Factors affecting the cost of weed biocontrol programs in New Zealand

Many national schemes for setting priorities for invasive weed management have emphasized the current or future impacts of the weed more than the cost or feasibility of control, perhaps because the latter may be difficult to estimate. As part of a project to improve prioritization of weed biocontrol targets in New Zealand, we investigated factors that were hypothesized to influence the cost of conducting weed biological control, using data from New Zealand programs. Taxonomic isolation of the target weed, relative to commercially important plants and native flora was not a significant influence on program cost, although we present evidence that disease, which to date has only affected agents released against taxonomically isolated weed targets, has masked the importance of taxonomic isolation in New Zealand. Opposition to biocontrol has caused delays, but has not had a major influence on the cost of biocontrol in New Zealand, probably because weed species with the greatest potential for opposition were identified during feasibility studies and avoided, or because conflicts were resolved by conducting cost-benefit analyses that were minor components of the total program costs. Only two factors explained virtually all the variance in program cost: program type (repeat programs were cheaper than novel/pioneering programs); and the number of agent species released. The predicted cost of future weed biocontrol programs can now be incorporated into decision-making tools ranking New Zealand weed biocontrol targets. Efficiencies in future programs are most likely to be gained by better agent selection so that fewer agents are released. For repeat programs this could be achieved by waiting until monitoring has been conducted overseas, so that the best agents or combination of agents can be selected for any particular weed. This reiterates the need for better post-release evaluation of weed biocontrol agent effectiveness worldwide.     

The value of simulating herbivory in selecting effective weed biological control agents

Invasive species have a significant economic and ecological cost and biological control can be a powerful tool in their management. Classical biological control practice involves the re-establishment of trophic links between specialist insect and fungal agents to regulate populations of invasive species. However, the permanent nature of biological control agent introductions raises concerns about the unintended consequences of such introductions on non-target organisms, particularly when such agents are ineffective on their target organisms. In this paper, we explore the current debate in the selection of agents for weed classical biological control. We then propose an alternate approach, based on studying plant response to simulated herbivory, that could minimize the chances of release of ineffective agents. Simulating herbivory could yield insights into the vulnerability of plants to certain types of damage. Selection of agents within guilds that are likely to have a significant influence on the plant can improve the chances of achieving biological control sooner and reduce the likelihood of releasing ineffective agents that may have non-target impacts. We propose a method by which simulated herbivory could be integrated into the agent selection process and discuss its strengths and shortcomings. We present case studies of two Neotropical weeds illustrating how this method could be applied.     

The role of pre-release efficacy assessment in selecting classical biological control agents for weeds—applying the Anna Karenina principle

The goals in selecting classical biological control agents for weeds are to identify agents that will be both safe for release and effective in controlling their target plants. The release of ineffective agents should be avoided, as these add to the costs and risks of biological control without contributing to its benefits. While the principles of host-specificity testing and risk assessment for weed biological control agents have been extensively debated and refined, there has been less attention given to assessing the probable efficacy of agents prior to release. This reluctance to undertake pre-release efficacy assessment (PREA) is probably based on concerns that it will both add to the cost of screening biological control agents and introduce a risk of wrongly rejecting effective agents. We used a project simulation model to investigate the implications of using PREA as an additional filter in the agent selection process. The results suggest that, if it can be done at a lower cost than host-specificity testing, the use of PREA as the first filter can make agent selection more cost-effective than screening based on host-specificity alone. We discuss examples of PREA and potential approaches. The impact of biocontrol agents is a function of their range, abundance, and per-capita damage. While it will always be difficult to predict the post-release abundance of biological control agents from pre-release studies, some estimates of potential range can be obtained from studies of climatic adaptation. For agents that affect the vegetative growth or survival of their target weeds, experimental measurement of per-capita damage is feasible and can contribute to a reduction in the numbers of ineffective agents released. The Anna Karenina principle states that success in complex undertakings does not depend on a single factor but requires avoiding many separate causes of failure. We suggest that, in biological control of weeds, the use of agents that are not sufficiently damaging is one such cause that can be partially avoided by the use of pre-release efficacy assessment.     

Nutrient composition of soil and plants may predict the distribution and abundance of specialist insect herbivores: implications for agent selection in weed biological control

Abstract  Refining the process of selecting specialist herbivores that are used as biological control agents to maximise effects on the targets can diminish the risk to non-target species. While biotic factors (e.g. plant demography and agent–host interactions) have been explored for clues to improve the way we make agent selection decisions, recent ecological research indicates that abiotic factors related to the habitat (e.g. plant and soil nutrient composition, and soil characteristics) are important predictors of insect herbivore community composition. In this paper we explore the relevance of plant nutrient composition to aid in selecting agents for the invasive Eurasian perennial Euphorbia esula (leafy spurge) in Illinois, USA. We propose that an approach that compares such abiotic factors across the native and invaded ranges of plants in conjunction with the community composition of specialist herbivores in the native range may yield valuable clues in selecting agents that are most likely to establish and regulate populations of the target weed.     

Opportunities for biological weed control in Europe

The development and application of biological weed control offer greatopportunities not only for farmers, nature conservationists and othervegetation managers but also for institutions and companies that wish tosell plant protection services and products, and for the general publicthat demands safe food and a visually attractive and diverseenvironment. Despite the obvious opportunities for biological weedcontrol, few control agents are actually being used in Europe. Potentialagent organisms have features that make them particularly strong anduseful for biological control, but they also have weaknesses. Weaknessesinclude a too narrow or too wide host specificity, lack of virulence, orsensitivity to unfavourable environmental conditions.Developing specific knowledge on the interaction between weeds andpotential biological control agents, as well as expertise to increasethe effect of control agents and so achieve sufficient weed control in acost-effective manner, should have the highest priority in researchprogrammes. From 1994 to 2000 most ongoing research on biological weedcontrol in Europe was combined in a cooperative programme. This COSTAction concentrated on the interactions between five target crop weedsand their antagonists (pathogens and insects), on furthercharacterisation of the specific blems and potential control agents andon the most suitable biological control approach.The next major challenge will be to apply the findings provided byCOST-816 to the development of practical control solutions. The leadingobjective of a new concerted research programme with European dimensionswill be to stabilise or even promote biodiversity in the most importantEuropean ecosystems by integrating biological weed control in themanagement of these systems.     

Testing biological control agent compatibility: Cyphocleonus achates and Larinus minutus on diffuse knapweed

While weed biological control success is typically achieved with one agent, multiple agents are invariably introduced. Biological control agents that share a host–plant may interact either directly or indirectly through changes in host–plant quality. Negative interactions could reduce the impacts of the agents on the density of their host–plant while positive interactions (facilitation) could improve biological control success.In the Okanagan Valley of British Columbia, Canada, initial declines in the invasive rangeland weed, diffuse knapweed (Centaurea diffusa) were attributed to the introduction of the weevil Larinus minutus. A second weevil, Cyphocleonus achates has recently become common on diffuse knapweed. We sought to determine if the recent increase of C. achates could threaten the success of L. minutus. We considered whether L. minutus colonisation or performance remained the same when C. achates was present, and whether the two agents acted independently to reduce plant performance.Neither changes in colonisation rates nor competitive interactions were apparent between C. achates and L. minutus. Both insects reduced plant performance and, for all metrics, the reduction in plant performance by one species was independent of the second. The two agents appear to be compatible and both should contribute to the control of diffuse knapweed. To assess how biological control agents interact requires understanding both their competitive interactions and their joint effects on the shared host.     

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

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

Microbial selection strategies that enhance the likelihood of developing commercial biological control products

Research interest in utilizing microorganisms to create a microbial environment suppressive to plant pathogens has increased exponentially in recent years. Despite intense interest in developing biological control agents, relatively few antagonists have achieved ‘commercial product’ status. The fact that such a small proportion of active laboratory antagonists are developed into biological control products is partly due to several features common to microbial selection strategies that are widely utilized to obtain putative biological control agents: (a) relatively few candidate microorganisms are tested; (b) microbes are selected based on the results of an assay that does not replicate field conditions; and (c) the amenability of microbes to commercial development is excluded as a selection criterion. Selection strategies that enhance the likelihood of developing commercial biological control products are described. These include making appropriate choices regarding the pathosystem for biological control, the method of microbe isolation, and the method of isolate characterization and performance evaluation. A model system of developing a biological control product active against Gibberella pulicaris (Fries) Sacc. (anamorph: Fusarium sambucinum Fuckel), the primary causal agent of Fusarium dry rot of stored potatoes, is used to illustrate the proposed selection strategy concepts. The crucial importance and methodology is described, of selecting strains with enhanced potential for commercial development based on a strain exhibiting both favorable growth kinetics and bioefficacy when grown in commercially feasible liquid media. Received 06 February 1997/ Accepted in revised form 29 May 1997     

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.     

Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control programme

The Florida Everglades have been invaded by an exotic weed fern, Lygodium microphyllum. Across its native distribution in the Old World tropics from Africa to Australasia it was found to have multiple location-specific haplotypes. Within this distribution, the climbing fern is attacked by a phytophagous mite, Floracarus perrepae, also with multiple haplotypes. The genetic relationship between mite and fern haplotypes was matched by an overarching geographical relationship between the two. Further, mites that occur in the same location as a particular fern haplotype were better able to utilize the fern than mites from more distant locations. From a biological control context, we are able to show that the weed fern in the Everglades most likely originated in northern Queensland, Australia/Papua New Guinea and that the mite from northern Queensland offers the greatest prospect for control.     

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

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

Monitored releases of Rhinoncomimus latipes (Coleoptera: Curculionidae), a biological control agent of mile-a-minute weed (Persicaria perfoliata), 2004–2008

Mile-a-minute weed, Persicaria perfoliata (L.) H. Gross, is an invasive annual vine of Asian origin that has developed extensive monocultures, especially in disturbed open areas in the Mid-Atlantic region of the United States. A host-specific Asian weevil, Rhinoncomimus latipes Korotyaev, was approved for release in North America in 2004, and weevils have been reared at the New Jersey Department of Agriculture Beneficial Insect Laboratory since then. By the end of 2007 more than 53,000 weevils had been reared and released, mostly in New Jersey, but also in Delaware, Maryland, Pennsylvania, and West Virginia. The beetles established at 63 out of 65 sites (96.9%) where they were released between 2004 and 2007, with successful releases consisting of as few as 200 weevils. Weevils were recorded at 30 additional non-release sites in New Jersey, where they had dispersed at an average rate of 4.3 km/year. Standardized monitoring of fixed quadrats was conducted in paired release and control sites at eight locations. Significant differences in mile-a-minute weed populations in the presence and absence of weevils were found at three locations, with reduction in spring densities to 25% or less of what they had been at the start within 2–3 years at release sites, while weed densities at control sites were largely unchanged. Mile-a-minute weed populations at a fourth site were similarly reduced at the release site, but without control data for comparison due to rapid colonization of the paired control site. At the other four locations, all on islands, mile-a-minute weed populations were reduced at both release and control sites without large weevil populations developing, apparently due to environmental conditions such as late frost and extreme drought.     

Host range testing and life history of the defoliator Hymenomima nr. memor: an unsuitable biological control agent for Schinus terebinthifolia in the U.S.A.

Host range of larvae of Hymenomima nr. memor (Lepidoptera: Geometridae) was examined in quarantine to evaluate its suitability as a biological control of Brazilian peppertree, Schinus terebinthifolia. Brazilian peppertree, S. terebinthifolia is an environmental and agricultural weed from South America that had invaded many subtropical and tropical areas of the world including Florida and Hawaii, USA. Laboratory life history and quarantine host range studies of H. memor were conducted with no-choice feeding tests. These tests included eight species of the Anacardiaceae and one species of Sapindaceae. Larvae of H. memor had five to six instars with each head capsule width increasing by 1.68-X. Development time from neonate to adult was 46.7?±?2.2 days. In host range tests, neonates completed development to the adult stage on all non-target species, except Toxicodendron radicans. Moreover, developmental times were delayed and pupal weights were reduced for larvae fed Spondias purpurea leaves. Due to the broad host range exhibited by H. memor larvae, this species will not be considered as a biological control agent of S. terebinthifolia in the continental U.S.A.     

A scientific approach to agent selection

Abstract  The prioritisation of potential agents on the basis of likely efficacy is an important step in biological control because it can increase the probability of a successful biocontrol program, and reduce risks and costs. In this introductory paper we define success in biological control, review how agent selection has been approached historically, and outline the approach to agent selection that underpins the structure of this special issue on agent selection. Developing criteria by which to judge the success of a biocontrol agent (or program) provides the basis for agent selection decisions. Criteria will depend on the weed, on the ecological and management context in which that weed occurs, and on the negative impacts that biocontrol is seeking to redress. Predicting which potential agents are most likely to be successful poses enormous scientific challenges. 'Rules of thumb', 'scoring systems' and various conceptual and quantitative modelling approaches have been proposed to aid agent selection. However, most attempts have met with limited success due to the diversity and complexity of the systems in question. This special issue presents a series of papers that deconstruct the question of agent choice with the aim of progressively improving the success rate of biological control. Specifically they ask: (i) what potential agents are available and what should we know about them? (ii) what type, timing and degree of damage is required to achieve success? and (iii) which potential agent will reach the necessary density, at the right time, to exert the required damage in the target environment?     

Field colonization, population growth, and dispersal of Boreioglycaspis melaleucae Moore, a biological control agent of the invasive tree Melaleuca quinquenervia (Cav.) Blake

Invasion of native plant communities by the Australian paperbark tree (“melaleuca”), Melaleuca quinquenervia, complicates restoration of the Florida Everglades. Biological control, within the context of a comprehensive management program, offers a means to suppress regeneration of melaleuca after removal of existing trees and a mechanism to forestall reinvasion. To meet this need, a biological control program commenced in 1997 upon the release of an Australian weevil (Oxyops vitiosa [Pascoe] [Coleoptera: Curculionidae]). Release of a second biological control agent, the melaleuca psyllid (Boreioglycaspis melaleucae Moore), followed in February 2002 at field sites containing mixed age-class melaleuca stands or coppicing stumps. Each site was inoculated with 7000–10,000 adult psyllids, with one exception where 2000 nymphs were released on seedlings the following December. Psyllid populations established everywhere irrespective of colony source, site conditions, or the quantity released, although numbers released and, to a lesser degree, colony age influenced the numbers of colonies produced. Quantity included in the release was the major determinant of the resultant number of colonies, although the duration of their tenure in quarantine culture may have also influenced this. One site, comprised mainly of coppicing stumps, contained 3.3 million psyllids per ha within 3 months after release. Less than 1% of the coppices at a similar site harbored psyllid colonies 2 months after release (May 2002), but this rose to 75% in October then to 100% by December. The census population exceeded 715,000 adults and nearly 11 million nymphs by late January 2003. Psyllid populations dispersed 2.2–10.0 km/year, with the slower rates in dense, continuous melaleuca stands and faster rates in fragmented stands. Over 1 million psyllids had been redistributed to 100 locations as of December 2005. This species now occurs throughout much of the range of melaleuca in south Florida due to natural range expansion as well as anthropogenic dissemination.     

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.     

Suggestions for unifying the terminology in biological control

This paper gives suggestions forunifying the terminology in biological controlacross different research disciplines, such asbiological control of arthropods, weeds andplant pathogens. It is suggested that use ofthe term `biological control' is restricted tothe use of living organisms. Four strategiesof biological control are outlined anddefined: (1) Classical biological control, (2) Inoculation biological control, (3) Inundationbiological control, and (4) Conservationbiological control. It is proposed to usethese four terms as defined, and avoid usageof the term `augmentation'. Terms for specificprocesses and modes of action (for example,`parasitoid' and `competitor') can be definedby usage within the different biologicalcontrol disciplines. Microbial control usuallyindicates biological control of invertebratesusing microbes and, as such, is a subdivisionof biological control. Use of additionalauxiliary terms such as biopesticide isdiscussed.     

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

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

Plant/pathogen interactions observed during host range testing of the rust fungus Uromyces pencanus,a classical biological control agent for Chilean needle grass (Nassella neesiana) in Australia and New Zealand

Nassella neesiana (Chilean needle grass) is a South American grass species that is a serious weed in Australia and New Zealand. The rust fungus Uromyces pencanus is a promising biocontrol agent that could be used to control the weed in both countries. Extensive host range testing has been conducted to explore the specificity of the rust. In this paper we discuss the different degrees of invasion by the rust of the tissues of target and non-target species; the plant defences elicited by such invasion at the cellular level; and their relevance to the biological control of Chilean needle grass.