The regulation of biological invasions is often focussed at the species level. However, the risks posed by infra- and inter-specific entities can be significantly different from the risks posed by the corresponding species, to the extent that they should be regulated and managed differently. In particular, many ornamental plants have been the subject of long-term breeding and selection programmes, with an increasing focus on trying to develop cultivars and hybrids that are less invasive. In this paper, we frame the problem of determining the risk of invasion posed by cultivars or hybrids as a set of six questions that map on to the key components of a risk analysis, viz., risk identification, risk assessment, risk management, and risk communication. 1) Has an infra- or inter-specific entity been proposed as “safe to use” despite at least one of the corresponding species being a harmful invasive? 2) What are the trait differences between the proposed safe alternative and its corresponding invasive species? 3) Do the differences in traits translate into a difference in invasion risk that is significant for regulation? 4) Are the differences spatially and temporally stable? 5) Can the entities be distinguished from each other in practice? 6) What are the appropriate ways to communicate the risks and what can be done to manage them? For each question, we use examples to illustrate how they might be addressed focussing on plant cultivars that are purported to be safe due to sterility. We review the biological basis of sterility, methods used to generate sterile cultivars, and the methods available to confirm sterility. It is apparent that separating invasive genetic entities from less invasive, but closely related, genetic entities in a manner appropriate for regulation currently remains unfeasible in many circumstances – it is a difficult, expensive and potentially fruitless endeavour. Nonetheless, we strongly believe that an a priori assumption of risk should be inherited from the constituent taxa and the onus (and cost) of proof should be held by those who wish to benefit from infra- (or inter-) specific genetic entities. The six questions outlined here provide a general, science-based approach to distinguish closely-related taxa based on the invasion risks they pose.

cultivars, hybrids, infra-specific genetic entities, invasive species, non-invasive cultivars, ornamental plants, seedless cultivars, sterility

Invasion is a population-level phenomenon (Petit 2004; Zenni et al. 2014). Nonetheless, most regulatory policies focus implicitly or explicitly at the species-level. Consequently, the enormous variation that exists at infra-specific levels is often not considered in regulatory frameworks. The inability to recognise differences below the species rank may lead to serious underestimation or overestimation of invasion risk (Gordon et al. 2016). For example, infra-specific entities can vary in the bioclimatic niches they occupy in their invasive ranges (Thompson et al. 2011; Gotelli and Stanton-Geddes 2015), their host-specificity (Goolsby et al. 2006), and the impacts they cause (Novoa et al. 2018). Likewise, invasions by inter-specific taxa are also very important: hybridisation is one of the major impacts caused by biological invasions (Huxel 1999; Yakandawala and Yakandawala 2011). Therefore, it is vital that policy and regulation can adequately address invasion risk at levels other than the species.

These issues are particularly significant in the context of horticulture. The introduction of plants as ornamentals constitutes a major pathway for invasive plants across the globe (Bell et al. 2003; van Kleunen et al. 2018). Many of the traits that are important for horticultural purposes can also promote invasiveness (Reichard and Hamilton 1997; van Kleunen et al. 2018), for example, the formation of dense thickets, profuse flowering, high fruit set, and wide environmental tolerance (Knight et al. 2011; van Kleunen et al. 2018). In contrast, some horticulturally-desirable traits lead to reduced competitive ability; for example, variegated leaves in plants can have lower photosynthetic performance than non-variegated leaves (Gaskin and Kazmer 2009). Horticulture, therefore, creates very particular ecologically-relevant biases in infra-specific and inter-specific genetic entities. Moreover, many ornamental plants have been subjected to artificial selection and breeding programmes to enhance specific attributes of interest (Reichard and White 2001; van Kleunen et al. 2018), leading, in some cases, to high diversity of genetic entities below and above the species rank. This can have direct consequences for the likelihood of an invasion. For example, above the species rank, hybridisation between two or more species or even genera can promote genetic diversity and increase invasiveness (Culley and Hardiman 2009; Gaskin and Kazmer 2009; Klonner et al. 2017). Below the species rank, cultivars of a species can differ in traits such as allelopathy (Alsaadawi et al. 2012; Al-Bedairy et al. 2013) and herbicide tolerance (Sterling et al. 2004). Horticulture, therefore, creates very particular ecologically-relevant biases in infra-specific and inter-specific genetic entities.

In response to the risks of biological invasions, several countries have enacted legislation to regulate the use and trade of invasive plant species. Many of these regulated species are, however, of great ornamental value, and so such regulations cause economic losses and directly impinge on individual rights (Wirth et al. 2004). Consequently, there has been pressure to either exempt particular genetic entities that are naturally “safe” or “non-invasive” or to develop cultivars that are more environmentally sustainable (Guo et al. 2004; Freyre et al. 2014).

A specific case in point is South Africa’s National Environmental Management: Biodiversity Act, Alien and Invasive Species Regulations of 2014 (Department of Environmental Affairs 2014), hereafter referred to as the NEM:BA A&IS Regulations. In an attempt to balance the goal of environmental protection with those of the horticultural industry, the regulations have provision to exempt infra- or inter-specific entities. Out of 379 plant taxa listed in the 2016 revised list, sterile cultivars or hybrids are not listed for 32 taxa, spineless varieties of two cactus species are exempted, and sterile forms of Pinus elliotti are regulated differently from fertile forms (Department of Environmental Affairs 2016; Suppl. material 1: Table S1). While excluding sterile cultivars or hybrids is a laudable effort to reduce potential conflicts, the regulations do not provide any guidance on how this is to be implemented, and only in one case, Duranta erecta “Sheena’s Gold”, is an acceptable cultivar specifically named. The regulations also implicitly assume that sterility is a necessary and sufficient condition to reduce invasiveness and impact. However, some of the most damaging invasive plants are predominantly sterile in their invasive range [e.g. water hyacinth (Eichhornia crassipes); (Zhang et al. 2010)], conversely, infra- or inter-specific entities might still be fertile, but either the reduction in fertility or changes in other traits mean that they pose an acceptable level of risk. Finally, the risk-reducing trait might not be stable, and so a ‘safe’ cultivar could revert to an ‘invasive’ plant [e.g., there is some indication that the spineless non-invasive cacti exempted under the NEM:BA A&IS Regulations might readily revert to spiny invasive forms (Novoa et al. 2019)]. While the consideration of sub-specific entities has been included in a recent risk analysis framework that is being used to provide scientific recommendations for the NEM:BA A&IS Regulations (Kumschick et al. 2020), the framework does not yet include a detailed protocol for how to analyse the relative risk of infra- or inter-specific entities.

To clarify the issue of how to separate “safe” cultivars from “risky” relatives, we developed a set of six questions (Fig. 1). The questions are framed so they align with the general steps of a risk analysis, i.e., risk identification, risk assessment, risk management, and risk communication.

Figure 1.

Six questions that should be answered if “safe” cultivars are to be differentiated from “risky” relatives in regulations on biological invasions. The questions align with the constituent parts of risk analysis as indicated by the dotted boxes. Each of the questions is explained in further details in the main text.

Question 1: Has an infra- or inter-specific entity been proposed as “safe to use” despite at least one of the corresponding species being a harmful invasive? To minimise the risk of invasion from known invasive ornamental species, the use of non-invasive and sterile forms has been promoted. Question 1 concerns identifying and specifying this problem. Is there a cultivar of an invasive ornamental species that is deemed to be safe? Is there sufficient demand for this cultivar to warrant answering the other questions? It is essential to assess the invasion risk of a supposedly non-invasive genetic entity in the context of the invasiveness of the closely-related invasive taxa or parent invasive taxa (Table 1). The list of (potentially safe) cultivars can be obtained from published cultivar names (e.g. International Cultivar Registration Authorities), nursery catalogues, and consultation with stakeholders such as plant breeders and wholesale nurseries.

Question 2: What are the trait differences between the proposed safe alternative and its corresponding invasive species? This question refers to measurable differences that could help us to characterise and differentiate between cultivars and the known invasive entity. These differences could either be due to underlying genetic differences or could be induced due to environmental factors. The traits could include vegetative traits (e.g., leaf size, presence of variegated leaves, presence of thorns and spines, height, and growth form) or reproductive traits (e.g., flower colour, phenology or number of fruits or seeds). In some cases, underlying genetic differences leading to sterility may not be easily detected from phenotypic traits and, therefore, further examination of cytological and genetic differences could be necessary.

Question 3: Do the differences in traits translate into a difference in invasion risk that is significant for regulation? In question 3, we relate the observed differences (seen in question 2) to differences in the level of invasion risk posed and whether any such differences in risk mean that the taxa sit on different sides of a regulatory decision point, i.e., specimens with one set of physical properties pose an acceptable level of risk, while others do not. The observable differences in traits of the related genetic entities may lower the invasion risk only if the fecundity is directly or indirectly lower than the known invasive form. Traits that are directly related to fecundity include pollination, length of flowering time, number of flowers, fertilisation, seed production, germination success, survival rate, and vegetative reproduction. Traits that indirectly affect fecundity include allelopathic potential, mycorrhizal mutualisms, and herbivore deterrence due to the presence of thorns or chemicals. To detect differences in fecundity between different genetic entities, it is necessary to grow them in the same common garden environment and monitor long term. Ideally, the fecundity (or offspring survival) should be so low that population growth rate is negative (Knight et al. 2011).

Question 4: Are the differences spatially and temporally stable? Question 4 concerns whether the changes in the observable traits are stable and no reversal to the parental conditions is likely (see examples in Table 2). The changes should ideally be genetically fixed and not induced by environmental factors or due to short term epigenetic modifications. Even genetic changes could be reversed due to occasional outcrossing with other genotypes. Therefore, long term common garden experiments under different experimental conditions should be performed. In order to ensure that fertility does not revert, cross-pollination experiments should be performed between the different non-invasive genetic entities under consideration and the known invasive form. However, ultimately a regulator is interested in whether reversion is likely in the context of where and when (and in what numbers) the entity will be used. If a cultivar is very popular and widely planted, an extremely rare reversion is more likely to happen than for unpopular cultivars, and on-going monitoring might be advisable (see Question 6).

Question 5: Can the entities be distinguished from each other in practice? Question 5 refers to the need that, if the regulation is to be implemented, the safe cultivar must be readily distinguishable from its invasive relatives. This is particularly important for management and regulation so that non-invasive genetic entities can be exempted and monitored. Phenotypic differences might depend on growing conditions, and so other assays (Table 3) should be performed whenever necessary. Molecular markers for specific cultivars could be developed so that they can be readily detected.

Question 6: What are the appropriate ways to communicate the risks and what can be done to manage them? Finally, question 6 requires a mechanism by which recommendations are developed together with stakeholders in a transparent and inclusive manner (e.g., Novoa et al. 2018). This should be based on the results from the previous questions.

Ultimately, the risk posed by a biological invasion is a function of population growth rate, spread rate, and subsequent impacts. Sterility in and of itself is neither a necessary nor sufficient condition to prevent damaging invasions. However, for some taxa (those that do not show asexual reproduction in particular) it is a sufficient condition and one that is particularly relevant to the development of “safe” cultivars from “risky” relatives. In this section, we review the biological bases of sterility and the different methods that have been developed to produce sterile cultivars. Furthermore, we discuss the different methods used to evaluate how “safe” a cultivar is. In each case, we highlight and discuss the links between these issues and how they address the six questions posed in Figure 1.

In this paper, we attempted to clarify the issue of distinguishing “safe” cultivars from “risky” relatives by recasting the problem as a set of six questions that align with the risk analysis process (Fig. 1). None of the individual questions is new; however, we hope that this formalisation will be valuable in providing an integrative framework for considering risks of infra- and inter- specific taxa. Although we focussed on ornamental plants, we believe that the set of questions can be extended to other situations (e.g., to breeds of animals), noting there will likely be additional ethical and cultural concerns.

While this set of six questions is, we believe, a useful formulation of the problem, answering the questions remains non-trivial. We highlighted the biological bases of reduced fecundity and sterility, and methods used to achieve and demonstrate this. However, there are many exceptions to each of the mechanisms and situations where particular methods do not work. In many cases, an unequivocal demonstration of sterility, and that any such sterility is stable, requires expensive and long-term field and molecular experiments. Various short-cut proxies of sterility have been proposed. For example, the risk of different Anigozanthos spp. cultivars hybridising is a function of the ratio of their genome sizes; therefore, genetic exchange between horticultural and invasive populations can be limited if only taxa with sufficiently different genome sizes are allowed to be planted (Le Roux et al. 2010). However, long-term experiments are often necessary, specifically for woody and perennial species, before any conclusive evidence can be drawn about their invasiveness. Thus, the problem of trying to differentiate “safe” cultivars from “risky” relatives remains.

We hope the six questions outlined here will provide regulators with a basic structure around which a regulatory framework or protocol can be built and provide the horticultural industry with clarity over what needs to be demonstrated if invasions are to be avoided. However, given that the risks of invasion and impact are known from the “risky” relative, we conclude that the precautionary principle should be applied if unwanted consequences are to be avoided. We strongly believe that an a priori assumption of risk should be inherited from the closely-related invasive taxa from which the proposed “safe” alternatives are derived. This implies that the onus (and cost) of proof should be held by those who wish to benefit from infra- or inter-specific genetic entities.

This paper emerged from a workshop on ‘Frameworks used in Invasion Science’ hosted by the DSI-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, 11–13 November 2019, that was supported by the National Research Foundation of South Africa and Stellenbosch University. The South African Department of Forestry, Fisheries and the Environment (DFFtE) are thanked for funding, noting that this publication does not necessarily represent the views or opinions of DFFtE or its employees. We thank Chris Daniels and Terence Mabela for discussions that helped to improve the paper.