Life history of Anomalococcus indicus (Hemiptera: Lecanodiaspididae), a potential biological control agent for prickly acacia Vachellia nilotica ssp. indica in Australia

Babul scale Anomalococcus indicus Ramakrishna Ayyar, a major pest of Vachellia nilotica (L.f.) P.J.H. Hurter & Mabb. on the Indian subcontinent, has been identified as a potential biocontrol agent for prickly acacia V. nilotica subsp. indica (Benth.) Kyal. & Boatwr. in Australia and was imported from southern India for detailed assessment. The life history of A. indicus under controlled glasshouse conditions was determined as a part of this assessment. Consistent with other scale species, A. indicus has a distinct sexual dimorphism which becomes apparent during the second instar. Females have three instars, developing into sexually mature nymphs after 52 days. The generation time from egg to egg was 89 days. Females are ovoviviparous, ovipositing mature eggs into a cavity underneath their body. An average of 802 ± 114 offspring were produced per female. Reproductive output was closely associated with female size; larger females produced more than 1200 offspring. Crawlers emerged from beneath the female after an indeterminate period of inactivity. They have the only life stage at which A. indicus can disperse, though the majority settle close to their parent female forming aggregative distributions. In the absence of food, most crawlers died within three days. Males took 62 days to develop through five instars. Unlike females, males underwent complete metamorphosis. Adult males were small and winged, and lived for less than a day. Parthenogenesis was not observed in females excluded from males. The life history of A. indicus allows it to complement other biological control agents already established on prickly acacia in Australia.     

A systematic approach to biological control agent exploration and prioritisation for prickly acacia (Acacia nilotica ssp. indica)

Abstract  Agent selection for prickly acacia has been largely dictated by logistics and host specificity. Given that detailed ecological information is available on this species in Australia, we propose that it is possible to select agents based on agent efficacy and desired impact on prickly acacia demography. We propose to use the 'plant genotype' and 'climatic' similarities as filters to identify areas for future agent exploration; and plant response to herbivory and field host range as 'predictive' filters for agent prioritisation. Adopting such a systematic method that incorporates knowledge from plant population ecology and plant–herbivore interactions makes agent selection decisions explicit and allow more rigorous evaluations of agent performance and better understanding of success and failure of agents in weed biological control.     

Localization of feeding of Anomalococcus indicus (Hemiptera: Lecanodiaspididae) and supplementary biological notes: towards the biological management of the invasive tree Vachellia nilotica indica (Fabales: Mimosoideae) in North-Eastern Australia

Summary. Management of the invasive Vachellia nilotica indica infesting tropical grasslands of Northern Australia has remained unsuccessful to date. Presently Anomalococcus indicus is considered a potential agent in the biological management of V. n. indica. Whereas generic biological details of A. indicus have been known, their feeding activity and details of their mouthparts and the sensory structures that are associated with their feeding action are not known. This paper provides details of those gaps. Nymphal instars I and II feed on cortical-parenchyma cells of young stems of V. n. indica, whereas nymphal instars III and adult females feed on phloem elements of older shoots. Nymphal instars and adults (females) trigger stress symptoms in the feeding tissue with cells bearing enlarged and disfigured nuclei, cytoplasmic shrinkage, cytoplasmic trabeculae, abnormal protuberances and uneven cell wall thickening, unusual cell membrane proliferation, and exhausted and necrosed cells. Continuous nutrient extraction by A. indicus can cause stem death. We provide evidence that A. indicus, by virtue of its continuous feeding activity and intense population build up, can be an effective biological-management agent to regulate populations of V. n. indica in infested areas.     

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

Prickly acacia, Acacia nilotica subsp. indica (Benth.) Brenan (Mimosaceae), a multi-purpose tree native to the Indian subcontinent, is a weed of national significance, widespread throughout the grazing areas of western Queensland and has the potential to spread throughout northern Australia. Biological control of prickly acacia has been in progress since the early 1980s, but with limited success to date. Based on genetic and climate matching studies, native surveys for potential biological control agents were conducted in 64 sites in Tamil Nadu state and 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) and two rust fungi. The number of species recorded at survey sites increased with the number of times the sites were surveyed. Using a scoring system based on field host range, geographic range, seasonal incidence and damage levels, we prioritised a scale insect (Anomalococcus indicus Ramakrishna Ayyar), two leaf-webbing caterpillars (Phycita sp. A and Phycita sp. B), a leaf weevil (Dereodus denticollis Boheman), 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 for preliminary host-specificity testing. Three insects (A. indicus, D. denticollis and Phycita sp. A) were imported into a quarantine facility in Brisbane, Australia where host-specificity tests are in progress.     

Implications of the changing phylogenetic relationships of Acacia s.l. on the biological control of Vachellia nilotica ssp. indica in Australia

Plant relationships have implications for many fields including weed biological control. The use of DNA sequencing and new tree building algorithms since the late 1980s and early 1990s have revolutionised plant classification and has resulted in many changes to previously accepted taxonomic relationships. It is critical that biological control researchers stay abreast of changes to plant phylogenies. One of the largest plant genera, Acacia, has undergone great change over the past 20 years and these changes have ramifications for weed biological control projects in a number of countries. Vachellia nilotica (prickly acacia) is a major weed in Australia, originating from the Indian subcontinent and Asia, and it has been a target for biological control since 1980. Once a member of Acacia, a large (>1,000 spp.) and iconic group in Australia, prickly acacia is now part of the genus Vachellia. Current knowledge suggests that Vachellia is more closely related to mimosoid genera than it is to Acacia s.s. There has also been a recent reclassification of legume subfamilies with subfamily Mimosoideae now part of subfamily Caesalpinioideae, and four new subfamilies. In this paper we review the changes that have occurred to this group since the prickly acacia biological control project began and discuss the implications for the project. A new host test list for quarantine testing is proposed. Developed following the modernisation of the centrifugal‐phylogenetic method, it is shorter than past lists, containing 46 species, although still lengthy because of the expectations of regulatory bodies, which are slower to accept advances in scientific knowledge. The list includes five Vachellia species, six “Mimoseae” species and 26 Acacia species. The number species from legume subfamilies other than the new Caesalpinioideae is greatly reduced.     

Life cycle and host range of Phycita sp. rejected for biological control of prickly acacia in Australia

Prickly acacia (Vachellia nilotica subsp. indica), a native of the Indian subcontinent, is a serious weed of the grazing areas of northern Australia and is a target for classical biological control. Native range surveys in India identified a leaf webber, Phycita sp. (Lepidoptera: Pyralidae) as a prospective biological control agent for prickly acacia. In this study, we report the life cycle and host‐specificity test results Phycita sp. and highlight the contradictory results between the no‐choice tests in India and Australia and the field host range in India. In no‐choice tests in India and Australia, Phycita sp. completed development on two of 11 and 16 of 27 non‐target test plant species, respectively. Although Phycita sp. fed and completed development on two non‐target test plant species (Vachellia planifrons and V. leucophloea) in no‐choice tests in India, there was no evidence of the insect on the two non‐target test plant species in the field. Our contention is that oviposition behaviour could be the key mechanism in host selection of Phycita sp., resulting in its incidence only on prickly acacia in India. This is supported by paired oviposition choice tests involving three test plant species (Acacia baileyana, A. mearnsii and A. deanei) in quarantine in Australia, where eggs were laid only on prickly acacia. However, in paired oviposition choice trials, only few eggs were laid, making the results unreliable. Although oviposition choice tests suggest that prickly acacia is the most preferred and natural host, difficulties in conducting choice oviposition tests with fully grown trees under quarantine conditions in Australia and the logistic difficulties of conducting open‐field tests with fully grown native Australian plants in India have led to rejection of Phycita sp. as a potential biological control agent for prickly acacia in Australia.     

Biology and host specificity ofWeiseana barkeri (Col.: Chrysomelidae): A biological control agent forAcacia nilotica (mimosaceae)

The leaf-feeding beetleWeiseana barkeri Jacoby feeds onAcacia nilotica (L.) Willdenow ex Delile in Kenya. Host specificity tests show it is host specific toA. nilotica and approval has been given for its field release in northwest Queensland. A novel rearing and host specificity-testing technique is reported whereA. nilotica foliage stimulates oviposition into strips of corrugated cardboard.     

Preliminary host specificity testing of Endophyllum osteospermi (Uredinales, Pucciniaceae), a biological control agent against Chrysanthemoides monilifera ssp. monilifera

Chrysanthemoides monilifera ssp. monilifera, indigenous to the Western Cape Province of South Africa, is a serious invader of native vegetation in south-eastern Australia. The rust fungus Endophyllum osteospermi causes witches' brooms on C. monilifera ssp. monilifera in South Africa, and is associated with a reduction in growth and seed production of its host under natural conditions, as well as mortality of severely infected bushes. This rust fungus is considered to be a potential biological control agent for use against C. monilifera ssp. monilifera in Australia. Endophyllum osteospermi has a long latent period, typically between 6 and 24 months between infection and the initiation of witches' brooms. This long latent period makes the logistics of doing traditional host specificity testing, in which all test plant species are inoculated and observed for symptom development, unfeasible for this rust fungus. Germination of aecidioid teliospores and penetration by basidiospores were observed on the surface of excised leaves of 32 test plant species at 4 days after inoculation, and compared to that on C. monilifera ssp. monilifera. Germinating aecidioid teliospores aborted on 14 test plant species, whilst no penetration was attempted on a further 12 test plant species. Penetration only occurred on nine of the 32 test plant species, in addition to C. monilifera ssp. monilifera. Inoculating whole plants of nine selected test plant species confirmed the above results. Therefore, only the test plant species in which penetration occurred, or at least was attempted, need to undergo comprehensive host specificity testing. Pending these results, E. osteospermi may be suitable for release in Australia for the biological control of C. monilifera ssp. monilifera.     

The host range of four new biotypes of Dactylopius tomentosus (Hemiptera: Dactylopiidae) from southern USA and their potential as biological control agents of Cylindropuntia spp. (Cactaceae) in Australia: Part II

Eight Cylindropuntia species have naturalised in Australia and pose serious economic, environmental and social impacts. The host range of four additional biotypes of D. tomentosus from southern USA was investigated. Feeding and development were restricted to the genus Cylindropuntia. However, they showed differences in specificity within this genus and some biotypes discriminated between the provenances of Cylindropuntia rosea and Cylindropuntia tunicata. Efficacy trials were conducted to determine whether populations of each biotype could be sustained on the naturalised Cylindropuntia species and if these populations could retard the growth or kill these plants. The ‘acanthocarpa’ biotype offers potential control of C. rosea (Lorne Station), while the ‘cylindropuntia sp.’ biotype shows great potential to control C. rosea (Grawin). The ‘cylindropuntia sp.’ biotype also had a high impact on Cylindropuntia kleiniae and Cylindropuntia imbricata, and a moderate impact on Cylindropuntia leptocaulis and Cylindropuntia prolifera. The ‘acanthocarpa?×?echinocarpa’ biotype had its greatest impact on C. tunicata (Grawin), killing this plant in 18 weeks. A fourth biotype, ‘leptocaulis’, was damaging to some species, but was less effective than the other biotypes. Cylindropuntia spinosior is the only naturalised species in Australia where no effective biocontrol agent has been found.     

Biology and host specificity of Aulacobaris fallax (Coleoptera: Curculionidae), a potential biological control agent for dyer’s woad,Isatis tinctoria (Brassicaceae) in North America

Dyer’s woad, Isatis tinctoria, a plant of Eurasian origin is a problematic weed in western North America against which a classical biological weed control programme was initiated in 2004. Three European insect species were selected as candidate agents to control this invasive species, including the root‐mining weevil Aulacobaris fallax. To determine its suitability as an agent, the biology and host specificity of A. fallax were studied in outdoor plots and in the field between 2004 and 2006 in its native European range. Aulacobaris fallax is a univoltine species that lays its eggs from March to August into leaf stalks and roots of dyer’s woad. Larvae mine and pupate in the roots and adults emerge from August to October. Up to 62% of the dyer’s woad plants at the field sites investigated were attacked by this weevil. In no‐choice host‐specificity tests, A. fallax attacked 16 out of 39 species and varieties within the Family Brassicaceae. Twelve of these are native to North America. In subsequent multiple‐choice tests, seven species, all native to North America, suffered a similar level of attack as dyer’s woad, while none of the European species were attacked. Our results demonstrate the importance of including test plant species that have not co‐evolved with the respective candidate agent. In sum, we conclude that the risk of non‐target effects is too high for A. fallax to be considered as a biological control agent for dyer’s woad in the United States.     

Life history and host range of Sauris nr. purpurotincta,an unsuitable biological control agent for Chinese tallowtree

Foreign surveys in China discovered a defoliating insect species feeding on the leaves of Chinese tallowtree (Triadica sebifera), an invasive weed of the southeastern U.S.A. The life history of this species, Sauris nr. purpurotincta (Lepidoptera: Geometridae), was examined and larval no-choice and adult multiple-choice host range tests were conducted in quarantine to evaluate their suitability for biological control of Chinese tallowtree. The results indicated that the larvae have five instars and require approximately 22 days to complete development to the adult stage. Host range tests indicated that the larvae could not feed and complete development on most species tested. However, 40% of the larvae survived when fed leaves of Hippomane mancinella, a state-listed endangered species in Florida, and all larvae survived when fed Morella cerifera, a common native species of the southeastern U.S.A. Multiple-choice oviposition tests indicated eggs were laid on leaves of both a south Florida native plant Gymnanthes lucida and Chinese tallowtree. Considering this broad host range, this species will not be considered further for biological control of Chinese tallowtree in the U.S.A.     

Observations on the host specificity and biology of Lixus salsolae (Col., Curculionidae), a potential biological control agent of Russian thistle, Salsola tragus (Chenopodiaceae) in North America

Abstract:  No-choice host specificity tests were performed on Lixus salsolae Becker (Col., Curculionidae) in a quarantine green house near Montpellier, France. Several varieties of seven species of economic and ornamental plants from six genera of Chenopodiaceae were tested. Adult feeding was observed on almost all test plants and larvae successfully developed on nine of the eleven species/varieties tested. Sex ratio of field-collected overwintering adults was close to 1 : 1. While no-choice tests may indicate a wider host range under field conditions, we no longer consider L. salsolae as a potential biological control agent of Salsola tragus L. (Chenopodiaceae) in North America.     

Biology and host range of Ophiomyia camarae Spencer (Diptera: Agromyzidae), a potential biocontrol agent for Lantana spp. (Verbenaceae) in Australia

The life history and host range of the herringbone leaf-mining fly Ophiomyia camarae, a potential biological control agent for Lantana spp., were investigated. Eggs were deposited singly on the underside of leaves. Although several eggs can be laid on a single leaf and a maximum of three individual mines were seen on a single leaf, only one pupa per leaf ever developed. The generation time (egg to adult) was about 38 days. Females (mean 14 days) lived longer than males (mean 9 days) and produced about 61 mines. Oviposition and larval development occurred on all five lantana phenotypes tested. Eleven plant species representing six families were tested to determine the host range. Oviposition and larval development occurred on only lantana and another nonnative plant Lippia alba (Verbenaceae), with both species supporting populations over several generations. A CLIMEX model showed that most of the coastal areas of eastern Australia south to 30°16′ S (Coffs Harbour) would be suitable for O. camarae. O. camarae was approved for release in Australia in October 2007 and mines have been observed on plants at numerous field sites along the coast following releases.     

Life history and host range of Alagoasa extrema (Coleoptera: Chrysomelidae: Alticinae), a potential biological control agent of Lantana spp. (Verbenaceae) in Australia

The life history and host range of the lantana beetle, Alagoasa extrema, a potential biocontrol agent for Lantana spp. were investigated in a quarantine unit at the Alan Fletcher Research Station, Brisbane, Australia. Adults feed on leaves and females lay batches of about 17 eggs on the soil surface around the stems of plants. The eggs take 16 days to hatch and newly emerged larvae move up the stem to feed on young leaves. Larvae feed for about 23 days and there are three instars. There is a prepupal non-feeding stage that lasts about 12 days and the pupal stage, which occurs in a cocoon in the soil, lasts 16 days. Teneral adults remain in the cocoon for 3 days to harden prior to emergence. Males live for about 151 days while females live for about 127 days. The pre-oviposition period is 19 days. In no-choice larval feeding trials, nine plant species, representing three families, supported development to adult. Three species, Aloysia triphylla, Citharexylum spinosum and Pandorea pandorana were able to support at least two successive generations. These results confirm those reported in South Africa and suggest that A. extrema is not sufficiently specific for release in Australia. Furthermore, it is not recommended for release in any other country which is considering biological control of lantana.     

Post-establishment assessment of host plant specificity of Arytainilla spartiophila (Hemiptera: Psyllidae), an adventive biological control agent of Scotch broom,Cytisus scoparius

Scotch broom, Cytisus scoparius (Fabaceae), is a shrub native to Europe that is invasive in the USA, New Zealand and Australia. The psyllid Arytainilla spartiophila has been purposely introduced to Australia and New Zealand as a biological control agent of C. scoparius, but is an accidental introduction to California. Lupines (Lupinus spp.) are the closest native taxon to Cytisus in North America, and are therefore considered to be at the highest risk for non-target damage. However, because no lupines are native to Australia or New Zealand, only one imported forage species was evaluated during prior host specificity testing. We conducted a laboratory nymphal transfer experiment, a field choice experiment and a field survey to assess risk to three lupine species (Lupinus albifrons, Lupinus bicolor and Lupinus formosus). In the laboratory, 20% of third-instar nymphs were able to develop to adulthood on L. formosus but not on the other lupine species, while 40% completed development on C. scoparius. In the field experiment, potted lupine and C. scoparius plants were placed beside large infested C. scoparius plants; oviposition occurred on all the potted C. scoparius plants, but on none of the lupines. In the field survey, no A. spartiophila eggs or nymphs were found on naturally occurring lupines growing adjacent to infested C. scoparius. The results indicate that A. spartiophila is not likely to damage or reproduce on lupines in the field. This study provides an example of how field studies can help clarify the host specificity of biological control agents.     

Host specificity testing,release and establishment of Urophora solstitialis (L.) (Diptera: Tephritidae), a potential biological control agent for Carduus nutans L., in Australia

The seed‐fly Urophora solstitialis was imported into Australia from southern France. Previous workers had shown that this seed‐fly limited its attack to selected members of the genus Carduus. Host specificity studies revealed that no native Australian plant tested from the family Asteraceae was a suitable host plant. Permission to release the fly was granted, and it was released in three regions of the New South Wales tablelands. The fly underwent a second generation at two of the release sites, and reasons for its failure to do so at the third are suggested. It has successfully established itself in all three regions, having completed a full seasonal cycle in the field.     

Gallerucida bifasciata (Coleoptera: Chrysomelidae), a potential biological control agent for Japanese knotweed (Fallopia japonica)

Host specificity of foreign natural enemies are becoming more and more critical in classical biological control programs, as concerns about potential risk from introduced biocontrol agents have been increasing recently. Understanding the insect's fundamental and ecological host ranges is the first step in determining the potential for introduction of an insect to control invasive plants. Japanese knotweed, Fallopia japonica (Houttuyn) Ronse Decraene (Polygonaceae) is an invasive weed in the United States and Europe. A leaf beetle, Gallerucida bifasciata (Coleoptera: Chrysomelidae) is an important natural enemy attacking this plant in Asia. However, its host range records were ambiguous. This study examined the beetle's host specificity through a set of choice and no-choice tests in the laboratory and field in its native China. Gallerucida bifasciata larvae were able to complete development on seven of 87 plant species in larval development tests, while adults fed and oviposited on 10 plants in no-choice tests. Multiple choice tests showed adults strongly preferred Fallopia japonica, Persicaria perfoliata (L.) H. Gross and Polygonum multiflorum Thunb over all other plants. Open field tests and field surveys further revealed that these three species were in its ecological host range. The results of this study suggest that G. bifasciata is a potential promising agent for control of Japanese knotweed in the United States and Europe, although additional host specificity tests and risk assessment should be completed.     

Life history and host range of Oxydia vesulia transpeneus,an unsuitable biological control agent of Brazilian peppertree

The suitability of Oxydia vesulia transpeneus (Cramer) (Lepidoptera: Geometridae) was assessed as a potential biological control agent of the invasive weed Brazilian Peppertree Schinus terebinthifolia Raddi. Larvae were collected in Brazil feeding on the plant in its native range and colonised in quarantine where life history and host range studies were conducted (27?±?2°C; 50RH). Development time from neonate to adults when fed Brazilian peppertree leaves was 48.0 (±2.2) days for females and 51.0 (±1.3) days for males. Larvae generally required five (occasionally six) instars to reach the adult stage. Females had greater pupal weights 1004.1 (±45.9) mg compared with males 668.5 (±19.7) mg. Larvae were tested on seven non-target plant species from Florida natives, ornamentals, to economic species. Larvae completed development on all but one of these valued plant species. These results suggest that the host range of O. vesulia is not sufficiently specific for release as a biological control against Brazilian peppertree in the USA.     

The biology and host specificity of the onion weed rust, Puccinia barbeyi, a potentially useful agent for biological control in Australia

Onion weed, Asphodelus fistulosus L., (Liliaceae) a weed of Mediterranean and Middle Eastern origin is widespread in southern Australia where it invades pastures making them unsuitable for grazing. A program of research is underway to discover natural enemies of this plant and to study their possible role in the biological control of onion weed. A rust fungus Puccinia barbeyi (Roum.) Magnus has been found to severely attack A. fistulosus . Observations on the biology of the rust confirmed that it is monoecious and microcyclic and multiplied essentially by aecial and telial stages, although occasionally urediniospores also appeared among teliospores. Several members of the Liliaceae exposed to the aeciospores of the rust remained unattacked indicating that it is most probably specific to Asphodelus spp. and thus its potential for the biological control of A. fistulosus in Australia should be studied further.     

Host specificity ofPareuchaetes insulata (Lep.: Arctiidae), a biological control agent forChromolaena odorata (Compositae)

Larvae of the arctiid moth,Pareuchaetes insulata, from Florida fed on the leaves ofChromolaena odorata, a serious composite, alien weed in Natal, South Africa. In starvation test trials using 48 plant species,P. insulata completed its development onC. odorata andAgeratum houstonianum. Subsequent attempts to cultureP. insulata on these two plants was only successful onC. odorata. The biology ofP. insulata is similar to that of two other well studiedPareuchaetes species namelyP. pseudoinsulata andP. aurata aurata. Repeated defoliation ofC. odorata byP. insulata could contribute to its control as has been found withP. pseudoinsulata in Guam.Pareuchaetes insulata has been approved for release as a biological control agent ofC. odorata in South Africa.