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AT LAST, BIOLOGICAL CONTROL OF BELLYACHE BUSH

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AT LAST, BIOLOGICAL CONTROL OF BELLYACHE BUSH

Dianne B. J. Taylor, Elizabeth L. Snow, Kerri Moore and Kunjithapatham Dhileepan Biosecurity Queensland, Department of Agriculture and Fisheries, Ecosciences Precinct, Boggo Road, Dutton Park, Queensland 4102, .

ABSTRACT

Jatropha gossypiifolia , commonly known as bellyache bush, is a serious weed of rangelands and riparian zones of northern Australia. Since bellyache bush became a target for biological control in 1997, only one agent has been released and this failed to establish. A renewed biological control effort has identified a number of potential agents. A small leaf-mining , Stomphastis sp. (: ), was imported from Peru into quarantine for further research in 2014. Newly emerged larvae mine directly into a leaf and remain there until pupation. No-choice host specificity testing of Stomphastis sp. has been completed for 43 test species. The moth laid eggs on numerous non- target species; however development of the agent only occurred on bellyache bush and its congener J. curcas , which is also a weed. Quarantine testing has thus confirmed that the leaf miner is highly host specific and suitable for release in Australia. An application to release this agent will be submitted to the Australian government in the near future. A second agent, divisella (Lepidoptera: ) from India, was imported into quarantine in 2015. The larvae of this moth feed on the leaves, stems and fruit of bellyache bush. No-choice host specificity testing of this agent is in progress. To date, complete development has occurred on five exotic species and two natives. The potential use of the two native species as hosts is being investigated further. Other prospective agents under consideration include a gall midge from Bolivia and a leaf-feeding midge from Paraguay.

Keywords: gossypiifolia, Stomphastis, Sciota, Australia

INTRODUCTION

Jatropha gossypiifolia L. () , commonly known as bellyache bush, is a serious weed of rangelands and riparian zones of northern Australia, and it has the potential to invade much of northern Australia (Heard et al. 2012). It forms dense thickets, reducing the usefulness of land for pastoral and grazing purposes. Monotypic stands supress seedling recruitment of native species, reducing biodiversity and impacting fire regimes due to reduced fuel load. The shallow root system causes increased erosion along creek and river banks (Bebawi et al. 2007). All parts of the are toxic to stock and humans. Biological control is an important component of the long-term management strategy for J. gossypiifolia in Australia. Biological control of bellyache bush was initiated in 1999. Since then, only one agent, the jewel bug, Agonosoma trilineatum (F.) has been released and there is no evidence of its establishment (Heard et al. 2012).

A renewed biological control effort, involving exploration in South America, identified a

4 number of potential biological control agents (Dhileepan et al. 2014). The most promising was a small leaf-mining moth Stomphastis sp. (Lepidoptera: Gracillariidae) which was

imported from Peru into quarantine in 2014 for further research. A second agent, Sciota Page divisella (Duponchel) (Lepidoptera: Pyralidae), was found on bellyache bush during opportunistic surveys conducted in India and was imported into quarantine in 2015. The larvae of this moth feed on the leaves, stems and fruit of bellyache bush. In this paper, we discuss the progress of quarantine testing for both of these species and future actions.

MATERIALS AND METHODS

Stomphastis sp.

Stomphastis sp. was imported into our quarantine facility in Brisbane in November 2014 (Taylor et al. 2016). Adult Stomphastis sp. are small (less than 1 cm long) and live for an average of 10 days under quarantine conditions. Females lay eggs singly on leaves. Newly emerged larvae mine directly into the leaf and remain in the leaf as they develop. Larvae exit the leaf to pupate, mainly on the leaf. A generation from adult to adult takes around 22 days under quarantine conditions (Taylor et al. 2016).

The host test list for Stomphastis sp. contains 43 species from the Euphorbiaceae and closely related families; 33 are native species and 10 are exotic species (Table 1). All test plants were subjected to no-choice oviposition/larval development trials, with at least five replicates conducted for most species. Twenty newly emerged, unsexed Stomphastis sp. adults were released into a 45 x 45 x 90 cm gauze covered cage, containing a single potted test plant. With each round of testing, at least one bellyache bush plant was also included as a control, however only ten newly emerged adults were released into this cage. Test plants were maintained until a new generation of adults were recovered from bellyache bush, at which time they are disposed of. Test species on which Stomphastis sp. completed development, were subject to choice oviposition/larval development trials with bellyache bush.

Sciota divisella

In India, S. divisella was observed feeding on bellyache bush, J. curcas and grantii Oliv., (Snow et al. 2016). A colony was established in quarantine in July 2015, with a further importation in October 2015 to augment the colony. Female S. divisella lay eggs in clumps or rows on leaves and the upper portions of stems of bellyache bush plants (Snow et al. 2016).

Native, crop and ornamental species from the Euphorbiaceae and closely-related families were included in the host testing. Initially test plants were subject to no-choice larval development trials, with at least five replicates for each species. Ten newly-hatched S. divisella larvae were carefully placed onto each potted test plant which were each enclosed in a 45 x 45 x 90 cm gauze covered cage. With each round of testing, at least one bellyache bush plant was also included as a control. Test plants were maintained until a new generation of adults were recovered from bellyache bush, at which time they are disposed of. Native species on which complete development occurred will be subject to further testing including oviposition and choice trials.

RESULTS

Stomphastis sp. 5 Under no-choice conditions, Stomphastis sp. females laid eggs on 29 of the 43 test species, predominantly on leaves at the top of the plants. Egg hatch occurred on 24 of Page these species. However, in all cases except on bellyache bush and J. curcas , the 1st instar larvae died shortly after emerging (Figures 1 and 2). When female Stomphastis sp. were provided with both bellyache bush and J. curcas , they oviposited at an equal rate on both species. The proportion of eggs that developed into adults was also similar for the two species.

Sciota divisella

To date larval development trials have been completed for 13 test species and partially completed for further 22 species (Table 1). These include 25 native and ten exotic species. Complete larval development has occurred on seven non-target species – five exotic species ( J.curcas, J. podagrica Hook. , esculenta Crantz., Euphorbia nerifolia L. and E. grantii ) and two native species ( Macaranga tannarius (L.) Müll.Arg. and E. plumerioides Teijsm. ex Hassk.) (Figure 3). In no-choice oviposition trials females have laid eggs on M. tannarius. Euphorbia plumerioides is yet to be tested.

DISCUSSION

No-choice tests are rigorous tests and identify the absolute host range; either feed/lay eggs on the test plant or die. Host specificity test results for Stomphastis sp. provide strong evidence that it is highly host specific and suitable for release in Australia. The non-target species on which eggs were laid have been shown to be unsuitable hosts by the absence of any larval development. Larval development only occurred on bellyache bush and J. curcas. Though not declared as a weed in Queensland, J. curcas is regarded as invasive and is an approved target for biological control in Australia. Utilisation of this species in the field by Stomphastis sp. would thus be beneficial. Jatropha curcas was the only congener of three tested to support any development of the past the first instar.

Biological studies conducted in quarantine demonstrated that Stomphastis sp. has both a short generation time and high fecundity. This bodes well for its future as a biological control agent. It is expected that like other Gracillaridae, Stomphastis sp. will be an adept disperser, a desirable characteristic given the expansive areas across which bellyache bush occurs. A release application will be submitted to the relevant regulatory bodies later this year. If approved for release, the release effort for Stomphastis sp. will be focussed in areas with major bellyache bush infestations, such as along the Burdekin River from Charters Towers to Home Hill, Hughenden and Gulf of Carpentaria, along the Gregory River and Normanton, and along the Palmer River in Cape York. Given the ease with which the insect can be reared, there will be an opportunity to explore partnerships with various community and NRM groups. Insects will also be supplied to stakeholders in the and (in partnership with the respective government bodies).

The second bellyache bush insect currently in our quarantine facility, S. divisella, is a highly damaging insect. However, due to the development of the insect on two native species ( M. tannarius and E. plumerioides ) and cassava ( M. esculenta ) during host testing, the insect is unlikely to be pursued for release. Testing of S. divisella is continuing on species partially tested (where feeding has occurred), as well as oviposition tests with

M. tannarius and E. plumerioides to elucidate results from larval development trials. Other 6 prospective insects under consideration for bellyache bush include a gall midge from Bolivia ( Prodiplosis longifila Gagné) and a leaf-feeding midge from Paraguay ( Prodiplosis Page sp. near longifila) (Dhileepan et al. 2014). The gall midge induces galls in shoot-tips, emerging leaves and stems of bellyache bush. Preliminary testing of the gall midge is in progress in South America and South Africa . If results are favourable, the gall midge will be imported into quarantine for further testing and research. Host specificity testing and field trials with the Jatropha rust, Phakopsora arthuriana , have been completed and indicate that it is highly host specific. Studies are currently in progress to determine if the rust is autoecious or heteroecious (completes its lifecycle on a single species or requires a second unrelated host).

ACKNOWLEDGEMENTS

This project was funded by Meat and Livestock Australia and the Queensland Government’s War on Western Weeds funding initiative. We thank Dr Stefan Neser (Plant Protection Research Institute, South Africa), Dr Marion Seier, Kate Pollard (CABI-UK), Victor Hugo Sanchez (Instituto National de Investigacion Agraria, Tarapoto, Peru), Dr A. Balu and S. Murugesan (Institute of Forest Genetics and Breeding, India), Dr Damian Rumiz (Santa Cruz, Bolivia) for their help with the overseas field studies, Dr Jurate De Prins (Royal Belgian Institute of Natural Sciences, Belgium) for her help with the identification and description of the leaf miner, David Fredericks for technical support and Dr Marianne Horak (CSIRO, Canberra) and Dr David Lees (Natural History Museum, UK) for their help with identifying the leaf webber. Thanks to Tony Pople for comments on this manuscript.

REFERENCES

Bebawi, F.F., Vitelli, J.S., Campbell, S.D., Vogler,W.D., Lockett, C.J., Grace, B.S., Lukitsch, B. and Heard, T.A. 2007. The biology of Australian weeds 47. Jatropha gossypiifolia L. Plant Protection Quarterly 22, 42-58.

Dhileepan, K., Neser, S. and J. De Prins. 2014. Biological control of bellyache bush (Jatropha gossypiifolia ) in Australia: South America as a possible source of natural enemies, pp. 5-10. In: Impson, F.A.C., Kleinjan, C.A., and Hoffmann, J.H. (eds), Proceedings of the XIV International Symposium on Biological Control of Weed , Kruger National Park, South Africa, 2-7 March 2014.

Heard, T.A., Dhileepan, K., Bebawi, F., Bell, K. and Segura, R. 2012. Jatropha gossypiifolia L. – bellyache bush. In ‘Biological control of weeds in Australia: 1960 to 2010’, eds M. Julien, R.E. McFadyen and J. Cullen, pp. 324-33. (CSIRO Publishing, Melbourne)

Snow, E. L., Dhileepan, K. and Taylor, D.B.J. 2016. The Jatropha webber ( Sciota divisella ): a potential biological control agent for Jatropha gossypiifolia (bellyache bush) from India. pp. 237-240. In: Randall, R., and Lloyd, S. Borger, C. (eds), Proceedings of the 20 th Australasian Weeds Conference, Weeds Society of Western Australia, Perth, 11-15 September 2016.

Taylor, D.B.J. and Dhileepan, K. 2016. Prospects for the biological control of Jatropha

gossypiifolia : Stomphastis sp. as a potential agent from South America. pp. 233-237. In: 7

Randall, R., and Lloyd, S. Borger, C. (eds), Proceedings of the 20 th Australasian Weeds Conference, Weeds Society of Western Australia, Perth, 11-15 September 2016. Page

Table 1. Host test list and replicates completed for no-choice tests. Test plants Status # Stomphastis sp. Sciota divisella Euphorbiaceae Jatropha gossypiifolia L. Target 36 16 Jatropha curcas L. I 5 5 Jatropha multifida L. O 5 4 Jatropha podagrica Hook. O 5 3 Aleurites sp. N 5 3 inophylla (G.Forst.) P.S.Green N 5 1 lechenaultii (DC.) Baill. N 6 5 Beyeria viscosa (Labill.) Miq. N 5 5 variegatum (L.) A.Juss. E 5 1 acronychioides F.Muell. N 7 5 Croton insularis Baill. N 5 3 Croton verreauxii Baill. N 5 Manihot esculentum Crantz C 6 3 Manihot grahamii Hook. I 6 pinifolius Desf. N 3 Acalyphoideae capillipes Müll.Arg. N 5 5 Alchornea ilicifolia (J.Sm.) Muell.Arg. N 5 Endospermum sp. N 5 5 Macaranga tanarius (L.) Müll.Arg. N 5 5 Mallotus philippensis (Lam.) Muell.Arg. N 5 2 Omphalea celata P.I.Forst N 6 3 Ricinus communis L. I 5 1 Euphorbioideae Euphorbia grantii Oliv . E 5 5 Euphorbia inermis Mill. E 3 Euphorbia nerifolia L. E 5 Euphorbia plumerioides Hassk. N 3 4 Euphorbia pulcherrima Willd. ex Klotzsch E 5 3 Euphorbia tannensis Spreng N 5 2 Euphorbia tithymaloides L. E 5 Homalanthus populifolius Graham N 5 3 Microstachys chamaelea (L.) Hook.f. N 5 Phyllanthaceae Antidesma bunius (L.) Spreng. N 5 3 Antidesma ghaesembilla Gaertn. N 5 Actephila lindleyi (Steud.) Airy Shaw N 5 5 Breynia cernua (Poir.) Mull.Arg. N 5 5 Breynia oblongifolia (Mull.Arg.) Mull.Arg N 3 3 Bridelia exaltata F. Muell. N 6 Cleistanthus hylandii Airy Shaw N 6 2 Flueggea virosa (Willd.) Voigt N 5 2 Glochidion ferdinandi (Muell.Arg.) F.M.Bailey N 5 3 Phyllanthus cuscutiflorus S.Moore N 5 swainii (Beuzev. & C.T.White) Airy Shaw N 5 5 Dissiliaria baloghioides F.Muell. ex Baill. N 5 5 Petalostigma pubescens Domin N 5 2 Sankowskya stipularis P.I.Forst. N 5

Putranjivaceae 8 deplanchei (Brongn. & Gris) Merr. N 5 2 (#Status: N=native, O=ornamental, C=crop, I=invasive). Page

Figure 1. 1st instar larval mines of Stomphastis sp. on Croton verreauxii Baill. (left) and (G.Forst.) P.S.Green (right) .

Figure 2. Stomphastis sp. damage to bellyache bush (left) and J. curcas (right) .

Figure 3. Sciota divisella feeding damage on bellyache bush (left) and on Euphorbia plumerioides (right).

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