Australasian Plant Pathology

, Volume 47, Issue 4, pp 379–387 | Cite as

The rust fungus Puccinia arechavaletae, a potential biological control agent of balloon vine (Cardiospermum grandiflorum) in South Africa. I: Biology

  • Andries Fourie
  • Alan R. Wood
Original Paper


Studies on the rust fungus Puccinia arechavaletae, were conducted to determine its potential for use as a classical biological control agent against the alien environmental weed Cardiospermum grandiflorum in South Africa. The production of basidiospores is a crucial stage in the life cycle of this microcyclic rust species, and was determined to optimally occur at 20 °C, under high relative humidity (above 90%), in the presence of free water. The first basidiospores were released from mature telia after being incubated for 4 h under optimum conditions, reaching a peak of production after 24 h. Germination of basidiospores optimally occurred at 20 °C, and they were extremely vulnerable to desiccation. Germinating basidiospores directly penetrated epidermal cells of South African C. grandiflorum within which a vesicle formed, followed by rapid radial colonization of the leaf tissue by fungal mycelium. The first symptoms observed were small chlorotic spots on the leaves from 14 days onwards, with telial pustules appearing between 14 and 21 days post inoculation. The rust P. arechavaletae was shown to be highly pathogenic towards South African C. grandiflorum, causing severe disease symptoms with a detrimental effect on plant health and vigor.


Cardiospermum grandiflorum Sapindaceae Classical biological control Invasive weed Environmental weed South Africa Puccinia arechavaletae 


Cardiospermum (Sapindaceae; Paullinieae) is a genus of 17 species (, of which four species are widespread in tropical regions (C. corindum L., C. grandiflorum Sw., C. halicacabum L. and C. microcarpum Kunth.), one is restricted to Namibia (C. pechuelii Kuntze), and the remaining species occur only in the Americas (Gildenhuys et al. 2013). Cardiospermum grandiflorum (balloon vine) is native from Mexico southwards to Argentina (Gildenhuys et al. 2013). It was first recorded in 1912 from South Africa, where it had probably been introduced as an ornamental plant. Since then it has become a weed in many parts of the country with the KwaZulu-Natal Province being the most severely affected (Henderson 2001, 2006; Olckers 2004). It is a serious invader of mostly forest margins, watercourses and urban open spaces in South Africa (Henderson 2001), and has also invaded other countries such as Australasia and Hawaii (Carroll et al. 2005; Simelane et al. 2011). In eastern Australia, C. grandiflorum is a declared environmental weed and has invaded areas throughout Queensland and in many districts of New South Wales (Batianoff and Butler 2002; Bear et al. 2001; Carroll et al. 2005). The smaller congeners, C. halicacabum and C. microcarpum, are also considered to be invasive or weedy in certain areas of the world (Anning and Yeboah-Gyan 2007; Carroll et al. 2005; Gildenhuys et al. 2013; Harris et al. 2007; Johnston et al. 1979).

Many characteristics contribute to the success of balloon vine as an invader. Sturdy stems with tendrils enable it to climb up and over other plants, where it forms dense canopies that completely smother the underlying indigenous vegetation. It produces large numbers of light-weight, inflated fruit capsules that are carried by wind, or which easily float on water dispersing the plant along waterways (Bear et al. 2001; Carroll et al. 2005; Gildenhuys et al. 2013; GISD 2005; Harden 2002). In addition, the seeds of Cardiospermum species are very hard, which may result in extended seed longevity in the soil (Johnston et al. 1979).

In South Africa, due to the increasing level of invasion together with the known invasiveness of balloon vine throughout the world, it is considered that balloon vine poses an increasing threat to natural vegetation. It is therefore classified as a category 1b invasive plant in South Africa (NEM:BA Act 10 of 2004; Alien and Invasive Species Regulations as published in the Government Gazette 1 August 2014), meaning that it is prohibited and must be controlled or eradicated wherever it occurs. There are at present no herbicides registered for use against balloon vine in South Africa and the only method of control is by physically removing plants, which is expensive and difficult to implement (Simelane et al. 2011). It is known from the literature that destructive pathogens do occur on C. grandiflorum in South America (Farr and Rossman 2018), and the plant was consequently targeted for biological control (biocontrol). In addition, the implementation of biocontrol against emerging weeds such as balloon vine, which are in a relatively early state of invasion, can potentially reduce clearing costs and increase the chance of successful control (Olckers 2004).

Field surveys were conducted in Argentina with the aim of finding potential pathogen and insect biocontrol agents. During these surveys, the rust fungus Puccinia arechavaletae Spegazzini, was observed to be damaging to C. grandiflorum under natural growing conditions in the field (McKay et al. 2010). Puccinia arechavaletae is an autoecious microcyclic rust fungus (Hennen et al. 2005), that completes its life cycle on a single host, making it an attractive prospect for biocontrol. Many pathogen biocontrol agents have been implemented successfully against alien invasive weed species throughout the world (Berner and Bruckart 2005; Ellison and Barreto 2004; Morin et al. 2006a; TeBeest et al. 1992), including South Africa (Morris 1991; Morris et al. 1999). This paper reports on the biology of P. arechavaletae, with the aim of using this rust as a classical biocontrol agent of balloon vine in South Africa. This includes studies on the influence of environmental factors on basidiospore production, the infection process, and pathogenicity studies.

Materials and methods

Germination of teliospores and production of basidiospores

An isolate of P. arechavaletae was collected during a field survey in Misiones Province in Argentina, from a biotype of C. grandiflorum that matches the morphology of the South African weed. This isolate was brought back to the quarantine facilities of the Agricultural Research Council – Plant Protection Research, Weeds Pathology Unit in Stellenbosch, South Africa. The rust was established on South African C. grandiflorum, and maintained by repeated inoculations of fresh plant material.

Balloon vine plants were inoculated using a similar inoculation procedure as used by Morin et al. (1993) for the microcyclic rust Puccinia xanthii Schwein. Briefly, leaf discs (8 mm in diameter) bearing mature telia (3–4 weeks old) of P. arechavaletae were cut from infected balloon vine plants, and placed onto the surface of 2% water agar in 90 mm Petri dishes (20 leaf discs/Petri dish), with the telia on the side away from the water agar. The Petri dish was inverted and fixed to the roof of a 25 cm diameter plastic plant pot. A plant of C. grandiflorum was also placed within a 25 cm diameter plastic plant pot. The inside of the pots, as well as the plant, were sprayed with a fine mist of sterile distilled water, the pot containing the telia inverted over the one with the plant, the pot chamber sealed with masking tape, and incubated at 20 °C for 24 h in the dark. After incubation the pot chambers were opened and the plant transferred to a temperature-controlled greenhouse at 25 °C ± 1 °C day temperature and 20 °C ± 1 °C night temperature for the duration of the study. Many individual plants could be inoculated, each in their own pot chamber, on the same occasion.

This inoculation method, or a modification thereof, was used for all experimental procedures detailed below. The modification was done to obtain germination of telia over microscope glass slides, allowing for quantification of basidiospore production under different environmental conditions.

A standard glass microscope slide (76 mm in length) was positioned upon a 45 mm Petri dish, which was placed within another 90 mm Petri dish. The microscope slide was elevated so that 20 ml of sterile distilled water could be placed within the larger Petri dish without the slide getting wet. Leaf discs (8 mm diameter) bearing mature telia were cut with a cork borer from infected C. grandiflorum leaves and divided into eight equal sections (each 6.28 mm2). One section was placed on a small block of 2% water agar in a 90 mm Petri dish with the telia on the side of the leaf not facing the water agar. The telial disc was lightly sprayed with a fine mist of sterile distilled water, and this Petri dish was inverted and placed over the Petri dish containing the microscope slide, and the two dishes were sealed with parafilm. Eight such inoculation chambers could be obtained using the eight pieces from one leaf disc (reducing variation in viability between telia), and these were incubated under various environmental conditions. After 24 h, the chambers were opened, a drop of Aniline blue in Glycerol added to the glass slide directly underneath where the leaf disc has been positioned, covered with a cover slip and observed microscopically so that the number of basidiospores could be determined.

The glass slides with stained basidiospores were examined under normal light using the 40 × eye objective of a Nikon microscope (Eclipse E600), equipped with a digital camera (DS Camera Head DS-5 M) and a control unit for visualization and measurements (DS Camera Control Unit DS-L1). The basidiospores were uniformly distributed directly underneath the telia, but numbers varied along the edges. As a result the fields examined were taken more to the center of the microscope slides. This magnification rendered a visible field on the camera control unit of 0.07084 mm2 (308 × 230 μm). All basidiospores present within a field were counted, and five fields were counted for each replicate sample or slide and the mean values determined. The number of basidiospores produced per mm2 were calculated from the means.

Effect of temperature on basidiospore production

Glass slides in inoculation chambers, as detailed above, were incubated in the dark at different temperatures ranging from 5 to 30 °C (5, 10, 12, 14, 16, 18, 20, 22, 24, 26, 28, 30). Five replicate inoculation chambers were used for each temperature and the number of spores determined.

Effect of relative humidity on basidiospore production

Glass slides in inoculation chambers were incubated as detailed above, but different saturated salt solutions were added to the inoculation chambers to alter the relative humidity (RH), instead of the sterile distilled water. The salts used were selected according to information from Dhingra and Sinclair (1986), to provide the following RH at 20 °C: NH4NO3 = 65.5%; (NH4)2SO4 = 80.5%; KCl = 85%; MgSO4.7H2O = 90%; KH2PO4 = 96.5%; and sterile distilled water for 100%. All the salts used were of analytical grade. Saturated solutions were prepared and 20 ml added to each inoculation chamber. Five replicate inoculation chambers were used for each RH and the number of spores determined after 24 h.

Basidiospore production process under optimum conditions

Basidiospore production was measured under optimal conditions (20 °C and 100% RH) using the inoculation chambers as detailed above, but the microscope slides were removed after 2, 4, 6, 8, 16 and 24 h following inoculation, and the number of basidiospores determined. Three replicate inoculation chambers were included for each time interval.

The percentage of basidiospores that had germinated under optimal conditions was determined for the same time intervals by inverting telial bearing leaf discs directly over a Petri dish containing 2% water agar (instead of glass slides). After each time interval a drop of Aniline blue in Glycerol was added directly to the surface of the agar plate, covered with a cover slip and 100 basidiospores per replicate examined under the light microscope for germination. Three replicate inoculation chambers were included for each time interval. Basidiospores were considered to have germinated if the length of the germ tube was at least equal to the spore diameter.

Effect of temperature on basidiospore germination

Glass slides in inoculation chambers, as detailed above, were incubated in the dark for 5 h at 20 °C, after which the Petri dishes were opened, the leaf discs bearing telia removed, the dishes resealed and then incubated at temperatures of 5, 10, 15, 20, 25, and 30 °C for a further 24 h. The percentage of basidiospores germinated was determined after examining 100 basidiospores per replicate. In addition the length of 10 randomly chosen germ tubes were measured using the light microscope, for each replicate. Four replicates were included for each temperature treatment.

Effect of exposure to relative humidity on basidiospore germination

Following the production of basidiospores under optimal conditions, the impact of RH during a further period of exposure to different RH levels on the germination of basidiospores, was determined. Basidiospores were produced in inoculation chambers, as detailed above, but the glass microscope slides were replaced with cover slips. After 5 h the inoculation chambers were opened, the cover slips with basidiospores removed, placed in chambers with a RH % ranging from 65 to 100 as used for the relative humidity study, and sealed with parafilm. After exposure for a further 0, 2, 4, 6, 8, and 24 h, the cover slips were removed from the RH chambers, inverted onto 2% water agar in Petri dishes, and then incubated at 20 °C for 24 h. Three replicate RH chambers were included for each exposure time interval, and 100 basidiospores per replicate were examined under the light microscope for germination.

Infection process on the host plant

Balloon vine plants were inoculated in pot chambers, as detailed above. Plants were examined for a month after inoculation for symptom development.

To examine teliospore germination and the production of basidiospores, cross sections were made of the telia bearing leaf discs that were used during the whole plant inoculations, at 1, 2, 3, and 4 h after exposure to favorable conditions. Samples were mounted in a drop of Aniline blue in Glycerol, and observed under a light microscope. For basidiospore germination and penetration studies, C. grandiflorum leaves were removed from inoculated plants and prepared for microscopical analysis at 4, 5, 6, 7, 8, 16 and 24 h following inoculation with P. arechavaletae, and daily thereafter for 14 days. The leaves were cleared and stained according to the method of Bruzzese and Hasan (1983) by placing the whole leaves in a clearing and staining solution for 24 to 48 h, and then destained for 2 h, after which the samples were examined under the light microscope. Three replicate plants with 3 replicate leaves were included for each time interval. The plants were monitored for 1 month for the expression of disease symptoms.

Impact of infection on plant growth

Seeds of C. grandiflorum were planted in autoclaved vermiculite and germinated in an incubator at 35 °C. The seedlings were transplanted into 18 cm pots containing exactly 2 L of a steam-pasteurized sand: bark mixture (1:1 v/v), and kept under normal greenhouse conditions. Every second day, the plants were randomly moved around in the greenhouse to facilitate similar growing conditions. Six week old plants were inoculated with P. arechavaletae as detailed above, in pot chambers. They were inoculated either once, twice or three times, with two weeks between successive inoculations. Uninoculated C. grandiflorum plants were included as controls, and eight replicate plants were used per treatment. Eight weeks following the first inoculations, the plants were visually rated for the severity of disease symptoms. The rating system is given in the key to Table 1.They were then harvested, their roots rinsed free from soil under running tap water, and air dried in paper bags for 14 days, after which the dry root- and shoot mass were determined.
Table 1

Disease severity and impact on the growth of C. grandiflorum at eight weeks after inoculation with P. arechavaletae


Disease severity

Dry weight (g)

Rating (0–4)a



Total biomass

Uninoculated control – Week 0


0.42 db

1.74 D

2.15 d

Uninoculated control – Week 8


1.50 a

5.27 A

6.77 a

Inoculated × 1 – Week 8


1.05 b

4.28 B

5.33 b

Inoculated × 2 – Week 8


0.73 c

2.78 C

3.5 c

Inoculated × 3 – Week 8


0.64 c

2.80 C

3.44 c

aDisease severity was determined by visually rating each plant on a scale of 0–4, where 0 = no visible symptoms e.g. chlorosis, or pustules present; 1 = little chlorosis or a few pustules present, up to 25% of leaf area affected; 2 = mild symptoms, up to 50% affected; 3 = severe symptoms, up to 75% affected, and 4 = extremely severe symptoms, more than 75% of total leaf area covered with rust pustules, with extensive necrosis

bTreatments followed by different letters are significantly different (p ≤ 0.05), according to Duncan’s multiple range test

Data analysis

Completely randomized designs were used for the whole-plant experiments, and all experiments were repeated twice. Data was statistically analysed according to Duncan’s multiple range test, using the SAS-system (SAS User’s guide 1999).


Effect of temperature on basidiospore production

Basidiospores of P. arechavaletae were produced over a reasonably wide temperature range, with high levels of production between 18 and 22 °C and an optimum temperature of 20 °C (Fig. 1). No basidiospores were produced below 10 °C, or above 28 °C.
Fig. 1

Effect of temperature on basidiospore production of Puccinia arechavaletae, 24 h after incubation at high relative humidity (100%). Scatterplot of 5 replicates per temperature, with a smoothed line running through the means

Effect of relative humidity on basidiospore production

The saturated salt solutions used in the small inoculation chambers allowed for maintenance of RH within the inoculation chambers. The telial discs, however, needed to be sprayed with a fine mist of distilled water to provide some free water for germination, without interfering with the RH. At optimal temperature, the highest production of basidiospores occurred at high relative humidity (100%) and sharply declined as RH was reduced (Fig. 2).
Fig. 2

Effect of relative humidity on basidiospore production of Puccinia arechavaletae, 24 h after incubation at 20 °C. Scatterplot of 5 replicates per temperature, with a smoothed line running through the means

Basidiospore production process under optimum conditions

Under optimal environmental conditions (20 °C and 100% RH), the first basidiospores released from teliospores were observed after 4 h, and numbers increased significantly the longer it was exposed to favourable conditions (Fig. 3). After 6 h, there were more than 1000 basidiospores mm−2 produced with a maximum of just over 10,000 mm−2 after 24 h. Germination under these same conditions was also rapid, with low levels detected after 6 h (9%), followed by a sharp increase to almost 100% after 24 h.
Fig. 3

Average production (primary y-axis; black line, ±s.e.), and germination (secondary y-axis; grey line, ±s.e.) of basidiospores over a 24 h period, from telia of Puccinia arechavaletae, after exposure to optimal environmental conditions (20 °C and 100% RH)

The effect of temperature on basidiospore germination

After 24 h, 93–95% of P. arechavaletae basidiospores germinated on the water agar surfaces, regardless of the temperature (5–30 °C) at which they were held after the initiation of germination under optimal conditions. Significant differences were however observed in germ tube length, with the longest measured at 20 °C, a little shorter at 25 and 30 °C, and notably shorter germ tubes produced at 15, 10 and 5 °C. (Fig. 4).
Fig. 4

Average germ tube length (± s.e.) of germinating basidiospores of Puccinia arechavaletae after 24 h incubation at different temperatures. Basidiospores were produced beforehand by incubating telia for 5 h at 20 °C, and thereafter they were incubated at the tested temperatures. Different letters above the bars are significantly different (p ≤ 0.05), according to Duncan’s multiple range test

Effect of exposure to relative humidity on basidiospore germination

Germination of basidiospores was strongly influenced by humidity during a period of exposure between production and germination. An average of 93.3% basidiospore germination was obtained immediately after their production (0 h exposure). At 100% RH, exposure for 2 h did not reduce the average germination percentage (93.3%), but longer exposure periods increasingly reduced it, with only 12% germination after 24 h of exposure. Exposure to lower RH had an immediate impact on spore viability. After just 2 h of exposure at 96.5% RH, only 8% germination was obtained, and this reduced to 1% at 24 h exposure. At 90% RH, only 1.3% germination was obtained after 2 h exposure, whilst no spores germinated after 6 h exposure (or longer) (Fig. 5). At RH of 85, 80 and 65%, no spores germinated after any period of exposure.
Fig. 5

Germination of Puccinia arechavaletae basidiospores after exposure for various time periods at varying relative humidity, followed by 24 h incubation at 20 °C. Relative humidity during period of exposure = 100% (solid black); 96.5% (solid grey), and 90% (dashed grey)

The infection process on the host plant

Telia on the abaxial leaf surface of C. grandiflorum were scattered or concentrically grouped together and contained one- or two-celled teliospores. The teliospores differed considerably in size with the one-celled spores measuring 19–25 × 16–19 μm (mean 21.4 × 17.8, n = 20), and the two-celled spores 20–23 × 15–21 μm (mean 26.3 × 18.7, n = 20). Their shape varied from globose, ellipsoid to oblong. The teliospores started to germinate within 1 h after exposure to favorable environmental conditions, which was visible as a grayish layer covering the spores. Germ tubes started to emerge from the apical germ pores of one-celled teliospores, while the two-celled teliospores predominantly germinated simultaneously through septal germ pores on the proximal cells, and sub-equatorial pores on the distal cells. Mature metabasidia (37–44 μm long) could be observed from 3 to 4 h, consisting of 4 individual cells after development of three septa, and each cell giving rise to a sterigmatum (7–10 μm long). A single basidiospore (7–8 × 10–11 μm) was produced on each sterigmatum, and basidiospore release was observed from 4 h onwards (Fig. 6). Germination of basidiospores on the leaf surface of C. grandiflorum started 6 h after the initiation of their production, with the majority of spores producing very short germ-tubes. Direct penetration of host epidermal cells mostly occurred, with the occasional formation of a small appressorium. Penetration was followed by the formation of a vesicle within the epidermal cell that was visible after 24 h. The first symptoms appeared on the leaves of C. grandiflorum as small chlorotic spots, typically 14 days following inoculation with P. arechavaletae. This was occasionally as early as 7 days post inoculation on newly emerged or young succulent leaves. Telia with teliospores first erupted from 14 to 21 days following infection by the rust basidiospores, mostly on the abaxial surfaces of leaves (Fig. 7), but also on C. grandiflorum stems. Young telia were reddish-brown in color, becoming darker brown to almost black as they matured.
Fig. 6

Germinating teliospore of Puccinia arechavaletae, showing the 4-celled metabasidium, each cell of which produces a basidiospore

Fig. 7

Mature telia of Puccinia arechavaletae on the abaxial leaf surface of Cardiospermum grandiflorum leaves, 21 days following inoculation

Impact of infection on plant growth

The first symptoms were visible after 2 weeks, thereafter the infected leaves became increasingly necrotic until they shriveled up and fell from the plant. The rust was also able to infect the stems of balloon vine. Close to 50% of the leaf area was infected on plants that were inoculated only once, and the disease severity significantly (p ≤ 0.05) increased for plants that were inoculated twice or thrice (Table 1). There was a significant decrease in the root-, shoot-, or total plant biomass, when inoculated with the rust (Table 1). One inoculation caused a marked decrease in dry plant weight, even though some re-growth did occur. Additional inoculations resulted in completely stunted plants that were not able to regrow by the end of the experiment. Despite inciting severe disease symptoms, there was no mortality of plants for any of the inoculation regimes by the end of the study.


Balloon vine, C. grandiflorum, is recognized as an invasive weed in various regions of the world, including in South Africa. The environmental parameters needed for successful infection of the weed C. grandiflorum by the rust P. arechavaletae were investigated during this study. This background information of the rust’s biology is essential for future studies, and possible implementation as a biocontrol agent of balloon vine in South Africa. It was observed during all the experiments carried out that the pedicels of the teliospores are persistent, therefore the teliospores are not a dispersal stage, and this function is only carried out by the delicate basidiospores. Basidiospore production by germinated teliospores was rapid, and very high quantities were produced at optimal temperature (20 °C) and RH (100%) conditions. Basisiospore production and germination was particularly sensitive to RH, these declining rapidly as RH decreased. Even when produced under optimal conditions for an initial period of five hours, and then exposed to reduced RH for as little as two hours, the percent germination dramatically declined. This indicates that the basidiospores are sensitive to desiccation, and it can be concluded that effective dispersal and successful infection will be restricted to rain events or nights with sufficient levels of dew formation when a RH of 100% occurs.

The short-lived, fragile, basidiospores will most probably limit the distribution of P. arechavaletae to areas with favorable environmental conditions (notably areas with relatively high rainfall) in South Africa. Additional field surveys are necessary to determine the climatic distribution of P. arechavaletae in its native range, this information could be used in the development of climatic matching models to predict the potential distribution of this rust fungus within South Africa.

Field surveys have shown that the rust fungus P. arechavaletae causes severe disease of C. grandiflorum in its native range (McKay et al. 2010). The current study demonstrated that the rust is highly pathogenic towards South African C. grandiflorum, and it is able to inflict considerable damage on the target weed. Host range testing needs to be performed before P. arechavaletae can be considered for release as a biological control agent against C. grandiflorum in South Africa.

Pathogenicity tests were conducted to firstly determine if P. arechavaletae is able to infect and cause significant disease on South African C. grandiflorum, and secondly to attempt an objective estimate of the potential impact of the rust on this weed. Although the rust did not cause plant mortality during this study, it was highly pathogenic towards balloon vine, causing severe disease symptoms, and having a detrimental effect on plant growth and vigour. The three inoculation regimes used provided good results in terms of impact on the plants, but they were still rather conservative. Numerous inoculation events may occur in the field, especially during extended periods of favourable environmental conditions. It will therefore be easy to amplify the potential impact of the rust under artificial conditions, for instance with repeated inoculations, but this will again most likely be a misrepresentation of what truly happens in the field. Morin et al. (2002) showed that repeated inoculations with the rust fungus Puccinia myrsiphylli (Thüm.) G. Winter, had a devastating effect on different growth indices of bridal creeper during a simulated greenhouse impact experiment. In the field the impact of this rust has been significant in coastal areas of Australia where environmental conditions are ideal for rust epidemic development, but its effects are not as prolific under suboptimal drier inland conditions (Morin and Edwards 2006; Morin et al. 2006b). In accordance with Berner and Bruckart (2005), it is important to keep in mind that greenhouse or laboratory tests are only crude measures of the field potential of any pathogen. One would only be able to measure the true potential of P. arechavaletae once it is released into the field.



We thank the research personnel at the USDA-ARS-South American Biological Control Laboratory in Argentina for their assistance in obtaining isolates of the rust, Puccinia arechavaletae for this study. Financial support for this research project was provided by the Department of Environmental Affairs, Natural Resources Management Programme (DEA:NRMP), South Africa.


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Copyright information

© Australasian Plant Pathology Society Inc. 2018

Authors and Affiliations

  1. 1.Weeds DivisionARC-Plant Protection ResearchStellenboschSouth Africa
  2. 2.FMC Agricultural SolutionsPretoriaSouth Africa

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