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biological control: Communities without parasitoids?
Available online at www.sciencedirect.com
ScienceDirect Editorial overview: Parasites/parasitoids/biological control: Communities without parasitoids? Paul J Ode and George E Heimpel Current Opinion in Insect Science 2016, 14:viii–x For a complete overview see the Issue Available online 19th March 2016 http://dx.doi.org/10.1016/j.cois.2016.03.006 2214-5745/# 2016 Elsevier Inc. All rights reserved.
Paul J Ode
Colorado State University, Bioagricultural Sciences & Pest Management, The Graduate Degree Program in Ecology, Fort Collins, CO 80523-1177, United States e-mail: [email protected] Paul J Ode is an associate professor in the Department of Bioagricultural Sciences and Pest Management at Colorado State University. His primary research interests are in the study of multitrophic interactions involving plant defense chemistry, insect herbivores, and their parasitoids. He is particularly interested in how plant defense chemistry influences host–parasitoid interactions as well as competition among parasitoids.
George E Heimpel
University of Minnesota, Department of Entomology, St. Paul, MN 55108 United States George E Heimpel is a Distinguished McKnight University professor of entomology at the University of Minnesota in the United States. He has been studying parasitoids and their importance to biological control in various contexts for over 20 years. Particular interests include sex determination in braconid parasitoids, physiological status and host-use patterns in parasitoids and the dynamics of parasitoid host specificity.
Current Opinion in Insect Science 2016, 14:viii–x
‘‘Find one in every car. You’ll see’’ was Miller’s (played by Tracey Walter) description of the ubiquitous Little Trees1 pine tree air fresheners in Alex Cox’s 1984 cult classic ‘Repo Man’. This description could equally apply to parasitoids attacking their insect hosts as a great majority of insect species as well as many other arthropod species (e.g., spiders) has a parasitoid species that can attack it. Insect parasitoids are parasitic as immatures, developing on a single host individual usually killing it, but as adults are free-living. Parasitoids are incredibly numerous and diverse. Approximately 10–25% of all insects are thought to be parasitoids [1,2] with as many as 2 million species worldwide [3], most of which remain undescribed. The majority of parasitoids (80% of known species) are in the order Hymenoptera, another 15% or so belonging to the Diptera, and the remaining species are found in five additional insect orders [2]. Certainly, much of the species diversity among the parasitoids is due to the typically high degree of host specificity. Yet, for all their acknowledged species richness and ubiquity, parasitoids are relatively underappreciated (and understudied) in their role in structuring communities. Given that plant–insect herbivore and pollinator interactions are some of the most dominant (in terms of number of species involved), parasitoids would be expected to have a key role in structuring communities. If we define communities as systems in which at least three species interact, parasitoids clearly play roles in a wide range of systems including plant– insect herbivore–parasitoid interactions, host–parasitoid–microbe interactions, intra-guild predation and competition, etc. Indeed, Price et al. [4] clearly advocated for incorporating parasitoids into studies of plant-herbivore interactions. Although several older reviews of parasitoid community ecology exist (e.g., [5,6]), most studies of trophic interactions focus primarily on bi-trophic relationships (e.g., plant–herbivore, host–parasitoid), or treat parasitoids as passive participants that ‘go along for the ride’ in more complex communities. Yet, as the seven reviews in this issue highlight, parasitoids can play important, if not central, roles in structuring the broader communities in which they exist. We attempt to fill some of the gaps in parasitoid community ecology in this issue. As Stireman points out in his review, the community ecology of nonhymenopteran parasitoids is vastly understudied compared to the hymenopteran parasitoids, even accounting for the fact that the number of hymenopteran parasitoid species outnumbers non-hymenopteran parasitoids by 4:1. Non-hymenopteran parasitoids differ from hymenopteran parasitoids in several respects that can alter their functioning in communities including the lack of a sclerotized, appendicular ovipositor (allowing wasps to lay eggs inside a host and find concealed hosts as well as delivery of www.sciencedirect.com
Editorial overview Ode and Heimpel ix
venoms into the host) resulting in very different parasitism strategies that affect host ranges and habitat use, which in turn influence community structure. For instance, many tachinid parasitoids that lay eggs on their hosts are restricted to attacking exposed hosts, while in other species the larvae actively search for hosts, taking some of the pressure of host-finding off the adult females. Apart from tachinids and phorids, little is known about host range and food webs of non-hymenopteran parasitoids. Clearly, much more work needs to be done to understand communities involving non-hymenopteran parasitoids. One promising area of research to elucidate the structure of parasitoid food webs involves the use of molecular tools to elucidate the structure of food webs involving such parasitoids. As Stireman points out, this can greatly advance our understanding of understudied groups such as the non-hymenopteran parasitoids. van Nouhuys explores this further in her review of the use of neutral genetic markers, in particular DNA barcoding, to study community and population structure as well as individual mating and dispersal behaviors. These highly sensitive techniques can detect parasitoid remains within hosts and vice versa as well as intra-guild predation. As more hostparasitoid communities are studied, it is becoming apparent that they are typically far more species-rich and complex than previously realized.
parasitoids are rare, they do exist and more examples are likely to be uncovered as more attention is devoted to this phenomenon. Whether such facilitation exists because of enhanced access to host nutrients or enhanced suppression of host immune responses needs to be explored further. Kaser and Ode extend this topic further by reviewing how parasitoids can mediate indirect interactions between herbivores. The most commonly documented natural enemy-mediated indirect interactions occur when the presence of one herbivore population increases the carrying capacity of a natural enemy, which then suppresses the population of a second, preferred herbivore. If the role of the natural enemy is ignored, or underestimated, the first herbivore would appear to be the stronger competitor — so-called ‘apparent competition’. Such indirect effects may generate a range of additional indirect interactions including apparent parasitism, commensalism, amensalism, or even mutualism. Current risk assessment procedures for screening prospective biological control agents focus on minimizing non-target impacts. Equally important, but rarely considered, is the range of community interactions in which imported natural enemies will likely engage. Not only do such studies provide direction in terms of how biological control programs can be managed and improved, they provide valuable insight into how species interactions involving parasitoids can structure communities. Furthermore, hyperparasitoids (parasitoids of parasitoids) can bring about similar indirect interactions among parasitoids.
The remaining five reviews in this issue explore the complexities of interspecific interactions involving parasitoids embebed within species-rich communities. Studies of the behavioral and population-level phenomena underpinning species linkages in such systems can provide important insight into the functioning and maintenance of these communities. The review by Tena et al. focuses on how the presence of honeydew produced by phloem-feeding herbivores (e.g., aphids and some scale insects) influences parasitoid–host population dynamics — sometimes involving the herbivore producing the honeydew, but many times not. Honeydew can be a critical source of nutrition for adult parasitoids. Yet, honeydew has its dark side; it can attract other predators (notably, ants), can be an important habitat for insect pathogens (along with the better-known plant pathogens), or potentially (albeit, yet to be demonstrated) be a reservoir of excreted plant chemicals — all of which can have negative effects on parasitoids. Tena and colleagues then explore how these variables can be applied to improve conservation biological control efforts.
Frago continues this line of inquiry into the role of intraguild predation and the effects of hyperparasitoids. A key message from this review is that longer-term (multi-generational) studies on more complex communities are necessary to fully understand emergent properties of diverse guilds of natural enemies on lower trophic levels. For instance, the presence of hyperparasitoids can shift the dominance, in terms of controlling an herbivore population, from one parasitoid to another. Furthermore, spatial complexity of the habitats in which communities occur can enhance stability and diversity of intraguild and interguild interactions and these can shift seasonally, again pointing to the need for multigenerational studies. Most studies addressing these questions have been conducted in agricultural ecosystems, which are inherently simplistic compared to natural ecosystems. Yet, Frago makes a compelling case for the idea that our understanding of community structure and function will be greatly enhanced by studying more complex, multi-generational systems.
The review by Cusumano et al. also focuses on biological control, this time from the perspective of competition, and even facilitation, between parasitoids. Competition between parasitoids may occur between adults foraging for suitable hosts as well as between larvae developing within the same host. While cases of facilitation among
Finally, Kaplan et al. examine the indirect tri-trophic interactions between plants (especially, plant defensive chemistry) and parasitoids that are mediated by herbivore physiology. Plant defensive chemistry may negatively affect developing parasitoids either directly if parasitoids encounter unmetabolized (or even sequestered) plant
www.sciencedirect.com
Current Opinion in Insect Science 2016, 14:viii–x
x Parasites/Parasitoids/Biological control
chemicals in the hemolymph of their hosts or indirectly if plant chemistry reduces host quality. More recently, it has been recognized that plant chemistry can interfere with the host’s ability to mount a successful immune response. Kaplan and colleagues also consider the effects of plant tolerance as a response to herbivory and its consequences for parasitoid success. In many respects, the implications of tolerance vs. resistance are expected to have very different outcomes for host-parasitoid relationships, although this idea is ripe for exploration. To date, very little attention has been paid to whether parasitoids influence plant investment in defense, although tantalizing clues suggest that these relationships exist in at least some systems. How pervasive these relationships are remains to be seen; yet, their potential to reshape how we view multi-trophic communities is very great.
broader spatial and temporal scales. More attention needs to be given to the role of parasitoids in affecting top-down control of herbivore populations; are parasitoids movers and shakers or are they passive participants — simply responding to the conditions to set by lower trophic levels? Only future research will tell. However, it is clear that the more we study the role of parasitoids in terrestrial arthropod communities, the more central these roles seem to be.
The following collection of seven reviews highlight what is unknown and understudied as much as they identify what is known. For instance, far more attention ought to be given to non-hymenopteran parasitoids as they present life histories and challenges very different from the hymenopteran parasitoids. More studies need to be conducted on more complex food web systems across multiple generations. These are needed to more fully understand the complexities of communities across
Current Opinion in Insect Science 2016, 14:viii–x
References 1.
LaSalle J, Gauld ID: Parasitic Hymenoptera and the biodiversity crisis. Redia 1991, 74:315-334.
2.
Eggleton P, Belshaw R: Insect parasitoids: an evolutionary overview. Philos Trans R Soc Lon B 1992, 337:1-20.
3.
Godfray HCJ: Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press; 1994.
4.
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE: Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 1980, 11:41-65.
5.
Lawton JH: The effect of parasitoids on phytophagous insect communities. In Insect Parasitoids. Edited by Waage J, Greathead D. Academic Press; 1986:265-287.
6.
Hawkins BA, Sheehan W: Parasitoid Community Ecology. Oxford: Oxford University Press; 1994.
www.sciencedirect.com
ScienceDirect Editorial overview: Parasites/parasitoids/biological control: Communities without parasitoids? Paul J Ode and George E Heimpel Current Opinion in Insect Science 2016, 14:viii–x For a complete overview see the Issue Available online 19th March 2016 http://dx.doi.org/10.1016/j.cois.2016.03.006 2214-5745/# 2016 Elsevier Inc. All rights reserved.
Paul J Ode
Colorado State University, Bioagricultural Sciences & Pest Management, The Graduate Degree Program in Ecology, Fort Collins, CO 80523-1177, United States e-mail: [email protected] Paul J Ode is an associate professor in the Department of Bioagricultural Sciences and Pest Management at Colorado State University. His primary research interests are in the study of multitrophic interactions involving plant defense chemistry, insect herbivores, and their parasitoids. He is particularly interested in how plant defense chemistry influences host–parasitoid interactions as well as competition among parasitoids.
George E Heimpel
University of Minnesota, Department of Entomology, St. Paul, MN 55108 United States George E Heimpel is a Distinguished McKnight University professor of entomology at the University of Minnesota in the United States. He has been studying parasitoids and their importance to biological control in various contexts for over 20 years. Particular interests include sex determination in braconid parasitoids, physiological status and host-use patterns in parasitoids and the dynamics of parasitoid host specificity.
Current Opinion in Insect Science 2016, 14:viii–x
‘‘Find one in every car. You’ll see’’ was Miller’s (played by Tracey Walter) description of the ubiquitous Little Trees1 pine tree air fresheners in Alex Cox’s 1984 cult classic ‘Repo Man’. This description could equally apply to parasitoids attacking their insect hosts as a great majority of insect species as well as many other arthropod species (e.g., spiders) has a parasitoid species that can attack it. Insect parasitoids are parasitic as immatures, developing on a single host individual usually killing it, but as adults are free-living. Parasitoids are incredibly numerous and diverse. Approximately 10–25% of all insects are thought to be parasitoids [1,2] with as many as 2 million species worldwide [3], most of which remain undescribed. The majority of parasitoids (80% of known species) are in the order Hymenoptera, another 15% or so belonging to the Diptera, and the remaining species are found in five additional insect orders [2]. Certainly, much of the species diversity among the parasitoids is due to the typically high degree of host specificity. Yet, for all their acknowledged species richness and ubiquity, parasitoids are relatively underappreciated (and understudied) in their role in structuring communities. Given that plant–insect herbivore and pollinator interactions are some of the most dominant (in terms of number of species involved), parasitoids would be expected to have a key role in structuring communities. If we define communities as systems in which at least three species interact, parasitoids clearly play roles in a wide range of systems including plant– insect herbivore–parasitoid interactions, host–parasitoid–microbe interactions, intra-guild predation and competition, etc. Indeed, Price et al. [4] clearly advocated for incorporating parasitoids into studies of plant-herbivore interactions. Although several older reviews of parasitoid community ecology exist (e.g., [5,6]), most studies of trophic interactions focus primarily on bi-trophic relationships (e.g., plant–herbivore, host–parasitoid), or treat parasitoids as passive participants that ‘go along for the ride’ in more complex communities. Yet, as the seven reviews in this issue highlight, parasitoids can play important, if not central, roles in structuring the broader communities in which they exist. We attempt to fill some of the gaps in parasitoid community ecology in this issue. As Stireman points out in his review, the community ecology of nonhymenopteran parasitoids is vastly understudied compared to the hymenopteran parasitoids, even accounting for the fact that the number of hymenopteran parasitoid species outnumbers non-hymenopteran parasitoids by 4:1. Non-hymenopteran parasitoids differ from hymenopteran parasitoids in several respects that can alter their functioning in communities including the lack of a sclerotized, appendicular ovipositor (allowing wasps to lay eggs inside a host and find concealed hosts as well as delivery of www.sciencedirect.com
Editorial overview Ode and Heimpel ix
venoms into the host) resulting in very different parasitism strategies that affect host ranges and habitat use, which in turn influence community structure. For instance, many tachinid parasitoids that lay eggs on their hosts are restricted to attacking exposed hosts, while in other species the larvae actively search for hosts, taking some of the pressure of host-finding off the adult females. Apart from tachinids and phorids, little is known about host range and food webs of non-hymenopteran parasitoids. Clearly, much more work needs to be done to understand communities involving non-hymenopteran parasitoids. One promising area of research to elucidate the structure of parasitoid food webs involves the use of molecular tools to elucidate the structure of food webs involving such parasitoids. As Stireman points out, this can greatly advance our understanding of understudied groups such as the non-hymenopteran parasitoids. van Nouhuys explores this further in her review of the use of neutral genetic markers, in particular DNA barcoding, to study community and population structure as well as individual mating and dispersal behaviors. These highly sensitive techniques can detect parasitoid remains within hosts and vice versa as well as intra-guild predation. As more hostparasitoid communities are studied, it is becoming apparent that they are typically far more species-rich and complex than previously realized.
parasitoids are rare, they do exist and more examples are likely to be uncovered as more attention is devoted to this phenomenon. Whether such facilitation exists because of enhanced access to host nutrients or enhanced suppression of host immune responses needs to be explored further. Kaser and Ode extend this topic further by reviewing how parasitoids can mediate indirect interactions between herbivores. The most commonly documented natural enemy-mediated indirect interactions occur when the presence of one herbivore population increases the carrying capacity of a natural enemy, which then suppresses the population of a second, preferred herbivore. If the role of the natural enemy is ignored, or underestimated, the first herbivore would appear to be the stronger competitor — so-called ‘apparent competition’. Such indirect effects may generate a range of additional indirect interactions including apparent parasitism, commensalism, amensalism, or even mutualism. Current risk assessment procedures for screening prospective biological control agents focus on minimizing non-target impacts. Equally important, but rarely considered, is the range of community interactions in which imported natural enemies will likely engage. Not only do such studies provide direction in terms of how biological control programs can be managed and improved, they provide valuable insight into how species interactions involving parasitoids can structure communities. Furthermore, hyperparasitoids (parasitoids of parasitoids) can bring about similar indirect interactions among parasitoids.
The remaining five reviews in this issue explore the complexities of interspecific interactions involving parasitoids embebed within species-rich communities. Studies of the behavioral and population-level phenomena underpinning species linkages in such systems can provide important insight into the functioning and maintenance of these communities. The review by Tena et al. focuses on how the presence of honeydew produced by phloem-feeding herbivores (e.g., aphids and some scale insects) influences parasitoid–host population dynamics — sometimes involving the herbivore producing the honeydew, but many times not. Honeydew can be a critical source of nutrition for adult parasitoids. Yet, honeydew has its dark side; it can attract other predators (notably, ants), can be an important habitat for insect pathogens (along with the better-known plant pathogens), or potentially (albeit, yet to be demonstrated) be a reservoir of excreted plant chemicals — all of which can have negative effects on parasitoids. Tena and colleagues then explore how these variables can be applied to improve conservation biological control efforts.
Frago continues this line of inquiry into the role of intraguild predation and the effects of hyperparasitoids. A key message from this review is that longer-term (multi-generational) studies on more complex communities are necessary to fully understand emergent properties of diverse guilds of natural enemies on lower trophic levels. For instance, the presence of hyperparasitoids can shift the dominance, in terms of controlling an herbivore population, from one parasitoid to another. Furthermore, spatial complexity of the habitats in which communities occur can enhance stability and diversity of intraguild and interguild interactions and these can shift seasonally, again pointing to the need for multigenerational studies. Most studies addressing these questions have been conducted in agricultural ecosystems, which are inherently simplistic compared to natural ecosystems. Yet, Frago makes a compelling case for the idea that our understanding of community structure and function will be greatly enhanced by studying more complex, multi-generational systems.
The review by Cusumano et al. also focuses on biological control, this time from the perspective of competition, and even facilitation, between parasitoids. Competition between parasitoids may occur between adults foraging for suitable hosts as well as between larvae developing within the same host. While cases of facilitation among
Finally, Kaplan et al. examine the indirect tri-trophic interactions between plants (especially, plant defensive chemistry) and parasitoids that are mediated by herbivore physiology. Plant defensive chemistry may negatively affect developing parasitoids either directly if parasitoids encounter unmetabolized (or even sequestered) plant
www.sciencedirect.com
Current Opinion in Insect Science 2016, 14:viii–x
x Parasites/Parasitoids/Biological control
chemicals in the hemolymph of their hosts or indirectly if plant chemistry reduces host quality. More recently, it has been recognized that plant chemistry can interfere with the host’s ability to mount a successful immune response. Kaplan and colleagues also consider the effects of plant tolerance as a response to herbivory and its consequences for parasitoid success. In many respects, the implications of tolerance vs. resistance are expected to have very different outcomes for host-parasitoid relationships, although this idea is ripe for exploration. To date, very little attention has been paid to whether parasitoids influence plant investment in defense, although tantalizing clues suggest that these relationships exist in at least some systems. How pervasive these relationships are remains to be seen; yet, their potential to reshape how we view multi-trophic communities is very great.
broader spatial and temporal scales. More attention needs to be given to the role of parasitoids in affecting top-down control of herbivore populations; are parasitoids movers and shakers or are they passive participants — simply responding to the conditions to set by lower trophic levels? Only future research will tell. However, it is clear that the more we study the role of parasitoids in terrestrial arthropod communities, the more central these roles seem to be.
The following collection of seven reviews highlight what is unknown and understudied as much as they identify what is known. For instance, far more attention ought to be given to non-hymenopteran parasitoids as they present life histories and challenges very different from the hymenopteran parasitoids. More studies need to be conducted on more complex food web systems across multiple generations. These are needed to more fully understand the complexities of communities across
Current Opinion in Insect Science 2016, 14:viii–x
References 1.
LaSalle J, Gauld ID: Parasitic Hymenoptera and the biodiversity crisis. Redia 1991, 74:315-334.
2.
Eggleton P, Belshaw R: Insect parasitoids: an evolutionary overview. Philos Trans R Soc Lon B 1992, 337:1-20.
3.
Godfray HCJ: Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press; 1994.
4.
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE: Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 1980, 11:41-65.
5.
Lawton JH: The effect of parasitoids on phytophagous insect communities. In Insect Parasitoids. Edited by Waage J, Greathead D. Academic Press; 1986:265-287.
6.
Hawkins BA, Sheehan W: Parasitoid Community Ecology. Oxford: Oxford University Press; 1994.
www.sciencedirect.com