(An International Journal for the Americas)
Volume 65, No. 1 March, 1982
TABLE OF CONTENTS
SYMPOSIUM: INSECT BEHAVIORAL ECOLOGY-'81
LLOYD, J. E.-Creation-"Science" and Functional Illiteracy: Spectre of
a Christmas Past Or Yet to Come? (An Editorial) -..................... 1
STIMAC, J. L.-History and Relevance of Behavioral Ecology in Models
of Insect Population Dynamics ........-......... --.....- ......... .....-- .... 9
ALCOCK, J.-Natural Selection and Communication Among Bark Beetles 17
FORREST, T. G.-Acoustic Communication and Baffling Behaviors of
Crickets ... --.............-....--...............------ -.... ............................... 33
SLANSKEY, F.-Insect Nutrition: An Adaptationist's Perspective ........ 45
RUTOWSKI, R. L.-Mate Choice and Lepidopteran Mating Behavior .......- 72
GREENSTONE, M. H.-Ballooning Frequency and Habitat Predictability
In Two Wolf Spider Species (Lycosidae: Pardosa) .--............... --83
BURK, T.-Evolutionary Significance Of Predation On Sexually Signal-
ing Males .-- -...- .....-...... -..----......................... 90
WALKER, T. J.-Sound Traps for Sampling Mole Cricket Flights
(Orthoptera: Gryllotalpidae: Scapteriscus) .--.--............................ 105
WALKER, T. J., R. C. LITTELL, AND NGO DONG--Which Mole Crickets
Damage Bahiagrass Pastures? --.........----...... ----.. .........---- 110
McCOY, C. W., AND T. L. COUCH-Microbial Control of the Citrus Rust
Mite with the Myoacaricide, Mycar .........----........... .........--- .... 116
KLINE, D. L., AND R. H. ROBERTS-Daily and Seasonal Abundance of
Culicoides spp. Biting Midges (Diptera: Ceratopogonidae) in
Selected Mangrove Areas in Lee County, Florida ..-.....................- 126
CHILDERS, C. C.-Seasonal Attack Patterns on "Hamlin" Orange by the
Cofee Bean Weevil in Florida ..............--............... .................. 136
PENA, J. E., AND V. WADDILL-Pests of Cassava in South Florida ........ 143
WHITCOMB, W. H., T. D. GOWAN, AND W. F. BUREN-Predators of
Diaprepes abbreviatus (Coleoptera: Curculionidae) Larvae ........ 150
KOSZTARAB, M.-Observations on Torvothrips kosztarabi (Thy-
sanoptera: Phlaeothripidae) Inhabiting Coccoid Galls .......-........ 159
SELHIME, A. G., W. G. HART, AND D. P. HARLAN-Dispersal of Amitus
hesperidum and Encarsia opulenta Released for the Biological
Control of Citrus Blackfly in South Florida .......---....-................... 165
Continued on Back Cover
Published by The Florida Entomological Society
THE FLORIDA ENTOMOLOGICAL SOCIETY
OFFICERS FOR 1981-82
President ----------.-...... ---...................................... W. L. Peters
Vice-President ......--..------........ -- .....................-- -.......... Abe White
Secretary ...---....... ....------------- ......... -----............. F. W. Mead
Treasurer .........-----------------.. ............. -.................-... D. P. Wojcik
E. C. Beck
W. Keith Collinsworth
Other Members of Executive Committee .- R. W. Flowers
R. G. Haines
D. C. Herzog
C. A. Musgrave Sutherland
Editor .. -----.. ----........... ............ ........... ... C. A. Musgrave Sutherland
Associate Editors ....-------------.................................... F. W. Howard
J. E. Lloyd
J. R. McLaughlin
C. W. McCoy
A. R. Soponis
H. V. Weems, Jr.
Business Manager .......----------- -----.............. ........... D. P. Wojcik
FLORIDA ENTOMOLOGIST is issued quarterly-March, June, September,
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Authors should consult "Instructions to Authors" on the inside cover of
all recent issues while preparing manuscripts or notes. When submitting a
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Manuscripts and other editorial matter should be sent to the Editor,
C. A. Musgrave Sutherland, 4849 Del Rey Blvd., Las Cruces, NM 88001.
Business matters for other Society officers can be sent to that individual at
the University Station address above.
This issue mailed March 30, 1982
Insect Behavioral Ecology-'81 Lloyd
CREATION-"SCIENCE" AND FUNCTIONAL ILLITERACY:
SPECTRE OF A CHRISTMAS PAST OR YET TO COME?
JAMES E. LLOYD
"I just want the religious alternative to
evolution taught in the schools, and to
be taught as science."
Maryland Legislator Patrick Scanello
"We are part of the first great age of the
world whose cultured inhabitants will never
seem quaint, superstitious, or silly to
"History repeats itself. That's one of the
things wrong with history."
Pragmatic insect behavioral ecology, an attempt to put modern knowledge
of evolutionary theory into service; to get insect biologists to think simul-
taneously (and creatively) about the basic, theoretical, and utilitarian
aspects of entomology; and to promote an understanding of our science by
the public, meets the abominable, creation-"science" snowjob head on.
To competent biologists, biology itself is scarcely more than the study of
evolution. Evolution is, for all practical purposes, fact. Natural selection,
though it may be tautological and philosophically a poor theory in the vari-
ous ways it is usually stated (e.g. "survival of the fittest"), and perhaps not
even capable of being falsified, is nevertheless profound and axiomatic
(C. Harris 1981). It provides the most useful insight for problem solving
that biological science has, and is the heart and soul of behavioral ecology.
But, the word evolution is a "red flag" to fundamentalists: "Scopes II"
occurred in Arkansas "because we had the temerity to insert the word
evolution into the discussion of biology" (Mayer 1981). I can imagine biology
being taught in public schools without mentioning evolution-in a "big lie"
of another sort we honor Columbus there, and he was a villian, driven by
personal ambition for extreme wealth and a hereditary title, and while de-
manding impossible tributes of gold and other negotiables, managed to kill
or export as slaves 80% of the people of Hispaniola within 15 years of the
time he "discovered" them (Wilcox 1977)-but it wouldn't be science, in-
stead merely an arbitrary collection of facts. What is seen as important or
necessary depends upon one's standards, sacred cows, and priorities, and
don't you "know" intuitively that there are many more coaches teaching
biology than there are biologists coaching football across the U.S.?
The Press called the Arkansas trial "Scopes II." Never! Thirty years of
worldly TV, lasers, gene-splicing, heart transplants, defeat of small pox and
"infantile paralysis," and a walk on the moon made Darrow and Bryan as
ancient as Pugnax the Gladiator and Ben Hur. In Dayton, plain, God-fearing
Florida Entomologist 65(1)
folks didn't want to and wouldn't be made to entertain thoughts that their
ancestors were apes; in Little Rock, affluent, lettered men of free will made
monkeys of themselves. Little Rock was a Monkeyrama, not a "Scopes II."
Was it part of the democratic degradation of science that H. L. Mencken
predicted (Bode 1969) ?
What I can't understand is where were the Press, the Scientific Societies
and Institutions, and the wiser and concerned religious leaders, before this
matter got out of hand? Were there no individuals like Mencken and T. H.
Huxley, stiff-jawed, combative hell-raisers to carry their message into the
tents and shake it under people's noses, in a manner of speaking? If
Muhammed Ali had been going to fight D. T. Gish, a CRS leader, he'd have
been heard! In my mind's ear I can hear him:
We're gonna take up his views on creation;
It'll be heard all across the Nation.
I'll fix him, and his sixes,
Put an end to his trickses,
You'll see a Darwinian demonstration!
The confrontation between science and creation-"science" has been a
floating pea-and-shell game. Until Little Rock the issues themselves were
seldom if ever honestly or squarely met. For example, when attention was
focused on their Sacrament of Created Fixity of Species, and it was pointed
out that the man-selected differences between, say, St. Bernard and Pekinese
dogs would merit species-level distinction, except for the genetic continuity
possible along the whim-cline of breeds between them, the creation-"scientist"
evolved his species into kinds and made his kinds open-ended taxa, maybe
genera, maybe families . Who could take their stuff seriously? Look at
discussions of the second law of thermodynamics, to disprove phylogeny. If
true, then we are only imagining ontogeny and embryology! And probabil-
ity? There is only one chance in 4 billion (world population) that it is I
sitting in my office (writing this editorial), and this must be multiplied by
the probability that my office should occupy the spot on the Earth's surface
that it does, to calculate the chances that I would be here-the statistics of
course show that it is impossible for me to write this in my office, and I
haven't even dealt with the actual writing yet! And this is the nature of the
arguments about probability and the origin of life.
Augustine probably considered the Genesis story, authority for creation-
"science" "knowledge," too naive for serious consideration (C. Harris 1981).
Harris quotes comments of a ninth century bishop that are appropriate:
"Things are believed now by christians of such absurdity as no one ever
could aforetime induce the heathen to believe." Only four years ago Ehren-
feld (1978) lightly dismissed contemporary belief in the Bible story as fact,
with the sentence I quoted at the head of this paper, preceded by the follow-
ing: "God created the world and all its creatures in the year 4004 B.C. We
have this on the assurance of the late Bishop James Ussher, who had many
supporters in the seventeenth and eighteenth centuries . Now, educated
people know more, and therefore must know better . Old myths have
wilted in the heat of scientific evidence . Time and knowledge have made
the good bishop merely quaint." Today I suspect Ehrenfeld must feel more
Insect Behavioral Ecology-'81 Lloyd
like the critic of Spiritualism 100 years ago who lamented, "What would I
have said six years ago to anybody who predicted that before the enlightened
nineteenth century was ended hundreds of thousands of people in this
country would believe themselves to be able to communicate daily with the
ghosts of their grandfathers?" (Moore 1977). One can view Spiritualism as
fun, nonsense, entertainment, or harmless superstition, like not stepping on
a crack, and so what? But, creation-"science" strikes me as a mischief, that
is not altogether innocent, and maybe even ominous.
The Creation Research Society is the organization that has raised the
most Cain, and, according to C. Harris (1981), has "more than 600 voting
members, all with graduate degrees in science"! Harris observes that this
Society "is unique among organizations with scientific pretensions in its in-
sistence upon homogeneity of thought among its members. Every applicant
[read supplicant, JEL] for membership must attest to his orthodoxy on the
following doctrines: . 'The Bible is the Word of God, and . all of its
assertions are historically and scientifically true in all of the original auto-
graphs . This means that the account of origins in Genesis is a factual
presentation of simple truths . .All basic types of living things, including
man, were made by direct creative acts of God during Creation Week as
described by Genesis . The great Flood described by Genesis . was an
historical event... .' "
In other words, while CRS members sport the apparent credentials of
science to promote their religion, they carry insurance that any threatening
findings of real science can't penetrate and displace the beliefs they intended
to "prove." Science? "Science."
In one of their standard tactics creation-"scientists" deliberately con-
found the meaning of the word theory, taking as its meaning only the trivial,
vulgar usage of "speculation" or "guess." Now, their bishops have standard
dictionaries and access to evolution texts, and know very well that by evolu-
tionary theory "we mean not mere hypotheses that life has evolved or that
natural selection is a major mechanism, but the body of interconnected
statements (often expressed in mathematical form) that describe the gen-
eral processes by which variations arise and are altered in frequency to
cause changes of the kind documented by paleoentology and systematics"
(Futuyma 1979). Interestingly, in California a year ago the judge said that
science teachers must stress that evolution is "theory" not dogma. I wonder
what he meant by that?
Creation-"scientists" have even equated their position with that of
Galileo, and argued that evolutionists protect their own orthodoxy and dogma
by not letting them publish, in professional, scientific journals, studies that
would disprove evolution. Poppycock! When this came up in Little Rock
testimony Judge W. Overton pressed the witness for an example and none
could be given (This will come up again). This ridiculous argument could
only convince someone outside of science. ,As you well know science is in-
tensely competitive, and publication space, grant support, legitimate sci-
entific ideas and citations are scrambled for and squabbled over. If anyone
could get convincing scientific evidence in support of anybody's creation
notion he would publish (we all have a deep personal interest in any factual
evidence relating to who, why, where, and if we are; that's why the study of
evolution upsets fundamentalists so much); if he could get evidence in sup-
Florida Entomologist 65 (1)
port of the story advocated by creation-"scientists" he would not only
publish, but would quickly submit a grant proposal to the keepers of the
funds that Christian* Fundamentalists mail in to support their radio and TV
preachers, hospitals, and other "good work" that is advertised in their media.
If a creation-"scientist" submitted solid evidence for a Genesis creation story,
certainly he would get the normal bruising we all get when we submit papers
to refereed journals, but I suspect, on the basis of reading history, and
bitter experience, and with my tongue only slightly in my cheek, that the
following would also happen: someone would look up similar and remotely
related papers, add a thought or two, and publish a review, thus "stealing"
his citations; someone would look into the old literature trying to find who
might have said something of the same sort first, because such a finding
carries prestige (see also C. Harris 1981); someone would look into his own
old papers and publish something to demonstrate that he had said it earlier;
someone would try to publish the same thing, in a different way, making it
look like he hadn't seen the original and had an independent discovery; and
someone else would publish something similar but mixed up, because it is
better to appear confused than not to appear at all. If a scientist discovered
evidence of one of the Genesis Creations he could even go on a lecture tour,
taking in a lot of churches and money, be an instant celebrity (and right-
fully so, and impossible to beat as an evangelist), and perhaps even go into
preaching, opening a new niche for unemployed biology and geology gradu-
There are many other false and dead issues that creation-"scientists"
have resurrected that could be discussed (for examples see Alexander 1978),
but a major point and conclusion is, that, because of the nature of indi-
vidual scientists, not only from their own personal concern as lonely, finite
humans, and their near-universal idealism and "noblesse oblige," but also
because of their private, free enterprise for personal scientific gain, there can
be no thought of conspiracy. If evolutionary theory or any of its parts are
to be disproved, it will be these biologists that will do it, and eagerly. I am
sure that the bishops of creation-"science" knew this, and that their less-
than-honest tactics themselves were their acknowledgement aforehand of a
losing cause, but I cannot fathom their goal or purpose. Sooner or later, they
must have known that even if they were at first successful in their ruse to
pass religion off as science (an approach used by Spiritualists a century ago,
Moore 1977), they would eventually arrive at a forum that would require
form and substance; and that deception-though it worked in early skirm-
ishes staged in provincial kangaroo courts or on their private media for
crowds that seems to have changed little since those that cheered the burn-
ing of heretics like Giordano Bruno, or Joseph Priestly's study, or the li-
braries at Alexandria and Constantinople-would not prevail.
As we have seen, Dave Ehrenfeld (1978) seems to have been wrong in
his judgement about contemporary intellectual sophistication in America.
But was he wrong in this statement about the critics of humanism (he is
a critic himself, but read his book) : "Periods of ferment and creativity have
always provided opportunities for evil, which has its own inventive genius.
And then a reaction occurs: 'saintly and ascetic' preachers arise and flourish
*Mention of a particular religion does not constitute an endorsement by IFAS, USDA, or
Insect Behavioral Ecology-'81 Lloyd
for a while, gaining popularity as they criticize not only the vices but also
the creations of others, and as they prophesy doom. Such criticism is gen-
erally short-lived; the public cannot tolerate it for long, for this kind of self-
denying reform soon becomes wearying, then boring, then irritating, and
ultimately threatening. At this point the . preachers are rejected .."
Because of the attention it has gotten, will creationism finally be ex-
amined in detail and dismissed, generally, permanently, and forgotten? Or,
is what we have seen a glimpse of a spiritual climate we can look forward
to? C. Harris (1981) says that "only a dull wit can fail to imagine the
dawn-or dusk-of a new Dark Age as the result of energy shortages,
famine, pollution, and so on." Colvinaux (1980), in his biological theory of
history, suggests that because in America we are gradually filling up our
niche spaces, laws will become more restrictive and oppressive, and limiting
of individual freedom. In fact, he suggests that the Russians, with their vast
real-estate, may ultimately have more individual freedom than we do! And
Melvin Harris (1977), in his examination of the relationship of cultures and
the ecological circumstances that have led to their development and form,
also sees us coming up on a period of transformation, and with thinly veiled
pessimism ends with advice not unlike that given to a mouse that has fallen
into a vat of milk-keep swimming and kick harder and maybe you will
churn up a lump of butter to climb out on. He observes that "Most people
are conformists. History repeats itself in countless acts of individual obedi-
ence to cultural rule and pattern, and individual wills seldom prevail in
matters requiring radical alterations of deeply conditioned beliefs and
The creation-"science" phenomenon is part of a larger cultural happen-
ing. Dayton was as far from Little Rock as it was from New Salem, but
Little Rock showed us that something was the same. Something hasn't
changed at all, and that same something will have a dominating influence on
a number of decisions that are about to be confronted.
I think we are talking about Functional Literacy. Florida public schools
administer literacy tests to their students by direction of the State Govern-
ment, and require them to demonstrate that they can perform essential,
everyday skills that are necessary for today's living-balancing a check book,
filling out an application, reading a map or bus schedule, etc. That Little
Rock occurred, that Legislator Scanello said what he did, that a top Amer-
ican leader said what he did (and a conservative, public intellectual squinted
along his upraised, patrician nose and said, "Ah, but it's true."), that the
national press didn't get the whole creation-"science" matter laughed off the
stage at its genesis, that some charismatic TV dean of news-time philosophy
didn't do a special on it, that the poll that "demonstrated" that some group
of Americans wanted a "democratic" treatment of a non-existent "choice"
wasn't jumped on by critics, that the Arkansas Governnor and Legislature
passed their bill, unread (that is not an evolutionarily stable explanation),
that their State's Attorney didn't tell whoever needed telling that the whole
thing smelled more like Lysenko's Russia than America, that ... Any num-
ber of events and actions tell us that a lot of people, and worst of all leaders,
professional gadflies, and public intellectuals, have failed an adult, func-
tional literacy test. And, the questions they missed were not merely on biol-
ogy, or evolution, or astro-physics, astronomy, geology, archaeology, anthro-
Florida Entomologist 65 (1)
pology, or science philosophy and practice, but also on the Constitution,
human nature, leadership, history, ethics, journalism, and even, and espe-
cially, theology and objective Biblical history.
"... so the gods
godmade man as he looks
looking like the gods
they godmade them
prick and hole
they godmade them
and the gods blessed them
and the gods said to them:
BREED A LOT AND FILL THE EARTH
AND TAKE IT OVER . ."
(Hebrew P Document, Genesis 1.1-2.4a; Doria and Lenowitz 1976) (at least
five individuals or groups, known as J1 J2, E, D, and P, separated by cen-
turies, contributed to Genesis and the four other books of the Pentateuch;
C. Harris 1981)
It is absurd to think that scientists must inform their legislatures that if
they require schools to teach Biblical creation as fact (if they teach evolu-
tionary theory) that it will be equally legitimate, actually necessary by law,
for our schools to teach (at least in a thought experiment that dispenses
with the Constitutional separation of church and state) every other Biblical
myth, story, parable, and miracle as fact, and somehow deal with the in-
ternal contradictions. They should know without being told. And they should
also know, that if such works are to be used as a data base for science, then
the credibility of the sources themselves must come under very close and
But! ....., just perhaps this is exactly what is needed! Perhaps it is
necessary for an educated electorate to be informed of the historical evi-
dence for their beliefs and "universal truths," since these historically have
had a major influence on rationality. If most Americans will cast their votes
(on crisis issues that will be developing) on the basis of theological informa-
tion from various religious instruction, without objective study of the history
of their culture's religious origins-study that takes into consideration con-
temporaneous ecology, demography, philosophy, politics, mythology, con-
temporaneous views of key personalities, and legal systems, and that has
been obtained and analyzed using the rules of evidence developed and estab-
lished by modern historians-then it is time for an enlightenment, a gnostic
An analysis of the religo-scientific data base would include close exami-
nation of parables, myths, and prophesies, the intents of their authors, and
their homologues and analogues in other cultures; as well as mutual con-
tradictions within prime sources, alternative translations and interpretations
of the same original material; and the analysis of the psychology, motives
and personalities of key actors, and the degree to which early writers ad-
justed and embellished their accounts, and, of course, their purposes for
Insect Behavioral Ecology-'81 Lloyd
doing this. Grant (1977) and Smith (1978) have some interesting informa-
tion and insights along these lines.
Such an examination of the new, double-speak, science data base must
especially focus on information that forms the substance, and essence of
modern Christianity, which seems, on the basis of the discovery of a number
of gospel-type documents in Egypt, to exclude equally legitimate, con-
temporaneous experience and interpretation that only became heritical post
facto, after the power politics of the second century A.D. From a historian
who analyzed the "Gnostic Gospels," "It is the winners who write history-
their way. No wonder, then, that the viewpoint of the successful majority
has dominated all traditional accounts of the origin of Christianity. Ec-
clesiastical christians first defined the terms (naming themselves 'orthodox'
and their opponents 'heretics') ; then they proceeded to demonstrate-at least
to their own satisfaction-that their triumph was historically inevitable, or,
in religious terms, 'guided by the Holy Spirit.' But the discoveries at Nag
Hammadi reopen fundamental questions. They suggest that Christianity
might have developed in very different directions-or that Christianity as we
know it might not have survived . ." (Pagels 1979).
At the end of World War II Japan underwent a major religious change,
and set aside an ancient tradition (at the insistence of the Allies). Such
things may be necessary for the cultural evolution and survival of a modern
nation-a punctuation in the evolution of self knowledge.
Each participant has reprints of his own paper. Paper-bound reprints of
the entire Symposium-81 are available from some participants and in quan-
tity from E. O. Painter Printing Co., DeLeon Springs, Fla. 32028 (25 at
$82.00). (Reprints of previous Symposium-'79 are also available.)
At the annual fall meeting of the Society in 1982, there will be another
symposium on insect behavioral ecology.
I thank the participants of the Symposium, and the Executive and Pro-
gram Committees of the F.E.S., especially W. Peters, N. C. Leppla, and D. P.
Wojcik for their enthusiastic cooperation, guidance, and support; and my
Symposium referees; and Tim Forrest, John Sivinski, Tom Walker and Steve
Wing for reading this manuscript. Florida Agriculture Experiment Station
Journal Series No. 3596.
ALEXANDER, R. D. 1978. Evolution, creation, and biology teaching. American
Biol. Tchr. 40: 91-104, 107.
BODE, C. 1969. Mencken. Southern Illinois Univ., Carbondale.
COLINVAUX, P. 1980. The fates of nations: a biological theory of history.
Simon and Schuster, N.Y.
DORIA, C., AND H. LENOWITZ (eds. and translators). 1976. Origins: creation
texts from the ancient Mediterranean. Anchor/Doubleday, N.Y.
EHRENFELD, D. 1978. The arrogance of humanism. Oxford Press, N.Y.
FUTUYMA, D. J. 1979. Evolutionary biology. Sinauer, Sunderland, Mass.
GRANT, M. 1977. Jesus: an historian's review of the gospels. C. Scribner's
and Sons, N.Y.
HARRIS, C. L. 1981. Evolution: genesis and revelations. S.U.N.Y., Albany.
Florida Entomologist 65 (1)
HARRIS, M. 1977. Cannibals and kings: the origins of cultures. Random
MAYER, W. V. 1981. quoted in A.P. news item, "Court fight started by a
word-evolution" (Miami Herald, 12 Dec.).
MOORE, R. L. 1977. In search of white crows. Oxford, N.Y.
PAGELS, E. 1979. The Gnostic Gospels. Random House, N.Y.
SCANELLO, P. 1981. Quoted by R. Lewin, in Weak creationist bill filed in
Maryland, Science 214: 773.
SMITH, M. 1978. Jesus the magician. Harper and Row, N.Y.
WILCOX, D. 1977. Ten who dared. Little, Brown and Co., Boston.
Left to right: F. Slanskey, J. L. Stimac, P. Wales, N. C. Leppla, M. H.
Greenstone, J. Alcock, T. E. Burk, R. L. Rutowski, and J. E. Lloyd. Photo-
graph by F. W. Mead, FDACS-DPI. 13 August 1981, Daytona Beach, FL.
e e -- e o e e e
ERRATUM Sivinski, J. 1980. Sexual Selection and Insect Sperm 63:99-111
pg. 103: . (Alexander 1974) should read (see Alexander 1974; for dis-
cussion of parental manipulation).
Insect Behavioral Ecology-'81 Stimac
HISTORY AND RELEVANCE OF BEHAVIORAL ECOLOGY
IN MODELS OF INSECT POPULATION DYNAMICS
JERRY L. STIMAC*
The object of studying population dynamics is to acquire a precise de-
scription of population behavior. Early models of population systems ignored
or oversimplified relevant biological data, and because there was an incom-
plete representation of the biological (life history) processes that collectively
drive the behavior of insect populations, the models were inadequate. Al-
though there have been many advances in models of insect populations since
the 1930's (Nicholson 1933, Nicholson and Bailey 1935), and these models
have gradually become more biologically realistic, insect population system
models have been slow to incorporate good quantitative descriptions of be-
havioral attributes of individuals. For example, single, fixed values are often
used to describe rates of insect development, feeding, mating, oviposition, and
mortality. Therefore, the realism in population models is often less than that
desired or possible, and less than that necessary for accurate accounting of
changes in population sizes.
What models of insect populations need is a greater incorporation of
models of insect behavior (Krebs and Davies 1978). This will improve our
models of insect predation, parasitism, and population dynamics. Currently,
insect population models omit such important phenomena as the switching of
prey sources (Holling 1966, Hassell 1978), interspecific interference or
avoidance (Hassell 1971), and immigration decisions. By noting how their
models are being used, behavioral ecologists can gain insight into how to
make behavioral models more realistic with respect to their representation
of resource constraints and mortality. Perhaps behavioral models could be
incorporated into process-oriented models of population systems as submodels
of insect behaviors which influence rates of population processes.
In this paper I will briefly review the history of insect population dy-
namics models, showing their gradual incorporation of behavioral/ecological
elements. Also, I will give some examples of why such incorporation is neces-
sary if insect population models are to be used in a predictive manner to aid
pest management decisions. Thirdly, I will suggest some ways by which be-
havioral ecology can become a more explicit part of insect population model-
Population models describe how the numbers of individuals in a popula-
tion change over time in a defined space. A predictive model describes how
population numbers will change given an initial state of the population and
set of environmental conditions. Over the past 50 years population models
have evolved to become very complex mathematical representations, and
*Jerry L. Stimac is an Assistant Professor in the Department of Entomology and Nema-
tology, University of Florida. He teaches a graduate course in Quantitative Approaches to
Insect Ecology in which several laboratory periods are devoted to construction and analysis of
insect population models. Simulation of insect population dynamics on computers is used
widely in his course as well as his research. He received his Ph.D. from Oregon State Uni-
versity in 1977 with an integrated major in Entomology and Statistics. Since joining the
faculty at University of Florida, he has concentrated his research on applications of com-
puter technology to agriculture and models of crop/pest systems.
Current address: Department of Entomology and Nematology, Building 175, University of
Florida, Gainesville FL 32611. Florida Agricultural Experiment Station Journal Series No.
Florida Entomologist 65(1)
computer simulation often is necessary to approximate solutions to the
equations. The need for greater incorporation of biological detail into popu-
lation models grew out of the desired applications for population models.
Recent emphasis on pest management has demanded more reliable predic-
tions of population status and behavior. Consequently, an evolution is oc-
curring from general population models describing trends, to specific popu-
lation models designed to accurately predict how the population will affect a
resource. Five principle stages in the evolution of population models are: (1)
general single species models, (2) two-species models without age structure,
(3) matrix models with age structure, (4) process-oriented population sys-
tem models, and (5) multiple species community system models.
The exponential and logistic growth models (Malthus 1798, Verhulst
1838, Pearl and Reed 1920; see discussion in Wilson and Bossert 1971) were
the first population models in which explicit mathematical representations
were used to predict population changes, and states at future times. These
models used a single differential equation to describe such changes:
rN, Exponential Growth
and dN r (K-N)N,
dt- K Logistic Growth
where r is the intrinsic rate of increase, N is the number of individuals
in the population and K is the carrying capacity of the environment.
These general models had great conceptual value in forcing scientists (and
others) to become more aware of the importance of resource constraints on
the behavior of individuals and the dynamics of populations. However, both
models were biologically oversimplified in that they assumed that all indi-
viduals in the population are the same age, and breed continuously. Variable
rates of reproduction, survival and resource utilization were ignored in both
In the late 1920's and early 1930's two-species population models began
to receive attention. The predator-prey model (Lotka 1925 and Volterra
1926) and the host-parasite model (Nicholson and Bailey 1935) used two
differential equations to describe changes in two interacting populations.
Like their predecessor single-species models, two-species models assumed
that all individuals in the population behaved alike. Numbers of encounters
of prey (hosts) and predators (parasites) were assumed to be directly pro-
portional only to prey density. Searching efficiency of the predator was as-
sumed not to be influenced by other predators or other environmental condi-
tions. Except in a very limited set of initial conditions, such models are in-
herently unstable and quite unrealistic for use in pest management applica-
tions because efficiencies of predators and parasites of pest species usually
are influenced by both abiotic and biotic conditions. Rates of predation and
parasitism can vary widely depending upon behavior of individuals in re-
sponse to local weather conditions and the presence or absence of intra- and
interspecific competition among natural enemies. For generalist predators
and parasites, rates of mortality inflicted on pest species can be influenced
heavily by the densities of alternate prey (non-pest species) or competitor
predators and parasites.
Insect Behavioral Ecology-'81 Stimac
Hassell and Varley (1969) modified the Nicholson-Bailey model by in-
corporating a coefficient to represent mutual interference among parasites.
As parasite density increases searching efficiency of parasites decreases:
Ht+1 = FHte-QPt(1-m)
Pt+ = Pt[1-e-Qtt(i-m)]
where H and P are the numbers of hosts and parasites, F is the net rate
of host increase, Q is the quest (searching area) constant and m is the
mutual interference constant.
The significance of this two-species model was that it recognized that search-
ing behavior of parasites must be incorporated into the model in order to
achieve population stability. That is to say, behavior of individuals is an
essential feature regulating the dynamics of a population. Although this
result may be viewed as an admission of the real world, it was still only a
small one. In the Hassell-Varley model the representation of searching area
was given by a single parameter value which was not adjusted in accordance
with the real behavioral attributes of the parasite or host. Incorporation of
the "mutual interference" parameter added a great deal of realism to the
Nicholson-Bailey model, but a mechanism for dynamically changing the
level of mutual interference as a function of observed behavioral attributes
of individuals was lacking.
The Leslie (1945) and Lefkovich (1965) matrix models divided the popu-
lation into age classes, with age (or stage) specific survival and reproductive
rates. Population performance was assumed to be a summation of per-
formances of each age class, and average survival and reproductive rates
were used for each age class. Behaviors of individuals within a class were
assumed not to affect rates of survival and reproduction, although biological
knowledge tells us that often behavioral attributes of individuals can
dramatically affect both survival and reproductive success.
of Environmental Simple Empirical Models
Variables (Temperature, Correspondences between
Humidity, Rainfall, ambient measurements and or
Solar Radiation, etc.) microclimatic conditions
Descriptions of Biological Processes 4
Rates of Biological Processes ] Population Performances
Fig. 1. Relationships between abiotic factors, physiological and behavioral
responses of individuals, and population performances.
Florida Entomologist 65(1)
INSECT POPULATION MODEL
MATED OVIPOSITION HATCHING MOULTING
ADULT 9 EGGS r > 1ST INSTAR 2ND INSTAR
MOTHS E LARVAE LARVAE
^ "MORTALITY MORTALITY MORTALITY F
MORTALITY MATING MORTALITY u MOULTING
ADULT d ADULT < 3RD INSTAR
MOTHS MOTHS LARVAE
MORTALITY MORTALITY MORTALITY
PUA_ 6TH INSTAR 5TH INSTAR 4TH INSTAR
LARVAE LARVAE LARVAE
FEEDING FEEDING FEEDING
PUPATION MOULTING MOULTING
Fig. 2. Conceptual population model of a lepidopterous insect species with
identified biological processes involved in transitions between stages. (Modi-
fled from Stimac and Barfield 1979.)
In an attempt to overcome the assumptions of static rates of survival and
reproduction within an age class of a population, process-oriented popula-
tion system models have evolved. In process-oriented models, modeling focuses
on the biological processes that occur during the life cycle and which ac-
count for changes in the age structure of a population. Rates of processes
can be represented by average values or by complex submodels incorporating
knowledge of thermodynamics and behavioral ecology (Sharpe and De
Michele 1977, Stimac 1977, Logan et al. 1979). Fig. 1 describes how rates of
biological processes are governed by both physiological and behavioral re-
sponses of individual organisms. The rates of these processes are necessary
for making predictions of population performances. Fig. 2 shows some ex-
amples of population processes that are modeled for an insect population.
Rates of mating, oviposition, feeding, development and mortality can be
influenced by behavior of individuals.1 Consequently, each process may re-
quire a detailed submodel with many equations in which knowledge of be-
havioral ecology is incorporated. This process-oriented modeling approach
offers a logical common ground for traditional behavioral and population
ecologists to unite efforts. Behavioral attributes can be altered by population
densities and population density changes can be modeled using feedback from
changes in behaviors of individuals. For polymorphic populations, the num-
ber of state-variable2 chains (boxes with stages in Fig. 2) can be increased
with linkages among morphotypes.
Population models such as shown in Fig. 2 can be linked together
through a resource base to form multiple species community system models
(Fig. 3). For example, a model of the soybean crop/pest community has
been conceptually represented as a five level crop/pest/natural enemy spe-
cies hierarchy (Stimac and Barfield 1979). Each module in the hierarchy
can be a process-oriented population model, describing changes in popula-
Insect Behavioral Ecology-'81 Stimac
SOYBEAN CROPIPEST COMPLEX
Fig. 3. A conceptual model of a soybean crop/pest/natural enemy com-
munity. (Modified from Stimac and Barfield 1979.)
tion numbers as a function of physiological and behavioral responses of
individuals to variations in abiotic and biotic factors. Although such a model
may involve derivation of thousands of equations, the modeling approach
offers the opportunity to incorporate all relevant knowledge of behavioral
and population ecology into a single system model. A great advantage to the
community system model is that it can be used to examine how behavioral
changes in individuals of one population (or subpopulation) affect popula-
tion or community performance.
In the process-oriented system models, submodels of each biological
process can vary in complexity. With greater complexity in submodel
structure, more biological knowledge is required. Since acquisition of biolog-
ical knowledge is costly, one strives to incorporate only the necessary amount
of knowledge required to obtain adequate behavior of the model. How does
one judge what biological detail is necessary? With process-oriented system
models, structural sensitivity analysis helps make such judgments. Given a
mathematical representation of a population (Fig. 2) or community system
(Fig. 3), the sensitivity of each population to changes in behavior of in-
dividuals governing a process can be examined. The general procedure for
performing structural sensitivity analysis of the population model is to
select a life history process, change the structure of the mathematical sub-
model representing that process, then examine the impact of the change on
population age structure and dynamics.
Processes for which a small change, in the structure describing the
process (or behavior of individuals governing the process) yield a large
change in population dynamics are extremely sensitive to behavioral changes.
The more sensitive a process is to changes in behavior of individuals, the
greater the need for incorporation of behavioral ecology into the model de-
scribing the process. Myers (1976) examined the influence of egg batch size
and clumping of egg batches on population performance and stability of an
insect population with an exhaustable food resource. Both egg batch size
Florida Entomologist 65(1)
and clumping of egg batches are determined by the oviposition behavior of
individual females. Therefore, using a population model in which the struc-
ture of the oviposition submodel was changed in accordance with changes in
egg laying behavior of female moths, the author was able to examine the
"importance" of oviposition behavior. The results showed that population
size and stability were highest when egg batch size was as large as could be
supported by the average food plant or slightly larger if larval dispersal
occurred. Clumping of egg batches on food plants increased population
stability when egg batches were small. Similarly, Stimac (1977) used a
process-oriented population system model to perform a sensitivity analysis of
oviposition for the cinnabar moth, Tyria jacobaeae (L.). Egg loading on
host plants was varied between 20 and 200 and population performance was
evaluated in terms of percent biomass change of the host plant after one
year. Egg loading varying between 40 and 200 eggs per plant showed only a
10-16% change in biomass of the host plant but at 20 eggs per plant more
than a 300% increase in host plant biomass was observed. Whether the
dynamics of cinnabar moth and its host plant fluctuated violently (unstable)
or showed low amplitude fluctuations (stable) depended upon oviposition
behavior of female moths. Because cinnabar moth dynamics were found to
be so sensitive to egg laying patterns, one can conclude that a population
model used to evaluate the biological control potential of the cinnabar moth
against its weedy host plant, Senecio jacobaea L., should include an oviposi-
tion submodel with a detailed description of egg laying behavior of females.
From the analyses of Myers (1976) and Stimac (1977) it is obvious that
average seasonal values representing complex behavioral/ecological processes
can lead to serious inadequacy of predictive population models. Other popu-
lation processes subject to dramatic changes from behavioral responses of
individuals are: (1) dispersal and migration; (2) mating success and mate
selection; (3) predation, parasitism, and host selection; and (4) feeding site
or host plant selection. Behavior of individuals governing these processes
can be heavily influenced by environmental conditions and can change
drastically over a short interval of time. Therefore, a predictive population
model used for pest management applications can require incorporation of
knowledge of behavioral ecology for one or all of these processes.
Finally, the essence of behavioral ecology is the understanding and use
of natural selection theory. Recognizing that environmental pressures re-
sult in the natural selection that drives population change and evolution
(e.g. pesticide resistance), a critical question is, can population models be
made to predict what will happen evolutionarily when we put pressure on an
insect population? An affirmative answer to this question depends upon the
ability of population and behavioral ecologists to unite their efforts for pur-
poses of constructing population system models which contain realistic de-
scriptions of behavioral attributes of individuals.
There has been a historical trend in population models toward incorpora-
tion of greater biological detail in descriptions of life history processes re-
sponsible for population changes. This evolution has been driven by the
knowledge that population performance is a function of both physiological
and behavioral responses of individuals to environmental conditions. Ignor-
Insect Behavioral Ecology-'81 Stimac
ing or oversimplifying critical biological components can lead to poor de-
scriptions of population changes, and models of little utility. For example,
the categorical use of mean values to represent population processes that are
subject to behavioral changes can lead to serious malfunctions in models, and
problems of interpretation. It is important that we make even greater use
of the knowledge and models of behavioral ecologists in dynamic models of
populations, especially if the population models are used in making pest
'For specific examples of how behavioral differences in feeding and migra-
tion can influence insect population performances, see the paper by Frank
Slansky, Jr. in this volume.
2A state variable is a variable representing the value or state of an entity
at a particular time. For example, the number of eggs, larvae, or pupae
present at a site at time t= 0, t=l, t=3, . ., t=n.
1 extend sincere thanks to Dr. J. E. Lloyd for stimulating my interest
in behavioral ecology, making me aware of the inappropriate representation
of this field in most models of insect populations, and for introducing me to
the work of Krebs and Davies. Thanks are also extended to C. S. Barfield
and F. Slansky, Jr. for critically reviewing this paper and offering con-
structive ideas and suggestions during the development of the manuscript.
HASSELL, M. P. 1971. Mutual interference between searching insect para-
sites. J. Anim. Ecol. 40: 473-483.
HASSELL, M. P. 1978. The dynamics of arthropd predator-prey systems.
Princeton Univ. Press, Princeton, N.J.
HASSELL, M. P., AND G. C. VARLEY. 1969. New inductive population model
for insect parasites and its bearing on biological control. Nature 223:
HOLLING, C. S. 1966. The functional response of invertebrate predators to
prey density. Mem. Ent. Soc. Canada 48: 1-86.
KREBS, J. R., AND N. B. DAVIES. 1978. Behavioral ecology: an evolutionary
approach. Sinauer Assoc., Inc., Sunderland, Mass. pp. 215-243.
LEFKOVICH, L. P. 1965. The study of population growth in organisms
grouped by stages. Biometrics 21: 1-18.
LESLIE, P. H. 1945. The use of matrices in certain population mathematics.
Biometrika 33: 183-212.
LOGAN, J. A., R. E. STINNER, R. L. RABB, AND J. S. BACHELER. 1979. A de-
scriptive model for predicting spring emergence of Heliothis zea popu-
lations in North Carolina. Environ. Ent. 8(1) : 141-146.
LOTKA, A. J. 1925. Elements of physical biology. Williams and Wilkins,
Baltimore, Md. (Reissued as, Elements of mathematical biology,
MALTHUS, T. R. 1798. An essay on the principle of population as it effects
the future improvements of society. London. (Reprinted by Macmillan
and Co., New York.)
MYERS, J. H. 1976. Distribution and dispersal in populations cabable of
resource depletion: a simulation model. Oecologia 23(4) : 255-269.
Florida Entomologist 65 (1)
NICHOLSON, A. J. 1933. The balance of animal populations. J. Anim. Ecol.
NICHOLSON, A. J., AND V. A. BAILEY. 1935. The balance of animal popula-
tions. Part I. Proc. Zool. Soc. London. pp. 551-598.
PEARL, R., AND L. J. REED. 1920. On the rate of growth of the population of
the United States since 1790 and its mathematical representation.
Proc. Nat. Acad. Sci. U.S.A. 6: 275-288.
SHARPE, P. J. H., AND D. W. DE MICHELE. 1977. Reaction kinetics of
poikilotherm development. J. Theor. Biol. 64: 649-670.
STIMAC, J. L. 1977. A model study of a plant-herbivore system. Ph.D. Diss.
Oregon State Univ., Dept. Ent., Corvallis. 240 p.
STIMAC, J. L., AND C. S. BARFIELD. 1979. Systems approach to pest manage-
ment in soybeans. Pages 249-259 in T. F. Corbin, ed. Proceedings of
World Soybean Research Conference II. Westview Press, Boulder,
VERHULST, P. F. 1838. Notice sur le loi que la population suit dans son
accroissement. Corresp. Math. Phys. 10: 113-121.
VOLTERRA, V. 1926. Variazioni e fluttuazioni del humero d'individui in specie
animal conviventi. Mem. Acad. Lincei 2: 31-113. (Variations and
fluctuations of the number of individuals in animal species living to-
gether. Transl. in Chapman, R.N. 1931. Animal ecology. McGraw-
Hill, New York. pp. 409-448.
WILSON, E. O., AND W. H. BOSSERT. 1971. A primer of population biology.
Sinauer Assoc., Inc., Sunderland, Mass. pp. 92-104.
Insect Behavioral Ecology-'81 Alcock
NATURAL SELECTION AND COMMUNICATION
AMONG BARK BEETLES
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.
Florida Entomologist 65 (1)
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
Insect Behavioral Ecology-'81 Alcock
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
+ + 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
Florida Entomologist 65(1)
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-
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, Vit6 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 excreta 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-
Insect Behavioral Ecology-'81 Alcock
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.
THE AGGREGATION PHEROMONE
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 Raffa 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-
EXAMPLES OF INSECTS IN WHICH MALES ARE KNOWN TO BE AT-
TRACTED BY THE SEXUAL SIGNALS PRODUCED BY OTHER CONSPECIFIC
./,yi,. I, l spp.
Pi. Y "'' 'i "'" demandata
Alcock and Pyle 1979
Ulagaraj and Walker 1973
Hardee et al. 1969
Tschinkel et al. 1967
Harris and Todd 1980
Florida Entomologist 65(1)
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
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
Insect Behavioral Ecology-'81 Alcock
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 attractantt" 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
Florida Entomologist 65 (1)
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 move 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 RELEASE 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
Insect Behavioral Ecology-'81 Alcock
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
Florida Entomologist 65 (1)
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
THE ANTI-AGGREGATION PHEROMONE:
MALE RELEASERS AND 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-
Insect Behavioral Ecology-'81 Alcock
preaching 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.
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 reproductivelyy 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
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
Florida Entomologist 65(1)
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-
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.
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 Raffa
Insect Behavioral Ecology-'81 Alcock
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
'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.
31n 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.
Florida Entomologist 65(1)
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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Insect Behavioral Ecology-'81 Forrest
ACOUSTIC COMMUNICATION AND
BAFFLING BEHAVIORS OF CRICKETS
T. G. FORREST*
In most crickets acoustic communication plays a major role in pair
formation. Generally the male produces a species-typical calling song and
conspecific females use these signals to locate "suitable" mates. The calling
songs of crickets have been used in a variety of studies including investiga-
tions of circadian rhythms (Loher 1972, Sokolove 1975), as aids in sys-
tematics (Alexander 1962), and more recently, in studies pertaining to re-
productive competition and sexual selection (Blum and Blum 1979, Gwynne
and Morris 1982). But very little work has been conducted on cricket sound
production and propagation.
Almost everyone is familiar with the calling songs of male crickets, but
few have actually approached and watched a songster perform under natural
conditions. The peculiar behaviors and often unusual postures males assume
while calling are surprising. Observations on these have prompted this paper,
although its foundation in the physical aspects of bioacoustics comes from a
paper by Michelsen and Nocke (1974). I will discuss the adaptive significance
of the calling postures of male crickets as related to the physical problems
associated with sound production.
THE VIBRATING MEMBRANE, AND A PROBLEM
In crickets sound is produced by the vibration of membranous areas of
the forewings (tegmina). These membranes are caused to vibrate during
stridulation when the scraper (plectrum) of the left tegmen is drawn across
the file (pars strides) of the right tegmen. These stridulatory structures
are closely associated with membranous areas of the wings that vibrate at
the tooth-impact frequency of the scraper on the file teeth (see Nocke 1971
and Sismondo 1979). Sound production occurs only on the closing stroke of
the wings and each wingstroke delivers a pulse of sound.
This vibrating membrane system can be imagined as a piston or disc
(Fig. la and b). When the disc vibrates (moves back and forth in space)
it produces sound waves, that is, compressions and rarefactions. As these
radiate away from the source the sound pressure (intensity) decreases due
to geometric spreading-the same acoustical energy occupies a larger vol-
ume. Ideally, for each doubling of distance from the source the sound
pressure decreases by 6 decibels.1
During vibration as the disc moves in one direction a compression is
produced on one side, and simultaneously a vacuum or rarefaction is created
on the opposite side of the disc. A single vibrating disc thus acts as a dipole
source with two sound outputs produced,,one on each side of the disc. The
outputs are equal in amplitude and have the same wavelength, but are op-
posite in phase (Fig. la and b).
*Tim Forrest is a graduate student at the Department of Entomology and Nematology,
University of Florida. His research interests include acoustic communication and sexual selec-
tion in the Orthoptera.
Current address: Department of Entomology and Nematology, University of Florida,
Gainesville, FL 32611. Florida Agricultural Experiment Station Journal Series No. 3563.
34 Florida Entomologist 65(1) March, 1982
--- ,- ,-q- - -- ,
B .'. C
Fig. la. Sound produced by vibration of disc or piston. As the disc moves
to one side (to right) it produces a compression of air molecules while
simultaneously producing a vacuum rarefactionn) on the opposite side of the
disc. Shading of circles represents the degree of molecular displacement in
sound waves (i.e. black circles represent compression and no circles represent
rarefaction). The rate of disc vibration determines the frequency of sound
lb. Phase relationship of output from vibrating disc. Outputs on opposite
sides of the disc are out of phase (180'). As sound waves radiate from
source the intensity decreases due to the same acoustic energy occupying a
1c. Sound field from a dipole source. If the vibrating disc is small, relative
to the wavelength of sound produced as in (ib), the two outputs will inter-
fere along the edges of the disc. Since they are opposite in phase, they cancel
each other. The result is a dumbell-shaped sound field.
When the size of the disc is small relative to the wavelength of sound
produced, as in crickets, the output from one side of the disc (membrane)
interferes with the output from the other side along the edges of the disc.
Since the two outputs are opposite in phase, they exactly cancel each other
(destructive interference). As a result, intensity measurements around the
disc are maximum perpendicular to the disc surface, but along the disc
edges no sound is perceived. The output is highly directional, with a
dumbbell-shaped sound field (Fig. 1c). The energetic cost of calling may
exceed 10 times that of resting (Prestwich and Walker 1981). Much of this
is wasted simply because the size of the disc is small compared to the wave-
length of the sound produced (diameter is less than 1/2 wavelength (X),
Olson 1957). Because crickets are small they have small wing membranes
that are inefficient sound producers.
There are two possible means of reducing the loss of acoustical energy
caused by the destructive interference of the outputs from the two sides of
the disc. One means is to produce higher frequency sounds with wavelengths
the disc. One means is to produce higher frequency sounds with wavelengths
Insect Behavioral Ecology-'81 Forrest
that are short compared to disc diameter. But high frequencies attenuate
more rapidly than low frequencies, and for a given input of energy are less
effective in long-range acoustic communication (Wiley and Richards 1978,
Michelsen 1978). To be efficient, crickets would have to produce sounds with
ultrasonic frequencies (Michelsen and Nocke 1974); but, to have an ap-
preciable range, these signals would have to be produced at higher intensities
and would require greater energy input. There is a conflict. The frequency
for efficient sound production (acoustic output/energy expenditure) is not
the best one for signal effectiveness (i.e. maximum range of the signal).
Compromises between efficiency and effectiveness seem evident in the
mole crickets. In species that call in specialized acoustic burrows (increased
efficiency) calling song frequencies are low (increased effectiveness) com-
pared to males of species that call without such burrows (Forrest 1982a).
A second possible mechanism that could increase the efficiency of sound
production is a baffle system. Simply stated, a baffle is an acoustical shield
or partition. A baffle used in conjunction with a dipole source partitions the
two acoustic outputs and prevents interference along the edges of the disc
or membrane. One such baffle system places the vibrating disc in a "speaker
cabinet" and the walls of the cabinet keep the outputs from the two sides
of the disc from interfering with each other (Fig. 2a). If the cabinet is
closed such that the distance from the disc to the cabinet's back wall is one
quarter of a wavelength of the sound produced, the cabinet ("a closed box")
will act as a resonating chamber. Sound produced on the box side of the disc
bounces off the cabinet's back wall and returns to the disc (total distance
1/2 X) in phase with the output of the other side of the disc (Fig. 2c). The
acoustic energy of the one output is used as mechanical energy to help drive
In another baffle system the sound radiator is placed in a channel (Fig.
2d). This directs the outputs away from each other, eliminating acoustic
interference. The channel walls prevent geometric spreading of the sound
waves and, if the waves are perfectly reflected in the channel, no attenuation
occurs (Michelsen 1978).
A third system puts the vibrating disc or membrane in a planar surface
or wall. The wall extends in all directions from the edges of the disc and
separates the two outputs of the dipole source (Fig. 2f).
In general, baffles act to increase the length of the acoustic path between
the front and back of the disc. In order to be efficient the distance of the
path must be at least one-quarter wavelength of the sound produced. At this
distance a "finite baffle" will behave as an "infinite baffle" (Olson 1957; see
also, Michelsen and Nocke 1974). However, the sound fields produced by an
acoustic radiator in a finite baffle deviate from theoretical fields predicted
assuming an infinite baffle. These deviations are minimized if the baffle is
irregularly shaped (Nichols 1946). These factors become important when
considering baffle systems used by crickets (below).
BAFFLES AND GROUND DWELLING GRYLLIDS
In crickets the vibrating membrane is located in the dorsal fields of the
forewings. Males of ground dwelling species call with the tegmina raised at
about a 450 angle to the body axis. A speaker cabinet is formed by the dorsal
and lateral fields of the elevated forewings, and the lateral fields form the
Florida Entomologist 65(1)
a @ 0
n @ c
0c a a
* 0 0
*g a a
Fig. 2. Baffle Systems.
a. "Speaker cabinet" type baffle system prevents interference along edges
of disc or membrane (arrow). The walls of the cabinet direct the output
from one side of the disc back and away from the other output. Shading of
circles shows amplitude of displacement of molecules where dark circles rep-
b. Calling posture of a ground dwelling gryllid, Anurogryllus arboreus,
shows "speaker cabinet" baffle system. Vibrating membranes are located in
dorsal fields of raised forewings. Cabinet "walls" are formed by lateral fields
and large hind femurs.
c. "Closed box" baffle system. The box acts as a resonating chamber.
Sound waves produced on the box side of the membrane bounce off the back
wall of the box and return to the membrane (total distance 1/2X) in phase
Insect Behavioral Ecology-'81 Forrest
walls of the cabinet (Fig. 2b). Nocke (1971 cf. fig. 8) has shown that there
is a reduction of acoustic interference at the sides of the membranes of
calling Gryllus campestris, but that interference occurs at the posterior ends
of the raised tegmina where no baffle exists. In another ground dwelling
species, Anurogryllus arboreus, Paul and Walker (1979) showed that some
interference exists both above and to the sides of calling males even though
lateral fields are also present in this species.
I have observed the postures of calling males of several species of crickets
and have noticed that the (broad) femurs of the hind legs are positioned
just below the lateral fields of the forewings (Fig. 2b). The femurs may ex-
tend the walls of the cabinet and increase the distance between the front
and back of the raised forewings. Sound fields of calling males with hind legs
and/or lateral fields removed may reveal the functions of these structures in
the baffle system. Comparative studies of species that have different fre-
quency signals but similarly sized membranes, lateral fields, and hind
femurs may also be revealing.
BAFFLES OF BURROWING CRICKETS
Numerous species of crickets are subterranean and live in extensive bur-
row systems. In many of these, males often call at the entrance of their bur-
row (e.g. Anurogryllus spp. Walker 1980, Walker and Whitesell 1981;
Gryllus spp. Alexander 1961). A male that positions himself at the burrow
entrance so that his raised tegmina fill the entrance, could be using the soil
surrounding the burrow as a baffle and the burrow system as a "speaker
cabinet" or "closed box" (see Fig. 2a and c). Gryllus rubens males sometimes
call from such a position. While calling, male Anurogryllus muticus con-
struct and situate themselves in depressions in the soil. Raised forewings are
held parallel to and 1/4 X away from the bottom of the depression. This sys-
tem acts as a closed box (in preparation). Males of Valerifictorus micado,
the Japanese burrowing cricket, are known to construct and call within a
hood at the entrance to their burrow (Alexander 1961). This structure must
have some effect on sound production, and perhaps that is its raison d'etre.
The most specialized burrowing crickets are mole crickets. In these spe-
cies the entire life of the animal may be spent underground, and males call
from within their burrows (Bennet-Clark 1970, Nickerson et al. 1979, Forrest
1982a). This calling habit is probably like placing a sound radiator in a
with output produced on the other side of the membrane. The acoustic energy
is used to help drive the membrane. Shading of circles are the same as in (a).
d. Sound waves in a channel. The walls of the channel direct sound out-
puts away from each other and prevent destructive interference of the two
sources. If the walls are perfectly reflective to sound waves no attenuation
occurs in the channel or tunnel.
e. Calling mole cricket in subsurface tunnel. Illustration shows similarity
to baffle system in (d).
f. Vibrating disc in planar baffle. The wall partitions two outputs and
prevents interference. Baffle systems need only be 1/4X of sound produced to
produce maximum efficiency.
g. Oecanthus burmeisteri looking up through and calling in a hole it has
made in sunflower leaf. The leaf acts like the partition, or wall, shown in
(f). (Redrawn from Prozesky-Schulze et al. 1975. Nature 255: 142-143).
Florida Entomologist 65(1)
channel: With the tegmina raised within the tunnel the surrounding soil
acts as an infinite baffle, and the tunnel as a channel or sound guide (Fig.
2e). Sound should travel great distances and remain at high intensity in the
burrow system because there is minimal attenuation and spreading loss in a
Males of four mole crickets (Gryllotalpa gryllotalpa, G. vineae, Scap-
teriscus acletus, and S. vicinus) construct specialized acoustic burrows that
open at the soil surface through an exponentially expanding horn (like the
bell on a musical instrument, such as a tuba). Bennet-Clark (1970) showed
that the horn increases the efficiency of sound production in Gryllotalpa
gryllotalpa and Gryllotalpa vineae. The bulb, an enlarged portion of the
tunnel approximately 1/4 X in length, is located anterior to the calling male
and is used to tune the horn. In G. vineae the horn also directs the output.
This directed output is believed to increase the probability that flying fe-
males will be "captured" by a male's sound field. No work has been con-
ducted on the efficiency of sound production in other species. It is known
that flying females of S. acletus and S. vicinus preferentially land at louder
calling males (Forrest 1982b) and this would escalate selection for in-
creased efficiency and power output.
BAFFLES AND VEGETATION INHABITING CRICKETS
Unlike ground dwelling and burrowing species, the males of most vege-
tation inhabiting species (Neoxabea, Oecanthus, Anaxipha, and Cyrtoxipha
spp.) hold their forewings at right angles to the body axis while calling. The
loss of acoustical energy to the sides of the crickets is so marked that Wil-
liams (1945), a violinist, on casual walks in the California countryside
noticed the directional output of a tree cricket, Oecanthus argentinus. I have
noticed that calling males of three Oecanthus spp. in Florida often perch
precariously on the edges of leaves and that males actually twist their bodies
to one side so that the lateral edge of the raised tegmen is adjacent to the
leaf edge (Fig. 3). This may increase the efficiency of sound production be-
cause the leaf acts as a partial baffle (i.e. a "wall" partially surrounding the
vibrating membranes). I have also observed many individuals of Orocharis
luteolira and two Anaxipha spp. calling in this way. Perhaps this is com-
mon in leaf inhabiting species.
Oecanthus males can also be found calling with their raised tegmina in
the notch of a leaf (Fig. 4). The leaf surrounds most of the vibrating wing
membranes and may increase the baffle effect of the leaf. I even observed a
male Oecanthus niveus calling with his raised tegmina between two leaves;
he had pulled one leaf closer to the other with a mesothoracic leg so that the
two leaf edges were adjacent to the lateral edges of both wings (Fig. 5) I
have also seen Oecanthus males calling with raised tegmina in leaf holes.
Here the leaf surface completely surrounded the raised wings. These holes
were made not by the cricket but by the feeding of other insects. These dif-
ferent calling postures may represent the evolutionary sequence to the leaf
baffle used by male Oecanthus burmeisteri (Prozesky-Schulze et al. 1975).
These males gnaw a pear-shaped hole in a leaf and situate themselves in it
so that the vibrating wing surfaces occupy the hole and are surrounded by
the leaf (Fig. 2g). The leaf baffle increases the amplitude of a male's calling
Insect Behavioral Ecology-'81 Forrest 39
Fig. 3-4. (3) Oecanthus male calling on leaf edge. The body axis of the
cricket is twisted so that the edge of one raised forewing is adjacent to the
leaf edge. The leaf acts as a partial baffle surrounding a portion of the
vibrating wing membranes. (4) Oecanthus male calling in leaf notch. Leaf
surfaces surround a large portion of wing membranes, increasing the effec-
tiveness of the baffle.
Florida Entomologist 65(1)
Fig. 5. Oecanthus niveus male calling between two leaves. The male is
using a mesothoracic leg to pull one leaf nearer to wing membranes. Note
the positions of the hind legs showing extreme twist of cricket's body.
song 2.5-3.5 times that of the same male calling without the baffle (Prozesky-
Schulze et al. 1975).
The leaves used as baffles are irregularly shaped with diameters greater
than 1/2 wavelength of the sound produced. This makes them effective in
increasing efficiency as well as reducing any deviations in sound fields (Olson
1957, Nichols 1946). That Oecanthus burmeisteri males have comparatively
low frequency calling songs (2000 Hz, Prozesky-Schulze et al. 1975) suggests
that increased efficiency may result in the evolution of a more effective long
range signal. A similar compromise between efficiency and effectiveness was
found in a comparative study of mole cricket calling songs (Forrest 1982a).
Walker (1969) observed another tree cricket, Oecanthus jamaicensis,
calling with its head and pronotum protruding through a small (5 mm)
hole in a leaf. While calling, the forewings were raised parallel and ad-
jacent to the leaf surface. Similar systems occur as morphological struc-
tures of male crickets and katydids. In the scaly crickets (Mogopolistinae)
and shield-back katydids (Decticinae) a pronotal shield covers the male
tegmina. Thiele and Bailey (1980) have shown that in a coneheaded katydid,
Mygalopsis marki, males with a similar pronotal shield have a sound field
characteristic of a mono-pole sound radiator. Apparently the shield com-
pletely dampens the output from the dorsal side of the membrane and the
result is a less directional, cardioid-shaped sound field, as compared to the
Insect Behavioral Ecology-'81 Forrest
dumbbell-shaped field of a dipole source. How this system affects the ef-
ficiency of sound production is unknown. Comparisons of sound fields and
energy expenditures of calling males before and after the removal of the
pronotum would answer this question.
The "closed box" system may occur in a number of Tettigoniidae (e.g.
Neoconocephalus spp.) that use very high frequency signals. The lateral
fields of the forewings are wide enough to act as efficient baffles and, because
of the high frequencies (short wavelengths) used, the distance between the
wing membranes and thoracic tergites (the back wall of the box) approxi-
mates 1/4 wavelength. This may add to the power output and decrease
energy needed to drive the oscillator. Bailey (1976) noticed that males of
Ruspolia spp. (Copiphorinae) adjust their position along stems or dried
leaves that have a "reflective property not fully understood" and increases
the output intensity. These katydids produce a mono-tonal calling song that
would be needed for such systems to be effective.
SIGNALING AND DIRECTIONALITY
The directional output of a cricket is a consequence of a dipole sound
radiator and the loss of acoustical energy due to destructive interference
along the edges of the radiator. Baffles used to increase efficiency will at the
same time reduce the directionality of the output. Directional signals, how-
ever, may be put to use if males "know" from which direction females will
approach. Males could direct signals toward incoming mates and at the same
time reduce some of the risk of attracting predators and parasitoids (Burk,
this symposium). If females are likely to approach from any direction, males
with directional signals can be expected to change positions periodically to
advertise in areas to their sides not covered by their sound fields. The calling
burrow of Gryllotalpa vineae is constructed so that it directs a male's output
upward toward flying females, and in such a way as to increase the likeli-
hood that a female will intercept the signal (Bennet-Clark 1970). Anurogryl-
lus arboreus is a flightless, burrowing cricket and females approach males
by walking. Males often climb tree trunks, and they call at a modal height
of 1 m. The broadcast area covered by a male's sound field is more than 10
times that of a male calling on the ground (Paul and Walker 1979). The
diameter of the tree trunk, as well as height from which males call, may
influence the broadcast area and directionality of a male's sound field.
Walker (1982) has shown that females actually prefer mates that call at
the modal height over males calling higher on the same trunk. Males of a
number of Gryllus spp. sometimes call on elevated perches, but factors that
influence these behaviors are unknown (Paul and Walker 1979).
Bailey and Thiele (1982) suggest that males might use directional signals
for spacing. In the katydid Mygalopsis marki, the spacing of males is de-
termined by the perceived intensity of neighboring males' calling songs. To
increase the distance of a competitor, a calling male might direct the most
intense part of his output toward the rival (Bailey and Thiele 1982). Gryllus
campestris males have a directional sound field and neighboring, calling
males are oriented at right angles to each other (Popov et al. 1975). Such
spacing would enable males to signal in areas near neighbors and keep the
individuality of a male's calling song intact (see Lloyd 1981).
Florida Entomologist 65 (1)
The energetic cost of calling by male crickets may exceed 10 times that
of resting (Prestwich and Walker 1981). Much of this energy input may be
wasted because of the small size of their vibrating membranes and the
physical properties of the sound generated by this dipole source. Since these
mating signals are fundamental to a male's reproductive success, selection
will act on males to reduce costs and increase transmission efficiency and
effectiveness. It appears that crickets have solved the physical problems of
acoustical efficiency through behavioral and structural adaptations, and
crickets in similar ecological situations seem to use similar baffle systems.
Many more adaptations probably exist that increase pair forming ef-
ficiency because selective forces have acted in the past and will continue to
act on this acoustic signaling system. But such forces are not restricted to
crickets or acoustic signals. One needs only watch and ask why such be-
haviors are adaptive.
Male crickets sing and females respond. Because of the small size of their
sound radiator (wing membranes) male crickets are faced with a problem.
To be efficient sound producers males must transmit high frequency signals.
But such signals are less effective.over long distances than are those of
Many species of crickets have various adaptations that increase ef-
ficiency and effectiveness. These adaptations are analogous to baffle systems
used by acoustic engineers. Cricket species with similar habits use similar
baffle systems. In ground dwelling crickets body parts function as "speaker
cabinets." Burrowing crickets use their subsurface homes as sound guides
and acoustic amplifiers, and vegetation inhibiting species use leaves as baffles.
I would like to thank Jim Lloyd, John Sivinski, and Tom Walker for
reading the manuscript and suggesting many improvements. Sue Wineriter
invested a considerable amount of time in the illustrations. I also thank Dr.
L. Prozesky and Nature for permission to use Figure 2g. This study was
funded in part by an NSF grant BNS 81-03554 to T. J. Walker.
1A decibel (dB) is a logarithmic unit that expresses the ratio of any two
(sound) powers or pressures. Power and pressure levels are usually ex-
pressed with respect to a reference level (e.g. power reference [Wr] = 10-12
Watts; pressure reference [P,] = .0002 d,ynes/cm2). Power level in dB can
be defined by the equation PWL = 10 log W/Wr where W is the power and
W, the power reference. Sound pressure level is defined by SPL = 20 log
P/P, where P is the pressure and P, the pressure reference.
Note that for a given number of decibels the sound pressure ratio (P/Pr)
is equal to the square root of the corresponding power ratio (W/W,).
Insect Behavioral Ecology-'81 Forrest
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in field crickets (Orthoptera: Gryllidae). Behaviour 17: 130-221.
ALEXANDER, R. D. 1962. The role of behavioral study in cricket classification.
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BAILEY, W. J. 1976. Species isolation and song types of the genus Ruspolia
Schulthess (Orthoptera: Tettigonioidea) in Uganda. J. Nat. Hist. 10:
BAILEY, W. J., AND D. R. THIELE. 1982. Male spacing behavior in the Tet-
tigoniidae: an experimental approach. Pages 000-000 in D. T. Gwynne
and G. K. Morris, eds. Orthopteran mating systems: sexual competi-
tion in a diverse group of insects. Westview Press, Boulder, Colo.
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tion in mole crickets. J. Exp. Biol. 52: 619-652.
BLUM, M. S., AND N. A. BLUM, eds. 1979. Sexual selection and reproductive
competition in insects. Academic Press, New York.
BURK, T. 1982. Evolutionary significance of predation on sexually signaling
males. Florida Ent. 65: 90-104.
FORREST, T. G. 1982a. Phonotaxis and calling in the Puerto Rican mole
cricket. (in preparation)
FORREST, T. G. 1982b. Calling songs and mate choice in mole crickets. Pages
000-000 in D. T. Gwynne and G. K. Morris, eds. Orthopteran mating
systems: sexual competition in a diverse group of insects. Westview
Press, Boulder, Colo.
GWYNNE, D. T., AND G. K. MORRIS, eds. 1982. Orthopteran mating systems:
sexual competition in a diverse group of insects. Westview Press,
LLOYD, J. E. 1981. Sexual selection: individuality, identification, and recog-
nition in a bumblebee and other insects. Florida Ent. 64: 89-118.
LOHER, W. 1972. Circadian control of stridulation in the cricket Teleogryllus
commodus Walker. J. Comp. Physiol. 79: 173-190.
MICHELSEN, A. 1978. Sound reception in different environments. Pages 345-
373 in M. A. Ali, ed. Sensory ecology. Plenum Pub. Corp.
MICHELSEN, A., AND H. NOCKE. 1974. Biophysical aspects of sound com-
munication in insects. Adv. Insect Physiol. 10: 247-296.
NICHOLS, R. H. 1946. Effects of finite baffles on response of source with
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NICKERSON, J. C., D. E. SYNDER, AND C. C. OLIVER. 1979. Acoustical burrows
constructed by mole crickets. Ann. Ent. Soc. America 72: 438-440.
NOCKE, H. 1971. Biophysik der Schallerzeugung durch die Vorderfluglel der
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OLSON, H. F. 1957. Acoustical engineering. D. van Nostrand, Princeton, N.J.
PAUL, R. C., AND T. J. WALKER. 1979. Arboreal singing in a burrowing
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PROZESKY-SCHULZE, L., O. P. M. PROZESKY, F. ANDERSON, AND G. J. J. VAN
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Florida Entomologist 65 (1)
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l r *
d .w IdiY
Insect Behavioral Ecology-'81 Slansky Jr.
AN ADAPTATIONIST'S PERSPECTIVE
FRANK SLANSKY JR.*
"I'm hungry," he thought and straightway began to eat the leaf he
was born on. And he ate another leaf.., and another ... and another.
And got bigger . and bigger . and bigger . Until one day he
stopped eating and thought, "There must be more to life than just
eating and getting bigger. It's getting dull." (Stripe the caterpillar,
in Paulus 1972).
"Insect nutrition? Aagh, that's boring stuff! Let's talk about something
else." This comment has been attributed to a well-known entomologist who
has done considerable pioneering research in insect nutrition. One person's
opinion, yes, but I suspect it is commonly held. When viewed from the nar-
row perspective of the basic nutritional requirements of laboratory colonies
feeding on artificial diets, insect nutrition, though supplying essential in-
formation for a complete understanding of insect life, is indeed "boring
stuff." The insects themselves must also share part of the blame; except for
their requirement of a dietary sterol, their nutritional needs differ in only
minor ways from those of vertebrates (Dadd 1973).
Insect nutrition was given a strong dose of much needed excitement with
the realization that not only are basic nutritional requirements important,
but so are the amounts and rates of food eaten, digested, assimilated and
converted to tissue growth, and that these can be affected by variation in
both basic nutrients and non-nutritional compounds (e.g. allelochemics) in
the food. This area of research has been called "insect dietetics" (Beck 1972,
Beck and Reese 1976) and "quantitative nutrition" (Scriber and Slansky
1981) (Fig. 1). When we examine and evaluate the changes in an insect's
behavior and regulatory physiology, as it attempts to cope with a variable
environment, and when we identify the ecological consequences and evolu-
tionary aspects of such behavior, then "insect nutrition" achieves a greater
significance by metamorphosing into "insect nutritional ecology" (Fig. 1).
I shall here identify the kinds of interactions we need to understand to
lay a solid foundation for a nutritional ecology of insects, and present some
THE PARADIGM OF NUTRITIONAL ECOLOGY
Paulus' quote above suggests that feeding and growth are basically
passive-flow, inflexible processes, similar perhaps to the diversion of a stream
to fill a pond: water or food flows in, and the pond or caterpillar gets larger.
This is a common misconception. Feeding and growth are active, dynamic
processes with feedback mechanisms and wide ranging ramifications through-
out an insect's life (Fig. 2, and below) 1.
*Frank Slansky Jr. is an assistant professor in the Department of Entomology and Nema-
tology at the University of Florida. His research interest is in the nutritional ecology of larval
and adult insects within both basic and applied contexts.
Current address: Department of Entomology and Nematology, University of Florida,
Gainesville, Florida 32611. Florida Agricultural Experiment Station Journal Series No. 3478.
1Superscripts refer to notes in the Appendix of this paper.
Florida Entomologist 65(1)
METAMORPHOSIS IN INSECT NUTRITION
CONCENTRATIONS AND PROPORTIONS _
FOOD CONSUMPTION AND UTILIZATION
BEHAVIOR AND REGULATORY PHYSIOLOGY ECOLOGY
ECOLOGY AND EVOLUTION
Fig. 1. The metamorphosis of insect nutritional ecology from nutrition
Fig. 2. Interactions of feeding behavior with other key behaviors. See
Appendix note 1 for specific examples.
SURVIVAL 4---* FEEDING <-- REPRODUCTION
Insect Behavioral Ecology-'81 Slansky Jr.
Whatever the historical roots underlying this misconception (emphasis on
mean values, pesticides and energy flow studies have had some role) 2, it
must be stressed that individuals in a population are not identical copies of
"passive, open-loop, energy partitioning devicess" (Hubbell 1971, p. 271;
see also Slobodkin 1965, Wellington 1977, and others). In addition to differ-
ences among species and populations in appearance, physiology and be-
havior, there are within-population differences in individual performance,
and this performance includes active modifications of physiological and
behavioral responses to a variable environment.
The basic paradigm for nutritional ecology can thus be stated as follows:
Within a particular realm of environmental conditions, there is a set of
states (e.g. a particular body size, color, wing loading ratio, proportion of
resources allocated to eggs, timing of life cycle events, etc.) which is
"optimum" in the sense that it will result in maximal fitness for the indi-
vidual (see McFarland 1977). We wish to identify how this optimal set of
states differs among species and populations, and within populations through
time, and the selective forces that bring about these differences (Fig. 3A).
Furthermore, we wish to answer the questions of how, and to what ex-
tent, an individual can alter, in response to a changing environment, its
physiological and behavioral processes (e.g. consumption rate, metabolism,
synthesis of glycerol for freezing tolerance, and extent of movement) to
achieve and maintain the optimal set of states. We also wish to identify the
ecological consequences (including changes in the timing and amount of
reproduction and in probability of survival) of alterations in these processes
and of inability to achieve and maintain the optimal set of states (Fig. 3B).
Finally, we wish to identify how the differences in process alteration and
in deviation from optimal states, in response to a particular change in the
environment, vary among populations and species, and to identify the con-
sequences for fitness of these differences (Fig. 3C). This will help us under-
stand the evolution of different lifestyles3.
This view of nutritional ecology is a useful way to structure and syn-
thesize research on both the basic and applied aspects of behavioral ecology.
Because of the primacy of feeding behavior, food allocation and associated
processes, and because of their pervasiveness throughout an organism's life,
an understanding of these processes should indicate the significance of varia-
tion in most of the other aspects of an organism's lifestyle. In other words,
investigating the underlying nutritional basis to many of the "decisions" an
insect might make in its lifetime will help us understand why they are made.
DECISIONS, DECISIONS, DECISIONS:
A DAY IN THE LIFE OF AN INSECT
The life of an insect is filled with decisions. In the sense used here, an
insect "makes a decision" when, after "evaluating" environmental inputs, it
responds in some manner (Hubbell 1971,'Dawkins and Dawkins 1973, Mc-
Farland 1977). The response may be to continue physiological and be-
havioral processes at their current levels. Or, the responses may be induc-
tory or compensatory. An inductory response involves a change from some
previously optimal set of states to a new set (e.g. see "Diapause" below); a
compensatory response involves an attempt to maintain some particular set
of states in the face of a changing environment (e.g. see "Feeding" below).
Florida Entomologist 65(1)
\ : : /
Fig. 3, A-C. The paradigm of nutritional ecology. A. Identification of (1)
the differences in the optimal set of states (e.g. body size, color, and wing
size, indicated by the three units of each symbol) for an individual of dif-
ferent species (different symbols), different populations, and different gen-
erations within a population (indicated by the reduction in size of the third
box), and (2) the selective factors (arrows) that bring about these differ-
ences. B. Identification of (1) the alterations in an individual's physiological
and behavioral homeostatic processes such as increased food consumption
(plus sign on left) in response to a deterioration in food quality (minus
sign on left) and increased time spent basking on the surface of a leaf (plus
sign on right) in response to a drop in ambient temperature (three minus
signs on right), in an attempt to achieve and maintain the optimal set of
states (indicated by the four boxes at the top), and (2) the ecological con-
sequences (dotted lines) resulting from the process alterations (e.g. in-
creased probability of mortality from increased exposure while feeding and
basking) and from inability to achieve a particular state (e.g. reduced fit-
ness because of the lowered fecundity indicated by the reduced size of the
rightmost box at bottom). C. Identification of (1) differences between an
individual of two species (e.g. a migratory one indicated by the boxes and a
non-migratory one indicated by the circles) when confronted with a change
in environment (e.g. a shortening of daylength indicated by the two minus
signs at left and right). The larva of the migratory species responds with
a moderate increase in food consumption (three plus signs at left) to
Insect Behavioral Ecology-'81 Slansky Jr.
In order to understand the evolution of these active responses within
their adaptive context, it is important, albeit often difficult, to distinguish
them from situations in which the insect responds passively with little
choice4. For decisions and responses involving metamorphosis, reproduction,
migration and diapause, the underlying neurohormonal integration and
physiological feedback mechanisms are reasonably well understood (Chen
1971, DeWilde and DeLoof 1973b, Chippendale 1977, Rankin 1978, Gilbert
et al. 1980). This is in contrast to the poorly understood cause/effect inter-
actions relating feeding, metabolism and growth to each other and to other
behaviors (Keister and Buck 1974, Barton Browne 1975, Steele 1976, Kam-
mer and Heinrich 1978, Bernays and Simpson 1981, Scriber and Slansky
1981). I shall now discuss some of the many decisions, and physiological and
behavioral responses that an insect may make, to demonstrate their under-
lying nutritional aspects and their consequences throughout the insect's
The timing of egg hatch can be critical to the survival of larvae that
feed on young leaf tissue. If an egg hatches too early before budburst the
larva may starve to death; if it hatches too late the leaves may have aged
sufficiently to render them a poor quality food (Feeny 1976, Gilbert 1980,
Schneider 1980) 6. Furthermore, the energetic cost of embryonic development
and maintenance may be considerable7, such that delay in egg hatch may
cause premature utilization of energy reserves destined for the larval
stage8. Species that overwinter in the egg or early larval stages may have
greater egg size and/or caloric content than related species that overwinter
as mature larvae or pupae (Purrington and Nielsen 1977, Anderson 1978,
see also Capinera 1979)9.
While the underlying nutritional aspects of feeding behavior are obvious,
the subtleties of the feeding responses are important to understand because
of their significance throughout an insect's life (Fig. 2). The feeding re-
sponses of phytophagous insects are strongly influenced by olfactory and
gustatory stimuli resulting from both nutritional and non-nutritional (espe-
cially allelochemical) compounds in the food. The response to allelochemicals,
including both feeding stimulants and deterrents, seems generally to be the
primary determinant in the insect's decision of whether or not to feed on a
particular plant (for reviews see Chapman 1974, Beck and Reese 1976,
Kogan 1977, Dethier 1980).
achieve the new state of increased wing size facilitating migratory flight by
the adult (increased size of rightmost lower box), whereas the larva of the
nonmigratory species responds with an even greater increase in food con-
sumption (five plus signs at right) to achieve its new state of increased
lipid storage (increased size of middle circle) to fuel metabolism in the
diapausing pupa. Ecological consequences (dotted lines) are as discussed in
B. Information on these optimal sets of states, responses and consequences
depicted in A-C allows us to better understand the evolution of different
Florida Entomologist 65(1)
Given an acceptable food, further decisions of how fast, of how often and
of how much to eat are required'0. Growth rate (including both rate of
development and final weight at pupation) has significant impact on fitness.
Therefore individuals of a particular species are expected to exhibit a cer-
tain feeding rate which will result in an optimal growth rate. The observed
feeding rate will probably be less than the physiological maximal rate be-
cause of certain costs associated with feeding11. That insects are not operat-
ing at their maximal feeding rate is indicated by the increase in food con-
sumption frequently observed in response to a deterioration in food quality
(Table 1). The degree to which different species exhibit this compensatory
response may be related to their lifestyle12. For further discussion of feeding
strategies (i.e. decisions and responses) see Hassell and Southwood (1978),
Mattson (1980), and Scriber and Slansky (1981).
The ultimate goal of a larva is to produce a reproductively competitive
adult. Therefore, it is perhaps not surprising that the decision to pupate, or
molt to adult in hemimetabolous insects, often depends on the attainment of
some minimal body weight (which is below its optimum)13 (Gilpin and
McClelland 1979, Nijhout 1979, Grabstein and Scriber 1981, and references
in Scriber and Slansky 1981). If a larva is subjected to poor food quality
(which slows its growth rate) it seems to evaluate the potential costs of
prolonged development (see Appendix note 11) versus the potential costs of
reduced adult size14. When growth is slowed before the larva has achieved
the minimal weight, the choice is probably moot-the potential costs of pro-
longed development are going to be less than those of producing an adult
too small to be reproductively competent. However, above the minimal weight
the larva may make a choice that balances the potential costs of prolonged
development and those of producing an adult whose size and performance are
somewhat reduced. The percentage of optimal weight at which the minimal
weight is evolutionarily adjusted varies between species and is probably
related to their particular lifestyle15.
In climates where year round activity is not possible, insects may become
dormant (i.e. diapause) to cope with the unfavorable season, or they may
migrate to an area with a favorable climate (see papers in Dingle 1978, and
section below). When diapause is facultative, the decision to do so is made
after evaluating certain environmental cues. Most frequently these are
changes in photoperiod and temperature (Hoffman 1978, Hoy 1978, Beck
1980, Masaki 1980, Taylor 1980b), although changes in food quality may
also be involved'6.
Diapause occurs in all life stages but within a speices it typically occurs
in only one stage. In phytophagous insects the pattern of seasonal change in
plant quality associated with different plant growth-forms may be a major
environmental factor influencing the evolution of which life stage over-
wintersL7. Whatever the overwintering stage, it frequently contains a greater
percentage of lipid reserves and/or is larger than non-diapausing individuals
(Lang 1963, Downer and Matthews 1976, Calow and Jennings 1977, Purring-
Insect Behavioral Ecology-'81 Slansky Jr.
ton and Nielsen 1977, Anderson 1978). Such changes in optimal states pre-
sumably are necessary to provide fuel for metabolism during the extended,
non-feeding diapause period even though the metabolic rate often is reduced
as much as 50-90% during diapause (Keister and Buck 1974, Stoffolano
1974, Bauman et al. 1978). The success of these changes in buffering against
the potential energetic costs of a prolonged diapause is indicated by the fact
that adults emerging from overwintering pupae are not necessarily less
fecund than non-diapausing individuals (Soni 1976, Blau 1978, Danks 1978,
Wallace and Merritt 1980). Common inductive responses by larvae preparing
to enter diapause include slowed development and increased food consump-
tion as they "stock up" on lipid reserves (Table 2, Downer and Matthews
1976, Calow and Jennings 1977).
In species that exhibit facultative migration, the decision to initiate
migratory flight is made by the adult after evaluating environmental cues
such as photoperiod, temperature and food. This process is similar to the
decision-making for entry into diapause (DeWilde and DeLoof 1973a, 1973b,
Johnson 1976, Rankin 1978)18 (but changes in food quality and quantity
appear to play a much greater role in influencing an adult's decision to
initiate flight than they do in influencing a larva's decision to diapause).
For example, in some insects mated females choose to begin laying eggs and
inhibit flight19 in the presence of adequate food; a lack of, or poor quality
food inhibits their oviposition and stimulates flight (Rankin 1978, Solbreck
and Pehrson 1979, Slansky 1980b). Furthermore, although only a few species
have been studied, food quality and other factors affecting larval per-
formance may also have a significant effect on adult movement (Mittler and
Sutherland 1969, Wellington and Maelzer 1967, Leonard 1971, Sanders and
Active flight is a costly process20, but whether migratory individuals
stock up on fuel reserves prior to flight is less clearly understood than is
the frequently seen increased lipid storage prior to diapause (Nayar and
Sauerman 1969, Solbreck 1972, and references therein, Downer and Matthews
1976, Slansky 1980c). In many species there are obvious differences in wing
and body sizes between migrant and nonmigrant individuals in a population
(Harrison 1980). This certainly suggests differences in the amount of food
consumed by larvae and the way it is allocated to building the adult, as well
as differences in adult feeding and fecundity (Waldbauer 1968, Raccah and
Tahori 1971, Dixon 1972, Rose 1972, Harrison 1980, Ono and Nakasuji
1980). The negative effects on fecundity of fuel utilization during flight
seem to be more severe for species that utilize carbohydrate for fuel (e.g.
most Diptera) than for those that utilize lipid (e.g. Homoptera and
Hemiptera) (references in Slansky 1980c) 21
In making a choice of oviposition site, a female may evaluate a number
of features of the food (e.g. plant size, leaf shape, color, odor, taste and
presence of other eggs; DeWilde and DeLoof 1973a, Labeyrie 1978b, Rausher
1978, 1979, Williams and Gilbert 1981). In species exhibiting a semelparous
Florida Entomologist 65(1)
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Insect Behavioral Ecology-'81 Slansky Jr. 53
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Florida Entomologist 65 (1)
TABLE 2. INDUCTIVE PROCESS AND STATE ALTERATION BY LAST INSTAR LARVAE
OF THE IMPORTED CABBAGEWORM, Pieris rapae, AS THEY PREPARE
TO ENTER PUPAL DIAPAUSE IN RESPONSE TO SHORT PHOTOPERIOD
(8L:16D), COMPARED TO LARVAE REARED IN A NON-DIAPAUSE IN-
DUCING PHOTOPERIOD (16L:8D) (SLANSKY,UNPUBLISHED DATA).
Process or State Magnitude and Direction
Altered of Alteration
Time in instar (days) 17% increase
Consumption rate (dry mg/day) 16% increase
Food consumed (dry mg) 29% increase
Growth rate (dry mg/day) 15% decrease
Weight Gained (dry mg) 7% decrease
Relative metabolic rate 33% increase
(dry mg metabolized/dry mg body wt./day)
Pupal lipid content (mg/pupa) 40% increase
reproductive strategy (Calow 1973), extensive egg production occurs very
soon after the adult ecloses, and there is probably little evaluation of en-
vironmental cues by the adult prior to oviposition. In such species, poor
food quality and other factors causing a reduction in the amount of larval
growth (and thus smaller adult size), frequently have a significant negative
impact on adult fecundity (Wellington and Maelzer 1967, Leuck and Perkins
1972, Yamada and Umeya 1972, Blau 1978, Wagner and Leonard 1979, Bar-
field et al. 1980, Barbosa et al. 1981, Moscardi et al. 1981) 22
At the other extreme are species exhibiting an iteroparous reproductive
strategy (Calow 1973). These species manifest repeated reproduction
throughout a relatively long-lived adult stage, and food consumption by the
adult is important to normal egg production. Decisions are made regarding
when to lay, how many, and sometimes even what kind of eggs to lay23. Such
decisions have great impact on the female's fitness (Smith and Fretwell 1974,
Smith 1976, Istock 1978, Taylor 1980a, Boggs 1981).
In species that feed on a protein source in the adult stage, suggesting
that feeding is required not only for adult maintenance but also to supply
the energy and nutrients for provisioning the eggs, egg production tends to
be closely linked to food consumption through a neurohormonal feedback
system (DeWilde and DeLoof 1973a, 1973b, Stoffolano 1974, Regis 1979
Solbreck and Pehrson 1979, Wise 1979, Slansky 1980a, 1980b). Thus a re-
duction in the quality or quantity of food for the adult female frequently
results in a delay in the onset, and a reduction in the rate, of egg production
(i.e. process alteration) 24, with the result of prolonging the female's life and
maintaining the size and hatchability of the eggs she does lay (i.e. main-
tenance of an optimal state) (Table 3, Warren 1924, Engelmann 1970, Calow
1973, Labeyrie 1978a). A further adaptive feature of the female's choice to
halt or reduce egg production under poor food conditions is that she does
not waste reproductive effort producing offspring with a low probability of
survival (Slansky 1980b).
In nectar-feeders and other insects that utilize a carbohydrate food
source, the role of adult food in influencing egg production is not as clear.
For only a few of these species is it known whether the food merely supplies
Insect Behavioral Ecology-'81 Slansky Jr.
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Florida Entomologist 65(1)
water, or if it also serves as an energy source. If the latter, the question
remains as to whether the energy is required solely for adult maintenance
(i.e. eggs are provisioned from energy and nutrients stored during the larval
stage) or to provision eggs as well. Baker and Baker (1975) found con-
siderable variation in sugar and amino acid contents of nectar of different
plant species, but there is a lack of data on the impact of this variation on
egg production (Shorey 1963, Van Handel 1965, Finch and Coaker 1969,
Hines et al. 1973, Fenemore 1979).
The decisions, discussed above, that an insect may make in its lifetime,
and many others not discussed (e.g. mate attraction, mate choice, parental
investment and nest building)26 all involve some underlying nutritional
component. They include compensatory responses to achieve and maintain
the optimal set of states of developmental time, weight gain (body size) and
fecundity, in the face of a nutritionally and otherwise variable environment,
and inductory responses, changes in optimal states in response to environ-
mental cues. These responses may include changes in amounts, rates and
timing of feeding behavior, metabolism, enzyme synthesis, resource alloca-
tion, flight behavior and other physiological and behavioral processes.
There are consequences for fitness, because of effects on survival and re-
production, resulting from these responses, and from the inability to achieve
and maintain the optimal set of states. Thus, differences among populations
and species in the kinds and magnitudes of these responses and optimal
states are expected to have evolved as adaptations to different lifestyles.
Herein lies the importance of the contribution of nutritional ecology to
questions of a basic nature. By understanding the nutritional responses and
consequences that occur throughout an organism's life we will achieve an
understanding of the ecology and evolution of different lifestyles expressed
by species that are migratory or non-migratory, specialized or generalized
feeders, herb or tree feeders, parasitic or predatory, and so on.
The fact that this basic information also has applied relevance to the
development of integrated pest management strategies has only recently
been recognized (Barfield and Stimac 1980, Levins and Wilson 1980). For
example, it is essential that we know the factors influencing the feeding,
growth, reproduction, movement and survival of pest insects. Only then can
we refine and couple models of pest population dynamics with models of crop
plant growth to produce models with greater precision and greater powers
of prediction of pest population size and crop plant damage (Hammond
et al. 1979, Barfield and Stimac 1980, 1981, Garner and Lynch 1981, Stimac,
this Symposium). Such information may also allow us to effectively manipu-
late the crop environment (such as through chemical fertilization and grow-
ing of resistant plant varieties) to disrupt the normal performance of the
pest (Leuck and Perkins 1972, Jones 1976, Meisner et al. 1977, Norris and
Kogan 1980, Tingey and Singh 1980)27. Thus, structuring and synthesizing
research on insect pests within the paradigm of nutritional ecology will yield
much useful information of broad relevance. Indeed, just as Stripe the
caterpillar found excitement in the prospect of metamorphosing into a
butterfly, so too can we find excitement in the unfolding wings of insect
Insect Behavioral Ecology-'81 Slansky Jr.
Feeding is an active, dynamic process with numerous feedback inter-
actions and consequences throughout an insect's life, affecting and being
affected by survival, growth, reproduction and movement. An insect must
make a number of decisions during its life, including when to hatch from
the egg; what, when and how much to eat; how much and what kinds of
nutrients to store prior to pupation; whether and when to diapause and/or
migrate; and when, how many, and sometimes even what kinds of eggs to
lay. These and other decisions all have an underlying nutritional basis. Thus
the paradigm of nutritional ecology that is presented involves viewing in-
sect nutrition within the contexts of behavior, ecology and evolution. It is
based on the premise that within a particular realm of environmental con-
ditions, there is an optimal set of states (e.g. a particular body size, color,
wing loading ratio, proportion of resources allocated to egg production, and
phenology) for the individuals in a population which yield their highest
fitness. Research in nutritional ecology involves identifying (1) how and to
what extent an individual can alter, in response to a changing environment,
various physiological and behavioral processes (e.g. consumption rate,
metabolism, excretion, and movement) in order to achieve and maintain the
optimal set of states; (2) the consequences for fitness (including changes
in the timing and amount of reproduction and in probability of survival)
both of the alterations in these processes and of the inability to achieve the
optimal set of states; and (3) how the optimal set of states, and (1) and
(2) above, differ among species, populations and within a population
through time. Nutritional ecology is a useful way to structure and synthesize
research on both the basic and applied aspects of insect behavior, and it
allows us to achieve a better understanding of the evolution of different
1The amount, rate and quality of food consumed by larvae influences
their growth rate, developmental time and final body weight (reviewed in
Scriber and Slansky 1981). Larval survival may also be affected (Barney
and Rock 1975, Hatchett et al. 1976, McWilliams and Beland 1977, Garner
and Lynch 1981) although the actual causes are seldom determined. These
could include: (1) a direct toxic effect brought about by an increase in the
concentration of an allelochemical in the food or by a metabolic impairment
due to poor nutrient quality (Gordon 1961, Meisner et al. 1977); (2) mortal-
ity due to starvation if essential feeding stimulants are not present in suf-
ficient concentrations, and/or if feeding deterrents and inhibitors are present
(for reviews see Chapman 1974, Beck and Reese 1976) ; (3) increased suscep-
tibility to biotic mortality agents through prolonged development, greater
exposure while feeding, and differential attractiveness of different plants to
predators and parasitoids (Slansky and Feeny 1977, Price et al. 1980, Vinson
and Iwantsch 1980a). Movement in the larval stage can also be affected by
food quality (Capinera and Barbosa 1976). A factor affecting growth may
feed back to affect feeding. For example, parasitoids frequently alter their
host's development, with concomitant changes in the host's feeding behavior
(Slansky 1978; Vinson and Iwantsch 1980b).
The amount, rate and quality of food consumed by adult insects influ-
ences their fecundity, movement and survival (Shorey 1963, Ellis et al.
1965, Kishaba et al. 1967, Dingle 1968, DeWilde et al. 1969, Finch and
Florida Entomologist 65(1)
Coaker 1969, Van Emden and Bashford 1969, Engelmann 1970, Rose 1972,
Van Duyn et al. 1972, Jensen et al. 1974, Labeyrie 1978a, Visscher et al.
1979, Harrison 1980, Slansky 1980a, 1980b). Feeding and development in
the larval stage may also influence performance by the adult through effects
on adult size, nutrient reserves and timing of oviposition (Leuck and Perkins
1972, McCaffery 1976, Ottens and Todd 1979, Barfield et al. 1980, Barbosa
et al. 1981, Moscardi et al. 1981).
Reproduction is intimately linked with adult feeding behavior (DeWilde
and DeLoof 1973, 1973b, Slansky 1980a) and survival (Calow 1973, Slansky
1980a, 1980b). The occurrence and amount of movement (flight) may have
an effect on subsequent timing and extent of egg production (Slansky 1980c
and references therein).
Reproductive performance may have significant, though often subtle, in-
fluences on subsequent larval performance. For example, early-laid eggs of
the gypsy moth, Lymantria dispar, are larger and contain more yolk than
late-laid eggs (Capinera et al. 1977). Larvae hatching from larger eggs ex-
hibit a greater tendency to disperse (Capinera and Barbosa 1976) whereas
larvae from the smaller eggs may exhibit prolonged development and pro-
duce larger, more fecund adults (Barbosa and Capinera 1978).
2Wellington (1977) discusses how our fetish for mean values seems to
have done much to distract us from studying insects as variable individuals,
and he suggests we "put the 'insect' back into 'insect ecology' ". Also, much
valuable research effort was diverted from studying basic insect biology
when we became stuck on the "pesticide treadmill" (van den Bosch 1978).
With current interest in integrated pest management programs, it has be-
come strikingly apparent how little we know about the basic biology of many
of our insect pests (Barfield and Stimac 1980). Furthermore, although the
concept of energy flow through trophic levels has done much to expand our
understanding of the structure and dynamics of ecosystems (Odum 1969),
it also seems to have diverted our interest from the behavioral ecology and
ecological functioning of individual organisms (Hubbell 1971). The role of
organism regulation was not denied (Odum 1962), but for the most part
individuals were viewed as passive energy-partitioners and -transducers,
hidden away in the "black boxes" of ecosystem energy flow diagrams. In
addition, although it was recognized that some organisms could have a
greater impact on nutrient cycling than on energy flow (Odum 1962), the
possibility that nutrient utilization could, in fact, be a primary determinant
of energy utilization seems to have been overlooked. Data indicating the
primary significance of nutrient utilization are now available for many spe-
cies of insects (Slansky and Feeny 1977, McNeill and Southwood 1978) and
other animals (Mattson 1980), and plants (Chapin 1980).
'Some attributes of different lifestyles: migratory vs. non-migratory,
specialized vs. generalized feeding, sap vs. foliage feeding, and aposematic
vs. cryptic coloration.
4Two examples to clarify this point: although insects do maintain a
certain degree of compensatory ability in relation to a change in tempera-
ture, the response of slower growth in a cooler temperature is probably a
passive response forced on the insect because of its inability to fully com-
pensate for the reduced temperature (Clarke 1967, Hochachka and Somero
1973, Casey 1977, Block and Young 1978). This should not be confused with
the much different question of the evolution of growth rates (Auerbach and
Strong 1981, Scriber and Slansky 1981).
The response of an insect to a potentially toxic allelochemical in its food
provides another example. Slansky and Feeny (1977) found that larvae of
the cabbageworm, Pieris rapae, feeding on three species of crucifers con-
sumed food and grew at rates much lower than expected in comparison to
Insect Behavioral Ecology-'81 Slansky Jr.
larvae feeding on a number of other crucifers. Variation in leaf water and
nitrogen did not explain these observations. These reduced rates were at-
tributed to unique allelochemicals presumably present in the three species
but not in the other crucifers. The problem arises in attempting to interpret
these responses. Did the larvae actively and adaptively respond to the
presence of potential toxins by reducing their consumption rate in order to
reduce their intake of these toxins and perhaps to not overload their de-
toxication system, with the result of a reduced growth rate? Or, did the
consumption of these toxins metabolicaly interfere with and therefore slow
growth rate, with the reduced consumption rate being merely a passive re-
sult? Slansky and Feeny (1977) did not resolve this issue, but Blau et al.
(1978) seem to have found an experimental and statistical protocol by which
to distinguish "toxic" effects on growth from those of a reduced consumption
rate. The actual "active choice" nature and physiological mechanisms of
many insect "decisions" remain to be determined.
5Unfortunately but understandably, we do not have, for any population
of insects, enough data to answer more than a few of the questions posed by
the paradigm of nutritional ecology. It is therefore necessary to piece to-
gether data from different species which answer certain of these questions
to indicate the kinds of decisions that these organisms might make, and the
kinds of consequences that might result. Many of the examples presented
here deal with phytophagous (plant eating) insects, because I am more
familiar with these through my own research, and because more studies
falling within the paradigm of nutritional ecology seem to have been done
with these-in contrast to carnivorous and detritivorous insects. However,
the concept of decisions and consequences also applies to insects in these
latter groups as well, but the specifics will of course vary with the type of
food (e.g. eating a plant leaf versus another insect), mode of feeding (e.g.
a sedentary larva vs. an active, hunting predator), and other aspects of the
particular organism's lifestyle.
"The food quality (for phytophagous insects) of the leaves of many
plants, and especially of grasses and trees, frequently exhibits a rapid de-
terioration as the leaves age. Changes that contribute to this deterioration
include increased leaf toughness, decreased water and protein contents, and
increased allelochemic content (Feeny 1976, Scriber and Slansky 1981). In
fact, this rapid deterioration in food quality of many grass and tree leaves
may have been a selective agent leading to the evolution of the egg and early
larval stages as the overwintering stages, as frequently seen in grass and
tree feeding species (Slansky 1974b; see "Diapause" section and Appendix
7Gilbert and Schneiderman (1961) found a 50% drop in lipid content
between egg and early larva in the cecropia moth (see also Richards 1959).
SEggs with reduced amounts of yolk have lower viability and produce less
vigorous larvae (Wellington and Maelzer 1967) exhibiting prolonged de-
velopment (Capinera et al. 1977, Barbosa and Capinera 1978) and suffering
greater mortality losses (Iwao and Wellington 1970). Although the eggs in
these cases had reduced yolk because they were among the late-laid eggs of
these female moths, delayed hatching of fully-yolked eggs, resulting in pre-
mature utilization of energy reserves, would probably have a similar effect
9Evolutionary changes in egg size and energy content would in turn have
consequences for adult size, energy and nutrient reserves, total fecundity,
1oOther decisions for some insects include choosing a particular mixture
of foods (Waldbauer and Bhattacharya 1973, Greenstone 1979) and choosing
food with particular allelochemics that are sequestered by the insect (Duffey
Florida Entomologist 65(1)
1980). The physiological control of feeding has recently been reviewed by
Bernays and Simpson (1981).
"If a larva decides to feed faster during a feeding bout and/or more
often (less time between feeding bouts) in order to increase feeding rate,
its ability to digest and assimilate food may decrease (e.g. because of a more
rapid passage of food through its gut). As long as the relative increase in
feeding rate exceeds the relative decrease in assimilation efficiency, the
assimilation rate (i.e. feeding rate X assimilation efficiency) will increase,
and, all else equal, growth rate will increase. However, beyond a point, for
example, where digestive enzyme production can no longer be increased,
then assimilation efficiency and rate will decrease. This decrease, coupled
with a probable increase in metabolic cost associated with feeding, digesting
and assimilating the food, will result in a decrease in growth rate with a
further increase in feeding rate (Smith 1976, Calow 1977, Scriber and
Slansky 1981). A further cost of an increased feeding rate may be an in-
creased exposure to biotic mortality agents. For example, a female para-
sitoid may be attracted to the odors released by fresh leaf damage at the
feeding site of a potential host larva (Sato 1979, see also Price 1975, Slansky
and Feeny 1977, Windsor 1978).
A larva on a food that has deteriorated in nutritional quality may suffer
a reduced growth rate either because it decides not to feed faster or because
it does not have the ability to feed faster. Potential costs of the resulting
lengthened development include prolonged exposure to mortality agents and
a delay in the timing of various aspects of its life cycle (i.e. phenology).
For example, prolonged development may subject the larva to even further
deterioration in food quality as the leaves age, and it may prevent the larva
from pupating and achieving cold-hardiness before the first killing frost.
For further discussion of the significance of timing in the life histories of
insects, see Taylor (1980a).
12Herrebout et al. (1963) suggested that the several-week-longer de-
velopmental time of larvae of certain moth species on Scots pine results from
their feeding less often during the day because their mode of protection
against enemies lies in their cryptic coloration and posture, in contrast to
the more frequent daytime feeding and more rapid development of the
aposematically colored larvae of certain other speices (see also Heinrich
13The value of the minimal weight at pupation for a particular species
has probably been adjusted by natural selection in relation to the smallest
weight that will supply the energy and nutrient reserves necessary to allow
metamorphosis to a reproductively competent adult.
14Potential costs of reduced adult size include a reduction in dispersal
powers, mating ability, length of life and fecundity, and a greater suscepti-
bility to predation (Yamada and Umeya 1972, Allen 1973, Hespenheide 1973,
Sanders and Lucuik 1975, Barfield et al. 1980, Barbosa et al. 1981, Moscardi
et al. 1981, and several papers in Blum and Blum 1979).
15In species such as Drosophila melanogaster that exploit an ephemeral
and frequently crowded food source, rapid development to a minimal weight
that is a low percentage of the optimal weight, would seem to have a large
selective advantage over a longer developmental time to a greater minimal
weight (Sang 1956, Robertson 1965, Collins 1977). On the other hand, in the
banded woollybear, Pyrrharctia isabella, which is univoltine and overwinters
as a diapausing pupa, a too-rapid development to pupation may risk pupal
desiccation and/or untimely utilization of metabolic reserves (Goettel and
Philogene 1978, and other references in Scriber and Slansky 1981). In such
species we might expect, in addition to a finely-tuned regulation of growth
in relation to environmental cues such as photoperiod, a minimal body weight
Insect Behavioral Ecology-'81 Slansky Jr.
that is closer to the optimum.
16The incidence of diapause may be increased in larvae feeding on poor
quality food (e.g. senescing or desiccated foliage), probably because the
resulting slower growth subjects the larvae to a greater number of diapause-
inducing photoperiod cycles, rather than because of a direct effect of a
photoperiod-induced change in plant quality (Danilevskii et al. 1970, Saun-
ders 1976, but see Morris 1967, DeWilde et al. 1969). On the other hand,
induction of diapause in parasitoids and hyperparasiotids seems to be more
directly related to the qualitative condition of their host (Fisher 1971,
McNeil and Rabb 1973).
17The food quality of the leaves of many trees and grasses often is
suitable for only a few weeks in the spring and early summer, in contrast to
that of many herbaceous plants in which nutritionally suitable leaves are
available for much of the growing season (Slansky 1974b, Scriber and
Slansky 1981). Because of this, I suggest that, in insect species whose larvae
feed on tree and grass leaves, there is selection to limit the number of gen-
erations and to time the appearance of their larvae for development early
in the growing season when the food quality is adequate. On the other hand,
species feeding on herbaceous plants are probably not under such selection
and would be expected to overwinter in the "more hardy" pupal stage as well
as exhibit more generations per growing season (Slansky 1974b, Masaki
Therefore I believe it is advantageous for tree and grass feeding species
to overwinter as adults that can quickly lay eggs, or as eggs because the eggs
can rapidly hatch into larvae and begin feeding. From the literature, I found
that of eighty-six species of butterflies in the temperate United States, (1)
about 85% of those species over-wintering in the adult or egg stage feed on
trees or grasses, (2) only about 45% of those species overwintering in the
pupal stage feed on trees or grasses, and (3) these species tend to have
fewer generations per growing season in contrast to those feeding on
herbaceous plants (Slansky 1974b). These data support the above hypothesis
and seem to indicate a further underlying nutritional basis to life history
1"In fact, reproductive diapause and migratory flight frequently co-occur
'"Such inhibition of flight sometimes includes histolysis of the flight
muscles (McCambridge and Mata 1969, Rankin 1978, Solbreck and Pehrson
20Metabolic rates during flight may be 50 to 100 times greater than
during rest (Kammer and Heinrich 1978).
'2In milkweed bugs (Oncopeltus fasciatus), as much as five hours of
tethered flight/day for six consecutive days has little negative effect on a
female's fecundity or length of life, even when starved during the six days.
I could detect no compensatory increase in feeding rate after flight, suggest-
ing that either the metabolic costs of tethered flight are not significant,
and/or the documented high rate of preflight feeding and associated lipid
storage are more than adequate to fuel relatively long duration flights
22The related question of whether similar sized adults produced from
larvae on different quality foods behave differently has received little atten-
tion (Barbosa and Capinera 1978, Wellington 1977) except within the con-
text of "quality control" of laboratory reared insects (Chambers 1977).
23In response to variation in food quality and quantity, some females may
decide to produce different kinds of offspring (i.e. an inductive response).
For example, many Hymenoptera and perhaps some aphids can choose which
sex each offspring will be (Gilbert 1980, Torchio and Tepedino 1980 and
Florida Entomologist 65(1)
references therein) and many aphids can vary the proportion of nymphs
destined to become alate (versus apterous) adults (Mittler and Sutherland
1969, Harrison 1980).
24This decision frequently involves the breakdown and absorption of eggs
within the female (Bell and Bohm 1975).
25From Table 3 we see that under conditions of food limitation (i.e. the
amount of milkweed seeds fed to these bugs was reduced 50% below the ad
lib. level), adult females of both 0. fasciatus and 0. cingulifer reduced their
rate of egg production. Thus the duration of egg production was either main-
tained (0. fasciatus) or extended (0. cingulifer). Egg quality was not re-
duced, as indicated by the values of fresh egg weight, percentage egg hatch,
and length of life of newly closed, starved nymphs, which were all similar
to those from fully fed females. Clutch size was also maintained at a normal
value. For 0. fasciatus on a 25% ration, egg quality and clutch size were
also maintained but the duration of egg laying was reduced. The importance
of maintaining egg quality is obvious, and there is indication that clutch size
is also relevant to survival of these gregarious, aposematically colored in-
sects (Slansky 1980b).
Under conditions of total starvation after eclosion, these bugs never
oviposit. However, after seven days of feeding (the conditions for the
starved bugs in Table 3), they do lay some eggs. It is evident that under
these conditions of starvation, egg quality for both 0. fasciatus and 0.
longirostris is again maintained, although clutch size is reduced to about one
half that of fully fed females. Thus in these species of Oncopeltus, main-
tenance of egg quality seems to rate the highest priority, followed by clutch
size and then rate and duration of egg laying.
260ne important criterion in mate choice frequently is body size, prob-
ably as an indicator of the mate's "vigor" and/or ability to make an optimal
nutritional contribution to the production of eggs (Leopold 1976, papers in
Blum and Blum 1979, Boggs and Gilbert 1979, Mullins and Keil 1980). For
thorough discussions of decisions involving nest building and occupancy, see
Brockmann and Dawkins (1979) and Brockmann (1980).
27Pesticides are frequently a component of pest management programs
and thus we need to know the factors influencing their efficacy, which may
vary as a function of the amount of food consumed by the insect pest, the
insect's nutritional status (e.g. lipid content) and the host plant fed on
(Gordon 1961, Raccah and Tahori 1971, Kea et al. 1978, Berry et al. 1980).
I thank Jim Lloyd for inviting me to participate in the symposium, for
suggesting the title of this paper and for extensive editorial assistance; Mary
Jane Angelo for assisting with the figures; Nell Backus for assisting with
figures, data tabulation and searching for numerous references; Anne
Buchanan for typing several versions of this paper; and the following per-
sons for their welcome comments, criticisms and discussion: Nell Backus,
Carl Barfield, Jane Brockmann, Janne Cookman, Bill Fisher, Hal Gordon,
Norm Leppla, Jim Lloyd, Lauren Schroeder, Mark Scriber, Jerry Stimac,
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Florida Entomologist 65 (1)
MATE CHOICE AND LEPIDOPTERAN
RONALD L. RUTOWSKI*
Our understanding of the evolution and adaptive features of animal mat-
ing behavior has dramatically improved in recent years as our understand-
ing of the process of sexual selection and its consequences have been refined.
Darwin (1871) first proposed sexual selection as the evolutionary process
that gave rise to bizarre and seemingly maladaptive traits such as the tail
of the peacock and the brilliant colors of male butterflies. He reasoned that
the negative effects of these traits on male survivorship were outweighed by
their positive effects on male reproductive success during courtship with
females and competition with other males for access to females. Ronald
Fisher (1958) later-1930-pointed out that in order for this process to
have begun in the first place there had to have been some reproductive ad-
vantage to those females who chose for mates, males with certain traits. He
argued that those traits used by females in mate selection must be corre-
lated with high quality genes possessed by the male or high quality paternal
care or investments the male has to offer.
More recently, Robert Trivers (1972) explained that females are gen-
erally expected to be more selective than males because they usually make a
larger investment in each offspring than does the male, and therefore have
more to lose by copulating with low quality mates. In other words, a female's
reproductive success may be viewed as being limited more by her ability to
acquire nutrients for the production and care of her offspring rather than
by the number of matings she obtains. Such a limitation would, in turn,
favor care in the selection of mates. Males, on the other hand, typically in-
vest little other than sperm in each of their offspring. Therefore their re-
productive success is limited primarily by the number of copulations they
can obtain rather than the number of gametes they can produce. Males,
then, are generally expected to search out females and to mate willingly with
any receptive female.
The mating behavior of the Lepidoptera generally conforms to these ex-
pectations. After eclosion, females attract males either visually (butterflies
and some moths) or chemically (most moths). A male searching for females
locates one by using these signals, flies towards her, and courts her by
barraging her with visual, chemical, and tactile signals. The male's chem-
ical signals are typically produced by specialized structures such as hair-
pencils or patches of specialized scales on the wings. Females are generally
passive during courtship but, if receptive, those of some species assume
postures that facilitate the act of coupling. Copulation lasts from less than
one to more than several hours after which the male departs and renews his
search for mates. The female, on the other hand, (after copulation) ceases
to emit sex attractants and becomes refractory to mating attempts by males.
Her behavior becomes concentrated on efforts to locate oviposition sites and
*Ronald L. Rutowski is an Associate Professor in the Department of Zoology at Arizona
State University. His general interest is in the adaptive aspects of signal structure and func-
tion in animals. His research is specifically concerned with the mating behavior of butterflies
and nudibranchs. Current address: Department of Zoology, Arizona State University, Tempe.
Insect Behavioral Ecology-'81 Rutowski 73
deposit eggs. However, after a time, and oviposition, females will remate
one or more times. Variations on this basic pattern exist and have been dis-
cussed with particular reference to mate location by Greenfield (1981).
Although the general features of lepidopteran mating behavior as out-
lined above are well known (for review, Silberglied 1977; Scott 1973) there
are two key questions that I would like to examine. First, do females prefer
to mate with some conspecific males and not others in ways that will have
positive effects on their fitness (i.e. reproductive success)? In spite of de-
tailed data on the mechanisms of reproductive isolation in both butterflies
and moths the question posed by Darwin remains.
Second, do male moths and butterflies discriminate among potential
mates? Recent data have suggested that male lepidopterans might not be as
unselective as the "typical" male insect. During copulation the male forms
a spermatophore within a special sac, the bursa copulatrix, in the female's
reproductive tract. The spermatophore contains not only sperm but a large
quantity of accessory gland secretions as well. Other sacs, such as the ap-
pendix bursa, also may be filled with male-imparted secretions. The total
quantity of material passed may be as much as 10 per cent of the male's
body weight (equivalent to a 90 kg human male passing 9 kg or about 9
liters of ejaculate in a single copulation). These secretions have been shown
to be used by females for oogenesis (Boggs and Gilbert 1979; Goss 1977)
and may be used for somatic maintenance, too. As suggested by Thornhill
(1976), these secretions may then be viewed as paternal investment of
which the male has only a limited supply. The accessory gland secretions
include proteins and lipids (Marshall 1980) which presumably are available
in very limited quantities to adult butterflies and moths-most of whom
feed only on nectar or not at all. If males are limited in their ability to
produce these secretions, they might benefit from being selective with re-
spect to who receives those secretions.
FEMALE CHOICE IN THE LEPIDOPTERA
There are a variety of ways in which females might gain by selecting
among conspecific males (Trivers 1972). First, they may assure themselves
of the highest quality genes for the fertilization of their eggs. The genes a
female receives from a male may improve the probability that the female's
offspring will survive and reproduce. Certainly, not all conspecific males are
identical with respect to the quality of the genes they carry. Second, if the
spermatophore contents and other secretions passed by the male at copula-
tion have a positive effect on a female's fitness, she might benefit by favoring
males that are capable of passing large quantities of secretions (Thornhill
1976). Males vary with respect to this ability. In particular, for some time
after copulation, typically about 24 hours, males can only produce smaller
spermatophores than those in the first copulation (George and Howard
1968; Howell et al. 1978; Marks 1976; Outram 1971; Rutowski 1978; Sims
1979). In addition, because males typically feed only on nectar or not at all
as adults, the supply of nutrient compounds (proteins, lipids, etc.) available
for these secretions decreases with age (George and Howard 1968; Howell
et al. 1978; Sims 1979) and the number of previous matings (Outram
1971). As an aside, it has been shown in a pierid butterfly that female re-
ceptivity is regulated in part by the extent to which the bursa copulatrix is
Florida Entomologist 65(1)
inflated by the secretions received from the male (Sugawara 1979). This
further suggests that the quantity of secretions passed is of importance to
How might females recognize or identify males with "good" genes or
large quantities of available secretions? Some filtering or selection of males
is expected to occur as a result of the difficulty of reaching adulthood and
locating a female. As Lloyd (1979) points out, the males that manage to
reach females are likely to be of higher than average genetic quality by
virture of their having made it at all (Lloyd's "passive filtering") and hav-
ing made it in spite of competition with other males (Lloyd's "passive selec-
tion"). In addition to these processes females may gain from actively
filtering out or discriminating among males as well.
Large males might be those with genes that have permitted them to make
maximum use of resources available as larvae and also thereby might be
those males with the largest quantity of secretions to give. In Colias eury-
theme (Pieridae) male forewing length is positively correlated with the
quantity of secretions passed during copulation (unpublished data). Wing
area and body weight might both be indicators of male size that females
Male age might also be important to females. Advanced age as indicated
by wing wear might be indicative of a male's survival abilities and thereby
the quality of his genes. There are several known age-related changes in
appearance in butterflies that could permit females to detect older males and
mate preferentially with them (Taylor 1973; Rutowski in press). On the
other hand, females might prefer young males since they are least likely to
have previously mated and hence will have a full supply of secretions. It is
predicted that in species with large spermatophores relative to male body
weight youthfulness should be favored by females more than in species whose
males produce relatively small spermatophores.1
Courtship persistence or performance might also be an important in-
dicator of male quality. These aspects of courtship could display male vigor
and thereby genetic quality. In Pieris protodice (Rutowski 1978) and Tri-
choplusia ni (Shorey and Gaston 1964) male interest in females wanes im-
mediately after a mating and low persistence by a male might therefore
indicate a depleted male. Greenfield (1981) has suggested that the minute
quantities of sex attractant emitted by female moths may represent an
active filtering (sensu Lloyd, 1979) process that favors males who perform
well in mate location.
It also seems likely that the aphrodisiac produced by males during court-
ship could serve as a signal of male quality. In several cases, it has been
shown or suggested that production of a fully potent aphrodisiac is de-
pendent on an appropriate larval diet (Conner et al. 1980; Edgar et al.
1976; Grula et al. 1980). To this extent the signal might indicate the quality
of the genes the male carries that are important in locating and utilizing
larval foodplants. A strong male scent might also indicate that he possesses
a large quantity of accessory gland secretions by virtue of success while
feeding as a larva. In Leucania separate (Hirai 1977) some components of
the male's signal decrease in concentration with age. Grant and Brady
(1975) had previously suggested that females might use such a cue as a
means of age discrimination among males. Thomas Eisner and William
Insect Behavioral Ecology-'81 Rutowski
Conner have proposed (Eisner 1980) that females may use the aphrodisiac
to assess a male's ability to sequester defensive compounds. They support
this hypothesis by pointing out that the aphrodisiacs of some butterflies and
moths are derivatives of defensive compounds and, as mentioned above, that
they are affected by larval diet. Lastly, Lloyd (1981) has hypothesized that
females might individually recognize males on the basis of individual varia-
tion in the aphrodisiac and that this ability could be important in mate
assessment and selection, especially in long-lived butterflies that fly trap-
Of particular interest in this regard are the danaid butterflies in which
production of the aphrodisiac is dependent upon alkaloids the male acquires
from certain plants as an adult (Schneider et al. 1975). Females reject
males denied access to alkaloid-containing plants (Pliske and Eisner 1969)
which shows that sexual selection is responsible for maintaining this pattern
of behavior among males but the factors that initially favored this sort of
choice behavior on the part of females remain obscure. In the monarch but-
terfly, Danaus plexippus, the males in North America have limited access to
alkaloid-containing plants and the courtship consists of an aerial takedown
followed by grappling on the ground (Pliske 1975). In this species, vigor may
have replaced the aphrodisiac as the mate choice cue used by females.
The potential exists for some of these cues that are attractive to females
to be "cheatable". For example, a male with little or no accessory gland
secretions might produce a large quantity of aphrodisiac to gain matings.
Presumably the genes for cheating would do better than those of honest
males who do not mate at all. Three factors may guard against cheating in
the Lepidoptera. First, because female receptivity is controlled at least in
part by the quantity of secretions passed by the male during copulation, if
a male passes nothing but sperm the female will probably remate immedi-
ately. Given sperm precedence in the Lepidoptera (for review, Parker 1970;
more recent examples, Etman and Hooper 1979; Sims 1979), a male will
gain little or nothing from matings in which little or no accessory gland
secretion is passed. Thus, males cannot afford to divert all energy from
secretions to signal production. Second, the cost of some signals may pre-
clude cheating. For example, if a male puts all his energy reserves into
pheromone production he may reduce his longevity to the point where he
gains nothing. Third, it is unlikely that female choice is made on the basis
of a single cue. This, too, would make lying difficult. These arguments in-
volve a compromise between the cost of being attractive and the likely bene-
fits from lying about one's true quality. In the final analysis, insufficient
data exists to evaluate the importance of cheating in the Lepidoptera.
There are a variety of studies that suggest that female lepidopterans
actively discriminate among conspecific males; however, for none of these
are the consequences of the discrimination for the female's fitness known or,
in some cases, clear. Sheppard (1952) has shown that females of the scarlet
tiger moth (Panaxia dominula) preferentially mate with males of a genetic
constitution different from their own. In this species there are two color
morphs whose expression is controlled by two alleles at a single locus. In
Sheppard's experiments homozygous females "actively rejected" males of
like genotype as did the heterozygous females. Moreover, preliminary experi-
ments suggested that females were responding primarily to a chemical dif-
76 Florida Entomologist 65(1) March, 1982
ference between males of the two genotypes.
Other studies document that certain kinds of males may be found in mat-
ing pairs more frequently than others. These studies suggest but do not show
that female choice is the causative factor. For example, as expected, the male
oak moths (Phryganida californica) found in copula are at least on some
days larger than males in a random sample from the population (Mason
1969). The African queen (Danaus chrysippus) occurs in two color morphs,
one of which appears to be preferred by females during certain times of the
year (Smith 1975). Female choice is also strongly implicated but not con-
clusively documented by Sanders (1975), who reported that virgin males
of the spruce budworm (Choristoneura fumiferana) successfully copulated
more frequently than previously mated males, and Byers' (1978) finding
that females of Euxoa messoria actively avoid remating with previous part-
ners. Both of these observations could be explained by mate choice on the
part of females to avoid previously mated males or by variation in male
Less direct evidence for female choice comes from observations of virgin
females actively rejecting conspecific males (Barrer and Hill 1977; Baker
and Carde 1979; Brower et al. 1965; Grant 1976; Pliske 1975; Rutowski
1978, 1979b). Rejection responses performed by virgins are varied and in-
clude (1) simply moving away, (2) assuming postures or performing dis-
plays that mechanically impede male attempts to couple, (3) initiating
special flight movements or patterns, and (4) doing nothing. These responses
are known to be elicited by performance of improper courtship sequences by
males (e.g. Baker and Carde 1979) and may be used to avoid matings with
males that are unattractive for other reasons as well. Future research
should compare males that are rejected by virgins with those that are ac-
cepted with respect to some of the traits discussed earlier.
From this literature survey, it is clear that studies explicitly examining
the occurrence of mate choice by females in the Lepidoptera are needed.
Specifically, these studies should include documentation of active discrimina-
tion by females among conspecific males on the basis of traits that vary
among males in naturally occurring populations, and demonstration that
females gain by engaging in these discriminations2
MALE CHOICE IN THE LEPIDOPTERA
Males cannot produce unlimited quantities of the secretions that are
passed to a female during copulation. This suggests that they might benefit
from discriminating among females and selecting as mates those that will
provide the greatest possible return on the investment passed to the female
during copulation. Among those traits that males might use to make sexual
choices are female size and age. Size is related to fecundity in a number of
butterflies and moths (Campbell 1962; Cook 1961; Marks 1976; Suzuki
1978) and so males might benefit from selectively mating with large females.
In addition, daily egg output decreases with age in a variety of lepidopterans
(Dunlap-Pianka et al. 1977; Gehring and Madsen 1963; Harvey 1977;
Labine 1968; Solomon and Neel 1974; Swier et al. 1976; Suzuki 1978).
Therefore, males might be expected to mate preferentially with young fe-
males because they have the greatest possible life expectancy and may be
Insect Behavioral Ecology-'81 Rutowski 77
less tattered and worn and thereby better able to locate and utilize oviposi-
tion sites and escape potential predators.
In the diurnal Lepidoptera visual cues are the most likely source of in-
formation about female size and age available to males. However, Gilbert
(1976) has shown that males discriminate among mated and unmated fe-
males using chemical cues, so this modality should not be dismissed. In
nocturnal species it is less clear what cues males might use to make such
discrimination. Perhaps the properties of the female's sex attractant pro-
vide information relevant to mate choice. The recently discovered importance
of trace components in the female's sex pheromone (Klun et al. 1979) sug-
gests the possibility of a fine-tuned discriminatory capability on the part of
the males which may play a role in mate selection. Lloyd (1981) proposed
that these trace components might be important in individual recognition of
females by males when they are confronted with convergent pheromone
plumes of several females. Recently, Ono (1980, 1981) has shown that the
tactile sensation of scales is important in eliciting copulatory attempts from
males of some moths. Assuming females lose scales as they age, this may
provide a mechanism for age discrimination by males.
There are several studies that indicate that males are sexually selective.
Because males are more active in initiating and maintaining courtship than
females, assays have been easier to design and as a result more is known of
their preferences with respect to courtship and mating partners. In the
gypsy moth (Porthetria dispar), males are less attracted to old virgins than
they are to young ones (Richerson et al. 1976). In addition, although small
females can be seen calling they do not attract males (Doane 1968). Rutow-
ski (in press) has shown that males of the checkered white butterflq (Pieris
protodice) spend more time courting large females than small individuals
and they also prefer young females to older ones. On the other hand, males
of the neotropical butterfly, Anartia fatima, have been shown (Emmel 1972,
1973; Taylor 1973) to focus their courtship attentions on females with
bands of white in their wings (old females) in preference to females with
bands of yellow (young females). The adaptive value of this preference is
Indirect evidence for male choice is seen when males leave virgin females
after a shorter-than-normal courtship (Brower et al. 1965; Pliske 1975;
Rutowski 1978, 1979a; Shapiro 1975; Shorey and Gaston 1964). In some
cases, males have even been seen leaving females that have assumed a re-
ceptive posture. These observations have been particularly common in males
that have recently mated (Rutowski 1979; Shorey and Gaston 1964) and
may reflect time budgeting in favor of nutrient acquisition when the returns
from mating are likely to be low because of the inability to produce a large
One of the primary interests of pragmatic entomologists is the monitor-
ing and control of populations of economically important insects. In recent
years increasing emphasis has been placed on exploiting the communication
systems of target insects to further these goals. It is clear that sexual selec-
tion, in particular the mate choice component of sexual selection, is likely
to have been an important force shaping the communication signals of the
Florida Entomologist 65 (1)
Lepidoptera. To date, the possibility that individual moths and butterflies
might vary in their ability to stimulate and attract members of the op-
posite sex has been ignored. To a large extent this has been because of tech-
nical difficulties that can now be overcome in analyzing individual differences
in the quantity and quality of pheromonal signals.
If such information were now to be collected there are two ways it could
potentially be utilized in biological control programs. First, if variation
among females is found in their attractants and thereby in their ability to
attract males, it may be possible to devise more effective synthetic lures or
confusion inducers than has previously been done. As a second line of attack,
it may be possible to permeate fields with chemicals mimicking the aphro-
disiacs of low quality males and further disrupt mating.
In short, evolutionary theory predicts that butterflies and moths may be
behaving in ways that are more complex than has been revealed by previous
investigations. Investigations into the behavior of the Lepidoptera guided
by sexual selection theory may provide pragmatic entomologists with new
weapons in their battle with insects.
Sexual selection theory predicts that female moths and butterflies should
be selective in their choice of mates, preferring those conspecific males with
traits that are correlated with "good" genes or those males that will impart
a large quantity of secretions during copulation that can later be used in
oogenesis or somatic maintenance. Because males are limited in their ability
to make these secretions they also should be selective in whom they court and
inseminate.3 Although explicit tests of these predictions are lacking and
needed, the available information suggests that females and males are be-
having in the ways predicted. It is expected that a thorough understanding
of sexual selection in the Lepidoptera may provide information useful to
pragmatic entomologists in their efforts to control and monitor populations
of pest insects.
I thank Dr. James Lloyd for inviting me to participate in this symposium
and Drs. John Alcock and Thomas Baker for their helpful comments on the
manuscript. This article was produced while I was supported by Grant No.
BNS 80-14120 from the National Science Foundation.
1If female butterflies prefer young males and if they recognize young
males by the lack of fading in their wing patterns, this might explain why
in sexually dimorphic species of butterflie? the males tend to have brighter
and more defined markings than the females. In essence, this argument sug-
gests the original adaptive basis for the female preference for brightly
colored males that Darwin originally suggested.
21 have not discussed the consequence of this choice for male behavior and
morphology but it should be kept in mind that as Fisher (1958) pointed out,
once female choice is established, a runaway process may be initiated in
which selection favors a male trait simply because it makes his offspring
more attractive to females, independent of the initial fitness benefits experi-
Insect Behavioral Ecology-'81 Rutowski
enced by females that selected males with this trait. This process has been
invoked by Baker and Carde (1979) to explaining many of the elaborate
scent-producing structures found in many moths and butterflies. Selection
may continue to favor female choice when its sole benefit is to maximize the
attractiveness of her male offspring.
3Mate choice should only be favored by selection in those ecological
circumstances in which the frequency of contacts with receptive members of
the opposite sex is high. Hence, those interested in studying sexual selection
in the Lepidoptera are advised to focus their attention on species with one
or more of the following characteristics: (1) population densities are high,
(2) adults are long-lived, and (3) adults form aggregations. With respect
to the later, many different types of aggregations have been reported in-
cluding all-male groups on hill tops (Shields, 1967), overwintering aggrega-
tions of monarch butterflies (Danaus plexippus) at which mating may be
common (Hill et al. 1976), and groups of adult male salt marsh caterpillars
(Estigmene acraea) in which one or more males has his coremata everted
(Mark Willis, personal communication).
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Insect Behavioral Ecology-'81 Greenstone
BALLOONING FREQUENCY AND HABITAT
PREDICTABILITY IN TWO WOLF SPIDER SPECIES
MATTHEW H. GREENSTONE*
The first evolutionary ecological treatments of terrestrial arthropod
migration appeared in the early 1960's (Johnson 1960; Kennedy 1961;
Southwood 1962). Since that time there has been a proliferation of studies
on the behavior, physiology, ecology and evolution of migration (see Dingle
1972, 1978, and 1980 for reviews). The insects, with their monopoly on true
flapping flight, spectacular mass migrations with seasonal returns (Urqu-
hart 1960; Hagen 1962; Rainey 1978), and status as crop pests, have re-
received the most attention. However, other groups of terrestrial arthropods
also migrate (Southwood 1962). The most impressive mass migations of
non-insect taxa are those of the spiders, which "balloon" on long buoyant
strands of silk. Episodes of such so-called aeronauticc behavior" are often
regional in scope and leave the countryside festooned with spent silken
"gossamer" (Comstock 1948).
The timing of migratory movements may correspond to climatic events.
For example in spiders aeronautic behavior peaks sharply during periods
of unseasonably warm and balmy weather which produces ideal conditions
for lifting the animals into swiftly moving air layers. However it is gen-
erally agreed that the tendency to migrate is a fixed rather than a faculta-
tive response to the immediate abiotic or biotic envrionment (Johnson 1960;
Kennedy 1961; Southwood 1962, 1977; Dingle 1972). The major selective
factor in the evolution of migratory behavior is presumed to be the pre-
dictability (defined below) of the habitat, with habitat unpredictability
favoring migratory behavior. If this "habitat predictability hypothesis" is
correct, the intensity or frequency of migratory behavior should decrease as
the predictability of the habitat increases.
In the only study of spiders that bears directly on the hypothesis, Richter
(1970) determined the ballooning frequencies of spiderlings of eight Dutch
species of the wolf spider genus Pardosa (Lycosidae) in relationship to
published information on the abundance (i.e., commonness) and "stability"
(both designated as low, intermediate, or high) of their typical habitats in
Britain. My analysis of his data indicates that ballooning frequency is sig-
nificantly inversely correlated with habitat abundance but not with habitat
stability'. Unfortunately his populations were not sampled from the habitats
described and there are uncertainties about the assignment of levels of
Concepts of stability and predictability'are central to various areas of
ecological theory but have only recently been rigorously defined. Predictabil-
*Matthew H. Grecnstone is an Assistant Research Scientist in the Department of En-
tomology and Nematology, University of Florida. The research reported here was performed
while he was a Lecturer in the Department of Ecology and Evolutionary Biology, University
of California, Irvine. His principal research interests include spider evolutionary ecology and
the application of serological methods to arthropod ecology. Current address: Department of
Entomology and Nematology, University of Florida, Gainesville, FL 32611.
Florida Agricultural Experiment Station Journal Series No. 3296.
Florida Entomologist 65(1)
ity may be thought of as comprising two components, constancy and con-
tingency (Colwell 1974), which are nicely illustrated by rainfall in Medi-
terranean climate regions. These regions are characterized by rainy winters
and largely rainless summers. In such areas rainfall has low constancy (be-
cause it doesn't always rain in all seasons) but fairly high contingency (be-
cause the presence and absence of rainfall are contingent on season, although
the exact month of onset or cessation of rains may vary from year to year).
Thus rainfall has moderate predictability in Mediterranean climates, with
constancy intermediate and contingency higher than for most other tem-
The predictability of rainfall is a major determinant of habitat pre-
dictability for some animals. Although all wolf spiders (Araneae: Lycosidae)
require free water for drinking (Parry 1954), differences in life style alter
the effect of rainfall on habitat predictability for the two species studied
here. Pardosa ramulosa (McCook) and Pardosa tuoba Chamberlin are
closely related species that are sympatric over much of their ranges in
California (Vogel 1970). P. ramulosa is highly specialized in both diet and
foraging mode, feeding on aquatic insects that it plucks from the surface of
standing water (Greenstone 1979, 1980). In the San Francisco Bay region,
which has a Mediterranean climate, it inhabits the banks of fresh- and salt-
water pools, some of them small, isolated, and seasonal. In the same region,
P. tuoba is found in extensive coastal prairie and scrub habitats, where it
feeds on terrestrial insects (Greenstone 1980). Because P. ramulosa requires
standing water, its habitats tend to be less predictable than those of P. tuoba,
to the extent that P. ramulosa has to retire from some habitats during the
dry season while P. tuoba can remain active throughout the year (Green-
stone 1980, Table 1).
The two species' habitats are in many cases adjacent and even nested
(Greenstone 1980), permitting a test of the habitat predictability hypothesis
in the absence of confounding climatic or other geographic variables. If the
hypothesis is correct P. ramulosa should have a higher ballooning frequency
than P. tuoba.
Egg-case-bearing females of both species were collected in April and
May of 1978, P. tuoba from coastal prairie habitats in Point Pinole Regional
Park and Jewel Meadow in Tilden Regional Park, and P. ramulosa from the
margins of pools in Point Pinole Regional Park, Jewel Meadow, and the
Petaluma Marsh (refer to Greenstone 1980 for complete habitat and locality
descriptions). The animals were maintained in the laboratory until the
spiderlings had hatched and dispersed from their backs. Each spiderling was
then transferred to its own 25 X 95 mm cotton-plugged shell vial, with
moisture provided by a distilled water-saturated cotton ball at the bottom
and a 3 mm diameter wooden applicator stick as a dry perch.
Ballooning behavior was assayed with an apparatus similar to that of
Richter (1967, 1970) (Fig. 1). Spiderlings were placed in groups of 4 or 5
on the tips of individual 5 mm diameter dowels in the air stream of a
variable speed electric fan directed upward at an angle of 45 degrees. Heat
and illumination were provided by a 250 watt incandescent lamp suspended
20 cm above the dowel tips, and temperature and wind speed were monitored
Insect Behavioral Ecology-'81 Greenstone
Fig. 1. Apparatus used in ballooning assays. Note thermocouple probe
among dowel tips and anemometer probe just to the right of the dowels.
Clock timer was used to time periods of wind and calm.
86 Florida Entomologist 65(1) March, 1982
with thermocouple and hot-wire anemometer probes mounted near the
spiderlings. All trials were run at a windspeed of 1.0 m/s and a temperature
of 27-280C, which are in the optimum range for other Pardosa species
(Richter 1970). Each animal was fed one adult vestigial-winged Drosophila
melanogaster before its ballooning trial.
Because intermittent air movements are more effective than continuous
ones in eliciting ballooning behavior in Pardosa species (Richter 1967), each
spider was observed during five 2-minute periods of wind separated by 1-
minute periods of calm. An animal was scored as a ballooner only if it
ballooned or exhibited "tip-toe" behavior, which normally precedes balloon-
ing (Richter 1970). Only second instar spiderlings (hatchlings) were tested
since they are more apt to balloon than older animals (Richter op. cit.).
Ninety-one P. tuoba and 285 P. ramulosa spiderlings were tested.
RESULTS AND DISCUSSION
The proportions of ballooners in the two species were .032 (3/91) for
P. tuoba and .098 (28/285) for P. ramulosa. These proportions are highly
significantly different (G = 22.638, p<<.001, log-likelihood ratio test, Sokal
and Rohlf 1969).
The results were in the expected direction and support the habitat pre-
dictability hypothesis. What are the broader implications of the results? On
a purely local level they may explain the absence of Pardosa tuoba from
Neil's Island, a collecting locality with typical P. tuoba habitat (Greenstone
1980, Table 1). Neil's Island is a true ecological island, comprising coastal
prairie, savannah and woodland habitats and entirely surrounded by
estuarine salt marsh. Since P. tuoba is never found in salt marsh, the only
way it could get to Neil's Island is by ballooning, which it does with low
frequency. Any arriving aeronaut would have to survive six or seven molts
to reach adulthood and locate a mate in order to reproduce. Furthermore
the relatively small size of the island may promote high extinction rates for
any populations that do manage to get established (MacArthur and Wilson
Ballooning, like other modes of arthropod migration, has broad theoretical
and practical implications.3 Both natural and managed habitats are distrib-
uted in time and space with varying degrees of predictability, and the ex-
istence of migration and diapause phenomena in terrestrial arthropods at-
tests to strong selection for tracking habitats in space and time. Because a
major aim of these symposia is the application of basic research to the solu-
tion of practical problems (Lloyd 1981) I shall confine my remaining re-
marks to a consideration of the possible practical implications of ballooning.
The relevance of ballooning to agriculture is evident given the variety of
spatial and temporal patterns in planting and harvest. Annual crops may
appear and disappear within and between regions with greater or lesser
spacing and regularity, while perennial crops tend by their nature to be more
predictable to their arthropod inhabitants (Ehler 1977). Though some
thought has been give to the movement of arthropod pests within this
habitat mosaic (Rabb and Kennedy 1979; Stimac 1982, this Symposium),
little has been given to the movement of their natural enemies. Spiders are
the most numerous and effective predators in some agricultural situations,
especially fruit orchards and rice fields (Kenmore 1980; Mansour et al.
Insect Behavioral Ecology-'81 Greenstone
1980; Kiritani 1976). Pest management schemes designed to disrupt pest
populations might also make it difficult for spiders to remain associated with
those populations. For example, the spacing or timing of crops might be
manipulated to discourage pest movements from field to field, or stubble
might be burned to destroy diapausing immature stages of the pest. In such
cases spider species from less predictable habitats with greater ballooning
frequencies could be artificially introduced. Alternatively, resident species
that are otherwise well-adapted to the pest and its habitat could be reared
in the laboratory, selected for higher ballooning frequency, and returned to
the field; lower-frequency ballooning populations could be selected for
perennial crops. This scheme is of course contingent on ballooning tendency
having high heritability, which is an implicit assumption of the habitat pre-
The quantitative study of ballooning is in its infancy. The only other
studies comparable to mine are those of Richter (1967, 1970), which also
involve wolf spiders. This is unfortunate because lycosids make up relatively
little of the aeronaut fauna, which is dominated by the Linyphiidae (Bris-
towe 1939; Duffey 1956). The linyphiids are unique, because with the ex-
ception of a few tiny species in other families (Horner 1974), they are the
only spiders small enough to balloon as adults as well as juveniles. This
means that they have survived most pre-reproductive mortality at the time
of ballooning and therefore have higher reproductive value and colonizing
potential than do juveniles (MacArthur and Wilson 1967). Since linyphiids
are known to be key predators in some crop systems (Kenmore 1980;
Yamanaka et al. 1972), knowledge of their ballooning biology may enable
us to raise their effectiveness as natural enemies, besides adding a new
dimension to our basic understanding of spider migration.
Spiders disperse by "ballooning" on long buoyant strands of silk. The
hypothesis that habitat unpredictability selects for high ballooning fre-
quencies of spiderlings was tested by comparing two wolf spider species with
populations in adjacent and nested Northern California habitats. Pardosa
tuoba is active throughout the year in coastal prairie and scrub habitats
where it feeds on terrestrial insects, while P. ramulosa is a specialist on
aquatic insects and requires open water to feed. Because the availability of
open water is somewhat unpredictable in Northern California, P. ramulosa
has a less predictable habitat than P. tuoba. P. ramulosa was found to have
the higher ballooning frequency, as predicted by the hypothesis. These re-
sults are relevant to a consideration of the role that spiders might play in
pest management schemes which make use of various spatial and temporal
'Abundance: rs = 0.844, p < .01; Stability: r, = 0.172, p > .10 (Spear-
man Rank Correlation Coefficient, Siegel 1956).
2Predictability and its components have been computed for coastal Cali-
fornia (Maiorana 1976) using 25 years of rainfall data, and show predicta-
bility and constancy lower than three subtropical to tropical and one tem-
88 Florida Entomologist 65(1) March, 1982
operate site, and contingency equivalent to that of a tropical site having
pronounced wet and dry seasons (Colwell 1974).
3Ballooning is not unique to spiders, being known also from various
Lepidopterous larvae, including forest pests such as Gypsy Moth (Portheria
dispar) (Leonard 1970) and Spruce Budworm (Choristoneura fumiferana)
(Wellington and Henson 1947).
I thank Jim Lloyd for his invitation to present this paper to the Insect
Behavioral Ecology Symposium, Mr. Christian Nelson of the East Bay
Regional Park District, Oakland, California, for permission to collect
spiders in the Regional Parks, and Mr. and Mrs. Lester Corda for permission
to collect on their property in the Petaluma Marsh. I also thank Steve
Arnold, Peter Kenmore, Jim Lloyd, John Lubina, and Tom Walker for com-
ments on various forms of this manuscript, and Peter Atsatt for essential
moral and material support. This work was supported by a Biomedical Re-
search Support Grant from the School of Biological Sciences, University of
BRISTOWE, W. S. 1939. The comity of spiders. Ray Society, London, England.
COLWELL, R. K. 1974. Predictability, constancy and contingency of periodic
phenomena. Ecology 55: 1148-1153.
COMSTOCK, J. H. 1948. The spider book. Cornel University Press, Ithaca,
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- 1978. Evolution of insect migration and diapause. Springer-Verlag,
1980. Ecology and evolution of migration. Pages 1-101 in S. A.
Gantreaux, Jr., ed. Animal migration, orientation and navigation.
Academic Press, New York.
DUFFEY, E. 1956. Aerial dispersal in a known spider population. J. Anim.
Ecol. 25: 85-111.
EHLER, L. E. 1977. Natural enemies of the cabbage looper on cotton in the
San Joaquin Valley. Hilgardia 45: 73-106.
GREENSTONE, M. H. 1979. Spider feeding behavior optimises dietary es-
sential amino acid composition. Nature 282: 501-503.
GREENSTONE, M. H. 1980. Contiguous allotopy in Pardosa ramulosa and
Pardosa tuoba (Araneae: Lycosidae) in the San Francisco Bay
region, and its implications for patterns of resource partitioning
within the genus. American Midl. Nat. 104: 305-311.
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Rev. Ent. 7: 289-326.
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dispersal by flight. Nature 186: 348-350.
KENMORE, P. E. 1980. Ecology and outbreaks of a tropical insect pest of
the Green Revolution, the Rice Brown Plant Hopper, Nilaparvata
lugens (Stal). Ph.D. Dissertation, Univ. of California, Berkeley.
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KIRITANI, K. 1976. Systems approach for management of rice pests. Proc.
XV Int. Congr. Ent. 1976 (1977). 591-598.
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lations of Portheria dispar (Lepidoptera: Lymantriidae). Canadian
Ent. 102: 239-249.
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coupling. Florida Ent. 64: 1-3.
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raphy. Princeton Univ. Press, Princeton, New Jersey.
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manders. Evolution 30: 599-613.
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spiders as biological control agents of Spodoptera littoralis larvae on
apple in Israel. Acta Oecol./Oecol. Applic. 1: 225-232.
PARRY, D. A. 1954. On the drinking of soil capillary water by spiders. J.
Exp. Biol. 31: 218-227.
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Carolina State Univ., Raleigh, North Carolina.
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proach. Pages 33-48 In H. Dingle, Ed., Evolution of insect migration
and diapause. Springer-Verlag, New York.
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species (Pardosa: Araneae: Lycosidae). Oecologia 5: 200-214.
SIEGEL, S. 1956. Nonparametric statistics. McGraw Hill, New York.
SOKAL, R. R., AND F. J. ROHLF. 1969. Biometry. Freeman, San Francisco.
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to habitat. Biol. Revs. Cambr. Phil. Soc. 37: 171-214.
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STIMAC, J. L. 1982. The relevance of behavioral ecology in models of insect
dynamics. Florida Ent. 65(1): 000-000.
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Toronto, Ontario, Canada.
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." . -."
^^-^!!--~ If '-'^
g ,,a _.!.,. k -,,m m. ,.
Florida Entomologist 65 (1)
EVOLUTIONARY SIGNIFICANCE OF PREDATION
ON SEXUALLY SIGNALLING MALES
"There are several very good reasons why courtship displays
should not exist at all. Firstly, they render the animal performing
them conspicuous, and therefore may attract predators. Secondly,
they are usually performed with such intensity that they not only
attract predators, but also claim the attention of the displaying
animal to such a degree as to make it particularly vulnerable to
attack from predators ..."
"Empirical evidence of increased mortality associated with inter-
sexual selection is uncommon."
(Gwynne & O'Neill 1980)
The male-female dichotomy has far-reaching implications. In most spe-
cies, females invest more heavily in offspring than males do. The factor
limiting a female's number of offspring is likely to be a resource affecting
how many eggs she can manufacture or safely deposit. For males, the lim-
iting factor is often simply the number of females impregnated. This dis-
parity has led to tremendous differences in mating behavior of the two sexes,
differences which have been discussed in a number of previous papers
(Trivers 1972, Thornhill 1980).
Compared to females, males vary widely in the number of offspring they
leave (Bateman 1948). For males, sex is an all-or-nothing, high stakes game,
where he who hesitates leaves few or no genes in the next generation. Selec-
tion favors male adaptations that lead to high reproductive success, such as
elaborate physical ornaments and conspicuous displays, even at the cost of
increased mortality (Fisher 1958, Trivers 1972). In this paper, I will ex-
amine what is possibly the most important mortality factor on sexually
active males, predation.
The importance of predation in the evolution of sexual behavior has been
somewhat unclear, as the two quotations given above indicate. I hope to
show that male-biased predation is both a common and an important factor
in the evolution of sexual behavior and communication.
CAUSES OF MALE-BIASED PREDATION
In this section, classes and some examples of male-biased predation are
given. Most of these concern insects, but where no clear insect examples have
been reported of a particular type of predation, relevant examples are given
from vertebrate literature. Examples are grouped into categories corre-
sponding to the causes of male vulnerability (Table 1). I have restricted
myself to heterospecific predation, including parasitoids as functionally
*Theodore Burk is a Postdoctoral Fellow employed through a cooperative agreement be-
tween the Insect Attractants, Behavior, and Basic Biology Research Laboratory, ARS, USDA
and the Department of Entomology and Nematology, University of Florida, Gainesville. He
obtained his D. Phil. in 1979 in the Animal Behavior Research Group, Oxford University,
where he was a Rhodes Scholar from Kansas. His research interests are in insect social be-
havior, especially aggressive behavior and acoustic communication.
Insect Behavioral Ecology-'81 Burk
TABLE 1. CAUSES OF MALE VULNERABILITY TO PREDATORS.
A. Active in open or conspicuous areas
B. Active at dangerous times
2. Spacing pattern
A. Clumped-economical to exploit
B. Regular-predictably encountered
4. Lack of accurate discrimination ("aggressive mimics")
5. Dangerous mating activities
6. Conspicuous displays
equivalent to predators. Cannibalism of males by females, reported in spiders
(Christenson and Goist 1979), mantids (Roeder 1963), ceratopogonid flies
(Downes 1978), and sphecid wasps (O'Neill and Evans 1981) could easily
fall into the general range of this paper but is not considered here.
One cause of male vulnerability to predation is the greater likelihood of
male activity in exposed areas or at high-risk times. The male mating
swarms of nematoceran Diptera and Ephemeroptera usually occur over
streams, in clearings, or adjacent to some conspicuous landmark (Downes
1969, Sullivan 1981). Such locations are found not only by receptive females,
but also by dragonflies, wasps, ceratopogonid and empidid flies, birds, and
bats (see references in Sullivan 1981). Downes (1970, 1978) has shown
that empidids and ceratopogonids respond to "swarm marker" topographical
features, hunting in appropriate spots even before prey males begin to
swarm. Big brown bats (Eptesicus fuscus) find likely areas by orienting to
the choruses of calling frogs or katydids, which occur in areas where other
insects are swarming (Buchler and Childs 1981).
Other male insects are also active for long periods in exposed locations.
Male Drosophila chase and court females on pieces of rotting fruit, where
they are vulnerable to predation by insectivorous birds (Spieth 1968). Davies
(1977) has shown that two British birds, the pied and gray wagtails,
specialize on various flies, especially dung flies (Scatophaga stercoraria),
whose males are present in large numbers on fresh dung pats.
Male insects may also be active at times when the risk of predation is
high. Female forest tent caterpillar moths (Malacosoma disstria) emerge
from cocoons and are receptive in early evenings. Male M. disstria must
search out and mate with newly emerging females before they are found by
competitors. This mate competition forces male moths to begin searching for
female cocoons during the daylight hours, and results in the capture of
many male moths by birds (Bieman 1980).
A second reason for male vulnerability lies in male spacing patterns. For
reasons discussed by Alexander (1975), displaying male insects often gather
into swarms or display groups. This clurmping may make it more eco-
nomically worthwhile for large predators to prey on displaying males. Bats
probably look for areas where insects are swarming because they are likely
to obtain high rates of energy intake with low searching and handling costs.
On the other hand, males that are regularly spaced throughout an area,
rather than aggregated into clumps, may also be vulnerable. Estes (1973)
has reported that male wildebeest are especially vulnerable to predation by
Florida Entomologist 65(1)
lions because their territorial fidelity results in regular male spacing. Lions
only move a short distance in any direction without encountering a territorial
male wildebeest, and male wildebeest are strongly attached to their territorial
sites and unwilling to flee from them.
Third, males may be less wary when involved in rigorous competition
with other males for mates. Nagamine and Ito (1980) reported on their
attempts to capture cicadas (Mogannia minute) that sometimes reach
epidemic proportions in sugarcane fields. In areas of low male density, with
few males calling, only about 60% of males could be captured. However, in
high density areas, where many males were calling, nearly 90% of males
could be captured. No such density differences in vulnerability were observed
in female cicadas. Schaller (1972) has given another example involving
lions and their prey: he observed male warthogs falling prey to lions be-
cause they were preoccupied with fights over access to females.
Fourth, males may become prey because they are not very rigorous in
the orientation of their sexual behavior. Selection against missing even re-
mote mating possibilities may lead males to court inappropriate objects.
Many male insects perch on vegetation and fly out to approach passing in-
sects of approximately the right size and shape; they then drive off con-
specific males and court females. Gwynne and O'Neill (1980) have described
the fate of male Philanthus wasps with this "perch-and-intercept" mating
strategy: many are eaten by passing robberfllies (Asilidae). (O'Neill and
Evans (1981) have also shown that female Philanthus hunt and eat inter-
cepting males.) Similarly, the prey of female Oxybelus sphecids are mainly
male flies with this type of mating strategy (Table 2) (Peckham and Hook
Lack of accurate discrimination accounts for the success of a small but
remarkable class of predators called "aggressive mimics." These predators
mimic females of a prey species in order to capture and eat unwary re-
sponding males. The cues used may be visual or chemical. Some species of
ceratopogonids have unusual abdominal appendages: these probably mimic
the cerci of mayflies, allowing these flies to enter mayfly swarms without
'Superscripts refer to notes in the appendix.
TABLE 2. MALE-BIASED PREDATION BY Oxybelus FEMALES (SPHECIDAE).
No. of prey
Species Males Females Prey
Oxybelus laetus 133 0 Calyptrate flies
0. packardi 55 1 Calyptrate flies
0. exclamans 16 0 Senotainia flies
0. subulatus 548 0 Therevid flies
0. subcornatus 568 0 Syrphid flies
0. uniglumis 429 7 11 Fly families
0. bipunctatus 787 5 14 Fly families
0. sparideus 80 16 Calyptrate flies
O. cressonii 37 1 Stratiomyid flies
et al. 1966, Kurczewski
References: Peckham and Hook 1980, Peckham et al. 1973, Bohart
Insect Behavioral Ecology-'81 Burk
provoking evasive maneuvers (Downes 1978). Bolas spiders (Mastophora
dizzydeani) catch flying moths with a sticky ball on the end of a silken
thread, resembling the bolas used by South American gauchos. Eberhard
(1977, 1980) showed that bolas spiders only capture male moths of a limited
range of species, by producing attractants that mimic the sex pheromones of
the female moths. Horton (1979) and Eberhard (1981) have provided other
examples of possible aggressive chemical mimicry. The best-studied case of
aggressive mimicry involves visual signals. Lloyd (1981) has made a series
of elegant studies of predation by female Photuris fireflies on males of other
firefly species. These "femmes fatales" answer the flashes of searching male
fireflies with appropriate flash responses, and eat the attracted males: they
have broken the "species-specific" flash codes of the prey species.2
The fifth category of male vulnerability includes species whose males are
required to perform dangerous precopulatory tasks. In many species of in-
sects, females only mate with males who provide them with a "nuptial gift"
of food, often a dead insect. Thornhill's (1978) study of scorpionflies showed
that such female-choice requirements lead males into danger. In two nuptial-
feeding species, one that hunts for prey to present to females (Panorpa sp.)
and another that robs prey from spider webs (Bittacus apicalis), males are
significantly more likely than females to be caught in spider webs. A third
species, Bittacus strigosus, is a natural control: no nuptial feeding occurs,
both males and females actively hunt for prey, and equal numbers fall prey
Sixth, predators and parasites may cue in on the conspicuous "calling
signals" or courtship displays of male insects. Such predators can be called
"signal interceptors." In insects, chemical, acoustic, and visual signals have
been most extensively studied, and signal interceptors have been found ex-
ploiting all three types.
Males of the Southern green stinkbug, Nezara viridula, produce a sex
pheromone that attracts female stinkbugs. Unfortunately for stinkbugs, it
also attracts a tachinid fly, Trichopoda pennipes, which oviposits on stinkbug
bodies (Harris and Todd 1980). Large numbers of stinkbugs fall victim: in
a Hawaiian population 64% of females and 71% of males (Mitchell and Mau
1971), in a Georgian population 35% of females and 44% of males (Todd
and Lewis 1976) were parasitized.
Male bark beetles of the genera Ips and Dendroctonus produce attractant
pheromones that not only attract other bark beetles (see Alcock, this sym-
posium), but also a wide variety of predators and parasites. These include
clerid and ostomid beetles, dolichopodid flies, and anthocorid bugs that prey
on adults and dipteran and hymenopteran parasitoids which attack im-
mature stages of bark beetles (Birch 1978, Dixon and Payne 1980, Greany
and Hagen 1981).
Females of several Photuris firefly species, previously mentioned as ag-
gressive mimics, are also visual signal interceptors (Lloyd and Wing ms.).
They fly after and catch flashing male fireflies; Lloyd and Wing were able
to attract Photuris females to a flashing light-emitting diode on the end of
a moving fishpole.
A recently discovered and exciting group of signal interceptors includes
those who respond to insect acoustic signals. Walker (1964) first noticed
housecats feeding on calling crickets and katydids. Subsequently, herons
Florida Entomologist 65(1)
TABLE 3. PARASITIZATION RATES OF Neoconocephalus trips BY Ormia linei-
Number Percent Number Percent
Month katydids parasitized katydids parasitized
A. Gainesville, FL
February 2 0
March 35 20 15 0
April 54 54 60 38
May 1 100
July 47 38 40 43
August 34 59 43 53
September 3 100 1 100
Total 173 45 162 40
B. Homestead, FL
June 9 89
July 11 91
August 10 90
September 9 89
Total 39 90
(Bell 1979) and spadefoot toads (Walker 1979) have been added to the list
of potential acoustically-orienting predators. Tuttle and Ryan (1981) have
shown that certain bats in tropical America cue in on the choruses of frogs:
J. J. Bellwood (pers. comm.) has demonstrated that at least four species of
neotropical bats are attracted to the calling songs of acoustic Orthoptera.
Insect parasites and parasitoids are also acoustic signal interceptors.
Corethrella flies locate and bite calling Hyla tree frogs (McKeever 1977).
A sarcophagid, Colcondamyia auditrix, parasitizes a cicada, Okanagana
rimosa, by orienting to cicada calling song and larvipositing on the cicada
(Soper et al. 1976).3
One tribe of tachinid flies, the Ormiini, are specialized acoustically-
orienting parasitoids of calling Orthoptera (Sabrosky 1953). Nutting (1953)
found that 72% of 18 calling Neoconocephalus robustus katydids collected on
Cape Cod were infested with the ormiine Euphasiopteryx brevicornis. Cade
(1975) demonstrated that E. ochracea orients to the calling song of a field
cricket, Gryllus integer, upon which it larviposits. Cade found parasitization
rates of calling males as high as 80%. I have been studying parasitization
of the katydid Neoconocephalus triops by another ormiine, Ormia lineifrons.
Like E. ochracea, 0. lineifrons can be attracted to tape recordings of its
host's calling song. In two widely separated areas in Florida, 0. lineifrons
takes a heavy toll of N. triops males. In Gainesville, N. triops is bivoltine;
in both generations parasitization of calling males is low early in the season
and high late in the season (Table 3a). In Homestead, 300 miles further
south, 0. trips is less seasonal and suffers very high parasitization for ex-
tended periods (Table 3b). 0. lineifrons larvae silence calling katydids in
about 5 days, killing them in 7-9 days. At times of heavy infestation, the