Understanding the status and extent of spread of alien plants is crucial for effective management. We explore this issue using Australian Acacia species (wattles) in South Africa (a global hotspot for wattle introductions and tree invasions). The last detailed inventory of wattles in South Africa was based on data collated forty years ago. This paper aimed to determine: 1) how many Australian Acacia species have been introduced to South Africa; 2) which species are still present; and 3) the status of naturalised taxa that might be viable targets for eradication. All herbaria in South Africa with specimens of introduced Australian Acacia species were visited and locality records were compared with records from literature sources, various databases, and expert knowledge. For taxa not already known to be widespread invaders, field surveys were conducted to determine whether plants are still present, and detailed surveys were undertaken of all naturalised populations. To confirm the putative identities of the naturalised taxa, we also sequenced one nuclear and one chloroplast gene. We found evidence that 141 Australian Acacia species have been introduced to South Africa (approximately double the estimate from previous work), but we could only confirm the current presence of 33 species. Fifteen wattle species are invasive (13 are in category E and two in category D2 in the Unified Framework for Biological Invasions); five have naturalised (C3); and 13 are present but there was no evidence that they had produced reproductive offspring (B2 or C1). DNA barcoding provided strong support for only 23 taxa (including two species not previously recorded from South Africa), the current name ascribed was not supported for three species and, for a further three species, there was no voucher specimen on GenBank against which their identity could be checked. Given the omissions and errors found during this systematic re-evaluation of historical records, it is clear that analyses of the type conducted here are crucial if the status of even well-studied groups of alien taxa is to be accurately determined.

Biological invasions, herbaria, inventory, invasive species, management plan, tree invasions, alien species lists

Every country needs up-to-date lists of introduced species to ensure that management actions are directed appropriately to deal with taxa at all stages of the introduction-naturalisation-invasion continuum (Latombe et al. 2017, McGeoch et al. 2012, Regan et al. 2002). Several types of errors and biases typically exist in such species lists. These include: insufficient survey information, inappropriate data resolution, undocumented data, inaccessible data, lack of sufficient information on native range distribution, incomplete information, misidentifications, unresolved ambiguities in the nomenclature, and un-described taxa (Latombe et al. 2017, McGeoch et al. 2012, Regan et al. 2002). For plants, sources of these errors and biases in the published literature, in museums, and in herbaria need to be assessed to create more comprehensive, accurate and reliable databases to inform management.

Australian Acacia species (wattles) are a good group to address the dimensions of these problems because: 1) introductions and plantings of species in this group have been fairly well documented; 2) wattles are amongst the most widely transferred tree species and well-studied invasive plant species in the world; and 3) wattles are often a priority for management (Marais et al. 2004), given the substantial negative impacts they can cause and the difficulties of controlling established invasions (Wilson et al. 2011).

Wattles have been introduced to many parts of the world for many purposes (Le Maitre et al. 2002, Kull and Tassin 2012) and they have played a major role in improving the livelihoods of communities (Kull et al. 2011, van Wilgen et al. 2011) and in economic growth (Griffin et al. 2011, Richardson et al. 2011). Despite these benefits, some wattle species have also become widespread invaders, threatening biodiversity by transforming ecosystems (Le Maitre et al. 2000, 2011).

Throughout this paper, we use the terms “Australian Acacia species” or “wattles” to refer to species formerly grouped in Acacia subgenus Phyllodineae, although several of these species (e.g. A. koa and A. simplex) do not actually have an Australian native range. We do not, however, consider species formerly grouped in other subgenera (e.g. even though A. bidwilli was formerly grouped in Acacia subgenus Acacia, is native to Australia and has been recorded as being introduced to South Africa, it is not part of this analysis). Richardson et al. (2011) estimated that of the 1022 wattle species formally described as of October 2010, at least 38% of these are known to have been moved by humans to areas outside their native ranges, at least 71 have become naturalised, and at least 23 have become invasive (i.e. have spread over substantial distances from planting sites) (see also Rejmánek and Richardson 2013).

Knowledge of the introduction history of these species is crucial for understanding and predicting their performance (Wilson et al. 2011) and to guide management strategies (van Wilgen et al. 2011). The long history of introductions and widespread dissemination of Australian Acacia species around the world has created opportunities to investigate factors that drive the success and failure of introductions, and to determine how native species respond to such events (Castro-Díez et al. 2011, Richardson et al. 2011).

South Africa has a long history of wattle introductions. Several species (notably A. cyclops, A. longifolia and A. saligna) were introduced in the early 18^th century by the Cape Colonial Secretary to stabilise dunes near Cape Town (Ross 1975, Poynton 2009); and, a few decades later, several species, e.g. A. decurrens, A. mearnsii, and A. melanoxylon, were introduced for timber production (Poynton 2009). Where these species were planted for forestry, native vegetation was removed to allow the acacias to establish without competition (Richardson and Rejmánek 2011). In the early 19^th century, several other species were introduced for ornamental purposes, e.g. A. baileyana, A. elata, and A. podalyriifolia (Donaldson et al. 2014a, b). As a result of this long and varied history, South Africa has the greatest recorded diversity of Australian Acacia species introductions and the most widespread wattle invasions of anywhere in the world (Richardson et al. 2011, Richardson and Rejmánek 2011, Rejmánek and Richardson 2013).

The history of wattle species introduced and planted for forestry purposes in South Africa was reviewed by Poynton (2009). However, the information on which this assessment was based was collated in the 1970s and needs updating. For example, recent surveys have shown that some species are much more abundant and widespread than previously thought (e.g. A. paradoxa; Zenni et al. 2009), and several species that were not listed by Poynton (2009) are now invasive (e.g. A. stricta; Kaplan et al. 2014).

Despite several decades of intensive management of invasive wattles in South Africa (van Wilgen et al. 2011, 2016), we know little about species other than those with substantial commercial value and those that are well-established invaders. What is known, however, is that invasions of Australian Acacia species are still increasing in geographical extent, abundance, and magnitude of impact (Henderson and Wilson 2017). Even the most widespread invasive species have not reached all potentially invasible sites (Rouget et al. 2004) and many naturalised species only began spreading recently (e.g. Zenni et al. 2009, Kaplan et al. 2012, 2014). Rouget et al. (2016) quantified different aspects of this “invasion debt” for wattles and found that southern Africa has a large invasion debt. If the invasion debt were realised, there will be a substantial escalation in the overall ecological and economic impacts of wattles (Richardson et al. 2015).

Richardson et al. (2011) reported that about 70 species of Australian Acacia species are known to have been introduced to South Africa, some as early as the 1830s (Adamson 1938, Poynton 2009). Fourteen species are currently considered invasive in the country (Rejmánek and Richardson 2013). There are also records of naturalised populations of A. adunca, A. cultriformis, A. fimbriata, A. pendula, A. viscidula, (Wilson et al. 2011, van Wilgen et al. 2011) and there are localised populations of what has been termed “A. retinodes” (which is likely A. provincialis – see Table 1) and A. ulicifolia (Wilson et al. 2011, van Wilgen et al. 2011). The identification of these naturalised species remains to be verified, and the status of other species reported in the country is unknown. This study therefore set out to determine: 1) how many Australian Acacia species have been introduced to South Africa; 2) which species are still present; and 3) what is the extent of naturalised populations.

We found evidence that 141 Australian Acacia species have been introduced to South Africa (Table 1). For 112 species there is a literature record (this is the only evidence available for 56 species), for 81 species there is a herbarium records (this is the only evidence for 27 species), and 23 species have been confirmed using a molecular approach (this is the only evidence for 2 species).

Of these 141 species, we could confirm the presence of only 33 species (Table 1, see Fig. 2 for images of some of these). In terms of Blackburn et al.’s (2011) Unified Framework for Biological Invasions (see Appendix 1 for a full description of the categories), 13 of these species are in category E, two are in category D2 (i.e. there are 15 invasive species). Five species are naturalised but not yet invasive (category C3). We found no evidence that the remaining 13 species have produced reproductively active offspring in South Africa; these taxa thus fall in category B2 or C1. Status reports on the five naturalised and one invasive species that had not previously been studied in detail are presented in Appendix 2.

Figure 2.

Examples of Australian Acacia species found in this study. A Acacia salicina with green pods in the Johannesburg Botanical Gardens B A. viscidula root sucker in a naturalised population in Newlands, Cape Town C A. pendula. Galls from a biological agent (Dasineura dielsi) released to control A. cyclops are visible in Bloemfontein D A. provincialis seedling showing juvenile bipinnate leaves attached to the stem and to the ends of the first few phyllodes, there are no bipinnate leaves on older phyllodes E A seed of A. piligera collected at Tokai, Cape Town F A planted individual of A. floribunda showing phyllodes and flower spikes in Johannesburg. Photos A–C, E, F: Nkoliso Magona; D: John Wilson

The estimate of 141 species is approximately double that of the previous estimate of 70 species (Richardson et al. 2011). These additional species include taxa not previously known from outside Australia (A. acuaria, A. latipes, A. leptospermoides, A. saliciformis, A. ulicina, and A. uncifera; Richardson et al. 2011).

We found one error and five misspellings on herbarium labels, these errors being perpetuated in subsequent literature sources. There were an additional three misspellings in literature sources (Table 2).

Only 23 species identities were confirmed either in this study or previously using a molecular approach (Table 1; Suppl. material 1). Of these two species (A. hakeoides and A. ramulosa) had not previously been recorded as having been introduced. For three species with a putative field identification, the molecular results did not correspond to the voucher specimens for the same species on GenBank (A. adunca, A. fimbriata, and A. floribunda). For a further three species, there was no voucher specimen on GenBank and so it was not possible to obtain molecular support for their putative identification (A. piligera, A. provincialis, and A. ulicifolia).

Notably, when this manuscript was under review, it was pointed out to us by Martin O’Leary, State Herbarium of South Australia, that A. retinodes had frequently been misapplied to A. provincialis in other countries, and, on further investigation, this appears to have been the case in South Africa as well.

Before this study, 70 Australian Acacia species were known to have been introduced to South Africa (Richardson et al. 2011). We found evidence that another 71 species had been introduced to the country. Of the revised list of 141 species for which records exist for introduction to, or presence in, South Africa (Table 1), we could confirm that at least 33 species are still present in the country.

There were four major reasons for the discrepancy between the list of species recorded as having been introduced to South Africa and the list of species confirmed to be still present in the country. First, during the survey, we came across an old experimental forestry trial set up to identify species suitable for dry-land agroforestry (Damara Farm in the Western Cape; see Suppl. material 4). Thirty-three Australian Acacia species were reportedly planted at Damara Farm (Gibbs 1998), of which we found 18 putative taxa (based on morphology and molecular analysis). None of these taxa has naturalised.

Second, specimens of several species are present in the National Herbarium in Pretoria but had not been included in previous lists because the herbarium records had not yet been digitised.

Third, species might no longer be present at their original sites of introduction. Many of the records (particular herbarium records that have not yet been digitised) were from historical forestry plantings. When we followed up, we found that many of these planting were no longer present — they had been transformed for infrastructure development, agriculture, or other forms of land use. Most cases, where listed species are no longer present, were within the municipal areas of the cities of Johannesburg and Pretoria that have been converted to stock farms. For example, all available records of A. cultriformis that were assessed in Gauteng Province are now under various forms of agriculture, while several records of other species in Poynton (2009) referred to arboreta that no longer exist.

Fourth, species might not have survived at sites of initial introduction due to unfavourable climatic conditions or biotic pressures; Poynton (2009) noted that most introduced Acacia species were grown in trial plantations, many of which did not survive.

Finally, it is possible that, despite our best efforts, our searches were inadequate to (re)locate some species. We suspect this is unlikely to be a major cause, as Australian Acacia species have been extensively studied and managed in South Africa, and as the taxa are often quite distinct from the native flora. Some “missing” species might feasibly be surviving in soil-stored seed banks (seeds of many wattle species can retain viability in the soil for several decades; Richardson and Kluge 2008). However, due to the fact that many herbaria specimens and literature reports lacked detailed locality data (longitude and latitude coordinates), it is possible that we simply were not looking in the right place.

Notably, however, there may be other localities like Damara Farm where multiple species have been cultivated and potentially still exist. Poynton (2009) noted that many old trial plantations were left unmanaged due to the closure of forest stations; records of these sites might not be reflected in the information sources that we consulted.

Whatever the reasons for discrepancies in past estimates of wattle introductions in South Africa, it is clear that there is a high invasion debt for Australian Acacia species in the country (Rouget et al. 2016). If this debt were paid, it would lead to a substantial escalation in the extent of invasions and overall ecological and economic impacts of the group (Richardson et al. 2015). There appears to be no clear set of life-history features, or syndromes of traits, that separate invasive from non-invasive Acacia species (Gibson et al. 2011), nor is there a clear phylogenetic signal for invasiveness in the genus (Miller et al. 2017). This suggests that factors associated with propagule pressure and residence time have been the dominant drivers of invasiveness in this genus in South Africa. This highlights the importance of dealing with nascent invaders before population sizes and spatial extent are sufficiently large to drive self-sustaining invasions.

One way of reducing this invasion debt is through proactive management approaches, e.g. the detection, identification, assessment, and control of naturalised populations before they are widespread invaders. Some of the naturalised populations of Australian acacias in South Africa occur only at a few sites and so eradication is possible, but for some species, A. cultriformis specifically, it is likely that they are present at other locations that were not detected in this study. During the field visits in the cities of Bloemfontein and Johannesburg, people that had A. cultriformis in their gardens reported that this species was present in many gardens in neighbouring areas. As this species has been widely planted, it is likely that the extensive seed bank and high climatic suitability (Motloung et al. 2014) could make it a high invasion risk (Wilson et al. 2011). Of the naturalised species that were detected in this study, A. cultriformis is the only one for which nation-wide eradication is likely to be not feasible (given the problems with locating all horticultural plantings).

Some of the taxa might also have been prevented from spreading due to the impact of biological control agents released to target the widespread Australian Acacia species. In this study, the biological control agents Dasineura dielsi (target species: A. cyclops) and Trichilogaster acaciaelongifoliae (target species: A. longifolia) were observed on both A. floribunda and A. pendula. Dasineura dielsi has previously been recorded on A. implexa, A. melanoxylon, A. longifolia and A. saligna (Impson et al. 2009, Kaplan et al. 2012). It is likely that the agents reduced seed production in a variety of introduced wattles, and potentially reduced the rate of spread of populations, though it is very unlikely they have resulted in the extirpation of any populations if there were no other management or land-use change.

Unlike other taxonomic groups of alien plants, where there are many misidentified herbarium records (e.g. Melaleuca spp.; Jacobs et al. 2017), we did not find many such misidentifications (though there is often little congruency between the molecular and morphological identifications). Our molecular approach could not resolve all taxonomic ambiguities, especially in cases where there was insufficient reference data for vouchers specimens (Parmentier et al. 2013) or short DNA sequence reads available (Stoeckle et al. 2011). This makes differentiation between closely related species difficult. Many of the species in our list (particularly those from Damara Farm) remained unidentified. This could be because DNA sequencing data for the gene regions that we used are not available for many wattle species and/or because many showed 100% similarity to more than one taxon for the gene regions that were sequenced. We assumed that these results indicated a very closely-related species. There is a need for detailed morphological characterisation to identify these taxa with certainty [colleagues are busy collecting comprehensive herbarium specimens (i.e. with reproductive structures) that will hopefully provide clarity on the species present]. Despite these limitations, our molecular data did yield some interesting results — including identifying new species not previously recorded in South Africa (A. hakeoides and A. ramulosa); and casting doubt on the identities of three species that have long been included in lists of alien Acacia species in the country (A. adunca, A. fimbriata, A. floribunda).

Finally, the misapplication of the name A. retinodes for A. provincialis that was only uncovered by a reviewer of this manuscript indicates the continuing need for international collaboration with identifications. Such mistakes can lead to confusions with management as A. retinodes suckers but A. provincialis does not [cf. the misapplication of the name Melaleuca ericifolia (a resprouter) to M. parvistaminea (a reseeder) — the lack of resprouting in the field was one of the main triggers for a re-evaluation of the identification (Jacobs et al. 2014)].

While the work presented here has not definitely resolved all of the issues around the identity of Australian Acacia species in South Africa, it is clear that available inventories of even supposedly well-known taxa can be misleading. Better quantification of current introduction status is crucial for producing effective management strategies and for estimating the resources needed control targeted populations of alien plants (Wilson et al. 2013). They are also essential if we are to have confidence in comparative analyses of invasions.

This work was supported by the South African National Department of Environment Affairs through funding of the South African National Biodiversity Institute’s Invasive Species Programme and the DST-NRF Centre of Excellence for Invasion Biology. DMR acknowledges additional support from the National Research Foundation (grant 85417). We thank Sthembiso Gumede, Owethu Nomnganga, Virgil Jacobs, Jan-Hendrik Keet, Ulrike Irlich, George Sekonya, Kanyisa Jama, and various Working for Water teams for assistance in the field; Fiona Impson and Philip Weyl for alerting us about naturalised populations; the Armstrong family for allowing us access to Damara Farm; and Carien Kleinjan, Fiona Impson, Giuseppe Brundu, and Martin O’Leary for valuable comments on drafts of the manuscript and for clarifying the identification of A. provincialis. We thank Megan Koordom for generating DNA sequencing data and Heidi Hirsch for assisting with databasing the resulting information.

Species status reports for naturalised Australian Acacia species (using standardised metrics proposed by Wilson et al. 2014)

Species: Acacia adunca G.Don [note molecular work suggests this might be another taxon]

Location: Groot Drakenstein (Bien Donne Farm). South Africa

Status: Naturalised; C3 under Blackburn: Individuals surviving outside of cultivation in location where introduced, reproduction occurring, and population self-sustaining.

Potential: Large proportion of the country is suitable.

Abundance: ~1000 plants (2014); lots of seeds stored in the seedbank

Population Growth Rate: Not known.

Extent: 1 population covering area of 0.27 ha as a closed canopy (i.e. condensed canopy area is also 0.27 ha).

Spread: From its native range, the seeds are spread by animal (ants and birds).

Impact: Has a potential to out-compete indigenous plants. Acacia adunca would fail a pre-border assessment as it scores higher than the threshold value of 6 that indicates species as being potentially invasive.

Threat: Not specifically studied, but likely similar to other Australian acacias (see Le Maitre et al. 2011).

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners. Herbarium specimens and the spotter website, South African Invasive Species, ISpot were examined.

Notes: Eradication plan in place

Contact: invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za

Species: Acacia cultriformis G.Don

Location: Grahamstown (Makana Botanical Garden and Grey Dam).

Status: Naturalised; C3: Individuals surviving outside of cultivation in location where introduced, reproduction occurring, and population self-sustaining.

Potential: Large proportion of the country is suitable.

Abundance: 35 plants (2015).

Population Growth Rate: No seedlings were found during the survey, so nothing is known of population growth rates.

Extent: Two populations covering area of 1.28 ha. (Condensed area of 0.0519 ha).

Spread: In South Africa the species might be spread via seeds by people who are jogging or cycling.

Impact: Has a potential to out-compete indigenous plants. Acacia cultriformis would fail a pre-border assessment as it scores higher than the threshold value of 6 that indicates species as being potentially invasive.

Threat: Not specifically studied, but likely similar to other Australian acacias (see Le Maitre et al. 2011).

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners. Herbarium specimens and the spotter website, South African Invasive Species, ISpot were examined.

Notes: Eradication plan in place.

Contact: nkoliso@sun.ac.za; invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za

Species: Acacia fimbriata G.Don [note molecular work suggests this might be another taxon]

Location: South Africa

Status: Invasive; D2: Self-sustaining population outside of cultivation that is a significant distance from the putative point of introduction.

Potential: Large proportion of the country is suitable.

Abundance: ~5 000 plants (2014); lots of seeds stored in the seedbank.

Population Growth Rate: Not known,

Extent: 3 populations covering area of 53 ha. (Condensed area 0.73 ha)

Spread: In its native range, seeds are spread by animal (ants and birds). It was introduced to botanical garden and now it is found naturalised at the botanic gardens and a waste dumping site (presumably taken there as garden refuse).

Impact: Has the potential to out-compete indigenous plants. Acacia fimbriata would fail a pre-border assessment as it scores higher than the threshold value of 6 that indicates species as being potentially invasive.

Threat: Not quantified.

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners. Herbarium specimens and the spotter website, South African Invasive Species, ISpot were.

Notes: Eradication plan in place

Contact: invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za

Species: Acacia piligera A.Cunn (Fabaceae)

Location: Tokai

Status: Naturalised; C3: Individuals surviving outside of cultivation in location where introduced, reproduction occurring, and population self-sustaining.

Potential: Not quantified.

Abundance: ~174 plants (2015); lot of seeds stored in the seedbank.

Population Growth Rate: Not known, but based on the observed seedling recruitment events occurred after rain and fire, it is believed that water and heat may be the cause of population growth rate.

Extent: One population covering area of 0.0947 ha. (condensed area of 0.0947 ha).

Spread: In its native range, the seeds are dispersed by animals (ants). In South Africa, it has not spread from its original cultivation area.

Impact: Not quantified

Threat: Not specifically studied, but likely similar to other Australian acacias (see Le Maitre et al. 2011).

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners; herbarium specimens and the spotter website, South African Invasive Species, ISpot were.

Notes: Eradication plan in place.

Contact: invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za

Species: Acacia provincialis A.Camus (A. retinodes Schltdl. mis-applied in South Africa) (Fabaceae)

Location: Tokai Arboretum

Status: Naturalised; C3: Individuals surviving outside of cultivation in location where introduced, reproduction occurring, and population self-sustaining.

Potential: A large proportion of the country is suitable for this species.

Abundance: <50 plants (2014); Relatively small seedbanks.

Population Growth Rate: Not known.

Extent: One population covering area of 0.25 ha. (as it is a closed canopy, condensed area is essentially the same, i.e. 0.25 ha)

Spread: In its native range, seeds are dispersed by animals (ants and birds).

Impact: Has the potential to out-compete indigenous plants. Acacia provincialis would fail a pre-border assessment as it scores higher than the threshold value of 6 that indicates species as being potentially invasive.

Threat: Not specifically studied, but likely similar to other Australian acacias (see Le Maitre et al. 2011).

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners. Herbarium specimens and the spotter website, South African Invasive Species, ISpot were examined.

Notes: Eradication plan in place

Contact: invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za

Species: Acacia viscidula Benth. (Fabaceae)

Location: Newlands forest.

Status: Naturalised; C3: Individuals surviving outside of cultivation in location where introduced, reproduction occurring, and population self-sustaining.

Potential: Large proportion of the country is suitable

Abundance: ~1200 plants (2014).

Population Growth Rate: Not known.

Extent: Two populations covering area of 3.5 ha. (Condensed area of 0.077 ha).

Spread: In its native range, seeds are spread by animals (ants and birds).

Impact: Has the potential to out-compete indigenous plants. Acacia viscidula would fail a pre-border assessment as it scores higher than the threshold value of 6 that indicates species as being potentially invasive.

Threat: Not specifically studied, but likely similar to other Australian acacias (see Le Maitre et al., 2011).

Survey method(s) used: Systematic walked transects to generate point distributions. Pamphlets were circulated to land owners. Herbarium specimens and the spotter website, South African Invasive Species, ISpot were examined.

Notes: Eradication plan in place. Plants are vigorous resprouters

Contact: invasivespecies@sanbi.org.za

Information compiled by: Nkoliso Magona, nkoliso@sun.ac.za