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Home , Buddleja, Buddlejaceae, Buddleja auriculata, Buddleja davidii, Buddleja globosa, Cionus

The disintegration of the and the biological control of davidii

M.K. Kay,1 B. Gresham,1 R.L. Hill2 and X. Zhang3

Summary The woody buddleia, Franchet, is an escalating problem for a number of resource managers in temperate regions. The ’s taxonomic isolation within the was seen as beneficial for its biological control in both and . However, the re- cent revision of the Scrophulariaceae has returned Buddleja L. to the Scrophulariaceae sensu stricto. Although this proved of little consequence to the New Zealand situation, it may well compromise Eu- ropean biocontrol considerations. Host-specificity tests concluded that the biocontrol agent, Cleopus japonicus Wingelmüller (Coleoptera, ), was safe to release in New Zealand. This - feeding proved capable of utilising a few non-target within the same clade as Buddleja but exhibited increased mortality and development times. The recent release of the weevil in New Zealand offers an opportunity to safely assess the risk of this agent to European belonging to the Scrophulariaceae.

Keywords: Cleopus, Buddleja, taxonomic revision, phylogeny.

Introduction there is no significant soil bank. The seed germi- nates almost immediately, and the density and rapid There are approximately 90 species of Buddleja L. early growth of buddleia seedlings suppresses other indigenous to the Americas, and (Leeu- pioneer species (Smale, 1990). wenberg, 1979), and a number have become natural- As a naturalized species, buddleia is a shade-intolerant ized outside their native ranges (Holm et al., 1979). colonizer of urban wastelands, riparian margins and Buddleia, Buddleja davidii Franchet, in particular, is an other disturbed sites, where it may displace indigenous escalating problem for resource managers in temperate species, alter nutrient dynamics and impede access regions and has been identified as a target for classi- (Smale, 1990; Bellingham et al., 2005). In New Zea- cal biological control in New Zealand (Kay and Smale, land, on sites prepared for exotic forest plantations, the 1990) and Europe (Sheppard et al., 2006). rapid growth of buddleia causes the suppression and a Buddleia is a large woody shrub of Asian origin that quantifiable loss of growth in newly planted Pinus ra- was introduced to the rest of the world as an ornamental diata Don. (Richardson et al., 1996). The inefficiencies species in the 1890s. It was considered naturalized in of conventional controls prompted the investigation of the UK in the 1930s and in New Zealand in the 1940s classical biological control (Kay and Smale, 1990). (Esler, 1988). It has many of the features that charac- The taxonomic isolation of a target weed from in- terize successful weed species, and it is ranked in the digenous and other valued non-target plant species re- top ten invasive plants of Britain (Crawley, 1987). It duces the risk posed by introduced biological control matures quickly, is capable of flowering in its first year agents. However, is far from an exact sci- of life and produces an extraordinary number of small ence, and the taxonomy of the paraphyletic Buddleja that are efficiently dispersed by wind. However, has had a chequered history. Buddleja has variously been placed within the families, Scrophulariaceae, Lo- ganiaceae, the conveniently promoted Buddlejaceae 1 Ensis, Private Bag 3020, Rotorua, New Zealand. and, most recently, returned to the Scrophulariaceae, 2 Hill & Associates, Christchurch, New Zealand. which has been a recognized repository for undefined 3 NAU, Plant Protection, Nanjing, . Corresponding author: M.K. Kay . (Tank et al., 2006). The on-going reconstruct- © CAB International 2008 ing of the Scrophulariaceae combines morphological,

287 XII International Symposium on Biological Control of embryological, molecular and chemical parameters, as Results well as the host preferences of specialist invertebrates (Stevens, 2001). A full account of trial results is available on the Envi- Fortunately, there are few close relatives of buddleia ronmental Risk Management Authority website (www. within the New Zealand indigenous Scrophulariaceae ermanz.org). Adult C. japonicus did not oviposit, or s.s., although the indigenous shrub, laetum feed, on any of the 35 species belonging to 24 plant G. Forst., , has now been relegated to the families outside of the Scrophulariaceae in either of tribe Myoporeae, within the same clade as Buddlejeae the preliminary trials in China or the trials conducted (Tank et al., 2006). Most other New Zealand genera in New Zealand. However, the weevil did lay a very previously placed in the Scrophulariaceae, including small number of eggs on a few of the 21 New Zea- the manifold Comm. ex Juss., are now better de- land indigenous species within the family Scrophula- fined in other clades within the Scrophulariaceae sensu riaceae s.l. These eggs were laid externally, rather than lato. in purposefully excavated sites, and failed to produce During a survey of and pathogens associated larvae. Larvae transferred to these plants also devel- with B. davidii in China, Cleopus japonicus Wingel- oped poorly. Within the Buddleja, C. japonicus müller (Coleoptera, Curculionidae) appeared to be a could complete development on all, except Buddleja potential biological control agent because of its appar- salviifolia (L.) Lam and Benth. but ent host specificity and ubiquity. The adults and larvae performed best and had a significant preference for B. feed externally on . Eggs are oviposited singly davidii (Table 1). within excavated leaf cavities, and the emergent slug- Newly emerged larvae transferred to the foliage of like larvae remain attached to the plant by secreting a 17 New Zealand indigenous Hebe species died quickly coating of viscous fluid. without completing development. One anomaly oc- The host-specificity studies reported in this paper curred when one larva of one replicate completed evaluated whether C. japonicus is a safe biological development to adult on the foliage of an ornamental control agent for buddleia in New Zealand. specimen of (A.Cunn.) Ckn. & Allan. One larva also completed development on each of the indigenous lineata Glück, [Limosellae Methods and materials Preliminary trials conducted in China tested species from 16 plant families. C. japonicus was then im- Table 1. Summary of feeding and oviposition trials ported into quarantine in New Zealand. The 76 plant for Cleopus japonicus presented as a ranking taxa tested in New Zealand were selected following the of host suitability within the genus Buddleja. internationally accepted ‘centrifugal phylogenetic sys- Ranking was determined from the combined tem’ of Wapshere (1974). The relative susceptibility of rankings of larval and adult feeding and ovipo- 14 Buddleja taxa was tested. Thirty-five New Zealand sition for each species. indigenous plant species were tested, including Genios- Buddleja species Section Origin Rank toma rupestre J.R. Forst.& G. Forst., the only endemic B. davidii Franch. Neemda SE Asia 1 representative of the , and 21 species from var. lochinch – – 2 the Scrophulariaceae s.l. Given the uncertain nature of var. weyeriana – – 3 Buddleja taxonomy, it was considered prudent to give B. madagascariensis Nicodemia Madagascar 3 extensive coverage of New Zealand spe- Lam. cies, particularly the many species of Hebe. A further B. japonica Hemsl. Neemda SE Asia 5 11 species of Scrophulariaceae s.l. that are exotic to B. alterniflora Neemda SE Asia 6 New Zealand were tested, along with 16 exotic species Maxim. from other families that commonly grow in association B. globosa Hope Neemda S America 7 with buddleia in New Zealand. The New Zealand trials B. lindleyana Neemda SE Asia 8 Fortune were conducted in a quarantine insectary maintained at B. parviflora Neemda N America 9 20°C ± 2 and 70% ±10 RH, 14-h photoperiod. H. B. K. Tests were run with naïve and pre-fed adults, in B. asiatica Lour. Neemda SE Asia 10 both choice and no-choice trials. The degree of feed- B. colvillei Neemda India 10 ing, oviposition and mortality was scored against that Hook. f. et Thoms of insects placed on concurrent buddleia controls. No- B. dysophylla Chilianthus S Africa 12 choice larval trials utilized both pre-fed and naïve first (Benth.) Radlk. instar larvae. To obtain naïve larvae, eggs of known age B. auriculata Neemda S Africa 13 were monitored closely for larval eclosion. Emerging Benth. larvae were transferred to the test plant material before B. salviifolia Neemda S Africa 14 feeding. (L.) Lam.

288 The disintegration of the Scrophulariaceae and the biological control of Buddleja davidii

(Scroph I.)] and elatinoides Benth. ex (2001)] within the Scrophulariaceae s.l. Allen (1960) Hook. f. [ (Scroph IV)], but adult noted that weevils of the Gymnetrini distinguished be- did not oviposit on these species. tween the (Scroph II) and the Scroph I Most exotic scrophularia appeared to be immune to clade and that they fed indifferently upon Scrophularia attack by the weevils, but larval and adult feeding and and . oviposition occurred on the weedy European species Westwood (1849 in Scott 1937) remarked that Cio- L., Stokes and nus scrophulariae L.; L. “¼long ago discovered the Natural System, and proved by the fact of their sometimes indiscriminately feeding on mulleins [Verbascum] and figworts [Scroph- Discussion ularia] that these plants were in truth closely allied in Nature.” Cleopus Dejean, belonging to a tribe (Cionini) of host- Scott (1937) records the same weevil feeding on specific ‘figwort’ weevils and the European represen- the introduced Cape figwortPhygelius capensis Benth. tatives (Cionus Clairville and Cleopus species), feed (Scroph I) and notes the observations, by others, of Ci- on Scrophularia, Verbascum and occasionally on ad- onus and Cleopus occasionally feeding on introduced ventive Buddleja (Walker, 1914, Hoffman, 1958; Cun- Buddleja in the UK. In the UK, the only specialist ningham, 1974, 1975; Williams, 1974; Read, 1976, Lepidopteran to occasionally feed on buddleia is the 1978; Bullock, 1987; Smith, 1992). Conversely, the mullein , Cucullia verbasci L., which normally Asian species, C. japonicus, has only been recorded has the same host range as the figwort weevils (Owen from B. davidii (Zhang et al., 1993), and this study and Whiteway, 1980). The flea , Longitarsus found that it could only complete its life cycle on a few spp. Latreille, also only have the hosts Scrophularia Buddleja taxa, but could feed on Scrophularia and Ver- and Verbascum, and in summary of these observations, bascum. The host associations of these species appear Allen (1960) stated: “Yet none of these insects, appar- to support the recent revision of the Scrophulariaceae ently, is known ever to attack Lanaria or (Fig. 1). [both of , Scroph II ] in a state of nature, Other invertebrates are also known to feed exclu- and I am aware of no instance of a feeder (of sively on these plant species, which have been recog- which there are many) having Scrophularia as a host.” nized as a distinct clade, Scrophulariaceae s.s. [‘Scroph Elements of the distinctive iridoid and terpenoid I’ of Olmstead and Reeves (1995) and Olmstead et al., phytochemistry of Buddleja have been shown to be

Buddlejeae (Af., Asia, N.Am. Buddleja***)

Teedieae (S.Af.)

(*)

Scrophularieae (NH, Scrophularia** & Verbascum**)

Limoselleae (S.Af.)

Leucophylleae (C.Am.)

Myoporeae (Aust.)

Aptosimeae (Af.)

Hemimerideae (S.Af.)

Figure 1. Summary of the phylogenetic relationships among the tribes and the unresolved genus, Phygelius, of the Scrophulariaceae sensu stricto (after Tank et al., 2006). Low (single asterisk) to high level (triple asterisk) of feeding by Cleopus japonicus.

289 XII International Symposium on Biological Control of Weeds biologically active (Yoshida et al., 1976; Houghton Bowers, M.D. (1988) Chemistry and coevolution: iridoid et al., 2003) and may well influence the invertebrate , plants and herbivorous insects. In: Spencer, feeding guild associated with this and closely related K.D. (ed.) Chemical Mediation of Coevolution. Academic genera. Iridoids are known to be feeding stimulants for Press, New York, pp. 133–165. specialist (Bowers, 1988) and deterrents Bullock, J.A. (1987) (L.), (Col., Cur- culionidae) feeding on Hope. Entomol- for generalists (Stephenson, 1982). ogist’s Monthly Magazine 123, 190. The study reported in this paper not only confirms Crawley, M.J. (1987) What makes a community invasible? the restricted host preference of the Cionini and demon- In: Gray, A.J., Crawley M.J. and Edwards, P.J. (eds) Colo- strates the low risk of C. japonicus to the New Zealand nisation, Succession and Stability. Blackwell Scientific, flora but also supports the current position of Buddleja London, UK, p. 429. within the new taxonomy. Bearing in mind that labora- Cunningham, P. (1974) Studies on the occurrence and dis- tory studies are thought to overestimate the host range of tribution of the genera Cionus and Cleopus (Col.: Cur- potential biological control agents (Hill, 1999), the host culionidae) in South Hampshire, 1973. Entomologist’s range of C. japonicus in the field may be more limited. Record 86, 184–188. However, these results cannot preclude the possibil- Cunningham, P. (1975) A convenience food for weevils of ity that, if released, C. japonicus could produce self- the genera Cionus and Cleopus (Col., Curculionidae). Entomologist’s Monthly Magazine 112, 1340–1343. sustaining populations on Verbascum, Scrophularia and Esler, A.E. (1988) The naturalisation of plants in urban Auck- Buddleja species. Four other species of Buddleja [B. land, New Zealand. Success of the alien species. New salviifolia L., Buddleja madagascariensis Lam., Bud- Zealand Journal of 26, 565–584. dleja globosa Hope and B. dysophylla (Benth.) Radlk.] Hill, R.L. (1999) Minimising uncertainty – in support of have already partially naturalized in New Zealand. The no-choice tests. In: Withers, T.M., Barton-Browne, L., early flowering B. salviifolia is valued as a spring nec- Stanley, J. (eds) Host-Specificity Testing in Australasia: tar source for (Kay and Smale, 1990). However, Towards Improved Assays for Biological Control. Scien- C. japonicus adults fed poorly, larvae failed to feed and tific Publishing, Indooroopilly, p. 1. no eggs were laid on B. salviifolia. It is unlikely that Hoffman, A. (1958) Faune de , vol. 62. Coléoptères this species would be colonized by C. japonicus. In Curculionides (Troisième Partie). Fédération Française contrast, B. madagascariensis is one of a number of des Sociétés de Sciences Naturelles, Éditions Paul Lech- evalier, Paris, pp. 1211–1233. Buddleja species to be considered strongly invasive on Holm, L., Pancho, J.V., Hergerger, J.P. and Plucknett, D.L. the west coast of USA and (Randall and Mari- (1979) A Geographical Atlas of World Weeds. Wiley, New nelli, 1996). It ranked highly as a host of C. japonicus. York, 391 pp. B. globosa is not considered to be invasive, and any at- Houghton, P.J., Mensah, A.Y., Iessa, N., and Hong, L.Y. tack by C. japonicus may limit the potential ornamen- (2003) Terpenoids in Buddleja: Relevance to chemosys- tal value of this species. B. dysophylla appeared to be a tematics, chemical ecology and biological activity. Phyto- poor host for C. japonicus, but it is rarely cultivated in chemistry 64, 385–393. New Zealand and is not considered invasive. Kay, M.K. and Smale, M.C. (1990) The potential for biologi- C. japonicus appears to have a restricted host range cal control of Buddleia davidii Franchet in New Zealand. and could be expected to be at least as host-specific as In: Bassett, C., Whitehouse, L.J. and Zabkiewicz, J.A. its European congeners. We conclude that it is possible (eds) Alternatives to the Chemical Control of Weeds. Min- istry of Forestry, FRI Bulletin 155, pp 29–33. that C. japonicus may cause minor damage to some Leeuwenberg, A.J.M. (1979) The Loganiaceae of Africa non-target scrophulareous species, particularly within XVIII Buddleja L.II: Revision of the African and Asiatic Buddleja, Verbascum and Scrophularia. These are all species. Mededelingen.Landbouwhogeschool Wagenin- weedy species or ornamentals of minor importance in gen 6, 1–163. New Zealand, but in Europe, the tribe Scrophularieae Olmstead, G.R. and Reeves, P.A. 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