Biological control of fruticosus agg. (blackberry): is the leaf the only option for ?

Jean Louis Sagliocco1 and Eligio Bruzzese1,2

Summary Rubus fruticosus aggregate (European blackberry) is a complex weed that is listed as a Weed of National Significance because of its economic and environmental impacts in temperate Australia. A biological- control program for R. fruticosus agg. commenced in the late 1970s and resulted in the release of the rust violaceum (Uredinales), because of its specificity and potential to suppress the weed through defoliation. The impact of the rust varies between R. fruticosus taxa and between locations and years. While the introduction of additional isolates of P. violaceum is being investigated by the Cooper- ative Research Centre for Australian Weed Management, a literature review was carried out to identify additional natural enemies that may have potential for the biological control of R. fruticosus agg. Results reveal that a fungus, an eriophyid mite and a number of deserve further consideration.

Keywords: , biological control, fungi, Rubus fruticosus.

Introduction Research Centre for Australian Weed Management has a current project aimed at the introduction of additional Rubus fruticosus L. aggregate (European blackberry) is isolates of P. violaceum with improved pathogenicity a complex weed that is listed as a Weed of National and targeted at a wider range of taxa of R. fruticosus Significance in Australia, because of its economic and agg. in Australia (Evans et al. 2003). There are, environmental impacts in the temperate climatic zones however, limitations to its effectiveness in suppressing of the south-east and south-west of the continent. The this complex weed comprising of several taxa and these Weeds of National Significance Blackberry Strategic are well documented (Evans et al. 1998, Pigott et al. Plan (ARMCANZ et al. 2001) states the following 2001). The current study is a review of the natural research and extension opportunity: “Concentrate on enemies recorded on R. fruticosus agg. in the literature further biological control options for blackberry with the view of identifying additional natural enemies growing in situations where current biological control that may complement the impact of the P. violaceum is not effective”. and increase the suppression of R. fruticosus agg. throughout its range in temperate Australia. Phragmidium violaceum (Schultz) Winter (black- berry leaf rust) is a useful and effective biological- control agent for R. fruticosus agg. in temperate Materials and methods southern Australia (Marks et al. 1984, Bruzzese & Field 1985, Bruzzese & Hasan 1986, Mahr & Bruzzese An extensive literature survey was undertaken in 1998, Evans & Bruzzese 2003). The Cooperative abstracts referring to R. fruticosus agg. and possible associated organisms using the following resources: reference works held in Australian libraries, Review of 1 Department of Primary Industries, Keith Turnbull Research Institute, Applied Entomology (1913–1972) and the electronic PO Box 48, Frankston, Victoria 3199, Australia. databases CAB Abstracts (1972–2003), Agricola 2 Cooperative Research Centre for Australian Weed Management, PO Box 48, Frankston, Victoria 3199, Australia. (1992–2002) and Current Contents. The Victorian Corresponding author: J.L. Sagliocco Plant Pest and Disease Collections Database, Agricul- . ture Victoria (2001) was also consulted to identify

141 Biological control of blackberry diseases of R. fruticosus agg. already recorded in “Marion”, “Evergreen”, “Kotata” and “Waldo” in Australia. All organisms found associated with R. fruti- Oregon, United States of America (USA) (Strik 1996) cosus agg. were checked for other associations and and on thornless blackberry cultivars “Thornfree” and organisms not restricted to R. fruticosus agg. were “Hull Thornless” in Hungary (Kövics 1997). There is rejected. only one record of this disease on a Rosaceae other than Rubus, Potentilla sterilis (Feige et al. 2001), but this needs to be confirmed. This disease was commonly Results recorded causing dieback of first-year canes of R. fruti- cosus agg. in southern by Bruzzese (1982b). A review of Australian and international databases and Septocyta ruborum infects only first-year canes and literature has identified additional fungal pathogens, symptoms only develop after a chilling requirement is insects and mites attacking R. fruticosus agg. in the met. Severely affected canes die the following spring Northern Hemisphere. Any fungal pathogen, or prior to flowering in the USA (Pscheidt 2002). mite recorded on Rubus idaeus (raspberry) and any Rubus spp. not included in the R. fruticosus agg. (Tutin et al. 1968) was excluded from the list of potential Eriophyes rubicolens (Canestrini) Acarina: biocontrol agents (Table 1). Additional exclusions were Eriophyidae fungal pathogens and insects already recorded This eriophyid mite was described from specimens attacking Rubus spp. in Australia (Bruzzese 1980a,b) or collected from R. fruticosus agg. at Veneto, Italy recorded in the Victorian Plant Pest and Disease (Canestrini 1891), and was included in the fauna of Collections Database. This list may not be exhaustive Italy (Canestrini 1892). The mite (also known as as a number of rare taxonomic texts on insects, mites Phyllerium rubi Fr.= Erineum rubi Pers.) is described and fungi could not be accessed at the time of this to produce erineum on the lower side of leaves of study. several wild species of Rubus spp. (Nalepa 1892) in eastern France (Nalepa 1929). The mite has no alterna- Septocyta ruborum (lib.) Petrack tive host (Amrine & Stasny 1994). (Coelomycetes) (blackberry purple blotch) Ectoedemia erythrogenella (de Joannis) This fungus is widespread in Europe on wild and commercial cultivars of R. fruticosus agg. (Koellreuter Lepidoptera: Nepticulidae 1952, Oort 1952, Punithalingam 1980, Kövics 1997). It Originally described from France (Joannis 1907), is also recorded as a disease of blackberry cultivars this univoltine Lepidoptera species has also been

Table 1. Organisms with potential for the biological control of Rubus fruticosus agg.

Organism Distribution Host plants Plant References association Fungi Coelomycetes Septocyta ruborum Northern Hemisphere Rubus fruticosus Stems Koellreuter (1952), Oort (1952), Punithaligam (1980) Acarina Eriophyidae Eriophyes rubicolens Italy, France Rubus fruticosus Leaf erineum Canestrini (1891, 1892), Nalepa (1892, 1929), Amrine & Stasny (1994) Lepidoptera Nepticulidae Ectoedemia erythrogenella Western Europe Rubus fruticosus Leaf miner Joannis (1907), Heath (1976) Cephidae Hartigia albomaculata Southern Europe Rubus fruticosus Stem borer Scheibelreiter (1979), Bruzzese (1982a, 1982b) Hymenoptera Claremontia alternipes Europe, Mongolia, Rubus spp. Leaf feeder Lacourt (1999) Siberia Empria excisa Europe, northern Rubus ulmifolius Leaf feeder Lacourt (1999) , Mongolia militaris Central and southern Rubus spp. Leaf feeder Lacourt (1999) Europe Macrophya montana montana Central and southern Rubus spp. Leaf feeder Lacourt (1999) Europe, Turkey, Iran Monophadnoides ruficrucis Central and southern Rubus ulmifolius, Leaf feeder Lacourt (1999) Europe, Turkey Rubus spp.

142 Biological control of blackberry recorded from the United Kingdom (UK), Switzerland, caused by this disease warrants further studies to deter- Austria, Italy and Majorca (Heath 1976). Females lay mine whether specialization and levels of pathogenicity eggs on leaves in July and larvae develop in leaf mines to different taxa of R. fruticosus agg. and commercial throughout summer until early winter. The literature cultivars exist. This fungus would complement the gives R. fruticosus agg. as the only recorded host plant. impact of P. violaceum by causing dieback of first-year canes in early spring, prior to defoliation of R. fruticosus Claremontia alternipes (Klug.) Benson, agg. by the rust. Hymenoptera: Tenthredinidae The absence of reported association of the lepidop- teran E. erythrogenella with blackberry species other This is reported to feed on R. fruticosus than R. fruticosus agg. strongly suggests that this (Lacourt 1999) and is one of the few sawfly species insect is specific to the weed. However, because the reported to feed on Rubus spp. Other species are insect has only one generation per annum and larvae Empria excisa (Thomson) Enslin, Macrophya militaris develop in a mine in a single leaf, it is unlikely that (Klug.) Taschenberg, Macrophya montana montana this damage would significantly contribute to the (Scopoli) Kirby and Monophadnoides ruficrucis biocontrol of R. fruticosus agg. (Brullé) Benson. None of these species are mentioned in the recent literature and a further literature search The cephid H. albomaculata was identified in the late through old references is required to evaluate their host 1970s as a potential biocontrol agent for R. fruticosus range. They are thought to have leaf-feeding larvae, but agg. and field surveys have clarified its biology and the number of generations each year is unknown. distribution. Host-specificity tests done in cages have shown oviposition on some Rubus spp. and Rosa spp. Hartigia albomaculata (Stein) (Bruzzese 1982a). However, it is believed that these Hymenoptera: Cephidae results were due to the testing procedure in the labora- tory because this insect was never recorded to attack This sawfly was identified in the literature and from plants other than R. fruticosus in the field. Further host- field surveys in Europe for organisms attacking R. fruti- specificity field tests under natural conditions in the cosus agg. (Scheibelreiter 1979). Hartigia albomacu- region of origin should confirm the host range of this lata is univoltine and parthenogenetic and attack is insect. If specificity is confirmed, H. albomaculata restricted to first-year canes of R. fruticosus. Females could be introduced to complement the effect of P. viol- were observed to lay eggs in May with larvae devel- aceum because of its mechanical destruction of first- oping in canes for 6 weeks before overwintering in a year canes. cocoon, with pupation occurring during the following The eriophyid E. rubicolens is the only mite species spring (Bruzzese 1982a). Field surveys in southern which appears to be restricted to R. fruticosus agg. France showed that H. albomaculata was common on Apart from information given by Nalepa (1892) on the Rubus ulmifolius. Plants of Rubus caesius, Rosa canina production of erineum induced by the mite’s feeding, and Rosa rubiginosa present at the same survey sites no information is available on its biology, abundance or were never found to be attacked. host range within taxa of R. fruticosus agg. This can only be confirmed through surveys in the region of Discussion origin and host testing. This study has identified that the choice of addi- More than 50 oligophagous species are tional natural enemies for biological control of R. fruti- reported associated with R. fruticosus agg., not to cosus agg. in Australia is restricted. The organisms mention a greater number of polyphagous species. listed in Table 1 have some potential and require further Among the organisms identified, some were not previ- investigation. The reason for the restricted list of candi- ously considered for the biological control of R. fruti- dates is because there are a number of native Rubus spp. cosus agg., while one insect was the subject of in Australia and a small but significant brambleberry preliminary investigations and testing. industry that uses blackberry cultivars of mixed Euro- The only fungal pathogen of additional interest as a pean and American parentage. Any candidate biocon- potential candidate for the biological control of R. fruti- trol agent needs to have the potential to inflict cosus agg. is the blackberry purple blotch fungus, S. significant damage to the weed and has to be shown to ruborum. Although this fungus has been recorded on be host-specific before permission for its release into some commercial cultivars containing principally the Australian environment is given. American genetic material in the USA and on some thornless blackberry cultivars of mixed American and European parentage in Europe, the extent of cultivation Acknowledgements and importance of these cultivars in Australia needs to be established. Although Punithalingham (1980) reports The authors thank the Department of Sustainability and that no physiologic specialization of this pathogen has Environment, State Government of Victoria, for been reported, the significant dieback of first-year canes funding this study.

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