Fungal pathogens of Calotropisprocera (rubber bush), with two new records from Brazil

Transcription

1 Atlstralasian Plant Pathology (1999) 28: Fungal pathogens of Calotropisprocera (rubber bush), with two new records from Brazil Robert W. BarretoA, Harry C. EvansB and Alan W.V. PomellaA *Departamento de Fitopatologia, Universidade Federal de Vi~osa, Viqosa , Minas Gerais, Brazil BCABI Bioscience, Ascot Centre, Silwood Park, Ascot, Berks, SL5 7TA, United Kingdom Corresponding author: R.W. Barreto ( Abstract Fungal pathogens associated with the asclepiadaceous weed Calotropisprocera (rubber bush) are documented from published, as well as unpublished sources. Two new host-pathogen associations from Brazil; Phaeoramularia calotropidis and Puccinia obllqua, are recorded. The latter species infects the host systemically and induces the formation of conspicuous and damaging witches' brooms. The rust appears to exert some control of C. procera in the more humid areas of Brazil and the biocontrol potential of this and the other listed pathogens is discussed. Additional keywords: 'algod%o de seda', cabbage tree, crown flower, kapok tree, king's crown, leafspot, 'leiteiro', 'queimadeira', rubber tree, rust, witches' broom Introduction Calotropis procera (Willd.) R.Br. or rubber bush, is a shrub or small tree in the family Asclepiadaceae, widely distributed in the Old World tropics, with an Afro-Asian origin (Gupta et al. 1966). It was first reported as a naturalised plant in northern Queensland around 1935 and is currently classed as a noxious weed in the Northern Territory and in northeast Western Australia. In these regions, it forms dense thickets on alluvial flats and commonly invades old cultivated land and overgrazed land. Mechanical and chemical control over the vast areas involved have made management of the weed difficult, expensive and often impractical (Parsons and Cuthbertson 1992). In Brazil, C. procera, was introduced into the northeast region at the beginning of the century (Kissmann and Groth 1992). It has become a problematic invasive weed of pastures and roadsides, and of unique natural ecosystems including scrubland ('caatinga') and savanna ('cerrado') (Ferreira 1973; Lorenzi 1991; Kissmann and Groth 1992). Biological control as a management strategy has already been attempted in Western Australia with arthropods (Cheam 1984), and potential agents have been identified in the Sudan (Parsons and Cuthbertson 1992). This paper reports the results of a literature and herbarium survey for the fungal pathogens of C. procera, supplemented by field observations made during general weed surveys in Brazil (Barreto and Evans 1995). This was originally requested by the Queensland Department of Lands (now Department of Natural Resources). Methods Literature and herbarium survey Mycological databases (Saccardo k Sylloge Fungorum, Petrak k Lists, Index of Fungi) were consulted for fungal pathogens listed on C, procera, or its synonym Asclepias procera Ait., including the host records of the herbarium of the International Mycological Institute (Herb. IMI). Field survey During weed surveys conducted in the Brazilian states of Minas Gerais and Bahia fi-om , roadside stands of C. procera were inspected for the presence of fungal pathogens. Diseased specimens were collected and subsequently examined microscopically. Spores of non-obligate pathogens were picked off with a fine needle and

2 streaked onto 10% potato-dextrose agar (PDA) and incubated at 25OC. Germinating spores were subcultured onto full strength PDA. Results New records are described and the fungi are classified according Hawksworth et al. (1995). Mitosporic fungi Phaeoramularia calotropidis (Ell. & Everh.) Kamal, Moses & Chaudhary, Mycological Research 94: 7 16, 1990 (Figure 1). Lesions on living leaves, amphigenous, initially grey and punctiform; becoming circular, dark grey and sooty in appearance, up to 15 mm diameter; coalescing and covering large areas of leaf surface. In culture: slow-growing, 8 mm diameter after 7 days at 25 C; stromatic, dark brown to black raised colonies covered by pinkish-white aerial mycelium; sporulation poor. Material examined: VIC , Barra Grande, Bahia, Brazil, 2 1 January The specimen from Bahia, the first record ofthis fungus from Brazil, agrees with the descriptions given by Chupp (1954) and Kamal et al. (1990). Chupp (1954) included it as Cercospora calotropidis Ell. & Everh. in his monograph and Figure 1 Leaf of Calotropis procera showing circular, sooty colonies of Phaeoramularia calotropidis. gave a list of synonyms, as well as recording it from both the Neotropics (West Indies, Central America, northern South America) and the Palaeotropics (Egypt, India). There is a large collection of this pathogen in Herb. IMI, including ten records from various parts of India, in which the leaves are often heavily infected, and five records from Pakistan, all with conspicuous leaf damage. In the seven collections from Sudan, however, the most severe damage is seen where leaves become distorted and completely covered with 'sooty mould'. There are other records fi-om Cuba, Dominican Republic, Jamaica, Venezuela, Egypt, Ethiopia, Kenya, Togo and My anmar. In Brazil, the fungus has also been collected from the states of Espirito Santo and Minas Gerais, typically from humid areas, and appears to be absent from semi-arid regions. Compared with the Afro- Asian records, however, damage has never been severe. Since Calotropis is an Old World genus, it can only be supposed that P calotropidis has been introduced with the plant as it has been moved around the Neotropics. A similar situation has been reported for a Phaeoramularia sp., originally described as Cercospora eupatorii Peck, a specific pathogen of Ageratina adenophora (Spreng) King & Robinson: crofton weed, which appears to have spread with its Mexican host plant throughout the Palaeotropics (Wang et al. 1997). Viegas (1961) listed the following records of mitosporic fungi on this host in South America: Ascochyta tripolitana Sacc., Cladosporium calotropidis F. L. Stevens and Placosphaeria calotropidis Gonz., Frag. & Cif. As these fungi were not observed in the field and no herbarium specimens were available, it is difficult to assess the nature of their association with C. procera. Other species associated with rubber bush that were listed in Saccardo (1 884; 1902; 19 13; 193 1) are: Phoma calotropidis (Thiim.) Sacc. from Sudan; Gloeosporium (= Colletotrichum) calotropidis El. & Ev. from East Africa; A. tripolitana from Libya; Cladosporium calotropidis from Puerto Rico; Napicladium calotropies H. Morstatt from East Africa; Phoma calotropidis Speg. from Senegal (Saccardo 193 1). Three other mitosporic hngi have been described from C. procera from the same locality in Pakistan, on dead branches of C. procera with no indication of their pathogenic status: Coniothyrium calotropidis Ahmad (1 964); Diplodia calotropidis Ahmad (1962); Hendersonia caloptropidis Ahmad (1 968).

3 Ascomycota Leveillula taurica (Lev.) Am. Powdery mildew on leaves of C. procera from Sudan (Tan 1955) appears to be uncommon and not particularly damaging. Mycosphaerella sp. Specimen in Herb. IMI from Venezuela; leaves covered with black sooty growth, causing leaf distortion. This is almost certainly M. calotropidis Viswanathan, originally described on living leaves of C. gigantea from India (Viswanathan and Tilak 1960); and possibly represents the teleomorph of Phaeoramularia calotropidis. The symptomatology is identical to that observed on leaves from the Sudan infected with Phaeoramularia. Basidiomycota Puccinia concrescens Ellis & Everhart ex Arthur, Mycologia 7: 240, Viegas (196 1) included a record ofthis rust species in association with C. procera. This record requires confirmation as this species was recorded by other authors only in association with Asclepias czrrassavica L. (Hennen et al. 1982; Jackson 193 1). Puccinia obliqua Berk. & Curt, apud Berkeley, Journal of the Linnean Society 10: 356, 1868 (Figures 24). Several synonyms are given by Arthur (1 9 15): with further additions by Jackson (193 I), Arthur (1934) and Lindquist (1 982). Jackson (1 93 1) noted that there are probably other synonyms which belong here among the numerous Puccinia species described on hosts in the Asclepiadaceae from South America. Lesions on living leaves and young stems; chocolate to dark brown pustules evenly spread on laminae abaxially and concentrated along leaf veins Figure 2 Old witches' broom caused by Puccinia obllqua on a branch of Calotropis procera. Figure 3 Leaves covered with telia of Puccinia obliqua. Figure 4 Teliospores of Puccinia obliqua (note obliquely attached pedicels). Bar = 20 pm. 128

4 adaxially; infection systemic leading to the formation of large witches' brooms often causing gross distortion of the infected branches; later becoming necrotic, leading to death of hypertrophied tissue. Internal mycelium intercellular, branched, septate, hyaline, producing haustoria. Spermogonia, aecia and uredinia unknown. Telia subcuticular, circular, up to 0.5 mm diameter, chestnut brown; paraphyses absent. Teliospores pedicellate, globose, subglobose, ovoid to obovoid, x pm, 1-septate, pm thick, often thicker at the apex, yellow to pale brown, smooth; pedicels often attached obliquely, cylindrical, up to 9 pm diameter, tapering towards the base. Teliospore germination simultaneous, resulting in the production of a pinkish mass of promycelia and basidiospores, easily mistaken for a mycoparasite. Material examined: Vic 19318, Monte Azul, Minas Gerais, Brazil, Nov This microcyclic rust has a broad host range within the Asclepiadaceae. Arthur (1934) recorded the rust in the United States of America on species of Gonolobus, Metastelma, Philibertia, Seutera and Mncetoxicum; Farr et al. (1989) added species of Asclepias, Calotropis, Cynanchum, Matelea, Morrenia and Sarcostemma to the list. In addition to hosts in these genera, Leon-Gallegos and Cummins (1981) included a species of Funastrum in Mexico and Lindquist (1982) also listed species of Oxypetalum and Rhyssostelma as hosts of P. obliqua in Argentina. Hennen et al. (1982) documented Brazilian rusts and their host genera and recorded P. obliqua on species of Ditassa, Gonolobus, Metastelma, Oxypetalum, Oxystelma, Philibertia and Widgrenia but not Calotropis. Observations made during a trip through the states ofminas Gerais (MG) and Bahia (BA) across a gradient of increasing aridity, have given some indications of the impact of P obliqua on C. procera and on the ecological limitations ofthis association. The first rusted plants were observed along roadsides near the city of Janauba (MG), showing heavy infection and conspicuous brooms. This condition prevailed as far as the MG-BA border. As aridity increased, the rust symptoms became less obvious and the weed appeared to be more problematic, invading pastures and forming monotypic stands. No rust was found on this host in the dry scrub vegetation (caatinga), characteristic of western Bahia. This is the first record of this host-rust association in Brazil and, indeed, the f ~st authenticated report in Latin America. There is an earlier record, however, in Herb. IMI from Venezuela (IMI , 1969), accessed as Puccinia sp. but with an annotation, 'Puccinia calotropidis sp. nov.'. Clearly, this was never validly published since it does not appear in the Index offungi. The formation of witches' brooms on other hosts has been noted previously by Arthur (1 934), 'sometimes systemic, even forming witches' brooms' ; Lindquist (1 982) and Leon-Gallegos and Cummins (1981) also reported the presence of witches brooms but not apparently to the extent on C. procera, where it is a highly visible symptom. Uredo calotropidis Cummins, Bulletin ofthe Torre): Botanical Club 79: 230, This taxon was originally described as Uredo 'calotrop[s]idis' on 'Calotrop[s]is' procera from Colombia: 'No rust has been reported on Calotrop[s]is and no asclepiadaceous rust has such uredia and urediospores' (Cummins 1952). In Herb. IMI there is a collection of this rust on C, procera from Cuba (IMI , 1967), where it is linked to 'Pucclnia calotropidis sp, nov.'. Since no uredinial stage has ever been associated with P. obliqua, which is a confvmed microcyclic species (Arthur 1934), this was obviously an erroneous conclusion, and the taxonomic affinities and indigenous host of Uredo calotropidis remain unresolved. Discussion Phaeoramularia calotropidis appears to have been carried with its host Calotropis procera as it has spread or been introduced through the Neotropics. There are no confirmed reports of its occurrence in Australasia but that may be because no mycological study of this host has been undertaken in the region. Based on the collections, P calotropidis does not seem to offer much potential as a biocontrol agent of rubber bush. Nevertheless, host damage on the Sudanese collections was consistently severe and Tarr (1955) reported it as common during the rainy season in central Sudan and on the Red Sea coast. This suggests that there are either pathotypic differences within the strains or that optimal conditions for infection occur in the Sudan. Within the natural range of C. procera, no collections of rust fungi have been made. In its exotic, neo-tropical range, however, two rust species have been reported. There is little information on the host

5 range of U. calotropidis but P obliqua is known to have an extremely wide range within the neotropical Asclepiadaceae. It is not surprising, therefore, that the range of I? obliqua expanded to include an exotic asclepiadaceous host such as C procera. This 'new encounter' would have been entirely predictable based on published data and is interpreted as a natural expansion of its host range rather than the more contentious host shift or 'jump' (Marohasy 1996). Although the rust can be extremely damaging, as observed in several localities in Brazil, host range tests are likely to confirm a wide host range, therefore preventing its use as a biocontrol agent in Australasia and the Old World. Possible sources of exploitable coevolved natural enemies would appear to be in the Middle East and Northeast Africa, particularly in the Sudan (Parsons and Cuthbertson 1992; Tarr 1955; Herb. IMI records). References Ahmad, S. (1 962) -Further contributions to the fungi of West Pakistan, 11. Biologia 8: Ahmad. S. (1964) - Contributions to the fungi of West Pakistan, IV. Biologia 10: 1-6. Ahmad, S. (1968) - Contributions to the fungi of West Pakistan, VII. Biologia 14: Arthur, J.C. (1915) - Uredinales of Porto Rico based on collections by F.L. Stevens. Mycologia 7: Arthur, J.C. (1 934) -Manual ofthe Rusts in Unitedstates and Canada. Purdue Research Foundation, Lafayette. Barreto, R.W. and Evans, H.C. (1995) -Fungal pathogens of weeds collected in the Brazilian tropics and subtropics and their biological control potential. Proceedings of the 8th International Symposium on Biological Control of Weeds (Eds E.S. Delfosse and R.R. Scott), pp DSIRICSIRO, Melbourne. Cheam, A.H. (1984) - A 'natural herbicide' against calotrope? Journal ofagriculture Western Australia 25: Chupp, C. (1954) -A Monogvaph of the Fungus Genus Cercospora. Privately printed, Ithaca. Cummins, G.B. (1 952) - Uredinales!?om various regions. Bulletin of the Torrey Botanical Club 79: Farr, D., Bills, G.F., Chamuris, G.P. and Rossman, A.Y. (1989) -Fungi on Plants and Plant Products in the United States. APS Press, St. Paul, Minnesota. Ferreira. M.B. (1973) - DF e Goias sob ameaqa de invasora. Cerrado 5: Gupta, R.K., Guar, Y.D., Mahotra, S.P. and Dutta, B.K. (1966) - Medicinal plants of the Indian arid zone. Journal d'agriculture Tropicale et de Botanique Applique'e 33: Hawksworth, D.L., Kirk, P.M., Sutton, B.C. and Pegler, D.N. (1995) - Dictionary ofthe Fungi (Eighth edition). CAB International, Wallingford. Hennen, J.F., Hennen, M.M. and Figueiredo, M.B. (1 982) - Indice das ferrugens (Uredinales) do Brasil. Arquivos do Institute Bioldgico de SGo Paulo 49: Jackson, H.S. (1 93 1) -The rusts of South America based on the Holway collection - V. Mycologia 23: Kamal, Moses, A.S. and Chaudhary, R. (1990) - Two new species and a new combination in Phaeoramularia from Uttar Pradesh, India. Mycological Research 94: Kissmann, J.G. and Groth, D. (1992) - Plantas Infestantes e Nocivas (Vol. III). BASF Brasileira S.A., SBo Paulo. Leon-Gallegos, H.M. and Cummins, G.B. (1 98 1) - Uredinales (Royas) de Mexico (Vol. 1.). Secretaria de Agricultura y Recursos Hidraulicos, Culiacan. Lindquist, J.C. (1982) - Royas de la Repliblica Argentina y Zonas Limitrofes. INTA, Buenos Aires. Lorenzi; H. (199 1) - Plantas Daninhas do Brasil. Editora Plantarum, Nova Odessa. Marohasy, J. (1996) - Host shifts in biological weed control: real problems, semantic difficulties or poor science? International Journal of Pest Management 42: Parsons, W.T. and Cuthbertson, E.G. (1992) -Noxious Weeds ofaustralia. Inkata Press, Melbourne. Saccardo, P.A. (1884) - Sylloge Fungorum 11. Saccardo, P.A. (1 902) - Sylloge Fungorum 16. Saccardo, P.A. (1913) - Sylloge Fungorum 22. Saccardo, P.A. (193 1) - Sylloge Fungorum 25. Tarr, S.A. J. (1955) - The Fungi andplant Diseases of the Sudan. Commonwealth Mycological Institute: Kew. Viswanathan, T.S. and Tilak, S.T. (1960) - Some new records of Mycosphaerella from India. Sydowia 14: Wang, F., Summerell, B.A., Marshall, D. and Auld, B.A. (1997) - Biology and pathology of a species of Phaeoramularia causing a leaf spot of crofton weed. Australasian Plant Pathology 26: Manuscript received 31 July 1998, accepted 23 November 1998.