|
SHOMAS J. WALKEF
iOEPT. OF ENTOMOLCC
UNIVERSITY OF FLORID
'i:NESVILLE, FLA. 32F:
(ISSN 0015-4040)
FLORIDA ENTOMOLOGIST
(An International Journal for the Americas)
Volume 63, No. 1 March, 1980
TABLE OF CONTENTS
SYMPOSIUM: INSECT BEHAVIORAL ECOLOGY-'79
LLOYD, J. E.-Insect Behavioral Ecology: Coming of Age in Bionomics
or Compleat Biologists Have Revolutions Too ..................---- 1
THORNHILL, R.-Competitive, Charming Males and Choosy Females:
Was Darwin Correct? .- ............-- ..-----..--------- 5
CADE, W.-Alternative Male Reproductive Behaviors .................- 30
FORREST, T. G.-Phonotaxis in Mole Crickets: Its Reproductive Signif-
icance ...... .- - ----.........-- -------.- ... 45
BROCKMANN, H. J.-Diversity in the Nesting Behavior of Mud-daubers
(Trypoxylon politum Say: Sphecidae) .-----.. -- -... ..- ...------... 53
SMITH, R. L.-Evolution of Exclusive Postcopulatory Paternal Care in
the Insects ....-...... ........ .. ....... -------- --- ----- 65
WALKER, T. J.-Migrating Lepidoptera: Are Butterflies Better Than
Moths? -....-- .............-----------.---.... 79
SIVINSKI, J.-Sexual Selection and Insect Sperm ...... .. ----- 99
---- ^ -- -e-----L-^
LOVESTRAND, S. A., AND J. B. BEAVERS-Effect of Diflubenzuron on Four
Species of Weevils Attacking Citrus in Florida --------------------_ 112
MA EN-PEI, AND YUAN YI-LAN-The Genus Pentamerismus from
China (Acari: Tenuipalpidae) ..........-------------------_ 116
MA EN-PEI, AND YUAN YI-LAN-Four New Species of the Genus
Tenuipalpus from China (Acari: Tenuipalpidae) ..----------- 118
MUCHMORE, W. B.-Pseudoscorpions from Florida and the Caribbean
Area. 10. New Mexobisium Species from Cuba ....----- ... .....-.. 123
KNAUSENBERGER, W. I., AND W. W. WIRTH-A New Species of Macro-
peza (Diptera: Ceratopogonidae) with Biological Notes on the
Genus ....--- ... .. -....-.. ...-...-.. -....-- --- .......... .......... 127
ASHLEY, T. R., E. R. MITCHELL, N. C. LEPPLA, AND E. E. GRISSELL-
Parasites Attacking Fall Armyworm Larvae, Spodoptera frugi-
perda, in Late Planted Field Corn .--.---.-.-.------ ...--........-.. 136
WILKINSON, R. C., A. P. BHATKAR, W. H. WHITCOMB, AND W. J. KLOFT
-Formica integra (Hymenoptera: Formicidae) 3. Trial Intro-
duction into Florida ..----.. ...-... ---. --.----- ...-...-...- 142
Continued on Back Cover
Published by The Florida Entomological Society
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._ E. C. Beck
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This issue mailed April 30, 1980
Insect Behavioral Ecology-'79
Introduction
INSECT BEHAVIORAL ECOLOGY:
COMING OF AGE IN BIONOMICS
OR
COMPLEAT BIOLOGISTS HAVE REVOLUTIONS TOO1
JAMES E. LLOYD
Department of Entomology and Nematology
University of Florida
Gainesville, FL 32611
"You could feel the presence of nineteenth-century museum directors
engaged, in their frock coats, in goniometrie and craniologie, busily
collecting and measuring everything, in the pious hope that mere
quantification would lead to understanding."
(Sagan 1979)
A little more than a year ago I had never heard of the expression be-
havioral ecology. I had at that time concluded, after years of not fitting into
any of the nominate subdisciplines of biology, that I had more in common
with whooping cranes than cattle egrets. Upon discovering a symposium vol-
ume entitled Behavioral Ecology (Krebs and Davies 1978) I knew that my
combination of biological interests was not a sterile chimera, or at least I
was not alone.
Behavioral ecology is a hybrid. According to Wilbur (1979) it happened
this way: Ecology and genetics began hybridizing almost a half century ago,
and then ecological genetics backcrossed with ecology. The result, population
biology, began progressive introgression into ethology during the past decade,
resulting in what some call sociobiology. What others have called the latter
should not be printed here, but sociobiology and behavioral ecology are about
the same. I find 2 noteworthy distinctions: In behavioral ecology one is not
expected to have an academic or theoretical opinion on human sexual be-
havior; and secondly, one need not admire or even profess interest in social
Hymenoptera. Wilbur's geneology for behavioral ecology may be historically
correct, but had Darwin been properly introduced to Mendel's replicators the
path would have been direct.
As a recognized subject area, behavioral ecology was born during an
incredibly exuberant theoretical period spermed on by George Williams'
(1966) critique of the then "current evolutionary thought." It is now enter-
ing an intensive animal-watching, hypothesis-testing phase, in the true
and best tradition of Darwin's hypothetico-deductive method (Ghiselin
1969). A revolution, ultimately of more import than those following dis-
covery of background-microwave-radiation by astrophysicists and helical
molecules by biochemists, and it is ours!
With their extensive knowledge of their animals and hard comparative
'University of Florida Agricultural Experiment Stations Journal Series No. 2178.
Florida Entomologist 63(1)
data from years of work, and from being specialists on the most bountiful,
ubiquitous, diverse, versatile, and neatly-tuned subjects that exist, entomol-
ogists have the opportunity to dominate the field. Their professional employ-
ment in what often amounts to applied insect behavioral ecology, provides
unique and enviable physical and technical advantages. This can be the
decade of the insect, and it can continue our current compensation for past
leadership and domination of theoretical biology by patrons of an ossified
aristocracy.
Behavioral ecology's most distinctive mark is the central position natural
selection theory plays in the interpretation and analysis of animal (and
plant) outdoor behavior, this theory having been correctly termed biology's
cogent paradigm (Barash 1977). A critic may ask, "But is not selective
thinking simply your current cogent paradigm? Won't it too pass and be
replaced like Lamarckism and mutationism in their time?" When selective
thinking is replaced it will be because of the ascendency of theory that it
itself has birthed. The midwives will be behavioral ecologists. Biologists may
have taken a long time to apply the same logic to their subjects that their
cultural antecedents did when they manipulated the heredity of hunting
hounds and fighting crickets, but selective thinking is the real Solomon's
Ring, and it will endure in some form.
In the insect bionomics business selective thinking makes predictions
(induces hypotheses) as to what should and should not be expected to occur
in biological systems. In agriculture it could even be called long-term-insect-
management thinking, or insect-management-thinking for tomorrow. Selec-
tive thinking would have predicted that resistance was likely in barn flies of
the fifties, and that screwworms raised in warm factories might not be
competitive on cool country mornings in Texas (Bush 1978), or that females
will eventually discriminate against sterile males, turning on only to wild
ones.
For practical purposes we need not worry if selection theory is "real
fact" any more than the chemist worries whether his Haworth molecular
model reflects a Universal truth. Pragmatism is as fundamental to behavioral
ecology as it is to applied entomology. The latter is practical in its purpose
and choice of goals and problems, the former in its methodology and termi-
nology. Behavioral ecology takes natural selection for granted, leaving the
fretting over old arguments, and the making of new ones from them, to
taxonomic nomenclaturists and philosophers. We don't need to prove natural
selection anymore (see Maynard Smith 1978). Consequently, we expect or-
ganisms to be adapted. When an insect is seen doing something, apply a
"unified-field-optimality-theory": More often than not when you observe an
insect in the field, what it is doing at the moment is the best thing it can
possibly be doing at that moment for maximizing its long-run reproduction.
I would not bet against adaptation with my own money. (However, I insist
on evidence that a biologist really knows what the organism is actually doing
-what the adaptation is. This, and not adaptation has been and continues to
be the real question.) As a null hypothesis, and the adaptationist's equivalent
of the geneticist's Hardy-Weinberg Law, an organism can even be presumed
to be perfectly adapted. With knowledge of organisms, biological economics,
and engineering, the approach can then be to prove otherwise, quantify, re-
evaluate, and begin afresh.
March 1980
Insect Behavioral Ecology-'79
Two features of behavioral ecology may deter or distress, and they re-
quire some explanation. Behavioral ecology employs models-word models,
game models, mathematical models-it even seems to substitute them for
reality in absurd oversimplifications. These are but conceptual tools intended
to cope with an unreasonable, indescribable, natural world. A model may
provide a point of view that is totally new, and permit escape from past
prejudices that have become dead ends. Consider, for example, the sequence
2 3 6 7 1 9 4 5 8. What is the rule that orders these numbers? . The rule
and its execution are elementary (first grade), but who would think of a
numerical arrangement being alphabetical? Now when I present the numer-
ical sequence 1 6 2 4 8 5 7 3 2 you have numerical and alphabetical solutions
in mind, and are probably looking for some totally different perspective as
well.
A second criticism concerns terminology and mode of expression. Teleol-
ogy and anthropomorphism appear rife. Bees not only have sisters, cousins
and nieces, but crickets and digger wasps have strategies, a bug demands,
like some errant macho Californian, proof of his fatherhood before paying
out paternity benefits, and rapists and transvestites are described from
Mecoptera. Insects sometime seem to have been endowed with human cogni-
tive power, and scientific papers seem to read like awardees from "a worst
from Reader's Digest" contest. This is but time- and space-saving shorthand,
and fun. In the recent past, the avoidance of such mild (but technically ex-
travagant) expression has been a fetish in biology. Perhaps because of
earlier sins behaviorists have felt they needed purity of expression to main-
tain scientific credibility and dignity. Perhaps they had little else they could
be sure of in their investigation of behavior and they made the most of what
they had. Or, perhaps because they focused on proximate problems, not
evolutionary ones that were remote from wiring and machinery, such ac-
curacy was imperative. It really makes no difference anymore. The alterna-
tive to this verbal economy is coinage of new terms (=jargon and profes-
sional isolation) with definitions specifying that each applies to organisms
other than man, and frequent and drawn-out explanations in the passive
voice of selective pressures and how ancestors succeeded and others failed
resulting in allelic substitutions and p and q changes, etc., etc., etc ..... Mis-
understanding resulting from present laxity is among the least of a student's
worries. What harm is done if I speak of a firefly thinking, or blowing his
little mind? If a reader can't translate, and tell from text what the long
story is, then the problem is not one of diction, and it runs too deeply
to be bridged in an extra sentence or word substitution. Catching an author
in a conceptual error of substance is more productive and enjoyable, and has
greater reward, than complaining that he speaks of his insects with terms
appropriate to little people. Perhaps he has found that his flies are more
agreeable than most people, and seem, more often, to know what they are
about.
The members of this Symposium are among the most energetic, interest-
ing, and cooperative biologists that a moderator/editor could hope to work
with, and I thank them for making my part so easy and enjoyable. Some
travelled considerable distance at their own expense to present their invita-
tional papers at the Society's annual meeting, and Entomology at large is
the beneficiary. Their collective effort is a stimulating and significant con-
Florida Entomologist 63(1)
tribution for the instruction of all entomologists from 4-H to Professor
Emeritus rank, and will perhaps stimulate others to produce such mini-texts.
These papers were written to be read with ease by any scientist or educated
layman, and technical details and asides have, for the most part, been placed
in appended notes.
At the annual fall meeting of the Society in 1980 another symposium on
insect behavioral ecology will be presented.
Each participant has paper-bound copies of the entire Symposium for
distribution, and persons wanting a copy of all papers need ask but one par-
ticipant. Each has separates of his own paper.
I thank the Executive Committee and the Program Committee of the
Society for their enthusiastic cooperation, guidance, and financial support. I
also thank various individuals for reviewing and making helpful suggestions
on manuscripts. I especially wish to thank Norm Leppla, Carol Musgrave
Sutherland, John Sivinski, Tom Walker, and Dan Wojcik.
LITERATURE CITED
BARASH, D. P. 1977. Sociobiology and behavior. Elsevier North-Holland,
New York, NY. 378 p.
BUSH, G. L. 1978. Planning a rational quality control program for the
screwworm fly. Pages 37-47 in The screwworm problem, R. H. Rich-
ardson, Ed. Univ. Texas, Austin, TX. 151 p.
GHISELIN, M. T. 1969. The triumph of the Darwinian method. Univ. Calif.,
Berkeley, CA. 287 p.
KREBS, J. R., AND N. B. DAVIES. 1978. Behavioral ecology. Sinauer Assoc.,
Sunderland, MA. 494 p.
MAYNARD SMITH, J. 1978. Optimization theory in evolution. Ann. Rev. Ecol.
Syst. 9: 31-56.
SAGAN, C. 1979. Broca's brain. Random House, New York, NY. 347 p.
WILBUR, H. M. 1979. (Book review for) Behavioral ecology, by J. R. Krebs,
and N. B. Davies. Science 205: 781.
WILLIAMS, G. C. 1966. Adaptation and natural selection. Princeton Univ.,
Princeton, NJ. 307 p.
March 1980
Insect Behavioral Ecology-'79 5
SYMPOSIUM PARTICIPANTS
From left: R. L. Smith, T. G. Forrest, J. Sivinski, H. J. Brockmann, J. E.
Lloyd, R. Thornhill, T. J. Walker, and W. H. Cade. Photograph by Dr. F. W.
Mead.
COMPETITIVE, CHARMING MALES AND
CHOOSY FEMALES: WAS DARWIN CORRECT?'
RANDY THORNHILL
Department of Biology
University of New Mexico
Albuquerque, NM 87131 USA
". it has been said by several critics that when I found that many
details of structure in man could not' be explained through natural
selection, I invented sexual selection; I gave, however, a tolerably clear
sketch of this principle in the first edition of the 'Origin of Species,'
and I there stated that it was applicable to man. This subject of
sexual selection has been treated at full length in the present work,
simply because an opportunity was here first afforded me . My con-
viction of the power of sexual selection remains unshaken . When
'This and subsequent superscript numbers refer to notes in an appendix, p. 19.
Florida Entomologist 63(1)
March 1980
naturalists have become familiar with the idea of sexual selection, it
will, as I believe, be much more largely accepted; and it has already
been fully and favorably received by several capable judges" (C. Dar-
win, 1874, Preface to Second Edition of The Descent of Man and Selec-
tion in Relation to Sex) (emphasis added).
Darwin's theory of sexual selection was outlined briefly in On the Origin
of Species in 1859. In The Descent of Man and Selection in Relation to Sex
(1871) Darwin expanded and documented his theory. He provided support
and arguments for sexual selection as the evolutionary force behind many
sexual characteristics of animals, including many sexual and racial differ-
ences in humans. Darwin pointed out the distinction between characteristics
promoting survival and those promoting reproduction. He viewed the char-
acteristics promoting reproduction as often contrary to survival but main-
tained by sexual selection because the benefit of the traits in reproduction
could exceed their cost in survival to the individual. Darwin felt that the
elaborate and often bizarre plumages of birds, the horn-like projections of
deer and some insects, and many other traits could best be explained in terms
of benefit to an individual's reproduction exceeding costs to an individual's
survival. The reproductive benefits associated with most secondary sexual
features, Darwin reasoned, were related to winning in the competition among
males for females and in coaxing females to mate.2
Darwin's theory of sexual selection was severely criticized by the capable
theoretician A. R. Wallace (1889). Wallace believed that the more elaborate
colors and morphologies of many male animals relative to females of the
same species evolved by natural selection rather than sexual selection. He
felt sexual differences function in mimicry, warning or protection, and spe-
cies and mate recognition. Huxley (1938, 1963) was an important later critic
of sexual selection. He felt that the term sexual selection should be replaced
(1938) and that sexual selection is less important than natural selection in
bringing about evolutionary change because selection operates primarily by
means of differential survival of individuals to maturity (1963: xviii-xix).
Mayr (1972) expressed the view that sexual selection has been a very useful
principle for analysis and prediction of sexual differences in animals. Otte
(1979) recently wrote that a distinct separation of sexual selection from
natural selection is without merit.3 Why was Darwin so convinced of "the
power" and ultimate wide acceptance of his theory of sexual selection? Sex-
ual selection has some features that are not components of natural selection
(West-Eberhard 1979a). It is important to distinguish 2 features to under-
stand the potency of sexual selection relative to natural selection. The first
feature is the absence of a definite limit to reproductive returns for indi-
viduals associated with a trait evolving by sexual selection. The second
feature is related to the first and is that male-male and male-female inter-
actions represent coevolutionary races. Darwin was aware of these features
and this provided the basis of his unyielding position on sexual selection
despite criticism.
These 2 features are fundamental to a broader category of selection
called social selection, a very useful category to distinguish.4 West-Eberhard
(1979a) has provided an analysis of the unique features of social selection
in terms of social behavior in general. In this paper I will discuss some of
West-Eberhard's (1979a) points as they relate to traits evolved by Dar-
Insect Behavioral Ecology-'79
winian sexual selection, i.e. traits selected because they allowed individuals
better access to superior mates. Such access may involve winning in male-
male competition and/or being chosen by females. The discussion focuses on
sexually-selected insectan features. The topics often associated with sexual
competition that related to this discussion are: 1) distinct differences in
reproductive success of individuals within populations, 2) divergence of
characters under selection, 3) the reduction of genetic variation underlying
sexual traits, 4) the weak relationship between the fitness of parents and
offspring, and 5) the relationship between sexual selection and nongenetic
differences between individuals.
ALTERNATIVE SPECIALIZATIONS AND
DIFFERENCES IN INDIVIDUAL REPRODUCTIVE SUCCESS
Darwin (1871) documented that sexual selection is a potent means by
which successfully reproducing individuals are determined through direct
competition. As evidence he cited the observable fights and ritualized ag-
gression and displays found in many animals. Unsuccessful individuals often
have their chances for reproduction significantly reduced or eliminated com-
pletely (see Darwin 1871, Wynne-Edwards 1962, Alexander 1974, Wilson
1975, West-Eberhard 1975, 1979a, papers in Blum and Blum 1979). It is
assumed that ritualized interaction during aggression and display evolved
because further escalation was unprofitable in terms of reproduction and
most social animals have alternatives to winning an individual sexual or
aggressive interaction. Social interactions clearly function as a means by
which individuals assess the capabilities of other individuals relative to their
own and "decide" on alternative ploys for reproduction (Parker 1974, West-
Eberhard 1979a). An animal can wait for a situation that more likely will
result in winning a social encounter, i.e., in dominating a competitor or being
chosen as a mate by a femaless. Also, the loser of a particular social inter-
action can adopt an alternative specialization or strategy other than wait-
ing (Parker 1974, Alcock 1979a, Ligon and Ligon 1978, Ligon in press, West-
Eberhard 1979a, 1979b). In the absence of alternatives an animal should
fight to the death, because death and losing in social contests without al-
ternatives are equal genetically. An alternative specialization is an alterna-
tive route to reproduction that is expected to be less successful than winning,
but more profitable than continuing conflict and direct competition at a par-
ticular time.5
For a long time we have known that males in some insect species show
considerable morphological variation in body size and size of structures like
horns and mandibles presumed to be associated with fighting (Darwin 1871).
Recently, studies have shown considerable variation in male behavior within
insect species and in some cases the behavioral variation has been related to
morphological variation. Detailed studies of variation in male mating be-
havior have been conducted on a dungfly, Scatophaga stercoraria L. (Parker
1970, 1979 and references therein, Borgia 1979), some wasps and bees
(Alcock et al. 1977, Alcock 1979a and references therein, Evans and O'Neill
1978, Hamilton 1979), grasshoppers (Otte 1972 and references therein),
crickets (Cade 1979 and references therein), fireflies (Lloyd 1979a and ref-
erences therein), other beetles (Eberhard 1979 and references therein, also
Florida Entomologist 63(1)
March 1980
see Otte and Stayman 1979, Hamilton 1979), and scorpionflies (Thornhill
1979a, 1979b, in press a).
Studies of the resource-based mating system of Panorpa scorpionflies
allow understanding of the costs and benefits of alternative strategies em-
ployed by winners and losers in sexual competition. Male Panorpa have 3
distinct behaviors leading to copulation. First, a male may disperse a long
distance pheromone while standing adjacent to a dead arthropod he had
found in the habitat. A female attracted to the pheromone feeds on the dead
arthropod during copulation. Second, a male may disperse pheromone from
the vicinity of a hard salivary mass that he secretes on the substrate and
upon which an attracted female will feed during copulation. In each of these
2 cases, males vigorously display to attracted females and aggressively de-
fend dead insects and salivary masses from other males that attempt to take
them. The third behavior employed by males is rape (Thornhill 1979a, in
press a, in press b).
Males of most species of Panorpa that I have studied have well-developed
salivary glands and may secrete salivary masses to feed females during
copulation. Males of all of these species sometimes feed females dead insects
during copulation. Nocturnal and crepuscular mating is typical of Panorpa,
which makes field observations difficult. However, I have observed rape in
nature in 7 species of Panorpa. Males of most of the species I have studied
exhibit rape in the laboratory.
A rape attempt involves a male without a nuptial offering (i.e., dead
insect or salivary mass) rushing toward a passing female and lashing out
his mobile abdomen at her. On the end of the abdomen is a large, muscular
genital bulb with a terminal pair of genital claspers. If the male successfully
grasps a leg or wing of the female with his genital claspers, he slowly at-
tempts to re-position the female. He then secures the anterior edge of the
female's right forewing in the notal organ, a clamp-like structure formed
from parts of the dorsum of the male's third and fourth abdominal seg-
ments. Females flee from males without nuptial offerings. If grasped by
such a male's genital claspers, females fight vigorously to escape. When the
female's wings are secured, the male attempts to grasp the genitalia of the
female with his genital claspers. The female attempts to keep her abdominal
tip away from the male's probing claspers. The male retains hold of the
female's wing with the notal organ during copulation, which may last a few
hours in some species. The insemination success by rapists is lower (11% of
attempts) than that of males with dead arthropods as nuptial offerings
(100%).
The behavior of females toward males with and without a nuptial offer-
ing is quite different. Females flee from males that approach them without
a nuptial offering; however, females approach males with nuptial offerings.
Also, females struggle to escape from the grasp of rapists, but females do
not resist coupling by the notal organ of males with nuptial offerings.
The fertilization rate of ejaculates of Panorpa rapists is unknown. Fe-
male Panorpa have been observed to mate twice in a day and up to 5 times in
a week. Data on ejaculate competition between males are unavailable for
Panorpa. However, an important generalization in insect reproductive be-
havior, supported by a large amount of comparative data, is that the last
male to mate with a female in a multiple-mating species fertilizes most of
Insect Behavioral Ecology-'79
the eggs that the female lays until she mates again (Parker 1970). If this
is the case in Panorpa, a successful rapist may obtain a fertilization rate
similar to a male that feeds a female a nuptial offering.
Panorpa males can apparently distinguish size of dead insects because
male aggression is most intense around large dead insects. Once in posses-
sion of a dead insect, males initiate pheromone emission to attract a female.
The female feeds on the dead insect during copulation. Males aggressively
excluded from dead insects by other males tend to adopt the behavior of
using salivary secretions as nuptial offerings; when salivary secretion is no
longer possible because of previous use of salivary masses in nuptial feed-
ing, males attempt rape.
Panorpa male behavior is directed by female preference of males. The
copulatory success of males possessing large dead insects is greater than
that of males guarding small dead insects. Also, males using dead insects as
nuptial gifts attract more females for copulation than males using salivary
masses, and males using salivary masses have a greater copulatory success
than rapists.
Although successful rape (i.e. including insemination) may be infre-
quent, it is an appropriate behavior for a male to adopt when he is aggres-
sively excluded from possession of a dead insect and his salivary secreting
abilities are exhausted. The fitness potentially gained by a Panorpa rapist is
understood when the behavior of these insects is coupled with their ecolog-
ical setting. A 5-year study of the 9 species of Panorpa in southeastern
Michigan reveals that the species overlap almost completely in their feeding
ecology and that dead insects are a limiting resource for these insects.
Panorpa compete primarily in an interference manner through intense intra-
and interspecific aggression around food. Competition for food influences the
fitness of competing Panorpa, since increased competition results in increased
movement and reduced adult longevity in these insects under natural condi-
tions (Thornhill in press c). A selective history involving competition for
food accounts for the evolution of the risky Panorpa behavior of feeding on
dead insects in the webs of spiders. About 25% of Panorpa foraging is in
spider webs, and web-building spiders cause 65% of adult Panorpa mortality.
The predation of Panorpa by web-building spiders is significantly male-
biased despite adult Panorpa sex ratios near unity. This bias is apparently
due to risky male behavior associated with obtaining a dead insect or feed-
ing in order to produce salivary masses for copulation (Thornhill 1975,
1978a). A Panorpa rapist need not incur these risks and thus rape results
in increased survival for the rapist.
If rapists avoid risks associated with obtaining food for copulation, why
do not all males use rape as their primary behavior? The answer must be
related to the greater fitness gained by males that feed females nuptial
offerings of dead insects or salivary masses. Male bittacid scorpionflies that
feed females large insects during copulation gain reproductive success be-
cause their mates lay more eggs and females prefer mates with large insects
(Thornhill 1976a, 1976b). That female fecundity may be related to quantity
or quality of nuptial offering in Panorpa is suggested by female preference
for males possessing large dead insects. In addition, male Panorpa using
nuptial feeding behavior may reduce the amount of subsequent feeding and
movement by their mates and thus reduce chances of mortality from web-
Florida Entomologist 63(1)
building spiders during the time females are laying eggs they have fertil-
ized. Since food is limited, and feeding is necessary for a female to experi-
ence high fecundity, rape is detrimental to females because during rape a
female is removed from activities associated with obtaining food. Also, the
struggling to escape from rapists by females suggests rape may reduce the
likelihood that a female can later obtain a resource-providing male. That is,
raped females may be detected and discriminated against to some extent by
males with nuptial offerings.
Yet another alternative specialization has been observed in studies of
Hymenoptera and Orthoptera. In some species apparently subordinate males
adopt "satellite" behavior.6 Cade (1979) investigated the costs and benefits
associated with this form of alternative specialization in field crickets. He
found noncalling (satellite) (? = subordinate) and calling males in the
same population of field crickets. Noncalling males position around a calling
male and intercept females attracted by the call. The calling males get more
matings than noncalling males, but silence in the later males results in less
exposure to parasitic flies that track cricket hosts acoustically.
Other examples of variable male mating behavior include pseudofemale
behavior in fireflies (Lloyd 1979a) and scorpionflies (Thornhill 1979b) and
fighting males and nonfighting males in some species of Hymenoptera and
beetles. The fighting vs. nonfighting alternatives are often associated with
specialized morphological variation in wingedness and horn and mandibular
structure, and in some cases the costs and benefits of the alternatives are
partially understood (Alcock et al. 1977, Alcock 1979a, Hamilton 1979). The
advantage of male size in fighting has been documented by Alcock et al.
(1977) for Centris bees in which variation in male size is related to varia-
tion in copulatory success. I will return to the evolution of alternative spe-
cializations after a discussion of other features of sexual selection.
The outcomes of competition for mates and of indirect reproductive com-
petition are quite different in terms of their influence on traits with con-
tinuous variation (West-Eberhard 1979a). Sexual selection (and social se-
lection in general) acting on behavioral and/or morphological variation may
often have a "stepped" effect on the reproductive success of individuals in a
population. When this occurs, the population will be divided into 2 or more
distinct reproductive categories, depending upon the extent of sexual selec-
tion. Under intense sexual selection as seen in highly polygynous animals
(e.g. lekking birds, mammals, and some insects; see Alexander 1975), 2
categories of individuals may emerge from the competition: highly success-
ful and non-reproductive. Under most circumstances, however, there are
categories of reproductive individuals between these 2 extremes. However,
the "stepped" effect on the reproductive success of individuals in a popula-
tion remains apparent and often there may be considerable difference in
reproductive success between individuals found on different "steps." The
losers in initial competition for high rBproductive success are predicted to
adopt alternative specializations in order to gain some reproduction. As
discussed in a later section, the "stepped" effect on reproductive success has
important consequences for understanding heritable variation in relation to
alternative specializations and female choice.
March 1980
Insect Behavioral Ecology-'79
THE EVOLUTION OF ELABORATENESS
Darwin created sexual selection theory in part to explain certain elab-
orate morphologies and displays. Indeed, sexual selection has often been
treated as different from natural selection because the former is often felt
to lead to elaborateness in male traits (Darwin 1871, Fisher 1930, Otte 1979,
West-Eberhard 1979a). Under sexual selection, elaborateness may evolve
because 1) of the lack of a definite upper limit to reproductive return to
individuals from traits important in sexual competition, 2) male-female
and male-male interactions coevolve and a trait typically can be countered
by a more adaptive modification, and 3) female choice can lead to "runaway"
evolution (Fisher 1930) of traits (West-Eberhard 1979a).
UPPER LIMITS TO SELECTION AND COEVOLUTION: Darwin (1874) used a com-
parison of limits to evolution under sexual and natural selection as an im-
portant way for distinguishing these 2 forms of differential reproduction
(West-Eberhard 1979a).7 This difference between natural and sexual selec-
tion that Darwin envisioned is fundamental to understanding the relative
potency of these 2 forms of selection (West-Eberhard 1979a). Darwin felt
natural selection could change a trait to a point at which further change
would result in only negligible reproductive returns for an individual. At
each step in the evolution of a trait under natural selection, individuals
received less and less reproductive success from the modification until the
"upper limit" is reached and the returns are so small that further evolution
stops. There is no definite upper limit to change in a trait evolving in the
context of sexual selection. The reproductive returns for a better trait as-
sociated with sexual competition, regardless of how minor the change, need
not decline. The only factor limiting the degree to which sexual selection can
elaborate a trait are constraints associated with selection in the context of
natural selection as recognized by Darwin.8
The absence of a decreasing reproductive return from a better trait in
sexual competition is clearly illustrated by the coevolutionary aspect of the
battle within the sexes (West-Eberhard 1979a). In general, any new ability
in relation to sexual competition that arises can effectively be countered by
an ability that confers more reproductive return. An individual's sexual en-
vironment evolves back, unlike an individual's nonsocial environment. A
tactic favored by sexual selection will spread until a better tactic arises and
so on.
The often bizarre morphological and behavioral features of many male
insects are indicative of the lack of a definite upper limit to adaptive return
associated with improvement for coping with a competitive and coevolving
sexual environment. Female-mimicking male scorpionflies (Thornhill 1979b),
abdominal clamps in male scorpionflies for holding females during rape
(Thornhill in press a), penis structure in male damselflies for removing
sperm deposited by competing males in the'spermatheca of females (Waage
1979), male mating swarms and aggregations in a variety of insects (Alex-
ander 1975, Thornhill in press d), the injection of confusing flashes into the
flash patterns of other males by fireflies (Lloyd 1979a, 1979b), cuckoldry
avoidance tactics in waterbugs (Smith 1976, 1979) reflect the coevolutionary
selective circumstances described. See Lloyd (1979b) for a fascinating dis-
cussion of male sexual tactics in fireflies and many other insects.
FEMALE CHOICE: According to much of sexual selection theory, choosy
Florida Entomologist 63(1)
March 1980
females are an important aspect of the sexual environment leading to
nonrandom differential reproduction of conspecific males. Darwin argued
that female tastes for male beauty caused in many cases the elaboration of
male morphologies and behaviors and "that the power to charm the female
has sometimes been more important than the power to conquer other males
in battle." Darwin assumed that females prefer certain males as mates be-
cause of their morphological and/or behavioral features and that this pref-
erence alone would lead to elaborateness. He did not attempt to explain how
such female preferences might have originated and he said little about se-
lective maintenance of these male traits other than that females preferred
them. The lack of any apparent connection between male ornamentation
and male fitness caused problems for the acceptance of the female choice
aspect of Darwin's theory. Wallace (1889) felt that female choice was un-
important for this reason and because of the lack of evidence that females
choose certain conspecific males over others as mates.9
Fisher (1930) provided only theory for Wallace's objections. Fisher ex-
plained how elaborate male traits could arise and then be maintained by
female choice via his so-called "runaway process." He assumed inheritance
of male traits. The first step in Fisher's scheme involves females finding
a male trait that confers enhanced survival on a female's offspring.
Any female with a preference for the male trait would gain reproductively
because she would produce fit sons. This would lead to the spread in the
population of the male trait as well as female preference for the trait. When
females with the preference became common, the second step or runaway
process could come into play. Any female with the preference that mates
with a male with the trait will produce attractive sons, i.e. sons preferred
by females. The advantage to females which choose males with the trait
during the runaway process would involve only the benefit gained because
females in the population have the same preference. Thus, any female with
the preference will produce more grandsons and so on as long as the female
preference remains the same through time. The elaboration of the trait will
continue because of its advantage due to female preference even after it has
exceeded the point in elaboration at which its advantage in ordinary natural
selection no longer exists. Natural selection may oppose further elaboration,
but the further development will continue as long as the advantage due to
female preference is offset by the disadvantage in natural selection. Elabora-
tion will stop at the point where further elaboration would cause greater
detriment to survival than the benefit gained through sexual selection.'1
Darwin realized that sexual selection, unlike natural selection, has no
definite upper limit and that sexual selection can act counter to the action
of natural selection, but at some point natural selection will prevent further
elaboration.
Fisher argued that females gain reproductive success only by producing
attractive sons during most of the evolution of attractive male features;
only initially was female preference envisioned to result in the production of
sons more fit to cope with environmental contingencies. Zahavi (1975),
Trivers (1976), Hailman (1977), Borgia (1979), and Thornhill (manu-
script) argue that females prefer certain male traits throughout their evolu-
tion because the traits result in the production of offspring capable of sur-
viving; the traits themselves convey information to females that the male
Insect Behavioral Ecology-'79
has abilities that are important for offspring survival and ultimately re-
production. I will return to these ideas later. Regardless of the theory one
uses to explain the evolution of male secondary sexual traits, all the theories
involve very rapid evolutionary change.
PROBLEMS WITH FEMALE CHOICE THEORY: The role of female choice in the
evolution of male traits remains controversial. There are 3 problems as fol-
lows: 1) there is little evidence that females actually prefer certain con-
specific males over others in nature; 2) many traits presumably preferred
by females do not seem to be obviously related to the choosy female's own
fitness or that of her offspring; and 3) genetic variation in male traits is
necessary to provide the adaptive basis for female choice, but little genetic
variation should be associated with traits under strong and continuous female
preference.
Wallace (1889) first criticized female choice theory because of few sup-
porting observations for females actually discriminating males. Huxley
(1938) made a similar criticism. Poulton (1890) supported Darwin's view of
the role of female choice and claimed that the lack of evidence stemmed
from the lack of attempts to observe animals in nature. Mayr (1972) ex-
pressed the view that the important role of female choice was beyond ques-
tion. His opinion was primarily based on observations "that females are very
fickle indeed and usually remain for a long time unimpressed by the displays
of large numbers of suitors before finally accepting one of them" (p. 92).
However, coyness may merely mean that females are discriminating about
the general ecological circumstances for reproduction other than the char-
acteristics of or resources controlled by a potential mate (see Williams 1966).
Also, West-Eberhard (1979a) has suggested that females might sometimes
behave in a coy manner simply because they are "afraid" of males which
often are larger and more aggressive. Clearly, coyness in itself is not evi-
dence for female choice.
The paucity of evidence for female preference in nature remains to date
an important problem in understanding the role of female choice in the
evolution of male traits. Most evidence for female choice is very indirect and
based on the distribution of females around males of different ages or sizes
or males that possess different amounts of some resource such as a territory
(see studies discussed in Wilson 1975, Davies 1978, Halliday 1978, Alcock
1979b, and Downhower and Browin in press). Also, female choice is often
inferred when females mate with some males and not others.11
Laboratory studies of female choice have revealed, in general, the same
kind of indirect evidence for female choice as field studies. For example,
Maynard-Smith (1956) found that female Drosophila subobscura mate more
with outbred than with inbred males. He inferred preference on the basis of
a difference in courtship behavior between the 2 types of males, but other
differences between the males unrelated to female choice could account for
the results.
One could argue that all the above examples involve female choice, be-
cause females have the option of staying with a male that will serve as a
mate or leaving and looking for another more suitable mate (see Maynard-
Smith 1978: 169). I feel that the argument alone is unsatisfactory. Females
under some circumstances may be forced to remain with certain males be-
cause, as is typical in many species, males are larger, more aggressive and/or
Florida Entomologist 63(1)
March 1980
more armored than females. The question of whether females choose males
can only be answered by direct field observation of females interacting with
males.
Few field studies have been directed at observing female behavior in
relation to criteria females use in mate choice.12 I have demonstrated that
females of the scorpionfly, Hylobittacus apicalis, prefer mates with large
nuptial prey over males with small or no prey in nature (1976a, 1977, 1979a,
in press e). The hangingfly system is perhaps unique in that individual
females can be watched and followed after they interact with males and the
witnesses of discriminating and nondiscriminating females assessed in nature.
To me it is clear that direct evidence for Darwinian female choice is
very meager. In actuality, male choice has been demonstrated in about as
many cases as female choice. Manning (1975) provides good evidence for
male preference for larger, more fecund females in Asellus isopods, and the
detailed work of Shuster (1979) on Thermosphaeroma isopods demonstrates
male preference for larger females and for females in an advanced stage
of reproduction. Some very fascinating hypotheses have been put forth
regarding how and why females may choose among males (Trivers 1972,
Zahavi 1975, Alexander 1975, Borgia 1979, Downhower and Brown in press,
and Lloyd 1979b) ; however, it has yet to be determined that females typ-
ically are discriminate of mates.
The second problem associated with our understanding of the role of
female choice is that many traits presumed to be preferred by females (e.g.,
elaborate male morphological features) do not seem to be correlated with
the choosy female's fitness or that of her offspring (see Maynard-Smith
1978, Borgia 1979, and Thornhill unpublished for detailed discussions). In
many species males have a resource in their possession that females ap-
parently assess. This resource may be a territory, nest site, food item, etc.
Females choosing males on the basis of resources that the female herself
will use or that will be provided to offspring present no problem for female
choice theory because of the immediate reproductive benefit that can be en-
visioned for a discriminating female. However, there have been few demon-
strations that females choosing certain resource-holding males over others
actually increase their own reproductive success, a critical demonstration if
one wishes to argue that female choice is adaptive (see Maynard-Smith 1966,
Thornhill 1976a, 1979a). Adaptive female choice is apparent in the scorpion-
fly Hylobittacus apicalis. Females assess males on the basis of the nuptial
prey which is presented to females by the male just prior to copulation.
Most females prefer males with large nuptial prey and such females lay
more eggs than females that do not exhibit discrimination of mates. Dis-
criminating females in this system may accrue other advantages-e.g. in-
creased survivorship because they do not expose themselves to predators-
but increased fecundity is the most apparent and relevant. Number of eggs
laid by a female is an important parameter of fitness in H. apicalis because
females drop eggs randomly among the leaf litter (thus oviposition site
selection is not related importantly to variation in female reproductive suc-
cess), egg size does not vary, and there is no parental care of young (Thorn-
hill 1976a, in press e).13
On the other hand, there are many species in which males do not display
a resource to females during courtship, which may consist only of complex
Insect Behavioral Ecology-'79
dances, flights and ritual chases often involving specialized male morphology.
In other species the only differences between males are in phenotypic traits
like size or age. It is species in which males show no parental care and no
protection or nurturing of the female that female choice theory is most
problematical, because the only benefit females are likely to receive is male
genes. How could the courtship antics of male insects and birds be related
to superior genes that would enhance offspring fitness?
Fisher's (1930) theory argues that the male traits preferred by females
only initially enhanced offspring survivorship. Indeed, when the runaway
process in Fisher's scheme comes into play, the further elaboration of the
trait by female choice is viewed as contrary to male offspring survival.
There are good examples of morphological traits of males that females are
suspected of using in mate choice that are actually contrary to survival.14
Zahavi (1975) proposed a theory he called the "handicap principle" as an
alternative to Fisher's "runaway" selection model. Zahavi argues that fe-
males should select males on the basis of traits that are true phenotypic
indicators of a male's genetic traits related to survival. He reasoned that
elaborate male characters represent a survival handicap to the male pos-
sessing them. A female preferring a male with such a handicap would be
assured of getting a father for her offspring with superior survival genes,
because the male had survived despite his handicap."1
Trivers (1976), Hailman (1977), and Thornhill (1979a, manuscript)
argue that female preference may be directed at discriminating certain
male traits that indicate male abilities of value for survivorship of both
sexes of offspring. Such traits might be under autosomal genetic control so
that both sexes of offspring would benefit (Trivers 1976, Thornhill 1979a).
For example, a female Hawaiian drosophilid that preferred a male with
colorful wings might be actually choosing a male with superior genes for
obtaining essential or rare nutrients as indicated to the female by the nature
or extent of wing pigment. Females preferring males with colorful wings
would produce sons and daughters with the ability to find and process the
essential or rare nutrient. A similar example might involve the antlers of
male deer, the size of which could indicate a male's ability to obtain and
process calcium. This line of thinking can be extended to include behaviors
as well as morphological features of males (Thornhill manuscript). These
theories are different from Fisher's notion because they explain benefit to the
discriminating female in terms of more than merely having attractive sons.
However, these theories, like Fisher's theory, when applied to explain male
traits in species without male parental care or male-provided nourishment
or protection to the female, depend on genetic differences between males that
are discriminated by females on the basis of phenotypic differences between
males.
The third problem associated with female choice results from population
genetics theory. The argument is that females which discriminate mates on
the basis of genetic differences between males (as expressed in the pheno-
type) will deplete additive genetic variance for fitness if only a small portion
of males mate. That is, female choice should lead to a low parent-offspring
correlation for fitness in the trait preferred. Phenotypic variation related
to fitness will not, according to this argument, reflect underlying genetic
fitness variation (Williams 1975, Maynard-Smith 1978, Halliday 1978,
Florida Entomologist 63 (1)
Harpending 1979). Many animals (Wilson 1975) including most insects
(Thornhill 1979a) are highly polygynous (only a few males may inseminate
most females); therefore, this criticism of female choice is widely applicable.
However, Maynard-Smith (1978) points out that despite this problem
females still appear to exercise choice in lekking bird species in which very
few males obtain most of the matings. For example, in lekking sage grouse
7% of the males copulate with 85% or more of the females visiting the male
aggregation and central males do most of the copulating (Wiley 1973).
Inter-male contests determine the position of males in the lek. The female
gets nothing from the central male but genes, as there is no male parental
care. It appears that females prefer these central males as mates as they
pass up copulations with peripheral males while moving toward the lek's
center. Maynard-Smith further states that the preference of central males
only makes sense if there is some inheritance of fitness associated with the
traits that enable a male to obtain the central position. He suggests that,
although small, there is enough genetic variation associated with male traits
contributed by harmful mutations and the establishment of newly intro-
duced favorable mutations to make female choice adaptive in lekking birds.
Variance in male copulatory success in some lekking insects may be as high
as in sage grouse (see Alexander 1975, Thornhill in press d). Borgia (1979)
provides a fascinating discussion of some alternative ways in which neces-
sary genetic variation can be maintained in lekking birds as well as other
highly polygynous animals.
On the other hand, female choice on the basis of "good genes" is not
necessary to account for lek structure or the relative mating success of
males in the lek as first explained to me by John Sivinski. If the central
area of the lek is safer in terms of reduced predation, female choice on the
basis of male genetic quality is not required for an understanding of the
female preference for the central male. This interpretation of female choice
in lekking birds is consistent with the predation-pressure hypothesis for
the evolution of lek behavior provided by Lack (1968) for birds and by
Spieth (1974) for Hawaiian drosophilids (see Thornhill 1978b, in press a).
GENETIC VARIATION AND THE INHERITANCE OF FITNESS
There is another very important point that counters the problem for
female choice theory created by the likelihood of little genetic variation
underlying male traits discriminated by females and thus virtually little or
no variation upon which further selection can act. The argument is simple
and has been overlooked until recently (see Alexander 1977, West-Eberhard
1979a). Sexual selection will not necessarily stop when genetic variation
underlying male traits is absent. Evolution (changes in gene frequency) due
to selection will cease without genetic variation, but selection can continue.
The nonrandom differential reproduction' associated with any form of selec-
tion results from phenotype differences. These differences may be totally
heritable, totally nonheritable, or some mixture of these 2 extremes. Selec-
tion will act on any differences whether genetic or nongenetic. Nonheritable
variation should be especially important as a basis of sexual selection (and
social selection in general, see West-Eberhard 1979a). Traits such as male
size, age, and general vigor are felt to be important in both male-male com-
petition for females and female choice. Variation in these traits may be to
March 1980
Insect Behavioral Ecology-'79
a large extent related primarily to differences in nutrition obtained di-
rectly by individuals and/or provided by parents.
For the reasons discussed earlier, sexual selection is a potent form of
non-random differential reproduction and thus a gene associated with success
in sexual competition should spread very rapidly to fixation. Selection for
better alternative genes following their introduction into the population will
also be rapid. Thus over most of evolutionary time genetic variation may be
irrelevant to the strength of sexual selection operating at any 1 time. The
most successful male Hawaiian drosophilid in the lek and the central male
sage grouse may be identical with other conspecifics in the lek in regard to
genes associated with achieving the dominant position which allows great
reproductive success. Tremendous reproductive success in these situations
may be due to phenotypic traits like size that are entirely nonheritable.
Females are expected to still exercise choice because: 1) the traits of the
preferred male (e.g. size) have related generally to offspring fitness over
evolutionary time, 2) any mutants deleteriously influencing offspring that
occur and are expressed in the phenotype of males would be detected and
avoided by such a preference, and 3) any mutants advantageously influenc-
ing offspring that occur and are expressed in the phenotype of males would
be detected and chosen by such a preference (also see Alexander 1977).
The arguments involving strong sexual selection using up genetic varia-
tion but then remaining potent as a form of nonrandom differential repro-
duction on the basis of nonheritable phenotypic differences can be applied
to traits under social competition in general (West-Eberhard 1979a). This
interpretation is consistent with population genetics fact and theory: char-
acters directly related to fitness have the lowest heritability in many species
(Mukai et al. 1972; Falconer 1960; see Harpending 1979 for recent discus-
sion). However, this interpretation may seem in conflict with our knowledge
of genetic variation in natural populations, because most species that have
been studied are genetically variable at a large number of loci (see Antono-
vics 1976). This includes "living fossils" like the horseshoe crab (Limulus
polyphemus); also included is the rare and highly polygynous orangutan,
one of the most genetically variable primates known (see Antonovics 1976
and references therein).
West-Eberhard (1979a) offers an hypothesis that could account for this
apparent inconsistency of sexual selection acting primarily on nonheritable
variation and high levels of genetic variation in natural populations. The
genetic variation observed may be the result of a reduction in the intensity
of natural selection in the presence of strong sexual selection. If traits im-
portant in mating competition (and social competition in general) are more
important than nonsocial traits in determining an individual's relative re-
productive success then slight inabilities in nonsocial traits may be sheltered
from selection in sexually successful individuals [e.g. the male that obtains
the most matings in a mating aggregation of lovebugs (Thornhill in press
d) or in certain Hawaiian Drosophila] In lovebugs the position of the male
in the aggregation determines a male's access to females and is decided by
the outcome of aggressive interactions (Thornhill in press d). The most
successful male may be less fit than another male at feeding in the adult
stage or at some other nonsexual task, but because of his sexual prowess
Florida Entomologist 63(1)
March 1980
he wins the mating competition and thereby perpetuates not only his
prowess but also his inadequacies which are sheltered from selection.
I now return to a discussion of alternative specializations often employed
by individuals under sexual selection which, although resulting in less genetic
success than winning, are attempts to obtain some reproductive success
despite defeat by males or discrimination by females. The typical view is
that alternative behavioral and morphological specializations are due to dif-
ferent genotypes (Gadgil 1972; Gadgil and Taylor 1975; Maynard Smith
and Parker 1976; Alcock 1979b; Parker 1979; Cade 1979; Borgia 1979). The
above discussion of sexual selection suggests an appropriate interpretation
other than that of genetic differences between winners and losers in the
sexual competition. The intraspecific variation in male insect behavior and
morphology observed, including the examples of alternative specializations
discussed earlier, could be facultative rather than genetically fixed, and
responses to phenotypic differences between males (West-Eberhard 1979a;
also see Alcock 1979a). Maynard Smith and Parker (1976) point out that
certain variable behaviors may not be based on genetic differences.
It is unclear whether alternative specializations occur in genetically fixed
ratios or are faculative in the sense of being situation or condition de-
pendent. The best evidence for the former situation involves the ratio of
wingless (fighting) and winged (dispersing) males in various species of
fig wasps (Hamilton 1979). West-Eberhard (1979a) suggests that genet-
ically fixed ratios of alternatives are most likely to evolve when an indi-
vidual has no ability to obtain information on the appropriateness of switch-
ing between alternatives during its lifetime, or when the information would
be available too late in an individual's development to allow initiation of an
adaptive change. West-Eberhard (1979a) feels that the fig wasps studied
by Hamilton fit these conditions.
Further, West-Eberhard (1979a) points out that the circumstances
favoring a faculative (situation or condition dependent) switch, when pos-
sible, will be more desirable than a genetic switch because: 1) a "big-winner"
alternative will typically exist, which will be far more profitable than any
other alternative. Individuals should therefore switch to an alternative other
than the most reproductive one when costs to reproduction (e.g. injury due
to male-male interaction) exceed benefits associated with the most repro-
ductive alternative; and 2) conditions favorable for switching to an alterna-
tive are dependent not only on the amount of resource available and the
number of competitors present, but also on an individual's ability to conquer
males and attract females relative to these abilities in other males. Thus,
circumstances for a switch to an alternative will often be unpredictable.
The point at which a faculative switch becomes advantageous corresponds
to that point where the benefit and cost ratios for the alternatives adopted
by an individual are equal. This point may be reached during development of
an immature individual or in the adult stage. Larval size may be a cue for
a faculative switch to an alternative specialization. For example, this may
explain small- and large-horned male beetles of the same species. One can
imagine a genetic program in such cases selected to evaluate and predict
future reproductive success from larval size and triggering appropriate
development. If success is unpredictable from larval circumstances but only
from adult experience appropriate genetic programs might direct adoption
Insect Behavioral Ecology-'79
of appropriate alternative strategies only after adulthood. In Panorpa
scorpionflies discussed earlier winners are males that control large nuptial
offerings. These males have won the male-male competition and will be
preferred by females as mates because of their offering. The other males
appear to be losers in the sense that they will obtain fewer matings. Access
to females will depend on the quality of their nuptial offering and/or their
ability at rape. The evidence suggests that the alternative behaviors that
may be employed by Panorpa males are not dependent on genetic differences.
The males appear to be facultative in their adoption of alternatives de-
pendent on conditions experienced as adults such as the nature and extent
of male-male competition and the availability of nuptial offerings (Thornhill
1979a, in press a).
I began this paper with the question: why was Darwin so convinced of
the power and ultimate wide acceptance of his theory of sexual selection?
Darwin was very knowledgable about the diversity of living things and was
impressed by male characteristics that did not seem to clearly relate to
coping with environmental contingencies. He envisioned, therefore, a different
process-sexual selection-to explain the traits that seemed neutral or nega-
tive to survival. He felt that both forms of sexual selection-male-male com-
petition and female choice-would be stronger on males than on females and
that 1 or both forms could explain even the most elaborate male features.
The role of male-male competition for females as a potent form of selection
has never been seriously disputed. Darwin was aware of its occurrence in
many animals and, indeed, it can be observed at will in most species. How-
ever, the role of mate choice as a process leading to nonrandom differential
reproduction of males is controversial and our understanding of this process
is just beginning. Darwin's conviction about the power of sexual selection
was soundly based in his understanding of the lack of a definite upper limit
to reproductive return from traits changing under sexual selection leading
to an accelerated coevolutionary race between and within sexes, a feature
sexual selection does not share with natural selection. Therefore, it is useful
to distinguish sexual selection from natural selection, but the former is
similar in potency and operation to the broader category of social selection
which defines all processes of nonrandom differential reproduction due to
the social environment.
APPENDIX
IThis paper is based on aspects of a paper by M. J. West-Eberhard
(1979a) that I feel presents important ideas for entomologists investigating
the sexual and social behavior of insects.
2The importance of the Process of non-random differential reproduction,
so-called natural selection, as a mechanism for evolutionary change was first
clearly stated by Darwin (1859) and Wallace (1889). Both of these theore-
ticians had similar ideas about the role of natural selection in the evolution-
ary process; however, Darwin's synthesis was much more complete and was
published earlier. Darwin and Wallace had very different views about the
role of sexual selection in evolution. Darwin defined the basic components of
his theory of sexual selection in 1859 in The Origin of Species. The follow-
ing passages were used by Darwin in 1859 to contrast natural and sexual
selection and to distinguish the 2 forms of sexual selection, male combat and
female choice:
Florida Entomologist 63(1)
"Sexual selection . depends, not on a struggle for existence, but on a
struggle between the males for possession of the females; the result is
not death to the unsuccessful competitor, but few or no offspring . .
Generally, the most vigorous males, those which are best fitted for their
places in nature, will leave the most progeny. But in many cases, victory
will depend not on vigour, but on having special weapons confined to the
male sex . Amongst birds, the contest is often of a more peaceful
character . there is the severest rivalry between the males of many
species to attract by singing the females . and successive males display
their gorgeous plumage and perform strange antics before the females,
which stand by as spectators, at last choose the most attractive part-
ner .... It may appear childish to attribute any effect to such apparently
weak means [female choice] . .. but if man can in a short time give
elegant carriage and beauty to his bantams, according to his standard of
beauty, I can see no good reason to doubt that female birds, by selecting,
during thousands of generations, the most melodious or beautiful males,
according to their standard of beauty, might produce a marked effect ....
I believe that when the males and females of any animal have the same
general habits of life, but differ in structure, colour, or ornament, such
differences have been mainly caused by sexual selection; that is, indi-
vidual males have had, in successive generations, some slight advantage
over other males, in their weapons,... or charms; and have transmitted
these advantages to their male offspring". (p. 88-90) (emphasis added).
The main points made by Darwin in 1859 and later in 1871 are: 1)
natural selection is the form of differential reproduction that leads to char-
acters associated with survival; 2) sexual selection is the form of differential
reproduction that leads to traits associated with competition for mates and
may lead to an elaborateness useless with respect to survival (or contrary
to survival, see Otte 1979); 3) differential reproductive success of males
under sexual selection occurs because of male-male competition for females
and female choice, 4) all sexual differences cannot be attributed to sexual
selection alone. Ghiselin (1969), Otte (1979), and Bajema (in press) pro-
vide discussion of other points conveyed by Darwin (1871, 1874) in his
original formulation of sexual selection theory.
3For the most part it appears that Darwin had firmly in mind a distinc-
tion between natural and sexual selection (see Otte 1979, West-Eberhard
1979a, Bajema in press). He was aware of their similarity in regard to
causing evolutionary change by differential perpetuation and their differ-
ence in regard to the types of traits resulting from each of the 2 types of
selection.
Some controversy has surrounded attempts to distinguish natural and
sexual selection and the utility of such a distinction. Wallace (1889) felt
that male-male competition is best considered as a form of natural selection,
and he felt female choice of conspecific males was generally unimportant
(except in humans; see Bajema, in press). Wallace (1889) wrote
"The term "sexual selection" must, therefore, be restricted to the direct
results of male struggle and combat. This is really a form of natural
selection, and is a matter of direct observation; while its results are as
clearly deducible as those of any of the other modes in which selection
acts. And if this restriction of the term is needful in the case of the
higher animals it is much more so with the lower. In butterflies the
weeding out by natural selection takes place to an enormous extent in
the egg, larva, and pupa states; and perhaps not more than one in a
hundred of the eggs laid produces a perfect insect which lives to breed.
March 1980
Insect Behavioral Ecology-'79
Here, then, the impotence of female selection, if it exists, must be com-
plete; for, unless the most brilliantly coloured males are those which
produce the best protected eggs, larvae, and pupae, and unless the par-
ticular eggs, larvae, and pupae, which are able to survive, are those which
produce the most brilliantly coloured butterflies, any choice the female
might make must be completely swamped. If, on the other hand, there is
this correlation between colour development and perfect adaptation to
conditions in all stages, then this development will necessarily proceed
by the agency of natural selection and the general laws which determine
the production of colour and of ornamental appendages" (p. 296).
In 1927 the distinguished entomologist 0. W. Richards said in his classic
paper on sexual selection in insects:
"The line between Natural and Sexual Selection is not, of course, sharply
marked, but some definition of their respective actions is necessary ....
A character that has been acquired or preserved by the action of Sexual
Selection must either be displayed to the other sex in courtship or used
to drive away rivals" (p. 299-300).
Although Huxley (1938) doubted the role of female choice and the wide-
spread existence of male traits contrary to survival evolved by sexual selec-
tion, he expressed a view similar to Darwin's on the distinction between
natural and sexual selection. He wrote in 1963:
". .we must differentiate between two quite distinct modes of natural
selection, leading to different types of evolutionary trend which we may
call survival (= natural) selection and reproductive (= sexual) selection
... survival selection is much the more important" ... (p. xviii).
Mayr (1972) feels that a distinction between natural and sexual selection
makes sense only if one adopts the meaning of fitness used by Darwin. Fit-
ness to Darwin meant well adapted for individual survival in the face of non-
biotic environmental contingencies. An individual's ability to acquire mates
through competition with other individuals was viewed by Darwin as that
individual's performance under sexual selection.
Williams (1966) was one of the first to clearly place all types of selec-
tion in the broad framework of general nonrandom differential reproduction
and thus provided a logical means of eliminating the separation between
sexual and natural selection. He pointed out that all adaptations must
ultimately enhance reproductive success and genetic perpetuation whether
the traits are associated with individual survival or direct reproduction.
(Also see Wilson 1975, Dawkins 1976, Alexander and Borgia 1979). Sexual
selection is simply a form of natural selection that acts in the context of
direct reproduction. All forms of selection involve nonrandom differential
reproduction, but natural and sexual selection describe the process as brought
about by Darwin's "hostile forces" and the sexual environment, respectively.
4West-Eberhard (1979a) has placed the topic of individual selection in
a broader and more realistic framework using the concept of social selection.
Social selection was outlined by Wynne-Edwards (1962) in his detailed
analysis of social behavior and later discussed by Crook (1972) in work on
primate social behavior (West-Eberhard, 1979a). Referring to social hier-
archies, Wynne-Edwards wrote:
"Its (the hierarchy) establishment places in their own hands . a
Florida Entomologist 63(1)
powerful selective force, which can conveniently be described as social
selection. It is similar to the one Darwin believed to apply in the more
restricted field of sexual selection" . (p. 139).
Crook (1972) expressed the view that sexual selection is a category of
social selection which is in turn a subset of natural selection. He argued that
reproductive competition between individuals determines which individuals
leave the most genes in successive generations and that this competition may
be direct or indirect. The outcome of direct reproductive competition is de-
termined by social interaction aimed at gaining access to essential com-
modities (e.g. food and mates), while winners and losers in indirect repro-
ductive competition are not determined by interaction with other individuals.
Therefore, 2 categories of natural selection can be distinguished on the basis
of the nature of the reproductive competition involved: environmental (=
ordinary, West-Eberhard 1979a; = natural, Darwin), and social. Social selec-
tion is defined by Crook (1972) as:
". . that process leading to the evolutionary enhancement of morpho-
logical allaesthetic and behavioral characteristics that function within a
social ssytem to provide biological advantages to the individual in rela-
tion to survival prior to reproduction, the formation of zygotes and the
birth and rearing to maturity of young or the progeny of close kin" (p.
269).
This definition encompasses 3 types of social selection (Crook 1972) : 1)
competition for resources (food, territories, oviposition sites, etc.) that are
essential for individual reproductive attempts and for parental investment
in offspring after a successful attempt; 2) differential reproduction in es-
tablishing and maintaining a social organization effective in nourishing and
protecting offspring of the individuals involved and their close kin (selection
in contexts of nepotism and non-nepotistic reciprocity), and 3) competition
for access to superior mates exemplified typically through male-male inter-
actions and female choice. Darwinian sexual selection is equal to the third
type of social selection.
"Outside the social Hymenoptera there is little evidence for waiting being
employed as a strategy in insects. West-Eberhard (1975, 1979b) has pro-
vided evidence that sub-dominant females employ waiting in certain social
wasps. The waiting strategy is commonly used by males of polygynous
vertebrates and is called bimaturism (e.g. Wilson 1975). Delayed maturity
in males relative to females allows males to attain larger size before initiat-
ing competitive interactions for females and status.
Recent work on "helpers at the nest" in birds reveals that help in rearing
the offspring of parents provided by younger birds allows the helpers the
best opportunity at future individual reproduction. Helping behavior results
in territory acquisition and future helpers for the helping individual. Help-
ing behavior is an alternative specialization that the birds adopt in circum-
stances when an attempt at direct reproduction is less profitable (Ligon
and Ligon 1978, Stallcup and WoolfenAen 1978, Ligon in press). Similar
"helpers at the nest" occur in some social wasps (West-Eberhard 1978,
1979b).
6In vertebrates alternative specializations associated with male mating
strategies occur in fish, frogs and toads, birds, and mammals (see Cade 1979,
Thornhill 1979a, 1979b, in press a). In these cases, dominated males employ
mating tactics very different from those used by dominant males. A frequent
circumstance involves dominant males possessing a territory that allows
them access to females, and subordinate males, often called "satellites",
March 1980
Insect Behavioral Ecology-'79
position themselves around the territory holder and intercept females at-
tracted to the territories of dominant males. Satellite males sometimes have
specialized morphology for "stealing" females attracted to dominant males.
Pseudofemale morphology and/or behavior is sometimes seen under these
circumstances. In 1 fish (the Gila topminnow, Constantz 1975), satellite
males have long, flexible "penises", allowing them to copulate with females
that are moving rapidly toward territorial males.
7Darwin (1874) wrote:
"In regard to structures acquired through ordinary or natural selection
there is in most cases, as long as the conditions of life remain the same,
a limit to the amount of advantageous modification in relation to certain
special purposes; but in regard to structures adapted to make one male
victorious over another, either in fighting or in charming the female,
there is no definite limit to the amount of advantageous modification; so
that as long as the proper variations arise the work of sexual selection
will go on" .. (p. 256).
sOn the topic of the interaction of natural and sexual selection, Darwin
wrote:
"Obscure tints have often been developed through natural selection for
the sake of protection, and the acquirement through sexual selection of
conspicuous colors appear to have sometime been checked from the danger
thus incurred .... natural selection will determine that . [secondary
sexual] characters shall not be acquired by the victorious males, if they
would be highly injurious, either by expending too much of their vital
powers or by exposing them to any great danger. The development, how-
ever, of certain structures . has been carried to a wonderful extreme;
and in some cases to an extreme which, as far as the general conditions
of life are concerned, must be slightly injurious to the male. From this
fact we learn that the advantages which favored males derive from con-
quering other males in battle or courtship, and thus leaving a numerous
progeny, are in the long run greater than those derived from rather more
perfect adaptation to their conditions of life." (1874, p. 256-7).
9Wallace (1889) wrote:
"Natural selection . acts perpetually and on an enormous scale in
weeding out the "unfit" at every stage of existence, and preserving only
those which are in all respects the very best. Each year, only a small
percentage of young birds survive to take the place of the old birds which
die; and the survivors will be those which are best able to maintain ex-
istence from the egg onwards, an important factor being that their
parents should be well able to feed and protect them, while they them-
selves must in turn be equally able to, feed and protect their own off-
spring. Now this extremely rigid action of natural selection must render
any attempt to select mere ornament utterly nugatory, unless the most
ornamented always coincide with "the fittest" in every other respect;
while, if they do so coincide, then any selection of ornament is altogether
superfluous. If the most brightly coloured and fullest plumaged males are
not the most healthy and vigorous, have not the best instincts for the
proper construction and concealment of the nest, and for the care and
protection of the young, they are certainly not the fittest and will not
survive, or be the parents of survivors . and as the direct evidence for
Florida Entomologist 63(1)
any such female selection is almost nil, while the objections to it are cer-
tainly weighty, there can be no longer any reason for upholding a theory
which was provisionally useful in calling attention to a most curious and
suggestive body of facts, but which is now no longer tenable" (p. 295).
lOFisher's model can be illustrated by a hypothetical example. One may
consider the evolution of elaborate male morphology displayed in courtship
in many insects, e.g., lekking Hawaiian drosophilids. Originally, a male with
slightly larger than average wings may have been better at flying and
escaping predators. Females preferring such males would perpetuate this
advantage through their male offspring. The frequency of males with larger
wings and of females with the preference would increase in frequency due
to this initial preference connected with increased female fitness. As females
with the preference for males with larger wings increased in frequency,
females would also benefit merely because of having preferred sons. As long
as the preference remained, it would increase wing size over evolutionary
time, even though beyond a certain size, larger wings might interfere with
the flight of a female's sons. The elaboration of wings would continue until
the advantage in mating success of males with large wings was offset by the
disadvantage of large wings in flight. When the net advantage in favor of a
further increase in wing size no longer exists, the runaway process would
stop. O'Donald (1962) developed Fisher's argument mathematically.
1The successful males may show differences in courtship behavior in
comparison to unsuccessful males, but this does not mean females choose
males on the basis of these differences. The fact that certain males obtain
more copulations than others may be entirely unrelated to female choice, and
only determined by male location in relation to female movements. A male's
location may be determined entirely by male-male interaction or by chance.
For example, in certain dragonflies the males that mate the most are those
defending territories at the time when females arrive (Campanella and
Wolf 1974).
12Females of some lekking birds may select mates on the basis of age
and/or size (e.g., Wiley 1975). Howard's (1978) work on bullfrogs indicates
female preference for males with suitable territories. Cronin and Sherman's
(1977) and O'Donald's (1972, 1973, 1974) work indicates female choice in
nonlekking birds in nature. Borgia (1979) provides good evidence for female
choice in dung flies (Scatophaga). A few laboratory studies have been
designed to observe female behavior in relation to apparently natural criteria
of mate choice with interesting results (see Collias and Victoria 1978,
Thornhill 1979a, in press a).
"Adaptive female choice involving male territory size may occur in the
arctic skua (a bird) (O'Donald 1977). However, the lack of correlation
between the number of young produced by females and indirect measure-
ments of territory quality (e.g. male harem size) often found in the well-
studied redwing black bird do not support an interpretation of adaptive
female choice (see Weatherhead and Robertson 1979).
14In the great-tailed grackle, the elaborate display morphology of males
apparently interferes with flight and thus contributes to the likelihood of
male mortality (Selander 1972). In the fishes Notobranchius guentheri
(Haas 1976), the three-spined stickleback (Semler 1971), and the guppy
(Haskins et al. 1961), nuptial coloration, apparently preferred by females,
makes males more subject to predation. Why should females prefer a mate
whose son will suffer a higher likelihood of mortality? Why do not females
prefer less elaborate or colorful males? Why does not natural selection favor
males with less elaborate plumage and nuptial color? Fisher's theory of
runaway evolution by female preference can supply an answer to these
March 1980
Insect Behavioral Ecology-'79
questions: male characters evolve to elaborateness simply because they are
attractive to females. However, another way to look at the matter of female
preference of males with specialized behaviors and morphologies that appear
contrary to male survival is that the traits may not be contrary to the sur-
vivorship of offspring (Trivers 1972, 1976; Zahavi 1975; Hailman 1977;
Thornhill 1979a, manuscript).
1"Again consider Hawaiian drosophilid males. Females preferring males
with elaborate structures would be choosing handicapped males because these
structures would interfere with other activities and increase the likelihood
of predation; however, the structures would be indicators of survivorship
ability despite the handicap incurred and the offspring could benefit. Males
not possessing the elaborate trait might be more fit than males with it, but
there is no way a female can be sure of this. The handicap possessed by a
male conveys to females his true genetic quality related to survivorship.
Zahavi's theory has received considerable attention from theorists. Both
verbal and mathematical genetic models have been used to analyze the condi-
tions under which the theory might apply (Davis and O'Donald 1976;
Dawkins 1976; Maynard Smith 1976, 1978; Zahavi 1977; Bell 1978; Halliday
1978; Borgia 1979; West-Eberhard 1979a). In general, these analyses indi-
cate that the original theory will only operate under very restricted circum-
stances (e.g., when genes coding for the handicap are non-additive and genes
for survival are additive or when the handicapping trait is non-genetic) (see
Bell 1978, Halliday 1978, Maynard Smith 1978, Zahavi 1977). The major
problem with the theory is that females with a preference for handicapped
males will produce offspring with the handicap. According to Maynard
Smith (1978), only if Fisher's runaway selection process was also operating
could Zahavi's form of sexual selection be effective. Maynard Smith (1978)
maintains that the theoretical conditions under which the handicap principle
can be shown to operate are not plausible, but in some modified form the
theory may be important. He ends the discussion of the handicap principle
by saying ". . I see little point in further discussion until it has been shown
to work in at least one plausible genetic model" (p. 174). Alcock (1979b) and
West-Eberhard (1979a) have pointed out that the handicap principle as
originally proposed is probably valid at some level because extravagant
features presumably preferred by females are handicaps in other contexts
as males would be better off in terms of survival without them. Before
Zahavi's theory is laid to rest, I feel it is worthwhile to test it using real
animals rather than computer simulated genetic models or verbal argu-
ments. I have attempted such a test with the scorpionfly H. apicalis (Thorn-
hill in press a).
ACKNOWLEDGMENTS
I thank Gary Dodson, Darryl Gwynne, Henry Harpending, Janice Moore,
Steve Shuster, Mary Jane West-Eberhard, and Bruce Woodward for helpful
criticisms on this paper. My insect work discussed is supported by National
Science Foundation grants DEB77-01575, DEB79-10193, and BNS79-12208.
Linda DeVries, Ann Hudgens, Debra McPhee, and Mary Thorpe profes-
sionally prepared the manuscript.
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ALTERNATIVE MALE REPRODUCTIVE BEHAVIORS
WILLIAM CADE
Department of Biological Sciences
Brock University
St. Catharines, Ontario
Canada L2S 3A1
Male-male competition and female mating preferences are often believed
to result in some males reproducing more successfully than others. The high
variance in individual male reproductive success is 1 aspect of the general
process of sexual selection. Although formalized by Darwin (1871) over a
century ago, the past decade has witnessed an important revival of interest
in sexual selection (Otte 1979). In 1 area of research, theoretical and
empirical studies have shown that the males of a species may pursue very
different mating behaviors. For example, some males defend territories and
signal visually or acoustically for mates. Other (satellite) males also occur
and sometimes intercept females enroute to the territory holder. This and
other forms of intraspecific variation occur in diverse types of animals,
including species from several orders of insects. Sometimes alternative male
sexual behaviors pose an interesting problem for applying natural selection.
If 1 behavior is more successful at acquiring mates, the alternative forms
of behavior should be eliminated or kept at a low frequency in the popula-
tion. My aim here is to review and discuss the evolutionary basis for the
occurrence of alternative male reproductive behaviors, and give specific ex-
amples that illustrate the need for a consistent terminology for the different
types of variation. I will also use the theory and categories of alternative
male reproductive behavior to analyze variations in the reproductive be-
havior of male field crickets.
TYPES OF MALE VARIATION
Alcock (1979) (see also Alexander 1975) outlined the general categories
Insect Behavioral Ecology-'79
of intraspecific variation in male sexual behavior. Categories of male be-
havior are most easily distinguished by their simultaneous occurrence in the
same population. On the other hand, the comparative approach has shown
that conspecific males in different populations or demes may behave very
differently. It is not difficult to see the operation of natural selection in
producing a single mode of behavior within a population. By the same token
the occurrence of different male behaviors in the same population but at
different times of the year poses no unusual obstacle to interpreting natural
selection. Populations in seasonally changing environments are generally
expected to have the evolutionary capacity for flexibility to meet changing
conditions. More interesting cases arise when variations occur at the same
time in a population. But as Alcock made clear, distinguishing between these
general types of variation is not always easy since intermediates occur. For
example habitat subdivisions may result in males spending part of their time
in 1 habitat and then another. Owing to differences in environmental or
social conditions, the same males may be predisposed to behave in 1 fashion
in 1 habitat, but in a different way elsewhere. A real problem is identify-
ing the population.
Alcock (1979) considered the mechanisms responsible for male behavioral
variation in a population. He recognized 2 possibilities; males are flexible
and can perform the various behaviors, or males are strictly programmed
genetically, thus each has but 1 behavioral role. These are 2 extremes since
males with a particular genetic composition may be predisposed under cer-
tain conditions to behave in a set way. Alcock characterized this situation as
an intermediate between a completely fixed behavioral polymorphism and
complete flexibility in the behavior of individuals. Although intermediates
are possible, it is somewhat confusing to think of a partially fixed behavioral
polymorphism.
STRATEGIES AND EVOLUTIONARY STABILITY
Some confusion over the general types of alternative male reproductive
behaviors is cleared up by applying the logic and language of evolutionarily
stable strategies (ESS). The ESS concept was first formalized by Maynard
Smith (1976) and it is usually used to model aggressive encounters.
Dawkins (1979) used ESS language to analyze simultaneously occurring
behavioral differences (including male sexual behavior) in a population and
the following scheme is based on his treatment.
Male sexual behaviors are often termed reproductive strategies, al-
though the term is criticized. Confusion over the meaning of the term
strategy results from various definitions applied to what are probably dif-
ferent phenomena, and the incorrect assumption of teleological implica-
tions. In the most accurate sense, a strategy is a genetically determined
behavior which can be judged only in relation to natural selection of alterna-
tives (Dawkins 1979). This definition means that an individual exhibits 1
reproductive strategy, although it may take different forms depending on
environmental circumstances. When 2 (or more) conspecific males behave
in different ways, it may also be the result of genetic differences between
males-i.e. 2 different strategies. Distinguishing between these alternative
explanations is difficult since it is not often possible to measure a genetic
Florida Entomologist 63(1)
March 1980
component in individual behavior. Important inferences can sometimes be
made based on the frequency and characteristics of individual behavior.
An ESS is a strategy which, when a certain frequency of the population
adopts it, is unbeatable reproductively compared to a given set of alterna-
tives. An equilibrium is also possible where 2 or more strategies are evolu-
tionarily stable against each other. Dawkins recognized that there may seem
a mixture of strategies in a population for 3 reasons: individuals have dif-
ferent pure strategies and a stable polymorphism exists; individuals have a
single mixed strategy and spend a certain portion of time in one behavior,
and then switch to another; and individuals have a single conditional strategy
and change their behavior in response to a specific environmental or social
event.
PURE STRATEGIES AND STABLE POLYMORPHISMS
Gadgil (1972) first modelled the occurrence of stable polymorphisms in
male sexual behavior. He reasoned that selection should favor highly com-
petitive reproductive behavior by immediate and high gains in individual
reproductive success. But the danger of damage and the energetic costs in-
volved in fighting (including the development of spines, horns, mandibles
and other male armaments) should reduce the survivorship of highly com-
petitive males. At the same time there are males programmed (genetically)
to avoid intense competition and the resulting costs of decreased survivor-
ship. But low investment in reproductive competition means that these males
mate infrequently in a certain period of time. Extended survivorship should,
however, allow these males to have more time in which to mate. The indi-
vidual witnesses of males pursuing a particular behavior may vary greatly
and should depend partially on the frequency of male types present. But the
important result is that the average reproductive success derived from both
behaviors is equal. In this case, the mixture of strategies is evolutionarily
stable, and any departure from an equilibrium will be countered by selection
reestablishing the equilibrium frequency. Frequency dependent selection will
operate such that when 1 behavioral morph becomes less common in the
population, the reproductive benefits derived from that strategy increase
(Charlesworth and Charlesworth 1975, Gadgil and Taylor 1975). Although
it is simpler to think of 2 discontinuous behavioral morphs (Halliday 1978),
the actual frequency distributions may be bimodal with some overlap
(Dawkins 1979, Gadgil 1972). The observed frequencies and the response to
selection will depend on the types of selective pressures and on the genetic
mechanism underlying the 2 strategies (Slatkin 1978).
Conclusive evidence of a stable polymorphism requires a knowledge of the
genetic contributions to alternative behaviors, repeated observations indicat-
ing the recurring nature of the alternatives, and at least an approximation
of the relative reproductive success derived from the different alternatives.
No case of a stable polymorphism of male behavior has been conclusively
demonstrated under field conditions, although such results have been obtained
in the laboratory (Ehrman and Probber 1878, but see O'Donald 1977). One
possibility for a field population showing a stable polymorphism is the Ruff,
Philomachus pugnax, a lek breeding bird in central Europe and Asia. Male
Ruffs are brilliantly colored and strut about clearly defined territories where
Insect Behavioral Ecology-'79
females are attracted and matings result. Satellite males who resemble
females in plumage also occur on and near territories and they copulate
with females attracted by territory holders. Mating success for both types
of males appears to depend on their relative frequencies, with the satellites
copulating more when they are fewer in relative number. Differences in male
color and behavior do not generally reflect individual age, and major transi-
tions between the 2 types of males do not occur. Based on the frequency of
individuals of both types, Hogan-Warburg (1966) and van Rhijn (1973)
argued that this is a case of a stable polymorphism. Breeding experiments
designed to determine the genetic component of male Ruff behavior have ap-
parently not been done, and it is conceivable that some environmental event
(such as egg hatching order) predisposes males to 1 behavior or the other.
That is, satellite and territorial males may represent 2 modes within a single
strategy.
MIXED STRATEGIES
In a mixed strategy males spend a certain portion of time in 1 behavior
then switch to an alternative. The shift in behavior does not correspond to
any environmental or individual factor such as female availability or age.
Behavioral changes instead are supposed to correspond to a programmed
probability of reproducing when a behavior is performed for a set time. The
mixed strategy concept is difficult to accept since animals capable of chang-
ing behavior should be selected to shift behavior to meet a changed environ-
ment. On the other hand, mixed strategies might be expected if the environ-
ment shifts frequently and in an unpredictable manner. But another dif-
ficulty with mixed strategies is that observers do not detect all stimuli which
an organism perceives. It is not always possible to identify environmental
events which correlate with behavioral changes. One can also suppose that
males differ in the mixture of time spent in the alternative behaviors, and
that these differences represent separate and stable alternatives.
These obstacles are overcome somewhat by detailed observation to
identify events important in the history of an organism, and to determine
individual frequencies of behavior. Such intensive studies on individual male
sexual behavior are very rare. The best study does not involve males, but
female reproductive behavior. Brockmann et al. (1979) analyzed the nesting
behavior of the great golden digger wasp, Sphex ichneumoneus. Female wasps
provision excavated tunnels with katydids on which they lay a single egg.
Wasps usually dig their own burrows, but females will also enter the nest of
another female while the latter is hunting for katydids. Each wasp will
provision the joint nest until they meet and fight, and 1 wasp leaves. Since
there is no individual tendency to dig or enter, a stable polymorphism is
ruled out. Evidence for a mixed strategy is that females entering a pre-
existing hole cannot distinguish occupied nests from abandoned ones, and
digging females sometimes abandon nests for no apparent reason. Most
importantly, the total number of eggs laid by females who had begun se-
quences by entering or digging are roughly equal when female time differ-
ences are considered. Females may therefore partition their time into 2
behaviors based on the probability of reproductive returns which, in some
fashion, is programmed genetically. That is, natural selection could operate
such that a mixed strategy exists within individuals. Brockmann et al.
Florida Entomologist 63(1)
stressed the probable importance of the frequency dependence of the 2 be-
haviors on reproductive success, but there is no indication that wasps are
responding to frequencies as events influencing the behavior adopted. It may
in principle never be possible to rule out environmental events, but female
wasp nesting behavior is a likely candidate for a mixed reproductive
strategy.
Beecher and Beecher (1979) claimed to have documented a mixed repro-
ductive strategy in male Bank Swallows, Riparia riparia. In this species
males routinely establish monogamous pair bonds and invest heavily in their
offspring. Alternatively, males attempt to copulate with females with whom
they are not pair bonded. Males attempt extra copulations by "chasing" a
mated pair when they leave a colony. The male with a mate often fights with
the "sexual chasers", and usually prevents their access to the female. Beecher
and Beecher identified this as a mixed reproductive strategy. The Beechers
maintained that mated males routinely participate in "sexual chases". But
data on the actual frequencies of the 2 behaviors shown by individuals are
not presented. In addition, little consideration was given to social or environ-
mental factors which might predispose a mated male to 1 behavior or
another on a given day. It is premature to label these behaviors a mixed re-
productive strategy. For example, the probability of a male being cuckolded
while he is on a "sexual chase" should strongly influence the male's tendency
to chase. If so, then male Bank Swallow behavior probably represents a
conditional strategy.
These examples underline the difficulty in distinguishing between a mixed
and conditional strategy as mentioned earlier. However, it is important to
retain both concepts since different and testable predictions arise from each
model. As additional research on variant reproductive behaviors becomes
available, deletion of the mixed strategy concept may become desirable. It
is presently more important that this and other terms be clearly defined and
the corresponding data be interpreted according to these definitions.
CONDITIONAL STRATEGIES
Conditional strategies are much easier to demonstrate than fixed poly-
morphisms or mixed strategies and it is probably in this category that most
cases of male variation in sexual behavior should be placed. Under a condi-
tional strategy, a male will behave in a particular way if certain conditions
prevail. In some cases the "decision" concerning the type of behavior per-
formed is reversible with males shifting their behavior depending on the
conditions present at the moment. On the other hand, a "decision" may be
irrevocable and thus require a male to perform in a set fashion from then
on. These "decisions" are made by a genetic program and do not require
conscious evaluation of the environment. Some conditions which might be
important in making behavioral decisionsn" include an individual's size
and/or age, population density, and the frequencies of males performing the
different behaviors.
Age differences are probably 1 of the most important conditions affecting
male reproductive behavior (Howard 1978). Males are generally selected to
increase their expenditure in sexual competition as they age. This relation-
ship results from a general decline in residual reproductive value with age
and represents a decrease in the costs attached to a particular level of ex-
March 1980
Insect Behavioral Ecology-'79
penditure since relatively less future reproduction is jeopardized. The same
general reasoning is used to interpret age-specific differences in reproductive
behavior within and between species (Charlesworth and Leon 1976, Parker
1974, Pianka and Parker 1975, Williams 1966). Howard (1978) extended
these earlier ideas of age-specific behavior and pointed out that older males
are more experienced in competition and will therefore be at an advantage
when matched with younger males, other factors being equal. Females might
also prefer older males since an older phenotype may indicate the presence
of genes which contributed to survival for extended periods. Female prefer-
ence for older individuals would involve genes for features other than sexual
behavior. This stipulation is necessary since under a conditional strategy all
variants have the same genetic mechanism producing the observed behaviors.
Further, many generations of female choice for reproductive behaviors
might reduce genetic variance for that particular trait, but this is a point
of contention.
Howard (1978) studied the age-specific mating patterns of the bullfrog,
Rana catesbeiana, in Michigan (see also Emlen, 1968, 1976). Male R.
catesbeiana mate in 1 of 3 ways: territorial males vigorously defend an area
where they sing and attract females; satellites intercept females attracted
by nearby calling males; and some males are opportunistic and call from
sites which they don't defend, but leave when challenged by other males. All
males perform the 3 behaviors, but territorial males tend to be the largest
and oldest; satellites are usually the smallest and youngest, and opportunists
are intermediate in size and age. (These bullfrogs live from 5 to 8 years.)
Mating success increases significantly with male body length in R.
catesbeiana, such that territorial males have the highest fitness. Little in-
formation is available on the mating success of a male when performing
satellite behavior in this species, but satellites intercepted up to 43% of
attracted females in the green tree frog, Hyla cinerea (Perrill et al. 1978).
Calling and non-calling males are known in other anurans (Wells 1977a, b)
and are probably related to age differences. Individual age may also be im-
portant in the occurrence of "floating" or non-territorial males in many bird
species (Smith 1978), but this is speculative.
Male bullfrog behavior is conditional upon age, but size is also important.
A possible case of a conditional strategy based on size without the complicat-
ing factor of age is in male bees, Centris pallida (Alcock 1976, 1979, Alcock
et al. 1977). In this species larvae develop in the ground with males emerg-
ing before females. Large males patrol specific areas close to the ground
and apparently use olfaction to locate newly molted females. Patrolling
males defend their area against other males. Upon finding a recently molted
virgin, large males dig up and mate with their find. Small males hover well
above the ground and chase after females missed by the larger conspecifics.
Large males are generally more successful, than small males at acquiring
mates. Alcock (1979) identified this as a possible fixed polymorphism, but he
labelled this speculation since no information on genetic differences between
large and small males was available. Male size differences are due, in part,
to the size of the brood chamber and the food fed to males as larvae. Al-
though different genotypes could be involved, this is not a necessary condi-
tion for the types of behavior observed. Small males may maximize their
reproductive success by hovering, since if they patrol they would lose fights
36 Florida Entomologist 63(1) March 1980
with larger males. Males behaving according to the condition "if small
hover," may simply be "making the best of a bad job" (Dawkins 1979) in
that they salvage whatever fitness is possible.
Population density is commonly thought to affect the sexual behavior of
a species. Otte and Joern (1975) modeled the level of territorial defense
expected under varying conditions of density in several grasshoppers. They
reasoned that as density increases the amount of effort invested in defense
also increases. Once the costs attached to defense are such that no net
benefit is likely, males switch to non-territoriality. This model is probably
applicable to many species. The effects of population density are to force
some males into alternative behaviors. This situation will be most pro-
nounced where a few males are able to control resources essential to fe-
males. For example, male Orange-Rumped Honeyguides, Indicator
xanthanotus, control female access to beeswax, an essential ingredient in
this bird's nest. Many males are unable to have territories around bee hives,
and they attempt to steal copulations from territorial males (Cronin and
Sherman 1976).
Males (and females) also monitor the reproductive behavior of com-
petitors and change their own sexual behavior accordingly. One example is
in scorpionflies, Hylobittacus apicalis (Thornhill 1979). Males present prey
to females as a nuptial offering and their fitness is affected by the size and
quality of the "gift". Spider predation is probably a major risk attached to
prey location by males. This cost of reproducing is reduced by males stealing
prey from other males, often by behaving like females. Successful "trans-
vestite" males avoid spiders and acquire females. Thornhill demonstrated
that males display both behaviors depending upon whether a suitable prey
organism or a conspecific male with prey is encountered first. Both of these
factors fluctuate. Thornhill termed these behaviors a mixed hunting strategy,
but in keeping with Dawkins' (1979) classification and that used here, this
situation is representative of a conditional strategy.
Reproductive strategies are often complex and may involve the inter-
action of several variables. It is possible that a single category does not fit
a species well, but a standard terminology facilitates an experimental ap-
proach to the study of these behaviors. Alternative forms of behavior are
usually first noticed by accident, but intensive observations on marked
individuals and experimental manipulation of important biological stimuli
(population density, presence of competitors and predators, etc.) should
generally allow mixed and conditional strategies to be distinguished. Condi-
tional and stable polymorphisms may be more difficult to tell apart. In some
cases males perform 1 behavior all their adult lives, but this might still be a
conditional "decision" based on social or environmental events when the male
was immature. In addition, in species where males switch behavior a stable
polymorphism cannot be ruled out unless the proportion of time spent in
each behavior is roughly equal for all males. A polymorphism could also
consist of 2 conditional strategies, the difference being in the amount of
time allocated to each behavior by the different types of males. In many
cases the necessary information to separate a conditional situation from a
stable polymorphism is the degree to which the alternative forms of be-
havior are inherited.
Insect Behavioral Ecology-'79
PARENTAL INVESTMENT AND ALTERNATIVE BEHAVIORS
Species characterized by alternative male reproductive behaviors are
probably common, but some species have males whose behavior varies little.
Alternative male behaviors should be most common where male reproductive
competition is high (Emlen and Oring 1975). Intense male reproductive
competition is predicted when male parental investment is negligible com-
pared to the female investment (Trivers 1972). In these species, females, by
virtue of their heavy investment of time and energy in eggs and developing
offspring, should mate with the "best" males available. Although a subject
of much interest, male quality may involve individuals being of the right
species, sexually competent, and perhaps some genetic quality of males which
suits them for a particular environment. At any rate, males investing little
parentally increase their fitness by repeated copulations. Males must there-
fore invest as heavily as other males, or they should opt out of the competi-
tion and assume an alternative behavior. (Male options may be exercised in
evolutionary or present time.) Intermediate levels of investment in male
competition should be selected against.
Howard (1978) further developed predictions concerning situations
where alternative behaviors are likely. He applied Orians (1969) model of
female choice and the evolution of polygyny to the occurrence of satellite or
parasitic males. Satellites should associate with males who have a high
probability of attracting females. The reproductive success of satellites is
expected to be equal to or greater than that which satellites would garner if
they were to adopt territorial behavior. Howard's focus was entirely con-
cerned with age and size conditional strategies, but his analysis is applicable
where other types of alternatives occur. Howard also believed that alterna-
tive behaviors should be prevalent where male reproductive success varies
greatly independent of age. Although alternative behaviors should be com-
mon where male parental investment is low and consequently mating effort
is high (Alexander and Borgia 1979), this is largely an untested prediction.
Scorpionflies might represent a possible exception in that the male nuptial
gift is a form of paternal investment (Thornhill 1976). A corollary of male
and female parental investments is a decrease in the degree of sexual
dimorphism. In scorpionflies it is precisely this close resemblance between
males and females which makes "transvestism" possible as an alternative
behavior.
REPRODUCTIVE COMPETITION IN FIELD CRICKETS
Male field crickets (Gryllinae) and other acoustical insects do not usually
contribute paternally (Alexander 1975), although there are many possible
exceptions (Mays 1971, Morris 1978). Mate competition resulting from
negligible paternal investment often takes'the form of acoustical signalling
between males for sexually receptive females. Alexander (1975) and Otte
(1977) reviewed the various forms of male signalling which represent re-
productive competition. Males may be territorial and through intense and
regular singing deter the approach of other males. Singing also attracts
females and a territorial male monopolizes the females in his area, some-
times aided by intense fighting with neighboring males (Alexander 1961,
Morris 1971). In addition, many aspects of male songs result from sexual
Florida Entomologist 63 (1)
March 1980
selection. Characteristics such as intensity, frequency, duration, and timing
are presumably adaptations to particular competitive and mate attracting
situations. (Alexander 1962 described the types of cricket songs.) Many
of these variations in male reproductive behavior are observed between
species or, in some cases, between populations of the same species. But in
several cases variations in male reproductive behavior occur simultaneously
in the same population (Feaver 1977, Otte 1972, Spooner 1968, Walker in
press). This section examines the occurrence of calling and non-calling male
behavior in terms of evolutionairly stable strategies in field crickets, pri-
marily Gryllus integer. Unless otherwise indicated, the following discussion
is based on findings reported elsewhere (Cade 1975, 1976, 1978, 1979a).
Gryllus integer commonly occurs in old fields and other grassy areas in
central Texas. In observations on populations of G. integer in and near San
Antonio and Austin, I repeatedly observed loose aggregations of calling
males within which non-calling males and females also occurred. Males call
for most of the night, although their song intensities vary greatly. Satellite
males walk or remain motionless near calling males and sometimes court
females attracted to the caller. Some non-calling males are also aggressive,
and physically attack callers. These behaviors occur until just before sun-
rise when the number of males calling increases greatly. At dawn non-calling
males still occur, but together with callers and females are often found in
small aggregations beneath rocks or vegetation. The dawn chorus is over in
a few hours and the crickets are usually quiet the rest of the day. Few ob-
servations of satellite matings and the ready attraction of females to tape
recorded songs is circumstantial evidence that calling generally results in
more matings per night than not calling. This presumed benefit of calling,
however, is offset by the acoustical attraction of a parasitoid dipteran,
Euphasiopteryx ochracea, whose larvae dovour the parasitized cricket in ca.
7 days (Fig. 1).
POPULATION DENSITY
When population density is low to moderate, most G. integer males call,
but at high densities, non-callers are common. In August and September the
second generation of G. integer matures and population density in an area
can be very high. In fact, 2600 crickets (most likely G. integer) were re-
ported from a Louisiana cotton field and caused much economic damage
(Folsom and Woke 1939). High population density in Texas was judged by
the number of calling males in an area and by the number of male and fe-
male G. integer observed flying to electric street lights (Cade 1979b).
The tendency for non-calling males to occur in field cricket populations
with increasing density was first demonstrated by Alexander (1961). He
reasoned that the increased probability of random male-female collisions
at high density resulted in increased benefits of not calling and searching
for mates. A higher level of territorial defense and a limit on the number
of suitable territories may also enhance the benefits derived from satellite
behavior. In G. integer, male ability to detect female scents (Otte and
Cade 1976) also benefits non-callers; males probably avoid more fights when
competitors are numerous. But wide areas remain uninhabited by G. integer
at times when satellites are observed elsewhere. These areas are demon-
strated to be suitable by the ready attraction of G. integer to tape recorded
Insect Behavioral Ecology-'79 39
/a-i It
Fig. 1. Female tachinid flies, Euphasiopteryx ochracea, are attracted to
Gryllus integer calling song. Flies deposit living larvae on their host which
burrow into and consume the cricket. Other larvae are deposited in the gen-
eral area of the cricket and may occasionally parasitize crickets attracted
by a male's calling (Drawing by E. Cade from photos by L. E. Gilbert).
calling song when played there. Suitability might, however, be judged in
terms of males already present and calling in an area (Ulagaraj and
Walker 1973), especially if some males are predisposed to non-calling. At
any rate, non-calling behavior is conditional on high density, although the
continued calling of some males demonstrates that the effects of density vary
between individuals.
TEMPORAL EFFECTS
The dawn chorus of G. integer indicates that calling is conditional on the
time of day for some males. It is puzzling that dawn calling occurs when
females are not phonotactic over long distances. Females are already close
to calling males and dawn calling may promote female sexual receptivity
rather than phonotaxis. That is, some females may require that males call
before accepting them as mates. However, in the field cricket, Teleogryllus
oceanicus, females required only the soft courtship song (not the rhythmic
calling song) before mating (Burk 1979): This study was carried out in
the laboratory using virgin females whose sexual receptivity may have been
unusually high. Little information is available on female mating preferences
in the field. Cricket courthship songs are not species specific. If there is a
chance of a heterospecific mating, as in field situations, females are expected
to require the species-specific calling song. Laboratory observations indicate
that females are still sexually receptive and matings occur at night and
around sunrise (Cade unpublished). Bird predators select against phono-
Florida Entomologist 63(1)
taxis by females and aggressive non-calling males, as well as the option for
males to search for females. Dawn calling tends to occur at lower song in-
tensities than earlier in the evening, but this relationship is not significant.
Those males that are calling softly probably avoid most fly parasites. Fly
parasites are still active at dawn, although their attraction to cricket song
is much reduced from that observed at dusk. The conditional behavior of
"call if it is dawn" is, therefore, very complex and is undoubtedly based on
these as well as other factors. It is important to note, however, that not all
satellite males commence calling at sunrise. For example, on 16 July 1979, I
observed 3 males calling in a pile of rocks (ca. 1.7 m x 0.75 m) at sunrise in
a vacant lot in San Antonio. A search of the pile uncovered 8 non-calling
males and 6 females. For the proceeding night I had only heard 1 male
calling in that location.
MALE-MALE AGGRESSION
Male field crickets are very aggressive and fight by kicking with the
hind legs and biting with the mandibles (Alexander 1961, Hsu 1929).
Physical attacks are not that frequently observed in the field, but do occur
between calling males and non-callers, and callers. Physical attacks usually
last but a few seconds with 1 combatant withdrawing. The effect of an
attack on a calling male is to interrupt his stridulation, and, perhaps
occasionally, displace him from his signalling station. [Calling males are
predicted to win these encounters as is the case in some katydids (Feaver
1977)]. If attacked calling males have a reduced ability to monopolize fe-
males in an immediate area, then other callers and aggressive non-callers
benefit, providing females are already present. This is speculative, but
Alexander (1961) demonstrated that dominant males attack subordinants
when the latter start to sing. Playback of taped calling song to calling males
also showed that some males adopt non-calling behavior when "threatened"
by a neighboring male. And some non-calling males commence calling when
neighboring callers become silent (and perhaps less "threatening"). The
conditional behavior of "call if aggression is unlikely" is quite complex.
Male size may also be involved in fighting ability (Alexander 1961, Cade,
unpublished), but fighting and calling are not necessarily that closely cor-
related, at least in field populations.
INDIVIDUAL DIFFERENCES
Aggression, density and time have effects on male reproductive com-
petition in G. integer and other field crickets, but important questions re-
main regarding the degree of individual differences. A high frequency of
fly parasitism in calling males compared to a low frequency in non-callers
may reflect an individual bias in acoustical behavior. This tentative con-
clusion is also based on observations of caged crickets, and on limited ob-
servations in an outdoor arena in Texas. More recently, intensive observa-
tions on an outdoor-arena population of G. integer in St. Catharines have
been carried out. Data on the individual acoustical behavior of males have
also been obtained from sound-relay monitored jars. This information in-
dicates that some male G. integer call very often, while others call very
infrequently. A few do not call. Differences in the acoustical behavior of
March 1980
Insect Behavioral Ecology-'79
reproductively mature males does not correlate with male size or age (Cade
and Wyatt, in prep.).
STRATEGY OR STRATEGIES
Alternative forms of male reproductive competition in G. integer involve
individual biases in behavior. But it is still impossible to distinguish between
a stable polymorphism with at least 2 strategies, or a single conditional
strategy with at least 2 behaviors. It is clear that calling behavior is con-
ditional with a complex interaction of factors affecting the "decision" to
call. The problem is in determining the underlying cause of non-calling be-
havior. The fact that some males do not call, or call at very reduced levels,
does not necessarily indicate a separate satellite strategy, but it remains
a possibility. A satellite strategy could be pure, or it could, more likely, be a
conditional behavior. A conditional satellite strategy is more likely since
males having such a genetic make up should be selected to call if no calling
males are available to parasitize.
If 2 conditional strategies are present in male G. integer, the poly-
morphism may be stable with the reproductive success derived from the 2
modes being roughly equal. Frequency dependence should be very important
in bringing about a fitness equilibrium (Brockmann et al. 1979, Dawkins
1979). Satellites would, for example, benefit more reproductively when there
are many callers and few non-callers. As selection resulted in increased
numbers of non-callers, the benefits attached to this behavior would decrease.
Frequency dependence should also be important in the behaviors of indi-
viduals even if there is but 1 conditional strategy in this species.
Direct evidence on the mating success of satellite and calling males is
not available. To estimate relative fitness I played taped G. integer song and
attracted flying crickets. Some attracted males typically began calling, and
others behaved as satellites. Attracted females walked in the general area
of the loudspeaker where they were courted by satellites. The satellites mated
infrequently, whereas females were readily attracted to the tape recordings.
In addition, I have observed only 1 mating by a satellite in the field (Cade
unpublished). But in the local arena satellites were often seen with females,
and the females sometimes had attached spermatophores indicating a recent
mating. At any rate, male mating frequency may not be a good estimate of
reproductive success since female G. integer mate many times (Sakaluk and
Cade 1980), and there is probably a high level of competition among sperm
from different males for eggs. More information on female mating prefer-
ences is necessary to judge the witnesses of males showing different behaviors.
Acoustically orienting flies, Euphasiopteryx ochracea, affect calling male
fitness. The level of fly parasitism fluctuates widely between summers (Cade
unpublished), and so must the resulting .longevity of callers. Calling and
non-calling males also occur in G. pennsylvanicus, a northern species ap-
parently free of fly parasitism in St. Catharines (Wyatt and Cade in
progress). In this species males are probably more flexible in their behavior
than male G. integer. If calling and non-calling behaviors in field crickets
in general evolved when flies were not present, the later exploitation of
cricket acoustics by flies should have lowered the fitness derived from calling
behavior. Otte (1977) described a potential sequence for the loss of calling
ability in some crickets, a trend seen fairly often (Walker 1974). In addi-
Florida Entomologist 63 (1)
March 1980
tion, the seasonal distribution of a silent cricket species, G. ovisopis, overlaps
greatly with E. ochracea in Florida (Mangold 1978, Veazey et al. 1976).
If calling and non-calling crickets represent separate strategies then fly
parasitism may be an agent maintaining both behaviors or 1 which favors a
shift to silence. But distinguishing between stable and unstable poly-
morphisms is a bit premature. In G. integer and in some other cases previ-
ously reviewed, it is very important to determine the genetic and environ-
mental factors contributing to male sexual behavior. Another immediate goal
is for researchers to adopt a common terminology in describing the various
possibilities. The terms of ESS are suitable for this purpose.
ACKNOWLEDGEMENTS
Research on sexual selection in acoustically communicating insects is
funded by the Natural Sciences and Engineering Research Council of
Canada through an individual operating grant (A6174) and by the Depart-
ment of Biological Sciences, Brock University. I thank D. Hickey, E. Cade,
R. D. Morris, S. Sakaluk, J. E. Lloyd and T. J. Walker for commenting on
the manuscript. Special thanks goes to J. E. Lloyd for inviting me to present
this paper at the 1979 meeting of the Florida Entomological Society. S. Wal-
lace and R. French provided expert typing of the manuscript and made help-
ful comments on its preparation.
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PHONOTAXIS IN MOLE CRICKETS:
ITS REPRODUCTIVE SIGNIFICANCE1
T. G. FORREST
Dept. of Entomology and Nematology
University of Florida
Gainesville, FL 32611 USA
The southern mole cricket, Scapteriscus acletus, is known throughout
the Southeast as an important agricultural and turfgrass pest. Several
decades of research on these insects have not yielded satisfactory control
methods, perhaps because little has been learned of their basic biology and
reproductive behavior. This lack of knowledge stems from the fact that
mole crickets are burrowing crickets, spending most of their lives under-
ground.
Male and female external morphologies are identical except for the fore-
wings. Male S. acletus, as in many cricket species, produce sound to attract
sexually responsive females (Alexander 1975). The sound producing ap-
paratus is manifest as a black spot on the male's forewing; it consists of a
scraper and a stridulatory file on each forewing. Sound is produced during
stridulation when the scraper of one wing rubs the file of the other wing.
Although this apparatus is typical of acoustical crickets, mole crickets
are unique in their acoustical behavior. Males call from within special bur-
rows they construct each night prior to calling. Using their fossorial fore-
legs and large pronotum, males pack and shape the opening of their burrow
into an exponentially expanded horn. Bennet-Clark (1970) has shown that
this shape amplifies male calling songs in 2 European mole crickets, Gryl-
lotalpa gryllotalpa and G. vineae. This amplification probably holds true for
S. acletus (Nickerson, Snyder, and Oliver 1979). Male S. acletus produce a
continuous trill during the calling period. This song is species-specific with
a carrier frequency of about 2.7 kHz modulated at 50 pulses per second
(Ulagaraj 1976).
I placed individual S. acletus males in soil-filled, 19-liter buckets. These
buckets were covered with aluminum screen to prevent the male escaping,
placed in a pit, and surrounded by a trapping device (Fig. 1). Males could
then be observed for calling behavior and responding animals trapped
around the buckets. A modification was made to assess flight from buckets:
the aluminum screen cover was removed and the entire trap covered with a
cylindrical hardware cloth cage. Individuals flying from buckets hit the cage,
fell, and were trapped around the buckets.
Twelve S. acletus males were monitored for nightly calling period with
respect to sunset (Fig. 2a). Individual males differed significantly in their
1Florida Agricultural Experiment Station Journal Series No. 2245.
Florida Entomologist 63(1)
March 1980
-Plywood Donut
5cm
' Soil Ground (Soil)
Bucket
Pit
Fig. 1. Bucket trap. Scapteriscus acletus males were placed in soil-filled,
19-liter, plastic buckets and observed for calling behavior. Animals attracted
to calling males were trapped around the bucket and an aluminum baffle pre-
vented escape. Flying mole crickets were trapped in inner donut A; those
crawling toward males were caught in outer donut B.
starting times and each male also showed smaller variation in its starting
time than in its stopping times. This smaller variation suggests some im-
portance in starting at this particular time or in not starting prior to the
time. Starting of calling correlates with starting of female flights, as meas-
ured by observing females confined in buckets (Fig. 2b). Males starting to
a Male Calling Period: S ac/elus (n12)
bAre--tt\------------- --- -----
----- -----v -
b Average Storting: Calling and Flight
LINHG -- (n :12d)
20 30 4 50 60 70
Minutes after Sunset
80 90 100
+cl0
110 12,
Fig. 2. a) Twelve S. acletus males caged outdoors were monitored for 12
nights for calling period with respect to sunset. Vertical lines are means,
horizontal lines are ranges, bars represent 95% confidence intervals of means.
Significant individual differences in starting times are evident, b) Fifteen
S. acletus females caged outdoors were observed for start of flight. Starting
of flight and male calling are closely correlated.
Insect Behavioral Ecology-'79
call too early would be wasting energy whereas those starting too late would
not attract early flying females.
Scapteriscus acletus flights occur from April to July in the spring with
a smaller flight from October to January in the fall. These flights consist of
about 80 percent females, and both males and females respond to calling
males (see below). These flights are the major form of dispersal in mole
crickets and allow a flying individual to monitor a large number of calling
males. If a flying female can hear calling males only if they are closer than
6 m (a conservative assumption), if flight speed is 11.8 km/h (Ulagaraj
1975), 0.01/m2 (Kleyla and Dodson 1978), a female in straight-line flight for
5 minutes should hear more than 60 calling males.
Females therefore have the opportunity to assay a large number of call-
ing males. If there are differences (significant to female reproduction-see
below) in these males revealed in their calls, then females should selectively
respond to certain males. High nightly variances in numbers attracted to
individual calling males in bucket traps suggest that females choose certain
males over others. Four males calling within 20 m of each other on 3
nights attracted totals of 66, 32, and 16 mole crickets. Each night 1 of the 4
males attracted a disproportionate share of the totals: 43 (65%), 28 (87%),
and 9 (56%) respectively. What parameters of the call do individuals use to
selectively respond to the call?
Until recently, prior to the revived interest in sexual selection, the chief
concern with acoustical insects was whether females responded principally,
or only, to conspecific calls (Alexander 1975). Conspecific attraction was
convincingly demonstrated by flying S. acletus. Of 179 S. acletus attracted to
12 S. acletus males and 12 S. vicinus males, only 2 were trapped at the
heterospecific call of S. vicinus, a number equaling that trapped at controls
(Table 1). Ulagaraj and Walker (1975) showed that this specificity was due
to differences in pulse rates and carrier frequencies of the 2 calls.
Scapteriscus acletus males show so little variation in those 2 param-
eters (Ulagaraj 1976) that it seems unlikely that females use them to choose
among conspecific males. Intensity, however, is one parameter that varies
greatly between males and in individual males on successive nights. More
than 100 years ago, Charles Darwin noted the importance of intensity in
female choice and male competition in acoustical Orthopterans.
". those individuals which were able to make the loudest or most con-
tinuous noise would gain partners before those which were less noisy. .."
Are females actually selecting louder males or is it that a louder call
travels farther and is therefore heard by more females? Increasing the
intensity at the sound source by 6 decibels (dB) will approximately double
TABLE 1. SPECIFICITY OF RESPONSE TO CAGED CALLING MALES BY S. acletus.
BUCKET TRAPS (FIG. 1), GREEN ACRES FARM, UNIVERSITY OF
FLORIDA, MAY 1979.
Sound source Number attracted
Conspecific (S. acletus) 175
Heterospecific (S. vicinus) 2
Control (No male) 2
Florida Entomologist 63(1)
the distance at which the sound can be heard. Sound radiates in all direc-
tions from the sound source. Predictions that can be made as to the effect of
a 6 dB increase in intensity on response to the call included these 3: 1)
If individuals fly in a single plane, maintain straight line courses of flight,
and come from outside the area of the sound field, twice as many should
respond. This doubling corresponds to the doubling of sound field diameter.
2) If individuals fly in one plane in a randomly changing direction or if they
come from within the sound field area, a 4-fold increase would be expected,
corresponding to the increase in sound field area. 3) If individuals fly
randomly at all heights there would be a predicted 8-fold increase in re-
sponse, corresponding to the increase in sound field volume. It does not seem
likely that this last prediction can hold true. Flying insects increase risks
and energetic costs at altitudes above or below some "optimal" height that
varies with the insect and the circumstances of the flight. Mole crickets, for
example, must fly high enough to avoid obstacles and low enough to detect
calls and minimize energetically expensive ascending flight. Most would be
expected to fly at nearly the same height on a given evening over given
terrain. Small variances in altitude of flight are known to be the case for
migrating butterflies (daytime) and migrating moths (night) (e.g. Arbo-
gast 1966, Schaefer 1976).
Individual S. acletus males in bucket traps were monitored for nightly
intensities during their calling period. Maximum intensity at a distance of
15 cm from the funnel opening was measured using a Model 2219 Bruel and
Kjaer sound level meter. Intensity rarely changed more than 1 dB during
the nightly calling period. Individuals attracted to the calling males were
counted at the end of the calling period.
When calling males were classified nightly as high or low intensity males
differing by 3-5 dB, on only 1 night (of 5) did a low intensity male attract
any individuals (Table 2). Total numbers attracted to high intensity males
were 52 compared to 3 attracted to low intensity males for the 5 nights. High
intensity males averaged 10 times as many attracted individuals per male
per night as low intensity males (Table 2). Differences other than intensity
TABLE 2. SIx NIGHTS WHEN CALLING MALES NO MORE THAN 20 METERS
APART COULD BE SEPARATED INTO HIGH- AND LOW-INTENSITY
CALLERS WITH THE GAP BETWEEN THE CATEGORIES 3-5 dB. No
INDIVIDUAL OCCUPIED THE SAME POSITION MORE THAN ONCE IN THE
5 NIGHTS.
Number of Number of Mole
Interval Callers Crickets Trapped
Date (dB) low dB high dB low dB high dB
11 Apr. 5 1 2 3 29
13 Apr. 4 2 1 0 3
15 Apr. 3 1 3 0 6
18 Apr. 3 1 2 0 6
21 Apr. 4 1 2 0 8
Average 1.2 2 0.6 10.4
Average/Male/Night 0.5 5.2
March 1980
Insect Behavioral Ecology-'79 49
in male calls were not controlled and could explain some differences in
attraction.
Mole cricket calls can be synthesized by electronic "artificial crickets,"
small, self-contained units that produce identical, constant signals at con-
trolled intensities. With these sound units it was possible to test flying mole
cricket response to the equivalent of identical calling males differing in in-
tensity alone.
Two blocks of 3 treatments each were tested for 22 nights. Treatments
consisted of: 1) high intensity (range 107-111 dB); 2) low intensity (6 dB
below high intensity); 3) control (no sound source). Intensities were meas-
ured 15 cm above the speaker. Signal output, calibrated weekly, was a 2.7
kHz carrier frequency modulated at 50 pulses per second.
Catching devices were the same as Ulagaraj and Walker (1975) and
were placed on the circumference of a 20 m diameter circle. Each of the
6 positions were 10 m from the circle center and adjacent treatments.
Treatments were randomized so that each treatment appeared in every
position within a block over a 3 night period. Sound units were assigned
a sequence around the circle and this sequence was unchanged with each
unit remaining within 1 of its original position.
The numbers caught in similar treatments were summed each night. No
mole crickets were trapped in controls during the 22 nights of testing. When
the ratio of numbers caught in high intensity traps to numbers caught at
low intensity traps is plotted against their sums (Fig. 3), the slope of the
regression line does not differ significantly from 0. High intensity traps
EFFECTS OF 6dB INCREASE: S. acletus
12
C
S10 ** *
S8-
6 -
3 0
*
r 4
0 2-
0 200 400 600 800 1000
TOTAL CAUGHT
Fig. 3. Results of 22 nights of broadcasting artificial S. acletus calls at
2 intensities 6 dB apart. Each dot is a nightly ratio of numbers trapped at
high intensity calls to numbers trapped at low intensity calls. Dashed line is
overall ratio (5.7). These results differ from those of Ulagaraj and Walker
(1975) and can be explained by female choice but not by simple physical
models.
Florida Entomologist 63(1)
March 1980
showed nearly a 6-fold increase in response compared to low intensity traps.
This increase is significantly higher (Table 3) than the 2 or 4-fold increase
expected for the 6 dB increase in intensity (see predictions above). Ulagaraj
and Walker (1975) reported a doubling in response with a 6 dB increase.
They used tape players, amplifiers, and speakers of questionable quality
and the calls may have been distorted at higher intensities.
It appears that smaller differences in intensities of naturally calling
males make larger differences in response (10-fold for 3-5 dB difference-
natural males; 6-fold for 6 dB difference-"artificial crickets"). The arti-
ficial crickets, both high and low intensities, were much higher in intensity
than natural males; perhaps selectivity decreases when the intensities com-
pared are both abnormally high. Morris et al. (1977) have shown that sound
power (intensity) is an important factor in response of females Conocep-
halus nigropleurum to taped male calls. I have shown that flying mole
crickets are selectively responding to louder calls and that they must be able
to distinguish between relative intensities of calls at the source.
To determine what affects the intensity of males in the field, 4 large males
(from the upper third of the male size range) and 4 small males (from the
lower third of the male size range) were monitored 15 days for intensity
(Fig. 4). Intensities were measured as before.
Two things appeared to affect intensities of males. After rainfall the
calls of both large and small males increased in intensity (Fig. 4). As days
passed without rainfall, and soils dried, intensities of calling gradually de-
creased over successive nights. Soil moisture probably affected the males'
ability to construct efficient exponential horns, and intensity output lowered.
The second factor affecting calling intensity was male size. Although ranges
overlapped, the average intensity of the large males was higher than that
for small males on every night. Male tegmina have certain sound resonating
membranes. A larger male is able to apply more power to larger membranes
and therefore would produce a call of higher intensity.
Why do flying mole crickets select louder males? Female mole crickets
build egg chambers in the soil and therefore soil moisture is an important
factor in egg deposition (Hayslip 1943). Females may use intensities of
males to locate areas of moist soil to lay eggs. Females may also use relative
intensities of males in an area as a cue to male size. Females responded to
higher intensity calls and therefore larger males who on the average are
better equipped genetically to acquire needed resources.
Male response to calling or tapes of calling conspecific males have been
shown to occur in several acoustical Orthopterans (e.g. Gryllus integer,
Cade 1979; Orchelimum spp., Feaver 1977, Morris 1971; Scapteriscus spp.,
TABLE 3. COMPARISON OF NUMBERS OF S. acletus TRAPPED AT 107-111 dB
("HIGH") AND AT 6 dB LOWER INTENSITY ("LOW").
Total catch (22 nights) 2979
Total catch (high) 2536
Total catch (low) 443
Ratio estimate (high/low) 5.7
95% Confidence interval 5.2-6.3*
*Binomial distribution p=0.85
Insect Behavioral Ecology-'79 51
90-
U t\
0 --
70 -
Large males
Small males
Ranfll Effect of Rainfall
and Male Size
on Intensity of Calling
0 I I I I I
TIME (Days of calling)
Fig. 4. Effects of soil moisture and male size on intensity of calling by
S. acletus males: large males (N=4) and small males (N=4) were mon-
itored nightly (20 May-4 June 1979). Squares and circles are mean inten-
sities of large and small males respectively. On any given night the calls of
large males were more intense than small males. Intensities increased for
males of both sizes after rainfall and gradually decreased over subsequent
successive dry days.
Ulagaraj and Walker 1973). Ulagaraj and Walker (1973) and Mangold
(1978) have shown that males of other acoustical Orthopteran species
(Neonemobius mormonius, N. cubensis, Oecanthus niveus, 0. celerinictus,
and Gryllus rubens) respond to taped calls of S. acletus. These cricket spe-
cies have mating calls with pulse rates similar to S. acletus and are all flying
crickets. This suggests that male response may be widespread, especially in
crickets that disperse by flight. Flying males can monitor calls to locate
suitable habitats to land. Flying male mole crickets may respond to louder
males to locate areas of high soil moisture and thereby good calling sites.
Increased soil moisture increases intensity of calling resulting in increased
numbers of females responding. Flying males may land near calling males
because of the females that are attracted. Most females have mated before
the first seasonal flight (Ulagaraj 1975). This raises the possibility that
males and females are able to find each other by other means-underground
or walking on the surface. Flying males may land near calling males and
search for females. Cade (1979, 1980) has demonstrated alternative male
tactics in the field crickets (Gryllus integer). Reasons for these alternative
behaviors include pressures on calling males who attract parasitoid flies,
Euphasiopteryx ochracea, and other conspecific males that may attack the
Florida Entomologist 63 (1)
caller. These parasitoids are also attracted to S. acletus calls (Mangold
1978); this result may be due to similarities in pulse rates of S. acletus and
G. integer calls.
The mating system of S. acletus appears to have a high amount of fe-
male choice resulting in high variances in the numbers attracted to indi-
vidual calling males. This selectivity correlates with calling intensity to a
degree greater than is predicted by physical models about sound fields. I
have shown that calling intensities are affected by soil moisture and male
size, and I have suggested reasons why intensities may be important in the
response of flying mole crickets. There are, however, questions that must be
asked but can not be answered at this time. 1) Can males mate with or
sequester more than 1 female on a given night? The individuals responding
to a male calling in a trapping device were unable to influence the male's
behavior. A male may stop calling after only 1 female enters his burrow and
therefore no other mole crickets may enter that evening. Preliminary tests
were inconclusive. 2) Do all females that respond to a male's call mate with
that male? Females responding to calls have previously mated. They may
use calls to locate suitable habitats and lay eggs fertilized by another male.
3) What do responding males do once they have landed near a calling male?
Do they run into the burrow and fight with the caller? Do they search for
females that the male is attracting? Are they using his call to locate a good
calling site and will they wait until the following night to compete for fe-
males by calling?
These questions and others must be addressed before male reproductive
success can be evaluated by the response of mole crickets to calls. This sys-
tem, because of its high amount of female response, offers an unparalleled
opportunity to study female choice in phonotaxis to male calls of acoustical
Orthopterans.
ACKNOWLEDGEMENTS
I thank Dr. Thomas J. Walker for his helpful criticism throughout the
research project, symposium, and writing of this manuscript. I appreciate
the encouragement and assistance of Dr. James E. Lloyd, and thank John
Sivinski and Bob Sullivan for help with the manuscript. Thanks go to Susan
Wineriter for the illustrations. William Oldacre, Oldacre Engineering,
Gainesville, FL developed and manufactured the "artificial crickets."
REFERENCES CITED
ALEXANDER, R. D. 1975. Natural selection and specialized chorusing behavior
in insects. Pages 35-77 in Insects, science and society. Academic Press,
New York.
ARBOGAST, R. T. 1966. Migration of Agraulis vanilla (Lepidoptera,
Nymphalidae) in Florida. Fla. Ent. 49(3): 141-5.
BENNET-CLARK, H. C. 1970. The mechanism and efficiency of sound produc-
tion in mole crickets. J. Exp. Biol. 52: 619-652.
CADE, W. H. 1979. The evolution of alternative male reproductive strategies
in field crickets. Pages 342-79 in M. S. Blum and N. A. Blum, Eds.
Sexual selection and reproductive competitions in insects. Academic
Press, New York.
-- 1980. Alternative male reproductive behaviors with special reference
to field crickets. Fla. Ent. 63: 30-45.
March 1980
Insect Behavioral Ecology-'79
FEAVER, MARIANNE. 1977. Aspects of behavioral ecology of three species of
Orchelimum (Orthoptera:Tettigoniidae). Ph.D. dissertation, Univ.
Michigan, Ann Arbor (Univ. Microfilms International, Ann Arbor).
199 p.
HAYSLIP, N. C. 1943. Notes on biological studies of mole crickets at Plant
City, Florida. Fla. Ent. 26: 33-46.
KLEYLA, P. C., AND G. DODSON. 1978. Calling behavior and spatial distribu-
tion of two species of mole crickets in the field. Ann. Ent. Soc. Am.
71: 602-4.
MANGOLD, J. R. 1978. Attractions of Euphasiopteryx ochracea, Corethrella
sp. and gryllids to broadcast songs of the southern mole cricket. Fla.
Entomol. 61: 57-61.
MORRIS, G. K. 1971. Aggression in male Conocephaline grasshoppers (Tet-
tigoniidae). Anim. Behav. 19: 132-7.
MORRIS, G. K., G. E. KERR, AND J. H. FULLARD. 1977. Phonotactic prefer-
ences of female meadow katydids (Orthoptera:Tettigoniidae:Cono-
cephalus nigrophleurum). Can. J. Zool. 56: 1479-87.
NICKERSON, J. C., D. E. SNYDER, AND C. C. OLIVER. 1979. Acoustical burrows
constructed by mole crickets. Ann. Ent. Soc. Am. 72: 438-40.
SCHAEFER, G. W. 1979. Radar observations of insect flight. Roy. Ent. Soc.
London Symp. 7: 157-97.
ULAGARAJ, S. M. 1975. Mole crickets: Ecology, behavior, and dispersal flight
(Orthoptera:Gryllotalpidae:Scapteriscus). Env. Entomol. 4: 265-273.
S 1976. Sound production in mole crickets (Orthoptera:Gryllotalpidae:
Scapteriscus). Ann. Ent. Soc. Am. 69: 299-300.
AND T. J. WALKER. 1973. Phonotaxis of crickets in flight: attraction
of male and female crickets to male calling songs. Science 182: 1278-9.
AND 1975. Responses of flying mole crickets to three param-
eters of synthetic songs broadcast outdoors. Nature 253: 530-2.
DIVERSITY IN THE NESTING BEHAVIOR
OF MUD-DAUBERS
(TRYPOXYLON POLITUM SAY; SPHECIDAE)*
H. JANE BROCKMANN
Department of Zoology
University of Florida
Gainesville, FL 32611 USA
The pipe-organ mud-dauber, Trypoxylon politum Say (Sphecidae:
Larrinae), constructs long tubular mud nests under bridges and in tree
holes. The female provisions each cell of her nest with paralyzed spiders,
lays an egg and seals the cell with a plug df mud (Cross et al. 1975). Build-
ing a new mud nest is the commonest method of acquiring one, but there are
at least 4 other ways. A female may abandon her nest at any stage in the
nesting sequence and another female may take it over. Sometimes a wasp
moves into a nest that is occupied by another, and the 2 then jointly pro-
vision the same brood cell. Occasionally a wasp parasitizes a conspecific by
*University of Florida Agricultural Experiment Station Journal Series No. 2232.
Florida Entomologist 63(1)
March 1980
breaking open the mud partition, removing the egg and replacing it with 1
of her own. Finally, Barber and Matthews (1979) have shown that pipe-
organ mud-daubers also use trap-nests, hollow twigs, or other existing
cavities. Whenever animals are found to have more than 1 way of achieving
the same functional end, we are presented with a most intriguing biological
problem: How are these differences in behavior of individuals maintained in
the population? It is very unlikely that all patterns would be equally success-
ful. Why is the inferior one not eliminated through the action of natural
selection?
I observed similar variation in the nesting behavior of the golden digger
wasp, Sphex ichneumoneus (L.) (Sphecidae; Sphecinae). The principles
developed during the Sphex study may shed some light on mud-dauber
behavior. At least superficially the nesting of the 2 species is similar.
Golden digger wasps dig burrows (frequently abandoning newly dug holes),
provision them with several paralyzed prey, lay an egg and seal the burrow
with soil (Brockmann and Dawkins 1979). As in mud-daubers, these wasps
are usually solitary, but occasionally 2 females jointly provision the same
brood cell. They viciously defend their nests from the intrusion of con-
specific females and in both species joint nesting usually ends in a fight
with only 1 of the 2 wasps laying an egg on the jointly-provided cache of
food. Golden digger wasps also nest in the abandoned nests of conspecifics
(but never in trap-nests).
Richard Dawkins, Alan Grafen, and I (Brockmann et al. 1979, Brockmann
and Dawkins 1979) tried to develop a model that would explain the diversity
of nesting behavior in S. ichneumoneus.1 If joint nesting were a functional
alternative to nesting alone, then joining and founding (starting a new nest
alone) behavior should be, on average, equally successful. Using the rates of
laying eggs as a measure of reproductive success, we found that when a
wasp joined another (or was joined) she was much less successful than when
she nested alone. This result suggests that joining behavior is being selected
against in our populations of digger wasps. Why, then, is joining so com-
mon?2
We found a possible explanation when we discovered that wasps who nested
in existing burrows utilized occupied and unoccupied nests in proportion to
their availability in the nesting area. This suggests that the wasps were not
distinguishing between occupied and unoccupied burrows, and were simply
using any suitable existing burrow they could find. We define, then, 2 ap-
parent nesting strategies: in 1, called "digging", wasps dig new nests and
in the other, called "entering", wasps use already existing burrows. After
entering there are 2 possible outcomes: sometimes the wasps end up in an
abandoned burrow by themselves, and sometimes the wasps end up in a nest
with another. Joint nesting, then, is not really a nesting strategy at all, but
rather a by-product of using already existing nests (since they do not tell
the difference between occupied and unoccupied burrows). We also found
that apparently the wasps dig or use existing burrows independently of
previous decisions, past success or searching difficulty, and that the 2
strategies do not show individual or seasonal variation or biases. It is as
though the animals are programmed with a decision rule that says, "dig
'This and subsequent superscript numbers refer to comments recorded in an Appendix,
p. 62.
Insect Behavioral Ecology-'79
with probability p, enter with probability 1-p". If the wasps are in fact pro-
grammed with such a stochastic rule (called a "mixed" strategy by ESS
theorists), then we expect on the theoretical grounds given by Maynard
Smith (1974) that the frequencies of digging and entering decisions will be
set by natural selection at a value such that the 2 are equally successful.
This, in fact, appears to be the case in 1 well-studied population of golden
digger wasps. The success of individuals (number of eggs laid divided by
the time spent on that nesting strategy) on the occasions when they dig
(including searching time) is approximately equal to the success of in-
dividuals on the occasions when they enter already existing burrows (includ-
ing occupied and unoccupied). It appears that digging and entering may be
2 functionally alternative nesting strategies.
But is equal success sufficient to maintain 2 such alternatives in a popu-
lation? It would be, only if the 2 strategies remain equally successful
through evolutionary time-which would seem most unlikely. There is an-
other feature to the model we developed which makes the long-term main-
tenance of alternative strategies more likely, namely frequency-dependence.
Digging a burrow is a costly, time-consuming undertaking. When a wasp
chooses to enter, she avoids the cost of digging but she may pay another
cost: she risks finding another wasp in possession and we have seen that
joint nesting is relatively unsuccessful. Whether she digs or enters, she may
be joined by another wasp. This is also less desirable than nesting alone.
When there are many wasps choosing to dig, there are many burrows being
made available for wasps that choose to enter. This means that as digging
increases in frequency, entering becomes more profitable. On the other hand,
as entering becomes more common, empty available burrows are correspond-
ingly less abundant, and the entering wasps increasingly run the risk of
joining another wasp. This has the effect of reducing the profitability of
entering when it is common. The frequency of digging relative to entering,
then, is held in balance by the kind of frequency-dependent advantage just
described. The mixed strategy, "dig with probability p enter with probability
1-p", is said to be evolutionarily stable, and the population exists at an
evolutionarily stable state with respect to these 2 forms of nesting.
Whenever there are alternative behavioral patterns being followed by an
animal, decisions or choices are being made. By decision I do not mean any
conscious action, but only that the animals are programmed to follow a
particular course of action; at a decision point an animal may change to a
different behavior. These programmed rules of behavior are the result of
natural selection just as surely as are the rules that govern morphological
development. Although there are 4 kinds of nesting activities in the digger
wasp, these apparently result from only 1 decision, whether to dig or enter.
Similarly, although wasps occasionally "usurp" the nests of other females,
this results from a decision to enter nests' which might have been abandoned,
not from a positive decision to usurp (Brockmann and Dawkins 1979).
The dig/enter mixed strategy may be unusual. What appear to be 2
alternative strategies may turn out to be the outcomes of 1 conditional
strategy. A conditional strategy is a programmed rule of behavior which is
followed only in particular circumstances. For example, in some bees large
males pursue 1 highly profitable mating pattern and small males pursue
other less successful ones (Alcock 1979, Alcock et al. 1976, 1977, 1978, Bar-
Florida Entomologist 63(1)
rows 1976). All individuals may be said to be programmed with the same
conditional rule, "if large, guard emergence sites; if small, patrol the area
looking for unmated females." There is no particular reason to expect that
2 behavioral patterns of 1 conditional strategy will be equally successful
(Dawkins 1980). In order to explain the presence of diverse patterns of be-
havior, the biologist must determine (1) the nature of the decisions that the
animals are making, (2) the outcomes of those decisions and (3) whether
or not the decisions are conditional on some particular circumstance. If, as
in the case of the digger wasps, we are unable to find any conditional
strategy (based on past success, searching difficulty, time of year, etc.), and
if we can find, as we did, a possible frequency-dependent advantage, then it
is plausible to hypothesize that the behavior is maintained as a part of a
mixed evolutionarily stable strategy in the population.3
I do not yet know whether the diverse nesting behavior found in pipe-
organ mud-daubers is an evolutionarily stable mixture or not, but I believe
that the concept may apply to some of the nesting patterns. Before going
into this, it is necessary to give more background on the wasps, their nesting
behavior and the manner in which I observed them.
I observed the behavior of pipe-organ mud-daubers under a bridge over
Hatchet Creek, Alachua County, FL.4 We individually marked 128 female
and 152 male wasps.5 Many were never seen again or appeared under the
bridge only briefly and then disappeared. We observed 83 females as they
built 103 mud nests for a total of 319 brood cells (mean 3.4 cells per mud
tube). We have complete records on all activities associated with 132 of these
cells. Running commentary notes were taken from about 0900 to 1700 each
day of the study. Since all wasps were individually marked, we knew when
more than 1 female was using a nest, when the female that had built a nest
was (or was not) using it and when a female was marauding the nest of
another. We also more casually observed the behavior of other species of
wasps which were nesting under the bridge.
At the beginning of a nesting sequence, a female flies about the nesting
area, presumably looking for a suitable place to build. She frequently sticks
her head into or briefly enters the nests of other wasps, and is often repelled
by a lunge and bite from the resident male (see below). She may walk re-
peatedly along 1 side of or on top of an active or old nest. After a sequence
of searching which lasts from an hour to most of a day, the female begins to
build, normally next to or on top of a new or old nest, rarely (4% of 103
nests) extending an old nest. Building a nest is a time-consuming process:
it may take 1 to 2 days to complete the outside of a 7 cm nest and line the
inside with a layer of mud. The female may abandon the nest after she has
completed the outside or after completing the entire nest.6 She may then
start another nest under the bridge or she may disappear altogether. Some-
times a female completes 1 or more cells ,before abandoning the nest. These
partially built or partially provisioned nests are readily adopted by other
females who repair them if damaged or line them with more mud if neces-
sary (Fig. 1).
The mud-dauber provisions her nest with any of a number of species of
locally available spiders (Muma and Jeffers 1945, Dorris 1970, Cross et al.
1975). After accumulating from 3 to 12 prey, she lays a large egg and then
immediately builds a mud partition. The partitioning takes only a few
March 1980
Insect Behavioral Ecology-'79
PARTITION OR
INTERCELLULAR
PLUG
S
Fig. 1. A flow diagram of the nesting behavior of Trypoxylon politum.
"S" refers to the searching behavior that precedes a nesting sequence. The
observed percent of brood cells (N = 132) completed using each nesting pat-
tern is given (except for trap-nesting which is estimated for another popula-
tion by Barber and Matthews 1979).
minutes, although she may continue to add mud for half an hour or more,
particularly if it is the last cell in the nest. In 2 or 3 days the egg hatches
into a larva which consumes the provided food and then spins a cocoon in
which it remains until the following spring when it pupates and emerges as
an adult (Cross et al. 1975).
In T. politum and other species in this subgenus (Trypargilum), males
show a most un-hymenopteran-like pattern. They remain in a female's nest
near the entrance and guard it from the intrusions of parasites, other males,
and females. A male may join a female's nest at any stage during the nest-
ing process and he may even help her: if he joins a nest while she is still
building it, he may smooth the wet mud on the inside walls of the tube with
his mandibles, just as a female does; if he is present while she is provision-
Florida. Entomologist 63 (1)
March 1980
ing the nest with spiders, he may push the spiders to the top of the tube
with his mandibles, as females do. He may make copulation attempts or
copulate with her briefly at any time, including while she is constructing the
mud tube, provisioning or building a partition.' However, if he is present
just before oviposition, there is a long sequence of courtship and multiple,
long copulations.8 The resident male defends the nest from intruders such
as parasitic cuckoo wasps and miltogrammine flies (Cross et al. 1975). He
also staunchly, although not always successfully, defends the nest from in-
truding males, and he appears to deter some intrusions by conspecific fe-
males. In another sphecid wasp in which the male guards the nest, Peckham
(1977) has demonstrated that the presence of a guarding male significantly
increases the survival of the brood. I suspect that the nests of T. politum
are similarly protected by the guarding behavior of the male.
As already mentioned, in addition to building new mud nests and taking
over abandoned nests, females show at least 3 other nesting patterns (Fig.
1). Occasionally a mud-dauber occupies and provisions a nest which is being
provisioned by another female, a pattern reminiscent of the joint nesting
described in golden digger wasps. Since females spend most of their time
away from the nest, 2 jointly nesting wasps may not meet for several days.
When they do a vicious fight ensues which may last up to 14 min (mean 2.8
min, N = 28). The 2 bite and grapple, often falling from the nest onto the
sand or into the water below. At the end of a fight, 1 of the females re-
enters the nest and successfully prevents the other's attempts to return.
Again, as in S. ichneumoneus, only 1 of the 2 wasps lays an egg on the
(joint) provisions. This individual is as likely to be the original owner as
the intruder (X2 Test, p = 0.76; N = 13). It seems at least plausible that
something like the S. ichneumoneus dig/enter mixed strategy model may
apply to mud-daubers ("build/enter"; also, individual females mix building
and entering). If this is true, we expect to find that mud-daubers will not be
distinguishing between occupied and unoccupied nests when they "enter".
Another prediction of the model is that the success rates of females on the
occasions when they choose to build or enter should be equal. When I have
collected these data (spring 1980), I will have hatching success rather than
rates of laying eggs as I did for the digger wasps. This was an important
weakness in the digger wasp study, since we had to ignore larval and pupal
mortality.
Intraspecific brood parasitism is a fourth form of nesting in these mud-
daubers. On 3 occasions I saw a female (which had no nest and appeared to
be searching for a place to build) enter a nest which had just been parti-
tioned by another wasp, chew a hole in the soft mud and remove just the egg
(observed twice) or the egg and the spider to which it was attached (ob-
served once). She then oviposited and rebuilt the partition with fresh mud.
Brood parasitism occurs only on the rare occasions when a wasp encounters
a mud partition that has not yet hardened (less than 30 min old). It seems
unlikely that this could be a functional alternative to other forms of nesting
and it is probably an example of a conditional strategy.
Barber and Matthews (1979) observed a fifth nesting pattern in T.
politum, the provisioning of bamboo trap-nests. Unlike other members of
the subgenus, T. politum line the cavity with mud. Barber and Matthews also
observed the wasps building mud nests in the same area and estimated that
Insect Behavioral Ecology-'79
only about 5% of the nesting was in existing cavities. They suggested that
where mud or appropriate nesting sites are scarce, T. politum may choose
these rather than building free nests of their own. Before man-made struc-
tures were so common, sites for free mud-nests might have been rare and
selection might have favored individuals utilizing existing cavities. At my
study site, wasps frequently nested under the bridge for a week or 2, left
for a week or 2 and then returned. It is likely that while they were gone,
they were nesting in the surrounding woodlands, either building free mud-
nests in cavities or using natural trap-nests such as hollow stems and beetle
galleries. It is even possible that there is a "cavity-nest/mud-nest" mixed
evolutionarily stable strategy. Evidence on this will be more difficult to ob-
tain than for the hypothesized "build/enter" mixed strategy.
In a sense a bridge is an optimal spot for a mud-dauber, with mud and
spiders close at hand and a good surface on which to build a nest. On the
other hand, the presence of conspecifics and other species may reduce the
quality of this location to the point where it may be more profitable for the
wasp to nest in an area that was previously considered sub-optimal (Brock-
mann 1979). At my study site, at least 3 species of sphecid wasps frequently
destroyed T. politum nests. Trypoxylon texense Saussure and Chalybion
californicum (Saussure) (Sphecinae) chewed open completed T. politum
nests [as well as those of Sceliphron caementarium (Drury); Sphecinae],
removed the contents, including spiders, larva or prepupa, and then re-
provisioned it themselves. Trypoxylon texense, T. johannis Richards, C. cali-
fornicum and particularly T. striatum Provancher stole mud from the out-
side of T. politum and S. caementarium nests often damaging them severely
and increasing their susceptibility to parasitism and desiccation. Trypoxylon
striatum was a champion at this. These wasps did not nest under the bridge
very often, and when they did they took over abandoned T. politum nests.
Many T. striatum came to the bridge from the surrounding woods (where
they were probably nesting in twig-nests) to gather mud from active and
inactive T. politum nests. Sometimes this chewing actually caused the T.
politum cocoon to fall to the ground, although the silk laid down on the
inside of the nest by the larva usually held the cocoon in place, even when
virtually all the mud was removed. Trypoxylon texense and T. striatum oc-
casionally gathered mud on their own, but they usually stole it from T.
politum nests. A chemical analysis has been made on the mud nests of S.
caementarium by Qureshi and Ahmad (1978). Interestingly, they found
that the mud of the nests contained organic compounds including paraffins
and ketones, which were thought to be used for waterproofing. The already-
worked mud on S. caementarium and perhaps T. politum nests, then, may
be superior to freshly-procured mud, and may be an important resource for
mud-stealing species.
Trypoxylon politum also, almost spitefully, damage the nests of con-
specifics. I have observed females entering a nest without a male and re-
moving the provisioned spiders. They did not use the spiders but simply let
them drop to the ground (14% of cells have 1 spider removed by a con-
specific female). Females even force their way in past guard males and re-
move provisioned spiders. When this happens, males usually try to copulate
with the intruding female. I have also observed a female gnawing holes in
the newly-built nest of a conspecific, allowing the mud to drop into the water
Florida Entomologist 63(1)
below the nest. In addition to the extensive marauding of nests by various
species, there is also a high incidence of interspecific nest parasitism (Cross
et al. 1975, Johnson 1974, Rau and Rau 1916). Bombyliid and sarcophagid
flies, cuckoo wasps and Melittobia destroy the provisions or larvae of a sig-
nificant number of T. politum nests (Table 1).
On theoretical grounds we would expect that as bridge nesting became
less profitable due to parasitism and intraspecific marauding, as space be-
came limiting or when mud was difficult to find, it would be more profitable
for females to search for and nest in twig-nests and other existing cavities.
As the success of twig-nesting (relative to bridge-nesting) decisions in-
creased, the frequency of twig nesting would rise in the population. This
TABLE 1. INCIDENCE OF MARAUDING AND PARASITISM IN A POPULATION OF
Trypoxylon politum FROM ALACHUA CO., FL.
Percent of Trypoxylon politum cells disturbed by:
Marauding*
Conspecific (N = 132) 0.8%
chewing on nests
brood parasitism 2.0%
removal of 1 spider 14.0%
Interspecific (N = 319)
Trypoxylon texense
chewing on nests 3.5%
brood parasitism 1.9%
Trypoxylon striatum
chewing on nests 5.0%
brood parasitism 0%
Chalybion californicum
chewing on nests 3.4%
brood parasitism 1.3%
Parasitism**
Bombyliid flies (Anthrax limatulus) 12.6%
Unknown pupae (probably sarcophagid) 1.2%
Cuckoo wasps (Chrysididae) 4.0%
Melittobia sp. 0.9%
Trypoxylon johannis 0.3%
Trypoxylon striatum 0.3%
Total loss from parasitism 19.4%
Unknown Causes**
Nothing in cell 0.6%
No larva, spiders only 0.6%
Dead larva 10.8%
Live larva, no metamorphosis 11.1%
Dead pupating wasp 1.5%
Total loss from unknown causes 24.7%
*From direct observation at Hatchet Creek in 1979 as described in text.
**From cells collected at Lochloosa Creek in 1978 and reared in the laboratory (N = 324);
55.8% of cells resulted in hatched adult wasps.
March 1980
Insect Behavioral Ecology-'79
would continue until twig nesting became so common that it was increas-
ingly difficult for wasps to find appropriate cavities and then selection would
begin to favor building. Thus, it is conceivable that mud nesting and twig
nesting may be mixed in an evolutionarily stable state such that the success
of each is on average equal, maintained by a frequency-dependent advantage.
Of course this is speculative and it needs the kind of hard evidence we pro-
vided for S. ichneumoneus.
Finally we can apply the theory to 1 of the mysteries of sphecid wasp
evolution: How have such extremely diverse nesting patterns evolved within
very closely related groups? Among the Sphecinae, for example, there are
burrow diggers (Sphex, Stangeella, Prionyx, Palmodes, Podalonia and
Ammophila), species that use burrows dug by other species (Chlorion
aerarium Patton) including their prey Chlorion maxillosum (Poiret) and
C. lobatum (Fabricius), twig and cavity nesters (Podium, Isodontia and
Hoplammophila), mud-daubers (Sceliphron and Trigonopsis), brood para-
sites (Chalybion) and primitively social species (Trigonopsis) (Bohart and
Menke 1976, Eberhard 1974, Peckham and Kurczewski 1978). Within the
Trypoxylini there are mud-daubers (Pison and Trypoxylon), species that
use the pre-existing mud-nests of other wasps (Pison and Trypoxylon) twig
and cavity nesters (Pisonopsis, Pison and Trypoxylon), wasps that use bur-
rows dug in the ground by other species such as bees (Pisonopsis clypeata
W. Fox and Pison nigellum Krombein) and females of 1 species apparently
dig burrows of their own (Pison chilensis Spinola) (Rau 1928, Janvier 1928,
Krombein 1950, 1967, Evans 1969, Bohart and Menke 1976, Menke and
Bohart 1979).
The mystery of these diverse nesting patterns takes on a new perspective
when we find nearly as much diversity in the nesting behavior of 1 species.
Female T. politum build free mud-nests, use existing nests, jointly occupy
nests, use trap nests and brood-parasitize conspecifics. Under the same
bridge, Trypoxylon texense use active and inactive nests and emergence holes
(often nesting inside broken pupal cases) of T. politum, S. caementarium
and C. californicum, as well as nesting in pre-existing cavities such as bolt
holes and cracks in the cement (see also Rau 1928). Hungerford and Wil-
liams (1912) observed this species nesting in burrows dug in a clay bank by
bees. Sphex ichneumoneus dig burrows, use existing nests and jointly oc-
cupy nests with conspecifics. The pattern of using burrows which were dug
by conspecifics (entering) may be a preadaptation among fossorial species
for using existing cavities (trap-nesting) in general. If this is true then we
might expect to find species in which females sometimes dig (and enter)
burrows and sometimes nest in existing cavities (trap-nest). The full range
of the apparently diverse nesting patterns of Sphecinae and Larrinae may
be found in just a few closely-related species. To a large extent the nature
of the variation available within a species determines the course of evolu-
tion. With such variability present in 1 species, it is easy to imagine how
members of 1 tribe or family might have evolved such diverse nesting pat-
terns. The problem of the evolutionary origins of diverse nesting patterns,
then, is replaced by the even more puzzling question of how such diversity is
maintained in 1 species. The concept of the mixed evolutionarily stable
strategy provides us with 1 mechanism by which such variability may be
maintained in a population.
Florida Entomologist 63 (1)
March 1980
APPENDIX NOTES
1We used the evolutionarily stable strategy or ESS approach pioneered
by Maynard Smith (1974, 1976) and developed by Parker (1978) and
Dawkins (1976, 1979). Natural selection is the differential survival of
alleles. If a new allele arises and spreads in a population, we can ask what
was it about that allele that increased the survival and reproductive abilities
of the individuals who carried it? Sometimes the answer to this question is
simple, such as it makes all individuals more resistant to parasitism. How-
ever, sometimes the answer to the question depends in part on the frequency
of that allele relative to others in the population. If the effect of an allele is
frequency-dependent, then the population will evolve toward an evolution-
arily stable state, an uninvadeable mixture of the 2 alleles (Dawkins 1980).
One familiar example of an ESS is Fisher's explanation of the sex ratio.
A population tends to evolve toward a 1:1 sex ratio (with equal investment
in the 2 sexes) because male-producing is favored when females are common
and vice versa.
As long as the average success rates of the alternative strategies remain
the same, the population will evolve toward the ESS. However, there is noth-
ing necessarily static about an ESS. If the success rate of a strategy changes
(for example if there were an increased rate of parasitism) then the ESS
will change and the population will begin to evolve toward the new ESS.
21 observed joint nesting by golden digger wasps at all 3 of my study
sites, but the frequency of the behavior differed. In Dearborn, MI 5% (ob-
served 1973 to 1975), in Exeter, NH 12% (1975) and in Northfield, MN
about 5% (1976) of the brood cells were the result of joint nesting (Brock-
mann and Dawkins 1980).
sSeveral authors have observed marked differences among populations in
the occurrence of certain behavioral patterns (eg. Evans and O'Neill 1978,
Alcock 1979). One explanation for such variability might be that the 2
patterns are frequency-dependent and that the success of 1 relative to the
other is different in the different locations. Hence the populations may be at
different evolutionarily stable states. Another explanation is that the start-
ing conditions for the populations may have been different, a situation that
is known to influence the final ESS. In either case these are very different
kinds of explanations for the presence of diverse nesting patterns than
would have been considered prior to the application of the ESS approach to
evolutionary problems (see Dawkins 1980 for further discussion).
4Observations were conducted from 28 June to 1 September 1979 with the
assistance of Martin Obin.
5Wasps were individually marked with dots of Testor's enamel paint after
briefly anesthetizing them with a small amount of CO,, from which they
nearly always recovered quickly.
6The reasons for these abandoning are not clear. Sometimes a female
abandons a nest because she has had a fight with another female or because
of the presence of intruders such as centipedes, crickets or ants. Other times
the female simply fails to return to the nesting area and I presume that she
may have died. But in a number of cases the wasp simply begins another
search and builds another nest near the first 1 or she begins to provision
another already existing nest.
7There are 2 kinds of copulations in T. politum, short and long (see be-
low). Short copulations are 3 to 12 sec (mean 6.6, N=54) and occur at any
time while the female is at the nest, such as when she is building, bringing
in a spider or making a partition.
SThe pre-oviposition sequence (from the time the last spider was brought
in to the time at which the female leaves the nest to gather mud for the
partition) lasts 6 to 23 min (mean 12.7 min, N=25) when a male is present.
Insect Behavioral Ecology-'79
The male alternately holds the female's head with his prothoracic legs and
copulates (3 to 8 copulations during a pre-oviposition sequence, mean 6;
N=25). These are long, 5 to 55 sec, copulations (mean 14.4, N=135). If the
male is not present the female oviposits after only about 2 to 5 min.
ACKNOWLEDGMENTS
I would like to thank Richard Dawkins, Jim Lloyd, Alan Grafen, and
Martin Obin for their help with this study. The research was supported by
a grant from the Harry Frank Guggenheim Foundation and the Division of
Sponsored Research, University of Florida.
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and N. A. Blum, Eds. Sexual Selection and Reproductive Competition
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E. M. BARROWS, G. GORDH, J. L. HUBBARD, L. KIRKENDALL, D. W.
PYLE, T. L. PONDER, AND F. G. ZALOM. 1978. The ecology and evolu-
tion of male reproductive behaviour in the bees and wasps. Zool. J.
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of the female bee, Centris pallida, by its male (Hymenoptera:
Anthophoridae). J. Zool., Lond. 179: 189-99.
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pallida Fox (Hymenoptera: Anthophoridae). Amer. Nat. 111: 145-55.
BARBER, M. C., AND R. W. MATTHEWS. 1979. Utilization of trap nests by
the pipe-organ mud-dauber, Trypargilum politum (Hymenoptera:
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BARROWS, E. M. 1976. Mating behavior in halictine bees (Hymenoptera:
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sas Ent. Soc. 49: 105-19.
BOHART, R. M., AND A. S. MENKE. 1976. Sphecid Wasps of the World. Uni-
versity of California Press, Berkeley, CA. 695 p.
BROCKMANN, H. J. 1979. Nest-site selection in the great golden digger wasp,
Sphex ichneumoneus L. (Sphecidae). Ecol. Ent. 4: 211-24.
AND R. DAWKINS. 1979. Joint nesting in a digger wasp as an
evolutionarily stable preadaptation to social life. Behaviour 71:
203-45.
A. GRAFEN, AND R. DAWKINS. 1979. Evolutionarily stable nesting
strategy in a digger wasp. J. Theo. Biol. 77: 473-96.
CROSS, E. A., M. G. STITH, AND T. R. BAUMAN. 1975. Bionomics of the organ-
pipe mud-dauber, Trypoxylon politum (Hymenoptera: Sphecoidea).
Ann. Ent. Soc. Amer. 68: 901-16.
DAWKINS, R. 1976. The Selfish Gene. Oxford University Press, Oxford,
224 p.
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Barlow and J. Silverberg, Eds. Sociobiology: Beyond Nature/Nurture?
Westview Press, Boulder, CO. (in press).
DORRIS, P. R. 1970. Spiders collected from mud-dauber nests in Mississippi.
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EBERHARD, W. G. 1974. The natural history and behaviour of the wasp
Trigonopsis cameronii Kohl (Sphecidae). Trans. R. Ent. Soc. Lond.
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EVANS, H. E. 1969. Notes on the nesting behavior of Pisonopsis clypeata
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and Belomicrus forbesii. J. Kansas Ent. Soc. 42: 117-25.
AND K. M. O'NEILL. 1978. Alternative mating strategies in the
digger wasp Philanthus zebratus Cresson. Proc. Natl. Acad. Sci. 75:
1901-3.
HUNGERFORD, H. B., AND F. X. WILLIAMS. 1912. Biological notes on some
Kansas Hymenoptera. Ent. News 23: 241-60.
JANVIER, H. 1928. Recerches biologiques sur les pr6dateurs du Chili. Ann.
Sci. Nat. Zool. 11: 67-207.
JOHNSON, M. D. 1974. Trypargilum politum (Say) as a host for Trichrysis
tridens (Lepeletier) (Hymenoptera: Sphecidae; Chrysididae). Proc.
Ent. Soc. Wash. 76: 448-9.
KROMBEIN, K. V. 1950. The Aculeate Hymenoptera of Micronesia. II. Col-
letidae, Halictidae, Megachilidae, and Apidae. Proc. Hawaiian Ent.
Soc. 14: 101-42.
-- 1967. Trap-nesting Wasps and Bees: Life Histories, Nests, and As-
sociates. Smithsonian Press, Washington, D.C. 570 p.
MAYNARD SMITH, J. 1974. The theory of games and the evolution of animal
conflicts. J. Theor. Biol. 47: 209-21.
MAYNARD SMITH, J. 1976. Evolution and the theory of games. Amer. Sci. 64:
41-45.
MENKE, A. S., AND R. M. BOHART. 1979. Sphecid wasps of the world: Errors
and omissions (Hymenoptera: Sphecidae). Proc. Ent. Soc. Wash. 81:
111-4.
MUMA, M. H., AND W. F. JEFFERS. 1945. Studies of the spider prey of several
mud-dauber wasps. Ann. Ent. Soc. Amer. 38: 245-55.
PARKER, G. A. 1978. Searching for mates. Pages 214-244. In: J. R. Krebs
and N. B. Davies, Eds. Behavioural Ecology: An Evolutionary Ap-
proach. Blackwell Scientific Publications, Oxford.
PECKHAM, D. J. 1977. Reduction of miltogrammine cleptoparasitism by
male Oxybelus subulatus (Hymenoptera: Sphecidae). Ann. Ent. Soc.
Amer. 70: 823-8.
-- AND F. E. KURCZEWSKI. 1978. Nesting behavior of Chlorion
aerarium. Ann. Ent. Soc. Amer. 71: 758-61.
QURESHI, M. Y., AND N. AHMAD. 1978. A study of the mud dauber nest
(Hymenoptera). Pak. J. Sci. 30: 79-83.
RAU, P. 1928. Field studies in the behavior of the non-social wasps. Trans.
Acad. Sci. St. Louis 25: 325-489.
-- AND N. RAU. 1916. The biology of the mud-daubing wasps as re-
vealed by the contents of their nests. J. Anim. Behav. 6: 27-63.
March 1980
Insect Behavioral Ecology-'79
EVOLUTION OF EXCLUSIVE POSTCOPULATORY
PATERNAL CARE IN THE INSECTS1
ROBERT L. SMITH
Department of Entomology
University of Arizona
Tucson, AZ 85721 USA
Among the many thousands of insect species whose reproductive behavior
is known, only about 100 have males that exclusively care for eggs and/or
young, and all but a few of these are water bugs in the subfamily
Belostomatinae. In fact, all recorded cases of exclusive postcopulatory pa-
ternal care are restricted to a few families in 1 order, the Hemiptera. These
include the Belostomatidae, Gerridae, Reduviidae, Coreidae, and Aradidae
(reviewed in Ridley 1978, Melber and Schmidt 1977, and see Appendix). Of
these, only representatives of the Belostomatidae and the Reduviidae have
been studied in sufficient detail to expose discernible pathways to the evolu-
tion of their paternal care. This paper will develop scenarios for giant water
bugs and assassin bugs with the hope of revealing principles generally useful
for understanding the evolution of paternal care in insects.
Several recent reviews and theoretical contributions (Trivers 1972,
Parker 1970, Dawkins and Carlisle 1976, Thornhill 1976, Emlen and Oring
1977, Maynard Smith 1977, Melber and Schmidt 1977, Ridley 1978) make
possible an elucidation of the general circumstances that have favored, and
the preadaptations that have permitted, paternal care to evolve. A synthesis
of these theories may predict where additional examples might likely be
found and, conversely, explain why exclusive paternal care is so rare in the
Class Insecta.
RESISTANCE TO THE EVOLUTION OF
POSTCOPULATORY PATERNAL CARE IN THE INSECTS
Several factors have mitigated against the evolution of paternal care in
insects. Insect eggs originally were selected to develop unattended on land.
Embryogenesis takes place within a wide range of temperatures uncontrolled
by parents. The chorion of the insect egg, recently recognized for its re-
markably complex structure (Hinton 1970), permits the encapsulated embryo
to breathe without desiccating, a spectacular achievement when one con-
siders that oxygen molecules that must enter are larger than the water
molecules that must be retained. Beyond this, the external chorionic micro-
structure of most insect eggs is capable of supporting a plastron (Thorpe
1950) when the egg is submersed in water. This gas film protects unattended
eggs from drowning when they are temporarily covered with water (Hinton
1969). Because of these original adaptations to a terrestrial existence, the
majority of insect ova are programmed to develop and hatch without care
from either parent.
In a substantial number of species, females have been selected to serve
'Arizona Agricultural Experiment Station MS No. 3085.
Florida Entomologist 63(1)
their embryos in ways that could not have been accomplished by males
(Eickwort 1980). All females provision their eggs with stored embryonic
food in the form of yolk, and only the female can expend time and energy to
locate appropriate microhabitat in which to deposit eggs; this assures
optimal developmental conditions for embryos and abundant resources for
emergent young. In many species, females have evolved special organs,
ovipositors, to accomplish this task and to secrete eggs in protected locations
less accessible to potential parasites and predators. Females of some species
protect their embryos by thickening the chorion of individual eggs or by
packaging the entire clutch in a protective covering, such as the dictyopteran
ootheca. Another female egg protection strategy has been to distribute eggs
over a wide area, decreasing their profitability to potential predators and
parasites (Price 1976). Finally, ovoviviparous and viviparous species have
simply declined to expose embryos to any potential external adversity. Most
of these female-centered adaptations are irreversible, and have left little or
no opportunity for a father to contribute.
Several services to eggs and young might be rendered with equal efficiency
by either sex or cooperatively by both sexes (i.e. nest construction, guarding,
external provisioning, and feeding), but in the overwhelming majority of
species that provide such services, the tasks are performed by females ex-
clusively (Wilson 1971, 1975; Melber and Schmidt 1977; Hinton 1977). There
have been several recent attempts to explain why this is so.
Referring primarily to birds, Emlen and Oring (1977) proposed that
exclusive male parental care is most likely to develop in groups having a
phylogenetic history of shared parental investment. If this were the case for
insects, the paucity of species with shared parental care might be proposed
to explain the rarity of exclusive paternal care. This does not hold for in-
sects, however, and the explanation would seem to beg the issue; most of the
factors favoring shared parental investment would also promote exclusive
male care.
Trivers (1972) has recognized that in species without parental care,
female fitness is limited by individual egg production, and male fitness by
the number of females the individual can inseminate. Nest building and egg
and young tending may have begun as relatively inexpensive chores for
female insects if feeding and egg production continued at a rate independent
of modest maternal activities. Also, sperm stored in the spermathecae of
most females assure fertility of subsequent clutches long after mating.
Hence, maternal nurture in many species of insects may be rendered with
little loss in future female fitness. Paternal care, on the other hand, is likely
to interfere with a male's potential for future parentage in that any time
spent caring is time lost courting and mating other females. This sexual in-
equity in cost for equal return has almost certainly offered considerable
resistance to the evolution of paternal care.
Dawkins and Carlisle (1976) provide an elegant explanation for the
rarity of paternal care in insects (and other animals having internal fer-
tilization) independent of sexual cost-benefit asymmetries. In species with
internal fertilization, there is time between mating and oviposition during
which the male can (and usually does for the reasons just discussed) desert
the eggs his sperm may eventually fertilize. This traps the female with her
eggs and no opportunity to manipulate their father.
March 1980
Insect Behavioral Ecology-'79
Finally, caring males must have high assurance of paternity (PA) for
brooded eggs and young. This would be especially true if brooding initially
conferred only a small net increase in fitness to recipient eggs and young. If
added net fitness and PA are both low, any caring genes that arise in a
population will diminish in frequency and eventually be lost. Surprisingly, a
preliminary model, to be developed in detail elsewhere, has indicated that if
added net fitness is very high, caring genes could initially increase in fre-
quency in spite of a very large fault in PA. However, virtually perfect PA
would be required to fix caring genes, because even a small fault would per-
mit noncaring genes to program successful cheating strategies.
Paternity assurance is a special problem for insects because of the fe-
male's ability to store sperm (Parker 1970). Stored sperm threaten caring
males with being cuckolded, i.e. brooding eggs fertilized by another male
(Trivers 1972). Therefore, PA for insects may often involve competition
between or among ejaculates within the female's reproductive tract. It should
be clear that paternal care will most likely evolve in those species where the
ejaculate of the current male preempts or displaces most or all previously
stored spermathecal sperm. Conversely, paternal care is unlikely to evolve
in species having a low rate of preemption or displacement. W. F. Walker
(personal communication) has recently reviewed sperm utilization strategies
in insects, and found that most species with high displacement have elongate
or tubular spermathecae, whereas the spermathecae of those with low dis-
placement are usually spherical or ovoid. Therefore, some candidate species
may have failed to evolve paternal care because their females' spermathecae
were maladapted to a high level of sperm displacement. In the membracids,
for example, over 40 species have caring mothers, but no example of paternal
care has been found in this group (T. K. Wood, personal communication).
Perhaps some Hemiptera have spermathecae unusually well adapted for
displacement, thus accounting for the occurrence of exclusive paternal care
in this and no other order.
PATERNAL CARE IN GIANT WATER BUGS AND ASSASSIN BUGS
In the giant water bug subfamily Belostomatinae, males carry eggs
deposited on their backs by conspecific females. Until the end of the 19th
century, it was believed that egg-bearing belostomatids were females carry-
ing their own eggs. Even as late as 1935, Bequaert declined to include mem-
bers of this group in his review of presocial Hemiptera because: "It has
been shown that in these insects the female forcibly seizes another individual
of the same species (usually a male, more rarely a female) on whose back
she lays the eggs." Dr. Bequaert had apparently overlooked Torre Bueno's
(1906) revelation that copulation takes place in connection with oviposition
for Belostoma flumineum Say, and Slater's (1899) observation that only
males bear eggs.
More recently, Voelker (1968) demonstrated that Limnogeton fieberi
Mayr always copulates with the female while receiving her eggs. I have
studied the courtship and mating behavior of Abedus herberti Hidalgo and
found that males of this species require the female to couple prior to ac-
cepting any of her eggs. Furthermore, oviposition is regularly interrupted
by male demands for additional bouts of copulation after an average of each
2 eggs that are laid (Smith 1979a). Cyclical copulation and oviposition has
Florida Entomologist 63(1)
in fact been a characteristic of all of several speices of Abedus and
Belostoma studied (Smith unpublished).
These observations led me to suspect that most of the eggs carried by a
male contain his genes, and therefore whatever brooding services rendered
them must represent a true paternal investment (Smith 1976a, 1976b,
1979a). I succeeded in validating this hypothesis by mating A. herberti
females competitively with genetically marked males (Smith and Smith
1976, Smith 1979b). The result was virtually complete paternity assurance
for all contestant males.
Torre Bueno (1906) and others have reported that male water bugs
"dislike" having their backs used as oviposition substrates and that they
attempt to get rid of the burden by kicking it off. This interpretation was
apparently based on observations of a real male option: discarding eggs in
the face of adverse brooding conditions. The option is frequently exercised
in the laboratory when encumbered bugs are confined to a featureless
aquarium, but rarely if the aquarium is provided with aquatic plants or other
resting substrate at the surface (Smith 1976a, b).
Modern studies (Voelker 1968; Cullen 1969; Smith 1976a, 1976b) have
demonstrated unequivocally that males provide essential services to eggs and
emerging nymphs. Limnogeton fieberi males regularly expose their eggs to
atmospheric air as do Belostoma flumineum, B. malkini Lauck, and Abedus
herberti. In addition, some Belostoma species use the hind legs to stroke eggs
while under water and Abedus herberti execute brood pumping (pushups)
to move water over the eggs and aerate them while below the surface (Smith
1976a, b).
Detached belostomatine egg pads covered with static water apparently
drown and eventually are attacked by fungi. Eggs exposed to open air
desiccate rapidly and the embryos die. A very small percentage hatch can be
achieved if a detached pad is placed in shallow water so that the unattached
ends of the eggs are exposed to atmospheric air, but the young nymphs have
great difficulty escaping the chorion. Most die and those that do escape are
usually deformed (Smith 1976a, b). Abedus herberti males are apparently
aware of eggs hatching on their backs and assist closing nymphs by going
below the surface and brood pumping vigorously until the hatching bugs
are freed from the chorion (Forey and Smith, in preparation). Brooding
A. herberti males are also inhibited from feeding on general newly hatched
nymphs that remain in the father's vicinity until their integuments have
hardened and they are able to disperse (Smith 1976b). Nonbrooding males
and females are in no way inhibited from cannibalism.
Brooding is an expensive occupation for male water bugs. The egg pad
on the back of a brooding male may weigh twice as much as the bug alone,
and its irregular wetted surface produces considerable drag as the bug
swims. Males with eggs swim only half as fast as males without eggs (Smith
1976b). The dynamics of brooding (i.e. frequent exposure of eggs to the
atmosphere, brood pumping, and egg stroking) betray the location of
brooders. (Nonbrooding males and females are morphologically and be-
haviorally cryptic.) These factors surely reduce the brooder's access to prey,
and may subject him to increased risk of being preyed upon. Furthermore,
brooding behavior itself has a caloric expense. Nonbrooding males do noth-
ing more than rest in a predatory stance and surface for air occasionally,
March 1980
Insect Behavioral Ecology--'79
while in extreme cases, a brooding A. herberti pumped 716 times and a B.
flumineum stroked its eggs 768 times in 1 hour. Also, a bug cannot spread
its wings and fly when they are covered with an egg pad, so the brooder
forfeits a dispersal option for the duration of his encumberment. By far the
most significant cost for a brooding male is his loss of opportunity for poly-
gynous mating; females reject encumbered males as mates (Smith 1979a).
Not all giant water bug males brood eggs. Females in the genus
Lethocerus (subfamily Lethocerinae) deposit their eggs in tight clutches on
emergent vegetation (e.g. Typha) at variable heights above the surface of
the water (Hungerford 1925, Rankin 1935, Menke 1963, Cullen 1969,
Tawfik 1969, Menke 1979). Lethocerus eggs are apparently hydrophobic.
Cullen (1969) noticed a significant difference in the height above the water's
surface at which eggs of Lethocerus maximus DeCarlo were laid during the
wet and dry seasons in Trinidad. The average height during the wet season
was approximately 7 times greater than during the dry season. Cullen
speculates that this behavior pattern is an adaptation to prevent eggs from
being submersed, and the large size of these ova (up to 7.4 mm) and their
relatively very low surface to volume ratio indicate an unfavorable rate of
gas exchange between the embryo and surrounding water. My future re-
search will address this problem and attempt to explain why members of
the genus are tied to emergent vegetation as an oviposition substrate.
The mating behavior of lethocerines has not been adequately studied, but
preliminary observations (Tawfik 1969, Smith 1975) have revealed an
aspect of great importance in the evolution of paternal brooding. Male
lethocerines mate a single female repeatedly and may guard her until she
lays her eggs. Male guarding of an appropriated mate is believed to be a
sperm competition strategy evolved to prevent preemption of the guarding
male's sperm by subsequent mating of the female with another male before
laying her eggs (Parker 1970, 1974). After eggs are laid, guarding ends,
and, male Lethocerus (unlike encumbered male Belostomatinae) are at
liberty to court and mate other females.
Paternal brooding has also been reported for 2 species of reduviids, a
group well known for maternal care of eggs and young (Hussey 1934,
Bequaert 1935, Wilson 1971, Melber and Schmidt 1977). Bequaert (1912,
1913) first found that in an African assassin bug Rhinocoris albopilosus
Signoret males guard the eggs; this observation was later confirmed by
Odhiambo (1959, 1960) who observed that the male "rides" on the female
for several hours after mating, then dismounts and remains with her for
2 or 3 days, during which time successive bouts of copulation may occur.
Ultimately, the female lays her first clutch of eggs shortly after a mating
bout. When the female completes her laying and moves away from the com-
pact mass of ca. 100 eggs, the male approaches and stands over the clutch.
Brooding males show extraordinary fidelity to the task through a variety of
adverse conditions. While brooding males do' not actively hunt for prey, they
may impale any that come within range of the guarded eggs. Only eggs are
brooded; males abandon young nymphs soon after they begin to hatch.
Odhiambo (1959, 1960) observed that the original female may return to
the guarded egg mass to add eggs. Even more remarkable, other females
also may add eggs to a common egg mass. Significantly (for reasons of
paternity assurance) females that contribute to the guarded clutch first
Florida Entomologist 63(1)
mate with the brooding male. The function of male guarding for this species
has not been established, but it is presumed that the brooding male must
repel potential egg parasites and predators.
Zelus sp., another tropical reduviid, not only guards eggs but also re-
mains with newly hatched nymphs for several days, and at least occasionally
feeds them. Ralston (1977) empirically determined that male brooding re-
duces egg parasitism by Telenomus sp. (Scelionidae) from 55% for un-
guarded eggs to 21% for those guarded. Ralston also demonstrated that
guarding males are significantly less likely to flee a simulated predator and
more inclined to attack simulated parasites than non-guarding males. He
noted that individual males of this species guarded as many as 7 egg masses.
Although the author (Ralston) implied that multiple masses may have been
deposited by a single female, it seems more likely that each mass was con-
tributed by a different female. Apparently Ralston never directly observed
mating and oviposition, but he inferred an association between the 2 ac-
tivities in his prediction: ". . that the guarding male is the genetic father
of at least some of the eggs he guards."
EVOLUTION OF PATERNAL CARE IN
GIANT WATER BUGS AND ASSASSIN BUGS
Lauck and Menke (1961) proposed that the Belostomatinae brooderss)
arose from the monotypic subfamily Lethocerinae (nonbrooders). Recall
that members of the genus Lethocerus all lay their eggs on stout emergent
vegetation in open air above the water. Lethocerus spp. are the largest
aquatic bugs, having apparently specialized for great size (presumably to
utilize large prey) in their divergence from the Nepinae of the Nepidae
(see China 1955). An increase in egg size accompanied this specialization
and the concomitant decrease in egg surface to volume ratio probably caused
gas exchange problems, placing an upper size limit on members of the
divergent line. A change in oviposition habits from subsurface endophytic or
exophytic (characteristic of nepids) to above surface exophytic (charac-
teristic of modern lethocerines) apparently lifted this upper size limit, per-
mitting the evolution of huge bugs (up to 110 mm in length).
Modern lethocerines are extremely strong fliers capable of long dispersal
flights which regularly expose adults to nonreproductive habitats, i.e.
aquatic habitats lacking emergent vegetation for oviposition (Riley 1896,
Menke 1963, Cullen 1969, Smith unpublished). It seems likely that transient
ancestral lethocerines may have enjoyed an advantage by extending their
stays in nonreproductive habitats, there exploiting food resources in a rela-
tively less competitive environment. Females, however, ultimately would have
been compelled to make dangerous dispersal flights to find habitats that
contained suitable oviposition substrate (emergent vegetation). Females
that could avoid searching for, and the intense competition in, traditional
oviposition sites would have enjoyed a competitive advantage over those con-
tinuing in these activities. Not only would they conserve time and lessen
risks to themselves, but their nymphs also would benefit from less competi-
tion for food and reduced predation if they hatched in a previously unex-
ploited habitat.
This assumes that these females found some alternative to emergent
vegetation as an oviposition substrate. One option would have been to lay
March 1980
Insect Behavioral Ecology-'79 71
eggs on the back of the male. The diminished aggressivity, and prolonged
interest in the female due to male guarding enhanced this possibility.
Hungerford (1920) provided an anecdote demonstrating the ease with which
this event may have occurred. He collected several Lethocerus sp. and
placed them in an aquarium with no substrate that would normally be used
for oviposition. He returned after several days to find that a female had
deposited a few eggs on the back of a male.
The distribution of modern genera (3 Old World, 2 New World) in the
subfamily Belostomatinae suggests that this special event must have oc-
curred before the breakup of Pangaea. A female in a species with ancestry
common to the 2 subfamilies mated a male, then laid some eggs on his back.
Actually this occurrence was probably repeated sporadically over a rela-
tively long period of time until the fortuitous pairing of some eggs (those
architecturally and physiologically preadapted to tolerate prolonged wetting)
with males predisposed to certain behavior patterns (those inclined to spend
much time at the water's surface).
It is noteworthy that Lethocerus spp. have long retractile air straps
(breathing tubes) that allow the bugs to breathe atmospheric air and secure
air stores while completely submersed. In contrast, all modern members of
the Belostomatinae have short spatulate air straps that force them to surface
when obtaining air. It seems probable that males with shorter than average
air straps may have been preadapted to brooding in that eggs attached to
their backs would have been exposed to the atmosphere. Repeated exposure
of eggs to the atmosphere would assure the hatching of some eggs from a
male's back.
Natural selection would have begun to favor females programmed to lay
eggs on their mates' backs if the value of these exceeded that of those laid on
emergent vegetation. Value, of course, is measured in the number of re-
sulting progeny that survive to reproduce. This value asymmetry could have
been achieved through differential survival of either eggs or nymphs. For
example, eggs on a male's back might have enjoyed differential survival due
to reduced parasitism, predation, and cannibalism. Surprisingly, not a single
datum exists on the parasites and predators of these huge eggs, but Cullen
(1969) provided an anecdote on egg cannibalism. In the laboratory, he ob-
served a female Lethocerus maximus ascend a sedge on which a clutch of
eggs had previously been laid by another female. The second female ate the
eggs of the first and replaced them with her own clutch.
Survival of eggs laid on males' backs in a new habitat need not neces-
sarily have been higher than that of those laid in traditional habitats on
emergent vegetation for the system to have progressed. The enormous ad-
vantage to nymphs of hatching into a previously unexploited habitat lacking
specific predators might easily have offset an initial low egg survivorship
during the transitional period. Corbet (1959) found that giant water bugs
constituted ca. 75% of the stomach contents of immature crocodiles in Lake
Victoria. Imagine the relief felt by the first nymphs that hatched from
brooded eggs in a crocodile-free environment!
Male water bugs may have initially tolerated being encumbered with eggs
if 1) they had equal or greater assurance of paternity for carried eggs over
those laid on inanimate substrate, and 2) if carrying eggs did not interfere
with their subsequent opportunities to mate. Both of these requisites are
Florida Entomologist 63(1)
likely to have been satisfied. A male that mates with a female and then al-
lows her to lay eggs immediately on his back would surely be the biological
father of most; males decorated with a few eggs were probably no less at-
tractive to conventional females who mated them and continued to deposit
their eggs on emergent vegetation.
As the frequency of females programmed to encumber males increased
in the population, so also the number of males carrying eggs. This in turn
began selecting a new female behavior-rejection of fully encumbered males.
There would be no advantage for females to mate with males whose prior
commitment precluded their investment in additional eggs.
Female choice for brooders and rejection of encumbered individuals
would now begin to impose a system cost on males: a reduction in oppor-
tunity for polygamy, immune to any male manipulation. The males' only
option would be to increase paternal investment, thereby appreciating the
value of eggs received. This led to the evolutionary refinement of PA
adaptations and the elaboration of male brooding skills. The resulting
further increased survivorship of brooded eggs would eventually expand the
female "conspiracy of choice" to fixation such that an encumbered male
would have no opportunity to mate while brooding.
Is this the end point? It could be if paternity assurance adaptations have
evolved to perfection. G. A. Parker (1970) reviewed the literature on sperm
competition and found that in the majority of insects that had been studied,
the last male to mate with a nonvirgin female succeeded in fertilizing from
about 50% to 95% of the eggs she laid. Generally most of the eggs not
fertilized by the last male were fertilized by stored sperm from the penulti-
mate male. Parker has intensively studied the yellow dungfly Scatophaga
stercoraria, and found its paternity assurance through sperm displacement
relatively high, ca. 80%.
Let us examine what might happen if the water bugs had evolved
paternity assurance only to an 80% level of efficiency. This would allow 20
of each 100 eggs brooded to have been fertilized by the female's previous
mate, and the 20% fault would provide opportunities for cheating. It should
be clear that a brooding male cannot disguise his commitment to eggs he
wears on his back, so how to beat the system? There are 2 plausible methods.
First, a male might mate repeatedly with a series of females, but decline to
receive any of their eggs. Second, the cheater might mate with a female,
receive her eggs, then kick the eggs off before meeting and courting addi-
tional females. In both cases, cheater males have removed the female
criterion for rejection: carried eggs. What advantage would accrue to
cheaters? Let us assume that 30 days are required for a male to brood a
clutch of eggs, and that females lay an average of 100 eggs on a male's back.
At the end of 30 days, an honest male will have brooded 100 eggs but
fathered only 80. If a cheater can mate 5 females in 30 days by declining to
receive eggs or by abandoning them after each mating, and the females each
subsequently mate and encumber honest males, the cheater will eventually
have fathered 100 eggs for a net gain of 20. The advantage of cheating
probably oscillated with the number of cheaters eventually to some equi-
librium with the level of opportunity provided by the average fault in
paternity assurance. Perfection of PA by the belostomatids (Smith 1979b)
has apparently blocked the opportunity for intrasexual cheating. This and
March 1980
Insect Behavioral Ecology-'79
the loss of the ability for eggs of the Belostomatinae to develop and hatch
unattended in open air apparently rendered the new system fixed and ir-
reversible, an evolutionarily stable strategy (Maynard Smith and Price
1973, Maynard Smith 1976).
At least 2 species of assassin bugs have independently evolved paternal
care in the form of egg guarding and I predict that others in this family
will eventually be found to have caring fathers. This prediction is based on
the apparent ease with which paternal care could evolve in species having
territorial males and males that assure paternity by mate guarding. Further-
more, the eggs of many reduviids would seem to be vulnerable to parasitism
and predation. These are laid in tight clutches on open plant parts and
seem to lack special defensive adaptations (Cobben 1968). Consequently they
could benefit from being guarded as attested to by the relatively large and
growing list of species that have maternal guarding (Wilson 1971).
Mate "riding" found in R. albopilosus is thought to be a PA adaptation
(Parker 1970, Sivinski 1977) similar to mate guarding by male Lethocerus.
It has the same effect, placing fathers in the vicinity of their eggs when laid
so that male caring could occur and be selected. Egg guarding by assassin
bug males might have initially cost individuals opportunities for polygynous
matings if searching were the historical mate acquisition method. Under
this circumstance, caring genes would be selected only if the gain in survivor-
ship of guarded eggs exceeded the potential gain from multiple clutches of
unguarded eggs. Emlen and Oring (1977) have indicated that the degree to
which an individual can take advantage of the potential for polygyny in its
environment depends on the amount of paternal care required for rearing
young. This concept might appropriately be reversed for male insects to
indicate that the amount of care a father may be willing to render should
depend on his opportunities for polygyny. If females are scarce or difficult
to find, or if a male is not a good seducer, he might advantageously provide
care even if it results in only a small increase in fitness to recipient progeny.
Females should always have benefited from having their eggs guarded, and
must have preferred nurturant males if they could be identified. Perhaps the
only sure way for a female to have discriminated caring from noncaring
males would have been to choose males already tending eggs. This would
be an excellent female decision (if males effectively guard multiple clutches)
because the brooding male has demonstrated not only his willingness and
commitment to brood, but also his ability to seduce, both desirable charac-
teristics from the female's standpoint. As noted earlier, Zelus and Rhinocoris
males receive multiple clutches for brooding. This female preference and its
potential for creating a high variance in male reproductive success surely
placed a premium on the virgin male's ability to rapidly secure a clutch of
eggs. This urgency may be reflected in the willingness of Rhinocoris males
to compete for the privilege of guarding a clutch of eggs irrespective of their
paternity (Odhiambo 1959). In this scheme, male territoriality would have
been created by selection for paternal guarding and female choice restored
polygyny for territorial males.
Another possible route circumvents the initial reduction in opportunity
for polygyny by assuming that assassin bug paternal care arose in species
initially having territorial males. If territoriality evolved as a mate acquisi-
tion strategy, males would have been selected to choose ideal feeding and/or
Florida Entomologist 63(1)
March 1980
oviposition sites attractive to females. Attracted females could be mated by
defending males in exchange for feeding or ovipositional privileges within
the territority. These kinds of territoriality have been documented for species
representing most insect orders (Price 1976). Intrasexual selection should
operate to perfect PA by sperm displacement for males that invest in ter-
ritory defense independent of paternal care. An outrageous sperm displace-
ment adaptation has recently been discovered in the damselfly Calopteryx
maculata (Beauvois) (Waage 1979). The territorial males of this species
have genitalia equipped with sperm extractors which they use to remove any
alien sperm present in the female's storage organ prior to ejaculation. Ter-
ritorial males with perfected PA mechanisms would certainly have been
excellent candidates for the evolution of paternal egg guarding.
Eggs laid in a defended territory may have enjoyed a small initial
survival advantage over those laid on undefended substrate with little cost
to the defending male. Some careless defenders (selected to repel conspecific
males) may have occasionally mistakenly repelled heterospecifics including
potential egg parasites and predators, thus incidentally protecting eggs and
young containing genes for imperfect discrimination in territorial defense.
Competition among males probably operated to optimize the system by
having eggs (or young nymphs) become the foci of heterospecific defense
while the entire territory continued to be defended against conspecific males,
some perhaps behaviorally disguised as females attempting to sneak copula-
tions with attracted females. Transvestite behavior could succeed as a cheat-
ing strategy in spite of perfected PA through sperm displacement if a
female impersonator were able to enter the territory, mate an attracted
female, then distract the resident male long enough for the female to oviposit.
It is not known that transvestite cheating occurs for either of the 2
reduviid species, but it does occur in fishes. Ridley (1978) has indicated that
in fishes with external fertilization, transvestite sneaking or cheating would
undermine female choice; this may occur even in fishes with internal fertil-
ization (e.g. Constantz 1975). Presumably territorial males of the 2 reduviid
species have had sufficient control over the policing of their territories to
prevent the diminution of female choice and reversal of the system.
SUMMARY
Factors that have resisted evolution of paternal care in the insect in-
clude: (1) A general inability of males to enhance the fitness of precocial
eggs and young; (2) the deterrent of irreversible maternal care adapta-
tions; (3) a sexual asymmetry of cost in future fitness (male loss of op-
portunity for polygyny) favoring maternal care; (4) the differentially
greater opportunity for males to abandon eggs due to internal fertilization;
(5) a problem with paternity assurance due to sperm storage by female
insects. Species minimally restrained by these factors would be predisposed
and preadapted to the evolution of paternal care, as seems to have been the
case for the Belostomatinae and 2 species of Reduviidae.
The belostomatid system evolved because males had the opportunity to
reduce parasitism and predation on eggs and to permit young to exploit new
habitats. Males were available to brood eggs because female guarding (a PA
strategy) kept them from abandoning their mates (and eggs) immediately
after copulation. Female choice created selection for paternal brooding and
Insect Behavioral Ecology-'79
stabilized the system by selecting against male polygyny. Intrasexual selec-
tion favored increased male investment and perfected PA. Finally, the
perfection of PA and physiological adaptations of eggs to being brooded
under water fixed the system by blocking alternative male strategies. This
general scheme may account for the evolution of paternal egg carrying in
some gerrids and the coreid Phyllomorpha laciniata (Villers) (see Ap-
pendix).
Male guarding of eggs and young as found in the Reduviidae seems to
have evolved via a slightly different pathway. Male bugs were capable of
defending vulnerable clutches of eggs against potential parasites and preda-
tors. Mate guarding by males (a PA strategy) and/or male territoriality (a
mate acquisition strategy) made males available at the time of oviposition.
Territorial males defended eggs against heterospecific threats with little
added effort while defending their territories against conspecific males.
Female preference for brooding males increased opportunities for polygyny
by brooders and resisted male cheating strategies. Intrasexual selection
strengthened existing PA systems and optimized paternal defense of eggs
and young. Neuroctenus pseudonymus Bergroth may have evolved paternal
guarding in a similar way (see Appendix).
The foregoing narratives provide plausible event sequences leading to
the evolution of paternal care for known and suspected insect examples. I
am confident, at least, that the key elements: opportunity, paternal avail-
ability, female choice, male-male competition, and paternity assurance, have
been identified. These may eventually be abstracted and incorporated into
mathematical models as tests of the proposed and alternative scenarios.
APPENDIX
Representatives of the hemipteran families Gerridae, Coreidae, and the
Aradidae are suspected of having paternal care, but have been inadequately
studied to confirm its existence. I append this review of what is known of
these species in the hope of stimulating further studies on them.
Paternal brooding may occur among the water skimmers (Gerridae).
An undescribed species of Rhagadotarsus has been shown to court females
while holding a floating or fixed object on the surface of the water (Wilcox
1972). Successful males mate with females which in turn use the guarded
object as an oviposition site. A single male may accumulate eggs from sev-
eral females, but it is not known how long a male may continue to guard his
substrate or of what benefit this guarding may be to eggs or hatching
nymphs.
Populations of pelagic species in the genus Halobates may be limited by
the availability of floating oviposition substrate. Females of these species
lay their eggs on a variety of floating objects including conspecifics (Walker
1893, Bequaert 1935). It seems unlikely that a female would be able to
attach eggs to her own body so it would not be surprising if male Halobates
were used in a manner similar to male' belostomatids. Anderson and Pol-
hemus (1976) discount this possibility suggesting that specimens recovered
with attached eggs were probably dead at the time eggs were attached to
them.
The male of a coreid bug, Phyllomorpha laciniata, from Europe has been
depicted carrying eggs attached to its back (Jeannel 1909). The drawing
shows an individual with 15 large eggs placed loosely and at random on its
concave back. The eggs appear to be held in place by a series of slanting
spines adorning the pronotum and lateral margin of the abdomen. Signif-
Florida Entomologist 63(1)
icantly, the eggs appear to be sufficiently large that the 15 might represent
the entire complement of a single female.
Bequaert (1935) excluded this species from consideration for the same
reason that the belostomatids were ignored, and Miller (1971) states that
both males and females have been observed with ova on their backs. He
suggests that the presence of eggs on both sexes may have been fortuitous,
the eggs having fallen from a nearby female; however, this seems highly un-
likely. Miller cites no authority for these observations, but it is not clear
that he was the observer. Apparently, early accounts of Phyllomorpha egg
carrying Jeannel 1909, Oliver 1909, Reuter 1909) have accumulated some
speculative embellishment while being carried forward in the literature.
This species needs to be intensively studied in order to validate or dis-
credit the early accounts, and if validated, to determine the genetic relation-
ship of egg-carrying adults to the eggs and discover the benefits of this sys-
tem to eggs. This system, if facultative, would be an extremely important
one to understand the evolution of paternal care.
Finally, paternal care is suspected in a species of flat bug (Aralidae).
McClure (1932) observed that after the female Neuroctenus pseudonymus
Bergroth laid her triangular masses of from 10 to 50 within channels cut
in wood and bark by wood-boring insects, she departed, and another adult
"probably the male" crawled astride the group and remained there until the
eggs hatched. This guarding extended over a period of at least 2 weeks.
Nothing is known of the genetic relationship of the guarding individual to
the eggs, or how guarding may influence survivorship of the clutch.
ACKNOWLEDGEMENTS
I thank J. E. Lloyd, J. Alcock, F. G. Werner, and R. E. Michod for review,
G. C. Eickwort for a preprint of his chapter on presocial insects, and C. W.
Schaefer for assistance in obtaining references. This paper is the result of
research supported by NSF Grant DEB76-24332.
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Insect Behavioral Ecology-'79
MIGRATING LEPIDOPTERA:
ARE BUTTERFLIES BETTER THAN MOTHS?*
THOMAS J. WALKER
Department of Entomology and Nematology
University of Florida
Gainesville, FL 32611 USA
A significant number of species of insects, especially Lepidoptera,1 breed
each summer hundreds of kilometers farther poleward than they overwinter.
Individuals must therefore be making the sort of long-distance, habitat-to-
habitat movements that entomologists generally term migration. This paper
examines the annual migration to higher latitudes of certain butterflies and
moths, and particularly the occurrence or nonoccurrence of return flights by
the progeny or grandprogeny of the individuals that flew poleward.
SUBJECT SPECIES
Ten species, 5 butterflies and 5 moths, are the principal examples in this
paper (Table 1). Each is believed to migrate northward in the eastern
United States in spring or summer and to produce 1 or more generations in
TABLE 1. FIVE BUTTERFLIES AND 5 MOTHS THAT ANNUALLY SPREAD NORTH-
WARD IN THE EASTERN UNITED STATES AND BREED IN AREAS UN-
SUITABLE FOR OVERWINTERING.
Species
Reference
Butterflies
Monarch
Cloudless sulphur
Buckeye
Gulf fritillary
Bean leafroller
Moths*
Fall armyworm
Velvetbean
caterpiller
Cabbage looper
Soybean looper
Beet armyworm
Danaus plexippus
(Danaidae)
Phoebis sennae
(Pieridae)
Precis coenia
(Nymphalidae)
Agraulis vanilla
(Heliconidae)
Urbanus proteus
(Hesperiidae)
Urquhart and Urquhart 1979
Walker 1978
Walker 1978
Walker 1978
Walker 1978
Spodoptera frugiperda Snow and Copeland 1969
Anticarsia gemmatglis
Trichoplusia ni
Pseudoplusia includes
Spodoptera exigua
Buschman et al. 1977
Chalfant et al. 1974
Mitchell et al. 1975
Mitchell 1979
*All are Noctuidae.
*Florida Agricultural Experiment Station Journal Series No. 2152.
1This and subsequent superscript numbers refer to notes in the appendix, p. 93.
Florida Entomologist 63(1)
March 1980
areas farther north than overwintering can occur. It should be emphasized
that evidence for individuals of a particular species not overwintering at any
particular northern latitude is always less than perfect.2 Nonetheless, all
indications support the conclusion that the 10 species in Table 1 breed each
summer much farther north in eastern United States than they overwinter.
For the monarch and the fall armyworm the northward seasonal spread has
been mapped (Baker 1978: 426; Snow and Copeland 1969); the former
reaches Canada by late May while the latter apparently arrives 2 months
later.3
The 5 moths in Table 1 are major pests, and 1 of the butterflies (U.
proteus) is a minor pest. Long distance movements of Lepidoptera, in the
eastern United States and elsewhere, are of more than academic interest.
MODELS OF MIGRATION
If one concedes that various species of North American Lepidoptera
regularly breed in areas far to the north of where they can overwinter, a
number of models may be used to accommodate the phenomenon. Three (Fig.
1) are of special interest:
Diffusion and freeze-back (Fig. la). Each spring the extent of suitable
habitats enlarges northward, reaching a maximum by midsummer. Wander-
ing, ovipositing females that happen to travel northward find unexploited,
productive habitats. The cumulative effect of random movements is a
diffusion-like net movement toward higher latitudes. Long distance unidirec-
tional flights are not involved; the rapidity and extent of spread depend on
the amount of "trivial" movement per female and the number of generations
during spring and summer. In fall, when cold weather moves southward, the
populations at higher latitudes are successively extinguished, and the winter
range is approximately the same as the year before.
Relieve population pressure (Fig. Ib). In spring, conditions in the over-
wintering area become favorable and populations rapidly increase. At some
threshold density, individuals (of the proper ontogenetic stage-perhaps
newly closed adults) emigrate. The emigrants may simply fly upward and
be carried in whatever direction the upper air is blowing. One result of
emigration is that the overwintering habitat is not destroyed by excessively
dense populations; another is that the emigrating individuals are carried
to unsuitable habitats (e.g. Atlantic Ocean or xeric grasslands) or to
(temporarily) suitable ones (e.g. summer breeding areas in the North). As
the populations build up in summer breeding areas, more emigration en-
sues. When fall arrives, breeding slows or ceases and the range contracts to
its winter extent because of cold-induced deaths at higher latitudes. The
principal difference between this and the previous model is that individuals
engage in long distance, unidirectional4 flights in response to high density.
Northward spread is rapid, not because all'or most emigrants go that direc-
tion but simply because those that do, go far.
The first 2 models present an evolutionary dilemma that is clearest in
the second: In the relieve-population-pressure model, those individuals that
unselfishly emigrate are not as well represented in the next overwintering
population as those that stay. Any genetic variation toward staying would
have a selective advantage over 1 for emigrating. In the diffusion-freeze-back
model all individuals are presumed to behave the same, but again, any
Insect Behavioral Ecology-'79
a DIFFUSION AND FREEZE-BACK
WINTER SPRING MIDSUMMER
LATE FALL EARLY FALL /
*.. .** freeze line
(No long-distance, unidirectional flights)
b RELIEVE POPULATION PRESSURE
WINTER
SPRING
x x x
.I: ~ :-;'-,;,:.:!''-
k LATE FALL
:-*:. :'-:. : 4
EARLY FALL
(Some individuals fly for and straight, then locally; others fly only locally.)
RETURN FLIGHT
WINTER
I I
r-------
MIDSUMMER
7* 7**.***.7
FALL A
(Flight southward in the fall)
Fig. 1, a-c. Three models that account for species annually breeding at
higher latitudes than they overwinter. (Upward is poleward.) (See text for
further explanation.)
Florida Entomologist 63(1)
genetic variation toward moving only short distances and avoiding poleward
movement would be favored. Each successive overwintering population should
have lesser frequencies of whatever genes promote spread into areas where
progeny or grandprogeny perish in the fall.
Return flight (Fig. Ic). In this model there is no evolutionary dilemma
because the genes that move northward in spring and summer return south-
ward in fall. The overwintering population includes not only genes from
those that stayed the previous spring but also from those that moved north-
ward. This model is not specifically concerned with the means of northward
movement (hence the blank rectangle in Fig. Ic), but it is noteworthy that
once a return flight is postulated, moving straight northward into the sum-
mer breeding area should often increase reproductive success more than
movements in other directions.
The evolutionary consequences of 3 alternative behavioral strategies are
made explicit in Table 2. The consequences of northward spread with no
return trip have already been discussed. The reproductive success of staying
compared to that of spreading northward and returning depends upon these
factors: (1) the average summertime increase per generation in the over-
wintering area compared to areas to the north, (2) number of generations
during the summer (south and north), and (3) extra mortality resulting
from migration. When the reproductive payoffs of the 2 strategies are equal
(as in Table 2), neither should replace the other. To some extent the rela-
tive payoffs will change depending on the frequencies of the alternative
strategies. For example, if only a few individuals remain in the overwinter-
ing area during the summer, their rate of increase should equal that of in-
dividuals moving northward; and, spared migratory mortality, they should
contribute more to the winter population. On the other hand, if only a few
individuals move northward, the payoff of staying is reduced and the average
increase per generation in the North may be greater-since even after 1 or
2 generations the resources of the summer breeding areas should be largely
unexploited. (If, at all frequencies, individuals moving northward fare better
than those that stay, that species should cease to breed in the overwintering
areas.) The particular values for parameters in the first 3 columns of Table
TABLE 2. EVOLUTIONARY CONSEQUENCES OF 3 GENETICALLY PROGRAMMED
ALTERNATIVE STRATEGIES. VALUES ARE HYPOTHETICAL AND AD-
JUSTED TO MAKE THE FIRST 2 BEHAVIORAL STRATEGIES HAVE
EQUIVALENT EFFECTS. SEE TEXT FOR FURTHER EXPLANATION.
Average Increase Return Contribution
increase per during trip to winter
Genotype generation* summer** mortality population
Stay 1 1 1
Spread northward;
return in fall 10 1000 0.999 1
Spread northward;
no return 10 1000 0
*Populations presumed to hold their own in already-occupied overwintering area and to
show rapid increase in newly occupied areas to the north.
**Assuming 3 generations in the North.
March 1980
Insect Behavioral Ecology-'79
2 should vary not only with the frequencies of the alternative strategies but
also with weather conditions (south and north) and with numbers of other
species (e.g. enemies, competitors, food sources).
The evolutionary forces bearing on staying or moving northward and
returning are complex, but genetically based behavioral rules that result in
a particular strategy may be fairly simple. The most complicated strategy
listed in Table 2 ("Spread northward, return in fall") is well within the
range of complexities demonstrated for genetic programming in insects.
Table 3 outlines a possible program6 and compares it with 1 that occurs in
aphids.7
Return flights are expected on the basis of evolutionary theory, and their
genetic programming is creditable-but do they occur in the 10 species of
Table 1? The answer for the 5 species of butterflies apparently is yes; for
the 5 species of moths no direct evidence of return flights exists. Are butter-
flies better (at coping with long range movements) than moths?
RETURN FLIGHTS IN BUTTERFLIES
The most convincing evidence for a return flight in butterflies is for the
monarch. Since 1938, F. A. Urquhart has headed a program of attaching
identifying labels to the wings of monarch butterflies-the equivalent of a
banding program for birds. Numerous monarchs tagged in the fall in the
North have been recovered along the Gulf coast and in central Mexico (Fig.
2b). (Directional flights northeastward in the spring also have been dem-
onstrated; see Fig. 2a.)
The evidence for a return flight in the other 4 subject species of butter-
flies is the same as the evidence in eastern monarchs prior to Urquhart's
tagging program: they are seen flying persistently in appropriate directions
TABLE 3. GENETIC PROGRAMS PRODUCING DIFFERENT PHENOTYPES DEPENDING
ON PHOTOPERIOD AND POPULATION DENSITY. THE 1 FOR MOTH OR
BUTTERFLY IS SPECULATIVE; THE 1 FOR PARTHENOGENETIC FEMALE
APHIDS IS SIMILAR TO A PROGRAM EXPERIMENTALLY VERIFIED FOR
THE VETCH APHID (LEES 1961).
Species
Conditions Phenotpye
Moth or butterfly
Photoperiod increasing and
density at maturity >D FLY NORTHWARD
Photoperiod at maturity
decreasing >2 min per day FLY SOUTHWARD
Otherwise MAKE, NO LONG-DISTANCE FLIGHT
Parthenogenetic female aphid
Photoperiod >15 h and
density >D PRODUCE ALATAE
Photoperiod >15 h and
density
Photoperiod <15 h PRODUCE SEXUAL FORMS
84 Florida Entomologist 63(1) March 1980
a Spring "- b Fal o/, V
/ 1' '
MONARCH
\ Donous plexippus
Fig. 2. Recoveries of monarchs tagged in winter (a) and late summer
(b). Redrawn from Urquhart and Urquhart (1978, 1979).
in the fall. Fall migratory flights are near the ground-i.e. in the boundary
layers-and singularly unidirectional. When a migrating individual comes
to an obstacle, such as a house or dense clump of trees, it rises and flies over
rather than deviating to the right or to the left. Nearly all individuals main-
tain approximately the same direction, and the direction is not noticeably
K *
influenced by wind or time of day (Fig. 3) (Arbogast 1966, Balciunas and
Knopf 1977).
/ i
Only the bright yellow, hard-to-ignore cloudless sulphur has been re-
\,, '' / MONARCH
heatedly observed in fall migration at localities widespread in eastern United
States (Fig. Recoveries observatif monarchs tagged all annually repeated) and ones, indicate
(b).a return flight to overwintering areas in the South. The pattern differs from1979).
that of the monarch in that most flights are towarnear the Florground-i.e in the boundaryinsula
layerS-and singularly unidirectional. When a migrating individual comes
to an obstacle, such as a house or dense clump of trees, it rises and flies over
rather than deviating to the right or to the left. Nearly all individuals main-
tain approximately the density and seassame direction, and the direction is not nomigraticeably
at Gainfluenced by wind or time of day (Fig. 3) (Arbogast 1966, Balciunas and
ware cloth (Fig. 5b) (Walker 1978, Walker and Riorden 1980). Southward
flights in the fallbright have been substantiated for 2 or more years fosulphur has been re-
peatedly observed in fall migrat were not detelocalities widespread in eastimatern United
States (Fig. 4). Most observations, and all annfrolly repeated ones, indicate 1,000
a return flight to overwignificantering southward movement starts in ttern differs fromSeptember
that of the monarch in that most flights are toward the Florida peninsula
and continues, whenever weather is favorable, into early November (Walker
I have studied the density and seasonal pattern of butterfly migrations
at Gainesville using special 2-way flight traps of polyester (Fig. 5a) or hard-
ware cloth (Fig. 5b) (Walker 1978, Walker and Riorden 1980). Southward
lights in the springfall have been substantiated for 2 or more years for 7 species
(Table 4), including 3 that were not detected visually. Estimated numbers
varied from nearly 4,000,000/km (bean leafroller, "1975") to about 1,000
(buckeye, 1979). Significant southward movement starts in early September
and continues, whenever weather is favorable, into early November (Walker
and Riorden 1980).
Flights in the spring were studied with the same traps. Only the buckeye
showed significant northward movement during more than 1 year (Table 5),
yet such movement must occur in any species that annually reoccupies
northern summer breeding areas. Failure to detect it in most species trapped
flying southward in the fall may be attributed to fewer spring migrants or
to higher or less direct flight-only butterflies that are flying low and uni-
directionally will strike the central barrier, rise, and work their way into
the catching device of a flight trap.
Insect Behavioral Ecology-'79
1020-1120 1150-1250 1500-1530 N
Cloudless Sulphur 6
'-60 25
r 90 91
,54- 47. 490
Gulf Fr till ry
58. 45'' 45I
Buckeye
5~o-
160 150 70'
Fig. 3. Flight directions of 3 species of butterflies observed during 3
periods (times at top), 7 October 1962, Gainesville, FL. All individuals
crossing a circle with a diameter of 15 m (cloudless sulphur) or 7.5 m (gulf
fritillary, buckeye) were classified as to which of 16 compass directions they
were flying. Arrows show mean vectors; r is a measure of scatter about
mean vector (Batschelet 1965).
RETURN FLIGHTS IN MOTHS
Visual monitoring of migratory flights of moths is seldom possible-most
moths fly at night and are difficult to identify on the wing even when flying
in daylight. Monitoring with Malaise traps seems a likely alternative, except
that most migratory flights of moths are apparently above the boundary
layer and out of reach of conventional flight traps.9
The migratory movements easiest to demonstrate for moths are flights
that result in seasonal reoccupation of areas from which earlier populations
have disappeared (e.g. northward movements of species in Table 1). In a
few species return trips can be substantiated with the same logic-the moth
occupies only 1 area at 1 time of year and only another at another; there-
fore, to-and-fro migration must occur. The best documented examples are
for the bogong moth of eastern Australial1 and the army cutworm of western
United States (Fig. 6). Both are noctuids, as are the 5 moths in Table 1, and
each flies to aestivation sites in the mountains in the spring and then to
breeding sites on the plains in the fall. Directional flights in appropriate di-
rections have been reported for both species (Common 1954, Pepper 1932,
Pruess and Pruess 1971), though the importance of such observations has
been questioned (Johnson 1969: 453).
Florida Entomologist 63(1)
March 1980
Fig. 4. Observed directions of late summer and fall migratory flights of
cloudless sulphur (data from Williams 1930, 1958; Lambremont 1968; Howe
1975; Urquhart and Urquhart 1976; Muller 1977; personal observations).
Solid arrows are observations made during more than 1 year.
At any rate, noctuid moths can migrate in opposite directions at ap-
propriate seasons, and individuals of the 5 species in Table 1 would benefit
by migrating southward in the fall from summer breeding areas in the
North. Without visual observations or flight-trap counts, how can the oc-
currence, or nonoccurrence, of return flights by the 5 be demonstrated? The
hypothesis of return migration warrants certain predictions that are subject
to refutation by experiment. The 4 tests that seem strongest are discussed
below in order of increasing cost.
Behavior in tethered flight. The flight of a tethered insect can indicate
whether it would migrate if free, and if so, what heading it would take. For
example, Dingle (1978) used duration of tethered flight in milkweed bugs
(Oncopeltus fasciatus) as an index of migration potential and showed that
long flights were more frequent when bugs had been reared under fall-like
conditions of lower temperatures (23 vs 27 C) and shorter photoperiods
(12L:12D vs 16L:8D). Sotthibandhu and Baker (1979) used a specially
constructed flight monitor to record the orientation of moths flying tethered
in the field; the moths showed compass orientation (without time compensa-
tion) so long as the moon or stars were visible.
For the 5 species of moths in Table 1, long-duration tethered flights
should be characteristic of moths reared under photoperiods and tempera-
tures typical of the North in late summer and fall and, especially if the
moths are reared at high densities, of the South in spring. Furthermore,
orientation should be southward for the former and northward for the latter.
Flights to "wrong" places. The hypothesis of return flights implies that
Insect Behavioral Ecology-'79
A
Fig. 5. Two-way flight traps used for monitoring migration in the
OF7: WIW ,- RR oi I .... -
boundary layer, Gainesville, FL. (a) Four polyester net traps used fall
1978 (Walker and Riorden 1980). Openings are ca. 6x2 m. (b) Hardware
cloth (1.3x1.3-cm mesh) malaise trap used 20 March 1979-date. Opening to
either side is ca. 6x3 m. Catching devices at either end are covered with
6x6-mm mesh hardware cloth.
. . .. 1. A4z jj'f '0
Fig. 5.Two-wa fligh trap sdfo oioin irtini h
bondrylye, aievile F.(a Fu plystrne tap se fl
1978(Waler nd Rordn 190).Openngsare a. x2 m (b Harwar
cloth(1.3x.3-cmmesh)malaie tra used20 Mach 199-dat. Opening t
eitersid i c. W m.Cathig eviesateiterendar cverd it
6x-m mshhadwreclth
Florida Entomologist 63(1)
March 1980
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Florida Entomologist 63(1)
March 1980
b
---- -- --
ARMY CUTWORM BOGONG MOTH
Chor zogrolis auxihoras Agrohs nfusa
Fig. 6. Approximate summer and winter ranges of 2 noctuid moths. (a)
Army cutworm spends summers in Rocky Mountains and is a pest of winter
wheat in the Great Plains (Pruess 1967). (b) Bogong moth spends summers
in Austrailian Alps and in the winter is a pest of wheat and other crops on
the Western Slopes to the north (Common 1954).
the moths in Table 1 fly in such a way as to have a high probability of
reaching certain areas, specifically northern breeding areas in spring and
southern overwintering areas in late summer and fall. Since migratory
flights apparently occur at altitudes where wind speeds exceed the moth's
air speed (see below), moths must time their takeoffs to take advantage of
favorable winds: they must predict in what direction the upper air will
carry them. Many cues are useful for such weather prediction (Muller 1979).
For example, the first warm evenings in the spring in the South usually
coincide with northward winds. However, weather prognostication is un-
certain, especially if local conditions are the only data that can be used. The
best programmed moth may occasionally fly into the upper air and be carried
in a disastrous direction. This line of reasoning leads to the following pre-
diction: when moths end up in nonadaptive ("wrong") places, weather pat-
terns should be anomalous. Testing this prediction calls for monitoring some
of the wrong places with light traps-e.g. drilling platforms in the Gulf"1
and areas north of normal breeding areas. Whenever large numbers of
moths are collected in a "wrong" place and back-tracked to their appropriate
source,12 the initiating weather (specifically the aspects that moths sense)
should be of a type that normally correlates with upper winds flowing in an
adaptive direction. For example, large numbers of fall armyworm moths (as
revealed by large numbers of eggs laid) arrived at Sault Ste. Marie, Ontario,
on the night of 3-4 Sept. 1973. Rose et al. (1975) concluded that they had
come from northern Mississippi, 1600 kni to the south, in about 30 h in
association with convective storms at the source and a northward low-level
jet wind.
Recapture of marked moths. Releasing marked moths may seem a hope-
lessly optimistic procedure for discovering where moths go, especially since
moths are too small to carry informative labels such as used by Urquhart
(1960) on monarchs and Roer (1968) on nymphalid butterflies. Furthermore,
moths are nocturnal and marked ones are unlikely to be visually detected
Insect Behavioral Ecology-'79
and then captured. However, a group of Chinese researchers that marked
and released hundreds of thousands of field-collected oriental armyworm
moths (Pseudaletia separate) recovered at least 7 spring-marked moths
>500 km to the north and 1 fall-marked moth 800 km to the south (Li et al.
1964, Baker 1978). The labor (and cost) of marking moths can be reduced
by machines such as the 1 developed by Wolf and Stimmann (1972) for
cabbage looper. It automatically marked up to 1500 moths an hour with
colored ink without adversely affecting their longevity or mating ability.
Rare elements could be added to the inks to permit detection of false positives
(Southwood 1978: 78).
The most economical way to use marked moths to test for moth migra-
tion patterns in the eastern United States would combine marking and re-
leasing massive numbers of field-collected or field-reared moths at mid
latitudes (35-400) with extensive light trapping to the north and south.
Movement in early summer should be predominantly to the north; in the fall,
predominantly to the south. Instances of contrary movements should be
analyzed as suggested in the previous section.
Radar observations with aircraft support. Modern radar units can be
used to track the flight of individual insects for several kilometers13 and to
determine their altitude, heading, and ground speed. Unfortunately, radar
images are inadequate to identify the species of insect being tracked, though
by measurements of size and wingbeat frequency a mosquito or locust need
not be confused with a moth (Schaefer 1976). The species followed can be
inferred when masses of a single species are known to be taking off or land-
ing in the observation area (cf. desert locusts or spruce budworm moths).
Otherwise, identification must depend on aircraft collection of samples from
the observed flight. The same aircraft can be used to monitor temperature
and wind conditions bearing on flight behavior. Thus far, the most surpris-
ing finding from radar observations of migrating insects is that individuals
in a flight at a given altitude are usually maintaining the same heading
(even at night and though widely spaced). The heading is generally down-
wind, making the insect's ground speed 2-6 m/s faster than wind speed
(Schaefer 1976). Sometimes the generally-adopted heading differs strongly
from downwind. For example, Riley (1975) reported a night-time flight of
insects (probably locusts) at a height of ca. 900 m in which individuals were
maintaining a common northeastward heading and flying at an airspeed of
5 m/s directly into a 2 m/s southwestward wind (i.e. ground speed was 3
m/s northeastward).
Radar observation with aircraft support could be used in eastern United
States to study flights of the moths listed in Table 1. The hypothesis of a
return flight would be refuted if their flight behavior did not enhance their
chances of traveling southward in the fall.14
DiscussioN
In the fall, butterflies return from breeding areas at higher latitudes.
Moths probably do, their migratory flights differing from those of butterflies
in ways summarized in Fig. 7. The preeminent determiner of the differences
seems to be that moths fly at night and butterflies in daylight. A proof of
Optimal height for migratory flights should increase from day to night
for a variety of reasons. During daylight, visually hunting aerial insectivores
Florida Entomologist 63(1)
~Im~Crc 1c
March 1980
Fig. 7. Comparison of flight strategies in migrating butterflies and moths.
this conjecture is that day-flying moths that migrate do so in the manner of
butterflies (e.g. 2 species of the genus Urania, Williams 1958). The counter
case, night-flying butterflies that migrate, is unknown.15
-such as kites and large swifts-make it dangerous to fly so high that
refuge cannot be reached quickly.16 At night, insects flying near the ground
are at greater hazard from obstacles that must be visually avoided and from
spider webs. During the day the smoothest (i.e. least turbulent) and warmest
air is near the ground.17 At night the smoothest and warmest air is often at
the top of a thermal inversion, exactly where migrating moths sometimes fly
(e.g. Johnson 1969: 449; Schaefer 1976: 188).s1
Flying low permits detection of food and host plants and makes it easy
for the migrating insect to stop briefly and feed or lay eggs. Migrating
butterflies frequently feed when they come upon suitable food (Richman and
Edwards 1976); in some species most migrating females have mated and
carry mature eggs (Williams 1930, Walker 1978); they presumably oviposit
along their migratory route.19 On the other hand, flight in the upper air
does not facilitate detection of food or hosts, and stop-and-go migration
would involve long descents and ascents. Since traveling in the boundary
layer is both slower and energetically more costly per km than traveling
downwind in the upper air, feeding during near-ground migration may be
necessary as well as convenient.
Migrating in the upper air likewise has problems as well as benefits.
Since the velocity of upper-air wind generally exceeds the migrant's air
speed, the migrant loses options and ease of control as to its direction of
travel. Unless it forecasts the winds correctly, it may travel in a direction
opposite that of its heading (assuming that it is programmed to fly in a par-
DAYTIME S,
FLIGHTS 1 oa
Obstacles Turbu ent S
visible to en eldom
migrants ware off
migrants, to below
predators be
IN Wind
BOUNDARY slowerthan
LAYER flight
Food and hosts
detectable, Travel "
stop-and-go flight nerge call
cheap costly ed
g forecast
Swings
INTERRUPTED
FOR FEEDING
8 EGG LAYING
Mull
COMPOSS7 NOCTURNAL
FLIGHTS
Smooth
Often Obstacles aloft;
off and migrants colder
course?,, hard to see below
4W
IN
UPPER
AIR
Food and hosts too
distant to detect;
costly
s top-and-go flight
NOT
INTERRUPTED
m
Insect Behavioral Ecology-'79
ticular compass direction) and may terminate its flight farther from a
suitable place than where it started. Whether moths migrating at night
can maintain compass orientation as butterflies do in daylight (Fig. 3) is
uncertain.20 Even if they can, the speed of the wind and the difficulties in
detecting wind direction make moths at greater risk of gross errors in
navigation than butterflies. However, moths that reach their programmed
destination may do so much more quickly than butterflies, and the average
total migratory risk for moths and butterflies need not be different.
Are butterflies better at migrating than moths? Maybe, maybe not; but
they surely do it differently.
ACKNOWLEDGEMENTS
I thank Dave Doying and Carl Barfield for permission to refer to un-
published data; Ken Prestwich and Al Riorden for advice in energetic of
flight and meteorology; and Carl Barfield, Susan Jungreis, J. E. Lloyd, and
Everett Mitchell for constructive criticism of the manuscript.
APPENDIX
1Annual movements to breeding areas at higher latitudes occur in at
least 6 insect orders: ORTHOPTERA, Schistocerca gregaria, Johnson 1969:
571; HEMIPTERA, Oncopeltus fasciatus, Dingle 1978; HOMOPTERA, leaf-
hoppers and aphids, Johnson 1969; COLEOPTERA, Diabrotica undecim-
punctata, Johnson 1969: 414-5; LEPIDOPTERA, this paper; DIPTERA,
Musca vetustissima, Hughes and Nicholas 1974, Hughes 1979.
2The difficulty with negative evidence is well illustrated by R. R. Baker's
(1978: 425-33) recent speculation that about 30% of D. plexippus in the
Great Lakes region hibernate rather than migrate southward. Experimental
evidence for inability to overwinter is surprisingly scanty and restricted to
A. vanilla (Randolph 1927), T. ni (Elsey and Rabb 1970), and S. frugiperda
(Wood, Poe, and Leppla 1979). More research of this type is of critical im-
portance in refining the questions relative to migration of the species in
Table 1. The weakest case for inclusion of a species in Table 1 is for P.
coenia. I have found no definite statement as to its absence in the North in
winter. Mather (1967 and personal communication) reported it overwinter-
ing as far north as Jackson, MS. Interestingly, it is the only species other
than the monarch with strong evidence for a northward flight in the spring
(Table 5).
3The first D. plexippus to arrive is much more likely to be seen than the
first S. frugiperda. Detailed mapping, based on extensive, systematic ob-
servations, is yet to be done for any species. The best data are for T. ni and
P. includes but the observations were limited to South Carolina and south-
ward. The lack of suitable data may be illustrated by P. coenia. Howe (1975:
137) reported it to occur north to southern Ontario and New England, but
how regularly does it reach that far north? When it does, does it success-
fully breed there?
4Unidirectional travel need not depend on a constant individual heading.
If the individual flies, in any direction, in an air stream that is moving much
faster than the individual's air speed, the individual's track will be chiefly
in the direction of the air stream. Only if emigration occurs near the ground,
where wind speeds are substantially less than air speeds, will the individual's
heading be the chief determinant of its track.
5C. B. Williams (1958: 132) understood and stated the dilemma clearly:
"If the habit of long-distance migration has persisted in certain insects for
Florida Entomologist 63(1)
March 1980
(presumably) millions of years, and if every individual which shows the
habit flies away from the breeding ground and is lost (as far as continuing
the species is concerned), then we have to admit that a habit which is com-
pletely fatal to all individuals possessing it can continue to persist for
countless generations!"
6The proposed program is more complicated, and perhaps more realistic,
than the one implied in Table 2 and in the discussion of frequency-dependent
selection. In Table 3, flying northward or staying in the overwintering area
in the spring is made conditional on density. The same genotype can produce
either behavior, and there need be no equilibrium between genotypes that
have the potential for one or the other (but not both). Dawkins (1979)
distinguished 3 phenomena that lead to continued mixtures of behaviors
within a deme: stable polymorphism, individual mixed evolutionarily stable
strategy, and conditional strategy. The strategy outlined in Table 3 for
migratory Lepidoptera is conditional; a stable polymorphism was described
in the discussion of maintaining a mixture of the first 2 behaviors in Table
2. Cade (1980), in this symposium, applied Dawkin's classification to male
reproductive behaviors.
7Aphids are especially useful in demonstrating conditional genetic pro-
grams because members of parthenogenetic clones can be studied, with all
differences in phenotypes attributable to different environments.
SThe boundary layer for an insect is the layer near the ground in which
its air speed exceeds wind speed, giving the insect potential control of its
track. The thickness of the boundary layer varies with wind speed and with
the insect's air speed. The 4 species in question generally fly within 2 m of
the ground. The monarch often flies higher but is more powerful and has a
top air speed of at least 40 km/hr (Urquhart 1960). It is also an accom-
plished soarer (Gibo and Pallett 1979).
9The flight traps that detected spring and fall migratory flights of
butterflies at Gainesville were operated 24 h per day and caught significant
numbers of moths. However, no biases in flight direction of the magnitude
typical of migrating butterflies were detected (Walker 1978, C. S. Barfield,
unpublished data).
o'Common (1954: 256) doubts that all Bogong moths aestivate, reporting
that an "occasional larva has been collected in a garden at Canberra in
December." However, he gives no evidence for summer breeding in the plains
to the north.
"A. N. Sparks (Sparks et al. 1975 and unpublished) ran blacklight traps
on unmanned oil platforms as far as 160 km from shore in the Gulf of
Mexico, south of Jeanerette, LA, 9 Sept.-21 Oct. 1973. The S. frugiperda and
S. exigua he collected (numbers but not dates given in Mitchell 1979) could
be used to test this hypothesis-provided these moths do not normally mi-
grate across the Gulf of Mexico to Central America in the fall.
12Back-tracking involves plotting the location of migrants at various
preceding times and dates on the basis of data and assumptions about wind
conditions, flight altitude, and flight speed. For examples, see Johnson 1969:
516-23, and Rose et al. 1975.
"The most commonly available radar units can track a single moth at
distances no greater than 2 km, but more specialized units can stretch this
to ca. 8 km. Swarms of moths can be detected at greater distances (Schaefer
1976, Skolnik 1978).
14To enhance their chances of traveling southward, moths might (1) fly
upward and submit themselves to passive transport in the upper air only
when local conditions were indicative of southward winds, (2) maintain
southward headings and fly only when the resulting track was southward-i.e.
fly only if winds are southward or too light to prevent progress southward.
Merely flying upward and maintaining altitude does not qualify as "return
Insect Behavioral Ecology-'79
flight" (sensu Fig. 1), even if it sometimes has the same result. As Rainey
(1978) pointed out, wheat rust fungi, by means of airborne spores, occupy
northern summer breeding areas each spring and return southward in the
fall. In making a "return flight," a moth must exert better control over its
destination than does a fungus spore.
15Williams (1930: 341) cited numerous records of migratory butterflies
flying at night, but most relate to individuals that may have been over water
since dusk.
6"The remarkable exception" (Williams 1930: 338) to migrating butter-
flies flying within a few meters of the ground is the monarch (see also Gibo
and Pallett 1979). However, monarchs are protected to a large extent from
bird predation by a heavy load of cardenolides acquired during larval feed-
ing (Brower and Glazier 1975). Nocturnal flights above the boundary layer
are endangered by predators too: echo-locating bats can catch flying insects
in total darkness. However, noctuid moths have tympana that are sensitive
to the hunting sounds of bats and can sometimes take successful evasive
action (Roeder 1966).
"Within the daytime convective layer, the region of thermally induced
mixing that sometimes extends upward 1 km or more, turbulence increases
with altitude at least for the first 50 m or so (Kaimal et al. 1976). The
warmth of the boundary layer air may be of importance to butterflies be-
cause they require a thoracic temperature of at least 27 C for controlled
flight (Douglas 1979) yet have a slow wingstroke rate and are not as well
insulated as moths.
IsTurbulence increases above the inversion layer. The fact that tempera-
tures are less above and below the top of the inversion layer is of uncertain
significance. Moths are insulated by their scales and can fly in cold air, but
whenever they are unable to maintain optimal flying temperature using only
the heat generated as a byproduct of flight, they can increase their efficiency
by flying in warmer air.
"1No data exist on the frequency of oviposition by butterflies enroute to
overwintering areas. Laying eggs has value only if the resulting progeny
have time to complete their development and follow their mother equator-
ward. Since a generation requires ca. 1 month (Urquhart 1960, Arbogast
1965) and fall migration lasts up to 2 months (Walker 1978, Walker and
Riorden 1980), early migrants should benefit from laying eggs. Arbogast
(1965: 30-3) found a peak of egg laying by A. vanilla corresponding to the
first half of fall migration through Gainesville, FL. Butterflies flying pole-
ward in the spring should oviposit because they are entering unexploited yet
suitable habitats and suitability of habitats farther along, and their own
survival, are uncertain.
20The means of orientation in migrating butterflies has not been proved,
but field observations (Fig. 3) are compatible with their using a time-
compensated sun compass, or a magnetic compass (Arbogast 1965, Kanz
1977, Lindauer 1977). Nocturnally migrating moths cannot use a sun com-
pass, yet they can maintain a common heading (Schaefer 1976). That this
heading is generally downwind suggests that the orientation may be in rela-
tion to the air stream rather than to the points of the compass. However,
orienting to an air stream while in it, especially at heights and times that
make visual cues from the ground unlikely, is at least as hard to explain as
heading in a compass direction at night. Actually, selecting an airstream
that is moving in the migratory direction may require that the moth do both!
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