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Host range in phytophagous insects: the potential role of

generalist predators

Article  in  Evolutionary Ecology · October 1989

DOI: 10.1007/BF02285261

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Evolutionary Ecology, 1989, 3, 299-311

Host range in phytophagous insects: the potential role of generalist predators

E. A. BERNAYS* Division of Biological Control, Department of Entomology and Department of Zoology, University of California, Berkeley, 1050 San Pablo Avenue, Albany, CA 94706, USA

Summary

The potential role of generalist natural enemies is presented as one of the important ecological pressures that select for narrow host range in phytophagous insects, and dominant relative to physiological bases for specialization. Experiments are described in three completely different systems indicating that generalist herbivores are more vulnerable to predation than specialist herbivores. The three predators were (a) the vespid wasp Mischocyttarus flavitarsus, (b) the Argentine ant lridomyrmex humilis and (c) the coccinellid beetle Hippodamia convergens. It is concluded the predators may provide strong selection pressure for maintenance and perhaps evolution of narrow host range in insect herbivores.

Keywords: Host range; evolution; herbivores; predation; selection.

Introduction

Phytophagous insects are relatively specific, feeding on only one or a few genera, or on plants in a single family or subfamily; probably fewer than 10% feed on plants in more than three different families (Chapman, 1982; Price, 1983; Bernays, 1984). In spite of this specificity, host use is often known to be quite labile with host changes occurring over periods ranging from a few to hundreds of years (e.g. Hsiao, 1982; Hare and Kennedy, 1986; Strong et al., 1984; Southwood, 1986) and artificial selection experiments show that oviposition choice and/or host utilization ability can often be significantly altered in only 12-16 generations (Gould, 1979; Claridge and den Hollander, 1980; Wasserman and Futuyma, 1981). Therefore the current patterns of host use should be seen as dynamic and the selective pressures operating now relevant in governing host range, in spite of constraints determined by past history (Zwolfer, 1982).

The unique secondary chemistry of the diverse species of plants we see today plays a dominant role in the behavior of phytophagous insects, providing positive and negative signals to ensure accurate host identification. Most would agree that such chemicals are generally the most important proximal cause of narrow host range (Bernays and Chapman, 1987). It is less certain what their role may be with respect to the ultimate, functional cause of the patterns we presently see (Bernays and Graham, 1988).

One of the reasons for believing they are not particularly important in this respect is the tendency for there to be a poor correlation between behavioral rejection of plants and unsuitability of the plants for growth and development (Bernays and Chapman, 1987; Bernays and Graham, 1988; Cottee et al., 1988; Usher et al., 1988; Wrubel and Bernays,. in press). A second factor to consider is the poor evidence overall for trade-offs between adaptation to one

* Present address: Department of Entomology, University of Arizona, Tucson, AZ 85721, USA.

0269-7653189 $03.00+.12 r 1989 Chapman and Hall Ltd

300 Bernays

host and fitness on a second host (e.g. Futuyma and Moreno, 1988; Gould, 1988). This implies that host plant selection behavior is influenced over evolutionary time by ecological factors at least as much as by physiological ones. Physiological specialization including highly developed detoxification abilities specific to the host compounds may often be secondary to the initial host specificity. It should be noted that an inability to utilize non-host plants by reason of their detrimental effects following ingestion, is sometimes used as a reason for restricted host range, yet the observed inability may be a consequence and not a cause of specialization (Bernays and Chapman, 1978).

Several types of ecological pressure may be important in the evolution of host range (Futuyma and Moreno, 1988; Thompson, 1988). There is unlikely to be one single factor which is of paramount importance, although it has been argued that generalist predators are likely to be strong selective agents leading to narrow host range (Brower, 1958; Bernays, 1988; Bernays and Graham, 1988). The pressure of natural enemies has been considered important in niche differentiation generally, and partitioning of host plant use a result of pressure from different species of parasitoids (Jefferies and Lawton, 1984; Lawton, 1986). The concept of 'enemy free space' and the possibility that natural enemies select for a change in host use is not new (Gilbert and Singer, 1975; Lawton, 1978; Smiley, 1978; Price, 1981; Smiley and Wisdom, 1985; Price et al., 1986). However, parasitoids have been the focus of most studies, and predators have had little attention, perhaps because quantifying predator mortality is so difficult.

In the present paper, data are presented supporting the hypothesis that predators are important in selecting for narrow host range. Assuming there are trade-offs in relation to different host ranges among herbivores, it could be argued that benefits such as resource availability would favor polyphagy, while specialization on the host plant would have other benefits, of which differential escape from generalist natural enemies might be one. The possible mechanisms involved include such obvious ones as host-specific crypsis and host-derived chemical defenses (as in many aposematic species). There may be others: morphological specializations for moving about on different types of plant surface (Moran, 1986a; Southwood, 1986; Kennedy 1987) may be an advantage in escape; phenological matching may be important in patterns of movement that favor specialists in escape from enemies (Moran, 1986b); host-fidelity may simply allow a passive odor crypsis (Bernays, 1988).

Experiments are described which seek to answer the question: are polyphagous insect species more vulnerable than oligophagous or monophagous ones to mortality from generalist natural enemies? If so, generalist predators may be expected to provide one of the selection pressures favoring the evolution and maintenance of narrow host ranges in insect herbivores.

Methods

Three systems were investigated to test the hypothesis. Firstly, the vespid wasp Mischocyttarus flavitarsus Saussure was examined for its predatory abilities on caterpillars of different host range, tested in a semi-natural system with caterpillar species pairs matched for size and density. Second, the Argentine ant Iridomyrmex humilis Mayr was examined for its behavior with freshly killed individual caterpillars to test whether palatability was a function of host range. Third, the coccinellid, Hippodamia convergens Gu6rin was tested for its ability to capture and eat aphids of differing host ranges on growing alfalfa plants.

Vespids

The wasps, Mischocyttarus flavitarsus, built their own nests and freely flew and foraged in a greenhouse of approx. 150 m 2. For routine feeding, dead larvae of species not used in

Host range in phytophagous insects 301

experiments were placed on a cafeteria in an open-topped 1 m 3 cage. Humming bird feeders with sucrose solution provided most of the carbohydrate requirements. Lepidoptera were reared in cages in other greenhouses or environment rooms and fed on appropriate host plants (Bernays, 1988). Wasp preference experiments were carried out in cages 1 m 3, with removable plexiglass tops, two sides of gauze and two sides of plexiglass. In any one experiment two caterpillar species with differing host ranges were used. Equal numbers (10-30) of each were employed and matched at the preferred size (1-2 cm)..One day prior to an experiment, pots with growing plants were placed in the cages such that their leaves were contiguous. There were 6-10 pots containing 3-8 plant species. This involved 1-3 host plants of the relative specialist, while the more generalist feeder had all or most of the plants as potential hosts. Caterpillars of each species were placed out on a host plant of the more restricted feeder. Over the following 24 h caterpillars fed, moved about, produced feces, and made food choices, with the top on the cage to prevent wasp entry. Then the top of the cage was opened and the cafeteria cage closed. The exact timing depended on the weather. On cloudy mornings start time was around 10.00-11.00, while on sunny mornings start time was as early as 08.00.

After placement, specialist feeders generally stayed on the few plants which were natural hosts while the more generalist species sometimes tended to wander off and settle on a variety of the plant species, which had been selected for their suitability. Thus, in a typical example, the polyphagous Trichoplusia ni was paired with the oligophagous Brassicae feeder, Pieris rapae. Plants included Brassica oleracea, a favored food of both; Tropaeoleum, a favored food of both, Pisum sativum, a food of T. ni, and Lycoperisicon esculenta, a food of T. ni. All insects were first placed on Brassica oleracea, but a proportion of the T. ni were found on the other species by next morning. This behavior meant that when the experiment began the wasps encountered the specialists at higher density on particular plants and the generalists at lower overall density.

Records were made of the wasp behavior either by hand or on Hewlett Packard hand held computers programmed as event recorders for: contact with any caterpillar on a plant, feeding or removing of any caterpillar on any plant, rejection of any caterpillar after contact on any plant. Experiments were terminated when 50% of either species was removed. This took from 35 min to 6 h, depending on the weather and the number of wasps which varied from about 25 to 75.

In this work larvae normally feeding within one plant family are considered specialists. They range from species feeding on only one genus, such as Agraulis vanillae on Passiflora, to species feeding widely within a family such as Manduca sexta on Solanaceae. Generalists are those species which naturally feed on plants from a number of different families.

In some experiments, generalist herbivores were tested against one another to see whether extreme differences were commonplace within this category. In one set of experiments, dead caterpillars of Trichoplusia ni were set out in arrays of differing density on different plant species to test how density alone might influence foraging success by this predator.

Ants

Thirty-one species of lepidopterans not feeding internally or in leaf rolls, were freshly killed and used to test relative acceptability to the predator, Iridomyrmex humilis. This test was thus independent of behavior or of direct plant effects. Thirteen species were classified as polyphagous: all of these have host ranges covering more than two different plant families. Ten species were classified as more or less cryptic specialists: these include specialists on a plant family or lower taxon (oligophagous and monophagous species). Eight species were classified as brightly colored specialists feeding in unconcealed places: these mainly feed on one or a very few genera. Most insects were collected as larvae or eggs from the field and fed on appropriate

302 Bernays

host plants until use. Some species were obtained from cultures and fed on normal host plants until use.

The Argentine ant was first found in California in 1905. It is abundant in the San Francisco Bay Area and commonly feeds on small larvae of many species of Lepidoptera; it is an important component of predator-related mortality. For experiments a trail from natural populations to a convenient greenhouse table was established by laying out a dish with cotton impregnated with sucrose. Small insects placed in the vicinity of such a trail were quickly seized by numerous workers.

In all experiments, acceptability of test species was compared with acceptability of a standard, the potato tuber worm, Phthorimaea operculella (Bernays and Cornelius, in press). Ants usually found the caterpillars within 1-2 min and their numbers would quickly increase. The numbers of ants at each caterpillar over a period of 1 min was used as a measure of preference between the two caterpillars. Ant accumulation at each larva in a trial was a combination of random encounter, the length of time that the ants stayed with the larvae, and possible short range recruitment.

For each test species, there were usually 10 replicates, and the positions of the test and standard caterpillar were alternated between each replicate. After each replication the majority of experienced ants were removed from the area. The trials were recorded on video tape and analyzed at slow speed. Numbers of ants in contact with each caterpillar were counted at every second for a period of 1 min and the total number of ants was summed over the minute to give number of ant-seconds in the minute. Most of this counting made use of a hand held Hewlett Packard computer programmed as an event recorder.

From these data the proportion of ant-seconds on the test species was calculated as a proportion of the total ant-seconds at both species in a trial. If both were equally acceptable the value would be 0.5. The relative palatability of the different lepidopteran species was determined by comparing the numbers of tests where the preference index for species fell above or below certain values. In three experiments potato tuber worm was compared against itself, to give three separate measures of the variability due to random encounter or any other factor not resulting from species differences.

Coccinellids Predation on aphids was tested with species pairs feeding on single alfalfa plants. Four species were used in five combinations: Therioaphis maculata (very specific), Acyrthosiphon kondoi (specific), Acyrthosiphon pisum (family specialist), Aphis fabae (polyphagous). Individuals of each species pair were placed on a plant 24 h prior to an experiment. At the s~art of an experiment, numbers of individuals of the two species were equalized, and ranged from 20 to 50 in any experiment. Both larvae and adults of Hippodamia convergens were freshly collected in the field on the day before an experiment and kept without food until use. At the end of the 24 h period the predator was introduced. One was placed on the plant and observed continuously for 1 h. Then the predator was left with the prey for a further 23 h, after which time a census was made of the remaining aphids. There were 7-20 replicates of each experiment. Four different observers took part in the monitoring. In each experimental replicate the potted plant was placed in a 6 liter plastic cage with gauze lid to prevent loss of the predator.

Results

Vespids Overall, the generalist caterpillar species were taken more readily than the more specialized; in

Host range in phytophagous insects

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Fig. 1. Generalist prey taken as a percentage of all prey taken by the vespid wasp Mischocyttarus flavitarsus when presented with two prey types with differing host range. The data represent results from 28 separate experiments. Among the relative specialists in any pair, species were classified as either 'cryptic' (single hatched bars) or 'aposematic' (double hatched bars).

26 out of 28 experiments, more of the generalist were taken, and of the 26, 23 had between 70% and 100% of all captures being the generalist (Fig. 1). In chi squared tests, or Fisher's exact tests within trials, comparing numbers taken or not taken on the host plant of the specialist, 20 out of the 28 experiments gave significantly more of the generalist taken (p < 0.05). On the other hand in five tests of generalists against generalists the percentages of one species taken were 21, 44, 46, 52, and 53.

In 2 experiments out of 28, testing specialists versus generalists, more of the specialists were taken: Pseudaletia unipuncta was taken in preference to Estigmene acrea; Phryganidia californica was taken in preference to Orgyia vetusta. In each of these cases an extremely hairy generalist was paired with a non-hairy rather cryptic relative generalist. It appears that the hairiness was an advantage against predation, although preliminary experiments suggest that this feature is a costly investment nutritionally.

304 Bernays

The specialists ranged from obviously aposematic such as Harrisina brillians through species like Papilio zelecaon with possible aposematism to clearly cryptic species such as Manduca sexta and Pareuptychia hessione. The clearest non-preference was in relation to the obvious aposematic species. In 9 out of 10 experiments all larvae taken in the experiment were the generalists. On the other hand, in only 1 out of 18 experiments where the specialist was more or less cryptic, was all mortality of the generalist in the pair (Fig. 1).

In this vespid system with 28 experiments, there is a clear pattern of greater mortality in the generalists than in the specialists. The reasons for this difference are multiple and in some cases can only be speculative. Observations indicate repellancy in at least one case. With the aposematic Uresiphita reversalis, wasps made no contact at all, even though the paired generalist was readily taken at lower density from the same plant. Deterrence upon contact appeared to occur in two conspicuous species, Battus philenor and Harrisina brillians. In the latter parts of the experiments, wasps made no contact and presumably had learned not to make the attempt. Different levels of deterrence even after biting were also indicated. In the conspicuous Euphydryas editha and Danaus plexippus, caterpillars were sometimes bitten and then left. In the Papilio species, rejection sometimes occurred after a few seconds of chewing. In the more cryptic Phryganidia californica, caterpillars were often half left, and the guts invariably left behind.

Other, unknown factors seem to be operating. In the cases of Manduca sexta and Pectinophora gossypiella, larvae which were attacked took somewhat longer to process than those of the paired generalist. In addition, while fights took place over individuals in the generalist category in these experiments, such battles were not similarly observed in these two specialist species. Although there are no data, there was an impression in these cases as well as in some of the categories mentioned above, that return visits to the exact sites where the insects were found were much more common in relation to the generalists. In a number of cases with the more cryptic species, wasps seemed not to find or recognize caterpillars. For example, during foraging on the plant wasps came within millimeters or even made contact with individuals of Pieris rapae, Pareuptychia hessione, Phryganidia californica, Manduca sexta, Spargania magnoliata and Colias eurytheme more than once without apparantly noticing their presence. The phenomenon was seen rarely with the more polyphagous species. The visually cryptic nature of these species to humans seems irrelevant however, as contact with generalists also appeared to be by chance. The effect, if real, is subtle. There did appear to be a somewhat different response in generalists to the proximity of the wasps: escape reactions were noticeable in generalists, while motionlessness was noticeable in some of the specialists. A possibility exists that some of the visually cryptic specialists were also chemically cryptic. We know that larvae of Manduca sexta have different cuticular wax profiles depending on diet (Espelie and Bernays, in press), although the significance of this for predators is not yet known.

Among the conspicuous species of specialist caterpillars, all of which would normally be labelled aposematic, there is no doubt that protection, in various modes, is effective against wasps, even though in some cases, wasps eventually took them when no other prey was available. Most of the species in this category also aggregate to a greater or less extent, and it is assumed that this is important in the effectiveness of learning to avoid the prey.

Among the more cryptic specialists, aggregation occurs to the extent that there may be accumulations on host plants, while surrounding vegetation is free. However, polyphagous species are sometimes clumped in this manner also, so that it is difficult to make generalizations concerning relative density on a local basis. In this study, in the limited spatial array with about six plant species, no obvious benefit accrued to polyphages spread among the plants, relative to cryptic specialists occurring at higher density on only one or two plants. Experiments with a

Host range in phytophagous insects 305

single dead species at different densities in one experiment, indicated that when there were 10 on one plant and 10 spread among 5 other plants, there was a trend for the aggregation to disappear faster.

Ants

When the potato tuber worm was tested against itself, the preference ratio in the three trials was 0.48 + 0.05, 0.49 + 0.04 and 0.56 + 0.06. This gives the baseline variability when the paired caterpillars are of the same species. As expected it does not differ significantly from 0.5.

Among the polyphagous species only 3 out of 13 had average preference values of 0.5 or more when compared with potato tuber worm, indicating that the potato tuber worm was extremely palatable. However, only 3 species had values less than 0.4. On the other hand, among oligophagous cryptic species 8 out of 10 had values less than 0.4, and this is overall significantly different from the pattern for polyphagous species (Fig. 2) (chi squared = 5.2, p < 0.05). This

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306 Bernays

indicates that polyphagous species are, for some reason, relatively more acceptable than the oligophagous (specialists) species that are more or less cryptic.

Brightly colored specialists, which would commonly be called aposematic, were distinctly less acceptable than polyphases (p < 0.001) and less acceptable than the more cryptic oligophages (p < 0.01) (Fig. 1). Uresiphita reversalis, a specialist on certain legumes containing quinolizidine alkaloids, was particularly unacceptable (preference value 0.09).

The results demonstrate that among externally feeding phytophagous lepidopterans, poly- phagous species tend to be more acceptable than those with more specialized feeding habits. With respect to brightly colored (usually aposematic) species, this is not particularly surprising, although this predator is not a visual hunter and this type of defense is usually associated with visual predators, especially vertebrates. Presumably the caterpillars concerned are not just noxious to predators normally associated with aposematism. In response to four of the eight supposedly aposematic caterpillar species, notable grooming movements followed contact with them. This was most obvious in response to Agraulis vanillae and Junonia coenia, but was also observed in Harrisina americana and Uresiphita reversalis.

Perhaps more interesting is the finding that even in the cryptic species with relatively narrow host range, there was a tendency for them to be less acceptable than polyphagous species. Reasons are unknown, although we have found that palatability of Manduca sexta to Argentine ant is influenced by the food ingested (Bernays and Cornelius, unpublished). This was not known at the start of this work and exact diets of the polyphagous larvae were not always well monitored. It is possible that cultures feeding solely on one plant could have been poor representatives of the species as a whole and added to the variability of the results.

A few oligophagous species were very palatable and thus did not fit the general trend. For example Plutella maculipennis larvae were among the most palatable. The tests with this species took place with well developed last instar larvae which had possibly entered the wandering phase. If so the gut would have been empty, and the larvae not representative of actively feeding individuals. Again, we have evidence with larvae of Manduca sexta that individuals that had not fed extensively prior to experiments were more acceptable than individuals that had fed well on host plants (Bernays and Cornelius, unpublished). There is thus the possibility that with carefully controlled larval feeding regimes more consistent differences may be obtained. In spite of the variation in certain treatments the data overall demonstrate differences in acceptability of the larvae and support the hypothesis that polyphagous herbivores are potentially more vulnerable to predation by generalist predators than those with narrow host ranges.

Coccinellids In experiments with aphids results demonstrate some differences between species in vulnerability to predation by the coccinellid predator (Table 1). The alfalfa specialist aphid, Therioaphis maculata was much more successful in escaping predation by Hippodamia convergens than the more generalist species, although the differences between it and Acyrthosiphon kondoi were marginal and not statistically significant. Both species of Acyrthosiphon escaped predation more than the extreme generalist Aphis fabae. Over all five sets of experiments the indication is that the more specialist species are in some way protected relative to the more generalist feeders. Little can be said of the reasons for the differences found, although several different behaviors were noted that may be relevant. For example, T. maculata was notably agile at jumping away and successfully landing again when the predator was very close; A. kondoi began to jump away or fall from the plant when the predator was as much as I cm away. More comprehensive studies are required on the aphid-coccinellid system and additional control experiments with predators

Host range in phy tophagous insects

Table 1. Relative vulnerability of different aphid species, tested in pairs, to predation by the coccinellid Hippodamia convergens. Behavioral trials represent the percent of encounters resulting in death of the aphid. The survival represents relative numbers of aphids surviving 24 h exposure to the predator.

307

Behavioral 24 h survival Experimental pair test test

T. maculata/A, pisum + *** + ** (15) (20)

T. maculata/A, kondoi + + (7) (7)

A. kondoi/A, fabae + ** + * (10) (8)

A. pisum/A, fabae + + * (11) (10)

T. maculata/A, fabae + ** + * (7) (10)

+ = generalist mortality greater; * = difference significant at p < 0.05; �9 * = difference significant at p < 0.01; *** = difference significant at p < 0.001 (Mann-Witney U tests). Numbers in parentheses = number of trials.

absent are required, but the data strongly suggest that the relative specialists have an advantage with respect to predation.

Discussion

These results demonstrate a marked advantage associated with being relatively host-specific, although the exact nature of the advantage is varied and not always clear. The significance of this finding is dependent, in part, upon how important predators may be in general. Among ecologists, opinions have varied widely though very commonly predation is rated very highly as a cause of mortality. Hairston et al. (1960) stated that herbivores were most often predator- limited, and a number of studies have clearly demonstrated that among caterpillars, predation can often be the most important cause of mortality (e.g. Dempster, 1984; Feeny et al., 1985; Jones et al., 1987). Holmes and co-workers (1979) presented data indicating bird predation averaging 37% of caterpillars per week in one system, and pointed out the tremendous selective pressure of bird predation on caterpillars especially for patterns of crypsis, substrate choice and feeding schedules. The multitude of known protective mechanisms does testify to the importance of predators, though the importance relative to other mortality factors overall may be impossible to gauge.

A number of isolated studies on a variety of insects substantiate the findings presented here. Thus, caterpillar behavior in the field has been shown to reflect natural enemy avoidance at the expense of maximizing food quality. They select leaves on their hosts which are relatively poor nutritionally but good for sheltering (Damman, 1987; Hunter, 1987; Stamp and Bowers, 1988). There is evidence among Drosophi la species that choice of narrow and inferior diet may be strongly selected for by mortality factors unrelated to the food (Jaenike, 1985; Wallin, 1988).

308 Bernays

Among Lycaenidae, where ant tending of the caterpillars is very common, those species where larval tending by ants regularly occurs (with consequently better protection from natural enemies), have a broader host range (Pierce and Elgar, 1985; Smiley, et al., 1988). Among insect herbivores on bracken, Pteridium aquilinum specialists were found to be better at avoiding predation by ants than were generalists (Heads and Lawton, 1984; 1985). Among other animal groups too, there is evidence that predation pressure has a profound effect on food selection patterns by the prey (e.g. Hay and Fenical, 1988; Lima, 1988). It seems however, that the general significance of the third trophic level in determining host plant specificity in insect herbivores has not been addressed to date.

In a very extensive set of experiments with three bird species Maclean and co-workers (Maclean et al., 1989) present data demonstrating that acceptability of adult Lepidoptera is relatively low in species that have a narrow host range. If larvae had been used, the case may have been even stronger since many species of lepidopterans sequester toxins as larvae but some of them do not retain the toxins into the adult stage (Bowers, 1988). In any case, the data appear strongly to support the present thesis.

If the pattern of advantage gained by host specificity is substantiated in other systems, one may ask what the trade-offs are that promote the stable existence of both polyphagous and specialized herbivores. Although this will be the subject of a later paper, it may be mentioned that polyphages may have advantages nutritionally (Futuyma and Philippi, 1987; Jones et al., 1987; Bernays and Graham, 1988; Lee and Bernays, 1988), while there is the more obvious advantage of resource availability. The importance of this was clearly pointed out by Beaver (1979) who showed that polyphagy was more common in habitats of increasing plant diversity where it was thought that specific host finding may be difficult.

Since larval nutritional needs alter during development (Dadd, 1985), the ideal food is assumed to be different for individuals at different stages of development. In species having the appropriate capacity for mobility, a sensory system allowing intake of differing plant species will allow a greater choice of food for improving nutrient balance throughout larval life. That insects possess the capability of making sophisticated nutritional decisions is now known (Waldbauer et al., 1984; Simpson et al., 1988).

An additional advantage may accrue in polyphages relative to monophages due to the fact that specialist herbivores may be more vulnerable to attack from parasitoids that can use the host plant as a cue (Price, 1986),

From an evolutionary point of view, the predominance of host plant specificity in herbivores may be at least partly explained by the selection pressures exerted by their predators, which are mostly generalists. Their broad range of prey is a buffer which can maintain the population size against variations in density of prey species (Comins and Hasseit, 1987), and thus maintain tong lived and consistent pressure on herbivores generally, rather than the more ephemeral functional responses of specific parasitoids. It remains a possibility however, that in some cases, such as endophytic species, increased protection from natural enemies followed the development of high degrees of specificity.

Acknowledgements

I wish to thank Junji Hamai and Mary Cornelius for help with the experiments, as well as numerous colleagues and students who helped in many small ways. This work was partly funded by NSF grant BSR 8805856.

Host range in phytophagous insects 309

References

Beaver, R. A. (1979) Host specificity of temperate and tropical animals. Nature 281, 139-41. Bernays, E. A. (1984) Arthropods for weed control in IPM systems. In Biological Control in IPM Systems

(M. A. Hoy and D. Herzog, eds) pp. 373-88. Academic Press, New York. Bernays, E. A. 0988) Host specificity in phytophagous insects: selection pressure from generalist predators.

Entomol. Exp. Appl. 49, 131-40. Bernays, E. A. and Chapman, R. F. (1978) Plant chemistry and acridoid feeding behaviour. In Coevolution

of Plants and Animals (J. B. Harborne, ed.) pp. 100-41. Academic Press, New York. Bcrnays, E. A. and Chapman, R. F. (1987) Evolution of deterrent responses by phytophagous insects. In

Perspectives in Chemoreception and Behavior (R. F. Chapman, E. A. Bernays and J. G. Stoffolano, eds) pp. 159-74. Springer-Verlag, New York.

Bernays, E. A. and Cornelius, M. Relative acceptability of caterpillars with different host ranges to the Argentine ant lridomyrmex humilis. Oecologia (in press).

Bcrnays, E. A. and Graham, M. (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886-92.

Bowers, M. D (1988) Recycling plant allelochemicals for insect defense. In Arthropod Defenses: Adaptive Mechanisms and Strategies of Prey and Predators (D. L. Evans and J. O. Schmidt, eds) New York Press.

Brower, L. P. (1958) Bird predation and foodplant specificity in closely related procryptic insects. Amer. Natur. 92, 183-7.

Chapman, R. F. (1982) Chemoreception: the significance of receptor numbers. Adv. Insect Physiol. 16, 247-356.

Claridge, M. F. and den Hollander, J. (1980) The 'biotypes' of the rice brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl. 27, 23-30.

Comins, H. N. and Hassell, M. P. (1987) The dynamics of predation and competition in patchy environments. Theoret. Pop. Biol. 31,393--421.

Cottee, P. K., Bernays, E. A. and Mordue, J. A. (1988) Comparisons of deterrency and toxicity of selected secondary plant compounds to an oligophagous and a polyphagous acridid. Entomol. Exp. Appl. 46, 241-7.

Dadd, R. (1985) Nutrition: organisms. In Comprehensive Insect Physiology Biochemistry and Pharmacology Vol. 4 (G. A. Kerkut and L. I. Gilbert, eds) pp. 313-90. Pergamon Press, Oxford.

Damman, H. (1987) Leaf quality and enemy avoidance by larvae of a pyralid moth. Ecology 68, 87-97. Dempster, J. P. (1984) The natural enemies of butterflies. In The Biology of Butterflies (R. I. Vane-Wright

and P. R. Ackery, eds) pp. 97-104. Academic Press, London. Espelie, K. and Bernays, E. A. Diet related differences in the cuticular wax of Manduca sexta

larvae. J. Chem. Ecol. (in press). Feeny, P. P., Blau, W. S. and Kareiva, P. M. (1985) Larval growth and survivorship of the black swallow-

tail butterfly in central New York, Ecol. Monogr. 55, 167-87. Futuyma, D. J. and Moreno, G. (1988) The evolution of ecological specialization. Ann. Rev. Ecol. Syst.

19, 207-34. Futuyma, D. J. and Philippi, T. E. (1987) Genetic variation and variation in responses to host plants by

Alsophila pometaria (Lepidoptera: Geometridae). Evolution 41,269-79. Gilbert, L. E. and Singer, M. C. (1975) Butterfly ecology. Ann. Rev. Ecol. Syst. 6, 365-97. Gould, F. (1979) Rapid host range evolution in a population of a phytophagous mite Tetranychus urticae

Koch. Evolution 33, 791-802. Gould, F. (1988) Genetics of pairwise and multispecies plant-herbivore coevolution. In Chemical Mediation

and Coevolution (K. C. Spenser, ed.) pp. 13-56. Academic Press, New York. Hairston, N. G., Smith, F. E. and SIobodkin, L. B. (1960) Community structure, population control, and

competition. Amer. Natur. 94, 421-5. Hare, J. D. and Kennedy, G. G. (1986) Genetic variation in plant-insect associations: survival of

Leptinotarsa decemlineata populations on Solanum carolinense. Evolution 40, 1031-43.

310 Bernays

Hay, M. E. and Fenical, W. (1988) Marin plant-herbivore interactions: the ecology of chemical defense. Ann. Rev. Ecol. Syst. 19, 111--45.

Heads, P. A. and Lawton, J. G. (1984) Bracken, ants and extrafloral nectaries. II. The effect of ants on the insect herbivores of bracken. J. Anita. Ecol. 53, 1015-932.

Heads, P. A. and Lawton, J. G. (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation. Ecol. Entomol. 110, 29--42.

Holmes, R. T., Schultz, J. C. and Nothnagle, P. (1979) Bird predation on forest insects: an exclosure experiment. Science 206, 462-5.

Hsiao, T. (1982) Geographic variation and host plant adaptation of the Colorado potato beetle. In Proc. Fifth Int. Syrup. Insect-Plant Relationships (J. H. Visser and A. K. Minks, eds) pp. 315-24. Pudoc, Wageningen, The Netherlands.

Hunter, M. D. (1987) Opposing effects of spring defoliation on late season oak caterpillars. Ecol. Entomol. 12, 373-82.

Jaenike, J. (1985) Parasite pressure and the evolution of amantin tolerance in Drosophila. Evolution 39, 1295-301.

Jeffries, M. J. and Lawton, J. H. (1984) Enemy free space and the structure of ecological communities. Biol. J. Linn. Soc. 23, 269-86.

Jones, R. E., Nealis, V. G., lves, P. M., Scheermeyer, E. (1987) Seasonal and spatial variation in juvenile survival of the cabbage butterfly Pieris rapae: evidence for patchy density dependence. J. Anim. Ecol. 56, 723-38.

Kennedy, C. E. J. (1987) Attachment may be a basis for specialization in oak aphids. Ecol. Entomol. 11, 291-300.

Lawton, J. H. (1978) Host-plant influences on insect diversity: the effects of space and time. In Diversity of Insect Faunas (L. A. Mound and U. N. Waloff, eds) pp. 105-25. Blackwells, Oxford, England.

Lawton, J. H. (1986) The effect of parasitoids on phytophagous insect communities. In Insect Parasitoids (J. Waage and D. Greathead, eds) pp. 265--87. Academic Press, London.

Lee, J. C. and Bernays, E. A. (1988) The declining acceptability of spinach: the role of aversion learning. Physiol. Entomol. 13, 291-301.

Lima, S. L. (1988) Vigilance and diet selection: a simple example in the dark-eyed junco. Can. J. Zool. 66, 593-6.

Maclean, D. B., Sargent, T. D. and Maclean, B. (1989) Discriminant analysis of Lepidopteran prey characteristics and their effects on the outcome of bird-feeding trials. Biol. J. Linn. Soc. 36, 295-311.

Moran, N. A. (1986a) Morphological adaptation to host plants in Uroleucon (Homoptera: Aphididae). Evolution 40, 1044-50.

Moran, N. A. (1986b) Benefits of host plant specificity in Uroleucon (Homoptera: Aphididae). Ecology 67, 108-15.

Pierce, N. E. and Elgar, M. A. (1985) The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid. Behav. Ecol. Sociobiol. 16, 209-22.

Price, P. W. (1981) Relevance of ecological concepts to practical biological control. In Biological Control in Crop Production (G. C. Papavisas, ed.) pp. 3-19. Allenheld, Osmun Montclair, New Jersey.

Price, P. W. (1983) Hypotheses on organization and evolution in herbivorous insect communities. In Variable Plants and Herbivores in Natural and Managed Systems (R. F. Denno and M. S. McClure, eds) pp. 559-98. Academic Press, New York.

Price, P. W. (1986) Ecological aspects of host plant resistance and biological control: interactions among three trophic levels. In Interactions of Plant Resistance and Parasitoids and Predators of Insects (D. J. Boethel and R. D. Eikenbary, eds) pp. 11-30. Ellis Harwood, Chichester, UK.

Price, P. W., Westoby, M., Rice, B., AIsatt, P. R., Fritz, R. S., Thompson, J. N. and Mobley, K. (1986) Parasite mediation in ecological interactions. Ann. Rev. Ecol. Syst. 17, 487-505.

Simpson, S. J., Simmonds, M. S. J. and Blaney, W. M. (1988) A comparison of dietary selection behaviour in larval Locusta migratoria and Spodoptera littoralis. Physiol. Entomol. 13, 225-38.

Smiley, J. (1978) Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201, 745-7.

Host range in phytophagous insects 311

Smiley, J. and Wisdom, C. S. (1985) Determinants of growth rate on chemically heterogeneous host plants by specialist insects. Biochem. Syst. & Ecol. 13, 305-12.

Smiley, J. T., Atsatt, P. R. and Pierce, N. E. (1988) Local distribution of the lycaenid butterfly, Jalmenus evagoras, in response to host ants and plants. Oecologia 76, 415-22.

Southwood, T. R. E. (1986) Plant surfaces and insects - an overview. In Insects and the Plant Surface (B. Juniper and T. R. E. Southwood, eds) pp. 1-22. Edward Arnold, London.

Stamp, N. E. and Bowers, M. D. (1988) Direct and indirect effects of predatory wasps (Polistes sp.: Vespidae) on gregarious caterpillars (Hemileuca lucina: Saturniidae). Oecologia 75, 619-24.

Strong, D., Lawton, J. H. and Southwood, T. R. E. (1984) Insects on Plants: Community Patterns and Mechanisms. Biackwells, Oxford, England.

Thompson, J. (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl. 4, 3-14.

Usher, B., Bernays, E. A. and Barbehenn, R. V. (1988) Antifeedant tests with larvae of Pseudaletia unipuncta: variability of behavioral response. Entomol. Exp. Appl. 48, 203-12.

Waldbauer, G. P., Cohen, R. W. and Friedman, S. (1984). Self-selection of an optimal nutrient mix from defined diets by larvae of the corn-earworm Heliothis zea (Boddie). Physiol. Zool. 57, 590-7.

Wallin, A. (1988) The genetics of foraging behaviour: artificial selection for food choice in larvae of the fruitfly, Drosophila melanogaster. Anita. Behav. 36, 106-14.

Wasserman, S. S. and Futuyma, D. J. (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae). Evolution 35, 605-17.

Wrubel, R. P. and Bernays, E. A. (in press). Effects of some plant secondary compounds on larvae of Manduca sexta. Entomol. Exp. Appl.

Zwolfer, H. (1982) Patterns and driving forces in the evolution of plant-insect systems. In Proc. Fifth Int. Syrup. Insect-Plant Relationships (J. H. Visser and A. K. Minks, eds) pp. 287-96. Pudoc, Wageningen, The Netherlands.

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