sign in sign up
<<
Home , Fumaria, Fumaria bastardii, Fumaria capreolata, Fumaria muralis, Fumaria officinalis, Fumaria parviflora

Potential biological control agents for fumitory ( spp.) in

M. Jourdan,1 J. Vitou,1 T. Thomann,1 A. Maxwell2,3 and J.K. Scott2

Summary Fumaria are increasingly problematic in the cropping regions of southern Australia, and one fumitory, Fumaria densifloraDC, has developed populations with herbicide resistance. Consequently, the potential for biological control was assessed. Nine species of fungi were found associated with Fumaria spp. in a survey of 33 sites in southern . According to the literature, species potentially host specific to fumitory includeCladosporium brachormium Berk. and Broome, Entyloma fumariae J. Schröt. and Peronospora affinis Rossmann. Of the detected on Fumaria spp. in France, the stem weevil, Sirocalodes mixtus Mulsant and Rey has potential as a biological control agent because it is thought to be host specific. None of these species were detected amongst the six pathogen spe- cies found during surveys of 64 locations in southeastern and southwestern Australia. The absence of pathogens and insects associated with Fumaria species in Australia, the lack of Fumaria spp. native to Australia, and few closely related crops or ornamental species, indicate that there are opportunities for research into the development of natural enemies for the biological control of fumitory.

Keywords: Fumaria species, biological control, field surveys, fungal pathogens, .

Introduction species and two subspecies: Boreau, L., Fumaria capreolata L. subsp. Fumitory species are weeds of many parts of the world, capreolata, F. densiflora, Fumaria indica (Hausskn.) mainly in cereal and legume cultivation, vineyards, Pugsley, Sond. ex W.D.J.Koch, Fu- wastelands and gardens, but have not been considered maria muralis Sond. ex W.D.J.Koch subsp. muralis, as a target for biological control. In Australia, fumitory L., Lamarck) is a problem in canola and pulse crops (particularly are introduced, mostly from (Australian Na- peas and lupins; Holding and Bowcher, 2004). Lemerle tional Botanical Garden, 2007 a, b; Norton, 2003). Fu- et al. (1996) found Fumaria species in 37% of 86 cereal maria species were found in all States of Australia and crops in southern New South Wales during a survey are abundant only in southern regions, mostly in New of weeds conducted in spring 1993. Agronomists and South Wales, Victoria, South Australia and Western farmers from this region ranked fumitory in the top ten Australia. The increasing importance of Fumaria spp. of 50 species in terms of potential threat. Fumaria den- and the rise of herbicide resistance point to the need siflora DC first evolved resistance to group K1/3 her- to investigate alternative means of control. This paper bicides (Ditroanilines and others) in New South Wales reports on preliminary surveys in France and Australia (NSW) (Heap, 2007), underlining that this species is the to find potential biological control agents. most important weed of the in Australia (Norton et al., 2004). In Australia, all Fumaria species (seven Methods Surveys in France

1 CSIRO European Laboratory, Campus International de Baillarguet, Surveys were conducted in France from April 2004 34980 Montferrier-sur-Lez, France. to May 2005. Populations of Fumaria were found at 2 CRC for Australian Weed Management and CSIRO Entomology, Pri- 33 sites out of 79 inspected, either in vegetable culture vate Bag 5, PO Wembley, WA 6913, Australia. or vineyards or on areas of freshly disturbed soil. The 3 AQIS, PO Box 606, Welshpool, WA 6986, Australia. Corresponding author: M. Jourdan . sites were distributed along five transects covering the © CAB International 2008 Riviera between Hyères, St Tropez and Lake Ste Croix

160 Potential biological control agents for fumitory (Fumaria spp.) in Australia

(circa 270 km), the Cévennes between Mount Aigoual in sterile 90 mm Petri dishes or plastic ‘take-away’ and Montpellier (ca. 110 km), the Pyrénées between containers (150 mm ´ 80 mm ´ 50 mm) sealed with The Boulou and Prades (ca. 130 km), the Atlantic coast Parafilm wrap or plastic cling film (Gladwrap). In -ad between Tarbes and St Jean de Luz (ca. 200 km) and dition, diseased shoot and root material was surface Bordeaux to Agen (ca. 150 km) and one longer transect disinfested by soaking in 2.5% sodium hypochlorite through agricultural regions (ca. 1580 km). (v/v) for 1 min, rinsed in three changes of sterile tap At each site, were searched visually for evi- water, blotted dry and plated onto 2% malt extract agar dence of disease. Samples of diseased tissue were col- (MEA; Difco) or water agar (20 g Difco agar made lected and examined in the laboratory. When a pathogen up to 1 l with deionised water). Pure fungal cultures was found associated with a symptom, after its fructifi- were obtained by transferring single spores or single cation in a humid chamber, a single spore was collected hyphal tips onto fresh media and maintained on MEA, with a sterile needle under a stereomicroscope, depos­ PDA or V8 juice agar (200 ml Campbell’s V8 juice, 3 g ited on a potato dextrose agar (PDA; Difco) Petri dish CaCO3, 15 g Difco agar made up to 1 l with deionised and placed in a controlled environment (20°C and 12 h water). Cultures were grown under white fluorescent photoperiod). Fungi were identified morphologically and near-UV light in a 12 h light:12 h dark photoperiod by microscopic observations. at 20°C in order to induce fruiting structures to facili- Plants were searched for evidence of insects at each tate species identification. site, and from four to ten entire plants were collected Small pieces of culture were mounted under acidi- then taken back to the laboratory in transparent plastic fied glycerol blue [0.05 % aniline blue (Gurr) in lacto bags for dissection. Plants with evidence of dam- glycerol] and investigated under the light microscope age were cut up and put in Petri dishes, on wet paper, to for the formation of fructifications. Fungal structures allow eggs or larvae to develop to the adult. were investigated on normal or phase-contrast settings (100–1000´), and 30 measurements were made of co- nidial dimensions. Fungi were identified according to Surveys in Australia standard mycological texts, and original descriptions Transects were made through grain-growing re- where indicated. gions in southeastern Australia (NSW and Victoria) and southwestern Australia between April and October 2005. The transects were made through districts where Results Fumaria species have been previously recorded, and crops and other roadside habitats were briefly searched Twelve genera including 15 identified species of fungal - for the presence of fumitory at intervals of approxi- pathogens have been reported in the literature as asso mately 25 km along the length of each transect. The ciated with Fumaria spp. (results not shown). Three transect distance travelled was approximately 1200 km species are considered to be potentially host specific in each of NSW and Victoria and 1800 km in south- at the level of the family and genus (Cladospo- western Australia. At sites where fumitory was de- rium brachormium Berk. and Broome (anamorphic tected, at least 20 plants from that site were examined Mycosphaerellaceae), Entyloma fumariae J. Schrot. closely over a 20- to 30-min period for symptoms of (Entylomataceae) and Peronospora affinis Rossmann disease and insect attack. Where arthropods were de- (Peronosporaceae)). tected or signs of attack were observed, this was noted. When fruits were present, these were exam- Surveys in France ined from at least 20 plants using a 10´ hand lens for evidence of insect-caused galls. Pathogens: Nine species of fungi were found asso- Representative samples from each disease category ciated with Fumaria species. Diseased leaves of Fu- were collected from each site, placed into polyethylene maria sp. with symptoms of leaf smut, E. fumariae, bags and stored in an insulated cool box with ice until were collected from six sites in November, January they were brought to the laboratory. Leaf symptoms and April. Symptoms of leaf smut appear as whitish were recorded, and pathogens were isolated and identi- spots on both sides of Fumaria leaves and occasio- fied as described below. nally petioles. Lesions become dark brown and enti- re leaves shrivel and eventually die. The three kinds of spores were observed, two external: primary spo- Fungal isolation and species identification: Sub- ridia (filiformes) and secondary sporidia on sterigma samples of diseased material were placed into humid (ballistospores). Microscopic examination of internal chambers for up to 14 days at 15°C and 20°C under a leaf tissues revealed masses of round, double-walled, 12 h near-UV light: 12 h dark photoperiod to encour- pale green-to-yellow spores typical of the ustilospo- age fungal sporulation. The humid chambers consisted res of Entyloma. E. fumariae was grown on artificial of two to three layers of moistened sterile filter paper culture medium (PDA) and formed ballistospores that

161 XII International Symposium on Biological Control of Weeds have a similar structure and form to those produced on Arthropods: No arthropods were found on Fumaria plants. in Australia during the surveys. There was evidence P. affinis was found on Fumaria spp. in ten sites of of possible sap-feeding insects on some plants at the 33 sites surveyed in France. The first symptoms a few sites; however, no causative insects were pre­ observed were small faint yellow spots on the upper sent on the plants. No arthropods associated with foliage. As they matured, fungus fruiting structures fumitory have been reported from Australia in the were visible on the lower leaf surface as conidiophores literature. bearing conidia. Two kinds of spores were observed in field material: conidia on conidiophores and oospores in infected leaves. Discussion Diseased plants of Fumaria spp. with symptoms of a The genus Fumaria is placed in the Subfamily Fumar- Cladosporium species were collected from 13 sites. Ex- ioideae in the Family (Lidén, 1986; Ste- tensive sporulation on leaves, and stems vens, 2007). In earlier taxonomic treatments, the sub- were observed. family is treated as the Family, Fumariaceae. Fumaria Two Alternaria spp. (anamorphic Pleosporaceae), is chiefly a Mediterranean group of 55 species with a Botrytis sp. (anamorphic Sclerotiniaceae), a Col- few species reaching India and east (Lidén, letotrichum sp. (anamorphic Phyllachoraceae), an 1986). There are no native Australian species in the Oidium sp. (anamorphic Erysiphaceae) and Phomop- Family Papaveraceae; the only genera of this fam- sis leptostromiformis (J.G. Kühn) Bubák (Valsaceae) ily in Australia apart from Fumaria are introduced were also found associated with diseased plants of species of Argemone (three species), Dicentra (one Fumaria spp. species), Eschsholzia (one species), Glaucium (two species), Hypecoum (one species), Papaver (six spe- Arthropods: The only two polyphagous aphid species cies), Platycapnos (one species), Pseudofumaria cited in the literature on Fumaria spp. were observed (one species), Roemeria (one species) and Romneya at three sites in France, Aphis fabae Scopoli and Mac- (two species) (Australian National Botanical Gardens, rosiphum euphorbiae (Thomas). A polyphagous lepi- 2007a,b). The only closely related crop to Fumaria is doptera, Plusia sp. (Noctuidae), was also observed at Papaver somniferum L. (poppy) which is grown in five sites. Otherwise, Sirocalodes mixtus Mulsant and Tasmania for production of pharmaceutical chemi- Rey (), with stem-mining larvae, was the cals (Laughlin et al., 1998). Fumaria species are also most common insect, being found at 13 of 33 sites. weeds in this crop (Baldwin, 1977). Related ornamen- tals grown in Australia include species of Chelido- Surveys in Australia nium, , Dicentra, Eschscholzia, Glaucium, Macleaya, Meconopsis, Romneya and Pseudofumaria Pathogens: The survey found fumitory at 64 of the (Spencer, 1997). Thus the absence of related native 160 sites visited throughout the grain-growing districts species and few related commercial species indicates of southern Australia. Six fungal species were identified that weedy Fumaria species could be ideal targets for from diseased fumitory plants: Alternaria alternata (Fr.) biological control. Keissl. (anamorphic Pleosporaceae), Alternaria dauci (J.G. Kühn) J.W. Groves and Skolko (anamorphic Ple- osporaceae), Davidiella tassiana (De Not.) Crous and U. Surveys Braun (Mycosphaerellaceae), Phoma sp. (anamorphic The identification of pathogens is provisionary, and Pleosporaceae), Pleospora sp. (Pleosporaceae) and Scle- further work is needed to confirm identifications with rotinia sp. (Sclerotiniaceae). In addition, several sapro- molecular techniques or by appropriate experts. The phytic and unidentified fungi that failed to sporulate were sampling was carried out in France during an excep- isolated from diseased material (data not shown). Olpid- tionally dry year (2005). Even so, up to five pathogens ium brassicae (Woronin) P.A. Dang. (Olpidiaceae), pre- were found per site, and what appeared to be sites with viously recorded on fumitory in Western Australia (WA), damaging infestations were found for P. affinis, E. fu- was not recorded in the current survey. No pathogenic mariae and P. leptostromiformis. A more complete pic- bacteria or nematodes were detected on fumitory. ture of the number of pathogens could be obtained by The fungi were identified from six different fumi- extending the survey to other western and southern Eu- tory species. F. muralis and F. capreolata were the only ropean areas where there is an abundance of Fumaria two species present in the WA surveys. In addition to species (Tutin et al. 1993). However, based on the lit- these two species, F. bastardii, F. densiflora, F. offici- erature, the survey in France has found most organisms nalis and F. parviflora were observed in the surveys of interest. This is also the first report of presence of of eastern Australia. The plants were not identified to E. fumariae in France. The sampling in Australia shows subspecies rank. F. indica was not detected in the cur- that this fungus and the other potential agents are highly rent survey. likely to be absent.

162 Potential biological control agents for fumitory (Fumaria spp.) in Australia

Pathogens tial agent, and further studies are needed to define the host-plant specificity of this insect. It has only been as- E. fumariae appears to be the most promising po- sociated with F. officinalis and F. parviflora in France tential agent especially as it attacks several Fumaria (Hoffmann, 1954). Adults have been found on Papaver species and is not present in Australia. E. fumariae has hybridum L. in (Campobasso et al., 1999). been found on F. muralis in Madeira Islands, Fumaria A second arthropod that is a potential agent is the rostellata Knaf in and Fumaria vaillantii cynipid wasp, Neaylax versicolor (Nieves-Aldrey). Loisel. in and (Vanky, 1994) and on The larvae of this wasp form galls in the fruits of Fu- F. parviflora in India (Zundel, 1953). Vanky (1994) maria species. It is the only cynipid found in Fumaria noted about E. fumariae in Europe ‘Rarely reported, spp. (Nieves-Aldrey, 2003; Askew and Nieves-Aldrey, almost certainly because E. fumariae is very incon- 2005) and has a distribution including southern France, spicuous’. and . We did not find it in our survey as Despite this, recent experience shows that Entyloma most of the plants were just flowering, and the few species can be successful agents. Barton et al. (2007) green fruits did not show any obvious wasp damage. report that Entyloma ageratinae R.W. Barreto and H.C. Evans was introduced in 1998 with success for the bio- logical control of mist flower, Ageratina riparia (Re- Conclusions gel) R.M. King and H.Robinson, in . By We have identified suitable organisms to be considered 2004, the proportion of leaves infected by the fungus for a biological control project in Australia. Any future increased to 60%. The estimated cover of A. riparia project will require relevant authorizations, and this in heavily infested plots decreased from 81% to 1.5% will be helped by a clearer understanding of the tax- with a corresponding recovery of the diversity of native onomy, identification and importance of Fumaria spe- vegetation (Barton et al., 2007). cies from Australia and the cost–benefits of control in P. affinis, an obligate plant parasite, was abundant cropping systems. at three sites in France and not reported from Austra- lia. It is associated with Fumaria species making it a candidate for further consideration for biological con- Acknowledgements trol. However, there is a report in Farr et al. (2007) of We thank the Grains Research and Development Corpo- a 1902 herbarium specimen from with P. affinis ration, the CRC for Australian Weed Management and on the leaves of Chenopodium album L. (Chenopodia- CSIRO for funding and facilities for this work. We also ceae). Host range tests are needed to establish if this is thank Steve Walker for comments on the manuscript. a valid host. The third species that could be considered is C. bra- chormium since it is only known from F. officinalis. References It has not been reported from Australia. Cladosporium species are known generally as saprophytes, but they Askew, R.R. and Nieves-Aldrey, J.L. (2005) A new genus and species of pteromalid (Hymenoptera, Chalcidoidea) can be also pathogens. Otherwise, there appears to be from Spain, parasitic in cynipid galls on Fumaria. Journal very little known about this fungus. of Natural History 39, 2331–2338. Australian National Botanical Gardens (2007a) http://www. Insects anbg.gov.au/chah/apc/interim/Fumariaceae.pdf. Australian National Botanical Gardens (2007b) http://www. Few insect species were found during the surveys anbg.gov.au/chah/apc/interim/Papaveraceae.pdf. and most of them are polyphagous. Little information Baldwin, B.J. (1977) Chemical weed control in oil-seed poppy on fumitory and insects is available in the literature. (Papaver somniferum). Australian Journal of Experimen- Three curculionids are cited on Fumaria (Hoffmann, tal Agriculture and Husbandry 17, 837–841. 1954). Sirocalodes quercicola Paykull is a gall former Barton, J., Fowler, S.V., Gianotti, A.F., Winks, C.J., de Beurs, developing in crown of F. officinalis and F. capreolata. M., Arnold, G.C. and Forrester, G. (2007) Successful bio- This species is found in Europe but is not common. logical control of mist flower (Ageratina riparia) in New Sirocalodes nigrinus Marsham is common in France Zealand: agent establishment, impact and benefits to the particularly in the southeast coastal region. The larvae native flora.Biological Control 40, 370–385. develop in stems on F. officinalis and F. parviflora. The Campobasso, G., Colonnelli, E., Knutson, L., Terragitti, G. and Cristofaro, M. (1999) Wild plants and their associated adult was also recorded on F. vaillantii, F. capreolata, insects in the Palearctic region, primarily Europe and Platycapnos spicata (L.) Bernh. (Hoffmann, 1954) and Middle East. US Department of Agriculture, Agricultural Papaver rhoeas L. (Campobasso et al., 1999). Research Service, ARS-147. 249 p. During our surveys, we only found the third spe- Farr, D.F., Rossman, A.Y., Palm, M.E. and McCray, E.B. (2007) cies, S. mixtus. It occurs throughout France, but it is Fungal Databases, Systematic Botany and Mycology Lab- more common in the Mediterranean region (Hoffmann, oratory, ARS, USDA. Available at: http://nt.arsgrin.gov/ 1954). This species could be considered as a poten- fungaldatabases/ (accessed March 15, 2007).

163 XII International Symposium on Biological Control of Weeds

Heap, I. (2007) The International Survey of Herbicide Re- Norton, G.M. (2003) Understanding the success of fumitory sistant Weeds. Available at: www.weedscience.com (ac- as a weed in Australia. PhD thesis. Charles Sturt Univer- cessed 7 Jan 2007). sity, Australia, 264 p. Hoffmann, A. (1954) Coléoptères Curculionides (Deuxième Norton, G.M., Lemerle, D. and Pratley, J.E. (2004) Persis- partie). Faune de France 59, 879–897. tence of Fumaria densiflora DC. seed in the field. In: Holding, D. and Bowcher, A. (2004) Weeds in winter pulses Sindel, B.M. and Johnson, S.B. (eds) Proceedings of the - integrated solutions. CRC Australian Weed Management 14th Australian Weeds Conference. Weed Science Society Technical Series 9, 1–11. of New South Wales, Australia, pp. 519–522. Laughlin J.C., Chung, N. and Beattie, B.M. (1998) Poppy Spencer, R. (1997) Horticultural Flora of South-Eastern cultivation in Australia. In: Bernath, J. (ed.) Poppy— Australia. Volume 2 Flowering Plants Dicotyledons Part the Genus Papaver. Harwood Academic, Amsterdam, 1. The Identification of Garden and Cultivated Plants. pp. 249–277. University of New South Wales Press, Sydney. Lemerle D., Yuan, T.H., Murray, G.M. and Morris, S. (1996) Stevens, P.F. (2007) Angiosperm Phylogeny Website. Version Survey of weeds and diseases in cereal crops in the south- 7. Available at: http://www.mobot.org/MOBOT/research/ ern wheat belt of New South Wales. Australian Journal of APweb/ (accessed May 2006). Experimental Agriculture 36, 545–554. Tutin, T.G., Burges, N.A., Chater, A.O., Edmonson, J.R., Lidén, M. (1986) Synopsis of Fumarioideae (Papaveraceae) Heywood, V.H., Moore, D.M., Valentine, D.H., Walters, with a monograph on the tribe Fumarieae. Opera Botan- S.M. and Webb, D.A. (1993) Flora Europaea. Cam- ica 88, 5–133. bridge University Press vol.1: Psilotaceae to Platanaceae. Nieves-Aldrey, J.L. (2003) Descubrimiento de la agalla y pp. 306–311. ciclo biológico de Neaylax versicolor (Nieves-Aldrey) Vanky, K. (1994) European smut fungi. Gustav Fischer (Hymenoptera, Cynipidae): primer registro de un cinípido Verlag, Stuttgart, 570 p. asociado a plantas papaveráceas del género Fumaria. Bo- Zundel, G.L. (1953) The Ustilaginales of the World. Pennsyl- letin de la Sociedad Entomológica Aragonesa 32, 111– vania State College School of Agriculture Department of 114. Botany Contribution 176, 1–410.

164