In South Africa: an Assessment of Invasiveness and Options for Management

South African Journal of Botany 87 (2013) 134–145

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South African Journal of Botany

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Montpellier broom (Genista monspessulana) and Spanish broom (Spartium junceum) in South Africa: An assessment of invasiveness and options for management

Sjirk Geerts a,b,⁎, Pieter W. Botha a,b, Vernon Visser a, David M. Richardson a, John R.U. Wilson a,b a Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa b Invasive Species Programme, South African National Biodiversity Institute, Kirstenbosch Research Centre, Claremont 7735, South Africa article info abstract

Article history: The legumes (Fabaceae) Genista monspessulana and Spartium junceum are major invaders in several other parts Received 25 October 2012 of the world, but not yet so in South Africa. We determine their current distributions in South Africa at different Received in revised form 23 February 2013 spatial scales, assess population structure (soil seed banks and size at reproduction) evaluate current manage- Accepted 25 March 2013 ment activities, and provide recommendations for control (including assessing the feasibility of nation-wide Available online 17 May 2013 eradication). G. monspessulana occurs at nine localities in three quarter-degree cells, covering a total of Edited by OM Grace 22.7 ha. S. junceum is much more widespread, occurring in 33 quarter-degree cells and is frequently cultivated in private gardens. All naturalised or invasive populations are in disturbed areas, mostly along roadsides. Once Keywords: established, G. monspessulana and S. junceum accumulate large, persistent soil-stored seed banks, ranging Fabaceae in size between 909 and 22,727 (median 1970) seeds/m2 and 0 and 21,364 (median 455) seeds/m2 for Legislation the two species respectively. Both species resprout vigorously after cutting and stump herbicide application Legumes (60% of G. monspessulana and 43% of S. junceum plants resprouted) which necessitates regular follow-ups. Management We estimate that over 10 years, at a cost of about ZAR 81,000 (1 ZAR = 0.114 US$ as on 6 October 2012), Soil seed banks G. monspessulana could be extirpated from South Africa. S. junceum is far more widespread and coupled Spatial scales with low effectiveness of control, abundance of seeds and seed longevity, eradication is unfeasible. We recommend that control methods used for S. junceum be improved to prevent resprouting, and that areas are managed to limit the movement of seeds and avoid further spread and establishment. Further studies are required to understand why these two species have failed to replicate the invasiveness shown in other parts of the world. © 2013 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction the tribe Genisteae, Fabaceae) seem particularly prone to becoming invasive. Native mainly to the Mediterranean Basin, broom species have been The distributions of many invasive plant species are to a large extent, introduced to many parts of the world across different biomes, and are determined by the extent of human usage of the species (e.g. Gravuer et therefore an important group for understanding legume invasions al., 2008; Lavergne and Molofsky, 2004; Procheş et al., 2012; Wilson et al., (GRIN, 2011). 2007, 2011). Legumes have been introduced globally for multiple uses, Introduced legumes are a prominent group of South Africa's invasive predominantly in agriculture and horticulture. Their nitrogen-fixing abil- flora; they make up 18% of the declared weeds in the Conservation of ity, drought resistance and the large number of edible species make them Agricultural Resources Act (CARA), and top the lists of invasive alien the second most important agricultural plant family after grasses species in most biomes (Henderson, 2007). At least 43 broom species, (Graham and Vance, 2003). Legumes are also popular in horticulture from eight genera, have been introduced into South Africa (Glen, for their showy flowers, hardiness and ability to thrive in nutrient-poor 2002). Of these, species from five genera (Ulex europaeus, Cytisus soils. For these reasons, and because of the long seed dormancy in scoparius, Lupinus angustifolius, Lupinus luteus, Genista monspessulana many species, legumes are among the most notorious contributors to and Spartium junceum) have naturalised or become invasive (SAPIA, the naturalised flora of the world (Binggeli, 1996; Paynter et al., 2003; April 2012). This paper focuses on two species introduced for horticul- Pyšek, 1998; Richardson and Rejmánek, 2011; Sánchez-Blanco et al., ture: G. monspessulana and S. junceum. 2012). A group of legumes known collectively as brooms (25 genera in G. monspessulana and S. junceum are classified as major weeds in parts of the world, other than South Africa, where they have been introduced for use as ornamentals or hedge plants (Parsons and ⁎ Corresponding author at: Department of Biodiversity and Conservation, Cape Peninsula, Cuthbertson, 2001). University of Technology, PO Box 652, Cape Town 8000, South Africa. Tel.: +27 21 4603215; fax: +27 21460 3193. G. monspessulana is a major invader in California (Cal-IPC, 2006) E-mail addresses: [email protected], [email protected] (S. Geerts). and is listed as a weed of national significance in Australia (Paynter

0254-6299/$ – see front matter © 2013 SAAB. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.sajb.2013.03.019 S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 135 et al., 2003) where it is controlled in a number of states (mainly 2.2. G. monspessulana distribution in South Africa Northern Victoria, Tasmania, New South Wales and South Australia). It is also invasive and widespread in New Zealand and Chile, and To locate G. monspessulana populations in South Africa we collated present in Hawaii (Parsons and Cuthbertson, 2001; Pauchard et al., records from the Southern African Plant Invaders Atlas, SAPIA (accessed 2008). S. junceum is a prohibited pest plant in parts of Australia April 2012; Henderson, 1998), the database of herbarium records (Thorp and Wilson, 1998) and is invasive in the Pacific Northwest of (PRECIS, 2012), an on-line spotter network (http://www.ispot.org.za/), the USA, California, Hawaii, Chile, and Peru (Bossard, 2000; Castro old plant lists (Adamson and Salter, 1950; Moll and Scott, 1981), and et al., 2005; DiTomaso and Healy, 2007; Ochoa and Antrade, 2003). unpublished records of the authors. Pamphlets with photographs Both species form dense monospecific stands, increase the fuel load and species descriptions were distributed among relevant land- for fires and displace native species (Bossard, 2000; Rejmánek and owners, conservation agencies and the public (Fig. S4). Local experts Randal, 1994). and conservation officers were consulted and the potential localities Surprisingly, given their major invasiveness in many parts of the they suggested were visited. All G. monspessulana populations iden- world, including areas with similar climates to South Africa, and the tified occurred in the south-western part of the Western Cape Prov- invasiveness of many other woody legumes in South Africa, neither ince (Fig. 2), which has a typical Mediterranean-type climate and of the two species is very widespread in South Africa (Henderson, nutrient-poor soils. 2001). In particular, G. monspessulana is only known from a few local- Mapping at each G. monspessulana population involved walking par- ities. S. junceum is more widespread and is mainly found along road- allel transects extending at least 100 m in all directions beyond the last sides (Bromilow, 2010) but also along rivers (Galatowitsch and plant encountered, except along streams where the search distance was Richardson, 2005; Meek et al., 2010) and is able to invade natural increased to 200 m. Each plant encountered was recorded. The current vegetation (Bromilow, 2010; Henderson, 2001). occupied area was calculated using convex-hull polygons based upon Based on an initial assessment, G. monspessulana is listed in the “1a” the Graham's scan algorithm in Arc-GIS 10. Plant cover was converted category of invasive plants (National Environmental Management: to 100% equivalent cover (“condensed ha”) and was calculated by buff- Biodiversity Act., 2009), which means that it requires compulsory ering each individual with its measured canopy area and dissolving controlwiththeaimoferadication.S. junceum is categorized 1b in the overlaps. For populations where canopy diameters were available for Western Cape Province (meaning that it needs to be controlled as part only a subset of plants, an average canopy diameter was used. of a management plan) and category 3 in the rest of South Africa (can be grown under permit). An assessment of the distribution and management options for 2.3. S. junceum distribution in South Africa these two species in South Africa is overdue. Therefore this study aims to: 1) determine the distributions of G. monspessulana and S. junceum In contrast to the limited distribution of G. monspessulana, S. junceum in South Africa, 2) determine size at reproduction, reproductive output is much more widespread and this enabled multi-scale comparisons. and soil seed bank, 3) assess effectiveness of current management This aids in finding determinants for occurrence at a larger scale (such activities, and 4) provide recommendations for national management as climate) but also at a smaller scale (such as local anthropogenic dis- strategies. turbance) (Deutschewitz et al., 2003; Trivedi et al., 2008). Furthermore, good knowledge of this species' spatial distribution will help to decide 2. Methods whether S. junceum should be targeted for eradication. For example, if S. junceum is widespread (occupies many quarter-degree cells) on a na- 2.1. Study species tional scale but only occurs in very few delineated populations in each quarter degree cell, eradication might be considered. If, however, the G. monspessulana and S. junceum are perennial shrubs of up to five distribution on a national scale is fairly limited (occupies few quarter metres tall. They flower profusely in spring and summer with typical, degree cells), but populations are many and hard to find on a smaller yellow, leguminous flowers, making flowering plants easy to detect. scale, eradication might not be feasible. The minimum age of reproduction, in both native and introduced To map S. junceum populations, we used SAPIA data at the national regions, is two years (Cal-IPC, 2006; Herrera et al., 2011). Seed pods and provincial scales (33 quarter degree cells; SAPIA April 2012) and burst open to disperse seeds 3–4 m from the parent plant, with detailed sampling for district and local scales. For district-scale map- secondary dispersal by ants (Adams and Simmons, 1991; Q. Paynter ping, we selected the Stellenbosch Municipality (831 km2) for ease pers. comm.; Gómez and Oliveras, 2003; Oliveras et al., 2007), of access, the variety of land-use types, and the location at the centre rain-wash, streams, agricultural products and in mud attached to of the regional range of S. junceum. Within this district we sampled all animals, vehicles and road maintenance machinery (Bossard, 2000; major and minor roads (narrow tarred roads, excluding those purely Parsons and Cuthbertson, 2001). Plants resprout vigorously when in suburbs) by car, for a total distance of 252 km. Maximum speed cut or burnt. was 70 km h−1, with a passenger on the lookout for plants. At each G. monspessulana has a large native range which includes southern locality, all plants were georeferenced and counted. Europe, northwest Africa and the temperate, western part of Asia At a local scale, sampling was done on foot along a 5-km stretch of (GRIN, 2011). Mature plants produce ~1200 seeds/year in California, road at the southern side of Helshoogte Pass, Stellenbosch (Fig. 3). >35,000 in Australia and 2500 in the native range (Herrera et al., This area was selected as it was the largest population recorded in 2011). Despite lower seed production in California, larger seed banks ac- the Stellenbosch Municipality, and also provided a test of whether cumulate because of the higher plant densities there [>12,000 m−2 plants could spread from the road-side into neighbouring vegetation seeds in California; 3774–30,297 m−2 seeds in Australia; but only (Table 1; Fig. 3). We surveyed the first 15 m systematically from the 547–4000 m−2 seeds in the native range (Adams and Simmons, 1991; road and extended the survey area if plants were observed beyond Herrera et al., 2011; Paynter pers. comm.)]. this (the surrounding vegetation was relatively low, making detec- S. junceum also has a large geographic native range extending tion beyond 15 m easy). from southern Europe, North Africa and the Canary Islands to the As an estimate of the total affected area South Africa-wide temperate western part of Asia (GRIN, 2011). It can produce between (condensed ha or net extent), we scaled up from the Stellenbosch 7000 and 10,000 seeds per season and, although we could find no quarter-degree cell based on our field observations and the number data on seed banks, it is likely that large seed banks accumulate of records recorded in SAPIA (13.2% of total records; this excludes (Bossard et al., 2000). records added during this study). 136

Table 1 Survey results for known records for Genista monspessulana in South Africa. All historical records were re-visited though in many cases no plants were found. SAPIA: Southern African Plant Invaders Atlas; PRECIS: National Herbarium Pretoria (PRE) Computerised Information System.

Locality Year QDGC Record origin Latitude Longitude Area occupied (ha) measured Number of plants Notes recorded using convex hull polygons

Newlandsa 1904 3318CD PRE 0420274, 0420276, −33.97116 18.44734 5 populations of 0.036,0.08, 0.224, 1462 Newlands Avenue SAPIA 342 0.039, 0.342 ha over 16.63 ha Newlands, Paradise road 1941 3318CD PRECIS s.n. 0 Probably same record as Newlands Avenue 134 (2013) 87 Botany of Journal African South / al. et Geerts S. Tokai Manor house a 2011 3418AB This study −34.05896 18.42053 5.56 379 Tokai Forest 2007 3418AB SAPIA 63169 −34.05694 18.43194 ~8 populations over ~1100 before pine clearing and Lower Tokai: Block A13a. ~12.5 ha (treated as one population) ~6000 seedlings afterwards (2011), currently b10 (Rebelo pers. com.) Tokai “The Mound”a 2011 3418AB City of Cape Town −34.05333 18.44589 0.04 30 plants in 2011, 2466 seedlings in 2012 Porter Estate Tokai 2011 3418AB C. Ramjukadh −34.05233 18.41722 ~10plants Cape Peninsula 1981 3418AB SAPIA 50247 Most likely same as Tokai records Cape region 1940 N/A PRE459129-0 Most likely same as Newlands or Constantia Kirstenbosch Botanical garden 1973 3318CD PRE420275-0 0 Near entrance road, cleared Van Riebeeck Park, Cape town ? 3318CD Tony Rebelo 0 Van Riebeeck Park (Deer Park) Vredehoek Cape town. From Tony Rebelo and D. Spear Newlands, Orangekloof 1981 3418AB, 3318CD Moll and Scott, 1981 0 Exact localities not provided; corresponds and Klein Constantia to Newlands, Orangekloof and Klein Constantia Newlands avenue, 1950 3418AB, 3318CD Adamson and Salter, 1950 0 Orangekloof not found on resurvey. Orangekloof pers. com. Jackie Pretorius

and Klein Constantia – Klein Constantia cellara 2011 3418AB This study −34.03820 18.41236 0.04 4900 Klein Constantia farm behind cellar 145 Klein Constantia dama 2011 3418AB This study −34.03526 18.40841 0.43 214 Klein Constantia farm dam Idas Valley, Stellenbosch 1972 3318DD PRE0463252, SAPIA 341 0 Ida's Valley, above Wedgewood. Somerset West district 1953 3418BB PRE15583 and Johan West 0 Near the Lourens River (pers. com) Op-die-Berga 2012 3319AB This study −33.02408 19.31142 0.06 657 Church property Dullstroom in Mpumalanga 1977 PRE515978-0 0 Misidentiﬁed should be Cytisus scoparius De Zalze, Stellenbosch 2013 3318DD This study −33.97138 18.82444 0.1 10 On a bank of the Blouklip River

a Study sites. S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 137

2.4. Population structure, reproductive size and reproductive output distributions and, consequently, have previously been used to model the distributions of alien plant species (Maiorano et al., 2012). Two dif- To determine age structure and size at reproduction, plant height, ferent modelling methods available in the BIOMOD package (Thuiller et perpendicular canopy diameters, basal stem diameter, presence of al., 2009) were used to build SDMs in R (R Development Core Team, flowers, pods and pod-stalks were recorded. The significance of plant 2012): (1) a regression method, Generalised Additive Models [GAM; measurements in predicting the presence of reproductive structures Hastie and Tibshirani (1990)], with a maximum of three degrees of was assessed using a generalised linear model, with a binomial error freedom; (2) Boosted Regression Trees [BRT; Ridgeway (1999)], with distribution, with signs of reproduction (0/1) as the response variable the optimal number of trees selected by ten cross validations and an and height (log), mean basal diameter (log), mean canopy diameter upper limit of 10,000 trees. The BIOMOD defaults for learning rate (log) and site (G. monspessulana: Tokai, Newlands, Constantia, Op- (0.001) and tree complexity (7 trees) were investigated using the die-Berg) as predictor variables. “gbm.step” function of Elith et al. (2008) and were found to produce pre- To calculate reproductive output, flowers were marked, and when dictive deviances curves that approached best predictive performance fruits dehisced, percentage fruit set determined and seeds counted. slowly and required more than 1000 trees to reach minimum error, as For total reproduction, the number of seeds per pod was multiplied by suggested by these authors. A total of ten runs of each model type the mean number of pods per plant (counted on ten average-sized were performed for each model type, with a new randomly- plants of 1 m tall). generated set of pseudo-absences used each time. The same number For G. monspessulana, all plants at Tokai (n = 379) and Klein of pseudo-absences as presences were used for the BRT models, and Constantia dam (n = 214), and a haphazard selection of those at Klein 1000 pseudo-absences for each GAM model run were used (with Constantia cellar (n = 360, 7.3% of total), Newlands Forest (n = 166, equal weighting for presences and absences for both model types), 11.4% of total) and Op-die-Berg (n = 108, 16.4% of total), were as recommended by Barbet‐Massin et al. (2012).Modelimportance measured. For reproductive output, flowers were marked and seeds was measured by calculating the mean Pearson correlation (r)between counted at Klein Constantia cellar (n plants = 26, n flowers = 1096). the fitted values of each variable and randomly permuted selection of For S. junceum, all plants on Helshoogte Pass (n =5159)were records for that variable (Thuiller et al., 2009). A randomly-selected measured. For reproductive output, flowers were marked and seeds subset of 70% of the data was used for model calibration, and the counted at Helshoogte Pass and at roadside populations in Stellenbosch, remaining 30% for model evaluation using the area under the receiver Bellville and Brackenfell (n plants = 64, n flowers = 1499). operating characteristic curve (AUC; Swets, 1988). AUC values were calculated four times for each model, by randomly selecting four different 2.5. Seed bank dynamics and seed viability calibration and evaluation datasets. Consensus predictions for the distributions of each species (Araújo and New, 2007) were obtained Soil cores of 22 cm2 were taken to a depth of by 10 cm since using the mean of all model runs, as recommended by Marmion et al. below this depth few broom seeds are found (Downey, 2000). Soil (2009). Consensus forecasts can help to improve model predictive accu- samples were dried at 60 °C, sieved (using a graduated stack of 8, 2, racy, but they are still dependent on the inclusion of ecologically- and 1.4 mm), and seeds counted. Seed viability was determined by realistic models, and it is still debatable as to how many models should a tetrazolium test (Peters, 2005). Seeds were mechanically scarified be used to build a consensus forecast (Araújo and New, 2007; Marmion and imbibed overnight at 25 °C. Seed coats were removed prior to et al., 2009). staining at 35 °C. For G. monspessulana, 33 soil cores were collected at representa- tive areas (i.e. typical density and plant size) in the Klein Constantia 2.7. Risk assessment cellar population. To determine the change in soil seed bank size with increasing distance from adult plants, the seed bank around a We assessed the risk of G. monspessulana and S. junceum in South large isolated individual was sampled. Four soil cores were taken Africa using the Australian weed risk assessment protocol of Pheloung perpendicular to the stem at 50 cm intervals in four directions. et al. (1999) and the guidelines of Gordon et al. (2010) for application For S. junceum, 36 soil cores were collected within a dense stand of of this system outside Australia. For G. monspessulana, an assessment mature plants at Helshoogte Pass. done for Tasmania (http://www.dpiw.tas.gov.au/)andforS. junceum In addition seeds stored for 26 years in dry, dark conditions in an an assessment for Hawaii (Hawaii Pacific weed risk assessment) were envelope were also tested to give some estimate of seed longevity. adapted to South African conditions. In answering question 2.01 of the protocol (is the species suited to South African climates?) we used the 2.6. Species distribution modelling predictions of the species distribution model.

Species presence records were obtained from the Global Biodiversity Information Facility (GBIF; http://data.gbif.org). Obviously spurious 2.8. Management and cost of clearing records (e.g. in the sea), duplicate records, and duplicates within 10′ grid cells were excluded resulting in 372 records for G. monspessulana To calculate the cost and efﬁcacy of current clearing methods, teams and 640 records for S. junceum. Species distribution models (SDMs) from the City of Cape Town's Early Detection and Rapid Response were built using the above mentioned presence records, a randomly- programme were monitored (S. junceum at Helshoogte, G. monspessulana generated set of pseudo-absences, and six different environmental at Klein Constantia dam, Tokai Manor and the Mound at Tokai). Plants factors. Using the strategy of Webber et al. (2011), pseudo-absences were cut at the base with loppers, saws or chainsaws and cut stems for each species were randomly chosen within Köppen–Geiger climate were treated with glyphosate herbicide (Glyphosate at 5% concentra- zones [sourced from the CliMond 10′ historical climate dataset tion, trademark Mamba 360SL) and biomass removed to a waste facili- (Kriticos et al., 2011)], within which presence records for the species ty. Efﬁcacy was assessed one year after the operations (2012) by in question occurred. The environmental variables selected [mean tem- recording resprouting and the number of emerging seedlings. To calcu- perature of the warmest quarter (BIO10), mean temperature of the late the effort (time and costs) required for G. monspessulana eradica- coldest quarter (BIO11), mean moisture index of the driest quarter tion throughout South Africa we assumed similar costs and clearing (BIO33), mean moisture index of the warmest quarter (BIO34) and efforts for all other populations. All maps were produced in ArcGIS 10 mean moisture index of the coldest quarter (BIO35) (Kriticos et al., (ESRI 2010) and statistical analyses conducted in R (R Development 2011)] are thought to be ecologically important for modelling plant Core Team, 2012). 138 S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145

Fig. 1. Genista monspessulana and Spartium junceum in South Africa. a) Typical G. monspessulana habitat in South Africa with plants growing in disturbed sites underneath native and/or alien trees. b) Only at Op-die-Berg, where the main population is growing beneath a Hakea salicifolia hedge, is there invasion into adjacent fynbos vegetation. c) A small resprouting G. monspessulana individual that should have been pulled and not cut. d) Spartium junceum occurs mainly along roadsides or disturbed sites amongst roads. e). S. junceum resprouting after clearing.

3. Results Pass occurred on the road verge (15 m) whereas in disturbed areas, S. junceum is found up to 60 m from the road. No individuals were 3.1. Current distribution at different spatial scales recorded in native vegetation. We estimated the total invaded area in South Africa to be 3.59 condensed ha. The earliest record of G. monspessulana in South Africa is from Newlands on the Cape Peninsula from 1904 (Pretoria National 3.2. Population structure, reproductive size and reproductive output Herbarium). Of the thirteen G. monspessulana records, nine populations still exist (Table 1). G. monspessulana occurs in patches, mostly The different populations of G. monspessulana differed substantially in disturbed and semi-shaded areas (Fig. 1a), such as parklands and in size distribution, but all appear to comprise multiple generations forestry plantations (Fig. 2c and d). All G. monspessulana populations (all curves on Fig. 4a are multi-modal). There were substantial differ- occur on the Cape Peninsula except for one population occurring ences between sites in the size of plants at the onset of reproduction; inland at Op-die-Berg in the Ceres district (Fig. 2b). This population 0.3 m was the minimum size observed for a reproductive plant and originated from a garden escapee. It has been cut regularly in most (73%) individuals taller than 1 m carried seeds (Fig. 4b). The the past 30 years, but continues to spread and is now invading average seed output for a 1 m-tall plant is 1959 (range 789–4894). undisturbed fynbos (Fig. 1b). The total invaded area for South Africa, When comparing all possible additive models to explain onset of re- allowing for some initial clearing (excluding Tokai, as no detailed production for G. monspessulana, the model with log (canopy diameter), spatial data were available for this site, see Table 1), is ~22.7 ha log (height) and site produced the best ﬁt in terms of AIC (a weight of (minimum convex hull) or 0.17 condensed ha. 0.72 out of 1 using the R function AICtab (package bbmle)). However, The ﬁrst S. junceum record in South Africa is from 1858 (McGibbon this only explained 28% of the variance. Log (height) was the best single 1858, as cited by Henderson (2006)). This species now occurs sporadi- predictor (18.7% variance explained), but again there appears to be cally across South Africa, but is most common in the extreme substantial inter-plant variation (e.g. Fig. 4b). south-west (Fig. 3a and b). In the Stellenbosch Municipality, S. junceum The S. junceum population along Helshoogte Pass has a consider- is found mainly in small roadside populations (Fig. 1c), except able proportion of small, immature plants, although plants of up to at Helshoogte Pass where there is a substantial population (5159 indi- 5 m tall were recorded (Fig. 5a). 64% of plants only start reproducing viduals) (Fig. 3d). Almost 40% of the plants along the Helshoogte when larger than 1 m, but again there is substantial inter-plant S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 139

Fig. 2. a) Predicted climatic suitability for Genista monspessulana. Records from the native and introduced ranges (excluding South Africa) were used to train the models. Two different modelling methods were used and model results combined into a single predicted probability of occurrence map (see Methods for details). The bold squares (QDGCs) indicate where G. monspessulana has been recorded. b) All G. monspessulana populations occur in the Cape Peninsula except for one inland population (see Table 1 for population details). Distribution of Genista monspessulana was mapped in detail at two of the study sites, c) Newlands and d) Tokai Manor (inset represents all Tokai populations). variation (Fig. 5b). The best-ﬁt additive model to explain reproduc- canopy of a large isolated individual decreased from 8123 seeds/m2 tive onset incorporated log (basal diameter), log (canopy diameter) within a 0.5 m radius to 1785 seeds/m2 at 2 m. Seed viability was 80%. and log (plant height) (AIC weight of close to 1), explaining 51.7% For S. junceum,seedbanksizerangedfromzeroto21,364seeds/m2, of the variance, but a model with only log (height) was almost as with a median of 455 seeds/m2. Seed viability in the soil was 73%. Seeds powerful, explaining 49.8% of the variance. Therefore, we would rec- collected and stored in an envelope for 26 years still had a viability of ommend that, if plants are to be measured to determine reproductive 37%. capability, recording plant height is sufﬁcient. Reproductive output is high, with a 2 m-tall plant producing an average of 3024 seeds. 3.4. Species distribution modelling

3.3. Seed bank dynamics and seed viability The modelled global distribution (excluding South Africa) of G. monspessulana exhibited high predictive accuracy (AUC = 0.838– The seed bank of G. monspessulana ranged from 909 to 0.868), with high probabilities of occurrence in Mediterranean-climate 22,727 seeds/m2 (median 1970 seeds/m2). The seed bank below the regions of the world (Fig. S3a). Temperature of the coldest quarter 140 S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145

Fig. 3. Distribution of Spartium junceum at a) national, b) provincial, c) district and d) landscape scales. (a) and (b) are based on records from the South African Plant Invaders Atlas (records accessed April 2012). For (a), the predicted climatic suitability for Spartium junceum records from the native and introduced ranges (excluding South Africa) were included. Two different modelling methods were used and model results combined into a single predicted probability of occurrence map (see Methods for details). QDSs indicate where S. junceum has been recorded. Total road distance surveyed for (c) is 252 km.

(r =0.494(GAM)andr = 0.467 (BRT)) and temperature of the important using a BRT (r =0.879c.f.r =0.222(GAM);Fig.S1c,d). warmest quarter (r =0.465(GAM)and r = 0.329 (BRT)) were the The predicted distribution in South Africa was very similar to that of most important predictors of G. monspessulana occurrence (Fig. S1a, b). G. monspessulana, except that S. junceum was predicted to have a In South Africa G. monspessulana was predicted to have a high probabil- wider distribution, particularly in the eastern part of the country ity of occurrence in the south-western part of the Western Cape and (Fig. 3a; Fig. S2b). Most of the existing populations occur within the along the southern coast (Fig. 2a, Fig. S2a). regions predicted to be climatically suitable (Fig. 3a). S. junceum was also predicted to have high probabilities of occurrence in Mediterranean-climate regions of the world (Fig. S3b) and 3.5. Risk assessments exhibited high predictive accuracy at a global scale (AUC = 0.910– 0.936). Mean temperature of the warmest quarter was the most Risk assessments indicate a high potential invasiveness for both spe- important predictor of occurrence using a GAM (r = 0.736 c.f. r =0.05 cies in South Africa (Pheloung et al., 1999). G. monspessulana obtained a (BRT)), but mean temperature of the coldest quarter was the most score of 20 (12 for biogeography, 5 for undesirable attributes and 3 for S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 141

Fig. 5. a) Plant height frequency distributions; and b) size at reproduction for Spartium junceum at Helshoogte Pass near Stellenbosch, produced as per Fig. 4. Fig. 4. a) Plant height frequency distributions; and b) size at reproduction for Genista monspessulana populations. The frequency distributions were produced using the function density[stats] in R. The presence of seed pod stalks, seed pods or flowers et al., 1998), after 10 years, 2 person days to monitor and clear all were used as proxy for reproductive maturity with some jitter added to prevent over populations will suffice. plotting. The fitted line for each site is from a generalised linear model with binomial For S. junceum, the total cost to clear the Helshoogte population of errors and log (plant height) as the explanatory variable. 5159 plants was ZAR 19,500 and took 91 person days. The treatment applied was not effective, with 127 or 43% of examined plants biology/ecology) and S. junceum a score of 16 (7 for biogeography, 3 for resprouting (n = 297 plants examined; Fig. 1d) and 3.7% of plants undesirable attributes and 6 for biology/ecology) (Appendix A). Species overlooked. Resprouting plants were mainly smaller individuals with with scores of 6 or higher are considered to have a high risk of becoming a stem diameter of 97 ± 2.5 mm (95% C.I.) versus a population mean invasive. of 127 ± 0.4 mm (95% C.I.). Within the sampling area (n = 297 plants), only 36 seedlings emerged a year after clearing.

3.6. Management and cost of clearing 4. Discussion

For G. monspessulana, initial clearing of a population of 215 plants High seed production, viability and longevity and a persistent seed took 5 person days and cost ZAR 3.22 per plant (Klein Constantia dam bank in the soil make G. monspessulana and S. junceum populations dif- population). This excludes the costs of herbicide, which was obtained ficult and costly to control. In addition, their capacity for resprouting from the Working for Water programme. Initial G. monspessulana and reaching reproductive age early, their rapid growth rates and ability treatments were only partly effective. One year after the initial clear- to fixnitrogen(Bossard, 2000; DiTomaso, 1998) mean that they could ing at Tokai Manor there were 228 (60% of total) resprouting individ- become widespread and damaging invaders in South Africa. uals, with stem diameters ranging from 1 to 40 mm, but only 54 new The distribution of G. monspessulana appears to be quite restricted, seedlings. After initial clearing of ~30 flowering plants in 2011 at the with only eight populations confirmed. However, the species has the Mound (Tokai) (T. Rossenrode pers. comm.), a follow-up treatment in ability to colonise natural vegetation, and is very invasive in other parts 2012 removed 2425 seedlings and 41 ~30 cm tall plants (seedlings of the world. A relatively large area of South Africa is climatically suitable, missed in the initial clearing) over 12 person days, at a cost of ZAR as predicted from species distribution models (Fig. 3a; Figs. S2a; S3a; 0.84 per plant. All plants were hand-pulled. Richardson and Thuiller, 2007). Formal risk assessment showed it to We estimate that it will take 586 person days or ZAR 81,000 over have a high risk of becoming invasive in South Africa, even more so 10 years to eradicate G. monspessulana from South Africa. A total of than S. junceum. Because options for eradicating it from South Africa 178 person days for adult plant removal is needed in the first year are available, we argue that the eradication of G. monspessulana should with 107 person days (assuming 60% resprouting rate) and 72 person be prioritised. days (6 populations × 12 person days) for seedling removal needed Achieving eradication will be a long-term undertaking if the decay in the second year. Assuming a constant rate of 60% resprouting and rates of G. monspessulana seed banks are similar to those of Scotch 50% removal of soil stored seed bank with annual clearing (Paynter broom (Cytisus scoparius), for which seed banks can persist for up to 142 S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 a decade (Smith and Harlen, 1991). Soil-stored seed banks can be reclassified category 1b nationally; this will ensure compulsory control managed through the application of fire (Alexander and D'Antonio, as part of an invasive species control programme. 2003a,b; Herrera-Reddy et al., 2012), but this has very limited feasi- Since S. junceum has no major impacts and does not spread into bility in the South African range of this species, as most populations native vegetation, it is not an immediate priority for classical biologi- occur in native forests and commercial plantations of alien trees cal control and should not rank high on the biological control priori- where fire cannot be used. Since plants do not achieve reproductive ties list (Nel et al., 2004). As such, while the introduction of a maturity until about two years of age (Adams and Simmons, 1991), biocontrol agent like the eriophyid mite, Aceria spartii, is worth additions to the seed bank can be halted with focused annual clearing considering as part of an integrated management approach, it need and regular removal of new seedlings. With a high percentage of not be prioritised (Craemer et al., 1996; Herrera-Reddy et al., 2012), resprouting, control should focus on hand-pulling, where possible, rath- as it remains to be seen whether this would be a cost-effective option er than cutting (Fig. 1e), since it has been shown to be an effective con- given the current lack of major impacts (cf. de Lange and van Wilgen, trol method (Alexander and D'Antonio, 2003a,b). Ideally, treatment 2010). should commence as soon as flowering starts, i.e. at the end of winter In this study we made use of a multi-scale mapping approach for when plants are easy to detect, but before seeds are produced. The S. junceum to disentangle the factors determining occurrence at added advantage is that wet soils make plants easy to pull up. This will different spatial scales i.e. climate at a large scale and roadside take more clearing time than brush cutting, as each plant needs to be disturbance at a small scale. Accurate spatial distribution at different handled individually, but our data suggest this will be the more effective scales enabled us to make informed recommendations whether in achieving eradication. eradication is a feasible option and illustrated the value of detailed Similar to G. monspessulana, high seed production and high seed dor- spatial mapping of an alien invasive species. mancy in S.junceumallow for a rapid build-up of a persistent seed bank Reasons for the limited distribution of both these species in South in the soil. Although often described as a copious seed producer, with Africa, despite their widespread invasiveness in other regions, remain large and long-lived seed banks (Bossard et al., 2000; Galloni and unexplained. Potential reasons include herbivory (Sheppard, 2000)and Cristofolini, 2003), the seed bank density of 450 seeds/m2 found for a small introduction effort (Atkinson, 2000). Although G. monspessulana S. junceum at Helshoogte Pass is lower than expected, considering is not used as a garden plant (pers. obs.), S. junceum is planted in Western the high seed production of more than 3000 seeds per individual. Cape gardens for its hardiness and long flowering time. Interestingly, The relatively low seed bank density might be due to the impenetrable South African Gmonspessulanaplants are smaller than in other invaded shale-derived soils at this site. Control efforts were somewhat ineffec- areas (Herrera et al., 2011); potentially suggesting that conditions tive. More than 43% of treated plants resprouted, which is not unexpect- for plant growth may be suboptimal. Another reason might be a lack ed since up to 90% of plants can resprout when treated in the rainy of pollinator mutualists (Richardson et al., 2000); pollen limitation in season (Bossard, 2000). Therefore, for effective control a more specific G. monspessulana has been demonstrated in other parts of the invasive protocol and a proper herbicide trial in South Africa is warranted, and, range (Parker and Haubensak, 2002). S. junceum in South Africa pro- as with G. monspessulana, smaller plants should be hand-pulled. duces fewer seeds than other invaded areas (Bossard et al., 2000). One Under both CARA and the weed risk-assessment protocol reason might be the highly specialised flowers, which require a specific (Appendix A), G. monspessulana is classified as a species with the po- pollinator heavy enough to trip the flowers (Cordoba and Cocucci, tential to become a major problem, and legislation should continue 2011). Whether these specialised pollinators are available in South to reflect this. Although some initial research on biological control Africa, and the extent to which they could limit the invasion, needs to for G. monspessulana has been conducted in Australia (Paynter et be determined through observations and plant breeding system experi- al., 2003), populations in South Africa are relatively small and unless ments (Geerts and Pauw, 2009; Ollerton et al., 2012). the focused (species-specific) annual clearing operations do not see Supplementary data to this article can be found online at http:// noticeable declines in G. monspessulana, classical biological control dx.doi.org/10.1016/j.sajb.2013.03.019. should not be required for this species. Given the number of populations, and more importantly, the very patchy distribution of S. junceum populations in South Africa, eradica- Acknowledgements tion of this species is improbable. Moreover, a large percentage of the seeds in the soil seed bank were viable, with viability as high as 37% in We thank Cedric Muofhe, Chris Brown, Jessica Kemp and Nicholas seeds stored for 26 years. As such, even small infestations would re- Bowker for assistance with fieldwork, Tarryn Rossenrode for organizing quire a decade or more of monitoring to confirm eradication clearing and Tony Rebelo for site localities. We acknowledge support (Panetta et al., 2011). from the Working for Water programme of the Department of Environ- Although S. junceum has been recorded as invading undisturbed mental Affairs both through SANBI's Invasive Species Programme, and fynbos (Bromilow, 2010; Henderson, 2001) and riparian vegetation via the collaborative project with the DST-NRF Centre of Excellence (Galatowitsch and Richardson, 2005; Meek et al., 2010), this was not for Invasion Biology on “Research for Integrated Management of Inva- observed in the current study, and all records are from disturbed areas sive Alien Species”. Additional funding was provided by Stellenbosch such as roadsides, wasteland and urban open spaces. This might partly University and the National Research Foundation (to SG and DMR). be an artefact of dispersal, and certainly the spatial distribution and frequent occurrence of S. junceum along roadsides in the Stellenbosch Municipality is consistent with landscape-scale dispersal along roads, Appendix A perhaps partly via mowing and roadwork equipment. The goal for S. junceum management should therefore be to limit Risk assessments of Genista monspessulana and Spartium junceum.We spread where possible, and improve the efficacy of current management assessed the potential invasiveness of both species in South Africa using practices. The Western Cape is the most climatically suitable for the Australian weed risk assessment protocol of Pheloung et al. (1999). S. junceum, but only focusing on the Western Cape is inadequate, as For S. junceum an Australian Weed Risk assessment from Hawaii (Hawaii there are areas in the south and east of the country that are also climat- Pacific weed risk assessment (HPWRA)) and for G. monspessulana aTas- ically suitable (Fig. 3a). Using a Bioclim model, Mgidi et al. (2007) found manian assessment (http://www.dpiw.tas.gov.au/inter.nsf/WebPages/ 45% of South Africa to be potentially suitable for invasion, whereas we SWEN7S74GE) were adapted for South African conditions. found 19%, including much of the eastern part of the country, to be suit- See references at: http://www.hear.org/pier/wra/pacific/spartium_ able, (Fig. 3a). Consequently, we recommend that this species is junceum_htmlwra.htm. S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145 143

Species: Genista monspessulana

Question Answer Reference

Is the species highly domesticated? No Species suited to South African climates Yes, Mediterranean climate of the fynbos biome. 1, 2, 3, this study Native of and invasive in regions with Mediterranean climates Quality of climate match data High This study Broad climate suitability (environmental versatility) Yes, occurs in more than three Köppen–Geiger climate zones 2, 3 Native or naturalised in regions with extended dry periods Yes, e.g. where naturalised in Australia 4, 5 Does the species have a history of repeated introductions outside its natural range? Yes 6 Naturalised beyond native range Yes 6 Garden/amenity/disturbance weed Yes 7 Weed of agriculture/horticulture/forestry No — invades “poorer pastures” 7 Environmental weed Yes 8 Congeneric weed Yes 9 Produces spines, thorns or burrs No Allelopathic Unknown Parasitic No Unpalatable to grazing animals Yes, except to goats 8 Toxic to animals Yes 8 Host for recognised pests and pathogens Unknown Causes allergies or is otherwise toxic to humans No Creates a fire hazard in natural ecosystems Yes 8, 10 Is a shade tolerant plant at some stage of its life cycle Unknown 11 Grows on infertile soils Yes 8 Climbing or smothering growth habit No Forms dense thickets Yes 8, pers.obs. Aquatic No Grass No Nitrogen fixing woody plant Yes 8 Geophyte No Evidence of substantial reproductive failure in native habitat No Produces viable seed Yes Hybridizes naturally Unknown Self-fertilisation Yes 12 Requires specialist pollinators No 13, pers.obs. Reproduction by vegetative propagation No Minimum generative time (years) 2 years 6 Propagules likely to be dispersed unintentionally Yes, along roads and streams 7, 8 Propagules dispersed intentionally by people No Propagules likely to disperse as a produce contaminant No Propagules adapted to wind dispersal No Propagules water dispersed Yes 14 Propagules bird dispersed No Propagules dispersed by other animals (internally) Unknown Propagules dispersed by other animals (externally) Yes, by ants 7, 15 Prolific seed production Yes 6, this study Evidence that a persistent propagule bank is formed (>1 yr) Yes 16, this study Well controlled by herbicides Yes 8 Tolerates or benefits from mutilation, cultivation or fire Yes 8, pers.obs. Effective natural enemies present in South Africa Unknown

1) Richardson and Thuiller (2007); 2) Global Biodiversity Information Facility; 3) Kottek et al. (2006); 4) Australian Government Bureau of Meteorology; 5) Australia's Virtual Herbarium; 6) Herrera et al. (2011);7)Parsons and Cuthbertson (2001);8)Bossard (2000);9)Haubensak et al. (2004); 10) Pauchard et al. (2008); 11) DiTomaso and Healy (2007); 12) Parker and Haubensak (2002); 13) Parker et al. (2002); 14) Hoshovsky (1986); 15) Gómez and Oliveras (2003); 16) Alexander and D'Antonio (2003a,b). 144 S. Geerts et al. / South African Journal of Botany 87 (2013) 134–145

Species: Spartium junceum

Question Answer

Is the species highly domesticated? No Species suited to South African climates Yes, mostly South-Western Cape (this study) Native of and invasive in regions with Mediterranean climates Quality of climate match data High (this study) Broad climate suitability (environmental versatility) No Native or naturalised in regions with extended dry periods Yes, e.g. where naturalised in Australia (refs) Does the species have a history of repeated introductions outside its natural range? Yes Naturalised beyond native range Yes Garden/amenity/disturbance weed No Weed of agriculture/horticulture/forestry No Environmental weed Yes Congeneric weed No Produces spines, thorns or burrs No Allelopathic No Parasitic No Unpalatable to grazing animals No Toxic to animals No Host for recognised pests and pathogens No Causes allergies or is otherwise toxic to humans Yes Creates a fire hazard in natural ecosystems Yes Is a shade tolerant plant at some stage of its life cycle No Grows on infertile soils Yes Climbing or smothering growth habit No Forms dense thickets Yes Aquatic No Grass No Nitrogen fixing woody plant Yes Geophyte No Evidence of substantial reproductive failure in native habitat No Produces viable seed Yes Hybridizes naturally Yes Self-fertilisation Yes Requires specialist pollinators Yes Reproduction by vegetative propagation No Minimum generative time (years) 2 years Propagules likely to be dispersed unintentionally Yes, along roads and streams Propagules dispersed intentionally by people Yes, as ornamental (but Category 1, so is limited) Propagules likely to disperse as a produce contaminant No Propagules adapted to wind dispersal No Propagules water dispersed Yes Propagules bird dispersed No Propagules dispersed by other animals (internally) Unknown Propagules dispersed by other animals (externally) Yes Prolific seed production Yes Evidence that a persistent propagule bank is formed (>1 yr) Yes Well controlled by herbicides Yes Tolerates or benefits from mutilation, cultivation or fire Yes Effective natural enemies present in South Africa No

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