Survey and prioritisation of potential biological control agents for prickly acacia (Acacia nilotica subsp. indica) in southern India

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Survey and prioritisation of potentialbiological control agents for pricklyacacia (Acacia nilotica subsp. indica) insouthern IndiaKunjithapatham Dhileepan a , Ayyapillai Balu b , SelvarajMurugesan b , Ponnusamy Senthilkumar b & Roger G. Shivas aa Biosecurity Queensland, Department of Agriculture , Fisheries &Forestry, Ecosciences Precinct , Dutton Park , QLD , Australiab Institute of Forest Genetics and Tree Breeding , Coimbatore ,Tamil Nadu , IndiaAccepted author version posted online: 03 Apr 2013.Publishedonline: 23 May 2013.

To cite this article: Kunjithapatham Dhileepan , Ayyapillai Balu , Selvaraj Murugesan , PonnusamySenthilkumar & Roger G. Shivas (2013): Survey and prioritisation of potential biological controlagents for prickly acacia (Acacia nilotica subsp. indica) in southern India, Biocontrol Science andTechnology, 23:6, 646-664

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RESEARCH ARTICLE

Survey and prioritisation of potential biological control agents forprickly acacia (Acacia nilotica subsp. indica) in southern India

Kunjithapatham Dhileepana*, Ayyapillai Balub, Selvaraj Murugesanb,

Ponnusamy Senthilkumarb and Roger G. Shivasa

aBiosecurity Queensland, Department of Agriculture, Fisheries & Forestry, Ecosciences Precinct,Dutton Park, QLD, Australia; bInstitute of Forest Genetics and Tree Breeding, Coimbatore,

Tamil Nadu, India

(Received 10 January 2013; returned 12 March 2013; accepted 19 March 2013)

Prickly acacia, Acacia nilotica subsp. indica (Benth.) Brenan (Mimosaceae), amulti-purpose tree native to the Indian subcontinent, is a weed of nationalsignificance, widespread throughout the grazing areas of western Queensland andhas the potential to spread throughout northern Australia. Biological control ofprickly acacia has been in progress since the early 1980s, but with limited successto date. Based on genetic and climate matching studies, native surveys forpotential biological control agents were conducted in 64 sites in Tamil Nadu stateand eight sites in Karnataka state from November 2008 to December 2011.Surveys yielded 33 species of phytophagous insects (16 species of leaf-feeders,eight species of stem feeders, four species with leaf-feeding adults and root-feeding larvae, two stem-borers and bark-feeders and three flower-feeders) andtwo rust fungi. The number of species recorded at survey sites increased with thenumber of times the sites were surveyed. Using a scoring system based on fieldhost range, geographic range, seasonal incidence and damage levels, we prioritiseda scale insect (Anomalococcus indicus Ramakrishna Ayyar), two leaf-webbingcaterpillars (Phycita sp. A and Phycita sp. B), a leaf weevil (Dereodus denticollisBoheman), a leaf beetle (Pachnephorus sp.), a gall-inducing rust (Ravenelia acacia-arabica Mundk. & Thirumalachari) and a leaf rust (Ravenelia evansii Syd. & P.)for detailed host specificity tests. The two rusts were sent to CABI-UK forpreliminary host-specificity testing. Three insects (A. indicus, D. denticollis andPhycita sp. A) were imported into a quarantine facility in Brisbane, Australiawhere host-specificity tests are in progress.

Keywords: native range survey; agent prioritisation; field host range; Acacianilotica; India; Australia

Introduction

Acacia nilotica subsp. indica (known as prickly acacia in Australia), a weed of

national significance, is widespread throughout the grazing areas of western

Queensland and has the potential to spread throughout northern Australia (www.

weeds.org.au/WoNS/pricklyacacia). In the natural grasslands of western Queensland,

over 7 million hectares and 2000 km of bore drains are infested with this weed

(Mackey, 1997). The weed is also present in the coastal regions of Queensland, in

the Northern Territory and Western Australia (Mackey, 1997). Prickly acacia

*Corresponding author. Email: [email protected]

Biocontrol Science and Technology, 2013

Vol. 23, No. 6, 646�664, http://dx.doi.org/10.1080/09583157.2013.788689

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http://www.weeds.org.au/WoNS/pricklyacacia

http://www.weeds.org.au/WoNS/pricklyacacia

http://dx.doi.org/10.1080/09583157.2013.788689

infestations in Queensland cost primary producers Au$ 9 m/year in lost pasture

production (Dhileepan, 2009). In such areas, prickly acacia forms impenetrable

thorny thickets, competes with native pasture species, facilitates the replacement of

native grasses with less stable, short-lived plants, prevents the growth of native plants

beneath the canopy, restricts stock access to watercourses and poses a threat to

nearly 25 rare and threatened animal species and two endangered plant communities,

by displacing native grasses (Spies & March, 2004).

Biological control of prickly acacia was initiated in the early 1980s, with native

range surveys conducted in Pakistan (Mohyuddin, 1986), Kenya (Marohasy, 1992)

and South Africa (Stals, 1997). Among the 43 phytophagous arthropods collected on

A. nilotica subsp. indica in Pakistan, two were introduced into Australia, but only the

seed-feeding bruchid Bruchidius sahlbergi Schilsky established. Three of the 90

phytophagous insects collected on A. nilotica subsp. subalata (Vatke) Brenan and

A. nilotica subsp. leiocarpa Brenan in Kenya were introduced into Australia. A leaf-

feeding geometrid Chiasmia assimilis (Warren) that was introduced from Kenya was

re-introduced again, collected on A. nilotica subsp. kraussiana (Benth.) Brenan from

South Africa. Of the three African insects, only C. assimilis established (Dhileepan,

2009). Thus far, the impact of B. sahlbergi on A. nilotica subsp. indica has been

insignificant (Radford, Nicholas, & Brown, 2001). C. assimilis became well

established at coastal sites in northern Queensland, but not widely in the arid

inland regions (Palmer, Lockett, Senaratne, & McLennan, 2007). As a result, more

effective biological control agents are needed for arid inland Australia, where the

introduced agents have established but not been effective.

The invasive prickly acacia population in Australia is native to the Indian

subcontinent (Wardill et al., 2005). In India, available information on insects and

plant pathogens associated with A. nilotica has been gathered from the perspective of

itemising forestry and nursery pests (e.g. Beeson, 1941; Dwivedi, 1993; Pillai et al.,

1995). There have been no systematic surveys conducted to catalogue phytophagous

insects and plant pathogens associated with A. nilotica in India. Hence, based on

genetic (Wardill et al., 2005) and climate matching (Dhileepan, Wilmot, & Raghu,

2006) studies, native range surveys were conducted in India (Dhileepan et al., 2010).

In this study, we catalogued phytophagous insects and rust pathogens associated with

prickly acacia in southern India. A scoring system based on field host range, feeding

guilds, geographic range, seasonal activities and damage levels was adopted to

prioritise five insects and two rust fungi for detailed host specificity testing in

quarantine as potential biological control agents for prickly acacia.

Materials and methods

Study organisms

In India, A. nilotica subsp. indica is a multi-purpose tree that occurs naturally and is

cultivated throughout the country. It is widely used in agroforestry, social forestry,

reclamation of wastelands and rehabilitation of degraded forests in India. The other

subspecies of A. nilotica that are native to India are A. nilotica subsp. cupressiformis

(Stewart) Ali & Faruqi and A. nilotica subsp. hemispherica Ali & Faruqi (Dwivedi,

1993). In southern India, A. nilotica subsp. tomentosa (Benth.) Brenan, a native of

Biocontrol Science and Technology 647

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central Africa, co-occurs with A. nilotica subsp. indica in Tamil Nadu, and A. nilotica

subsp. cupressiformis co-occurs with A. nilotica subsp. indica in Karnataka state.

Native range surveys

A total of 64 sites across 20 districts (administrative areas within States) in Tamil

Nadu and eight sites across two districts in Karnataka were surveyed (Table 1).

Surveys were conducted throughout the year, with all sites visited at least once in

three-month intervals from November 2008 to December 2011. In survey sites with

juvenile and young trees, the entire tree canopy was inspected visually for the

presence of insects, or signs of feeding damage or disease symptoms. In sites with

mature trees, branches of trees that could be accessed from the ground were

sampled visually for insects and diseases. At each site, incidence of insects or insect

damage and disease symptoms were recorded, along with details on the subspecies

status of the A. nilotica, plant stage (seedlings, juveniles or trees), co-occurring

vegetation (e.g. other Acacia spp.) and weather details (temperature and relative

humidity) at the time of sampling. Any immature states of insect were brought to

the laboratory at the Institute of Forest Genetics & Tree Breeding (IFGTB) and

reared to adults for identification. At each site, two to three research staff spent a

minimum of one hour surveying for insects and rust pathogens. Survey sites were

predominantly forestry plantations in tank beds and isolated plants on the

roadsides or on embankment on agricultural lands. All insects and rust fungi

collected on A. nilotica were first matched with previously identified specimens at

the IFGTB, Coimbatore, India. If necessary, the specimens were then sent to

taxonomic experts and agencies within India (Indian Agricultural Research

Institute, Kerala Forest Research Institute, Tamil Nadu Agricultural University,

Indian Forest Research Institute, University of Agricultural Sciences � Bangalore

and Zoological Survey of India) and overseas (British Museum of Natural History,

CABI � UK, CSIRO, Queensland Plant Pathology Herbarium and Queensland

Museum) to confirm their identifications.

Field host range

At 51 of the 72 sites, subsp. indica and subsp. tomentosa were both present but subsp.

indica and subsp. cupressiformis occurred together only at six sites (Table 1). There

were 12 survey sites with only subsp. indica and three sites with only subsp.

cupressiformis, which all occurred in Karnataka (Table 1). There was no site with

only subsp. tomentosa. Where two subspecies co-occurred, both were sampled with

equal time spent on each subspecies. Field specificity of various phytophagous

arthropods and rust pathogens at subspecies level was documented. Other Acacia

species, Acacia leucophloea (Roxb.), Acacia ferruginea DC, Acacia senegal Willd.

(natives of India), Acacia horrida (L.) Willd. (native of Africa) and other non-target

trees occurring at the survey sites were also surveyed to ascertain the ecological host

range of insects found on A. nilotica. Sampling on the non-target Acacia spp. and

other tree species at each survey site was restricted to only the agents that were

collected on A. nilotica.

648 K. Dhileepan et al.

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Table 1. Prickly acacia survey sites in southern India.

State District Site/town Latitude Longitude Acacia nilotica subspecies

Tamil Nadu Coimbatore Veerakeralam 11800.303? 076854.908? indica�tomentosa

Vedappatti 10859.298? 076854.901? indica�tomentosa

Perur 10859.316? 076853.848? indica�tomentosa

Allikulam 11814.897? 077806.690? indica�tomentosa

Ellaipalayam 11811.444? 077803.928? indica�tomentosa

A. Mettupalayam 11815.421? 077807.208? indica�tomentosa

Pudupalayam 11815.635? 077807.981? indica�tomentosa

Madurai Thirumal Periyatank 09843.080? 078802.527? indica

Melakottai 09847.084? 077858.896? indica�tomentosa

Virudhunagar Nalakundukanmai 09836.279? 078805.423? indica�tomentosa

Sivagangai Periyasanthani 09849.860? 078834.200? indica

Allur kanmai 09850.117? 078831.760? indica

Keeranur 09851.422? 078834.546? indica�tomentosa

Kiluvachi 09850.213? 078831.816? indica�tomentosa

Tuticorin Sambakulam 09830.820? 078832.352? indica�tomentosa

Malapattakulum 08846.905? 077851.451? indica

Ulakkudi 08848.012? 077852.352? indica�tomentosa

Tirunelveli Vettuvankulum 08846.917? 077851.462? indica�tomentosa

Thirupani karsal Kulam 08845.408? 077834.902? indica�tomentosa

Sadayaneri 08845.408? 077836.988? indica�tomentosa

Tanjore Pala Aeri 10843.998? 078858.989? indica�tomentosa

Kathattipatti 10842.045? 078854.522? indica�tomentosa

Rayaram Aeri 10842.045? 078858.522? indica�tomentosa

Sayalkudi Aeri 10833.949? 078831.229? indica�tomentosa

Vaduvur Vadapathai 10844.756? 078819.982? indica�tomentosa

Erode Thatankuttai 11814.898? 077822.707? indica�tomentosa

Kenjanoor 11830.542? 077 812.496? indica�tomentosa

Salem Kakapalayam 11833.428? 078800.429? indica�tomentosa

Periya Krishnapuram 11839.517? 078825.709? indica�tomentosa

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Table 1 (Continued )


Madoor Kulam 11839.517? 078825.709? indica�tomentosa

Villupuram Sithanangoor 11844.374? 079801.205? indica�tomentosa

Agoor 12816.852? 079833.875? indica�tomentosa

Azoor 12814.553? 079833.041? indica�tomentosa

Puliyanur 12818.507? 079833.813? indica�tomentosa

Thiruvanamalai Chathra 12817.985 079804.162? indica�tomentosa

Thempallipatu 12817.985? 079804.161? indica�tomentosa

Arugavur 12824.818? 079806.327? indica�tomentosa

Kanjipuram Kalabiranpuram 12834.343? 079853.829? indica�tomentosa

Thenneri 12850.964? 079850.469? indica�tomentosa

Pillaipakam 12834.343? 079853.829? indica�tomentosa

Thiruvallur Athivaragapuram 13807.879? 079826.300? indica�tomentosa

Chinanagapoondi 13807.437? 079821.768? indica

Periyaramapuram 13807.870? 079826.309? indica

Kakavakam 13818.086? 079859.774? indica

Pudukottai Ramakavundanpatti 10828.616? 078827.241? indica�tomentosa

Kilananjur 10834.609? 078848.364? indica

Melanajur 10835.184? 078848.226? indica�tomentosa

Kavinadu 10822.917? 078846.683? indica�tomentosa

Theni Rajapovalasamuthira 10800.745? 077827.372? indica�tomentosa

Vedakanmai 10809.741? 077844.670? indica�tomentosa

Mathuvar Kulam 10809.531? 077841.548? indica�tomentosa

Ramanathapuram Urapuli Kanmai 09851.386? 078834.494? indica�tomentosa

Villathur 09830.823? 078832.355? indica�tomentosa

Trichy Sevalur Kanmai 10840.522? 078830.500? indica�tomentosa

Manaparai Kulam 10837.305? 078824.974? indica�tomentosa

Manikampalayasathram 10838.698? 078827.643? indica

Paluvanji 10828.615? 078827.241? indica�tomentosa

Kingini Kulam 10 856.026? 078812.280? indica�tomentosa

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Ariyalur Keelapaluvur 11802.875? 079804.038? indica�tomentosa

Melapaluvur 11802.900? 079802.811? indica�tomentosa

Dindigul Veriyapur Karadu, 10827.814? 077838.728? indica

Eramanaicken Pattikulum 10828.980? 077834.910? indica

Polonkinaru 10835.586? 077811.833? indica�tomentosa

Karur R.Pudukkottai 11856.020? 078812.169? indica

Karnataka Chamraj Nagar Bendakudi. 12800.942? 076848.969? indica�cupressiformis

Chathra 11851.835? 076857.297? indica�cupressiformis

Upalamsathevay 11856.457? 076855.218? indica�cupressiformis

Barukuppa 12800.282? 076849.455? cupressiformis

Nanjangud Bendrahali 11851.867? 076840.082? cupressiformis

Kunoorpura 12800.035? 076850.348? indica�cupressiformis

Sinthuvallipura 12802.255? 076840.503? indica�cupressiformis

Kadkola 12811.687? 076840.069? indica�cupressiformis

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Prioritisation process

For all insects and rust pathogens collected during the survey that were identified to

species level, previous host records and pest status were used to first eliminate known

crop pests and polyphagous insects and pathogens. Based on a literature search, a

score between ‘1’ and ‘5’ was given (1�pest of crops; 2�host records across diverse

plant families; 3�host records restricted within Mimosaceae; 4�host records

limited to Acacia species; 5�host records limited to A. nilotica) for each insect and

rust fungi. Insects and rust pathogens with a score of ‘3’ or less were eliminated from

the prioritisation process.Based on field host range recorded during the current survey, a score between ‘1’

and ‘5’ was given (1�hosts across diverse plant families; 2�occur on multiple

genera, within a plant family; 3�occur on a wide range of Acacia species; 4�limited

to few closely related Acacia species; 5�restricted to A. nilotica) for each insect and

rust fungi. Insects and rust pathogens with a score of ‘3’ or less were eliminated from

the prioritisation process.

For geographic range, a score between ‘1’ and ‘5’ was given (1�collected from

less than 20% of the survey sites; 2�collected from 20 to 40% of the survey sites; 3�collected from 40 to 60% of the survey sites; 4�collected from 60 to 80% of survey

sites; 5�collected from more than 80% of survey sites) for each insect and rust fungi.

For seasonal incidence, a score between ‘1’ and ‘5’ was given (1�occur less than

three months in a year; 2�occur between three and five months in a year; 3�occur

between six and eight months in a year; 4�occur between 9 and 10 months in a year;

5�occur more than 10 months in a year) for each insect and rust fungi.

For damage levels (1�no visible symptoms; 2�visible, but minor symptoms;

3�seasonal damage � defoliation, shoot dieback, etc.; 4�loss of vigour � complete

defoliation, shoot dieback, etc.; 5�field mortality), a similar scoring was given

based on visual field observations.

Data analysis

For each survey site, the number of times the site was visited, along with the number

of times each agent (insect or rust species) was collected over the survey period

(2008�2011) were recorded. From this, the percentage of survey sites from which

each insect or rust pathogen was collected and the percentage of times each insect or

rust species was collected from each site was calculated and used to determine the

scores described above. All phytophagous insects and the rust pathogens collected

from all sites over the three-year period were arranged according to the sampling

season (January�March; April�June; July�September; and October�December). The

incidence and proportion of survey sites from which each insect and rust pathogen

was collected in each quarter was also calculated. This information was used to score

seasonal incidence for all phytophagous insects and rust pathogens.

One way-ANOVA and t-tests were used to compare the number of phytophagous

insect species collected from sites between states, between districts and between sites

with different combinations of A. nilotica subspecies. Regression analysis was used to

study the relationship between the number of times each site was surveyed and the

number of agents collected at each site. All analyses were performed using SigmaStat

3.5. All results in the text are presented as means9standard error.


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Results

Phytophagous insects and plant pathogens

A total of 33 species of phytophagous insects were collected over three years (2008�2011) in southern India (Table 2). These included 16 leaf-feeders, eight stem-feeders,

four species with leaf-feeding adults and root-feeding larvae, two stem-borers and

bark-feeders and three flower-feeders. Species-level identification was made for 28

insects (Table 2). Two rust fungi (Ravanelia acacia-arabicae Mundk. & Thirum and

Ravanelia evansii Syd. & P.; Table 2) and six other fungal plant pathogens

(Ganoderma spp., Fusarium solani (Mart.) Sacc., Lasiodiplodia theobromae (Pat.)

Griffon & Maubl., Fomes spp., Rhizoctonia solani J.G. Kuhn, Phellinus fastuosus

(Lev.) Ryv.) were also collected on prickly acacia from southern India. The average

number of species recorded at each survey site differed significantly between various

districts (F17,54�1.898; P�0.039), but the difference was not significant between

Tamil Nadu (10.490.6) and Karnataka (10.191.3) states (t�0.217, df�70, P�0.829). The number of species recorded at each survey site varied significantly

depending on the number of times the site was surveyed (F7,54�8.45; PB0.001) and

the number of species collected in each survey site increased with the increase in the

number of times the site was surveyed (Figure 1). There was no significant difference

in the number of phytophagous insects and rust fungi collected from survey sites with

subsp. cupressiformis alone (14.790.88), with subsp. indica alone (10.590.89), with

subsp. indica�cupressiformis (8.591.06) and with subsp. indica�tomentosa (10.39

0.67; F3,69�0.939; P�0.424).

Geographic range and seasonal incidence

There was a significant variation in the percentage of survey sites from where various

insects and rust fungi were observed over the three-year period (F30, 341�16.59;

PB0.001). The scale insect Anomalococcus indicus Ramakrishna Ayyar (Hemiptera:

Lecanodiaspidae) was the most widespread, occurring in 100% of the survey sites

throughout the year (Table 2). Severe infestations of A. indicus (Figure 2) caused

defoliation, wilting and death of affected branches or the entire tree. Other agents

that are distributed widely and occur throughout the year include Dereodus

denticollis Boheman (Coleoptera: Curculionidae), Eumeta crameri (Westwood)

(Lepidoptera: Psychidae), Isturgia disputaria (Guenee) (Lepidoptera: Geometridae),

Phycita sp. A. (Lepidoptera: Pyralidae), Oxyrhachis tarandus Fab. (Hemiptera:

Membracidae), R. acacia-arabicae Mundk. & Thirum (Uredinales: Raveneliaceae)

and Pachnephorus sp. (Coleoptera: Chrysomelidae) (Table 2). Phycita sp. A. causedsevere defoliation in young and mature trees throughout the year. Defoliation by

I. disputaria was observed in all survey sites, predominantly from September to

January (Table 2), coinciding with the north-east monsoon. For other insects, their

distribution was limited, or they were only active seasonally, or they caused only

minor feeding damage (Table 2). Phycita sp. ‘B’ collected from only 38% of the

survey sites was active only during three to six months in a year (Table 2).

The gall rust R. acaciae-arabicae was observed in 68% of the survey sites

(Table 2). It produces uredinia and telia on leaflets, predominately on the upper

surface. Associated spermogonia and aecia occur on fruits, inflorescences and shoot

tips, causing hypertrophy that result in galls (Figure 3). Rust infection on leaves


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Table 2. Feeding habits, geographical range (mean9standard error) and seasonal incidence (mean9standard error) of phytophagous insects and rust

fungi catalogued on prickly acacia in southern India.

Seasonal incidence � 2008�2011 (% sites with agent)

Agent species Order: Family

Feeding

habit

Geographic

range

(% sites

with agent)

January�March

April�June

July�September

October�December

Insects

Anomalococcus indicus

Ramakrishna Ayyar

Hemiptera: Laecanodiaspidae Stem 10090.0 7795.5 6997.2 5895. 4 7096.2

Nippococcus sp. Hemiptera: Pseudococcidae Stem 1996.7 593.0 1195.8 291. 6 791.4

Paracoccus marginatus Williams

& Granara de Willink.

Hemiptera: Pseudococcidae Stem 993.5 291.3 191.3 492.1 191.3

Oxyrhachis tarandus Fab. Hemiptera: Membracidae Stem 7798.7 5293.9 4396.1 48911.1 5197.7

Homoeocerus signatus Walker Hemiptera: Coreidae Stem 6196.8 1995.9 15910.9 1791.2 1792.1

Chrysocoris purpureus

(Westwood)

Hemiptera: Scutelleridae Stem 1698.9 491.5 190.9 190.9 891.0

Ledra mutica Fab. Hemiptera: Cicadellidae Leaf 4198.3 690.6 190.7 593.5 692.2

Flata ferrugata (Fab.) Hemiptera: Flatidae Leaf 3598.2 1492.7 593.3 1094.8 893.5

Phycita sp. A Lepidoptera: Pyralidae Leaf 7695.7 3792.7 2295.2 2395.3 4296.3

Phycita sp. B Lepidoptera: Pyralidae Leaf 34910.1 894.8 1296.9 793.3 1295.6

Isturgia disputaria (Guenee) Lepidoptera: Geometridae Leaf 8297.2 3497.2 4695.0 4695. 2 5297.6

Ascotis infixaria Walker Lepidoptera: Geometridae Leaf 1297.2 2 91.5 0.0 290.9 691.5

Hyposidra successaria Walker Lepidoptera: Geometridae Leaf 2398.9 590.9 190.3 291.5 792.5

Selepa celtis Moore Lepidoptera: Noctuidae Leaf 6698.9 3091.5 17910.6 26912. 4 2792.5

Steblote siva (Lefebvre) Lepidoptera: Lasiocampidae Stem/bark 6496.2 3194.5 1996.7 1795 .0 2494.5

Euproctis scintillans Walk. Lepidoptera: Lymantridae Leaf 2894.0 1092.4 1296.7 891.6 1691.9

Euproctis lutana Walk. Lepidoptera: Lymantridae Leaf 993.8 390.6 2 91.0 491.5 290.9

Dasychira mentosa (Hubner) Lepidoptera: Lymantridae Leaf 5298.4 2293.9 1195.2 1596.7 2090.7

Inderbela quadrinotata Walker Lepidoptera: Metarbelidae Stem 4698.1 1291.5 995.3 690.8 891.9

Eumeta crameri (Westwood) Lepidoptera: Psychidae Leaf 9892.1 5698.3 55910.2 4891.0 4995.9

Pteroma plagiophleps Hampson Lepidoptera: Psychidae Leaf 5994.3 1691.9 23913.8 2293.3 1897.9

65

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Seasonal incidence � 2008�2011 (% sites with agent)

Agent species Order: Family

Feeding

habit

Geographic

range

(% sites

with agent)

January�March

April�June

July�September

October�December

Psiloptera fastuosa (Fab.) Coleoptera: Buprestidae Stem 491.9 190.3 290.9 290.3 0.0

Dereodus denticollis Boheman Coleoptera: Curculionidae Leaf/root 7697.1 3599.6 5193.8 4297.6 4298.2

Dereodus mastos Herbst. Coleoptera: Curculionidae Leaf/root 1294.1 494.2 1692.8 2093.1 893.5

Hypolixus truncatulus (Fab.) Coleoptera: Curculionidae Leaf 2794.7 592.8 1299.9 391.5 391.4

Myllocerus spp. Coleoptera: Curculionidae Flower 7996.4 2995.8 3999.6 2994.9 3995.6

Cryptocephalus sp. Coleoptera: Chrysomelidae Leaf 34910.1 0.0 291.5 592.8 1296.1

Pachnephorus sp. Coleoptera: Chrysomelidae Leaf/root 62910.8 40912.3 3797.1 4897.7 36910.5

Diapromorpha truncatulus Fab. Coleoptera: Chrysomelidae Leaf/root 2395.9 13 96.1 493.8 791.1 1495.7

Clyda succinata Lacord Coleoptera: Chrysomelidae Leaf 4098.6 1395.5 996.1 15913.5 893.3

Oxcetonia versicolor (Fab.) Coleoptera: Scarabaeidae Flower 893.2 191.4 592.8 191.2 190.5

Mylabris sp. Coleoptera: Meloidea Flower 1094.9 0.0 492.5 2293.3 190.5

Sthenias sp. Coleoptera: Cerambycidae Stem/bark 4499.1 190.7 0.0 290.6 391.5

Rust fungi

Ravanelia acacia-arabicae

Mundk. & Thirumalachari

Uredinales: Raveneliaceae Stem/leaf/

fruit

7094.4 3598.1 35917.4 3995.5 43915.8

Ravenelia evansii Syd. & P. Uredinales: Raveneliaceae Leaf 66�4.3 2795.2 1195.5 895.2 1494.8

Bio

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resulted in premature yellowing and leaf shedding. No seed development occurred

from galled fruits or inflorescences, and galling in shoot tips arrested the shoot

development. The spermogonial and aecial stages are found from December to

March, whereas the uredinia and telia are found during most of the year. The leaf

rust R. evansii (Uredinales: Raveneliaceae) was recorded in all sites with R. acaciae-

arabicae, often co-occurring along with telial stages of R. acaciae-arabicae. In the

northwest India, the leaf rust was collected from four sites (Nadiad, Tarapur, Talala

and Veraval) in Gujarat, but not in Rajasthan. In the field, only uredinia and telia

were observed on the upper leaflet surface.

n = 3

n = 13

n = 19

n = 13

n = 12

n = 4

n =5 n = 3

y = 9.0713Ln(x) – 0.566

R2 = 0.8901

0

5

10

15

20

25

30

0 5 10 15 20 25

No. of times surveyed

No.

of a

gent

s co

llect

ed

Figure 1. Relationship between the number of times each site was surveyed and the number of

agents recorded (mean9standard error) at the survey sites over a three-year period.

Figure 2. The scale insect (A. indicus) encrusting Acacia nilotica subsp. indica stem.


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Field host range

Twenty of the 33 insect species collected during the survey were either known crop

pests or polyphagous insects (Table 3). Eight species of insects (A. indicus, Phycita sp.

‘A’, Phycita sp. ‘B’, I. disputaria, D. denticollis, Dereodus mastos Herbst.,

Pachnephorus sp. and Cryptocephalus sp.) and two rust fungi (R. acacia-arabicae

and R. evansii) were observed only on A. nilotica, and not on any non-target plants

co-occurring in the survey sites. Pachnephorus sp. and R. acacia-arabicae were

restricted to A. nilotica subsp. indica, while A. indicus, Phycita sp. ‘A’, Phycita sp. ‘B’,

I. disputaria, D. denticollis and D. mastos were observed on all three subspecies of

A. nilotica (indica, cupressiformis and hemispherica). However, Diapromorpha turcica

Fab., Clytra succincta Lacordaire, Hypolixus truncatulus (F.), Mylloceros spp,

Figure 3. Rust galls on Acacia nilotica subsp. indica caused by aecial stage of R. acaciae-

arabicae causing hypertrophy on leaf rachis (A), stem (B), and immature (C) and mature (D)

fruit pods.


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Table 3. Recorded and observed non-target host plant species of insects and rust pathogens

collected on prickly acacia in southern India.

Agent species Recorded and observed non-target hosts

Insects

A. indicus Acacia leucophilea (Roxb.) Willd., Vachellia farnesiana (L.) Willd., A.

catechu (L.) Willd., Oliv., Ziziphus mauritiana Lam., Piper nigrum L.

Nippococcus sp. Polyphagous crop pest

P. marginatus Polyphagous crop pest

O. tarandus A. planiferons Wight and Arn., A. tortilis Hayne, A. catechu (L.) Willd.,

Oliv., A. auriculiformias A.Cunn. ex Benth., Prosopis julifera (Sw.) DC.,

P. cineraria (L.) Druce. Leucaena leucocephala (Lam.) de Wit, Albizia

spp., Tectona grandis L.f., Tamarindus indica L., Cassia fistula L.,

Dalbergia latifolia Roxb., D. sissoo Roxb., Santalum album L., Morus

nigra L., Phyllanthus emblica L., Cassia spp., Ficus spp., Trewia nudiflora

L., Sesbania grandiflora (L.) Poiret. Azadirachta indica A. Juss. Ricinus

communis L., Z. mauritiana, Jatropha curcas L., Bauhinia purpurea L.

H. signatus P. julifera, L. leucocephala, Albizia spp., D. sissoo

C. purpureus A. auriculiformis, J. curcas, J. nana Dalzell & Gibson. Populus deltoides

W. Bartram ex Humphry Marshall. P. emblica, D. sissoo, Calotropis

procera (Aiton) W.T. Aiton.

L. mutica Mangifera indica L., S. album

F. ferrugata Vitis vinifera L.

Phycita sp. A NA

Phycita sp. B NA

I. disputaria Delonix regia (Boj. ex Hook.) Raf., A. tortilis. A. mearnsii De Wild.

A. infixaria T. grandis, Camellia sinensis (L.) Kuntze

H. successaria Ipomoea batatas (L.) Lam., Shorea robusta Roth., S. talura Roxb.

S. celtis A. catechu, Duabanga grandiflora (Roxb. ex DC.) Walpers. Morus alba

L., S. robusta, P. emblica, Solanum melongena L.

S. siva A. senegal Willd., A. tortilis, P. julifera, P. cineraria Z. mauritiana Albizia

spp., Moringa oleifera Lam., Colospermum mopane (Kirk ex Benth.) Kirk

ex J. Leon., T. indica, Psidium guajava L.

E. scintillans Polyphagous crop pest

E. lutana Polyphagous crop pest

D. mentosa Polyphagous crop pest

I. quadrinotata A. catechu, Punica granatum L., M. indica, M. oleifera, J. curcas.

E. crameri A. catechu, A. tortilis, Peltophorum pterocarpum (DC.) K. Heyne.

Casuarina equisetifolia L., Ailanthus spp., D. sissoo, T. indica.

P. plagiophleps S. album. T. indica Albizia falcataria (L.) Backer, Rhizophora mucronata

Lam., Paraserianthes falcataria (L.) Nielsen. D. regia, Cocos nucifera L.

P. fastuosa A. catechu, A. karroo Hayne. Terminalia arjuna (Roxb.) Wight & Arn., T.

grandis, Swietenia mahagoni (L.) Jacq.

D. denticollis NA

D. mastos Manilkara zapota

H. truncatulus Amaranthus spp., Ziziphus spp., D. sissoo

Myllocerus spp. A. catechu, P. julifera, L. leucocephala, Albizia spp.

Cryptocephalus

sp.

NA

Pachnephorus sp. NA

D. turcica A. catechu, L. leucocephala, Mikania micrantha H.B.K

C. succinata P. julifera, P. cineraria


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Nipaecoccus sp. were all found feeding on non-target A. planifrons Wight & Arn. andProsopis juliflora (Sw.) DC at the survey sites.

Agent prioritisation

Twenty species of insects that are known to be polyphagous and crop�pest insects;

and all plant pathogens (Ganoderma spp., F. solani (Mart.) Sacc., L. theobromae

(Pat.) Griffon & Maubl., Fomes spp., R. solani J.G. Kuhn, P. fastuosus (Lev.) Ryv.)

other than the two rust fungi (R. acacia-arabicae and R. evansii) were excluded from

priority list due to their wide host ranges. Based on host plant records, field host

specificity, geographic range, seasonal incidence and damage levels (Table 4), the

following agents have been prioritised in decreasing order for detailed host specificitytests in Australia (for insects) and UK (for rusts): A. indicus�Phycita sp. A�R.

acaciae-arabicae�D. denticollis�Phycita sp. B�R. evansii. Since the host specificity

tests for I. disputaria sourced from Africa, Pakistan and India have already been

completed, this agent was not included in the priority list.

Discussion

Plant genotype and climate matching identified India for exploration for biological

control agents for A. nilotica subsp. indica in arid inland regions of northern

Australia. Potential agents have been prioritised here for host specificity tests based

on ecological host range, native range distribution and potential impacts. Foreffective biological control of A. nilotica subsp. indica, seedlings and juveniles need to

be targeted (Kriticos, Brown, Radford, & Nicholas, 1999), using either leaf-feeding

agents or shoot feeding agents or a combination of both (Dhileepan, Lockett,

Robinson, & Pukallus, 2009). Hence, survey efforts on prickly acacia have focused

more on juvenile plants, and on leaf and stem feeding agents than on root and seed

feeding agents. Since Acacia is the largest genus (with over 950 endemic species) of

flowering plants in Australia (Orchard & Wilson, 2001), field host range was given

priority while prioritising potential agents for detailed host specificity testing.More than 70 species of insects have been reported on prickly acacia in India (e.g.

Pillai et al., 1995). In the current survey, only 33 species of insects have been

documented on prickly acacia. This was possibly due to restricted geographic range

(focusing on Tamil Nadu and Karnataka states in southern India) of the survey


Agent species Recorded and observed non-target hosts

O. versicolor Polyphagous crop pest

Mylabris sp. P. julifera

Sthenias sp. NA

Rust fungi

R. acacia-

arabicae

NA

R. evansii A. sieberiana DC., A. macrothyrsa Harms., A. gerrardii Benth., A.

rehmanniana Schinz., A. robusta Burch., A. seyal Del. (all in Africa)

NA, not available.


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Table 4. Scores for prioritisation of potential biological control agents for prickly acacia from

southern India. For scoring criteria, refer to materials and methods.

Agent species

Host

plant

records

Field

host

range

Geographic

range

Seasonal

incidence

Damage

levels

Priority

score

Priority

rank

Insects

A. indicus 4 5 5 5 5 20 1

Nippococcus

sp.

0 1

P. marginatus 0

O. tarandus 1 1

H. signatus 1 1

C. purpureus 0

L. mutica 0 0

F. ferrugata 0

Phycita sp. A NA 5 5 5 4 19 2

Phycita sp. B NA 5 2 2 4 13 6

I. disputaria 3 4 3 3 2 12 Agent

rejecteda

A. infixaria 0

H. successaria 0

S. celtis 0

S. siva 2 2

E. scintillans 0

E. lutana 0

D. mentosa 0

I. quadrinotata 0

E. crameri 0

P. plagiophleps 1

P. fastuosa 0

D. denticollis 5 5 5 4 1 15 4

D. mastos 0

H. truncatulus 0

Myllocerus

spp.

0

Cryptocephalus

sp.

NA 3 2 2 1 8 Nil

Pachnephorus

sp.

NA 5 4 3 2 14 5

D. turcica 2 1

C. succinata 3 1

O. versicolor 0

Mylabris sp. 0 1

Sthenias sp. NA NA 2 1 1 4 Nil

Rust fungi

R. acacia-

arabicae

5 5 4 4 3 16 3

R. evansii 3 5 2 1 2 10 7

NA, not available.aBased on earlier no-choice host specificity tests conducted under quarantine in Australia using insectsfrom Pakistan, Kenya and India (Palmer, 2004).


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efforts. Likewise, more than 15 species of plant pathogens have been reported on

prickly acacia in India (e.g. Dwivedi, 1993). In this study, we recorded only a limited

number of plant pathogens, as our survey efforts have focused mainly on rust fungi.

Not all the insects, mites and pathogens collected during the survey could be

identified due to scarce taxonomic expertise, but it does appear that there is little

overlap, particularly for prioritised species, with those collected from north-western

India recently and Pakistan (Mohyuddin, 1986). It is therefore likely that a distinct,different groups of insects and rusts may be encountered in central (Chhattisgarh,

Maharashtra and Madhya Pradesh) and northern (Uttar Pradesh, Bihar and

Jharkhand) states of India, where such surveys have not been done. All the insect

species prioritised from India so far as potential biological control agents are from

southern India. This was possibly due to more species in the southern India than in

the north-western India, which in turn may be the result of more rigorous and

systematic survey efforts in southern India than in the north-western India. This is

further supported by the positive relationship between the number of species

recorded and number of times the site was surveyed (Figure 1). Several of the

lepidopterans (e.g. Phycita spp.), coleopterans (e.g. Pachnephorus sp., Sthenias sp.,

Myllocerus sp., Mylabris sp., Cryptocephalus sp.) and hemipterans (e.g. Nipaecoccus

sp.) could not be identified to species level thus making it difficult to search for their

host records. So, prioritisation of agents has been mainly based on their field host

range. More emphasis was given to shoot feeding agents, which are not present in

Australia, since A. nilotica subsp. indica is susceptible to shoot herbivory (Dhileepan

et al., 2009).The scale insect (A. indicus), the only shoot-feeding agent that showed specificity

for A. nilotica in the field, was widely distributed, active throughout the year and

caused severe damage to A. nilotica in the field. It is native to the Indian

subcontinent and has been reported as a pest of A. nilotica in India (Pillai et al.,

1995) and Bangladesh (Baksha & Islam, 1996). A. indicus has been reported on

Vachelliaa farnesiana (L.) Willd., A. leucophloea (Ben-Dov, 2006), Acacia catechu (L.)

Willd. Oliv., Ziziphus mauritiana Lam. (Beeson, 1941) and Piper nigrum L. (Koya,

Devasahayam, Selvakumaran, & Kalli, 1996). However, in a no-choice host

specificity tests using potted test plants, no crawler establishment or nymphal

development of the scale insect occurred on A. farnesiana, Acacia auriculiformis,

Acacia planiferons, A. leucophloea, A. catechu or P. nigrum (Balu et al., 2012,

unpublished data). During the field surveys in southern India, the scale insect

was observed only on A. nilotica, and not on other previously reported hosts

(A. farnesiana, A. leucophloea, A. catechu, Z. mauritiana and P. nigrum). Hence, the

scale insect was prioritised for host specificity tests. The scale insect was imported

into quarantine in Australia in January 2011 and detailed host specificity tests are inprogress. Other shoot feeding insects collected during the survey [e.g. Steblote siva

(Lefebvre), O. tarandus Fab., Acalolepta cervina (Hope) and Inderbela quadrinotata

Wlk.] are polyphagous.

Among the leaf-feeding insects, Phycita sp. A, Phycita sp. B, I. disputaria,

Pachnephorus sp. and D. denticollis have been prioritised. For Phycita sp. A, it was

difficult to determine potential non-target species at risk from literature searches

due to uncertainty regarding its taxonomy. Hence, based on field host range, native

geographic range, seasonal incidence and field defoliation levels in India, Phycita

sp. A was imported into a quarantine facility in Australia in January 2011


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for detailed host specificity tests. The geometrid I. disputaria, a major pest of

A. nilotica in India, has been recorded on Acacia tortilis, Acacia mollissima and

Acacia decurrens in Africa (Kruger, 2001). This agent was included in the list of

prioritised agents in view of its field host specificity, wide geographic range, activity

throughout the year and damage potential in India. Based on earlier no-choice

host specificity tests of the leaf-feeding geometrid (I. disputaria) from Pakistan,

Kenya and India, conducted under quarantine in Australia (Palmer, 2004), this

agent was not tested further. Among the other leaf-feeding insects, D. turcica Fab.

has been reported on other hosts like Mikania micrantha Kunth ex H.B.K.

(Abraham, Abraham, & Joy, 2002), Leucaena leucocephala (Lam.) de Wit (Nair,

2001), Lagerstroemia sp. (David & Ananthakrishan, 2004) and A. catechu (Beeson,

1919). Adults of C. succincta Lacordaire have been reported feeding on leaves of

Prosopis cineraria (L.) Druce in India (Verma, 1985). However, host record

searches were not possible for insects not identified to species (e.g. Phycita spp.,

Pachnephorus sp., Cryptocephalus sp., Sthenias sp. and Nipaecoccus sp.). Among

the remaining insects, D. denticollis has been reported only on A. nilotica in India.

The leaf-weevil (D. denticollis) insect was imported into quarantine in Australia in

November 2012.

All plant pathogens [Ganoderma spp., F. solani (Mart.) Sacc., L. theobromae

(Pat.) Griffon & Maubl., Fomes spp., R. solani J.G. Kuhn, Phellinus fastuosus (Lev.)

Ryv.] other than the two rust fungi (R. acacia-arabicae and R. evansii) were also

excluded due to their wide host range records (e.g. Bakshi, 1971; Dwivedi, 1993).

The gall-rust (R. acaciae-arabicae) was originally described by Mundkur and

Thirumalachar (1946) on A. nilotica (misapplied syn A. arabica Willd.) from

Mysore, Karnataka state in India. Later, Kapoor and Agarwal (1974) and

Bagyanarayana and Ravinder (1988) treated R. acaciae-arabicae, as a synonym

of R. evansii. In Africa, R. evansii has been reported from A. sieberiana DC.,

A. macrothyrsa Harms, A. gerrardii Benth., A. rehmanniana Schinz, A. robusta

Burch. and A. seyal Delile (Cannon, 2008). After recent surveys in India, Shivas,

Balu, Singh, Ahmed, and Dhileepan (2013) showed that the two rusts, R. acaciae-

arabicae and R. evansii, were distinct species that could be easily separated by

morphology of the urediniospores. The two rust species were exported to CABI

(UK) from India in 2010. Host-range testing using both urediniospore and aecidial

spore accessions of R. acaciae-arabicae from Tamil Nadu, India and uredinospore

accessions of R. evansii from Tamil Nadu and Gujarat, India, under quarantine

conditions at CABI UK, revealed that both rust species infected and produced

viable and infective urediniospores on an Australian native species, Acacia

sutherlandii (F. Mueller) F. Mueller (Seier, Ellison, Corta, Day, & Dhileepan,

2013). Although sporulation on A. sutherlandii by both rusts were always

accompanied by dark necrotic lesions, indicating that this non-target species is

not a natural host, the risks posed by both rust species to Australian acacias, in

particular A. sutherlandii, that grow sympatrically with the target weed in Australia

(Seier et al., 2013), are unacceptably high and hence no further work on the two

rusts has been pursued.


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Acknowledgements

The authors thank M. Senthilkumar, Mrs Mahalakshimi (Institute of Forest Genetics and TreeBreeding, Coimbatore, Tamil Nadu, India), Syed Irfan Ahmed, Sangeeta Singh, K.K.Srivastava, Mahadeo Gorin and Anamika Sharma (Arid Forest Research Institute, Jodhpur,Rajasthan, India) for the field surveys; N. Krishnakumar (Director, IFGTB, Coimbatore,India) and T.S. Rathore (Director, AFRI, Jodhpur, India) for the facilities; Bill Palmer, S.Raghu and Dane Panetta for comments on earlier versions of the manuscript; and Meat &Livestock Australia for funding the study. They also thank the Indian Council of ForestryResearch and Education for providing permission to run this collaborative research project inIndia. They are grateful to V.V. Ramamurthy (Indian Agricultural Research Institute, NewDelhi), Mathew George (Kerala Forest Research Institute, India), S.K. Gupta (ZoologicalSurvey of India, Kolkata); Thomas Simonsen, Kevin Tuck Marion, John Chainey, SharonShute (British Natural History Museum); Marion Seier, Harry Evans (CABI, UK); LaurenceMound (CSIRO Entomology, Canberra) for identification of various insects, mites and rustspecies collected during this study.

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Survey and prioritisation of potential biological control agents for prickly acacia (Acacia nilotica subsp. indica) in southern India

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