Background
The study
of plant-insect interactions is necessarily
multidisciplinary. Historically, however, the leaps
forward have usually involved specific aspects of the
interaction. In the early the 20th century, several
biologists recognized the importance of plant secondary
metabolites in host choice (e.g. Vershaffelt, Brues,
Fraenkel) and in the 1950s and 1960s the mechanisms of
host-plant choice by insects was a major focus of study
(e.g. Kennedy, Schoonhoven, Dethier, Jermy, Ishikawa).
The 1960s and 1970s saw a flowering of theories invoking
the importance of chemical defenses in the co-evolution
of plants and their associated insects (e.g. Ehrlich,
Raven, Feeny, Rhoades and Cates). Other groups,
meanwhile, were contributing to our understanding of
broader community-level interactions (e.g. Janzen, Root,
Strong, Zwolfer, Gilbert, Southwood, Price). Eventually,
sophisticated studies of chemicals and their roles in
interactions evolved, and the field of chemical ecology
was born (e.g. Eisner, Berenbaum, Brattsten, Rosenthal,
Rothschild).
More
recently, a host of additional approaches have been
added. Nutritional ecology (e.g. Scriber, Slansky,
Simpson) phylogenetics (e.g. Mitter, Moran, Farrell,
Pasteels), biogeography and genetics (e.g. Singer,
Gould, Rausher, Via, Jaenike, Futuyma, Feder, Thompson,
Mitchell-Olds) have all provided unique insights, and
the impacts of other trophic levels in herbivory are now
better appreciated (e.g. Gilbert, Lawton, Strong, Dicke,
Stamp, Denno). Finally, it has become abundantly clear
that plants are quite active participants in their
interactions with herbivores (e.g. Coley, Bryant,
Baldwin, Tumlinson, Tallamy, Karban).
In
addition to these topics and many new researchers in
them, important contributions now come from
morphologists, neurobiologists, palaentologists and
molecular biologists. My presentation will focus on some
new and little-tested ways to think about and study the
interactions of plants and insects. My attempt to
explain the pertinence of these novel interactions will
require that I draw together a number of the disciplines
involved, though I cannot attempt to review the whole
field.
Introduction
My
principal focus concerns the insect rather than the
plant and, in particular, on how insect neurobiology
affects the plant-insect interaction at all levels.
Behavior, including host plant-related behavior is an
expression of neurobiology that is modified by many
physiological factors. Limitations inherent to the
nervous system constrain how much information may be
processed and can influence choices made, attentiveness
to diverse stimuli, and responsiveness to risk (e.g. of
predation). Evolutionary adaptations of the sensory
system and brain for accommodating these constraints may
govern how host affiliations evolve. Changes in the
nervous system as a result of experience may also affect
fitness in different ways. Both genetically and
environmentally based neurological traits may help
explain patterns of herbivore-host associations and diet
breadth.
Making a
choice among plants
Insects
searching for an acceptable host plant must first locate
and identify the appropriate plant species. We know that
the speed of host-finding may be important. There may be
time limits for various reasons, while other ecological
circumstances commonly impose a need for speed, such as
when resources are rare or scattered and predators make
searching risky. The accuracy with which host taxa are
selected, and individual plant quality assessed, are
also important, especially for insects with narrow host
ranges and specific nutritional requirements for larval
development. If the speed, accuracy and quality of
choices are all to be maximized by very small animals in
a very complex sensory world, strong selection for
efficient neural processing might be expected as might
the adoption of high-contrast signals (Bernays & Wcislo,
1994).
The
majority of insect species use a very restricted number
of hosts that typically share characteristic
phytochemicals, some volatile and some nonvolatile. A
subset of these compounds seems to be of great
importance for identification of the host (see Bernays &
Chapman, 1984; Städler, 1992; Schoonhoven et al., 1998),
and in some extreme specialists great sensitivity to one
or a few host-specific chemicals totally dominates in
host selection (e.g. Ferguson et al., 1983; Pereyra &
Bowers, 1988; Roessingh et al., 1997). Plant taxa
heavily endowed with relatively unusual chemicals or
suites of chemicals (non-apparent plant syndrome of
Feeny, 1975) are often hosts for relatively large
numbers of specialist insect species (e.g.Berenbaum,
1983). In addition, specialists tend to be deterred more
than generalists by non-host secondary metabolites. I
will make the case that specialists benefit from the
strong contrasts between cues from hosts and non-hosts.
Additional
mechanisms for acceptance/rejection used by different
insect groups may heighten perceived contrast in various
ways. An insect’s response to a chemical mixture may not
be predictable based on its responses to each chemical
separately. Specifically, interactions among chemical
stimulants at the level of the chemoreceptors can result
in major changes in concentration-response functions of
particular stimulants, with deterrents reducing input
from positive inputs and vice versa (e.g. Shields &
Mitchell, 1995; Schoonhoven et al., 1998)). I will
demonstrate how such interactions could potentially
alter the total input from a mixture of conflicting
inputs to either a clear positive or a clear negative
signal. Such process may be important in producing the
particular and synchronous firing of a suite of taste
cells, that appears to occur in some beetles only when
the requisite mixture of plant chemicals is present
(Sperling & Mitchell, 1991). In addition, highly
synergistic effects of multiple host compounds are seen
in some cases (e.g. Städler & Buser, 1984; Spencer et
al., 1999), Thus a variety of mechanisms can provide the
clear signal needed for rapid decision-making in a
highly complex chemical world. Data so far suggest that
the predominant mechanisms vary among insect taxa. In
any case, the mechanisms could influence the
evolutionary lability of host associations, and the
trajectory for a clade of insect herbivores evolving
with respect to host affiliation.
Some
herbivorous insects alter their preferences as a result
of experience. In some cases this results from increased
or decreased sensitivity of their chemoreceptors to
certain metabolites (Renwick & Lopez, 1999). So far,
such changes have been recorded in species that feed on
plants in at least several genera and lead to increased
acceptability of the experienced food, sometimes with a
concomitantly decreased acceptability of other potential
foods - once again, an increase in contrast between
alternatives. Diet quality also alters relative
acceptability of alternatives depending on nutrient need
- a flexibility dependent on variation in the strength
of inputs from different nutrient chemoreceptors
(Simpson & Raubenheimer, 1993).
A minority
of insect herbivore species are extreme individual
generalists, apparently adapted to situations where food
plant quality or abundance is variable or unpredictable,
or to situations where the food plants may all be very
rich in potentially noxious secondary metabolites. 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 (e.g.
Bernays et al., 1997).
Evidence
for limited efficiency among generalists
Data will
be presented from experiments with butterflies (Janz &
Nylin, 1997), caterpillars (Bernays & Minkenberg, 1997),
whiteflies (Bernays, 1999), aphids (Bernays & Funk,
1999) and grasshoppers (Bernays, 1998), indicating that
having a choice of suitable foods reduces efficiency of
foraging, and that the specialists have significant
advantages. These benefits include the amount of time
taken to reach the host plant, the times taken to make
decisions to accept or reject potential food, the time
taken to begin ingestion 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 and the ability to choose
superior hosts in the presence of a choice of
mixed-quality hosts are shown to be greater in
specialists than relative generalists.
Fitness
benefits of behavioral efficiency in host choice
Data will
be presented indicating that efficient decision-making
has positive fitness effects. This appears to be true
for ovipositing insects not just with respect to
limitation on time overall, but also for evasion of
predation through rapid oviposition. Evidence will also
be presented for costs associated with the poor quality
decisions made by the relatively generalized Lepidoptera
and Hemiptera due to reduced growth rate, reduced
survivorship and reduced fecundity (Janz & Nylin, 199 7;
Bernays & Minkenberg, 1997). Locomotor activity is known
to be risky with respect to predator and parasitoid
attack, and field studies demonstrate that predation may
be 100x more likely during feeding than during resting
(Bernays, 1997), thus illustrating fitness costs of with
reduced feeding rates. In addition I argue that
intermittent, hesitant, or picky feeding behavior and
any kind of dithering is dangerous not only because it
is conspicuous, but because an animal attentive to
food-related activities is unlikely to be attentive to
simultaneous environmental risks (Dukas, 1998).
Since
protein is often at low concentration in leaves
(especially older leaves) and the nitrogen requirements
of insects tend to be relatively high, herbivores often
compensate 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
since less time must be spent feeding and vulnerable to
predators. Indeed, perhaps the fitness advantage
associated with predator avoidance exceeds that enjoyed
due to increased growth rate. Safety and growth are
important together of course at a 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 lineages with similar types of food indicates the
adaptive value of these structures (Bernays & Janzen,
1988; Bernays, 1991). Furthermore, evolution of
mouthparts can be very rapid (Carroll & Boyd, 1992). In
view of the ever-present risk of predation, structures
that determine handling time may be under great
selection pressure. Indeed, the preponderance herbivores
that feed on young easily-handled leaves, is probably a
matter of safety as much as nutrition.
Secondary
chemistry of plants
Among the
hundreds of thousands of phenols, alkaloids, terpenoids,
iridoids, flavonoids, steroids, and other chemical
compounds of plants have been the subject of
considerable study (Rosenthal & Berenbaum, 1991). Many
appear to have no effects at all on insect herbivores,
while others stimulate feeding and/or growth. Some are
sequestered, and of these many are clearly toxic in
general and serve as plant defenses against many
herbivores Such chemicals have often been considered
toxic when close study demonstrated they were actually
deterrent only, the effects on test insects due to
starvation. Some herbivores, however, suffer deleterious
postingestive effects and perform poorly in some way, or
learn to avoid the plant as a result of feeding on it
and move elsewhere, both of which can be bad outcomes.
In many cases, it is not at all clear whether an ability
to deal with toxins has been lost, as suggested in the
case of grass-feeding grasshoppers (Bernays, 1990), or
whether the plants have evolved specific defenses
against particular insect herbivores (Berenbaum, 1983).
It seems likely that both scenarios occur.
Sequestering these secondary metabolites for defense
against predators is also common among herbivores
(Bowers, 1990). Besides clear and well-documented
fitness benefits of sequestration in highly aposematic
species, there are many more subtle cases, in which
insects deposit chemicals in the cuticle yet are not
warningly colored (Bernays et al., 1991), and others
where they gain protection from predators as a result of
the gut contents alone (Sword, 1999). Although such
processes are not specifically relevant to the theme of
neuroecology, they do highlight once more the crucial
importance of natural enemies in the lives of insects on
plants.
In this
presentation, I will also emphasize the very important
roles of plant secondary metabolites in signaling. First
of all the remarkable diversity chemicals found among
plant taxa and within individual plants allows
potentially clear signals for every specialist
herbivores at taxonomic levels from plant species to
plant family (Bernays, 1996). That butterflies such as
checkerspots home in on plants from multiple families,
simply because of the presence of iridoid glycosides in
host plants that are otherwise extraordinarily diverse
physically and chemically (Bowers, 1983), is startling
evidence of the influence of simple chemical signals on
insect behavior. Evidence is beginning to suggest that
such cases are not unusual. In addition, deterrence of
non-host compounds, being greater for specialists,
increases sensory contrast between host and nonhost.
Diversity
and the association of insect and plant clades
It has
become clear from both fossil studies (Labandiera, 1998)
and molecular phylogenies (Farrell & Mitter, 1993) that
among all the herbivorous insect groups studied, great
diversification is historically associated with the
expansion and increased diversity of angiosperms.
Although this could arise through coevolutionary
processes associated with arms races, I argue that it
could be at least partly the result of herbivore
tracking diverse genotypes in a plant population and
subsequent speciation of herbivores on established plant
host races or species.
The
selective pressures 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,
and would thus be acting through the agency of
ecological risk. So, as plants changed and diversified
chemically, insect herbivores, being so dependent on
specific cues, also changed and diversified so that
discrimination of signals from hosts could be maintained
at maximum levels of contrast. In this way, vigilance
for predators could be maintained at maximum levels.
Evidence for tracking chemicals in this way has been
demonstrated in one study of a group of beetles and
their host plants (Becerra, 1997), and a model is
presented to further illustrate this scenario.
Although I
will make the case for tracking of chemotypes, it is not
impossible for diversification of insect herbivores,
driven by such neural processes, to result from
coevolutionary processes. However, rather than invoking
toxins, the currency would be in terms of signal
information.
Plants as
active players
The
widespread occurrence of herbivory-induced chemical
changes in plants (Karban & Baldwin 1997; Agrawal et
al., 1999) will be discussed not only as a direct
defense but also as an indirect one, that plays on the
vulnerability of these small herbivores to multiple
risks from predators and parasitoids. Plants may
encourage mortality of herbivores by causing them to
decrease vigilance. This could involve increased
searching and foraging activity, intermittent feeding,
and restlessness that is induced by unusual or
increasing levels of ingested secondary metabolites.
Conclusions
The
synthesis presented here 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, namely the constraints on
neural processing and the diverse effects of these
constraints in ecology and evolution. I believe that
this approach will allow us to understand more about all
aspects of the insect-plant interaction in a way that
has been difficult in recent decades. The importance of
avoiding anthropomorphism and subjectivity in the study
of animals may have mitigated against the study of them
as individuals with behavioral and neural limitations
that impact every aspect of their lives.
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Copyright:
The copyrights of this original work belong to the
authors (see right-most box in title table). This
abstract appeared in Plenury lecures– Abstract Book
I – XXI-International Congress of Entomology,
Brazil, August 20-26, 2000.