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Seasonal Trends in Colonisation of Protea Infructescences by Gondwana- Myces and Ophiostoma Spp

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Seasonal Trends in Colonisation of Protea Infructescences by Gondwana- Myces and Ophiostoma Spp South African Journal of Botany 2005, 71(3&4): 307–311 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY EISSN 1727–9321 Seasonal trends in colonisation of Protea infructescences by Gondwana- myces and Ophiostoma spp. F Roets1, LL Dreyer1* and PW Crous2 1 Department of Botany, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa 2 Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands * Corresponding author, e-mail: [email protected] Received 6 April 2004, accepted in revised form 18 November 2004 Seasonal growth of the fungal genera Gondwanamyces of Protea. A definite seasonal pattern was observed, with and Ophiostoma (hereafter referred to as ophiosto- colonisation numbers peaking during the wetter winter matoid fungi) on the floral parts of serotinous Protea- months. P. laurifolia was found to be a new host for ceae flowers was investigated. Several new Protea host Ophiostoma splendens and Gondwanamyces capensis. species were found and new knowledge emerged Ophiostomatoid fungi were restricted to dead floral parts, regarding the tissue types colonised by these fungi. and fruiting structures were never observed on living Although floral parts of a wide range of Proteaceae were plant tissue. Both the vector organisms and the specific examined, ophiostomatoid fungi were exclusively ecological function of the ophiostomatoid fungi are still collected from the infructescences of serotinous species unknown, and require further investigation. Introduction The floral diversity of the Cape Floristic Region (CFR) is world- two genera, namely Ophiostoma H. Syd. and P. Syd., renowned. This area includes the Fynbos Biome, which including the species Ophiostoma protearum Marais and contains most of the c. 9 000 plant species (Goldblatt and Wingf., O. splendens Marais and Wingf. and O. africanum Manning 2000) found within the CFR. The fynbos contains Marais and Wingf. (Sporothrix Hektoen and Perkins three dominant plant families: Ericaceae, Restionaceae and anamorphs), and Gondwanamyces Marais and Wingf. Proteaceae (Cowling and Richardson 1995), of which the including the species Gondwanamyces capensis (M.J. Proteaceae is often the structurally dominant member. Wingf. and P.S. van Wyk) Marais and Wingf., and G. The Proteaceae is diverse in terms of number of species proteae (M.J. Wingf., P.S. van Wyk and Marasas) Marais and the range of morphological forms that exist within the and Wingf. (Knoxdaviesia Wingf. et al. anamorphs). These family. In the south-western Cape alone, there are more than two ascomycete genera share the same morphological 330 species in 14 genera (Rebelo 1995). In total, 13 of these characteristics of spherical ascocarps with long necks, but genera are Cape-centred, with 10 endemic to the area (Rourke differ in their anamorphs (Wingfield and Van Wyk 1993) 1998). The Proteaceae is the seventh largest family of vascular and cycloheximide tolerance (Marais 1996). plants in the CFR, with 96.7% of its members confined to this Morphologically similar genera with similar long perithecial area (Goldblatt and Manning 2000). Protea L. species are of necks from the Northern Hemisphere are insect-vectored considerable economic importance to South Africa in terms of (Davidson and Robinson-Jeffrey 1965, Davidson et al. 1967, eco-tourism, horticulture and the dried-flower industry. Davidson 1978, Dowding 1984), and cause important tree Several fungi that are closely associated with the Protea- diseases such as Dutch elm disease (Braisier 1988) and ceae have been discovered and described (Crous et al. 2000a, oak wilt (Sinclair et al. 1987). Some authors have suggested 2000b, Swart et al. 2000, Taylor and Crous 2000, Taylor 2001). that these fungi may also assist bark beetles to overwhelm Many of these cause fungal infections, including diseases of host tree resistance (Christiansen and Solheim 1990), the leaves, stems, roots and seedlings (Crous et al. 2000a, hinting at the existence of mutualistic relationships between 2000b). Very limited attention has, however, been focussed the fungi and the insect vectors. on the apparently non-pathogenic fungi associated with these There is a strong morphological similarity between Northern plants (Marais and Wingfield 1994, Taylor et al. 2001). Hemisphere Ophiostoma species that occur in the galleries Five ophiostomatoid fungal species are currently known of bark beetles on trees (Wingfield et al. 1999) and the to inhabit the infructescences of some serotinous Protea Ophiostoma and Gondwanamyces species present in Protea species, where they are thought to grow as saprobes (Marais infructescences. The morphological similarities revolve around and Wingfield 2001). These ophiostomatoid fungal the flask-shaped ascomata with long necks that are present species are only associated with the infructescences of in both groups. This morphological arrangement suggests Protea species from South Africa. They are grouped into insect spore dispersal. Spores collect in a sticky mass at the 308 Roets, Dreyer and Crous tips of the necks, where insects can readily come into contact Proteaceae were collected from various sites in the Stellen- with them (Upadhyay 1981, Wingfield et al. 1993). bosch region, South Africa (Table 1). Species were selected These morphological similarities are, to some extent, according to the availability of their infructescences in the corroborated by an rDNA-based molecular phylogeny of the region. Their infructescences were examined for the ophiostomatoid fungi by Marais et al. (1998). In this phylogeny, presence of ophiostomatoid perithecia and their anamorphs, the southern hemisphere members of Ophiostoma form a using a dissecting microscope (X100 magnification). This well-supported monophyletic group sister to the type species enabled the identification of the ideal infructescence age for of Ophiostoma, O. piliferum (Fr.) Syd. and P. Syd., which is detecting fungal growth. Ten fruiting structures (c. one year a Northern Hemisphere representative. The southern African old) of each of these species were then collected at each members of the genera Gondwanamyces and Ophiostoma, site (30 samples in total for each species) at three-month however, are clearly paraphyletic, which suggest that the intervals (from February 2000 to November 2001) and morphological similarities between these two genera must be inspected for the presence of ophiostomatoid fungal fruiting the result of convergent evolution (Wingfield et al. 1999). structures. Fungi were identified directly from the host To date, ophiostomatoid fungi in Protea species have only material and from isolations done on Petri dishes containing been found in insect-infested flower heads (Wingfield et al. 2% malt extract agar (MEA; Biolab, Midrand, South Africa) 1988), suggesting that one or more of these insects could and Sigma Streptomycin sulphate (0.04g l–1). act as vector of the fungal spores. Insects associated with In addition, a selection of other Proteaceae present at the Protea infructescences belong to a wide range of families study sites, the Betty’s Bay/Kleinmond area and the Cape (Coetzee and Giliomee 1987a, 1987b, Coetzee 1989, Point Nature Reserve (Western Cape Province), were Wright 1990, Visser 1992). The putative vectors of G. screened for the presence of ophiostomatoid fungi in their proteae have, however, been narrowed down to only two flower heads at different times of the year. These included species, and the vectors for O. splendens have been several Protea species (P. compacta R. Br., P. lepido- narrowed down to four species (Roets 2002). Further carpodendron (L.) L., P. longifolia Andrews, P. magnifica Link, molecular studies are underway to identify the vectors of P. grandiceps Tratt, P. scabra R. Br. and P. speciosa (L.) L.), each of the southern African ophiostomatoid species. a number of Leucospermum R. Br. species (L. conocar The aim of the present study was to examine the seasonal podendron (L.) H. Beuk, L. oleifolium (P.J. Bergius) R. Br. growth patterns of ophiostomatoid fungi within Protea and L. cordifolium (Salisb. ex Knight) Fourc.), two infructescences, while also scanning this niche for new Leucadendron R. Br. species (L. laureolum (Lam.) Fourc. fungal and host associations. The nature and extent of and L. xanthoconus (Knutze) K. Schum.), Diastella ophiostomatoid colonisation were also investigated. thymelaeoides (P.J. Bergius) Rourke, Mimetes cucullatus (L.) R. Br., Aulax umbellata (Thunb.) R. Br. and Spatalla Materials and Methods curvifolia Salisb. ex Knight. These plants were not included in the three-monthly monitoring due to the limited numbers Seasonality and host specificity of available flower heads they presented. They were merely included to help determine the host range of the different Six-month- to one-year-old infructescences and other fruiting fungal species. structures (e.g. cones) of 11 species belonging to the Table 1: Collection sites of Proteaceae infructescences and other fruiting structures in the Stellenbosch region of South Africa Proteaceae species Population site Grid reference Leucadendron rubrum Burm. f. Jonkershoek S: 33° 58.591' E: 18° 56.817' Leucadendron rubrum Stellenbosch Mountain S: 33° 56.743' E: 18° 52.711' Leucadendron salignum Bergius Jonkershoek S: 33° 59.210' E: 18° 57.361' Leucadendron salignum Stellenbosch Mountain S: 33° 56.743' E: 18° 52.711' Protea acaulos L. Jonkershoek S: 33° 59.210' E: 18° 57.361' Protea burchellii
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