ArticlePDF AvailableLiterature Review

Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation

February 2001
Annual Review of Entomology 46(1):703-27

February 2001
46(1):703-27

DOI:10.1146/annurev.ento.46.1.703

Source
PubMed

Authors:

Elizabeth A Bernays

The University of Arizona

This review points out the problem of processing multiple sensory inputs and provides evidence that generalists suffer a disadvantage compared with specialists with respect to efficiency of host plant choice and discrimination. The specialists' mechanisms for improved efficiency are discussed as well as some of the processes that may be selected to increase processing efficiency in generalists. The fitness consequences of differences in efficiency of specialists and generalists are pointed out. One of the major disadvantages for generalists is the increase in vulnerability to ecological risks, especially risks imposed by various natural enemies. Efficiency-related factors are indicated as previously underestimated elements that could influence host affiliations including diet breadth and changes in host plant use.

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Annu. Rev. Entomol. 2001. 46:703–27

NEURAL LIMITATIONS IN PHYTOPHAGOUS

INSECTS: Implications for Diet Breadth

and Evolution of Host Affiliation

E. A. Bernays

Entomology Department, University of Arizona, Tucson, Arizona 85721;

e-mail: schistos@ag.arizona.edu

Key Words specialization, herbivore, plant-insect interactions, neural constraints

■ Abstract This review points out the problem of processing multiple sensory inputs

and provides evidence that generalists suffer a disadvantage compared with special-

ists with respect to efﬁciency of host plant choice and discrimination. The specialists’

mechanisms for improved efﬁciency are discussed as well as some of the processes

that may be selected to increase processing efﬁciency in generalists. The ﬁtness con-

sequences of differences in efﬁciency of specialists and generalists are pointed out.

One of the major disadvantages for generalists is the increase in vulnerability to eco-

logical risks, especially risks imposed by various natural enemies. Efﬁciency-related

factors are indicated as previously underestimated elements that could inﬂuence host

afﬁliations including diet breadth and changes in host plant use.

CONTENTS

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 704

Detection of Relevant Information

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 705

Discrimination and Choice Among Alternatives

. . . . . . . . . . . . . . . . . . . . . . . . . 705

Task Attentiveness

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 706

Vigilance Against Risk

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 706

EVIDENCE FOR LIMITED BEHAVIORAL EFFICIENCY AMONG

GENERALISTS

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 707

MECHANISMS FOR EFFICIENCY IN SPECIALISTS

. . . . . . . . . . . . . . . . . . . . . 710

THE NONSPECIALIST’S DILEMMA AND SOME SOLUTIONS

. . . . . . . . . . . . 712

FITNESS BENEFITS OF BEHAVIORAL EFFICIENCY IN HOST

CHOICE AND FEEDING

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 715

DIVERSITY OF INSECTS AND PHYTOCHEMICALS AND

ASSOCIATION OF INSECT AND PLANT CLADES

. . . . . . . . . . . . . . . . . . . . . 717

CHANGES IN HOST AFFILIATION

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 719

CONCLUSIONS

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 721

0066-4170/01/0101-0703$14.00

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704 BERNAYS

INTRODUCTION

Behavior is the link between physiology and ecology of animals. Because behavior

is an expression of neural processes modiﬁed by physiological and environmental

factors, it is central to understanding interactions of organisms; therefore, studies

of both the functioning and constraints of the nervous system are important in

understanding animal evolution (104). For example, inherent limitations of the

nervous system constrain how much information may be processed in a given time

(49, 55, 98). This simple fact has major repercussions in ecology, and, in this re-

view, I make the case for neural limitations as a primary factor in phytophagous

insects’ interactions with plants, including their coevolution with plants.

Rapid, accurate perceptual judgments are relatively easy when choices are

strictly limited, but difﬁculties increase sharply as the perceived choices increase,

so that mechanisms for selecting and canalizing information are very important

(81). Generalists must make choices among a large number of options, and they

must do so with a nervous system that is deﬁnitely limited in its capacity to deal

with multiple inputs. It is known that, in humans, selective attention to subsets of

sensory inputs at any one time is critical for normal behavior (132).

Most experimental studies that demonstrate the constraints on processing sen-

sory information have dealt with vision. For example, animals cannot undertake

computations of the inputs across a whole visual ﬁeld at once. Instead, attention

to parts of the visual ﬁeld changes over time so that the whole can be interpreted

over a period (87). There may be sequential attentiveness to different stimuli in

order to encompass a large ﬁeld, or there may be prolonged engagement with a

few stimuli in order to evaluate them more fully (48). Paying attention to subsets

of the visual ﬁeld has been demonstrated to be important ecologically in a number

of contexts. Thus, the ability of birds to more readily notice cryptic prey with

experience indicates that certain visual cues have assumed speciﬁc importance,

and functionally this allows them to feed at a faster rate on a prey species that is

abundant (101, 105, 128). It follows that, if certain elements of the visual ﬁeld are

typically conspicuous, then they should be generally detected more readily than

elements that blend into the background. This is the presumed basis for the value

of visual “sign stimuli” used by animals in many different contexts, especially

intra- and interspeciﬁc communication (56, 129).

The need for attentiveness to relevant stimuli at any particular time does in-

volve all sensory modalities, however, and many different levels of the nervous

system (81). A generalist must compute a large amount of information from differ-

ent modalities and, in changing attentiveness to different stimuli, must also retain

other inputs in memory for comparison and subsequent evaluation. Animals have

extensive capacities for working memory, allowing them to make accurate be-

havioral selections after some experience. An alternative strategy, however, that

might be adaptive in a relatively predictable environment would be to have en-

hanced sensitivity to a few relevant and important stimuli and thereby simplify

the problem of selective attention. Such a strategy should require fewer receptors

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NEURAL LIMITATIONS IN INSECTS 705

and smaller memory capacity. It would involve more ﬁxed responses and perhaps

more decisiveness and faster reaction times. Presumably there is a tradeoff be-

tween the saving in neural machinery and efﬁcient decision making on the one

hand and the ﬂexibility of the broad sensory capacity combined with an ability

to switch attentiveness and an extensive use of learning on the other hand. The

former describes a specialist, while the latter describes a generalist.

In all animals cognitive decisions are complicated also by the fact that they must

be made in the context of a constantly changing internal chemical environment of

nutrients (116), toxins (66), hormones, and neuromodulators (2), as well as diverse

neural oscillatory processes (28) and complex, even chaotic neural interactions

(44). This complexity will inﬂuence the ﬁnal commands issued by the central

nervous system for a particular behavior, but, in this report, I focus on sensory

inputs from the environment and the importance of attentiveness in achieving

efﬁcient behavior under any particular set of internal conditions.

Since Levins & MacArthur (83) ﬁrst suggested that generalist insect herbivores

may ﬁnd it relatively difﬁcult to choose among alternative host plants, a number of

authors have proposed that neural limitations have greater signiﬁcance among gen-

eralists than among specialists (29, 47, 53, 54, 62, 64, 78, 82). Others have pointed

to the likelihood of neural constraints in insect herbivores as a reason for various

observed limits in insects’ behavioral repertoires (84, 95, 103). However, few at-

tempts have been made to make a synthesis of these ideas and to draw together the

available relevant material on phytophagous insects.

Identiﬁably different issues need to be considered in the context of neural

limitations. They are not mutually exclusive, and their relative importance varies

from one insect group to another and also in relation to the degree of specialization

of the insect being studied.

Detection of Relevant Information

For a predator, detecting cryptic prey is a major issue and requires attentiveness

to ﬁne details of prey features that may vary at different times, and for herbivores,

detection of both visual and olfactory cues can be important. Visually, shape or

reﬂectance pattern matter to some species, whereas chemically there may be par-

ticularly attractive mixtures of common green plant chemicals and chemicals that

occur in particular host taxa (19, 112). From work on humans, it is certainly

known that detection of “targets” becomes signiﬁcantly more difﬁcult as the target

becomes similar to alternative aspects of the visual ﬁeld, the “distracters” (81).

Host-speciﬁc characters that are conspicuous to the particular herbivore and stand

out from nonhost characters would be an advantage, particularly for specialists.

Discrimination and Choice Among Alternatives

This problem has been studied extensively in humans, and it is well known that

the more items there are to choose from, the longer it takes to make the choice.

It is in this context perhaps that herbivores have the greatest challenge. For them,

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706 BERNAYS

one of the environmental complexities is that communities of plants display an

unparalleled array of different volatile and nonvolatile chemicals (69), many

if not most of which are detectable by insect sensory systems, and many are

potentially noxious. Furthermore, nutritionally, plants demonstrate extreme varia-

tion so that decisions should involve some evaluation of nutrient quality. Idea-

lly, the best choices for food or oviposition must be made in a minimal amount of

time.

It is likely that optimizing both host quality and time taken for the decision

is difﬁcult. The individual may make very good decisions with respect to host

quality but take time to make them, or the individual may make rapid decisions,

perhaps compromising on host quality. Such alternatives have been demonstrated

often in other animals (52, 99). For small animals such as insects that often use

odor-conditioned upwind movements to locate food, decisions must be made ﬁrst

at a distance and then in the proximity of the plant or at contact. Finally, there

may be decisions concerning the precise plant part to utilize. For less than ideal

foods, a further decision may involve when to stop feeding (or when to leave a

host without laying a full complement of eggs). When comparing insect herbivores

with different diet breadths, efﬁciency may be measured in either quality (relative

ﬁtness value of the host selected, proportion of errors made, etc) or time taken to

make decisions.

Task Attentiveness

When a ﬁnal host choice has been made, attentiveness to the task of egg laying

or feeding must ensue rapidly and be maintained long enough to ensure that these

behaviors are completed without delay, so that predator avoidance behaviors and

full attention to all environmental risks can be quickly resumed. A generalist, with

a choice of similarly attractive hosts, may be more readily distracted by competing

sensory information about such alternatives than is a specialist, whose sensory

input or attentiveness is dominated by the speciﬁc host cues.

Vigilance Against Risk

The attention to host cues should not be so demanding of neural effort that poten-

tially more important inputs, such as the presence of a predator, are not noticed.

An inability to attend to danger during decision making while foraging has been

demonstrated to increase predation risk in ﬁsh (89), birds (85), and other animals

(115). Unlike vertebrates, insect herbivores are faced with a bewildering diver-

sity of predator and parasitoid types (124). The problem for them is potentially

much greater, because the cues associated with risk are extremely diverse, and the

numbers of natural enemies are also commonly large, so that a specialist, with less

host-related sensory information to process, may have an advantage in this context.

This review is an examination of the potential importance of neural limitations in

host plant choice by phytophagous insects. I ﬁrst provide evidence for the difﬁculty

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NEURAL LIMITATIONS IN INSECTS 707

they have in making decisions and for advantages accruing to specialists in each of

the four categories discussed above. I then discuss mechanisms by which specialists

may deal with informational complexity and the ways in which generalists may

improve their handling of potential sensory overload. I then survey the adaptive

signiﬁcance of efﬁcient decision-making processes, including obvious beneﬁts

of choosing high-quality food, the ways in which time may be limiting, and the

subtle but highly signiﬁcant role of improved decision making in attentiveness,

vigilance, and escape from natural enemies. I argue that these ecological beneﬁts

provide a strong case for the evolution and maintenance of restricted diets by

insect herbivores. I further suggest that evolution of phytophagous insect diversity

and the coevolution of insects and plants are directly related to neural limitations

and can be seen as a product of adaptations of nervous systems for channeling

information and making efﬁcient decisions.

EVIDENCE FOR LIMITED BEHAVIORAL

EFFICIENCY AMONG GENERALISTS

Data from a variety of herbivorous insect species now indicate that there are indeed

limitations on efﬁciency of the decision-making process. These data involve time

spent making a decision, ability to make the best choice among hosts of variable

quality, and levels of distraction during a host-related activity. Where comparisons

between specialists and generalists have been speciﬁcally tested, the specialists

have the advantage.

Little data are available on relative abilities of herbivores with different diet

breadths to detect host plants, because it is difﬁcult to determine what has been

detected before the insect approaches or reaches a plant, but a few observations

point to a problem and suggest that further work would be instructive. For example,

Papaj (96) showed that ovipositing females of the pipevine swallowtail Battus

philenor tend to specialize on one species of host plant at any one time and that, if

they do not, then host plants are found at a lower rate. At different times, however,

these butterﬂies might focus on alternative species. Focusing attention on one leaf

shape or developing a “search image” for a speciﬁc leaf shape apparently made

detection easier, and may be called an attentional shift (52a).

An interesting contrast is seen between the generalist species of Heliothis moths

and the closely related specialist, Heliothis subﬂexa. Many plants are highly at-

tractive to the generalists but are unsuitable for oviposition (61), but H. subﬂexa,

is strongly and solely attracted to its only host, Physalis spp. (131), suggesting

that the specialist is superior at detecting the appropriate host. Another suggestive

contrast is between the generalist aphid Myzus persicae, which lands indiscrimi-

nately on hosts and nonhosts (76), and the specialist aphid Cavariella aegopodii,

which is speciﬁcally attracted by host monoterpenes (39). In the realm of actual

detectability, however, no experimental contrasts between insects with different

diet breadths have been undertaken.

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708 BERNAYS

Ability to choose plants that are suitable hosts has been examined among but-

terﬂies with contrasting diet breadths. In a group of species and populations of

species that all utilize the nettle Urtica dioica, experiments were conducted to

compare those speciﬁc to nettle with those that also use a range of additional plant

species. The butterﬂies were given a choice of healthy green nettle plants and

senescing ones that were less suitable for growth of the caterpillars. The species

or populations of species with the greatest dietary restriction to nettle chose to lay

eggs on the healthy plants over the senescing ones, whereas the species or popu-

lations with broader host ranges did not distinguish between them, even though,

for all species, the healthy plant was the best choice for their offspring (74). This

difference is consistent with the notion that the generalists were less efﬁcient in

choosing accurately, perhaps because of neural limitations.

Experiments with four species of generalist larval Lepidoptera and four of

Hemiptera showed that, when a choice was available, individuals commonly did

not select the most favorable host or the best mixture for growth and development

(26, 119). Although there may be various functional explanations for this appar-

ently suboptimal behavior, the data are consistent with the notion that making the

most appropriate choices incurs some difﬁculty. Detailed observations on one of

the lepidopterans, Grammia geneura, showed that, although decisions were made

quickly, they tended to be poor decisions with respect to what was known to be

best choices for growth.

A comparative study of different populations of the aphid Uroleucon ambrosiae

with different diet breadths demonstrated that, during a 24-h choice test, the relative

generalists remained on unsuitable hosts long after the specialists had moved on

to the Ambrosia triﬁda, the superior host for both populations (22). These limited

data so far suggest that the specialists have an advantage with respect to accuracy

(i.e. ﬁtness value) of the choices made.

More comprehensive studies were undertaken to examine the question of time

taken to make decisions. Experiments with the generalist grasshopper Schisto-

cerca americana showed that individuals reared as specialists with a choice of

identical artiﬁcial foods made feeding decisions threefold more quickly and fed

with one-tenth of the amount of interruption compared with individuals reared

with a choice of similar artiﬁcial foods having different ﬂavors (11). In contrast to

the available studies on Lepidoptera, grasshoppers appear to make decisions about

eating particular foods that are generally good for growth (16, 116), although they

may often reject plants that could enable them to grow well because of the presence

of deterrent compounds (6, 7, 41). However, grasshoppers take time to make the

decisions, the decisions being longer for developmental generalists than for devel-

opmental specialists. Non-food-related sensory inputs can also interfere with the

food choice behaviors, because, in the experiments described above, the grasshop-

pers were tested a second time in a novel environment (a differently shaped cage)

and the differences between those with diverse foods and those with identical

foods became more marked. Recently, studies with the same species of grasshop-

per feeding on one or two different host plants have provided similar results, with

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NEURAL LIMITATIONS IN INSECTS 709

the individuals that have a choice of two foods taking longer to make decisions

and spending protracted times foraging (14).

A variety of experiments with the aphid U. ambrosiae demonstrated beneﬁts

in foraging efﬁciency for relatively specialized individuals (22). Populations of

this species differ in diet breadth although, for all of them, A. triﬁda is the most

acceptable host. Comparisons were made among these populations with respect to

some host-related behaviors in both choice and nonchoice situations. For example,

alates were tested in a wind tunnel with a single plant of A. triﬁda located upwind.

Those from the relatively specialized populations found the favored host in a wind

tunnel more quickly than did those of the relatively generalized populations, even

though there were no other plants present. It is not known whether this represents

a difference in detectability, or decisiveness, or some other factor, but no variables

relating generally to size or activity level of the aphids were observed. Experiments

with apterae that had a choice of A. triﬁda and various nonhosts provided in close

proximity, demonstrated that the specialists found A. triﬁda signiﬁcantly sooner

than did the generalists. Also, apterae placed on the favored hosts all probed quite

quickly, but the specialists reached the phloem, on average, hours sooner than did

the generalists. These data not only demonstrate a strong contrast between the

insects with different diet breadths but suggest that the specialists are more highly

stimulated or aroused by the host cues than the generalists when the stringency on

host acceptance has also apparently become relaxed. In all experiments, aphids

from the more specialized populations were relatively more efﬁcient.

Other observations are suggestive, although they do not provide deﬁnite evi-

dence. For example, Carey (36) showed that in the blue butterﬂy Glaucopsyche

lygdamus, those individuals that specialized their oviposition activity on one of

the available hosts were more likely to lay an egg in the limited landing time

than those that alternated among hosts. To evaluate the relative time taken to

make decisions by butterﬂies with different diet breadths would be worthwhile.

Certainly, some butterﬂies may make many lengthy visits to alternative individ-

ual host plants, spending ≥30 min in the process, before ﬁnally deciding on

one (117), and, with such times involved, differences would be relatively easy to

monitor.

With respect to task attentiveness, it is clear from the results on grasshoppers

described above that part of the problem for individuals reared as generalists was

that meals were interrupted relatively more frequently and for longer periods,

suggesting that these generalists were being distracted, and observations showed

that individuals in this food treatment were more likely to antennate alternative

foods during their meals. In a different study, detailed observations on the highly

polyphagous Bemisia tabaci showed conclusively that adults with a choice of

potential foods spent less time on any single food than those with only one food

plant present. Indeed, individuals were highly likely to move away from the best

food plant if additional plant species were present, but they were most likely to

stay on the food plant if only conspeciﬁc plants were in the vicinity (12). These

data suggest that individuals were distracted when there was additional relevant

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710 BERNAYS

food-related information present, which may have complicated their sensory

processing.

Further studies are required to enable us to generalize, but to date specialization

appears to be associated with measurable and signiﬁcant advantages. These ben-

eﬁts vary with the insect taxon but include the amount of time taken to reach the

host plant, the time taken to make decisions to accept or reject potential food, the

time taken to begin ingestion or to lay an egg, and the time spent in pauses during a

meal. In addition, the degree of ﬁdelity to the most suitable host in the presence of

less suitable host species and genotypes or the ability to choose superior hosts in

the presence of a choice of mixed-quality hosts is shown to be greater in specialists

than in relative generalists.

No studies are available that compare specialists and generalists within a taxon

in their degree of vigilance against natural enemies or their ability to escape

attack. A comparative study with caterpillars under attack from vespid wasps

clearly demonstrated that specialists had a major advantage (5), but the relative

importance of vigilance and other factors such as different kinds of defense was

not documented. That grasshoppers switched from their rearing cages to novel

cages increased the time taken to make feeding decisions (11) does suggest that

attentiveness to nonfood factors (i.e. potential risk) had some impact, especially

since this was greater for the individuals reared as generalists than for individuals

reared as specialists.

MECHANISMS FOR EFFICIENCY IN SPECIALISTS

Insects searching for an acceptable host plant must ﬁrst locate and identify an

appropriate plant species. Accurate selection of host taxa and proper assessment

of individual plant quality should also be achieved with minimum time under most

ecological conditions. If speed, taxonomic accuracy, and quality of choices are

all to be maximized by very small animals in a very complex sensory world, the

adoption of high-contrast signals would be expected, as well as other processes

that improve the efﬁciency of neural processing (29). Certainly it has been known

for a long time that unambiguous signals are required for efﬁcient release of re-

ceiver behavior (71). Such are the widely occurring species-speciﬁc “sign stimuli”

ﬁrst described in detail for intraspeciﬁc interactions among stickleback ﬁsh (130).

These speciﬁc signals enable animals to use simple rules of behavior, ensuring

rapid recognition and discrimination and quick, appropriate responses. Among

phytophagous insects, in which chemicals are of paramount importance, it has

been known for some time that plant secondary metabolites can provide insects

with such signals (63).

The majority of insect herbivores are relative specialists, using a very restricted

number of hosts that typically share characteristic phytochemicals, some vola-

tile and some nonvolatile. A subset of these compounds seems to be of great

importance for identiﬁcation of the host (for reviews, see 19, 112, 122).

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NEURAL LIMITATIONS IN INSECTS 711

Among specialists that have been studied so far, most seem to be speciﬁcally

and highly sensitive to particular host odor components (1, 67, 127) or to charac-

teristic mixtures of volatile compounds (110, 133). Such sensitivity of olfactory

systems is normally seen as an adaptation to host ﬁnding, especially when it can be

demonstrated that the herbivore is attracted (usually by odor-conditioned anemo-

taxis) over long distances. For example, the cabbage seed weevil Ceutorhynchus

assimilis is attracted from >20 m by isothiocyanates in its host plant (57). There

are additional functions for such sensitivity, however; the attentiveness or arousal

achieved from perception of these chemicals may be important in odor-conditioned

visual stimulation that may be the mechanism of synergism among chemical and

visual cues used in host discrimination (68). Just as in vertebrates, a mechanism

for increasing attentiveness to particular cue types could increase detectability of

related ones (8). I argue here that speciﬁc host odors have an important role to play

in efﬁcient (rapid and accurate) detection and decision making. In other words,

the speciﬁc odor forms a high-contrast signal that rapidly releases the appropriate

behavior.

Sensitivity may be achieved through having relatively large numbers of olfac-

tory receptors (37). For the aphid species U. ambrosiae, the specialists had sig-

niﬁcantly larger numbers and sizes of secondary rhinaria than the generalists (23).

There may be a high proportion of the olfactory receptors speciﬁcally tuned to

particular host odors. This has been demonstrated in the cabbage seed weevil,

for example, in which 30% of the olfactory neurons on the antennae respond

to the isothiocyanates of its host (32). Finally, for insects in which vision is

of paramount importance, such as many butterﬂies (106), visual cues may be

more important than odors, and a specialist could home in on a particular shape

especially if its host plant has a leaf shape that is characteristic in the speciﬁc

location.

Odors may function in behavioral efﬁciency after contact with the host, increas-

ing arousal, attentiveness, and decisiveness, but for most specialists examined in

sufﬁcient detail, gustatory cues that signal the speciﬁc host are also important and

arguably play similar roles. In some extreme specialists, great sensitivity to one

or a few host-speciﬁc chemicals appears to result in such chemicals being the

dominant factor in host selection (60, 100, 112). That butterﬂies such as check-

erspots utilize plants from multiple families, simply because of the presence of

iridoid glycosides in host plants that are otherwise extraordinarily diverse physi-

cally and chemically (33), is startling evidence of the impact and dominance of

simple chemical signals on insect behavior and host use. Evidence is beginning

to suggest that such cases are not unusual. Indeed, in a recent study, the sensi-

tivity of the cabbage root ﬂy to a novel chemical in brassicas was found to be

so extreme that the sensitivity of the chemoreceptors is actually in the range nor-

mally associated with pheromone detection (108). It is too soon to tell whether

such phenomena are widespread, but their very occurrence may suggest a value

greater than host identiﬁcation per se. The remarkable diversity of chemicals found

among plant taxa and within individual plants allows potentially clear signals for

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712 BERNAYS

every specialist herbivore, whether it specializes at the level of plant species, tribe,

or family (9). The convergent evolution of certain chemical products in different

plant groups also has allowed certain insect species to use unrelated host plants, as

with the Lepidoptera, for example, which use iridoid glycosides (checkerspot but-

terﬂies) or glucosinolates (cabbage butterﬂies) for host identiﬁcation. That plant

taxa heavily endowed with relatively unusual chemicals or suites of chemicals are

often hosts for relatively large numbers of specialist-insect species (4) could also

suggest that the chemicals are not just plant defenses to be overcome but strong

cues that are useful for insects in that they provide signals for making positive

choices.

As well as being sensitive to and attracted by host-speciﬁc chemicals, special-

ists tend to be deterred more than generalists by nonhost secondary metabolites

(18, 27), and I suggest that specialists beneﬁt from the strong contrasts between

positive cues from hosts and negative cues from nonhosts.

THE NONSPECIALIST’S DILEMMA

AND SOME SOLUTIONS

Presumably, beneﬁts of polyphagy outweigh disadvantages for those species that

use many host plants, but, because efﬁciency of decision making is likely to be of

great signiﬁcance in an ecological setting (see below), one might expect there to be

selection for mechanisms to ameliorate problems of reduced efﬁciency. One such

mechanism may be to maintain a larger and more sophisticated nervous system,

as suggested by Levins & MacArthur (83; see below). Many insect species are

oligophagous and perhaps gain some of the neural advantages of speciﬁcity while

retaining some ﬂexibility. However, several neural processes may aid improved

contrasts for the insect. Interactions among sensory inputs at the sense organ or

beyond can function to reduce ambiguous inputs, increasing the likelihood of

a clear negative or positive signal. For example, each sensory system has some

kind of lateral inhibition whereby the dominance of a particular sensory input is

enhanced by reduction of competing but minor inputs. This is best known in the

visual system, but there is evidence of its occurrence in other sensory modalities,

including hearing and olfaction (9).

In general it is thought that negative and positive inputs are additive centrally,

although the weights of these input types may differ (112). If the contact chemore-

ceptor cells respond to positive and negative inputs independently, then an additive

effect would lead an insect to respond to whatever the balance may be at a particular

time. If a positive input such as sugar is held constant, increasing concentrations

of a deterrent such as nicotine result in a typical concentration-response effect but

one that is shifted to the positive side by the presence of the sucrose. Among phy-

tophagous insects, interactions among chemical stimulants at the level of chemore-

ceptors commonly occur, with deterrents reducing input from positive neurons and

vice versa (112, 114, 134). Simple models illustrate that such interactions between

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NEURAL LIMITATIONS IN INSECTS 713

positive and negative chemicals in the sensillum can sharply alter the shape of

dose response functions so that a gradual change without interactions becomes a

step function when interactions occur (9). Critical experiments are needed to test

the relevance of this observation in practice, but Blaney & Simmonds (31) suggest

that such interactions may be more common in insects with broad host ranges. If

so, this may be seen as one of the ways in which an insect with less deﬁnitive

signal detection for high-quality hosts may improve its ability to make a positive

or negative decision quickly. An additional factor among caterpillars may be

that specialists are more readily deterred by nonhost compounds, thus improving

contrast between host and nonhost (21).

It has also been shown in generalist grasshoppers that the ﬁring of one contact

chemoreceptor cell can inhibit the ﬁring of another with different speciﬁcity in

the same sensillum—an interactive effect occurring after the production of the

generator potential (134). This ﬁnding has parallels in lateral inhibitory mecha-

nisms described for a variety of other sensory systems that are known to sharpen

resultant images. Such processes may also be important in producing the particular

and synchronous ﬁring of a suite of taste cells, which appears to occur in some

beetles only when the requisite mixture of plant chemicals is present (121). With

respect to the olfactory system, there is also clear evidence of lateral inhibition at

the level of the olfactory lobes and at other steps beyond the peripheral interactions

(43).

Highly synergistic behavioral effects of multiple host compounds have been

described (120, 123) that may depend on the many additional processes occur-

ring more centrally in the nervous system and the necessary ﬁltering of the most

appropriate information at any particular time (see 9 for additional references).

Similarly, behavioral studies indicate that insects, like other animals, respond dif-

ferently to the same level of inputs depending on current behavior. A butterﬂy

laying an egg, for example, is relatively insensitive to disturbance (97), and any-

one who has spent time observing insect behavior has probably been struck by the

fact that individuals are less readily disturbed during many activities than when

they are apparently resting. Central ﬁltering or modulation of circuitry ensures that

one behavior is given priority at any one time.

Plasticity of behavior is undoubtedly critical among species whose choices of

hosts vary in availability unpredictably. In such cases, ﬁne-tuning of the nervous

system through experience may provide many of the beneﬁts enjoyed by special-

ists. Many species narrow their preferences as a result of experience (75), although

the underlying mechanisms are not known (30), but in some cases the change

was shown to result from increased or decreased sensitivity of their chemorecep-

tors to certain metabolites (107). Thus, currently relevant cues may be enhanced

by increasing sensitivity to them, while alternative cues may become deterrents.

Fine-tuning may also occur centrally, narrowing the range of positive and neg-

ative cues that are attended to (97). There is no reason to assume that there is

a correlated change in normally measured performance characteristics, because

the phenomenon is even found in male tephritid ﬂies that are not feeding and are

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714 BERNAYS

separated from females. In this case, experience with fruit of one type predisposes

the ﬂies to land on the same fruit type again and also makes it less likely that they

will land on an alternative fruit type (102).

Associative learning may serve to increase efﬁciency of decision making as well

as having other possible ﬁtness beneﬁts (46, 50, 73). It is generally expected to have

greatest value among generalists for reasons related to choosing highest-quality

hosts or most abundant suitable hosts. In the context of the argument presented

here, it should also have value in improving rapidity of decision making.

Associative learning has been given most attention in ﬂower visitors, especially

honey bees and bumble bees and, as generalists, the ﬁndings are also relevant to

generalist herbivores. Improved efﬁciency of foraging has been the major focus, in

particular choosing a ﬂower type (shape, color, and odor) with high or consistent

levels of nectar and choosing a ﬂower type for which the mechanics of handling

have been learned (optimized) (e.g. see 88). What has had less study is the pos-

sibility that the attentiveness aspect of the learning process may be important in

itself. By focusing on speciﬁc cues (even successive ones, each for a short time),

a bee can be more effective in decision making at each point of its foraging activ-

ity. This case has been further argued elsewhere (13). There is a study, however,

demonstrating speciﬁcally that bees can selectively attend to minor cues in an en-

vironment. Individuals were unable to learn two camouﬂaged shapes for a food

reward, but, after training to the two shapes without camouﬂage, they were able

to attend to them when camouﬂaged (136).

In addition to adaptive aspects of learning in bees and other ﬂower visitors,

memory constraints have typically been put forward as a mechanism underlying

ﬂoral constancy; that is, because it may be difﬁcult to learn and keep in memory a

variety of ﬂoral types requiring different types of manipulation, bees should show

ﬁdelity to one ﬂoral type for extended periods. However, it is difﬁcult to weigh

the relative importance of limitations on memory and limitations on information

handling when there are several behavioral options at any particular time (42)—

perhaps, with limitations on processing, single-minded attentiveness to a few cues

has as much of a role to play as limitations on the capacity for short- or long-term

memory. It is interesting that, even in the absence of nectar rewards, individual

bees consistently go to artiﬁcial ﬂowers of particular colors, with different bees

focusing on different colors and each switching only after a period of ﬁdelity (70).

This suggests that there is an innate pattern of remaining constant to one cue for a

period, irrespective of memory factors or rewards.

A minority of insect herbivore species are extreme individual generalists, appar-

ently adapted to situations in which food plant quality or abundance is variable or

unpredictable or the food plants are all very rich in potentially noxious secondary

metabolites (119). Such herbivores engage in food mixing, eating a variety of

plants and frequently making choices about what to eat and what to ignore. Such

food mixers often appear to be stimulated by novel chemicals, potentially reducing

the inefﬁciency and complexity of decision making (15, 17, 119). In addition, in

the grasshopper Taeniopoda eques, runs of ﬁdelity to one plant species occurred

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NEURAL LIMITATIONS IN INSECTS 715

even during series of encounters with diverse plant species, suggesting that, like

bees, they focused sequentially on particular food items (29).

Diet quality alters relative acceptability of alternatives depending on nutri-

ent need—a ﬂexibility that is dependent on variation in the strength of inputs

from different nutrient chemoreceptors (116). Such physiological feedback may

improve the speed or accuracy of decision making although, among herbivores,

it has been clearly demonstrated so far only in grasshoppers and in generalist

caterpillars.

FITNESS BENEFITS OF BEHAVIORAL EFFICIENCY

IN HOST CHOICE AND FEEDING

I argue that behavioral efﬁciency is considerably more than simply an ability

to choose a reasonable host (26, 74). Speed of host ﬁnding and host choice has

several potential beneﬁts, and these are compounded with the need for choosing an

appropriate plant taxon and individual plant or plant part of relatively high quality.

Clearly, choosing the best of available alternatives is very important and may be

optimized in species that are egg limited.

Speed is particularly important for ovipositing insects that are time limited

for any reason, such as those that have limited suitable ﬂight periods (44, 77). In

a more general sense speed has been considered important in optimal foraging

models and in apostatic food selection, in which time is at a premium because

of resource limitation and/or competition (113, 125). Speed of decision making

may be much more critical for survival in phytophagous insects, however. I argue

that, for animals as small as insects, the ecological risks are sufﬁciently severe

that attentiveness to them is always important and that time takes on an additional

signiﬁcance in decision-making processes themselves. In particular, time mat-

ters in that fast decisions reduce opportunity for predation during foraging. The

limits on simultaneous processing of diverse sensory inputs may impose a need

for selective attention to different tasks in succession. Focusing attention on ﬁnd-

ing and choosing host plants reduces attentiveness to other risks and necessitates

haste in the choice of host and execution of host-related behaviors. Alternatively,

divided attention between foraging and escape from predators means that the sim-

plest possible cues about resources would be an advantage. Although not studied

speciﬁcally in insects, it is well known in birds and ﬁsh and mammals that foraging

and predator avoidance compete for attention, with outcomes that usually involve

a reduced ability to obtain suitable food (79, 85, 90, 91, 135) if not greater levels

of predation (52a, 79). The neural limitations that require selective attention and

lead to divided attention under predation risk have measurable costs. The problem

is further compounded by the fact that vigilance cannot be maintained for long

periods without rest (51).

Predation risk is one that is difﬁcult to quantify and thus to evaluate as a selective

factor in herbivore-plant interactions, but there are indications that this has often

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716 BERNAYS

TABLE 1 Results of observations on numbers of active predators and numbers of insect

herbivores in ten 0.25-m

spaces in a Costa Rican rainforest during a period of 15 min

No. of invertebrate No. of visible Ratio of predators:

predators insect herbivores insect herbivores

Mean 6 3 2:1

Range 2–11 0–9 2:0–2:1.5

been greatly underestimated. It is not that predation (as well as parasitism) isn’t

recognized as one of the major risks of insect herbivores; extraordinary levels and

types of predation have been documented in numerous systems (see 124). Rather,

the minute-by-minute implications with respect to behavioral choices have not

been thoroughly considered. One indication of the instantaneous importance of

predators for insect herbivore behavior was obtained from observations on rela-

tive numerical abundance of insect herbivores and predaceous invertebrates over

a period of time in tropical vegetation. From ten 15-min continuous observa-

tions of forest edge plots (1 m high × 1 m wide × 0.25 m deep) in the Costa

Rican rainforest, the average numbers of active invertebrate predators and par-

asitoids (including jumping spiders, reduviid bugs, ants, and wasps) exceeded

those of visible herbivores (caterpillars, plant-sucking Hemiptera, grasshoppers,

and leaf beetles) by nearly 2 to 1 (Table 1). The relatively large numbers of natural

enemies of herbivores is a reﬂection of their mobility and provides direct evi-

dence of the persistent problem of this kind of ecological risk, requiring constant

attention.

Continuous watching of caterpillars for 10 h each day in the ﬁeld in California

demonstrated considerable predation by invertebrate predators, even on an apose-

matic species. Furthermore, the predation was ≤100-fold more likely during feed-

ing than during resting (10), thus illustrating a ﬁtness beneﬁt of rapid feeding rates.

Even ﬂoral visitors such as bees may beneﬁt greatly from learned efﬁciency in this

context, such as may develop in the course of ﬂoral constancy, because preda-

tion and parasitism risk at ﬂowers can be very high (93). In addition, I argue that

intermittent, hesitant, or picky feeding behaviors and any kind of dithering are dan-

gerous not only because an insect is conspicuous but because an animal attentive

to food-related activities is unlikely to be attentive to simultaneous environmental

risks (49).

Nutrient quality interacts with the problems of risk and attentiveness. Because

protein is often at low concentrations in leaves (especially older leaves) and the

nitrogen requirements of insects tend to be relatively high, herbivores often com-

pensate by eating large amounts. Not only is high-quality food better for growth,

but the risk of mortality via predation is reduced on nutritious hosts because less

time must be spent feeding and thus being vulnerable to predators. Indeed, per-

haps the ﬁtness advantage associated with predator avoidance exceeds that of

increased growth rate. Safety and growth are important together, of course, in a

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NEURAL LIMITATIONS IN INSECTS 717

larger time scale—feeding on high-quality foliage may also reduce development

time, reducing the lifetime risk.

Leaves present very diverse physical challenges, and highly diverse solutions

have been found by insects through adaptations of mouthpart morphology. The

frequency with which certain mandible types have evolved in separate insect lin-

eages with similar types of food indicates the adaptive value of these structures

(8, 25). Furthermore, evolution of mouthparts can be very rapid (35). In view of

the ever-present risk of predation, structures that determine handling time may be

under great selection pressure. Indeed, the preponderance of herbivores that feed

on young, easily handled leaves is probably a matter of safety as much as nutrition.

In summary, the ﬁtness advantage of behavioral efﬁciency measured as speed

of ﬁnding and deciding on a host and of executing behaviors is largely a function

of escape from natural enemies, at least for insect herbivores.

A completely different but additional potential ﬁtness advantage of specialists

is the predicted simpliﬁcation of their nervous systems. Specialist grasshoppers

have smaller numbers of gustatory sensilla than do generalists (37), and studies

clearly indicate that, as diet breadth has decreased in various taxa, the numbers of

receptors have diminished, with the few extreme specialists having fewest contact

chemoreceptors (38). Even rearing individuals in an environment with reduced

sensory input can cause the development of fewer olfactory and gustatory sensilla

(20, 40, 109). However, in the aphid, U. ambrosiae, larger numbers of antennal

sensilla were found in populations that had narrower diets than in those with

broad diets (23). Nothing is known about the investment in other parts of the

neural machinery, although there are indications that the sizes of various parts of

the integrative center of insect brains are correlated with behavioral complexity

(see 29 for additional references). It is also true that, in the Orthoptera, in which

generalists predominate, brain size overall is much greater than in similarly sized

hemipteroid or holometabolous species, in which specialists predominate. Further

work is needed to establish whether there are adaptive patterns with respect to diet

breadth.

DIVERSITY OF INSECTS AND PHYTOCHEMICALS

AND ASSO CIATION OF INSECT AND PLANT CLADES

It has become clear from both fossil studies (80) and molecular phylogenies (58, 59)

that, among all of the herbivorous insect groups studied, great diversiﬁcation is

historically associated at some level with the expansion and increased diversity of

angiosperms. Furthermore, among sister clades of insects with different feeding

habits, it is the phytophagous ones that have diversiﬁed to a remarkable degree.

In the face of the extraordinary diversity of plant secondary metabolites, chem-

istry appears to provide the link between insect diversity and angiosperms, with

the best known scenario entailing coevolutionary arms races between insects and

plants.

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718 BERNAYS

Among the hundreds of thousands of plant phenols, alkaloids, terpenoids, iri-

doids, ﬂavonoids, steroids, and other secondary chemicals, many appear to have no

effects at all on insect herbivores, whereas others stimulate feeding and/or growth.

Some are sequestered, either obviously in aposematic species (34) or in the cuticle

of species not warningly colored (24), although some insects gain protection from

predators as a result of the gut contents alone (126). Many are clearly toxic in gen-

eral and serve as plant defenses against many herbivores (111). It is not at all clear

whether an inability to deal with toxins reﬂects an ability that has been lost, as sug-

gested for grass-feeding grasshoppers (6, 21), or whether the plants have evolved

speciﬁc defenses against particular insect herbivores (4). Both seem likely. When

there are more or less congruent clades of particular insect taxa and their host

plants, arms races and coevolution tend to be invoked as the underlying reasons

for both the diversity of insect herbivores and patterns of phylogenesis (59). How-

ever, the compilation of studies presented by these authors indicates that, although

some degree of congruence in insect and plant phylogenies is common, it is rarely

precise.

Theoretically, patterns of parallel phylogenies could also easily arise from herbi-

vore tracking of diverse genotypes in a plant population and subsequent speciation

of herbivores on established plant host races or species. Neither fossil nor molec-

ular studies are likely to resolve the issue of precisely when changes occurred in

either plant or insect, so that the mechanism underlying patterns of congruence

will remain uncertain. Many recent phylogenetic studies show relatively very poor

correlation between insect and host plant clades (3, 65, 92), with strong evidence

for repeated moves between different established plant lineages. There is often

an indication that insects have moved to plants with similar chemical proﬁles,

regardless of whether the plants are related. Further resolution of the alternatives

through phylogenetic studies requires, in addition, knowledge of plant chemistry

and insect behavior at least. The clearest evidence for tracking chemicals in this

way has been demonstrated in one study of a group of beetles and their host plants

(3). The question then is, do they track a suite of chemicals that they are able to

tolerate (or even beneﬁt from because they obtain protection by using the chemi-

cals as defense) or do they track a chemical or suite of chemicals that provides the

signals of their host plants? The latter has sometimes been described as a neural

constraint, yet such a constraint carries with it the great advantage of having a

clear sign stimulus.

If strong and unambiguous cues assist insect herbivores in making rapid deci-

sions and remaining attentive to a particular host during feeding or oviposition,

selection on the sensory system and its central nervous projections would favor

those insects that match the ﬁne-tuning of their detection of distinctive signals

with particular plant chemotypes. Because the primary value of this ability relates

to survival in the presence of predators, selection on the nervous system would

thus be acting through mechanisms that could improve vigilance. In any case, as

plants changed and diversiﬁed chemically, insect herbivores, being so dependent

on speciﬁc cues, might also have changed and diversiﬁed so that discrimination

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NEURAL LIMITATIONS IN INSECTS 719

of signals from hosts could be maintained at maximum levels of detection and

contrast in every particular population. Many secondary chemicals in plants have

been considered toxic when closer study has demonstrated that they are actually

deterrents only (18), the effects on test insects being caused by starvation. The

interesting thing about this ﬁnding is that it demonstrates how dependent the in-

sects in question have become on particular cues that characterize their normal

hosts. It also illustrates the limitations incumbent on specialists that have opti-

mized in the direction of behavioral efﬁciency on one plant chemotype. Thus the

evolution of highly sensitive chemoreceptors for detecting host-speciﬁc chemi-

cals, while valuable for behavioral efﬁciency, may greatly restrict what can be

accepted.

Testing this hypothesis requires examining populations of particular insect her-

bivore species, establishing the level of speciﬁcity of relevant receptors for host-

speciﬁc compounds, and comparing the degree of vigilance with the speciﬁcity

of the receptor or neural pathway. For example, survivorship in the presence of

predators would be correlated with degree of match between receptor speciﬁcity

and presence of speciﬁc compounds in the host(s).

Interestingly, even if tracking of plant chemotypes were to be ﬁrmly established

as a major process in evolution of host afﬁliation, coevolutionary processes could

still be important. However, rather than invoking arms races and toxins, the cur-

rency would be in terms of signal information. For example, a herbivore may use

chemical A as a sign stimulus for its host. Populations of the plants may evolve

to produce an enzyme altering A to B. If there is rigidity in the chemosensory

system of the herbivore that relates to sign stimuli, plants with B may escape her-

bivory until variation in the herbivore allows a switch to plants containing B as the

appropriate signal.

CHANGES IN HOST AFFILIATION

An insect herbivore species may show genetically based changes in its speciﬁcity

(how many plant species it uses) or in the rank order of its preference (which plant

species is preferred). Speciﬁcity evolves in both directions in some phytophagous

groups. Rank order preference changes are the basis of host shifts seen in clades

of highly specialized insects. With respect to speciﬁcity, in the absence of risk

(ecological or physiological), an ability to use many plant species is an advantage.

By contrast, using few or one plant species can improve ﬁtness when there are

tradeoffs obtained on different plants either for physiological or for ecological

reasons. Physiological factors examined usually involve growth and development

or correlates of these such as digestion and detoxiﬁcation ability. Ecological factors

have not had the same attention but could involve such things as the differential

crypsis (46a) and other morphological traits that inﬂuence escape from natural

enemies and, as I emphasize here, the ability to ﬁnd, select, and attend to the speciﬁc

plant so efﬁciently that vigilance towards natural enemies can be maintained or

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720 BERNAYS

TABLE 2 Possible changes that may occur neurally to effect behavioral changes in relation

to plants

Genetic change Effect

Binding-protein conformation Determines nonpolar compounds carried

to dendrite of chemoreceptor

Change in conformation of protein at Inﬂuences sensitivity of cell to particular

receptor site on chemoreceptor compounds

Alter numbers of receptor sites for Alter sensitivity of cell to particular

particular chemicals on chemoreceptor compounds

Alter second messenger or membrane Alter sensitivity of + or − cell overall

properties of + or − chemoreceptor

Alter gene expression pattern of receptor Switch effect of stimulation from + to −

proteins on + and − cells or vice versa

Alter wiring of sense cells or interneurones Switch effect of stimulation from + to −

or vice versa

Alter levels of one or more neuromodulators Alter weighting of different + and − inputs

at one or more synapses

Alter sign of synaptic inputs anywhere in Alter weighting of different + and − inputs

the path to controlling center

enhanced. Variation in rank order of preference within and between populations

of an insect species may be the norm (45, 46, 72, 94, 118, 128), in which case one

can envisage opportunities for divergence into separate species with different hosts

(46a).

If it is true that the basis for limited host use in the majority of phytophagous

insects lies with behavior (neural) rather than with postingestive constraints as

suggested elsewhere (18), then it is to the nervous system that we must look for

variation. Table 2 lists the major types of change that could occur. Some appear

to be more likely for changes of speciﬁcity, whereas others may be more likely for

changes of preference.

Evolutionary change in sensory processes and patterns of host afﬁliation are

probably strongly inﬂuenced by the group of insects concerned. At the level of

order, it should be noted that orthopterans have large brains and very large num-

bers of sensilla (38) and probably depend on integrative processes more than on

directly labeled lines from chemoreceptors that clearly deﬁne sign stimuli. Lep-

idopteran larvae, by contrast, have very small numbers of chemoreceptors and

simple brains. For this reason, a small change in a receptor or synapse may

have a large impact on behavior of a caterpillar but little effect on behavior of

a grasshopper. Thus it has been argued that nonorthopteroid insects may evolve

detection and discrimination systems relatively rapidly (37) and so be able to track

plant chemical evolution in a way that is less likely for grasshoppers. If this were

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NEURAL LIMITATIONS IN INSECTS 721

so, it would provide additional evidence for the importance of coevolution of insect

receptor systems and plants. In other words, it would provide a mechanistic basis

for commonly found congruence in plant and insect clades and for phytophagous

insect diversity.

CONCLUSIONS

This review depends on knowing the insect—understanding it as an organism. The

details of behavior and physiology, especially neurophysiology, have suggested

a theoretical approach to the study of insect-plant interactions, speciﬁcally the

limitations of the nervous system and the effects of these limitations in ecology and

evolution. It is suggested that the combination of neural limitations on processing

favors reduced diet breadth and that the selection pressure probably acts through

effects on vigilance and, thus, ultimately via natural enemies.

ACKNOWLEDGMENTS

I am grateful to various friends and colleagues for discussion about these issues

including Reuven Dukas, Michael S Singer, Dan Funk, Dan Papaj, and especially

Reg Chapman, whose critical appraisal made this work much better.

Visit the Annual Reviews home page at www.AnnualReviews.org

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Annual Review of Entomology

Volume 46, 2001

CONTENTS

BIOGEOGRAPHY AND COMMUNITY STRUCTURE OF NORTH

AMERICAN SEED-HARVESTER ANTS, Robert A. Johnson 1

MATING BEHAVIOR AND CHEMICAL COMMUNICATION IN THE

ORDER HYMENOPTERA, M. Ayasse, R. J. Paxton, J. Tengö 31

INSECT BIODEMOGRAPHY, James R. Carey 79

PREDICTING ST. LOUIS ENCEPHALITIS VIRUS EPIDEMICS:

Lessons from Recent, and Not So Recent, Outbreaks, Jonathan F. Day 111

EVOLUTION OF EXCLUSIVE PATERNAL CARE IN ARTHOPODS,

Douglas W. Tallamy 139

MATING STRATEGIES AND SPERMIOGENESIS IN IXODID

TICKS, Anthony E. Kiszewski, Franz-Rainer Matuschka, Andrew

Spielman 167

GENETIC AND PHYSICAL MAPPING IN MOSQUITOES: Molecular

Approaches, David W. Severson, Susan E. Brown, Dennis L. Knudson 183

INSECT ACID-BASE PHYSIOLOGY, Jon F. Harrison 221

EVOLUTION AND BEHAVIORAL ECOLOGY OF

HETERONOMOUS APHELINID PARASITOIDS, Martha S. Hunter,

ames B. Woolle

251

SPECIES TRAITS AND ENVIRONMENTAL CONSTRAINTS:

Entomological Research and the History of Ecological Theory, Bernhard

Statzner, Alan G. Hildrew, Vincent H. Resh 291

Genetic Transformation Systems in Insects, Peter W. Atkinson, Alexandra

C. Pinkerton, David A. O'Brochta 317

TESTS OF REPRODUCTIVE-SKEW MODELS IN SOCIAL INSECTS,

H. Kern Reeve, Laurent Keller 347

BIOLOGY AND MANAGEMENT OF GRAPE PHYLLOXERA,

Jeffrey Granett, M. Andrew Walker, Laszlo Kocsis, Amir D. Omer 387

MODELS OF DIVISION OF LABOR IN SOCIAL INSECTS, Samuel N.

Beshers, Jennifer H. Fewell 413

POPULATION GENOMICS: Genome-Wide Sampling of Insect

Populations, William C. Black IV, Charles F. Baer, Michael F. Antolin,

Nancy M. DuTeau 441

THE EVOLUTION OF COLOR VISION IN INSECTS, Adriana D.

Briscoe, Lars Chittka 471

METHODS FOR MARKING INSECTS: Current Techniques and Future

Prospects, James R. Hagler, Charles G. Jackson 511

RESISTANCE OF DROSOPHILA TO TOXINS, Thomas G. Wilson 545

Annu. Rev. Entomol. 2001.46:703-727. Downloaded from arjournals.annualreviews.org

by University of Arizona Library on 09/26/05. For personal use only.

CHEMICAL ECOLOGY AND SOCIAL PARASITISM IN ANTS, A.

Lenoir, P. D'Ettorre, C. Errard, A. Hefetz 573

COLONY DISPERSAL AND THE EVOLUTION OF QUEEN

MORPHOLOGY IN SOCIAL HYMENOPTERA, Christian Peeters,

Fuminori Ito 601

JOINING AND AVOIDANCE BEHAVIOR IN NONSOCIAL INSECTS,

Ronald J. Prokopy, Bernard D. Roitberg 631

BIOLOGICAL CONTROL OF LOCUSTS AND GRASSHOPPERS, C.

J. Lomer, R. P. Bateman, D. L. Johnson, J. Langewald, M. Thomas 667

NEURAL LIMITATIONS IN PHYTOPHAGOUS INSECTS:

Implications for Diet Breadth and Evolution of Host Affiliation, E. A.

Bernays 703

FOOD WEBS IN PHYTOTELMATA: ""Bottom-Up"" and ""Top-

Down"" Explanations for Community Structure, R. L. Kitching 729

Annu. Rev. Entomol. 2001.46:703-727. Downloaded from arjournals.annualreviews.org

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Evolution of chemosensory genes in Colorado potato beetle, Leptinotarsa decemlineata

Article

Full-text available

Dec 2023

Associating with plant hosts is thought to have elevated diversification of insect herbivores, which comprise the majority of global species diversity. In particular, there is considerable interest in understanding the genetic changes that allow host-plant shifts to occur in pest insects and to determine what aspects of functional genomic diversity impact host-plant breadth. Insect chemoreceptors play a central role in mediating insect-plant interactions, as they directly influence plant detection and sensory stimuli during feeding. Although chemosensory genes evolve rapidly, it is unclear how they evolve in response to host-shifts and host specialization. We investigate whether selection at chemosensory genes is linked to host-plant expansion from the buffalo burr, Solanum rostratum, to potato, Solanum tuberosum, in the super-pest Colorado potato beetle (CPB), Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). First, to refine our knowledge of CPB chemosensory genes, we develop novel gene expression data for the antennae and maxillary-labial palps. We then examine patterns of selection at these loci within CPB, as well as compare whether rates of selection vary with respect to nine closely related, non-pest Leptinotarsa species that vary in diet breadth. We find that rates of positive selection on olfactory receptors are higher in host-plant generalists, and this signal is particularly strong in CPB. These results provide strong candidates for further research on the genetic basis of variation in insect chemosensory performance and novel targets for pest control of a notorious super-pest.

Adult Feeding Experience Determines the Fecundity and Preference of the Henosepilachna vigintioctopunctata (F.) (Coleoptera: Coccinellidae)

Article

Full-text available

Apr 2024

Both larvae and adults of the Henosepilachna vigintioctopunctata feed on leaves of potatoes, tomatoes, and eggplants. Given the variation in planting times of host plants in the Jianghan Plain, host switching between larvae and adults of H. vigintioctopunctata is inevitable to ensure continuous food availability. We evaluated the effect of consistent versus diverse larval and adult host plant feeding experience on growth performance, fecundity, longevity, and feeding preferences of H. vigintioctopunctata through match-mismatch experiments. Host plant quality significantly influences larval development and adult reproduction. Potatoes are identified as the optimal host plant for H. vigintioctopunctata, whereas eggplants significantly negatively affect the adult fecundity. Adult stage host feeding experience determines the fecundity of H. vigintioctopunctata, irrespective of the larval feeding experience. The fecundity of H. vigintioctopunctata adults on eggplant leaves remains significantly lower than that observed on potato leaves. Similarly, adult H. vigintioctopunctata demonstrate a preference for consuming potato leaves, irrespective of the larval feeding experience. Although host switching between larval and adult stages offers lesser benefits for the performance of herbivorous insects compared to a consistent diet with potato leaves, it maintains H. vigintioctopunctata population continuity amidst shortages of high-quality potato hosts.

Electrophysiological and behavioral responses of Lygus hesperus Knight (Hemiptera: Miridae) to host plant volatiles

Article

Full-text available

Feb 2024
CHEMOECOLOGY

Lygus hesperus Knight is a polyphagous pest of major concern to numerous cropping systems across western North America. Lygus hesperus exhibits well-documented host preferences which may be used to develop behavioral management strategies for this pest. This study sought to identify plant volatiles that mediate L. hesperus host preferences and assess the potential of those compounds to improve monitoring and management of this pest. Gas chromatography with electroantennographic detection was applied to identify antennally active compounds in headspace extracts from four host plants of varying attractiveness. Y-tube olfactometer assays were then conducted to determine L. hesperus responses to each of these 17 antennally active compounds individually. Six compounds attracted female L. hesperus, and subsequent tests revealed that females were attracted to an equal-parts blend of these six attractive compounds versus clean air, and that this blend was as attractive as flowering Medicago sativa. We then examined L. hesperus attraction to attractive compounds individually and an equal-parts blend of five attractive compounds in the field. An equal-parts blend of five attractive compounds was tested in strawberry, whereas the blend and each individual component were tested in alfalfa. In both field settings, neither the individual compounds nor the blend increased L. hesperus capture rates compared to unbaited control traps. Low attraction in the field could result from a masking effect of background volatiles or the failure to include important compounds in tested blends. It remains important to assess whether the compounds tested in this study may facilitate L. hesperus management in other cropping systems.

Bentuk Serangan Spodoptera frugiperda J.E. Smith pada Tanaman Selain Jagung di Kabupaten Kulon Progo

Article

Full-text available

Feb 2024

Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) merupakan hama utama pada tanaman jagung, bersifat invasif dan polifag yang berasal dari Benua Amerika dan telah masuk ke Indonesia pada awal tahun 2019. Sifat polifag yang dimiliki oleh S. frugiperda dapat menyebabkan hama ini menyerang tanaman tingkat tinggi lainnya, seperti padi, kacang-kacangan, kapas, dan tanaman Poacee lainnya. Penelitian ini dilakukan untuk menganalisis jenis serangan dari S. frugiperda yang paling sering ditemukan pada tanaman inang alternatif dan menganalisis jenis tanaman inang alternatif yang paling sering digunakan S. frugiperda di Kabupaten Kulon Progo, D.I. Yogyakarta. Penelitian ini dilakukan di sekitar perkebunan jagung pada 12 kecamatan yang terdapat di Kabupaten Kulon progo. Penentuan lokasi pengambilan sampel ditentukan dengan menggunakan metode purposive. Kriteria tanaman inang yang diambil adalah yang didapatkan gejala serangan dari S. frugiperda dicirikan dengan adanya paket telur, terdapat kotoran atau bekas aktivitas makan larva, atau lubang bekas gigitannya. Berdasarkan penelitian yang telah dilakukan didapatkan hasil berupa adanya serangan dari S. frugiperda pada tanaman tingkat tinggi lain selain jagung pada 12 kecamatan di Kabupaten Kulon Progo. Jenis serangan yang paling banyak ditemukan adalah berupa lubang bekas gigitan larva S. frugiperda pada daun dan jenis tanaman inang yang paling sering digunakan oleh S. frugiperda di Kabupaten Kulon Progo adalah Pennisetum purpureum.

Chemosensory detection of glucosinolates as token stimuli for specialist insects on brassicaceous plants: discovery and impact

Article

Full-text available

Dec 2023
J COMP PHYSIOL A

In this paper, we take a historical perspective by going back to Verschaffelt’s landmark study published in 1910, in which he found that glucosinolates were used as token stimuli by larvae of Pieris butterflies, specialist feeders on plants in the family Brassicaceae. This classic discovery provided key evidence for Fraenkel (Science 129:1466–1470, 1959) to elaborate on the function of secondary plant substances and for Ehrlich and Raven (Evolution 18:586–608, 1964) to put forward the hypothesis of insect–plant coevolution. The discovery by Schoonhoven (Kon Nederl Akad Wetensch Amsterdam Proc Ser C70:556–568, 1967) of taste neurons highly sensitive to glucosinolates in Pieris brassicae was an important milestone in elucidating the chemosensory basis of host-plant specialization. The molecular basis of glucosinolate sensitivity was elucidated recently (Yang et al., PLoS Genet 17, 2021) paving the way to unravel the evolution of gustatory receptors tuned to glucosinolates that are crucial for host-plant selection of Pieris butterflies. We propose a hypothetical model for the evolution of labeled-line neurons tuned to token stimuli.

Spread your wings: insect–plant–landscape interactions mediate the wing shape of a multivoltine polyphagous insect

Article

Full-text available

Dec 2023
OIKOS

Wing morphology may affect the foraging efficiency of polyphagous insects via effects on their flight ability. Variations in wing morphology may be triggered by host plant quality, while landscape composition can also play a role in filtering the ability of vari-ants to colonize new habitats. We investigated how intraspecific variations in wing morphology in a polyphagous insect are mediated by the quality of local resources and the role of the landscape in filtering these variations. We used Bemisia tabaci MEAM-1 (Hemiptera: Aleyrodidae) as a model since the existence of morphotypes that engage in long- and short-distance flights has been proposed previously. We collected B. tabaci adults in the vegetative, flowering, and senescence stages of tomato plants on 15 farms embedded in distinct landscape types. We also performed a greenhouse experiment to evaluate whether resource quality influences B. tabaci wing shape. The wing shape of individuals was measured using geometric morphometry analyses. We found sexual dimorphism in wing shape, with males presenting more straight wings and females with more elongated wings. The dispersal morphotypes appear with more rounded wings at the vegetative (colonizing individuals) and senescence stages (dispersing indi-viduals). When the resource is predictable (flowering stage), the wing shape becomes more adapted for short-distance flights, possibly dictated by an intergenerational effect that facilitates habitat exploitation. The natural vegetation acted as an environmen-tal filter in morphotype selection by impairing individuals’ movement among habitat patches. We showed for the first time that insect–plant–landscape interactions mediate intraspecific variation in the wing morphology of B. tabaci. This polyphagous mul-tivoltine pest insect presents a specialized morphological response to food resource quality, and the amount of natural vegetation may constrain its movement across the landscape. Our results indicate that local resources and landscape features produce interacting bottom–up effects that affect polyphagous insects’ morphological variation within the habitat.

Preliminary observations of the gustatory function of sensilla on antennae of the female Spodoptera littoralis (Lepidoptera: Noctuidae): from single compounds to complex natural stimuli

Article

Full-text available

May 2024

Mervat A. Seada

The gustatory system in insects is composed of detectors screening different panels of ligands, which enable or suppress life behaviors depending on the context. Single sensillum electrophysiology recordings were conducted from the antennal sensilla chaetica of an adult female moth of Spodoptera littoralis to ascertain whether these sensilla have a gustatory function. Five test stimuli (NaCl, sucrose, ethanol, green cotton leaves extract, and conspecific larval frass extract) were used to stimulate each sensillum. Two types of gustatory sensilla chaetica located on the same flagellomere of the distal third of the antenna were characterized, each sensillum enclosed three gustatory receptor neurons (N1, N2, and N3). Overall, responses (spikes/s) were higher in the case of low concentration of sucrose and higher concentration of ethanol than of salt and higher concentration of sucrose. Individual differences were observed in the response patterns of these sensilla to the tested stimuli but functional sensillum types could not be identified. Higher concentrations of sucrose, ethanol extracts of green cotton leaves, or conspecific larval frass significantly stimulated the same neuron of ventral and lateral sensilla chaetica. Response patterns revealed that antennal gustatory sensilla contain gustatory neurons, which are possible receptors for host-plant recognition. Moreover, stimulation of the female's antennae with the phagostimulative sucrose evoked activation of the proboscis extension reflex with dose-dependent responses. Differences in sensilla distribution and their response patterns suggest that gustatory sensilla on the antennae of the female S. littoralis have a key role in adaptation and host plant recognition.

Evolution of Tephritid Flies (Diptera – Tephritidae): Adaptive Evidence Through Mitochondrial Genome Variations

Preprint

Full-text available

Jan 2024

Host‐dependent larval migration and parasitism risk in a polyphagous moth

Article

Feb 2024

Female herbivorous insects are expected to oviposit on the host plant providing the best performance of the offspring. However, in some insects the larvae are mobile and are not totally dependent on the mother's choice. They can change host plant when conditions for development or exposure to natural enemies vary between individual plants within a patch. Here we study larval migration and preference between two host plants, cotton and alfalfa, in the Egyptian leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Previous studies have shown that although larval performance is better on cotton, females prefer to oviposit on alfalfa, and this preference corresponds to a higher survival of the eggs. In this study, S. littoralis larvae showed directed movement between host plants and were found to prefer alfalfa over cotton in field test in Egypt, as well as in laboratory selection of feeding site assays. To determine effects by natural enemies, the parasitism rates and various life‐history traits were measured for one larval parasitoid, Microplitis rufiventris Kokujev (Hymenoptera: Braconidae), on several host plants including cotton and clover (equivalent host plant to alfalfa). Overall, parasitism was higher on cotton and parasitoid performance (cocoon mass, adult longevity, and female egg load) was better on cotton compared to clover. This fact suggests an enemy‐free space on clover and alfalfa, as parasitism rate is higher on cotton, and the parasitoid performance is also better on cotton‐fed larvae.

Enantiospecific Attraction of Lygus Lineolaris Palisot De Beauvois (Hemiptera: Miridae) to a Ubiquitous Floral Volatile in the Field

Preprint

Full-text available

Dec 2023

Herbivorous insects utilize olfactory and visual cues to orient on suitable host plants, and such cues can be employed to facilitate insect monitoring. Lygus lineolaris Palisot de Beauvois is a polyphagous pest throughout North America. Monitoring this pest as it moves between crop and non-crop hosts remains challenging and a lack of effective monitoring tools complicates management of this insect. In this study, we examined the electrophysiological and behavioral responses of L. lineolaris to the volatile emissions of two crop hosts: Medicago sativa and Fragaria ananassa . Gas chromatography with electroantennographic detection was applied to identify antennally active compounds in headspace extracts of flowering host plants, before responses to individual compounds were examined in the field. Five compounds consistently elicited antennal depolarizations in adult L. lineolaris and, of these, (±)-linalool increased female L. lineolaris capture rate in the field. Subsequent experiments examined the influence of visual cues and stereochemistry on capture rate, revealing that lures containing (±)-linalool and ( S )-(+)-linalool significantly increased female L. lineolaris capture rates compared to traps baited with ( R )-(-)-linalool and controls, indicating that L. lineolaris is attracted to ( S )-(+)-linalool. While lures increased capture on red traps, this was not the case for white traps, emphasizing the importance of visual cues in L. lineolaris monitoring. This study demonstrates that L. lineolaris is attracted to ( S )-(+)-linalool in the field, and that attraction depends on trap color. This knowledge is expected to improve L. lineolaris monitoring in agricultural systems.

Effects of ecological interactions on forager diets: competition, predation risk, parasitism and prey behaviour. – In: Diet selection: an onterdisciplinary approach to foraging behaviour

Article

Jan 1993

Andrew Sih

The natural control of insects in pinewoods. I. Factors influencing the intensity of predation by songbirds

Article

Jan 1960

L. Tinbergen

Phylogenetic determinants of insect/plant community diversity

Article

Jan 1993

Addresses diversity of phytophagous insects and their host plants from a phylogenetic perspective. This approach is particularly successful because host use by many phytophagous insects is a relatively conservative trait, and in extreme cases host and insect phylogenies are tightly concordant. The authors focus on evidence bearing on Ehrlich and Raven's "escape and radiation' hypothesis, which postulates that insect and host lineages have evolved successive adaptations to one another (new defenses by plants, and new counteradaptations by insects), and that each group experienced bursts of diversification while it (temporarily) had the upper hand. Among the most striking finds is that one plant defense, secretory canals, is consistently associated with higher plant diversity within clades possessing this trait. Speciation rate is not higher in the tropics; rather, the latitudinal gradient in species diversity may result because insect clades originated in the older tropics, and only later colonised more recent temperature environments. -from Editors

The Evolution of Deterrent Responses in Plant-Feeding Insects

Chapter

Jan 1987

A plant deterrent may be defined as “a chemical which inhibits feeding or ovi-position when present in a place where insects would, in its absence, feed or oviposit” (Dethier et al. 1960). In general, we believe that behavioral deterrence caused by such chemicals in plants plays a major role in host selection (Dethier 1954; Jermy 1966; Bernays and Chapman 1977), and the chemicals effectively protect most plants from most insects. All plants have a complex profile of secondary compounds ranging in number from a few to hundreds and there are an estimated 100,000–400,000 different secondary compounds in terrestrial plant species (Swain 1977). Most that have been investigated are deterrent to one or other of the insect species tested. The more restricted the insect’s host range, the more compounds that are found deterrent and the lower the threshold for rejection of such deterrents (Jermy 1983).

Ontogenic Changes in Feeding Behavior

Chapter

Jan 1995

L. Barton Browne

The feeding behavior of insects changes, often radically, according to their stage of development, with individuals in different developmental stages differing as regards amounts and, often, the kinds of food they eat. It is well known, for example, that the larvae and adults of most holometabolous insects have very different feeding behaviors and diets. Perhaps less widely recognized are the less striking, but nonetheless still substantial, changes which can occur during larval development, both within and between instars, and during adult life in relation to stages of somatic and reproductive development and to the level of an insect’s reproductive activity.

A discussion on ritualization of behaviour in animals and man

Article

Jan 1966

J. Huxley

Interactions between predators and prey

Article

Jan 1991

John A Endler

Host plant chemicals responsible for attraction and oviposition in Acrolepiopsis assectella

Article

Jan 1982

Information Overload and Food Selection

Chapter

Jan 1990

Manfred Milinski

It is said that Julius Caesar was able to dictate two different letters to two secretaries almost simultaneously, switching between letters sentence after sentence. The fact that this anecdote has been passed on to our time suggests that Caesar’s ability is appreciated as an exceptional one. Given that the anecdote is true, modern experimental psychology would tell us that Julius Caesar’s brain must have had a supernormal channel capacity. Normally the nervous system is limited in its ability to process sensory data (= channel capacity) which makes it increasingly difficult to fulfil two different tasks at the same time, as each single task gets harder (Broadbent 1965, Blough 1979).

Antennal responses of Ceutorhynchus assimilis and Psylliodes chrysocephala to volatiles from oilseed rape

Article

Jan 1989

Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation

Abstract

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