Plant Protection Quarterly Vol.16(2) 2001 63 problems due to also occur in several parts of Asia, Africa and the Car- Gall-inducing and biological control of ibbean (Navie et al. 1996, Mahadevappa L. () 1997). Parthenium hysterophorus is a vigorous

A,B A B and fast-growing annual plant that pro- S.K. Florentine , A. Raman and K. Dhileepan duces nearly 60 000 florets, each bearing A The University of Sydney – Orange, PO Box 883, Orange, New South Wales one seed (K. Dhileepan, unpublished ob- 2800, Australia. servations). The seeds persist in the soil B Tropical Weeds Research Centre, Department of Natural Resources, PO Box for a long time, with nearly 50% of the 187, Charters Towers, Queensland 4820, Australia. seed bank remaining viable up to six years (Navie et al. 1998). Different chemical, biological and cul- tural methods have been adopted to man- Summary Introduction age this weed in Australia and in other Weeds invade agricultural ecosystems Parthenium hysterophorus L. (parthenium parts of the world. Use of herbicides has and degrade productive land. Parthen- weed, white top, false ragweed) was acci- proved uneconomic (Holman and Dale ium hysterophorus, introduced acciden- dentally introduced into Australia from 1981). Biological control offers great po- tally into Australia from the United the United States of America. It was first tential to minimize and manage P. hystero- States of America, not only affects pro- recorded in Queensland in the 1950s phorus, especially in the heavily-infested ductive land, but also causes severe (Everist 1976). At present it is reported areas of Central Queensland (McFadyen health problems to humans. Since gall- throughout much of Queensland and oc- 1992). inducing are increasingly be- curs in small pockets along roadsides in As an effort towards biological control, coming useful in weed management northern New South Wales (McFadyen nine species and one pathogenic campaigns, we discuss in this paper the 1995) and in the Northern Territory rust fungus from Central America were benefits of using gall-inducing insects in (Navie et al. 1996). In the last two decades, released in Queensland between 1980 and the biological control of weeds, targeting this species has caused severe economic 1999 (Table 1). Among these, a gall-induc- P. hysterophorus which is a major prob- and ecological impacts in Queensland. It ing , strenuana Walker lem weed in Queensland. We evaluate has spread to nearly 170 000 km2 in (: ) and a gall- the capability of two gall-inducing in- Queensland with an estimated loss of inducing weevil, Conotrachelus albocinereus sects against P. hysterophorus. The gall- farm productivity up to 40% (Chippen- Fiedler (Coleoptera: Curculionidae) ap- inducing moth, Epiblema strenuana and dale and Panetta 1994). It is a serious pear to have the potential for control- the gall-inducing weevil, Conotrachelus health hazard and induces allergic derma- ling P. hysterophorus (McFadyen 1992, albocinereus display significant morpho- titis, hay fever and asthma in more Dhileepan et al. 1996, Raman and logical and physiological impacts on P. than 20% of the exposed population Dhileepan 1999, Treviño et al. 1999, hysterophorus indicating them to be ef- (McFadyen 1995, Cheney 1998). Manage- McFadyen 2000). This paper discusses the fective organisms for use in biological ment of this species is expensive (Chip- strengths and advantages of using the gall control in Australia. pendale and Panetta 1994) and control moth and the gall weevil for the manage- programs from 1977 to 1992 have cost ment of P. hysterophorus, as well as sum- nearly $3.5 m in Australia (McFadyen marizes the benefits in using galling ar- 1992). Severe economic and health thropods in weed management and the

Table 1. Biological control agents released in P. hysterophorus-infested areas in Australia. Biological Country Year of Year of Biology Impact References control agents of origin release establishment on host Bucculatrix parthenica Mexico 1984–85 na Leaf mining + McClay et al. (Lepidoptera: ) (1990) Conotrachelus albocinereus Argentina 1995–97 2000 Stem galling na McFadyen (Coleoptera: Curculionidae) (2000) ithacae Mexico 1998–99 2000 Root boring na Dhileepan (Lepidoptera: ) (pers. obs.) Epiblema strenuana Mexico 1982–85 1983 Stem galling +++ McFadyen (Lepidoptera: Tortricidae) (1989) Listronotus setosipennis Brazil and 1982–86 1983 Stem boring ++ Wild et al. (Coleoptera: Curculionidae) Argentina (1992) Platphalonida mystica Argentina 1992–96 na na na Dhileepan and (Lepidoptera: Tortricidae) McFadyen (1997) Smicronyx lutulentus Mexico 1981–83 1996 Seed feeding + McFadyen and (Coleoptera: Curculionidae) McClay (1981) Stobaera concinna Mexico 1983–85 1992 Sap sucking Nil Dhileepan and (Hemiptera: Delphacidae) McFadyen (1997) Zygogramma bicolorata Mexico 1981–83 1990 Leaf feeding +++ Dhileepan and (Coleoptera: Chrysomelidae) McFadyen (1997) Puccinia abrupta var. parthenicola Mexico 1992 1994 Pustule forming na Dhileepan and (Fungi: Uredinales) on leaves McFadyen (1997) + = low. ++ = moderate. +++ = high. na = data unavailable. 64 Plant Protection Quarterly Vol.16(2) 2001 nature of physical and physiological (1996) indicate the vulnerability of the damage caused by these arthropods. host plant to moisture stress and the gall acting as a metabolic sink as the key Why gall-inducing insects hold strengths in using gall insects in weed promise in weed control? management. Use of plant-feeding arthropods and pathogenic fungi is preferred in weed Mechanism of damage by gall- management programs, because such a inducing insects practice is ecologically sound and eco- Gall-inducing insects play a major role in nomically viable (Shepherd 1993). Gall- redirecting photo-assimilates from the ac- inducing insects have played a key role in tive meristems of the host to the gall site biological weed control activities through- (Abrahamson and Weis 1987). An active out the world (Julien and Griffiths 1998). gall performs as a metabolic sink trapping Among plant-feeding insects, only those the nutrients and transporting them to tis- belonging to 20 Families classified under sues lying close to larva, through localized seven Orders have the ability to induce cellular modifications (Raman 1987, galls on their host plants. Within the Rohfritsch 1988). Galls act as sinks of en- broad context of insects used in weed bio- ergy as well, to subserve the nutritional logical control, only 2% of them are gall needs of the parasitic galler (Stinner and inducers (Meyer 1987). Gall-inducing in- Abrahamson 1979, Raman and Abraham- sects have a narrow host range and they son 1995). High levels of soluble nutrients severely impair the growth and develop- such as the sugars and amino acids exist ment of the host plant (Harris and in the feeding layers of tissues in galls (Ra- Shorthouse 1996). They induce structural man 1994). In the galls induced by (Lalonde and Shorthouse 1984, Raman Phanacis taraxaci on the common dande- and Dhileepan 1999) and metabolic lion (Taraxacum officinale), up to 70% of changes (Daley and McNeil 1987, carbon was redirected to the gall, to pro- Paquette et al. 1992, Raman 1994) in the vide nutrition to the growing larva Figure 1. Epiblema strenuana- host plant. Their ability to significantly af- (Bagatto et al. 1996). In addition to photo- induced gall on P. hysterophorus, fect host-plant growth and metabolism, assimilates, galls accumulate mineral nu- cut open longitudinally to show the and their narrow host range indicate that trients in their specialized nutritive tissue mature larva (scale bar: 1 mm). they could be an ideal group for the (Abrahamson and McCrea 1985, Short- biological control of weeds. The gall house and Gassmann 1994). During early weevil, Rhinocyllus conicus (Coleoptera: stages of development of galls induced by through a window cut by the mature larva Curculionidae) on the thistles (Carduus Hemadas nubilipennis on Vaccinium angusti- before pupation (McFadyen 1986, Raman nutans and C. acanthoides) (Shorthouse and folium, minerals such as copper, nickel, and Dhileepan 1999). Lalonde 1984); the seed-, Urophora iron and zinc remained higher in the The weevil, C. albocinereus is active at cardui (Diptera: Tephritidae) on Cirsium galled tissue than in the ungalled tissue night and feeds on the stems and leaves of arvense; the fly, Pegomya cutricornis (Bagatto and Shorthouse 1994, Shorthouse P. hysterophorus. Adults live for up to three (Diptera: Anthomyiidae) on Euphorbia et al. 1986). Early developmental pressure months. The female weevil chews the epi- virgata and E. esula (Shorthouse and of galls acting as the nutrient sinks for the dermal and outer cortical tissue of the Gassmann 1994); the stem-gall fly, inhabiting insect increases energy alloca- shoot. She lays eggs singly in the feeding Procecidochares utilis (Tephritidae: Diptera) tion from the storage reserves of the plant scar sites and sometimes on leaf axils and on Eupatorium adenophorum (Swaminthan organ; in some instances, the development covers them with frass. A neonate larva and Raman 1981) are some of the well of the insect progeny depends on the re- bores directly into the stem (Figure 2). The documented examples of gall inducers sources mobilized at the galled organ (e.g. larvae remain inside the gall until mature, used in weed management practice. leaf) and from the immediate neighbour- and then move to the soil for pupation Larvae of gall-inducing arthropods hood. Such an activity of drawing re- (McFadyen 2000). feed actively on flower heads (Lalonde sources from the neighbourhood repre- and Shorthouse 1984), stems (Gassmann sents active manipulation of the normal Impact of E. strenuana and C. and Shorthouse 1990, Raman and host-transport mechanisms by the gall in- albocinereus on P. hysterophorus Dhileepan 1999), leaves (West and Short- ducer (Larson and Whitham 1991). Trial infestations of E. strenuana on about house 1981) and roots (Shorthouse and 50 plant species belonging to 28 families Gassmann 1994). This process creates a Epiblema strenuana/C. albocinereus indicate that this moth caused a powerful nutrient sink (Jankiewicz et al. 1970) in the and P. hysterophorus interactions impact on P. hysterophorus in particular galled region and thus weakens the host- Natural history of E. strenuana and C. (Jayanth 1987). E. strenuana only attacks plant metabolism. Gall-inducing arthro- albocinereus related species such as the annual rag- pods exist in adverse environmental con- Epiblema strenuana lays eggs on young weed (Ambrosia artemisifolia), perennial ditions such as deserts and saline leaves of P. hysterophorus. Emerging larvae ragweed (A. psilostachya) and noogoora marshes, since they are better adapted and mine the leaf briefly, then move to the burr ( pungens) (McClay 1987). acclimatized to those conditions than are closest vegetative axillary meristems. E. strenuana attacks different developmen- their free-living relatives (Fernandes and They enter the stem and their feeding ac- tal stages of P. hysterophorus (rosette, pre- Price 1991, Tscharntke 1988). The gall be- tion induces a gall. After considerable flowering and flowering stages) and in- ing a ‘concealed’ habitat, made of several movement down the stem, the larvae turn duces galls of different morphologies; layers of host-plant tissue, protects the in- by 180° and commence feeding in an up- younger shoots respond with vigorous, ducers from extreme environmental situa- ward direction (Figure 1). When larvae spherical galls and older shoots with tions (Martel 1995). Summarizing the im- stop feeding, cells in that area degenerate weaker, fusiform galls (Raman and pact of gall inducers on the management and die. Pupal stage ranges between four Dhileepan 1999). Field investigations on of noxious plants, Harris and Shorthouse and six days, and adult emerge the impact of E. strenuana on parthenium, Plant Protection Quarterly Vol.16(2) 2001 65 demonstrate that rates of infes- tation range between 7 and 55, 43 and 90, 85 and 95% on the ro- sette, pre-flowering, and flow- ering stages, respectively. The average number of galls per plant increased with age. Fur- ther, E. strenuana, reduced the number of plants attaining the flowering stage by 45% and re- duced flower production by 38% (Dhileepan and McFadyen 1997). Presence of E. strenuana larvae on P. hysterophorus re- duced plant height, mature capitula, and viable seeds by 34, 74, and 74%, respectively (Navie et al. 1998). Host specificity studies on C. albocinereus prior to their re- lease in Australia gave the fol- lowing results. Of 36 genera of Asteraceae tested, C. albo- cinereus fed only on P. hystero- phorus and its close relative, (McFad- yen 1993). Under controlled, glasshouse conditions, the re- lease of 10 C. albocinereus larvae per plant reduced the plant height by 34%, root biomass by 41%, number of mature ca- pitula by 21%, and viable seed set by 18%. There was also a strong impact on the pre-flow- ering stage of P. hysterophorus Figure 2. Conotrachelus albocinereus- Figure 3. Mature gall induced by Epiblema by reducing the formation of induced gall on P. hysterophorus cut strenuana (cross sectional view), showing the mature capitula and viable open longitudinally to show a young feeding damage by larva (*) disrupting the seeds by 46 and 47%, respec- larva (scale bar: 1 mm). vascular cylinder and the cortical parenchyma tively (David 1998). (arrows: nutritive cells, scale bar: 100 µm). Both E. strenuana and C. albocinereus induce single- chambered galls 1–2 cm long and 1 cm wide. Galls are initi- ated by larval feeding on the central cortical callus paren- chyma and such a stimulus in- duces the stem to enlarge and grow into galls (Figure 3). Larval feeding activity of E. strenuana impacts on P. hystero- phorus by rendering the phloem and associated vascular paren- chyma inactive. Intense feeding fractures the vascular traces and consequently plant parts above the gall suffered vigour loss due to disruption of fluid movement. Organic nutrients (e.g. starches and lipids) syn- thesized by the host plant are mobilized rapidly at the gall sites (Figure 4) to provide nutri- tion for the developing larvae. The active metabolic response of the host plant by synthesiz- ing and accumulating second- Figure 4. Mature gall induced by Epiblema strenuana (cross sectional view). ary metabolites in the galled re- Parenchymatous nutritive tissue (arrows: lipid droplets, differential staining with oil gion and the physical action of o’red, Jensen 1964) (scale bar: 100 µm). 66 Plant Protection Quarterly Vol.16(2) 2001 vegetative axillary buds which grow into new branches; such a process creates higher numbers of sites for infestation by gall-moth populations. The result is greater opportunity for the gall-moth populations to attack and damage an indi- vidual plant. Loss of contour of the stomatal aperture probably results in higher rates of transpi- ration in the galled regions, and this in turn increases importation of nitrogenous material through xylem and associated parenchyma (Zwölfer and Arnold- Reichart 1993), and eventually intensify- ing stress in the host tissue. Such a devel- opment becomes critical in the shoot galls of parthenium because it affects portions of shoot beyond the gall. E. strenuana and C. ablocinereus place frass between the frac- tured vascular traces and that prevents the vascular tissues from establishing repara- tory bridges. This process affects the host plant’s recovery processes. Assessments of biological control agents released on P. hysterophorus indicate that E. strenuana has proliferated both extensively and vigor- ously causing severe impact on the rosette stages of P. hysterophorus in particular (McFadyen 1992). Figure 5. Mature gall induced by C. albocinereus (cross sectional view). Galls protect the larvae of E. strenuana Parenchymatous nutritive tissue around the vascular trace (arrows: starch, and C. albocinereus from extremes of dry differential staining with I-KI, Jensen 1964) (scale bar: 100 µm). and wet environmental conditions that prevail in Queensland (McFadyen 1992, Dhileepan et al. 1996). This insect–plant the larva by placing the frass at the frac- galls in the roots of C. nutans (Harris and relationship helps the concealed biological tured vascular strands stall the develop- Shorthouse 1996). However, S. jugoslavica, control agents, such as the gall inducers to ment of reparatory vascular bridges. In E. strenuana and C. albocinereus share a few proliferate, and provides an advantage young galls, polysaccharides were mobi- common behavioural traits: all feed and over the biological control agents that feed lized through interfascicular parenchyma stimulate development of callus paren- externally. to cells in close proximity to the larvae chyma, rupture vascular connections and (Raman and Dhileepan 1999). As in the deposit frass between the disconnected Acknowledgments galls induced by E. strenuana, the young vascular strands in mature galls. Rachel E. McFadyen (Department of galls of C. albocinereus also accumulate As gall-inducers, E. strenuana and C. Natural Resources, Brisbane, Queens- starches and lipids in cells close to the lar- albocinereus manipulate the normal meta- land), William T. Parsons (Mt. Eliza, Vic- val head (Figure 5). With the growth of the bolic pathways of P. hysterophorus, to toria), Joe Scanlan (Department of Natural gall, supplementary nutrients (e.g. miner- maintain a continuous supply of nutrients Resources, Toowoomba, Queensland), als), which would otherwise be available for their development and survival. Con- and two anonymous referees reviewed for the plant’s growth and reproduction, sequently, they place their host plant un- this paper and offered constructive com- are transported to the growing gall. Such der an intense metabolic stress, particu- ments. Marjorie Wilson (The University of a draining effect places P. hysterophorus larly when attacked by large insect popu- Sydney, Orange) offered editorial advice. under a severe physiological stress (Ra- lations. Although both infest P. hystero- We thank all of them. This work was com- man and Dhileepan 1999). In mature galls, phorus under similar temporal and spatial pleted under the Resource Management— the stem epidermal cells show active pro- regimes, the gall-inducing behaviour of R&D Grants (#NRM/185/001:1221:BV:IT) liferation, especially around the stomata, the two differs, especially at the time of from the Department of Natural Re- pushing them outwards. The stomata at gall initiation. The moth larva preferen- sources (Government of Queensland). the summits of the elevated regions re- tially travels over a distance from tender, main permanently closed. expanded foliage to the vegetative axillary References bud. The weevil larva does not move at all; Abrahamson, W.G. and Weis, A.E. (1987). Discussion from the site of oviposition, soon after Nutritional ecology of gall Models evaluating the biological control emergence, it bores through the stem tis- makers. In ‘The nutritional ecology of efficiency of a few tephritids and sues and places itself deeper in the cortical insects, mites and spiders’, eds F. Coleoptera that induce galls on some region. The first larval instar of the gall Slansky and J.G. Rodriguez, p. 235. weedy Asteraceae are available (Harris moth destroys the vegetative axillary (Wiley, ). and Shorthouse 1996). The Sphenoptera meristem by its feeding action and thereby Abrahamson, W.G. and McCrea, K.D. jugoslavica (Coleoptera: Buprestidae)– removes the potential site for further in- (1985). Seasonal nutrient dynamics of Carduus nutans system is similar to the P. festation by other gall moth larvae. Al- Solidago altissima (Compositae). Bulletin hysterophorus–E. strenuana–C. albocinereus though this reduces competition within of Torrey Botanical Club 112, 414-20. system, although S. jugoslavica attacks the populations of E. strenuana, P. hystero- Bagatto, G. and Shorthouse, J.D. (1994). shoot–root transition zone and induces phorus responds by producing new Seasonal acquisition of mineral Plant Protection Quarterly Vol.16(2) 2001 67 nutrients by a chalcid gall on lowbush Harris, P. and Shorthouse, J.D. (1996). Ef- strenuana in Eastern Australia. Proceed- blueberry. Entomologia Experimentalis et fectiveness of gall inducers in weed bio- ings of the 10th National Noxious Applicata 73, 61-6. logical control. The Canadian Entomolo- Plants and Conference, ed. D. Bagatto, G., Paquette, L.C. and Short- gist 128, 1021-55. Brown, p. 227-358. (NSW Agriculture house, J.D. (1996). Influence of galls of Holman, D.J. and Dale, I.J. (1981). and Fisheries, Sydney, NSW). Phanacis taraxaci (cynipid wasp) on car- Parthenium weed threatens Bowen McFadyen, R.E. (1989). Ragweed, bon partitioning within common dan- Shire. Queensland Agricultural Journal parthenium and noogoora burr control delion, Taraxacum officinale. Entomologia 107, 57-60. in the post-Epiblema era. Proceedings of Experimentalis et Applicata 79, 111-7. Jankiewicz, L.S., Flich, H. and Anlow- the 5th Biennial Noxious Plants Confer- Cheney, M. (1998). Determination of the szewski, H.A. 1970. Preliminary study ence, ed. P. Gorham p. 5-8. (Weeds Sci- prevalence of sensitivity to parthenium on translocation of 14C-labelled assimi- ence Society of Victoria, Melbourne, 32 in areas of Queensland affected by the lates and PO4 towards the gall evoked Australia). weed. Master of Public Health Thesis, by Cynips (Diplolepis) quercusfolii on oak McFadyen, R.E. (1992). Biological control Queensland University of Technology, leaves. Marcellia 36, 163-72. against parthenium weed in Australia. Brisbane, Queensland, p. 118. Jayanth, K.P. (1987). Investigations on the Crop Protection 11, 400-7. Chippendale, J.F. and Panetta, F.D. (1994). host-specificity of E. strenuana (Walker) McFadyen, R. E. (1993). Report on the bi- The cost of parthenium weed to the (Lepidoptera : Tortricidae), introduced ology and host specificity of the stem- Queensland cattle industry. Plant Pro- for biological control trials against galling weevil Conotrachelus sp. (Col.: tection Quarterly 9, 73-6. Parthenium hysterophorus in India. Jour- Curculionidae). A potential biocontrol Daley, P.F. and McNeil, J.N. (1987). nal of Biological Control 1, 133-7. agent against parthenium weed. Re- Canopy photosynthesis and dry matter Jensen, W.A. (1962). ‘Botanical histochem- port of the Department of Natural Re- partitioning of alfalfa infested by the al- istry’, p. 408 (W.H. Freeman, New sources, Alan Fletcher Research Sta- falfa blotch leafminer (Agromyza York). tion, Brisbane, Queensland, p. 1-9. frontella (Rondani)). Canadian Journal of Julien, M.H. and Griffiths, M.W. (1998). McFadyen, R.E. (1995). Parthenium weed Plant Science 67, 433-43. ‘Biological control of weeds. A world and human health in Queensland. Aus- David, J.-M. (1998). Efficacy of the catalogue of agents and their target tralian Family Physician 24, 1455-9. stem galling weevil Conotrachelus weeds’, 4th edition, p. 223. (CABI Pub- McFadyen, R.E. (2000). Biology and host albocinereus as a biological control agent lishing, Oxford). specificity of the stem-galling weevil for parthenium weed (Parthenium Lalonde, R.G. and Shorthouse, J.D. (1984). Conotrachelus albocinereus Fiedler (Col.: hyetrophorus L.). Report of the Depart- Developmental morphology of the gall Curculionidae), a biocontrol agent for ment of Natural Resources, Alan of Urophora cardui (Diptera: parthenium weed Parthenium hystero- Fletcher Research Station, Brisbane, Tephritidae) in the stems of Canada phorus L. (Asteraceae) in Queensland. Queensland. thistle (Cirsium arvense). Canadian Jour- Biocontrol Science and Technology 10, Dhileepan, K. and McFadyen, R. (1997). nal of Botany 62, 1372-84. 195-200. Biological control of parthenium in Larson, K.C. and Whitham, T.G. (1991). Meyer, J. (1987). ‘Plant galls and gall in- Australia: progress and prospects. Pro- Manipulation of food resources by a ducers’, p. 291 (Gebrüder Bornträger: ceedings of the 1st International Con- gall-forming aphid: the physiology of Berlin/Stuttgart) ference on Parthenium Management, sink-source interactions. Oecologia 88, Navie, S.C., McFadyen, R.E., Panetta, F.D. eds M. Mahadevappa and V.C. Patil, p. 15-21. and Adkins, S.W. (1996). The biology of 40-4 (The University of Agricultural Mahadevappa, M (1997). Ecology, distri- Australian weed 27. Parthenium Sciences, Dharwad, India). bution, menace and management of hysterophorus. Plant Protection Quarterly Dhileepan, K., Madigan, B., Vitelli, M., parthenium. Proceedings of the 1st In- 11, 76-88. McFadyen, R., Webster, K. and ternational Conference on Parthenium Navie, S.C., Panetta, F.D., McFadyen, R.E. Treviño, M. (1996). A new initiative in Management, eds M. Mahadevappa and Adkins, S.W. (1998). Behavior of the biological control of parthenium. In and V.C. Patil, p. 1-12 (The University buried and surface-sown seeds of ‘The Proceedings of the 11th Australian of Agricultural Sciences, Dharwad, In- Parthenium hysterophorus. Weed Research Weeds Conference’, ed. R.C.H. Shep- dia). 38, 335-41. herd, p. 309-12. (Weeds Science Society Martel, J. (1995). Performance of Eurosta Paquette, L.C., Bagatto, G. and of Victoria, Australia). solidaginis (Diptera: Tephritidae) and Shorthouse, J.D. (1992). Distribution of Everist, S.L. (1976). Parthenium weed. Epiblema scudderiana (Lepidoptera: nutrients with the leaves of common Queensland Agricultural Journal 102, 2. Tortricidae), two gall-formers of dandelion (Taraxacum officinale) galled Fernandes, G.W. and Price, P.W. (1991). goldenrod, in roadside environments. by Phanacis taraxaci (Hymenoptera: Comparison of tropical and temperate Environmental Entomology 24, 697-706. Cynipidae). Canadian Journal of Botany galling species richness: the roles of en- McClay, A.S. (1987). Observations on the 71, 1026-31. vironmental harshness and plant nutri- biology and host specificity of Epiblema Raman, A. (1987). On the transfer cell-like ent status. In ‘Plant– interac- strenuana (Lepidoptera: Tortricidae), a nutritive cells of the galls induced by tions: evolutionary ecology in tropical potential biocontrol agent for thrips. Current Science, 56, 737-8. and temperate regions’, ed. P.W. Price, Parthenium hysterophorus (Compositae). Raman, A. (1994). Adapational integration T.M. Lewinsohn, G.W. Fernandes and Entomophaga 32, 23-34. between gall-inducing insects and their W.W. Benson, p. 91-115. (John Wiley, McClay, A.S., McFadyen, R.E. and host plants. In ‘Functional dynamics of New York). Bradley, J.D. (1990). Biology of phytophagous insects’, ed. T. N. Gassmann, A. and Shorthouse, J.D. (1990). Bucculatrix parthenica Bradley sp. (Lepi- Ananthakrishnan, p. 249–77. (Oxford Structural damage and gall induction doptera: Bucclatricidae) and establish- and IBH Publishing Co., New Delhi, by Pegomya curticornis and Pegomya ment in Australia as a biological control India). euphorbiae (Diptera: Anthomyiidae) agent for Parthenium hysterophorus Raman, A. and Abrahamson, W.G. (1995). within the stems of leafy spurge (Asteraceae). Bulletin of Entomological Morphometric relationships and en- (Euphorbia × pesudovirgata) (Euphorb- Research 80, 427-32. ergy allocation in the apical rosette iaceae). The Canadian Entomologist 122, McFadyen, R.E. (1986). The effect of cli- galls of Solidago altissima (Asteraceae) 429-39. mate on the stem-galling moth Epiblema induced by Rhopalmyia solidaginis 68 Plant Protection Quarterly Vol.16(2) 2001 (Diptera: ). Environmen- gall by the midge Paradiplosis tumifex tal Entomology 24, 635-9. (Diptera: Cecidomyiidae). Canadian Raman, A. and Dhileepan, K. (1999). Journal of Botany 60, 131-40. Qualitative evaluation of damaged by Wild, C.H., McFadyen, R.C., Tomely, A.J. Epiblema strenuana (Lepidoptera: and Wilson, B.W. (1992). The biology Tortricidae) to the weed Parthenium and host specificity of the stem-boring hysterophorus (Asteraceae). Annals of the weevil Listronotus setosipennis (Col., Entomological Society of America 92, Curculionidae) a potential biocontrol 717-23. agent for Parthenium hysterophorus Rohfritsch, O. (1988). Food supply mecha- (Asteraceae). Entomophaga 37, 591-8. nism related to gall structure, the exam- Zwölfer, H. and Arnold-Reichart, J. (1993). ple of Geocrypta galii Lw. (Cecido- The evolution of interaction and diver- myiidae, Oligotrophini) on sity in plant–insect systems: The mollugo. Phytophaga 2, 1-17. Urophora–Eurytoma food web in galls of Shepherd, R.C.H. (1993). The theory and Palaearctic Carduae. In ‘Biodiversity protocols for biological control of and ecosystem function’, eds E.D. weeds. Proceedings of the symposium: Schulze and I.A. Monney, Ecological The role of biological control in weed Studies 99, 211-33. management, ed. R.C.H. Shepherd, p. 144-7 (The Weeds Science Society of Victoria, Inc., and the Department of Conservation and Natural Resources, Victoria, Australia). Shorthouse, J.D. and Gassmann, A. (1994). Gall induction by Pegomya curticornis (Stein) (Diptera: Anthomyiidae) within the roots of spurges Euphorbia virgata Waldst. and Kit and E. esula L. (Euphorbiaceae). The Canadian Ento- mologist 126, 193-7. Shorthouse, J.D. and Lalonde, R.G. (1984). Structural damage by Rhinocyllus conicus (Coleoptera: Curculionidae) within the flower heads of nodding thistle. The Canadian Entomologist 116, 1335-43. Shorthouse, J.D., West, A., Landry, R.W. and Thibodeau, P.D. (1986). Structural damage by female Hemadas nubilipennis (Hymenoptera: Pteromalidae) as a fac- tor in gall induction on lowbush blue- berry. Canadian Entomologist 118, 249-54. Stinner, B. R. and Abrahamson, W.G. (1979). Energetics of the Solidago canadensis – stem gall insect – parasitoid guild interaction. Ecology 60, 918-26. Swaminthan, S. and Raman, A. (1981). On the morphology of the stem galls of Eupatorium adenophorum Spreng. (Compositae) and the natural enemies of the cecidozoan, Procecidochares utilis Stone (Tephritidae: Diptera). Current Science 50, 294-5. Treviño, M., Ambatali, F. and McFadyen, R. (1999). A new biocontrol introduc- tion against Parthenium hysterophorus in Queensland. Proceedings of the 12th Australian Weeds Conference, eds A.C. Bishop, M. Boersma, and C.D. Barnes, p. 244. (Weeds Science Society of Tas- mania, Australia). Tscharntke, T. (1988). Variability of grass Phragmites australis in relation to the behavior and mortality of gall-inducing midge Giraudiella inclusa (Diptera, Cecidomyiidae). Oecologia 76, 504-12. West, R.J. and Shorthouse, J.D. (1981). Morphology of the balsam fir needle