Can natural enemies of current insect pests provide biotic resistance to future pests?

1. Economic pests jeopardize agricultural production worldwide. Classical biological control, comprising the import of exotic natural enemies to control target pest populations, has a successful history in many countries. However, little is known about how these natural enemies contribute to the suppression of pests that are yet to arrive. Biotic resistance theory, though, posits that communities resist species invasions as a result of natural enemies.
2. We assessed the potential of the resident exotic parasitoid wasp fauna in New Zealand (intentionally‐introduced biological control agents and unintentionally‐introduced species) to provide biotic resistance against possible future pests. A dataset was generated containing resident exotic parasitoid species (Ichneumonoidea: Braconidae; Ichneumonidae) in New Zealand, as well as their known global host ranges and the pest status of host species, to infer the potential for biotic resistance.
3. The known exotic ichneumonoid fauna in New Zealand comprises 65 species. These species associate with 107 host species in New Zealand, of which 54 species are pests. However, the current exotic species could potentially suppress 442 pest species not yet occurring in New Zealand.
4. This approach could be used to inform pest management programmes worldwide. Future research should consider how biotic resistance from the established parasitoid fauna can be used to inform specific decisions with respect to classical biological control.

     

Success and safety in the biological control of environmental weeds in New Zealand

Biological control, using specialist insect herbivores and plant pathogens, can be a self‐sustaining, cost‐effective and low‐risk tool for the management of environmental weeds. Agents have been recorded attacking non‐target plants in New Zealand and elsewhere, but the effects are usually minor and/or transitory. It seems probable that only two cases, worldwide, will result in significant damage to non‐target plants (representing 0.5% of the nearly 400 insect, mite, or fungal species used in classical weed biocontrol). Both of these cases were predictable from host range testing. Negative indirect, or ‘downstream’, ecological effects from specific weed biocontrol agents are difficult to predict and measure. They are probably insignificant compared to the impacts of the invasive plants that the agents are introduced to control. However, it is necessary to balance the risks associated with any introduction against the environmental benefits from controlling a weed to a predicted level. Recent analyses suggest that success rates are better than generally perceived. For New Zealand programmes, where enough time has lapsed to allow assessment, we calculate a full/partial success rate of 83%. Many of the costs associated with environmental weeds are difficult to quantify. Detailed risk assessment will make biological control programmes more expensive and time‐consuming, so that reliance on non‐biological management methods for environmental weeds may actually increase. The costs of biocontrol programmes against some New Zealand weeds can be kept down by using research already carried out in Australia and other countries, and the process is reciprocal. Developing international consortia of sponsors is also a potential way to fund programmes against weeds shared by several countries.     

Microevolution in biological control: Mechanisms, patterns, and processes

Microevolution may determine both the safety and efficacy of classical biological control. Despite a growing body of literature, there are several key unanswered questions regarding the role of evolution in biological control: (1) How common is local adaptation of natural enemies to their hosts or the environment in the native range? How critical is it for success of biological control to find locally adapted agents for importation? (2) Does adaptive evolution following introductions play an important role in biological control? (3) Do introductions of biological control agents impose bottlenecks in population size that reduce genetic variation, and is reduced genetic variation associated with low fitness and poor performance? (4) How great is the risk of evolution of host range of biological control agents? (5) What is the risk of target pests evolving resistance to biological control agents? If pests evolve increased resistance, will biological control agents evolve mechanisms to overcome that resistance? Here, we review the four fundamental processes of microevolution, and discuss how they interact in the context of biological control. We discuss our current state of knowledge regarding the outstanding questions, highlight the types of experiments that can address them, and suggest ways to use microevolution to define risks, and enhance efficacy and safety of biological control.     

Exotic ladybirds for biological control of herbivorous insects – a review

Since the late 19th century, exotic ladybirds (Coleoptera: Coccinellidae) have been used extensively for suppressing herbivorous insects of economic importance. In recent decades, the introduction of non‐native biological control (BC) agents has been greatly limited due to the awareness of the potential non‐target effects of introductions. Nonetheless, recent episodes of biological invasions of economically important pests have raised the need to carefully consider whether the expected benefits of pest control go beyond the possible environmental risks of introduction. To better understand the factors that contributed to successful BC programs, here we review the literature behind classical and augmentative BC using exotic ladybirds. Additionally, by means of case studies, we discuss the BC efficacy of selected exotic species, e.g., Coccinella septempunctata L., Harmonia axyridis (Pallas), and Hippodamia variegata (Goeze), and their position within the communities of predators in the introduced areas of USA, Canada, and Chile. In Europe, much of the research on exotic ladybirds has been conducted on the undesired impact of H. axyridis. Therefore, we summarize the risk assessment data for this species and review the field research investigating the ecological impact on European aphidophagous predators. According to the BIOCAT database of classical BC programs, 212 ladybird species belonging to 68 genera have been released in about 130 years of BC activity, with 14.6% of introductions having resulted in partial, substantial, or complete control of the target pest. However, because post‐release evaluation of establishment and BC success has not always been conducted, this rate could underestimate the successful cases. Among other factors, ladybird establishment and pest suppression mostly depend on (1) intrinsic factors, i.e., high voracity, synchronized predator‐prey life cycle, and high dispersal ability, and (2) extrinsic factors, i.e., adaptability to the new environment and landscape composition. This review contributes to improved understanding of ladybirds as exotic BC agents.     

Mate finding, dispersal, number released, and the success of biological control introductions

Abstract.

• 1 An analysis of published data and a mathematical model of the population dynamics of introduced parasitoids were used to explore the possibility that biological control introductions fail because an Allee effect drives small, introduced populations extinct. Such an Allee effect would arise because low densities, resulting from dispersal into a new environment, lead to failure to mate, which leads to a male-biased sex ratio, which, if extreme enough, could cause population extinction.
• 2 For chalcidoids, ichneumonoids and tachinids, the proportion of parasitoid populations that established when introduced for control of lepidopteran pests increased with the number of parasitoids per release, the total number released, and the number collected when each variable was analysed separately. For chalcidoids alone, establishment increased with the number of releases for this variable analysed separately. However, stepwise logistic regression of establishment on these variables included only the total number released for chalcidoids and the number per release for ichneumonoids and tachinids. This suggests that an Allee effect may limit the establishment of introduced parasitoids more than stochastic environmental variation or lack of genetic variation.
• 3 A reaction-diffusion model of parasitoid introductions was developed, which included mate finding, dispersal, reproduction and survival. Sensitivity analysis showed that the critical number of females needed to establish a population decreased hyperbolically as mate detection distance and net reproductive rate were increased, but the critical number increased linearly as mean-square displacement was increased. The critical number of females did not change when the gross distance traversed per generation was varied. This was because increased area searched by males compensated for increased displacement. Changing from virgin females producing all males (arrhenotoky) to virgin females producing no progeny increased the critical number of females by over 30%.
• 4 The analysis of past introductions and the sensitivity analysis of the reaction-diffusion model both suggested a threshold of about 1000 insects per release to ensure establishment of introduced parasitoids. The implications of our results for the design of biological control introductions are discussed. Limitations in retrospective analyses and current knowledge indicate the need for an experimental approach to introductions.

     

Biological control and sustainable food production

The use of biological control for the management of pest insects pre-dates the modern pesticide era. The first major successes in biological control occurred with exotic pests controlled by natural enemy species collected from the country or area of origin of the pest (classical control). Augmentative control has been successfully applied against a range of open-field and greenhouse pests, and conservation biological control schemes have been developed with indigenous predators and parasitoids. The cost-benefit ratio for classical biological control is highly favourable (1:250) and for augmentative control is similar to that of insecticides (1:2-1:5), with much lower development costs. Over the past 120 years, more than 5000 introductions of approximately 2000 non-native control agents have been made against arthropod pests in 196 countries or islands with remarkably few environmental problems. Biological control is a key component of a 'systems approach' to integrated pest management, to counteract insecticide-resistant pests, withdrawal of chemicals and minimize the usage of pesticides. Current studies indicate that genetically modified insect-resistant Bt crops may have no adverse effects on the activity or function of predators or parasitoids used in biological control. The introduction of rational approaches for the environmental risk assessment of non-native control agents is an essential step in the wider application of biological control, but future success is strongly dependent on a greater level of investment in research and development by governments and related organizations that are committed to a reduced reliance on chemical control.     

The EVect of Release Size on the Probability of Establishment of Biological Control Agents: Gorse Thrips ( Sericothrips staphylinus ) Released Against Gorse ( Ulex europaeus ) in New Zealand

Many biocontrol agents released against alien weeds and pests fail to establish in the field. Here, we ask whether better release strategies could improve the likelihood of successful establishment. A manipulative field experiment was used to investigate the relationship between the probability of establishment and the number of individuals released for a weed biocontrol agent. In this experiment, replicated releases of 10, 30, 90, 270 and 810 gorse thrips, Sericothrips staphylinus Haliday, were made on to isolated gorse bushes in New Zealand. The sampling eY ciency was determined using a further experiment in which known numbers of thrips were released on to bushes. The data obtained showed that in approximately nine out of 10 releases of 10 thrips, at least one thrips would be found. The thrips in the size of release experiment were sampled 1 year after their release. A higher proportion of the small releases became extinct during this time period: thrips were recovered from 100% of the releases of 270 and 810 thrips, but only from 33% of releases of 10, 30 and 90 thrips. Using gorse thrips as an example, a protocol was developed to determine the optimal release size for biocontrol agents. It is suggested that for a fixed number of insects available for release, smaller releases may increase the overall establishment rate. W hile a single large release can easily become extinct by chance, it is extremely unlikely that a large number of small releases will do so over the same time period. The optimal release size (i.e. that which maximizes the average number of successful establishments) for gorse thrips in New Zealand might be fewer than 100 thrips/ release site. This contrasts with the current strategy in New Zealand of 1000 thrips/release and the suggestion in the biocontrol literature that large releases optimize establishment. Over 1 year of observation the thrips had no eVect on gorse growth rate. The EVect of Release Size on the Probability of Establishment of Biological Control Agents: Gorse Thrips ( Sericothrips staphylinus ) Released Against Gorse ( Ulex europaeus ) in New Zealand     

Propagule pressure as a driver of establishment success in deliberately introduced exotic species: fact or artefact?

A central paradigm in invasion biology is that more releases of higher numbers of individuals increase the likelihood that an exotic population successfully establishes and persists. Recently, however, it has been suggested that, in cases where the data are sourced from historical records of purposefully released species, the direction of causality is reversed, and that initial success leads to higher numbers being released. Here, we explore the implications of this alternative hypothesis, and derive six a priori predictions from it. We test these predictions using data on Acclimatization Society introductions of passerine bird species to New Zealand, which have previously been used to support both hypotheses for the direction of causality. All our predictions are falsified. This study reaffirms that the conventional paradigm in invasion biology is indeed the correct one for New Zealand passerine bird introductions, for which numbers released determine establishment success. Our predictions are not restricted to this fauna, however, and we keenly anticipate their application to other suitable datasets.     

Environmental safety of biological control: Policy and practice in New Zealand

Introduction of biological control agents into New Zealand is regulated under the Hazardous Substances and New Organisms Act 1996 (HSNO). The legislation is strongly focused on the health and safety of people and the environment. HSNO is implemented by the Environmental Risk Management Authority, a quasi-judicial body of 6–8 people appointed by the Minister for the Environment. The process by which biological control applications are received and processed is described. Two case studies of weed biological control agents which have been through the HSNO process, and the scientific issues that arose in considering the environmental safety of these agents are discussed. The case studies presented are the applications to release the gall fly Procecidochares alani (Diptera: Tephritidae) to control mist flower Ageratina riparia, and three biological control agents, Macrolabis pilosellae (Diptera: Cecidomyiidae), Cheilosia urbana, and Cheilosia psilophthalma (Diptera: Syrphidae) for biological control of hawkweeds (Hieracium spp.). Both applications were approved for agent release into the environment.     

Patterns of bird invasion are consistent with environmental filtering

Predicting invasion potential has global significance for managing ecosystems as well as important theoretical implications for understanding community assembly. Phylogenetic relationships of introduced species to the extant community may be predictive of establishment success because of the opposing forces of competition/shared enemies (which should limit invasions by close relatives) versus environmental filtering (which should allow invasions by close relatives). We examine here the association between establishment success of introduced birds and their phylogenetic relatedness to the extant avifauna within three highly invaded regions (Florida, New Zealand, and Hawaii). Published information on both successful and failed introductions, as well as native species, was compiled for all three regions. We created a phylogeny for each avifauna including all native and introduced bird species. From the estimated branch lengths on these phylogenies, we calculated multiple measurements of relatedness between each introduced species and the extant avifauna. We used generalized linear models to test for an association between relatedness and establishment success. We found that close relatedness to the extant avifauna was significantly associated with increased establishment success for exotic birds both at the regional (Florida, Hawaii, New Zealand) and sub‐regional (islands within Hawaii) levels. Our results suggest that habitat filtering may be more important than interspecific competition in avian communities assembled under high rates of anthropogenic species introductions. This work also supports the utility of community phylogenetic methods in the study of vertebrate invasions.     

Historical factors mediate the effects of interspecific competition

Biotic interactions, such as interspecific competition, are potentially important in determining whether introduced species succeed or fail to establish wild populations. Such effects may be difficult to detect, however, because the outcome of interspecific competition may depend on historical and largely unpredictable circumstances such as the timing of introductions and the number of individuals of each species introduced. I used a stochastic birth-death model to explore the effects of interspecific competition, the timing of introductions and the numbers of individuals of each species introduced, on invasion success in a two-species competitive system. I then compared the model predictions with actual data on establishment outcomes for passerine birds introduced to New Zealand, for which we have data on the timing of introductions, the size of release populations, and a measure of the strength of per capita competition (the degree of morphological similarity among species). The model and data agree well, suggesting that interspecific competition was an important determinant of invasion success in this assemblage, but that the outcome of competition depended critically on circumstances such as the timing of introductions and number of individuals released. Hence, while there is a deterministic component to invasion success in this assemblage (morphologically similar species are less likely to establish), historical circumstances played a critical role in mediating the outcomes.     

THE INTRODUCTION INTO AUSTRALIA OF BIOLOGICAL CONTROL AGENTS OF HYPEROMYZUS LACTUCAE (L.) (HOMOPTERA: APHIDIDAE)

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An account is given of the importation and release in Australia of the hymenopterous parasites Aphidius sonchi Marshall and Praon volucre (Haliday) (Ichneumonoidea: Aphidiidae) as biological control agents of the sowthistle aphid, Hyperomyzus lactucae (L.), the vector of lettuce necrotic yellows virus, a serious disease of lettuce in Australia and New Zealand. The establishment of A. sonchi is documented.     

Establishment and impact of insect agents deployed for the biological control of invasive Asteraceae: prospects for the control of <Emphasis Type="Italic">Senecio madagascariensis</Emphasis>

Several invasive Asteraceae have been targeted for biological control worldwide, with variable success. Senecio madagascariensis Poiret, which invades agricultural lands in Australia and Hawaii, is a recent target. Since several potential insect agents were recorded in the plant’s native range in South Africa, we assessed biocontrol efforts against asteraceous weeds to determine those most likely to deliver success. Some 108 insect species, from five orders and 23 families, were deployed against 38 weed taxa, mostly in the mainland USA, Canada, Australia and New Zealand. Coleoptera (mainly Curculionidae and Chrysomelidae), Diptera (Tephritidae) and Lepidoptera (Tortricidae) featured the most. Despite high establishment success (73% of releases across countries), only 37% of successful releases achieved meaningful impact. Although root-feeding and stem-feeding insects appeared to be the best candidates, neither insect family nor feeding guild significantly influenced the probability of success. This synthesis of the global contribution of different guilds of specialist herbivores to the management of invasive Asteraceae is guiding the selection of candidate agents for the biocontrol of S. madagascariensis in Australia.     

Mistakes in the analysis of exotic species establishment: source pool designation and correlates of introduction success among parrots (Aves: Psittaciformes) of the world

Aim To evaluate the effect of mis‐specifying the correct comparison of species pools in the study of species characteristics associated with the biological introduction of exotic species. Methods We use a high quality data set on biological introductions of parrots (Aves: Psittaciformes). These data allow us to examine relationships between life history traits and probability of successful transition through an introduction stage when the species pool is both correctly and incorrectly specified. Results For the establishment of introduced parrot species, nearly half of the predictor variables showed different patterns of significance when an incorrect pool was specified. Multivariate analysis identified entirely different sets of variables as independent predictors of establishment success, depending on the species pool used. Correct pool specification identified that introduced parrot species have been more likely to establish if they have broader diets and are more sedentary. Main conclusions Conclusions from the analysis of biological introductions are likely to depend on the specification of the species pool for such analyses. In the analysis of parrot introductions, this was particularly apparent in establishment success following release. Further studies that analyse the introduction pathway need to examine the effects of pool mis‐specification so that the generality of our results can be assessed.     

Reproductive characteristics of invasive hyperparasitoid Baeoanusia albifunicle have implications for the biological control of eucalypt pest Paropsis charybdis

Hyperparasitoids can impede the establishment of primary parasitoid biological control agents or limit their control capacity. Although modern quarantine practices generally prevent hyperparasitoids being introduced with biological control agents, introductions can occur via natural pathways or accidentally with incoming passengers and cargo. In New Zealand, Baeoanusia albifunicle Girault is a self-introduced hyperparasitoid of Enoggera nassaui Girault, an intentionally introduced control agent of the eucalypt pest Paropsis charybdis Stål. A self-introduced primary parasitoid, Neopolycystus insectifurax (Girault), also parasitises P. charybdis in New Zealand. We assessed B. albifunicle biology to better understand its potential to disrupt P. charybdis control. It was determined that B. albifunicle is an obligate solitary hyperparasitoid with a longer lifespan, lower fecundity and longer generation time than its host. The hyperparasitoid reduced effective parasitism by E. nassaui to <10% in the lab, indicating it may limit control of the first P. charybdis generation by slowing spring population growth. It was confirmed that N. insectifurax is not hyperparasitised by B. albifunicle and therefore has some potential to substitute for any hyperparasitoid-driven decline in E. nassaui.     

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.     

If and when successful classical biological control fails

Classical biological control of insects has a long history of success, with high benefit–cost ratios. However, most attempts to introduce a biological control agent have been unsuccessful, largely because the agent does not establish in the new environment. This perspectives paper discusses the possibility that even successful biological control may eventually fail, although records show that this is far from a common event. A documented example of eventual biological control failure is discussed and the prospect for future failures analyzed. Part of this analysis is based on an introduced weevil pest in New Zealand and its successful parasitoid biological control agent. The potential fragility of this host–parasitoid relationship is considered, as well as why it may indeed be starting to show signs of instability; this is particularly from the point of view of New Zealand’s often species-poor agricultural ecosystems.     

Accounting for differential success in the biological control of homopteran and lepidopteran pests

One of the strongest patterns in the historical record of biological control is that programmes targeted against lepidopteran pests have been far less successful than those targeted against homopteran pests. Despite fueling considerable interest in the theory of host–parasitoid interactions, biological control has few unifying principles and no theoretical basis for understanding the differential pattern of success against these two pest groups. Potential explanations considered here include competitive limitation of natural enemy establishment, the influence of antagonistic parasitoid interactions, generation time ratio, and gregarious parasitoid development. An analysis of the biological control record showed that on average six natural enemies have been introduced per pest for both pest groups, providing no evidence of a differential intensity of competition. Similarly, use of a discrete time host–parasitoid model showed that antagonistic interactions that are common among parasitoids of Lepidoptera should not limit the success of biological control as such interactions can readily be counteracted by host refuge breaking. A similar model showed that a small generation time ratio (coupled with a broad window of host attack) and gregarious development can facilitate the suppression of pest abundance by parasitoids, and both were found to be positively associated with success in the biological control record. Of the four explanations considered here, generation time ratio coupled with a broad window of host attack appears to provide the best explanation for the differential pattern of success.     

Should the flower bud weevil Anthonomus santacruzi (Coleoptera: Curculionidae) be considered for release against the invasive tree Solanum mauritianum (Solanaceae) in New Zealand?

The invasive tree Solanum mauritianum Scop. has been targeted for biological control in South Africa and New Zealand, by deploying insect agents that could constrain its excessive reproductive output. The flower-feeding weevil Anthonomus santacruzi (Curculionidae) was approved for release in South Africa in 2007 but following the loss of the original culture in quarantine, new stocks were introduced from Argentina in 2008–2009. This study was initiated to confirm that the host range of the new culture was the same as that of the previous one, but also to assess the risks associated with the weevil's release in New Zealand. Different testing procedures, including no-choice tests and multi-choice tests in different arenas, produced inconsistent and ambiguous results. During no-choice tests, oviposition and larval development to adulthood occurred on three non-target species including two native South African and one native New Zealand Solanum species. However, subsequent multi-choice tests and a risk assessment suggested that the risks of anything more than collateral damage to non-target Solanum species are low. Overall, these data do not deviate substantially from the results of the original quarantine tests which facilitated the release of A. santacruzi in South Africa in 2009. Although we argue that none of the New Zealand native and cultivated species are at risk, stronger evidence from open-field trials and chemical ecology studies may be required to convince the regulatory authorities that A. santacruzi is suitable for release in New Zealand.