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.     

Prioritising potential guilds of specialist herbivores as biological control agents for prickly acacia through simulated herbivory

Understanding plant response to herbivory facilitates the prioritisation of guilds of specialist herbivores as biological control agents based on their potential impacts. Prickly acacia ( Acacia nilotica ssp. indica ) is a weed of national significance in Australia and is a target for biological control. Information on the susceptibility of prickly acacia to herbivory is limited, and there is no information available on the plant organ (i.e. leaf, shoot and root in isolation or in combination) most susceptible to herbivory. We evaluated the ability of prickly acacia seedlings, to respond to different types of simulated herbivory (defoliation, shoot damage, root damage and combinations), at varying frequencies (no herbivory, single, two and three events of herbivory) to identify the type and frequency of herbivory that will be required to reduce the growth and vigour. Defoliation and shoot damage, individually, had a significant negative impact on prickly acacia seedlings. For the defoliation to be effective, more than two defoliation events were required, whereas a single bout of shoot damage was enough to cause a significant reduction in plant vigour. A combination of defoliation + shoot damage had the greatest negative impact. The study highlights the need to prioritise specialist leaf and shoot herbivores as potential biological control agents for prickly acacia.     

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.     

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.     

Prioritisation of potential agents for the biological control of the invasive alien weed,Pereskia aculeata (Cactaceae), in South Africa

Pereskia aculeata Miller (Cactaceae) is an invasive alien species in South Africa that is native in Central and South America. In South Africa, P. aculeata outcompetes native plant species leading to a reduction in biodiversity at infested sites. Herbicidal and mechanical control of the plant is ineffective and unsustainable, so biological control is considered the only potential solution. Climatic matching and genotype matching indicated that the most appropriate regions in which to collect biological control agents were Santa Catarina and Rio de Janeiro provinces in Southern Brazil. Surveys throughout the native distribution resulted in 15 natural enemy species that were associated with the plant. Field host range data, as well as previous host plant records, were used to prioritise which of the species were most likely to be suitably host specific for release in South Africa. The mode of damage was used to determine which species were most likely to be damaging and effective if released. The most promising species prioritised for further study, including host specificity and impact studies, were the stem-wilter Catorhintha schaffneri Brailovsky & Garcia (Coreidae); the stem boring species Acanthodoxus machacalis Martins & Monné (Cerambycidae), Cryptorhynchus sp. (Curculionidae) and Maracayia chlorisalis (Walker) (Crambidae) and the fruit galler Asphondylia sp. (Cecidomyiidae). By prioritising the potential biological control agents that are most likely to be host-specific and damaging, the risk of conducting host specificity testing on unsuitable or ineffective biological control agents is reduced.     

Modeling the potential global distribution of suitable habitat for the biological control agent Heterorhabditis indica

Entomopathogenic nematode (EPN) Heterorhabditis indica is a promising biocontrol candidate. Despite the acknowledged importance of EPN in pest control, no extensive data sets or maps have been developed on their distribution at global level. This study is the first attempt to generate Ecological Niche Models (ENM) for H. indica and its global Habitat Suitability Map (HSM) for H. indica to generate biogeographical information and predicts its global geographical range and help identify of prospective areas for its exploration and to help identify the suitable release areas for biocontrol purpose. The aim of the modeling exercise was to access the influence of temperature and soil moisture on the biogeographical patterns of H. indica at the global level. Global Heterorhabditis indica ecosystems. CLIMEX software was used to model the distribution of H. indica and assess the influence of environmental variable on its global distribution. In total, 162 records of H. indica occurrence from 27 countries over 25 years were combined to generate the known distribution data. The model was further fine‐tuned using the direct experimental observations of the H. indica''s growth response to temperature and soil moisture. Model predicts that much of the tropics and subtropics have suitable climatic conditions for H. indica. It further predicts that H. indica distribution can extend into warmer temperate climates. Examination of the model output, predictions maps at a global level indicate that H. indica distribution may be limited by cold stress, heat stress, and dry stresses in different areas. However, cold stress appears to be the major limiting factor. This study highlighted an efficient way to construct HSM for EPN potentially useful in the search/release of target species in new locations. The study showed that H. indica which is known as warm adapted EPN generally found in tropics and subtropics can potentially establish itself in warmer temperate climates as well. The model can also be used to decide the release timing of EPN by adjusting with season for maximum growth. The model developed in this study clearly identified the value and potential of Habitat Suitability Map (HSM) in planning of future surveys and application of H. indica.     

Diversity and impact of herbivorous insects on Brazilian peppertree in Florida prior to release of exotic biological control agents

Brazilian peppertree, Schinus terebinthifolia Raddi (Anacardiaceae), is a South American plant that is highly invasive in Florida. The impact of insect herbivores on the performance of Brazilian peppertree was evaluated at two locations in Florida using an insecticide exclusion method. Although 38 species of insect herbivores were collected on the invasive tree, there were no differences in growth or reproductive output of insecticide protected and unprotected trees, providing evidence that insect feeding had no measurable impact on tree performance. The majority of insects collected on Brazilian peppertree were generalists, and several were serious agricultural pests.     

Prioritizing areas in the native range of hygrophila for surveys to collect biological control agents

Native to Southeast Asia, Hygrophila polysperma is an invasive aquatic weed of lotic habitats in the southern United States and Mexico. An increase in the number of water bodies invaded by hygrophila since 1990 suggests that current methods employed to control this weed are inadequate. Classical biological control may be a viable option for long term regulation of hygrophila in the invaded range. In this study, we used the Maximum Entropy Species Distribution Model (MaxEnt) to prioritize climatically suitable native habitats in India and Bangladesh for conducting exploratory surveys to collect biological control agents. In total, 164 point occurrences from the United States and Mexico and 20 predictor variables, including 19 bioclimatic variables and altitude, were used to predict the native distribution of hygrophila. Performance of the model was statistically verified using threshold dependent binomial tests and area under the curve (AUC) score of the receiver operating characteristic (ROC) curve plot. The results showed that the model performed significantly better than random in both binomial tests and AUC analyses. High suitability of occurrence of hygrophila was predicted in the northeastern region of India and northern and eastern parts of Bangladesh. Based on percent omission of known native occurrences, a color-coded final distribution map was prepared to prioritize areas for conducting future surveys. Our study proposes a technique that can be useful for prioritizing areas in native ranges for exploratory surveys to collect biological control agents.     

Exploration for native parasitoids of Asian longhorned beetle in China as prospective biological control agents

1. Native to China and the Korean Peninsula, the Asian longhorned beetle (ALB) Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae) is a high-risk invasive pest of hardwood trees.
2. To explore the potential of biological control of ALB in the United States, we conducted surveys of ALB parasitoids using sentinel logs in five geographical regions (Beijing, Gansu, Guizhou, Shanghai, and Yunnan) in China from 2019 to 2022.
3. Seven hymenopteran larval parasitoid species, Bracon planitibiae Yang, Eurytoma chinensis Yang, Heydenia sp., Oxysychus glabripennis Yang, Sclerodermus guani Xiao et Wu, Spathius anoplophorae Yang, and Zolotarewskya anoplophorae Yang, were collected in Beijing. Four, three and two of these species were also found in Shanghai, Guizhou, and Yunnan, respectively. No parasitoid was found in Gansu.
4. Mean parasitism rates by all parasitoid species were 3.6%–15.8% in Beijing, 1.4%–16.4% in Guizhou, 1.6%–7.1% in Shanghai, and 5.8% in Yunnan.
5. Spathius anoplophorae and O. glabripennis were the two most dominant parasitoids collected consistently in the four different regions and may be considered as prospective agents for biological control introduction against ALB in the United States.
6. We discuss some underlying ecological mechanisms that might contribute to the rarity of egg parasitoids and future opportunities and challenges for biological control of ALB.

     

Control of Pseudophilothrips ichini (Thysanoptera: Phlaeothripidae) with acephate to exclude a biological control agent of Schinus terebinthifolia

Post-release monitoring of biological control agents to determine impact on the target weed has recently received increased priority. Several methods are available to measure the impact of a biological control agent by manipulating the agent population while measuring fitness of the weed. Brazilian peppertree, Schinus terebinthifolia is one of the most damaging weeds in subtropical areas of Florida and Hawaii. A biological control agent, the thrips, Pseudophilothrips ichini is a sap-feeder that shows high levels of specificity and causes severe distortion of leaf tips of the weed. Thrips populations of this species and a generalist thrips, the red banded thrips Selenothrips rubrocinctus were experimentally manipulated by applications of the systemic insecticide acephate by both foliar applications and by an inserted encapsulated formulation. Foliar applications protected plants against red banded thrips for 29 days and against the biological control thrips, P. ichini for 22 days after treatment. Control with inserts were initially low but was achieved after 60 days and this control continued for 182 days after treatment. Manipulation of these biological control thrips populations with foliar or inserted formulations will assist in the determination of biological control agent impact.     

The use of molecular assays to identify plant pathogenic organisms vectored by biological control agents

The planthopper Prokelisia marginata VanDuzee (Homoptera: Delphacidae) has beenconsidered for the biological control of theweed Spartina alterniflora Loisel(Poaceae) in Willapa Bay, Washington, U.S.A. Prokelisia marginata is a stenophagousphloem-feeding insect with the potential totransmit bacterial plant diseases that could bemoved by less-specific vectors to other plantspecies. Initial assays with PCR primers thatare putatively specific for phytoplasmas gavepositive results in Spartina. However,subsequent analyses did not indicate thetransmission of the pathogen by theplanthopper. We sequenced the 16S ribosomalRNA (rRNA) gene of the bacterial species thatgave positive results in PCR. Comparisons withsequences available in GenBank suggested thatthe positive results using the putativelyspecific PCR primers were due to the presenceof such bacteria as Pseudomonas, Holomonas, Vibrio, and Acinetobacter. We did not find phytoplasmasin either Spartina or the planthopperP. marginata.     

Effect of mechanical damage on emission of volatile organic compounds from plant leaves and implications for evaluation of host plant specificity of prospective biological control agents of weeds

Assessment of host plant specificity is a critical step in the evaluation of classical biological control agents of weeds which is necessary for avoiding possible damage to non-target plants. Volatile organic compounds (VOCs) emitted by plants likely play an important role in determining which plants attract and are accepted by a prospective arthropod agent. However, current methods to evaluate host plant specificity usually rely on empirical choice and no-choice behavioural experiments, with little knowledge about what chemical or physical attributes are stimulating the insect. We conducted experiments to measure the quantitative and qualitative effects on emission of VOCs caused by simple mechanical damage to leaves of plants known to differ in suitability and attractiveness to a prospective agent. More VOCs were detected from damaged than from undamaged leaves for all three species tested. Discriminant analysis was able to correctly distinguish the taxonomic identity of all plants based on their VOC profiles; however, the VOCs that discriminated species among undamaged leaves were completely different from those that discriminated among damaged leaves. Thus, damaged and undamaged plants present different VOC profiles to insects, which should be considered when conducting host plant specificity experiments. An unacceptable non-target plant, Centaurea cineraria, emitted all except one of the VOCs that were emitted by its preferred host plant, Centaurea solstitialis, indicating the importance of compounds that are repellant in host plant specificity. Centaurea cyanus emitted fewer VOCs than C. solstitialis, which suggests that it lacked some VOCs important for host plant recognition.     

Identification of priority areas in South America for exploration of natural enemies for classical biological control of Tetranychus evansi (Acari: Tetranychidae) in Africa

The red spider mite Tetranychus evansi Baker and Pritchard is a pest of tomato in East and Southern Africa. It is probably native to South America. Three models were established to identify priority areas for the search of natural enemies in South America for classical biological control of this pest in Africa. The models were based on the concept of “fundamental ecological niche”, predicting regions in South America that have similar environmental conditions to areas where the mite is a problem in Africa, using Desktop-GARP (Genetic Algorithm for Rule-set Production). Based on the model established with data sets from Kenya and Zimbabwe, it was determined that priority areas include areas in Brazil, Argentina, Paraguay and Uruguay, as well as some restricted areas in other South American countries.     

Comparisons of the thermal physiology of water hyacinth biological control agents: predicting establishment and distribution pre‐ and post‐release

Investigations into the thermal physiology of weed biological control agents may elucidate reasons for establishment failure following release. Such studies have shown that the success of water hyacinth biological control in South Africa remains variable in the high‐lying interior Highveld region, because the control agents are restricted to establishment and development due to extreme winter conditions. To determine the importance of thermal physiology studies, both pre‐ and post‐release, this study compared the known thermal requirements of Eccritotarsus catarinensis (Carvalho) (Hemiptera: Miridae) released in 1996, with those of an agent released in 1990, Niphograpta albiguttalis (Warren) (Lepidoptera: Pyralidae) and a candidate agent, Megamelus scutellaris Berg (Hemiptera: Delphacidae), which is currently under consideration for release. The lower developmental threshold (t_o) and rate of development (K) were determined for N. albiguttalis and M. scutellaris, using a reduced axis regression, and incorporated into a degree‐day model which compared the number of generations that E. catarinensis, N. albiguttalis, and M. scutellaris are capable of producing annually at any given site in South Africa. The degree‐day models predicted that N. albiguttalis (K = 439.43, t_o = 9.866) can complete 4–11 generations per year, whereas M. scutellaris (K =502.96, t_o = 11.458) can only complete 0–10 generations per year, compared with E. catarinensis (K = 342, t_o = 10.3) which is predicted to complete 3–14 generations per year. This suggests that the candidate agent, M. scutellaris, will not fare better in establishment than the other two agents that have been released in the Highveld, and that it may not be worth releasing an agent with higher thermal requirements than the agents that already occur in these high‐lying areas. Thermal physiology studies conducted prior to release are important tools in biological control programmes, particularly those in resource‐limited countries, to prevent wasting efforts in getting an agent established.