AÇOREANA, 1997, 8(3): 375-381

RAMULARIA RUBELLA AND UROMYCES RUMICIS INFECTING OBTUSIFOLIUS lN THE Luís Silva, João Tavares & Raphael Brasseur Departamento de Biologia, Universidade dos Açores 9500 Ponta Delgada, São Miguel, Açores, Portugal

ABSTRACT Rumex spp. (), namely L., are considered as weeds in permanent pastures in São Miguel island (Azores), demanding manual and cheItÚcal control. However, R. obtusifolius are found to be heavily infected by rubella (Bon.) Nannf. or by Uromyces rumieis (Schom.) Wint. This is the first record of R. rubella for the Azores. This hyphomycete infects alI the phenophases of R. obtusifolius and is found widely distributed on São Miguel island. Infected leaves of R. obtusifolius may present more than ane hundred red spots each, as welI as conidiophores and conidia. U. rumicis, already recorded for the Azares on Rumex pulcher L., was now found infecting a11 the phenophases of R. obtusifolius in São Miguel island. Leaves infected by the rust become chlorotic and covered by uredosori and uredospores. ln late summer teleosori and teleospores were also found. Both fungi are potential biological control agents of Rumex spp. in the Azores. RESUMO O género Rumex (Polygonaceae) inclui várias espécies consideradas como infestantes nas pastagens permanentes da ilha de São Miguel, nomeadamente Rumex obtusifolius L., que exigem medidas de luta química e manuaL No entanto, algumas dessas espécies encontram-se infectadas por Ramularia rubella (Bon.) Nannf. ou por Uromyces rumicis (Schum.) Wint. Este é o primeiro registo de R. rubella para os Açores. Este hifomicete, muito comum em São Miguel, infecta todas as fenofases de R. obtusifolius. As folhas infectadas podem apresentar mais de uma centena de pequenas manchas circulares vermelhas, e as manchas podem conter tufos de conidió• foros com conídios. U. rumíeis, já registado para os Açores em Rumex pulcher L., foi agora encontrado em todas as fenofases de R. obtusifolius cm São MigueL As folhas infectadas por esta ferrugem apresentam-se cloróticas e cobertas por uredos­ soros e uredosporos, acabando por morrer. No fim do Verão encontraram-se teleos­ soros e teleosporos. Ambos os fungos são potenciais antagonistas de R. obtusi­ foliu.> nos Açores.

INTRODUCTION agricultural surface. ln the Azores the climate is temperate and rainy Pasture for caule raising is the with small variations in temperature, most important econornic activity in and high leveIs of rain fall and the Azores Archipelago, comprising relative humidity. Mean annual nearly 50% of the surface of the temperature varies from 17 to 11°C, islands and about 62 % of the and rain faU from 1000 to 2500 376 AÇOREANA 1997, 8(3): 375-381 mm/year, at 70 and 800 m respec­ frequency or by nitrogen fertilisation. tively. A slightly acidic soil was Natural enemies for the biological formed from volcanic piroclastic control of R. pulcher were surveyed, material. namely insects (Scott, 1984; Scott & Afier 1950 cattle breeding became Way, 1989; Scott & Sagliocco, more important with the increase of 1989, 1991a, b) and fungi (Schubi­ pasture areas and number of live ger, 1985; Meinicke, 1987). caUle, and the development of dairy ln the Azores, Oliveira (1989) industry (Oliveira, .1989). ln the found R. obtusifolius, Rumex con­ Azores 40% of the income is glumeratus Murray, Rumex angio­ originated by agriculture, involving carpus Murb., R. crispus and R. 50% of the working popuIation and pulcher in the pastures, where they originating 80% of the exportations are considered as important weeds, (Anonymous, 1995). Traditionally demanding manual and chemical the production is accomplished by control. However, Rumex spp. pennanent pastures of gramineae and plants in the Azores were found to be Tripholium repens L. The pasture is heavily infected by Ramularia rubella used intermittently, but many (Bon.) Nannf. (Hyphomycetes) or pastures are submitted to 12 grazing by Uromyces rumicis (Schum.) Wint periods per year. Cattle is left in the (Uredinales). field year round and milk is collected This is the first record of R. in the pastures (Oliveira, 1989). rubella for the Azores, where it in­ Rumex obtusifolius L. (Polygon­ fects all the phenophases of R. obtu­ aceae) is not appreciated by cattle sifolius and is found widely dis­ (Cavers & Harper, 1964) and is tributed in São Miguel lsland. considered as a major weed in Cen­ Uromyces rumicis, already recorded tral Europe. Together with Rumex for the Azores on R. pulcher (Dennis crispus L. and Rumexpulcher L. it is et aI., 1977) was now found infect­ known world-wide as a weed. ing all the phenophases of R. obtusi­ Chemical control is expensive and folius in São Miguel. Both fungi are not pennanent, and seed stock in the potential biological control agents of soil is enormous (Huber-Meinicke, Rumex spp. in the Azores. ln this 1989). R. pulcher is also a major work, abundance of Rumex spp. in weed in Mediterranean like climatic São Miguel lsland (Azores) was regions of south-western Australia estimated, and the natural enemies which has proved difficult to control surveyed in 1995/1996. by chemical and cultural means (Scott, 1984). Niggli et alo (1993) METHODS concluded that established dock plants cannot be controlled to any Spatíal distribution of Rumex extent by strong competition of spp. in the pastures was evaluated by grasses, by variation in the cutting counting the number of plants in 100 SILVA ET AL.: RAMULARIA & UROMYCES INFECTING RUMEX 377 m2 using a 1 m2 sampling unit, in frequent, and U. rumicis is predomi­ four pastures with different leveIs of nantly found in oId leaves, at the infestation. Distributions were fitted base of the , although in labora­ to the Poisson, the Negative Bino­ tory, 5 to 6 leafed plants are readily mial model or to'the Normal distri­ infected by exposure to infected bution (Scherrer, 1984). plants. Groups of uredosori with Abundance of Rumex spp. in São brown uredospores were found, Miguel island was evaluated by sur­ each formed by a central sorus en­ veying 30 pastures, using Braun­ circled . by several sori, causing Blanquet sociability and cover coef­ chlorosis and dead of basal leaves. ficients. R. obtusifolius leaves infected with Natural enemies were searched R. rubella may present more than for in the leaves and flowers of one hundred red spots each. ln ma­ Rumex spp. plants. ture spots a central hole may appear as a consequence of leaf tissue RESULTS necrosis. ln many spots conidio­ phores and conidia are present. R. obtusifolius was found in São Other Rumex spp. natural ene­ Miguel island from 100 to 750 m of mies found in São Miguel included altitude. Percentage of each socia­ Spodoptera littoralis (Lepidoptera, bility coefficient (1 to 4) was 70, 20, Noctuidae) and Aphis fabae Scopoli 7, and 3% respectively. Percentage (Homoptera, Aphididae), the first . of pastures with different cover co­ causing heavy defoliation on R. ob­ efficients (+ to 3) were 47, 23, 13 tusifolius. and 17 % respectively. The distri­ bution of R. obtusifolius in a pasture DISCUSSION is considerably irregular, higher cover and sociability is found near R. obtusifolius was found in all field hedges, at the field entrance, the range of permanent pastures in near water tanks, at the bottom of São Miguel island, what agrees with field slopes, in drainage lines, and previous work (Oliveira, 1989). where caule movement is frequent (at The spatial distribution of the milk collection points). weed in the pasture will determine Distribution of R. obtuSlfolius in how the herbicide shou1d be applied the Azorean pastures varied from a (Christensen et aI., 1996). ln lightly negative binomial distribution to a infested pastures, where the weed normal distribution (Figs. 1 and 2). may be present in aggregates, 10- Ramularia rubella and Uromyces calised application of Assulame will rumicis are widespread in the island, be recommended, in order to save from 100 to 700 m of altitude, and herbicide, while at heavily infested are both present in 75% of the pas­ pastures, where the distribution of tures. Generally, R. rubella is more the weed may be more regular, 378 AÇOREANA 1997, 8(3): 375-381

25

~ 20 ...A E '-l 15 ....o JlO.. E z= 5

O O 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Number of plants per sample

FIG. 1. Frequency distribution of 100 I m2 samples of Rumex obtusifolius in a light1y infested pasture at São Miguel island. This dístribution :fitted a Negative Binomial distribu­ tion with k=2,8l (X2 test, p=0,91). Average ± standard error 3,03±2,48. 9 8

7

° 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 Number of plants per sample FIG. 2. Frequency distribution of 100 1 m2 samples 01' Rumex obtusifolius in a heavily infested pasture at São Miguel island. This distribution 1'itted a Normal distribution (X 2 test, p=0,08). Average ± standard error = 16,85±O,77. SILVA ET AL.: RAMULARIA & UROMYCES INFECTING RUMEX 379 a general spray would be recom­ mycelia (Schubiger et ai., 1985). mended. ln alI cases the dense dock ActuaIly, uredospores are found year stands that generally .occur at field round in the Azores, while hedges, field entrance, near water teleospores were found only by the tanks, the bottom of field slopes, in end of summer. drainage lines and at mi1k collection ln the Azores, both fungi should points should be eliminated, since be thorou\!',;, ", .cyed and they they will probabIy contribute to in­ should be, cl.">ldered in a integrated crease the infestation. control programme for pasture pests The host range of R. rubella is and weeds. Introduction of a com­ very restricted, since only species of pIementary natural enemy, like a the subgenus Rumex have been in­ specific root borer should be care­ fected (Strassle et ai., 1986). Ac­ fully considered, in order to preserve cording to Meinicke (1987) this fun­ Rumex azoricus Rech., an endemic gus might possibly controI a stand of species. docks if combined with a parasite of the roots or a chemical herbicide. ACKNOWLEDGEMENTS Propagation of mycelium in sub­ mersed culture seems to be the only Thanks are due to Professor G. method for mass production of in­ Defago and to the Federal Institute of oculum of R. rubella (Meinicke, Technology, ETH Zurich, for biblio­ 1987). graphic support. Raphael Brasseur U. rumieis was considered a bio­ was supported by Eurodisseia. controI agent due to its effects on R. crispus and R. obtusifolius (Inman, LITERA TURE CITED 1971; Schubiger, 1985) and to the specialisation of the rust both in di­ ANONYMOUS, 1995. Conclusões cariotic and haplontic phases. do VIII Congresso da Agricultura Rusted R. crispus and R. obtusi­ dos Açores, 3 pp. Federação folius pIants a]ways have a reduced Agrícola dos Açores, Velas. number of leaves and a significant CA VERS P.R., & J.L. HARPER, 10ss of dry weight of roots and 1964. Rumex obtusifolius L. and leaves (Schubiger, 1985). ln the R. crispus, L. Journal of Ecolo­ Azores, interactions between U. ru­ gy, 52: 737-766. mieis and other natural enemies, like CHRISTENSEN, S., T. HEISEL & Spodoptera littoralis are possible, A M. WALTER, 1996. Patch since similar processes were found spraying in cereaIs. ln: BROWN, by Hatcher et ai. (1994). Ranuncu­ H, G.W. CUSSANS, M.D. lus ficaria, the haplontic phase host, DEVINE, S.O. DUCK, C. FER­ is not present in the Azores, and the NANDEZ-QUINT ANILHA, A. over winters' on the primary HELWEG, RE. LABRADA, M. host probably as uredia or vegetative LANDES, P. KUDSK & J.C. 380 AÇOREANA 1997. 8(3): 375-381

STREIBIG (eds.), Proceedings of nitrogen fertilization and cutting the Second International Weed frequency on the competitive abil­ Control Congress Copenhagen, ity and the regrowth capacity of 1996, pp. 963-968. Department Rumex obtusifolius L. in several of Weed Control and Pesticide grass swards. Weed Research, Ecology, Flakkebjerg. 33: 131-137. DENNIS, R.W.G., D.A. REID & OLIVEIRA, lN.B., 1989. A pas­ B.M. SPOONER, 1977. The tagem permanente da ilha de São Fungi of the Azores. Kew Bul­ Miguel (Açores): estudo fitosso­ letin, 32(1): 85-136. ciológico e primeia abordagem do HATCHER, P.E., N.D. PAUL, ponto de vista agronómico. 366 P.G. AYRES & J.B. WHIT­ pp. Tese de Doutoramento, Uni­ T AKER, 1994. Interactions versidade dos Açores, Ponta Del­ between Rumex spp., herbivores gada. and a rust fungus: Gastrophysa SCOTT, J.K., 1985. Candidate viridula grazing reduces subse­ insects for the biological control quent infection by Uromyces ru­ of Rumex pulcher. ln: DEL­ mieis. Functional Ecology, 8: FOSSE, E.S. (ed.), Proceedings 265-272. VI International Symposium Bio­ HUBER-MEINICKE, G., G. DE­ logical Control Weeds, 19-25 FAGO & L. SEDLAR, 1989. August 1984, Vancouver, Cana­ Ramularia rubella (Bon.) Nannf. da, pp. 829-835. Agriculture as a potential mycoherbicide Canada. against Rumex weeds. Botanica SCOTT, J.K., & M.l WAY, 1989. Helvetica, 9911: 81-89. Host plant specificity and biology INMAN, R.E., 1971. A preliminary of Rhodometra sacraria (L.) evaluation of Rumex rust as a (Lepidoptera: Geometridae) in biological control agent for curly South Africa. Journal of the en­ dock. Phytopathology, 61: 102- tomological Society of southern 107. Africa, 52(2): 245-251. MESSIEAN C.M., D. BLAN­ SCOTT, J.K., & J.L. SAGLIOC­ CARD, F. ROUXEL & R. LA­ CO, 1989. Biology and host­ FON, 1991. Les maladies des specificity of Pegomya solennis plantes maraícheres, 552 pp. (Diptera, Anthomyiidae), a possi­ INRA, Paris. ble biological control agent for MEINICKE, G.R., 1987. Grund­ Rumex spp. in Australia. Acta lagen zur Ampfer-Bekampfung Oecologica/ Oecologia Applicata, mit Ramularia rubella (Bon.) 10(2): 157-163. Nannf, 82 pp. Dissertation ETH SCOTT, J.K., & J.L. SAGLIOC­ Zürich Nr. 8389. CO, 1991a. Host-specificity of a NIGGLI, U., J.NÓSBERGER & J. root borer, Bembecia chrysidi­ LEHMANN, 1993. Effects of formis (Lep.: Sesiidae), a poten- SILVA ET AL.: RAMULARIA & UROMYCES INFECTING RUMEX 381

tial control agent for Rumex spp. Dissertation ETH Zürich Nr. (Polygonaceae) in AustraIia. En­ 7888. tomophaga, 36(2): 235-244. SCHUBIGER, F.X., G, DÉFAGO, SCOTT, J.K., & J.L. SAGLIOC­ L. SEDLAR & H. KERN, 1985. CD, 1991b. Chamaesphecia do­ Host range of the hapIontic phase ryliformis (Lep.: Sesiidae), a sec­ of Uromyces rumicis. ln: ond root borer for the control of DELFOSSE, E.S. (ed.), Praceed­ Rumex spp. (Polygonaceae) in ings oJ the VI International Sym­ Australia. Entomophaga, 36(2): posium, Biological Contral oJ 245-25l. Weeds, 19-25 August 1984, Van­ SCHERRER, B., 1984. Biostatis­ couver, Canada, pp. 653-659. tique, 850 pp. GaeHin Morin Agriculture Canada. , Editeur, Québec. STRASSLE, A., G. DEFAGO, H. SCHUBIGER, F.X., 1985. Grund­ KERN & L. SEDLAR, 1986. lagen Jür die biologische Bekamp­ Ovularia obliqua (Cooke) Jung von Rumex obtusifolius L. Oudem.- Host specificity and und R. crispus L. mit Uromyces conidiation in axenic culture. rumicis (Schum.) Wint., 96pp. Biologia, 41(9): 847-852.