sign in sign up
<<
Home , Acacia cardiophylla, Acacia conferta, Acacia falcata, Acacia filicifolia, Acacia lasiocarpa, Acacia macradenia

Proceedings of the XIV International Symposium on Biological Control of Weeds, pp 21-30. F.A.C. Impson, C.A. Kleinjan and J.H. Hoffmann (eds). 2-7 March 2014, , South .

Biological control of prickly ( nilotica subsp. indica): Current research and future prospects

K. Dhileepan*1, D.B.J. Taylor1, C.J. Lockett1, A. Balu2, M.K. Seier3, S. Murugesan2, R.A. Tanner3, K.M. Pollard3, N. Kumaran1 and S. Neser4

1 Biosecurity Queensland, Department of Agriculture, Fisheries and Forestry, Ecosciences Precinct, Boggo Road, Brisbane, 2 Institute of Forest Genetic and Breeding, Coimbatore, Tamil Nadu, 3 CABI – UK, Bakeham Lane, Egham, Surrey, TW20 9TY, UK 4 ARC- Protection Research Institute, Queenswood, Pretoria,

Keywords: , Acacia nilotica, Biological control, host-specificity.

Abstract.

Prickly acacia, Vachellia nilotica subsp. indica (syn. Acacia nilotica subsp. indica) (), a major weed in the natural of western Queensland, has been a target of biological control since the 1980s with limited success to date. Surveys in India, based on genetic and matching, identified five and two rust pathogens as potential agents. Host-specificity tests were conducted for the insects in India and under quarantine conditions in Australia, and for the rust pathogens under quarantine conditions at CABI in the UK. In no-choice tests, the brown -webber, Phycita sp. A, (: ) completed development on 17 non-target plant . Though the showed a clear preference for prickly acacia in oviposition choice trials screening of additional test-plant species was terminated in view of the potential non-target risk. The scale Anomalococcus indicus (: Lecanodiaspididae) developed into mature gravid females on 13 out of 58 non-target plant species tested. In the majority of cases very few female scales matured but development was comparable to that on prickly acacia on four of the non-target species. In multiple choice tests, the scale insect showed a significant preference for the target weed over non-target species tested. In a paired-choice trial under field conditions in India, crawler establishment occurred only on prickly acacia and not on the non-target species tested. Further choice trials are to be conducted under natural field conditions in India. A colony of the green leaf-webber Phycita sp. B has been established in quarantine facilities in Australia and host-specificity testing has commenced. The -rust Ravenelia acaciae-arabicae and the leaf-rust Ravenelia evansii (Puccineales: Raveneliaceae) both infected and produced viable urediniospores on Vachellia sutherlandii (Fabaceae), a non-target Australian native plant species. Hence, no further testing with the two rust species was pursued. Inoculation trials using the gall mite Aceria liopeltus (Acari: Eriophyidae) from V. nilotica subsp. kraussiana in South Africa resulted in no gall induction on V. nilotica subsp. indica. Future research will focus on the leaf-weevil Dereodus denticollis (Coleoptera: Curculionidae) and the leaf-beetle Pachnephorus sp. (Coleoptera: Chrysomelidae) under quarantine conditions in Australia. Native range surveys for additional potential biological control agents will also be pursued in northern and western Africa.

Queensland (Mackey, 1997). Infestations also occur in the Introduction coastal regions of Queensland, in the Northern Territory and Prickly acacia, Vachellia nilotica subsp. indica in (Mackey, 1997). In Queensland, cost of (Benth.) Kyal. & Boatwr. (Fabaceae) (previously Acacia the weed to primary producers is approximately Au$ 9 nilotica subsp. indica) is a serious weed of the grazing areas m/year in lost pasture production (Dhileepan, 2009). of western Queensland and has the potential to spread Prickly acacia forms impenetrable thorny thickets, throughout northern Australia (Mackey, 1997; Dhileepan, competes with native pasture species, prevents the growth 2009). Prickly acacia infests over 7 million hectares of of native beneath the canopy, restricts stock access to natural grasslands and over 2 000km of bore drains in western watercourses and poses a threat to nearly 25 rare and

*Corresponding author: [email protected] 21 Dhileepan et al. threatened species and two endangered plant Raveneliaceae) infecting and inducing on communities (Spies and March, 2004). rachides and pods, and a leaf-rust Ravenelia evansii Syd. & P. Syd. (Pucciniales: Raveneliaceae) (Dhileepan et al., Mechanical and herbicide treatments are available to 2013; Shivas et al., 2013). This reports on progress manage prickly acacia (Spies and March, 2004), especially with the testing of the above prospective agents and also a in areas with low-density infestations, but their use is not leaf gall-mite Aceria liopeltus Meyer (Acari: Eriophyidae) always economical (Mooy et al., 1992). Prickly acacia is from South Africa (Witt, 2004; Stals, 1997). Other not susceptible to fire, but fire has the potential to reduce its prospective agents from India and Africa are identified for seed banks by promoting seed germination (Radford et al., future assessment. 2001a), enabling follow-up chemical control. Though livestock has limited impact on prickly acacia (Radford et 2. Materials and Methods al., 2002), camels (Spies and March, 2004) and goats (Tiver et al., 2001), in conjunction with traditional methods, have 2.1. Prospective biological control agents been shown to reduce the cost of control. Several species Colonies of the brown leaf-webber Phycita sp. A and of native insects feed on prickly acacia in Australia, but the scale A. indicus were established in the insectary, at the none have a major impact (Palmer et al., 2005). Classical biological control is considered the most viable option for Institute of Forest Genetics and Tree Breeding (IFGTB), long-term, sustainable management of prickly acacia in Coimbatore, Tamil Nadu, India, using field collected larvae and pupae (for the leaf-webber) and adults (for the scale Australia. insect). The colonies were maintained on potted prickly Biological control of prickly acacia was initiated in the acacia plants in insect proof cages (60 cm x 60 cm x 100 early 1980s, with native range surveys conducted in Pakistan cm) or on prickly acacia foliage held in glass jars (30 cm x (Mohyuddin, 1986), Kenya (Marohasy, 1992) and South 15 cm) sealed with white muslin cloth. The shoots were Africa (Stals, 1997). Out of the 43 phytophagous inserted into a glass vial containing tap water to maintain collected on V. nilotica subsp. indica in Pakistan, two were freshness of the foliage. Efforts were also made to establish assessed and introduced into Australia, but only the seed- a colony of the leaf-weevil D. denticollis, using field feeding bruchid Bruchidius sahlbergi Schilsky (Coleoptera: collected adults. In addition, colonies of the brown leaf- Chrysomelidae) established. Six out of 90 phytophagous webber Phycita sp. A, the green leaf-webber Phycita sp. B insects collected on V. nilotica subsp. subalata (Vatke) and the scale A. indicus were established in a QC3 Brenan and V. nilotica subsp. leiocarpa Brenan in Kenya quarantine facility at the Ecosciences Precinct (ESP) in were tested, but only four agents were introduced into Brisbane, Australia, using insects imported from India. Australia. The leaf-feeding moth Chiasmia assimilis Field collected larvae and pupae (for the brown and green (Warren) (Lepidoptera: Geometridae) originally introduced leaf-webbers) and gravid females (for the scale insect). The from Kenya, was subsequently collected from another host colonies were maintained on potted prickly acacia plants V. nilotica subsp. kraussiana (Benth.) Kyal. & Boatwr. in (grown from seed collected in Queensland) under controlled South Africa and re-introduced to Australia. Of the four quarantine glasshouse conditions (22-27°C, 14 h light: 10 h African insects introduced, only C. assimilis established dark and 60-70% RH). The gall-rust R. acaciae-arabicae (Dhileepan, 2009), but whether this was due to introduction sourced from Coimbatore, Tamil Nadu, India, and the leaf- from Kenya or South Africa is unknown. Thus far, the rust R. evansii sourced from Tarapur, Gujarat, India were impact of B. sahlbergi on V. nilotica subsp. indica has been established and maintained as uredinial on potted insignificant (Radford et al., 2001b). Chiasmia assimilis prickly acacia plants under controlled temperature and light became well established at coastal sites in northern conditions (temperature 25°C day/20°C night, Queensland, but not widely in the arid inland regions supplementary lighting of 12 h light/day) in a QC2 (Palmer et al., 2007). As a result, more effective biological quarantine facility at CABI Europe in Egham, UK. In South control agents are needed for arid inland Australia, where Africa, the gall-mite A. liopeltus is widespread and often the introduced agents have either not established or are abundant causing leaf distortion and stunting on V. nilotica established but not effective. subsp. kraussiana. A series of inoculation trials were conducted on V. nilotica subsp. indica and V. nilotica subsp. The prickly acacia population in Australia is native to kraussiana in South Africa. the (Wardill et al., 2005) with which there is a good climate match to northern Australia 2.2. Host-specificity tests (Dhileepan et al., 2006), thus surveys for prospective new agents were conducted in India (Dhileepan et al., 2013). The host-specificity test list comprising 74 plant Based on field host range in India, a number of species were species that was used in the testing of previous agents (e.g. prioritized for further evaluation. These included; two leaf- Palmer et al., 2007) has been updated to incorporate the webber Phycita spp. (Lepidoptera: Pyralidae), a name changes resulting from recent taxonomic changes to stem-infesting scale insect Anomalococcus indicus Acacia lato (Maslin, 2001; Orchard and Maslin, 2003; Ramakrishna Ayyar (Hemiptera: Lecanodiaspididae), a Kodela and Wilson, 2006). leaf-weevil Dereodus denticollis Boheman (Coleoptera: Curculionidae), a leaf-beetle Pachnephorus sp. Host- specificity tests in India were conducted either (Coleoptera: Chrysomelidae), a rust fungus Ravenelia under laboratory conditions (Phycita sp. A and acaciae-arabicae Mundk. & Thirum. (Pucciniales: D. denticollis) or in the field (A. indicus). Testing in

22

Biological control of prickly acacia

Australia (Phycita sp. A, Phycita sp. B and A. indicus) was When required, no-choice and choice continuation trials conducted under quarantine conditions. Preliminary host- were also carried out to ascertain the ability of any of the specificity tests for the two rust fungi were conducted in the non-target test plant species to sustain the insect populations quarantine facility at CABI (UK). over multiple generations.

2.2.1. India 2.2.3. CABI - UK A series of no-choice tests were conducted for three of Prickly acacia and 16 closely-related test plant species the prospective agents at IFGTB (Table 1). A minimum of (Table 1), exported to CABI-UK from Australia either as five replicates of each test plant was used. Unfed neonate seeds or bare-rooted plants, were used in the host-specificity Phycita sp. A larvae (10 larvae per replication) and field tests. A minimum of six replicate plants of each species collected D. denticollis adults (10 adults per replication) (except for Acacia filicifolia Cheel & M.B.Welch with one were introduced onto potted test plants (with prickly acacia replicate and R.Br. with three replicates) plants as controls), by enclosing them either in insect-proof were used in the host- specificity tests. cages or sleeves. Test plants and controls inoculated with Urediniospores were inoculated onto leaves of prickly Phycita sp. A were monitored daily to determine the acacia (control) and various test plants (treatments) and duration of larval and pupal stages, and the proportion of inoculated plants were sprayed with a mist of sterile water larvae and pupae developing into pupae and adults, before incubation in a dew chamber at 20oC for 24 hrs. respectively. As a Phycita sp. has been reported as a pest of After removal from the dew chamber, inoculated plants two phylogenetically unrelated, but economically important were maintained in a designated quarantine greenhouse plants, mango (Mangifera indica L.) and cashew chamber and regularly assessed for any signs of chlorosis (Anacardium occidentale L.) (both Anacardiaceae), they and sporulation of the rust and/or any plant defence were included in the host-specificity tests for Phycita sp. A reactions for a minimum of six weeks. The final evaluation (Table 1). For D. denticollis, duration of adult survival was of macroscopic and microscopic symptoms of all test plants recorded on prickly acacia and non-target test plant species, was undertaken up to 10 weeks after inoculation. and since there was no oviposition under laboratory conditions, larval survival and development studies could 2.2.4. South Africa not be conducted. For A. indicus, gravid field-collected females (10 females per replication) were attached to the In South Africa, potted plants of V. nilotica subsp. test plants or prickly acacia controls maintained in the field kraussiana grown from seeds sourced from a single within the IFGTB campus, and the proportions of crawlers susceptible host tree (with heavy mite infestation) from developing to gravid females were recorded. Eight test Pretoria, South Africa and potted plants of V. nilotica subsp. plant species, from the genera Vachellia, Acacia and indica grown from seeds sourced from Queensland, , were used (Table 1). Since A. indicus has been Australia were used in host susceptibility tests. Testing was reported from black pepper (Piper nigrum L., Piperaceae) conducted in a quarantine facility at the ARC-Plant in India, black pepper was included as a test plant species Protection Research Institute (ARC-PPRI), Queenswood, (Table 1). South Africa. Galls of A. liopeltus used in the inoculation trials were collected in March 2014 from V. nilotica subsp. A field choice trial involving potted Neptunia major kraussiana at 14 sites. Galls from each site were (Benth.) Windler (seeds sourced from Australia) and prickly divided into three groups, one was attached to the shoot tips acacia plants, placed under the canopy of scale-insect infested prickly acacia plants within the IFGTB campus of V. nilotica subsp. indica plants, the second to V. nilotica (Coimbatore, India), was initiated in January 2014. Both subsp. kraussiana plants and the third retained in a fridge for confirmation of identification of the mites. After N. major and prickly acacia plants were sampled at monthly inoculation, the plants were sampled at weekly intervals for intervals to monitor crawler establishment and evidence of gall initiation and to record gall abundance. development. 3. Results 2.2.2. Australia 3.1. Phycita sp. A The test plant species included in host-specificity tests In no-choice tests in India, larvae of Phycita sp. A fed conducted under quarantine conditions in Australia are and completed development on two of the eleven non-target listed in Table 1. The potential host ranges of prospective test plants, Vachellia planifrons (Wight and Arn.) Ragup., biological control agents were initially evaluated using no- Seigler, Ebinger & Maslin and Vachellia leucophloea choice tests. Batches of test plants were screened as they became available and in each batch potted prickly acacia (Roxb.) Maslin, Seigler & Ebinger (Table 1). However, plants were included as positive controls. A minimum of very few larvae developed into adults on these plants (34% on A. planifrons, 26% on V. leucophloea). Larvae did not five replicates of each test plant was used. Test plant complete development on the nine other non-target test species with evidence of feeding and development and/or plant species tested (Table 1). oviposition in no-choice tests were subjected to choice tests.

23

Dhileepan et al.

Table 1. Test plant species used in host specificity tests for prickly acacia biological control agents. # N = Native; I = Invasive; E = Exotic; C = Crop; NC = No-choice test; PC-O = Paired choice test for oviposition; PC-F = Paired choice field trail; CT = Continuation Trial; MC = Multiple Choice test. NC (in bold, black text) = test plants on which neonate larvae (Phycita sp. A) developed into adults, crawlers (A. indicus) developed into females and the rust (R. acaceae-arabicae and R. evansii) produced viable spores; NC (in bold, black text and underlined) = test plants on which the neonate Phycita sp. A. larvae/ A. indicus crawlers developed into adults comparable to prickly acacia; CT (in bold, black text) = test plants that supported multiple generations in no-choice conditions. NC (standard, grey text) = no larval/crawler development; PC-O (standard, grey text) = no oviposition; PC-F (standard, grey text) = no A. indicus crawler settlement; MC (standard, grey text) = no larval/crawler settlement.

24

Biological control of prickly acacia

In Australia, no-choice larval host-specificity testing A. mearnsii) supported multiple generations of Phycita sp. was completed for 28 plant species. Non-target feeding and A, though the duration of larval developmental was longer development of Phycita sp. A larvae through to adults on A. baileyana (57 days) and A. mearnsii (58 days) than on occurred on the following 17 native non-target test plant V. nilotica subsp. indica (48 days). Furthermore, fewer eggs species: F.Muell., Acacia oshanesii were laid by females that developed on A. baileyana (64 ± F.Muell. & Maiden, Acacia podalyriifolia A.Cunn. ex 29 eggs per female) and A. mearnsii (117 ± 25 eggs per G.Donn., Acacia macradenia Benth., De female) than by those which developed on V. nilotica subsp. Wild., Vachellia sutherlandii (F. Muell.) Koedela, Acacia indica (159 ± 63eggs per female). deanei (R.T.Baker) Welch, Coombs & McGlynn, Acacia spectabilis A.Cunn. ex Benth., Acacia conferta A.Cunn. ex 3.2. Anomalococcus indicus Benth., Acacia cardiophylla A.Cunn. ex Benth., Acacia irrorata Seiber ex Streng., A. filicifolia, Acacia On prickly acacia in India, A. indicus crawlers parramattensis Tind., Acacia lasiocarpa Benth., Acacia established and developed into mature females 35 to 45 days after inoculation (462 ± 31 females per plant). On Vachellia alata W.T. Aiton, Acacia terminalis (Salisb.) J.F. Macbr. tortilis (Forssk.) Galasso & Banf, both crawler and Vachellia bidwillii Benth. (Table 1). establishment and reproductive maturation of female Acacia mearnsii (36% of the neonate larvae developed nymphs (2 ± 1.4 females per plant) were significantly lower into adults) and A. baileyana (20% of the neonate larvae than on prickly acacia, none of the crawlers that established developed into adults) were shown in no-choice larval on V. tortilis developed into females that produced progeny. feeding trials to be the greatest non-target risks. In paired- No crawler establishment occurred on the other eight non- choice tests involving prickly acacia and A. mearnsii, and target test plant species (Table 1). prickly acacia and A. baileyana, eggs were exclusively laid Under quarantine conditions in Australia, no-choice on prickly acacia. tests have been completed for 58 test plant species. Among In no-choice larval development continuation trials, them, 13 test plants species supported the development of two of the non-target test plant species (A. baileyana and crawlers to reproductively mature females. However, only 25

Dhileepan et al. four (Acacia falcata Willd., V. sutherlandii, N. major and In host-specificity tests, R. acaciae-arabicae infected Neptunia monosperma F.Muell. ex Benth.) supported high and produced viable and infective urediniospores on an numbers of mature adults. Australian native species, V. sutherlandii. Sporulation of R. acaciae-arabicae on V. sutherlandii was always In multiple-choice trials using prickly acacia, accompanied by dark necrotic lesions, indicating that this A. falcata, V, farnesiana and Parachidendron pruinosum non-target species is not a natural host (Seier et al. 2013). (Benth.) Nielsen in quarantine, crawlers showed a Re-inoculation of urediniospores produced on significantly higher preference for prickly acacia (55% V. sutherlandii on to prickly acacia and V. sutherlandii crawler settlement) than for A. falcata (28% crawler resulted only in successful sporulation on the natural host settlement), V. farnesiana (15% crawler establishment) and V. nilotica subsp. indica. Inoculation of V. sutherlandii P. pruinosum (3% crawler settlement). In a choice trial with aeciospores of R. acaciae-arabicae evoked few involving N. major and prickly acacia under natural field macroscopic symptoms and did not result in any uredinial conditions in India, crawler establishment was evident only sporulation. on prickly acacia and not on the non-target N. major when assessed over a two month period. Currently, a similar 3.6. Ravenelia evansii choice trial, conducted at multiple locations in the field in India and involving all four non-target test plant species Under quarantine conditions the leaf-rust (R. evansii) which supported substantial development in no-choice tests established easily and was maintained as uredinial under quarantine conditions, is being pursued. on potted prickly acacia plants. The uredinial cycle of the rust was completed in 12-14 days but there was no evidence 3.3. Phycita sp. B of telia on infected prickly acacia plants. In India, both uredinia and telia of R. evansii have been recorded on The green leaf-webber Phycita sp. B was imported into prickly acacia. quarantine in Brisbane, Australia, in October and December 2013, and a laboratory colony has been successfully Since R. acaciae-arabicae infected and produced established. The moth lays eggs on individual leaflets of viable spores on an Australian native non-target plant live plants. The eggs hatch in about four days, and the entire (V. sutherlandii), host-specificity tests for the leaf-rust lifecycle is completed in six weeks. Under quarantine (R. evansii) commenced with V. sutherlandii. Ravenelia conditions, the moth breeds throughout the years, with no evansii infected and produced viable spores on evidence of a winter diapause. No-choice oviposition and V. sutherlandii; however, sporulation was not accompanied larval development tests have commenced. by visible plant necrosis or lesions as observed for the gall- rust R. acaciae-arabicae. Re-inoculation of spores ex 3.4. Dereodus denticollis V. sutherlandii onto V. nilotica subsp. indica and V. sutherlandii resulted in successful sporulation on both of In India, only adult leaf-weevils were seen feeding on these species. In view of the potential non-target risk to prickly acacia in the field. Details of its oviposition sites Australian native acacia species, no further work on this rust and larval host are unknown. Very few eggs have been will be pursued. recovered under laboratory conditions, and there was no evidence of larvae in the soil or in in India or Australia. 3.7. Aceria liopeltus In no-choice trials in India, the adults fed on A. auriculiformis leaves, and nibbled on V. farnesiana and The gall-mite (A. liopeltus), which induces leaflet galls V. tortilis leaves, but did not survive on these non-target on V. nilotica subsp. kraussiana in South Africa, was species for more than three days. In contrast, the adult leaf- suspected to be specific to this subspecies. In inoculation weevils fed and survived for over a year on V. nilotica trials in South Africa gall induction occurred on three of the subsp. indica under laboratory and field cage conditions in 14 subsp. kraussiana plants tested, with up to 399 galls per India, and in quarantine in Australia. However, in the plant, but there was no evidence of gall induction on absence of substantive oviposition, it was not possible to V. nilotica subsp. indica. No further work involving establish a laboratory colony. A. liopeltus from South Africa will be pursued.

3.5. Ravenelia acaciae-arabicae 3.8. Other prospective agents In India, uredinia and telia of the gall-rust R. acaciae- The leaf-beetle Pachnephorus sp. is found only on arabicae were found on infected leaves, and the aecia V nilotica subsp. indica in southern India. So far, only induced galls on rachides, shoots and pods, of V. nilotica adults have been observed in the field. It is suspected that subsp. indica. Under quarantine conditions, inoculation of the beetle lays eggs in the soil and that the larvae are R. acaciae-arabicae urediniospores on V. nilotica subsp. feeders, but there are no details available on its life-cycle or indica leaves consistently resulted in high levels of its larval host. Permits to import Pachnephorus sp. from infection, with abundant uredinial sporulation on pinnules India have been obtained, and the leaf-beetle will be and rachides. The infection cycle took about three weeks to imported into the Brisbane quarantine facility in Oct/Nov complete. The rust also regularly produced teliospores, but 2014. spermogonia or aecia were not recorded.

26

Biological control of prickly acacia

In Africa, a cecidomyiid (Lopesia niloticae Gagne) conducted, as the moth laid eggs indiscriminately on all induces leaflet galls on V. nilotica subsp. kraussiana in surfaces, including the cage walls in quarantine. The moth South Africa and on V. nilotica subsp. subalata and also showed a greater preference for larger plants over V. nilotica subsp. leiocarpa in Kenya. In view of its ability smaller plants for oviposition under quarantine conditions. to induce galls on multiple subspecies of V. nilotica in This is supported by field observations in India, where the Africa, prospects of this cecidomyiid inducing galls on incidence of Phycita sp. A was always on larger trees with subsp. indica appear promising. no evidence of damage on small plants and seedlings. It is likely that the moth selectively oviposits on large prickly 4. Discussion acacia trees in India. A choice oviposition trial involving large trees of various test plant species (both native to India The , the largest genus of and Australia) is not feasible under quarantine conditions. flowering plants in Australia with over 950 endemic species Further evaluation of Phycita sp. A was discontinued in (Orchard and Wilson 2001), has recently been split into five Australia but will be pursued in India. genera: Acacia Mill., Vachellia Wright & Arn., Senegalia Raf., Britton & Rose and Seigler & The gall-rust R acaciae-arabicae, native to India, has Ebinger (Orchard and Maslin 2003; Kodela and Wilson only been reported on V. nilotica subsp. indica in India. 2006). The close affinity of prickly acacia to the Australian Under quarantine conditions the gall-rust infected and native Vachellia and Acacia species makes biological produced viable and infective urediniospores on control efforts more difficult. Any potential biological V. sutherlandii, however it is not regarded as a suitable field control agent for prickly acacia in Australia needs to be host (Seier and Tanner, 2011; Seier et al., 2013). Field tests species specific in order to pose no significant risk to involving both V. nilotica subsp. indica and V. sutherlandii Australian native species. in India would help to resolve the host-specificity of the gall-rust. Laboratory trials suggested that the potential non- Vachellia nilotica is a polytypic species with nine target risk to Australian , in particular V. sutherlandii known subspecies (Dwivedi, 1993). Subspecies of that grows sympatrically with prickly acacia in Australia, is V. nilotica exhibit significant morphological and genetic unacceptably high and hence no further work was pursued diversity, with each subspecies having a distinct geographic on the rust in the quarantine in the UK. These trials could range within the overall native range. Various subspecies resume if field trials in India suggest that V. sutherlandii is of V. nilotica with overlapping native geographic ranges not at risk. also share a common complex, but the species complex associated with subspecies endemic to southern The leaf-rust R. evansii was shown to infect and and eastern Africa (subsp. kraussiana, subsp. subalata and sporulate on V. sutherlandii under quarantine conditions. subsp. leiocarpa), northern Africa (subsp. nilotica, subsp. However, in contrast to the gall-rust, infection with tomentosa (Benth.) Kyal. & Boatwr. and subsp. Adstringens R. evansii produced no macroscopically visible plant (Schumach.) Kyal. & Boatwr.) and southern (subsp. defence reactions (e.g. necrotic lesions) on V. sutherlandii indica, subsp. cupressiformis (J.L.Stewart) Ali and subsp. (Seier and Pollard, 2012). This indicates a more compatible hemispherica (Ali & Faruqi) Ali) are distinct without much host-pathogen interaction and it is, therefore, most likely overlap (Dwivedi, 1993). Some of the arthropods found on that V. sutherlandii would become infected if it encounters V. nilotica subspecies native to Africa (e.g. the psyllid the leaf-rust in the field. The leaf- rust (R. evansii) has also Acizzia melanocephala Burckhardt & Mifsud, from Kenya been reported from (DC.), Vachellia and South Africa, and the gall-mite A. liopeltus from South macrothyrsa (Harms) Kayl. & Boatwr., Vachellia gerrardii Africa) are host specific at subspecies level, and thus were (Benth.) P.J.H. Hurter, Vachellia rehmanniana (Schinz) found not to be suitable as a biological control agent for Kyal. & Boatwr., (Burch.) Kyal. & subsp. indica (Witt, 2004; Palmer and Witt, 2006). Boatwr. and (Del.) P.J.H. Hurter in Africa (Cannon, 2008). In view of the potential non-target risks, Among the five insect species and two rust fungi no further work on the leaf-rust has been pursued. sourced on subsp. indica from India, testings have been completed for one insect (Phycita sp. A) in Australia and The scale insect (A. indicus) is the only shoot-feeding preliminary testing for both rust fungi (R. acaciae-arabicae agent that showed specificity for V. nilotica in the field in and R. evansii) in the UK. India (Dhileepan et al., 2013). In India, the scale insect has been reported on V. farnesiana, V. leucophloea (Ben-Dov, Host-specificity tests for Phycita sp. A under 2006), S. , Ziziphus mauritiana Lam. (Beeson, quarantine in Australia produced surprising results – larvae 1941) and P. nigrum (Koya et al., 1996). During a four-year completed development on 17 non-target test plant species field survey in India (2008-2012), the scale insect was in no-choice tests, while adults laid eggs only on the target documented only on V. nilotica subsp. indica and V. nilotica weed under choice conditions. In India, it completed subsp. cupressiformis, and not on any of the previously development on two non-target plant species, but there was reported hosts. The scale was also not found on V. tortilis, no evidence of its larvae on these two non-target trees in the a non-target plant that sustained crawler establishment and field, in spite of them co-occurring with prickly acacia development in no-choice tests in India, or on V. nilotica (Dhileepan et al., 2013). This suggests that oviposition subsp. tomentosa, an African subspecies grown widely in behaviour could be the key mechanism in host selection. India along with native subspecies (indica and However, no-choice oviposition tests could not be cupressiformis). Based on field level specificity of the scale

27

Dhileepan et al. insect to V. nilotica subspecies in India, and the choice test Acknowledgements results from Australia and India, a more realistic field We thank N. Kumaran, David Perovic (Ecosciences choice trial involving multiple non-target plant species Precinct, Brisbane, Australia), M. Senthilkumar, across multiple trial sites will be conducted in India. If Mahalakshimi, (Institute of Forest Genetics and Tree proven to be host specific in this proposed choice trial in Breeding, Coimbatore, Tamil Nadu, India), Syed Irfan India, host-specificity tests under quarantine in Australia Ahmed, Sangeeta Singh, K.K. Srivastava, Mahadeo Gorin will recommence. and Anamika Sharma (Arid Forest Research Institute, For D. denticollis there was no consistent oviposition Jodhpur, Rajasthan, India) for the field collection of insects or evidence of larval development in the laboratory, despite and rust fungi; Institute of Forest Genetics and Tree trials using different soil types (sandy, clay and peat) and Breeding, Coimbatore, Tamil Nadu, India and ARC-PPRI, supplementary adult feeding (e.g. honey, pollen and acacia South Africa for facilities; Bill Palmer, Tony Pople and Joe flowers) to encourage oviposition. Lack of oviposition also Scanlan for comments on earlier versions of the manuscript; resulted in the failure to establish laboratory colonies for and Meat & Livestock Australia, Rural Industries Research other prospective biological control agents for prickly and Development Corporation and Queensland acacia from South Africa (Witt et al., 2006; Palmer et al., Governments (War on Western Weeds) for funding the 2012). study. Future host-specificity tests in Australia will focus on References the green leaf-webber (Phycita sp. B), the leaf-weevil (D. denticollis) and the leaf-beetle (Pachnephorus sp.) Beeson, C.F.C., 1941. The ecology and control of forest under quarantine conditions. All three insects are known to insects of India and neighbouring countries, Dehra be specific to V. nilotica subsp. indica under field conditions Dun, India: Vasant Press, 1007 pp. in India. Two of them (Phycita sp. B and D. denticollis), have been imported in to the quarantine facility at ESP and Ben-Dov, Y., 2006. A systematic catalogue of eight Scale Insect families (Hemiptera: Coccoidea) of the world host-specificity testing for the green leaf-webber is Aclerdidae, Asterolecaniidae, Beesoniidae, currently in progress. Carayonemidae, Conchaspididae, Dactylopiidae, Though the no-choice tests for the gall-mite Kerriidae and Lecanodiaspididae. Amsterdam: (A. liopeltus) sourced from V. nilotica subsp. kraussiana Elsevier, 368 pp. produced inconsistent results under quarantine conditions in Cannon, P.F., 2008. Ravenelia evansii. IMI Descriptions of South Africa, it is evident that the gall-mite from this Fungi and No. 1754. CABI, Bakeham Lane, subspecies is unlikely to use prickly acacia in Australia. In Egham, Surrey, UK. previous trials a similar outcome occurred, viz. only 40% establishment of V. nilotica subsp. kraussiana plants and no Dhileepan, K., Wilmot, K.A.D.W., Raghu, S., 2006. A gall establishment on V. nilotica subsp. indica (Witt, 2004). systematic approach to biological control agent Further screening of A. liopeltus will be pursued using mite- exploration and selection for prickly acacia (Acacia galls sourced from V. nilotica subsp. indica co-occurring nilotica ssp. indica). Aust. J. Entomol. 45, 302-306. with endemic V. nilotica subspecies (subsp. nilotica in and Somalia; subsp. tomentosa in Ethiopia and Dhileepan, K., 2009. 2. Acacia nilotica ssp. indica. In: Sudan; subsp. adstringens in Somalia) in North Africa Muniappan, R., Reddy, D.V.P., Raman, A. (Eds.), Weed (Dwivedi, 1993). Biological Control with Arthropods in the Tropics: Towards Sustainability, Cambridge University Press, Future research will also focus on testing the UK, pp. 17-37 susceptibility of V. nilotica subsp. indica to the leaflet galling cecidomyiid (L. niloticae), sourced from V. nilotica Dhileepan, K., Balu, A., Senthilkumar, P., Murugesan, M., subsp. kraussiana in South Africa and from V. nilotica Shivas, R., 2013. Survey and prioritisation of potential subsp. leiocarpa and V. nilotica subsp. subalata in Kenya, biological control agents for prickly acacia (Acacia under quarantine conditions in South Africa. nilotica ssp. indica) from southern India. Biocontrol Sci. Techn. 23, 646-664. So far surveys for potential biological control agents have been conducted in south-east Asia (India and Pakistan) Dwivedi, A.P., (1993). Babul (Acacia nilotica): A and southern (South Africa) and eastern (Kenya) Africa. multipurpose tree of dry areas. Jodhpur, India: Arid Since there have been no surveys undertaken in northern Forest Research Institute, Indian Council of Forestry and western Africa where three native subspecies (subsp. Research and Education, pp. 226. nilotica, subsp. tomentosa and subsp. adstringens) co-occur Kodela, P.G., Wilson, P.G., 2006. New combinations in the with subsp. indica, attempts will be made to conduct genus Vachellia (Fabaceae: ) from surveys in this geographic region (e.g. Sudan, Egypt, Australia. Telopea 11, 233–244. northern , , , Mali and Benin), when it is safe to do so. Koya, K.M.A., Devasahayam, S., Selvakumaran, S., Ka1li, M., 1996. Distribution and damage caused by scale insects and mealy bugs associated with black pepper

28

Biological control of prickly acacia

(Piper nigrum L.) in Indian. J. Entomol. Res. 20, 129- and seedlings in the Astrebla grasslands of northern 136. Australia. J. Arid Environ. 49, 795-807. Mackey, A.P., 1997. The biology of Australian weeds 29. Radford, I.J., Nicholas, D.M., Brown, J.R., 2001b. Acacia nilotica ssp. indica (Benth.) Brenan. Plant Prot. Assessment of biological control impact of seed Q. 12, 7-17. predators on the invasive Acacia nilotica (Prickly acacia) in Australia. Biol. Control 20, 261- Marohasy, J., 1992. Biocontrol of Acacia nilotica using 268. insects from Kenya. Final report to Australian Wool Corporation. Alan Fletcher Research Station, Radford, I.J., Nicholas, D.M., Tiver, F., Brown, J.R., Queensland Department of Lands, Brisbane, Kriticos, D.J., 2002. Seedling establishment, mortality, Queensland, Australia. tree growth rates and vigour of Acacia nilotica in different Astrebla : Implications for Maslin, B.R., 2001. Introduction to Acacia. Flora of invasion. Austral Ecol. 27, 258-268. Australia, 11, 3-13. Seier, M.K., Tanner, R.A., 2011. Host specificity testing of Mohyuddin, A.I., 1986. Investigations on the natural the prickly acacia rust Ravenelia acacia-arabicae enemies of Acacia nilotica in Pakistan. Final Report, Mundk. & Thirum. (previously reported as R. evansii Commonwealth Institute of Biological Control, Syd. & P. Syd.). Final Report, 1 June 2010 - 31 May Rawalpindi, Pakistan, 116 pp. 2011. CABI, UK. 31 pp. Mooy, L.M., Scanlan, J.C., Bolton, M.P., Dorney, W. J., Seier, M.K., Pollard, K.M., 2012. Preliminary host 1992. Management guidelines derived from ecological specificity testing of the prickly acacia rust Ravenelia studies of prickly acacia (Acacia nilotica). In: evansii Syd. & P. Syd. Final Report, 1 October 2011 - Richardson, R G. (Ed.), Proceedings of the First 31 March 2012. CABI, UK. 17 pp. International Weed Control Congress, Volume 2, International Weed Science Society and Weed Science Seier, M.K., Ellison, C.A., Cortat, G., Day, M. and Society of Victoria, Monash University, Melbourne, Dhileepan, K. (2013) How specific is specific enough? Australia, pp. 347-349. - case studies of three rust species under evaluation for weed biological control in Australia. In: Wu, Y., Orchard, A.E., Maslin, B.R., 2003. Proposal to conserve the Johnson, T., Sing, S., Raghu, S., Wheeler, G., Pratt, P., name Acacia (Leguminosae: Mimosoideae) with a Warner, K., Center, T., Goolsby, J. and Reardon, R. conserved type. Taxon 52, 362–363. (Eds.), Proceedings of the XIII International Orchard, A.E., Wilson, A.J.G., (Eds.) 2001. Flora of Symposium on Biological Control of Weeds, USDA Australia, Volumes 11A & 11B, Mimosaceae, Acacia, Forest Service, Hawaii, USA, pp. 89–96 Parts 1 & 2. Australian Biological Resources Study Shivas, R.G., Balu, A., Singh, S., Ahmed, S.I., Dhileepan, (ABRS), Canberra, and CSIRO Publishing, K., 2013. Ravenelia acaciae-arabicae and Ravenelia Melbourne. evansii are distinct species on Acacia nilotica subsp. Palmer, W.A., Vitelli, M.P., Donnelly, G. P., 2005. The indica. Aust. Mycologist 31, 31-37. phytophagous insect fauna associated with Acacia Spies, P., March, N., 2004. Prickly acacia: National case nilotica subsp. indica (Mimosaceae) in Australia. studies manual. Natural Heritage Trust and Aust. Entomologist 32, 173-180. Department of Natural Resources and Mines, Palmer, W.A., Witt, A.B.R., 2006. On the host range and Queensland, Australia. 97 p. biology of Acizzia melanocephala (Hemiptera: Stals, R., 1997. A survey of phytophagous organisms Psyllidae), an insect rejected for the biological control associated with Acacia nilotica in South Africa. Final of Acacia nilotica subsp. indica (Mimosaceae) in Report to the Queensland Department of Natural Australia. Afr. Entomology, 14, 387-390. Resources. ARC-Plant Protection Research Institute, Palmer, W.A., Lockett, C.J., Senaratne, K.A.D.W., Pretoria, South Africa. 113 p. McLennan, A., 2007. The introduction and release of Tiver, F., Nicholas, M., Kriticos, D., Brown, J. R., 2001. Chiasmia inconspicua and C. assimilis (Lepidoptera: Low density of prickly acacia under sheep grazing in Geometridae) for the biological control of Acacia Queensland. J. Range Manage. 54, 382-389 nilotica in Australia. Biol. Control, 41, 368-378. Wardill, T.J., Graham, G.C., Manners, A., Playford, J., Palmer, W.A., Lockett, C., Dhileepan, K., 2012. Acacia Zalucki, M., Palmer, W. A., Scott, K.D., 2005. The nilotica ssp. indica – prickly acacia. In: Julien, M., importance of species identity in the biocontrol McFadyen, R.E and Cullen, J. (Eds.), Biological process: identifying the subspecies of Acacia nilotica control of weeds in Australia: 1960 to 2010, CSIRO (Leguminosae: Mimosoideae) by genetic distance and Publishing, Melbourne, pp. 18-28. the implications for biological control. J. Biogeogr. 32, Radford, I. J., Nicholas, D. M., Brown, J. R., 2001a. Impact 2145-2159. of prescribed burning on Acacia nilotica seed banks

29

Dhileepan et al.

Witt, A.B.R., 2004. Aceria liopeltus Meyer (Acari: Eriophyidae) and Asterolecanium conspicuum Brain (Hemiptera: Asterolecaniidae), two potential biological control agents for Acacia nilotica ssp. indica (Mimosaceae) in Queensland, Australia. Afr. Entomol. 12, 142-146. Witt, A.B.R., Steenkamp, H.E., Palmer, W.A., 2006. Initial screening of Pseudomalegia cf. lefevrei (Coleoptera: Chrysomelidae), a potential biological control agent for Acacia nilotica (L.) Willd. ex Del. ssp. indica (Benth.) Brenan (Mimosaceae) in Australia. Afr. Entomol. 14, 384-386.

30