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.     

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.     

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.     

Isolation and characterization of microsatellite loci from Acacia nilotica ssp. indica (Mimosaceae)

Five microsatellite loci are presented for prickly acacia, Acacia nilotica ssp. indica (Benth.) Brenan, an introduced weed of national significance in Australia. These microsatellite loci were obtained through the construction of an enriched library and their use will enable us to determine the genetic origin and extent of genetic diversity of this weed in Australia.     

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

ABSTRACT

Prickly acacia, Vachellia nilotica ssp. indica (Benth.) Kyal. & Boatwr, is a significant weed of northern Australia and has been a target of weed biological control in Australia since the 1980s. Following native range surveys in India, the scale insect Anomalococcus indicus Ayyar was identified as the most promising agent and was imported into Australia for further research. A. indicus is a major pest of prickly acacia on the Indian subcontinent, where it causes shoot tip dieback and plant death. Despite field observations suggesting the species was specific to V. nilotica, A. indicus completed development on 17 of the 84 non-target plant species tested during no-choice host specificity trials under quarantine conditions. Of these, Acacia falcata, V. bidwillii, V. sutherlandii and Neptunia major supported high numbers of mature females in all replicates. All of these species were utilised in choice trials. Combined risk scores indicate that V. sutherlandii, N. major and A. falcata may be attacked in the field. Due to the limited ability of scale insects to disperse, only those non-target species that occur on the Mitchell grass downs (i.e. V. sutherlandii) are considered to be at risk. Nevertheless, in view of the disparity between quarantine test results and the observed field host specificity of A. indicus in India, field trials are currently being conducted in India using Australian native species on which complete development has occurred. The future of A. indicus as a biological control agent for prickly acacia in Australia will be determined once results from these field trials are known.     

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.     

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.     

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.     

Revision of the Pepila fuscomaculata species-group and description of four new species from Australia (Coleoptera: Chrysomelidae: Alticinae)

Abstract The Pepila fuscomaculata species-group from Australia, including P. fuscomaculata ( Baly 1877 ), P. hypocrita ( Blackburn 1896 ), P. submetallescens ( Baly 1877 ), P. tumbyensis ( Blackburn 1896 ), P. blackburni sp. n., P. brittoni sp. n., P. nikitini sp. n. and P. reidi sp. n., is analysed. A key to all the species is presented. Line drawings of male and female genitalia of all species are included. Brief ecological and zoogeographical data are also reported.     

大猿叶虫夏滞育的诱导：基于定量的光周期反应

为了探明大猿叶虫Colaphellus bowringi Baly夏滞育诱导的光周期时间测量特性, 我们通过室内实验系统比较了该虫在25℃、 不同长光照条件下,夏滞育的发生以及诱导50%个体进入夏滞育所需求的光 暗循环数。结果表明：不同长光照诱导的夏滞育比率有显著差异, 其中15 h或16 h光照诱导的滞育比率最高, 短于或长于这两个光照其滞育率均明显下降。在不同光 暗循环实验中, 14 h诱导的滞育比率均低于50%, 诱导50%个体进入夏滞育所需求的光 暗循环数在L15∶D9, L16∶D8, L17∶ D7和L18∶D6分别为2.61, 3.72, 4.64和5.92 d, 处理间存在显著差异。这些结果提示该虫夏滞育的诱导是基于定量的光周期反应。     

Effects of thermoperiods on diapause induction in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae)

Abstract. The effects of thermoperiods on diapause induction in continuous darkness or under a 12 : 12 h LD photoperiod were investigated in the cabbage beetle, Colaphellus bowringi Baly, a typical short‐day species. The diapause response curves both at different constant temperatures and at the thermocycle of format CT x: (24 ? x) h (16 : 28 °C) under continuously dark rearing conditions showed that the incidence of diapause depended mainly on whether or not the mean temperature was ≤20 °C or >20 °C. If the mean temperature was ≤20 °C, all individuals entered diapause; if >20 °C, the incidence of diapause declined gradually with increasing mean temperatures. The thermocycle (CT 12 : 12 h) with a series of different cryophases (8–22 °C) and thermophases (24–32 °C) under continuous darkness demonstrated a cryophase response threshold temperature of approximately 19 °C and a thermophase response threshold temperature of approximately 31 °C. Thermoperiodic amplitude (temperature difference between cryophase and thermophase) was shown to have a significant influence on diapause induction at the mean temperatures of 22, 23 and 24 °C, but not at ≥25 °C. Thermoperiodic responses under LD 12 : 12 h clearly showed that the incidence of diapause was influenced strongly by the photophase temperature. The thermoperiod under LD 12 : 12 h induced a much lower incidence of diapause than the thermoperiod with the same temperature in continuous darkness. The ecological significance of thermoperiodic induction of diapause in this species is discussed.     

Distribution, biology and host range of Rhembastus sp. (Coleoptera: Chrysomelidae), a candidate for the biological control of Bryophyllum delagoense (Crassulaceae) in Australia

The biology and host range of a leaf-beetle, Rhembastus sp. (Coleoptera: Chrysomelidae: Eumolpinae) from Madagascar, was studied under quarantine laboratory conditions in South Africa to determine its potential as a biological control agent of Bryophyllum delagoense (Ecklon & Zeyher) Schinz (Crassulaceae) in Australia. Favourable attributes of the beetle include relative ease of culturing, multiple generations per year, and high levels of damage inflicted by adults, which feed on the plantlets produced at the end of each leaf, and root feeding larvae. The adults therefore have an impact on the reproductive potential of the plant and larval feeding on the roots hampers the uptake of water and may even facilitate secondary infections by pathogens. Despite indications from field surveys in Madagascar that Rhembastus sp. has a narrow host range, preliminary no-choice and multiple-choice trials in quarantine revealed that it could complete its development on five non-target species in the family Crassulaceae. Extensive host range trials still have to be undertaken in Australia before the beetle can be considered for release.     

Larval parasitoids of Lilioceris lilii (Coleoptera:Chrysomelidae) in Sweden and potential for biological control

A survey of the parasitoid complex of lily leaf beetle (Lilioceris lilii) was conducted in Sweden from 2006 to 2007. Total parasitism varied between 21 and 57%. The most abundant parasitoids were the ichneumonids Lemophagus errabundus and L. pulcher and the eulophid Tetrastichus setifer. The potential for biological control is discussed.     

Introduction, Rearing, and Host Range of Aerenicopsis championi Bates (Coleoptera: Cerambycidae) for the Biological Control of Lantana camara L. in Australia

The biology and host range of the cerambycid beetle Aerenicopsis championi Bates, a potential biological control agent for the weed Lantana camara L., were studied. A. championi is a univoltine species associated with L. camara, L. urticifolia, and L. hirsuta in Mexico and Central America. In Mexico, adult emergence occurred in May and June at the start of the rainy season. Larvae fed within the stems over a 9- to 12-month period and caused damage to the plant. The insect was imported into Australia, where a procedure for rearing it in the laboratory was developed. Host-range tests indicated that adults oviposited and larvae commenced development in L. camara and L. montevidensis but not in any of 57 other species tested. A CLIMEX model indicated that most areas infested with lantana in Australia would have a favorable climate for A. championi. Permission to release this insect in Australia was obtained and three small releases were made in southern Queensland in February 1995.     

Field evaluation of entomopathogenic nematodes for biological control of striped flea beetle, Phyllotreta striolata (Coleoptera: Chrysomelidae)

The striped flea beetle, Phyllotreta striolata (F.) (Coleoptera: Chrysomelidae) is a key pest of crucifer vegetables in Southern China. The use of entomopathogenic nematodes (EPNs) within an integrated pest management approach may offer an effective and environmentally safe strategy to suppress outbreaks of this pest. In the present study, the efficacy of Steinernema carpocapsae All and Heterorhabditis indica LN2 for the control of P. striolata in the field was evaluated, as well as the combined application of EPNs and azadirachtin against the pest. Both nematode species were capable of reducing populations of the soil-dwelling stages of P. striolata, thus leading to a reduction of the adult populations and the associated shot-hole damage on the leaves. Nematode treatments also increased cabbage yields as compared to the control and azadirachtin treatments alone. Azadirachtin alone was not effective to prevent damage by P. striolata, but it could enhance the control effect of S. carpocapsae shortly after application. Osmotically treated infective juveniles (IJs) of S. carpocapsae All performed as well as untreated IJs.     

The role of photoperiod and temperature in determination of summer and winter diapause in the cabbage beetle,Colaphellus bowringi (Coleoptera: Chrysomelidae)

The cabbage beetle, Colaphellus bowringi, is a short-day species undergoing an imaginal summer and winter diapause. Its photoperiodic response highly depends on temperature. All adults entered diapause at ≤ 20 °C regardless of photoperiods. High temperatures strongly weakened the diapause-inducing effects of long daylengths. The diapause-averting influence of short daylengths was expressed only at high temperatures (above 20 °C). This indicates that the beetle has a cryptic ability to reproduce in summer. In fact, summer and winter diapause were induced principally by relatively low temperatures in the field, whereas photoperiod had less influence on diapause induction. The critical daylength for the autumnal population was between 12 h and 13 h. By transferring from a long day to a short day or vice versa at different times after hatching, it was shown that the sensitive stage with regard to photoperiod was the larva, whereas a long day was photoperiodically more potent than a short day. The sensitive stage to temperature encompassed the larval, pupal and adult stages. This different response pattern serves to ensure that the beetle enters summer and winter diapause in time. The selections for non-diapause trait under laboratory (at 25 °C) and natural conditions (at >24 °C) showed that the beetle could lose its sensitivity to photoperiod very rapidly.     

Drakensbergianella rudebecki, New Genus and New Species from the Mountains of Southern Africa, and Taxonomic Observations on Gabonia Jacoby and Related Genera (Insecta, Coleoptera, Chrysomelidae, Alticinae)

Drakensbergianella rudebecki, a new genus and new species of flea beetle (Chrysomelidae, Alticinae) found at high elevations from Southern Africa (Drakensberg mountains) is described. This new genus is closely related to the genus Gabonia Jacoby, 1893 but is easily distinguishable mainly by: the metasternum shorter than the length of the middle coxal cavities; the legs with femora and tibiae clearly elongate, especially the hind ones; the antennae generally longer than body in both sexes, especially in males; the metafemoral spring with inner side of the ventral lobe not angled; the metathoracic wings strongly reduced. Line drawings of male and female genitalia, metafemoral springs, and scanning electronic micrographs of particular morphological aspects of the taxa considered are provided. Finally, a brief discussion about Gabonia and related genera in the Afrotropical region with a key for the identification, is also reported. Moreover, the following new combination is proposed: Longitarsus ruandensis Weise, 1910 = Montiaphthona ruandensis Weise, 1910 n. comb.     

Minimum threshold for establishment and dispersal of Lilioceris cheni (Coleoptera: Chrysomelidae): a biological control agent of Dioscorea bulbifera

The successful establishment or failure of a new population is often attributed to propagule pressure, the combination of the number of independent introduction events, and the number of individuals released at each event. The design of optimal release strategies for biological control agents benefits from an understanding of the impact of propagule pressure on the species being released. The dispersal rate of individuals from nascent population foci can also affect establishment success. We assessed the minimum threshold for establishment and measured dispersal of Lilioceris cheni (Coleoptera: Chrysomelidae), a biological control agent for Dioscorea bulbifera (Dioscoreales), air potato. Replicated releases of 10, 50, and 100 adults of L. cheni were conducted on the east and west coasts of south Florida. Dispersal was measured from 19 of these sites plus 19 additional release locations in south and central Florida. Lilioceris cheni established populations from all three release sizes with no apparent influence of site location. Releases of 10, 50, and 100 adults resulted in 50%, 67%, and 85% establishment, respectively. Beetles dispersed an average of 1.41?±?0.515?km/yr. Dispersal distance was significantly affected by the time since release but not the number of individuals released. Our results suggest that future releases of 100 individuals could be spaced several kilometres apart on the landscape to facilitate rapid colonisation of D. bulbifera infestations.     

Rearing of two predators,Thanasimus dubius andTemnochila virescens, for the biological control ofIps grandicollis in Australia

Rearing methods for two coleopterous predators,Thanasimus dubius andTemnochila virescens, imported into Australia for the biological control ofIps grandicollis, were developed. Bionomic data obtained from laboratory rearings between 1982–1987 showed thatT. dubius eggs took about 7 days to hatch and that duration of the larval stage was about 42 days. Observations showed thatT. dubius had a prolonged prepupal stage (x=56.4 days, range 14–274 days), which was probably non-diapausal in nature. Mean adult longevity was 50 days (range 1–358 days).Temnochila virescens eggs took almost 9 days to hatch, and a lengthy larval stage (x=155.4 days, range 73–333 days) was observed. Mean duration of the pupal stage was 14 days (range 7–28 days). A long preoviposition period (x=141 days, range 47–206 days) was observed, and adults were very long-lived (x=232.7 days, range 14–667 days). Capacity for increase (r_c) calculated from rearing data suggested that numbers ofT. dubius could be increased faster thanT. virescens. Mortality between 1982–1987 averaged about 70% for both species. However, mortality ofT. dubius in 1987 increased significantly, suggesting that inbreeding or other methodological factors could be responsible. A mass-rearing method usingIps-infested pine billets was developed as a cheaper alternative to laboratory rearing, and was shown to be effective in producing large numbers of insects for release.