A survey of fungal plant pathogens associated with weed infestations ...

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Australasian Plant Pathology, 2005, 34, 369–376

A survey of fungal plant pathogens associated with weed infestations of barberry (Berberis spp.) in New Zealand and their biocontrol potential N. W. WaiparaA,B , L. A. SmithA , A. F. GianottiA , J. P. WilkieA , C. J. WinksA and E. H. C. McKenzieA A Manaaki

Whenua Landcare Research, 231 Morrin Road, Tamaki Campus, University of Auckland, Private Bag 92170, Auckland, New Zealand. B Corresponding author. Email: [email protected]

Abstract. Since the introduction and subsequent naturalisation of five species of Berberis into New Zealand, two species, B. glaucocarpa and B. darwinii have become aggressive invaders of both agricultural and native ecosystems throughout many regions. Both are now targets for a biological control program. A survey for pathogens to be used as potential classical or inundative biocontrol agents was initiated on weed infestations in New Zealand. Five species of primary plant pathogens were found to be associated with systemic leaf, flower and/or fruit disease symptoms, Colletotrichum gloeosporioides, C. acutatum, Pestalotiopsis sp., Phomopsis sp., and Sclerotinia sclerotiorum. The aecial stage of a barberry rust, Puccinia graminis, was recorded from the flowers of B. glaucocarpa, which is a new host record for New Zealand. Additional keywords: inundative biological control, invasive weed, plant diseases, barberry rust.

Introduction Five species of Berberis have naturalised in New Zealand. Berberis darwinii (Darwin’s barberry) and B. glaucocarpa (barberry) have been widely dispersed throughout New Zealand and have become serious environmental weeds. A third barberry species, B. vulgaris (European barberry), although widespread in Canterbury and Otago (Webb et al. 1988) does not yet appear to be as invasive. The remaining two species (B. soulieana and B. wilsoniae) have very limited distributions (Webb et al. 1988). B. darwinii is endemic to Chile and Patagonia (Webb et al. 1988). First introduced into New Zealand in 1946, this species is now widely distributed from the East Cape region southwards, with major stands occurring in Southland and lower North Island. An evergreen shrub growing to ∼4 m tall and found particularly in higher rainfall areas, this species is invasive of native forest or plantation pine (Pinus radiata) stands as well as open hill slopes. Farmers and regional councils view B. darwinii as an expanding threat to pastoral and conservation values and, as a recent immigrant, it will likely continue to move into suitable habitats. Further large infestations are likely to be identified (McGregor 2002). B. glaucocarpa, from the western Himalaya, is common throughout lowland areas of New Zealand (Webb et al. 1988). Extensively used as hedging, this species of barberry, like B. darwinii, is invasive in a wide range of habitats with © Australasian Plant Pathology Society 2005

stands occurring in coastal reserves, grazed dairy pastures and drier sheep grazed slopes from Northland to Southland. First recorded in 1916, it arrived in New Zealand earlier than B. darwinii, and has had longer to naturalise and occupy its potential range. Large stands, as seen with gorse (Ulex europaeus) and broom (Cytisus scoparius), occur but are not yet common. According to a feasibility study (McGregor 2002), both species are serious threats primarily to sparsely vegetated areas of bush and scrub. The invasiveness of these species arises mainly from their production of large quantities of fruits, which are eaten and subsequently dispersed by birds and possums (Allen and Wilson 1992; Williams and Karl 1996). B. vulgaris has a more restricted distribution than either B. darwinii or B. glaucocarpa, being found predominantly in inland areas of Canterbury and Otago. Although first recorded in the wild in New Zealand some 40 years before any other species of barberry, it appears far less invasive than B. darwinii and B. glaucocarpa; its propensity to disperse seems to be more limited (McGregor 2002). This paper presents the results of a survey of fungal pathogens associated with Berberis species and the potential for their use as biocontrol agents of the weed is discussed. Such a survey also represents step 4 in a classical biological control program (Harley and Forno 1992). 10.1071/AP05049

0815-3191/05/030369

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Australasian Plant Pathology

Methods In consultation with the Department of Conservation, regional councils and Landcare Research staff, barberry infestations throughout New Zealand were identified and a sampling program was undertaken to determine if any damaging pathogens were present. B. glaucocarpa, B. darwinii and B. vulgaris were sampled from a total of 43 sites across both the North and South Islands between November 2003 and March 2004 (Fig. 1). Six B. glaucocarpa sites (Stonehurst Farm, Deadman’s Island, Brancott Station, Kowhai River, Cheviot, and Kurow) were visited a second time during February or March 2004 to monitor any seasonal differences in the fungi present. Plant specimens from 25 sites were collected and lodged with the Allen Herbarium (CHR) at Landcare Research, Lincoln, as

N. W. Waipara et al.

voucher records of plant species from which fungal pathogens were sampled. At each site, ten plants were selected and closely inspected for signs of pathogen damage. Other barberry plants in the area were examined more superficially for obvious disease symptoms. Any diseased leaves, leaf petioles, stems, flower buds, flowers, flower petioles or fruit found were placed in paper bags, kept cool and sent to Landcare Research’s laboratory in Tamaki for microscopic examination and culturing. In the laboratory, disease symptoms were recorded and necrotic areas were examined for fungal reproductive structures using a dissecting microscope. On microscopic examination, a number of samples exhibiting suspected fungal infection and disease symptoms were then selected for isolation onto microbiological media (Table 1). Small

Fig. 1. Barberry (Berberis glaucocarpa, B. darwinii, B. vulgaris) sites sampled for fungi in 2003 and 2004.

Fungal pathogens on Berberis spp. in New Zealand


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Table 1. Number of fungal isolations and tissue fragmentsA from barberry samples plated onto media

Table 2. Fungal colonisation (%)A and total number of fungi isolatedB from diseased barberry tissue fragments

Host

Host

Leaf

Sample type Flower

Fruit

B. glaucocarpa B. darwinii B. vulgaris

32 (261) 8 (90) 1 (12)

5 (35) 3 (18) –

11 (96) 2 (20) –

48 (392) 13 (128) 1 (12)

Total

41 (363)

8 (53)

13 (116)

62 (532)

A

Total

Total number of plant tissue fragments plated (in parentheses).

fragments of tissue (3 mm2 ) were cut from the edge of diseased areas and surface sterilised. Sterilisation was usually by immersion in 95% ethanol for 2–3 s, then in 2% hypochlorite for 1–3 min, depending on the toughness of the tissue, followed by rinsing twice in sterile water. The number of tissue fragments plated for each sample was dependent on the number of symptoms observed (Table 1). Immersion in ethanol was omitted on some occasions for tender young leaves or buds. The tissue fragments were blotted dry with sterile filter paper and placed on potato-dextrose agar (Difco Labs, Detroit, MI, USA) with 0.02% streptomycin sulphate (Sigma, St Louis, MI, USA) contained in 9 cm Petri dishes. Plates were incubated under near ultraviolet and white light (12 h photoperiod) at temperatures of 22 ± 2◦ C (day) and 18 ± 2◦ C (night). Fungal colonies that grew out of the tissue fragments and produced diagnostic spores were identified to the species level where possible. Representative isolates were deposited as cultures into the International Collection of Microorganisms from Plants (ICMP) at Landcare Research (http://www.landcareresearch.co.nz/ research/biodiversity/fungiprog/icmp). Representative portions of leaf, flower and fruit samples that exhibited leaf lesions were also placed on moist blotting paper inside a sealable plastic tray (humidity chamber). Samples were incubated at room temperature and were misted with distilled water, when required to maintain elevated humidity for 7–10 days, or until any fungal sporulation developed from the diseased tissues. This method is often particularly useful to observe any latent pathogen infection present on the samples. Fungal identification was undertaken by direct microscopic examination. A rust fungus found at Brancott Station Marlborough was sent to Dr Catherine Aime (USDA ARS Systematic Botany and Mycology Lab, Beltsville, MD, USA) for identification using DNA sequencing. The specimen was sequenced with rust-specific primers that amplify 1400 bp extending from the 5.8 S through ITS2 and the first two divergent domains of the 28 S. Identification was completed by blast analysis on NCBI GenBank. A dried specimen of the rust has been deposited in the New Zealand Fungal Herbarium (PDD), Tamaki, Auckland, as PDD 78317.

Results Many diseased plants were observed across all sites, but B. glaucocarpa appeared to be more susceptible to systemic fungal infection and disease damage than B. darwinii. Percent fungal colonisation [(total number of fungal isolates divided by the number of tissue fragments) × 100] of B. glaucocarpa, B. darwinii and B. vulgaris averaged across all tissue types collected during our survey was found to be 95.7, 98.4 and 58.4%, respectively (Table 2). There was similarly high colonisation of fruit fragments on both B. glaucocarpa and B. darwinii, with several

Mean fungal colonisation (%)B Leaf Flower Fruit

Total

B. glaucocarpa B. darwinii B. vulgaris

88.9 (232) 91.4 (32) 115.6 (111) 92.2 (83) 111.1 (20) 115.0 (23) 58.4 (7) – –

95.7 (375) 98.4 (126) 58.4 (7)

Total

88.7 (322)

95.4 (508)

98.1 (52) 115.5 (134)

Fungal colonisation % = [(total number of fungal isolates divided by the number of tissue fragments) × 100]. B Total number of fungi isolated from fragments (in parentheses). A

tissues, particularly the berry fruit, often having more than one fungus present. Fungal colonisation was also higher in the leaf and flower tissues of B. darwinii than in B. glaucocarpa (Table 2). Although low fungal colonisation was observed for B. vulgaris, only one sample of leaves was plated, so further surveying would be required to determine a more representative sample of the fungi present on this species. A total of 508 fungal isolates was obtained from a total of 532 barberry tissues plated (Table 2). As most of the tissues plated were from leaf spots on B. glaucocarpa (261 pieces), the greatest numbers of fungi were correspondingly also from B. glaucocarpa. A total of 52 fungi was obtained from flower tissues and 134 fungi from barberry fruit (Table 2). Most fungi (375) were isolated from B. glaucocarpa, reflecting the higher number of samples collected for that host. B. glaucocarpa tissues also appeared to be more susceptible to infection by fungi than B. darwinii, a result that was supported by field observations. A total of 21 fungal species was identified on isolation plates from the three barberry species; 19 from B. glaucocarpa, 14 from B. darwinii, and two from B. vulgaris. A further three species were identified separately from plant tissues; a barberry rust, Puccinia graminis was found on B. glaucocarpa flowers; and Aspergillus niger and a species of Rhizopus were directly observed sporulating on wizened B. glaucocarpa berries. Of the 24 identified species, only five species were associated with significant disease symptoms and plant damage: Colletotrichum acutatum, Colletotrichum gloeosporioides, Pestalotiopsis sp., Phomopsis sp., and Sclerotinia sclerotiorum (Table 3). The remaining species are predominantly saprophytic or secondary/opportunistic/sporadic pathogens, probably infecting the host after damage, insect feeding or infection by a primary pathogen, and are therefore unlikely to be sufficiently virulent and/or host specific to be useful as biocontrol agents (Table 4). Colletotrichum spp. were the most commonly isolated fungi across all tissues, with C. gloeosporioides being the most frequently isolated species (128 isolates) (Table 4). Phoma, Phomopsis and other unidentified Coelomycete

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Table 3. Relative abundance of primary pathogens collected from three Berberis species throughout New Zealand Pathogen Colletotrichum gloeosporioides

Total sites (isolates) 13 (128)

Colletotrichum acutatum

9 (57)

Pestalotiopsis sp.A

5 (14)

Sclerotinia sclerotiorumA

1 (2)

Phomopsis sp.

A

12 (64)

Affected tissues, symptoms and host records Young Leaves: Isolated from black lesions that were variable in shape and size. Together, many of these lesions often appeared as a black–red freckled mottle on the leaves. Mature Leaves: Isolated from many different irregular shaped blotches and lesions variable in size and colour. On B. glaucocarpa the lesions were bright red–wine red–brown in colour. On B. darwinii the lesions could be red in colour with a yellowish margin. Occurred on leaves of both species at most of the collection sites. Flowers: Isolated from black–brown dieback on petioles of the flower inflorescence. Also isolated from black petioles and buds of the flower inflorescence where orange spore masses were observed within some lesions. Fruit: Isolated from shrivelled blackened berries. Also from discoloured grey lesions on the berry stalks. Leaves: Isolated from lesions that were variable in colour, shape and size. Black–dark brown–purple–red lesions of circular to irregular shape and size. Lesions were also visible on the underside of the leaf. Fruit: Isolated from blackish tissues on ripe fruit Both these Colletotrichum species can cause serious ‘anthracnose’ diseases on numerous plant species in New Zealand (Young and Fletcher 1997; Pennycook 1989), but can also be saprophytic on the plant tissues of many hosts. Leaves: Isolated from reddish-brown lesions on the leaf edge. The lesions were surrounded by a yellowish chlorotic tissue that spread from the leaf edge into the middle of the leaf. In New Zealand, this genus has been isolated from many different introduced and native plant species (Pennycook 1989). Symptoms appeared as small circular black lesions (2–5 mm) on unripe and ripening berries. S. sclerotiorum, also known as white soft rot or white mould, is a virulent primary pathogen of many horticultural crop species with a very wide host range in New Zealand (Pennycook 1989) and an even wider range worldwide (Farr et al. 2004). Leaves: Isolated lesions were variable in colour, shape and size. Dark brown–wine red–purple– bright red lesions of circular to irregular shape and size (1–10 mm). Lesions were also sometimes visible on the underside of the leaf. Flower: Appeared as blackened tissue in flower buds and flower petioles. Fruit: Isolated from ripening and ripe fruit that had blackened and had a withered appearance. Also isolated from purplish lesions on the fruit of B. darwinii. Phomopsis species are widespread primary pathogens of plant species in New Zealand (Young and Fletcher 1997; Pennycook 1989).

Isolated from B. darwinii only.

fungi were also frequently isolated in the survey (Table 4). Alternaria alternata was the commonest secondary pathogen isolated in the survey with 33 isolates being recovered, mainly from leaf tissues. The remaining species were rare or occasionally isolated, with low frequency. Excised plant tissues incubated in humidity chambers demonstrated that Botrytis cinerea infection caused significant disease of barberry plant tissues (Table 5) and was able to cause complete bunch rot of fruit and flower inflorescences. Although B. cinerea was observed to be uncommon using culturing methods (Table 4), results from the humidity chambers showed the fungus was present and able to cause latent infections of all barberry tissues (Table 5). Barberry rust Orange pustules of a rust fungus were found on a few flowers of B. glaucocarpa collected from Brancott Station in

November 2003 (Fig. 2). Deoxyribonucleic acid sequencing techniques identified the rust as Puccinia graminis as its ITS sequence was identical to AF468044 Puccinia graminis (compared across 400 bp) and AY 114289 Puccinia graminis f. sp. tritici (compared across 1 kb). The record of P. graminis on the flowers of B. glaucocarpa represents a new host/pathogen record for New Zealand, and the first report of the rust on the flowers (normally reported from leaves) of any Berberis species. In our nationwide survey this was the only specimen collected, and it was not recovered from the same site when it was revisited 4 months later. Epiphytic colonisation on Darwin’s barberry Orange/red circular growths were observed on leaves of eight samples of Darwin’s barberry (Fig. 3), at two locations (Barberry Road and Mouats Saddle, Catlins). All leaves collected were covered in these growths, most probably



373

Table 4. Number of fungal isolates from Berberis species collected at 40 New Zealand sites during 2003–2004 Fungi

B. glaucocarpa Flower Fruit

Leaf Acremonium spp. (n = 2)A Alternaria alternata Aureobasidium pullulans Botrytis cinerea Cladosporium spp. (2) Coelomycete spp. (>4) Colletotrichum acutatum Colletotrichum gloeosporioides Diaporthe sp. Epicoccum nigrum Fusarium spp. (4) Fusicoccum sp. Penicillium sp. Pestalotiopsis sp. Phoma spp. (>3) Phomopsis sp. Sclerotinia sclerotiorum Stemphylium sp. Sterile Dark Sterile Hyaline Unidentified Yeast spp. (2) Total fungi A

Total

Leaf

B. darwinii Flower Fruit

Total

B. vulgaris Leaf Total

2 11 3 3 4 26 41 67 0 2 8 1 0 0 32 16 0 1 7 2 5 1

2 1 2 2 0 2 0 12 0 0 1 0 1 0 6 3 0 0 0 0 0 0

3 7 9 1 2 2 14 41 0 1 1 3 0 0 9 17 0 0 1 0 0 0

7 19 14 6 6 30 55 120 0 3 10 4 1 0 47 36 0 1 8 2 5 1

0 9 4 1 3 1 2 1 0 0 8 1 0 13 10 23 0 4 0 2 1 0

0 3 3 2 0 0 0 5 0 0 0 0 0 1 0 5 0 0 0 0 0 1

0 2 2 2 2 0 0 2 0 0 2 0 0 0 9 0 2 0 0 0 0 0

0 14 9 5 5 1 2 8 0 0 10 1 0 14 19 28 2 4 0 2 1 1

1 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 2 0

8 33 23 11 11 31 57 128 4 3 20 5 1 14 66 64 2 5 8 4 8 2

232

32

111

375

83

20

23

126

7

508

n = number of different species isolated. Table 5. Number of barberry samples with latent infection by Botrytis cinerea and Colletotrichum spp. Host Leaf B. glaucocarpa B. darwinii Total A B

Latent infection and sporulation Flower Fruit Bot Col Bot Col

Total Bot Col

BotA

ColA

8 (A2B ) –

2 –

4 2

1 –

4 (A1) 1

2 1

16 3

5 1

8

2

6

1

5

2

19

6

Bot = Botrytis cinerea, Col = Colletotrichum. A = Alternaria sporulation also observed (n = number of samples with Alternaria).

caused by a very common alga, Cephaleuros, growing on the leaf surface (S. Pennycook, personal communication). On further examination after scraping the algal spots from the leaf surface, it was found the leaves were still intact and the epidermis appeared unaffected. Further research would be required to ascertain if these have any impact on the host through possible reduction of leaf area available for photosynthesis, but this was beyond the scope of the present study. Discussion A high level of fungal colonisation was observed on both B. glaucocarpa and B. darwinii, as both species exhibited a wide range of disease symptoms on leaf, flower and fruit tissues. Across all barberry tissues plated, the mean fungal

colonisation was 95.4%, which is relatively higher than that recorded from two previous surveys of plant pathogens of other New Zealand weeds species (Winks et al. 2004). Disease damage on B. glaucocarpa was often widespread, particularly in areas where the plant was also experiencing water stress. As the disease symptoms were observed on both young leaves and reproductive tissues (flowers and fruit), these pathogens could significantly affect the growth and spread of the weed in some areas. Approximately 21 different fungal species were recovered on plates and a further three by direct methods. A number of fungal isolates were cosmopolitan saprophytes or secondary/weak pathogens with little potential as either classical biocontrol agents or inundative mycoherbicides as they lack the required virulence to be considered as

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Fig. 2. Puccinia graminis Berberis glaucocarpa.

pustules


on

flower

petioles

of

Fig. 3. Colonisation of Berberis darwinii leaves caused by the alga, Cephaleuros.

agents. However, five species of primary plant pathogens associated with leaf, flower and/or fruit disease symptoms, Colletotrichum gloeosporioides, C. acutatum, Pestalotiopsis sp., Phomopsis sp., and Sclerotinia sclerotiorum, may warrant further investigation. C. gloeosporioides was consistently recovered in lesions on diseased barberry tissues and is common in New Zealand (di Menna and Parle 1970; Pennycook 1989; Young and Fletcher 1997). Host specific strains are known (Walker 1980) and have been developed as both classical and inundative biocontrol agents against a number of weed species. The first plant pathogen to be registered as a bioherbicide was a virulent strain of C. gloeosporioides (f. sp. malvae) for control of weed species belonging to the Malvaceae such as round-leaved mallow (Malva pusilla) (Morin et al. 1996; Mortensen and Makowski 1992). In Canada, C. gloeosporioides (f. sp. hypericum) is a highly virulent pathogen that infects all aerial parts of St John’s Wort (Hypericum perforatum) (Morrison et al. 1998). Hawaiian

researchers have also introduced a strain of the fungus to Hawaii and French Polynesia, resulting in the successful biocontrol of Miconia calvescens in both places (Killgore et al. 1997; E. M. Killgore, personal communication). Additional weed biocontrol with C. gloeosporioides strains are also underway for dodder (Cuscuta australis), northern jointvetch (Aeschynomene virginica), dwarf mistletoe (Arceuthobium tsugense) and Hakea sericea (Van Rooj and Wood 2003). S. sclerotiorum, although reported to cause many economically significant disease losses to crops (Pennycook 1989), has also been formulated as an inundative mycoherbicide for the control of giant buttercup, Ranunculus acris (Verkaaik et al. 2004) and Californian thistle, Cirsium arvense (Hurrell et al. 2001; Harvey et al. 1994) in New Zealand. This fungus is also capable of causing disease on a number of other weed species such as ragwort, Senecio jacobaea, in New Zealand (Waipara et al. 1993). Although this fungus is plurivorous on many crop plants there is often minimal risk to non-target hosts when using this as mycoherbicide in non-cropping systems (Bourdôt et al. 2001). Given recent developments in the formulation technology and risk assessments of using this fungus for weed biocontrol, the prospects of using Sclerotinia-based products against barberry may be warranted. Phomopsis species have also been associated with minor shoot damage on gorse and broom (Johnston et al. 1995); however, no biocontrol potential for these isolates was observed during glasshouse inoculation trials (Johnston and Parkes 1994). Phomopsis species have a wide host range across other plant species (Pennycook 1989; Young and Fletcher 1997), with many associated with pre- and postharvest diseases on a variety of economic crops (Pennycook 1989; Farr et al. 1989). To date there are no or few examples of using strains or species of either C. acutatum, Pestalotiopsis or Phomopsis for weed biocontrol, although Phomopsis amaranthicola is under development as a post-emergence bioherbicide against pigweeds (Amaranthus spp.) in Florida, USA (Morales-Payan et al. 2003). Further research is needed to elucidate the prospects of C. acutatum or Pestalotiopsis, as few successful overseas examples are reported for developing these fungi as biocontrol agents. Two species of Phomopsis have previously been reported on barberry species elsewhere (Farr et al. 2004), but none of the remaining pathogens identified in New Zealand have yet been reported from any barberry species. The origin of such pathogens on New Zealand barberry populations is therefore unknown. Further research is needed to elucidate whether these pathogens were introduced from the exotic range with the original importation of the host, subsequent dispersal events, or selection of local pathogenic strains post introduction.


The observation of P. graminis on the flowers of B. glaucocarpa was significant as a new host/pathogen record for New Zealand and may also be the first time the rust has been found on the flowers of any Berberis species. P. graminis has a worldwide distribution on many Berberis spp. (Farr et al. 2004). The rust has a heteroecious life cycle that involves both uredinial and telial infection of a broad range of grasses and cereals of economic importance (Pennycook 1989). This is the first time the additional aecial life stage has been found in New Zealand, and is significant as the aecial stage on Berberis species is an integral part of its lifecycle in North America and Europe (McGregor 2002). Thus, Berberis species are alternate hosts for P. graminis and provide an over-wintering reservoir for infection of cereals and grasses in the ensuing spring, an additional reason for controlling Berberis infestations. In addition, as aecia are not a repeating stage in the life cycle, aeciospores from the pustules found on B. glaucocarpa could only infect a cereal or grass host and would not spread directly to other B. glaucocarpa plants. In New Zealand, the rust also appears to be rare on Berberis spp., causes limited disease symptoms on this host, and therefore has little biocontrol potential against barberry. The most promising species isolated were C. gloeosporioides and Phomopsis sp., for which pathogenic host-specialised strains of these fungi have been reported in other weed biocontrol projects overseas, as well as S. sclerotiorum, which is currently under development for biocontrol of other weed species. Further research is now proposed to investigate the full inundative biocontrol potential of these pathogens that were associated with significant leaf, flower and fruit disease symptoms using inoculation trials to further elucidate their taxonomy, epidemiology and pathogenicity. Acknowledgements We thank the many Department of Conservation and Regional Council staff for assistance with sampling, and the many land owners for allowing access across their land. Dr Catherine Aime (USDA ARS Systematic Botany and Mycology Lab, Beltsville, MD, USA) for DNA sequencing work. Shaun Pennycook for fungal/algal biosystematics assistance and manuscript draft reviews. National Biocontrol of Weeds Collective New Zealand for financial support. References Allen RB, Wilson JB (1992) Fruit and seed production in Berberis darwinii Hook, a shrub recently naturalised in New Zealand. New Zealand Journal of Botany 30, 45–55. Bourdôt GW, Hurrell GA, Saville DJ (2001) Risk analysis of Sclerotinia sclerotiorum for biological control of Cirsium arvense in pasture: ascospore dispersal. Biocontrol Science and Technology 11, 119–139. doi: 10.1080/09583150020029808


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