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Generalist caterpillars are attacked by both predators (e.g., black-capped chickadee feeding on a caterpillar, on left) and parasitoids (e.g., generalist noctuid Himella intractata Morrison (currently, H. fidelis Grote) parasitized by a hymenopteran parasitoid, on right). Photographs: left by C. Skorik, right by M.S.S. (Online Þgure in color.)
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Natural enemies often cause significant levels of mortality for their prey and thus can be important agents of natural selection. It follows, then, that selection should favor traits that enable organisms to escape from their natural enemies into "enemy-free space" (EFS). Natural selection for EFS was originally proposed as a general force in struc...
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Context 1
... the larval parasitoidÕs exposure to bird predation while in the host. To test these predictions, we examined data from a forest food web constructed by Singer and colleagues in Middlesex County, CT, in late springÐ early summer (MayÐJune; Singer et al. 2012). An assemblage of dietary generalist caterpillars occupying eight different tree taxa ( Acer rubrum L., Betula lenta L., Carya spp., Fagus grandifolia Ehrhart, Hamamelis virginiana L., Prunus serotina Ehrhart, Quercus alba L., and Quercus rubra L.) served as the hosts for parasitoids, with caterpillars and parasitoids subjected to concomitant predation by insectivorous birds ( Fig. 4). To determine the frequency of parasitism of each caterpillar species on each tree species, we systematically collected caterpillars from haphazardly chosen branches, reared the caterpillars in the laboratory on the same tree species from which they were collected, and tallied the proportion of caterpillars that yielded parasitoid ßies and wasps (see full methods in Farkas and Singer 2013). These data were collected over Þve Þeld seasons (2004 Ð2008) at three forest sites separated by Ͼ 10 km (Cockaponset State Forest, Haddam; Hurd State Park, East Hampton; MillerÕs Pond State Park, Durham, CT). To determine the magnitude of bird predation of caterpillars on each tree species, we collected caterpillars from tree branches with bird exclosures along with caterpillars from paired control branches lacking exclosures (for full methods, see Singer et al. 2012). This same general methodology of bird exclusion has been used in Ͼ 50 previous studies to quantify the effect of bird predation on arthropods (Mooney et al. 2010). In our study, bird exclosures were in place over a 3-wk period before caterpillar collection; these exclosures permit access by insects (including parasitoids) but keep out birds and most other vertebrate predators. Caterpillar densities on each branch were calculated as the number of caterpillars/total leaf area of the branch. Total leaf area for each branch was estimated as the number of leaves multiplied by the average leaf area (mean area of 10 undamaged leaves randomly sampled from each branch). The magnitude of bird predation was expressed per pair of branches as a log response ratio: ln(caterpillar density without birds/caterpillar density with birds). The mean log response ratio per tree species was our measure of the magnitude or effect size of bird predation of caterpillars on each tree species. The bird predation data were collected over two Þeld seasons (2008 Ð2009) at the same time of year and sites used for measuring parasitism in earlier years. We observed that the frequency of parasitism of generalist caterpillars varied among tree species (Farkas and Singer 2013). As observed in similar studies (Barbosa et al. 2001, Lill et al. 2002), these differences in parasitism among tree species were consistent over the 5-yr period (i.e., no tree species ϫ year interaction). To address the EFS for parasitoids hypothesis, we separately tested the effect size of bird predation per tree species and the effect of generalist caterpillar density per tree species on the total mortality of generalist caterpillars from parasitoids per tree species, pooled over all years. In these analyses, we used ...
Context 2
... caterpillars occupying eight different tree taxa (Acer rubrum L., Betula lenta L., Carya spp., Fagus grandifolia Ehrhart, Hamamelis virginiana L., Prunus serotina Ehrhart, Quercus alba L., and Quercus rubra L.) served as the hosts for parasitoids, with caterpillars and parasitoids subjected to concomitant predation by insectivorous birds (Fig. 4). To determine the frequency of parasitism of each caterpillar species on each tree species, we systematically collected caterpillars from haphazardly chosen branches, reared the caterpillars in the laboratory on the same tree species from which they were collected, and tallied the proportion of caterpillars that yielded parasitoid ßies ...
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Citations
... However, the percentages of parasitism of D. longicaudata have not affected the levels of parasitism of native parasitoids . Percentages of parasitism from native parasitoids are usually less than 5% (López et al. 1999;Sivinski et al. 2000b), and most host larvae are "free spaces" that are used by D. longicaudata (Murphy et al. 2014). This is a very important advantage in the use of D. longicaudata as a biocontrol agent in competitive tropical or subtropical environments (Miranda et al. 2015;Murillo et al. 2019). ...
Augmentative release of parasitoids is a suitable strategy to control fruit fly populations. Parasitoid release is relevant because it may be used strategically to integrate with other control methods. Augmentative Biological Control (ABC) aims to release high densities of mass produced into an area to suppress the population growth rate of the target fruit fly species. In Latin America, there are several examples of ABC against Ceratitis capitata (Wiedemann) and against species of the Neotropical genus Anastrepha Schiner. The introduced parasitoid Diachasmimorpha longicaudata (Ashmead) is the main species used in ABC programs. Successful outcomes have been achieved in Mexico and central-western Argentina by D. longicaudata mass releases. In “BioPlanta San Juan,” Argentina, D. longicaudata is mass reared on larvae of C. capitata Vienna-8 (tsl) strain. This parasitoid is released in irrigated semiarid fruit-growing valleys. On the contrary to Mexico, D. longicaudata is mass produced on larvae of Anastrepha ludens (Loew) at the biofactory of the Fruit Fly National Program to release it over larger subtropical areas. Post-release data have shown higher values than 50% of host mortality. This chapter provides particular information on the use of biological control, within the area-wide program in environmentally distinguishable regions. Advantages, social problems, and their relation with costs are also discussed.
... Such changes in insect voltinism can create a temporal mismatch between host insects and their natural enemies [3]. If natural enemies are not able to track changes in the voltinism of their host, additional herbivore generations might enter enemy-free space, potentially resulting in higher infestation levels and increased plant damage in natural and agricultural systems [4]. While parasitoids are major natural enemies of insect herbivores, the impact of shifts in the voltinism for host-parasitoid interactions remains largely unexplored [5]. ...
... Herbivores have frequently evolved traits that allow them to enter a point in space or time where the natural enemy is not present or active, a concept commonly referred to as enemyfree space [4]. Likewise, herbivores have often dispersed to locations where the natural enemies are not present, for example, through rare long-distance dispersal events [6][7][8]. ...
With climate change, plant-feeding insects increase their number of annual generations (voltinism). However, to what degree the emergence of a new herbivore generation affects the parasitism rate has not been explored. We performed a field experiment to test whether the parasitism rate differs between the first and the second generations of a specialist leaf miner (Tischeria ekebladella), both in the naturally univoltine and bivoltine parts of the leaf miner's distribution. We found an interactive effect between herbivore generation and geographical range on the parasitism rate. The parasitism rate was higher in the first compared to the second host generation in the part of the range that is naturally univoltine, whereas it did not differ between generations in the bivoltine range. Our experiment highlights that shifts in herbivore voltinism might release top-down control, with potential consequences for natural and applied systems.
... Another factor that may contribute to speciation on novel hosts is that these may allow organisms to escape from their natural enemies into "enemy-free space" (EFS) 23 . Most studies on the potential explanatory power of EFS in structuring ecological niches have focused on host use by parasitoids 24,25 . However, EFS is likely to be a much more general phenomenon. ...
We found that Drosophila species vary in their susceptibility to the broad-spectrum entomopathogen, Metarhizium anisopliae (strain Ma549). Generalist species were generally more resistant than dietary specialists, with the cactophilic Drosophila buzzatii and Drosophila sechellia, a specialist of the Morinda citrifolia (Morinda) fruit, being most susceptible. Morinda fruit is reported to be toxic to most herbivores because it contains Octanoic Acid (OA). We confirmed that OA is toxic to Drosophila spp., other than D. sechellia, and we also found that OA is highly toxic to entomopathogenic fungi including Ma549 and Beauveria bassiana. Drosophilasechellia fed a diet containing OA, even at levels much less than found in Morinda fruit, had greatly reduced susceptibility to Ma549. This suggests that specializing to Morinda may have provided an enemy-free space, reducing adaptive prioritization on a strong immune response. Our results demonstrate that M. anisopliae and Drosophila species with divergent lifestyles provide a versatile model system for understanding the mechanisms of host–pathogen interactions at different scales and in environmental context.
... Our results may suggest that for quasi-gregarious parasitoids such as T. japonicus, the number of eggs in an egg mass may not be a dominant factor in their assessment of egg mass quality; traits of individual eggs that vary interspecifically, for example, may have relatively more importance (e.g., Sabbatini-Peverieri et al. 2021). Alternatively, as discussed by Murphy et al. (2014), female parasitoids also seek refuges or enemy free space to ensure survival of their offspring, and this may be expressed through variation in certain host-use traits. In the present scenario, the adaptability of T. japonicus to exploit a wide range of egg mass sizes may be an important factor in ensuring enemy free space from top-down selective forces (such as predation or hyperparasitism), with the assumption being that smaller egg masses may be less conspicuous and therefore less susceptible to intraguild predation. ...
Predicting how much of a host or prey population may be attacked by their natural enemies is fundamental to several subfields of applied ecology, particularly biological control of pest organisms. Hosts or prey can occupy refuges that prevent them from being killed by natural enemies, but habitat or ecological refuges are challenging or impossible to predict in a laboratory setting—which is often where efficacy and specificity testing of candidate biological control agents is done. Here we explore how intraspecific variation in continuous traits of individuals or groups that confer some protection from natural enemy attack—even after the natural enemy has encountered the prey—could provide partial refuges. The size of these trait‐based refuges (i.e., the proportion of prey that survive natural enemy encounters due to protective traits) should depend on the relationship between trait values and host/prey susceptibility to natural enemy attack and on how common different trait values are within a host/prey population. These can be readily estimated in laboratory testing of natural enemy impact on target or nontarget prey or hosts as long as sufficient host material is available. We provide a general framework for how intraspecific variation in protective host traits could be integrated into biological control research, specifically with reference to nontarget testing as part of classical biological control programs. As a case study, we exposed different host clutch sizes of target (pest) and nontarget (native species) stink bug (Hemiptera: Pentatomidae) species to a well‐studied exotic biocontrol agent, the egg parasitoid Trissolcus japonicus (Hymenoptera: Scelionidae). We predicted that the smallest and largest clutches would occupy trait‐based refuges from parasitism. Although we observed several behavioral and reproductive responses to variation in host egg mass size by T. japonicus, they did not translate to increases in host survival large enough to change the conclusions of nontarget testing. We encourage researchers to investigate intraspecific variation in a wider variety of protective host and prey traits and their consequences for refuge size.
... 269). In a spatial context, enemy-free space corresponds to a species living in habitat patches where there are fewer or no natural enemies, a phenomenon that has been observed in several empirical systems (Denno et al. 1990;Fox and Eisenbach 1992;Berdegue et al. 1996;Murphy 2004;Cole et al. 2005;Heisswolf et al. 2005;Kaminski et al. 2010;Roy et al. 2011;Murphy et al. 2014;Greeney et al. 2015). Ideal free distributions of predators and their prey yield enemy-free space when patches of lower quality for the prey are also lower quality for the predator (Schreiber et al. 2000;Schreiber and Vejdani 2006). ...
Species interact in landscapes where environmental conditions vary in time and space. This variability impacts how species select habitat patches. Under equilibrium conditions, evolution of this patch selection can result in ideal free distributions where per capita growth rates are zero in occupied patches and negative in unoccupied patches. These ideal free distributions, however, do not explain why species occupy sink patches, why competitors have overlapping spatial ranges, or why predators avoid highly productive patches. To understand these patterns, we solve for coevolutionarily stable strategies (coESSs) of patch selection for multispecies stochastic Lotka-Volterra models accounting for spatial and temporal heterogeneity. In occupied patches at the coESS, we show that the differences between the local contributions to the mean and the variance of the long-term population growth rate are equalized. Applying this characterization to models of antagonistic interactions reveals that environmental stochasticity can partially exorcize the ghost of competition past, select for new forms of enemy-free and victimless space, and generate hydra effects over evolutionary timescales. Viewing our results through the economic lens of modern portfolio theory highlights why the coESS for patch selection is often a bet-hedging strategy coupling stochastic sink populations. Our results highlight how environmental stochasticity can reverse or amplify evolutionary outcomes as a result of species interactions or spatial heterogeneity.
... Topdown effects are mediated by herbivore defence-related traits. For example, sheltered and aposematic herbivores are exploited less by visual-cued predators (e.g., birds) but more by parasitoids ("enemy-free space" hypothesis, tested and supported by Gentry & Dyer, 2002;Hrcek et al., 2013;Murphy et al., 2014; for aposematic herbivores, Singer et al., 2014). ...
... Topdown effects are mediated by herbivore defence-related traits. For example, sheltered and aposematic herbivores are exploited less by visual-cued predators (e.g., birds) but more by parasitoids ("enemy-free space" hypothesis, tested and supported by Gentry & Dyer, 2002;Hrcek et al., 2013;Murphy et al., 2014; for aposematic herbivores, Singer et al., 2014). ...
... Gentry and Dyer (2002) did not report seasonal differences in parasitism rate, However, neither did they find disproportional shelter builders were associated with certain season as in our study. Stronger top-down effects of parasitoids on shelter builders also support the "enemy-free space" hypothesis (Gentry & Dyer, 2002;Hrcek et al., 2013;Murphy et al., 2014) and add evidence to the few quantitative studies investigating parasitism rates in the tropics (Gentry & Dyer, 2002;Hrcek et al., 2013;Baer & Marquis, 2020;Jeffs et al., 2021). Alternatively, we are aware of the possibility that our few data points with more than one parasitism incidence could drive our top-down effects. ...
Bottom‐up effects from host plants and top‐down effects from predators on herbivore abundance and distribution vary with physical environment, plant chemistry, predator and herbivore trait and diversity. Tri‐trophic interactions in tropical ecosystems may follow different patterns from temperate ecosystems due to differences in above abiotic and biotic conditions.
We sampled leaf‐chewing larvae of Lepidoptera (caterpillars) from a dominant host tree species in a seasonal rainforest in Southwest China. We reared out parasitoids and grouped herbivores based on their diet preferences, feeding habits and defence mechanisms. We compared caterpillar abundance with leaf numbers (‘bottom‐up’ effects) and parasitoid abundance (‘top‐down’ effects) between different seasons and herbivore traits.
We found bottom‐up effects were stronger than top‐down effects. Both bottom‐up and top‐down effects were stronger in the dry season than in the wet season, which were driven by polyphagous rare species and host plant phenology. Contrary to our predictions, herbivore traits did not influence differences in the bottom‐up or top‐down effects except for stronger top‐down effects for shelter‐builders. Our study shows season is the main predictor of the bottom‐up and top‐down effects in the tropics and highlights the complexity of these interactions.
... These patterns have led several authors to hypothesize that parasitoids preferentially use well-defended hosts in order to gain "enemy-free space" (Jeffries and Lawton 1984) from potential predators of their hosts (Gentry and Dyer 2002;Murphy et al. 2014). Negative associations between predation and parasitoid mortality of caterpillars in both temperate (Murphy et al. 2014) and tropical (Baer and Marquis 2020) forests support this hypothesis. ...
... These patterns have led several authors to hypothesize that parasitoids preferentially use well-defended hosts in order to gain "enemy-free space" (Jeffries and Lawton 1984) from potential predators of their hosts (Gentry and Dyer 2002;Murphy et al. 2014). Negative associations between predation and parasitoid mortality of caterpillars in both temperate (Murphy et al. 2014) and tropical (Baer and Marquis 2020) forests support this hypothesis. These associations likely represent behavioral adaptations on the part of the parasitoids (i.e., parasitoids attracted to defended hosts have been selected for). ...
Parasitoids are among the most diverse and important enemies of caterpillars. They are key components of the multitrophic communities in which caterpillars are sandwiched, and they have played a profound role in shaping caterpillar morphology, ecology, physiology, and behavior. Here, we review the natural histories and ecologies found in major parasitoid groups, with focus on the ichneumonoid wasps (especially Braconidae) and the Tachinidae (or “bristle flies”). We briefly examine aspects of the community patterns of caterpillar parasitoids, caterpillar traits that influence parasitism, host ranges of parasitoids, and what recent research employing genetic data is beginning to reveal about caterpillar-parasitoid associations. Finally, we assess how major anthropogenic environmental changes including habitat loss and fragmentation, invasive species, global warming, and agricultural intensification are affecting parasitoids and their interactions with hosts.KeywordsLepidopteraHymenopteraDipteraParasitism rateTritrophic interactionsFood webNatural enemiesBraconidaeIchneumonidaeChalcidoideaParasitic waspKoinobiontIdiobiontTachinidaeHost rangeEnemy-free spaceDNA barcodingMetabarcodingClimate changeHabitat fragmentationAgricultural intensificationHuman impacts on insect decline
... Selection from parasitoids may oppose selection from generalist predators for narrow herbivore diet breadth: several studies show that chemicals sequestered by specialist insect herbivores can be used by specialist parasitoids and predators as search cues (Köpf et al. 1997;Zvereva and Rank 2004;). These sequestered chemicals may also make the herbivore a superior host for parasitoids because a chemically protected host will also protect the parasitoids developing inside it (Murphy et al. 2014). Alternatively, the sequestered chemicals may constrain the herbivore's immunological defenses against parasitoids (e.g., Smilanich et al. 2009). ...
We review evidence for predators as agents of selection for the evolution of dietary specialization by insect herbivores. Since being proposed in the 1980s, this “enemy-free space” hypothesis has garnered much attention, but relatively little testing. Most tests have used caterpillars to address the community-level prediction that generalist predators preferentially attack dietary generalist herbivore species relative to their specialist counterparts. Both qualitative and quantitative aspects of our review found mostly supporting evidence for this prediction. We also reviewed literature on various mechanisms proposed for the superior anti-predator defenses of specialist herbivores, including sequestration of plant allelochemicals, specific camouflage, increased behavioral efficiency, and greater ability to suppress herbivore-induced plant volatiles. Considerable evidence supports allelochemical sequestration as a primary mechanism for the anti-predator advantage of specialists. Specific camouflage and increased feeding efficiency seem likely mechanisms based on evidence from limited testing. In contrast, the evidence indicates that specialists are no better than generalists at suppressing herbivore-induced volatiles. The mechanistic part of our review prompted us to propose a refinement of the enemy-free space hypothesis: the greater the dependence of anti-predator defenses on taxonomically specific host plant traits, the stronger the selection for the evolution of dietary specialization in herbivores. This refinement makes new predictions intended to spur mechanistic and evolutionary tests of the enemy-free space hypothesis.KeywordsAllelochemicalsBehavioral efficiencyCamouflageChemical sequestrationCoevolutionDietary nicheDietary specializationEvolutionFeeding decisionsHerbivore-induced plant volatilesHost manipulationHost rangeHost specificityInformation processing hypothesisInsect herbivoresLepidopteraNatural enemiesNatural selectionNeural constraints hypothesisParasitoidsPhysiological efficiency hypothesisPlant secondary metabolitesPolyphagyPredation
... Quadrus cerialis has been recorded as host to Apanteles Förster (Braconidae), Goniozus Förster (Bethylidae), Hyposoter Förster (Ichneumonidae) and Siphosturmia Coquillett (Tachinidae) (Janzen (2020), studying a community of caterpillars that build shelters, found a negative correlation between parasitism and predation of the herbivore, which was modulated by shelter traits. Their results provide support for the parasitoid enemy-free space hypothesis (Murphy et al. 2014), which proposes that parasitoids prefer hosts that are less likely to be killed by predators. ...
Aximopsis gabrielae Zhang, Gates and Campos sp. nov. is described from southern Mexico in the Yucatan Peninsula, Mexico. This species is a koinobiont gregarious larval-pupal endoparasitoid of the caterpillar of Quadrus cerialis (Stoll) (Lepidoptera: Hesperiidae) feeding on the shrub Piper amalago L. (Piperaceae) in the semievergreen
forest. This is the first record of Aximopsis parasitoids on Hesperiidae (Lepidoptera). Morphological, biological, ecological and geographical data are integrated to delineate the new species.
... Its larvae feed preferentially on a several plant species, and were found to include in their diet certain plant species that are nutritionally inferior, but provide chemicals that increase their chances of survival after parasitization (Singer & Stireman 2003). From these and many other examples (Williams et al. 2001;Singer et al. 2004;Murphy et al. 2014;Hu et al. 2020), we may infer that host-plant preferences are governed not only by nutritional quality, but also by the third trophic level, natural enemies. ...
Based on the “enemy-free space” hypothesis, in order to avoid natural enemies, insects may prefer host plants that are nutritionally suboptimal but are less visited by their natural enemies. The fall webworm, Hyphantria cunea Drury has more than 600 reported hosts. Chouioia cunea, a parasitoid wasp, is the main natural enemy of H. cunea. We addressed the question whether the preference of H. cunea for host plants correlate with attractiveness of the plants to C. cunea. H. cunea larvae were reared on leaves of eight different host plants, and the relationship between H. cunea host preference and preferences of the parasitic wasp were evaluated. The preferred host plant of female H. cunea was mulberry, Morus alba. Compared with other plants, M. alba was a poor nutritional host for H. cunea. However, compared with other host plants, M. alba attracted fewer natural enemies C. cunea. GC-MS combined with GC-EAD analysis revealed six compounds in the volatiles of different plant HIPVS after feeding by H. cunea. Behavioral assays showed that tridecane alone did not elicit any attraction or repellency responses of the host H. cunea or the parasitoid C. cunea. When tridecane was mixed with other HIPVS, however, the mixture could attracted C. cunea and repelled H. cunea. Notably, only M. alba HIPVS did not contain tridecane. Thus, H. cunea exploits M. alba as an enemy-free space, minimizing attacks by the parasitoid C. cunea. This information underscores that adaptive responses of herbivores need to be considered in the context of multi-trophic relationships rather than optimizing herbivore growth on the most nutritionally adaptive plant host.
