Natural Selection and Communication among Bark Beetles

Author(s): John Alcock

Source: The Florida Entomologist, Vol. 65, No. 1 (Mar., 1982), pp. 17-32
Published by: Florida Entomological Society
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 Insect Behavioral Ecology-'81 Alcock 17

NATURAL SELECTION AND COMMUNICATION

AMONG BARK BEETLES
JOHN ALCOCK*

It is populations, not individuals, of bark bettles that have created prob-

lems for the forest manager. Moreover, populations of these insects have gen-
erally proven to be remarkably resilient despite the best efforts of humans
to control them. It is not surprising therefore that entomologists who have
studied bark beetles have come to think of the population as the primary
biological unit and have, perhaps grudgingly, grown to admire the seemingly
adaptive properties of the populations they have studied. This view has led,
however, to a tendency to interpret the behavior of individual beetles as
adaptations that have evolved to promote the reproductive welfare of the
group. By many entomological accounts, bark beetles are paragons of co-
operation who work together to achieve "reproductive efficiency" for the
population as a whole (e.g. Renwick and Vite 1969, Shorey 1973, Wagner
et al. 1981) while at the same time preserving variant behaviors for future
species-threatening contingencies (Atkins 1980). The following paragraph
from a recent paper by Coulson (1979) is representative of this attitude:
"Since high costs in the form of mortality to adults are undoubtedly as-
sociated with the search for relatively rare susceptible hosts, and as elaborate
communicative mechanisms have evolved to enhance this search, it is reason-
able to assume that behavioral mechanisms also exist that are directed to the
efficient utilization of the basic habitat unit. Under-utilization would affect
the chances of assembling a sufficiently large population to colonize new
hosts in the next generation. On the other hand, over-utilization would result
in mortality in the form of intraspecific competition between later life stages
for food and perhaps habitat."
Coulson seems to be saying that bark beetles cooperate in calling each
other to rare food sources where they will space their nest burrows so as to
use the host tree completely and yet regulate the number of progeny they
produce so as to prevent over-population of the tree. This is done supposedly
to maximize the number of recruits for the next generation, and thereby re-
duce the risk of extinction of the species.
This paper will argue that the assumption of a population benefit as the
evolutionary basis for cooperation is totally unjustified because it so com-
pletely violates what is currently known about population genetics and the
evolutionary process. The goal of this paper will be to construct reasonable
explanations for the behavior of bark beetles that are consistent with a
modern understanding of genetics and natural selection. I shall employ the
now almost universally accepted working hypothesis of evolutionary biologists
that behavioral traits must in some way help individuals reproduce as suc-
cessfully as possible in the face of competition from their fellow beetles and
other utilizers of the food in certain trees. I hope to show how this approach
is thoroughly different from the "good of the group" hypothesis (Alexander

*John Alcock is a Professor of Zoology at Arizona State University. His research centers
on the reproductive behavior of solitary bees and wasps but he has also published on a variety
of other insects. His book, Animal Behavior, An Evolutionary Approach (Sinauer, 1979 2nd
Ed.) is popular in its field. Current Address: Department of Zoology, Arizona State Univer-
sity, Tempe, AZ 85287.

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18 Florida Entomologist 65(1) March, 1982
1975, Lloyd 1979) and I intend to reevaluate the pervasiveness of coopera-
tion in these beetles.

THE DECLINE AND FALL OF GROUP SELECTION

It is entirely true that many species have become extinct and this
naturally leads to the deduction that living species must have some prop-
erties that have enabled them to avoid this fate. The logic of this deduction
sustained biologists for many years in the uncritical acceptance of the
proposition that traits have evolved to further the interest (i.e. survival) of
the species as a whole. The culmination of this philosophy was V. C. Wynne-
Edwards's (1962) book that championed the argument that group selection,
the differential survival of populations (based on genetic differences among
them), was a major mechanism for evolutionary change'. His basic theme
was that species that failed to regulate their numbers were more likely to
become extinct than populations that could sustain themselves at some
optimum level (one that was not so high as to run the risk of exhausting
key resources on which the species depended). Wynne-Edwards believed that
if it were to a population's survival advantage for its members to reduce
their reproductive output, then such self-sacrificing traits would be main-
tained by group selection because of their species-preserving function.
But as many authors have shown since 1962, none better than G. C.
Williams (1966), group selectionism a la Wynne-Edwards is plagued by a
fatal flaw. Consider a population composed of individuals that fail to
realize their reproductive potential so as not to exceed the population size
most congenial for the long-term survival of the species. A population of
this sort would be vulnerable to invasion by a mutant individual that prac-
ticed reproductive maximization. The genes of this individual and his de-
scendants should become increasingly common over time by outreproducing
the reproductive self-sacrificers. If this situation persists, natural selection
would inexorably eliminate the genes that are "good for the group" even if
in the long run their presence might prevent extinction of the species. It is
the relative number of surviving offspring produced by different genotypes
that determines the frequency of competing alleles in the next generation,
not the value of an allele to the preservation of a species.
It follows therefore that the working hypothesis for an evolutionary bi-
ologist must be based on individual selection, namely that an animal's traits
should contribute to individual reproductive success and that any benefits to
the group as a whole are purely incidental effects. This holds even in cases
that superficially appear to promote group cooperation and "reproductive
efficiency". An excellent example is the case of synchronous flashing by
populations of male fireflies. Lloyd (1971, 1973a,b, 1977) has shown that
group formation by males and synchrony in flashing can occur because
asynchronous or isolated males are unattractive to females and so will fail
to reproduce. Individuals engage in group behavior in order to compete more
effectively for the opportunity to communicate with potential mates.
Despite examples of this sort and despite 15 years in which Williams's
critique of group selectionist thinking has been widely accepted, there per-
sists the temptation to interpret animal behavior as designed (evolved) to
prevent the extinction of species. This temptation is particularly strong in
cases in which signaling individuals are found in groups. To counteract this

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 Insect Behavioral Ecology-'81 Alcock 19
temptation let us consider the reproductive consequences for individuals that
participate in a communication system (Otte 1974, Lloyd 1977).

WHAT IS COMMUNICATION?

The odors emanating from a bark beetle can be detected by others who
may use the information in various ways. For example, one bark beetle may
be drawn to the odor of another and establish a burrow near the sender.
Through their association the two may gain an advantage in overcoming
the toxic or entrapping defenses of the tree they have selected to colonize.
Such a case of mutual reproductive benefit is very different from the inter-
action that occurs when the same bark bettle odors are perceived by preda-
tory clerid beetles. Here the clue (bark beetle odor) has a negative reproduc-
tive effect on the sender (as it may result in its death) while enhancing the
fitness of the predatory receiver. The reciprocal effect is also possible, with
the producer of a cue gaining at the expense of the respondent. (An example
are those predatory female fireflies that mimic the attraction signal of a
female of another species in order to draw males of the prey species to them).
Otte (1974) claims, and I agree, that in interactions in which either the
signaler or receiver is harmed, exploitation rather than communication oc-
curs. The exploiter can either detect a cue associated with its victim or pro-
vide a mimetic signal that resembles a communication message normally
used beneficially by the receiver. Any definition of communication is of course
a semantic issue but, however labelled, there is a real and significant dis-
tinction between cues (signals) that have a positive effect for both signaler
and receiver as opposed to those with a benefit for just one interactant and
a negative reproductive effect for the other (Table 1). Only when both those
that release and those that respond to a cue gain from the interaction will
individual selection favor the maintenance (and further elaboration) of the
(communication) system. If signalers are consistently damaged by the re-
lease of their signal, selection will favor mutants that happen not to produce
the reproductively disadvantageous "message" for their exploiters' benefit.
Likewise, if the fitness of a receiver is on average reduced by reacting to a

TABLE 1. SOME MAJOR POSSIBLE EFFECTS ON THE REPRODUCTIVE SUCCESS OF

AN INDIVIDUAL THAT PRODUCES A CUE AND AN INDIVIDUAL THAT
RESPONDS TO THAT CUE.

Reproductive Effect Definition of Interaction

Emitter Receiver
+ + Communication: Both interactants gain
+ - Deceitful Exploitation: The signaler induces
the receiver to do something that harms the
receiver but benefits the signaler
+ Eavesdropping Exploitation: The receiver
takes advantage of a cue provided by the
signaler and reduces the signaler's fitness
in the process

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20 Florida Entomologist 65(1) March, 1982
signal, individual selection will favor others in the population that happen
not to be responsive to the damaging cue.
With this argument in mind we shall consider the effects of bark beetle
"communication signals" on the fitness of individuals participating in the
system. Instead of assuming that the function of a signal is to promote the
welfare of the group, we shall approach the matter with skepticism and an
alertness to the possibility of exploitation and competition rather than uni-
form cooperation2.

THE LIFE HISTORY OF Dendroctonus pseudotsugae

In order to make our analysis more manageable, the discussion will focus
primarily on one bark beetle species, D. pseudotsugae, whose behavior has
been unusually well studied thanks to the work of Julius Rudinsky and his
associates (Rudinsky 1969, Rudinsky and Michael 1974, Rudinsky and Ryker
1976, 1977, Rudinsky et al. 1976, Ryker in prep.). All of the major com-
munication signals exhibited by this species have been found in other bark
beetles (see Nijholt 1970, Wood 1973, Vite and Francke 1976) and so its
behavior can be taken as reasonably typical of the group and used to il-
lustrate some points about the evolution of communication in these insects.
It is the females of D. pseudotsugae, not the males, that first colonize a
host tree in the spring in the northwest. Often the tree selected is a recently
dead or dying Douglas fir but the beetles have the capacity to attack living,
healthy trees as well. When the female burrows into the bark of the tree to
reach its nutritious phloem she innoculates the host with a fungus that in-
vades the water transport system of Douglas fir. If sufficient colonists attack
the tree it will die even if it was healthy originally. Large numbers of
colonists do sometimes assault a host in a very short time (up to 15,000
settlers in one day). Mass attack occurs because as females form their gal-
leries in the bark, the tree becomes far more attractive to flying beetles
searching for a host. The incoming beetles detect a complex bouquet of odors
from the exereta and debris in the burrows of the already established fe-
males. These frass chemicals include frontalin, methylcyclohexenol, and
methylcyclohexone (MCH) as well as volatile monoterpenes "released" by
the host tree. These combined substances attract both males and additional
females when MCH is present in low concentration. The new females find
unoccupied places to burrow into the tree; the arriving males search for
females to court. When a male finds a burrow producing MCH in relatively
low concentration he approaches the entrance, stops, and chirps by rubbing
his abdomen against his elytra. This is the first stage in courtship that may
lead to copulation and pair formation (the male may remain with his mate
to guard her and to help remove the products of gallery formation from the
burrow). During courtship both the female and the male release large quan-
tities of MCH. At high concentrations, MCH no longer acts synergistically
with the other attractants of the pheromone mixture but instead inhibits the
arrival of new settlers. In a densely infested region of a tree with many pairs
of mated beetles, the amount of MCH present becomes high with the result
that this region is no longer attractive to incoming females or males.
Thus MCH can be said to act (1) at low concentrations as an aggrega-
tion pheromone that attracts beetles of both sexes, and, at high concentra-
tions, as both (2) an anti-aggregation pheromone that deters additional fe-

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 Insect Behavioral Ecology-'81 Alcock 21

male settlers, and (3) a masking pheromone that blocks the response of
males to the female pheromone. Let us look critically at each of these sup-
posed communication functions to determine if they are compatible with
what is presently known about genetics and selection.

PHEROMONE
THE AGGREGATION
In the insect literature generally (e.g. Cross 1973, Joose and Koelman
1979) and the bark beetle literature in particular, chemicals released by one
individual are said to be an aggregation or attractant pheromone if members
of the same sex are attracted to the compounds. In bark beetles pheromones
of this sort are known from at least 17 species representing 5 genera (Wood
and Bedard 1976). The use of the term "pheromone" implies that the re-
leased chemicals serve an evolved communicatory function which in the case
of bark beetles is generally thought to be the formation of a sufficiently
large attacking force to overwhelm the defenses of the host tree (Birch
1978). Not all supporters of this view have employed a group selectionist
perspective (although statements such as those by Coulson (1979) to the
effect that the beetles are cooperating in order to produce as large a next
generation as possible imply that a group benefit is the primary function of
the trait). Those researchers that have operated within an individual selec-
tionist framework have proposed that through pheromonal communication
both the signaling residents and responding recruits benefit reproductively
through their combined efforts to destroy the defenses of the tree. Rigorous
tests of this proposition have, however, rarely been done (but see Raff a and
Berryman, in prep.) and there is reason for caution in attributing a co-
operative goal for aggregating individuals.
There are many cases of supposed "aggregation signals" in which either
the signaler or the receiver clearly does not benefit from the interaction. For
example, males of many insects are attracted by the sexual signals produced
by other males (Table 2) and in these cases it is highly probable that the
joiner is attempting to take advantage of the signaler. A famous case in-

TABLE 2. EXAMPLES OF INSECTS IN WHICH MALES ARE KNOWN TO BE AT-

TRACTED BY THE SEXUAL SIGNALS PRODUCEDBY OTHER CONSPECIFIC
MALES

Group Species Reference

Cicadas Magicicada spp. Alexander 1975

Katydid Orchelium vulgare Morris 1971
Trypetid fly Dacus tryoni Fletcher 1968
Otitid fly Physiphora demandata Alcock and Pyle 1979
Grasshopper Syrbula fuscovittata Otte 1972
Mole crickets Scapteriscus spp. Ulagaraj and Walker 1973
Forrest 1979
Wasps Eucerceris spp. Alcock 1975
Bee Euglossa imperialis Kimsey 1980
Beetles Anthonomus grandis Hardee et al. 1969
Tenebrio molitor Tschinkel et al. 1967
Pentatomid bug Nezara viridula Harris and Todd 1980

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22 Florida Entomologist 65(1) March, 1982
volves field crickets of the genus Gryllus in which some males are drawn to
the vicinity of chirping conspecifics where they lie silently in wait to steal
females attracted to the caller (Cade 1979, 1980). To label male singing an
aggregation call simply because other males come to the singer would be
misleading at best. The cricket's song has evolved to attract females to the
singer. Both female receiver and male sender may benefit from the communi-
cation signal. But other males may exploit this system for their own ad-
vantage. By not singing a satellite male may avoid predators and parasites
attracted by the call (another class of exploiters) while at the same time
siphoning off receptive females that come to the singer. Thus the satellite
gains (+ effect) but the signaler loses (-); the aggregative effect of the
call on males is therefore an incidental by-product of what is functionally a
sexual signal favored by individual selection because of its utility to the
sender in male-female interactions. The attracted satellites impose a selec-
tive cost on the singing male that decreases the overall benefit of the calling
behavior.
Despite examples of this sort, the possibility that insects may be at-
tracted to cues provided by others for the purposes of exploitation rather
than cooperation has not been fully explored in the case of bark beetles. Let
me assume the role of devil's advocate and suggest how the aggregation of
females of D. pseudotsugae that results from the low level releases of MCH
from resident females within a host could be rather more exploitative than
cooperative. As noted at the outset, females of this and many other bark
beetles usually attack dying trees. When this happens additional colonists do
not help defuse the defenses of the host because the tree is already es-
sentially helpless. The arrival of competitor females only reduces the food
available for the brood of the established "signaler". Raffa and Berryman
(in prep.) have shown that in D. ponderosae there is a strong negative cor-
relation between density of attacks in cut (i.e. defenseless) logs and pupal
production per female. Thus there is no gain for the supposed message sender
but instead a loss3; the receiver benefits by taking advantage of olfactory
cues associated with the colonist to locate a suitable host. This then is not
cooperative communication in any meaningful sense of the word but ex-
ploitation of one individual by another.
Why then do signalers produce an "aggregation pheromone" when in a
"safe" tree? First, the costs of eliminating all volatile by-products of diges-
tion may be so great (given that females must process large quantities of
wood material through the gut and detoxify plant terpenes by creating new
compounds-Renwick and Hughes 1975) that this disadvantage would out-
weigh any benefits gained by removing all cues as to the feeding females'
location. Second, females do gain by attracting conspecific males. Low con-
centrations of MCH may be released for this purpose with female competi-
tors exploiting the cue to locate a relatively safe food resource4.
But what about those (relatively rare?) occasions in which some females
colonize a healthy host with intact resin defenses. Under these circumstances
it has been assumed, but only conclusively demonstrated for D. ponderosae
(Raffa and Berryman, in prep.), that the risk of death from resin entrap-
ment is reduced for the original settler (or her progeny) if she is joined by
other females. If we accept this hypothesis as applicable to D. pseudotsugae
as well, then an early colonizer will benefit if it draws additional females to

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 Insect Behavioral Ecology-'81 Alcock 23
its living host. But will the respondents also gain? It could be that on average
females gain by flying to sources of dilute MCH because on average the host
tree discovered in this way will be dead or weakened. But when the tree is
healthy and in the earliest phase of attack, the risk of death from resin
flows will be relatively high. It is at least possible that under these condi-
tions joining the signaler does not maximize the reproductive chances of a
settler. Perhaps the initial colonists of a healthy tree exploit dispersing
females to make the tree safer for them at the expense of those they attract
to the host. In this context it may be significant that females of the moun-
tain pine beetle, Dendroctonus ponderosae, produce more aggregation
pheromone when burrowing in hosts that have relatively large amounts of
protective resin (Vite and Pitman 1968, Raffa and Berryman, in prep.). In
contrast, when a female finds a safe host she may gain if she can reduce the
rate of colonization to some degree. This assumes that the first successful
colonists can realize greater reproductive gains than latecomers as demon-
strated for D. ponderosae (Raffa and Berryman, in prep.). The sooner a
female produces her young, the larger they will be relative to the progeny
of later arrivals, and the greater their competitive edge in the race to con-
sume the limited supply of host phloem. Thus for a safe host, reduced
amounts of "attractant" may be released. On the other hand, but for a
dangerous one, residents with a tenuous foothold on the tree may gain by
"amplifying" the cues that indicate the host is being utilized so as to lure
additional females to the site.
Joiner females should benefit if they can avoid exploitation and there-
fore are predicted to prefer safe hosts (if these are available and the fe-
males have the energy and time to find them). The fact that colonization
rates are not a simple linear function of the number of resident beetles in a
tree supports this prediction. Over the first few days of colonization of a host
the number of new recruits is relatively low but once the population of
residents reaches a certain level there is an explosive take-off in the number
of beetles attracted to the tree (Gieszler et al. 1980). The number of new
females of D. ponderosae settling on a living host per established female
rises steeply until the attack density reaches about 40 females per square
meter after which the attracted females to established female ratio col-
lapses rapidly (Raffa and Berryman, in prep.). The 40 female figure is the
density that insures the death of a living lodgepole pine; only females within
dead wood succeed in rearing offspring. Thus mass attack, with relatively
many females attracted per established colonist, occurs when the concentra-
tion and perhaps quality5 of the aggregation pheromone indicates to po-
tential joiners that their chances of living and producing viable offspring
are good given the number of already established beetles.

THE SIGNIFICANCE OF MASS ATTACK

Advocates of the "cooperative beetle" hypothesis have focused primarily

on just one phase of the colonization of healthy trees (the mass attack)
while ignoring interactions that take place in the very earliest stages of
colonization, as well as the interactions that occur on trees that are dead or
dying from causes other than the beetles. But even during mass colonization
of a healthy tree the emphasis on cooperation may have been overdone. As
the firefly example illustrates, synchrony of action does not automatically

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24 Florida Entomologist 65 (1) March, 1982
justify a conclusion of cooperation for group benefit. It is true that by join-
ing in a mass attack newcomer females contribute to the speedy demise of a
living tree. But this may not be their primary goal. Raffa and Berryman (in
prep.) have shown that in colonizing a living tree there is a trade-off be-
tween getting in too early (and thereby risking death) and getting in too
late (and thereby attempting to reproduce in a tree whose resources will be
depleted before one's progeny can reach maturity). An early colonist who
survives may do very well because of the competitive advantages of its off-
spring; a late arrival may have a low probability of dying from resin en-
trapment but also a low probability of finding a productive region of the
tree. Mass attack may be the consequence of individuals racing to take ad-
vantage of a relatively safe and relatively productive resource before their
fellows have exploited it.

THE ANTI-AGGREGATION PHEROMONE:

FEMALE SIGNALERS AND FEMALE RECEIVERS

As the number of colonists increases on a healthy tree there will come a

point (probably quite early in the attack) when any gains to the resident
signaler from attracting more females are outweighed by the reduction in
her production of surviving brood caused by increased competition for food.
Thus although attractive signalers might benefit very early in the infesta-
tion, the effect of releasing the "aggregation pheromone" eventually must
become negative for them (Table 3). Established females would seem to have
everything to gain if they could prevent the arrival of additional colonists
at the point when new settlers reduced their reproductive output. Females of
D. pseudotsugae do release large quantities of MCH when contacted by a
male and this substance does tend to inhibit settling by bark beetles. When
many resident females are releasing MCH, incoming females are usually
repelled and will land elsewhere on the host or nove to neighboring trees or
continue dispersing farther still. The discoverer of this effect, Julius Rudin-
sky (1968, 1969), called the released MCH a "masking pheromone" implying
that females altered their attractant pheromone to make it less readily de-
tected by incoming females. This interpretation has been adopted by Mat-
thews and Matthews (1978) in their recent text on insect behavior which
states that by releasing MCH the resident female is "camouflaging the
normally attractive odor she has produced in her frass". But if this were

TABLE 3. POSSIBLE FITNESS EFFECTS FOR A RELEASER OF AN "AGGREGATION

PHEROMONE" AND FOR AN INDIVIDUAL THAT RESPONDS POSITIVELY
TO THE ODOR.

Fitness Effects for Stage of Infestation of a

-Releaser of Odor -Attracted Individual Tree with Intact Defenses

+ + + or - Very Early
+ + Early
0 or + ++ Middle
+ Late
Very Late

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 Insect Behavioral Ecology-'81 Alcock 25
true it raises two questions. First, why doesn't the signaling female simply
cease to release the assembling scent instead of producing a specially altered
signal. By not providing any signal at all a female would not have to manu-
facture and store MCH in quantities prior to its release and she would not
provide a cue which could alert dispersing beetles to the location of a host.
Second, why do female receivers fail to detect MCH or permit themselves to
be repelled from a region of a tree by concentrated MCH? Let us deal with
each question in turn.
There are at least two problems with the no-pheromone option. First, as
noted earlier, it is doubtful that a female could remove all volatile traces of
her activity without incurring high metabolic expenses especially if the
attractant cues are detoxification by-products. Second, because trees are
colonized unevenly, heavily infested regions may be adjacent to sections that
are lightly attacked. The interests of the beetles in the two areas may be in
conflict. In the low density locale individuals might gain by attracting addi-
tional colonists. They would release aggregation pheromones that would
draw other beetles to the tree, some of which might settle in the pheromone-
less area, having no way to discriminate fully occupied from non-occupied
sectors of the host. Therefore it is to the advantage of resident females, even
after mating, to continue to provide an unequivocal signal of their presence,
provided that this deters additional settlers.
But why are additional settlers deterred? Rudinsky (1969) writing in
an era when the difficulties with group selectionist thinking were not widely
appreciated stated, "The survival value of the mask is clear. It tends to
distribute evenly the available males, while both preventing overcrowding
with resultant brood mortality and allowing the mass attack necessary to
overcome host resistance." But if it were not to the reproductive advantage
of signaler to provide the signal and advantageous for the receiver to re-
spond by avoiding the MCH source, then the system would break down, what-
ever its group benefits. Perhaps the large release of MCH serves first to
announce to the chirping male that the female is potentially receptive. Sec-
ondarily it provides a cue that other individuals might use to modify their
own behavior for their own advantage. MCH concentration offers a measure
of population density in the host which arriving females can use to assess
their reproductive chances. By releasing additional MCH after contacting a
male, a resident female (whose sexual peromone has done its job of attract-
ing a mate) may be attempting to make her site appear more crowded than
it actually is and so less attractive to would-be colonists.
The fact that females automatically release quantities of MCH upon
hearing a male at their gallery entrances, apparently without respect to
population density in the host, suggests to me again that the primary func-
tion of MCH is sexual. Otherwise we would expect that population density,
not the arrival of a male, would determine whether or not the female con-
tinued to produce the "aggregation bouquet".
The deterrent effect that MCH has on arriving beetles may occur because
it is generally in the reproductive interests of the dispersing beetles to avoid
settling in trees with few remaining resources. The degree to which a joiner
gains by landing on a host is largely a function of the current population
density there which determines the food available for its progeny. The de-
gree to which signaler and joiner probably gain varies depending on the

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26 Florida Entomologist 65 (1) March, 1982
stage of attack and need not be equal at any time (Table 3). Some indi-
viduals may join relatively crowded trees because they have in some way
determined (unconsciously) that their chances of finding a superior host are
slight-either because hosts are extremely rare, or the risks of dispersal are
great, or their physiological condition makes prompt settling desirable.
Therefore some individuals could gain reproductively by landing on a high
density host, even though their reproductive success will be less than if they
had found an ideal tree and even though their decision to colonize adversely
affects the reproductive success of their neighbors (Table 3). In living
lodgepole pine the density of attacking D. ponderosae regularly exceeds 60
females per m2 which is the point at which pupal production per female be-
gins to decline sharply (Raffa and Berryman, in prep.).
But if the reproductive chances of a female are nil if she were to land on
a fully settled host or if her alternative options are profitable, then it be-
comes to her advantage to use information about colonist density provided
by the MCH signal to avoid certain trees. When the reproductive interests
of the signalers and receivers coincide, MCH does function as an anti-
aggregation pheromone, but it is important to recognize that the interests
of the two classes of interactants will only be the same under rather special
conditions.

THE ANTI-AGGREGATIONPHEROMONE:
MALE RELEASERSAND MALE RECEIVERS

The same argument applies to the release of MCH by males (after they
reach a female's burrow) and to the response of conspecific males to the
MCH stimulus. To the extent that this augments the female's MCH signal,
the male's action can be seen as a contribution to the repulsion of additional
female settlers whose presence would reduce the reproductive success of his
mate and so reduce the number of his progeny. It can be argued that the
male signal is also a "mask" directed at other males that counteracts the
attractant fraction of the female's odor thereby reducing competition from
rival males. This function has been ascribed to the release of a male
pheromone in the case of the armyworm Pseudaletia unipuncta by Hirai
et al. (1978). They perceived a group benefit of the behavior because the male
that released the "inhibitory pheromone" was promoting "the increased re-
productive efficiency (that) results when multiple males are prevented from
competing for a single female."
Both the group selectionist hypothesis of Hirai et al. (1978) and the
hypothesis that individual males gain by hiding receptive females from other
males have a logical flaw. If it were not to the reproductive advantage of a
male receiver to be "inhibited" from approaching the source of male
pheromone, then individual selection would favor those males that re-
sponded differently. Thus male MCH probably is not a masking pheromone
but a clear signal to would-be competitors that the signaling male is near a
receptive female. This repels approaching males because a female with a
male guard is unlikely to be easily secured. In D. pseudotsugae males de-
fend their mates vigorously and it is probable that the first male to enter a
female burrow has a substantial advantage over later arrivals. Even so,
fights do occur (Rudinsky and Michael 1974, Ryker, in prep.) indicating that
males will sometime not avoid concentrated MCH if they can gain by ap-

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 Insect Behavioral Ecology-'81 Alcock 27
proaching the source (that is, if they can determine that their opponent is
relatively weak or small and if the option to continue the search for an un-
secured female is not likely to be productive). Often, however, potential
male joiners gain by moving on when they receive the MCH signal and thus
the release of the compound and the "typical" response to it have positive
fitness effects on both sender and receiver of the message.

CONCLUSIONS

Since individual beetles are the product of natural selection and there-
fore attempt to reproduce as much as possible, our view of bark beetle com-
munication must take on a distinctive character. If nothing else I have tried
to suggest that the interactions between resident beetles and attracted join-
ers could be much more complex (and more interesting) than one would con-
clude from the "cooperative beetle" hypothesis. There is little doubt that
bark beetles do sometimes communicate with pheromones and do sometimes
achieve mutualistic goals as a result (Raffa and Berryman, in prep.). But
the perspective presented here argues that they do so only when certain
conditions enable them to use and respond to signals in ways that further
their individual reproductive interests. Beetles that gratuitously raise the
reproductive success of others while damaging their own reproductive
chances are not likely to be long represented in the gene pool of the species.
I am confident that future research on bark beetle communication will con-
firm that reproductive competition is at the heart of the interactions among
individual beetles and that the animals possess the ability to adjust or vary
their signals and responses in subtle but adaptive ways.
Those interested in controlling populations of bark beetles can take com-
fort in the recognition that they are not opposed by a monolithic cooperative
pest all of whose members are working and sacrificing for the common goal
of population growth. Instead the enemy is composed of reproductively self-
ish individuals that may attempt (unconsciously of course) to exploit their
fellow beetles. Ideally it would be possible to control bark beetles by using
their evolved abilities against them. Thus the tactic of releasing large
amounts of synthetic MCH over trees vulnerable to D. pseudotsugae appears
promising because it exploits the adaptive (reproductively selfish) tendency
of receivers to avoid crowded areas with low reproductive potential (Ryker,
in prep.). At the same time, this and any other system of control based on
manipulation of the animal's communication network must contend with
some problems.
First, not all individuals can be expected to respond identically in releas-
ing pheromones or responding to a given concentration of aggregation or
anti-aggregation pheromone. An intriguing and plausible possibility raised
by Raffa and Berryman (in press) is that the genetic make-up of individuals
in some bark beetle populations may undergo cyclical changes in response to
fluctuations in overall population size. In populations that have reached
epidemic proportions, selection may favor females that have a low threshold
for settling in living trees. The odds are good that some females from the
very large pool of dispersing individuals will also settle in the tree and help
render it defenseless. The progeny of these colonists will profit from the
thick phloem of the once vigorous tree. But during the low population phase
of the "cycle", selection would favor highly discriminating females that were

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28 Florida Entomologist 65 (1) March, 1982
reluctant to settle in all but the "safest" of trees as the probability of
acquiring the additional recruits to defeat a healthy tree are slim at these
times. Thus host discrimination responses may not be static at all but instead
could be a dynamic reflection of fluctuating selection pressures.
In addition, any one beetle may be able to adjust its signal release or
signal reaction depending upon the conditions it encounters or has experi-
enced. Only one-fifth of the females of the southern pine beetle that land
on apparently suitable hosts actually burrow into the tree during the mass
attack phase (Burt et al. 1980). This may be due to genetic differences or
environmental and experiential differences among the females. Likewise as
many as one-half of the western pine beetles that establish galleries in trees
may subsequently emerge again (presumably after reproducing to some ex-
tent) to disperse to other trees. This suggests that the beetles may be able
to alter their tactics even after seeming to commit themselves to one course
of action (Wood and Bedard 1976). I have little doubt that the same kind of
intra-specific variation in behavior occurs with respect to the anti-aggrega-
tion pheromone.
Control programs that are based on the typological thinking that there is
one standard response by all members of a target species to a particular
situation or signal are therefore unlikely to succeed. Variation among indi-
viduals and the behavioral flexibility of specific beetles create a kind of
"resistance" that could thwart even sophisticated biological control measures
just as thoroughly as insecticide-resistant mutations have sabotaged chem-
ical control efforts in some cases. For this reason it is unfortunate that the
attempt to document the degree of behavioral variation within a species and
the range of options open to individuals has barely begun in bark beetle re-
search (but see Raffa and Berryman, in prep.).
As these features of bark beetle communication are discovered it will be
important to explore the adaptive basis for the variation. Do individuals of
different age, size, potential fecundity, and past dispersal experience react
differently to aggregation and anti-aggregation cues in ways that promote
their reproductive success? Do individuals react to living, damaged and dead
hosts in different ways? Does the abundance and pattern of distribution of
potential hosts correlate well with differences in signal and response be-
havior? If the beetles are as adaptively flexible and variable in their be-
havior as I suspect, then they will in many respects be a more formidable
foe than one composed of individuals all of whom follow a single route of
sacrifice for group success. In the long run an awareness of how individual
beetles achieve reproductive success in a variable and socially competitive
environment should contribute to the development of measures that will
have a better chance of truly controlling bark beetle populations.

ACKNOWLEGEMENTS

Participation in this symposium was funded in part by a U.S. Depart-

ment of Agriculture-sponsored program entitled "The Integrated Pest Man-
agement R & D Program for Bark Beetles of Southern Pines", Forest Service
Southern Station Cooperative Agreement 1981-8 with the University of
Florida. Dr. Randy Thornhill sent me a pre-publication copy of his manu-
script (written with L. Kirkendall) that assesses "aggregation signals" in
a similarly skeptical fashion. Dr. Kenneth F. Raffa provided a copy of Raff a

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 Insect Behavioral Ecology-'81 Alcock 29
and Berryman (in prep.), a paper I found extremely valuable. Dr. Lee C.
Ryker and Dr. James Lloyd provided help with the literature search and
constructively reviewed the manuscript as did Dr. Ron L. Rutowski. I espe-
cially thank Dr. Lloyd for inviting me to the symposium and Dr. Ryker for
his generous and knowledgeable assistance with matters pertaining to bark
beetle behavior.

APPENDIX

'In order for group selection to occur within a species, three conditions
must be met. (1) Certain groups within the species must survive and others
must become completely extinct. (2) There must be genetic differences be-
tween the two categories of groups. (3) These genetic differences must con-
tribute to the differences in the probability of survival of a unit. Under these
restrictive conditions it is theoretically possible for the differential survival
of groups to lead to changes in the frequency of competing alleles within a
population. Most workers feel however that these requirements for group
selection are not often met. More importantly still, selection at the individual
level should almost always successfully counteract group selection when
group selection happens to favor genetically self-sacrificing behavior. In
other words, an allele favored by group selection can be eliminated by indi-
vidual selection (see the text), leading to the conclusion that individual
selection is the more potent force for evolutionary change.
2Communication is a special form of cooperation. Cooperative behavior
of all sorts can evolve through individual selection but only if the par-
ticipants generally gain more reproductively than they lose by assisting the
other individuals with whom they are interacting. Special circumstances are
required if a helpful action is to lead to mutual benefit and therefore any
hypothesis that a behavior is truly cooperative deserves special scrutiny.
3In some species of bark beetles additional colonists may help the signaler
even if they cannot reduce the danger from the tree's defenses. The gain
could come from overwhelming the consumption capacity of the local preda-
tors, thereby reducing the risk of attack for any one resident. But little
evidence exists on whether established residents experience great mortality
from their enemies. Another possible benefit for the resident that attracts
additional colonists of its species occurs when there is interspecific competi-
tion for the tree's resources. When two rival species occupy the same host in
equal numbers, larval survival for both may be severely reduced (Birch
1978). This could favor individuals that can attract sufficient numbers of
conspecifics to make the tree unattractive to members of other species (but
only if conspecific juveniles are less damaging than those of other species).
Interspecific interactions based on chemical signals are common among bark
beetles (e.g. Birch 1978; Birch et al. 1980).
4The work of Brand et al. (1976) showing that an aggregation pheromone
component (verbenone) is produced by a fungus in D. frontalis raises the
possibility that bark beetle pheromones are produced by the insect's gut flora
and fauna for the benefit of these fellow travelers (Birch 1978). It is not
unlikely that the survival and reproduction of the fungus is facilitated in
trees that experience mass attack by the beetles. It would be ironic if the
fungal symbionts manufactured verbenone to exploit or manipulate their
bark beetle hosts for their own reproductive purposes.
5Raffa and Berryman (in prep.) suggest that the interaction between a
living host tree and its beetle colonists will affect the mix of volatile chem-
icals emanating from an attacked tree and this in turn could provide cues
that incoming beetles might use to judge the acceptability of the host. In
particular, the ratio of a detoxification product (e.g. trans-verbenol in D.

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30 Florida Entomologist 65 (1) March, 1982
ponderosae) to its resinous precursor (e.g. alpha-pinene) could be corre-
lated with the stage of attack. If the resinous precursor dominated the odor
bouquet about a tree, the tree would probably be healthy, and in the process
of releasing quantities of defensive resins to repel its attackers. Such a tree
would often not be a good bet for a dispersing beetle. But if beetle density
were higher (or if the defenses of the tree were intrinsically weaker), resin
flows would be less, and the established beetles could convert a large pro-
portion of this material into its detoxification by-product. This in turn would
be correlated with a tree that was succumbing to attack. Selection would
favor colonists programmed to find such a combination of odors particularly
attractive because of the improved likelihood of surviving and reproducing
successfully within such a tree.
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