Improving the agent selection, release and evaluation process: the role of bioclimatic modelling

The value of CLIMEX models to inform biocontrol programs was assessed, including predicting the potential distribution of biocontrol agents and their subsequent population dynamics, using bioclimatic models for the weed Parkinsonia aculeata, two Lantana camara biocontrol agents, and five Mimosa pigra biocontrol agents. The results showed the contribution of data types to CLIMEX models and the capacity of these models to inform and improve the selection, release and post release evaluation of biocontrol agents. Foremost among these was the quality of spatial and temporal information as well as the extent to which overseas range data samples the species’ climatic envelope. Post hoc evaluation and refinement of these models requires improved long-term monitoring of introduced agents and their dynamics at well selected study sites. The authors described the findings of these case studies, highlighted their implications, and considered how to incorporate models effectively into biocontrol programs.

Will biological control of Lantana camara ever succeed? Patterns, processes & prospects

Despite biocontrol research spanning over 100 years, the hybrid weed, commonly referred to as Lantana camara, is not under adequate control. Host specificity and varietal preference of released agents, climatic suitability of a region for released agents, number of agents introduced and range or area of infestation appear to play a role in limiting biocontrol success. At least one of 41 species of mainly leaf- or flower-feeding insects has been introduced, or spread, to 41 of the 70 countries or regions where lantana occurs. Over half (26) of these species have established, achieving varying levels of herbivory and presumably some degree of control. Accurate taxonomy of the plant and adaptation of potential agents to the host plant are some of the better predictors of at least establishment success. Retrospective analysis of the hosts of introduced biocontrol agents for L. camara show that a greater proportion of agents that were collected from L. camara or Lantana urticifolia established, than agents that were collected from other species of Lantana. Of the introduced agents that had established and were oligophagous, 18 out of 22 established. The proportion of species establishing, declined with the number of species introduced. However, there was no trend when oceanic islands were treated separately from mainland areas and the result is likely an artefact of how introductions have changed over time. A calculated index of the degree of herbivory due to agents known to have caused some damage per country, was not related to land area infested with lantana for mainlands nor for oceanic islands. However, the degree of herbivory is much higher on islands than mainlands. This difference between island and mainland situations may reflect population dynamics in patchy or metapopulation landscapes. Basic systematic studies of the host remain crucial to successful biocontrol, especially of hybrid weeds like L. camara. Potential biocontrol agents should be monophages collected from the most closely related species to the target weed or be phytophages that attack several species of lantana. Suitable agents should be released in the most ideal ecoclimatic area. Since collection of biocontrol agents has been limited to a fraction of the known number of phytophagous species available, biocontrol may be improved by targeting insects that feed on stems and roots, as well as the agents that feed on leaves and flowers.

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.

Scat contents of the spotted-tailed quoll Dasyurus maculatus in the New England gorges, north-eastern New South Wales

In 1313 scats of the spotted-tailed quoll Dasyurus maculatus, collected over 5 years from the gorge country of north-eastern New South Wales, the most frequent and abundant items were derived from mammals and a restricted set of insect orders. These quolls also ate river-associated items: waterbirds, eels, crayfish, aquatic molluscs and even frogs. Macropods contributed most of the mammal items, with possums, gliders and rodents also being common. Some food, particularly from macropods and lagomorphs, had been scavenged (as shown by fly larvae). The most frequent invertebrates were three orders of generally large insects Coleoptera, Hemiptera and Orthoptera, which were most frequent in summer and almost absent in winter scats. Monthly mean numbers of rodent and small dasyurid items per scat were inversely related to these large insects in scats. The numbers of reptile items were inversely related to the numbers of mammal (especially arboreal and small terrestrial mammal) items per scat, thus types of items interacted in their occurrences in monthly scat samples. Frequencies of most vertebrate items showed no seasonal, but much year-to-year, variation. This quoll population ate four main types of items, each requiring different skills to obtain: they hunted arboreal marsupials (possibly up trees), terrestrial small mammals and reptiles (on the ground), and seasonally available large insects (on trees or the ground), and scavenged carcases, mostly of large mammals but also birds and fishes (wherever they could find them).

Specificity of Carvalhotingis visenda (Hemiptera: Tingidae) as a biological control agent for cat's claw creeper Macfadyena unguis-cati (Bignoniaceae) in Australia

Biological control is considered the most suitable management option for cat's claw creeper, Macfadyena unguis-cati, a major environmental weed in coastal and sub-coastal areas of Queensland and New South Wales, Australia. The potential host range of the leaf-sucking bug, Carvalhotingis visenda (Hemiptera: Tingidae) was evaluated on the basis of nymphal survival and development, adult feeding and survival, and oviposition preference using choice and no-choice tests involving 38 plant species in 10 families. In no-choice tests, although adults survived on a few of the non-target plants, no eggs were laid on any of the non-target plants. In no-choice condition, the tingid oviposits and completes nymphal development only on M. unguis-cati. There was also no visible feeding damage on any of the non-target plants. In choice tests, adults showed distinct preference for M. unguis-cati, and the preference level increased over time as the tingids moved away from the non-target plants. At the end of the trial no adults were evident on any of the non-target plants. Host specificity tests confirm that the tingid is a highly host specific biocontrol agent, and does not pose risk to any non-target plants in Australia. This agent has been approved for field release by the relevant regulatory authorities in Australia.

The host range and biology of Cometaster pyrula; a biocontrol agent for Acacia nilotica subsp. indica in Australia

Prickly acacia, Acacia nilotica subsp. indica (Benth.) Brenan, a major weed of the Mitchell Grass Downs of northern Queensland, Australia, has been the target of biological control projects since the 1980s. The leaf-feeding caterpillar Cometaster pyrula (Hopffer) was collected from Acacia nilotica subsp. kraussiana (Benth.) Brenan during surveys in South Africa to find suitable biological control agents, recognised as a potential agent, and shipped into a quarantine facility in Australia. Cometaster pyrula has a life cycle of approximately 2 months during which time the larvae feed voraciously and reach 6 cm in length. Female moths oviposit a mean of 339 eggs. When presented with cut foliage of 77 plant species, unfed neonates survived for 7 days on only Acacia nilotica subsp. indica and Acacia nilotica subsp. kraussiana. When unfed neonates were placed on potted plants of 14 plant species, all larvae except those on Acacia nilotica subsp. indica and Acacia nilotica subsp. kraussiana died within 10 days of placement. Cometaster pyrula was considered to be highly host specific and safe to release in Australia. Permission to release C. pyrula in Australia was obtained and the insect was first released in north Queensland in October 2004. The ecoclimatic model CLIMEX indicated that coastal Queensland was climatically suitable for this insect but that inland areas were only marginally suitable.

Susceptibility of source plants to sugarcane Fiji disease virus influences the acquisition and transmission of the virus by the planthopper vector Perkinsiella saccharicida

Fiji leaf gall (FLG) caused by Sugarcane Fiji disease virus (SCFDV) is transmitted by the planthopper Perkinsiella saccharicida. FLG is managed through the identification and exploitation of plant resistance. The glasshouse-based resistance screening produced inconsistent transmission results and the factors responsible for that are not known. A series of glasshouse trials conducted over a 2-year period was compared to identify the factors responsible for the erratic transmission results. SCFDV transmission was greater when the virus was acquired by the vector from a cultivar that was susceptible to the virus than when the virus was acquired from a resistant cultivar. Virus acquisition by the vector was also greater when the vector was exposed to the susceptible cultivars than when exposed to the resistant cultivar. Results suggest that the variation in transmission levels is due to variation in susceptibility of sugarcane cultivars to SCFDV used for virus acquisition by the vector.

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

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.

Temporal patterns in incidence and abundance of Aconophora compressa (Hemiptera: Membracidae), a biological control agent for Lantana camara, on target and nontarget plants

The membracid Aconophora compressa Walker, a biological control agent released in 1995 to control Lantana camara (Verbenaceae) in Australia, has since been collected on several nontarget plant species. Our survey suggests that sustained populations of A. compressa are found only on the introduced nontarget ornamental Citharexylum spinosum (Verbenaceae) and the target weed L. camara. It is found on other nontarget plant species only when populations on C. spinosum and L. camara are high, suggesting that the presence of populations on nontarget species may be a spill-over effect. Some of the incidence and abundance on nontarget plants could have been anticipated from host specificity studies done on this agent before release, whereas others could not. This raises important issues about predicting risks posed by weed biological control agents and the need for long-term postintroduction monitoring on nontarget species.

Maximising the contribution of native-range studies towards the identification and prioritisation of weed biocontrol agents

Effective study in the native range to identify potential agents underpins all efforts in classical biological control of weeds. Good agents that demonstrate both a high degree of host specificity and the potential to be damaging are a very limited resource and must therefore be carefully studied and considered. The overseas component is often operationally difficult and expensive but can contribute considerably more than a list of herbivores attacking a particular target. While the principles underlying this foreign component have been understood for some time, recently developed technologies and methods can make very significant contributions to foreign studies. Molecular and genetic characterisations of both target weed and agent organism can be increasingly employed to more accurately define the identity and phylogeny of them. Climate matching and modelling software is now available and can be utilised to better select agents for particular regions of concern. Relational databases can store collection information for analysis and future enquiry while quantification of sampling effort, employment of statistical survey methods and analysis by techniques such as rarefaction curves contribute to efficient and effective searching. Obtaining good and timely identifications for discovered agent organisms is perhaps the most serious issue confronting the modern explorer. The diminishing numbers of specialist taxonomists employed at the major museums while international and national protocols demand higher standards of identity exacerbates the issue. Genetic barcoding may provide a very useful tool to overcome this problem. Native-range work also offers under-exploited opportunities for contributing towards predicting safety, abundance and efficacy of potential agents in their target environment.

Local dispersion and damage of Corymbia citriodora subsp. variegata (Myrtaceae) regrowth by eriophyid mites (Acari: Eriophyoidea).

Eriophyid mites (Acari: Eriophyoidea: Eriophyidae: Rhombacus sp. and Acalox ptychocarpi Keifer) are recently-emerged pests of commercial eucalypt plantations in subtropical Australia. They cause severe blistering, necrosis and leaf loss to Corymbia citriodora subsp. variegata (F. Muell.) K.D. Hill & L.A.S. Johnson, one of the region's most important hardwood plantation species. In this study we examine the progression, incidence and severity of these damage symptoms. We also measure within-branch colonisation by mites to identify dispersive stages, and estimate the relative abundance of the two co-occurring species. Rhombacus sp., an undescribed species, was numerically dominant, accounting for over 90% of all adult mites. Adults were the dispersive stage, moving mostly within branches, but 12% of recruitment onto new leaves occurred on previously uninfested branches. Damage incidence and severity were correlated, while older leaves had more damage than younger leaves. "Patch-type" damage was less frequent but was associated with higher mite numbers and damage scores than "spot-type" damage, while leaf discoloration symptoms related mostly to leaf age.

The host range of Isturgia deeraria, an insect considered for the biological control of Acacia nilotica in Australia

The geometrid caterpillar Isturgia deerraria was imported from Kenya into quarantine facilities in Australia as a potential biological control agent for prickly acacia, Acacia nilotica subsp. indica (Benth.) Brenan (family Mimosaceae). The insect was then tested on 30 plant species presented to neonate larvae as a no-choice cut foliage test and 13 plant species presented as a no-choice potted plant test. In these tests the insect was able to complete its life cycle on 13 native Acacia spp. and also on Acacia farnesiana and the exotic ornamental Delonix regia (family Caesalpiniaceae). The tests supported field observations that the insect has a host range spanning many leguminous species and as such the insect could not be considered for release in Australia.

Metabolite mobilization in the stem galls of Parthenium hysterophorus induced by Epiblema strenuana inferred from the signatures of isotopic carbon and nitrogen and concentrations of total non-structural carbohydrates

Parthenium hysterophorus L. (Asteraceae) is a weed of national significance in Australia. Among the several arthropod agents introduced into Australia to control populations of P. hysterophorus biologically, Epiblema strenuana Walker (Lepidoptera: Tortricidae) is the most widespread and abundant agent. By intercepting the normal transport mechanisms of P. hysterophorus, the larvae of E. strenuana drain nutrients, other metabolic products, and energy, and place the host plant under intense metabolic stress. In this study, determinations of total non-structural carbohydrates (TNC) levels and carbon and nitrogen isotope ratios of fixed products in different parts of the plant tissue, including the gall, have been made to establish the function of gall as a sink for the nutrients. Values of δ13C and δ15N in galls were significantly different than those in proximal and distal stems, whereas the TNC levels were insignificant, when measured in the total population of P. hysterophorus, regardless of plant age. However, carbon, nitrogen, and TNC signatures presented significant results, when assayed in different developmental stages of P. hysterophorus. Carbon isotope ratios in galls were consistently more negative than those from the compared plant organs. Nitrogen isotope ratios in galls, on the contrary, were either similar to or less negative than the compared plant organs, especially within a single host-plant stage population (i.e., either rosette, preflowering, or flowering stage). TNC levels varied within compared plant populations. The stem distal to the gall functioned more efficiently as a nodal channel than the stem proximal to the gall, especially in the translocation of nitrogenous nutrients. Our findings indicate that the gall induced by E. strenuana functions as a sink for the assayed nutrients, although some variations have been observed in the patterns of nutrient mobilization. By creating a sink for the nutrients in the gall, E. strenuana is able to place the overall plant metabolism under stress, and this ability indicates E. strenuana has the necessary potential for use as a biological-control agent.