Title: Florida Entomologist
Full Citation
Permanent Link: http://ufdc.ufl.edu/UF00098813/00066
 Material Information
Title: Florida Entomologist
Physical Description: Serial
Creator: Florida Entomological Society
Publisher: Florida Entomological Society
Place of Publication: Winter Haven, Fla.
Publication Date: 1991
Copyright Date: 1917
Subject: Florida Entomological Society
Entomology -- Periodicals
Insects -- Florida
Insects -- Florida -- Periodicals
Insects -- Periodicals
General Note: Eigenfactor: Florida Entomologist: http://www.bioone.org/doi/full/10.1653/024.092.0401
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Bibliographic ID: UF00098813
Volume ID: VID00066
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: Open Access

Full Text

(ISSN 0015-4040)


(An International Journal for the Americas)

Volume 74, No. 1 March, 1991


Announcement 74th annual meeting ........................................ ............ i


FRANK, J. H., AND E. D. McCoy-Introduction To Attack and Defense: Be-
havioral Ecology of Defense. Medieval Insect Behavioral Ecology, and
Chaos ...................................................... ............................. 1
SHEA, C. S., AND J. T. ROMEO-Nutritional Indices: Do They Explain Toxicity
of Calliandra Amino Acids? ............................................................ 10
KLOCKE, J. A., AND I. KUBo-Defense of Plants Through Regulation of Insect
Feeding Behavior .............................................. ...................... 18
BREWSTER, C. C., AND J. C. ALLEN-Simulation of Plant Resistance in a Cel-
ery-Leafminer-Parasitoid Model .................................... ............ 24
TURLINGS, T., AND J. H. TUMLINSON-Do Parasitoids Use Herbivore-Induced
Plant Chemical Defenses to Locate Hosts? ....................................... 42
ALLEN J.-Chaos and Coevolution: Evolutionary Warfare in a Chaotic Predator-
Prey System .............................................. ...... .................... 50

Research Reports

PRICE, J. F., AND D. J. SCHUSTER-Effects of Natural and Synthetic Insec-
ticides on Sweetpotato Whitefly, Bemisia tabaci, (Homoptera:
Aleyrodididae) and its Hymenopterous Parasitoids ............................ 60
MARENCO, R. J., R. E. FOSTER, AND C. S. SANCHEZ-Residual Activity of
Methomyl and Thiodicarb Against Fall Armyworm in Sweet Corn in
Southern Florida ............................................... ...................... 69
Choice in Ground Crickets (Gryllidae: Nemobiinae) ............................ 74
and Rates of Parasitism by Nymphal and Adult Parasites of the Salt-
Marsh-Inhabiting Planthoppers Prokelisia marginata and P. dolus ......... 81
STILING, P., B. V. BROADBECK, AND D. R. STRONG-Population Increases of
Planthoppers on Fertilized Salt-Marsh Cord Grass May Be Prevented By
Grasshopper Feeding ............................................ .................... 88
JIRON, L. F., AND I. HEDSTROM-Population Fluctuations of Economic Species
of Anastrepha (Diptera: Tephritidae) Related to Mango Fruiting Phenology
in Costa Rica ................................................ .......................... 98
ANDERSON, R. S.-A New Species of Plocetes From the Florida Keys With Notes
on Other Species Occurring in the United States (Coleoptera: Cur-
culionidae; Curculioninae; Tychiini) .............................................. 105

Continued on Back Cover

Published by The Florida Entomological Society

P resident .................................... ............................................... J. F. Price
President-E lect ............................. .......................................... J. L. Knapp
Vice-President .......................................................................... D F. W illiam s
Secretary ... .................................................................. ..... J. A Coffelt
Treasurer ................................ .............................................. A C K napp
Other Members of the Executive Committee
J. E. Eger J. E. Pefia J. R. Cassani J. Hogsette
J. R. McLaughlin S. Valles M. Lara
J. R. McLaughlin, USDA/ARS, Gainesville, FL ....................................... Editor
Associate Editors
Agricultural, Extension, & Regulatory Entomology
Ronald H. Cherry-Everglades Research & Education Center, Belle Glade, FL
Michael G. Waldvogel-North Carolina State University, Raleigh, NC
Stephen B. Bambara-North Carolina State University, Releigh, NC
Biological Control & Pathology
Ronald M. Weseloh-Connecticut Agricultural Experiment Sta., New Haven, CT
Book Reviews
J. Howard Frank-University of Florida, Gainesville
Chemical Ecology, Physiology, Biochemistry
Louis B. Bjostad-Colorado State University, Fort Collins, CO
Ecology & Behavior
John H. Brower-Stored Product Insects Research Laboratory, Savannah GA
Theodore E. Burk-Dept. of Biology, Creighton University, Omaha, NE
Forum & Symposia
Carl S. Barfield-University of Florida, Gainesville
Genetics & Molecular Biology
Sudhir K. Narang-Bioscience Research Laboratory, Fargo, ND
Medical & Veterinary Entomology
Arshad Ali-Central Florida Research & Education Center, Sanford, FL
Omelio Sosa, Jr.-USDA Sugar Cane Laboratory, Canal Point, FL
Systematics, Morphology, and Evolution
Michael D. Hubbard-Florida A&M University, Tallahassee
Howard V. Weems, Jr.-Florida State Collection of Arthropods, Gainesville
Willis W. Wirth-Florida State Collection of Arthropods
Business M manager ............................................. ...................... A. C. Knapp
FLORIDA ENTOMOLOGIST is issued quarterly-March, June, September, and De-
cember. Subscription price to non-members is $30 per year in advance, $7.50 per copy;
institutional rate is $30 per year. Membership in the Florida Entomological Society,
including subscription to Florida Entomologist, is $25 per year for regular membership
and $10 per year for students.
Inquiries regarding membership and subscriptions should be addressed to the Busi-
ness Manager, P. O. Box 7326, Winter Haven, FL 33883-7326.
Florida Entomologist is entered as second class matter at the Post Office in DeLeon
Springs and in Winter Haven, FL.
Manuscripts from all areas of the discipline of entomology are accepted for consider-
ation. At least one author must be a member of the Florida Entomological Society.
Please consult "Instructions to Authors" on the inside back cover.
This issue mailed March 29, 1991


The 74th annual meeting of the Florida Entomological Society wil be held August
4-7, 1991 at the Ritz Carlton Hotel, 280 Vanderbilt Beach Road, Naples, Florida 33963;
telephone (813 598-3300. Registration forms and information will be mailed to members
and will appear in the Newsletter and the March, 1991 issue of Florida Entomologist.


The deadline for submission of papers and posters for the 74th annual meeting of
the Florida Entomological Society will be May 15, 1991. The meeting format will be
similar to those in the past with eight minutes allotted for presentation of oral papers
(with 2 minutes for discussion) and separate sessions for members who elect to present
a Poster Exhibit. There will be student paper and poster sessions with awards as in
previous years. Students participating in the judged sessions must be members of the
Florida Entomological Society and registered for the meeting.

David F. Williams, Chairman
Program Committee, FES
Medical and Veterinary Entomology Research Laboratory
Gainesville, Florida 32604
(904) 374-5982 or 374-5903

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Insect Behavioral Ecology '90 Frank & McCoy

Introduction To


Entomology and Nematology Department, 970 Hull Road,
University of Florida, Gainesville, FL 32611, USA

E. D. McCoY
Department of Biology, University of South Florida,
Tampa, FL 33620, USA


Behavior of ants and bees was perceived by medieval European writers as virtuous.
Singing by crickets and cicadas was perceived as profligate. Medieval writers used
these precepts to impart order to human behavior. Aggressive behavior by antlions was
noted by a medieval writer, but defensive behavior by insects, the complement of
aggression, was overlooked. Crickets were credited with medicinal properties, perhaps
by error of transcription. Public perception of insect behavior may have deteriorated
in the ensuing centuries. Plants use chemicals in defense against herbivores, and hu-
mans use chemicals extracted from plants to defend other plants. Herbivores extract
chemicals from plants in defense against predators and parasitoids. Parasitoids use
chemical cues to detect herbivores, aided by the plants themselves. The concept of
chaos provides an explanation of some complexities, though it seems the antithesis of
medieval order.


El comportamiento de homigas y abejas fue considerado virtuoso por escritores
europeos medievales. El canto de grills y chicharras fue considerado vicioso. Los escri-
tores medievales ulitizaron estos preceptos para impartir orden al comportamiento
human. El comportamiento agresivo de la hormiga 16on fue observado por un escritor
medieval, pero el comportamiento defensive de insects, el complement de la agresi6n,
fue obviado. A los grills les fueron acreditadas propiedades medicinales, probablemente
por error de transcripci6n. La percepci6n pfblica del comportamiento de insects puede
haberse deteriorado en los siglos subsiguentes. Las plants usan sustancias quimicas
como defense en contra de herbivoros, y los humans utilizan sustancias quimicas ex-
traidas de las plants para defender otras plants. Los herbivoros extraen los quimicos
de las plants como defense en contra de depredadores y parasitoides. Los parasitoides,
ayudados por las plants, utilizan sefiales quimicas para detectar herbivoros. El con-
cepto de caos provee una explicaci6n de algunas complejidades, anque ellas lucen como
la antitesis del orden medieval.

Our previous introductions to behavioral ecology symposia used citations from early
literature to explain the origins of modern concepts (Frank & McCoy 1989, 1990). In
this introduction we examine the reductionist concepts of medieval writers to emphasize
the hazards of modern reductionism in insect behavioral ecology.

2 Florida Entomologist 74(1) March, 1991

The zoological work of Aristotle was largely neglected in 12th century Europe, and
a new category of writings on animal behavior was developing: the bestiary. Bestiaries
concerned animals that the writers believed to be real, such as ants, bees and crickets,
as contrasted with animals widely perceived to be purely mythical, such as centaurs,
mermaids and wyverns. Inclusion of behaviors of dragons, griffins, and unicorns shows
that the writers believed and borrowed heavily from folklore, and did not limit the
accounts to their own observations.
Antecedents of the medieval bestiary have been traced to a work in Greek but not
derived from the work of Aristotle. It was written "before 140 BC" (Cook 1921), "prob-
ably ... the second century AD" (Clark & McMunn 1989), "in second century Alexan-
dria" . [by an] "anonymous author, Physiologus, or "The Natural Historian" . .
[whose] identity .. will probably never be discovered" (Ives & Lehmann-Haupt 1942).
It, in turn, had origins in Indian, Hebrew, or Egyptian legends (Curley 1979. It was
translated into Latin before 431 AD and numerous other languages (Cook 1921), but it
is from the Latin versions that the various medieval bestiaries descend (Clark &
McMunn 1989). The purpose of these bestiaries was not to interpret animal behavior;
in fact the behaviors described were often misinterpreted. Instead, bestiaries were
written as a means of instruction: to influence the behavior (and thus ecology) of hu-
Under the next four headings we examine the behavior of insects as described in a
few of the medieval bestiaries. Generally it is clear how the examples were intended to
influence human behavior. In zoology, the common names ant, antlion, bee, cicada and
cricket refer not to species, but to families (Formicidae, Myrmeleontidae, Apidae,
Cicadidae and Gryllidae) of insects. The plurality dictated by the familial reference
allows us to write "the ants", "the antlions", etc., but does not accord with literary use.
By writing "an ant" we can serve the zoological meaning but not the literary, and by
writing "the ant" we can serve the literary but not the zoological meaning. So we have
chosen to omit the definite article "the" at introduction of ant, antlion, etc. Latin,
because it does not use an article "the", here has an advantage over English and French.


The author, Theobaldus, was perhaps abbot of Monte Cassino in 1022-1035 AD
(Rendell 1928). Whoever he was, he wrote a metrical bestiary in Latin concerning 12
animals. A version of this bestiary (Phisiologus Theobaldi Episcopi), printed in Col-
ogne in 1492, has 18 metrical lines followed by almost two pages of interpretive text
under the heading formica (ant), the only example drawn on an insect. Below are the
18 lines, separated by virgules, and followed by a translation [a composite of translations
by Rendell (1928) and Eden (1972)].
De formica. Exemplum nobis prebet formica laboris/ Quando suo solitum portat in
ore cibum/ Inque suis factis res monstrat spirituales/ Quas (quia iudeus non amat), inde
reus/ Ut valeat brume fieri secura future/ Dum calor in terra non requiescit en/ Nosque
laboremus fratres, dum tempus habemus/ Securi fieri tempore iudicii/ Hec frumenta
legit, si comperit ordea spernit/ Tuque novam legem college non veterem/ Sed ne de
pluviis aspersum germinet udis/ Aut id ne pereat esse quod nequeat/ Granum (quod
legit) prudens formica bipertit/ Hoc est quod binas lex habet una vias/ Que terrena sonat
simul et celestia donat/ Nunc mentem pascit, et modo corpus aliit/ Nos ut lex repleat
famis formido recedat/ Tempore iudicii, quod simile est hyemi.
Ant provides us with a model of labor when it carries its food in its mouth. In this
it shows spiritual qualities that the Jew does not love, wherefore he stands accused. To
be free of worry for the coming winter it does not rest while there is warmth, so let us
work, brothers, while we have time, to be free of worry at the judgement. It harvests
grain; if it finds barley seeds it rejects them; I harvest the new law, not the old. But

Insect Behavioral Ecology '90 Frank & McCoy

to prevent the grain from germinating, splashed by rain, or to prevent itself from
perishing, unable to eat, the ant prudently bisects the harvested grain. That is, one law
has dual interpretation; what sounds earthly simultaneously appears heavenly. Now it
feeds the mind and so nourishes the body. Would that it fill us so that the terror of
hunger recede at the time of judgement, which is like winter.


Greek versions of Physiologus included pupJK'nKoXkovToC which vanished from later,
Latin versions perhaps because the mythical nature of this antlion became too much for
later writers to accept (White 1958). This antlion (myrmikoleontos) was supposed to
have a carnivorous father with the face of a lion and herbivorous mother with the face
of an ant, resulting in an ant-like offspring with the face of a lion. The unfortunate
offspring, torn between herbivory and carnivory, was doomed to starve. The moral
interpretation given was that it is not proper for the religious to be of two minds (Curley
Guillaume le Clerc, otherwise known as Guillaume le Normand, compiled his bestiary
early in the 13th century; its religious purpose was evident in the title as well as in
Guillaume's statement that the examples were "to benefit the soul" (Beer 1986). It was
not the first bestiary written in France or in French, but was written in octosyllabic
verse and may be the most literary (Curley 1979). Among Guillaume's lengthy and
moralizing treatment of formi (ant) in some versions is brief reference to formicaleon
antlionn), and these are the only insects represented. Original wording about formica-
leon is given below as reproduced by Reinsch (1892, with a translation [based on trans-
lations by Druce (1923) and Pierre Jolivet, but rewritten by Howard Frank in the
octosyllabic style of the original]. This account of formicaleon is anomalous in the text
because it bears no moral message.
Formicaleon. Uncor i a altre formi/ Que nul de eels que jeo vos di/ Qui formicaleon
a non/ Des formiz est cil le lion/ Si est li plus petiz de toz/ Li plus hardiz e li plus proz/
Altres formiz het durement/ En la puldrere element/ Se musce, tant est veziez/ Quant
les altres venent charge/ Sor els de la puldrere salt/ Si les occit, se les assault.
There ss yet another ant/ Different from those I've told you of/ Known by the name
of antlion/ Among the ants it is the lion/ It is the smallest of them all/ It is the hardiest
and the most wise/ The other ants it hates bitterly/ In the dust quite skilfully/ It conceals
itself, so clever it is/ When the others come with loads/ Out of the dust it jumps upon
them/ It assaults them and it kills them.


The author of this work is unknown, but it was printed in 1508 by Vincenzo Berruerio
in Mondovi, Piedmont (Davis 1958, McCulloch 1963). Its Latin prose text includes 2
sections on insects: apis bee) and cicada (cicada), the latter as follows [translation by
Bruce Woods].
De cicada. Natura sive proprietas Cicade talis est quod tantus delectatur suo cantu
quod obliviscitur omnium et sic moritur obmisso cibo. Unde illi homines possunt cum
cicade suis actibus culparari qui tantus delectatur suo cantu id est vanitatibus et delec-
tationibus huius mondi quod bonorum omnium sunt obliti et obmisso cibo id est Christi
corpore private moruntur id est ad penas dampnantur ietiferas et eternas nam nesciunt
nomen nostri regis et duplici conlaudare nec laudabunt postquam sunt ab eorum corpora
separate luxta illud non mortui laudabunt te domine neque omnes qui descendunt in
The nature or character of cicada is such that it delights in its own song to such an
extent that it forgets all and dies for lack of food. Whence those men are able, with the

4 Florida Entomologist 74(1) March, 1991

Fig. Cicada. From the Mondovi Libellus de Natura Animalium (1508). Note the 6
pairs of legs. The only medieval illustration of antlion discovered by Druce (1923) is in
a 15th century bestiary which has a crude illustration of this insect facing an ant, each
with 4 pairs of legs.

cicada, to be blamed for their own actions, who delight in their own song, that is [their]
vanities and the delights of this world, to such an extent that they have become forgetful
and die for lack of food, that is the body of [their] private Christ that is they are
condemned to an eternal and death-bringing punishment, for they do not know the name
of our king and they, in a two-faced fashion, have praised greatly but they will not
praise after they are separated from their bodies. In a like manner the dead will not
praise you, Lord, nor those who descend into the underworld.


Richard de Fournival was born in Amiens in 1201, becoming canon, deacon, and
chancellor of Notre Dame of Amiens, where his brother was bishop (Beer 1986).
Whereas the bestiaries of Bishop Theobald and of Guillaume le Clerc were collections
of self-contained exhortations, Richard de Fournival's bestiary was written as a flowing,
integrated composition. All of the earlier bestiaries had a religious purpose, but
Richard's did not. No doubt this alone was seen seen as iconoclastic and as a daring act
for a clergyman to commit. But Richard's subject was love; in his bestiary he used the
technique of the earlier bestiaries but adapted it to try to persuade his lady-love that
she should love him. And he wrote his bestiary not in Latin, but in French, which some
have claimed is the language of love. Some versions of the Bestiaire d'amour contain
a response, which counters Richard's arguments. The author of the response is un-
known, but Beer (1986/ believes that it was written by a woman.
Richard uses behavior of a crisnon cricket) and of eis (bees) in advancing his cause
d'amour. The response argues the irrelevance of Richard's mention of cricket, and
ignores his mention of bees. The following passages in medieval French are from a
version examined by Segre (1957), with a translation [modified by Howard Frank after
a translation by Beer (1986)].
Crisnon [d'amour]. Et une autre raisons de ce meisme si est prise en la nature del
crisnon don't je me sui molt pris garde. Car sa nature si est ke li kaitis aime tant sen

Insect Behavioral Ecology '90 Frank & McCoy

canter k'il se muert en cantant, tant en pert sen mangier et tant s'en laie a pourcachier.
Et por che me sui jou pris garde ke li chanters m'a pau valu ke je m'i puisse tant fier
ke j'en perdisse nis moi, si ke ja li chanters ne m'i socourust; nomeement a chou ke je
esprovai bien ke a l'eure ke je miex cantai et ke je niiex dis en cantant, adont me fu il
pis. Ausi comme del chine.
And another reason for the same is found in the nature of a cricket of which I took
great heed. For such is its nature that the poor beast so loves to sing that it dies in
song, goes without food and neglects to look for it. And for that I paid heed because
singing has been of so little value to me that I can be so sure that I would lose myself
in song, so that song would not save me; especially since I found that at the hour when
I sang best and most lyrically, things were worst for me. Just as with the swan.
Crisnon [response]. Et pour cesti raison, sire et maistres, je ne prenderai mie garde
au crisnon don't je vous ai oi parler. Car encore li plaise ses chans tant que il s'en laisse
apourcachier et muire par tel defaute, ne m'est il mie grans mestiers que je prengne
warde a vos paroles, qui ont sanlanche de moi mestre a vostre volent6; et me sanle que
je ne m'i doi mie del tout assefirer, selone le nature du cisne.
And for this reason, lord and master, I shall pay no attention to the cricket of which
I heard you speak. For though it enjoys its song so much that it lets itself starve and
dies as a consequence, it does not help me to pay attention to your words, which are
designed to subject me to your will; it seems to me that I must not trust them at all,
as is the nature of the swan.
Eis [d'amour]. Et il est escrit es natures ke les eis n'ont mie oie, et neporquant
quant uns vaisseaux d'eis est essam6s, on les maine a sifle et a cant, ne mie pour che
k'eles l'oent, mais il pert bien a lour oevres signories ke leur nature est si noble et si
ordenee, selonc lor maniere, k'il ne puet mie estre ke bons ordenemens et parfais les
trespast, k'eles ne le sentent. Et cil ki ont letit et etendu les hautes philosophies seventh
bien combien musike puet, et a chiax ne puet mie estre chel6 qu'en toutes les coses ki
sont n'a si parfaite ordinance comme en chant, ne si esquise.
And it is written in books on nature that bees have no ears, and regardless, when
a hive of bees has swarmed, they are led by whistle and song, not because they can
hear it, but it follows clearly from their signal works that their nature is so noble and
so ordered, as is their behavior, that good organization and perfection cannot pass by
them without being perceived by them. And those who have read and understood the
high philosophies know well how much music can accomplish, and it cannot be doubted
that nothing among all things that exist has such a perfect order as a song, nor so
exquisite. [there seems to be no response to this].


A manuscript written in England about 1100 AD is preserved in the Bodleian Li-
brary at Oxford University and is known as the Bodley Herbal and Bestiary (Hassall
1978). It offers medicinal uses for plants and animals, including one insect: grillus
(cricket) [with translation by Howard Frank]:
De grille ad qui paralisi temptantur: Grillis adeps remedii afferet his qui paralisi
De claritatem oculorum: Grillis et soricis combustiones cum melle miseant et inde
cotidie mane gustent. Item alter: Adipem de grillo cum melle attico et opobalsamo
aequis ponderibus de eo inunguatur.
Ad somnum, qui non dormiunt: Grillis adipe front tempora inungues.
From the cricket for those afflicted with paralysis: Cricket fat brings a remedy to
those who are paralysed.
For clarity of the eyes: Mix burnt crickets and shrews with honey, and taste every

Florida Entomologist 74(1)

morning. Alternatively, anoint with cricket fat and Athenian honey in equal parts by
A soporific for those who cannot sleep: Anoint the forehead with cricket fat.
The Bodley Herbal and Bestiary is not descended from Physiologus, but is an ab-
breviated version of a treatise ascribed to Sextus Placitus (? 4th century AD) and
entitled De virtutibus bestiarum in arte medicine (Hassall 1978). Such works on
medicinal arts were copied by hand, and mutations were introduced, deliberately or by
error. Some of the variants in works derived from Sextus Placidus use De grille, and
others use De gliris (Howald & Sigerist 1927). It seems more probable that the dor-
mouse (glis) rather than the cricket (grillus) would be found to have the fatty tissue
(adeps) which would be employed for such medicinal arts as curing paralysis (item 1),
clearing the eyes (items 2, 3) and promoting sleep (item 4). Could it be that generations
of English, following instruction to use adipem de grillo as transcribed by a dyslexic
12th century cleric, were unable to achieve the sleep that they had been led to expect?
The Bodley Herbal and Bestiary is a herbal and pseudo-bestiary. Although the
English word herbal exists to describe a work dealing with medicinal properties of
plants, there is no word to describe a work dealing with medicinal properties of animals,
leading to misappropriation of the word bestiary. A similar problem occurs in Chinese
and Japanese where the word that, because of its context, we have to translate as
pharmacopoeia (a work dealing with medicinal materials of plant, animal and mineral
origin), incorporates a character meaning plant, but no character meaning animal (Frank
& Kanamitsu 1987). Pharmacopoeias in these two cultures are of at least as great
antiquity, and were at least as prevalent for at least as wide a range of maladies as in
medieval Europe.


Fables have their place in behavioral ecology (Frank & McCoy 1989). However, the
animals playing roles in fables have at least a modicum of human behavior and they
communicate with humans and with animals of other species in the lingua franca of the
time. In contrast, animal behavior depicted in bestiaries was thought to be factual.


The demise of bestiaries in England was given impetus by Thomas Browne's (1646)
questioning of the facts during the renaissance of science. Not only was Browne outspo-
ken in his criticism of the "commonly received tenents" presented in bestiaries, but he
also was an early user of the words autochthon and indigenous which still are employed
in ecological writing (Frank & McCoy 1990). Thereafter, books on insects such as Mouf-
fet's (1658) Theater of insects were written primarily for secular, not religious, pur-
Only ant, antlion, bee, cicada and cricket are mentioned in the bestiaries consulted
by us, whereas the writers, if not cloistered in scriptoria throughout their lives, must
have encountered at least hundreds of species of insects. This emphasizes that bestiaries
were not zoological works, but employed imagery from animal behavior to moralize on
human behavior. That the behavior attributed to cricket by de Fournival is the same
as the behavior attributed to cicada in the Mondovi Libellus (see above) did not matter;
the names of the insects were only labels for the ascribed behavior, which was itself
only a vehicle to influence human behavior.
If religion was the opiate of the masses in medieval Europe, an opiate in modern
North America is organized sports. If animal behavior was used to guide the religious
in medieval Europe, so animal symbols are used to foment the support of followers of

March, 1991

Insect Behavioral Ecology '90 Frank & McCoy

football teams, political parties, and even nationalism in the modern USA. The propo-
nents are less inventive on the subject of animals, and only the symbolism remains.
Lacking other explanations for the few insects in bestiaries, we suppose attitudes to-
ward insects have changed little since the middle ages: ". . insects, if they get anywhere
near you . whomp them with a hard-cover work of fiction at least the size of Moby
Dick" (Barry 1990).
If the public was no more enlightened about insects in 12th century Europe than in
20th century North America, observational powers of the artists who illustrated the
bestiaries were not acute. Even the 16th century illustration of a cicada in the Mondovi
Libellus (Fig. 1) shows this animal to have 12 legs. Did the writers, too, ignore the real
world to concentrate on their compositions, and did they prefer to use the religious
materials available to them in libraries as opposed to drawing from worldly events
outside the confines of religious fraternities?
We were surprised to find no mention of mantis, whose symbolism is apparent in
the name "praying mantis", nor of gnat, nor of demoiselle. Absence of their mention is
not because medieval scribes were too fastidious to write about behavior equivalent to
that of the feeding habits of female mosquitoes, mating habits of damselflies and man-
tids, or defensive behavior of bombardier beetles. After all, female dragons [origin:
large serpent] were credited with devouring the heads of their mates during copulation,
and bonnacons [orig: bison] with using flatulence for defense (White 1960, Clark 1975).
The reader is referred to Eisner & Aneshansley (1982) and Zinner (1989) for accounts
of defensive behavior of bombardier beetles. Defense is the topic of this symposium.
Contributions include defense of plants against insects and of insects against other


Medieval observers sought explanations for the natural things around them. They
saw within the behavior of insects and other beasts moral guidance for the actions of
man. Never mind that the observations were, in hindsight, often badly flawed or even
contrived; these early observers were operating within the bounds of the "natural his-
tory" of their time. Their world was a simple place compared to ours, and its lessons
were obvious. Surely, we could never be accused by later generations of scientists of
the same short-sightedness as we have accused the authors of bestiaries. We are indeed
vulnerable to such criticism, however, because of the reductionist nature of modern
science. Reductionism implores us to see the natural world in a simple way: complex
natural phenomena are thought to be reducible to a series of straightforward and rela-
tively easily-comprehended processes. One potential trap in the reductionist method,
when employed in disciplines such as ecology and ethology, however, is to assume that
processes uncovered by reduction in one case can be used to explain all other similar
instances. In other words, the trap is in assuming that such processes are general, and
thus akin to physical "laws."
This trap is nowhere more evident than in the field of plant-insect-interactions. It
once seemed that pressures brought by herbivores on plants could cause the plants to
evolve defensive mechanisms against herbivory, and that if a particular kind of herbi-
vore were dependent upon a particular kind of plant, then the plant's defensive
mechanisms could cause the herbivore to evolve some way to overcome them. Direct
reciprocal evolution ("co-evolution") thus could explain the plant-insect relationships we
see all around us. But, for a number of reasons, this ready explanation must be viewed
with caution (see Janzen 1980). Furthermore, co-evolution, even if it could be demon-
strated to be operating in a particular case, may be a far more complex process than
envisaged originally. On this note, we turn to the contributions to this symposium,

Florida Entomologist 74(1)

which show in exquisite detail some of the complexities involved in the relationships
between plants and insects.
At least three important themes are evident in the contributions. The first is that
plant-insect relationships may be manifested in a variety of ways. That is, potential
defensive avenues open to plants are many, and simple, predictable responses of herbi-
vores to plant defenses apparently are few. For example, defensive chemicals need not
be "toxic" in the common sense of the term. Toxicity may derive more subtly, by means
of, say, regulation of insect feeding behavior (Klocke & Kubo) or regulation of growth
and long-term survival (Shea & Romeo). In either case, the chemicals involved seem to
be but a part of the plant's defensive repertoire.
The second theme is that plant-insect relationships often cannot be viewed profitably
outside their natural context. It seems likely, for instance, that the outcomes of many
relationships are altered in the presence of predators, parasitoids, and perhaps even
competitors of herbivorous insects (ecologists refer to relationships that change in this
way as "higher-order relationships"). Chemicals released by plants in response to her-
bivory may be used by parasitoids to locate hosts (Turlings & Tumlinson). Recruitment
of parasitoids by plants may provide them with defensive capabilities beyond those
conveyed by the chemicals alone. Yet, one should not leap too quickly to the assumption
that it is necessarily to the plant's advantage, evolutionarily, to involve parasitoids as
much as possible in the defensive option available to it. Such findings have obvious
implications for IPM programs.
The final theme dealing with the complexity of plant-insect relationships involves
the idea of co-evolution itself. An implicit assumption in one's positing evolution as the
basis for a particular relationship may be that the co-evolutionary interaction is stable.
A simple, phenomenological model demonstrates that co-evolution is not a stabilizing
force a priori, however (Allen). Once more, the particular circumstances of the relation-
ship are important, in that they determine whether co-evolution will work for or against
chaotic dynamics of the populations.
We must conclude that our notions of plant-insect relationships indeed have been
short-sighted. The world in which these relationships reside is not as simple as we might
have supposed, or hoped. Like the medieval observers of nature, we have been operat-
ing within the bounds of what we perceive to be right, and, also like them, when our
perceptions are limited, we must suffer the criticisms of more sophisticated observers.
The difference between then and now seems largely to involve the rapidity with which
such criticisms are levelled.


We are indebted to Helena Puche (Entomology & Nematology Dept., University of
Florida) for translating abstracts for all symposium contributions into Spanish, to Pierre
Jolivet (Gainesville, Florida) for help with medieval French, and to Bruce Woods (Class-
ics Dept., University of Florida) with medieval Latin. John Capinera and Tom Walker
(Entomology & Nematology Dept., University of Florida) kindly offered critical com-
ments on a manuscript draft. This is University of Florida, Institute of Food & Agricul-
tural Sciences, journal series no. R-01292.


BARRY, D. 1990. A campaign likely to bug Congress. Gainesville Sun (7 October
1990): 1D, 10D.
BEER, J. (ed.) 1986. Master Richard's bestiary of love and response. Univ. California
Press; Berkeley, xxxi + 83 p.

March, 1991

Insect Behavioral Ecology '90 Frank & McCoy

BROWNE, T. 1646. Pseudoxia epidemic: Or, enquiries into very many received te-
nents, and commonly presumed truths. Edward Dod; London, [18 +] 386 p.
CLARK, A. 1975. Beasts and bawdy. Taplinger; New York, 159 p.
CLARK, W. B., AND M. T. MCMUNN (eds.) 1989. Beasts and birds of the Middle
Ages. The bestiary and its legacy. Univ. Pennsylvania Press; Philadelphia, xii
+ 224 p.
COOK, A. S. (ed.) 1921. The Old English Physiologus. Yale Univ. Press; New Haven.
Yale Studies in English vol. 63, vi + 25 p.
CURLEY, M. J. (ed.) 1979. Physiologus. Univ. Texas Press; Austin, xliv + 92 p.
DAVIS, J. L. (ed.) 1958. Libellus de Natura Animalium. A fifteenth century bestiary.
Dawson; London, viii + 64 p.
DRUCE, G. C. 1923. An account of the jwup1JqiKokov-Tot or ant-lion. Antiquaries J. 3:
EDEN, P. T. (ed.). Theobaldi "Physiologus" with introduction, critical apparatus, trans-
lation and commentary. Brill; Leiden, viii + 83 p.
EISNER, T., AND D. J. ANESHANSLEY. 1982. Spray aiming in bombardier beetles:
Jet deflection by the Coanda effect. Science 215: 83-85.
FRANK, J. H., AND K. KANAMITSU. 1987. Paederus, sensu lato (Coleoptera:
Staphylinidae): Natural history and medical importance. J. Med. Ent. 24: 55-91.
AND E. D. McCoY. 1989. Behavioral ecology: From fabulous past to chaotic
future. Florida Ent. 72: 1-6.
- AND ---- 1990. Endemics and epidemics of shibboleths and other things
causing chaos. Florida Ent. 73: 1-9.
HASSALL, W. O (ed.) 1978.1 Bodley Herbal and Bestiary. Oxford Microform Publ.;
Bicester, Oxford; Major Treasures in the Brodleian Library no. 8, 6 microfiche.
HOWALD, E., AND H. E. SIGERIST. 1927. Liber medicine Sexti Placiti papyriensis
ex animalibus pecoribus et bestiis vel avibus [p. 235-298, IN:] Corpus medicorum
latinorum. B. G. Tevbner; Leipzig, Vol. 4.
IVES, S. A., AND H. LEHMANN-HAUPT. 1942. An English 13th Century bestiary. A
new discovery in the technique of medieval illumination. H. P. Kraus; New York,
45 p. + 8 pl.
JANZEN, D. H. 1980. When is it coevolution? Evolution 34: 611-12.
MCCULLOCH, F. 1963. The Waldensian bestiary and Libellus de Natura Animalium
Medievalia et Humanistica 15: 15-30.
MOUFFET, T. 1658. The theater of insects: Or, of lesser living creatures. Vol. 3, p.
[i-xii +] 889-1136 [IN:] Topsell, E. (ed.) The history of four-footed beasts and
serpents. E. Cotes; London [reprinted 1967, Da Capo Press; New York].
REINSCH, R. (ed.) 1892. Le bestiaire. Das Thierbuch des normannischen Dichters
Guillaume le Clerc zum ersten male vollstandig nach dem Handschriften von
London, Paris und Berlin [reprinted 1967, Martin Siindig; Wiesbaden, 441 p.]
RENDELL, A. W. (ed.) 1928. Physiologus. A metrical bestiary of twelve chapters by
Bishop Theobald printed in Cologne 1492. John & Edward Bumpus; London,
xxviii + 34 + 100 p. + 15 pl.
SEGRE, C. (ed) 1957. Li bestiaires d'amours di maistre Richart de Fornival e li re-
sponse du bestiaire. Riccardo Ricciardi; Milan, ccxxxvi + 143 p.
WHITE, T. H. (ed.) 1960. The bestiary, a book of beasts, being a translation from a
Latin bestiary of the 12th century. Capricorn Books, G. P. Putnam's Sons; New
York, 296 p.
ZINNER, K 1989. Besouros-bombardeiros. Ciencia Hoje 9(54): 50-56.

Florida Entomologist 74(1)


Department of Biology,
University of South Florida
Tampa, FL 33620


Calliandra leaves and the nonprotein imino acids they contain possess insecticidal
activity. In order to determine the role these compounds play in Calliandra resistance
to herbivory, feeding experiments were performed using larvae of the polyphagous
herbivore Spodopterafrugiperda Smith, and nutritional indices were calculated. Statis-
tically significant growth inhibition occurred with the total amino acid fraction and
trans-5-hydroxypipecolic acid, and there was a trend toward similar inhibition with
several other imino acids. The efficiency with which larvae converted assimilated food
into biomass (ECD) was reduced by the total amino acid fraction as well as by two imino
compounds. The consumption index (CI) and the diet digestibility (AD) were unaffected
by amino acids. Leaf material caused significant growth inhibition, increased mortality,
and a dramatic decrease in the growth and survival of progeny. Leaf material lowered
AD, raised relative consumption rates (RCR) and lowered the efficiency of conversion
of the ingested food (ECI). The data suggest that nonprotein amino acids acting as
toxins via negative effects on insect nutritional physiology are part of Calliandra resist-
ance to herbivory.


Las hojas de Calliandra y los iminoacidos no-proteinicos que ellas contienen, poseen
actividad insecticide. Para determinar el papel que estos compuestos juegan en la resis-
tencia de Calliandra a la herbivoria, se desarrollaron experiments de alimentaci6n
usando larvas del herbivoro polifago Spodopterafrugiperda Smith, y fueron calculados
indices nutricionales. Se encontr6 una inhibici6n del crecimiento estadisticamente sig-
nificativa entire la fracci6n total de aminoacidos y el Acido trans-5-hydroxypipec6lico, asi
como una tendencia similar de inhibici6n en muchos otros imino Acidos. La eficiencia con
la cual las larvas convirtieron alimento asimilado en biomasa (ECD) fue reducida por la
fracci6n total de aminoacidos asi como dos compuestos imino. El indice de consume (CI)
y la digestibilidad de la dieta (AD) no fueron afectadas por los aminoAcidos. Las hojas
causaron una significativa inhibici6n del crecimiento, un incremento en la mortalidad, y
una reducci6n dramatic en el crecimiento y la sobreviviencia de la progene. Las hojas
disminuyeron el AD, incrementaron la tasa relative de consume (RCR) y disminuyeron
la eficiencia de conversion del alimento ingerido (ECI). Los datos sugieren que amino-
Acidos no-proteinicos actuando como toxinas a trav6s de efectos negatives sobre la
fisiologia nutricional de insects, son parte de la resistencia de Calliandra a la herbivoria.

Many nonprotein amino acids play ecological roles in protecting plants from insect
herbivores. The majority of studies, however, report insecticidal activity without ad-
dressing the mechanism, although several modes of action for these compounds are
known. Nonprotein amino acids: 1. can function as antimetabolites of their protein
amino acid analogues. Canavanine does this when it substitutes for arginine on an
insect's arginyl-tRNA synthetase and produces anomalous insect proteins (Dahlman &
Rosenthal 1976). Another nonprotein amino acid, albizzine, depresses asparagine syn-
thetase activity (Lea & Fowden 1975). 2. can function as feeding deterrents affecting
sensory perception as do Acacia amino acids to acridids (Evans & Bell 1979) .3. may

March, 1991

Insect Behavioral Ecology '90 Shea & Romeo

negatively affect nutritional physiology resulting in suboptimal foraging and growth.
L-Dopa reduces the digestibility of the artificial diet of the black cutworm, Agrotis
ipsilon Hufnagel, and also the efficiency of conversion of assimilated food into biomass
(Reese & Beck 1976).
The tropical mimosoid legume Calliandra consists of some 150 + species of woody
shrubs to large trees largely confined to the New World. Although not yet exploited
on a large scale, at least one species is cultivated for firewood. Foliage is rich in protein,
and cattle and goats consume it freely. Bees use its nectar for producing honey (National
Academy Press 1983). The genus has been designated as a potentially exploitable trop-
ical plant group needing further scientific investigation (Uribe et. al. 1984). Calliandra
haematocephala, used in this study, is native to Bolivia and widely cultivated in south
Florida. In the field and in cultivation, Calliandra plants are relatively free from insect
The amino and imino acids (amino acids with a heterocyclic nitrogen ring) of Cal-
liandra are individually moderately toxic to aphids and larvae of lepidopteran pests
belonging to Spodoptera and Heliothis genera (Romeo 1984, Romeo & Simmonds 1989).
It is common for a plant to produce a series of structurally related defensive compounds
that may act additively or synergistically (Berenbaum 1985). Pipecolic acid and its
various hydroxylated derivatives (Fig. 1) found in the leaves, sap, and seeds of Cal-
liandra species act synergistically in causing feeding deterrency and toxicity in aphids
(Simmonds et al. 1988). The presence of a nonprotein sulphur-containing amino acid
further enhances the activity of the pipecolic acids.
Some modes of action previously have been eliminated as explanations of the biolog-
ical activity of pipecolic acids: 1. As higher homologues of proline they are too big to
substitute for this imino acid and produce anomalous insect proteins as the lower
homologue, azetidine-2-carboxylic acid, does (Fowden et al. 1967). 2. Although the
mono- and di-hydroxy pipecolic acid derivatives are similar in structure to known al-
kaloidal glycosidase inhibitors, they lack enough hydroxyls to act as competitive sugar
mimics (Fellows and Nash, personal communication). In contrast trans-trans-trans-
trihydroxypipecolic acid with its single extra hydroxyl is a specific inhibitor of human
beta-D-glucuronidase and alpha-L-iduronidase (Cenci di Bello et al. 1984). 3. They do
not appear to alter taste reception in lepidopterans. In electrophysiological recordings
of taste sensilla of Spodoptera littoralis, responses did not correlate significantly with
feeding behavior (Romeo & Simmonds 1989).
With the above explanations of toxicity excluded, we decided to use Waldbauer's
(1968) nutritional indices as a way of getting at the possible mechanism of action. A
series of feeding studies was performed using the polyphagous herbivore Spodoptera
frugiperda, and five nutritional indices were computed. All compounds and extracts
were assayed using concentrations at or below their naturally occurring levels in Cal-


Source of Chemicals. Trans-5-hydroxypipecolic acid was purchased from Sigma
Chemical Co., St. Louis, MO. The other imino acids were from stock supplies previously
isolated in our laboratory.
Source of Insects. Eggs of Spodoptera frugiperda were obtained from the USDA
Basic Biology and Insect Attractants Laboratory in Gainesville, FL.
Preparation of Diets and Extracts. The control diet was the pinto bean based
artificial diet of Burton (1969). Leaf powder and imino acid containing diets were pre-
pared according to the method of Romeo (1984): crystalline chemicals and finely ground
leaf powder were added to the dry ingredients of the pinto bean diet. Leaf powder was
prepared from locally obtained Calliandra haematocephala Hassk leaves dried in an
oven (24 hr, 1000 C) and ground (40 mesh) in a Wiley mill. The aqueous fractions of C.

Florida Entomologist 74(1)



Fig. 1. Structure of Pipecolic Acid and Derivatives.
Pipecolic Acid R, = R2 = Rs = R4 = H
T-5-OH PIP R4 = OH, R1 = R2 = Ra = H
C-5-OH PIP R3 = OH, R1 = R2 = R4 = H
rTT-4,5-OH PIP R2 = R3 = OH, R1 = R4 = H
TT-4,5-OH PIP R2 = R4 = OH, R1 = R4 = H

haematocephala were prepared by extracting from ground leaves with 50% ethanol.
The extract was filtered, concentrated, redissolved in methanol-chloroform-water
(12:5:1), and extracted again with chloroform and water. The aqueous portion was
evaporated to dryness (in vacuo) and redissolved in a small amount of deionized water.
The amino acid fraction was obtained by applying the aqueous extract to a series of
ion-exchange columns (CG 120 cation exchange resin, elution with ammonia followed by
CG 400 anion exchange resin, elution with acetic acid). For 100% plant equivalency
experiments, an amount of leaf powder equal to the amount of diet to be made (on a
dry weight basis) was extracted and the extract added to the dry ingredients of the
artificial diet.
Bioassay. Treatment groups consisted of 20 neonate (less than 24 hours old) larvae
which were kept in individual 2 oz. cups with lids and maintained in a growth chamber
(25C, 70-90% relative humidity, 12 hr light/ 12 hr dark). In the leaf powder experiment,
larvae were fed with an excess of fresh weighed diet each day. Larvae and unconsumed
diet were weighed daily after day 10. Frass was collected daily. In the imino acid and
leaf extract experiments, neonate larvae were placed on diet cubes that were sufficient
for the entire experimental period. In order to minimize error in computation of nutri-
tional indices, size of diet cubes was adjusted so they would be largely consumed during
the feeding program (Schmidt & Reese 1986). Larvae and unconsumed diet were
weighed and frass collected at the end of these experiments. Frass dry weight was
determined directly after drying in an oven at 100 C for 24 hr. Larval and diet dry
weights were determined by aliquot. Five randomly chosen larvae from each of the last
three instars were frozen, dried and weighed. Instars averaged 16% dry weight (range
= 14-20). Similarly, diet cubes were dried to determine initial and final dry weights.
Humidity in the cups containing larvae was high; diet desiccation ranged from 0-2%.

March, 1991

Insect Behavioral Ecology '90 Shea & Romeo 13

Nutritional Indices. These were calculated according to the method of Waldbauer
(1968). Measurements were made of: Relative Consumption Rate (RCR), the consump-
tion rate corrected for mean body weight (used in the leaf powder experiment); Con-
sumption Index (CI), the consumption rate corrected for final body weight (used in the
imino acids experiment due to the lack of daily weighing); Approximate Digestibility
(AD), the proportion of ingested food actually assimilated; Efficiency of Conversion of
Digested food (ECD), a measure of the animal's ability to convert assimilated food into
biomass; Efficiency of Conversion of Ingested food (ECI), a measure of the ability to
convert ingested food into biomass. ECI varies with AD and ECD and is dependent
upon them.

food eaten (mg)
mean larval wt (mg)/day

food eaten (mg)
CI =
final larval wt (mg)/day

amount ingested (mg) frass produced (mg)
amount ingested (mg)

weight gain (mg)
amount ingested (mg) frass produced (mg)

weight gain (mg)
amount ingested (mg)

Significant differences in larval weights and in nutritional indices were determined
by ANOVA and Tukey's test for unequal sample size. Significant differences in mortal-
ity were determined by Chi Square Analysis.


The effects of incorporation of leaf powder into artificial diet of the fall armyworm
are illustrated in Table 1. Only the group fed 5.0% C. haematocephala leaf powder
showed a significant increase in mortality, but all leaf powder diets caused growth
inhibition in the early instars as reflected in the larval weights on day 10. Higher
concentration leaf powder diets reduced the efficiency with which larvae converted
ingested food into biomass (ECI). A dramatic 39% reduction was seen. This was accom-
panied by an increase in the consumption rate (RCR), so larvae were not deterred from
feeding. Reduction or a trend towards reduction in AD was seen in all animals fed leaf
powder. Only the 2.5% leaf powder diet significantly lowered assimilation conversion
efficiency (ECD).
None of the individual imino compounds tested caused a significant increase in mor-
tality or abnormal larvae, but all imino compounds incorporated into artificial diet
slowed larval growth relative to controls (Table 2). The greatest effect observed on day
8, a 48% growth inhibition, resulted from the 0.5% trans-5-hydroxypipecolic acid incor-
poration. The 0.1% concentration of this same compound still produced a 34% growth

Florida Entomologist 74(1)



Mortality 10 Day Wt
Treatment (%) (mg) RCR ECI AD ECD

Control 11 268 1.27 0.23 0.48 0.54
1.0% C.h 25 162* 1.10 0.22 0.35* 0.65
2.5% C.h 10 181* 1.99* 0.14* 0.40 0.36*
5.0% C.h 35* 214* 1.75* 0.14* 0.34* 0.48*

*p < 0.05

inhibition. The other imino acids show an apparent trend toward reduced growth. Nut-
ritional indices were affected in only 3 instances. ECD's were lower in larvae fed trans-
5-hydroxypipecolic acid and trans-trans-4,5-dihydroxypipecolic acid. ECI was also low-
ered by the latter compound. None of the compounds affected the consumption rate, as
evidenced by the CI values, nor the AD of the food.
When the aqueous and amino acid extracts of C. haematocephala leaves were incor-
porated into artificial diet at 100% plant equivalency, dramatic effects on growth were
seen (Table 3). Larvae fed the total aqueous fraction weighed less than 1.0% of control
larvae on day 8 and seemed not to have grown at all. Nutritional indices could not be
calculated for this group due to the small amount of diet consumed and frass produced.
A 20% reduction in growth occurred with the amino acid fraction. As with individual
amino acids there were no affects on CI or food digestibility (AD). ECD was significantly
depressed, but no more than with individual amino acids.
A limited experiment in which second generation larvae were raised on the same
diet as their parents produced striking results (Table 4). Eighth day treatment larval
weights were less than 10% of control. Mortality was significant. Egg viability of second
generation was also severely affected (8% for 2.5% leaf powder moths vs 54% for con-

(T5 = Trans-5-hydroxypipecolic acid; C5 = cis-5-hydroxypipecolic acid; TC = trans-cis-
4,5-dihydroxypipecolic acid; TT = trans-trans-4,5-dihydroxypipecolic acid)

Mortality 8 Day wt
Treatment (%) (mg) CI ECI AD ECD

Control 0 256 0.46 0.27 0.43 0.66
0.5% T5 5 134* 0.47 0.25 0.49 0.53*
0.1% T5 0 169* 0.48 0.30 0.43 0.71
0.1% TC 0 230 0.45 0.28 0.38 0.68
0.1% C5 10 195 0.47 0.26 0.45 0.59
0.1% TT 5 222 0.48 0.23* 0.49 0.52*

* p < 0.05

March, 1991

Insect Behavioral Ecology '90 Shea & Romeo


Mortality 8 Day wt
Treatment (%) (mg) CI ECI AD ECD

Control 15 246 0.52 0.27 0.45 0.66
Amino acids 15 194* 0.52 0.27 0.49 0.57*
Aqueous fract. 15 2*

*p < 0.05


Most of the mortality and growth inhibition among larvae fed C. haematocephala
leaf powder occurred during the first week after larval eclosion (i.e., in the first three
intars). Greater sensitivity of young larvae to plant defenses is not unusual (Shaver &
Parrot 1970). Feeding on a toxin free artificial diet for the first 48 hours after hatching
can dramatically improve growth (Reese 1983). Less growth inhibition was observed in
this study than in an earlier one (Romeo 1984). We attribute the discrepancy to the
added stress of daily weighing in the earlier study, a major difference in experimental
Nutritional indices are useful in suggesting possible mechanisms of antibiosis
(Scriber & Slansky 1981, Reese 1983, Manuwoto & Scriber 1986). The decreased diet
conversion efficient (ECI) seen in larvae fed the higher concentrations of leaf powder
is reflective of both lower diet digestibility (AD) and lower conversion efficiency of
digested food (ECD). Low ECD values usually result from the presence of a toxin or
from a nutrient imbalance (House 1974, Scriber & Slansky 1981). Fiber content will
lower AD, but the magnitude of the reduction in the treatment groups appears too great
to be explained by fiber alone. Digestibility reducing compounds such as tannins and
protease inhibitors may also contribute to this low AD. The increased RCR's caused by
the higher concentrations of leaf powder diets are probably a response to lower diet
digestibility. Herbivorous insects often increase consumption to compensate for low
digestibility (Scriber & Slansky 1981; Brown 1975). Diet digestibility and ECD are not
necessarily independent of one another. Factors that caused lower ECD values may
have caused an even greater depression of ECD if they had been incorporated into a
more digestible diet. The often observed inverse relationship between AD and ECD
can be the result of homeostatic mechanisms (Reese & Beck 1976).
Imino compounds did not deter larvae from feeding, as evidenced by the CI values
obtained. This is consistent with previous antifeedant assays conducted on other
lepidopteran species (Romeo & Simmonds 1989). As expected, imino compounds had no


8 Day Wts
Treatment Mortality (mg)

Control 0 333
2.5 % leaf 20* 13*
5.0 % leaf 25* 17*

Florida Entomologist 74(1)

effect on diet digestibility, but the reduction of conversion efficiency of assimilated food
(ECD) shown by two of them (trans-5-hydroxypipecolic acid and trans-trans-4,5-dihyd-
roxypipecolic acid) is in accord with other studies on the nutritional effects of nonprotein
amino acids (Reese & Beck 1976; Dahlman 1977). These compounds behave like
physiological toxins and are apparently taken up from the gut into the hemolymph
where they adversely affect metabolism. The lowered ECD could be due to the energetic
cost of detoxification or to interference with normal amino acid metabolism. Scriber &
Slansky (1981) point out the effects of amino acid imbalances on increased catabolism,
slowed growth and reduced conversion efficiency. Since our individual imino compounds
were fed at such low levels, there appears to be more than a mere amino acid imbalance
The effects of individual imino compounds on growth, survival and diet usage were
assayed at or below the levels at which they are found in plants (Romeo 1984). The
effects of individual amino acids on growth and nutritional indices were limited to a few
cases. If the synergistic effects on both toxicity and deterrence, previously observed in
aphids (Simmonds et al. 1988) also occur in Spodoptera, we would expect a greater
growth depression and also a depression of the consumption index from the total amino
acid fraction. These were not observed (Table 3). This appears then to be another
example of varying effects of the same compounds on different test organisms, and
re-emphasizes the importance of using caution in forming generalizations. An additional
point for consideration is that combinations of toxic/deterrent amino acids may be less
so when combined with the normal protein amino acids present. This is usually over-
looked in designing bioassays.
The second generation effects suggest a fruitful area for further study. The obser-
vance of such pronounced negative effects on fecundity and growth of progeny, in
organisms which survive the initial round of selection, indicates that the toxicity of
allelochemicals is even more complex than usually envisioned. How many times have
potentially important bioactive compounds been overlooked because they produced no
results in initial screenings?
In answer to the question raised by the title of the paper, this study suggests that
nonprotein imino acids are partially responsible for some of the observed antibiotic
effects of Calliandra leaves. Specifically, the reduction in assimilation conversation effi-
ciency (ECD) appears to have a nonprotein imino acid component. The energetic costs
of processing Calliandra leaves are probably increased by the presence of these com-
pounds. It is difficult, of course, to compare bioassay results of leaf powder experiments
with those of individual compounds, since the biological activity of an allelochemical
depends upon the environment in which it is encountered (Scriber & Slansky 1981). In
this regard it is noteworthy that the aqueous fraction (which includes the amino acids)
essentially stopped all larval growth. This provides evidence for the existence of other
potent water soluble allelochemicals in Calliandra.


This material is based upon work supported by the National Science Foundation
under grant no. BSR 8400277.


BERENBAUM M. 1985. Brementown revisited: interactions among allelochemicals in
plants. Rec. Adv. Phytochem. 19: 171-194.
BROWN, L. B. 1975. Regulatorymnechanisms in insect feeding. Adv. Insect Physiol.
11: 1-116.

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Insect Behavioral Ecology '90 Shea & Romeo

BURTON, R. L. 1969. Mass rearing the corn earworm in the laboratory. USDA ARS,
Specific inhibition of human beta-D-glucuronidase and alpha-L-iduronidase by a
trihydroxy pipecolic acid of plant origin. FEBS. 176: 61-64.
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on the tobacco hornworm, Manduca sexta. J. Insect. Physiol. 22: 265-271.
EVANS, C. S., AND E. A. BELL. 1979. Non-protein amino acids of Acacia species
and their effect on the feeding of the acridids Anacridium melanorhodon and
Locusta migratoria. Phytochemistry 18: 1807-1810.
FOWDEN, L., D. LEWIS, AND H. TRISTRAM. 1967. Toxic amino acids: their action
as antimetabolites. Adv. Enzymol. 29: 89-163.
HOUSE, H. L. 1974. Nutrition, pp. 1-62 in M. Rockstein (ed.). The physiology of
Insecta V. Academic Press, NY.
LEA, P. J., AND L. FOWDEN. 1975. The purification and properties of glutamine-de-
pendent asparagine synthetases isolated from Lupinus albus. Proc. R. Soc. Lon-
don 192: 12-26.
MANUWOTO, S., AND J. M. SCRIBER. 1986. Effects of hydrolyzable tannin on growth
and development of two species of polyphagous lepidoptera: Spodoptera eridania
and Callosamia promethea. Oecologia 69: 225-230.
NATIONAL ACADEMY PRESS. 1983. Calliandra: A Versatile Small Tree for the
Humid Tropics. Washington, DC, pp. 3-7.
REESE, J. C. 1983. Nutrient-allelochemical interactions in host plant resistance.
American Chem. Soc. Symp. Series 208: 231-242.
-- AND S. D. BECK. 1976. Effects of allelochemicals on the black cutworm,
Agrotis ipsilon; effects of p-benzoquinone, hydroquinone, and duroquinone on
larval growth, development and utilization of food. Ann. Ent. Soc. America 69:
ROMEO, J. T. 1984. Insecticidal imino acids in leaves of Calliandra. Biochem. Syst.
Ecol. 12: 293-297.
-- AND M.S.J. SIMMONDS. 1988. The effect of non-protein amino acids from
Calliandra plants on the aphid, Aphisfabae. Biochem. Syst. Ecol. 16: 623-626.
SCHMIDT, O. J., AND J. C. REESE. 1986. Sources of error in nutritional index studies
of insects on artificial diet. J. Insect Physiol. 32: 193-198.
SCRIBER, J. M., AND F. SLANSKY. 1981. The nutritional ecology of immature in-
sects. Annu. Rev. Ent. 26: 183-211.
SHAVER, T. N., AND W. L. PARROT. 1970. Relationship of larval age to toxicity of
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SIMMONDS, S. J., J. T. ROMEO, AND W. M. BLANEY. 1988. Nonprotein amino acid
feeding deterrents from Calliandra, pp. 59-68 in J. T. Arnason, B.J.R.
Philogene, and P. Morand [eds.]. Insecticides of plant origin. ACS Symposium
Series No. 387.
URIBE, B., A., OSPINA, AND E. FORERO. 1984. Program Interciencia de Recursos
Biologicos; Guadalupe; Bogota, Colombia pp 104-107.
WALDBAUER, G. P. 1968. The consumption and utilization of food by insects Adv.
Insect Physiol. 5: 229-288.

Florida Entomologist 74(1)


Division of Entomology and Parasitology
College of Natural Resources
University of California
Berkeley, CA 94720


Feeding deterrents, or antifeedants, are chemicals that can protect plants from
insect herbivory through regulation of insect feeding. The sensitivity of a given species
of an insect herbivore is dependent upon the quantity and chemical structure of the
feeding deterrent.
Feeding deterrency can be caused by an effect of the chemical on chemoreception
and/or on the centers that regulate feeding and metabolism. Feeding deterrents primar-
ily affect the feeding behavior of insects, but often they are also toxic if fed upon.
Examples of feeding deterrents that play an important role in the multichemical
defense of plants from insects are azadirachtin isolated from Azadirachta indica
(Meliaceae) and rhodojaponin III isolated from Rhododendron molle (Ericaceae). These
two terpenoidal plant products, so effective in nature, are currently being tested for
use in commercial insect control.


Hay quimicos que disuaden o que impiden que coman, y que pueden protejer a las
plants de insects herbivores a trav6s de la regulaci6n del acto de comer. La sen-
sibilidad de una especie en particular de insecto herbivoro, depend de la cantidad y de
la estructura quimica de lo que lo disuade que coma.
El que no coman puede ser causado por el efecto del quimico en el receptor quimico,
y o por el centro que regular el acto de comer y del matabolismo. Los disuadores de que
coman, principalmente afectan el compartamiento de c6no comen los insects, poro a
menudo tambien son t6xicos si se comen.
Ejemplos que disuaden el comer y que juegan un important papel en la defense
multi-quimica de plants hacia insects, son azadiractin aislados de Azadiracta indica
(Meliaceae) y aislados de rodojaponin III de Rhododendrom molle (Ericaceae). Estos
dos products terpenoidales de plants, tan efectivos en la naturaleza, se estin actual-
mente probando para su uso en el control commercial de insects.

Feeding deterrents, also known as antifeedants, are substances that result, either
temporarily or permanently depending on potency and structure, in the cessation of
feeding (Kubo & Nakanishi 1977). The importance of these compounds in plant-insect
relationships has been well-documented and it is probable that in nature, all non-host
plants contain feeding deterrents (Schoonhoven 1982).
Although insect feeding deterrents can be found in many classes of plant compounds,
some of the most potent and widespread are terpenes (Harborne 1989). In this paper,
we will discuss two plant terpenes, the tetranortriterpene azadirachtin isolated from


March, 1991

Insect Behavioral Ecology '90 Klocke & Kubo





Fig. 1. The chemical structures of two naturally occurring insect feeding deterrents.

Azadirachta indica A. Juss. (Meliaceae) and the diterpene rhodojaponin III isolated
from Rhododendron molle (Bl.) G. Don (Ericaceae) (Fig. 1), which protect the plants
in which they are found through regulation of insect feeding behavior.
Both A. indica and R. molle have long been used as insecticides in the areas where
they grow (Perry 1980, Grainge & Ahmed 1988). For example, the effects of the leaves
of A. indica on insect feeding behavior were reported over fifty years ago in India,
where the tree is indigenous (Volkonsky 1937) and the flowers of R. molle indigenous
to China, have been sold for many years as a commercial insecticidal preparation in
Chinese drug stores (McIndoo 1945).
In more recent times, due to the rapid developments in the isolation, identification,
and bioassay of plant products, a number of biologically active compounds from A.
indica (Jones et al. 1989) and from R. molle (Klocke et al 1990a) have been reported.
These compounds, representing various structural types eliciting various biological ac-
tivities against insects, are components of the multichemical plant defense against her-
bivory so often observed in nature (Kubo et al. 1983). Although feeding deterrency
forms only a part of the multichemical defense of these plants, its importance in nature
and its implications for commercial insect control warrant its study.

Florida Entomologist 74(1)


The potency of the antifeedant effect of azadirachtin and rhodojaponin III against
several species of insects was determined using host plant leaf disk bioassays. The
compounds, following their isolation and purification from plants (Yamasaki et al. 1986,
Klocke et al. 1990a), were dissolved in acetone and applied (25 /l) to the surface of
disks (50 mm2) punched from suitable host plants (i.e., potato for the Colorado potato
beetle, Leptinotarsa decemlineata (Say) and cotton for the fall armyworm, Spodoptera
frugiperda (J. E. Smith) and the tobacco budworm, Heliothis virescens (Fabr.) (Klocke
et al. 1990b). Following solvent evaporation, the leaf disks were arranged with their
upper (treated) surfaces exposed in a circle between two moistened absorbant pads. In
this way, the untreated lower surface remained in contact with moisture to prevent
drying out, while only the treated surface was exposed to the insects. In the "no choice"
leaf disk bioassays, the insects (third instar larvae) were presented only with treated
disks. In the "choice" leaf disk bioassays, the insects were presented with both treated
and untreated disks simultaneously. The PC95 value, the minimal protective concentra-
tion of compound (gg/disk) at which >95% of the control, while <5% of the treated,
leaf disks were eaten was determined for each compound from 8-10 replicates/concentra-
tion (Klocke & Kubo 1982, Yamasaki & Klocke 1989).
The plant compounds were bioassayed further using suitable whole plants (i.e.,
potato for L. decemlineata, cotton for S. frugiperda, and tomato for the tobacco
hornworm, Manduca sexta (L.)). The compounds were either solubilized in 0.05%
tween-80 and sprayed (20 ml) onto the foliage or solubilized in 0.5% Triton-X-100 and
poured (100 ml) onto the soil of potted plants (Hu et al., submitted; Klocke et al. 1990b).
After 24 hours, 15-20 third and fourth instar larvae were transferred to each of the
treated plants. After the control plants were almost completely consumed, plant damage
and larval survivorship were assessed. Three replicates were used for each treatment.
The plant compounds were tested also in an artificial diet bioassay (Chan et al. 1978,
Kubo & Klocke 1983). Neonate larvae of H. virescens and S. frugiperda were transfer-
red to treated diet in a controlled environment (relative humidity, temperature, and
photoperiod) and observations were made on their nutrition, growth, development, and
survivorship. After 10 days, LC50 and ECSo values, the lethal concentration for 50%
mortality and the effective concentration for 50% growth inhibition, respectively, were
determined from log probit analysis (Litchfield & Wilcoxon 1949).


In the "choice" leaf disk bioassays with azadirachtin, S. frugiperda was the most
sensitive (PC9g= 0.1 /ig/disk) and L. decemlineata the least sensitive (PC95= 75 pg/
disk) of the species tested. H. virescens was of an intermediate sensitivity (PC95 = 6
pg/disk). In similar bioassays with rhodojaponin III, L. decemlineata was the most
sensitive (PC95 = 3 pg/disk) and H. virescens the least sensitive (PC 95= >50 ig/disk).
S. frugiperda was of an intermediate sensitivity (PC95 = 6 Ag/disk). As illustrated here,
it is difficult to predict the sensitivity of a given species of insect to a given feeding
deterrent and therefore sensitivity must be determined empirically.
The acute sensitivity of S. frugiperda to azadirachtin observed in the leaf disk bioas-
says was observed also in whole corn plants sprayed with 600 ppm of azadirachtin, a
concentration which, applied as a prophylactic, resulted in complete plant protection
from S. frugiperda (Klocke & Barnby 1989). This level of activity was the same as that
of lannate, a synthetic insecticide. On the other hand, potato plants treated with the
same amount of azadirachtin were not protected from feeding by L. decemlineata.
The foliage of potted tomato plants was completely protected from feeding by M.

March, 1991

Insect Behavioral Ecology '90 Klocke & Kubo

sexta by drenching the soil with 10 mg of azadirachtin. Thus, azadirachtin afforded plant
protection through systemic translocation from the roots to the foliage of the tomato
plants. A similar systemic translocation was observed when the soil of potted potato
plants was drenched with 10 mg of azadirachtin; no L. decemlineata larvae, which
readily fed on the treated plants, were able to pupate (Klocke & Barnby, submitted).
A systemic mode of action in plants is an important attribute of feeding deterrents
because insects often prefer to feed on new plant tissue which would be unprotected if
not sprayed continuously. Through systemic translocation, even new tissue is protected
without additional sprayings (Schoonhoven 1982).
The feeding deterrent effect of azadirachtin was demonstrated using artificial diet
bioassays with H. virescens and S. frugiperda. When fed on treated diet, larvae of H.
virescens consumed less food, gained less weight, and were less efficient at converting
ingested and digested food into biomass (Barnby & Klocke 1987). Consumption and
weight gain were reduced at concentrations of azadirachtin (0.1-0.3 ppm) lower than
those affecting the utilization efficiencies (0.5 ppm). This reduced consumption may
reflect, at least in part, sensory detection and avoidance, as has been demonstrated for
this insect (Simmonds & Blaney 1984).
Besides the effects of azadirachtin on deterrent receptors, several reports have
attributed a part of its antifeedant effect to a disruptive influence on the centers that
regulate feeding and metabolism (Redfern et al. 1982, Sieber & Rembold 1983, Schluter
& Schulz 1984). We found that a single dose of azadirachtin injected either orally (1 Ig)
or directly into the hemocoel (0.3 jg) of mature H. virescens larvae resulted in a lower
rate of consumption of diet (from 269 mg to 196 mg of diet) (Klocke et al. 1987).
Azadirachtin fed in artificial diet to larvae of H. virescens or S. frugiperda caused
growth inhibition (ECo5= 0.07 and 0.4 ppm, respectively) and mortality (LC5o= 0.8
and 1.0 ppm, respectively) (Kubo & Klocke 1986). The mortality was due to a disruption
in the molting process caused by a reduction in the titers of brain hormone
(prothoracicotropic hormone) in the treated insects (Barnby & Klocke 1989). A similar
effect on insect development was observed when larvae of L. decemlineata fed on potato
plants treated systemically with 10 mg of azadirachtin. The larvae, while not deterred
from feeding on the treated foliage, were unable to pupate and eventually died (Klocke
and Barnby, submitted).
A toxic effect of feeding deterrents is important since starving insects often will
attempt to feed on any potential food available to them, even that treated with feeding
deterrents. That is, insects can become desensitized to the antifeedant effect (Blaney
et al. 1986). In addition, not all species of insects are deterred from feeding on any given
antifeedant. Therefore, an effective antifeedant should have feeding deterrency as its
primary effect and toxicity as its secondary effect (Klocke & Barnby 1989).
Larvae of L. decemlineata were more sensitive to rhodojaponin III than to
azadirachtin, both in the leaf disk and in the whole plant bioassays. Potted potato plants
sprayed with 75 ppm of rhodojaponin III were completely protected from feeding by
this insect. As in the leaf disk bioassays, larvae of S. frugiperda were less sensitive to
rhodojaponin III since a concentration of at least 5000 ppm was required to deter them
completely from feeding on cotton foliage.
Rhodojaponin III was more potent to both L. decemlineata and S. frugiperda in "no
choice" than in "choice" leaf disk bioassays (PC95 = 1 and 2 /g/disk in the "no choice"
assays, respectively, and PC95 = 3 and 6 pg/disk in the "choice" assays, respectively)
(Klocke et al. 1990a). A similar result was reported when other plant products were
tested against L. decemlineata, prompting the authors to hypothesize that at least a
part of the antifeedant effect was due to toxicity rather than completely to chemorecep-
tion (Alford et al. 1987). In support of this hypothesis, we found rhodojaponin III to be
a growth inhibitor (ECo = 3 ppm) and an insecticide (LCo = 9 ppm) when incorporated
into artificial diet and fed to neonate S. frugiperda.

Florida Entomologist 74(1)

The effectiveness of feeding deterrents in host plant resistance in nature has led to
their study as potential commercial insect control agents (Schoonhoven 1982). For exam-
ple, azadirachtin is being evaluated in laboratories in both university and industry for
its potential in commercial insect control (Klocke 1989). The need for new insecticides
with a mode of action specific for target pest insects is widely recognized. Perhaps plant
compounds, such as the antifeedants, can provide models for our future needs in com-
mercial insect control.


Financial support for some of the results presented in this paper were provided by
grants PCM-8314500 and INT-8700865 from the U.S. National Science Foundation to
J.A.K. We thank Dr. A. C. Dorsaz for critical comments.


feedant activity of limonin against the Colorado potato beetle (Coleoptera:
Chrysomelidae). J. Econ. Entomol. 80: 575-578.
BARNBY, M. A., AND J. A. KLOCKE. 1987. Effects of azadirachtin on the nutrition
and development of the tobacco budworm, Heliothis virescens (Fabr.) (Noc-
tuidae). J. Insect Physiol. 33: 69-75.
AND 1989. Effects of azadirachtin on levels of ecdysteroids and
prothoracicotropic hormone-like activity in Heliothis virescens (Fabr.) larvae. J.
Insect Physiol. 36: 125-131.
BLANEY, W. M., L. M. SCHOONHOVEN, AND M.S.J. SIMMONDS. 1986. Sensitivity
variations in insect chemoreceptors; a review. Experientia 42: 13-19.
rapid diet preparation method for antibiotic phytochemical bioassay. J. Econ.
Entomol. 71: 366-368.
GRAINGE, M., AND S. AHMED. 1988 Handbook of plants with pest-control proper-
ties, p. 234. John Wiley & Sons, New York.
HARBORNE, J. B. 1989. Recent advances in chemical ecology. Nat. Prod. Rep. 6:
JONES, P. S., S. V. LEY, E. D. MORGAN, AND D. SANTAFIANOS. 1989. The chemis-
try of the neem tree, in M. Jacobson (ed.), 1988 Focus on phytochemical pes-
ticides. CRC Press, Boca Raton, Florida.
KLOCKE, J. A. 1989. Plant compounds as sources and models of insect control agents,
in H. Wagner, H. Hikino, and N. R. Farnsworth (eds.), Economic and medicinal
plant research, Vol. 3, pp. 103-144. Academic Press, London.
-- AND I. KUBO. 1982. Citrus limonoid by-products as insect control agents.
Entomol. Exp. Appl. 32: 299-301.
---, AND M. A. BARNBY. 1989. Plant allelochemicals as sources and models of
insect control agents, in C. H. Chou and G. R. Waller (eds.), Phytochemical
ecology: allelochemicals, mycotoxins and insect pheromones and allomones. Insti-
tute of Botany, Academia Sinica Monograph Series No. 9, Taipei, Taiwan.
Allelochemicals in insect control: azadirachtin as an antifeedant and ecdysis in-
hibitor. Proceedings 31st International Congress of Pure and Applied Chemistry,
Section 4, pp. 150-169, Sofia, Bulgaria.
--, M. -Y. Hu, S. -F. CHIU, AND I. KUBO. 1990a. Grayanoid diterpene antifeed-
ants and insecticides from Rhododendron molle. Phytochemistry (in press).
-- M. A. BARNBY, AND A. BUTZ. 1990b. Insect growth and development in-
hibitors screening techniques of phytochemicals, in M. Jacobson and I. Kubo
(eds.), Focus on phytochemical pesticides, Vol. 2 (in press). CRC Press, Boca
Raton, Florida.

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KUBO, I., AND K. NAKANISHI. 1977. Insect antifeedants and repellents from African
plants, in P. A. Hedin (ed.), Host plant resistance to pests. Symposium Series
62, pp.165-178, American Chemical Society, Washington, D.C.
- AND J. A. KLOCKE. 1983. Isolation of phytoecdysones as insect ecdysis in-
hibitors and feeding deterrents, in P. A. Hedin (ed.), Mechanisms of plant resist-
ance to insects. Symposium Series 208, pp. 329-346, American Chemical Society,
Washington, D.C.
--, AND J. A. KLOCKE. 1986. Insect ecdysis inhibitors, in M. B. Green and P.
A. Hedin (eds.), Natural resistance of plants to pests, roles of allelochemicals.
Symposium Series 296, pp. 206-219, American Chemical Society, Washington,
--, T. MATSUMOTO, AND J. A. KLOCKE. 1983. Multichemical resistance of the
conifer Podocarpus gracilior (Podocarpaceae) to insect attack. J. Chem. Ecol.
10: 547-559.
LITCHFIELD, J. T. JR. AND F. WILCOXON. 1949. A simplified method of evaluating
dose-effect experiments. J. Pharmacol. Exp. Therapeu. 96: 99-11.
MCINDOO, N. E. 1945. Plants of possible insecticidal value: a review of the literature
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Plant Quarantine, Washington, D.C.
PERRY, L. M. 1980. Medicinal plants of East and Southeast Asia, p. 133. The Mas-
sachusetts Institute of Technology, Cambridge, Massachusetts.
REDFERN, R. E., T. J. KELLY, A. B. BORKOVEC, AND D. K. HAYES. 1982. Ecdys-
teroid titers and molting aberrations in last-stage Oncopeltus nymphs treated
with insect growth regulators. Pestic. Biochem. Physiol. 18: 351-356.
SCHLUTER, U., AND W. D. SCHULZ. 1984. Structural damages caused by neem in
Epilachna varivestis: a summary of histological and ultrastructural data I. Tis-
sues affected in larvae, in H. Schmutterer and K.R.S. Ascher (eds.), Natural
pesticides from the neem tree (Azadirachta indica A. Juss.) and other tropical
plants. Proceedings 2nd International Neem Conference, German Agency for
Technical Cooperation, Eschborn, Germany.
SCHOONHOVEN, L. M. 1982. Biological aspects of antifeedants. Entomol. Exp. Appl.
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SIEBER, K. -P., AND H. REMBOLD. 1983. The effects of azadirachtin on the endocrine
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lepidopterous larvae, in H. Schmutterer and K.R.S. Ascher (eds.), Natural pes-
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azedarach. Archs. Inst. Pasteur Alger 15: 427-432.
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salannin as an antifeedant against the Colorado potato beetle, Leptinotarsa de-
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356: 220-226.

Florida Entomologist 74(1)


Central Experiment Station
Centeno, Via Arima P. 0.
Trinidad, W. I.

Department of Entomology and Nematology
University of Florida
Gainesville, FL 32611-0740


Mathematical models and computer simulations are useful for examining alternative
control strategies to include in Integrated Pest Management (IPM) programs. A three-
tropic-level model comprising the celery plant, Apium graveolens L., the leafminer
Liriomyza trifolii [Diptera: Agromyzidae) and the parasitoid Digllyphus intermedius
(Hymenoptera: Eulophidae) was developed. Both antixenotic and antibiotic celery plant
resistance were included along with the parasitoid, to examine their effects on leafminer
larval populations. Better control of the leafminer was observed when these types of
resistance were included in combination with the parasitoid, when compared to the
parasitoid acting alone. However, the parasitoid acting alone seemed to be better than
either of the two forms of resistance in the absence of the parasitoid. The use of models
to study the interaction of plant resistance and biological control in IPM programs is


Los models matemiticos y las simulaciones en computadora son herramientas tiles
para examiner estrategias de control alternatives para ser incluidas en programs de
Manejo Integrado de Plagas (IMP). Un modelo de tres niveles tr6ficos formado por la
plant de apio, Apium graveolens L., minador de la hoja, Liriomyza trifolii (Diptera:
Agromizidae) y el parasitoide Digylphus intermedius (Hymenoptera: Eulophidae) fue
desarrollado. Ambas resistencias, antixen6tica y antibi6tica de la plant de apio fueron
incluidas junto con el parasitoide, para examiner sus efectos sobre la poblaci6n larval
del minador de la hoja. Un mejor control del minador de la hoja fue observado cuando
estos tipos de resistencia fueron incluidos en combinaci6n con el parasitoide, en compara-
ci6n con el parasitoide actuando solo. Sin embargo, pareciera que el parasitoide actuando
aisladamente ejerciera un mejor efecto que si alguna o ambas formas de resistencia
actuaran en ausencia del parasitoide. El uso de models para estudiar la interacci6n de
la resistencia de plants y el control biol6gico en programs de IPM es enfatizado.

Control strategies for management of the leafminer Liriomyrza trifolii (Burgess)
have concentrated on the use of insecticides (Wolfenbarger 1978; Alverson & Gorsuch
1982; Parrella et al. 1982; Grafius & Hayden 1988). Chemicals from various pesticide
groups e.g. chlorinated hydrocarbons, organophosphates and pyrethroids have been
tried (Parrella et al. 1981). Because of insecticide resistance problems (Schuster &
Everett 1983, Parrella et al. 1984, Keil & Parrella 1990), control strategies have been
shifting towards use of plant extracts e.g., neem, Azadirachta indica (Fagoonee &

March, 1991

Insect Behavioral Ecology '90 Brewster & Allen

Toory 1984), insect growth regulators e.g., avermechtin, cyromazine (Parrella et al.
1983a, Grafius & Hayden 1988), and biological control using natural enemies (Parrella
et al. 1983, Heinz & Parrella 1989). In general, the shift in emphasis has been towards
adopting an integrated approach to managing leafminer pests (Trumble & Ouiros 1988).
Plant resistance and biological control have been cited as primary factors to be
considered in pest control (Wilson & Huffaker 1976). Host-plant resistance is being
exploited for inclusion in Integrated Pest Management programs for leafminer control
(Kennedy et al. 1987, Trumble & Ouiros 1988). Integrated strategies should have no
adverse effects on the biological agents, but should allow for expression of the biological
agent's full potential to ensure that maximum benefits are attained (Stimac 1990).
Three categories of resistance were outlined by Painter (1951, 1958). The first is
antixenosis or nonpreference response of insects to plants. Plants either possess or lack
certain characteristics that exert adverse effects on pest behavior. Next is antibiosis
where the plant causes certain adverse effects on insect development, survival and
oviposition. Finally tolerance, where the plant is able to support certain levels of attack
or withstand infestation without loss of vigor or yields, as would occur with otherwise
susceptible plants.
In this study, the method suggested by Stimac (1990) is modified and adopted in
which a three-trophic-level model is used to examine the effects of a biological control
agent, a parasitoid, Diglyphus intermedius (Girault), on the leafminer population when
the celery crop system has been altered by inclusion of antixenotic and/or antibiotic
types of plant resistance to pest attack.


The dynamical behavior of L. trifolii on celery was examined to test the effects of
plant resistance mechanisms in combination with parasitoid attack on the leafminer
population. A model which included three trophic levels the celery plant, the leafminer
and the parasitoid was developed, and computer simulation was used to evaluate
different combinations of inputs for leafminer management.
Each trophic level model was formulated separately as ordinary differential equa-
tions (ODE's), and the trophic levels were linked to each other by "Type 2" functional
responses. The ODE's were solved by rectangular integration using small timesteps
(0.01 d), and the parameters were calculated from data in the literature as temperature
functions. The computer program was developed with FORTRAN77 and compiled using
Microsoft FORTRAN 4.1 on an IBM-compatible microcomputer. Initial conditions for
simulation were specified by adult leafminer and parasitoid densities surrounding the
test area, migration coefficients for each insect, initial celery leaf-area and the time of
Antixenotic resistance was included by adjusting the standard oviposition rate of
adult female leafminers. A celery plant that possessed a high degree of antixenotic
resistance was simulated by decreasing the standard oviposition rate for the leafminer
two-fold, whereas a susceptible plant or one with little antixenotic resistance was simu-
lated by a two-fold increase in the standard oviposition rate of female leafminers. Anti-
biotic resistance was simulated by increasing the survival of leafminer larvae two-fold.
To simulate an antibiotically susceptible plant, standard larval mortality was decreased
A series of computer experiments was conducted after running the standard model
for comparison. This model was assumed to contain a certain standard level of both
antixenotic and antibiotic resistance. In the other experiments, in addition to the pres-
ence of the parasitoid, both antixenotic and antibiotic resistance were included either
separately or together at levels above and below the standard levels. In addition, to

Florida Entomologist 74(1)

test the effects of interaction of these resistance mechanisms with parasitoid attack, the
latter was excluded in some of the experiments.
The importance of monitoring pest populations throughout the second phase of celery
growth has been emphasized (Musgrave et al. 1977, Guzman et al. 1980, Foster &
Sanchez 1988). This was based on the fact that leaves produced during the first phase
of growth were seldom marketable. In determining the effects of the above control
strategies therefore, leafminer larval density was recorded first at 60 days afte trans-
planting (representing the start of the second phase in the model)], then at the peak
population, and finally at harvest (100 days after transplanting). All densities were
reported on the basis of number per 100 cm2 of celery leaf.


Celery Submodel

The celery plant is the first trophic level in the system. In this submodel leaf-area
is used as the index of plant growth. This index was found to be as good a measure of
celery growth as fresh weight, dry weight, petiole number and petiole height, and was
also found to be highly correlated with these indices (Strandberg 1985). More important,
however, is the fact that leafminer adult female oviposition and also larval feeding both
depend on leaf-area. In addition, Musgrave et al. (1976, 1977) found that leafminer
attacks in celery were cumulatively greater on outer older leaves, and that the tender
leaflets of the youngest central foliage were seldom mined. Therefore, an age-class
distribution of leaf-area was used. susceptible age celery leaf-area was then assigned to
an 'oviposition window'. The mathematical representation for this submodel is therefore
given as,

(immature ares) x, = f(t) ax1z
(oviposition window) x = a1,x aax2 ea-6 ( )X
2 x,+w2
(old area) xs = a2x ayx
(attack area) w = ea Y ( X ) a2w, . .(i)
2 x,+w2

where x, = dx1/dt (the rate of change of xi). f(t), is the rate of leaf-area input into the
model and ai's are the reciprocal of the residence time of the area in xi's (i.e., develop-
mental rates). These parameters (ai's) are time-independent and estimates are given in
Table 2.
Leaf-area in x2 moves out of this age-class by two processes. First, there is develop-
ment into x, at the specific rate a2, but also a certain proportion of area in x2 is attacked
by leafminers and therefore accumulates as attacked area in w2. The rate of accumula-
tion per leafminer female is a product of e, the leafminer egg laying function (or eggs/
female/day), a (area/egg), the area reserved by adult female leafminer for an egg plus
subsequent feeding area for the closed larva, and x2/(x2 + 2), the proportion of area
left in the 'oviposition window' that can be attacked.

Leafminer Submodel

The second trophic level, the leafminer was divided into six developmental stages:
eggs, L1 larvae, L2 larvae, L3 larvae, pupae and adults. The larval stage was modeled
as a distributed delay network with three stages. Data were available only for the whole
larval stage, but it was necessary to model the instars in this stage separately in order

March, 1991

Insect Behavioral Ecology '90 Brewster & Allen

to facilitate the parasitism function. The method used for formulating the delay was
based on that developed by Manetsch (1976) and modified by Vansickle (1977) to include
attrition The mathematical form of this submodel can be written as:

Y/6 X2
(eggs) y, = e--(x- blyi P.iYI
(L1 larvae) y2 = bly2 3b2y 12Y22
(L1 larvae) y = 3b2y2 3b2Ys y3g3(y3)Q3z4 L23
(L3 larvae) y4 = 3b2Y3 -3b2y4- Y4g4(Y4)Q4z4 2Y4
(pupae) Y5 = 3b2Y4 bs5s paY5
(adults) ye = b36 +- [Xm 6X2 + Dm(je-y)]
A .... (ii)

where e, x2, and w2 are the same as in the celery submodel. bi's are the reciprocal of
the residence times in the respective stages, M i's are the mortality rates, and yi's are
the parasitoid maximum attack rates on the leafminer larval stages. These parameters
are temperature-dependent.
The average sex ratio for L. trifolii was observed by Zehnder & Trumble (1984) to
be close to 1:1. This is reflected by dividing total leafminer adults (Y6) by two to obtain
the number of adult female leafminers. The proportion of unattacked leafarea, x2/
(x +w2), is used to limit egg production based on leaf-area available for attack in the
leaf age oviposition window, x2.
Adult female parasitoids (z*4) have been shown to have a preference for 3rd instar
leafminer larvae, with a decreased preference for 2nd instar larvae (Patel 1987). To
reflect this, the rate of attack assigned to each stage is made different i.e., y3 is not
equal to y4.
The function gi(Yi), represents the functional response of the parasitoid to leafminer
larval density or the per parasitoid attack rate as a function of leafminer larval density
(Holling 1959, 1964, Allen 1990). In this model, a Type 2 functional response was as-
sumed where gi(Yi) = i/ (A + yi), with A = yi/2, which represents the larval density
at which the attack rate is one half of the maximum rate. Alternatively, gi(yi) can be
represented as (1-exp(-kiyi)), where ki are constants equivalent to the reciprocal of the
critical host densities, the values above which the attack rates are nearly independent
of larval density, yi (Smerage et al. 1980, Patel 1987).
Qi represents the proportion of unattacked larvae available for attack by the
parasitoid, and can be thought of as,

Qi -- .... (iii)
yi + +Z2 + Z3

where the zi's are parasitoid eggs, larvae and pupae, respectively. Female parasotoids
have been shown to locate mines by palpating the leaf (Hendrickson & Barth 1978).
Parasitoid eggs, larvae and pupae are to be found within these mines, and the larval
stages there are potential hosts for parasitoids regardless of whether they have already
been attacked. In addition, since D. intermedius is a solitary insect (Hendrickson &
Barth 1978), each egg, larva and pupa represents an individually-attacked leafminer
larva. The sum of these parasitoid stages therefore equals the number of attacked
The leafminer adult stage includes a migration model to allow for movement of
adults into the cropping area during crop growth. This model is given as,

28 Florida Entomologist 74(1) March, 1991

Total Migration = Taxis + Diffusion
P ax2 P ay6
x6 -- + -Dm -
A Or A Or
-- ~m 96x2 + Dm (6-1y6)
A A .... (iv)

The form of this model is analogous to that listed in Okubo (1980 p.82) which is of the
a dx, a0 aY
-- {xy6 }+ -- (D- ) . . (v)
ar dr Or Or

where X is the chemotactic coefficient, D, diffusivity, and r, a linear distance. From
eqs. (iv) and (v) ax2/ar and dx2/ dr represent the gradient of attractive leaf-area x, across
the boundary of the test area i.e., x2 inside minus x2 outside. The latter term is zero
since it is assumed that there is no x2 outside the boundary. Therefore 0xg/ar simply
becomes x2. The gradient of adults across the boundary is represented by yd/8r. In its
simplest form this is the difference between the density of adults outside (Y6) and inside
y6) the test area. P/A is the perimeter to area ratio used to adjust the density of insects
for the dilution effect of different size areas on migration. The smaller the test area the
higher this ratio and the larger the effect of migration on the density in the test area.


The parasitoid population is divided into four developmental stages: egg, larva,
pupa, and adult. The mathematical form of this submodel is given as:

(eggs) z1 = Oz4 (y Y3(y3)Qa + 4g4(4)Q4 C1Z1 P1
(larvae) z2 = czz c2 P2z2
(pupae) 3 = C2Z2- c3 03s 3
(adults) z4 = C3Z- C4Z 4 + [pz4W2 + Dp(4 (vi)

where 0, the ratio of eggs laid to hosts killed, ci, the reciprocal of residence times in
the respective stages, and Pi, the mortality rates, are functions of temperature.
Parasitoids have been shown to locate their hosts by cueing on volatiles produced
by plants upon attack by hosts (Lewis & Tumlinson 1988, Godfray & Wage 1988, Turl-
ings et al. 1990, 1991). This concept was used in formulating the migration model for
the parasitoid. Taxis of parasitoids was therefore made dependent on attacked celery
leaf area (w2) from eq. (i).


Data available in the literature were used to calculate most of the parameters in the
model as temperature functions. This was first done in cases where L. trifolii interacted
with celery. Other parameters were calculated from data available for the interaction
of the leafminer with other crops and also from data on the closely related species L.
sativae (Parrella et al. 1983b, Zoebisch & Schuster 1987). Biological intuition and reason-
able model behavior were used to estimate parameters for which data were lacking or
scarce. We do not attach any biological significance to equations derived from data.
These equations are simply based on curves that conveniently described the existing

__ _ __I_~

__ 1

Insect Behavioral Ecology '90 Brewster & Allen 29

The only environmental factor forcing the model is temperature. Simulations were
carried out using an annual sinusoidal temperature function applied to the growing
period (100 days) of the crop (Fig. 1). This cycle was derived from maximum and
minimum temperature data for Lakeland, Florida for the years 1935 to 1974 (Allen
1977). The period of high temperature beginning on day 200 was chosen as the trans-
planting time for input into the model.
Table 1 and Fig. 2 show the parameters used to describe celery growth. The parame-
ter a as described earlier (eqs. (i)) represents the area occupied by an egg plus that
which subsequently is consumed by a larva. This area is thought to be reserved by an
adult female leafminer at oviposition. Data and some estimation put this area as close
to 1.0 cm2 of celery leaf.
The average longevity of celery petioles was found by Musgrave et al. (1977) to
range from 5-6 weeks to 7-9 weeks. In this model an average of 8 weeks was chosen.
Based on this, estimates of the residence times of leaf-area within each age-class were
determined, and the reciprocals of these are the developmental rates of the leaf age
classes (ai's in eqs. (i)) (Table 1).
D. intermedius was chosen as the representative parasitoid because in celery, it
tends to predominate (Johnson & Hara 1987). In addition, more data were available for
this than any other parasitoids of L. trifolii, and the difficulty in modeling a natural
enemy complex required that a choice be made. Data for D. intermedius were obtained
from cases where this parasitoid interacted with L. trifolii although this may have
occurred on crops other than celery.
Parasitoid species are known to exhibit variability in their sex ratios (Doutt et al.
1976). Differences in the sex-ratio of D. intermedius on two bean species were observed

Annual Temperature Cycle
Lakeland, Florida 1935-1974


T= 5.5Cos((2 /365) (Day-200))+22.4

) 27

Q 23


0 73 146 219 292 365
Day of the Year

Fig. 1. 39 yr. average temperature cycle for central Florida (C) fitted to a sine wave.

Florida Entomologist 74(1)


Parameter Data Source Function or Rate*

leaf Musgrave et al. (1978)
area(LA) Guzman et al. (1979)
Mishoe et al. (1978) LA = k/(1 + ea-It)
Foster & Sanchez (1988) f(t) = krea-^(1 + e"a)-

al Musgrave et al. (1979) 0.048/day
a2 Musgrave et al. (1977) 0.048/day
a3 Musgrave et al. (1977) 0.071/day

a Fagoonee & Toory (1984)
Bodri & Oetting (1985)
Parrella & Bethke (1988) 1.0 cm2/miner/egg

k = 7115.47 a = 14.025 r = 0.1049 t = time e = exp
# In addition to the data sources, some estimations were used to
parameters listed.

determine the

by Hendrickson & Barth (1978). Since no data were available for the parasitoid on
celery, the simplest case of 1:1 sex-ratio was used in this model. Therefore z*4 represent-
ing adult female parasitoids (eqs. (ii) and (vi)) is equal to z4 divided by two.

Celery Plant Growth













50 75 100 125 150 175
t = Age of Plant (d)
Fig. 2. Cumulative leaf-area and growth rate of celery. The rate,
simply the derivative of the cumulative curve.




100 CD



f(t) in eqs.(i), is

March, 1991

Insect Behavioral Ecology '90 Brewster & Allen


Parameter Data Source Function or Rate

E Leibee (1984) 0.1729eo.2145T 0.0292e 2o6T

bi Leibee (1984) 0.4821nT 1.196
b2 Leibee (1984) 0.007T 0.00587
b3 Leibee (1984) 0.015960 1407T 0.0084eo.157T
b4 Leibee (1984) -2.47x10 = 0.0023T

Al Zoebisch (1988) (1.437T 2.968)x10l
A2 Patel (1981) 0.343-0.032T + 0.0008T2
A3 Liebee (1984) 0.283/(37.0- T) 0.008

T = temperature e = exp

Parameters used for the leafminer and parasitoid models are given in Table 2 and
Fig. 3, Table 3 and Fig. 4, respectively. The 'Logan-type' curve (Logan et al. 1976,
Allen 1988) for representing development rate and ovipositional functions was used
where possible. This type of curve adequately represented both leafminer egg laying
and pupal development where data points were available beyond the optimum temper-

Leafminer Egg Laying Function

10 16 22 28
T = Temperature (oC)

0 65


0 39

0 26

0 13

34 40 n -

Leafminer Adult Mortality Function

b4= -2.47 x 10-3 + 0.0023T
s 0.076
O c .

0 048
0 0


16 22 28
T = Temperature (OC)

34 40

Leafminer Development Functions
-- b,=04821nT- I 19
- b,= 00077- 0 0587
b=0 0 1596exp(O.1407) -0.0084exp(0 157T)

10 16 22 28 34 40
T = Temperature (oC)

Leafminer Mortality Functions
-- Eg:p,=(1.4365T-2968)x10-3
S.- Lra o 0.0008T- 0 032T + 0 343
0 6 Pupa. 0 2831/(37 0 T)- 008
d d
0 12

11 004
S "
II 00 '_-- ^

10 t6 22 28
T = Temperature (C)

0 25

020 5

0 15

0 10


0 00

34 40

Fig. 3. Parameters for the leafminer submodel, eqs.(ii), as temperature functions.
(a) oviposition rate (b) developmental rates, (c) adult mortality rate, and (d) immature
stage mortality rates.

35 i E= 729exp(245T) 0-0292exp(0
= 0.1729exp(0.2145T)- 0.0292exp(0 2

0 020


Florida Entomologist 74(1)


Parameter Patel (1987) -10.979 + 1.926T-0.04T2

o Patel (1987) -1.1056 0.148T 0.0031T2

cx Patel & Schuster (1983) -1.1079 + 0.139T 0.0023T2
c2 Patel & Schuster (1983) -0.625 + 0.0639T- 0.0012T2
cs Patel & Schuster (1983) -0.377 + 0.0404T- 0.00067T2
c4 Patel (1987) 0.00599eo.s5T

P1 Patel & Schuster (1981) 0.4168- 0.0362T + 0.0009T2
P2 Patel & Schuster (1981) 1.204x10-4 T2.12
P3 Patel & Schuster (1981) 7.076x10-4 T7692

T = temperature e = exp

Parameters for the migration model i.e., ki, Dm, ,p and Dp were the most difficult
to determine. In no case had these coefficients for these two insects been determined.
Therefore, for simulation, P/A was combined into Xm, Dm, Xp and Dp and adjustments
made until a "reasonable" model output was obtained. In all simulations reported here
we used (P/A)km = 0.0001 cm-2 d-1, (P/A)Dm = 0.001 d-', (P/A)xp = 0.01 cm-2 d-1,
(P/A)Dp = 0.001 d-1, and the "background" densities of the leafminer and parasitoid
outside the field were ye = 0.005 cm-2, 4 = 0.005 cm-2.


The simulation results for the standard model are given in Fig. 5. Leafminer larval
density after 60 days was 10 larvae/100 cm2 of leaf with a peak density of 11 larvae/100
cm2 occurring after 70 days. Density at harvest (100 days) dropped to ca. 7 larvae/100
cm2. Adult parasitoid density at the same period was ca. 20 adults/100 cm2 of leaf. Since
the standard model was assumed to contain the standard levels of both antixenotic and
antibiotic resistance it was used as the check for the other scenarios.
The plant was made more susceptible (decreased antixenotic resistance) by increas-
ing the leafminer oviposition rate (e) two-fold in the model, eqs. (ii). With this modifica-
tion the leafminer larval population peaked after 60 days at 60 larvae/100 cm2 of leaf.
At harvest the density had dropped to 28 larvae/100 cm2. Parasitoid density at 100 days
exceeded 100 adults/ 100 cm2 of leaf (Fig. 6(a)). However, when the plant was made
more resistant to oviposition by decreasing the oviposition rate two-fold, larval density
at 60 days remained very low at 2 larvae/100 cm2 with a peak at ca. 3 larvae/100 cm2 of
leaf after 80 days and a final density of ca. 2 larvae/100 cm2. The parasitoid ended with
a density of ca. 4 adults/100 cm2 of leaf (Fig. 6(b)). To test whether the reduction in
larval density was due to the decreased oviposition rate, to parasitoid attack or both,
we ran this model excluding the parasitoid. In this case leafminer larval density was as
low as 5 larvae/100 cm2 at 60 days but exceeded 100 larvae/100 cm2 after 100 days (Fig.
6(c)). This type of resistance was therefore much more effective in the presence of a
When antixenotic resistance (i.e., e) was kept at the standard level but antibiotic
resistance was altered by adjusting larval mortality (A2 in eqs. (ii)), the following were
observed. When the plant was made susceptible by reducing larval mortality two-fold,
the leafminer larval density peaked at 22 larvae/100 cm2 after 60 days but dropped to
11 larvae/100 cm2 at harvest, while the parasitoid had a density of ca. 43 adults/100 cm2

March, 1991

Insect Behavioral Ecology '90 Brewster & Allen 33

Parasitoid Specific Attack Function Ratio of Parasitoid Eggs Laid:Hosts Killed
>1 15.0 1.00

1= -10.9794 + 1.926T -0.04T2 a = -1.16 + .1482 0.0031 b
' 13 4 084

M 2

S 8.6 C
-. 7.0
10 15 20 25 30 35 0.20_
T = Temperature (oC) 10 1; 22 32 24 40

Parasitoid Derelopment Functions T Temperature (C)
Parasitoid Adult Mortality Function
1.5 00.6 o
O 010
-- e1= -79 +l. i 0.9T -0.0023T2 1
S-- c= .60.6+ .069T 0.00120e C
S1.2 C- -0.+0.4= 0.00599erp(0.08449T) d
12 i - e,=-0.3770 + 0.0M04T 000067 0.48 0 06

0.0 0.36 006

c / o = T
> 00.

o E = 0 0.02
003 002
'C0 OC------------------

S10O 16 22 23 34 40
0.0 0.CC
10 !6 22 28 34 40 T =Temperature ("C)
T = Temperature (C)

Parasitoid Mortality Functions
S- Egg: PI= 0.4168- 0.032+0-2 09tc0
I* .. LafrrPia: z= 1. x 104Oa
S023 -PU PI 7= 7.076 x10"-l4T


I 002 /-

10 16 22 28 24 40

T = Temperature ("C)

Fig. 4. Parameters for the parasitoid submodel, eqs. (vi), as temperature functions.
(a) attack rate, (b) ratio of parasitoid eggs laid:hosts killed, (c) developmental rates, (d)
adult mortality rate. (e) immature stage mortality rates.

at 100 days (Fig. 7(a)). When the plant was made resistant to larval attack by increasing
larval mortality two-fold, larval density was 2 larvae/100 cm2 of leaf after 60 days
peaking at ca. 4 larvae/100 cm2 of leaf after 90 days. This was also the density at 100
days. The parasitoid had a density of ca. 5 adults/100 cm2 of leaf at 100 days (Fig. 7(b)).
Again to test whether this low density was due to resistance, the parasitoid, or both,
the model was rerun excluding the parasitoid. In this case, the leafminer had a low

Florida Entomologist 74(1)

March, 1991

Leafminer-Parasitoid Interaction
on Celery (Standard Run)

24 48 72 96
Days After Transplanting


Fig. 5. Results of the standard model for L. trifolii-D. intermedius interaction on

larval density of 4 larvae/100 cm2 after 60 days. The density however exceeded 100
larvae/100 cm2 at 100 days (Fig. 7 (c)). It is again obvious that this type of resistance
works better in the presence of the parasitoid.
We investigated what would happen if both resistance mechanisms were altered. In
the first case, the standard level of antixenotic resistance was lowered (e set to 2 E)
while antibiotic resistance was increased (A2 set to 2 A2). In this case larval density
was ca. 13 larvae/100 cm2 after 60 days but peaked between 70-80 days at ca. 16 larvae/
100 cm2. The density at harvest was ca. 12 larvae/100 cm2 of leaf. Parasitoid density
after 100 days was ca. 29 adults/100 cm2 of leaf (Fig. 8(a)). When both antixenotic
resistance and antibiotic resistance were increased by decreasing oviposition rate (e set
to e/2) and increasing larval mortality ( p set to 2 /2), larval density at 60 days was
reduced below the standard run (Fig. 5) reaching ca. 0.4 larvae/100 cm2. It later peaked
at 1 larvae/100 cm2 after 90 days. The parasitoid density remained low at 0.7 adults/100
cm2 after 100 days (Fig. 8(b)). This "double jeopardy" plant resistance in effect slowed-
down the whole interaction compared to the standard run.


Systems models and computer simulations provide an efficient and effective method
for evaluating alternative control strategies for L. trifolii and other insect pests. This
methodology used by Stimac (1990) and modified here provided the mechanisms by
which the biological control agent D. intermedius and celery plant resistance were
integrated and examined for their effects on the leafminer larval population.
Host-plant antixenotic and antibiotic resistance can be attributed to several factors
including plant physical form, nutritional deficiencies, presence or absence of certain



0 0.15

z 0.05


Insect Behavioral Ecology '90 Brewster & Allen

Leafminer-Porositoid Interaction
on Celery


z 0.2

0 24 48 72
Days After Transplanting





1 .2



z 0.3


96 120

Leafminer-Parasitoid Interaction
on Celery

* Leafminer b
o Parasitoid

-' -

0 24 48 72
Days After Transplanting

96 120

Leafminer-Celery Interaction

0 24 48 72 96 1 20
Doys After Transplanting

Fig. 6. Results of simulation where standard antixenotic resistance was increased
over that in Fig. 5. (a) resistance was decreased two-fold (b) resistance was increased
two-fold, and (c) resistance was increased two-fold but the parasitoid was excluded.

Florida Entomologist 74(1)

March, 1991


0 20 40 60 80 100 120

-*- miner -- paraeltold adults



o.2 b

0.1 -



0 "
0 20 40 60 80 100 120

miner -+ parultold adult








0 20 40 60 80

100 120

-- miner

Fig. 7. Results of simulation where standard antibiotic resistance was increased
over that in Fig. 5. (a) resistance was decreased two-fold, (b) resistance was increased
two-fold, and (c) resistance was increased two-fold but the parasitoid was excluded.

Insect Behavioral Ecology '90 Brewster & Allen


0 20 40 60 80 100

miner --- parasltold adults



0 20 40 60 80 100

-- miner parasitold adults

Fig. 8. Results of simulation where both both standard antixenotic and antibiotic
resistance were changed over that in Fig. 5. (a) antixenotic resistance was decreased
two-fold while antibiotic resistance was increased two-fold, and (b) both antixenotic and
antibiotic resistance were increased two-fold.

Florida Entomologist 74(1)

volatile chemicals, or plant biochemicals (Bech 1965). For example, in bean Phaseolus
vulgaris L., high trichome density acted as a physical deterrent to leafminer attack
(Fagoonee & Toory 1983), while in tomato, egg-larval mortality was higher on plants
with a low nitrogen content than on plants with higher nitrogen content (Minkenberg
& Fredix 1989). When 159 accessions of Apium species were examined by Trumble &
Quiros (1988), they observed in some species the possible existence of both antixenotic
and/or antibiotic resistance to leafminer attack. The former type they attributed to the
presence of repellant chemicals or to the lack of stimulants. This tended to affect feeding
and oviposition by adults. The latter type was suggested based on decreased pupation
and emergence of adults. It must be understood that there would be instances where
it may be difficult to categorize plant resistance mechanisms as either antixenotic or
antibiotic (Beck 1965). Nevertheless in this model (eqs. (ii)) antixenotic resistance in
the celery plant was reflected simply by adjusting the oviposition rate (e) of the leaf-
miner, while antibiotic resistance was included by adjusting leafminer larval mortality
The results indicate that the combination of host-plant resistance and biological
control may prove to be a more efficient strategy for pest control compared to any of
these two strategies employed separately. The potential for pest control by plants
possessing either of the two types of resistance has been evident (Alverson & Gorsuch
1982, Kennedy et al. 1987). The type of pests and the crop involved may determine
which of these resistance types is more desirable. In celery for example, antixenotic
resistance may be more desirable especially since leafminer adult feeding and oviposition
could reduce photosynthetic rates (Trumble et al. 1985). However, Trumble & Quiros
(1988) pointed out that since the leafminer is a polyphagous insect, antixenotic resistance
may encourage undesirable intercrop movement and therefore anthbiotic resistance
may provide better extended control.
The exclusion of the parasitoid from both the antixenotic and antibiotic scenarios
resulted in far less control of the leafminer (Fig. 6(c) and Fig. 7(c)), when compared to
the scenarios where the parasitoid was included (Fig. 6(b) and Fig. 7(b)). Larval density
in both resistance/no-parasitoid scenarios at 60 days after transplanting was quite low,
and was in fact only slightly greater than that of the resistance/parasitoid scenarios at
the same period. However, when the parasitoid acted along (Fig. 5), the density after
60 days was at least 6 times greater than in the resistance/no-parasitoid and the resist-
ance/parasitoid scenarios. Resistance therefore may have had more effect at low larval
density while the parasitoid was better at higher larval density. It is not surprising
then that Bergman & Tingey (1979) found that working together, biological control and
plant resistance provided density-independent mortality at low density and density-de-
pendent mortality at higher density.
Though control using the parasitoid and plant resistance may appear to be adequate,
one must also look at the effects of resistance on the parasitoid population. In both
scenarios where high resistance was included, the final parasitoid populations were
quite low compared to the standard model. The adverse effects of plant resistance on
natural enemy populations have been recognized (Herzog & Funderburk 1985). Plant
resistance could affect natural enemies by reducing the host level below the natural
enemy's searching ability (Painter 1951). In addition, resistance may alter a host's
physiology and behavior to the extent that it affects the success of the natural enemy.
A cautious approach to employing a combination of resistance and biological control in
Integrated Pest Management has therefore been emphasized (Herzog & Funderburk
1985). Such integration may be even more useful for crops with long growing periods.
In the case of celery where the growing periods is short (a maximum of 100 days), or
in the case of greenhouse crops where releases of parasitoids are often possible, low
numbers of parasitoids at the end of the crop's growing period would be little cause for

March, 1991

Insect Behavioral Ecology '90 Brewster & Allen


We are grateful to Dr. Antonio Soto-Mayor, ARS Location Coordinator, Mayaguez,
Puerto Rico for a graduate student stipend to the senior author which made this re-
search possible and to Dr. Sherlie West for local coordination. We would like to thank
Drs. Jim Jones and J. Howard Frank for their reviews of the manuscript. Helpful
discussion and suggestions by J. M. Jones, R. M. Peart and G. H. Smerage is gratefully
acknowledged. This is Florida Agricultural Experiment Station Journal Series No. R-


ALLEN, J. C. 1977. A tree model for simulating pest management strategies in citrus.
Proc. Int. Soc. Citriculture 2: 507-511.
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40 Florida Entomologist 74(1) March, 1991

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Florida, 163 p.

Florida Entomologist 74(1)


Insect Attractants, Behavior and Basic Biology Research
Laboratory, Agricultural Research Service,
U.S. Department of Agriculture,
Gainesville, Florida 32611


Herbivore-induced plant chemical responses are usually considered direct defenses
against the herbivorous attackers. Recent findings show that a third tropic level can be
involved as well. Herbivore-injured plants release relatively large amounts of volatiles
that are attractive to natural enemies of the herbivores. The host-searching behavior
of the generalist parasitoid Cotesia marginiventris is mediated by such plant produced
volatiles. Since plant and entomophage both profit from this interaction it has been
suggested that the plant responses serve to recruit the entomophages. Here we argue
that induced production of plant chemicals evolved first as a direct defense against
herbivores, and that the attractive function likely evolved secondarily. Results of a
plant palatability experiment are given to provide preliminary support for a defensive
function. Plants that were induced to release volatiles that are known to be attractive
to the parasitoid became less palatable to the herbivore beet armyworm.

Las respuestas quimicas herbivoro-inducidas en plants son comunmente con-
sideradas como defenses directs en contra del herbivoro. Recientemente, fue encon-
trado que un tercer nivel tr6fico puede tambien estar relacionado. Plantas dafiada por
herbivoros liberan relativamente grandes cantidades de volatiles que son atractivos a
enemigos naturales de los herbivoros. El comportamiento de bdsqueda del hospedero
del parasitoide generalista Cotesia marginiventris es inducido por estos products vol-
Atiles vegetables. Como ambos plant y entom6fago se benefician de esta clase de interac-
ci6n, se ha sugerido que las respuestas de la plant sirven para reclutar al entom6fago.
Aqui, nosotros argumentamos que la funci6n a postriori de los quimicos es preferib-
lemente secundaria y que en base a una producci6n de quimicos de la plant, una funci6n
direct defensive deberia haberse formado. Los resultados de los experiments de
palatabilidad de la plant son utilizados para sustentar esta hip6tesis. Plantas inducidas
a liberal volatiles que se conocen como atrayentes del parasitoide, se convirtieron en
menos atractivas al hervivoro cogollero de la remolacha.

Plant defensive strategies against herbivores have mostly been observed as interac-
tions at two trophic levels (Levin 1976, Rhoades 1979, Kogan & Paxton 1983, Coley et
al. 1985). The involvement of a third trophic level has only recently been demonstrated.
It has been shown that plants under herbivore attack may actively attract predators
(Dicke & Sabelis 1988, Dicke et al. 1990a, 1990b) and parasitoids (Turlings et al. 1990b).
The attraction of natural enemies of the herbivorous attackers is mediated by the release
of relatively large quantities of volatiles by herbivore-injured plants.
Here we present some details of an interaction between corn (Zea mays L.) seed-
lings, beet armyworm (Spodoptera exigua Hiibner) larvae, and the generalist parasitoid
Cotesia marginiventris (Cresson). A feeding experiment with beet armyworm larvae
was conducted to obtain preliminary evidence for the hypothesis that the plant response
may primarily be a direct defensive response against its herbivore attackers.

March, 1991

Insect Behavioral Ecology '90 Turlings & Tumlinson


The larval endoparasitoid, Cotesia marginiventris, attacks the early stages of many
lepidopterous larvae. Host-seeking females of this parasitoid use airborne semiochemi-
cals emitted by the microhabitat of the hosts. Flight tunnel bioassays have shown that
plants damaged by the hosts are the main source of these attractive volatiles (Turlings
et al. 1990a).
Collections and analyses of the volatiles that are released by herbivore-damaged
plants revealed an active release comprising mainly terpenoids by the plants in response
to herbivore-damage (Turlings et al. 1990b, 1990c). A striking difference was observed
in the quantities of terpenoids released by plants that were subjected to herbivore
damage for an extended period (Fig. Ic) and plants that underwent fresh herbivore
damage (Fig. Ib). This difference is the result of a lag time that is necessary for the
plants to build up their response (Turlings et al. 1990b). Undamaged plants appear
virtually odorless (Fig la).
The plant response cannot be induced by artificial damage unless the damaged sites
are treated with the regurgitant of larvae (Turlings et al. 1990b). One of the functions
of the plant-released volatiles may be the recruitment of natural enemies of herbivore
attackers (Dicke & Sabelis, 1988; Dicke et al. 1990a, 1990b), but we propose that the
plant response primarily evolved as a direct defense against the caterpillars. If this is




S 1 4 IS2
24: 1 IS1

S5 6

C 32L
4 5 6 7 S2
24j 1 IS1

16 2 3 10

9 12 15 18 21 24 27 30 33

Fig. 1. Gas chromatographic profiles of volatiles released by corn seedlings. A)
Undamaged seedlings, B) seedlings freshly damaged by BAW larvae, and C) seedlings
that were damaged overnight by BAW larvae.
The numbered peaks are: 1) (Z)-3-hexenal, 2) (E)-2-hexenal, 3) (Z)-hexen-l-ol, 4) (Z)-3-
hexen-l-yl acetate, 5) linalool, 6) (3E)-4,8-dimethyl-1,3,7-nonatriene, 7) indole, 8) a-
trans-bergamotene, 9) (E)- p-farnesene, 10) (E)-nerolidol, and 11) (3E,7E)-4,8,12-
trimethyl-1,3,7,11-tridecatetraene. Methods followed Turlings et al. (1990b, c).

44 Florida Entomologist 74(1) March, 1991

true, we can expect that seedlings under herbivore attack become not only attractive
to parasitoids but also less palatable to the caterpillars. This hypothesis was tested


Insects and Plants

Beet armyworm (BAW) was reared according to the method described by King &
Leppla (1984). Initially, the larvae were fed on a laboratory-prepared pinto bean diet.
Thr larvae were placed on corn seedlings eight to eighteen hours before their use in
Corn (Zea mays L., var. "loana Sweetcorn") seedlings were grown in a greenhouse
and used in bioassays when they were 6-8 days old.

Treatment of Plants

Corn seedlings with three clearly distinguishable leaves were damaged artificially
with razor blades (Fig. 2). Each leaf was scratched so that approximately 2 cm2 of their
surface was damaged. The plants were treated with the regurgitant of third instar
corn-fed BAW larvae. Regurgitation was induced by holding the larvae with a pair of
forceps near the buccal cavity. Then, the "spit" was rubbed directly from the mouth
parts of the larvae onto the damaged sites (Fig. 2). This type of treatment is known to
induce the release of exceptionally high amounts of terpenoids in the seedlings several
hours after treatment (Turlings et al. 1990b).
The leaves were used in the feeding experiments either 0-1 h, 5-6 h, or 17-19 h after
treatment. One group of four seedlings was damaged late in the afternoon to be used
in a feeding experiment the following day (18 1 h later). For the other tests, an
additional eight seedlings were treated the following morning.

Feeding Experiments

Four of the eight seedlings that were treated in the morning were cut immediately
after treatment and taken to the lab together with four untreated control plants. The
second leaf of each seedling was severed just below where the leaf attaches to the stem,
and the severed ends were wrapped in wet cotton. The number 2 leaves (Fig. 2) of a
treated seedling and a control seedling were crossed over each other on a glass plate
as shown in Fig. 3. A Plexiglas overlay (4.5 x 4.5 cm2) with four 1 cm diam. holes in
it, was placed over the seedlings such that two of the holes would expose sections of
the treated leaf and the other two holes would expose the control leaf (Figure 3). The
overlay exposed a portion of the treated leaf that was not damaged and an equivalent
portion of the control leaf. For a particular test, four sets of treated and control seed-
lings were used under four different overlays.
Six late-second-instar BAW larvae were placed in the center of each overlay and a
plastic petri-dish cover was placed over the larvae and the four holes (Fig. 3). To ensure
that the leaves were pressed flat onto the glass plate, beakers, each containing 80 ml
water, were placed on top of the petri-dish covers. For one hour, the larvae were
allowed to feed on the exposed leaf sections. At the end of a feeding period, the beakers,
petri-dish lids and larvae were removed. The portion eaten from the exposed sections
of each leaf was estimated by two experimenters and averaged for the treated and the
control leaves.

Insect Behavioral Ecology '90 Turlings & Tumlinson

Fig. 2. Treatment of corn seedlings. Leaves numbered 1 and 3 were scratched over
an area of approximately 2 cm2 and the regurgitant of one BAW larvae was rubbed over
the same area.

Each experiment was replicated 8 times for the three time periods. To compare
palatability of treated versus control leaves data were compared statistically with a
paired T-test (- <0.05).


Immediately (0-1 h) after damage and treatment with BAW regurgitant leaves of
corn seedlings were eaten by BAW larvae as much as control leaves (Fig. 4). However,
5-6 h after treatment the leaves apparently were less palatable. Significantly less was
eaten from the treated plants than from the control plants. After 17-19 h, treated leaves

Florida Entomologist 74(1)


(r -J


WC /f / N
'1' V /

'- (Ij

Fig. 3. Setup for feeding experiment. A treated and a control corn leaf (CL) with
stems wrapped in wet cotton (WC) were crossed over each over on a glass plate. A
Plexiglass overlay (PO) with four 1 cm2 holes was placed on top of the leaves. BAW
larvae were allowed to feed on the leaves through the holes under a petri dish lid (PL).

still appeared to be less palatable, but differences between treated and control leaves
were not statistically significant.
The experiment was conducted such that the 0-1 h treatments were run in the
morning, the 17-19 h treatments (damaged the previous evening) were run early after-
noon, and the 5-6 h treatments late afternoon. It is possible that later during the day
the larvae were hungrier and therefore ate more in the afternoon (5-6 h experiment).
This possible difference in appetite is unlikely to have an effect on the preference for
control versus treated seedlings. If it does have an effect, it is to be expected that the
hungrier insects would be less selective.


The results presented here show that several hours after wounding and treatment
with caterpillar regurgitant, corn seedlings become less palatable to BAW larvae (Fig.
4). This time period of induced plant defense coincides with an observed dramatic in-
crease in terpenoids released by seedlings that underwent the same treatments in ear-
lier experiments (Turlings et al. 1990b).

March, 1991

Insect Behavioral Ecology '90 Turlings & Tumlinson


60 -
6T = 0.208 T = 2.802 T = 1.657

P = 0.841 P = 0.026 P = 0.142

48 -

< 36 -



0-1 5-6 17-19

Fig. 4. BAW feeding preference for treated versus control leaves. Amount of feeding
during one hour tested 0-1, 5-6, and 17-19 hr after leaves had been damaged and rubbed
with BAW regurgitant. The T and P values were derived from a paired T-test (a>0.05).

Wound-induced changes in plants that render them less palatable to herbivores are
common. The most detailed studies on wound-induced plant responses have been on the
accumulation of proteinase inhibitors throughout wounded tomato and potato leaves
(e.g., Green & Ryan 1972). Broadway et al. (1986) provided evidence for the hypothesis
that the buildup of proteinase inhibitors in damaged plants reduced the leaf quality for
feeding herbivore larvae. They showed that leaf material with high levels of proteinase
inhibitors caused a highly significant reduction in growth rate of BAW larvae. Pinpoint-
ing the chemical changes that are responsible for the inhibition of feeding is difficult.
Increases in the contents of tannins (e.g., Wratten et al. 1984), isoflavonoids (e.g.,
Russell et al. 1978 Hart et al. 1983) terpenoids (e.g., Mihaliak et al. 1987), alkaloids
(e.g. Baldwin 1988a, 1988b), cucurbitacins (e.g., Carroll & Hoffman 1980) have all been
associated with reduced feeding. In most of these cases these chemical changes cannot
be conclusively linked to palatability changes.
In several cases, high terpenoid content was correlated with a drop in plant quality
as a food source to herbivores. Nerolidol, one of the compounds released by corn in
response to BAW damage (Fig. 1), is a feeding deterrent to gypsy moth, Lymantria
dispar, larvae (Doskotch et al. 1980). Mihaliak et al. (1987) suggest that the soybean
looper, Pseudoplusia includes, which also feeds on corn, is negatively affected by high
terpenoid levels. They showed that larval consumption, growth and survival decline as
the leaf terpene content increases. The much studied sesquiterpenoid aldehyde gossypol
present in cotton has detrimental effects on several lepidopterous species (Gunasena et
al. 1988).
Studies on rodents provide some additional indirect evidence that terpenoids are
involved in plant defenses against herbivores Meadow voles that feed on conifer seed-

48 Florida Entomologist 74(1) March, 1991

lings show a preference for certain spruce and pine species, while they leave other
species untouched. Bucyanayandi et al. (1990) compared levels of crude protein, total
nonstructural carbohydrates total phenols, and monoterpenes in the bark to detect
differences between seedlings that the voles would attack and those that they would
not attack. They concluded that the presence of specific monoterpenes is more important
in defense mechanisms of conifer seedlings than relative levels of nutrients or total
Severe browsing by snowshoe hares induces deciduous trees and shrubs to produce
adventitious shoots that are extremely unpalatable to the hares (Bryant 1981). Bryant
(1981) found that these adventitious shoots contain exceptionally large quantities of
terpene and phenolic resins. Repellency by these resins was clearly demonstrated.
These examples indicate that plants are capable of waging chemical warfare against
herbivorous attackers. Several of the chemicals involved are terpenoids. Obviously,
from these examples and the preliminary results presented here we cannot conclude
that the volatiles that attract the parasitoid are also responsible for the observed de-
crease in feeding on treated plants. The results do, however, provide us with some
indirect support for the hypothesis that the release of volatiles is part of a defensive
response directed at herbivores.
It still remains to be determined whether effective deterrence against herbivore
attack can be induced in corn by just damage or whether the regurgitate is actually
required. Karban & Carey (1984) found that when cotton seedlings were exposed to
spider mites, new growths of these plants were less susceptible to further mite infesta-
tions. Karban (1985) showed that mechanical abrasion of cotton cotyledons was sufficient
to cause resistance to spider mites. It is possible that damage alone causes a defensive
reaction in the plants, but that herbivore-specific factors, like saliva, enhance this re-
sponse as has been shown for the volatiles released from corn damaged by BAW larvae
(Turlings et al. 1990b).
We can still only speculate about the function of the volatiles. Plants that originally
developed the trait of producing terpenoids must have a direct selective advantage. The
attraction of entomophagous insects to these volatiles cannot be expected to have de-
veloped simultaneously. It seems more likely that the production of terpenoids was
favored because they had a direct detrimental effect on herbivores. Over time,
parasitoids and predators may have exploited the release of the plant-produced chemi-
cals as cues to locate hosts or prey, thereby adding new selective pressures favoring
the production of, and particularly, the release of these chemicals by the plants. It is
conceivable that the chemicals were at first mainly toxins against the herbivores or
by-products or precursors of such chemicals, and that active release into the environ-
ment was not benefitial to the plants. Attraction of natural enemies of herbivores may
have favored mechanisms that allow the plants to actively release these chemicals. As
semiochemicals, the chemicals may also repel and deter herbivores, or may even serve
in the communication between plants as suggested by Dicke et al. (1990b). Over time
the signaling function may even have exceeded the toxic function in importance.


We thank John Simmons for conducting several of the feeding experiments, Dr.
Hans. Alborn for assisting in estimating the leaf areas eaten, and Drs. H. Frank, Philip
McCall, Fred Petitt, and Felix Wackers for their comments on the initial manuscript.


BALDWIN, I. T. 1988a. Short-term damage induced increases in tobacco alkaloids
protect plants. Oecologia 75: 367-370.

Insect Behavioral Ecology '90 Turlings & Tumlinson 49

BALDWIN, I. T. 1988b. Damage-induced alkaloids in tobacco: Pot-bound plants are
not inducible. J. Chem. Ecol. 14: 1113-1120.
proteinase inhibitors: A defense against herbivorous insects? Entomol. exp. appl.
41: 33-38.
BRYANT, J. P. 1981. Phytochemical deterrence of snowshoe hare browsing by adven-
titious shoots of four Alaskan trees. Science 213: 889-890.
BUCYANAYANDI, J..D., L. -M. BERGERON, AND H. MENARD. 1990. Preference of
meadow voles (Microtus pennsylvanicus) for conifer seedlings: chemical compo-
nents and nutritional quality of bark of damaged and undamaged trees. J. Chem
Ecol. 16: 2569-2579.
CARROLL, C. R., AND C. A. HOFFMAN. 1980. Chemical feeding deterrence mobilized
in response to insect herbivore and counteradaptation by Epilachna tredecim-
notata. Science 209: 414-416.
COLEY, P. D., J. P. BRYANT, AND F. S. CHAPIN III. 1985. Resource availability and
plant antiherbivore defense. Science 230: 895-899.
DICKE, M., AND M. W. SABELIS. 1988. How plants obtain predatory mites as body-
guards. Neth. J. Zool. 38: 148-165.
AND AE. DE GROOT. 1990a. Isolation and identification of volatile kairomone
that affects acarine predator-prey interactions. Involvement of host plant in its
production. J. Chem. Ecol. 16: 381-396.
1990b. Plant strategies of manipulating predator-prey interactions through al-
lelochemicals: Prospects for application in pest control. J. Chem. Ecol. 16: 3091-
DOSKOTCH, R. W., H. -Y. CHENG, T. M. ODELL, AND L. GIRARD. 1980. Nerolidol:
An antifeeding sesquiterpene alcohol for gypsy moth larvae from Melaleuca
leucadendron. J. Chem. Ecol. 6: 845-851.
Effects of caryophyllene, caryophyllene oxide, and their interaction with gossypol
on the growth and development of Heliothis virescens (F.) (Lepidoptera: Noc-
tuidae). J. Econ. Entomol. 81: 93-97.
HART, S. V., M. KOGAN, AND J. D. PAXTON. 1983. Effect of soybean phytoalexins on
the herbivorous insects Mexican bean beetle and soybean looper. J. Chem. Ecol.
9: 657-672.
KARBAN, R. 1985. Resistance against spider mites in cotton induced by mechanical
abrasion. Entomol. exp. appl. 37: 137-141.
KARBAN, R., AND J. R. CAREY. 1984. Induced resistance of cotton seedlings to
mites. Science 225: 53-54.
KING, E. G., AND N. C. LEPPLA. 1984. Advances and Challenges in Insect Rearing.
Agric. Res. Serv., USDA, U. S. Government Printing Office, Washington, D.C.
KOGAN, M., AND J. D. PAXTON. 1983. Natural inducers of plant resistance to insects,
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Society, Washington, D.C.
LEVIN, D. A. 1976. The chemical defenses of plants to pathogens and herbivores.
Annu. Rev. Ecol. Systems. 7: 121-159.
MIHALIAK, C. A., D. COUVET, AND D. E. LINCOLN. 1987. Inhibition of feeding by
a generalist insect due to increased volatile leaf terpenes under nitrate-limiting
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In G. A. Rosenthal and D. H. Janzen [eds.]. Herbivores: Their Interactions with
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Florida Entomologist 74(1)

Cotesia marginiventris to the micro-habitat of its hosts. Entomol. Exp. Appl.
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Department of Entomology and Nematology
University of Florida
Gainesville, Florida 32611-074


A model of coevolution in a simple but potentially chaotic predatory-prey system is
developed. Coevolution is introduced by making parameters functions of lagged density
as if natural selection had affected them. Increasing attack rate and decreasing predator
mortality rate were found to be destabilizing, producing more chaos and less phase-lock-
ing as revealed by bifurcation diagrams. In general, when the prey was more responsive
to natural selection the model was more stable, and when the predator was more respon-
sive to selection, the model was less stable, having more chaotic behavior and less
phase-locking. It is concluded that in this simple, phenomenological model that coevolu-
tion is not a priori a stabilizing force, and it depends on the circumstances whether
coevolution will work for or against chaotic dynamics.


Un modelo de evolucidn en un sistema simple, pero potencialmente depredador-presa
ca6tico fue desarrollado. La coevaluaci6n fue introducida elaborando funciones
parametro de densidad retardado como si la selecci6n natural las hubiera afectado.
Incrementos en la tasa de ataque y de crecimiento en la tasa de mortalidad del depre-
dador tuvieron un efecto desestabilizante, produciendo mas caos y menos fase-de-cierre
como es revelado por los diagramas de bifurcaci6n. En general, cuando la presa fue mas
reactiva a la selecci6n natural, el modelo fue mas stable, y cuando el depredador fue
mas reactive a la selecci6n, el modelo fue menos stable, teniendo mayor compor-
tamiento ca6tico y menor fase-de-cierre. Se concluy6 que en este modelo simple y
fenomenol6gico que la coevoluci6n no es una fuerza a priori, y ella depend de las
circunstancias tanto como la coevoluci6n trabajara para o en contra de la dinAmica ca6

Virtually all of the population interactions of animals seem at first glance to be
inherently destructive and therefore unstable. Why consumer organisms do not over-

March, 1991

Insect Behavioral Ecology '90 Allen

exploit their resources to the point of mutual extinction is one of the great classical
questions of ecology (see for example, Elton 1962, or Slobodkin 1964). One might think
that natural selection, lacking foresight, would produce ever more efficient consumers
thus leading to greater instability and chance of extinction, yet the world is awash with
herbivores, predators, parasites and pathogens.
One of the standard answers for why this is so is that the resource species (plants,
prey, hosts, etc.) retaliate with defenses against their attackers (Pimentel 1968, Pimen-
tal & Soans 1970). Schaffer & Rosenzweig (1978) have argued for the existence of a
coevolutionary stable state (CSS) where the rates of victim and attacker evolution are
equal but with opposite effects. This idea was originally developed for stable stationary
systems, and so it is somewhat uncertain in the context of a cyclic or chaotic system.
The diversity of such defenses was suggested by Witz (1990) in last year's symposium
where he found 371 references to antipredator mechanisms in 16 journals from 1969 to
1989 alone. Recent research in chemical and behavioral ecology suggests a mind-bogg-
ling web of "communication" between trophic levels: predacious fireflies that lure their
firefly prey by mimicking the prey species' flash patterns (Lloyd 1980, 1984, 1990),
cricket parasitoids attracted by cricket songs (Cade 1975, Walker 1986), moths that jam
bat sonar with ultrasonic pulses (Dunning 1968a, 1968b), host detection by chemically
mediated "learning" in parasitic wasps (Lewis & Tumlinson 1988) and plants that sum-
mon parasitoids with chemical attractants when they are under attack by the
parasitoid's host insect (Turlings et al. 1990, Turlings & Tumlinson 1991).
This paper will investigate the effects of coevolution in a simple (but potentially
chaotic) predator-prey model in which the explicit biological details of attack and defense
as illustrated in the examples above are modelled only in a phenomenological way. That
is, the examples are both numerous and sophisticated enough to assume a priori that
the genetics and mechanisms are present for very tightly coupled coevolution to occur
between natural enemies. Models of coevolution can easily become entangled in a mass
of detail. For example Levin et al. (1990) consider each chemical toxin and detoxifier
in a plant-herbivore system explicitly, and Schaffer & Rosenzwig (1978), from a rather
small amount of genetic detail, required a large amount of mathematical detail in deriv-
ing their CSS for a relatively simple system. A primary consideration of the present
paper will be whether an otherwise chaotic system tends to be stabilized by the inclusion
of coevolutionary effects between the interacting species. This question is of some im-
portance in the debate on whether chaotic systems would tend to be produced by the
effects of natural selection (Allen 1989, Berryman & Millstein 1989, Nisbet et al. 1989,
Lomnicki 1989, Mani 1989, Seger 1988).


We start with a "nongenetic" predatory-prey system similar in spirit to the model
discussed in last year's symposium (Allen 1990a) and to the models discussed by Schaffer
(1988). The model used here is capable of complex dynamics including chaos,
quasiperiodicty, and phase-locking with the forcing cycle. It is given by

(prey) x = [rc) x) -yg(x)y]T
(predator) y = [yg(w)y ty]T
(lagged prey) w = [(x-w)ITw]T
where: = 1 + 8cos(2rrt)
and T= the period of .

which will be referred to as the "no selection" model since it contains no selection
effects. 0 is the forcing cycle which multiples the prey reproductive rate ( 4 = 1 +
&cos(2 vt), 0 > S> 1). f(x) is the prey's reproductive function (e.g. x(l-x) for logistic

52 Florida Entomologist 74(1) March, 1991

reproduction) and g(x) is the predator's functional response (Holling 1959, 1965) (e.g.
x/(1 + x) for a type 2 response). x represents the time derivative of x, the model is in
dimensionless form, and time is in units of the forcing period, T. This is useful in the
analysis to be done below where we sample the system at the forcing period to look for
phase-locking with the forcing cycle. In other words, we just sample system (1) at every
time unit and "speed-up" (multiply) the whole right-hand-side by T (in time units/forcing
period). This puts the model on a per forcing period time unit thus allowing us to vary
T and still sample every time unit a much more time-efficient computer method than
waiting T time units to obtain one point. Notice that the numerical response, g(w), is
a function of prey density in the past, w, i.e., that it takes some time for the predator's
reproductive rate to respond to an increase in prey density. The mean time lag in this
effect is 7,. The prey species has a reproductive rate r, the predator has a maximum
attack rate, y, and experiences a constant mortality rate, A.
We now introduce a kind of phenomenologicall" genetics into the above model in
which predators exert selection pressure upon prey to develop defenses. We will assume
that this is expressed as a reduced attack rate where the attack rate, y, is replaced by
ye Xy (Fig. la) in which y represents lagged predators or predators in the past. The
past predators are generated by "pouring" predators through a distributed delay chain
as per Macdonald's (1978) "linear chain trick" (see also Manetch 1976). It is further
assumed that the prey must pay a proportional reproduction cost for their defense such
that r is reduced to re 9(Fig. lb). The net result of these assumptions is a new model

(prey) x = (re-.f(x) -Y-"-; i I.,iJT
(predator) y = [ye- g(w)y py]T
(lagged prey) w = [(x-w)/Tr]T
y1 = [3(y-yl)/Ty]T
Y2 = [3(y1-y2)/T,]T
(lagged predators) y = [3(y2y)k]T

which involves selection of increased prey defenses by increased predator density in the
past. It should be noted that Ty, the mean time lag of the effect, might be thought of
as being approximately equal to one prey generation although the effect will be spread
over a longer time by the action of the 3-stage delay chain, yi, and in reality by all sorts
of genetic mechanisms which might cause longer time lags. X can be thought of as a
measure of the strength of the selection pressure, and by this parameter we can inves-
tigate the effects of selection for prey defenses since, when X = 0, we have system (1)
with no selection of defenses.
We now consider a more complete model in which the predator "fights back" by
having its attack rate, y, be increased by lower prey densities in the past, i.e., that
reduced prey densities put selection pressure on the predator to develop a higher attack
rate. (Note that this applies best to a species-specific predator since a generalist pre-
dator may simply switch to another prey species when prey are rare.) This effect is
introduced by letting y be replaced by ye" (Fig. Ic) so that the highest attack rates
result from low prey densities in the past. As with the prey, we assume a cost to the
predator such that its mortality is higher for low prey densities in the past due to its
investment in a higher attack rate. Thus 1. is replaced by e (Fig. Id). in which low
prey densities in the past produce a higher current predator mortality rate representing
the cost of developing greater prowess. Combining these ideas with the prey selection
model, system (2), we obtain

Insect Behavioral Ecology '90 Allen

Selection by Predators
for Prey Defense

Past Predators (y)
Selection by Prey for
Increased Attack Rate

Past Prey (x)

Cost of Defenses
for Prey.

Past Predators (y)
Cost of Increased Attack
Rate to Predators

Past Prey (x)

Fig. 1. Illustration of the coevolution functions in the model, eq. (3). (a) Decreasing
attack rate as a function of past predator density (prey develop defenses). (b) Cost to
the prey of defenses. (c) Increased attack rate for low density of past prey (predators
improve their prowess). (d) Cost to predators of increased prowess (higher mortality

(prey) x =
(predator) y =
(Lagged prey) w =

[re xyf(r)- ye- X-tg(x)y]T
[ye ~-"`g(w)y Re-"y]T
[(X w)/T7]T

For Selection Purposes

xi = [3(x-xX)/T]T 1 = [3(y-y,)/ry]T
x2 = [3(xl x2)/ ]T y = [3(y1-y2)/'T]T

(lagged prey) = [3(x2-x)/Tx]T ~ [3(y2--)/Ty]T (lagged predator)

which will be called the "coevolution" model since it involves selection effects on prey
by high predator densities and on predators by low prey densities. Note that system
(1) is just a special case of (3) where X and v are zero. K measures the responsiveness
of the prey to selection pressure by high predator densities, and v measures the respon-
siveness of the predator to selection pressure by low prey densities. The delay chains
xi and yi are simply a mathematical trick for generating lagged prey, i, are lagged
predators, y. The emergence pattern from the delay chain is determined by the number
of stages in the chain (arbitrarily chosen to be three in our case) and the main residence

Florida Entomologist 74(1)

time in the delay ( T or Ty). Narrow emergence patterns are generated by a high
number of stages in the delay chain and long time lags by high values of r. Thus the
force of natural selection can be given a past distribution whose position and width can
be controlled. While these attributes of the selection process can be controlled, this
paper will concentrate on the more basic questions of the effect of coevolution itself and
the force of natural selection i.e., on the parameters h and v. The prey reproductive
function will be logistic, i.e., f(x) = x(1-x), and the functional response will be type 2,
i.e., g(x) = x/(1+ x).
We can also examine two additional areas of interest: the cost associated with in-
creased defenses or prowess and the sensitivity to selection (X and v). There is an
implicit "cost" effect in the model in that the effect of selection increases or decreases
at the same rate automatically depending only on past densities. The automatic rever-
sal implies a cost effect else the reversal would not occur. There are, however, the
explicit cost effects on reproduction, re-" for the prey and the Re-" for the predator
in eq. (3) which we might therefore call the "no free lunch" model since there are explicit
population level costs associated with selection. As an alternative to this, we can com-
pare a "free lunch" model in which there are no costs for increased defenses or prowess.
This model is simply the no free lunch model, eq. (3), with the cost terms missing, i.e.:

x = rf(x) ye-XY-'g(x)y
w =ye- '-,' Ry

where the lag equations have been omitted since they are identical to eq. (3).


In the coevolution model, eq. (3), there are 10 parameters: r, T, 8, y, Y Tx, Ty,
X and v. Even the no selection model, eq. (1), has 6 parameters: r, T, 8, rw, y and /.
Since exploration of this total parameter space is a massive computational problem, no
attempt will be made here to penetrate this unknown area. Instead attention is focused
on a comparison of the no selection model with the coevolution model changing one
parameter at a time and looking for differences in stability and the occurrence of chaotic
dynamics. Parameters of particular interest are the prey reproductive rate, r, the attack
rate y, the predator mortality rate, A, and the sensitivity of the prey and predator to
selection, X and v respectively. The other parameters are judged to be a bit more
peripheral to the interaction and will be held at the following constant but seemingly
reasonable values: T = 15, 8= 0.5, r, =4, ,T= 10 and ry = 10.
Viewing the model output at intervals equal to the period of the forcing cycle, T,
will reveal if the model is phase-locked with the forcing cycle. If the model is truly
periodic, (phase-locked) a repeating points) will be observed after transient behavior
has died away. If this process is repeated for a range of values of a parameter then
(plotting the parameter on the x-axis and the model output on the y-axis) we obtain a
plot of model behavior as the parameter changes (a "bifurcation" diagram). At each
parameter increment along the x-axis we typically calculate 25 forcing periods and
discard them as transients and then plot the model at the next 100 forcing periods. This
process is repeated for each computer screen pixel along the x-axis whose scale length
is the range of the parameter to be investigated. Phase-locked (periodic) behavior will
be revealed as a line or lines where the points) are repeating over and over even though
100 have been plotted. For example, 4 lines indicate that over that parameter range
there are 4 forcing cycles for each cycle of the population (4 to 1 phase-locking).
Using the method just described, the selection model and the coevolution model are
compared in Fig. 2. The parameters T, 6, Tw, and r7 are held constant at the values

March, 1991

Insect Behavioral Ecology '90 Allen


a ,,

2. ;

0.25 0.35 0.15 0. 55 0.65 0 75


).01 0.05 0.09 0.13 0.17 0. 2




'C -( -^ ":

0.35 0.45 0.55 0. 65 0.75

0. 25 0.35 0.45 D 55 0 65 0 75


2 : '*

0.OL 0.05 0.09 0.13 0 17 0 21

Fig. 2. Comparison of the no selection model (left panels) with the coevolution model
(right panels). (a,b) prey reproductive rate. (c,d) predator attack rate. (e,f) predator
mortality rate. Lines indicate phase-locking. Diffuse "fuzzy" areas indicate chaos.
Banded areas with tight boundaries usually indicate quasiperiodic behavior. Parameters
given in text.

given above, and the remaining parameters are r=0.5, y=0.5, A =0.05 (except for
the one which is being varied). In the coevolution case, X = 0.2 and u= 0.5. In Fig. 2 we
first vary the prey reproductive rate (Fig. 2a,b) then the attack rate (Fig. 2c,d) and
then the predator mortality rate, (Fig. 2e,f). The no selection model is plotted on the
left, and the coevolution model on the right. There appears to be an overall tendency
for the coevolution model to phase-lock a bit more with the forcing cycle and to have
slightly smaller amplitude oscillations in the predator population. In both models in-
creasing the attack rate tends to produce chaos and larger oscillations, and increasing
the predator mortality rate tends to be stabilizing, finally phase-locking one to one with
the forcing cycle (Fig. 2e,f). In general it appears that when the predator is doing well
(high attack rate, low mortality rate) both the no selection and the coevolution models
tend to be destabilized with the effect being somewhat larger for the no selection model.
We now examine the question of costs of defense or increased prowess and the
sensitivity of the prey and predator to selection (X and v respectively). In Fig. 3 the

56 Florida Entomologist 74(1) March, 1991

a b -
2.- 29"" .8..0. .
a "2 2.1

----- -- --

0.0 0 2 0.4 0.6 0. L. 0 .0 0.2 0.1 0.6 0. .0

x-axis is ., the predator's sensitivity to selection. Parameters are the same as ,ig. 2.
full coevolution model (the "no free lunch" model, eq. (3)) is plotted in (a,b) and the

e l v 0.ers .6 0., is pl 0.2 04 06 a a a a

Fig. 3. Comparison of prey which are sensitive to selection () = 0.2) (left panels)
with prey which are insensitive to selection ( = 0.02) (right panels). (a,b) The "no free
lunch" model (eq(3)). (c,d) The "free lunch" model (eq. (4)). The most chaotic behavior
occurs in the no free lunch model with insensitive prey and sensitive predator (3b). The
x-axis is u, than one whh s nstity to ton. aramers ar the prsame as Fig. 2.

full coevolution model (the "no free lunch" model, eq. (3)) is plotted in (a,b) and the
"free lunch" version, eq. (4), is plotted in (c,d). In addition, the left panels (a,c) illustrate
a prey which is sensitive to selection ) = 0.2), and the right panels (b,d) illustrate an
insensitive prey (X = 0.02). In general, it appears that the "no free lunch" version (a,b)
is a little less stable than the "free lunch" model (c,d), the latter having more phase-lock-
ing and less chaos. In addition, a prey which is sensitive to selection (a,c) appears to
be more stable than one which is not (b,d). In particular, the most chaotic situation is
the no free lunch model in which the prey is not very responsive to selection and the
predator is responsive (Fig. 3b for the higher values of predator sensitivity).
One interesting question is whether coevolution tends to prevent chaotic dynamics,
and increasing the sensitivity of the prey to selection seemed to be stabilizing in Fig.
3. With this in mind and using the no free lunch model (eq.. (3)) we increase the prey's
sensitivity to selection (K) from 0 to 1, holding other parameters as before (predator
sensitivity, v, = 0.5) (Fig. 4). The model is observed to progress from a regime of
alternating bands of chaos, bifurcating phase-locking and quasiperiodicity of decreasing
amplitude until it finally phase-locks 1 to 1 with the forcing cycle when the prey are
highly sensitive to selection. Thus it seems that the model is indeed stabilized if the
prey are very sensitive to selection whereas no such effect was noted for the no free
lunch model (Fig. 3a,b) when the predator's sensitivity to selection is increased.


At this point apologies are extended to readers who would argue that eq. (3) is not
a true model of coevolution. At issue is how one defines "evolution" and "coevolution".

Insect Behavioral Ecology '90 Allen




a 12 I I.

0.0 0.2 0.4 0.6 0.8 1.0

Fig. 4. Stabilizing effect of the prey's sensitivity to selection (k) on the no free lunch
model (eq. (3)). Increasing the predator's sensitivity to selection (v) has a tendency to
destabilize the model (Fig. 3a,b). Parameters are the same as Fig. 2).

Evolution might be defined as "change in the genetic makeup of a population with time"
(Keeton & Gould 1986) or perhaps "a change in gene frequency from generation to
generation" (Hickman et al. 1984). Coevolution might be defined as "an evolutionary
change in a trait of the individual in one population in response to a trait of the individ-
uals of a second population, followed by an evolutionary response by the second popula-
tion to the change in the first" (Janzen 1980). Roughgarden (1979) defines coevolution
as "the simultaneous evolution of interacting populations." Schemeke (1983) has
criticized Janzen for overemphasizing interaction and Roughgarden for underemphasiz-
ing it. No attempt will be made here to add another definition to this confusion, and
some confusion over such a complicated subject is probably inevitable and may be a
good thing. The main point is that the model, eq. (3), is not totally excluded by any of
these difinitions if one is willing to accept a phenomenological model which avoids gene-
tic details in favor of a lagged density dependence of parameters. Levin et al. (1990)
seem to lean strongly in favor of such simplifications. Perhaps another worrisome thing
to some readers is the total lack of allowance for mutations or new variants entering
the populations. The model is guilty of this. It tacitly assumes that all of the genetic
variation to accomplish the observed parameter changes is already in place, and that
the changes are simply the result of changes in the frequencies of existing genes by
density-dependent selection pressure.
This finally brings us to the question of whether coevolution tends to prevent chaotic
dynamics in population interactions. It appears in this model (eq. (3)) that things can
go either way: if the prey is more sensitive to selection the model tends to be more
stable, but if the predator is more sensitive it tends to be less stable. This suggests
that coevolution is not a priori a stabilizing force, i.e., that it can go either way depend-
ing on circumstances. One argument which can be applied is the "life-dinner" principle
(Dawkins & Krebs 1979). Since the prey is running for its life and the predator only for
its dinner, the force of selection is thought to be stronger on the prey. In the present

58 Florida Entomologist 74(1) March, 1991

context, this means that X > v which would tend to have a stabilizing influence. There
is a flaw in this argument however in that it says nothing about the densities of the
prey and predator, i.e., at low predator densities the force of selection on the average
prey might be extremely low because predators are rare, while the force of selection
on the predator is relatively constant and may then be greater than that on the prey.
Thus in the present model it is not really valid to apply the life-dinner idea to say that
selection pressure is always greater on the prey since the pressure is time-varying
depending on past density. X and v represent a time-lagged response to selection spread
over several generations and as such say very little about a single encounter. Over a
long time it is just as important to the predator's survival to obtain its dinner as it is
for the prey to escape.
Finally, one additional point needs to be made clear. That is that self-destructive
systems (by definition) do not last long. Thus, wildly chaotic populations that go to
extremely low densities may have a high extinction rate, killing all the members of the
population. Extinction of wildly chaotic systems has nothing to do with biology, genetics
or natural selection in that reproduction is not a necessary part of the process. There
is much evidence that the solar system was once a much more chaotic system than it is
now (Wisdom 1989), but no one would argue that it was stabilized by Darwinian selec-
tion. Nevertheless the same mechanism probably operates on ecological systems,
eliminating chaotic systems which go to extremely low densities, and this process can
be "stabilizing" without involving Darwinian selection (Allen 1990b). It would seem that
there is some danger of confusing the results of this process with the results of ordinary
natural selection and attributing them to natural selection. In view of this and the result
here that coevolution may be indifferent to dynamics, it seems relevant to ask: Is the
occurrence of chaos independent of natural selection except for coincidental effects
which can be either positive or negative?


I would like to thank Bill Schaffer, Dept. of Ecology and Evolutionary Biology,
Univ. of Arizona and Mark Kot, Dept. of Applied Mathematics, Univ. of Washington
for helpful discussion and reviews of the manuscript. This is Florida Agricultural Exper-
iment Station Journal Series No. R-01277.


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Florida Entomologist 74(1)


University of Florida
Institute of Food and Agricultural Sciences
Gulf Coast Research and Education Center
5007 60th Street East
Bradenton, Florida 34203


The naturally derived compounds, abamectin, extract of neem seed (Azadirachta
indica A. Jussieu), pyrethrin formulated with piperonyl butoxide and certain synthetic
organic pyrethroid, carbamate, organophosphorus and chlorinated hydrocarbon insec-
ticides were applied to mixed lifestage and adult populations of Bemisia tabaci (Gen-
nadius) infesting poinsettia (Euphorbia pulcherrima Willdenow). Permethrin alone and
in combination with piperonyl butoxide, fenpropathrin, esfenvalerate, abamectin and
pyrethrin formulated with piperonyl butoxide provided greatest reductions in numbers
of both nymph and adult B. tabaci. Neem seed extract reduced nymphs only and en-
dosulfan and lindane reduced adults only. Lindane was the only insecticide evaluated
that did not reduce the parasitoids, Encarsia sp. and Aleurodiphilus sp., below levels
found on nontreated plants. Phytotoxicity to poinsettia occurred on plants treated with
dimethoate, carbaryl, methamidophos and insecticides containing piperonyl butoxide.


Se aplicaron insecticides de los compuestos naturalmente derivados, abamectin,
extractos de semillas de "neem" (Azadirachta indica A. Jussieu), piretrin formulado
con but6xido piperonil y ciertos sinteticos piretroides organicos, carbamentos, or-
ganofosfatos, hidrocarburos clorinados, a poblaciones de mixtas etapas de desarrollo y
a poblaciones adults de Bemisia tabaci (Gennadius) que infestaban pionsetas (Euphor-
bia pulcherrima Willdenow). Permitrin solo y en combinaci6n con but6xido de piperonil,
fenpropatrin, esfenvalerato, abamectin y piretrin formulado con but6xido de piperonil
caus6 la mayor reducci6n en el numero tanto de ninfas como de adults de B. tabaci.
Extractos de semillas de "neem" redujo solo las ninfas y endosulfan y lindano reducieron
los adults solamente. Lindano fue el unico insecticide evaluado que no redujo el
parasitoide Encarsia esp. o a Aleurodiphilus esp., a niveles mAs bajo que aquellos
encontrados en las plants no tratadas. Fitotoxicidad ocurri6 en plants de poinsetas
tratadas con dimetoate, carbaril, metamidofos y con insecticides conteniendo but6xido
de piperonil.

Sweetpotato whitefly, Bemisia tabaci (Gennadius), is recognized as a major pest of
tropical/subtropical, field-grown crops such as cotton, tobacco, cassava, potato, soybean,
squash and eggplant (Gameel 1972, Lopez-Avila & Cock 1986) and other crops. Damage
from this insect in commercial greenhouse and field-grown ornamentals was first re-
ported on poinsettias (Euphorbia pulcherrima Willdenow) in Florida during 1986 (Ham-
mon & Salguero 1987, Osborne & Price 1987, Price et al. 1987). Since then, sweetpotato
whitefly has extended its range to greenhouses in temperate North America and

March, 1991

Price & Schuster: Sweetpotato Whitefly and Its Parasitoids 61

Europe, apparently through relocations of infested, ornamental, propagative stock
(Anonymous 1987, Collier 1988).
Considerable work has been performed world-wide to evaluate chemicals for sweet-
potato whitefly control on cotton. Sharaf (1986) reviewed chemical control and concluded
that carbamate insecticides and soil applied systemic insecticides have performed best
overall. This species has developed resistance to certain organophosphorus and pyreth-
roid insecticides used in cotton and other crops (Prabhaker et al. 1985). Coudriet et al.
(1985) has shown that 2% aqueous solutions of neem seed extract repelled adults, pro-
longed nymph development and increased nymph mortality of sweetpotato whitefly on
cotton. Fenpropathrin alone and in combination with petroleum oil reduced adult sweet-
potato whiteflies on that crop (Ishaaya et al. 1986).
Information is lacking concerning side effects of insecticides on parasitoids of B.
tabaci. However, considerable information is available concerning effects on the Encar-
sia formosa Gahan parasitoid of the greenhouse whitefly (Trialeurodes vaporariorum
(Westwood)). Harbaugh & Mattson (1976) found that among commonly used greenhouse
insecticides, nicotine sulfate and resmethrin were less toxic to E. formosa than were
endosulfan, malathion and naled. Excellent summaries of effects of pesticides on E.
formosa are provided by Foster (1980) and Ravensberg & Roddenberg-Verschoor
Because insecticides remain an important management tool in ornamentals and likely
will be necessary to permit ornamentals production where sweetpotato whitefly exists,
effective chemicals from various natural and synthetic insecticide groups should be
identified. Sweetpotato whitefly resistance to insecticides also needs to be monitored.
In addition, the effects of pesticides on the parasitoids of the sweetpotato whitefly in
ornamentals should be identified to provide a basis for management schemes that in-
clude biological control. Little is known about the biological and chemical aspects of
sweetpotato whitefly management in ornamental crops.
Experiments were performed to evaluate the naturally derived compounds, abamec-
tin, extract of neem seed (Azadirachta indica A. Jussieu) and pyrethrin formulated
with piperonyl butoxide in addition to certain pyrethroid, carbamate, organophosphorus
and chlorinated hydrocarbon insecticides for management of sweetpotato whitefly on
poinsettia. Since parasitoids may be important for management of sweetpotato whitefly,
studies on the effects of insecticides on sweetpotato whitefly parasitoids were per-


Experiment 1: Effects of Frequent Spraying

Individual rooted cuttings of 'Gutbier V-14 Glory' poinsettias were placed in 15 cm
pots on 5 June 1987. Plants were grown with single stems. Five weeks after setting,
64 plants were placed into a research greenhouse beside a similar number of poinsettias
and tomatoes (Lycopersicon esculentum Miller) having a dense population of sweet-
potato whiteflies (more than 50 adults per leaf) parasitized with Encarsia sp. and
Aleurodiphilus sp. (Hymenoptera:Aphelinidae) parasitoids. Plants were arranged in
four blocks of 15 treatments with each plot consisting of a single plant. Adult insects
were shaken from infested plants to colonize experimental poinsettias evenly. The pre-
viously infested plants remained beside the experimental plants to assure that all plots
were subject to whitefly and parasitoid colonization. Sprays were applied to upper and
lower leaf surfaces at highest concentrations recommended for whitefly control at a
spray volume equivalent to 946 liter/ha. Chemicals used were: carbaryl, oxamyl,
acephate, dimethoate, methamidophos, endosulfan, lindane, esfenvalerate, fenpropath-
rin, permethrin (alone and in combination with piperonyl butoxide), pyrethrin formu-

62 Florida Entomologist 74(1) March, 1991

lated with piperonyl butoxide, abamectin and neem seed extract. These were delivered
with a 7.6 liter, CO2 pressurized sprayer (2.8 kg/cm2) and wand outfitted with an open
cone nozzle (250 core and No. 3 disk). Spraying began two weeks after host plants
initially were infested with whiteflies but before signs of parasitization were evident.
The whitefly population consisted then mostly of adults, eggs and first through third
instars. Treatment applications were made on 21, 24, 28 and 31 July and on 4 and 7
Several evaluations were made to determine the impact of insecticide sprays on
whiteflies and their host plants. Nymphs were considered dead when they lost their
normal yellow-green color, turgidity and smooth cuticle structure. Numbers of live
nymphs (first through early fourth instars) (LN), dead nymphs (DN), live late fourth
instars (pupae) (LP), dead pupae (DP), pupal exuviae with adult whitefly emergence
fissures (EW) and similar exuviae with round parasitoid emergence holes (EP) were
counted on 27 July, 3 and 10 August. The whiteflies which were counted were those
found within the area bounded by the two adjacent main veins at the widest point of
the leaf, the midrib and the outer edge of the leaf blade. Leaves sampled were the first
large leaf that began developing after potting (27 July sample) and the lowest leaf
remaining on the plant (3 and 10 August samples). Percentage nymph mortality was
calculated by 100 (DN/(LN + DN + LP + DP + EW + EP)).
Leaves taken on the two earliest samples were retained individually in 946 ml,
cardboard, ice cream cartons for 3 wk. to allow adult whiteflies and parasitoids to
emerge and die. Adults were counted soon thereafter. Phytotoxicity to leaves (color,
texture and form) was evaluated on 30 July and 4 August (before any sprays were
applied that day).

Experiment 2: Effects of Dried Residues (A)

An experiment was conducted on 5 August to evaluate the effects of dried chemical
residues on adult sweetpotato whiteflies. Four replicates of poinsettia plants, grown as
in the previous experiment but never exposed to whiteflies, were treated with the
insecticide sprays used in Experiment 1. Once residues had dried, a large, middle leaf
was removed from each plant and leaves were placed individually into a water vial
inside a 1.9 liter, clear, plastic container equipped with large screened openings on one
side and top. Twenty-five adult whiteflies were taken from poinsettias in a laboratory
colony and transferred into each container. Containers were placed into a ventilated
insectary maintained at 27 20 C. Numbers of the transferred adults that lived or died
were recorded after 48 h.

Experiment 3: Effects of Dried Residues (B)

A third study evaluated the effects of dried residues of another group of toxicants
on adult whitefly mortality. Three repetitions of an experiment in four replications were
conducted on 15, 22 and 24 July. Chemicals evaluated included bendiocarb and the
chemicals used in the previous experiments excluding oxamyl, dimethoate,
methamidophos, esfenvalerate and neem seed extract. Methods were similar to Exper-
iment 2, except that only 10 adults were introduced into each cage. Data from the three
repetitions were combined for analysis.


Numbers of adult whiteflies and parasitoids reared from leaves were square root
transformed and percentage data were transformed to the arcsine to stabilize error
variance. Data from all experiments were analyzed using analysis of variance. Means

Price & Schuster: Sweetpotato Whitefly and Its Parasitoids 63

maeU Q Ua U

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64 Florida Entomologist 74(1) March, 1991

were separated by Duncan's new multiple range test. Analysis of variance for parasitoid
data is based on the assumption that without the experimental treatments, parasitiza-
tion would have occurred equally among all plots. The general linear model procedure
was used in these analyses (SAS Institute 1985, 113-137). Data are reported in the
original scale.

Experiment 1: Effects of Frequent Spraying

Nymph mortality on nontreated plants was low (Table 1). On 27 July, only permeth-
rin alone and in combination with piperonyl butoxide, abamectin and fenpropathrin
resulted in greater nymph mortality than on the nontreated plants. One week later
plants treated with all treatments except carbaryl and acephate had higher nymph
mortality than nontreated plants. On 10 August, plants treated with permethrin in
combination with piperonyl butoxide and abamectin had the highest levels of nymph
control. A slightly lower level of control was achieved with permethrin alone, fenpropath-
rin, esfenvalerate, pyrethrin formulated with piperonyl butoxide and oxamyl.
Very few round emergence holes, indicative of parasitization, were found among the
pupal exuviae on 3 August (Table 2). One week later, there was evidence of significantly
more parasitoids emerging from the nontreated plants than from plants treated with
any of the chemical insecticides. Chemical insecticides can reduce parasitoids by
eliminating hosts in addition to direct chemical effects. Therefore, the ratio of emerged
parasitoids on a particular date to the sum of emerged parasitoids and whiteflies, ex-
pressed as percent, more clearly represents the direct effects of chemical insecticides
on parasitoid populations. Data indicate that all insecticides, except lindane, signifi-
cantly reduced parasitoid activity below that of the nontreated checks. Representative
specimens of parasitoids collected from this experiment were identified as Encarsia sp.
and Aleurodiphilus sp. (Aphelinidae: Hymenoptera) and are held in the Florida Collec-
tion of Arthropods, Gainesville.
Numbers of pupal exuviae that possessed the emergence fissures indicative of non-
parasitized whiteflies (Table 2), provided good evaluation on 3 and 10 August of the
effectiveness of chemical insecticides at reducing whitefly numbers. Insecticides with
the greatest properties for reducing whitefly population development on both dates
were permethrin alone and in combination with piperonyl butoxide, fenpropathrin, es-
fenvalerate, pyrethrin formulated with piperonyl butoxide, oxamyl, abamectin and
neem seed extract (3 August evaluation only).
Similar information was gained by rearing to the adult stage immature whiteflies
and parasitoids present on treated leaves (Table 3). On 27 July, whitefly populations
were reduced best by permethrin in combination with piperonyl butoxide followed by
six other treatments: permethrin alone, esfenvalerate, pyrethrin formulated with
piperonyl butoxide, methamidophos, abamectin and neem seed extract. On 3 August,
results were similar except that methamidophos did not perform as well as it had earlier
and endosulfan and fenpropathrin were more effective on the later sampling date. On
27 July, all insecticides suppressed parasitoid populations compared with the nontreated
check; on the next sample date, all insecticides except lindane suppressed parasitoid
Phytotoxicity unacceptable on poinsettia plants was present 24 h after the first
application of permethrin in combination with piperonyl butoxide (bronze discoloration
on abaxial leaf surface), pyrethrin with piperonyl butoxide (bronze discoloration on
abaxial leaf surface) and dimethoate (brown spotting on adaxial leaf surface). After five
applications, phytotoxic symptoms were more evident and additional unacceptable
phytotoxicity was present on plants treated with carbaryl (distorted new growth) and
methamidophos (necrosis on leaf margins).

Price & Schuster: Sweetpotato Whitefly and Its Parasitoids 65

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Florida Entomologist 74(1)

March, 1991

O O 0 o

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Price & Schuster: Sweetpotato Whitefly and Its Parasitoids 67

Experiment 2: Effects of Dried Residues (A)

Adult whitefly mortality on plants with insecticide residues on 5 August are pre-
sented in Table 3. There was no adult mortality attributable to carbaryl, dimethoate or
neem seed extract, although mortality resulted from all other insecticides. The greatest
adult mortality from residues occurred on plants treated with permethrin in combination
with piperonyl butoxide, fenpropathrin, esfenvalerate, pyrethrin formulated with
piperonyl butoxide, endosulfan and lindane.

Experiment 3: Effects of Dried Residues (B)

All chemicals tested reduced numbers of adults below levels in the nontreated checks
(Table 4). The lowest mortality of adults occurred on plants treated with carbaryl,
bendiocarb and acephate; greatest mortality occurred on plants treated with fenpropath-
rin, pyrethrin formulated with piperonyl butoxide, endosulfan and lindane. An inter-
mediate level of adult mortality occurred on plants treated with abamectin, permethrin
alone and permethrin in combination with piperonyl butoxide. It is unknown why 14%
fewer adults than in the earlier experiment died from exposure to residues of permeth-
rin in combination with piperonyl butoxide.


These data indicate that the naturally derived compounds, abamectin, extract of
neem seed and pyrethrin formulated with piperonyl butoxide and certain pyrethroid,
chlorinated hydrocarbon and carbamate compounds can be useful to manage selected
stages of B. tabaci. However, pyrethrin formulated with piperonyl butoxide may not
be useful on poinsettias since phytotoxicity occurred in this study. The wide range of
effective chemicals, if permitted and properly used, may delay selection toward a sweet-


Concnb % Mortality + SEM

Nontreated 9.3 6.4 E
Bendiocarb 76W 120.0 43.0 14.2 CD
Carbaryl 50W 120.0 28.1 9.9 D
Acephate 75S 60.0 52.2 21.1 C
Endosulfan 50W 60.0 99.1 1.6A
Lindane 25W 30.0 100.0 0.0 A
Fenpropathrin 2.4EC 24.0 100.0 0.0 A
Permethrin 2EC 24.0 84.9 4.1B
Permethrin 2EC + 24.0
Piperonyl butoxide 8EC 240.0 81.9 + 5.9 B
Pyrethrins (6%) + 0.6
Piperonyl butoxide (60%) 6.0 100.0 0.0 A
Abamectin 0.15EC 1.2 75.8 7.3 B

"Values within a column followed by the same letter are not significantly different (P
= 0.05; Duncan's (1955) multiple range test).
bGrams of active ingredient per 100 liters of preparation.

68 Florida Entomologist 74(1) March, 1991

potato whitefly strain resistant to insecticides. Among all insecticides evaluated only
the chlorinated hydrocarbon, lindane (effective against adult B. tabaci), would be useful
in a management program that conserves the indigenous parasitoids, Encarsia sp. and
Aleurodiphilus sp.


The authors are grateful for Aphelinidae identifications provided by M. Rose and L.
Stange and for the technical support provided by Ken Kiger, Curt Nagle, Sue Trammel,
Emily Vasquez and Preston Young. Partial funding for this research was provided by
The Fred C. Gloeckner Foundation. Poinsettia plants were donated by Paul Ecke Poin-
settias, Encinitas, CA. This manuscript was approved for publication as Florida Agricul-
tural Experiment Station Journal Series No. 9774.


ANONYMOUS. 1987. Sweetpotato whitefly. Geiger News. 22(4): 1.
COLLIER, R. 1988. Regional news Southern region. Antenna. 12(2): 72-3.
whitefly (Homoptera: Aleyrodidae): Effects of neem-seed extract on oviposition
and immature stages. Environ. Entomol. 14(6): 776-9.
FOSTER, G. N. 1980. Control of tomato pests. The West of Scotland Agric. College
Tech. Note No. 80. 4pp.
GAMEEL, 0. I. 1972. A new description, distribution and hosts of the cotton whitefly
Bemisi tabaci (Gennadius) (Homoptera Aleyrodidae). Rev. Zool. Bot. Africa. 86
(1-2): 50-64.
HAMMON, A. B., AND V. SALGUERO. 1987. Bemisia tabaci, sweetpotato whitefly in
Florida. Florida Dept. Agric. Div. Plant Industry Entomol. Circ. 292. 2pp.
HARBAUGH, B. K., AND R. H. MATTSON. 1976. Insecticide effects on Encarsia
formosa Gahan, parasite of the greenhouse whitefly, Trialeurodes vaporariorum
(Westwood). J. Am. Soc. Hort. Sci. 101(3): 228-33.
ISHAAYA, I., M. AUSTERWEIL, AND H. FRANKEL. 1986. Effect of the petroleum
oil Virol on toxicity and chemical residue of fenpropathrin applied against adults
of Bemisi tabaci (Homoptera:Aleyrodidae) as high- and low-volume sprays. J.
Econ. Entomol. 79(3): 596-9.
LOPEZ-AVILA, A., AND M. J. W. COCK. 1986. Economic damage, pp. 51-4 in M. J.
W. Cock [ed.], Bemisia tabaci a literature survey on the cotton whitefly with
an annotated bibliography. C. A. B. Int. Inst. of Biol. Control. 121 pp.
OSBORNE, L. S., AND J. F. PRICE. 1987. Five pests that really bug you: The
whitefly. GrowerTalks 51(2): 34-9.
PRABHAKER, N., D. L. COUDRIET, AND D. E. MEYERDIRK. 1985. Insecticide re-
sistance in the sweetpotato whitefly, Bemisia tabaci (Homoptera: Aleyrodidae).
J. Econ. Entomol. 78(4): 748-52.
PRICE, J. F., D. J. SCHUSTER, AND D. E. SHORT. 1987. Recent advances in manag-
ing the sweetpotato whitefly on poinsettia. Florida Ornamental Growers' Assoc.
Newsletter 10 (5): 1-5.
pesticides on natural enemies. Koppert B. V. Tech. Bull. 1. 22 pp.
SHARAF, N. 1986. Chemical control of Bemisia tabaci. Agric., Ecosystems and En-
vironment 17: 111-27.
SAS INSTITUTE, INC. 1985. SAS Users Guide: Statistics, Version 5 Edition. SAS
Institute, Cary, N.C. 956 pp.

Marenco et al.: Residual Activity of Insecticides 69


University of Florida
Institute of Food and Agricultural Sciences
Everglades Research and Education Center
P.O. Box 8003
Belle Glade, FL 33430


The residual activities of methomyl and thiodicarb were evaluated based on the
control of fall armyworm larvae at various post-application intervals in laboratory bioas-
says with leaves of field treated sweet corn. Mortality of second and fifth instar larvae
were not significantly different for either of the two insecticides. Foliage fed to larvae
three h after application (day 0) resulted in 50-60% mortality for methomyl and >95%
mortality for thiodicarb. Mortality resulting from methomyl residues ranged from 5-50%
and 1-15% at 1 and 2 d post-application, respectively. Larvae exposed to thiodicarb
treated foliage suffered >90% mortality for the first 4-5 d and 70-80% on day 9.
Thiodicarb residues induced about 50% mortality of fifth instar larvae on day 14.

Se evaluaron las actividades residuales de metomil y tiodiocarbo basado en el control
del gusano cogollero a various intervalos despu@s de aplicados en bioensayos en el
laboratorio con hojas de maiz dulce tratadas en el campo. La mortalidad del segundo y
tercer estadio larval no fue significativamente diferente para ninguno de los dos insec-
ticidas. Follaje dado a comer a larvas despues de tres horas de la aplicaci6n (dia 0),
result en una mortalidad de 50-60% para metomil y >95% para tiodicarbo. El resultado
de mortalidad con residues de metomil oscil6 entire 5-50% y 1-15% de 1 y 2 dias Irespec-
tivamente despues de la aplicacion. Residuos de tiodicarbo inducieron como un 50% de
mortalidad en larvas en el quinto estadio en el dia 14.

The fall armyworm (FAW), Spodopterafrugiperda (J. E. Smith), is the primary pest
attacking sweet corn grown in the Everglades agricultural area of southern Florida
(Foster 1989). USDA standards (USDA 1954) require sweet corn receiving the grade
of "U. S. Fancy" have less than 10% of the ears injured by smut, decay, worms, insects,
rust, discoloration, birds, or other means. Foster (1989) reported that most growers
consider 2% to be the maximal amount of FAW and corn earworm damage that they
can tolerate. Taylor and Wilkowske (1984) reported that over 21% of the total production
costs for sweet corn was spent on pesticides during the 1982-83 growing season.
Methomyl and thiodicarb are both recommended for FAW control in sweet corn
(Johnson 1988). Hofmaster (1980) reported that both of these insecticides provided
greater than 90% control of FAW on sweet corn. Pitre (1986) found that methomyl gave
effective control on sorghum seed heads, but suggested that the level of susceptibility
in Florida appeared to be declining. Methomyl is a insecticide-nematicide killing mainly

'Current address: Standard Fruit Company, Research Department, La Ceiba, Honduras.
2Department of Entomology, Purdue University, W. Lafayette, IN 47907.

70 Florida Entomologist 74(1) March, 1991

by contact with complementary stomach poison activity (Thomson 1989). Methomyl
provides fast knockdown when insects contact the insecticide. Ware (1975) reported
that methomyl is highly soluble in water and Sheets et al. (1982) reported that residues
of methomyl on coastal bermudagrass declined rapidly after application and at 7 d
post-application, about 7% of the initial deposit remained.
Foster (1985) reported thiodicarb as the most effective labeled insecticide in southern
Florida for the control of FAW in sweet corn. Thiodicarb acts mainly as an ingestion
or stomach toxicant with some complementary contact activity (Thomson 1989, Anony-
mous 1988). Thiodicarb is relatively insoluble in water and organic solvents and does
not readily penetrate the surfaces of insect cuticle or leaves. This results in little contact
toxicity to insects and little or no translaminar activity in plants. Because of the low
vapor pressure of thiodicarb, little or no fumigant action has been noted (Anonymous
1988). Meister (1985) listed thiodicarb as having foliar residual activity up to 14 d or
longer depending on rainfall, crop, and environmental conditions. The insecticidal prop-
erties of thiodicarb are not adversely affected by high temperature or light (Anonymous
The objective of this study was to evaluate the residual activity of methomyl and
thiodicarb in sweet corn based on the control of FAW larvae at various post-application
intervals as determined from laboratory bioassays. Methomyl was chosen because it is
the most commonly used insecticide by sweet corn growers in southern Florida and
thiodicarb because of its reported effectiveness (Foster 1985). These data will help us
to develop proper strategies for using these two insecticides for controlling FAW on
sweet corn in southern Florida.


The experiment was conducted in 1988 and 1989 at the Everglades Research and
Education Center near Belle Glade, Florida. In 1988, a strip of sweet corn (c.v. 'Florida
Staysweet') 120 m long and four rows wide (0.91 m between rows) was planted on 31
August. In 1989, a strip 160 m long and eight rows wide was planted on 14 February.
For each study the area was divided into three sections, two of which were treated with
either methomyl at a rate of 507 g (AI) per ha or thiodicarb at a rate of 844 g (AI) per
ha. The third area was used as an unsprayed control. In the 1988 study, pesticide
treatments were applied on 20 September to V8 stage sweet corn (Herman 1986) with
a CO2 powered backpack sprayer. A delivery rate of 321 liters per ha of insecticide
solution was used to assure adequate coverage and penetration (Pitre 1986, Young
1979). In the 1989 study, the pesticide treatments were applied on 27 March to V8 stage
sweet corn with a high clearance sprayer delivering 403 liters per ha of insecticide
solution. There was no rain during either experiment. Corn leaves that were exposed
at the time of application were marked at the base with a permanent marker to identify
the leaf surfaces that had received an insecticide treatment.
Leaf sections (25 cm2) were taken daily from fully emerged leaves on 40 randomly
selected plants for each treatment for 7 d in 1988 and 14 d in 1989. Eight leaf sections
were placed in a sterilized, disposable, plastic petri dish (100 by 15 mm) along with five
FAW larvae. The FAW larvae used in the study were the F2 progeny from a laboratory
culture that was initiated from larvae that were field collected from sweet corn near
Belle Glade 6 wk prior to each study. The larvae were maintained at 27 1 C, 78
5% RH, L:D 15:9 photoperiod. The FAW larvae used in 1989 were reared on sweet
corn foliage and the ones used in 1989 were reared on commercial diet (Bioserv Inc.,
General Purpose diet #9000). Larval instars were determined by length, based on the
method presented by Cherenguino & Menendez (1975). Fifth instar larvae were used
in 1988 and second and fifth instars were used in 1989. A 15 by 15 cm cheesecloth section
was placed over the foliage before the petri dish was closed to ensure a tight fit. The

Marenco et al.: Residual Activity of Insecticides 71

cheesecloth prevented the escape of small larvae, but allowed air exchange and absorbed
excess himidity. The experiments were arranged in completely randomized designs
with five replications. The experimental unit consisted of three petri dishes containing
a total of 15 larvae, for a total of 75 larvae per treatment.
Mortality counts were made 24, 48, and 72 h after the larvae were placed on the leaf
sections. Larvae that did not move within 30 s after being prodded were considered
dead. Percentage kill was corrected for each 24 h period with Abbott's formula (Abbott
1925). Data were analyzed by analysis of variance and least significant difference (P <
0.05) mean separation (SAS Institute 1982).


Percentage mortality of larvae exposed to methomyl treated foliage was not signif-
icantly greater 48 or 72 h after exposure than at 24 h (P < 0.05). In contrast, larvae
exposed to thiodicarb treated foliage had a significant increase in mortality when the
exposure time was increased from 24 to 48 h, but not from 48 to 72 h. Therefore,
mortality percentages from 48 h after exposure were used for analysis.
In the 1988 study, fifth instar larvae fed foliage one d after application (day 1) had
>95% mortality for thiodicarb and almost 50% for methomyl (Fig. 1). Mortality resulting
from methomyl residues dropped rapidly to 15% by day 2 and near zero by day 3. In
contrast, thiodicarb resulted in >95% mortality up to 7 d after application.
Mortality rates for second versus fifth instar larvae were similar for the two insec-
ticides studied in 1989 (Figs. 2 and 3). Foliage fed to second instar larvae 3 h after
application (day 0) resulted in nearly 60% mortality for methomyl and almost 100%
mortality for thiodicarb (Fig. 2). Mortality resulting from methomyl residues dropped
to 5% by day 1 and near zero by day 2. Second instar larvae exposed to thiodicard
treated foliage suffered >90% mortality for the first 5 d (except day 4) and >70% on
day 9. Second instar larvae were not tested beyond 9 d post-treatment because sufficient
larvae were not available.



t 60
o Methomyl
m [ Thiodicarb



1 2 3 5 7
Days Post-Treatment
Fig. 1. Mortality of fifth instar larvae after 48-h exposure to corn foliage treated
with methomyl or thiodicarb 1 to 7 d prior to exposure (1988 study). Mortality corrected
for control mortality using Abbott's formula. Treatment means are significantly differ-
ent for each date (LSD, P < 0.05).

72 Florida Entomologist 74(1) March, 1991





0 1 2 3 4 5 7 9
Days Post-Treatment

Fig. 2. Mortality of second instar larvae after 48-h exposure to corn foliage treated
with methomyl or thiodicarb 1 to 9 d prior to exposure (1989 study). Mortality corrected
for control mortality using Abbott's formula. Treatment means are significantly differ-
ent for each date (LSD, P < 0.05).

Foliage fed to fifth instar larvae 3 h after application resulted in >50% mortality for
methomyl (Fig. 3). The mortality resulting from methomyl residues dropped to 20% by
day 1 and 10% by day 2. Treatment with thiodicarb resulted in mortality of >90% for
the first 4 d post-treatment. Mortality remained >80% through day 9 and on day 14
mortality was about 50%.
The selection of the proper spray interval depends on a number of factors, including
the effectiveness and residual activity of the insecticide used, the crop phenology, the
rate of growth of the crop, the population dynamics of the pest, the weather, and, of
course, economics and required pre-harvest intervals. Methomyl, primarily a contact

w Methomyl
80- Thiodicarb

14 60*


0 20

0 1 2 3 4 5 7 9 11 14
Days Post-Treatment

Fig. 3. Mortality of fifth instar larvae after 48-h exposure to corn foliage treated
with methomyl or thiodicarb 1 to 14 d prior to exposure (1989 study). Mortality cor-
rected for control mortality using Abbott's formula. Treatment means are significantly
different for each date (LSD, P < 0.05).

Marenco et al.: Residual Activity of Insecticides 73

insecticide, provides little residual control of FAW on sweet corn. The selection of a
proper spray interval would depend largely on FAW densities. Because of the lack of
residual activity, at higher densities, frequent applications of methomyl would be neces-
sary to attempt to kill those larvae that had survived previous applications and those
that had hatched since the last application. These applications may need to be applied
as often as every 2-4 d to control newly hatching larvae before they migrate to protected
areas of the plant where they are difficult to reach with insecticide sprays. In contrast,
thiodicarb, primarily an ingestion toxicant, provides a high level of residual activity for
9 d and some control at 14 d after application. Therefore, the duration of the spray
interval for thiodicarb would depend on the rate of plant growth and rainfall as well as
the level of FAW infestation. If there were no rainfall, plant parts that received a
thiodicarb application could be assumed to be safe from FAW attack for about nine d,
although newly exposed leaf surfaces would be vulnerable to FAW feeding. In sum-
mary, based on laboratory bioassays, methomyl provided little residual control of FAW
on sweet corn, and thiodicarb provided nine d or more of acceptable control under
southern Florida conditions.


We thank Rhone-Poulenc Ag, Company and E. I. DuPont de Nemours and Co. (Inc.)
for supplying materials for this study. Florida Agricultural Experiment Station Journal
Series No. R-00466.


ABBOTT, W.S. 1925. A method for computing the effectiveness of an insecticide. J.
Econ. Entomol. 16: 265-267.
ANONYMOUS. 1988 Larvin. Rhone Poulenc Ag. Company. 50 pp.
CHERENGUINO, R. S., AND A. L. MENENDEZ. 1975. Biology and habits of the
whorlworm, Spodoptera frugiperda, in El Salvador. Program cooperative cen-
troamericano para el mejoramiento de cultivos alimenticios. (PCCMCA) 21: 251-
FOSTER, R. E. 1985. Control of lepidopterous pests of sweet corn in the Everglades.
Proc. Florida State Hort. Soc. 98: 266-268.
FOSTER, R. E. 1989. Strategies for protecting sweet corn ears from damage by fall
armyworm (Lepidoptera: Noctuidae) in southern Florida. Florida Entomol. 72:
HERMAN, J. C. 1986. How a corn plant develops; special report No. 48. Iowa State
University of Science and Technology Coop. Ext. Serv. Ames, Iowa. 21 pp.
HOFMASTER, R. N. 1980. The fall armyworm. The Veg. Growers News 34(12): 2-3.
JOHNSON, F. 1988. Insect control guide; vegetable crops. Florida Coop. Ext. Serv.
Bull. IX Y1-16. University of Florida, Gainesville, Florida.
MEISTER, R. T. 1985. Farm chemicals handbook '85. Meister Publ. Co. 441 pp.
PITRE, H. N. 1986. Chemical control of the fall armyworm (Lepidoptera: Noctuidae):
An update. Florida Entomol. 69: 570-578.
SAS INSTITUTE. 1982. SAS user's guide: Statistics. SAS Institute, Cary, N.C.
SHEETS, T. J., W. V. CAMPBELL, AND R. B. LEIDY. 1982. Fall armyworm control
and residues on methomyl on coastal bermudagrass. J. Agric. Food Chem. 30:
TAYLOR, T. G., AND G. H. WILKOWSKE. 1984. Costs and returns from vegetable
crops in Florida, season 1982-83 with comparisons. Univ. Florida Agric. Expt.
Sta. Info. Rpt. 199 pp.
THOMSON, W. T. 1989. Agricultural chemicals: book I insecticides. Thomson Publica-

Florida Entomologist 74(1)

USDA. 1954. United States standards for grades of green corn. USDA Pub. 19 FR
WARE, G. W. 1975. Pesticides, an auto-tutorial approach. W. H. Freeman and Com-
pany, San Francisco.
YOUNG, J. R. 1979. Fall armyworm: control with insecticides. Florida Entomol. 62:


National Center for Physical Acoustics
University of Mississippi
University, MS 38677

Dept. of Biology
University of Mississippi
University, MS 38677


To infer mating preferences of female Neonemobius sp., we monitored their proxim-
ity to males paired in laboratory enclosures. Females were found significantly more
often near the larger of the males, and more often near a calling male than a silent one.
The proportion of time individual males were observed calling was significantly corre-
lated with male size. Females did not prefer virgin to mated males. When allowed to
mate, females mated with the larger of the pair 5 of 7 times. Female preference for
large males may result from selection on females to obtain larger investments from
males. Female nemobiine crickets feed on glandular secretions provided by males during
mating. Large males may offer more material, and females may use male calling songs
as a cue to male size.


Para inferir la preferencia copulatoria de hembras de Neonemboius sp., chequeamos
su proximidad a machos apareados en jaulas en el laboratorio. Las hembras se encontra-
ron significativamente mas a menudo cerca de los machos mAs grande, y mas cerca del
macho que llamaba que del silencioso. La proporci6n del tiempo que se observe a los
machos llamando estudo significativamente correlacionado con el tamafo del macho. Las
hembras no prefirieron a machos virgenes sobre sobre aquellos que habian copulado.
Cuando se les permiti6 copular, las hembras copularon con el mAs grande de la pareja
en 5 de 7 veces. La preferencia de las hembras por machos grandes pudiera ser por la
selecci6n de hembras para obtener mayores inversiones de los machos. Grillos hembras
de nemobiine se alimentan de segregaciones glandulares proveidas por machos durante
la copulaci6n. Los machos mAs grande pudieran ofrecer mAs material, y las hembras
pudieran usar los cantos llamativos como una pista del tamanio del macho.

March, 1991

Forrest et al.: Mate Choice in Ground Crickets

Mating in many insects involves nuptial feeding by the female (Thornhill 1976, Thor-
nhill & Alcock 1983). In crickets nuptial feeding may take many forms. Although not
generally considered nuptial feeding, female crickets usually eat the spermatophores
produced by their mate, and in some species this may be a considerable number (17 in
a single mating, Orocharis luteolira, T. G. Forrest personal observation). In Gryllodes
supplicans, a proteinaceous spermatophylax accompanies the spermatophore and is
eaten by the female (Sakaluk 1984). In some species, females feed on glandular secre-
tions produced by the male (eg. Oecanthus spp., Walker & Gurney 1967), or on male
body parts (eg. Hapithus agitator, Alexander & Otte 1967). Courtship feeding may
function to delay spermatophore removal before the sperm have emptied from the
ampulla into the female's spermatheca (Sakaluk 1984). Materials eaten by females may
be incorporated into eggs and increase female fecundity (Gwynne 1984). Sakaluk &
Cade (1980, 1983) showed that female Gryllus integer and Acheta domesticus that mated
repeatedly produced more offspring than those allowed only a single mating.
Mate choice in field crickets (Gryllinae) has received much attention because males
usually offer little more than sperm to mates. Thus, this system offers a means to
examine female choice of males that differ in their genetic, rather than material, contri-
bution to offspring. Gryllus females have been shown to prefer larger males (G.
bimaculatus, Simmons 1988) and older males (G. veletis and G. pennsylvanicus, Zuk
1987). Differences in the calling song of male crickets are used by females in making
the discrimination (Crankshaw 1979, Hedrick 1986, Simmons 1988, Zuk 1987).
During copulation, female ground crickets (Nemobiinae) feed on the proximal tibial
spur of the male's hind leg and eat the glandular material that exudes from the wound
(Mays 1971). If investment by males increases the fitness of females, selection should
act on female behavior to increase the investment they obtain from males. For instance,
if male size is a direct indicator of the amount of his investment, females should mate
preferentially with larger males (Gwynne 1982, Bailey et al. 1990).
We used a paired choice experiment to examine female choice of males differing in
size. We also examined whether a male's mating history (virgin or non-virgin) or his
propensity to call influenced the female's decision.


Crickets used in the experiment were the F1 progeny of Neonemobius sp. females
(N= 3-8) collected 18 May 1989 at Roosevelt State Park, Scott Co., Mississippi. Off-
spring were reared in plastic enclosures containing 3-5 cm sand. Ground dog chow was
provided ad libitum. The sexes were separated prior to adulthood and held 4-8 per
enclosure. Voucher specimens have been deposited in the University of Mississippi
Entomology Museum. Tape recordings of males are kept by T. G. Forrest.
Paired choice experiments were carried out in the laboratory using plastic enclosures
(13 x 28 x 12 cm). The bottom of each enclosure was covered with moist sand 2.5 4.0
cm deep, and the enclosure was partitioned into three sections using screen wire. The
middle section was further subdivided into three equal areas using cardboard partitions
(A, B, and C; Fig. 1).
Prior to the experiment, we estimated male sizes by measuring their mass to the
nearest 0.1 mg using a Sartor model AR1014 balance. Eighteen males were ranked
relative to mass. Males were paired to keep the same realtive size difference between
the larger and the smaller of the pairs. Large males were paired with medium, and
medium-sized males paired with smaller males (see paired symbols, Fig. 2).
Males from each pair were randomly assigned to the outer sections of an enclosure
(male A and B; Fig. 1). A virgin female was placed in the central section of the enclosure.
The screen wire partitions allowed the female to see the males and hear their calling

Florida Entomologist 74(1)



Male A Female Male B


Fig. 1. Enclosure used in paired choice experiments. Males of different sizes were
randomly assigned to an end section (Male A, Male B). Screen partitions allowed females
in the central section to hear and see males. Cardboard partitions divided the female's
section into three equal areas and prevented her from seeing both males at the same
time. Female position (area A, B or C) and whether males were calling were scored
during each observation.

songs. However, the cardboard partitions kept the female from viewing more than one
male at a time. A 2.5 cm strip of plastic tape placed along the sides and top edge of the
screen partitions prevented crickets from climbing over the screen partitions. We pro-
vided ground dog chow for each cricket in small plastic dishes. The female's food was
located in the center of the enclosure. There were nine replicates.
Each day we made three observations separated by two or more hours (between
0730-0930, 1130-1330 and 1530-1730 hours). During each observation we noted the loca-
tion of the female with respect to the three areas in her section (near male A, male B
or Center; Fig. 1). We also noted whether the males were calling. Because males often
stopped stridulating when the enclosure was approached, a male was considered calling
if his wings were raised in the characteristic 'calling position.
During the first week, both males in the enclosure were virgin with intact tibial
spurs. After the first observation on the sixth day of the experiment all partitions were
removed. The following day (about 30 hours), the males were removed, weighed and
checked to see if mating had occurred (i.e. tibial spurs were damaged). The experiment
was repeated for a second week using the same males (one dead male was replaced)
and new, virgin females. The difference in mass between paired males ranged from
1.6-6.1 (beginning of first week) and from 0.6-9.3 mg (beginning of second week).
Statistical comparisons were made using Wilcoxon's signed rank test for paired
observations (Sokal & Rohlf 1981). In comparisons involving female choice, the number
of observations of a female positioned near small (or virgin) males was compared to the
number near large (or mated) males. For male calling, the comparisons were between
the number of times small and large paired males were observed calling. Simple product-
moment correlation between male mass at the beginning of the experiment (size) and
the proportion of observations (square root transformed) males were found calling was

March, 1991

Forrest et al.: Mate Choice in Ground Crickets







Mass (mg)

Fig. 2. Relationship between mass of individual males at the beginning of the exper-
iment (week I) and the proportion of observations (n=29-31) each was found calling.
Each point represents data from one individual. Data points with the same symbol show
data from males paired during the experiment. Correlation between mass and propor-
tion of observations calling (square root transformed) is significant (r=0.53, p<0.05).

calculated (Sokal & Rohlf 1981). During both weeks in one enclosure, one male of the
pair died; data on female choice after the death of the males and calling data for males
in this replicate were not used in any of the analyses. Female choice data from another
replicate during the second week were discarded because the female was a last instar


We made 247 observations of female positions during the two week period. In paired
choice comparisons, the 17 females were significantly more likely to be found near the
large male (N= 17, T, = 19.5, P<0.005; week I: N=9, T= 6, p<0.03; week II: N=8,
T = 9, NS). When only one of the two males was calling and the females were closer to
one of them, they were found near the calling male more often (59 of 71 observations).
When both males were calling and the female was near one of them, she was more likely
to be next to the large male (15 of 20 observations).
At the end of the first week, four females mated with large males, one mated with
a small male, one mated with both males. During the entire experiment, when females
mated with only one male of the pair, the larger male was chosen 5 of 7 times. There
was no significant difference between female proximity to virgin or non-virgin males
during the second week of the experiment N = 5, T, = 6, NS).
During the two week period, large males were observed calling significantly more
often than the smaller males paired with them (N= 8, T,= 4, p<0.03). There was a

_ I I I I

v v



- ______

78 Florida Entomologist 74(1) March, 1991

significant correlation between male size and the proportion of observations males called
(r=0.53, p<0.05, Fig. 2).


Male size and calling influenced the positions of females in our experiment. Females
can apparently judge male size without contact and may use the calling song as the cue.
We did not measure the sound output of the males in the experiment. However, calling
song intensity has been shown to be directly related to male size in a number of orthopte-
ran species (Scapteriscus acletus and S. vicinus, Forrest 1983; Anurogryllus arboreus,
Walker 1983a; Mygalopsis marki, Bailey and Thiele 1983, Gryllus bimaculatus, Sim-
mons 1988), and females often respond preferentially to louder songs (Gryllus integer,
Cade 1979; Scapteriscus acletus and S. vicinus, Forrest 1983, Forrest & Green 1991;
Conocephalus upoluensis and Requena verticalis, Bailey 1985).
In our study females also mated with large males more often than smaller males (5
of 7). Whether this preference occurs in natural populations of ground crickets has not
been examined. In nature, about 80 percent of the males have their tibial spurs damaged
(i.e. are mated, Mays 1971). Five males collected from Roosevelt St. Park late in the
season (15 Oct 1989) ranged in weight from 21.3 36.6 mg. Only one of them did not
have both spurs chewed; it was the smallest male. Whether the differences in male
mating success can be attributed to female choice or passive attraction depends on
whether females use a decision rule in choosing mates (Parker 1982, 1983). If females
prefer males that call over males that remain silent, as suggested by our data, then
differences are due to female choice.
What benefit female ground crickets gain from mating with larger males is unknown.
Larger males might provide a larger nuptial offering. In katydids, a male's sper-
matophylax may be 2-20 percent of his body weight (Gwynne 1983). Female Con-
ocephalus nigropleurum always mate with a larger male when given a choice, presum-
ably to obtain a larger investment from the male (Gwynne 1982). Gwynne (1988) has
also shown that nutrients from the spermatophylax are incorporated into eggs fertilized
by the investing male, and that the investment may increase the number and size of
the eggs produced (Gwynne 1984).
Interestingly, the juvenile female's data that were discarded from the analysis were
similar to those of adults. She was found near the larger male on 13 of 15 observations,
but did not (or was not allowed to) mate with either of the males. Fulton (1915) observed
an immature female feeding on the metanotal gland of an adult male Oecanthus. Imma-
ture nemobiine females may respond to adult males and attempt to obtain nuptial food
without mating. Bell (1980) found Oecanthus females often engaged in such opportunis-
tic feeding, consuming the glandular secretions of males while they interacted with
recent mates.
Nuptial feeding may also prevent females from removing the spermatophore before
the sperm have emptied (Sakaluk 1984). In another nemobiine, Allonemobiusfasciatus,
females terminate copulation earlier if the male's tibial spurs are covered and she is
unable to feed on the glandular material (Bidochka & Snedden 1985). However, the
duration of spermatophore attachment did not differ between females that were allowed
to feed on the spur and those that were not (Bidochka & Snedden 1985).
Time and duration of calling by male crickets are often variable (Walker 1983b), and
have been shown to have an underlying genetic component (Cade 1981, Hedrick 1988).
We observed large male ground crickets calling significantly more often than small
males paired with them, and there was a significant correlation between male size and
the proportion of time observed calling (Fig. 2). Calling behavior may be conditionally
dependent on size or the presence of other males. Large males might have more energy

Forrest et al.: Mate Choice in Ground Crickets 79

to invest in sound production and call to advertise their 'vigor' (Burk 1989, Ryan 1989).
Small males may call less often when caged with another male, because in nature this
would encourage aggressive interaction from other, larger males (Burk 1983). One pos-
sible reason for the low correlation between a male's mass and amount of calling (Fig.
2) is that medium-sized crickets may call differently when competing with smaller males
compared to when paired with males of similar or larger size. Small males may be
predisposed to become silent, satellite males (Cade 1979).


We wish to thank Dr. Gary Miller for providing many of the materials for the
experiment and for his comments on the manuscript. Two anonymous reviewers offered
several suggestions that much improved the paper. The Department of Biology, Univer-
sity of Mississippi provided financial support. T. G. Forrest is supported by USDA
grant #88-38203-3906 to the National Center for Physical Acoustics.


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Stiling et al.: Nymphal Parasites of Salt-Marsh Planthoppers 81


Department of Biological Science
Florida State University
Tallahassee, FL 32306-2043


Elenchus koebelei (Strepsiptera) and Pseudogonatopus arizonicus (Dryinidae) are
recorded as parasitoids of nymphs and adults of Prokelisia marginata and P. dolus in
north Florida salt marshes. Prokelisia spp. are new host records for P. arizonicus.
Parasitized hosts can be found year round. Average monthly levels of parasitism vary
between 0 and 1% for Pseudogonatopus and between 0 and 20% for Elenchus. Both
superparasitism and multiparasitism of Prokelisia hosts was noted. The maximum
number of recorded parasites per host was four for Elenchus and two for
Pseudogonatopus. Only two of 88,354 hosts were found to contain both parasites at the
same time. Dryinid larvae may be hyperparasitized, but the hyperparasite responsible
could not be reared out.


Se registra a Elenchus koebelei (Estresiptera) y a Pseudogonatopus arizonicus
(Drinida) como parasitoides de ninfas y de adults de Prokelisia marginata y de P.
dolus en saladares pantanosos del norte de la Florida. Prokelisia spp. es un registro
nuevo como hospedero para P. arizonicus. Hospederos parasitados se pueden encontrar
todo el afio. El promendio mensual de parasitismo varia entire 0 y 1% Pseudogonatopus
y entire 0 y 20% para Elenchus. Se not6 el superparasitismo y multiparasitismo de
hospederos de Prokelsia. El registro mayor de parasitismo por hospedero fue de cuatro
en Elenchus y dos en Pseudogonatopus. Solo dos de 88,354 hospederos se encontraron
que contenian ambos parAsitos al mismo tiempo. Larvas de drinidas pudieran ser hiper-
parasitadas, pero el hiperparAsito responsible no se pudo criar.

Prokelisia marginata (Van Duzee) is a common inhabitant of salt-marsh cord grass
Spartina alterniflora Lois on both the Gulf and Atlantic coasts of Florida (Denno et al.
1980, 1985, 1986; Stiling & Strong 1982). Nymphs and adults are attacked by two types
of parasitoids, a strepsipteran, Elenchus koebelei Pierce, and a dryinid (Stiling & Strong
1982). We had previously reared out and identified the strepsipteran, but we had been
unable to rear out dryinids from Prokelisia until 1989. The current paper identifies the
dryinid as Pseudogonatopus arizonicus Perkins. We had previously thought that
parasitism by either parasitoid was very infrequent in Florida, never exceeding 5%
(Stiling & Strong 1982). More widespread samples in 1988 and 1989 have revealed that

'Present address: Department of Biology, University of South Florida, Tampa, FL 33620-5150

Florida Entomologist 74(1)

average levels of parasitism by strepsipterans may approach 20% but that parasitism
from dryinids never exceeds 1%. The present paper details these results and provides
information on the biology of both parasites.
It is also worth noting that what long had been known as Prokelisia marginata was
split into two species, P. marginata and P. dolus (Wilson), in 1982 (Wilson 1982). Denno
et al. (1987) have noted the presence of P. dolus and P. marginata in Florida and
Atlantic marshes, and we have recently recorded both species in our north Florida
study sites (unpublished). There are no major differences in life history between the
two Prokelisia species, and the most striking ecological difference is that P. dolus is
found in backmarsh situations, away from the seashore, whereas P. marginata occurs
more toward the shore and less in the backmarsh (Denno et al. 1987). This paper also
compares rates of parasitism between P. dolus and P. marginata nymphs and adults.


We took 200 sweep samples from Spartina alterniflora in Wakulla County, Florida,
at eight different sites every month from June 1988 through May 1989, for a total of
19,200 sweep samples. Each series of 200 sweeps was emptied into a bag, returned to
the laboratory, and sorted for parasitized and unparasitized nymphs and adults of Pro-
kelisia. Estimates of parasitism levels throughout the year were based on combined
samples of nymphs and adults from all sites each month. Sample size was at least 1500
Prokelisia each month and usually many more. Statistical comparisons of parasitism
levels in P. dolus and P. marginata and in male planthoppers and female planthoppers
were made by means of Wilcoxon's distribution-free rank sum test (Hollander & Wolfe
1973). In addition, we reared out adult dryinids from Prokelisia for identification pur-
poses, and we present some information on the biology of these parasitoids together
with some new information on the strepsipterans. Nymphal or adult Prokelisia exhibit-
ing dryinid sacs (defined in results section) were caged on Spartina leaves in the labo-
ratory at room temperature, 25 20C, 72 2% RH. When dryinid larval development
was complete, the dryinid larva exited the host, killing it. The exiting dryinid larva
usually spun a cocoon on the cork stopper of the clip cage. No cocoons were spun on


We found no evidence that either Elenchus or Pseudogonatopus prefers either
species of host. We examined males of 7,637 P. dolus and 16,044 P. marginata and
found parasitism rates of 8.24% and 8.33%, respectively, for Elenchus (W* = 0.015, P
= 0.492) and 0.026% and 0.031% for Pseudogonatopus (W* = 0.001, P < 0.50). We
believe neither P. arizonicus nor E. koebelei discriminates between the two species of
planthopper, so for the purposes of this study we have pooled data from the two hosts.

Elenchus koebelei

The adult male is free living, but the abdomen of the neotenic, parasitic female
remains embedded in the host's hemocoel; only its cephalothorax protrudes to the ex-
terior. Males mate with females while the latter are still inside their hosts. Female
Strepsiptera are viviparous; eggs fill the body cavity, where they develop into minute,
mobile, triungulid larvae. The larvae hatch within the female's body and reach the
exterior through a brood canal. In the case of Prokelisia hosts, the larvae locate host
nymphs and adults and bore into the body cavity. Once inside hosts, triungulids undergo
hypermetamorphosis, molting into grublike, legless larvae that show sexual differenti-

March, 1991

Stiling et al.: Nymphal Parasites of Salt-Marsh Planthoppers 83

ation after the second molt. Extruded male puparia are dark and most commonly appear
from between host abdominal segments 7 and 8. In Elenchus females, the pupal stage
is suppressed, and the adult becomes sexually mature after extrusion of the
cephalothorax through the host's cuticle. The extrusion of the female cephalothorax is
evidenced only by two small holes and is much less obvious (for examples in other host
planthoppers, see diagrams by Hassan 1939, Kathirithamby 1982). Our earlier samples
in 1980 and 1981 scored only male strepsipterans, and we believe this was a major
reason for our low recorded rates of parasitism. Extrusion of female larvae only occurs
when the host is adult, but the cephalothorax of the male is extruded from fifth- and,
less commonly, fourth-instar nymphs (Table 1). Such strepsipteran extrusion patterns,
in which the female parasite appears only in adult hosts, are apparently a general
phenomenon in most homopterans (Hassan 1939, Williams 1957). In our study, the sex
ratio of Elenchus was about 1:1 (2,936 males, 2,978 females). Hassan (1939) also found
an even sex ratio in the strepsipterans parasitizing delphacids in England.
We recorded 173 cases of superparasitism (Table 2). The maximum number of para-
sites we found in a nymph was three and in an adult four (two males and two females).
Where superparasitism occurs, the parasites may be extruded either on the same side
of the host's abdomen or on different sides. Greathead (1970) reported that when two
parasites were present they are "almost invariably" extruded on opposite sides of the
host. We found just the opposite pattern (Table 3). Of a total of 54 cases in which two
parasites were extruded, either in nymphs or in adults, in 47 of those cases, the para-
sites were extruded on the same side. We have insufficient data to say what really
happens at even higher levels of superparasitism, but Greathead (1970) reports that
any pattern is lost and extrusion occurs wherever there is space.
Parasitism levels of Prokelisia spp. by Elenchus varied considerably in the course
of the year, from less than 4% to over 18% (Fig. 1), although this temporal variation
showed no clear pattern. Some evidence of spatial variation was apparent; values be-
tween 2% and 40% were recorded at different sites at the same times (Stiling et al.
unpublished data).

Pseudogonatopus arizonicus

Our rearing of Pseudogonatopus arizonicus from Prokelisia is a new host record
for this species. Both the adult male and the adult female of Pseudogonatopus are free
living, but only the male is winged. Females are wingless and ant-like in appearance.
In addition to being parasites, female P. arizonicus can be voracious predators. We
observed newly emerged females to attack and eat two Prokelisia nymphs within 10
minutes. Nymphs were lifted completely into the air and supported by the front legs
and ovipositor of the dryinid.
Immature dryinid larvae are extruded in a sac from between the abdominal segments
of the host. The sac, composed of cast larval skins, usually appears between segments
5 and 6. Most of the dryinid sacs observed were seen on nymphs. Of 163 sacs observed


Sex of host

Sex of strepsipteran Male Female Nymph

male 446 593 1897
female 1581 1397 0

Florida Entomologist 74(1)

EXAMINED = 88,354.

No of parasites n

In adult Prokelisia

1 male
2 males
3 males
1 female
2 females
3 females
1 male and 1 female
1 male and 2 females
2 males and 2 females

In nymphal Prokelisia

1 male
2 males
3 males



in the present study, 118 were visible on nymphs, 38 on adult female Prokelisia, and
only 7 on male Prokelisia. Only once did an individual host support more than one
dryinid sac; that host was a nymph collected in November 1989, and the two sacs
protruded from opposite sides of the host's abdomen.
From dryinid cocoons, we reared out 6 adult dryinids, 1 male and 5 females. The
average length of time spent in the pupal stage was 21.17 days, S.D. = 1.17. We found
one dryinid larva to be hyperparasitized by three endophagous larvae, but we were not
successful in rearing them out.
Percent parasitism of Prokelisia by P. arizonicus was extremely low and varied
between 0% in August and September 1988 and 0.71% in June 1988. The highest
parasitism recorded at any one site was only 3.49%.


Number and sex of strepsipterans
Position in 1 female
host abdomen 2 females 2 males and 1 male 3 males 3 females

In adult Prokelisia

One same side 11 10 2 0 0
On different sides 3 2 1 1 1

In nymphal Prokelisia

On same side -- 24 -- 1 --
On different sides 1 -- 0 --

March, 1991

Stiling et al.: Nymphal Parasites of Salt-Marsh Planthoppers 85





2 12-

I 10-

5 8-



0-- -0 -
0- -" *'---*- 4---- -- - ----__----

A M J J' A'S 0 N D J'F' M A 'M
1988 1989

Fig. 1. Seasonal trends in parasitism rates of Prokelisia spp. by Elenchus koebelei
(Strepsiptera) (solid line) and Pseudogonaptopus arizonicus (Dryinidae) (dashed line)
on north Florida salt marshes.


Pseudogonatopus arizonicus (Dryinidae) and Elenchus koebelei (Strepsiptera) are
both parasites of nymphal and adult Prokelisia in north Florida salt marshes. This
paper reports the first record of Pseudogonatopus arizonicus from Prokelisia spp.,
there being no record of Prokelisia as a host in Olmi's extensive revision of the
Dryinidae (Olmi 1984). Denno (1983) swept Haplogonatopus americanus from New
Jersey marshes and assumed that this was the species likely to be attacking P. mar-
ginata (Denno pers. comm.). Interestingly, Denno (1977) had earlier swept dryinids in
the genus Pseudogonatopus from Spartina patens in New Jersey. Both E. koebelei and
P. arizonicus can be found in hosts year round, though it is unclear how many genera-
tions the parasites pass through per year. Only 2 individuals out of 88,354 hosts
examined contained both a dryinid sac and a strepsipteran larva-many fewer than
would be expected by chance from our observations of 163 hosts with dryinids and 6235
with strepsipterans (X2 = 7.52, df = 1, p < 0.01)-so the parasites do not attack the
same hosts or cannot survive in the same hosts. Multiparasitism of homopteran hosts
by strepsipterans and dryinids is generally not common. After extensive collections of
grassland homopterans in Britain over many years, Waloff (1990) recorded only one
such case. However, Raatikainen (1987) recorded 207 multiparasitized individuals in
15,878 Javasella pellucida taken between 1958 and 1964, which is a multiparasitism
rate of 1.3%.
Superparasitism was recorded in both parasitoid species, but was more commonly
noted in E. koebelei; a maximum of four strepsipterans were found in one host. The

86 Florida Entomologist 74(1) March, 1991

maximum number of strepsipteran pupae found in other Homoptera varies from three
in Ulopa reticulata adults in Britain (Waloff 1981) to five in Dicranotropis muiri on
Mauritius (Williams 1957) and even seven in Poophilus costalis in Uganda (Greathead
1970). Indeed, Greathead (1970) argues that the number of parasites per host is limited
only by space, and he documents a correlation between host size and degree of
parasitism. In this respect, because females are larger than males in most planthopper
and leafhopper species, they may exhibit a higher degree of superparasitism (Greathead
1970) and suffer a higher overall amount of parasitism. In Prokelisia spp., however,
we found that male and female hosts were parasitized to about the same extent (males,
8.30%, n = 23,681; females, 7.97%, n = 24,795; W* = 0.13; P < 0.45). Williams (1957)
reported no effect of host sex on the number of extruded parasites in D. muiri and
argued that, though the abdomen of the male was smaller than that of the female, the
integument allows considerable distention in both sexes.
Levels of parasitism by dryinids are extremely low and probably inconsequential to
the population dynamics of the host. Dryinids may, however, affect host populations
more by direct predation; females of other dryinid species have been thought to eat
over 100 hosts in their lifetimes (see references given by Waloff & Jervis 1987). Levels
of parasitism by E. koebelei, the strepsipteran, are much higher, varying, on average,
between 0 and 20%. At some sites, parasitism levels may approach 40% in some months
(Stiling et al. unpublished data), and E. koebelei may have a substantial impact on
Prokelisia densities. These results contrast with results from New Jersey marshes,
where there are three generations of Prokelisia per year (Denno 1983). In the first
generation of nymphs in New Jersey, levels of parasitism by strepsipterans and dryinids
combined may be as high as 80% (Denno 1983), but parasitism levels in the second and
third generations are less than 5%. Our results suggest that parasitism of Prokelisia
nymphs and adults may have a more consistent but less dramatic effect in Florida
marshes than in those of New Jersey.


Jim Cronin provided the parasitized Prokelisia hosts from which we were able to
rear out dryinid parasites. Dr. A. S. Menke, Systematic Entomology Laboratory, Ag-
ricultural Research Service, U.S. Department of Agriculture, identified the dryinid as
Pseudogonatopus arizonicus. Financial support provided by N.S.F. grants BSR
8703416 to Donald Strong and BSR 9007429 to Donald Strong and Peter Stiling.


DENNO R. F. 1977. Comparison of the assemblages of sap-feeding insects (Homop-
tera-Hemiptera) inhabiting two structurally different salt marsh grasses in the
genus Spartina. Environ. Entomol. 6: 359-372.
Migration in heterogeneous environments: differences in habitat selection be-
tween the wing-forms of the dimorphic planthopper, Prokelisia marginata
(Homoptera: Delphacidae). Ecology 61: 859-867.
DENNO, R. F. 1983. Tracking variable host plants in space and time, pp. 291-341 in
R. F. Denno and M. S. McClure (eds.), Variable plants and herbivores in natural
and managed systems. Academic Press, New York.
DENNO, R. F., L. W. DOUGLAS, AND D. JACOBS. 1985. Crowding and host plant
nutrition: environmental determinants of wing-form in Prokelisia marginata.
Ecology 66: 1588-1596.
DENNO, R. F., L. W. DOUGLAS, ANDD. JACOBS. 1986. Effects of crowding and host
plant nutrition on the development and body size of the wing-dimorphic planthop-
per, Prokelisia marginata. Ecology 67: 116-123.

Stiling et al.: Nymphal Parasites of Salt-Marsh Planthoppers 87

Practical diagnosis and natural history of two sibling saltmarsh-inhabiting plan-
thoppers (Homoptera: Delphacidae). Proc. Entomol. Soc. Washington 89: 687-
GREATHEAD, D. J. 1970. A study of the host relations of Halictophagus pontifex
Fox (Strepsiptera), a parasite of Cercopidae (Hem., Aphrophorinae), in Uganda.
Bull. Entomol. Res. 60: 33-42.
HASSAN, A. I. 1939. The biology of some British Delphacidae (Homopt.) and their
parasites with special reference to the Strepsiptera. Trans. R. Entomol. Soc.
London 89: 345-384.
HOLLANDER, M., AND D. A. WOLFE. 1973. Nonparametric statistical methods.
John Wiley & Sons, New York.
KATHIRITHAMBY, J. 1982. Elenchus sp. (Strepsiptera: Elenchidae), a parasitoid of
Nilaparvata lugens (StAl) (Homoptera: Delphacidae) in peninsular Malaysia, pp.
349-361 in Proceedings of the international conference on plant protection in the
tropics, March 1982, Kuala Lumpur, Malaysia.
OLMI, M. 1984. A revision of the Dryinidae (Hymenoptera). Mem. American En-
tomol. Inst. 37(1): 1-946, 37(2): 947-1913.
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pellucida (F.) (Hom. Dephacidae). Annales Agricultura Fennici Supplement 6:
STILING, P. D., AND D. R. STRONG. 1982. The parasitoids of the planthopper Pro-
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Entomol. 6: 103-113.
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lphacidae (Homoptera: Auchenorrhyncha). The Entomologist 109: 47-52.
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88 Florida Entomologist 74(1) March, 1991


Department of Biological Science
Florida State University
Tallahassee, FL 32306-2043


We fertilized four separate areas of salt-marsh cord grass, Spartina alterniflora, in
northwest Florida to examine the effect of increased foliar nitrogen on herbivorous
insects. Two of the experimental plots were located where Spartina grew as a shoreline
fringe; two others were pure isolated offshore islets of Spartina. Application of fertilizer
in winter and early spring resulted in significant increases in foliar nitrogen through
the following August at all sites. The two most common and damaging herbivores
throughout the growing season were the planthopper Prokelisia marginata (Homopt-
era: Delphacidae) and the grasshopper Orchelimum fidicinium (Orthoptera: Tet-
Populations of planthoppers on islets responded positively to Spartina fertilization.
The increase in Prokelisia densities disappeared in August shortly after nitrogen levels
of fertilized islets dropped to approximate those of controls. In the fall, planthopper
populations on islets increased dramatically, despite low nitrogen levels. On mainland
patches, Prokelisia densities did not always increase on fertilized patches, and there
were no large population outbreaks of Prokelisia in the fall. Densities of grasshoppers
increased on mainland fertilized patches, whereas on offshore islets grasshoppers were
rarely observed. These observations are consistent with the idea that grasshoppers can
depress Prokelisia populations. Cage experiments confirmed that grasshoppers can
reduce the numbers of Prokelisia. Simulation of grasshopper feeding by clipping of the
tops of Spartina plants also reduced Prokelisia densities. On offshore islets, because
grasshoppers were very rare, they did not have a sufficient effect to depress Prokelisia


Nosotros abonamos cuatro Areas separadas de saladares pantanosos de la hierba
Spartina alterniflora en el noroeste de la Florida para examiner los efectos del aumento
de nitr6geno en el follaje en insecto herbivoros. Dos de las parcelas experimentales
estaban situadas donde Spartina crecia como margen costero; las otras dos eran dos
islitas puramente aisladas de Spartina. La aplicaci6n de abono en el invierno y al prin-
cipio de la primavera result en significantes aumento de nitr6geno foliar hasta e in-
cluyendo a Agosto en todos los lugares. Los dos mAs importantes y comunes herbivoros
durante la temporada de crecimiento fueron el saltahojas Prokelisia marginata
(Hom6ptera: Delfacida) y el saltamonte Orchelimunfidicinium (Ort6ptera: Tetig6nide).
Poblaciones de saltahojas en las islitas respondieron positivamente al abono de Spar-
tina. El aumento en la densidad de Prokelisia desapareci6 en Agosto poco despu6s que
los niveles de nitr6geno en las islitas abonadas bajaron aproximadamente igual al del
testigo. En el otofio, poblaciones de saltahojas en las islitas aumentaron dramAticamente
a pesar de niveles bajos de nitr6geno. En tierra firme, habia Areas donde la densidad
de Prokelisia no siempre aument6 en las Areas abonadas, y no hubieron brotes de
poblaci6n de Prokelisia en el otofio. La densidad de los saltamontes aument6 en las

'Present address: Department of Biology, University of South Florida, Tampa, FL 33620-5150.

Stiling et al.: Effects of Fertilization on Salt-Marsh Insects 89

areas abonadas en tierra firme, mientras que en las islitas raramente se veian. Estas
observaciones son consistentes con la idea que los saltamontes pueden deprimir pob-
laciones de Prokelisia. Experimentos con jaulas confirmaron que los saltahojas pueden
reducir el nimero de Prokelisia. Se simul6 el dafio que los saltamontes hacen cuando
comen, cortando la parte de arriba de las plants de Spartina, lo que tambien redujo la
densidad de Prokelisia. Puesto que los saltamontes eran muy raro en las islitas, no
tuvieron un efecto suficiente para disminuir la densidad de Prokelisia.

Literature reviews on the effects of fertilization have produced conflicting conclu-
sions. After reviewing 18 laboratory and field nutrition-interaction studies, Onuf (1978)
concluded that a general correlation could be found between the susceptibility of plants
to insect attack and nitrogen levels. On the other hand, Stark (1964), in a review of 15
tree-insect interactions involving nitrogen fertilizers, showed that insect survival was
reduced. Strauss (1987) has documented how fertilization can have a variety of effects
on insect communities. In her experiments, fertilization increased the numbers of
phloem-feeding insects on Artemisia in Minnesota. Patrolling by ants also increased,
and increased ant activity prevented chewing insects from increasing; in fact chewers
decreased significantly on fertilized plots. Hargrove et al. (1984) also showed how it
may be possible to get conflicting results of fertilization within a single study system.
Fertilized black locust trees initially incurred higher losses to chewing insects. In time,
however, they began to gain protection from herbivory and to exhibit lower densities
of insects than controls. The protection arose from a tolerance response, in which
greater photosynthetic area was produced, and a resistance response, in which insect
preference shifted to foliage of nonfertilized trees. Hargrove et al. suggested that con-
flicting reports in the literature about the effect of fertilization may be due in part to
the length of observation period following the experiment.
For Spartina alterniflora, Vince et al. (1981) reported increased herbivore diversity
following Spartina fertilization along the coast of Massachusetts. They reasoned that
species diversity increased because several of the dominant phytophagous species did
not respond to increasing dietary nitrogen, whereas many rarer species benefited from
nutritional changes. The reason was not that dominant species do not respond to nitro-
gen per se but that they were held in check by natural enemies, especially spiders. In
northwest Florida, Silvanima & Strong (1991) found some effect of fertilization on den-
sities of Prokelisia in the spring but not over the rest of the year. Here we reexamine
the effects of fertilization on planthoppers and grasshoppers on Spartina alterniflora
stands in northwest Florida and show how these two herbivores interact.
Spartina plants are of a uniform height in gulf coast habitats (Denno & Grissell 1979,
pers. obs.) and do not exhibit the height polymorphism that is apparent on Atlantic
coasts, where "tall" forms grow along streamsides and "short" forms on the rest of the
marsh (Denno & Grissell 1979). In Florida, pure stands of S. alterniflora grow both in
shoreline fringes and on small islets formed at the highest point of oyster bars and
mudflats. Such islets make excellent study sites because of their homogeneity and iso-
lation. At our study sites, mature flowering spikes of Spartina die back annually in
early winter. Although some sprouting occurs throughout the growing season, the
majority of plants begin to rejuvenate in March and thus grow as a cohort.
Prokelisia marginata Van Duzee (Homoptera: Delphacidae) is the numerically do-
minant herbivore in most Spartina salt marshes (Smalley 1959, Denno 1977). Recently,
the closely related P. dolus has also been shown to live on Spartina marshes (Denno
et al. 1989), but it generally occurs in high back-marsh situations and is only rarely
present on the isolated offshore islets or seaside fringes used here (pers. obs.). Pro-
kelisia marginata was common in all our study areas from March through December
and overwintered primarily as eggs. Eggs are laid in the basal portion of the leaf, where

90 Florida Entomologist 74(1) March, 1991

the adults and older nymphs feed. Young nymphs, however, often migrate to the leaf
tips, which are commonly curled longitudinally and may provide shelter as well as food.
Prokelisia is multivoltine; more than 10 generations pass in a year (Strong 1989). Much
evidence exists to suggest that Auchenorrhyncha often select hosts, especially host
grasses, on the basis of leaf nitrogen levels (Prestidge & McNeill 1983).
The grasshopper Orchelimum fidicinium Rehn and Hebard (Orthoptera: Tet-
tigoniidae) is the most damaging herbivore in the marsh and often chews on over 80%
of the available Spartina leaves in north Florida salt marshes. It is univoltine (Smalley
1960); nymphs first appear in April, and adults die in early October, when overwintering
eggs are laid. These grasshoppers feed by scraping and chewing the adaxial leaf sur-
faces, and the resultant damage, which is readily apparent as bare white patches on
tattered leaves, remains through October. Feeding occurs primarily on the upper half
of the leaf, which may severely affect the suitability of this area for young Prokelisia
nymphs. Grasshoppers are only commonly found on mainland Spartina; they are rare
on offshore islets, and grasshopper damage there is negligible.


Eight study areas near St. Marks Wildlife Refuge, Wakulla County, northwest
Florida, each measuring 2 m x 2 m, were selected as study areas and named as follows:
islets 5 and 6, Deans west and Deans east, Old Creek fertilized and unfertilized, and
Brent's patch fertilized and unfertilized. We applied fertilizer to islet 6, Deans west,
Old Creek fertilized, and Brent's patch fertilized by drilling 36 10-cm-deep holes spaced
40 cm apart and adding equal amounts of fertilizer. The total application rate was 1512
kg ha-1, applied as 70% ammoniacal and 30% nitrate in three equal amounts on February
16, March 6, and April 7, 1981. The other areas were left unmanipulated as controls.
Our intent was to increase plant nitrogen levels on experimental patches for a short
time, to determine whether Prokelisia densities increased, to allow nitrogen levels to
return to normal, and to observe whether Prokelisia densities showed a corresponding
decrease. In other words, we wanted to see whether Prokelisia densities closely tracked
plant nitrogen levels in the field. Sample leaves of five plants were collected from each
experimental and control plot for nitrogen analysis on each of four different dates
through the year, freeze dried, homogenized, and run in duplicate on a Carlo-Erba CHN
elemental analyzer.
Censusing for Prokelisia or Orchelimum was done biweekly from May to November.
On each plot, plants were examined visually for both nymphal and adult Prokelisia. We
assessed populations of the more mobile Orchelimum by passing a long pole through
the grass and counting the number of jumping grasshoppers. On mainland patches,
where grasshoppers were common, we obtained a measure of grasshopper herbivory
by counting the number of leaves chewed by Orchelimum. No other grasshopper regu-
larly chews Spartina leaves in our study area, and Orchelimum damage is unique and
very distinct, resulting in tattered and shredded leaves. We also erected two cages
containing different grasshopper densities. One cage (termed "high-density") contained
the highest observed "natural" densities of grasshoppers, retaining all the nymphs that
had emerged from overwintering eggs. An identical cage (termed "low-density") con-
tained very low densities of grasshoppers, which had barely resisted our attempts at
total grasshopper removal by hand. Cages consisted of 2-mm mesh screening supported
on a galvanized frame sunk deep into the substrate. Finally, we attempted to simulate
the mechanical damage caused by grasshoppers on some plants by clipping the top 15
cm of all leaves in a 3 x 3 m area of an offshore islet. The treatment was performed on
September 16 at a time when the Prokelisia population consisted entirely of eggs.
Because planthopper eggs are laid near leaf bases, this treatment did not directly re-

Stiling et al.: Effects of Fertilization on Salt-Marsh Insects 91

move individuals from the population. Prokelisia censuses were conducted on clipped
plots and nearby control plots for one generation.


Fertilization resulted in treatment patches with higher nitrogen concentrations than
control patches from spring through early August (P < 0.01, t-test) (Fig. 1). After
August nitrogen concentrations on fertilized patches fell to approximate those of con-
trols. Our differences in nitrogen levels between fertilized and control plots in spring
are similar to those documented by Vince et al. (1981), and control values are in general
accord with other reported values for Spartina (Mendelssohn 1979, Hopkinson &
Schubauer 1984).
On islets, Prokelisia densities were consistently higher on fertilized than on control
islets through August (Kolmogorov-Smirnov, P < 0.05) (Fig. 2). Following the con-
vergence of nitrogen levels between treatment and control patches, densities of P.
marginata on fertilized islets fell to control levels. By October, control densities greatly
exceeded those on treatment plots. This effect was probably not related to nitrogen
levels, because the largest increases in Prokelisia densities occurred on control plots,
which had never been fertilized. The highest number of grasshoppers found on an islet
was one on a control and three for a fertilized islet, these being totals for an entire
season. Grasshopper damage was negligible.
On the mainland plots, grasshopper numbers and numbers of leaves damaged by
grasshoppers were consistently and obviously higher on fertilized plots than on controls,
and both types of mainland plots had much higher grasshopper herbivory than islets.
One fertilized plot (Brent's Patch) showed little difference in Prokelisia density relative


Fig. 1. Mean % total foliar nitrogen from the four fertilized Spartina patches (solid
symbols) and the four control plots (open symbols), with standard deviations.

M 'A M J J A S O

Florida Entomologist 74(1)






Fig. 2. Total numbers (nymphs and adults) of Prokelisia marginata on fertilized
offshore islets (solid symbols) and control offshore islets (open symbols), (a) Deans west
and Deans east, (b) islets 5 and 6.

to the control (Kolmogorov-Smirnov, P > 0.05); the other treatment area, at Old Creek,
showed an increase in Prokelisia numbers on fertilized plots over control plots during
the spring (Kolmogorov-Smirnov, P < 0.05) (Fig. 3). Both areas showed their strong
spring pulse of Prokelisia from April to June, before grasshopper damage was heaviest.
The site where Prokelisia densities remained unchanged from controls in spring,
Brent's Patch, had relatively high grasshopper damage at that time; the site where
Prokelisia densities increased, Old Creek, had low grasshopper damage in May and
June. After grasshopper damage became heavy in late June, Prokelisia numbers re-
mained low for the rest of the season on all plots. There was no big autumn peak of
Prokelisia at these sites, as there was on the islets.
Inside the low-density grasshopper cage, the density of P. marginata nymphs and
adults showed an obvious increase, 6-fold over densities inside the "high"-density grass-
hopper cage (Fig. 4). Prokelisia could not escape from cages because the mesh was fine
enough to retain them all, and counts from the cages cannot be compared directly to
uncaged areas because of this drastic influence on migration (Strong & Stiling 1983).
Simulation of grasshopper feeding, by clipping of plants, also reduced Prokelisia densi-
ties over the course of one generation (Fig. 5). Clipping did not significantly decrease
nymphal hatch, but it did increase mortality of young nymphs. Although clipping may
slightly reduce leaf area, up to 100 nymphs can successfully develop on one leaf, so at
these Prokelisia densities, leaf-area reduction per se is not likely to have caused a great

March, 1991

Stiling et al.: Effects of Fertilization on Salt-Marsh Insects 93

500- 25o ao e.o
.00 t |
C) 0
S400- O 0 -
0 0 A 0 i j A S O

35 30 a IS

1 00- a

ot 0 5- H A 0/
0 E


Zn 750 C

rr 1

Fig. 3. (a)-(b) Total numbers (nymphs and adults) of Prokelisia marginata on fer-
tilized mainland patches (solid symbols) and control patches (open symbols). (a) Brent's
patch, (b) Old Creek. (c)-(d) Numbers of Orchelimum grasshoppers on fertilized main-
land patches (solid symbols) and control patches (open symbols). (c) Brent's patch, (d)
Old Creek. (e)-(f) Grasshopper herbivory on fertilized (solid symbols) and control (open
symbols) plots. (e) Brent's patch, (f) Old Creek.

deal of nymphal mortality. Furthermore, although the mechanical action of clipping may
not well simulate the chemical changes and general shredding inflected by grasshoppers,
the effects of clipping on Prokelisia densities are similar to the effects of grasshoppers.


We had originally replicated our fertilization experiment four times and expected to
compare the numbers of Prokelisia and Orchelimum on four fertilized plots to those
from four control plots. In actuality, our four fertilized areas gave different results
depending upon the numbers of grasshoppers present. This is an interesting result and
underscores the difficulty of creating true replicates in nature. In spring, Prokelisia
marginata responded positively to fertilization treatments on Spartina islets where
grasshoppers were absent. Its population densities tracked nitrogen concentrations
until the summer. Density differences between treatment and control plots disappeared
shortly after nitrogen concentrations in fertilized plots dropped to approximate those
of controls, and indeed the trend reversed on some islets after this date. Whether or
not fertilized plants had developed some kind of resistance to insect attack by this time
(either because of heavy Prokelisia feeding or because of heavy grasshopper damage),
as suggested by Hargrove et al. (1984), remains open to speculation.
Fig 3(a-bToanubr(nmhanadlsofPkEtii agn nfr

as suggested by Hargrove et al. (1984),- remains open to speculation.

Florida Entomologist 74(1)







A M J J' A' S O N D


Fig. 4. Prokelisia and Orchelimum densities inside low density grasshopper cages
(solid symbols) and high density grasshopper cages (open symbols).

March, 1991

Stiling et al.: Effects of Fertilization on Salt-Marsh Insects 95



a. 4-


2- Not clipped

S- clipped

Fig. 5. Prokelisia densities on clipped and unclipped Spartina patches over the
course of one generation. Bars indicate least significant intervals. Clipped patches had
the top 15 cm of leaf removed on September 16.

Prokelisia populations can obviously be influenced by the nutritional status of the
host plant. However, on islets, even when nitrogen levels are at their lowest, in the
fall, Prokelisia populations reach their highest numbers, indicating that host-plant qual-
ity is not always of prime importance in influencing herbivore numbers. Although using
nitrogen levels as a measure of nutritional status may be simplistic, especially for
phloem feeders such as Prokelisia, foliar nitrogen has proved to be a good indicator of
plant quality for other delphacids (Mochida et al. 1977) and for Prokelisia (Vince et al.
1981, Silvanima & Strong 1991). Host plant nitrogen is well correlated with soluble
nitrogen (Prestidge 1982) and soluble nitrogen has been widely used as an indicator of
plant quality for Prokelisia (Denno 1985, Denno et al. 1985). Interestingly Denno et al.
(1985) also noted an increase in Prokelisia density in the fall despite a drop in soluble
protein levels in salt marshes in Maryland and despite the fact that in paired choice
tests Prokelisia showed a feeding and oviposition preference for more nutritious plants
(Denno 1985).
On our islet sites, the effects of grasshoppers were minimal. On mainland patches
of Spartina, where grasshoppers were common, herbivory by grasshoppers increased
so dramatically on fertilized plants that Prokelisia densities did not increase. Moreover,
grasshopper damage was so severe that it prevented the large population pulses of
Prokelisia in the fall on both control and fertilized plots. High densities of grasshoppers
inside cages depressed Prokelisia populations. This appears to be a clear case of asym-
metrical interspecific competition by resource exploitation. That is, one of the com-
petitors, the grasshopper, has a much greater effect on the other competitor, Pro-
kelisia, than vice versa. Such amensalism is common in nature (Lawton & Hassell 1981).
We observed most grasshoppers to feed preferentially near leaf tips. Other salt-
marsh grasshoppers species such as 0. concinnum and Conocephalus hygrophilus are
known to feed preferentially near the apices of Juncus roemerianus leaves because this

Florida Entomologist 74(1)

region is nutritionally superior to other areas of the leaf (Parsons & de la Cruz 1980).
In Rhode Island marshes Conocephalus grasshoppers can damage a large fraction of
Spartina alterniflora; the average damage per spike is 59% (Bertness et al. 1987), and
all spikes exhibit some damage. Although most Prokelisia eggs, adults, and older
nymphs are found near the leaf base, young nymphs are commonly found near the leaf
apex (Stiling & Strong 1982). They may be sheltering, in the often curled tips, from
predators or abiotic factors such as heavy rain or high tides. Damage to the leaf tips
by grasshoppers increases nymphal mortality probably by depriving young nymphs of
such refuges, rather than by removing so much material that hoppers starve to death.
Some of our results are in agreement with observations of Prokelisia during other
Spartina fertilization experiments. Recently Silvanima & Strong (1991) demonstrated
limited increases of Prokelisia on fertilized shoreline Spartina where no grasshoppers
occurred. Prokelisia densities increased in the spring but not over the rest of the year,
though the numbers of Prokelisia at their study site were an order of magnitude below
those recorded at any of our sites. Vince et al. (1981) showed no response by P. mar-
ginata to increasing dietary nitrogen under field conditions in Massachusetts, despite
a recorded preference for high-nitrogen plants in the laboratory. These authors also
noted a strong preference by grasshoppers in their marsh for fertilized plots, but the
species, Conocephalus, was different, and the overall densities of grasshoppers at their
sites were an order of magnitude lower than those in our Florida marshes. Also, Con-
ocephalus grasshoppers feed primarily on flower spikes rather than on leaves, so gras-
shoppers probably do not compete so severely with Prokelisia in North Atlantic
marshes. Instead, Vince et al. (1981) hypothesized that increased predation by spiders
reduced Prokelisia population sizes on their fertilized plots. It is valuable to note that
similar results, i.e. no increase in Prokelisia densities in salt marshes, of fertilization
in two different areas may result from different mechanisms.
Why grasshoppers occur more commonly on the mainland than on offshore islets is
not clear but may be related to the presence of more refuges from high tides on the
mainland (Vince et al. 1981), where higher vegetation such as Juncus roemerianus is
present. We released 50 grasshoppers on each of seven islets on July 1, 1981, and within
a week only 1 or 2 could be found. Two subsequent introductions of 500 grasshoppers
on each of two other islands fared little better; densities were at control levels of 1 or
2 within a month. Also, Juncus itself is heavily damaged by grasshoppers and may be
a valuable alternative host for Orchelimum.


Avis James and Jacqui Stiling assisted greatly with the field work. Jim Cronin, Tony
Rossi, Jay Silvanima, Sharon Strauss, and Ann Throckmorton offered comments on the
manuscript. This research was supported by National Science Foundation grants DEB
791828, DEB 8206856, and BSR 8703416 to D. R. Strong and by the Department of
Biological Science, Florida State University. Present address for B.V.B. is Agricultural
Research Center, Route 4, Box 63, Monticello, FL 32344.


BERTNESS, M. D., C. WISE, AND A. M. ELLISON. 1987. Consumer pressure and
seed set in a salt marsh perennial plant community. Oecologia 71: 190-200.
DENNO, R. F. 1977. Comparison of the assemblages of sap-feeding insects (Homopt-
era-Hemiptera) inhabiting two structurally different salt marsh grasses in the
genus Spartina. Environ. Entomol. 6: 359-372.
DENNO, R. F. 1985. Fitness, population dynamics, and migration in planthoppers:
the role of host plants, pp 623-639, In: M. A. Rankin, Ed. Migration: mechanisms
and adaptive significance. Contributions in Marine Science (Supplement) 27.

March, 1991

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