Translating host-specificity test results into the real world: The need to harmonize the yin and yang of current testing procedures

In its modern era, the discipline of biological control can be perceived as being subject to a series of tensions due to differences in philosophy, different needs, and different practices; these include the view that biological control is environmentally friendly and desirable vs. the view that any organism alien to a particular habitat should be considered an undesirable invasive, the need to protect nontarget species vs. the need to introduce the most effective biological control agents and the need to know what an agent might attack under normal field conditions vs. the restrictive nature of current testing procedures. These tensions are particularly manifest in the area of host-specificity testing where researchers interact most directly with regulators and policy-makers and recent “incidents” of nontarget use by biological control agents in three regions have brought them to the fore. The empirical tension between needing more certainty about agent host-range in the real world and being obliged to test this primarily under highly restricted conditions is of most concern to researchers. This paper suggests ways to reduce this through improvements in (1) what plants are tested, (2) how the selected plants are tested, and (3) how the test data are interpreted and communicated to regulators. It is argued that the currently used centrifugal phylogenetic method for selecting test plant lists should be modernized to accommodate the many recent improvements in knowledge of plant phylogenetic relationships and insect host-choice evolution and behavior. The reliance on quarantine-based testing is briefly examined and low- and high-technology alternatives considered. Both these are rejected, at least in the short-term, as being impractical, and the use is proposed of comparative laboratory-based vs. open-field host tests against a few key nontarget species to proactively calibrate subsequent quarantine data and aid interpretation of results obtained under artificial conditions. While these improvements should help better translate host-test results to real-world outcomes, it is essential that there be increased transparency in the communication of these results to regulators, with discussions of different components of risk, such as localized vs. widespread and short-term collateral damage vs. long-term evolutionary impact. Harmonizing the tensions that currently impinge on biological control can only be achieved through improving the quality of information provided, which will help regulators make decisions that are based more on knowledge and less on the often ill-perceived fears of the public.     

Risk and ethics in biological control

All introduced natural enemies present a degree of risk to nontarget species. Since most biological control programs use relatively host-specific natural enemies, the risk to nontarget species is generally very low, particularly from biological control of weeds, which uses extensively tested and validated host-specificity testing procedures to predict risk. However, many of the published comments about risks of biological control are superficial or misleading, often inappropriately lumping risk from all taxa of agents as “the risk of biological control,” and ignore the potential benefits, rather than dealing with species-by-species risk and benefits. Particularly confounding accurate predictions is the common mixing of parameters of hazard and exposure in discussions of risk. In this paper, traditional risk analysis techniques are discussed and adapted for biological control. How people perceive risk is the key to understanding their attitude to risk. Some of the criticisms of biological control relating to inadequate post-release monitoring are valid and the ethical responsibilities of biological control scientists in this area are also discussed. Biological control scientists should address objectively the criticisms of biological control, continue to review and adjust current host-specificity testing procedures and make appropriate changes. This process will result in better science, ultimately delivering more focused programs, and altering the perception of risk from biological control agents by objective observers.     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

A two-phase open-field test to evaluate the host-specificity of candidate biological control agents for Heliotropium amplexicaule

This paper describes an open-field host-specificity test conducted to make a preliminary evaluation of the safety of four candidate agents for the biological control of Heliotropium amplexicaule, an invasive weed of South American origin. These agents were a leaf-eating beetle, Deuterocampta quadrijuga, a flea-beetle, Longitarsus sp., that feeds on leaves as an adult and roots as a larva, a shoot-feeding thrips, Haplothrips heliotropica, and a cell-sucking bug, Dictyla sp. During the first phase of the experiment, the four agents were given a choice between the target weed and six species of nontarget plant of varying degrees of phylogenetic relatedness. All four species were found to feed and reproduce on only H. amplexicaule and the closely related H. nicotianaefolium (a member of the same section of the genus Heliotropium). No plants outside this genus were attacked. For the second “no-choice” phase, the host-plants used in Phase 1 were cut, forcing the insects to use either other plant species within the plots, emigrate, or die of starvation. Heliothrips heliotropica disappeared rapidly from the plot, while D. quadrijuga persisted for several days on Heliotropium arborescens with some exploratory nibbling and then disappeared. Host-choice behavior of these species therefore remained unchanged, even in the absence of the primary host-plants. In contrast, adults of Longitarsus sp. rapidly colonized and fed on H. arborescens when the preferred hosts were removed. It therefore demonstrated a wider host-range under these more extreme conditions. In fact, on some plots, feeding commenced on H. arborescens before the “no-choice” phase, once the two preferred Heliotropium species were heavily damaged by these insects. The two-phase test is shown here to be a useful way of measuring host-choice behavior under “normal” conditions of choice and under more extreme conditions, such as it might occur were an agent to locally destroy the target weed following its release. It therefore provides a more refined assessment of the risk that would be posed to nontarget plants by the release of weed biological control agents.     

Exotic biological control agents: A solution or contribution to arthropod invasions?

Biological control is a valuable and effective strategy for controlling arthropod pests and has been used extensively against invasive arthropods. As one approach for control of invasives, exotic natural enemies  from the native range of a pest are introduced to areas where control is needed. Classical biological control began to be used in the late 1800s and its use increased until, beginning in 1983, scientists began raising significant concerns and questions about nontarget and indirect effects that can be caused by these introductions. In recent years, similar issues have been raised about augmentative use of exotic natural enemies. Subsequently, international guidelines, national regulations and scientific methods being used for exotic natural enemies in biological control have changed to require appropriate specificity testing, risk assessment and regulatory oversight before exotic natural enemies can be released. National and international standards aimed at minimizing risk have increased awareness and promoted more careful consideration of the costs and benefits associated with biological control. The barriers to the implementation of classical and augmentative biological control with exotic natural enemies now are sometimes difficult and, as a consequence, the numbers of classical biological control programs and releases have decreased significantly. Based in part on this new, more careful approach, classical biological control programs more recently undertaken are increasingly aimed at controlling especially damaging invasive arthropod pests that otherwise cannot be controlled. We examine evidence for these revised procedures and regulations aimed at increasing success and minimizing risk. We also discuss limitations linked to the apparent paucity of post-introduction monitoring and inherent unpredictability of indirect effects.     

Safety of Microorganisms Intended for Pest and Plant Disease Control: A Framework for Scientific Evaluation

Microorganisms are enormous but largely untapped natural resources for biological control of pests and diseases. There are two primary reasons for their underployment for pest or disease control: (1) the technical difficulties of using microorganisms for biological control, owing to a lack of fundamental information on them and their ecology, and (2) the costs of product development and regulatory approvals required for each strain, formulation, and use. Agriculture and forestry benefit greatly from the resident communities of microorganisms responsible for naturally occurring biological control of pest species, but additional benefits are achieved by introducing/applying them when or where needed. This can be done as (1) an inoculative release, (2) an augmentative application, or (3) an inundative application. Because of their specificity, different microbial biocontrol agents typically are needed to control different pests or the same pest in different environments. Four potential adverse effects are identified as safety issues (hazards) associated with the use of microorganisms for the biological control of plant pests and diseases. These are: (1) displacement of nontarget microorganisms, (2) allergenicity to humans and other animals, (3) toxigenicity to nontarget organisms, and (4) pathogenicity to nontarget organisms. Except for allergenicity, these are the same attributes that contribute to the efficacy of microbial biocontrol agents toward the target pest species. The probability of occurrence of a particular adverse nontarget effect of a microbial biocontrol agent may be a function of geographic origin or a specific trait genetically added or modified, but the safety issues are the still the same, including whether the microorganism intended for pest or disease control is indigenous, nonindigenous (imported and released), or genetically modified by traditional or recombinant DNA (rDNA) technology. Likewise, the probability of occurrence of a particular adverse nontarget effect may vary with method of application, e.g., whether as an aerosol, soil treatment, baits, or seed treatment, and may increase with increased scale of use, but the safety issues are still the same, including whether the microorganism is used for an inoculative release or augmentative or inundative application. Existing practices for managing microorganisms in the environment (e.g., plant pathogens,Rhizobium,plant inoculants) provide experience and options for managing the risks of microorganisms applied for pest and disease control. Moreover, experience to date indicates that any adverse nontarget effects, should they occur, are likely to be short-term or transitory effects that can, if significant, be eliminated by terminating use of the microbial biocontrol agent. In contrast, production agriculture as currently practiced, such as the use of tillage and crop rotations, has significant and long-term effects on nontarget organisms, including the intentional and unintentional displacement of microorganisms. Even the decision to leave plant pests and diseases unmanaged could have significant long-term environmental effects on nontarget organisms. Potential safety issues associated with the use of microbial biocontrol must therefore be properly identified and compared with the impact of other options for managing the pest or leaving the pest unmanaged. This paper provides a scientific framework for this process.     

Reproductive biology of invertebrates. Volumes I and II: Edited by K. G. Adiyodi and R. G. Adiyodi,Wiley, New York, 1983. 770 pp. and 692 pp. $110.00 and $94.00

Biological control agents (biorationals) are increasingly important in pest control concepts. Certain insect viruses, particularly the baculoviruses (nuclear polyhedrosis viruses), are considered to have potential as biological pesticides and could be used widely in the environment. Therefore, test animals must be selected and methods and laboratory systemsdeveloped to evaluate the safety of these agents to nontarget species. A simple laboratory system has been designed and used to determine risks of infectivity and pathogenicity of an insect Baculovirus, originally isolated from the Alfalfa looper, Autographa californica, to a nontarget arthropod, the grass shrimp, Palaemonetes vulgaris, by dietary exposure. This laboratory method also permits evaluation of other microbial biorationals against nontarget aquatic species, and provides an inexpensive standardized procedure of safety testing. Results from this study indicated that histopathological, ultrastructural, and serological methods used provided no evidence that experimental exposure to the virus in our test system caused viral infection or related pathogenicity in the grass shrimp.     

Risk and ethics in biological control

All introduced natural enemies present a degree of risk to nontarget species. Since most biological control programs use relatively host-specific natural enemies, the risk to nontarget species is generally very low, particularly from biological control of weeds, which uses extensively tested and validated host-specificity testing procedures to predict risk. However, many of the published comments about risks of biological control are superficial or misleading, often inappropriately lumping risk from all taxa of agents as “the risk of biological control,” and ignore the potential benefits, rather than dealing with species-by-species risk and benefits. Particularly confounding accurate predictions is the common mixing of parameters of hazard and exposure in discussions of risk. In this paper, traditional risk analysis techniques are discussed and adapted for biological control. How people perceive risk is the key to understanding their attitude to risk. Some of the criticisms of biological control relating to inadequate post-release monitoring are valid and the ethical responsibilities of biological control scientists in this area are also discussed. Biological control scientists should address objectively the criticisms of biological control, continue to review and adjust current host-specificity testing procedures and make appropriate changes. This process will result in better science, ultimately delivering more focused programs, and altering the perception of risk from biological control agents by objective observers.     

Field assessment of host plant specificity and potential effectiveness of a prospective biological control agent, Aceria salsolae, of Russian thistle, Salsola tragus

The eriophyid mite, Aceria salsolae de Lillo and Sobhian, is being evaluated as a prospective classical biological control agent of invasive alien tumbleweeds, including Salsola tragus, S. collina, S. paulsenii and S. australis, in North America. Previous laboratory experiments to determine the host specificity of the mite indicated that it could sometimes persist and multiply on some nontarget plants, including Bassia hyssopifolia and B. scoparia. These are both European plants whose geographic range overlaps that of the mite, but the mite has never been observed on them in the field. A field experiment was conducted in Italy to determine if the mite would infest and damage these plants under natural outdoor conditions. The results indicate that this mite does not attain significant populations on these nontarget plants nor does it significantly damage them. Salsola tragus was heavily infested by A. salsolae, and plant size was negatively correlated to the level of infestation. Although S. kali plants were also infested, their size did not appear to be affected by the mites. The other nontarget plants were not as suitable for the mite in the field as in previous laboratory experiments. We conclude that there would be no significant risk to nontarget plants as a result of using A. salsolae as a biological agent to control Salsola species in North America.     

Field host-specificity of the mile-a-minute weevil,Rhinoncomimus latipes Korotyaev (Coleoptera: Curculionidae)

The safe practice of biological control relies, in part, on an accurate evaluation of a potential agent’s host-specificity via testing through a “filter of safety”. The results of laboratory tests may differ from those obtained in open field host-specificity tests, where agents are able to use their full range of host-selection behaviors. It was hypothesized that Rhinoncomimus latipes (Coleoptera: Curculionidae), the biological control agent released against mile-a-minute weed, Persicaria perfoliata (Polygonaceae), would not feed or oviposit on nontarget plants in a two-phase, open field setting. Ten weevils were placed at the base of each of 13 test plant species in a randomized complete block design with six replicates. Weevils placed at the base of mile-a-minute weed were marked with yellow fluorescent dust, and yellow weevils were subsequently found only on mile-a-minute. Weevils placed at the base of nontarget plants (marked with red fluorescent dust) rapidly colonized mile-a-minute weed. Three hours after release, the number of R. latipes found on mile-a-minute weed was significantly higher than predicted by a random distribution of weevils on all test plants. The likelihood of finding more weevils on mile-a-minute compared to nontarget plant species was 31.0% at 3 h and increased to 96.5% at 44 h after release. Whereas prerelease studies showed feeding at low levels on 9 of the 13 plant species tested here, under open field conditions R. latipes did not feed on any nontarget plant species and dispersed from these plants. In an open field setting, where the weevil was able to use its full range of host-selection behaviors, there was no observed risk of nontarget effects for any species tested.     

Field assessment of the risk posed by Diorhabda elongata,a biocontrol agent for control of saltcedar (Tamarix spp.), to a nontarget plant,Frankenia salina

The biological control program for saltcedar (Tamarix spp.) has led to open releases of a specialist beetle (Chrysomelidae: Diorhabda elongata) in several research locations, but the controversy over potential impacts to native, nontarget plants of the genus Frankenia remains unresolved. To assess the potential for nontarget impacts under field conditions, we installed cultivated Frankenia spp. (primarily two forms of Frankenia salina but also including Frankenia jamesii) at locations in Nevada and Wyoming where D. elongata densities and saltcedar defoliation were expected to be very high, so insects would be near starvation with high probability of attacking nontargets if these were suitable hosts. Subsequent insect abundance was high, and only minor impact (<4% foliar damage) was observed on both forms of F. salina under these ‘worst case’ conditions; there was no impact to F. jamesii. No oviposition nor larval development were observed on any plants, there was no dieback of damaged F. salina stems, and plants continued growing once insect populations subsided. These results under ‘natural’ field conditions contrast with caged host-range tests in which feeding, development and minor oviposition occurred on the nontarget plant. Other ecological factors, such as distance from target plants to natural Frankenia spp. populations, inhospitable conditions for agent survival in such sites, and intrinsic insect behavior that makes colonization and/or genetic adaptation highly unlikely, lead us to conclude that nontarget impacts following program implementation will be insignificant or absent. Host range testing of new agents, while necessary to ensure safety, must put greater attention on assessing the ecological context where agents will be establishing, and on balancing speculated risks against potential benefits of biological control.     

Field assessment of the risk posed by Diorhabda elongata, a biocontrol agent for control of saltcedar (Tamarix spp.), to a nontarget plant, Frankenia salina

The biological control program for saltcedar (Tamarix spp.) has led to open releases of a specialist beetle (Chrysomelidae: Diorhabda elongata) in several research locations, but the controversy over potential impacts to native, nontarget plants of the genus Frankenia remains unresolved. To assess the potential for nontarget impacts under field conditions, we installed cultivated Frankenia spp. (primarily two forms of Frankenia salina but also including Frankenia jamesii) at locations in Nevada and Wyoming where D. elongata densities and saltcedar defoliation were expected to be very high, so insects would be near starvation with high probability of attacking nontargets if these were suitable hosts. Subsequent insect abundance was high, and only minor impact (<4% foliar damage) was observed on both forms of F. salina under these ‘worst case’ conditions; there was no impact to F. jamesii. No oviposition nor larval development were observed on any plants, there was no dieback of damaged F. salina stems, and plants continued growing once insect populations subsided. These results under ‘natural’ field conditions contrast with caged host-range tests in which feeding, development and minor oviposition occurred on the nontarget plant. Other ecological factors, such as distance from target plants to natural Frankenia spp. populations, inhospitable conditions for agent survival in such sites, and intrinsic insect behavior that makes colonization and/or genetic adaptation highly unlikely, lead us to conclude that nontarget impacts following program implementation will be insignificant or absent. Host range testing of new agents, while necessary to ensure safety, must put greater attention on assessing the ecological context where agents will be establishing, and on balancing speculated risks against potential benefits of biological control.     

The contribution of conservation biological control to integrated control of Bemisia tabaci in cotton

Integrated control systems are based on the complimentary contribution of chemical and biological control fostered by conservation of natural enemies. Yet, in the 50 years since the integrated control concept [ICC] [Stern, V.M., Smith, R.F., van den Bosch, R., Hagen, K.S., 1959. The integrated control concept. Hilgardia 29, 81–101] was introduced there are few operational programs and even fewer attempts to analyze the mechanisms that allow chemical and biological control to act in concert. The dearth of demonstrable evidence for the ICC has eroded the credibility of biological control and its usage in operational IPM plans. We used in situ life tables within an experimental design to measure and compare the contribution and interaction of biological control and insecticides as tactical components within three pest management systems for Bemisia tabaci (Gennadius) in cotton. Insecticides were the key factor immediately following applications of broad-spectrum materials or one of two selective insect growth regulators (IGRs), and this mortality replaced that provided by natural enemies. Two to six weeks later, however, mortality from natural enemies, primarily predation, in the IGR regimes rebounded to the high levels observed in untreated controls and became the key factor. Mortality from natural enemies remained depressed in the broad-spectrum insecticide regime. Single IGR applications were sufficient to suppress B. tabaci populations throughout the season, while up to five broad-spectrum applications were needed to achieve comparable control. The chemical residual of IGRs was limited to several weeks, demonstrating a key role for mortality from conserved natural enemies that extended the control interval. This “bioresidual” allows for long-term, commercially-acceptable pest suppression following the use of selective insecticides. We provide a rare experimental illustration of integrated control, where chemical and biological controls “augment one another”. Our approach and methodology could be applied to demonstrate and validate integrated control in many other systems, addressing a critical need for implementation of biological control in practicing IPM systems.     

Evaluation of cell substrates for the production of biologicals: Revision of WHO recommendations: Report of the WHO Study Group on Cell Substrates for the Production of Biologicals, 22–23 April 2009, Bethesda,USA

Evaluating cell substrates for producing vaccines and other biologicals is one of the critical aspects in assuring quality and safety of these products. As part of its mission in setting standards for biological products, WHO provides recommendations for manufacturing and evaluating biologicals. Regular updates of the guidance documents are important to manufacturers and regulators worldwide. WHO Expert Committee on Biological Standardization (ECBS) identified a need for revising the requirements for cell substrates (WHO TRS 878, annex 1). In response, WHO established a Study Group (SG) in 2006 that prepared an updated set of recommendations for using cell substrates for the production of biologicals. A summary of the proposed changes that the SG made in 2007 is available at WHO web site (http://www.who.int/biologicals/publications/meetings/areas/vaccines/cells/en/index.html). Draft revised recommendations were circulated to regulators, manufacturers and other experts for comments in April 2009.The SG held its third meeting on 22–23 April 2009 to review progress in the revision and to propose further improvements. In addition, the experts discussed the need for reference preparations, reference cell banks, and standardization of testing methodologies. The SG proposed clarifications of the rationale for in vivo testing as well as the potential for applying new methods for in vitro testing for detecting microbial agents. In line with this, WHO should conduct review of the current manufacturers' practice in using tests for microbial agents and interpreting these results. Additionally, WHO should take a lead in developing an International Standard for nucleic acid amplification test (NAT) for detecting mycoplasma contamination in cell substrates. WHO Collaborating Centers will lead this initiative, involving other relevant institutions in this area. Finally, advice on the replacement of the WHO Vero reference cell bank 10–87 with respect to the source of cells and re-characterization of the bank was provided. The intended use of the replacement cell bank would be the same as for the current cell bank, which is to serve as a source of well-characterized cells for establishing master cell banks for the production of biologicals. The SG will report outcomes of its discussion to the ECBS at its next meeting in October 2009 for further considerations and advice regarding the proposed course of action.     

Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants

Research on host specificity testing protocols over the last 10 years has been considerable. Traditional experimental designs have been refined and interpretation of the results is benefiting from an improved understanding of agent behavior. The strengths, weaknesses, and best practice for the different test types are now quite clearly understood. Understanding the concept of fundamental host range (the genetically determined limits to preference and performance) and using this to maximize reliability in predicting field host specificity following release (behavioral expression of the fundamental host range under particular conditions) are still inconsistently understood or adopted despite having been identified as the critical steps in analyzing the threats posed by biological control agents to the agriculture and biodiversity of novel environments. This needs to be consistently understood and applied so the process of testing can follow a recognized process of risk analysis from hazard identification (identifying life stages of the agent that pose a threat and defining their fundamental host range) to uncertainty analysis based on the magnitude (predicted field host specificity following release) and likelihood of threats (predicted actual damage and impact) to nontargets. Modern molecular techniques are answering questions associated with subspecific variation in biological control agents with respect to host use and the chance of host shifts of agents following release. Guidelines for assessment of nontarget impacts need to recognize and adopt such recent developments and emphasize a general increased understanding of the evolution of host choice and the phylogenetic constraints to shifts in host use. This review covers all these recent advances for the first time in one document, highlighting how inconsistent interpretation by biological control practitioners can be avoided.     

Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants

Research on host specificity testing protocols over the last 10 years has been considerable. Traditional experimental designs have been refined and interpretation of the results is benefiting from an improved understanding of agent behavior. The strengths, weaknesses, and best practice for the different test types are now quite clearly understood. Understanding the concept of fundamental host range (the genetically determined limits to preference and performance) and using this to maximize reliability in predicting field host specificity following release (behavioral expression of the fundamental host range under particular conditions) are still inconsistently understood or adopted despite having been identified as the critical steps in analyzing the threats posed by biological control agents to the agriculture and biodiversity of novel environments. This needs to be consistently understood and applied so the process of testing can follow a recognized process of risk analysis from hazard identification (identifying life stages of the agent that pose a threat and defining their fundamental host range) to uncertainty analysis based on the magnitude (predicted field host specificity following release) and likelihood of threats (predicted actual damage and impact) to nontargets. Modern molecular techniques are answering questions associated with subspecific variation in biological control agents with respect to host use and the chance of host shifts of agents following release. Guidelines for assessment of nontarget impacts need to recognize and adopt such recent developments and emphasize a general increased understanding of the evolution of host choice and the phylogenetic constraints to shifts in host use. This review covers all these recent advances for the first time in one document, highlighting how inconsistent interpretation by biological control practitioners can be avoided.     

Building Taxon Substitution Guidelines on a Biological Control Foundation

When a species becomes extinct, its ecological functions are lost as well. Taxon substitution is a controversial approach to restoring such functions via introduction of non‐native species known to serve similar functions elsewhere. Due to the possibility of nontarget effects from such introductions, taxon substitution has been proposed and implemented in only a few systems, but these attempts have successfully restored functions. As a conservation tool, taxon substitution bears similarity to biological control, wherein species are also introduced for their ecological function with consideration of potential nontarget effects. To improve both the safety and efficacy of taxon substitution, regulatory bodies that currently issue guidelines for biological control can do the same for taxon substitution. Indeed, many biological control guidelines would apply well to taxon substitution. We examine the standard practices followed by biological control programs and propose corresponding taxon substitution guidelines. Integration of taxon substitution into the existing national and international environmental management conversation will improve the tool and has the potential to enhance conservation efforts across a wide diversity of systems if appropriate and stringent precautions are taken.