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Oecologia (2001) 128:153–163 DOI 10.1007/s004420100679 N. Stamp Enemy-free space via host plant chemistry and dispersion: assessing the influence of tri-trophic interactions Received: 24 May 2000 / Accepted: 6 February 2001 / Published online: 24 March 2001 © Springer-Verlag 2001 Abstract It has been argued that generalist natural enemies of insect herbivores provide a major selection pressure for restricted host plant range. This idea is a subset of the enemy-free space (EFS) hypothesis, whereby insect herbivores escape their enemies by being scarce in space and time and/or chemically defended via containing plant allelochemicals. To date, there are only two complete tests of EFS via host plant chemistry and two via host plant dispersion, and only two of these tests support the EFS hypothesis. However, three corollaries to existing views on EFS are sufficiently supported by data to warrant direct testing of the view that EFS is obtained via host plant chemistry's effects on enemies of insect herbivores. So the issue remains. Resolution will require a more collaborative, methodological approach to examine the relative importance of the major multiple factors that shape patterns of feeding specialization of insect herbivores. Predation is certainly one of these factors, but its role is still not clear. Keywords Predator–prey interaction · Specialist insect herbivores · Host plant range · Generalist predators · Parasitoids Introduction A primary focus in ecology and evolution has been to develop an understanding of the rich diversity of species, and one of the most species-rich groups is insect herbivores. One characteristic of this group is that most insect herbivores are specialized feeders; 70% of insect herbivores restrict their feeding to one plant family (Bernays and Chapman 1994), and 90% are restricted to three or fewer families (Bernays and Graham 1988). One factor contributing to the diversity of insect herbivores is host plant defensive chemistry. Ehrlich and Raven (1964) N. Stamp (✉) Department of Biological Sciences, Binghamton University, State University of New York, Binghamton, NY 13902-6000, USA e-mail: [email protected] noted the pattern of related butterfly species using plants that were chemically related or taxonomically (and thus presumably chemically) related, which led to the idea of coevolution occurring between host plants and their specialist insect herbivores. A number of studies provide evidence for such coevolution (Farrell et al. 1992; Farrell and Mitter 1994; Becerra 1997). But other factors besides the effect of host plant defensive chemistry on herbivores may also serve as selection pressures for feeding specialization by insect herbivores. It is not clear which factors are most important and when. In a past review of plant-herbivore interactions, Bernays and Graham (1988) stated, “We argue that generalist natural enemies of herbivorous insects provide a major selection pressure for restricted host plant range. The significance of plant chemistry is...in terms of regulating behavior, while the chemical coevolutionary theories are...of limited value.” They further state, “...chemical coevolution between plants and herbivores has been overemphasized, and that generalist natural enemies, especially predators of the herbivores, may be the dominant factor in the evolution of narrow host [plant] range.” Finally, they make the statement, “Plant chemistry is but one of many potential pressures and probably not the predominant one, in spite of its recent popularity and clear importance in behavior.” A primary point of the Bernays and Graham review was that host plant specialization by herbivores may reduce predation because the herbivores are then scarce in space and time and/or chemically defended to some degree via plant allelochemicals. Their discussion focuses on the effect of plant allelochemicals on herbivores and their enemies and so much of the discussion in this paper will do the same. Most herbivorous insects contain, at the least, sublethal dosages of allelochemicals to an insect predator. The protective chemicals occur in the form of plant matter in the herbivore’s gut and/or allelochemicals sequestered across the gut lining. Allelochemicals may occur in the herbivore's tissues even when a specialist herbivore feeds on novel host plant species (Strohmeyer et al. 1998), and insect herbivores, especial- 154 ly specialist feeders, may bioaccumulate plant allelochemicals in their tissue (Bowers 1992; Bowers and Stamp 1997). Insect herbivores are likely to be rejected by predators when they eat plants that yield extracts that deter predators (Dyer 1995). Thus, this idea that predators are an important selective pressure for host plant specialization by insect herbivores is appealing. Although host plant chemistry per se is clearly very important in shaping feeding specialization by insect herbivores, it seems likely that there is also a “top-down” effect through predators being affected by, and so avoiding, plant allelochemicals contained in their prey. In the same journal containing the Bernays and Graham (1988) article, several people argued that the patterns of feeding specialization generated by invertebrate herbivores were complicated by factors other than host plant chemistry and predators, and that the interaction of the entire set of factors was important (Barbosa 1988; Courtney 1988; Ehrlich and Murphy 1988; Fox 1988; Janzen 1988; Jermy 1988; Rausher 1988; Schultz 1988; Thompson 1988). They agreed that the effect of the third trophic level needed more attention, but they felt that the third trophic level was unlikely to be the dominant force proposed by Bernays and Graham. Since then, there has been some attention on the effect of plant chemistry on predators, with a focus on the assessment of three corollaries. If generalist predators, via avoiding exposure to noxious plant chemicals, act as a selective force that narrows host plant range of invertebrate herbivores, we might expect that generalist predators: (1) can learn to avoid prey containing detrimental plant chemicals, (2) avoid specialist herbivores and more readily attack generalist herbivores, and (3) suffer a reduction in fitness when they have a diet of prey containing detrimental plant chemicals. Evidence for these ideas would provide circumstantial support for the Bernays and Graham (1988) view that predation is an important selective force for feeding specialization by insect herbivores. In this review, I focus on some of the evidence for these corollaries. Effect of allelochemical-containing prey on natural enemies Most invertebrate predators come into contact with at least some plant allelochemicals in their herbivorous prey, via the prey's gut, and/or sequestered in prey tissue. For instance, predatory wasps tear prey apart and ball up pieces of tissue that are used to provision larvae at the nest; in this process, their faces and mouths get covered with the prey’s body fluid. Often wasps spend much time wiping and grooming their heads, antennae and legs after tearing apart caterpillars containing plant allelochemicals, and sometimes the wasps reject the prey in the process (Stamp 1992). Extra-oral feeders, such as spiders and predatory hemipterans, inject enzymes into prey and then suck up the partially digested fluid (Cohen 1995), which may contain allelochemicals from prey tissue and gut. In contrast to insectivorous birds, invertebrate predators usually capture prey about their own size and, thus, are likely to acquire a relatively high dosage of allelochemicals. Often, invertebrate predators are deterred by plant allelochemicals contained in their prey. Predatory wasps preferred palatable to unpalatable prey (Rayor et al., in press). Invertebrate predators attacked specialist herbivores less frequently than generalist feeders (Bernays 1988; Bernays and Cornelius 1989; Dyer 1995). Dyer (1995) showed that the lower frequency of attack on specialist herbivores was positively correlated with prey defensive chemistry and plant defensive chemistry. Invertebrate predators can learn to avoid prey that contain allelochemicals (Gelperin 1968; Berenbaum and Miliczky 1984; Brown 1984; Vasconellos-Neto and Lewinsohn 1984; Malcolm 1986; Paradise and Stamp 1990, 1993; Traugott and Stamp 1996b; Rayor et al., in press). For example, initially predatory wasps frequently attacked Junonia coenia caterpillars; however, after a few days, the wasps began rejecting this prey species (Stamp 1992), which sequesters relatively high levels of allelochemicals (iridoid glycosides) from its host plants (Bowers and Collinge 1992). Experienced wasps can distinguish between palatable and unpalatable prey without having to kill them first (Bernays 1988). These results suggest that such predators could act as selective agents for increased host plant specialization by insect herbivores. The negative responses by predators to specialist herbivores also suggest that ingesting such prey is detrimental to predators. Some results indicate that allelochemical-fed prey can have a negative effect on predator development, growth rate and fecundity (reviewed in Rowell-Rahier and Pasteels 1992) and, thus, can contribute to an antagonistic relationship between some plants and invertebrate predators. For example, predatory stinkbugs given caterpillars reared on some of the allelochemicals found in tomato leaves took longer to develop and were smaller in size (Stamp et al. 1991; Traugott and Stamp 1996a). Prey fed milkweed seeds (containing cardenolides) reduced the consumption and growth rate of praying mantids (Paradise and Stamp 1993). When predatory wasps were given unpalatable prey, fewer offspring were produced, the offspring were smaller and the percent of male offspring was reduced, compared to that of wasps given palatable prey (Stamp, in press). Clearly, unpalatable prey can have negative effects on the fitness correlates of invertebrate predators. However, other studies show that under some conditions allelochemical-fed prey can have little or no effect on some invertebrate predators (Malcolm 1992; Osier et al. 1996; Stamp et al. 1996). Whether allelochemicalfed prey have a negative impact on invertebrate predators or not depends on various factors. For example, some invertebrate predators can detoxify toxic chemicals to some degree (Yu 1987). Consequently, some predators may not be susceptible to plant chemical defenses ingested via prey, whereas others are (Malcolm 1992). The 155 concentration of an allelochemical is also a factor. For instance, with increasing concentration of allelochemicals in the diet of prey, the negative impact on invertebrate predators increased substantially (Stamp et al. 1991; Traugott and Stamp 1996a). Different prey species affect the growth of predators differently (Landis 1937; Drummond et al. 1984). For example, with prey fed the same host plant species, predatory stinkbugs had a higher growth rate when fed a prey species that does not bioaccumulate iridoid glycosides (Vanessa cardui caterpillars) versus a prey species that does (J. coenia) (Strohmeyer et al. 1998). The effect of allelochemicals on insects has been shown to change with age of the insect (Schowater et al. 1977; Larsson and Tenow 1979; Scriber and Slansky 1981; Stamp et al. 1996). The poor growth of invertebrate enemies given prey raised on plant allelochemicals may reflect the poor nutritional state of the prey on an allelochemical diet and/or the direct effects of the allelochemicals on the invertebrate enemies (El-Heneidy et al. 1988). Therefore, a consequence of the effects of plant allelochemicals via prey is that invertebrate predators can be classified as “included”, “peripheral”, or “excluded” (Malcolm 1992). “Excluded” predators are unable to survive on prey, due to host plant chemistry encountered via prey. “Included” predators successfully exploit prey without detrimental effects from host plant chemistry. In contrast, “peripheral” predators experience reduced survivorship, smaller size and/or delayed development, due to host plant chemistry encountered via prey and/or the effect of host plant chemistry on the nutrition of the prey. Most generalist predators are probably “peripheral” in most situations. Consequently, variation in the effectiveness of peripheral predators in handling host plant chemistry encountered via prey is likely to be the key to understanding the ecology and evolution of interactions between herbivorous prey and their invertebrate predators (Malcolm 1992). What might cause variation in response to host plant chemistry in prey by “peripheral” predators, or what might shift an “included” predator to the category of “peripheral”, or even to “excluded”? The two major factors besides prey quality that have a large impact on invertebrate predators are temperature and prey abundance. The effect of plant allelochemicals in the diet of prey on the growth of invertebrate predators is a function of temperature. For example, at a cool thermal regime (18°C), predatory stinkbugs were not affected by increasing concentrations of rutin (a common allelochemical in plants) in the diet of their prey, but at a warm thermal regime (28°C), they were negatively affected by increasing concentrations of rutin (Stamp et al. 1991). In this case, the predator would fall in the category of “included” at the cool thermal regime but in the category of “peripheral” at the warm thermal regime. When the effect of temperature and plant allelochemicals on insects has been examined simultaneously, often there was an interactive effect between the two factors, and when this occurred usually there was an increasingly negative effect of allelochemicals at the warmer thermal regime (Stamp and Osier 1998). The other major factor besides prey quality and temperature that has a large impact on invertebrate predators is prey abundance. The array of prey species in the environment affects where invertebrate predators forage. Insect predators can exhibit a functional response to high densities of prey (Morris 1963; Tostowaryk 1971; Nakasuji et al. 1976). Consequently, predators may switch from one area to another in response to prey density, or from one prey type to another (Rabb and Lawson 1957), although they may switch to new prey slowly (Rabb and Lawson 1957; Yamasaki et al. 1978). However, frequently, invertebrate predators experience times when prey in general are scarce or, if plentiful, most prey are too large to be captured (Anderson 1974; Wise 1975; Evans 1982a, b, 1983; Hurd and Eisenberg 1984; Lenski 1984; Hurd and Rathet 1986; Wiedenmann and O’Neil 1990, 1991; Legaspi and O'Neil 1994). Prey scarcity can result in prolonged developmental time of immature predators (Legaspi and O’Neil 1994) and delayed reproduction of females (Wiedenmann and O’Neil 1990). Developmental time of immature predators may be longer when they come from poorly fed females (Legaspi and O’Neil 1994). When generalist insect predators experience periods of prey scarcity and when available prey contain allelochemicals, predators might be forced to include prey containing sublethal levels of allelochemicals in their diet. The effect of allelochemical-containing prey on insect predators may be greater when prey are scarce. For example, allelochemical-fed prey had no adverse effect on growth of an insect predator when prey were plentiful, whereas when prey were scarce, allelochemical-fed prey increased the negative effects of prey scarcity on predator growth (Bozer et al. 1996; Weiser and Stamp 1998). The ability to handle plant chemical defenses may reflect the availability of nutrients (Duffey 1980; Slansky and Wheeler 1992). With prey scarcity, nutrients that may facilitate dealing with plant defenses may be limiting. Such an effect of prey scarcity may be fairly common among invertebrate predators primarily feeding on insect herbivores. In sum, data on invertebrate predators support the three corollaries, which suggests that invertebrate predators may provide a strong selective pressure for feeding specialization by insect herbivores. But the data also indicate that invertebrate predators should not be thought of as static entities, i.e., a particular predator species may exert selective pressure under some conditions but not under others. Evidence for the corollaries also occurs in studies about the response of birds and parasitoids to plant allelochemicals. It is clear that birds have served as a selection pressure on herbivorous insects (Heinrich 1979, 1993; Heinrich and Collins 1983), that some bird species have more physiological susceptibility to particular allelochemicals than others (Fink and Brower 1981; Brower 1984), and that plant allelochemicals can 156 adversely affect weight gain and feather development of nestlings (L. Pezzolesi and A. Clark, SUNY-Binghamton, unpublished data). Although many parasitoids may feed on and within tissue likely to be free of allelochemicals (reviewed by Gauld et al. 1992), many others are likely to be exposed to plant allelochemicals contained within their hosts. Even when the concentrations in host tissue are relatively low, plant allelochemicals can have detrimental effects on fitness correlates of endoparasitic koinobionts, parasitoids that are fairly specialized in the use of habitat and host (Thurston and Fox 1972; Campbell and Duffey 1979; Barbosa et al. 1986, 1991; El-Heneidy et al. 1988). So parasitoids may provide a selection pressure on herbivores that reflects the parasitoids’ response to plant allelochemicals. Ascertaining enemy-free space Overall, these results infer that generalist predators or parasitoids could provide selection pressure for a restricted host plant range for insect herbivores. They also suggest that specialist parasitoids could provide selection pressure for a broader host plant range for insect herbivores. So the issue of the role of predators and parasitoids in shaping the pattern of feeding specialization by invertebrate herbivores remains equivocal. The idea that insect herbivores may escape generalist enemies by narrowing host plant range and specialist enemies by broadening host plant range is a subset of the enemy-free space hypothesis. The definition of enemy-free space is “ways of living that reduce or eliminate a species' vulnerability to one or more species of natural enemies” (Jeffries and Lawton 1984). Some of the “habits” that can generate enemy-free space (EFS) are adaptations in morphology and size, position, interspecific interaction, visibility, and chemistry (Berdegue et al. 1996). So host plant chemistry and host plant rarity, via their effects on enemies, are just two of several potential habits that could confer EFS to invertebrate herbivores. To examine the idea of EFS via host plant chemistry’s effect on natural enemies, a good place to start is with the general EFS criteria established by Berdegue et al. (1996). They proposed three working hypotheses that must be tested and accepted to conclude that EFS exists and the enemies have had a significant role in shaping the EFS. Firstly, their hypothesis (H1A1) is that the fitness of the prey in the presence of enemies is less than that in the absence of enemies. Such a finding establishes the importance of the enemies on the prey’s fitness. Secondly, their hypothesis (H2A1) is that the fitness of the prey in the alternative (potential EFS) habit with enemies is greater than that in the original habit with enemies. Such a finding establishes that the alternative habit provides enemy-free space. But it does not indicate the role of predation in shaping enemy-free space. Thirdly, their hypothesis (H3A1) is that the fitness of the prey in an alternative habit without enemies is less than in the origi- nal habit without enemies. Such a finding establishes that there is a cost to this EFS when predators are absent and, consequently, we can be sure that predation is the major factor generating this EFS habit. This shows the relative importance of predation compared with other unidentified factors, such as resource limitations (e.g., via food quality and competition), that can shape a pattern of feeding specialization by an insect herbivore. Hypotheses 1 and 2 support the idea that enemies are a factor in shaping the feeding niche of an insect herbivore. But all three of these one-tailed, alternative hypotheses must be supported to conclude that predation is a dominant force in generating enemy-free space for the species under consideration (Berdegue et al. 1996). With these criteria in mind, we can examine the studies on invertebrate herbivores in which all three hypotheses have been tested, or for which there are data to examine the hypotheses. Berdegue et al. (1996) reviewed the literature for nonagricultural terrestrial and freshwater arthropod systems to evaluate the state of the EFS hypothesis, and found 41 studies that examined the idea. Of those, 17, or 41%, were on terrestrial systems. Using Berdegue et al.’s criteria, only one that had host plant chemistry as the mechanism for EFS was a complete test, and it did not meet all three of Berdegue et al.’s criteria for supporting the EFS argument. A search of the literature for more recent studies revealed only one in which host plant chemistry affecting the natural enemies of herbivores was the likely mechanism. Using Berdegue et al.’s criteria, that study did support the EFS argument. It is worth reviewing these two studies to ascertain why there are so few tests of EFS via host plant chemistry influencing natural enemies. EFS via host plant chemistry test no. 1: willows, herbivorous beetles and carnivorous beetles The first study was conducted by Denno et al. (1990). Their system was two leaf beetle species that specialized on willows. One of these beetle species (Phratora vitellinae) defended itself with secretions made from host plant allelochemicals (salicylates and other phenolic glycosides). The other (Galerucella lineola) lacked this ability. Performance on three species of willow was evaluated. Two willow species were rich in salicylates (Salix fragilis and S. dasyclados) and one was poor (S. viminalis). The chemical-secreting beetle specializes in salicylate-rich willows, and so may obtain EFS by a narrower host plant range than the non-secreting beetle that uses a wider range of willows (Fig. 1A). The predators were coccinellid beetles (Adalia bipunctata). Hypothesis 1 The insect predators caused a high level of mortality. This result fits the EFS criteria of Berdegue et al. (1996). 157 Fig. 1A, B A specialist insect herbivore (Phratora vitellinae) prefers a willow species (Salix fragilis) that has high concentrations of salicylates, which it sequesters. A Relative to generalist predators, the potential EFS via host plant chemistry for P. vitellinae is the salicylate-rich willow species. B In the absence of predators, P. vitellinae’s performance on S. fragilis is similar to that on S. viminalis, which does not meet the EFS criteria. Data for the herbivore (Galerucella lineola), which does not sequester salicylates, are shown also. Modified from Denno et al. (1990) Hypothesis 2 The fitness (i.e., survival) of the “specialist” herbivores (P. vitellina) on a salicylate-rich or proposed EFS host plant (S. fragilis) with the predators was greater than their fitness on a salicylate-poor host plant (S. viminalis) with the predators. This result fits the EFS criteria. Hypothesis 3 The fitness (i.e., survival) of the “specialist” herbivores (P. vitellina) on a salicylate-poor host plant without the predators was less than their fitness on a salicylate-rich, or proposed EFS, host plant without the predators (Fig. 1B). This result does not fit the EFS criteria. There are two explanations for this last result. First, it may be that some other factor, by itself or in conjunction with predation, plays a role in the use of the salicylaterich host plant by P. vitellina beetles. For example, nutritional quality of the host plants may be different and influence the herbivores (Denno et al. 1990; Berdegue et al. 1996). Therefore, other potential factors would need to be evaluated. Niches of insect herbivores are shaped by a variety of factors, including host plant defensive chemistry, host plant nutritional quality, host plant abundance, competition, pathogens, predators, and parasitoids. The second explanation illustrates a fundamental problem with examining EFS related to plant chemistry. From an evolutionary perspective, it is difficult to evaluate where EFS has played a role. The hypothesis that there should be a cost in terms of fitness to the herbivore for use of a salicylate-rich host plant when enemies are absent, is logical, but it ignores the possibility of selection against the cost, which over time could reduce the cost to the point of making it undetectable. Just as there are mechanisms that may reduce the cost of defense to host plants in their interaction with herbivores (Simms 1992; Gershenzon 1994), we should expect in insect herbivores selection against the cost of utilization of host plants. Therefore, predation may be an important factor, and perhaps even the most important factor, in shaping an EFS habit, even though data used to test Berdegue et al.’s hypothesis 3 may not support the EFS criteria. So due to evolutionary issues, a “clean” test (i.e., as described by Berdegue et al. 1996) may be quite difficult to obtain. But we can examine how EFS might come about; that is, we can investigate the potential mechanisms. EFS via host plant chemistry test no. 2: plant family Asteraceae, a leafminer and parasitoids The second study was conducted by Gratton and Welter (1999), and it illustrates the point about investigating potential mechanisms. Their system was leafminer larvae of a fly that specializes on the sunflower Helianthus annuus. The novel host plants were also in the family Asteraceae: H. maximilianii, Ambrosia artemisiifolia, Taraxa- 158 Fig. 2A, B A specialist insect herbivore (L. helianthi) oviposits on one species (Helianthus annuus) in the Asteraceae. A Relative to generalist parasitoids, the potential EFS via host plant chemistry is that plant species (H. annuus). Relative to specialist parasitoids, the potential EFS via host plant chemistry is other species of Asteraceae, i.e., novel host plant species that the herbivore can use. B Response by three categories of parasitoids. Endoparasitoids dominated in 1994 and 1996 but less so in 1995 (H Helianthus annuus, C Centaurea solstitialis, A Ambrosia artemisiifolia, M Helianthus maximilianii, T Taraxacum officinale). Modified from Gratton and Welter (1999) cum officinale, and Centaurea solstitialis. The larvae were manually transferred to novel host plants by inserting the larvae into pinholes in the leaf epidermis. The plants were exposed to enemies under field conditions. By using leafminers, the set of enemies was limited to parasitoids. The working hypothesis was that specialist parasitoids act as selective agents for host plant shifts that result in an increase in diet breadth of the host insects (Lawton 1986; Bernays and Graham 1988; Weseloh 1993; Fig. 2A). Since most parasitoids are more specialized than insect predators in habitat and/or host use, their host insects, at least the exposed feeders, are more likely to escape their parasitoids by broadening their range of host plant use than by narrowing it. Hypothesis 1 There was not a direct test, but observational data indicate enemies caused significant mortality. This result fits the EFS criteria of Berdegue et al. (1996). Hypothesis 2 When endoparasitoids, which are more specialized by habit, dominated the parasitoid assemblage, parasitoidcaused mortality of the leafminers in the novel, or proposed EFS, plants averaged 17% less than in the normal host. This result fits the EFS criteria. Presumably host plant chemistry contributed to this result. For example, perhaps the novel host plants provided fewer recognizable volatile cues for the specialist parasitoids. Hypothesis 3 Feeding trials indicated that larval survivorship was greater on the original host plant; i.e., the original host plant provided better food, and so there was a cost of the shift to novel host plants. This result fits the EFS criteria. However, in 1 of the 3 years, generalist ectoparasitoids dominated the parasitoid assemblage, and then mortality among the original and novel host plants was simi- 159 lar (Fig. 2B; 1995). This result does not support the EFS view of the effect of generalist enemies. The EFS view is that generalist enemies select for a narrowing of host plant range (Bernays and Graham 1988). So we would expect that mortality caused by generalist parasitoids would be less on the original host plant, presumably the evolved EFS for these specialist leafminers, relative to generalist enemies (Fig. 2A). Perhaps that result would have occurred if the miners were only exposed to the generalist ectoparasitoids rather than to a parasitoid assemblage made up of both endoparasitoids and ectoparasitoids. So another important message from this study is that as environmental conditions changed, the advantage to the herbivores of a host plant shifted or, in this case, increasing diet breadth, changed. But where does this study leave us in terms of understanding the role of host plant chemistry in influencing the herbivore’s parasitoids? The underlying feature of the parasitoid-leafminer interaction is the response by the parasitoids to the host plant. However, we do not know whether the specialist parasitoids had greater difficulty finding the novel host plants and/or were repelled by the novel host plants. Furthermore, tests were not conducted to ascertain the effect of host plant chemistry on survivorship of the parasitoids (because the leafminers were dissected to determine parasitism). So the study suggests how host plant chemistry may play a role, but it does not actually examine that issue. (Sato and Ohsaki 1987). The third pierid (P. melete) encapsulated the parasitoid eggs, so it has a physiological defense whereby it kills the parasites. P. rapae: hypothesis 1 Parasitoids caused a high level of mortality, as required by the EFS criteria of Berdegue et al. (1996). Hypothesis 2 P. rapae was successful in new sites until parasitoid numbers increased, as required by the EFS criteria. Hypothesis 3 P. rapae was successful in new sites without parasitoids, which does not support the EFS criteria. The spatial-temporal availability of the host plants, rather than parasitoids, contributes to the herbivores moving to new sites. P. napi: hypothesis 1 Mortality due to parasitoids was high in one of the areas. Data were not gathered to test EFS but seem to support the EFS criteria. EFS via host plant dispersion test no. 1 The other way that use of host plant species by herbivores may convey EFS is through herbivore specialization (narrowing of host plant range), resulting in greater spatial dispersion of the herbivores, and so the herbivores are less likely to be found by enemies. There are only two complete tests of EFS for insect herbivores via spatial-temporal patterns. The study by Ohsaki and Sato (1990) provides an example of EFS in an agricultural situation. In Japan, cultivated and wild crucifers are used by three species of pierid butterfly larvae. A braconid parasitoid, Apanteles glomeratus, causes considerable mortality of Pieris rapae. The other two pierid species, Pieris melete and Pieris napi, are infrequently parasitized. The question was: what accounted for this difference? More specifically, what EFS mechanisms might be involved here? The pierid (P. rapae) that was heavily utilized by the parasitoid appeared to escape parasitism by continually colonizing newly available sites before the parasitoid did. In the study area, the second pierid (P. napi) was a specialist on rock cresses, even though the plants were poor quality for larval growth. The rock cresses in the study area grew under other weeds and, consequently, the P. napi larvae were less apparent to the parasitoids. So the EFS mechanism was low host plant apparency. In another area of Japan, P. napi uses a different host plant species, one which is more apparent, and correspondingly, it suffers a high parasitism rate there Hypothesis 2 Pieris napi was more successful in the other site. Data were not gathered to test EFS but seem to support the EFS criteria. Hypothesis 3 P. napi had poor larval growth on rock cresses in the area where the host plants were unapparent. That is, there was a cost to EFS. This fits the EFS criteria. The current status of EFS Overall, there are only two “complete” tests of EFS, via plant chemistry affecting natural enemies, and only two “complete” tests of EFS, via spatial-temporal patterns affecting natural enemies. Why are there so few studies of the EFS phenomena, via host plant chemistry and dispersion? Firstly, perhaps the EFS hypothesis has been already accepted or rejected by the scientific community. Consequently, perhaps it is not perceived as an interesting idea to test, or as an idea that is fundable. The Berdegue et al. (1996) review clearly makes the point that there are few 160 “complete” tests of the EFS hypothesis, and a close look reveals the paucity of “complete” tests examining the idea that EFS for insect herbivores can be created by increasing or decreasing host plant range. This would suggest that it is premature to accept or reject the hypothesis, at least as it applies to plant-insect herbivore interactions. Secondly, perhaps the problem is that any test will have to be system specific. So the question then is: how many tests do we need to make a generalization about the EFS hypothesis? It took hundreds of studies (as of 1983, over 500; Connell 1983) on the role of competition in structuring communities and a lot of debate to arrive at a generalization (e.g., Schoener 1982; Simberloff 1984). Furthermore, usually when we test hypotheses in ecology and evolution, we choose systems to maximize the likelihood of rejecting the null hypotheses and accepting the alternative (our “working”) hypotheses. This is the “if it occurs, it will occur here” approach. But that will not give us an accurate picture of how important EFS is or when it is important. The key for EFS research on plant-insect systems would be a very methodical and coordinated approach by a group of researchers to ensure that an appropriate range of systems was investigated and comparable approaches taken. By doing that, it might take only five studies to ascertain the basic pattern. Although this strategy is seldom utilized in ecological studies, it can be a very powerful one. Thirdly, perhaps the problem is that multiple causes are at work in shaping niches. Therefore, often univariate tests about the role of EFS, competition, etc. do not provide satisfactory explanations. For example, the parasitoid patterns found for tropical versus extra-tropical regions (Gauld and Gaston 1994) suggest that the direct effects of host plant chemistry and dispersion on insect herbivores are probably more important than parasitoid pressure in shaping feeding specialization by insect herbivores in the tropics. Therefore, multiple factors should be examined to assess the relative effects. The relative effects of multiple factors can be assessed with path analysis (Ullman 1996). For instance, levels of a resource, such as light, can be manipulated, which will alter the carbon:nutrient balance in plants and so alter the concentrations of allelochemicals (Bryant et al. 1983). The effect of different concentrations of allelochemicals on insect herbivores can be measured in the presence and absence of predators (Fig. 3). The effect on predators can also be measured. Fourthly, perhaps the problem is that predators and parasitoids are not static entities. The effect of host plant chemistry on natural enemies varies with other conditions with which the natural enemies must contend, such as temperature and prey abundance. So the presence of natural enemies, or susceptibility of herbivores to natural enemies, does not indicate constant selective pressure. One way to deal with this is to conduct experiments long enough to see how the pattern of interaction changes with different environmental conditions (e.g., tests over multiple years, as in Gratton and Welter 1999). Also, one Fig. 3 Example of a design for a path analysis of multiple factors in a system of plants used by insect herbivores attacked by insect predators. For a path analysis to ascertain the relative effects of various factors on response by, and performance of the herbivores, different levels of a factor can be tested. The factors of interest are: resources for plants, plant availability, and presence of predators. In the category of resources for plants, light and soil nutrients are two important resources that will affect: (1) concentration of plant nutrients, (2) allocation to mass and reproduction, and (3) defenses. An experiment could manipulate a resource for plants; e.g., soil nitrate could be set at low and high levels. For plant availability, an experiment could manipulate plant species and/or dispersion. In addition, the predator factor can be tested via absence versus presence of predators. The arrows show the interactions of interest, and point to an effect on one factor by another predator species is unlikely to provide a strong enough selection pressure to generate an EFS pattern. Examining a guild, as Gratton and Welter (1999) did, provides a better picture. A path to resolving the future status of EFS Resolution about the relative role of the third trophic level in shaping the patterns of feeding specialization of insect herbivores would be useful because it would help us understand the pattern of species diversity in plants, invertebrate herbivores, and invertebrate enemies. The advantage of the EFS framework is that it provides an explicit way to evaluate the role of host plant chemistry and dispersion on the herbivores’ enemies. However, because there very likely would be selection against the costs of dealing with plant allelochemicals, of locating dispersed host plants and of EFS habits, it is difficult to ascertain the relative effects of host plant chemistry, host plant dispersion, and enemies on shaping feeding patterns of herbivores. Accordingly, the case studies discussed here suggest that we cannot determine where EFS, via the effects on enemies of host plant chemistry and dispersion, has occurred, but we can examine the process by which it may evolve. This latter research strategy is a kind of reductionism. The utility of reductionism is “to find points of entry into otherwise impenetrably complex systems” (Wilson 1998). Specifically, descriptive study of natural systems is unlikely to enlighten us much because whenever there are data supporting the Berdegue et al. hypotheses 1 and 2 (so suggestive of EFS), it is also probable that data will not support hypothesis 3 due to selection against the cost of the EFS habit. In contrast, experiments that manipulate a system for the purpose of examining the effects of 161 expansion of host plant range (e.g., Gratton and Welter 1999) can be informative. But such studies should determine why survivorship is higher on novel plants and, in particular, the role of allelochemicals. For example, in the leafminer-Asteraceae system, we would like to know to what extent the parasitoids: (1) found the novel host plants, (2) found the novel plants but could not handle the external environment of the plant (e.g., due to trichomes), and (3) oviposited in the leafminers, but with low survivorship of offspring due to poor host nutrition and/or plant allelochemicals. Once again, path analysis would be useful in resolving these issues. Furthermore, the effects of plant dispersion could be examined by conducting experiments that vary the relative density of the original and novel host plants. Spatial and temporal scales should also be incorporated. But while the effect of spatial-temporal scale on the herbivore’s avoidance of enemies can be investigated, the effect of spatial-temporal scale on the range of host plant species used by the herbivore cannot be evaluated because manipulation of the herbivore requires placing it on the novel host plants (i.e., oviposition may not occur there). Experiments that manipulate a system for the purpose of examining the effects of narrowing host plant range could also be done. In this case, predation (or parasitism) could be increased to determine if it would cause a reduction in number of host plant species used, and if a reduction corresponds to the negative effect of plant allelochemicals on the predators. By using an introduced predator that causes significant mortality or an introduced herbivore, the problem of previous selection against cost of using EFS could be avoided, i.e., there has not been time for selection against such a cost. 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