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[ The harlequin bug (Murgantia histrionica; top left) is a specialist herbivore on Isomeris arborea, an endemic plant species of the California coastal sage scrub ecosystem (top right). The bug's eggs (bottom center) are parasitized by two parasitoid natural enemies, Trissolcus murgantiae (bottom left) and Ooencyrtus johnsonii (bottom right). The harlequin bug and its parasitoids exhibit many attributes of pest-enemy systems in general, and of Homopteran pest systems in particular. First, the bug is a specialist herbivore on a long-lived host plant, similar to many Homopteran pests that attack long-lived crop plants (e.g., citrus, olive, stone fruits), and its only natural enemies are the two specialist parasitoids. Second, the bug and parasitoids exhibit the same life history and population dynamics as Homopteran pest systems, with an invulnerable adult stage of the herbivore and a persistent host-parasitoid interaction with host densities maintained at low levels. Third, the parasitoids engage in the same types of interactions as the natural enemies of Homopteran pests (exploitative competition and multiparasitism). Fourth, the bug is a minor pest of crucifers in the southeastern U.S. and the parasitoids are potential control agents. These attributes make this community an ideal model system for investigating the efficacy of natural enemies in pest suppression. ]
Kidd, D. & Amarasekare, P. (2012) The role of transient dynamics in biological pest control: insights from a host–parasitoid community. Journal of Animal Ecology, 81, 47–57.
Our current understanding of host–parasitoid relationships has been strongly influenced by the quest for stability and persistence, and consequently, is based on a large body of theory that has focused on the assumption of equilibrium dynamics. In an elegant analysis of a host–parasitoid model parameterized from laboratory observations, Kidd & Amarasekare broaden our understanding by contrasting the parameters that influence transient versus equilibrium dynamics. Their study highlights the importance of parasitoid handling time, competitive exclusion and intraspecific interference in the transient dynamics of a model host–parasitoid community.
Biological pest control, the suppression of a pest population by natural enemies, is one aspect of the broader theory of consumer–resource relationships that has been widely used in the population management of invasive arthropod pests. The historical record of biological pest control has documented some spectacular successes in the suppression of invasive pests through deliberate introductions of specialized natural enemies from the invader’s region of origin. One of the earliest and best known examples is the introduction of the vedalia beetle from Australia for suppression of the cottony cushion scale that was ravaging the burgeoning citrus industry in California toward the end of the 19th Century (Caltagirone & Doutt 1989). However, the historical record also clearly documents a greater frequency of failures in which the natural enemies fail to suppress the target pest in the recipient range. As examples of large-scale experiments in population ecology, the successes and failures of introductions for biological pest control have long been a source of inspiration for theoretical ecologists (e.g. Thompson 1929; Nicholson & Bailey 1935; Hassell 1978; Murdoch, Briggs & Nisbet 2003). An extensive theoretical literature has provided a valuable framework for understanding the dynamics of host–parasitoid interactions (Mills & Getz 1996; Murdoch, Briggs & Nisbet 2003; Briggs 2009), but surprisingly little progress has been made in identifying opportunities to improve the success of biological control introductions (Mills 2006; Murdoch 2009).
In this issue, Kidd & Amarasekare (2012) provide some remarkable new insights that serve both to illuminate and to reinvigorate what had become a rather static period in the analysis of host–parasitoid relationships. By drawing attention to the simple premise that equilibrium might never be achieved in agricultural systems because of frequent management disturbance, they argue that insights from the shorter-term transient dynamics of host–parasitoid interactions could be even more informative than those from the longer-term equilibrium dynamics. They base their study on the harlequin bug (Murgantia histrionica) and its two specialist egg parasitoids Telenomus and Ooencyrtus as a model host–parasitoid community (see Fig. 1). Initially, they use laboratory observations of parasitoid functional responses (number of hosts attacks in relation to host density) and conversion efficiencies (offspring per host attacked) to parameterize a simple population model. Subsequently, they examine the transient and equilibrium dynamics of the model to evaluate the extent of host suppression by the two parasitoids.
Based on the assumption that agricultural disturbance leads to the dominance of transient dynamics in host–parasitoid systems, three key novel insights arise from this study that have implications for the practice of biological pest control. First, the parameters of the parasitoid functional response and conversion efficiency that lead to greater host suppression differ between transient and equilibrium dynamics. Second, the use of multiple parasitoids could compromise the success of biological pest control if a species that induces greater transient fluctuations in pest abundance can exclude another that induces weaker transient fluctuations. Third, while intraspecific parasitoid interference compromises the degree of pest suppression at equilibrium, it could be more beneficial in reducing the magnitude and duration of transient fluctuations in pest abundance.
The first insight arises from transient dynamics, an issue that has broad relevance for ecological systems (Hastings 2004) and has been gaining greater application in conservation biology for predicting the response of managed populations to disturbance (Ezard et al. 2010) as well as in biological pest control (Mills 2001). The high frequency of disturbance in agricultural systems can often prevent the local persistence of pests and/or parasitoids, and result in host–parasitoid dynamics that are better described as a transient interaction. In an elegant analysis of their parameterized model, Kidd & Amarasekare (2012) show that the greatest host suppression at equilibrium is achieved by the parasitoid (Ooencyrtus) with the highest attack rate and conversion efficiency. In contrast, however, the parasitoid (Telenomus) with the shortest handling time (time taken to complete the attack of a single host individual) generates the lowest fluctuation in transient host abundance. This distinction is strongest when negative density dependence in the host population is weak, a scenario that might well apply to agricultural systems where pests are unlikely to experience much resource limitation.
The transient dynamics of the model are characterized by oscillations induced by the inverse density dependence that arises from a saturating functional response. The amplitude and duration of the oscillations in host population abundance are driven by the interplay between negative density dependence and risk of parasitism. In the model used by the authors, the risk of parasitism is primarily influenced by parasitoid handling time, which determines the per-capita number of hosts attacked when the functional response saturates at higher host densities. However, the question of whether the reproductive success of insect parasitoids is limited solely by the time available to locate hosts (i.e. through handling time), or additionally by the availability of mature eggs, has been a topic of much recent debate (Rosenheim 2011). Nonetheless, in addition to the efficiency of resource use through host attack and conversion, an effective parasitoid for use in biological pest control might also need a functional response that saturates at a high per-capita attack rate. While such linkages between traits might indeed be constrained by life history trade-offs, as noted by the authors, this insight provides an interesting new perspective for evaluating the most effective parasitoids for use in biological pest control.
The question of multiple introductions in biological pest control and the coexistence of specialist consumers on a single limiting resource has been a long-standing debate in ecology since the classic Lotka-Volterra competition model was advanced in the 1920s. Kidd & Amarasekare (2012) contribute to this debate by adding a second insight that the greater resource-use efficiency of a parasitoid that provides more effective host suppression at equilibrium can also lead to the rapid exclusion of another parasitoid that could provide better suppression of transient oscillations. Although the biological pest control record does provide examples of competitive displacement, parasitoid coexistence is also common in nature and can be mediated by multiple factors that include parasitoid density dependence (Murdoch, Briggs & Nisbet 2003), intraguild predation (Amarasekare 2000) and both temporal (Amarasekare 2007) and spatial (Bonsall et al. 2004) niche partitioning among parasitoids. At present, whether the potential for detrimental effects of competitive exclusion in the short term is real or results from a model that is too simplified to represent the complexities of natural systems is not clear, but the point is well taken and deserves greater attention through future research.
Density dependence through intraspecific parasitoid interference has long been considered an important stabilizing factor in host–parasitoid interactions (Hassell & Varley 1969), although it is detrimental to the goal of biological pest control because of the classic trade-off between stability and host suppression (Murdoch, Briggs & Nisbet 2003). However, in a more disturbed agricultural environment where transient dynamics tend to dominate, Kidd & Amarasekare (2012) show that as a stabilizing mechanism, parasitoid interference might actually be beneficial by helping to dampen the transient oscillations induced by a saturating functional response. While parasitoid interference has been well-documented under captive laboratory conditions (Hassell 1978), we have yet to understand fully its broader importance in the field (Bernstein 2000). One of the main reasons for this is that, in a spatially heterogeneous environment, parasitoid movement creates a tight linkage between interference and the aggregative response of parasitoids to host density among patches (Mills & Wajnberg 2008). Whether this tight linkage would allow the same stabilization of transient oscillations in a spatially explicit model, as found in the local model of Kidd & Amarasekare (2012), remains unknown, but the potential generality of their insight is once again both appealing and novel.
The three new insights obtained by Kidd & Amarasekare (2012) from the premise that transient dynamics tend to dominate in disturbed agricultural environments provide a refreshing perspective that will undoubtedly stimulate renewed interest in host–parasitoid dynamics. However, the model used by the authors is necessarily simplified and ignores other aspects of host–parasitoid systems such as stage structure, spatial and temporal heterogeneity, and host refuges from parasitism. In addition, Childs, Bonsall & Rees (2004) have argued that agricultural disturbance leads to increased demographic stochasticity, which can also influence the degree of host suppression and parasitoid persistence. Thus, while Kidd & Amarasekare (2012) have introduced an exciting new perspective that broadens our understanding of hostparasitoid relationships, the implications of this study for the practice of biological pest control are less clear. One advantage of hypotheses generated from transient dynamics is that they are much more amenable to experimental testing and validation than has been the case for corresponding insights obtained from equilibrium models (Hastings 2004). However, the practical value of these novel insights for biological pest control will depend on the ease with which the various parameters can be measured in the evaluation of potential biological control agents and on the relative importance of extrinsic (disturbance) versus intrinsic (transient dynamics) factors as drivers of pest abundance in specific agricultural environments.