Session 9 409 Host Specificity Testing, Release and Successful Establishment of the Broom Gall Mite (Aceria genistae) in Australia and New Zealand for the Biological Control of Broom (Cytisus scoparius) J. -L. Sagliocco 1, A. Sheppard 2, J. Hosking 3, P. Hodge 4, Q. Paynter 5, H. Gourlay 6 and J. Ireson 7 1 Biosciences Research Division, Department of Primary Industries, Frankston, 3199, Victoria, Australia jeanlouis.sagliocco@dpi.vic.gov.au 2 CSIRO Ecosystems Sciences, GPO Box 1700, Canberra, 2601, ACT, Australia andy.sheppard@csiro.au 3 Department of Primary Industries, Tamworth Agricultural Institute, Calala, 2340, NSW, Australia john.hosking@industry.nsw.gov.au 4 c/o CSIRO Ecosystems Sciences, GPO Box 1700, Canberra, 2601, ACT, Australia 5 Landcare Research, St Johns, Auckland, 1072, New Zealand paynterq@landcareresearch.co.nz 6 Landcare Research, Lincoln, 7640, New Zealand gourlayh@landcareresearch.co.nz 7 Tasmanian Institute of Agricultural Research, University of Tasmania, New Town 7008, Tasmania, Australia john.ireson@utas.edu.au Summary A form of the eriophyid mite, Aceria genistae (Nalepa) was tested between 1999 and 2001 against 34 test plant taxa and cultivars from 12 tribes for its specificity towards the invasive shrub Scotch broom, Cytisus scoparius (L.) Link, and was shown to be highly specific. The mite was approved for release in Australia and New Zealand where redistribution and monitoring programs have been put in place. After three years, 106 releases of the mite have been conducted in Australia with a 32% establishment rate. In New Zealand, 40 releases have been made with 50% establishment. Both countries are continuing releasing this mite and are monitoring its establishment. Introduction The leguminous shrub Scotch broom, Cytisus scoparius (L.) Link (Fabaceae) is native to the UK, western, southern and central Europe. There it is considered moderately weedy and it occasionally colonises forest areas and pastures. Elsewhere, it has become a serious invader in several countries: eastern and western USA including Hawaii, British Columbia, Australia, New Zealand, Chile and India. Mechanical and chemical control methods of broom in invaded natural ecosystems are difficult to implement, expensive, have negative environmental impacts and require follow-up due to large seed banks and reinvasion by seedlings and young (Downey and Smith 2000; Paynter et al 1998). A number of demography studies have focused on patterns and processes of broom invasion in its native range (France) (Paynter et al. 2003; Paynter et al 1998) and its introduced range in Australia (Downey and Smith 2000; Paynter et al 2003; Sheppard et al 2002; Waterhouse 1988) and New Zealand (Paynter et al. 2003; Williams 1981). In addition, studies in the weed s native range have highlighted the role of natural enemies in limiting
410 Session 9 broom performance (Waloff and Richards 1977), especially the potential of arthropods to reduce seed production and broom longevity (Rees and Paynter 1997). Broom in Australia and New Zealand are largely devoid of specialist insect herbivores (Memmott et al 2000), indicating that biological control may have some potential to control broom in these countries. New Zealand (NZ) began a broom biological control program by releasing the seed feeding beetle, Bruchidius villosus (Fabricius) and the sap-sucking psyllid, Arytainilla spartiophila (Förster) in 1987 and 1993 respectively. Meanwhile, an accidental introduction of the broom twig-mining moth, Leucoptera spartifoliella Hübner resulted in extensive damage to broom in NZ south island (Syrett et al 1999). Building on New Zealand s experience, CSIRO (The Commonwealth Scientific and Industrial Research Organisation) and the New South Wales Department of Agriculture imported L. spartifoliella from NZ and released it in 1993 (Wapshere and Hosking 1993), followed by releases of A. spartiophila in 1994 and B. villosus in 1995 (Syrett et al 1999). A fourth agent, the eriophyid gall, Aceria genistae (Nalepa) was identified as a potential biological control agent during European field surveys (Hosking 1990; Syrett et al 1999; Wapshere and Hosking 1993). A. genistae was originally described by Nalepa from galls developing on Scotch broom in eastern France. The known native range of the mite includes the UK, Italy, Spain and central Europe. Colonies of A. genistae start at the inner base of stem buds and cause growth deformities on bud burst becoming round, pubescent galls. Several overlapping generations develop in galls during spring and summer. Non-woody galls wither in late summer and autumn, forcing mites to crawl into dormant stem buds where they overwinter. Gravid females are also wind dispersed in spring and there is a sex ratio of about 1:20 male: females (J-L Sagliocco pers. obs.). Aceria genistae is probably a complex of specific forms or sibling species. It has been recorded on a number of Genisteae species including Cytisus spp., Ulex europaeus L., Genista spp. and Spartium junceum L. (Castagnoli 1978). However, Cromroy (1979) (Cromroy 1979) noted that eriophyids are often highly host-specific, even to the level of plant form. Castagnoli (1978) has shown that A. genistae developing on broom did not develop on S. junceum, while the mites found on Spartium are a separate species (redescribed as Aceria spartii). Mites identified as A. Genistae discovered on stunted shoot tips of gorse and French broom, Genista monspessulana (L.) L.A.S. Johnson in the USA caused limited damage and did not develop on any other species (Chan and Turner 1998). Similarly, mites identified as A. genistae were found infesting gorse, U. europaeus but not broom, in New Zealand (Manson 1989). Host specificity testing Methods Initial testing of A. genistae by CABI (the Centre for Agriculture and Biosciences International) and CSIRO was conducted with a small number of broom s close relatives at CSIRO European laboratory in Montferrier (France). Field tests were carried out under natural conditions in a native broom infestation where Cytisus striatus (Hill) Rothm., Chamaecytisus palmensis (H.Christ) F.A.Bisby & K.W.Nicholls, Spartium junceum L., Genista tinctoria L., Medicago arborea L., Laburnum anagyroides Medik. and C. scoparius were planted as test. After two years, A. genistae galls were only on C. scoparius and no attack on any of the species tested had been observed. Additional tests were conducted in a glasshouse where A. genistae galls were tied onto C. palmensis and U. europaeus with C. scoparius as a control. Gall development occurred on C. scoparius only. The high specificity of the mite towards C. scoparius resulted in comprehensive host specificity study being conducted in Australia. A. genistae galls collected in the Cevennes mountains range, north of Montpellier (France) were shipped to the CSIRO quarantine facility in Canberra for rearing and further evaluation against a number of Australian and New Zealand native plant species (Table 1). In quarantine, mites were inoculated onto broom where they developed galls, providing a large colony for host specificity tests. There are no Australian native plant species in the tribe Genisteae. Therefore, the focus of the testing was on species of economic importance in the Genisteae and other related tribes in the Faboideae, plus native species in related tribes, with less intensive testing of representative Australian natives in other subfamilies of the Fabaceae. Plants tested for New Zealand included local cultivars of two Lupinus
Session 9 411 species and seven species representing all native genera with the exception of the monophyletic genus Montigena. Between 1999 and 2001, 34 taxa and cultivars from 12 tribes were tested as part of the risk assessment required to obtain release permits for the mite in Australia and in New Zealand (Table 1). Each test consisted of five replicates of one taxon paired with five C. scoparius of similar size as controls. Each plant tested had dormant buds required for mite development. A. genistae galls were harvested from broom gall-producing kept in quarantine, and each gall was scored for number of mites present. Five to ten galls with comparable numbers of mites were then tied onto the foliage of each test plant and control and covered with a plastic bag for 72 hours to prevent galls drying out too quickly and to encourage mites to migrate out of the galls. Test and control were kept at temperatures of 18 C (day) and 12 C (night) (10 hrs light: 14 hrs dark) under high intensity artificial light for one month to help mites colonise while there was no bud development. After one month temperatures were increased to 20 C (day) and 15 C (night) (12 hrs light: 12 hrs dark) to initiate bud growth resulting in gall formation caused by mite feeding activity. After three to five months, and once several galls had developed on control, all fresh buds on the test were dissected for mite presence. When test were too large, an area equivalent to the smallest test was sub-sampled for mite presence. Host specificity testing Results Among the species tested, some initial gall development was observed on S. junceum and C. palmensis. However mites did not survive and no further development was observed. Initial gall formation was also observed on Cytisus Crimson King, an ornamental with C. scoparius parentage, but mite survival did not occur. No gall development or mite presence was observed on any other species including all Australian and New Zealand natives. Approval for release in Australia In 2002, CSIRO submitted an application to federal agencies to obtain approval for release of A. genistae into the Australian environment. After examining the submission, AQIS (the Australian Quarantine and Inspection Service) Plant Biosecurity Australia and the Department of Environment approved release of the mite in the environment. In 2003, before the mite was released, a broom fungus that had been ruled out as a broom potential biological control agent for Australia due to lack of specificity (Morin et al 1999) was discovered in the Canberra mite culture (Morin et al 2006). Consequently, the mite culture had to be destroyed and its release was postponed. A lack of funding caused further delays. In 2006, with joint funding from the Australian Government and the Department of Primary Industries (DPI), Frankston, Victoria, Australia imported the mite into quarantine in Frankston and a clean colony protocol was developed using the transfer of individual mites. Mite populations were increased by transferring mites onto new for several generations until approval for release was granted. Outside quarantine, broom were inoculated with mites to provide material for releases. In October 2008, the first releases were conducted in the Australian Alps in eastern Victoria, and a rearing colony was established in Tasmania. Subsequently, Tasmania provided galls to South Australia and New South Wales (NSW) for releases. Approval for release in New Zealand As A. genistae was already present in New Zealand on gorse (Manson 1989), Environmental Risk Management Authority approval to release the broom form was not required. Nevertheless, testing of the broom form from Europe was conducted as if it was a new organism to New Zealand. Ministry of Agriculture and Fisheries approval to release A. genistae from containment was granted in November 2007. Releases and establishment in Australia In Victoria a number of nursery sites intended for detailed monitoring of mite survival and dispersal were established using two release methods. In autumn, two to four broom bearing galls were planted in the ground at the edge
412 Session 9 of an infestation, and were watered and fertilised to allow their establishment and mite migration. A direct release technique was also used. It consisted of attaching broom branches with galls on 20 wild at the edge of the infestation and marking each plant with surveyor tape for later monitoring. At release sites to be assessed for mite establishment, only the later method was used. Monitoring of transferred and gall numbers, mite presence and gall formation was conducted at all sites twice a year, in spring and autumn, mostly because of the difficulties to access most of the remote release sites in the high country. In the other states, the second release method was mostly used and monitoring was conducted whenever possible. During the period 2008-2011, at total of 106 releases of A. genistae were conducted in four states. Releases were conducted in the Australian Alps (Victoria), throughout the state of Tasmania, around Adelaide (South Australia), near Canberra (southern NSW) and in the Northern Tablelands (NSW).The altitude of most of the release sites ranged between 220 and 670 m, the highest sites being at 1,500 m altitude at Barrington Tops (southern end of the Northern Tablelands in NSW). In 2011, establishment of the mite had been confirmed at 34 of the sites (32 %) (Table 2). Releases of the mite and monitoring of its establishment and dispersal are continuing. In the field, mites were observed to induce gall formation after 6-12 months. Although the program still being in its early stage, mites were observed to establish and cause gall formation faster in Tasmania than in Victoria, both under semi-natural conditions and in the field. Releases and establishment in New Zealand Since 2008, 40 releases of the mite have been made in New Zealand. Establishment has been confirmed at approximately 50% of these sites. Gall formation at many sites has been extensive, covering much of infested broom with some mature bearing hundreds of galls. Significant damage has been recorded in some areas where whole branches of broom have been observed to suffer dieback and in some cases whole have died. Gall formation has also been found on broom in the absence of gall mites although these galls have a different architecture to those caused by A. genistae. Initial observations suggest that a disease (unidentified Fusarium) is associated with gall formation and mite activity (Daniel Than pers. comm.). It is not yet known if the mite may enhance disease occurrence and if it plays a role in plant dieback. Discussion The C. scoparius form of A. genistae was shown to be restricted to this weed and during host specificity studies did not survive on different taxa tested. The mite was released in 2008 both in Australia and New Zealand and since then each country has implemented release and monitoring programs. In Australia, the mite has so far established at a third of the release sites, while in New Zealand the establishment success rate is currently at about 50%. Releases are on-going in both countries. In Australia, differences in the time required for mites to develop galls in the field have been observed between Victoria and Tasmania as well as with establishment success rate. It is not known if this is due to climatic reasons or the occurrence of different broom plant forms in these states. Mite activity results in severe stunting of growth and reduction of plant biomass, reduced seed production and very occasionally reported plant death in its native range. Plant death has been observed in New Zealand following release, although this has not been observed in Australia yet. In Victoria, a field study is currently underway to quantify the impacts of the mite and other natural enemies. Acknowledgements Funding for the host specificity studies of A. genistae between 1990 and 2003 was provided by the Barrington Tops Broom Council, NSW State Forests, the Hunter Pastoral Company and the NSW Government through its Environmental Trusts. The importation of A. genistae in Victoria in 2006 was funded by the Australian Government s Defeating the Weeds Menace program (DWM) and DPI Victoria. The releases in the four states in Australia were funded by the Australian Government s Caring for Our Country program (CFOC) with, in Victoria, co-funding from DPI and financial support from the Goulburn-Murray Water Corporation and Parks Victoria. Acknowledgements are due to Helen Parish (Landcare Research, Lincoln, New Zealand) and Richard Hill (Richard Hill and Associates,
Session 9 413 Lincoln, New Zealand) for their contribution in establishing mite colonies, Richard Holloway, Wade Chatterton (University of Tasmania, Hobart) and Susan Ivory (SARDI, Adelaide, South Australia) for their workand commitment in rearing and releasing the mite. References Castagnoli, M. (1978) Ricerche sulle cause de deperimento e moria dello Spartium junceum L. in Italia. Eriophyes genistae (Nal.) e E. spartii (G. Can.) (Acarina: Eriophyoidea): Ridescrizione, cenni di biologia e danni. Redia 61, 539 550. Chan, K.L. and Turner, C.E. (1998) Discovery of the gall mite Aceria genistae (Nalepa) (Acarina: Eriophyidae) on gorse and French broom in the United States. Pan- Pacific Entomologist 74, 55 57. Cromroy, H.L. (1979) Eriophyoidea in biological control of weeds, in Recent Advances in Acarology. In 5th International Congress of Acarology (ed J.G Rodriguez) 473 475. Academic Press, New York, San Francisco, London, Michigan State University, East Lansing, Michigan. Downey, P.O. and Smith, J.M.B. (2000) Demography of the invasive shrub Scotch broom (Cytisus scoparius) at Barrington Tops, New South Wales: Insights for management. Austral Ecology 25, 477 485. Hosking, J.R. (1990) The feasibility of biological control of Cytisus scoparius (L.) Link. Report on overseas study tour, June-September 1990, unpublished report, New South Wales Department of Agriculture and Fisheries, Tamworth, Australia. Manson, D.C.M. (1989) New species and records of eriophyid mites from New Zealand. New Zealand Journal of Zoology 16, 37 49. Memmott, J., Fowler, S.V., Paynter, Q., Sheppard, A.W. and Syrett, P. (2000) The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitats. Acta Oecologica 21, 213 222. Morin, L., Jourdan, M. and Paynter, Q. (1999) The gloomy future of the broom rust as a biocontrol agent. In Proceedings of the X International Symposium on Biological Control of Weeds, 4 14 July 1999, pp. 633 638, Montana State University, Bozeman, Montana, USA (ed Spencer, N) (2000). Morin, L., Sagliocco, J.-L., Hartley, D., Hosking, J.R., Cramond, P. and Washington, B. (2006) Broom rust in Australia. In 15th Australian Weeds Conference, Managing Weeds in a changing climate (eds Preston, C., Watts, J.H. and Crossman, N. D.) pp. 573-576. Weed Management Society of South Australia, Adelaide Convention Centre, 24 28 September 2006, Adelaide South Australia. Paynter, Q., Downey, P.O. and Sheppard, A.W. (2003) Age structure and growth of the woody legume weed Cytisus scoparius in native and exotic habitats: Implications for control. Journal of Applied Ecology 40, 470 480. Paynter, Q., Fowler, S.V., Memmott, J. and Sheppard, A.W. (1998) Factors affecting the establishment of Cytisus scoparius in southern France: implications for managing both native and exotic populations. Journal of Applied Ecology 35, 582 595. Rees, M. and Paynter, Q. (1997) Biological control of Scotch broom: Modelling the determinants of abundance and the potential impact of introduced insect herbivores. Journal of Applied Ecology 34, 364 377. Rowell, R.J. (1991) Ornamental Flowering Shrubs in Australia. NSW University Press, Sydney. Sheppard, A.W., Hodge, P., Paynter, Q. and Rees, M. (2002) Factors affecting invasion and persistence of broom Cytisus scoparius in Australia. Journal of Applied Ecology 39, 721 734. Syrett, P., Fowler, S.V., Coombs, E.M., Hosking, J.R., Markin, G.P., Paynter, Q.E. and Sheppard, A.W. (1999) The potential for biological control of Scotch broom (Cytisus scoparius) (Fabaceae) and related weedy species. Biocontrol News and Information 20, 17 33. Waloff, N. and Richards, O.W. (1977) The effect of insect fauna on growth, mortality and natality of broom, Sarothamnus scoparius. Journal of Applied Ecology 14, 787 798. Wapshere, A.J. and Hosking, J.R. (1993) Biological control of broom in Australia. In Proceedings of the 10th Australian and 14th Asian-Pacific Weed Conference (eds Swarbrick, J.T., Henderson, C.W.L., Jettner, R.J., Streit, L., and Walker, S.R.) pp. 94 98, Brisbane, Australia, 6 10 September 1993. Waterhouse, B.M. (1988) Broom (Cytisus scoparius) at Barrington Tops, New South Wales. Australian Geographical Studies 26, 239 248. Williams, P.A. (1981) Aspects of the ecology of broom (Cytisus scoparius) in Canterbury, New Zealand. New Zealand Journal of Botany 19, 31 43.
414 Session 9 Table 1. Results of host specificity tests conducted by CSIRO with Aceria genistae Plant species tested No. of replicates Mean no. galls attached/plant Test duration (weeks) Tribe Genisteae, Subtribe Genistineae Cytisus alba 5 10 28 No Yes Cytisus Crimson King 5 10 28 Yes Yes Chamaecytisus palmensis (H.Christ) F.A.Bisby & K.W.Nicholls 9 7.6 27, 34 No Yes Spartium junceum L. 5 5.4 66 No Yes Genista monspessulana (L.) L.A.S.Johnson 5 10 23 No Yes Laburnum x watereri (G.Kirchn.) Dippel 6 6.7 14 No Yes Ulex europaeus L. 5 10 29 No Yes Lupinus angustifolius L. cv Yandee 5 6.8 13 No Yes Lupinus angustifolius cv Merritt 5 6.2 13 No Yes Lupinus angustifolius L. * NZ origin 5 6.2 13 No Yes Lupinus polyphyllus Lindl* 4 5.8 20 No Yes Subfamily Faboideae, Tribe Bossiaeeae Bossiaea buxifolia A.Cunn. 5 10 25 No Yes Goodia lotifolia Salisb. 4 8.3 22 No Yes Hovea acutifolia A.Cunn. ex G.Don 5 6.6 19 No Yes Hovea montana (Hook.f.) J.H.Ross 4 10 26 No Yes Tribe Crotalarieae Crotalaria cunninghamii R.Br. 5 5.2 22 No Yes Tribe Sophoreae Sophora microphylla Aiton* 5 6.1 16 No Yes Tribe Indigofereae Indigofera australis Willd. 5 8 27, 19 No Yes Tribe Loteae Live mites on test Galls on control
Session 9 415 Plant species tested No. of replicates Mean no. galls attached/plant Test duration (weeks) Live mites on test Galls on control Lotus australis Andrews 5 10 27 No Yes Tribe Mirbelieae Davesia mimosoides R.Br. 5 5.4 16 No Yes Dilwynia juniperina Lodd., G.Lodd. & W.Lodd. 5 5.4 17 No Yes Dillwynia prostrata Blakely 5 7 18 No Yes Eutaxia baxteri Knowles & Westc. 5 6.2 21 No Yes Oxylobium ellipticum (Vent.) R.Br. 5 10 25 No Yes Podolobium ilicifolium (Andrews) Crisp & P.H.Weston 5 6.2 20 No Yes Pultenaea microphylla Sieber ex DC. 4 10 25 No Yes Pultenaea juniperina Labill. 5 6.2 20 No Yes Viminaria juncea (Schrad.) Hoffmanns. 5 5.4 25 No Yes Tribe Galegeae Clianthus puniceus (G.Don) Sol. ex Lindl.* 5 6.2 15 No Yes Carmichaelia arborea (G.Forst.) Druce* 5 5 21 No Yes Carmichaelia kirki Hook.f. * 5 5 21 No Yes Carmichaelia monroi Hook.f. * 5 5 15 No Yes Carmichaelia stevensonii (Cheeseman) Heenan* 5 6.4 15 No Yes Carmichaelia torulosa (Kirk) Heenan* 5 5.4 24 No Yes Tribe Phaseoleae, Subtribe Glycininae Glycine clandestina J.C.Wendl. 5 5.8 15 No Yes Subtribe Kennediinae Hardenbergia violacea (Schneev.) Stearn 4 10 27 No Yes
416 Session 9 Plant species tested No. replicates Mean no. galls attached/plant Test duration (weeks) Live mites on test Tribe Trifolieae Medicago polymorpha L. 5 6.8 18 No Yes Medicago sativa L. 5 7 18 No Yes Trifolium repens L. 5 5.8 19 No Yes Trifolium subterraneum L. 5 6.4 18 No Yes Subfamily Mimosoideae, Tribe Acacieae Acacia dealbata Link 5 10 25 No Yes Galls on control Acacia melanoxylon R.Br. 5 10 26 No Yes * species tested for approval assessment in New Zealand Some gall development occured Some gall development occurred but mites did not survive The taxonomy of ornamental broom cultivars is poorly defined in Australia. We chose to select one with and one without C. scoparius as a likely parent. We have selected Cytisus praecox Crimson King which is considered a cultivar of Cytisus scoparius or Cytisus scoparius Andreanus crossed with Cytisus multiflorus (Rowell 1991) and a cultivar named Cytisus alba Snow Queen. There is no species called Cytisus alba, but Cytisus albus (Lam.) Link is now considered to be Cytisus multiflorus (L Hér.) Sweet while Cytisus albus Hacq. is now considered to be Chamaecytisus albus (Hacq.) Rothm. The main parent of the selected hybrid Cytisus alba Snow Queen is probably Cytisus multiflorus as this species is the parent of a number of ornamental broom hybrids (Rowell 1991). Table 2. Releases and establishment of A. genistae in Australia for the period 2008-2011 State No. sites where releases conducted No. sites with establishment confirmed Proportion established Victoria 37 8 0.21 Tasmania 37 17 0.46 South Australia 26 9 0.34 NSW 6 1 0.17 Total 106 34 0.32