Session 9 Post-release Evaluation and Management 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. Sagliocco1, A. Sheppard2, J. Hosking3, P. Hodge4, Q. Paynter5, H. Gourlay6 and J. Ireson7

1Biosciences Research Division, Department of Primary Industries, Frankston, 3199, Victoria, Australia [email protected] 2CSIRO Ecosystems Sciences, GPO Box 1700, Canberra, 2601, ACT, Australia [email protected] 3Department of Primary Industries, Tamworth Agricultural Institute, Calala, 2340, NSW, Australia [email protected] 4c/o CSIRO Ecosystems Sciences, GPO Box 1700, Canberra, 2601, ACT, Australia 5Landcare Research, St Johns, Auckland, 1072, New Zealand [email protected] 6Landcare Research, Lincoln, 7640, New Zealand [email protected] 7Tasmanian Institute of Agricultural Research, University of Tasmania, New Town 7008, Tasma- nia, Australia [email protected]

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 implement, expensive, have negative environmental impacts and require follow-up due to large seed banks and reinvasion by seedlings and young plants The leguminous shrub Scotch broom, Cytisus (Downey and Smith 2000; Paynter et al 1998). scoparius (L.) Link (Fabaceae) is native to the UK, A number of demography studies have focused western, southern and central Europe. There it is on patterns and processes of broom invasion in its considered moderately weedy and it occasionally native range (France) (Paynter et al. 2003; Paynter colonises forest areas and pastures. Elsewhere, it et al 1998) and its introduced range in Australia has become a serious invader in several countries: (Downey and Smith 2000; Paynter et al 2003; eastern and western USA including Hawaii, British Sheppard et al 2002; Waterhouse 1988) and New Columbia, Australia, New Zealand, Chile and Zealand (Paynter et al. 2003; Williams 1981). In India. Mechanical and chemical control methods of addition, studies in the weed’s native range have broom in invaded natural ecosystems are difficult to highlighted the role of natural enemies in limiting

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broom performance (Waloff and Richards 1977), as Aceria spartii). Mites identified as A. Genistae especially the potential of arthropods to reduce seed discovered on stunted shoot tips of gorse and production and broom longevity (Rees and Paynter French broom, Genista monspessulana (L.) L.A.S. 1997). Broom plants in Australia and New Zealand Johnson in the USA caused limited damage and are largely devoid of specialist insect herbivores did not develop on any other species (Chan and (Memmott et al 2000), indicating that biological Turner 1998). Similarly, mites identified as A. control may have some potential to control broom genistae were found infesting gorse, U. europaeus in these countries. New Zealand (NZ) began a but not broom, in New Zealand (Manson 1989). broom biological control program by releasing the seed feeding beetle, Bruchidius villosus (Fabricius) Methods and the sap-sucking psyllid, Arytainilla spartiophila (Förster) in 1987 and 1993 respectively. Meanwhile, an accidental introduction of the broom twig-mining Host specificity testing moth, Leucoptera spartifoliella Hübner resulted in extensive damage to broom in NZ south island (Syrett Initial testing of A. genistae by CABI (the et al 1999). Building on New Zealand’s experience, Centre for Agriculture and Biosciences CSIRO (The Commonwealth Scientific and International) and CSIRO was conducted with a Industrial Research Organisation) and the New small number of broom’s close relatives at CSIRO South Wales Department of Agriculture imported European laboratory in Montferrier (France). Field L. spartifoliella from NZ and released it in 1993 tests were carried out under natural conditions in (Wapshere and Hosking 1993), followed by releases a native broom infestation where Cytisus striatus of A. spartiophila in 1994 and B. villosus in 1995 (Hill) Rothm., Chamaecytisus palmensis (H.Christ) (Syrett et al 1999). A fourth agent, the eriophyid gall, F.A.Bisby & K.W.Nicholls, Spartium junceum L., Aceria genistae (Nalepa) was identified as a potential Genista tinctoria L., Medicago arborea L., Laburnum biological control agent during European field anagyroides Medik. and C. scoparius were planted as surveys (Hosking 1990; Syrett et al 1999; Wapshere test plants. After two years, A. genistae galls were only and Hosking 1993). A. genistae was originally on C. scoparius and no attack on any of the species described by Nalepa from galls developing on Scotch tested had been observed. Additional tests were broom in eastern France. The known native range conducted in a glasshouse where A. genistae galls of the mite includes the UK, Italy, Spain and central were tied onto C. palmensis and U. europaeus with Europe. Colonies of A. genistae start at the inner C. scoparius as a control. Gall development occurred base of stem buds and cause growth deformities on on C. scoparius only. The high specificity of the mite bud burst becoming round, pubescent galls. Several towards C. scoparius resulted in comprehensive host overlapping generations develop in galls during specificity study being conducted in Australia. A. spring and summer. Non-woody galls wither in late genistae galls collected in the Cevennes mountains summer and autumn, forcing mites to crawl into range, north of Montpellier (France) were shipped dormant stem buds where they overwinter. Gravid to the CSIRO quarantine facility in Canberra for females are also wind dispersed in spring and rearing and further evaluation against a number of there is a sex ratio of about 1:20 male: females (J-L Australian and New Zealand native plant species Sagliocco pers. obs.). ‘Aceria genistae’ is probably a (Table 1). In quarantine, mites were inoculated onto complex of specific forms or sibling species. It has broom plants where they developed galls, providing been recorded on a number of Genisteae species a large colony for host specificity tests. including Cytisus spp., Ulex europaeus L., Genista There are no Australian native plant species spp. and Spartium junceum L. (Castagnoli 1978). in the tribe Genisteae. Therefore, the focus of the However, Cromroy (1979) (Cromroy 1979) noted testing was on species of economic importance in the that eriophyids are often highly host-specific, even Genisteae and other related tribes in the Faboideae, to the level of plant form. Castagnoli (1978) has plus native species in related tribes, with less shown that A. genistae developing on broom did intensive testing of representative Australian natives not develop on S. junceum, while the mites found in other subfamilies of the Fabaceae. Plants tested for on Spartium are a separate species (redescribed New Zealand included local cultivars of two Lupinus

XIII International Symposium on Biological Control of Weeds - 2011 Session 9 Post-release Evaluation and Management 411 species and seven species representing all native In 2002, CSIRO submitted an application to genera with the exception of the monophyletic genus federal agencies to obtain approval for release of Montigena. A. genistae into the Australian environment. After Between 1999 and 2001, 34 taxa and cultivars examining the submission, AQIS (the Australian from 12 tribes were tested as part of the risk Quarantine and Inspection Service) Plant Biosecurity assessment required to obtain release permits for the Australia and the Department of Environment mite in Australia and in New Zealand (Table 1). Each approved release of the mite in the environment. In test consisted of five replicates of one taxon paired 2003, before the mite was released, a broom fungus with five C. scoparius of similar size as controls. Each that had been ruled out as a broom potential biological plant tested had dormant buds required for mite control agent for Australia due to lack of specificity development. A. genistae galls were harvested from (Morin et al 1999) was discovered in the Canberra broom gall-producing plants kept in quarantine, and mite culture (Morin et al 2006). Consequently, the each gall was scored for number of mites present. mite culture had to be destroyed and its release was Five to ten galls with comparable numbers of mites postponed. A lack of funding caused further delays. were then tied onto the foliage of each test plant and In 2006, with joint funding from the Australian control and covered with a plastic bag for 72 hours to Government and the Department of Primary prevent galls drying out too quickly and to encourage Industries (DPI), Frankston, Victoria, Australia mites to migrate out of the galls. Test and control imported the mite into quarantine in Frankston and plants were kept at temperatures of 18° C (day) and a clean colony protocol was developed using the 12° C (night) (10 hrs light: 14 hrs dark) under high transfer of individual mites. Mite populations were intensity artificial light for one month to help mites increased by transferring mites onto new plants colonise plants while there was no bud development. for several generations until approval for release After one month temperatures were increased to 20° was granted. Outside quarantine, broom plants C (day) and 15° C (night) (12 hrs light: 12 hrs dark) were inoculated with mites to provide material for to initiate bud growth resulting in gall formation releases. In October 2008, the first releases were caused by mite feeding activity. After three to five conducted in the Australian Alps in eastern Victoria, months, and once several galls had developed and a rearing colony was established in Tasmania. on control plants, all fresh buds on the test plants Subsequently, Tasmania provided galls to South were dissected for mite presence. When test plants Australia and New South Wales (NSW) for releases. were too large, an area equivalent to the smallest test plants was sub-sampled for mite presence. Approval for release in New Zealand

Results As A. genistae was already present in New Zealand on gorse (Manson 1989), Environmental Risk Management Authority approval to release the Host specificity testing broom form was not required. Nevertheless, testing of the broom form from Europe was conducted as if Among the species tested, some initial gall it was a new organism to New Zealand. Ministry of development was observed on S. junceum and C. Agriculture and Fisheries approval to release A. genistae palmensis. However mites did not survive and no from containment was granted in November 2007. further development was observed. Initial gall formation was also observed on Cytisus ‘Crimson Releases and establishment in King’, an ornamental with C. scoparius parentage, Australia but mite survival did not occur. No gall development or mite presence was observed on any other species In Victoria a number of nursery sites intended including all Australian and New Zealand natives. for detailed monitoring of mite survival and dispersal were established using two release Approval for release in Australia methods. In autumn, two to four broom plants bearing galls were planted in the ground at the edge

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of an infestation, and were watered and fertilised disease (unidentifiedFusarium ) is associated with to allow their establishment and mite migration. A gall formation and mite activity (Daniel Than pers. direct release technique was also used. It consisted comm.). It is not yet known if the mite may enhance of attaching broom branches with galls on 20 wild disease occurrence and if it plays a role in plant dieback. plants at the edge of the infestation and marking each plant with surveyor tape for later monitoring. Discussion At release sites to be assessed for mite establishment, only the later method was used. Monitoring of transferred plants and gall numbers, mite presence TheC. scoparius form of A. genistae was shown to and gall formation was conducted at all sites twice be restricted to this weed and during host specificity a year, in spring and autumn, mostly because of the studies did not survive on different taxa tested. difficulties to access most of the remote release sites The mite was released in 2008 both in Australia in the high country. In the other states, the second and New Zealand and since then each country has release method was mostly used and monitoring was implemented release and monitoring programs. conducted whenever possible. During the period In Australia, the mite has so far established at a 2008-2011, at total of 106 releases of A. genistae were third of the release sites, while in New Zealand the conducted in four states. Releases were conducted in establishment success rate is currently at about 50%. the Australian Alps (Victoria), throughout the state Releases are on-going in both countries. In Australia, of Tasmania, around Adelaide (South Australia), differences in the time required for mites to develop near Canberra (southern NSW) and in the Northern galls in the field have been observed between Victoria Tablelands (NSW).The altitude of most of the and Tasmania as well as with establishment success release sites ranged between 220 and 670 m, the rate. It is not known if this is due to climatic reasons highest sites being at 1,500 m altitude at Barrington or the occurrence of different broom plant forms in Tops (southern end of the Northern Tablelands in these states. Mite activity results in severe stunting NSW). In 2011, establishment of the mite had been of growth and reduction of plant biomass, reduced confirmed at 34 of the sites (32 %) (Table 2). Releases seed production and very occasionally reported of the mite and monitoring of its establishment plant death in its native range. Plant death has been and dispersal are continuing. In the field, mites observed in New Zealand following release, although were observed to induce gall formation after 6-12 this has not been observed in Australia yet. In Victoria, months. Although the program still being in its early a field study is currently underway to quantify the stage, mites were observed to establish and cause impacts of the mite and other natural enemies. gall formation faster in Tasmania than in Victoria, both under semi-natural conditions and in the field. Acknowledgements

Releases and establishment in New Zealand Funding for the host specificity studies of A. genistae between 1990 and 2003 was provided by Since 2008, 40 releases of the mite have been the Barrington Tops Broom Council, NSW State made in New Zealand. Establishment has been Forests, the Hunter Pastoral Company and the NSW confirmed at approximately 50% of these sites. Gall Government through its Environmental Trusts. The formation at many sites has been extensive, covering importation of A. genistae in Victoria in 2006 was much of infested broom plants with some mature funded by the Australian Government’s Defeating plants bearing hundreds of galls. Significant damage the Weeds Menace program (DWM) and DPI has been recorded in some areas where whole Victoria. The releases in the four states in Australia branches of broom plants have been observed to were funded by the Australian Government’s Caring suffer dieback and in some cases whole plants have for Our Country program (CFOC) with, in Victoria, died. Gall formation has also been found on broom co-funding from DPI and financial support from plants in the absence of gall mites although these the Goulburn-Murray Water Corporation and galls have a different architecture to those caused Parks Victoria. Acknowledgements are due to Helen by A. genistae. Initial observations suggest that a Parish (Landcare Research, Lincoln, New Zealand) and Richard Hill (Richard Hill and Associates,

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Lincoln, New Zealand) for their contribution in in Australia. In 15th Australian Weeds Conference, establishing mite colonies, Richard Holloway, Wade Managing Weeds in a changing climate (eds Preston, Chatterton (University of Tasmania, Hobart) and C., Watts, J.H. and Crossman, N. D.) pp. 573-576. Susan Ivory (SARDI, Adelaide, South Australia) for Weed Management Society of South Australia, their workand commitment in rearing and releasing Adelaide Convention Centre, 24–28 September 2006, the mite. Adelaide South Australia. Paynter, Q., Downey, P.O. and Sheppard, A.W. (2003) Age structure and growth of the woody legume References weed Cytisus scoparius in native and exotic habitats: Implications for control. Journal of Applied Ecology Castagnoli, M. (1978) Ricerche sulle cause de 40, 470–480. deperimento e moria dello Spartium junceum L. in Paynter, Q., Fowler, S.V., Memmott, J. and Sheppard, Italia. Eriophyes genistae (Nal.) e E. spartii (G. Can.) A.W. (1998) Factors affecting the establishment of (Acarina: Eriophyoidea): Ridescrizione, cenni di Cytisus scoparius in southern France: implications for biologia e danni. Redia 61, 539–550. managing both native and exotic populations. Journal Chan, K.L. and Turner, C.E. (1998) Discovery of the gall of Applied Ecology 35, 582–595. mite Aceria genistae (Nalepa) (Acarina: Eriophyidae) Rees, M. and Paynter, Q. (1997) Biological control on gorse and French broom in the United States. Pan- of Scotch broom: Modelling the determinants of Pacific Entomologist 74, 55–57. abundance and the potential impact of introduced Cromroy, H.L. (1979) Eriophyoidea in biological insect herbivores. Journal of Applied Ecology 34, control of weeds, in Recent Advances in Acarology. 364–377. In 5th International Congress of Acarology (ed J.G Rowell, R.J. (1991) Ornamental Flowering Shrubs in Rodriguez) 473–475. Academic Press, New York, San Australia. NSW University Press, Sydney. Francisco, London, Michigan State University, East Sheppard, A.W., Hodge, P., Paynter, Q. and Rees, M. Lansing, Michigan. (2002) Factors affecting invasion and persistence Downey, P.O. and Smith, J.M.B. (2000) Demography of of broom Cytisus scoparius in Australia. Journal of the invasive shrub Scotch broom (Cytisus scoparius) Applied Ecology 39, 721–734. at Barrington Tops, New South Wales: Insights for Syrett, P., Fowler, S.V., Coombs, E.M., Hosking, J.R., management. Austral Ecology 25, 477–485. Markin, G.P., Paynter, Q.E. and Sheppard, A.W. Hosking, J.R. (1990) The feasibility of biological control (1999) The potential for biological control of Scotch of Cytisus scoparius (L.) Link. Report on overseas broom (Cytisus scoparius) (Fabaceae) and related study tour, June-September 1990, unpublished weedy species. Biocontrol News and Information 20, report, New South Wales Department of Agriculture 17–33. and Fisheries, Tamworth, Australia. Waloff, N. and Richards, O.W. (1977) The effect of insect Manson, D.C.M. (1989) New species and records of fauna on growth, mortality and natality of broom, eriophyid mites from New Zealand. New Zealand Sarothamnus scoparius. Journal of Applied Ecology Journal of Zoology 16, 37–49. 14, 787–798. Memmott, J., Fowler, S.V., Paynter, Q., Sheppard, A.W. Wapshere, A.J. and Hosking, J.R. (1993) Biological and Syrett, P. (2000) The invertebrate fauna on control of broom in Australia. In Proceedings of broom, Cytisus scoparius, in two native and two exotic the 10th Australian and 14th Asian-Pacific Weed habitats. Acta Oecologica 21, 213–222. Conference (eds Swarbrick, J.T., Henderson, C.W.L., Morin, L., Jourdan, M. and Paynter, Q. (1999) The Jettner, R.J., Streit, L., and Walker, S.R.) pp. 94–98, gloomy future of the broom rust as a biocontrol agent. Brisbane, Australia, 6–10 September 1993. In Proceedings of the X International Symposium on Waterhouse, B.M. (1988) Broom (Cytisus scoparius) Biological Control of Weeds, 4–14 July 1999, pp. 633– at Barrington Tops, New South Wales. Australian 638, Montana State University, Bozeman, Montana, Geographical Studies 26, 239–248. USA (ed Spencer, N) (2000). Williams, P.A. (1981) Aspects of the ecology of broom Morin, L., Sagliocco, J.-L., Hartley, D., Hosking, J.R., (Cytisus scoparius) in Canterbury, New Zealand. Cramond, P. and Washington, B. (2006) Broom rust New Zealand Journal of Botany 19, 31–43.

XIII International Symposium on Biological Control of Weeds - 2011 414 Session 9 Post-release Evaluation and Management on Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Galls plants control No No No No No No No No No No No No No No No No No Live Yes† mites mites plants on test test on 28 28 66 23 14 29 13 13 13 20 22 19 25 26 22 16 Test 27, 34 27, 19 (weeks) duration 8 10 10 10 10 10 10 7.6 5.4 6.7 6.8 6.2 6.2 5.8 8.3 6.6 5.2 6.1 Mean no. galls no. Mean attached/plant

5 5 9 5 5 6 5 5 5 5 4 5 4 5 4 5 5 5 No. of of No. replicates Aceria genistae * * (H.Christ) F.A.Bisby & K.W.Nicholls & K.W.Nicholls (H.Christ) F.A.Bisby R.Br. L. cv Yandee cv Merritt Aiton Willd. A.Cunn. ex G.Don A.Cunn. (Hook.f.) J.H.Ross (Hook.f.) Salisb. † § Plant speciesPlant tested ‘Crimson King’ ‘Crimson Cytisus Chamaecytisus palmensis Spartium junceum L.‡ Genista monspessulana (L.) L.A.S.Johnson (G.Kirchn.) Dippel (G.Kirchn.) Laburnum x watereri L. europaeus Ulex Lupinus angustifolius Lupinus angustifolius Lupinus angustifolius L. * NZ origin Lupinus polyphyllus Lindl Bossiaeeae Tribe Faboideae, Subfamily Bossiaea buxifolia A.Cunn. Hovea acutifolia montana Hovea Goodia lotifolia Crotalarieae Tribe Crotalaria cunninghamii Loteae Tribe Tribe Sophoreae Tribe Sophora microphylla Indigofereae Tribe australisIndigofera Tribe Genisteae, Subtribe Genistineae Subtribe Genisteae, Tribe alba Cytisus Table 1. Results of host specificity tests conducted by CSIRO with Table

XIII International Symposium on Biological Control of Weeds - 2011 Session 9 Post-release Evaluation and Management 415 Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes plants control Galls on No No No No No No No No No No No No No No No No No No Live mites mites plants on test test on 27 16 17 18 21 25 20 25 20 25 15 21 21 15 15 24 15 27 Test (weeks) duration 7 5 5 5 10 10 10 10 5.4 5.4 6.2 6.2 6.2 6.4 5.4 6.2 5.4 5.8 Mean no. galls no. Mean attached/plant 5 5 5 5 5 5 5 4 5 5 5 5 5 4 5 5 5 5 No. of of No. replicates * (Cheeseman) Heenan (Andrews) Crisp & P.H.Weston Crisp (Andrews) (Schneev.) Stearn (Schneev.) (G.Forst.) Druce * (G.Forst.) (Vent.) R.Br. (Vent.) Hook.f. * Hook.f. Labill. Lodd., G.Lodd. & W.Lodd. R.Br. Blakely J.C.Wendl. Hook.f. * Hook.f. (Schrad.) Hoffmanns. Andrews Plant speciesPlant tested australis Lotus Tribe Mirbelieae Tribe mimosoides Davesia Dilwynia juniperina Dillwynia prostrata & Westc. Knowles baxteri Eutaxia Oxylobium ellipticum Podolobium ilicifolium Sieber ex DC. microphylla Pultenaea Pultenaea juniperina Viminaria juncea Galegeae Tribe Sol. ex Lindl.* (G.Don) puniceus Clianthus Carmichaelia arborea Carmichaelia kirki Carmichaelia monroi Carmichaelia stevensonii * Heenan torulosa (Kirk) Carmichaelia Phaseoleae, Glycininae Subtribe Tribe Glycine clandestina Kennediinae Subtribe violacea Hardenbergia

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Yes Yes Yes Yes Yes Yes plants control Galls on as a likely parent. We have as a likely parent. We No No No No No No plants on test test on Live mites Live mites (Lam.) Link is now considered to be C. scoparius 18 18 19 18 25 26 Test (weeks) duration ‘Andreanus’ crossed with Cytisus multiflorus ‘Andreanus’ (Hacq.) Rothm. The main parent of the selected hybrid (Hacq.) Rothm. but Cytisus albus 0.32 0.17 0.34 0.46 0.21 7 10 10 6.8 5.8 6.4 Mean no. galls no. Mean attached/plant Proportion established Proportion Cytisus alba, or Cytisus scoparius - Chamaecytisus albus 5 5 5 5 5 5 licates No. rep 1 9 8 34 17 Cytisus scoparius ment confirmed ment Australia. We chose to select one with and without Australia. We - with establish sites No.

as this species is the parent of a number ornamental broom hybrids (Rowell 1991). Hacq. is now considered to be Snow Queen’. There is no species called Snow Queen’. 6 26 37 37 106 in Australia for the period 2008-2011 A. genistae in conducted Cytisus multiflorus Cytisus alba No. sites where releases where sites No.

‘Crimson King’ which is considered a cultivar of ‘Crimson King’ L. L. R.Br. (L’Hér.) Sweet while Cytisus albus (L’Hér.) L. L. Link Snow Queen’ is probably Snow Queen’ Total NSW South Australia South Tasmania Victoria State Plant speciesPlant tested Tribe Trifolieae Tribe Medicago polymorpha Medicago sativa Medicago Trifolium repensTrifolium Trifolium subterraneumTrifolium Subfamily Mimosoideae, Tribe Acacieae Tribe Mimosoideae, Subfamily dealbata Acacia Acacia melanoxylon Acacia Cytisus multiflorus selected Cytisus praecox (Rowell 1991) and a cultivar named ‘ Cytisus alba ‘ * 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 2. Releases and establishment of Table

XIII International Symposium on Biological Control of Weeds - 2011