Weed Biocontrol Agents Research Articles

First record of Heterotrioza chenopodii (Reuter, 1876) (Hemiptera: Psylloidea: Triozidae) in Tunisia

AbstractThis is the first report of the psyllid species, Heterotrioza chenopodii (Reuter, 1876), in Tunisia. This species was collected in November 2019 on Chenopodium album growing in the greenhouse of the Higher School of Agriculture, Kef, Northwestern Tunisia. Elements of colouration of adults and immatures are reported in this paper and considerations about the use of this species as a weed biocontrol agent are discussed.

Accidental introduction of Candidatus Liberibacter europaeus into New Zealand via a weed biocontrol agent from the UK

The bacterium, Candidatus Liberibacter europaeus (Leu) was reported in New Zealand (NZ) in 2011 in Scotch broom, Cytisus scoparius Link, and its biocontrol agent, Arytainilla spartiophila Förster (Hemiptera: Psyllidae). The aim of the study was to investigate the pathway by which Leu arrived in NZ using a retrospective risk assessment of Leu being accidentally imported with the broom psyllids in the 1990s. We developed species-specific primers for Leu detection and carried out end-point and real-time PCR analyses for Leu in potential host plants and broom psyllids throughout NZ to test two hypotheses: 1) Leu was accidentally released in NZ in broom psyllids in 1993; or 2) Leu was present in NZ pre-1993, and maintained in cultivated plants via cuttings/grafting, or in wild Scotch broom populations via shared parasitic plants. There was strong evidence to support the arrival of Leu with broom psyllids in NZ. Firstly, methods used to import broom psyllids from the UK provided a likely pathway for inadvertent release of Leu, which at the time was unknown to science, into NZ. Secondly, Leu in NZ Scotch broom plants was significantly associated with the presence of broom psyllids, with Leu absent from plants at sites without psyllids. In contrast, there was no evidence suggesting Leu was present in NZ before the release of broom psyllids: Leu was not found in ornamental brooms or pears, Pyrus communis L. (a Leu host in Europe), and parasitic plants were too uncommon to maintain Leu in wild Scotch broom. In addition, Leu in UK Scotch broom and broom psyllids has a matching partial 16S sequence to NZ Leu. It remains uncertain whether Leu is pathogenic in Scotch broom, or symptomless as in pears. Unpredictable impacts of Ca. Liberibacter spp. in different plant species probably implies that psyllids considered as future weed biocontrol agents will need to be free of these potential plant pathogens. This accidental introduction of Candidatus Liberibacter europaeus into NZ via a weed biocontrol agent happened because detection methods for unculturable organisms were not developed at the time. Molecular characterisation of insect microbiomes could become an essential procedure for pre-release safety screening of biocontrol agents that are potential vectors of plant pathogens.

Locomotory responses to olfactory cues during host‐finding can inform environmental safety assessments of biological weed control agents

AbstractIn weed biological control programs, the safety assessment of an agent currently relies on no‐choice and choice feeding, development, and oviposition cage tests. However, confined conditions restrict insect behavior, potentially producing false positive host‐use results that can prematurely disqualify agents, reducing opportunities for successful weed biocontrol. To minimize risks of nontarget attack and maximize successful biocontrol outcomes, it is useful to investigate an agent’s pre‐contact responses to olfactory cues from target and nontarget plant species during host‐selection. Here, we tested how the locomotory behavior of the biocontrol agent Mogulones crucifer Pallas (Coleoptera: Curculionidae) differed when exposed to olfactory cues from its host, the invasive herbaceous Cynoglossum officinale L. (Boraginaceae), versus cues from closely related nontarget species. We used olfactometer behavioral assays, comparing M. crucifer responses to volatiles from C. officinale and nontarget plant species. We observed and measured the duration of resting and walking behaviors, as well as frequencies of arrestment or persisted resting, by M. crucifer in response to these odor sources. In total, 22 confamilial plant species were tested, including five species federally listed as threatened or endangered (T&E) in the USA. Mogulones crucifer consistently responded to C. officinale volatiles with greater duration of resting and frequencies of arrestment behavior compared to other plant species. In contrast, M. crucifer behavior was unaffected by odors of confamilials of C. officinale or responded with repellence to these odors in the olfactometer. These data suggest that in the invaded North American range, M. crucifer is unlikely to use nontarget olfactory cues to find or come into contact with tested nontarget plants, including the tested T&E species. Results from this study improve predictions of M. crucifer’s host‐use in the introduced range and illustrate the potential of this novel approach as a component of pre‐release environmental safety assessments of weed biocontrol agents.

The effects of intraspecific hybridization on the host specificity of a weed biocontrol agent

Hybridization can alter the host-specificity and fitness of herbivorous insects when the hybridizing populations are adapted to different hosts. It is less clear what the effects of admixture may be when genetically distinct populations are crossed that have similar and narrow host ranges. We tested the effects of hybridization between an Italian and Swiss population of the ragwort flea beetle, Longitarsus jacobaeae, a biocontrol agent for tansy ragwort, Jacobaea vulgaris, in the USA. Development success, development time, and fecundity of parental and first- and second-generation hybrids were assessed on the primary host and ten closely related plant species in no-choice larval transfer experiments. Four of the non-target species supported limited development but none represented novel host use of hybrids compared to the parents. Development time showed maternal effects on one of the non-target species where offspring of crosses with Italian mother developed slower. Percent larval development was significantly greater for one replication of a non-target species, indicating a plant genotype effect. Overall, hybridization did not result in changes of the fundamental host range or improved performance of hybrids on non-target species even when some hybrid lineages exhibited hybrid vigor on the primary host. These findings underscore the reliability of currently-employed host-specificity testing procedures that identify the fundamental host range of potential agents. Our results also support the newly advocated approach to promote intraspecific hybridization in biocontrol agents when the parental populations have similar and narrow host ranges to increase genetic variation and create novel genotypes to facilitate adaptation and persistence in the new range.

Functional response of Amblyseius herbicolus (Acari: Phytoseiidae) on Sericothrips staphylinus (Thysanoptera: Thripidae), an ineffective biocontrol agent of gorse

Sericothrips staphylinus was introduced to New Zealand as a biological control agent for gorse, Ulex europaeus (Fabales: Fabaceae), an invasive weed of European origin, but has proven to be an ineffective agent. We investigated and compared the functional responses of a predatory mite found on gorse in New Zealand, Amblyseius herbicolus, with two well-known mite predators of thrips: Amblydromalus limonicus, and Neoseiulus cucumeris when fed on varying densities (2, 4, 8, 16, and 24/491 mm2) of S. staphylinus first instar larvae. We also compared the functional response of A. herbicolus on S. staphylinus with previously published data for mite predators of thrips. Amblyseius herbicolus, A. limonicus, and N. cucumeris all exhibited a type II functional response. A. herbicolus generally exhibited higher capture rates and lower handling times than those reported for other predatory mites that are effective biocontrol agents of pest thrips on crops, except for A. limonicus. These results indicate that the presence of A. herbicolus on gorse in New Zealand is a likely explanation for the failure of S. staphylinus as a weed biocontrol agent.

Observations of parasitoid behaviour in both no‐choice and choice tests are consistent with proposed ecological host range

AbstractThe solitary larval endoparasitoid Eadya daenerys Ridenbaugh (Hymenoptera: Braconidae) is a proposed biocontrol agent of Paropsis charybdis Stål (Coleoptera: Chrysomelidae, Chrysomelinae), a pest of eucalypts in New Zealand. Eadya daenerys oviposition behaviour was examined in two assay types during host range testing, with the aim of improving ecological host range prediction. No‐choice sequential and two‐choice behavioural observations were undertaken against nine closely related species of New Zealand non‐target beetle larvae, including a native beetle, introduced weed biocontrol agents, and invasive paropsine beetles. No behavioural measure was significantly different between no‐choice and two‐choice tests. In sequential no‐choice assays the order of first presentation (target–non‐target) had no significant effect on the median number of attacks or the attack rate while on the plant. Beetle species was the most important factor. Parasitoids expressed significantly lower on‐plant attack rates against non‐targets compared to target P. charybdis larvae. The median number of attacks was always higher towards target larvae than towards non‐target larvae, except for the phylogenetically closest related non‐target Trachymela sloanei (Blackburn) (Coleoptera: Chrysomelidae, Chrysomelinae). Most non‐target larvae were disregarded upon contact, which suggests that the infrequent attack behaviour observed by two individual E. daenerys against Allocharis nr. tarsalis larvae in two‐choice tests and the frass of Chrysolina abchasica (Weise) was probably abnormal host selection behaviour. Results indicate that E. daenerys is unlikely to attack non‐target species apart from Eucalyptus‐feeding invasive paropsines (Chrysomelinae). Non‐lethal negative impacts upon less preferred non‐target larvae are possible if E. daenerys does attack them in the field; however, this is likely to be rare.

English

English

Genome Assembly of the Ragweed Leaf Beetle: A Step Forward to Better Predict Rapid Evolution of a Weed Biocontrol Agent to Environmental Novelties.

Rapid evolution of weed biological control agents (BCAs) to new biotic and abiotic conditions is poorly understood and so far only little considered both in pre-release and post-release studies, despite potential major negative or positive implications for risks of nontargeted attacks or for colonizing yet unsuitable habitats, respectively. Provision of genetic resources, such as assembled and annotated genomes, is essential to assess potential adaptive processes by identifying underlying genetic mechanisms. Here, we provide the first sequenced genome of a phytophagous insect used as a BCA, that is, the leaf beetle Ophraella communa, a promising BCA of common ragweed, recently and accidentally introduced into Europe. A total 33.98 Gb of raw DNA sequences, representing ∼43-fold coverage, were obtained using the PacBio SMRT-Cell sequencing approach. Among the five different assemblers tested, the SMARTdenovo assembly displaying the best scores was then corrected with Illumina short reads. A final genome of 774 Mb containing 7,003 scaffolds was obtained. The reliability of the final assembly was then assessed by benchmarking universal single-copy orthologous genes (>96.0% of the 1,658 expected insect genes) and by remapping tests of Illumina short reads (average of 98.6 ± 0.7% without filtering). The number of protein-coding genes of 75,642, representing 82% of the published antennal transcriptome, and the phylogenetic analyses based on 825 orthologous genes placing O. communa in the monophyletic group of Chrysomelidae, confirm the relevance of our genome assembly. Overall, the genome provides a valuable resource for studying potential risks and benefits of this BCA facing environmental novelties.

The regulatory process and costs to seek approval for the development and release of new biological control agents in New Zealand

The New Zealand Environmental Protection Authority (EPA) is responsible for regulating the importation and development in containment and release of new organisms in New Zealand. This includes exotic biological control agents. We highlight the regulatory process that biocontrol practitioners need to comply with in addition to the costs to apply to the EPA to seek approval for the development and release of new biocontrol agents in New Zealand. We discuss the structure of the costs to develop and take new microbial endophytes to control pests of economically valued plants to market and to develop and release new microbial pathogen and invertebrate biocontrol agents of weeds. We conclude by examining the benefit–cost ratio of weed biocontrol agents that were approved for release and the economic benefit of endophytes within the context of the costs to seek approval from the EPA.

Impact of generalist predation on two weed biocontrol agents in New Zealand

The broom leaf beetle (Gonioctena olivacea) and the Honshu white admiral butterfly (Limenitis glorifica) have been introduced into New Zealand as biocontrol agents of the weeds Scotch broom (Cytisus scoparius) and Japanese honeysuckle (Lonicera japonica) respectively. However, neither agent has been successful yet. Larval predation of these species could be a factor affecting their success, and this hypothesis was tested using various predator-exclusion treatments. Survival of broom leaf beetle larvae increased c. five-fold by sleeving Scotch broom seedlings in fine mesh. In contrast, survival was unaffected by excluding either crawling predators using sticky barriers or larger predators using chicken wire. Survival of Honshu white admiral butterfly larvae increased c. ten-fold by excluding either crawling predators using sticky barriers or flying predators using a fine-mesh sleeve. Simultaneously excluding both crawling and flying predators resulted in a c. 23-fold increase in survival. These results suggest that larval predation could be limiting the populations of both broom leaf beetle and Honshu white admiral. Future biocontrol programmes could prioritise candidate agents accordingly.

Next generation biological control – an introduction

Next generation biological control – an introduction

Laboratory tests to estimate the non-target impacts of four Aphidius spp. parasitoids in the field

A ‘risk score’ approach to help determine the potential impact of biological control agents on non-target species, previously proposed for weed biocontrol agents, was examined in an ex post study for insect biocontrol agents. ‘Risk scores’ (% parasitism for non-target aphid species/% parasitism for target aphid species) were calculated for 19 aphid (New Zealand adventive and indigenous) species and 4 introduced (New Zealand) Aphidius biocontrol species, based on previously published choice and no-choice host range laboratory testing. Field hosts for each Aphidius parasitoid and aphid host combination were also examined through an extensive literature review. Strong correlations between ‘risk scores’ for both choice and no-choice laboratory assays and field host binary values (host: yes or no) were obtained for each Aphidius/aphid dataset, but there was no threshold score that indicated using the approach to predict parasitoid field host ranges could result in type II errors. In contrast, a second analysis that categorized aphid hosts as ‘major field hosts’, if literature records indicated high (≥15%) levels of parasitism in the field, showed a clear threshold risk score predicting whether an aphid was a major field host in no-choice tests. We conclude that this approach could potentially be used to predict the likelihood of the impact of Aphidius biocontrol agents on non-target aphid species. We discuss the pros and cons of this approach to help scientists and regulators in the assessment for new biocontrol agent introductions, including the need for this ‘risk score’ approach to be tested on a greater range of insects.

How Safe Is Weed Biological Control? A Global Review of Direct Nontarget Attack

This review summarizes all known direct nontarget attack (NTA) cases of intentionally released or actively redistributed weed biological control agents, in order to allow for an objective risk-benefit analysis when choosing the most appropriate method for controlling invasive plants. Of 457 agents intentionally released until 2008, 60 (13.1%) have been recorded attacking nontarget species in the field. Of 1517 releases made using the 457 agent species, 122 (8.0%) resulted in NTA. Both proportions have declined over time. Three-quarters of all NTA cases occurred on plant species in the same family as the target weed. Approximately one-half of NTA cases were predicted/predictable. In the majority of unpredicted cases (93.5%), the respective nontarget plant species had not been tested prerelease. There were only four cases of “false negatives” (less than 1%), where the impacted plant species had been tested prerelease and deemed not at risk.The incidences of unpredicted nontarget attack of intentionally released weed biocontrol agents decreased over time and this trend is thought to continue with scientific advancements. What is most needed is more systematic postrelease monitoring to compare with prerelease host range testing to further advance the predictability of host use of biocontrol agents.

Constraints in weed biological control: contrasting responses by implementing nations

The compilation of papers in this Special Issue (SI) derives from a Symposium at the 25th International Congress of Entomology, in 2016, entitled “Rise or demise? A global outlook on the future of classical biological weed control”. In the SI-opening-paper, a summary of the 5th edition of the world catalogue of weed biocontrol agents and their target weeds provides a comprehensive international perspective. Weed biocontrol implementation is beleaguered by perceptions of risk and restrictive regulatory procedures, notably in the USA, and less so in Canada. Thus, most of the papers in this SI comprise accounts of innovative responses to these challenges from scientists in the USA. Political and funding issues have inhibited weed biocontrol in Australia over the past decade, but there appears to be a gradual reversal of this trend in recent years. In contrast, in New Zealand and in South Africa, the practice is flourishing, and there are significant recent initiatives in Europe. Overall, the contributions in the SI suggest an optimistic prognosis for weed biological control.

A proposal to use plant demographic data to assess potential weed biological control agents impacts on non-target plant populations

Weed biocontrol programs aim to reduce the spread and population growth rate of the target plant while stabilizing or increasing populations of those native species considered under threat by invasive plants. This goal is not unique to weed biocontrol but applies to all other invasive plant management techniques, though such information is rarely collected. Without this information, success of management interventions can be ambiguous, and regulatory agencies, the public, policy makers, funders and land managers cannot be held accountable for chosen treatments. A fundamental reform, including use of demographic studies and long-term assessments, are essential to guide weed biocontrol programs. We propose to add use of plant demography (an assessment of how environmental factors and ecological interactions, for example competition, disease or herbivory, may affect plant populations by altering survival, growth, development and reproductive rates of plant individuals) during host specificity risk assessments of potential biological control agents. Demographic models can refine assessments of potential impacts for those plant species that experience some feeding or larval development during host specificity testing. Our proposed approach to focus on impact on plant demography instead of attack on plant individuals is useful in appropriately gauging threats potential weed biocontrol agents may pose to non-target species after field release.

Direct effects of insecticides on common ragweed-implications for natural enemy exclusion trials.

Experimentally applying pesticides is an important method to assess the efficacy of weed biocontrol agents, but potential direct effects of the chemicals on plant performance are controversial or unknown. We assessed how three broad-spectrum insecticides applied in combination affect the performance of the widely invasive, crop-yield reducing, allergenic common ragweed (Ambrosia artemisiifolia L.) in an insect-free environment. Spraying insecticides had no significant effects on aboveground dry weight, seed and pollen output or pollen allergenicity, and only explained 1-8% of variation in these parameters. Our insecticide treatment can hence be applied to assess biocontrol impact on biomass and reproductive output of common ragweed. As our insecticide treatment delayed senescence, however, other methods of insect exclusion should be preferred when studying common ragweed phenology.

A glimpse into the compatibilities and conflicts between arthropods and fungal biological control agents of aquatic weed waterhyacinth

Interspecific interactions play an important role in ecosystem functioning. Several biocontrol agents are being introduced for the control of invasive species like the aquatic macrophyte, waterhyacinth, Eichhornia crassipes, in the hope of improving the eco-friendly natural control mechanism. Due to their overlapping niches, interspecific interactions among the biocontrol agents is high and there is a paucity of information on possible positive or negative impact they may have on each other hence affecting the biocontrol. Therefore studies on their interaction become even more important. In order to understand such possibilities, three potential fungi, Fusarium oxysporum (FO), F. roseum (FR), Paradendryphiella salina (PS) and two host-specific arthropods Orthogalumna terebrantis (OT) and Neochetina bruchi (NB) were applied on water hyacinth plants singly and in various combinations (OT, NB, FO, FO + OT, FO + NB, FR, FR + OT, FR + NB, PS, PS + OT, PS + NB). Observations were made on percentage damage caused by these agents to water hyacinth. Biocontrol agents applied in combination had cumulative impact on the target weed. FO + NB and FO + OT treated plants showed enhanced damage percentage of about 90%, after 120 h. But FR + NB and PS + NB treated plants were far less damaged compared to when these agents were applied separately. PS also had a repelling effect on NB. Results of such interactions are often variable and less predictable, especially under field conditions. These results demonstrate the need for studies on biotic interactions among biocontrol agents, prior to release of the biocontrol agents of weeds.

Thermal tolerance of Liothrips tractabilis, a biological control agent of Campuloclinium macrocephalum recently established in South Africa

AbstractThe South American herb Campuloclinium macrocephalum (Less.) DC. (Asteraceae; pompom weed), which invades grasslands, savannas, and wetlands in South Africa, is a recent target for biological control. A foliage‐deforming thrips, Liothrips tractabilis Mound & Pereyra (Thysanoptera: Phlaeothripidae), was released in South Africa in 2013, following confirmation of its host specificity and damage potential in quarantine. However, weed biocontrol agents sometimes fail to establish or have the desired impact because they are poorly suited to the climate of the new range. Thermal tolerance trials, within the range of 15–32.5 °C, were conducted prior to the thrips’ release to determine its developmental threshold and to generate a degree‐day model to highlight areas best suited for its establishment in South Africa. These laboratory data were validated by outdoor trials. The thrips completed development from egg to adulthood at all except the lowest and highest laboratory test temperatures, with developmental duration decreasing with increasing temperature. The lower developmental threshold was estimated at 9.6 °C with 546.9 degree days required to complete development. Within the regions invaded by C. macrocephalum in South Africa, the thrips was predicted to complete 3–9 annual generations. Developmental times in the outdoor trials were largely consistent with those in the laboratory. Liothrips tractabilis is largely compatible with the broader South African climate and seems likely to establish and proliferate on C. macrocephalum populations throughout the country. These predictions have partially been verified in that L. tractabilis has become established at several sites in South Africa, many of these in colder, high‐altitude areas which were predicted to support fewer annual generations.

Non-target effects of insect biocontrol agents and trends in host specificity since 1985.

Abstract Non-target impacts of parasitoids and predaceous arthropods used for classical biological control of invasive insects include five types of impact: (1) direct attacks on native insects; (2) negative foodweb effects, such as competition for prey, apparent competition, or displacement of native species; (3) positive foodweb effects that benefited non-target species; (4) hybridization of native species with introduced natural enemies; and (5) attacks on introduced weed biocontrol agents. Examples are presented and the commonness of effects discussed. For the most recent three decades (1985-2015), analysis of literature on the host range information for 158 species of parasitoids introduced in this period showed a shift in the third decade (2005-2015) towards a preponderance of agents with an index of genus-level (60%) or species-level (8%) specificity (with only 12% being assigned a family-level or above index of specificity) compared with the first and second decades, when 50 and 40% of introductions had family level or above categorizations of specificity and only 21-27 (1985-1994 and 1995-2004, respectively) with genus or 1-11% (1985-1994 and 1995-2004, respectively) with species-level specificity. In all three decades, 11-12% of introductions could not be classified in this manner due to lack of information. Recommendations for future actions to improve this record are made: (1) distinguish host use from population-level impact; (2) develop country-level online summaries of relevant information; (3) plan biological control projects with conservation partners; and (4) conduct post-release comparisons of actual impact to predicted risk based on quarantine studies.

Investigating the poor performance of heather beetle, Lochmaea suturalis (Thompson) (Coleoptera: Chrysomelidae), as a weed biocontrol agent in New Zealand: Has genetic bottlenecking resulted in small body size and poor winter survival?

Heather beetle (Lochmaea suturalis), has underperformed as a biocontrol agent when compared with the damage it does to native heather in Europe. Mean heather beetle body size, measured by elytron area, was 10% smaller in NZ populations compared with beetles from northern UK where the NZ beetles originated. Previous research in Europe showed that small beetles suffer higher winter mortality. Field-collected heather beetles in NZ show a positive relationship between body size and the proportion of pre-overwintering food reserves (lipids) they contained. Beetles that died in an overwintering experiment had lower proportional lipid reserves, and a smaller mean body size, than surviving beetles. Smaller body size in NZ is probably mostly due to a severe founder effect: line-rearing of beetles in NZ to eliminate a microsporidian disease, and poor establishment success, resulted in NZ beetles being derived from one or two field-collected females from one UK site. Several measures of genetic variability in NZ beetles compared with beetles from the UK indicated severe genetic bottlenecking. In particular, reductions in heterozygosity in NZ versus UK beetles were a close match to theoretical heterozygosity after a severe bottleneck. Heather beetle populations from southern UK were genetically distinct from those sampled from northern UK, and previous collecting showed higher microsporidian infestations in beetles from southern UK compared with northern beetles. Mean elytron area was 2.2% smaller in the southern UK population compared with the northern population. Genetic rescue of NZ heather beetles could use beetles from the northern UK that have slightly larger body size and lower levels of microsporidian infection.