded area could double every 5–8 years. In the Northern Cape, the estimated total invaded area increased by almost a million hectares between 2002 and 2007, which is equivalent to 27.5% per year, and this occurred at a time during which ZAR 390 million (2012 values) was spent on control (van Wilgen et al. 2012). A more recent update (RT Shackleton unpubl. data) found that the public works clearing projects had treated 203,000 ha of the area invaded by Prosopis between 2000 and 2015. Each site also received on average 2.7 follow up clearings. The cost of these measures amounted to ZAR 1.8 billion (unadjusted for inflation) over the same period. The project started in 1995, but cost estimates prior to the year 2000 are not available. Between 2000 and 2016, Prosopis glandulosa (Mesquite), and Prosopis hybrids increased their range from 40 to 112, and 390 to 481 quarterdegree grid cells, increases of 180% and 23% respectively (Henderson and Wilson 2017), suggesting that control is doing little to stop the spread of these trees.

# 21.7.4 Invasive Plant Control in the Kruger National Park (Mpumalanga and Limpopo Provinces)

Van Wilgen et al. (2017) provided a recent review of alien plant control in the Kruger National Park (KNP). There have been attempts at control in the KNP since the mid-1950s, but in the late 1990s these attempts were broadened, and between 1997 and 2016, over ZAR 300 million was spent on invasive alien plant control. Good progress was made with the control of several species, notably Sesbania punicea (Red Sesbania), Opuntia stricta (Australian Pest Pear), Lantana camara (Lantana) and two species of invasive alien aquatic plants. In all of these cases, progress with reducing populations of the invasive species was due to biological control. Nonetheless, much effort was also directed towards species that were subsequently recognised as being of lower priority. For example, 38% of available funds was spent on alien annuals between 1997 and 2016. Funds were sometimes directed towards these annuals to meet the goals of employment creation in areas where priority species were not present. The absence of documented assessments of the potential impact of various species also allowed managers to base their decisions on perceptions of the relative impact of candidate species. In addition, because management goals were focussed on inputs (funds disbursed, employment created) or outputs (area treated), there was a lack of monitoring the ecological outcomes of control operations.

# 21.7.5 Control of Chromolaena odorata in the HluhluweiMfolozi Park, KwaZulu-Natal

In 1978, managers of the 90,000 ha Hluhluwe-iMfolozi Park (HiP) in KwaZulu-Natal first noticed the presence of the alien shrub Chromolaena odorata (Triffid Weed). By 2003, this species had increased in extent and covered almost half of the HiP (Dew et al. 2017). A concerted control programme was then implemented at a cost of ZAR 103 million, and by 2011 the invasions were reduced to acceptably low levels (Fig. 21.4). The success came about because the management team applied several aspects of best practice, including a dedicated "rapid response" team, the integration of fire and mechanical clearing, a focus on areas of low infestation, flexibility with regard to the deployment of teams, regular monitoring and generous funding. In addition, te Beest et al. (2017) reported that "the team was only paid following completion of a contract and after a thorough inspection of the quality of the work by the Project Manager". Many other control projects in South Africa unfortunately did not incorporate these features, and this may well account for the differences in success. This programme essentially focussed on a single species, and the control of other invasive taxa in the HiP was not documented.

Fig. 21.4 Area invaded by Chromolaena odorata (Triffid Weed) in Hluhluwe-iMfolozi Park, and areas cleared and followed up between 2000 and 2013. Figure redrawn from te Beest et al. (2017) with permission

# 21.8 Managing Conflict Species

## 21.8.1 Conflict Species in South Africa

Conflict-generating invasive alien species are defined as species that have relatively high value for some people, while at the same time being capable of invading natural vegetation and generating high levels of negative impact (van Wilgen and Richardson 2014; Zengeya et al. 2017). There are several prominent examples of such species in South Africa (Table 21.2). The management of species that fall into this category is complicated because opposing value systems have to be accommodated. In South Africa, this issue has been addressed in a number of ways, discussed in the sections below.

## 21.8.2 Catering for Conflict Species in Regulations

Species listed as invasive in South Africa's A&IS Regulations have to be controlled, and may not be cultivated or traded. However, permits will be granted for some species (listed as Category 2) that have commercial value. These can be cultivated and traded under permit, but the permit-holder can be held liable for spread of the species. Some listed invasive species may be exempted from control requirements if there are many individual plants that have significant ornamental value (Category 3). These individual plants may be retained (e.g. in gardens), but may not be further cultivated, traded, or replanted (i.e. the species are phased out rather than attempting to actively remove them from private property). It is currently unclear whether or not these regulatory approaches are effective (van Wilgen and Wilson 2018).

# 21.8.3 Using Biological Control Agents to Reduce Seed Output

Proposals for the control of invasive Australian Acacia species were initially strongly resisted by the wattle industry (Stubbings 1977). Ecologists working in the field of biological control subsequently proposed the use of seed-feeding and gall-forming agents for these trees, and these were released following protracted negotiations with representatives of the wattle industry. These agents have been markedly successful in reducing seed output (Moran and Hoffmann 2012), and have substantially slowed the spread of these species in many areas (Henderson and Wilson 2017; Hill et al. 2020b, Chap. 19).

## 21.8.4 Using Sterile Cultivars

The use of sterile cultivars (for example in the case of Pinus and Australian Acacia species used in commercial forestry) is sometimes proposed as a solution to the problem of invasions that originate from commercial plantations, but there are no documented cases of where this has been successful in South Africa. It has also been shown that large reductions in fecundity do not necessarily adequately reduce the population growth rates of long-lived species, which remain an invasion threat (Knight et al. 2011). In addition, while modern technologies such as genetic modification may be used to develop sterile varieties (Miao et al. 2012), forestry companies stand to lose environmental certification status as certifying bodies prohibit the use of genetically modified organisms (van Wilgen and Richardson 2012). Similarly, the use of sterile cultivars of horticultural species has been proposed as a means of reducing conflicts. There are, however, still several open research questions as to the nature and stability of sterility required to sufficiently reduce the risk, and whether sterility on its own would be sufficient to prevent invasions (Richardson and Petit 2005).

## 21.9 Returns on Investment from Control Measures

The economic costs of plant invasions, and the economic benefits of control, have also been the subject of a few studies in South Africa. One study (De Lange and van Wilgen 2010) suggested that the cost of some impacts (lost water, grazing and biodiversity) was currently about ZAR 6.5 billion per annum, but would become much higher as invasions grow. In the case of biological control of invasive plants, all studies have estimated very high returns on investment. By comparing the costs of biological control research and implementation to the benefits of restored ecosystem services, or avoided ecosystem degradation, and avoided ongoing control costs, biological control was shown to be extremely economically benefitial, with estimated benefit:cost ratios ranging from 8:1 up to 3726:1 (van Wilgen and De Lange 2011).

To estimate a return on investment from mechanical and chemical alien plant control measures, it would be necessary to know both the historic cost of control, and the value of impacts avoided due to control. There are no reliable estimates of the value of impacts avoided due to control. It is well known, though, that the cost per unit area to control an invasion rises exponentially as the density of the invasion increases (Marais et al. 2004). If invasions can be contained while they still occupy a smaller area, at relatively low densities, returns on investment from control operations should be positive. At some point, as yet unquantified, the cost of effective control would exceed the cost of the impact, and attempts to mechanically or chemically control invasions at this stage would deliver negative returns on investment (Fig. 21.5). More research is needed on this aspect to gain a better understanding.

Fig. 21.5 Hypothetical representation of increases in the costs of impact, and the costs of control, associated with alien tree invasions. The cost of control increases exponentially as the invaded area and the density and size of trees increase. Control becomes economically unsustainable at the point at which the costs of control are exceeded by the costs suffered as a result of invasion (From van Wilgen and Richardson 2014). There are, of course, many other potential forms of these relationships—impact is often negligible at low densities, but rises exponentially once a threshold has been passed, while there are often fixed costs to controlling an area (related e.g. to issues of access and the minimum size of a control team). Of particular concern is that in general by the time an invasion has very obvious impacts, the cost of control is already several fold greater than the cost of pre-emptive management. If control costs vastly exceed impact costs (as per the far right of the graph), it has been proposed that control should not be attempted, and focus should rather be placed on deriving benefits from such "novel ecosystems". There are, however, various criticisms of this concept, e.g. that it might encourage managers to give up when it would be preferable to implement control

There have been mixed findings regarding returns on investment from alien plant control projects. In a cost-benefit analysis of six sites in the Eastern Cape, Hosking and Du Preez (2004) concluded that "catchment management on all the sites carried out by the Working for Water Programme is inefficient"; benefit:cost ratios ranged between 0.03 and 0.75, indicating negative returns on investment, although though the benefits of associated employment creation were not included. By modelling the spread of alien plants and their effects on water runoff, with and without attempts at control, in the Western Cape's Berg River catchment, van Wilgen et al. (1997) concluded that such control would be "effective and efficient". The estimated delivery cost of water, with and without the management of alien plants, was 57 and 59 c kl-<sup>1</sup> respectively. The projected clearing costs used in arriving at this estimate were around ZAR 180,000 per year for initial clearing over 10 years, followed by about ZAR 25,000 per year for maintenance thereafter (1997 ZAR values). The actual costs eventually amounted to almost ZAR 50 million by 2015 (2015 ZAR; 8.3 times greater than the net present value of costs estimated in 1997, Fill et al. 2017). Despite considerable reductions in the cover of alien plants by 2015, the invasions were still present over much of the area, albeit at reduced densities. The outcome that was projected in 1997 had therefore not been realised, because control methods were not effectively applied, and because the control costs were underestimated (Fill et al. 2017).

Finally, the potential returns on investment from invasive plant control operations have been the subject of several recent studies that compared the outcomes of various management scenarios (Vundla et al. 2016; Mudavanhu et al. 2016; Morokong et al. 2016; Nkambule et al. 2017). The scenarios included different rates of spread, included or excluded value-added products using biomass from invasive plants, and included or excluded private sector co-funding. The inclusion of co-funding and value-added products delivered more favourable returns on investment, and a failure to intervene at all would deliver negative outcomes. These operations could therefore be financially viable, but the accuracy of the predictions depends on whether or not the underlying assumptions will hold. These assumptions include that effective and professional clearing would continue into the future; that co-financing would be available; that due compensation for the services rendered and the value-added products produced would be realised; that the extent of the invasions was accurately known; and that the costs had been accurately estimated. Most, or even all, of the above assumptions will not hold, however, because alien plant invasions are rarely accurately mapped (see, for example, Cheney et al. 2018); the costs of control are routinely under-estimated by a factor of 3–7 times; there are low levels of efficiency associated with control work; and including value-added products could lead to unintended consequences. Consequently, there can only be a low level of confidence in these predictions of the return on investment from control projects.

## 21.10 Synthesis

There are a number of points that can be made with regard to the effectiveness of mechanical and chemical control measures. Firstly, as widespread invasions by alien plants can bring about substantial costs, it would obviously be beneficial to reduce invasions as far as possible. In South Africa, the largest proportion of funding for control operations comes from the Working for Water programme (WfW) within the Department of Environmental Affairs. Between 1995 and 2017, WfW spent ZAR 15 billion (unadjusted for inflation) on alien plant control, but this has only been enough to deal with between 2 and 5% of the estimated extent of invasions each year, and so the most important invasive species continue to spread (van Wilgen et al. 2012; Henderson and Wilson 2017).

Control interventions have nonetheless succeeded in reducing the extent of invasions in some areas. Early work demonstrated that the systematic implementation of a careful plan resulted in the reduction of populations of invasive alien trees and shrubs to maintenance levels (Macdonald et al. 1989). Where concerted efforts have been made to remove invasive trees from fynbos catchment areas, marked declines in the density have been achieved (Fill et al. 2017; van Rensburg et al. 2017). One estimate (McConnachie et al. 2016) suggested that the invaded area in the fynbos-clad Hawequas mountains would have been almost 50% higher if control operations had not been carried out. Ongoing control has also reduced the extent of invasions of several species in savanna ecosystems, including Lantana camara, Opuntia stricta, and Chromolaena odorata (van Wilgen et al. 2017; Dew et al. 2017; te Beest et al. 2017). At several localised sites, therefore, control measures have been effective. The picture changes when progress is assessed at a national scale, however, because plant invasions have generally continued to grow, some substantially (Henderson and Wilson 2017). Meaningful progress in reducing widespread invasions to a maintenance level, therefore, can arguably only be made if the available funding is focused on priority sites and species (Box 21.2). Essentially, the conscious practice of conservation triage (Bottrill et al. 2008) will need to be introduced, and this will require agreement on which species, and which areas, to target for control. Because alien plants spread more rapidly than they are being removed, current control efforts could fail if funds are spread too thinly, as suggested by modelling exercises (Higgins et al. 1997; van Wilgen et al. 2016). If adequate funding were re-directed to agreed priority areas, then the chances of achieving control in those areas would increase. Similarly, by focussing on priority species, scarce funds could be concentrated where they would be most effective. For example, funding for the control of Pinus and Australian Acacia species in fynbos is divided equally between these two taxa (van Wilgen et al. 2016). Pinus species, however, will eventually cover a much larger area than Acacia species if allowed to spread. If funds were diverted from Acacia species (which are under more effective biological control) to Pinus, then the eventual outcome would be far more favourable. Although prioritisation studies have already been initiated (e.g. Forsyth et al. 2012), it is going to be challenging to get managers to accept the need for triage, because terminating projects where funds have already been expended will understandably meet with resistance (see also Foxcroft et al. 2020, Chap. 28, Sect. 28.7). In conclusion, the implementation of focused, well-funded and well-managed control measures should bring invasions down to a maintenance level in many priority areas. Such interventions should bring very attractive returns on investment, but they will require some fundamental changes to the current modus operandus.

#### Box 21.2 Wisdom from the Past

Alien plant control has been considered, and practiced, in South Africa for many decades. The question arises as to whether we can learn from this experience. Two quotes, in particular, seem relevant.

In his report on the conservation of the vegetation of the Cape Floristic Region, Prof. C.L. Wicht noted that "it seems, at present, that unless enormous sums of money are expended on their [invasive alien plant] eradication or control they will become dominant everywhere except in nature reserves and other selected areas where they will constantly be destroyed"

#### Box 21.2 (continued)

(Wicht 1945). There are two important aspects to this quote. First, there was an assumption that attempts to bring alien plant invasions down to maintenance levels would focus only on protected areas, and second, that a focus on protected areas would be the only way in which at least a representative portion of the unique Cape vegetation could be retained. In essence, this was an early call for the need to practice conservation triage. This concept (whereby some invaded land is abandoned to invasions, with control focussing on areas where progress can be made) has recently re-emerged (Bottrill et al. 2008; van Wilgen et al. 2016), but is controversial.

In the 1970s, the Department of Forestry embarked on an ambitious campaign aimed at eliminating invasive alien Hakea shrubs from vast areas in the southwestern mountains of what was then the Cape Province. John Fenn, regional director of forestry in the Western Cape, noted in 1980 that "By using new methods and techniques, the brush-cutter became the most useful and effective machine for these operations. The costs of eradicating dense areas of Hakea dropped dramatically. Labour units used per hectare dropped from 22 to 5, and in certain areas, dropped as low as 1.5 units per hectare. All of a sudden the clearing of these vast areas of Hakea no longer looked impossible" (Fenn 1980). This is a clear indication that mechanised techniques are essential if the goals of reaching a maintenance level are to be achieved. However, the current practice of relying on manual and labour-intensive clearing (to maximise employment opportunities) has reduced efficiency levels, resulting in a lack of progress towards the goals of reaching a maintenance level (Fill et al. 2017).

Acknowledgements BvW and JRW thank the DSI-NRF Centre for Invasion Biology and the South African National Research Foundation for support (grants 109467, 85412 and 86894). LCF acknowledges South African National Parks, the DSI-NRF Centre for Invasion Biology, Stellenbosch University, and the National Research Foundation of South Africa (Grant Numbers IFR2010041400019 and IFR160215158271). The South African Department of Environment, Forestry, and Fisheries (DEFF) are thanked for funding the South African National Biodiversity Institute noting that this publication does not necessarily represent the views or opinions of DEFF or its employees.

## References