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Crespi & Abbot: Evolution of Kleptoparasitism
THE BEHAVIORAL ECOLOGY AND EVOLUTION OF
KLEPTOPARASITISM IN AUSTRALIAN GALL THRIPS
BERNARD CRESPI AND PATRICK ABBOT1
Behavioural Ecology Research Group, Department of Biological Sciences
Simon Fraser University, Burnaby BC V5A 1S6 Canada
1Current address: Department of Ecology and Evolutionary Biology,
University of Arizona
ABSTRACT
We used a combination of behavioral-ecological and molecular-phylogenetic data
to analyze the origin and diversification of kleptoparasitic (gall-stealing) thrips in the
genus Koptothrips, which comprises four described species that invade and breed in
galls induced by species of Oncothrips and Kladothrips on AustralianAcacia. The ge-
nus Koptothrips is apparently monophyletic and not closely related to its hosts. Two
of the species, K. dyskritus and K. flavicornis, each appears to represent a suite of
closely-related sibling species or host races. Three of the four Koptothrips species are
facultatively kleptoparasitic, in that females can breed within damaged, open galls by
enclosing themselves within cellophane-like partitions. Facultative kleptoparasitism
may have served as an evolutionary bridge to the obligately kleptoparasitic habit
found in K. flavicornis. Evidence from phylogenetics, andAcacia host-plant relation-
ships of the kleptoparasites and the gall-inducers, suggests that this parasite-host
system has undergone some degree of cospeciation, such that speciations of Kopto-
thrips have tracked the speciations of the gall-inducers. Quantification of kleptopar-
asitism rates indicates that Koptothrips and other enemies represent extremely
strong selective pressures on most species of gall-inducers. Although the defensive
soldier morphs found in some gall-inducing species can successfully defend against
Koptothrips invasion, species with soldiers are still subject to high rates of successful
kleptoparasite attack. Gall-inducing thrips exhibit three main types of life-history ad-
aptation that have apparently evolved in response to kleptoparasite pressure: (1)
"fighters", which exhibit long-lived galls and soldier morphs, (2) "runners", which
have quite short-lived galls, from which offspring disperse as second instar larvae,
and (3) "hiders", whose galls are long-lived, especially tight-sealing, and induced on a
taxonomically-distinct group ofAcacia host plants that is seldom attacked.
Key Words:Acacia, cladistics, gall thrips, kleptoparasites, sociality
RESUME
Para analizar el origen y la diversificaci6n de trips cleptoparasitos del g6nero Kop-
tothrips, se estudiaron aspects sobre su comportamiento, ecologia, y filogenetica mo-
lecular. Este g6nero tiene cuatro species descritas que invaden y se crian dentro de
agallas inducidas por species de Oncothrips y Kladothrips en Acacia spp. australia-
nas. El g6nero Koptothrips parece ser monofiletico y no estrechamente relacionado
con sus hospederos. Las species de K. diskritus y K. flavicornis parecen representar
dos grupos de species estrechamente relacionadas o de razas que difieren en sus hos-
pederos. Tres de las cuatro species de Koptothrips son cleptoparasiticas facultativas;
las hembras pueden criarse dentro de agallas danadas y abiertas protegiendose con
unos tejidos parecidos al papel celofan. El habito de cleptoparasitismo facultativo pa-
rece haber servido como un puente evolutivo hacia el cleptoparasitismo obligado como
el encontrado en K. flavicornis. La evidencia filogenetica y de las relaciones entire la
Acacia hospedera y los cleptoparasitos y los insects agalleros, sugiere que este sis-
tema de parasito-hospedero ha tenido alguin grado de co-especiaci6n ya que la espe-
Florida Entomologist 82(2)
June, 1999
ciaci6n de Koptothrips ha copiado la especiaci6n de los agalleros. La cuantificaci6n de
las proporciones de cleptoparasitismo indica que Koptothrips y otros enemigos natu-
rales representan presiones selectivas sumamente fuertes sobren la mayoria de las
species de agalleros. Aunque los soldados defensivos que ocurren en algunas species
de trips agalleros pueden defender las agallas con 6xito contra la invasion de Kopto-
thrips, las species con soldados de todos modos estan sujetas a altas proporciones de
ataque exitoso por cleptoparasitos. Los trips agalleros exhiben tres tipos principles
de adaptaci6n que han evolucionado al parecer en respuesta a la presi6n ejercida por
los cleptoparasitos: (1) "peleadores", que produce agallas duraderas y soldados; (2)
"escapadores", que produce agallas bastante efimeras y de las cuales la descendencia
se dispersa durante los segundos instares larvales; y (3) "escondedores", cuyas agallas
son duraderas, selladas firmemente, y que son inducidas en un grupo taxon6mica-
mente distinto de plants hospederas de Acacia que raramente son atacadas.
To survive, grow, and reproduce, all animals must engage in one or both of two
strategies: utilize resources that they themselves obtain, or steal resources from oth-
ers. Broadly construed, biological criminals include all predators, parasites, and par-
asitoids, but we usually consider parasitism as the primary example of illicit resource
use. Natural selection for parasitic thievery might be expected to increase in strength
with the value of the resources used, but so also would natural selection for defense.
Indeed, defense against parasites has been considered the main selective pressure for
much of the spectacular, beautiful, and stunningly-complex diversity of adaptation,
including sex (Hamilton et al. 1990), sexual selection (Hamilton and Zuk 1982; Ander-
sson 1994), social cooperation (Lin 1964; Lin and Michener 1972; Alexander 1986),
immune systems, and even multicellularity itself (Frank 1994). How the evolutionary
dynamics of host-parasite attack and defense play out for any set of species depends
on the variation available for selection, the genetic bases of the variation, and the de-
gree to which each party can control resource use. As such, in-depth analyses of the
ecology and evolution of particular host-parasite systems are necessary to uncover the
general principles underlying the forms and maintenance of these two strategies.
The purpose of this paper is to describe and test hypotheses for the origin, evolu-
tion, and behavioral ecology of kleptoparasites in Australian gall thrips, especially
with reference to the evolution of various forms of defense against these enemies.
Kleptoparasites are a special subset of natural enemies that usurp valuable physical
resources from the creator or obtainer, and thus fit most closely with our human per-
spective on theft. We first describe the natural history and ecology of kleptoparasitic
thrips and their victims, thrips that induce galls on species of AustralianAcacia. Sec-
ond, we present evidence from phylogenetics designed to uncover the evolutionary or-
igins of the kleptoparasitic lifestyle, and the patterns in its diversification. Finally, we
present data from behavioral-ecological studies that are focused on understanding
the ecology and evolution of these host-kleptoparasite interactions, and we fit these
data on processes into our phylogenetic framework.
MATERIALS AND METHODS
Natural history of Australian gall-inducing thrips and their kleptoparasites
A total of 21 described species of gall-inducing thrips in the genera Kladothrips, On-
cothrips, and Onychothrips induce galls on phyllodes petioless modified to function as
leaves) ofAcacia in the sections Plurinerves, Juliflorae, and Phyllodinae (Mound et al.
1996). Three described species, K. rugosus, 0. habrus, and 0. waterhousei, apparently
Crespi & Abbot: Evolution of Kleptoparasitism
each represents a suite of host-specific sibling species, inducing galls on different spe-
cies of plant (Crespi et al. 1998). Galls are induced on young, actively-growing phyl-
lodes by single adult macropterous females, and in some Kladothrips species a male
sometimes joins a female during gall initiation. During the period from gall initiation
until closure, females of Oncothrips tepperi, 0. habrus, Kladothrips rugosus, Onycho-
thrips arotrum and Ony. tepperi have been observed to fight with one another over gall
ownership, using their enlarged, armed forelegs (Crespi 1992a,b, Mound and Crespi
1995). All other known gall-forming species, except Oncothrips rodwayi and 0. anten-
natus, have notably enlarged forelegs in the females which are also indicative of fight-
ing. Males are also known to fight one another during gall induction in K. rugosus, and
their enlarged forelegs suggest that males also fight in K. ellobus and K. acaciae.
After successfully inducing a gall, the enclosed female lays eggs on the inner sur-
face of the gall, which develop into larvae that feed within the gall. Three main forms
of life-history are exhibited in the gall-inducers. First, in some species (Kladothrips
rugosus, K. acaciae, and K. ellobus), the length of time spent in the gall by developing
larvae is short relative to other gall-inducers on Acacia, on the order of 1-2 months,
and mature second-instar (i. e., last-instar) larvae apparently leave the gall prior to
pupation in the soil (B. Crespi and B. Kranz, personal observation). Second, in some
species (Oncothrips tepperi, 0. habrus, 0. waterhousei, 0. morrisi, K. hamiltoni, and
K. harpophyllae), some or all of the offspring produced by the foundress develop into
wing-reduced or wingless "soldier" morphs, which have enlarged forelegs that they
use to defend the gall against interspecific invaders (Crespi 1992b; Mound and Crespi
1995; Crespi et al. 1997; Crespi and Mound 1997). Third, some species (Oncothrips
antennatus, 0. schwarzi, Onychothrips arotrum, Ony. tepperi, Ony. zygus and K. aug-
gonsaxxos) do not exhibit soldier morphs, but the offspring of the foundress all eclose
within the gall. A variant of this life cycle is exhibited by Oncothrips sterni, in which
a cohort of wingless, larviform, non-soldier adults develop within the gall, and appar-
ently breed and contribute to the production of winged dispersers (Mound et al. 1996,
Crespi and Mound 1997).
The genus Koptothrips comprises four described species, K. xenus, K. zelus, K. dys-
kritus, and K. flavicornis (Mound 1971, Crespi 1992a, Crespi and Mound 1997), all of
which kleptoparasitize galls of the gall-inducers. K. xenus and K. zelus are host-spe-
cific, attacking Kladothrips ellobus and K. acaciae respectively, whereas specimens
that key to K. dyskritus attack the various sibling species of K. rugosus (and possibly
other taxa), and specimens that key to K. flavicornis attack 0. tepperi, 0. habrus, 0.
waterhousei, K. rugosus, and several other species. Koptothrips are found in galls of
all stages, from recently-founded by the gall-inducer to at least several months old.
Galls are usually invaded by single females, which attack and attempt to kill the gall-
forming thrips inside. If successful, a female Koptothrips produces a single brood of fe-
male and male offspring, which disperse from the gall as adults. In K. zelus and K. xe-
nus, multiple females may invade a gall, in which case the females are each found in
a small section of the gall which is partitioned from other sections by a cellophane-like
material, apparently produced by the thrips (Crespi and Mound 1997). Females of K.
dyskritus have also been collected from within cellophane-like partitions that they
create with accessory gland secretions to enclose them within sections of damaged,
otherwise-open galls of K. rugosus that no longer contain any of the gall-inducers
(Crespi, unpublished data; see also Mound et al. 1997).
Encounters between females of K. flavicornis and K. dyskritus, and adults of various
species of Oncothrips and Kladothrips, have been observed in galls in the laboratory
(Crespi 1992b, Crespi and Mound 1997). Winged foundresses of the gall-inducers, and
soldier morphs in the Oncothrips and Kladothrips with soldiers, will fight the Kopto-
thrips, attempting to grasp and kill them with their enlarged forelegs, which are armed
Florida Entomologist 82(2)
June, 1999
at the apex with sharp, pointed fore-tarsal teeth. The Koptothrips usually fight back,
also by grasping and stabbing with their forelegs and fore-tarsal teeth, and if they suc-
cessfully pierce a gall-inducer with their fore-tarsal teeth, the pierced individual usu-
ally dies within a few minutes (Crespi and Mound 1997). Galls successfully invaded by
any of the four Koptothrips taxa always contain a dead foundress or a dead foundress
and founder male, which indicates that invading Koptothrips kill the gall-inducers.
Molecular-phylogenetic analysis
The first main goal of our phylogenetic analysis was to assess the taxonomic status
of Koptothrips flavicornis and K. dyskritus collected from galls of host thrips species
on different host plants. Each of these two described species may represent either a
single, more or less panmictic, generalist species, or a suite of more or less specialized
species, each attacking a different species of gall-inducing thrips. For K. flavicornis,
Mound (1971) noted that specimens collected from the galls of different host thrips of-
ten vary considerably in color, ranging from bicolored with a reddish head and yellow
abdomen, to brownish, to black. Although mitochondrial DNA sequence data cannot
unambiguously indicate species status, levels of divergence between putative taxa
can help in achieving this goal (Avise 1994).
The second main goal of our phylogenetic analysis was to evaluate the evolution-
ary relationships between the Koptothrips and their hosts. Alternative hypotheses for
these relationships, all of which have been discussed with reference to other taxa (e.
g. Bourke and Franks 1991, Choudhary et al. 1994, Ward 1996, Lowe and Crozier
1997, Morris et al. 1998) include: (a) monophyly of the kleptoparasites, and of the
hosts, and a lack of sister-taxon status between the two; (b) monophyly, and sister-
taxon status, of the kleptoparasites and hosts; (c) monophyly of the kleptoparasites,
but paraphyly of the hosts with respect to the kleptoparasites, such that the parasites
evolved from within the host lineage; or (d) sister-taxon relationships between each or
most of the pairs of hosts and parasites, such that neither is monophyletic. As dis-
cussed below, these hypotheses imply different sets of ecological and behavioral mech-
anisms for the origin and diversification of the hosts and kleptoparasites.
To infer a phylogeny for the gall-inducing thrips, we used a combination of data
from mitochondrial DNA sequence from the COI and 16S genes, adult morphological
characters, and gall morphology characters (Crespi et al. 1998). For the kleptopara-
sites, we used about 450 base pairs of mitochondrial DNA sequence from the COI gene
for all taxa, with about 250 base pairs of 16S for some taxa. Sequence data for most
of the gall-inducers included here is given in Crespi et al. (1998), and all other data (e.
g., for all of the Koptothrips) is described and analyzed below. Procedures used for
DNA isolation, PCR, and sequencing, and sequence for the gall-inducing taxa, are de-
scribed in Crespi et al. (1998). As described below, we used Gynaikothrips ficorum as
our outgroup (Crespi et al. 1998), and maximum parsimony analysis and neighbor
joining in PAUP 4.0 (Swofford 1998) to analyze the data. We used 500 bootstrap rep-
licates with neighbor joining to assess the robustness of the neighbor joining tree;
maximum parsimony bootstrapping was computationally impossible due to the large
number of taxa in our data set.
Measurement of kleptoparasitism rates
We collected data on rates of successful kleptoparasitism in the field to evaluate
the prevalence and patterns of kleptoparasitism in different host species. Galls were
collected from numerous sites throughout Australia (Table 1) directly into 60-100%
Crespi & Abbot: Evolution of Kleptoparasitism
ethanol. Any given site includes galls from one to several dozenAcacia trees, and we
either collected all galls encountered (when galls were rare), or collected so as to ob-
tain a representative sample of galls with respect to variation in size. For all species,
hosts or kleptoparasites in galls from a given site are quite synchronized in their life
cycle, as a result of breeding cued by either an annual cycle of new shoot growth, or
rainfall.
We dissected galls in the laboratory and recorded the species of thrips inside, and
their life-cycle stages present, as well as the presence of other invaders. The predom-
inant non-thysanopteran invaders were lepidopteran larvae (mainly or all species of
Lepidoptera in the family Cosmoptyrigidae, one to a gall), which eat gall tissue from
the inside and lead to a drastic reduction in thrips numbers, but usually do not kill all
of the gall inhabitants. In some galls, both Koptothrips and a lepidopteran larva were
present, but Koptothrips and gall-forming thrips never coexisted alive, except in sev-
eral galls of Oncothrips antennatus on Acacia adsurgens. We calculated percent Kop-
tothrips invasion as the number of galls containing live Koptothrips divided by total
gall number, and made similar calculations for non-thysanopteran invaders (lepi-
dopteran and dipteran larvae). Thus, the kleptoparasitism data refer to rates of suc-
TABLE 1. RATES OF SUCCESSFUL KOPTOTHRIPS KLEPTOPARASITISM, AND PARASITISM BY
LEPIDOPTERANS AND DIPTERANS ("OTHER INVADERS"), GIVEN AS MEANS AND
STANDARD DEVIATIONS (AVERAGING ACROSS COLLECTIONS). = GALL-INDUC-
ING THRIPS SPECIES WITH SOLDIER MORPHS.
%
Number of Number Koptothrips % Other
Gall-inducing thrips species collections of galls invaders invaders
*Oncothrips morrisi 1 24 0.29 0
*Oncothrips waterhousei 2 68 0.32 (0.003) 0.44 (0.09)
*Oncothrips habrusl 5 240 0.23 (0.18) 0.17 (0.07)
*Oncothrips habrus2 2 38 0.08 (0.002) 0.51 (0.37)
*Oncothrips tepperi 10 423 0.31 (0.26) 0.29 (0.23)
Oncothrips rodwayi 3 125 0.07 (0.02) 0.30 (0.24)
*Kladothrips hamiltoni 6 215 0.25 (0.15) 0.36 (0.17)
*Kladothrips harpophyllae 1 20 0.25 0.35
Kladothrips rugosusl 6 237 0.19 (0.15) 0.24 (0.19)
Kladothrips rugosus2 6 171 0.04 (0.04) 0.03 (0.04)
Kladothrips rugosus3 4 133 0.03 (0.06) 0.11 (0.19)
Kladothrips ellobus 6 147 0.40 (0.26) 0.16 (0.21)
Kladothrips acaciae 4 84 0.35 (0.30) 0.03 (0.06)
Oncothrips antennatusl 3 105 0.24 (0.04) 0.19 (0.01)
Oncothrips antennatus2 10 315 0.02 (0.05) 0.45 (0.25)
Onychothrips arotrum 6 229 0 0.16 (0.13)
Onychothrips tepperi 1 11 0 0
Oncothrips habrusl = 0. habrus onAcacia melvillei; 0. habrus2 = onA. pendula; K rugosusl = onA. pendula;
K rugosus2 = onA. melvillei; K rugosus3 = onA. tephrna; 0. antennatusl = onA. adsurgens; 0. antennatus2 =
onA. aneura.
Florida Entomologist 82(2)
June, 1999
cessful attack and invasion. We have no information concerning what proportion of
attacks by Koptothrips is unsuccessful, except to note that dead Koptothrips adults
are occasionally found within galls containing live gall-forming thrips (Crespi 1992a,
Mound and Crespi 1995). Many attacks could be aborted, however, before the invader
fully enters the gall.
RESULTS
Molecular Phylogenetics
The percent sequence divergence in the COI gene between K. flavicornis collected
from different host thrips taxa andAcacia species ranged from 0 to 5.6% (with most
of the values between 2.5 and 5.6%), and divergences for K. dyskritus ranged from 0.5
to 6.9% (with one value of 0.5%, and five values between 5.5% and 6.9%). For K. flav-
icornis, divergences were especially low between specimens collected from two differ-
ent host thrips species on the same host plant (0.2% for specimens collected from
K. rugosus and 0. waterhousei onA. loderi, and 0.2% for specimens collected from K.
rugosus and 0. waterhousei onA. ammophila).
Maximum parsimony analysis of the mitochondrial DNA and morphology data
yielded six shortest trees of length 1484. The strict consensus of these trees was well
resolved (Fig. la) and indicated that the gall-inducing thrips, and the Koptothrips,
each forms a monophyletic group. Within the Koptothrips, each described species was
also monophyletic, with K. xenus and K. zelus most basal, K. zelus forming the sister-
group to K. dyskritus, and (K. zelus + K. dsykritus) as sister-group to K. flavicornis.
Neighbor-joining analysis of the COI and 16S mitochondrial DNA data yielded a
tree that was closely-similar to the maximum parsimony tree, the main differences
being the monophyletic status of (Koptothrips dyskritus +K. xenus +K. zelus), and sis-
ter-taxon status of Koptothrips xenus and K. zelus, in the neighbor joining tree (Fig.
ib). About half of the nodes in the neighbor-joining bootstrap tree were well-sup-
ported by the bootstrap (with support of 70% or higher) (Fig. ic). In particular, the
bootstrap provided strong support for monophyly of the gall-inducers, and monophyly
of the kleptoparasites, but it provided relatively weak support for the placements of
K. zelus and K. xenus.
Consideration of the host plants inhabited by the gall-inducing thrips and their
kleptoparasites, with respect to their positions in the maximum-parsimony phylogeny,
reveals a notable pattern: the relatively basal kleptoparasite species K. xenus and K.
zelus attack the relatively-basal host species Kladothrips acaciae and K. ellobus re-
spectively. Moreover, all four of these species are host-insect and host-plant specific,
and all are quite morphologically distinct from their closest relatives (Mound 1971).
This finding suggests that, as described in detail below, the diversification of Kopto-
thrips and their gall-inducing hosts has involved some degree of cospeciation. Further
evidence for cospeciation is provided by two additional patterns. First, K. dyskritus,
which apparently descended from the ancestor of (K. xenus + K. zelus), attacks prima-
rily K. rugosus, which apparently descended from the ancestor ofK. ellobus and K. aca-
ciae. Second, K. flavicornis, which is sister-taxon to the other Koptothrips taxa, mainly
attacks gall-inducing thrips in the (Oncothrips morrisi + 0. waterhousei + 0. habrus +
0. tepperi + 0. rodwayi) clade, which forms the sister-group to the Kladothrips species.
The two Koptothrips taxa that appear derived with respect to K. xenus and K. ze-
lus, K. dyskritus and K. flavicornis, each attacks multiple species of gall-inducing
thrips, and the gall-inducing thrips that they attack, primarily K. rugosus, 0. water-
housei, and 0. habrus, also each appears to represent a set of closely-related species
Crespi & Abbot: Evolution of Kleptoparasitism 153
(la) MAXIMUM PARSIMONY
K.ellobus I
K.rugosus(melvillei) I
K.rugosus(pendula) L
K.rugosus(marano) 9
K.rugosus(tephrina)
K.rugosus(micro)
K.rugosus(omalo)
K.rugosus(papyro)
K.rugosus(ammoph)
K.rugosus(cana)
K.rugosus(loderi)
K.acaciae to
K.harpophyllae
K.hamiltoni
0. rodwayi u
O.habrus(pendula) 3
O.habrus(melvillei) Q
O.tepperi z
O.waterhousei(tephrina) H
O.waterhousei(omalo) I
O.waterhousei(ammoph) I
O.waterhousei(cana)
O.waterhousei(micro) C
O.waterhousei(papyro)
O.waterhousei(ancis)
-- -- O.waterhousei(Ioderi)
O.waterhousei(marano)
O.morrisi
O.antennatus(aneura)
O.antennatus(adsurgens)
Ony.pilbara
O.torus
K.augonsaxxos
O.sterni
Ony.arotrum
Gynaikothrips
K. flavicornis-A
K. flavicornis-C I
K. flavicornis-P |
K. flavicornis-1I
K. flavicornis-J
K. flavicornis-L E
K. flavicornis-M I-I
K. flavicornis-N w
-- K. flavicornis-O
K. flavicornis-K
K. flavicornis-H
---- K. flavicornis-F O
K. flavicornis-G o
K. flavicornis-D
K. flavicornis-E
K. flavicornis-B
K. dyskritus-A
K. dyskritus-B
K. dyskritus-C
K. dyskritus-D
K. zelus
K. xenus
Fig. 1. (a) Strict consensus of six most-parsimonious trees of length 1484, inferred
using heuristic searching in PAUP 4.0. For the gall-inducing species comprising sib-
ling species or host races on different host plants, the thrips species name is followed
by a code for the species name of the Acacia. For the Koptothrips, specimens of K. fla-
vicornis and K. dyskritus collected from galls from different host-thrips species are
given unique letter codes. Complete host localities and other collection information is
available from BJC.
Florida Entomologist 82(2)
(Ib) NEIGHBOR JOINING
K~ellobus
K.acaciae
K.rugosus(melvillei)
K.rugosus(pendula)
K.rugosus(marano)
K.rugosus(cana)
K.rugosus(papyro)
K.rugosus(ammoph)
K.rugosus(tephrina)
It- .K.rugosus(micro)
K.rugosus(omalo)
K.rugosus(loderi)
K i K.harpophyllae
----- K.hamiltoni
0. rodwayi U
O.habrus(pendula) 3
O.habrus(melvillei)
O.tepperi
O.waterhousei(marano) H
O.waterhousei(papyro)
g O.waterhousei(ancis)
SO.waterhousei(loderi) A
O.waterhousei(tephrina) 4
O.waterhousei(omalo)
O.waterhousei(ammoph)
O.waterhousei(cana)
O.waterhousei(micro)
O.morrisi
O.antennatus(aneura)
O.antennatus(adsurgens)
Ony.pilbara
0.torus
-K.augonsaxxos
O.sterni
Ony.arotrum
Gynaikothrips
K. flavicornis-A
K. flavicornis-B
K. flavicornis-C
K. flavicornis-D I
K. flavicornis-E
K. flavicornis-F W
-- K. flavicornis-G
K. flavicornis-H H
K. flavicornis-I M
K. flavicornis-J
K. flavicornis-K
Sr K. flavicornis-L P4
K. flavicornis-M
K. flavicornis-N 0
K. flavicornis-O0
K. flavicornis-P 4
K. xenus
K. zelus '
L K. dyskritus-A M
K. dyskritus-B I
K. dyskritus-C I
K. dyskritus-D I
Fig. 1. (b) Neighbor-joining tree, inferred from the mitochondrial COI and 16S
DNA data. For the gall-inducing species comprising sibling species or host races on
different host plants, the thrips species name is followed by a code for the species
name of the Acacia. For the Koptothrips, specimens of K. flavicornis and K. dyskritus
collected from galls from different host-thrips species are given unique letter codes.
Complete host localities and other collection information is available from BJC.
June, 1999
Crespi & Abbot: Evolution of Kleptoparasitism 155
(Ic) BOOTSTRAP NEIGHBOR JOINING
K.ellobus
71 K.rugosus(pendula)
57 K.rugosus(marano)
K.rugosus(cana)
57 100 K.rugosus(tephrina) I
57 60 _i K.rugosus(micro)
K.rugosus(omalo)
55 K.rugosus(papyro)
K.rugosus(ammoph)
K.rugosus(loderi)
K.acaciae
66 K.rugosus(melvillei) W0
5-- K.harpophyllae
K.hamilton,
0. rodwayi u
72 | O.habrus(pendula) 4
L.l_77 O.habrus(melvillei) Q
60 O.tepperi z
-- 61--- O.waterhousei(tephrina) H
87 '-- O.waterhousei(omalo)
SO86 0.waterhousei(ammoph)
100 O.waterhousei(cana) 1
O.waterhousei(micro)
196 O.waterhousei(papyro) o
97 O.waterhousei(ancis)
O.waterhousei(loderi)
O.waterhousei(marano)
O.morrisi
O.antennatus(aneura)
99 -- O.antennatus(adsurgens)
58 -- Ony.pilbara
95-- 0.torus
52 -- K.augonsaxxos
O.sterni
Ony.arotrum
Gynaikothrips
K. flavicornis-A
K. flavicornis-C I
63 59 K. flavicornis-D I
_E K. flavicornis-E 1
73 K. flavicornis-F 0
F--2 t K. flavicornis-G H
52 K. flavicornis-H
88 5 99 --- K. flavicornis-I h
K. flavicornis-J '
86 K. flavicornis-K a
59 59 K. flavicornis-L '
63 59 K. flavicornis-M 3
94 89 K. flavicornis-N P4
K. flavicornis-0 0
K. flavicornis-P E-
K. flavicornis-B C4
K. xenus r
100 K. dyskritus-A
55 94 K. dyskritus-B M
50 -- K. dyskritus-C I
K. dyskritus-D I
K. zelus I
Fig. 1. (c) Neighbor-joining bootstrap tree (500 replicates). For the gall-inducing
species comprising sibling species or host races on different host plants, the thrips
species name is followed by a code for the species name of the Acacia. For the Kopto-
thrips, specimens of K. flavicornis and K. dyskritus collected from galls from different
host-thrips species are given unique letter codes. Complete host localities and other
collection information is available from BJC.
Florida Entomologist 82(2)
June, 1999
on different Acacia host-plants (Crespi et al. 1998). However, whereas K. dyskritus
primarily attack species of Kladothrips rugosus, K. flavicornis commonly attack 0.
waterhousei and 0. habrus, 0. tepperi, 0. rodwayi, and sometimes K. rugosus. These
data suggest that the diversification of Koptothrips has involved an expansion of host
range if K. flavicornis represents a single species, or a radiation involving diverse
hosts if it represents a suite of closely-related sibling species.
Mapping of the behavior of Koptothrips onto the maximum-parsimony phylogeny
reveals another notable result: Koptothrips xenus, which is one of the three Kopto-
thrips taxa known to be facultatively kleptoparasitic, is basal with respect to the lin-
eage giving rise to the obligately-kleptoparasitic taxon K. flavicornis. Thus,
facultative kleptoparasitism is inferred as ancestral for the genus Koptothrips, with
one inferred shift to obligate kleptoparasitism. This finding supports the hypothesis
that kleptoparasitism in Koptothrips originated as a facultative alternative, and be-
came obligate in association with the speciation event that gave rise to K. flavicornis.
In our neighbor-joining tree, the three facultatively-kleptoparasitic Koptothrips
taxa form a monophyletic group, which is sister-taxon to K. flavicornis, and (K. xenus
+ K. zelus) also forms a monophyletic group. This phylogeny is also broadly compatible
with a cospeciation model, in that the two main lineages of hosts, Oncothrips and Kla-
dothrips, are attacked respectively by the two main lineages of kleptoparasites, K. fla-
vicornis and (K. dyskritus + K. zelus + K. xenus), and the K. zelus and K xenus
lineages appear old and divergent relative to the other two Koptothrips species. The
weakness of the bootstrap support for the positions of K. xenus and K. zelus in this
tree indicates that we cannot consider the results of the maximum-parsimony and
neighbor-joining analysis incompatible. These analyses also tell us that additional
data from a more slowly-evolving molecule would help to resolve the positions of these
two species.
Kleptoparasitism Rates
Data on rates of successful kleptoparasitism, and successful invasion by lepi-
dopterans and dipterans, are summarized in Table 1. Four patterns are notable in
these data. First, the highest kleptoparasitism rates are found in the two species, Kla-
dothrips acaciae and K ellobus, that are attacked by the host-specific, morphologi-
cally-specialized invaders Koptothrips zelus and K. xenus. Second, rates of
kleptoparasitism are also quite high in five of the six species of gall-inducing thrips
with soldier castes, with on the order of one-quarter to one-third of galls successfully
invaded. Indeed, rates of Koptothrips invasion are about twice as high overall in spe-
cies with soldiers as in species without soldiers. Third, some of the lowest rates of
kleptoparasitism are exhibited by three species, Onychothrips arotrum, Onychothrips
tepperi, and Oncothrips antennatus on Acacia aneura, that are related phylogeneti-
cally, all being found in the same monophyletic group. Moreover, this clade is unusual
in that all of its species induce galls on Acacia species in the section Juliflorae,
whereas all of the other species induce galls onAcacia in the section Plurinerves. Fi-
nally, rates of invasion by non-thysanopterans, mainly lepidopterans and dipterans,
do not show the same clear interspecific patterns as those for kleptoparasites; instead,
almost all of the gall-inducers are heavily beset by these enemies.
DISCUSSION
The main goal of this study is to understand the evolutionary and behavioral-eco-
logical dynamics of the kleptoparasite-host relationships found in Koptothrips and
gall-inducing thrips on Australian Acacia. To achieve this goal, we have (1) used mi-
Crespi & Abbot: Evolution of Kleptoparasitism
tochondrial DNA data to assess the taxonomic status of two taxa, Koptothrips flavi-
cornis and K. dyskritus, that attack multiple species of gall-inducing thrips on
multiple host plant species; (2) tested hypotheses for the evolutionary origin of klep-
toparasitism in these insects, (3) analyzed the phylogenetic and behavioral-ecological
patterns of diversification of Koptothrips, with respect to the diversification of their
hosts, and (4) used data on rates of kleptoparasitism in different species to draw in-
ferences concerning its importance as a selective pressure. Our hypothesis for the or-
igin and diversification of Koptothrips and their hosts is depicted and summarized in
Fig. 2, and described in detail below.
Gall -inducers
5 K. rugosus
Koptothrips Kopto. dyskritus
4
K. ellobus
Kopto. xenus
6
SK. acaciae
Kopto. zelus
Oncothrips
lineage
Kopto. flavicornis
Fig. 2. Hypothesized scenario for the broad-scale evolutionary relationships be-
tween Australian gall-inducing thrips on Acacia and their Koptothrips kleptopara-
sites. (1) Origin of the genus Koptothrips, via a host shift onto Acacia, attacking the
ancestor of the (Oncothrips + Kladothrips) lineage of gall-inducers. (2) Ancestor of
(Oncothrips + Kladothrips) splits into two genera, and, as a result, Koptothrips splits
into two lineages, one giving rise to (K. xenus + K. zelus + K. dyskritus) (which attack
Kladothrips), the other giving rise to K. flavicornis (which attack Oncothrips). (3) On-
cothrips lineage and Koptothrips flavicornis lineage diversify. (4) Kladothrips acaciae
and K. ellobus descend from the ancestral Kladothrips lineage, leading to the evolu-
tion of their host-specific Koptothrips, K. zelus and K. xenus. (5) Next, Kladothrips
rugosus originates along the Kladothrips lineage, leading to the evolution of Kopto-
thrips dyskritus. K. rugosus and K. dyskritus diversify together, onto different species
ofAcacia in the section Plurinerves. (6) Some Koptothrips flavicornis lineages expand
their host range by attacking Kladothrips rugosus that are on the same host plant as
their ancestral Oncothrips hosts. By plausible alternative phylogenies, Kladothrips
acaciae and K. ellobus may be sister-taxa, and Koptothrips zelus and K. xenus may
also be sister taxa. We stress that this diagram represents a hypothesis that, although
consistent with our available data, requires additional testing.
Florida Entomologist 82(2)
June, 1999
The levels of mitochondrial DNA sequence divergence found between specimens of
K. flavicornis and K. dyskritus collected from different species of host thrips on differ-
entAcacia species range up to 7% and average about 3%. These values are consistent
with the hypothesis that each of these named species actually comprises a set of mul-
tiple closely-related sibling species or host races. However, we also note that some of
the pairwise divergences within these taxa are very low, below 0.5%, and that two of
these low divergence values are for samples of K. flavicornis collected from different
species of host thrips (K. rugosus and 0. waterhousei) each on the same host plant (A.
loderi or A. ammophila). These findings strongly suggest that whereas some K. flavi-
cornis are sufficiently genetically divergent from others that high levels of gene flow
are unlikely to be occurring between them, the K. flavicornis attacking different host
thrips species on the same host plant may well be conspecific. Further analysis of the
systematic status of K. flavicornis and K. dyskritus requires quantification of genetic
variation both between and within putative conspecific populations, and experimen-
tal transfer of Koptothrips between host thrips and host plants.
Our phylogenetic analyses indicate that the genus Koptothrips, and its gall-inducing
host species, are each monophyletic. These results falsify the hypothesis that Kopto-
thrips arose from within the lineage of gall-inducers onAcacia, ostensibly via intraspe-
cific kleptoparasitism during gall induction (Crespi 1992a). Because our phylogeny does
not yet include genera of thrips on Australian Acacia other than Oncothrips, Kladot-
hrips, Onychothrips, and Koptothrips (Mound 1971), we must turn to other information
to assess whether or not Koptothrips and their gall-inducing hosts are (1) sister-taxa,
such that they share a common ancestor, or (2) not closely related, such that kleptopar-
asitism arose via a host-plant shift. Using a cladistic morphological analysis of Austra-
lian Phlaeothripines, Morris et al. (1998) have shown that the latter hypothesis is
supported. By their analysis, the genus Koptothrips is not closely-related to its gall-in-
ducing hosts, nor is it found in a clade of thrips that inhabits Acacia; instead, it appears
to be related to species of Teuchothrips, which induce simple leaf-roll or curl galls on a va-
riety of plant taxa. Since Koptothrips are not known to attack Teuchothrips, these results
suggest that the genus Koptothrips originated, and evolved its kleptoparasitic habit, in
conjunction with a major host-plant shift ontoAcacia (Morris et al. 1998). This hypothe-
sized scenario for the origin of Koptothrips is depicted as stage 1 in Fig. 2. Whether the
progenitors of Koptothrips were gall-inducers like Teuchothrips, or non-galling plant
feeders, cannot be inferred from the phylogenetic information available to date.
What might be the ecological basis and evolutionary significance of kleptoparasit-
ism originating in association with a host-plant shift? Morris et al. (1998) suggest that
the habit of invading galls could have facilitated host-shifting because galls provide a
highly favorable microhabitat, especially in a climate like that of arid-zone Australia.
Thus, the advantages of using galls as domiciles could have helped offset the disad-
vantages of adapting to live on a novel host plant. Moreover, in the same way that
host-plant shifts by phytophagous insects can be facilitated by escape from natural
enemies (Brown et al. 1995, Feder 1995, Shorthouse and Brooks 1998), we suggest
that host-insect shifts by incipient enemies could be facilitated by a lack of evolved de-
fenses of their hosts. Support for a hypothesis of host-shifting coinciding with the or-
igin of kleptoparasitism comes from remarkably parallel situations in two taxa
unrelated to gall thrips: (1) in Eriosoma aphids, kleptoparasitism of galls has also ap-
parently originated via a host-plant shift (Akimoto 1981, 1989), and (2) in yucca
moths, phylogenetic evidence indicates that non-pollinating 'cheater' species origi-
nated in association with host-plant shifts (Pellmyr et al. 1996). Our hypothesis of
evolutionary cheating arising as a result of ecological-phylogenetic saltation could be
tested further by designing phylogenetic studies to uncover the ecological habits of
Crespi & Abbot: Evolution of Kleptoparasitism
the closest honest relatives of such cheaters, rather than focussing just on the para-
sites and hosts when analyzing the origin of the parasites.
Phylogenetic and behavioral data suggests that, in addition to involving a host-
plant shift, the origin of kleptoparasitism in Koptothrips may also have involved a fac-
ultative stage. This hypothesis is supported by the observation that K. xenus, K. zelus
and K. dyskritus can create cellophane-like partitions in damaged, open galls bereft
of gall-inducers, and breed successfully inside. By contrast, the obligately-kleptopar-
asitic K. flavicornis apparently cannot do so. We suggest that the primordial Kopto-
thrips used damaged, open galls for breeding, as do some Grypothrips and Katothrips
(Crespi et al. 1997), that facultative kleptoparasitism evolved via selection for obtain-
ing a better, larger, and fresher resource for breeding, and that obligate kleptopara-
sitism evolved in the K. flavicornis lineage via evolutionary refinement of usurpation
behavior (see Field 1992 for description of similar patterns in some Hymenoptera).
This hypothesis fits with West-Eberhard's (1986) model of evolutionary transitions
arising from facultative alternative behaviors, and it could be tested via more-de-
tailed study of Koptothrips morphology and behavior in the context of their phylogeny.
In particular, we need better resolution and support for the phylogenetic placements
of Koptothrips xenus and K. zelus, for which neighbor-joining and maximum-parsi-
mony yield differing, albeit weakly-supported, results.
Once a parasitic habit has evolved, diversification of parasite lineages can proceed
via two main mechanisms: cospeciation, such that the parasites simply track the spe-
ciations of their hosts (Page 1994), and host-shifting, such that parasites move be-
tween host species more or less respective of the phylogenetic affinities of their
current and future hosts. Our phylogenetic data indicates that the oldest split in the
gall-inducers onAcacia in the section Plurinerves was between the genera Oncothrips
and Kladothrips, and it suggests that this split was mirrored by Koptothrips klepto-
parasites, as they diversified into two clades, K. flavicornis, which attack mainly On-
cothrips, and (K. zelus + K. xenus + K. dyskritus), which attack species of Kladothrips
(stage 2 in Fig. 2). Moreover, within the Kladothrips lineage, K. acaciae and K. ellobus
are the most-basal species, and they are attacked by the two Koptothrips species that
appear relatively old and basal, K. zelus and K. xenus. These relationships are also
supported by the similarity in levels of divergence in mtDNA between K. xenus and K.
zelus (14%), and between K. ellobus and K. acaciae (13.3%), which suggests that the
two pairs of lineages may be of similar ages.
What of K. dyskritus and K. flavicornis? K. flavicornis, which our phylogeny iden-
tifies as the sister-taxon to the other Koptothrips species, attack species of gall-induc-
ers in the sister-taxon of (K. acaciae + K. ellobus + K. rugosus), which comprises
species of Oncothrips. This pattern suggests that the ancestor of K. flavicornis at-
tacked the ancestor of (0. morrisi + 0. waterhousei + 0. habrus + 0. rodwayi + 0. tep-
peri) (stage 3 in Fig. 2), and has diversified by some combination of cospeciation, host
shifting, and perhaps independent speciation. The descent of K. dyskritus from the
ancestors of K. xenus and K. zelus is compatible with the observation that K. dyskritus
primarily attack Kladothrips rugosus, a lineage that has descended from the ancestor
of K. acaciae and K. ellobus (stages 4 and 5 in Fig. 2). Thus, our phylogeny is consis-
tent with the hypothesis that cospeciation was also involved in the evolution ofK. dys-
kritus. Finally, the observation that some K. flavicornis attack K. rugosus, as well as
species of Oncothrips, suggests that some K. flavicornis lineages have undergone a
host-insect range expansion, to include K. rugosus in their list of victims (stage 6 in
Fig. 2). Our data also indicate that theAcacia host plants have mediated the putative
expansion of host range: in both cases where K. flavicornis attack both Oncothrips and
Kladothrips, the two species of gall-inducers are on the same host-plant species.
Florida Entomologist 82(2)
June, 1999
Further analyses of the evolution of across trophic-level interactions in Kopto-
thrips and their hosts requires: (1) more thorough sampling of the Koptothrips from
different host thrips and host plants, (2) more detailed elucidation of the taxonomic
status of the K. flavicornis and K. dyskritus attacking different hosts, (3) statistical
analysis of cospeciation models (Page 1994), (4) better understanding of the mecha-
nisms responsible for cospeciation and host-shifting, (5) better support for the phylo-
genetic positions of Koptothrips zelus and K. xenus. However, the data presented here
suggest that Koptothrips and their hosts have evolved together via some combination
of cospeciation and host shifting, which will make them especially useful for analyz-
ing the causes of these disparate processes.
Within lineages, kleptoparasitism evolves as a consequence of natural selection on
both the parasites and their hosts, and our data on rates of kleptoparasitism allows
us to assess its importance as a selective pressure in host species that differ in various
aspects of their life history. Our quantification of rates of parasitism by Koptothrips
and non-thysanopterans has uncovered four main patterns.
First, the highest rates of Koptothrips kleptoparasitism occur in Kladothrips ello-
bus and K. acaciae, the only two species with host-specific kleptoparasites, Kopto-
thrips xenus and K. zelus. These high kleptoparasitism rates may be due in part to
highly-developed parasite specialization, if higher kleptoparasite efficiency has
evolved as a consequence of adaptation to single rather than multiple hosts (see Ber-
nays and Graham 1988). Similarly high rates of successful attacks by specialist ene-
mies have been reported in a subsocial pentatomid bug (Eberhard 1975), and in some
species of gall aphids (e. g., It6 1989, Moffett 1989, Stern and Foster 1996).
Second, rates of successful Koptothrips parasitism are also quite high in almost all
species with soldiers. At first glance, this result might appear paradoxical, because be-
havioral evidence from numerous species with soldiers indicates that soldiers fight,
and often kill, invading Koptothrips (Crespi and Mound 1997, Crespi unpublished
data). However, such defense, though often spectacular, is frequently impossible or in-
effectual: Koptothrips sometimes invade galls before any soldiers have closed (Crespi
and Mound 1997), and Koptothrips are often victorious in their fights with soldiers.
Moreover, if high rates of kleptoparasitism were important in selecting for the origin
of soldier castes (Crespi 1996, Crespi et al. 1998), then such high rates should not sur-
prisingly be instrumental in maintaining soldiers.
The hypothesis that parasite pressure has been an important cause of the origin
and maintenance of sociality could be analyzed further by comparing parasite and
predator pressure between non-thysanopteran taxa with and without soldiers or other
types of worker that defend. At present, such data are available for only two taxa (see
also Crespi and Choe 1997). Moran (1993) compared rates of successful predation by
a gall-specializing fly larva between a Pemphigus gall aphid species with soldiers, and
a Pemphigus species without soldiers, for galls taken from the same tree. The aphid
species with soldiers had lower predation rates than the species without soldiers for
most of the season, but rates of unsuccessful attack on the species with soldiers are
unknown. Schwarz (1994) found higher rates of parasitism by encyrtid wasps and
cuckoo bees, and higher levels of cooperative nests and nest aggregation, in montane
populations of the allodapine bee Exoneura robusta (= bicolor) than in heathland pop-
ulations of the closely related species Exoneura nigrescens. Rates of parasitism by en-
cyrids did not covary with colony site at either location, but higher numbers of females
may help in defense against cuckoo bees. By contrast, larger colony sizes have been in-
ferred to enhance protection of brood against ants inAllodapula melanopus (Michener
1971), in Exoneura robusta (Schwarz 1986, 1994) and in Exoneura nigrescens (Bull
and Schwarz 1996). Among allodapines in general, species exhibiting eusociality ap-
Crespi & Abbot: Evolution of Kleptoparasitism
pear more beset by inquiline bees than are species with only solitary nests, but
whether high inquilinism rates are a cause or effect of sociality is not yet known.
Third, some species of gall-inducing thrips, notably some K. rugosus, 0. antennatus
from Acacia aneura, Onychothrips arotrum, and Onychothrips tepperi, exhibit very
low rates of Koptothrips parasitism. This interspecific variation in kleptoparasitism
rates may be due in part to the different life-histories of the lineages involved. In some
species, such as K. rugosus and K. ellobus, the life-cycle appears to be quite short rel-
ative to the other gall-inducers (several months, compared to over nine months in
other taxa), and the offspring of the foundress apparently disperse from the gall as
second-instar larvae and pupate in the soil (B. Crespi and B. Kranz, personal observa-
tion). As a result, some of these taxa may keep kleptoparasitism rates low by escaping
in time (i. e., minimizing the time that they are vulnerable to invasion). By contrast,
species of Onychothrips, and 0. antennatus, inhabit galls that appear to be more
tightly sealed than those of other species. The galls are long-lived in these species, and
offspring of the foundress all eclose within the gall. In addition, all of the gall-inducing
thrips in the lineage containing Onychothrips, 0. antennatus, 0. sterni, and K. augon-
saxxos are found on Acacia in the taxonomic section Juliflorae, whereas all other gall-
inducing thrips inhabitAcacia in the section Plurinerves (Mound et al. 1996). Of all of
the gall-inducers in this lineage, only 0. antennatus on A. adsurgens suffers from
much Koptothrips kleptoparasitism, and we have never found Koptothrips in galls of
0. sterni, K. augonsaxxos, 0. torus, or Ony. pilbara (Crespi, unpublished data).
Taken together, these observations suggest that gall-inducing thrips have three
distinct strategies for reducing the impact of Koptothrips: 'hiding' (living in tightly-
sealed galls, on host plants that may be less suitable for the kleptoparasites), 'fighting'
(maintaining soldier morphs), or 'running' (escaping in time, via an accelerated life cy-
cle). These latter two strategies are provided a striking parallel in gall aphids, some of
which also exhibit soldiers and long-lived galls, while others lack soldiers and develop
relatively rapidly (Moran 1993, Stern 1998). Our data also indicate that, in gall-induc-
ing thrips, each of the three strategies is more or less successful in different species.
The fourth pattern shown in our kleptoparasitism data is that, in contrast to the re-
sults for Koptothrips kleptoparasites, almost all species of gall-inducing thrips are
heavily attacked by species of parasites in other insect orders, primarily lepidopteran
and dipteran larvae (see also Mound et al. 1996). Some of these species feed upon gall
tissue, while others feed upon thrips eggs, and all cause a major reduction in thrips
numbers, if not total reproductive failure. Behavioral observations indicate that soldiers
are ineffective against lepidopteran larvae within their galls, because the larvae remain
within silken, frass-covered tunnels with only their sclerotized head capsule exposed
(Crespi, personal observation). Moreover, the caterpillars bite at soldiers that approach,
usually removing their antennae in the process, in a behavior that, if it represents an
adaptation, could be aptly termed 'sensory castration'. Analysis of the influences of the
various non-thysanopteran enemies of gall thrips on their life-histories and behavior
must await in-depth study of these enemies and their mechanisms of subversion.
What ecological factors might have ultimately led to the high kleptoparasitism
rates, and the differences among gall-inducing thrips species in kleptoparasitism
rates? Among Hymenoptera, factors promoting a high incidence of interspecific and
intraspecific kleptoparasitism include high host synchrony and density, and concom-
itant highly seasonal environments (Wcislo, 1987; see also Petanidou et al. 1995). In
accordance with Wcislo's hypothesis and results for Hymenoptera, the life cycles of al-
most all gall-forming thrips are normally highly synchronized by being tied to the
synchronous production of new foliage, which occurs either annually in the spring, or,
in highly-arid regions, unpredictably, after rare heavy rainfalls.
Florida Entomologist 82(2)
June, 1999
What can our analyses of kleptoparasitism in gall thrips tell us about host-para-
site interactions in social insects in general? One of the main findings of this study,
that gall thrips taxa with soldiers suffer rates ofKoptothrips kleptoparasitism at least
as high as those of related taxa without soldiers, compells reconsideration of the idea
that the presence of a complex social adaptation coincides with a high success rate of
that adaptation (see also Tallamy and Schaeffer 1997). Rather than viewing social be-
havior as an evolutionary pinnacle (e. g., Wilson 1971, 1990), perhaps it sometimes ac-
tually represents a relatively low and local adaptive peak, eroding and barely
maintained as soldiers and workers fight their way uphill under an onslaught of en-
emies. And although we might consider this pattern as leading to a pessimistic view
of life, we must recall that without such thieves, there might be no such beautiful an
adaptation as cooperation in an insect so otherwise-ignoble as a thrips.
ACKNOWLEDGMENTS
We thank the Natural Science and Engineering Research Council of Canada and
the National Geographic Society for financial support, and T. Chapman, R. Crozier, B.
Kranz, B. Maslin, D. Morris, T. Neville, N. Pierce, M. Schwarz, L. Vawter, J. Zammit,
and CSIRO Entomology for help with collection and logistics.
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Lloyd: Firefly Brachyptery and Wing "Polymorphism"
ON RESEARCH AND ENTOMOLOGICAL EDUCATION III:
FIREFLY BRACHYPTERY AND WING "POLYMORPHISM" AT
PITKIN MARSH AND WATERY RETREATS NEAR SUMMER
CAMPS (COLEOPTERA: LAMPYRIDAE; PYROPYGA)
JAMES E. LLOYD
Department of Entomology and Nematology
University of Florida, Gainesville 32611
ABSTRACT
The origin, evolutionary malleability, and sometimes loss of insect wings, gossa-
mer structures whose existence has reshaped the natural world, is one of the most in-
teresting and enigmatic dramas of insect biology. Lampyridae have long been known
for the reduced wings that occur in females of some genera, but in all previously
known examples it is a fait accompli, with little or no intraspecific variation. Such
variation occurs in and among populations of the little daytime firefly Pyropyga nig-
ricans, and also, among these populations there appears to be variation in sexual in-
volvement in the phenomenon, with brachypterous males also occurring at some
localities. This firefly provides an opportunity for students, both in summer classes
and as solitary individuals, to study the evolutionary biology of wings, from adaptive
significance to sexual selection and population ecology and genetics, to speciation, and
in a variety of habitats from strands on northern glacier lakes to southwestern mon-
tane stream sides and beyond, to west-coast marshes.
Key Words: Lampyridae, Pyropyga, brachyptery evolution, deme divergence, speciation
RESUME
El origen de las alas de los insects, su maleabilidad evolutiva, y algunas veces su
ausencia, son unos de los mas interesantes y enigmaticos dramas de la biologia de los
insects. Los Lampyridae se reconocen desde hace tiempo por las alas reducidas de las
hembras de algunos g6neros, y en todos los ejemplos conocidos anteriormente en esta
familiar las alas reducidas son un hecho con poca o ninguna variaci6n. Sin embargo,
polimorfismo en las alas ocurre entire poblaciones y entire individuos de una misma po-
blaci6n de la pequena luciernaga diurna Pyropyga nigricans, y tambien dentro de es-
tas poblaciones parece haber variaci6n en la participaci6n del fenomeno en la
atracci6n sexual. Esta luciernaga brinda una oportunidad a los estudiantes tanto en
classes de verano como individualmente para estudiar la biologia evolutiva de las alas
desde su significancia adaptativa en la selecci6n sexual, en la ecologia poblacional y
en la genetica, hasta la especiaci6n, y ademas en una variedad de habitats desde las
orillas de los lagos glaciares del norte hasta los bordes de riachuelos montanos en el
suroccidente y mas alla en los pantanos de la costa este.
In this symposium series I have passed along notes on the natural history of fire-
flies I have met in the field, as I might in written lectures (Letters) to an introductory
biology class, in the spirit of the initial introduction by John Sivinski. I continue here
with the story of a firefly that has no adult lantern nor nocturnal activity, but instead
uses pheromone communication in broad daylight. This is another illustration that
taxonomists-in this example the late John Wagoner Green-have valuable observa-
Florida Entomologist 82(2)
June, 1999
tions and speculations on their taxa that go unnoticed indefinitely, hidden away in es-
oteric papers, perhaps archived in personal field books after their authors have passed
on, unless we make special effort to help them out into the open. An informed teacher
can place such memorabilia in a larger biological context and use them as vehicles to
introduce, sketch, and add human interest to a general subject area. Publication of
such lessons makes these useful notes and essays available to others to initiate
projects at several levels of biological sophistication, beginning with field exploration
in particular, and should be encouraged as a legitimate method of primary publication.
This is what I do here, though the background and related information is abbreviated.
In this example, a cryptic treasure buried in the revision of a small and "not espe-
cially interesting" genus of Lampyridae was recalled by a teacher/researcher ("your
present author") who recognized the phenomenon in specimens collected by a student
doing a summer project. It involves shortcomings, so to speak, of firefly wings and
elytra, and why it is that such valuable adaptations as flight and protective body ar-
mament can be traded away or lost. The subtexts of the phenomenon, the "whys" of se-
lection and adaptation, and the wheree" of population divergence should invite the
attention and investigation of student and professional biologists.
In known cases of wing reduction in fireflies members of a species are short-
winged to approximately the same degree. In other words, the transformation events
are passages of the past, and in our time each is seemingly complete, a done deed as
they say. Cantharoid taxonomist Green discovered unique and perhaps yet unfinished
examples when he revised the genus of "little daytime fireflies," Pyropyga, in 1961.
The nominal species of interest occurs across North America and individuals of both
sexes are typically long winged. Green's two populations in which wings were shorter
than typical for this firefly were 2500 miles apart, embedded it would seem in an in-
finite number of local populations of long-winged individuals. In 1973 Terry Butler in-
vited my attention to some unusual specimens that she had found along the shore of
Douglas Lake in northern Michigan, at the University of Michigan Biological Station
(UMBS), near Pellston. With this as introduction, let us begin the lesson . after this
brief message: The Internet (electronic) publication of this paper has additional fig-
ures as InfoLink attachments to illustrate the text; these are color slides of the fire-
flies and their sites. These are cited in text here by their number as ILR figures.
Legends for InfoLink figures are included here in this printed version in the End
Notes section. These copyrighted illustrations may be used freely with this citation:
J. Lloyd, Univ. of Florida.
Letter XIX
On Becoming A Glowworm-The Disappearance Of Firefly Wings and Flight,
Over Time and Space (Lampyridae: Pyropyga nigricans)
When I am working on a problem, I never think about beauty. I think
only how to solve the problem. But when I have finished, if the solution
is not beautiful, I know it is wrong.
(R. Buckminster Fuller, architect)
Dear Fireflyers, The wings of insects fascinate many entomologists before their fu-
tures catch up with them and they become entomologists. I can imagine that soon af-
ter the painful light of conscious thought first glimmered in a hominids head, he and
she envied the wings of dragonfly and butterfly, for with them they would not have to
walk over rough ground all the way to a watering or wintering place. Entomologists
Lloyd: Firefly Brachyptery and Wing "Polymorphism"
attribute some of the great success of their beloved subjects to wings, whether success
is measured by the phenomenal number of species or the equally unbelievable num-
ber of life-styles and niches taken by them, or by their diversity of form. Insects do
more than fly with their wings. They rub them and broadcast rap, they wave them and
push molecules of sex pheromones toward potential mates, and in southeast Asia tree-
swarming fireflies use them as upper jaws of clamps that hold partners tightly,
against intrusions of pushy interlopers perched all 'round (Fig. 1).
With the adaptive advantages offered by wings, one must wonder why it is that
over evolutionary/geological time the females of several firefly species have greatly re-
duced and sometimes even lost theirs. How could such a conspicuous handicap be fa-
vored by natural selection? Unfortunately, in known cases of wing reduction in fireflies
all members of a species are short-winged to approximately the same degree. This
means that in each of these lineages the happening is in the past, and we can only ob-
serve products, not the process as it is occurring. Probably this is to be expected, for it
may require only a few tens or hundreds of generations to go to completion.
But, remarkably, there is one North American firefly that today, even now as you
read this, appears to be in the process of losing its wings, and this reduction seems to
be proceeding differently, to have reached a different condition in each of the few local
populations presently known to exist. If this is correct, this firefly is a living model for
evolution/adaptation studies, with something to teach us about how wings may some-
times be lost by fireflies. It may also show us how the gene pools of local populations
may become isolated from nearby parent populations, with each being a living exper-
iment and a unique step in a passage of possibility toward becoming a new species.
Fig. 1. Copulation clamp employed by a male of Pteroptyx valida in a firefly tree
near Bangkok, Thailand. The tip of the male's elytra are pushed under those of his fe-
male (at right) and tightly down against the top of her abdomen; at the same time the
tip of his abdomen is pushed up against hers from below, holding her in a vice-like grip.
Florida Entomologist 82(2)
June, 1999
The named species of promise is Pyropyga nigricans (Say) (Fig. 2), and as pres-
ently understood, this little daytime firefly occurs across northern United States and
southern Canada, and southward in the west into Mexico (Fig. 3). My education by
this firefly began in 1973 when Terry Butler, a student doing a project under my di-
rection at the University of Michigan Biological Station collected some remarkable
specimens with much-shortened wings along the shore of the "Bug Camp's" Douglas
Lake (Fig. 4). When I saw them I recalled that master taxonomist John Wagoner
Green (Fig. 5) had mentioned this phenomenon in his 1961 taxonomic revision of the
genus Pyropyga. In the section on P. nigricans he noted:
"In an interesting series [of specimens] collected by Peter Rubtzov at
Pitkin Marsh in Sonoma County, California, the elytra in both sexes are
definitely shortened, exposing several abdominal segments. In another
series, collected by the author on the shores of Lake Champlain, near
Plattsburg, NY, the same incipient brachyptery [short wingedness] is ev-
ident in the females but not in the males. Possibly this phenomenon is
associated with permanent moisture." (page 68)
The Pitkin marsh fireflies were collected during a botanical survey of the marsh in
1951-52. In 1990 Rubtzov sent me photos and additional information about the site;
Fig. 6 shows the spot where the fireflies were abundant. He wrote: "(the beetles were
especially numerous in an open, marshy area with very wet, soggy ground covered by
sedges and other wetland herbs ... there was no significant open water ... only a very
narrow, sluggish creek, overgrown by wetland vegetation, in the vicinity)" Green's
own Lake Champlain locality was probably a cobble beach, such as or perhaps even
the same one shown in Fig. 7 (ILR 1999, Fig. 1), where I found the fireflies in June
1998, 62 years after Green collected his series of specimens.
To put a repeatable, quantitative method into the evaluation of the wing-reduction
phenomenon, measurements are needed. This presents two problems, but both seem
to be manageable: (1) to see and measure flight wings of preserved dry specimens,
they first must be softened (relaxed), then one wing removed from beneath its elytron,
unfolded, and placed on a microscope slide. Fortunately there is a strong correlation
between elytra and flight wing lengths (Fig. 8). Thus, elytral length can be used as a
rapid and reliable indicator of flight wing length, and no dissection or specimen mu-
tilation is needed. (2) Flight wing and elytron lengths vary with specimen size; thus,
their lengths must be calibrated for overall body size. To do this, I divided the elytral
length of a each specimen by that specimen's pronotal width-body dimensions are
commonly used for such calibration in taxonomic keys (see sketch in Fig. 9). I will use
this ratio (quotient) to compare wing reductions among P. nigricans specimens of di-
verse body sizes. (Ear lengths in certain breeds of show dogs, when laid forward must
not reach the nose, to demonstrate appropriate "conformation to breed"!)
I borrowed and measured Greens two series of specimens from Pitkin Marsh and
Lake Champlain. In Fig. 9 note the vertical dotted line at ratio 2.25, which I placed to
separate Greens short- and long-winged specimens, cueing on and quantifying the
evaluation he made. I will use this line for reference in charts of measured P. nigri-
cans from other localities. What initially made Green's discovery especially interest-
ing, in addition to the virtual certainty that his two populations had not been in
genetic contact for some geological time, was that there was an apparent sexual dif-
ference in the occurrence of brachyptery. Let your mind run with this for a moment-
does this indicate significant differences between the two populations in alleles,
genes, strength of selection favoring brachyptery, immigration and the degree of iso-
lation from neighboring demes, mate choice and sexual selection, number of genera-
tions since the initial appearance of brachyptery in each population, stage of
Lloyd: Firefly Brachyptery and Wing "Polymorphism"
Fig. 2. Habitus of Pyropyga nigricans (Say), a carbon dust drawing by Laura Line.
This firefly was named Pyropyga fenestralis by Melsheimer in 1846, but Thomas Say's
name of 1823 has priority (see Green 1961).
Florida Entomologist 82(2)
nr Plattsburg, Lake Champlain
j ii : iiii i:, Douglas Lake \ .. :
Pitkin Marsh
Working distribution
of P. nigricans
Fig. 3. Distribution map of Pyropyga nigricans, with general distribution based on
locality labels of identified specimens. Green's two localities, Pitkin marsh in Sonoma
County, CA and Plattsburg on Lake Champlain in Clinton County, NY, and the loca-
tion of Douglas Lake in Cheboygan County in northern Michigan, are indicated.
Question marks indicate areas of uncertainty of occurrence perhaps only tempo-
rary gaps in my specimen data.
ecological succession of the site . or is it merely the result of sampling error (i.e.,
Green's small samples)?
Figure 10 shows the elytral ratios of specimens that Butler and I collected and
measured from various locations along the shoreline around Douglas Lake in 1973,
and Fig. 11 shows ratios of a sample I made 25 years later (ILR 1999, Fig. 2). Note that
the sexual involvement is different from that observed in either of Green's two sam-
ples, that the female ratio is bimodal (has two peaks) with separation falling near
Green's line, and that male ratios range broadly but never as low as those of females.
This pattern is also shown by Cheboygan County specimens that are archived in the
University of Michigan Museum of Zoology (Fig. 12). These specimens were collected
between 1917 and 1969, many from the Douglas Lake vicinity.
Are there more variations around unexplored lakes and marshes in North Amer-
ica? In the course of identifying fireflies for several museums I have viewed many spec-
imens of P. nigricans and measured some of them, to have size records, and have found
a few other brachypters. Some were archived in the American Museum (NYC) collec-
tion, and were collected in 1961 and 1964 at McMillan Camp near Silver City, NM, by
lepidopterist Frederick Rindge and his family (Fig. 13). Specimen labels indicated that
they were collected at 6800 feet elevation. Rindge replied to my letter of habitat in-
quiry, after consulting his field notes, that the camp was "situated in a rather small
river bottom, with a profusion of ponderosa pine, oak and junipers, plus a great assort-
ment of smaller trees and shrubs. But being in this rather narrow canyon, the stream
was always nearby." This location sounds to me as though it shares features with
shoreline strands, with unfriendly and isolating habitats on each side! Figure 14
shows the ratios of all of the other North American specimens I have measured.
June, 1999
Lloyd: Firefly Brachyptery and Wing "Polymorphism"
Fig. 4. A brachypterous female P. nigricans, originally photographed for me by
Gary Williams at the Bug Camp in 1973; this print was made from the original and is
of lesser quality. Note that the dorsal tip of her abdomen (pygidium) is narrowly
rounded; those of males are truncate. Her elytral ratio is 1.6.
Fig. 5. Taxonomist John Wagoner Green at his desk, about 1960. This photo was
provided by the California Academy of Sciences, where Green had taxonomized.
Florida Entomologist 82(2)
June, 1999
- ~ ~
2' *~ ". ~v~S
Fig. 6. P nigricans site in Pitkin Marsh, Sonoma County, CA; this photograph was
taken by the late Prof. William Hovanitz and provided to me by botanist Peter Rubtzov
(see text). Fireflies were most numerous in the area in front of the large shrub at the right.
Fig. 7. P. nigricans 1998 site near Plattsburg, NY on Lake Champlain. Green's site
was near, perhaps even this one. Fireflies occurred within a few feet of the water, on
sand and cobbles. This print was made from a color slide, and lacks the quality that a
monochrome negative would have given.
Lloyd: Firefly Brachyptery and Wing "Polymorphism" 17
6.4 .
6-
5.6-
52-
5.2 -
14.8 -
4.4-
4-
3.6-
3.2-
2.8
vo ..o''*
#33, female *
\ *- *
0 s@ *
S.-' #40, male
** S
*6' n=151
s *. r=0.96
.* * f(x) = 8.3E-1*x + 5.2E-1
SR^2 = 9.2E-1 E
3 3.4 3.8 4.2 4.6 5 5.4
Wing Length (nunm)
58 6'2 6.6
5.8 6.2 6.6
Fig. 8. Elytron length as a function of wing length, showing their strong correla-
tion. This permits the easily measured elytral length to be used to assess wing reduc-
tion. Measurements were made by Terry Butler and me.
( Shortened (micropterous) ---- "Normal" (macropterous)
Pitkin Mars
h
"Green's line"
Females, 9
Males, 19
1 I I I I I I I I I I I I I I I I
1,2 1,4 1.6 1.8 2 2.2: 2.4 2.6 2.8 3
3- Plattsburg
I2-
1J 0 Females, 3
Males, 7
pnw
i.I......*
ell
UT fI -
1.2 1.4 1.6
1.8 2 2.2 2.4 2.6
Elytra Ratio (ell/pnw)
Fig. 9. Quantification of elytral reduction occurring in each of Green's specimen se-
ries. Elytra ratio is the quotient of elytral length divided by pronotal width; note
sketch. Note that sexual involvement is different in the two samples.
2.8 3
Florida Entomologist 82(2)
June, 1999
1.8 2 2.2 2.4
Elytra Ratio (ell/pnw)
Figs. 10-12. Quantification of elytral reduction in Douglas Lake fireflies and vicin-
ity. Elytra ratio = elytral length/pronotal width. Note that sexual involvement is dif-
ferent from that seen in Green's two samples, shown in Fig. 9 (see text).
Now I excitedly ask, with anticipation, if we are seeing wing length in evolutionary
transition, are there brachypterous populations of different ages out there to be sam-
pled for comparison, to be found by wading around marshes and lakes in old tennis
shoes? One especially interesting exploration would be to follow the outlet of Douglas
Lake-the Maple River-and see whether (a younger population of?) brachypters oc-
cur at its mouth where it enters Burt Lake on its water's way to the St. Lawrence and
Atlantic (ILR 1999, Fig. 3). I found none where I looked near a boat ramp, nor at an-
other and unspoiled but accessible strand on this lake. Recalling Green's personal
field discovery, Lake Champlain has a long shoreline and many islands and streams.
My 1998 sample from near Plattsburg is similar in ratio to his 1936 sample (Fig. 15).
The map in Fig. 16 shows suspicious localities identified by ratio values (ratios < 2.25)
shown in Fig. 14.
There are many places to look, when you consider all of the thousands of glacier
lakes advertised by Minnesota, Wisconsin, and Michigan, to say nothing of lakes and
canyons scattered throughout the general range of P. nigricans (ILR 1999, Fig. 4).
Over the past century geologists have learned that the space that became Douglas
Lake began as a large, long-lasting chunk of ice, broken from the terminal end of a
melting, brittle glacier, leaving a pit (kettle) in the gravel, and that what is now firefly
shoreline has been developing in wind and waves and a changing water level for 9500
years. They also know that the climate has changed from cold and damp to warm, and
the surrounding forests, from spruce to pine to oak and other hardwoods. They also
tell us that Douglas Lake will eventually drain out the Maple River to Burt Lake. So
many lakes, so much happening, so little time ...
Lloyd: Firefly Brachyptery and Wing "Polymorphism"
1
:4*-- Green's line
6-
Females, 4
4 McMillan Camp NM Males,10
2- Males, 10
Fn EnH*
1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8 3
00
80l- 14 Females, 146
60 USA, general 0 Males, 205
0 A; I ; I I I I I
1.2 1.4 1.6 1.8 2 2.2 12.4 2.6 2.8 3
6 -Plattsburg NY
5 Green's Males, 7
4 Green's Females, 3
3- 1998 Males, 10 H
2 1998 Females, 8 I
1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8 3
Elytra Ratio (ell/pnw)
Figs. 13-15. Charts showing (13) elytral reduction in P. nigricans from a site in
New Mexico; (14) elytra ratio in a general sample of P. nigricans; and (15) a 1998
Plattsburg sample combined with Green's original sample. Elytra ratio = elytral
length/pronotal width. (see text)
I made a few observations on P. nigricans' mating behavior at Plattsburg and Dou-
glas Lake. Mating occurred from sunrise to midday, with males and possibly females
too being attracted to female pheromones (Fig. 17; ILR 1999, Fig. 5). Adults remained
within a few feet of the shoreline and after coupling they turned tail-to-tail; though
tiny, pairs were conspicuous on sand, gravel, and stones (ILR 1999, Figs. 6 and 7).
Winged males rarely flew, and when they did their flights were short, typically less
than a meter in length; I saw only one flying in 1998. Figures 18-20 show activity "pro-
files" made along beaches at the two localities. Larvae were found walking along
beaches at Douglas Lake within a meter of the waterline on damp sand (ILR 1999,
Fig. 8). I never found nocturnal activity by juveniles or adults.
To conclude and highlight, questions of natural selection happily arise-why are
individuals with shorter wings better at reproducing, at leaving offspring with their
alleles in such ecological situations, than are individuals with longer and flight-capa-
ble wings? This phenomenon in insects has been noted and considered by a succession
of naturalists for more than a century. The strand habitat, that is, the shorelines of
lakes, rivers, and oceans, and around islands, has often been associated with wing re-
duction and loss. Among possibilities that have been considered and that could fit
here: if this firefly gains little or nothing from flight, allelic substitutions from strong
selection in pleiotropic contexts could substitute alleles that produce reduced wings;
energetic savings realized by not building wings could be diverted into eggs or mate
Florida Entomologist 82(2)
Green's original localities
additional & possible sites
: working distribution
Fig. 16. Known and suspected P. nigricans brachypter locations. Isolated lakes and
montane canyons are promising situations.
Fig. 17. When females were placed in a net-covered dish on the Douglas Lake
beach males and females quickly approached (appeared) and walked up onto the net.
Inset shows male atop another, and their spatulate pygidia. Red mites are common on
these fireflies; there is one in the inset, spreading the lower male's wings.
June, 1999
Lloyd: Firefly Brachyptery and Wing "Polymorphism" 177
M; 5.5 6 6.5 7 7.5 8 8.4 9 9.5 10 10.5 11 11.7
> 1- Diogenes Point, Douglas L, 9 July 1998
1 15- 19 Mating Pairs
6 males abuptly on El Females
ageof emaMales
8.4 8.8 9.2 9.9 10.2 10.8 11.2 11.4 11.8 12.1 13.9
I I IB I I [ I l
8 8.5 9 9.5 10 10.5 11 11.5 12 12.5 13 13.5 14 14.5 15 15.5 16 16.5
Time Of Day (hours since midnight)
Figs. 18-20. Adult activity profiles for two sites. (18) A systematic census in the site
at Plattsburg; (19) a systematic census at a site on Douglas Lake; (20) a nonsystem-
atic collection of incidental counts made on several days at the Douglas Lake site.
search (and provide an advantage over short geological time); because flyers can be
blown over open water away from limited or narrow habitats, having wings may often
be fatal (a genetic lethal!) in such situations.
Of special interest in strand inhabiting P. nigricans, is whether their genetic iso-
lation from nearby, say, just-inland demes is primarily geographical (spatial), or if
mate choice and sexual selection have become involved and promote genetic isolation.
This consideration properly enlarged brings fireflyers into the realm of sympatric spe-
ciation models, which, in my view, is a too-neglected aspect of taxonomic thought for
insect fancying naturalists afield.
Perhaps it will be found that the population of fireflies in Pitkin Marsh, interpreted
for sake of mental jogging as nearing maturity, has proceeded further toward wing re-
duction stability than other P. nigricans now known. Maybe this population is very old
and began somewhere else, within walking distance of course, on a strand around a
now dried up pond or lake? Surely, when we have more data on these little daytime
fireflies, and now I explain this letter's obscure title, we will understand more of the
evolution of wing reduction and loss in luminous glowworm and lightningbug fireflies.
ENDNOTES
I thank John Sivinski, Steve Wing, and Jade Williams for reading the manuscript,
and Flora MacColl for technical assistance in the preparation of the manuscript and
Florida Entomologist 82(2)
June, 1999
for preparing the InfoLink attachments; Juan Manuel Alvarez for translating the ab-
stract into Spanish for the resume, Peter Rubtzov for photographs and ecological in-
formation on the Pitkin Marsh site; and Frederick Rindge for ecological information on
the McMillan Camp site. I thank the staff and administration of the University of
Michigan Biological Station (LIMBS) in 1973 and 1998, for use of their outstanding fa-
cilities and equipment, for bringing key references in their library to my attention, and
for their unstinting cooperation. I especially want to thank Terry Butler, the student
who saw something "peculiar" about the Douglas Lake brachypters and brought them
to me, and then collected and measured many of them; Gary Williams, for taking the
photograph of the firefly in Fig. 4 and teaching me the fundamentals of darkroom pho-
tography; and Jack Burch for his kind hospitality, answers to snail questions, and
barge piloting during the 1998 survey of sites along the circumference of Douglas Lake.
Archived specimens from several collections have been viewed over several years,
and I thank each of the curators and collection managers for loan of these specimens.
Their institutional affiliations and collections are here indicated by name and "Arnett
coden": Lee H. Herman, American Museum of Natural History (AMNH); Mark F.
O'Brien and Richard D. Alexander, Museum of Zoology, Univ. of Michigan (UMMZ);
Hugh Powell, Staten Island Museum; Norman D. Penny, California Academy of Sci-
ences (CASC); Jerry Pilney and Alan Morgan, Dept. of Earth Sciences, Univ. of Water-
loo, Canada; Robert E. Lewis, Dept. of Entomology, Iowa State Univ. (ISUI); Brett C.
Ratcliffe and Charlie Messenger, Systematics and Research Coll., Univ. of Nebraska
(DEUN); the late Floyd G. Werner, Dept. of Entomology Coll., Univ. Arizona (UAIC);
Roland L. Fischer, Michigan State Univ. Coll. (MSUC); Bruce Gill, National Museum
of Natural Sciences (CNCI), Canada; Robert H. Turnbow, Jr., Dept. of Entomology
Coll., Univ. of Georgia (UGCA).
The following enumerated statements are figure legends for color illustrations
(slides) that appear as InfoLink attachments to this article in the electronic publication
of this issue of the Florida Entomologist, and which are cited in text here as ILR 1999,
Fig.#: 1. The strand on Lake Champlain near Plattsburg where I made behavior obser-
vations in June 1998, and probably near and similar to Greens 1936 collection site. 2.
Diogenes Point on Douglas Lake; the July 1998 observation site was the open strand
seen to the right. 3. The Maple River, looking downstream just inside the outlet at the
southwest corner of Douglas Lake, where the stream begins its woodsy flow to Burt
Lake, 118 feet lower in elevation and a mile and a half in distance. 4. A stony strand on
the Ontario side of the Ottawa River in Canada, at about 46 N Latitude; to my eye it
looks much like the Plattsburg locality, but I found no P. nigricans. 5. A shorter-winged
male P. nigricans that has been attracted to a cage of females. Note the spatulate py-
gidium that readily identifies him as a male, and a female's silhouette in the cage below
the net. He feeds at least four red mites (Acarini), common parasites of shoreline in-
sects. 6, 7. Coupled pairs of P. nigricans on a cobble and on a twig on the shore of Lake
Champlain. Such pairs are easily spotted, and some (all?) remain coupled for hours. 8.
A wind-swept beach on North Fish Tail Bay, Douglas Lake, where 14 larvae were seen
(hunting?) along three feet of the shoreline on damp sand; all were within two feet of the
waters edge. Florida Agricultural Experiment Station Journal Series Number R-06817.
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ARNETT, R. J., AND G. ALLAN SAMUELSON. 1969. Directory of coleoptera collections of
North America (Canada through Panama). Dept. Entomology, Purdue Univ.
Lafayette. 123 pp.
BUSH, G. L. 1994. Sympatric speciation in animals: new wine in old bottles. Trends in
Ecology and Evolution. 9: 285-288.
Sivinski et al.: Kleptoparasitism and Phoresy 179
GREEN, J. W. 1961. Revision of the species of Pyropyga (Lampyridae). Coleopterists
Bulletin. 15: 65-74.
HESS, W. N. 1920. Notes on the biology of some common Lampyridae. Biological Bul-
letin. 38: 39-76.
LLOYD, J. E. 1972. Chemical communication in fireflies. Environmental Entomology.
1: 265-266.
LLOYD, J. E., AND S. R. WING 1981. Photo story (copulation clamp). Florida Entomol-
ogist 64(3): 459.
ROFF, D. A. 1986. The evolution of wing dimorphism in insects. Evolution. 40: 1009-
1020.
RUBTZOV, PETER. 1953. A phytogeographical analysis of the Pitkin Marsh. The Was-
mann Journal of Biology. 11: 129-219.
SCOTT, I. D. 1922. Inland Lakes of Michigan. Annual Report of Board of Geological
Survey for 1920. Lansing. 383 pages.
SPURR, S. H. 1956. Michigans forests over ten thousand years. Michigan Alumnus
Quarterly Review. 62: 336-341.
SPURR, S. H., AND J. H. ZUMBERGE. 1958. Late pleistocene features of Cheboygan and
Emmet Counties, Michigan. American Journal of Science. 254: 96-109.
WAGNER, D. L., AND J. K. LIEBHERR. 1992. Flightlessness in insects. Trends in Evolu-
tion and Ecology. 7: 216-220.
WING, S. R., J. E. LLOYD, AND T. HONTRAKUL. 1983. Mate competition in Pteroptyx
fireflies: wing cover clamps, female anatomy, and mating plugs. Florida Ento-
mologist. 66: 86-91.
Sivinski et al.: Kleptoparasitism and Phoresy
KLEPTOPARASITISM AND PHORESY IN THE DIPTERA
JOHN SIVINSKI1, STEVE MARSHALL2 AND ERIK PETERSSON3
1USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology
P. 0. Box 14565, Gainesville, FL 32604
2Department of Environmental Biology, University of Guelph
Guelph, Ontario, N1G 2W1, Canada
'Department of Zoology, Uppsala University
Villavagen 9, S-752 36 Uppsala, Sweden
ABSTRACT
Spiders, dung-feeding scarabs, social, and prey-storing insects provide predictable
and concentrated sources of food for a variety of thief flies (kleptoparasites) and their
larvae. Whenever waiting in the vicinity of the "host" for an opportunity to exploit its
resources is more energy efficient and less dangerous than foraging among hosts, a
number of intimate relationships between the fly and host may evolve. In extreme
cases, flies may become long-term phoretic associates that travel with hosts even
while the latter is in flight. The behaviors and ecologies of kleptoparasitic Diptera are
Florida Entomologist 82(2)
June, 1999
reviewed with special attention paid to the adaptations of Sphaeroceridae phoretic
upon Scarabaeidae. The mating systems of kleptoparasitic flies are influenced by the
type of resource that is stolen; flies associated with predators are mostly female, while
those found on scarabs are of both sexes. These differences are discussed in terms of
mate location, sperm competition, and mate choice.
Key words: Sphaeroceridae, Milichiidae, Chloropidae, mating system, mate choice
RESUME
Para una variedad de moscas ladronas (cleptoparasiticas) y sus larvas, las aranas,
escarabajos peloteros, insects sociales e insects que almacenan sus press son
fuente de alimento predecible y concentrada. Siempre que sea mas eficaz y menos pe-
ligroso el esperar en la cercania del hospedero para aprovecharse de sus recursos en
lugar de buscar alimento entire los hospederos, varias relaciones ecol6gicas intimas
entire la mosca y su hospedero podrian evolucionar. En casos extremos, las moscas
pueden volverse socios foreticos, viajando con sus hospederos mientras 6stos vuelan.
Se examinan el comportamiento y la ecologia de los dipteros cleptoparasiticos dandole
atenci6n especial a las adaptaciones de las moscas for6ticas Sphaeroceridae en Scara-
baeidae. El sistema de apareo de las moscas cleptoparasiticas es influenciado por el
tipo de recurso que se robe; las moscas asociadas con depredadores son en su mayoria
hembras, mientras que aquellas asociadas con escarabajos son de ambos sexos. Se dis-
cuten estas diferencias en cuanto a la localizaci6n de la pareja, competencia de la es-
perma, y la elecci6n de la pareja.
Thus what the world calls good business is only a way
To gather up the loot, pack it, make it more secure
In one convenient load for the more enterprising thieves.
Chuang Tzu, 250 B.C.
In this unpredictable and competitive world, many arthropods have found it adap-
tive to sequester, and sometimes personally guard, resources for their future use or
the use of their offspring. For example, some dung beetles spend many hours shaping,
moving, burying, and shielding a fecal fragment they may either eat, or into which
they may lay an egg (Halffter & Edmonds 1982). Caching results in a delay between
taking possession of a resource and its final consumption, and during this period own-
ers are vulnerable to thieves (kleptoparasites). Other invertebrates at risk from klep-
toparasites simply take a relatively long time to consume their food; e.g., certain web-
building spiders may take minutes to hours to masticate and preorally digest a victim.
Again, delay exposes predators to thieves, and the robbers that exploit both cachers
and slow-eaters are often small Diptera.
A number of these tiny kleptoparasitic flies have intimate relationships with their
larger "hosts" (Table 1). Some are phoretic and spend hours or days upon the bigger
animal, not feeding, but simply waiting for it to obtain the item the fly wishes to share.
In such cases it is presumably more efficient and less hazardous to wait for a partic-
ular host to obtain something valuable than it is to search for a host that happens to
be feeding or burying at that particular time. Other flies wait near their host and can
join it in an instant. The reasons for closeness are similar to those that have lead to
phoresy, but perhaps the lack of mobility inherent in phoresy or the danger of contin-
ually clinging to a giant has resulted in a looser association. In still other instances
kleptoparasites search out "wealthy" arthropods and contacts are brief and sporadic.
Sivinski et al.: Kleptoparasitism and Phoresy
TABLE 1. REPRESENTATIVES OF VARIOUS FORMS OF KLEPTOPARASITIC FLIES AND
WHETHER OR NOT THEY PRACTICE PHORESY. P = PHORESY, CA = CLOSE ASSO-
CIATION, I.E., FLIES REMAIN IN THE VICINITY OF THE "HOST" BUT NOT UPON IT,
A "?" AFTER A NOTATION REFLECTS A BELIEF THAT EITHER PHORESY OR CLOSE
ASSOCIATION IS PRACTICED BUT THAT UNEQUIVOCAL OBSERVATIONS ARE
MISSING, AND A "." REPRESENTS AN ABSENCE OF DATA.
Type of
Species Host Association Citation
Adult kleptoparasites of social insects (food thieves)
Apis mellifera P Askew 1971
Vestigipoda myrmolar-
voidea (Phoridae)
Termitophodrides het-
erospinalis (Phoridae)
Termitoxeniinae
(Phoridae)
Aenictus sp.
(Formicidae)
Cornitermes similis
(Isoptera)
Isoptera
Malaya spp. (Culicidae) Formicidae
CA Disney 1996
P Bristowe 1924
Disney &
CA Kistner 1997
Farquharson
CA 1918
Adult kleptoparasites of predatory arthropods (food thieves)
Gaurax sp. (Chloropidae) Araneidae
Phyllomyza sp. Nephila clavipes
(Milichiidae) (Araneidae)
Phyllomyza sp. Nephila clavipes
(Milichiidae) (Araneidae)
Rhinocornis cuspidatus
(Reduviidae)
Misumena vatia
(Thomisidae)
Bristowe, 1941,
P Ismay 1977
Robinson &
P Robinson 1977
Sivinski &
P (?) Stowe 1980
Desmometopa sorida
(Milichiidae)
Conioscinella spp.
(Chloropidae)
Neophyllomyza wulpi
(Milichiidae)
Anomoeoceros punctula-
tus (Chloropidae)
Olcella cinerea
(Chloropidae)
Olcella quadrivittata
(Chloropidae)
Olcella trigramma
(Chloropidae)
Argiope bruennichii
(Araneidae)
Argiope argentata
(Araneidae)
Scolopendra veridis
(Scolopendridae)
Ommatius minor
(Asilidae)
Araneidae
Nephila clavipes
(Araneidae)
Reduviidae
Asilidae
Mantodea
P Richards 1953
Robinson &
P Robinson 1977
P Sivinski 1985
P Biro 1899
P/CA Ismay 1977
CA Sivinski 1985
CA Marshall 1998
Sivinski 1985
Braula coeca
Reduviidae
Florida Entomologist 82(2)
June, 1999
TABLE 1. (CONTINUED) REPRESENTATIVES OF VARIOUS FORMS OF KLEPTOPARASITIC
FLIES AND WHETHER OR NOT THEY PRACTICE PHORESY. P = PHORESY, CA =
CLOSE ASSOCIATION, I.E., FLIES REMAIN IN THE VICINITY OF THE "HOST" BUT
NOT UPON IT, A "?" AFTER A NOTATION REFLECTS A BELIEF THAT EITHER PHOR-
ESY OR CLOSE ASSOCIATION IS PRACTICED BUT THAT UNEQUIVOCAL OBSERVA-
TIONS ARE MISSING, AND A "." REPRESENTS AN ABSENCE OF DATA.
Type of
Species Host Association Citation
Zodarium frenatum
(Zodariidae)
Argiope aurantia
Nephila clavipes
(Araneidae)
Nephila clavipes
(Araneidae)
Zelus trimaculatus
(Reduviidae)
Nephila clavipes
(Araneidae)
Araneida
Reduviidae
Araneida
Reduviidae
Thomisus onuustus
(Thomisidae)
Phidippus multiformis
(Salticidae)
Nephila clavipes
(Araneidae)
Didactylomyia longimana Nephila clavipes
(Cecidomyiidae) and other Araneida
Culicoides bauri
(Ceratopogonidae)
Atrichopogon sp.
(Ceratopogonidae)
Microphor obscurus
(Empididae)
Microphor crassipes
(Empididae)
Megaselia sp. (Phoridae)
Lonchaea chorea (F.)
(Lonchaeidae)
Nephila clavipes
(Araneidae)
Araneidae
Araneidae
Araneidae
Nephila clavipes
(Araneidae)
Enoplognatha ovata
(Clerk) (Theridiidae)
Harkness &
CA Ismay 1975
Sivinski &
CA Stowe 1980
Eisner et al.
(?) 1991
Robinson &
Robinson 1977
Sivinski &
Stowe 1980, Eis-
ner et al. 1991
Sivinski 1985
Eisner et al.
CA (?) 1991
Mik 1898
Biro 1899
Mik 1898
Biro 1899
Knab 1915
Frost 1913
Eisner et al.
CA (?) 1991
Sivinski &
CA Stowe 1980
Sivinski &
Stowe 1980
Downes &
Smith 1969
Downes &
Smith 1969
Laurence 1948
Sivinski &
Stowe 1980
Dobson 1992
Trachysiophonella pori
(Chloropidae)
Paramyia nitens
(Milichiidae)
Neophyllomyza spp.
(Milichiidae)
Milichiella sp.
(Milichiidae)
Desmometopa m-atrum
(Milichiidae)
Desmometopa
singaporensis
(Milichiidae)
Desmometopa m-nigrum
(Milichiidae)
Desmometopa latipes
(Milichiidae)
Desmometopa sp.
(Milichiidae)
Sivinski et al.: Kleptoparasitism and Phoresy
TABLE 1. (CONTINUED) REPRESENTATIVES OF VARIOUS FORMS OF KLEPTOPARASITIC
FLIES AND WHETHER OR NOT THEY PRACTICE PHORESY. P = PHORESY, CA =
CLOSE ASSOCIATION, I.E., FLIES REMAIN IN THE VICINITY OF THE "HOST" BUT
NOT UPON IT, A "?" AFTER A NOTATION REFLECTS A BELIEF THAT EITHER PHOR-
ESY OR CLOSE ASSOCIATION IS PRACTICED BUT THAT UNEQUIVOCAL OBSERVA-
TIONS ARE MISSING, AND A "." REPRESENTS AN ABSENCE OF DATA.
Type of
Species Host Association Citation
Lonchaea laticornis Meig. Enoplognatha ovata
(Lonchaeidae) (Theridiidae)
Setisquamalonchaea
fumosa (Egger)
(Lonchaeidae) Araneida
Dobson 1992
Dobson 1992
Larval kleptoparasites of oviposition ingress (thieves of developmental resources)
Taeniostola limbata Cyrtotrachelus sp. Kovac &
Hendel (Tephritidae) (Curculionidae) P Azarae 1994
Larval Kleptoparasites of social insects (thieves of developmental resources)
Myrmecophilous Phoridae Formicidae CA Disney 1994
Cataclinusa pachycondy-
lae (Phoridae) Formicidae P Wheeler 1910
Larval kleptoparasites of prey storing insects (thieves of developmental resources)
Miltogrammine
(Sarcophagidae) Sphecidae, Vespidae CA Evans 1966
Lepidophora spp.
(Bombyliidae) Sphecidae, Vespidae Hull 1973
Lasiopleura grisea Bembix cameroni
(Chloropidae) (Sphecidae) Evans 1973
Larval kleptoparasites of dung-feeding scarabs (thieves of developmental resources)
Ceroptera rufitarsis
(Sphaeroceridae)
Ceroptera sivinskii
(Sphaeroceridae)
Ceroptera longicauda
(Sphaeroceridae)
Ceroptera longiseta
(Villeneuve)
(Sphaeroceridae)
Ceroptera nasuta (Ville-
neuve) (Sphaeroceridae)
Ceroptera equitans (Col-
lin) (Sphaeroceridae)
Biroina myrmecophila
(Sphaeroceridae)
Norrbomia lacteipennisi
(Sphaeroceridae)
Scarabaeus sacer
(Scarabaeidae)
Geotrupes egeriei and
others (Scarabaeidae)
Peltotrupes pofundus
Mycotrupes gaigei
(Scarabeidae)
Pachylomera sp.
(Scarabaeidae)
Catharius sp.
(Scarabaeidae)
Scarabaeus gangeticus
(?) (Scarabaeidae)
Cephalodesmius ar-
miger (Scarabaeidae)
Scarabaeidae
P Lesne 1896
Sivinski 1983
Marshall &
Montagnes 1988
J. S., pers. obs.
P Roubaud 1916
P Roubaud 1916
Fletcher 1909,
P Collin 1910
Montieth &
P Storey 1981
P Steyskal 1971
Florida Entomologist 82(2)
June, 1999
TABLE 1. (CONTINUED) REPRESENTATIVES OF VARIOUS FORMS OF KLEPTOPARASITIC
FLIES AND WHETHER OR NOT THEY PRACTICE PHORESY. P = PHORESY, CA =
CLOSE ASSOCIATION, I.E., FLIES REMAIN IN THE VICINITY OF THE "HOST" BUT
NOT UPON IT, A "?" AFTER A NOTATION REFLECTS A BELIEF THAT EITHER PHOR-
ESY OR CLOSE ASSOCIATION IS PRACTICED BUT THAT UNEQUIVOCAL OBSERVA-
TIONS ARE MISSING, AND A "." REPRESENTS AN ABSENCE OF DATA.
Type of
Species Host Association Citation
Norrbomia frigipennis Many species of
(Sphaeroceridae) Scarabaeidae including
the genera Canthon,
Phanaeus, and
Onthophagus P Sivinski 1983
Norrbomia singularis Canthon spp. and Copris
(Sphaeroceridae) spp. (Scarabaeidae) P Sivinski 1983
Pterogramma sp. Canthon pilularius,
(Sphaeroceridae) Phanaeus spp. and
others (Scarabaeidae) CA Sivinski 1983
In this examination of thievery and phoresy we first review the various forms of
kleptoparasitism, and make a distinction between flies that feed upon the resources
of the host (adult kleptoparasites) and those who put their offspring in a position to
steal (larval kleptoparasites). Particular attention is called to those species that prac-
tice phoresy and other forms of close association, and the advantages and difficulties
of staying near the host are discussed. We point out that phoretic kleptoparasites
sometimes accumulate in high densities on hosts, and that this intimacy has affected
other parts of the flies' natural history, notably their sexual behaviors. The various
mating systems of phoretic kleptoparasites are compared and contrasted, and hypoth-
eses are offered about the roles of mate searching, mate choice, and sperm competition
in their evolution. Finally, we consider the vulnerability of different types of re-
sources, and whether accessibility has influenced the diversity of various kleptopar-
asite guilds.
Adult Kleptoparasites (Particularly of Predaceous Arthropods)
Certain invertebrate predators are untidy eaters whose insect prey may be drip-
ping with hemolymph and digestive secretions, and torn open to expose organs and
fats. Such soups are repasts for various milichiid and chloropid flies, who lick up fluids
either from the surface of the prey or from the predator's jaws (Fig. 1).
Spiders are the most commonly noted mounts of phoretic kleptoparasites. The
chloropid Guarax sp. has been collected from orb-web spiders (Bristowe 1941, Ismay
1977), and a group of eleven Panamanian milichiids, Phyllomyza sp., was observed on
the cephalothorax of the araneidNephila clavipes (L.) over a period of four days (Rob-
inson & Robinson 1977). Another (?) Phyllomyza sp., was found upon N. clavipes in
Florida (Sivinski & Stowe 1980).
Other phoretic associations include the milichiid Desmometopa sorida (Fall6n)
which rides the backs of reduviids (Richards 1953) and a Florida chloropid, Conios-
cinella sp. mounted on the scolopendromorph centipede, Scolopendra veridis Say (Siv-
inski 1985). Biro (1899) observed up to three individuals of the New Guinean milichiid
Sivinski et al.: Kleptoparasitism and Phoresy
Fig. 1. Acalypterates feeding on the hemipteran prey of the large spider Nephila
clavipes. One individual is perched upon the chelicera of its host, while another can be
seen with a fluid droplet in its mouthparts. Kleptoparasitic flies often imbibe consid-
erable amounts and swell up to a substantial girth. (Photograph by J. S.)
Neophyllomyza wulpi Hendel (as Desmometopa minutissima Wulp) perched on the
thoraxes of the asilid Ommatius minor Doleschall. By removing and marking phoret-
ics, he discovered that they quickly remounted hosts from distances of up to 12 paces.
Pairs of riding milichiids were common and they would take a position between the
robber fly's wings, one facing forward and the other back (see also Kertesz 1897, Mik
1898).
The majority of adult food-kleptoparasites are not phoretic, but many seem to be
closely associated with hosts nonetheless (Table 1, see Sivinski 1985 and cit.). Some
species appear to wait near predators and gather at a kill in a matter of seconds. For
example, the Floridian chloropid Olcella cinerea (Loew) can instantaneously arrive on
the freshly captured prey of Nephila clavipes (Sivinski 1985), and Olcella quadrivittata
(Sabrosky) can quickly find certain kinds of prey items being consumed by mantids and
asilids (Marshall 1998). The cecidomyid Didactylomyia longimana (Felt) consumes the
liquified prey of spiders and is one of the rare instances of adult feeding in the family
(Sivinski & Stowe 1980). It also rests in spider webs, hanging by its front legs with its
tarsi placed between adhesive droplets. While nonkleptoparasitic cecidomyids also
hang in webs, the habit might have additional advantages for a kleptoparasite.
Still other kleptoparasites appear to forage widely and may not be "waiters" at all.
At least some of these flies use volatiles from the defensive compounds of the prey to
locate a meal. Coreidae and Pentatomidae trapped by spiders are particularly attrac-
tive to milichiids such as Paramyia nitens (Loew), Neophyllomyza sp., Milichiella sp.,
and Desmometopa sp. (Eisner et al. 1991, Aldrich & Barros 1995). One component of
the defensive sprays of these bugs, trans-2-hexanol, attracts kleptoparasites when ap-
plied to dead moths whose bodies are not normally fed upon by the flies (Eisner et al.
1991). Other kinds of prey items, including Acanthosomatidae and Staphylinidae,
Florida Entomologist 82(2)
June, 1999
with strong defensive chemicals have also been associated with kleptoparasitic flies
(Marshall 1998), but most species of kleptoparasitic acalypterates have been collected
from aculeate Hymenoptera carcasses in the process of being eaten. There is also
some evidence that predator digestive secretions are attractive to Didactylomyia
longimana, and a phorid and a ceratopogonid species (Sivinski & Stowe 1980). Much
remains to be discovered about chemical cues and the foraging of thief flies.
In addition to specialized kleptoparasites there are instances of certain Empid-
idae, Anthomyiidae, and Sarcophagidae feeding in spider webs, but this feeding may
be opportunistic (Irwin 1978). Recently, several species of lonchaeids have been seen
partaking of spider's prey in English gardens and doing so in a careful and methodical
manner that suggests specialization (Dobson 1992).
Caution is an admirable quality in a kleptoparasite that has to deal with the formi-
dable dangers of a gargantuan predator and perhaps an entangling web. The empidid
Microphor crassipes Macquart is a frequent prey of its spider host (Laurence 1948, see
also the toll spiders take of kleptoparasitic panorpids, Thornhill 1978). Paramyia ni-
tens, in spite of extremely elongate mouthparts that should aid it to safely sup between
a spider's jaws, is sometimes captured and killed by its host (Sivinski & Stowe 1980).
McCook (1889) found a similar fly "trussed up near the spot where it had lately fed."
The threat posed by a predator may dictate the degree of intimacy between the
kleptoparasite and its host. While phoresy might allow the quickest response to a cap-
ture and be competitively superior to waiting farther away from a limited resource, it
could also be more perilous. A sort of compromise may occur in the Ugandan chloropid
Anomoeoceros punctulatus Becker which hovers, even in strong winds, directly below
the chelicerae of web-building spiders (Ismay 1977).
Just as solitary predators obtain and hold desirable resources, so too do social in-
sects which transport high-value foodstuffs from the field to their colonies. Like soli-
tary predators, social insects also attract the attentions of kleptoparasitic flies.
Phoretic adults of Braula coeca Nitzsch (the bee louse) feed on liquids taken from the
mouths of honey bees (Askew 1971). The Brazilian phorid Termitophodrides het-
erospinalis Borgmeier is also phoretic and rides on the backs of worker termites (Bris-
towe 1924). Calliphoridae in the Old World genus Bengalia feed either as
kleptoparasites or as facultative predators of various ant genera from which they
snatch prey or brood (Maschwitz & Schonegge 1980). Mosquitoes in the genus Malaya
also steal food from ants, hovering over their mouths and some cases even tapping the
ant's antennae to solicit regurgitation (Farquharson 1918). Two phorid species are
known to solicit food from ants (Disney 1994), and one milichiid feeds on the anal
droplets of workers (Jacobson 1909). Perhaps the most remarkable association be-
tween an adult kleptoparasite and a social insect host is that of the recently discov-
ered Malaysian phorid Vestigipoda myrmolarvoidea Disney and ants of the genus
Aenictus (Disney 1996). Females of the fly are legless, wingless, larviform myrmeco-
philes which live in the ant colony, where they are apparently fed and cared for by the
worker ants. Many Phoridae are larval kleptoparasites of ants and termites (e.g. Wil-
son 1971, Disney & Kistner 1997), and in many species females have greatly reduced
wings, but no other phorid adults are known to be as integrated into the host social
structure as is V myrmolarvoidea.
Larval Kleptoparasites (Particularly of Aculeate Hymenoptera and Dung-feeding
Scarabs)
Obtaining food for offspring, rather than for oneself, is the second great "motive"
for kleptoparasitism by Diptera, and often for adult phoresy as well. This category is
a complex one, and the nearly invariable relationship between phoresy and kleptopar-
Sivinski et al.: Kleptoparasitism and Phoresy
asitism when only adults consume the resources of the host (phoretic adults are klep-
toparasites) is not necessarily the case in instances where eggs are laid by phoretic
adults in the vicinities of their associates (not all phoretic adults have kleptoparasitic
larvae). The distinction requires some initial scrutiny, and we discuss flies that are
phoretic but which probably take nothing of importance from their mounts nor com-
pete with its offspring. Following this we examine the two best described forms of lar-
val kleptoparasitism. First we review kleptoparasitism of aculeate Hymenoptera, and
the sometimes close associations kept by the adults and larvae of such flies with their
hosts. We then turn to some of the most common and easily observed kleptoparasites,
the diverse and tenaciously phoretic Sphaeroceridae that ride upon dung beetles and
lay eggs in the feces sequestered by their hosts.
The Reasons for Phoresy in Flies That Oviposit in the Vicinities of Other Arthropods
(Kleptoparasitism vs Inquillinism). There are various "motives" for the phoretic rela-
tionships of adult flies who lay their eggs in the vicinities of other arthropods, and not
all of these phoretic flies are kleptoparasites. However, in most cases of phoresy,
whether involving a kleptoparasite or not, a larval resource associated with the
mount is unpredictably available, and the best way to exploit it is to wait on the spot
for its sudden appearance. One phoretic fly that is not a kleptoparasite is the sphaero-
ceridAcuminiseta pallidicornis Villeneuve, which rides on the backs of giant (20 cm)
millepedes in West Cameroon (Disney 1974, Roubaud 1916). It apparently breeds in
millipede droppings and mounted flies wait for their hosts to defecate (riding phorids
on the same hosts may also lay their eggs in the feces, Schmitz 1939, see also phoretic
insects that develop in the dung of sloths, Waage & Montgomery 1976, Ratcliffe 1980,
and macropodids, Norris 1991). Some species of Sphaeroceridae and Drosophilidae
are phoretic on terrestrial crabs for similar reasons, but lay eggs on the hosts and
have larvae which stay on the host and develop in the microbe-rich waste material
that accumulates on the "felt glands" (Gomez 1977, Carson 1967).
Alternatively, the medium in which the larvae of phoretic flies develop is not just
a byproduct of the larger animal, but a valuable resource that has been sequestered
or produced by the host. For example, a tephritid, Taeniostola limbata Hendel, lays its
eggs in the oviposition holes bored by large weevils into bamboos (Kovac & Azarae
1994). One or two individuals will spend hours on the elytra of the beetle waiting for
it to complete its laborious chore, then hop off and be the first to lay their eggs. If the
fly larvae compete with the beetle grub for food or space, then T limbata could be cat-
egorized as a kleptoparasite. The two major forms of larval kleptoparasitism are re-
viewed below.
Kleptoparasites of Aculeate Hymenoptera. Nests of social Hymenoptera and food
stores of solitary Hymenoptera support a wide variety of kleptoparasitic larval
Diptera, although it is sometimes difficult to distinguish between kleptoparasitic and
scavenging habits among the former group. In some cases the association between the
larval kleptoparasite and its host is quite close, as in the phorid Cataclinusa pachy-
condylae (Brues), which attaches itself to a host ant larva and steals food as its asso-
ciate is fed masticated prey (Wheeler 1910). Other myrmecophilous phorid larvae are
highly specialized, though not phoretic, and are groomed and fed by worker ants (Dis-
ney 1994).
Food stores of solitary aculeates are an obvious target for theft, and are attacked
by a wide variety of specialized kleptoparasites. Both pollen-storing (Moradeshaghi &
Bohart 1968) and flesh-storing species are robbed by larval miltogrammine Sarcoph-
agidae. Adult miltogrammines are usually closely associated with the nesting area
rather than the adult host itself, typically mating nearby and larvipositing in or
around the entrance to the host nest. Some miltogrammines, especially the genus Se-
notainia, are more closely associated with the adult host, and have earned the name
Florida Entomologist 82(2)
June, 1999
"satellite flies" for their habit of tracking foraging adult sphecid wasps. Satellite flies
deposit larvae in the nest or on prey as it is being carried into the nest (Evans 1966).
Other Miltogramminae (Ptychoneura spp.) deposit fully incubated eggs directly on the
host (Day & Smith 1981). Larval kleptoparasites of solitary aculeates are also found
in the Bombyliidae and Chloropidae. Species of the bombyliid genus Lepidophora de-
velop on the provisions of Vespidae and Sphecidae (Hull 1973), and the chloropid
Lasiopleura grisea Malloch has been reared from the nests of the sphecid Bembix
cameroni (Evans 1966).
Kleptoparasites of Dung-feeding Scarabs. A diverse group of kleptoparasitic Sphaero-
ceridae ride upon dung-feeding scarabs in order to reach oviposition sites (Chobaut 1896,
Roubaud 1916, Villeneuve 1916, Fletcher 1909, Collin 1910, Moulton 1880, Knab 1915,
Steyskal 1971, Fig. 2). In fact, the term "phoresy" was coined by Lesne (1896) to describe
the behavior of the sphaerocerid Ceroptera rufitarsis Meigen riding on the "Sacred
Scarab", Scarabaeus sacer L., in the sand dunes behind Algerian holiday beaches.
The clumped and ephemeral nature of dung and its often substantial food value
(e.g., human feces are ~50% bacteria) can result in fierce competition among its con-
sumers (Wilson 1971, Bartholomew & Heinrich 1979, Rabkin & Silverman 1979). A
number of scarabs avoid such competition by burying caches of feces, both for their
own consumption and as food for their larvae. Burials can occur either near the drop-
ping, in which case the burrow may be relatively deep (e.g, Phanaeus spp.), or the fe-
ces can be shaped into a ball and rolled a considerable distance before being buried in
a shallow burrow (e.g., Canthon spp.). In one Florida cattle pasture the feces cached
by scarabs contained 11x fewer Nematocera, 7x fewer nonphoretic Sphaeroceridae, 4x
fewer Cyclorrhapha, and 6x fewer predaceous insects than the above ground "pats"
from which the buried dung had been detached (Sivinski 1983).
These less-contested caches are in turn exploited by kleptoparasites, which in-
clude not only flies but even tiny phoretic Scarabaeidae (Hammond 1976). Of course
by sidestepping many small competitors the kleptoparasite is confronted with a single
very large one, the beetle itself. But scarabs are messy eaters, and there is often a good
deal left over, some smeared into the burrow walls. In the laboratory, the numbers of
offspring of the kleptoparasite Norrbomia frigipennis (Spuler) developing in food
caches of the ball-rolling scarab Canthon pilularius (L.) decreased 63% when the bee-
tle was also included (Sivinski 1983, the extraordinary range of adult size in this spe-
cies may reflect some broods facing exceptional nutritional difficulties). A thief fly
might also have the opportunity to oviposit in a more long lasting "brood ball" contain-
ing the offspring of the beetle, although there are special problems associated with
this situation including parent beetles removing foreign insects from the dung mass
and the encasing of the feces in soil (e.g. Halfter 1997).
In Florida there is a number of kleptoparasitic sphaerocerids, including a species
with reduced eyes, Ceroptera sivinskii Marshall, that principally attaches itself to
beetles that start their burrows under feces, and a mostly crepuscular species, Norr-
bomia singularis (Spuler) (Sivinski 1983, Marshall 1983). There is even a species,
Ceroptera longicauda Marshall, that exploits a "non-dung beetle", the scarab Peltotru-
pis profundus Howden which may bury decaying organic material or fungus (J. S.,
personal observation., see also the Australian scarab Cephalodesmius armiger West-
wood which constructs brood masses from green leaves and its kleptoparasite Biroina
myrmecophila (Knab & Malloch) [Montieth and Storey 1981]). The most abundant
kleptoparasitic species in north Florida is the previously mentioned Norrbomia fri-
gipennis, an attractive black fly with white wings and red eyes. It rides upon a broad
range of "rolling" and "burying" scarab hosts (Sivinski 1983), although in the labora-
tory it has a slight preference for species of Phanaeus, which are among the larger of
the available dung beetles (Petersson & Sivinski 1997).
Sivinski et al.: Kleptoparasitism and Phoresy
Fig. 2. The phoretic sphaerocerid Ceroptera longicaudata upon the geotrupin My-
cotrupes gaigei Olson & Hubbell. This fly rides on species of the related genus Pel-
totrupes. The burrows of these beetles are often very deep (sometimes 3>m), and at
such depths their brood materials are likely to be safe from most other thieves and
predators. (Photograph by S. M.)
The seasonal pattern of N. frigipennis abundance in north Florida may reflect the
advantages of kleptoparasitism (Sivinski 1983). In late winter and early spring the
community of Diptera developing in bovine dung undergoes a change. Nematocera,
particularly Sciaridae and nonphoretic sphaerocerids, become less numerous while
calypterates, principally Sarcophagidae, increase rapidly. It may be that the large,
quick growing flesh flies competitively exclude most sphaerocerids. Norrbomia fri-
gipennis is an exception to the trend, its numbers continue to expand, perhaps be-
cause it avoids contact with calypterates by ovipositing in scarab dung stores.
While kleptoparasitism appears to be a means of avoiding competition and unfa-
vorable environmental conditions the benefits of phoresy are more obscure, especially
in light of the considerable costs in terms of time. Mature adult sphaerocerids of many
species, includingN. frigipennis, ride their hosts underground and once buried cannot
leave until they accompany the departing beetle to the surface (Sivinski 1983). Newly
closed adults are prodigious diggers, but this does not seem to be the case once their
exoskeletons harden. A fly can expect to spend a day, and perhaps several days or
more, buried alive with its host, a sizable portion of a -10-12 day life span.
Why stay with a particular scarab? Why not go from beetle to beetle depositing
eggs in the dung that each is rolling or pushing into its burrow? In fact some klepto-
parasites, Ceroptera longiseta (Villeneuve) and C. nasuta (Villeneuve) from central Af-
rica, ride beetles as they move feces but oviposit as the balls are being buried and do
not get trapped beneath the surface (Roubaud 1916). An unidentified Florida Ptero-
gramma spp. follows scarabs rather than rides and appears to oviposit on dung as it
Florida Entomologist 82(2)
June, 1999
disappears underground (Sivinski 1983, see a Mexican species with similar following
habits in Halffter & Matthews 1966). Why don't other kleptoparasites subscribe to
this seemingly more sensible practice? Perhaps the eggs could be damaged as the feces
are manipulated and packed into a burrow. Whatever the reason, N. frigipennis were
only reared from dung caches that had been buried for at least 4 hours (Sivinski 1983).
When oviposition is best accomplished underground, flies need to stay close to a host
that might dig out of sight at any second. Given the need to stay close, it is probably
cheaper to ride the beetle than to walk behind it. It may also be safer to be attached to
one of the larger and least vulnerable animals in the dung-feeding community. Preda-
tors abound around droppings, and some, such as the reduviid Apiomerus crassipes
Fab., even appear to follow fecal odors in order to locate hunting grounds (Sivinski
1983; an African Ceroptera sp. rides underneath scarabs, suggesting a predator that
can glean flies from a beetles dorsum, [Hanstrom 1955-67]). When flies are committed
to a beetle it might further be prudent to stay with it as it flies from one dropping to an-
other and so avoid the risk of not finding a host in a new location. Norrbomia frigipen-
nis clings to flying scarabs, particularly species of Phanaeus, and up to a dozen or so
flies can be seen packed into forward-facing ranks on the great and glittering protho-
rasic shield of a male P. index MacLeay as it buzzes by (see Vulinec 1997).
The Distribution of the Sexes in Flies Phoretic upon Predators and Dung Beetles
With a few revealing exceptions to be discussed later, the flies from all six families
that are found upon predators or their prey are females (Sivinski 1985 and cit.; see
however records for occasional male milichiids and lonchaeids in Eisner et al. 1991,
and Dobson 1992). Presumably it is only females that require proteins, probably for
egg production. But why don't males take advantage of female concentrations in order
to find mates?
There are two general reasons why males might not be found in the same places
as females (Thornhill & Alcock 1983). The first is that the females in certain locations
have no sexual value. Suppose females of a particular species control copulations and
mate only once. As a consequence males will search for virgins and tend to accumulate
at emergence sites (or swarm sites; see Sivinski & Petersson 1997). By the time fe-
males are feeding or ovipositing they are likely to have already been inseminated,
making it too late for males to look for sexual encounters in such spots. Mosquitoes
provide a commonly encountered example of this phenomenon (Sivinski 1984). For
the most part the bloodthirsty legions hovering about our heads and the flanks of cat-
tle are composed entirely of females that have copulated previously, over small water-
filled containers, pond margins, or swarm markers.
The second reason males may not search for females at a feeding site is that the
resources are too abundant relative to the numbers of females. The low probability
that a female will be at any particular spot makes foraging among sites, or loitering
at a site, an expensive and time-consuming business. Some of the predator kleptopar-
asites seem to be very rare (see Sivinski 1985), and males could search among spiders
or wait around a particular web for a very long and unrequited time before encoun-
tering a mate. Presumably, males would instead either concentrate their efforts
around oviposition/emergence sites (probably decaying vegetation and seeds or grass
tillers in the case of milichiids and chloropids, Ferrar 1987, Teskey et al. 1976) or par-
ticipate in swarms or leks at "encounter-convention" sites (e.g. Parker 1978).
Which, if either, of these explanations accounts for seldom seen predator-klepto-
parasite males is unknown, although the second, an unfavorable ratio of females to
feeding sites, has a shred of circumstantial support. Matings on the bodies of preda-
tors and on their prey have been observed in two species of the chloropid genus Olcella
Sivinski et al.: Kleptoparasitism and Phoresy
Fig. 3. An unusual sight, mating by the predator-kleptoparasite Olcella quadriuit-
tata on prey held by its robber fly host. Typically, only females of such flies are found
on or near the "host", and mating in association with a predator has only been ob-
served in a few species of this genus. (Photograph by S. M.).
(Sivinski 1985, Marshall 1998, Fig. 3), both of which appear to be "waiters", i.e., they
instantly appear on prey captured by spiders, robber flies, and possibly mantids. Both
species can be unusually abundant at certain times and places. Perhaps high popula-
tions of females make it profitable for males to also wait around large predators. A
higher female to host predator ratio means males have a reasonable expectation that
females will show up at any particular host.
Among dung beetle-kleptoparasites everything is different. Males are as common
as females on the backs of scarabs and flies engage in repeated copulations both above
and below ground (Fig. 4). In laboratory arenas female N. frigipennis spent an average
of 25% of their time repeatedly mating (in one case 70%, Sivinski 1983). It is the po-
tential for multiple inseminations that is probably responsible for males following a
relatively few females underground and consequently diminishing their chances of
finding new mates. Typically, sperm from the last of a series of inseminations are used
to fertilize most of the eggs a female lays (Parker 1970). Because oviposition occurs un-
derground, the opportunity for the valuable last mating is beneath the surface as well.
In some instances, large numbers of flies and hosts might even allow both male
and female flies to choose a mount on the basis of its sexual opportunities, i.e., the pro-
spective mates and sexual rivals already on board the scarab. These kinds of choices
would be reflected in the composition of beetle-back groups. Large and small groups
of N. frigipennis on the ball-rolling scarab C. pilularis tend to have female-biased sex
ratios (Sivinski 1982, Petersson & Sivinski unpub.). When the patterns of male and fe-
male abundances are compared to random distributions, the sex ratio biases appear
to be due largely to males being less numerous than expected in small groups and fe-
males being much more common in large groups than chance would predict. It is plau-
sible that a male would avoid unoccupied beetles or those with a few other flies
Florida Entomologist 82(2)
June, 1999
Fig. 4. A group ofNorrbomia frigipennis wait and mate upon the head and protho-
racic shield of a male of the dung feeding scarab Phanaeus index. This is a common
association in Florida, and the fly can be found riding beetles as they walk on the sur-
face, burrow in the ground, and fly through the air. (Drawing by Kevina Vulinec).
aboard, otherwise he could wind up underground without a sexual partner. On the
other hand, a female, particularly a mated female, might benefit from belonging to a
small group because her offspring would face fewer competitors. But, if this is the
case, why are females "over represented" in large groups? Perhaps there are sexual
reasons. Either virgin females or females seeking superior mates would have a
greater pool of sexual partners to sample in larger groups.
There is some support for the notion that some mated females do not prefer large
groups (Petersson& Sivinski, unpub.). In a laboratory experiment where mated and
virgin N. frigipennis of both sexes had a choice of mounting one of a pair of beetles
with different numbers of freeze-dried conspecifics glued to the elytra, the only signif-
icant response was that mated females avoided large groups. In keeping with the ar-
gument that virgins would prefer larger groups, there was a significant positive
Sivinski et al.: Kleptoparasitism and Phoresy
correlation between the proportion of virgin females in field collected groups and the
size of the groups.
The notion that at least some females prefer a large sample of prospective mates
supposes that they can choose from what is available or, in the absence of choice, that
the "fittest" males on beetle-back have greater access to females. There is no obvious
male courtship in N. frigipennis that would serve to advertise desirable characteris-
tics. However, large size is an easily perceived trait that might indicate "genetic qual-
ity" or be advantageous in competitions between males. If so, it might also be a quality
females would like to see inherited by their sons. In the laboratory where large and
small males were placed with a single female, the proportion of large male encounters
with females that lead to copulation was significantly higher than those involving
small males (Sivinski 1984). It could be that females preferred large males and were
more likely to acquiesce, or that large males were better able to force themselves onto
uncooperative females. It also appears that male-male competition filters out the
smaller males and makes them less likely to contact females. Small males are just as
liable as large to initiate an interaction with another male, but they are much less
likely than large males to encounter females. This suggests that the vicinities around
females are "controlled" by large males who exclude smaller rivals. There is also a
negative correlation between male size and the proportion of time actually spent on
scarabs, as opposed to following behind them. Again, perhaps larger males are able to
dispossess the smaller and keep them from locating mates.
Conclusion: Kleptoparasite Diversity
Flies are the master thieves of their world. Take for example the predictably lo-
cated and exposed food-treasures suspended in a spider's web. Only the formidable
owner and her entangling snare stand in the way of a surfeit of protein, and a number
of bold arthropods take the risk for the reward. Among these are other spiders (e.g.
Vollrath 1979), a mirid bug (Davis and Russell 1969), scorpionflies (Thornhill 1975),
damselflies (Vollrath 1977), fireflies (Provonsha 1998), and even Lepidoptera larvae
(Robinson 1978). But no other kleptoparasitic group, of insects at least, seems to be as
abundant, or as diverse, as the Diptera. Much the same may be said for the insects
found infesting the dung-stores of scarabs, and flies, particularly species of Phoridae,
are a major component of the "food-sharing" fauna living in the underground nests of
social insects (e.g. Wilson 1971; Disney & Kistner 1997).
However, there appear to be differences in diversity within these various klepto-
parasite guilds. For example, the symbionts of dung beetles are largely (entirely?)
Sphaeroceridae, although flies of this family are certainly not the only Diptera found
near feces. The only known exception in north Florida is a sort of proto-kleptoparasit-
ism practiced by the sarcophagid Ravinia derelicta (Walker) which preferentially
larviposits in the dung balls of Canthon pilularis and in the soft, moist "work faces"
on the feces where the beetles labor (Sivinski 1983). On the other hand, the dipteran
kleptoparasites of spiders include species of Milichiidae, Chloropidae, Lonchaeidae,
Phoridae, Empididae, and even Nematocera in the families Ceratopogonidae and Ce-
cidomyiidae.
The barriers these different types of hosts place around their resources must differ
in permeability to the flies that prowl outside them. Perhaps the subterranean nature
of food stores in scarabs and ground-dwelling social insects presents a more formida-
ble problem to the typical fly than the open air exposure of prey held in jaws or sus-
pended in a web. The above ground nests of social wasps and bees may be even more
impenetrable. Only the tiny bee louse, apparently alone among all of the sugar-seek-
ing flies, has been able to exploit the riches of the honeybee.
Florida Entomologist 82(2)
June, 1999
ACKNOWLEDGMENT
We thank Jim Lloyd, Denise Johanowicz, and Sid Mayer for many helpful com-
ments on earlier drafts of the manuscript. Jim Lloyd deserves further gratitude for
showing J.S. his first phoretic fly. Valerie Malcolm prepared the manuscript, and Gina
Posey helped gather and organize the often obscure and peculiar literature of klepto-
parasitism.
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Florida Entomologist 82(2)
June, 1999
DEDICATION OF 1998 ARMYWORM SYMPOSIUM TO
DR.BILLY RAY WISEMAN: PLANT RESISTANCE EXPERT
DAVID J. ISENHOUR1 AND FRANK M. DAVIS2
1DeKalb Genetics Corp., 3100 Sycamore Road, DeKalb, IL 60115
2USDA/ARS, P.O. Box 5367, Mississippi State, MS 39762
ABSTRACT
Dr. Billy Ray Wiseman of et al. the United States Department of Agriculture, Ag-
ricultural Research Service, Insect Biology & Population Management Research Lab-
oratory at Tifton, GA has authored or co-authored over 300 refereed scientific papers,
book chapters, review papers and/or bibliographies dealing primarily with plant re-
sistance to insect pests, especially lepidopterans attacking corn and sorghum. He and
his co-workers have released over 80 germplasm lines of corn and sorghum resistant
to the fall armyworm, Spodoptera frugiperda (J. E. Smith), corn earworm, Helicov-
erpa zea (Boddie), and sorghum midge, Contarinia sorghicola (Coquillett), during his
31 years of federal service. Additionally, his field and laboratory techniques are widely
used by researchers around the world.
Key Words: Fall armyworm, host plant resistance
RESUME
El Dr. Billy Ray Wiseman del Departamento de Agricultura de los Estados Unidos,
Servicio de la Investigaci6n Agricola, Laboratorio de Investigaciones sobre la Biologia
del Insecto y el Manejo de Poblaciones, en Tifton, GA, ha producido o co-producido mas
de 300 escritos cientificos arbitrados, capitulos de libros, resenas y/o bibliografias que
tratan principalmente sobre resistencia de las plants a insects plaga, especialmente
insects lepid6pteros que atacan al maiz y al sorgo. Durante sus 31 anos de servicio
federal, 61el y sus colegas han plantado mas de 80 lineas de germoplasma de maiz y
sorgo que son resistentes al gusano cogollero del maiz, Spodoptera frugiperda (J. E.
Smith), al gusano del elote del maiz, Helicoverpa zea (Boddie), y a la mosquita del
sorgo, Contarinia sorghicola (Coquillett). Adicionalmente, sus tecnicas de campo y de
laboratorio son utilizadas por investigadores en todo el mundo.
The 1998 Armyworm Symposium is dedicated to Dr. Billy Ray Wiseman (Fig. 1),
for his many contributions to plant resistance, especially to corn and sorghum insect
pests.
Billy was born March 28, 1937, as the fourth child of Calvin and Beulah Wiseman
of Sudan, TX. He was raised on a farm and received all of his secondary education
from the Sudan school system. His high school activities included sports (football and
basketball) and being a member and officer of the Future Farmers of America. Billy's
senior year was highlighted when named valedictorian of his class.
After graduation, he entered Arlington State College and finished his undergrad-
uate B.S. Degree in Agricultural Education at Texas Tech in 1959. His graduate de-
grees were earned from Kansas State University under the direction of Dr. Reginald
Painter, the father of host plant resistance to insects. In 1961, Billy received a M.S.
Armyworm Symposium '98: Isenhour & Davis
V
Fig. 1. Dr. Billy Ray Wiseman: Plant Resistance Expert.
^: *^c
Florida Entomologist 82(2)
June, 1999
Degree with a double major in Entomology and Horticulture. At this point, he ob-
tained a direct commission as an officer in the U.S. Army Medical Service Corp and
served about three years in the Womack Army Hospital's Preventive Medicine Section
at Fort Bragg, NC. It was during this period that he met an Army nurse named Gladys
Mary Striegler from Hye, TX. A romance began that led to their marriage on Novem-
ber 2, 1963.
After completion of military duty, Billy and Gladys returned to Kansas State Uni-
versity where he pursued a doctoral degree in Entomology. October 3, 1966 was a spe-
cial day in Billy's life. On this day, Billy passed his final Ph.D. orals and Gladys had
their first child, William Samuel Wiseman II. Two years later they became the proud
parents of a daughter, Amy Lucretia.
Billy began his professional career in 1967 at Stillwater, OK with ARS-USDA under
the supervision of entomologist, Harvey Chada. After a year, he transferred to what
was then called the Southern Grain Insects Research Laboratory (ARS-USDA) at Tif-
ton, GA where he has served as a research entomologist for the last 31 years. Billy has
worked under the directorship of H. C. Cox, Alton Sparks and Charlie Rogers.
During his career, he has authored or co-authored over 300 refereed scientific pa-
pers, including 13 book chapters, review papers or bibliographies (see list of fall ar-
myworm papers). His ability to work effectively with his colleagues is evidenced by co-
authoring papers with over 110 scientists. Additionally, he and his co-workers have
released 80 corn and sorghum germplasm lines having resistance to either the fall ar-
myworm (Spodoptera frugiperda (J. E. Smith)], corn earworm [Helicoverpa zea (Bod-
die)], or sorghum midge [Contarinia sorghicola]. Billy has continuously transferred
useful technologies to his colleagues in the areas of field screening of corn and sor-
ghum for resistance to insect pests, bioassaying for antibiotic plant compounds in the
laboratory, and determining mechanisms and bases of resistance. Also, he was a mem-
ber of the team that discovered the chemical compound, maysin, as the major antibi-
otic factor in silks of some corn genotypes to the fall armyworm and corn earworm.
Along with his research duties, Billy found time to teach two courses in plant re-
sistance at the University of Florida. For 17 years, he traveled to Gainesville on the
weekends to teach students principles of plant resistance and methodologies used in
developing insect resistance plants and in understanding the mechanisms and bases
of resistance. During these years he also served as graduate advisor for two Ph.D. stu-
dents and as a committee member for four other students.
Incredibly, Billy, a highly productive bench scientist and part-time teacher, also
found the time and energy to provide leadership and service to regional and national
entomological societies, corn and sorghum groups and plant resistance workshops
and symposiums. He chaired the Entomological Society of America's (ESA) member-
ship committee, served as president of the Southeastern Branch of ESA and as the
Branch's representative on the ESA Governing Board. He was one of the organizers
of the Southeastern Branch's Armyworm Symposium. Recently, Billy was one of three
organizers of two international symposiums on the development of corn resistant to
insects held at CIMMYT in Mexico. Proceedings of these symposia provide present
and future researchers with a foundation of information on entomological and plant
breeding techniques used to develop resistant corn and recent advances and utiliza-
tion of resistant germplasm. Anyone that has worked with Billy on a conference, sym-
posium or committee soon realizes how efficient and prompt this man is in completing
tasks assigned him.
Through the years, Billy's peers have recognized him as an outstanding scientist
and cooperator, as an effective entomology leader and as an expert in plant resistance
to insects. The following are comments from his peers concerning their thoughts of Billy.
Armyworm Symposium '98: Isenhour & Davis
Dr. Wiseman's contributions to fall armyworm control are well-known through his
many scientific reports and resistant germplasm releases. Without question these ac-
complishments have earned him the deserved reputation of host plant resistance ex-
pert. Dr. Wiseman's colleagues know him as a scientist who, whether a leader or
member of a team, will always give more than is expected to the research effort. Per-
haps one of his greatest contributions to armyworm research is how he always in-
spires and assists other researchers to do their best. From the beginning of my career
in entomology, and especially during the past several years, I have benefited greatly
from his mentorship.
I have been associated with Billy Wiseman for over thirty years. He has been a
gentleman, an outstanding teacher and researcher. He understood host plant resis-
tance when I first met him, but since then he has added much scientific information
to our research base. Billy has studied several crops and several insects and their in-
teractions. He is an authority for host plant resistance with corn and the corn ear-
worm and fall armyworm in the field and in the laboratory. Dr. Wiseman is one of the
most cooperative scientists I know. He has freely shared his research information, his
talent for presenting it, as well as the research tools he has developed. Billy's nature
motivates scientists to work cooperatively and collaboratively and makes the world a
better place to live as he has shared his talents around the world.
Billy Wiseman is a hard worker, dedicated to increasing our knowledge and under-
standing of plant resistance to insects. You can count on his use of appropriate exper-
imental design, statistical analysis and interpretation of the data. His interests
extend beyond the mechanisms of plant resistance to interactions between plant re-
sistance and other control strategies such as the use of insect pathogens, parasitoids
and predators and their potential use in integrated pest management. His love of
teaching has helped to keep him current on developments in his area of specialty and
made him willing to take the time to explain things to cooperators who come from a
different specialty. Billy's enthusiasm and cooperative nature have made it a joy to
work with him to investigate interactions between plant resistance and insect patho-
gens of fall armyworm and corn earworm.
Is Billy Wiseman an expert in host plant resistance? You bet he is! He has spent his
career looking at how those crawling creatures interact with so many important crop
plants. This does, however, bring up a very important question: Why is he so good at
what he does? I think I know the answer. If a DNA analysis of Billy were to be run,
the results would probably show a positive match with several corn and sorghum
pests. This would help to explain why he knows those pests so well. He is also a posi-
tive match with his colleagues. I have cooperated with Billy on many research projects
over the past several years. I know him to be an excellent researcher and he is totally
unselfish when it comes to sharing data and publishing results. Billy is top notch.
I have known Dr. Billy Wiseman for just a little over 10 years. Yet, it seems like I
have known him twice as long. From my perspective, these were all positive experi-
ences. During this time, I have had a good opportunity to see some of his contributions
toward the betterment of humanity. He has a continual willingness to aid others with-
out looking for recognition-a true team player. When I worked at the IBPMRL in Tif-
ton, although we were on separate projects, Billy did not hesitate to offer suggestions
from his years of experiences. I appreciated his professionalism and quickly recog-
nized and respected his depth of knowledge of host plant resistance, and other sub-
jects. I have published with Billy and because I value his frankness and expertise, I
have also asked him to review some of my manuscripts. Not only do I much appreciate
his helpful comments, but he always returns the reviews so quickly! Thanks for help-
ing my career along in so many ways. Traveling by car to distant meetings provides a
Florida Entomologist 82(2)
June, 1999
good opportunity to foster a closer bond with colleagues. It was always a good pleasure
to travel with Billy. I recall his long patience and his much agreeableness. Also, I have
had the pleasure to become acquainted with his family; he is obviously a caring hus-
band and father. It has been a good pleasure to share part of the highway of life with
Billy. Thanks for being such a good role model.
It has been both an extreme privilege and a great benefit to me to have had the op-
portunity to be both a cooperator and friend of Bill Wiseman. I cannot imagine how
lacking my career and my life would have been had I not known him.
Not only do his peers consider him an expert in plant resistance to insects but
some have nominated him for special recognition. Some honors that Billy has received
are: Fellow of the Entomological Society of America; J. E. Brussart Award (Southeast-
ern Branch of ESA); Achievement Award from the Florida Entomological Society for
Significant Contributions to the Science and Technology of Plant Resistance to In-
sects, and Achievement Award of Excellence as Senior Scientist, USDA-ARS, South
Atlantic Area.
Dr. Billy R. Wiseman has distinguished himself as an expert in plant resistance to
insects, a highly productive scientist, a mentor to students and colleagues, an extra
special collaborator, a leader in entomological activities and a true gentleman. There-
fore, it is our pleasure and honor to dedicate the 1998 Armyworm Symposium to Dr.
Billy Ray Wiseman-Plant Resistance Expert.
A Listing of B. R. Wiseman's Fall Armyworm Publications
(1966-1997)
WISEMAN, B. R., R. H. PAINTER, AND C. E. WASSOM. 1966. Detecting corn seedling dif-
ferences in the greenhouse by visual classification of damage by the fall army-
worm. J. Econ. Entomol. 59: 1211-1214.
WISEMAN, B. R. 1967. Resistance of corn, Zea mays L., and related plant species to the
fall armyworm, Spodoptera frugiperda (J. E. Smith). Dissertation. Kansas
State University. 198 pp.
WISEMAN, B. R., C. E. WASSOM, AND R. H. PAINTER. 1967. An unusual feeding habit
to measure differences in damage to 81 Latin American lines of corn by the fall
armyworm, Spodoptera frugiperda. Agron J. 59: 279-281.
WISEMAN, B. R., R. H. PAINTER, AND C. E. WASSOM. 1967. Preference of first instar fall
armyworm larvae for corn compared with Tripsacum dactyloides. J. Econ. En-
tomol. 60: 1738-1742.
MCMILLIAN, W. W., M. C. BOWMAN, R. L. BURTON, K. J. STARKS, AND B. R. WISEMAN.
1969. Extract of chinaberry leaf as a feeding deterrent and growth retardant
for larvae of the corn earworm and fall armyworm. J. Econ. Entomol. 62: 708-
710.
WISEMAN, B. R., AND W. W. MCMILLIAN. 1969. Competition and survival among the
corn earworm, the tobacco budworm, and the fall armyworm. J. Econ. Entomol.
62: 734-735.
WIDSTROM, N. W., W. W. MCMILLIAN, AND B. R. WISEMAN. 1970. Resistance in corn
to the corn earworm and the fall armyworm. IV. Earworm injury to corn in-
breds related to climatic conditions and plant characteristics. J. Econ. Entomol.
63: 803-808.
WISEMAN, B. R., W. W. MCMILLIAN, AND N. W. WIDSTROM. 1970. Husk and kernel re-
sistance among maize hybrids to an insect complex. J. Econ. Entomol. 63: 1260-
1262.
WISEMAN, B. R., W. W. MCMILLIAN, AND M. C. BOWMAN. 1970. Retention of laboratory
diets containing corn kernels or leaves of different ages by larvae of the corn
earworm and the fall armyworm. J. Econ. Entomol. 63: 731-732.
MCMILLIAN, W. W., A. N. SPARKS, B. R. WISEMAN, AND E. A. HARRELL. 1972. An eco-
nomical high capacity freeze-dryer. J. Georgia Entomol. Soc. 7: 64-67.
Armyworm Symposium '98: Isenhour & Davis
MCMILLIAN, W. W., AND B. R. WISEMAN. 1972. Separating egg masses of the fall ar-
myworm. J. Econ. Entomol. 65: 900-903.
WIDSTROM, N. W., B. R. WISEMAN, AND W. W. MCMILLIAN. 1972. Resistance among
some maize inbreds and single crosses to fall armyworm injury. Crop Sci. 12:
290-292.
WISEMAN, B. R., R. JOHNSON, N. W. WIDSTROM, AND W. W. MCMILLIAN. 1972. A sor-
ghum planter for small experimental plots. Agron. J. 64: 557-558.
WISEMAN, B. R., D. B. LEUCK, AND W. W. MCMILLIAN. 1973. Effects of fertilizers on
resistance of Antigua corn to fall armyworm and corn earworm. Florida Ento-
mologist. 56: 1-7.
WISEMAN, B. R., J. FRENCH, W. W. MCMILLIAN, AND J. W. TODD. 1973. Insecticide
treatment to reduce loss in yield of sorghum caused by sorghum insects.
J. Georgia Entomol. Soc. 8: 123-126.
WISEMAN, B. R., D. B. LEUCK, AND W. W. MCMILLIAN. 1973. Effect of crop fertilizer on
feeding of larvae of fall armyworm on excised leaf sections of corn foliage.
J. Georgia Entomol. Soc. 8: 136-141.
WISEMAN, B. R., W. W. MCMILLIAN, D. B. LEUCK, AND N. W. WIDSTROM. 1973. Host
plant resistance and its relationship to insect population suppression, pp. 40-
42 in Proc. FAO/IAEA Training Course on Use of Radioisotopes and Radiation
in Entomology. 123 pp.
WISEMAN, B. R., W. W. MCMILLIAN, AND N. W. WIDSTROM. 1973. Insect resistance
studies on sorghum at Southern Grain Insects Research Laboratory, pp. 59-60
in Proc. 8th Bien. Grain Sorghum Res. Util. Conf., Lubbock, TX.
LEUCK, D. B., B. R. WISEMAN, AND W. W. MCMILLIAN. 1974. Nutritional plant sprays:
Effect on fall armyworm feeding preferences. J. Econ. Entomol. 67: 58-60.
WISEMAN, B. R., W. W. MCMILLIAN, AND N. W. WIDSTROM. 1974. Techniques, accom-
plishments, and future potential of breeding for resistance in corn to the corn
earworm, fall armyworm, and maize weevil, and in sorghum to the sorghum
midge, pp. 381-393 in F. G. Maxwell and F. A. Harris [eds.], Proc. Summer Inst.
on Biological Control of Plant Insects and Diseases, Univ. Press of Mississippi,
Jackson. 647 pp.
MCMILLIAN, W. W., N. W. WIDSTROM, AND B. R. WISEMAN. 1976. Yield losses in South
Georgia field corn resulting from damage by several insects. J. Georgia Ento-
mol. Soc. 11: 208-211.
WISEMAN, B. R., N. W. WIDSTROM, AND W. W. MCMILLIAN. 1976. Techniques for eval-
uating for plant resistance in corn to corn earworm and fall armyworm, pp. 11-
12 in Proc. 2nd Biennial HPR Workshop, Tucson, AZ.
MARTIN, P. B., AND B. R. WISEMAN. 1979. Management of fall armyworms in the
southeastern U.S.: the fall armyworm problem in grain sorghum. 11th Biennial
Grain Sorghum Research and Utilization Conf. 11: 10-11.
WISEMAN, B. R. 1979. Integrated control of sorghum insects in the U.S. 11th Biennial
Grain Sorghum Research and Utilization Conf. 11: 14-17.
WISEMAN, B. R., AND F. M. DAVIS. 1979. Plant resistance to the fall armyworm. Flor-
ida Entomologist. 62: 123-130.
WISEMAN, B. R., AND F. M. DAVIS. 1979. A flow chart for plant resistance investiga-
tions, pp. 194-196, in Proc. FAO/IAEA Training Course on Use of Radioisotopes
and Radiation in Entomology.
GARDNER, W. A., B. R. WISEMAN, P. B. MARTIN, AND E. F. SUBER. 1980. Insect pests
of sorghum: description, occurrence, and management, pp. 16-27 in R. R. Dun-
can [ed.], Proc. Sorghum Shortcourse, The Univ. of Georgia Coll. of Agric. Exp.
Stns. Spec. Pub. No. 6. 44 pp.
MARTIN, P. B., B. R. WISEMAN, AND R. E. LYNCH. 1980. Action thresholds for fall ar-
myworm on grain sorghum and Coastal bermudagrass. Florida Entomologist.
63: 375-405.
MCMILLIAN, W. W., B. R. WISEMAN, AND N. W. WIDSTROM. 1980. Dent and sweet
corns: Influence of defoliation, plant age, and genotype on yield. J. Georgia En-
tomol. Soc. 15: 373-377.
Florida Entomologist 82(2)
June, 1999
WISEMAN, B. R., F. M. DAVIS, AND J. E. CAMPBELL. 1980. Mechanical infestation de-
vice used in fall armyworm plant resistance programs. Florida Entomologist.
63: 425-432.
WISEMAN, B. R., B. G. MULLINIX, AND P. B. MARTIN. 1980. Insect resistance evaluations:
Effect of cultivar position and time of rating. J. Econ. Entomol. 73: 454-457.
WISEMAN, B. R., AND N. W. WIDSTROM. 1980. Comparison of methods of infesting
whorl-stage corn with fall armyworm larvae. J. Econ. Entomol. 73: 440-442.
GARDNER, W. A., B. R. WISEMAN, P. B. MARTIN, AND E. F. SUBER. 1981. Identification
and control of lepidopterous pests of grain sorghum, pp. 11-16 in R. R. Duncan
[ed.], Proc. of the Grain Sorghum Shortcourse, The Univ. of Georgia Coll. of Ag-
ric. Exp. Stns. Spec. Pub. No. 8. 57 pp.
MCMILLIAN, W. W., B. R. WISEMAN, AND N. W. WIDSTROM. 1981. An evaluation of se-
lected sorghums for multiple pest resistance. Florida Entomologist. 64: 198-
199.
WISEMAN, B. R., N. W. WIDSTROM, AND W. W. MCMILLIAN. 1981. Fall armyworm re-
sistant corn variety identified. USDA News Release SR 61-81. 1 p.
WISEMAN, B. R. 1981. Infestations of FAW in sorghum: greenhouse and field methods.
12th Biennial Grain Sorghum Research and Utilization Conf. 12: 98.
WISEMAN, B. R., AND W. P. MORRISON. 1981. Components for management of field
corn and grain sorghum insects and mites in the United States. USDA-ARS
ARM-S-18. 18 pp.
WISEMAN, B. R., W. P. WILLIAMS, AND F. M. DAVIS. 1981. Fall armyworm: resistance
mechanisms in selected corns. J. Econ. Entomol. 74: 622-624.
WISEMAN, B. R., N. W. WIDSTROM, AND W. W. MCMILLIAN. 1981. Effects of 'Antigua
2D-118' resistant corn on fall armyworm feeding and survival. Florida Ento-
mologist. 64: 515-519.
GROSS, H. R., JR., J. R. YOUNG, AND B. R. WISEMAN. 1982. Relative susceptibility of a
summer-planted dent and tropical flint corn variety to whorl stage damage by
the fall armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 75: 1153-1156.
WISEMAN, B. R., AND L. GOURLEY. 1982. Fall armyworm (Lepidoptera: Noctuidae): in-
festation procedures and sorghum resistance evaluations. J. Econ. Entomol.
75: 1048-1051.
WISEMAN, B. R., R. C. GUELDNER, AND R. E. LYNCH. 1982. Resistance in common cen-
tipedegrass to the fall armyworm. J. Econ. Entomol. 75: 245-247.
LYNCH, R. E., W. G. MONSON, B. R. WISEMAN, AND G. W. BURTON. 1983. Bermuda-
grass resistance to the fall armyworm (Lepidoptera: Noctuidae). Environ. En-
tomol. 12: 1837-1840.
WILLIAMS, W. P., F. M. DAVIS, AND B. R. WISEMAN. 1983. Fall armyworm resistance
in corn and its suppression of larval survival and growth. Agron. J. 75: 831-832.
WISEMAN, B. R., F. M. DAVIS, AND W. P. WILLIAMS. 1983. Fall armyworm: larval den-
sity and movement as an indication of nonpreference in resistant corn. Protect.
Ecol. 5: 135-141.
WISEMAN, B. R., L. GOURLEY, AND H. N. PITRE. 1983. Some studies of resistance to the
fall armyworm. Proc. 13th Biennial Grain Sorghum Research and Utilization
Conf. 13: 135.
WISEMAN, B. R., AND N. W. WIDSTROM. 1984. Fall armyworm damage ratings on corn
at various infestation levels and plant development stages. J. Agric. Entomol.
1: 115-119.
WISEMAN, B. R., R. C. GUELDNER, AND R. E. LYNCH. 1984. Fall armyworm (Lepi-
doptera: Noctuidae) resistance bioassays using a modified pinto bean diet. J.
Econ. Entomol. 77: 545-549.
WISEMAN, B. R., H. N. PITRE, L. GOURLEY, AND S. L. FALES. 1984. Differential growth
responses of fall armyworm larvae on developing sorghum seeds incorporated
into a meridic diet. Florida Entomologist. 67: 357-367.
CHANG, N. T., B. R. WISEMAN, R. E. LYNCH., AND D. H. HABECK. 1985. Fall armyworm
(Lepidoptera: Noctuidae) orientation and preference for selected grasses. Flor-
ida Entomologist. 68: 296-303.
Armyworm Symposium '98: Isenhour & Davis
CHANG, N. T., B. R. WISEMAN, R. E. LYNCH, AND D. H. HABECK. 1985. Influence of N
fertilizer on the resistance of selected grasses to fall armyworm larvae. J. Agric.
Entomol. 2: 137-146.
CHANG, N. T., B. R. WISEMAN, R. E. LYNCH, AND D. H. HABECK. 1985. Fall armyworm:
expressions of antibiosis in selected grasses. J. Entomol. Sci. 20: 179-188.
ISENHOUR, D. J., B. R. WISEMAN, AND N. W. WIDSTROM. 1985. Fall armyworm (Lepi-
doptera: Noctuidae) feeding responses on corn foliage and foliage/artificial diet
medium mixtures at different temperatures. J. Econ. Entomol. 78: 328-332.
WISEMAN, B. R. 1985. Types and mechanisms of host plant resistance to insect attack.
Insect Sci. Applic. 6: 239-242.
WISEMAN, B. R., H. N. PITRE, AND S. L. FALES. 1985. A laboratory bioassay for sor-
ghum resistance to the fall armyworm. Proc. 14th Biennial Grain Sorghum Re-
search and Utilization Conf. 14: 63.
WISEMAN, B. R. 1985. IPM of fall armyworm and panicle caterpillars in sorghum, pp.
219-226, in Proc. of the International Sorghum Entomology Workshop, 15-21
July 1984, Texas A&M University, College Station, TX.
WISEMAN, B. R. 1985. Development of resistance in corn and sorghum to a foliar- and
ear/panicle-feeding worm complex, pp. 108-124 in Proc. 40th Annu. Corn &
Sorghum Research Conf., Dec. 11-12, 1985, Chicago, IL.
CHANG, N. T., B. R. WISEMAN, R. E. LYNCH, AND D. H. HABECK. 1986. Growth and de-
velopment of fall armyworm (Lepidoptera: Noctuidae) on selected grasses. En-
viron. Entomol. 15: 182-189.
HAMM, J. J., AND B. R. WISEMAN. 1986. Plant resistance and nuclear polyhedrosis vi-
rus for suppression of the fall armyworm (Lepidoptera: Noctuidae). Florida En-
tomologist. 69: 541-549.
LYNCH, R. E., W. G. MONSON, B. R. WISEMAN, G. W. BURTON, AND T. P. GAINES. 1986.
Relationship of forage quality to developmental parameters of the fall army-
worm (Lepidoptera: Noctuidae). Environ. Entomol. 15: 889-893.
PAIR, S. D., B. R. WISEMAN, AND A. N. SPARKS. 1986. Influence of four corn cultivars
on fall armyworm (Lepidoptera: Noctuidae) establishment and parasitization.
Florida Entomologist. 69: 566-570.
WISEMAN, B. R., AND N. W. WIDSTROM. 1986. Mechanisms of resistance in 'Zapalote
Chico' corn silks to fall armyworm (Lepidoptera: Noctuidae) larvae. J. Econ.
Entomol. 79: 1390-1393.
WISEMAN, B. R., R. E. LYNCH, K. L. MIKOLAJCZAK, AND R. C. GUELDNER. 1986. Ad-
vancements in the use of a laboratory bioassay for basic host plant resistance
studies. Florida Entomologist. 69: 559-565.
WISEMAN, B. R., H. N. PITRE, S. L. FALES, AND R. R. DUNCAN. 1986. Biological effects
of developing sorghum panicles in a meridic diet on fall armyworm (Lepi-
doptera: Noctuidae) development. J. Econ. Entomol. 79: 1637-1640.
CHANG, N. T., R. E. LYNCH, F. A. SLANSKY, B. R. WISEMAN, AND D. H. HABECK. 1987.
Quantitative utilization of selected grasses by fall armyworm larvae. Entomol.
exp. appl. 45: 29-35.
ISENHOUR, D. J., AND B. R. WISEMAN. 1987. Foliage consumption and development of
the fall armyworm (Lepidoptera: Noctuidae) as affected by the interactions of
a parasitoid, Campoletis sonorensis (Hymenoptera: Ichneumonidae), and resis-
tant corn genotypes. Environ. Entomol. 16: 1181-1184.
WISEMAN, B. R. 1987. Host plant resistance to insects in crop protection in the 21st
century, pp. 505-509, in Edwin D. Magallonaa [ed], Proceedings of the 11th In-
ternational Congress of Plant Protection. International Plant Protection: Focus
on the Developing World. Manila, Philippines, October 5-9, 1987.
DAVIS, F. M., W. P. WILLIAMS, J. A. MIHM, B. D. BARRY, J. L. OVERMAN, B. R. WISE-
MAN, AND T. J. RILEY. 1988. Resistance to multiple lepidopterous species in
tropical derived corn germplasm. Mississippi Agric. and Forest Exp. Sta. Tech.
Bull. 157, 6 pp.
ISENHOUR, D. J., AND B. R. WISEMAN. 1988. Incorporation of callus tissue into artifi-
cial diet as a means of screening corn genotypes for resistance to the fall army-
Florida Entomologist 82(2)
June, 1999
worm and the corn earworm (Lepidoptera: Noctuidae). J. Kansas Entomol. Soc.
63: 303-307.
WISEMAN, B. R., AND G. R. LOVELL. 1988. Resistance to the fall armyworm in sorghum
seedlings from Ethiopia and Yemen. J. Agric. Entomol. 5: 17-20.
WISEMAN, B. R., AND D. J. ISENHOUR. 1988. Feeding responses of fall armyworm lar-
vae on excised green and yellow whorl tissue of resistant and susceptible corn.
Florida Entomologist. 71: 243-249.
WISEMAN, B. R., AND D. J. ISENHOUR. 1988. The effects of prebioassay treatment of re-
sistant and susceptible corn silks on the development of the corn earworm and
fall armyworm. J. Agric. Entomol. 5: 247-251.
ASHLEY, T. R., B. R. WISEMAN, F. M. DAVIS, AND K. L. ANDREWS. 1989. The fall army-
worm: A bibliography. Florida Entomologist. 72: 152-202.
DAVIS, FRANK M., W. P. WILLIAMS, AND B. R. WISEMAN. 1989. Methods used to screen
maize for and to determine mechanisms of resistance to the southwestern corn
borer and fall armyworm, pp. 101-108 in Toward Insect Resistant Maize for the
Third World, Proc. Intl. Symp. on Methodologies for Developing Host Plant Re-
sistance to Maize Insects. CIMMYT.
ISENHOUR, D. J., AND B. R. WISEMAN. 1989. Parasitism of the fall armyworm (Lepi-
doptera: Noctuidae) by Campoletis sonorensis (Hymenoptera: Ichneumonidae)
as affected by host feeding on silks of Zea mays L. cv. Zapalote Chico. Environ.
Entomol. 18: 394-397.
ISENHOUR, D. J., B. R. WISEMAN, AND R. C. LAYTON. 1989. Enhanced predation by
Orius insidiosus (Hemiptera: Anthocoridae) on larvae of Heliothis zea and
Spodoptera frugiperda (Lepidoptera: Noctuidae) caused by prey feeding on re-
sistant corn genotypes. Environ. Entomol. 18: 418-422.
LYNCH, R. E., K. F. NWANZE, B. R. WISEMAN, AND W. D. PERKINS. 1989. Fall army-
worm (Lepidoptera: Noctuidae) development and fecundity when reared as lar-
vae on different meridic diets. J. Agric. Entomol. 6: 101-111.
WISEMAN, B. R. 1989. Methodologies used for screening for resistance to fall army-
worm in sorghum. International Workshop on Sorghum Stem Borers, ICRISAT
Center, November 17-20, 1987, Patancheru, India. pp. 119-128.
WISEMAN, B. R., AND R. R. DUNCAN. 1989. Growth, development, and survival of fall
armyworm fed panicles of isogenic sorghum lines in an artificial diet. Florida
Entomologist. 72: 556-558.
BUNTIN, G. D., AND B. R. WISEMAN. 1990. Growth and development of two polypha-
gous lepidopterans fed high- and low-tannin sericea lespedeza. Entomol. exp.
appl. 55: 69-78.
DIAWARA, M. M., B. R. WISEMAN, AND D. J. ISENHOUR, AND G. R. LOVELL. 1990. Resis-
tance to fall armyworm in converted sorghums. Florida Entomologist. 73: 111-117.
ISENHOUR, D. J., R. C. LAYTON, AND B. R. WISEMAN. 1990. Potential of adult Orius in-
sidiosus (Hemiptera: Anthocoridae) as a predator of the fall armyworm,
Spodoptera frugiperda (Lepidoptera: Noctuidae). Entomophaga 35: 269-75.
WISEMAN, B. R. 1990. Plant resistance: A logical component of sustainable agricul-
ture. Annual Plant Resistance to Insects Newsletter, Vol. 16, p. 40.
WISEMAN, B. R. 1990. Plant resistance to insects in the southeastern United States-
an overview. Florida Entomologist. 73: 351-358.
WISEMAN, B. R., AND F. M. DAVIS. 1990. Plant resistance to insects attacking corn and
grain sorghum. Florida Entomologist. 73: 446-458.
WISEMAN, B. R., R. C. GUELDNER, R. E. LYNCH, AND R. F. SEVERSON. 1990. Biochem-
ical activity of centipedegrass against fall armyworm larvae. J. Chem. Ecol.
16:2677-2690.
DIAWARA, M. M., N. S. HILL, B. R. WISEMAN, AND D. J. ISENHOUR. 1991. Panicle-stage
resistance to Spodoptera frugiperda (Lepidoptera: Noctuidae) in converted sor-
ghum accessions. J. Econ. Entomol. 84: 337-344.
DIAWARA, M. M., B. R. WISEMAN, AND D. J. ISENHOUR. 1991. Bioassay for screening
plant accessions for resistance to fall armyworm (Lepidoptera: Noctuidae) us-
ing artificial diets. J. Entomol. Sci. 26: 367-374.
Armyworm Symposium '98: Isenhour & Davis
DIAWARA, M. M., B. R. WISEMAN, D. J. ISENHOUR, AND N. S. HILL. 1991. Panicle feed-
ing resistance to Spodoptera frugiperda (Lepidoptera: Noctuidae) and its rela-
tionship to some chemical characteristics of sorghum accessions. Environ.
Entomol. 20: 1393-1402.
DIAWARA, M. M., B. R. WISEMAN, AND D. J. ISENHOUR. 1991. Mechanism of whorl
feeding resistance to fall armyworm among converted sorghum accessions. En-
tomol. exp. appl. 60: 225-231.
DUNCAN, R. R., D. J. ISENHOUR, R. M. WASKOM, D. R. MILLER, M. W. NABORS, G. E.
HANNING, B. R. WISEMAN, AND K. M. PETERSEN. 1991. Registration of
GATCCP100 and GATCCP101 fall armyworm resistant hegari regenerants.
Crop Sci. 31: 242-244.
GUELDNER, R. C., M. E. SNOOK, B. R. WISEMAN, N. W. WIDSTROM, D. S. HIMMELS-
BACH, AND C. E. COSTELLO. 1991. Maysin in corn, teosinte, and centipede grass,
pp. 251-263 in Paul A. Hedin [ed.] Naturally Occurring Pest Bioregulators.
ACS Symposium Series 449.
ISENHOUR, D. J., R. R. DUNCAN, D. R. MILLER, R. M. WASKOM, G. E. HANNING, B. R.
WISEMAN, AND M. W. NABORS. 1991. Resistance to leaf-feeding by the fall ar-
myworm (Lepidoptera: Noctuidae) in tissue culture derived sorghums. J. Econ.
Entomol. 84: 680-684.
ISENHOUR, D. J., AND B. R. WISEMAN. 1991. Fall armyworm resistance in progeny of
maize plants regenerated via tissue culture. Proceedings Fall Armyworm Sym-
posium 1990. Florida Entomologist. 74: 221-228.
WILSON, R. L., B. R. WISEMAN, AND G. L. REED. 1991. Evaluation of J. C. Eldredge
popcorn collection for resistance to corn earworm, fall armyworm (Lepidoptera:
Noctuidae), and European corn borer (Lepidoptera: Pyralidae). J. Econ. Ento-
mol. 84:693-698.
WISEMAN, B. R., AND H. R. GROSS. 1991. Dr. John R. Young-- Economic Entomologist.
Florida Entomologist. 74: 189-193.
WISEMAN, B. R., AND D. J. ISENHOUR. 1991. Development of fall armyworm on diets
containing resistant and susceptible corn silks. Proceedings Fall Armyworm
Symposium 1990. Florida Entomol. 74: 214-220.
CARPENTER, J. E., AND B. R. WISEMAN. 1992. Spodoptera frugiperda (Lepidoptera:
Noctuidae) development and damage potential as affected by inherited sterility
and host plant resistance. Environ. Entomol. 21: 57-60.
DIAWARA, M. M., B. R. WISEMAN, D. J. ISENHOUR, AND N. S. HILL. 1992. Sorghum re-
sistance to whorl feeding by larvae of the fall armyworm (Lepidoptera: Noctu-
idae). J. Agric. Entomol. 91: 41-53.
DIAWARA, M. M., B. R. WISEMAN, AND D. J. ISENHOUR. 1992. Spodoptera frugiperda
resistance in developing panicles of sorghum accessions. Insect Sci. Applic. 13:
793-799.
GUELDNER, R. C., M. E. SNOOK, N. WIDSTROM, AND B. R. WISEMAN. 1992. A TLC
screen for maysin, chlorogenic acid, and other possible resistance factors to the
fall armyworm and the corn earworm in Zea mays. J. Agric. Food & Chem. 40:
1211-1213.
RIGGIN, T. M., B. R. WISEMAN, D. J. ISENHOUR, AND K. E. ESPELIE. 1992. Incidence of
fall armyworm (Lepidoptera: Noctuidae) parasitoids on resistant and suscepti-
ble corn genotypes. Environ. Entomol. 21: 888-895.
SUMNER, H. R., H. R. GROSS, AND B. R. WISEMAN. 1992. Pushcart mounted rotary ap-
plicator for infesting plants with the larvae of Spodoptera frugiperda (Lepi-
doptera: Noctuidae). J. Econ. Entomol. 85: 276-280.
WIDSTROM, N. W., W. P. WILLIAMS, B. R. WISEMAN, AND F. M. DAVIS. 1992. Recurrent
selection for resistance to leaf-feeding by fall armyworm on maize. Crop Sci. 32:
1171-1174.
WISEMAN, B. R. 1992. Foliage-feeding Lepidoptera insects attacking sorghum in the
Americas. Sorghum Newsl. 33: 40-45.
WISEMAN, B. R. 1992. Entomological roles in the enhancement of maize with resis-
tance to Heliothis zea and Spodoptera frugiperda, pp. 103-115 in H. 0. Gevers
Florida Entomologist 82(2)
June, 1999
[ed.], Proc. of the Ninth South African Maize Breeding Symp. 1990, Rep. of
South Africa Dept. Agric. Dev. Tech. Com. No. 232.
WISEMAN, B. R., M. E. SNOOK, D. J. ISENHOUR, J. A. MIHM, AND N. W. WIDSTROM.
1992. Relationship between growth of corn earworm and fall armyworm larvae
(Lepidoptera: Noctuidae) and maysin concentration in corn silks. J. Econ. En-
tomol. 85: 2473-2477.
RIGGIN, T. M., ESPELIE, K. E., B. R. WISEMAN, AND ISENHOUR, D. J. 1993. Distribution
of fall armyworm (Lepidoptera: Noctuidae) parasitoids on five corn genotypes
in South Georgia. Florida Entomologist. 76: 292-302.
SIMMONS, A. M. AND B. R. WISEMAN. 1993. James Edward Smith taxonomic author
of the fall armyworm. Florida Entomologist. 76:271-276.
SNOOK, M. E., R. C. GUELDNER, N. W. WIDSTROM, B. R. WISEMAN, D. S. HIMMELS-
BACH, J. S. HARWOOD, AND C. E. COSTELLO. 1993. Levels of maysin and maysin
analogues in silks of maize germplasm. J. Agric. Food & Chem. 41: 1481-1485.
WIDSTROM, N. W., W. P. WILLIAMS, B. R. WISEMAN AND F. M. DAVIS. 1993. Registra-
tion of GT-FAWCC(C5) maize germplasm. Crop Sci. 34: 1422.
WISEMAN, B. R. AND D. J. ISENHOUR. 1993. Response of four commercial corn hybrids
to infestations of the fall armyworm and corn earworm (Lepidoptera: Noctu-
idae). Florida Entomologist. 76: 283-292.
WISEMAN, B. R. AND C. E. ROGERS. 1993. History of the Insect Biology and Population
Management Research Laboratory, USDA-ARS, University of Georgia,
Coastal Plain Experiment Station, Tifton, Georgia 1961-1993, pp. 229-238 in
Max H. Bass [ed.] The University of Georgia Coastal Plain Experiment Station.
The First 75 Years. Lang Printing Co., Tifton, GA. 353 pp.
YANG, G., K. E. ESPELIE, B. R. WISEMAN, AND D. J. ISENHOUR. 1993. Effect of corn fo-
liar cuticular lipids on the movement of fall armyworm (Lepidoptera: Noctu-
idae) neonate larvae. Florida Entomologist. 76: 302-316.
YANG, G., B. R. WISEMAN, AND K. E. ESPELIE. 1993. Movement of neonate fall army-
worm (Lepidoptera: Noctuidae) larvae on resistant and susceptible genotypes
of corn. Environ. Entomol. 22: 547-553.
YANG, G., B. R. WISEMAN, D. J. ISENHOUR, AND K. E. ESPELIE. 1993. Chemical and ul-
trastructural analysis of corn cuticular lipids and their effect on feeding by fall
armyworm larvae. J. Chem. Ecol. 19: 2055-2074.
RIGGIN, T. M., B. R. WISEMAN, D. J. ISENHOUR, AND K. E. ESPELIE. 1994. Functional
response of Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae) to
Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) on meridic diet
containing resistant or susceptible corn genotypes. Zeitschrift fur angewandte
Entomologie. 117: 144-150.
WISEMAN, B. R. 1994. Plant resistance to insects in integrated pest management.
Plant Disease 78: 927-932.
WISEMAN, B. R. AND D. J. ISENHOUR. 1994. Mechanisms of resistance in maize to Heli-
coverpa zea and Spodoptera frugiperda. Proc. 10th South Africa Maize Breed-
ing Symposium. 10: 51-55.
WISEMAN, B. R. 1994. Dedication of 1994 Armyworm Symposium to Dr. Robert L.
Burton and Mr. E. A. Harrell: Experts in insect rearing. Florida Entomologist.
77: 397-401.
WISEMAN, B. R. 1995. Breeding insect resistance into plants. National Conservation
Tillage Digest. December: 21-22.
WISEMAN, B. R. 1996. Examples of successes in plant resistance. National Conserva-
tion Tillage Digest. February: 19-21.
WISEMAN, B. R., D. J. ISENHOUR, AND R. R. DUNCAN. 1996. In vitro production of fall
armyworm (Spodoptera frugiperda) resistant maize and sorghum plants, pp.
67-80 in Y. P. S. Bajaj [ed.] Biotechnology in Agriculture and Forestry 36. So-
maclonal Variation II.
WISEMAN, B. R. AND R. R. DUNCAN. 1996. An evaluation of Paspalum spp. leaf sam-
ples for antibiosis resistance against Spodoptera frugiperda (J. E. Smith) (Lep-
idoptera: Noctuidae) larvae. Turfgrass Management. 1: 23-36.
Armyworm Symposium '98: Steinkraus & Young 209
WISEMAN, B. R., F. M. DAVIS, W. P. WILLIAMS. 1996. Resistance of a maize genotype,
FAWCC(C5), to fall armyworm larvae. Florida Entomologist. 79: 329-336.
WISEMAN, B. R., J. E. CARPENTER., AND G. S. WHEELER. 1996. Growth inhibition of
fall armyworm (Lepidoptera: Noctuidae) larvae on diets of nonhost plants.
Florida Entomol. 79: 302-311.
DAVIS, F. M., B. R. WISEMAN, W. P. WILLIAMS, AND N. W. WIDSTROM. 1996. Insect col-
ony, planting date, and plant growth stage effects on screening maize for leaf-
feeding resistance to fall armyworm. Florida Entomologist. 79: 317-328.
WISEMAN, B. R. 1996. Maize plant resistance to fall armyworm larvae, 1995. Arthro-
pod Management Tests: 1996. 21: 419-420.
SNOOK, M. E., B. R. WISEMAN, AND N. W. WIDSTROM. 1997. Chemicals associated with
maize resistance to corn earworm and fall armyworm, pp. 32-45 in Proc. Symp.
on Insect Resistant Maize: Recent research advances and utilization of resis-
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WISEMAN, B. R. 1997. Mechanisms of resistance in maize to corn earworm and fall ar-
myworm. Proc. Symp. on Insect Resistant Maize: Recent research advances
and utilization of resistance. CIMMYT. Nov. 27-Dec. 3, 1994.
WISEMAN, B. R. 1997. Factors affecting a laboratory bioassay for antibiosis: Influ-
ences of the plant and insect, pp. 211-216 in Proc. Symp. on Insect Resistant
Maize: Recent research advances and utilization of resistance. CIMMYT. Nov.
27-Dec. 3, 1994.
WISEMAN, B. R. 1997. Plant resistance to the fall armyworm, Spodoptera frugiperda.
Trends in Entomology. 1: 1-30.
Armyworm Symposium '98: Steinkraus & Young
BACILLUS THURINGIENSIS FOR USE AGAINST ARMYWORM,
PSEUDALETIA UNIPUNCTA (LEPIDOPTERA: NOCTUIDAE),
ON WHEAT
D. C. STEINKRAUS AND S. Y. YOUNG
Department of Entomology, University of Arkansas
Fayetteville, AR 72701
ABSTRACT
Spray table tests with Bacillus thuringiensis (Javelin WG) on wheat leaves against
armyworm, Pseudaletia unipuncta (Haworth), showed that 1st and 3rd instars had
LC50s of 0.09 and 0.55 kg per ha, respectively, 7 d after treatment. Wheat sprayed in
the field in 1995 with Javelin WG at rates of 0, 0.28, 0.56, 1.12, and 2.24 kg per ha re-
sulted in 82% and 62% 1st instar mortality 7 d after feeding on treated flag and mid-
dle leaves, respectively, at the highest rate. In 1996, the test was repeated and
mortality was higher, with 98, 97, and 92.9% 1st instar mortality 7 d after feeding on
treated flag, middle, and bottom leaves, respectively, at the highest rate. Third instars
were less susceptible, with 89, 81, and 76% mortality 7 d after treatment at the high-
est rate on flag, middle, and bottom leaves, respectively. Leaf position had little effect
on spray droplet numbers or mortality of larvae fed treated leaves, indicating that
spray distribution was relatively even throughout the wheat canopy.
Florida Entomologist 82(2)
June, 1999
Key Words: biological control, microbial control, spray distribution
RESUME
Pruebas de atomizaci6n en hojas de trigo con rocio de Bacillus thuringiensis (Jave-
lin WG) contra el gusano cortador, Pseudaletia unipuncta (Haworth), demostraron que
los ler y 3er estadios tenian, respectivamente, los LC50s de 0.09 y 0.55 kg por ha, 7 dias
despu6s de las aplicaciones. Pruebas de campo llevadas a cabo 1995 en trigo rociado
con Javeline WG con dosis de 0, 0.28, 0.56, 1.12, y 2.24 kg por ha resultaron en una
mortalidad de 82% y 62% en el primer estadio 7 dias despu6s de alimentarse en las ho-
jas terminales y medias, respectivamente, tratadas con la dosis mas elevadas. En
1996, se repitieron las pruebas obteniendo una mortalidad mas alta, con el 98, 97, y
92.9% de mortalidad del primer estadio despu6s de 7 dias de alimentarse en las hojas
terminales, medias y basales, respectivamente, con las dosis mas elevadas. El tercer
estadio fue menos susceptible, con una mortalidad de 89, 81, y 76% 7 dias despu6s del
tratamiento con las dosis mas elevadas en hojas terminales, medias, y basales, respec-
tivamente. La posici6n de la hoja tuvo un efecto pequeno en el numero de gotas de rocio
o en la mortalidad de las larvas que se alimenaron en hojas tratadas, indicando que la
distribuci6n del rocio fue relativamente uniform a traves de toda la corona del trigo.
The armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae) is a
pest of wheat in the US, with large acreages of heading wheat requiring treatment in
some years (Breeland 1958, Guppy 1961, Clark et al. 1994). Biological insecticides are
not registered in Arkansas for use on wheat. Three baculoviruses and six B. thuring-
iensis products were effective against P. unipuncta in laboratory assays on diet but
were ineffective at a range of rates in field trials on commercial wheat (Steinkraus &
Young 1994, Young & Steinkraus 1996). In those previous field trials, 4 and 7 d after
treatment there were no significant differences between numbers of larvae in control
and treatment plots. The main objective of this investigation was to determine if spray
coverage significantly influenced performance ofB. thuringiensis on wheat. This was
tested by determining spray deposition throughout the wheat canopy with water sen-
sitive cards and by feeding armyworm larvae treated leaves from three leaf positions.
MATERIALS AND METHODS
Gravid female armyworm moths were collected each year in early spring from an
ultraviolet light trap. Moths were held in aquaria and fed a mixture of honey, beer,
and water (9:7:14). Eggs were collected daily on folded wax paper fans attached to the
sides of the aquaria and held at 290C until hatch. Larvae were placed on semisyn-
thetic diet (Burton 1969) in 270 ml wax-coated paper cups at 290C until ready for use
in the tests as either 1 d old 1st instars or 3rd instars.
Wheat, ('Cardinal'), was planted 17 November 1995 and 15 September 1996 on the
Arkansas Agricultural Research and Extension Center in Fayetteville, AR and grown
according to commercial practices for the area.
Spray Table Test
On 15 May 1995, when heading wheat was in the soft dough stage [stage 7.7 of Zadoks
et al. (1974)], middle leaves were cut from plants, placed in plastic bags to minimize dry-
ing, and brought to the laboratory. The leaves were placed upper surface up on a 91 by 91
cm board for spraying. Treatments were Javelin WG (Sandoz Crop Protection Corpora-
Armyworm Symposium '98: Steinkraus & Young
tion, Des Plaines, IL) at 0, 0.56, 1.12, and 2.24 kg per ha. Treatments were applied using
a boom-type sprayer, with two TX-6 nozzles spaced 50.8 cm apart, at a pressure of 40 psi
and a spray table with a speed of 4.8 km per h. The sprayed leaves were briefly air dried,
then single leaves were placed individually into 28-ml plastic rearing cups. Either a 1st
instar or 3rd instar was placed on the leaf, the cup capped and held at 290C for 3 d. Treat-
ments consisted of 25 larvae per instar per rate and the test was replicated four times for
both 1st and 3rd instars. All larvae on treated leaves in cups were placed into sealed clear
plastic containers that contained a wetted paper towel to minimize desiccation of the
wheat leaves. After 3 d mortality was recorded and surviving larvae were transferred to
semi-synthetic diet in individual 28-ml rearing cups. Larvae were held on diet until the
7th day after treatment and mortality was again recorded. Data were corrected for con-
trol mortality by Abbott's formula (Abbott 1925). The lethal concentration mortality re-
sponse was estimated by the probit response (SAS Institute 1990). Failure of 95%
confidence limits to overlap was used as a criterion for significant difference.
Field Tests
Field tests were conducted in 1995 and 1996 to determine penetration of B. thuring-
iensis spray droplets into the wheat canopy, specifically droplet numbers hitting flag,
middle and bottom leaves. In all field tests, wheat was heading [stages 4.5-7.7 of Zadoks
et al. (1974)]. Each test was a randomized complete block design, replicated four times
over time (one replicate per day). Plots were 2.1 x 9.2 m with 1.8 m borders around
plots. Treatment rates were Javelin WG at 0, 0.28, 0.56, 1.12, and 2.24 kg per ha. Treat-
ments were applied using a backpack CO2 sprayer with a 2-row boom and two TX-6 noz-
zles per row set 0.5 m apart calibrated to deliver 95 1 per ha at 4.8 km per h. After the
spray dried, 25 flag, middle, and bottom leaves were collected at random from each
treatment, placed in plastic bags and transported to the laboratory. Assay of Javelin
WG on these leaves was with 1st and 3rd instars as described in the spray table test
above. Field tests were made on the following dates: 1st instars were tested 24-27 May
1995, 3rd instars were tested 14-17 May 1996 and 1st instars 20-23 May 1996. Mortal-
ity data were transformed by arcsin squareroot, analyzed with ANOVA, and means
separated by LSD (P < 0.05). Pearson correlation coefficients were determined for treat-
ment rate correlation with mortality by day and leaf position (SAS Institute, 1990).
Water sensitive paper cards (Ciba-Geigy, Basle, Switzerland), 52 x 76 mm, were
placed in the wheat field to monitor spray distribution at different heights of the
wheat canopy. Card placement heights were based on the mean heights of flag, middle
and bottom leaves on 25 randomly chosen plants in each year. Cards were held hori-
zontally by metal, double-prong hair clips hot glued to wire flags placed in the plots.
Each wire flag had cards at heights of 45, 28, and 14 cm from the ground in 1995 and
43, 23, and 13 cm in 1996. Two card-holding flags were randomly placed in each plot
prior to spray application (2 cards per height per treatment per day). Cards were col-
lected immediately after the spray dried and brought into the laboratory. Droplets
were counted with a hand lens in four areas per card using a 0.25 cm2 window placed
at random on the water sensitive cards. Mean numbers of droplets per 0.25 cm2 were
determined for each leaf height and treatment. Means by rate within a leaf position
and by leaf position within a rate were separated by LSD tests (SAS Institute 1990).
RESULTS
Spray Table Test
The lethal concentration curve for Javelin WG-treated wheat leaves fed to 1st in-
stars resulted in a LC,0 after 3 d of 0.53 kg per ha (Table 1). Mortality was much higher
Florida Entomologist 82(2)
June, 1999
TABLE 1. DOSAGE MORTALITY CURVES (KG/HA) FOR P. UNIPUNCTA LARVAE ON JAVELIN
WG-TREATED WHEAT LEAVES USING A SPRAY TABLE.
Days after
Instar treatment LC,0 (FI) LC,, (FI) Slope Chi-square P>
1st 3 0.53 (0.43-0.65) 5.52 (3.26-13.45) 1.256 0.001
7 0.09 (0.05-0.12) 0.71 (0.56-1.04) 1.392 0.001
3rd 3 1.70 (1.34-2.38) 11.01 (6.51-24.14) 1.580 0.001
7 0.55 (0.47-0.63) 4.12 (2.85-6.94) 1.458 0.001
7 d after treatment when the LC,0 was 0.09 kg per ha. Third instars were approxi-
mately 3 and 6 fold less susceptible than 1st instars after 3 and 7 d, respectively.
These data show that B. thuringiensis killed small larvae on treated wheat leaves and
has potential for P. unipuncta control on wheat when timed against small larvae. The
LC,0 rates after 7 d for 1st and 3rd instar were lower than rates recommended for con-
trol of some lepidopterous larval pests on other crops (Johnson and Jones 1996).
Field Tests
At the time of the field tests, plant heights from base of stem to top of head in 1995
and 1996 were 57.5 (3.1) and 56.7 (1.9) cm, respectively [means, (SE)]. Heights of the
flag, middle, and bottom leaves were 45.3 (1.8), 27.5 (0.9), 13.9 (0.7) cm in 1995, and
43.2 (0.9), 22.9 (0.6), and 12.6 (0.5) cm in 1996, above the ground, respectively [means,
(SE)]. The spray distribution data (Table 2) indicated, that in most cases within a leaf
position, significantly more droplets were found on cards in the control treatment (wa-
ter only) than in the Javelin WG treatments (Table 2). There was seldom any differ-
ence in droplet density within a test and leaf position in those treated with Javelin
WG. While in most cases significantly fewer droplets were counted on the bottom
leaves relative to numbers on the flag leaves, it appears that inadequate penetration
of the wheat canopy by B. thuringiensis sprays was not the cause of lack of efficacy in
the field tests of Steinkraus & Young (1994) and Young & Steinkraus (1996).
In the 1995 field test, 1st instar mortality increased significantly with increases in
Javelin rate at 3 and 7 d for flag and middle leaf positions (Table 3). Bottom leaves
were senescing at the time of the test and therefore, data for this leaf position were
not used. There were no significant differences in mortality due to leaf positions
within a day, again showing that Javelin WG coverage of flag and middle leaves was
similar. Mortality after 3 d was low in all treatments with only 47 and 25% mortality
at the highest rate on the top and middle leaf, respectively. While the mortality at the
higher rates was significantly higher at 3 d than the control, it was never greater than
50%. Mortality was higher after 7 d with 82 and 62% dead at the highest rate on the
flag and middle leaves, respectively. Although most rates did not show a significant
difference in mortality with leaf height (flag or middle leaf), in most cases mortality
was higher on the flag leaf.
In the 1996 test using 1st instars, there was a significant positive correlation be-
tween increased Javelin WG rate and mortality for each day and leaf position (Table
4). In all cases significantly more larvae were killed in the Javelin WG treatments
than the controls. Larval mortality after 3 d was higher than in the 1995 test with
mortality at the highest rate reaching approximately 70% at all three leaf positions.
Mortality after 7 d was higher reaching approximately 90% at 1.12 kg per ha at all
Armyworm Symposium '98: Steinkraus & Young
TABLE 2. NUMBERS OF B. THURINGIENSIS SPRAY DROPLETS ON WATER SENSITIVE PAPER
CARDS AT HEIGHTS OF FLAG, MIDDLE, AND BOTTOM WHEAT LEAVES IN 1995
AND 1996 FIELD TESTS.
Mean (SE) # droplets (per 0.25 cm2)1
Card locations
Javelin rate2
(kg/ha) Flag leaf Middle leaf Bottom leaf
24-27 May 1995 Test
0 66.9 (9.1) aA 60.8 (8.9) aA 40.4 (5.9) a B
0.28 37.0 (3.7) b A 33.4 (4.5) b A 21.4 (2.7) bc B
0.56 39.9 (3.8) b A 34.3 (2.9) b AB 30.9 (3.8) ab B
1.12 19.9 (3.1) cA 19.4 (3.2) cA 14.6 (2.3) cA
2.24 55.2 (5.5) aA 43.7 (3.7) b B 41.5 (4.4) a B
14-17 May 1996 Test
0 68.2 (10.7) aA 61.6 (12.6) aA 66.4 (14.9) aA
0.28 47.7 (4.8) b A 44.1 (2.9) b AB 32.7 (4.6) b B
0.56 39.0 (4.6) b A 28.5 (3.0) b AB 22.2 (1.5) b B
1.12 38.6 (9.2) b A 41.6 (6.9) b A 30.7 (4.6) b A
2.24 42.6 (6.8) b A 35.2 (5.6) b AB 25.1 (7.4) b B
20-23 May 1996 Test
0 72.0 (9.1) aA 57.9 (8.1) aA 55.8 (7.3) aA
0.28 51.4 (4.4) b A 42.6 (4.1) ab AB 37.9 (5.1) b B
0.56 55.9 (4.5) b A 48.9 (4.5) ab AB 41.5 (3.0) b B
1.12 43.0 (3.0) b A 37.8 (5.1) b A 25.4 (2.2) c B
2.24 52.5 (5.2) b A 39.4 (3.4) b B 41.8 (1.9) b B
'Means within a column followed by the same lower case letter or within a row followed by the same capital
letter did not differ significantly (ANOVA, LSD).
'ANOVA statistics for rate: 24-27 May 1995 Test, 0 rate (F = 4.05; df= 2; P = 0.0219); 0.28 rate (F = 7.93; df
= 2; P = 0.0008); 0.56 rate (F = 2.56; df= 2; P = 0.0851); 1.12 rate (F = 1.36; df = 2; P = 0.2648); 2.24 rate (F =
4.65; df= 2; P = 0.0128): 14-17 May 1996 Test, 0 rate (F = 0.14; df = 2; P = 0.8686); 0.28 rate (F = 4.12; df = 2; P
= 0.0412), 0.56 rate (F = 5.85; df = 2; P = 0.0154), 1.12 rate (F = 0.69; df= 2; P = 0.5311); 2.24 rate (F = 5.47; df
= 2; P = 0.0188): 20-23 May 1996 Test, 0 rate (F = 2.06; df= 2; P= 0.1565); 0.28 rate (F = 2.82; df= 2; P= 0.0859);
0.56 rate (F = 3.35; df = 2; P = 0.0580); 1.12 rate (F = 5.65; df= 2; P = 0.0125); 2.24 rate (F = 8.10; df = 2; P =
0.0031).
'ANOVA statistics for flag leaf card locations: 24-27 May 1995 test (F = 12.05, df= 4; P = 0.0001); 14-17 May
1996 test (F = 3.05; df = 4; P = 0.0395); 20-23 May 1996 Test (F = 3.65; df = 4; P = 0.0148).
'ANOVA statistics for middle leaf card locations: 24-27 May 1995 Test (F = 10.04; df= 4; P = 0.0001); 14-17
May 1996 Test (F = 4.40; df= 4; P = 0.0103); 20-23 May 1996 Test (F = 2.31; df= 4; P = 0.0792).
'ANOVA statistics for bottom leaf card locations: 24-27 May 1995 Test (F = 8.57; df= 4; P = 0.0001): 14-17 May
1996 Test (F = 9.18; df= 4; P = 0.0002); 20-23 May 1996 Test (F = 6.55: df= 4; P = 0.0006).
three leaf positions. There was no significant increase in mortality by increasing rate
from 1.12 to 2.24 kg per ha. As in the 1995 test mortality was similar across leaf po-
sitions within a rate and day, showing that Javelin WG was penetrating the canopy
and providing a similar dose to larvae feeding at all leaf positions.
In the 1996 test with 3rd instars, there was a significant positive increase in mor-
tality with rate increases for all leaf positions and both days (Table 5). After 3 d, mor-
Florida Entomologist 82(2)
June, 1999
TABLE 3. PERCENTAGE MORTALITY OF 1ST INSTAR P. UNIPUNCTA FED B. THURINGIEN-
SIS-TREATED FLAG AND MIDDLE WHEAT LEAVES TREATED IN THE FIELD
(1995)1.
Mean (SE) % Mortality2
3 day 7 day
Javelin WG
rate (kg/ha) Flag leaf Middle leaf Flag leaf Middle leaf
0 3.0 (1.0) aA 4.0 (2.8) aA 11.0 (3.4) aA 8.0 (3.6) aA
0.28 29.0 (9.7) b A 23.0 (9.9) b A 56.0 (9.5) b A 41.0 (9.3) b A
0.56 32.0 (11.2) b A 17.0 (3.0) b A 52.0 (5.6) b A 45.0 (2.5) b A
1.12 33.0 (5.9) b A 34.0 (9.0) b A 66.0 (8.2) ab A 62.0 (6.8) b A
2.24 47.0 (3.4) b A 25.0 (5.5) b B 82.0 (5.8) cA 62.0 (12.9) b B
r for rate3 0.70 0.58 0.81 0.76
P > r 0.0006 0.0074 0.0001 0.0001
Bottom leaves were senescing and were not suitable food for the larvae, so data is not presented.
Within day means in a column (lowercase) or row (upper case) followed by the same letter are not signifi-
cantly different (ANOVA, LSD, P > 0.05). ANOVA statistics for rate by leaf position within a day are as follows:
df= 4 in all cases; 3 d statistics, (flag leafF = 8.68, P = 0.0016), (middle leafF = 4.34, P = 0.0211); 7 d statistics,
(flag leaf F = 12.34, P = 0.0003), (middle leaf F = 7.90, P = 0.0023). ANOVA statistics for leaf position by day
within a rate are as follows: df = 1 in all cases; 0 rate (3 day F = 0.01, P = 0.9314), (7 day F = 0.52, P = 0.5239);
0.28 rate (3 day F = 0.72, P = 0.4571) (7 day F = 5.74, P = 0.0963); 0.56 rate (3 day F = 0.85, P = 0.4249), (7 day
F = 1.10, P = 0.3706); 1.12 rate (3 day F = 0.02, P = 0.8865), (7 day F = 0.29, P = 0.6269); 2.24 rate (3 day F = 21.8,
P = 0.0185), (7 day F = 11.68, P = 0.0419).
'Pearson correlation coefficients (SAS 1990).
tality on flag leaves ranged from 17% at 0.28 kg per ha to 59% at 2.24 kg per ha.
Mortality at 7 d was higher in most treatments and at the highest rate ranged from
76 to 89%. In no cases were there significant differences between mean mortalities
due to leaf position within a day and rate.
DISCUSSION
The spray table test showed that greater than 50% mortality of 1st instar P. uni-
puncta could be achieved at recommended rates of B. thuringiensis on middle wheat
leaves at either 3 or 7 days. Mortality occurred slowly and it was not possible to
achieve a 50% mortality level at recommended rates of Javelin WG with 3rd instars
at 3 d. Mortality levels in field-sprayed wheat tests were similar to those in the spray-
table test indicating that spray distribution on leaves was satisfactory at all plant
heights. Mortality in 3rd instars exposed to Javelin WG on wheat was slightly higher
in the field test (Table 5) than would be expected based on the spray table data. For
example, in the spray table test, even at 7 d, the LC,0 was 4.12 kg per ha, whereas, in
the field test, 89% were killed at 7 d at 2.24 kg per ha. This was unexpected since in
the spray-table test mortality of 3rd instars had been several times less than that of
1st instar. Further testing will be required to explain these differences.
Results of the spray tests suggest that B. thuringiensis has potential to control
P. unipuncta on wheat if treated as small larvae. These results are different from
those of small-plot commercial wheat field tests in which several B. thuringiensis
products failed to significantly reduce populations of P. unipuncta larvae (Steinkraus
TABLE 4. PERCENTAGE MORTALITY OF 1ST INSTAR P. UNIPUNCTA FED B. THURINGIENSIS-TREATED FLAG, MIDDLE, AND BOTTOM WHEAT LEAVES
TREATED IN FIELD (1996).
Mean (SE) % Mortality'
3 day 7 day
Javelin rate
(kg/ha) flag leaf middle leaf bottom leaf flag leaf middle leaf bottom leaf
0 1.0 (1.0) aA 1.0 (1.0) aA 3.0 (1.9) aA 3.0 (1.9) aA 2.0 (1.2) aA 12.0 (3.6) a B
0.28 26.2 (7.3) b A 22.1 (8.0) b A 54.3 (8.2) be B 58.7 (8.4) b A 54.7 (6.9) b A 78.8 (11.6) be B
0.56 54.0 (6.6) cA 50.0 (6.2) cA 49.7 (11.1) b A 88.0 (5.9) cA 84.0 (7.1) cA 74.2 (10.0) bA A
1.12 56.0 (11.4) c A 65.0 (6.8) d A 66.7 (6.0) be A 90.0 (4.8) c A 92.0 (1.6) cd A 89.9 (3.4) cd A
2.24 70.7 (11.5) cA 76.7 (6.0) e A 72.8 (5.9) cA 98.0 (1.2) cA 97.0 (1.9) dA 92.9 (1.9) d B
r for rate2 0.83 0.91 0.77 0.87 0.90 0.76
P > r 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
'Within day means in a column (lower case; ANOVA, LSD) or row (upper case, ANOVA, LSD) followed by the same letter are not significantly different (P > 0.05). ANOVA statistics for
rate by leaf position within a day are as follows: df= 4 in all cases; 3 d statistics, (flag leafF = 19.28, P = 0.0001), (middle leafF = 234.17, P = 0.0001), (bottom leafF = 21.52, P = 0.0001);
7 d statistics, (flag leaf F= 66.53, P = 0.0001), (middle leafF = 100.50, P = 0.0001), (bottom leaf F= 50.18, P = 0.0001). ANOVA statistics for leaf positionby day within a rate are as follows:
df= 2 in all cases; 0 rate (3 day F = 0.43, P = 0.6679), (7 day F = 5.95, P = 0.377); 0.28 rate (3 day F = 17.19, P = 0.0033); 0.56 rate (3 day F = 0.27, P = 0.7690), (7 day F = 2.77, P = 0.14060;
1.12 rate (3 day F = 0.42, P = 0.6766), (7 day F = 0.17, P = 0.8497); 2.24 rate (3 day F = 0.05, P = 0.9483), (7 day F = 5.71, P = 0.0409).
'Pearson correlation coefficient (SAS 1990).
TABLE 5. PERCENTAGE MORTALITY OF 3RD INSTAR P. UNIPUNCTA FED B. THURINGIENSIS-TREATED FLAG, MIDDLE, AND BOTTOM WHEAT LEAVES
TREATED IN FIELD (1996).
Mean (SE) % Mortality'
3 day 7 day
Javelin rate
(kg/ha) flag leaf middle leaf bottom leaf flag leaf middle leaf bottom leaf
0 6.0 (2.0) a 4.0 (2.3) a 10.0 (3.4) a 8.0 (3.2) a 9.0 (4.1) a 23.0 (5.2) a
0.28 17.0 (4.4) b 15.0 (4.7) ab 16.0 (4.9) ab 36.0 (5.9) b 32.0 (3.3) b 35.0 (10.4) ab
0.56 18.0 (3.5) b 20.2 (10.9) abc 21.0 (10.7) ab 50.0 (4.8) b 44.3 (13.2) bc 40.0 (14.1) ab
1.12 34.0 (6.6) c 37.0 (6.6) bc 35.0 (9.1) bc 56.0 (7.1) b 63.0 (10.7) cd 56.0 (10.3) bc
2.24 59.0 (7.4) d 44.0 (12.6) c 47.0 (13.8) c 89.0 (4.4) c 81.0 (4.1) d 76.0 (8.5) c
r for rate2 0.86 0.74 0.61 0.89 0.86 0.69
P >r 0.0001 0.0002 0.0043 0.0001 0.0001 0.0007
'Within day means in a column (lower case; ANOVA, LSD) followed by the same letter are not significantly different (P > 0.05). No significant differences were found for mortality by
leaf position within a day and treatment (statistics not presented). ANOVA statistics for rate by leaf position within a day are as follows: df was 4 in all cases; 3 d statistics, (flag leafF =
33.50, P = 0.0001), (middle leafF = 5.75, P = 0.008), (bottom leafF = 6.15, P = 0.0062); 7 d statistics, (flag leafF = 22.57, P = 0.0001), (middle leafF = 11.61, P = 0.0004), (bottom leafF =
8.53, P = 0.0004).
'Pearson correlation coefficient (SAS 1990).
Armyworm Symposium '98: Steinkraus & Young
& Young 1994, Young & Steinkraus 1996). This may have been due to unexamined fac-
tors such as larval size during the tests. The field populations treated in the efficacy
tests of Steinkraus & Young (1994) and Young & Steinkraus (1996) were of mixed ages
with most 3rd instars or older. As the tests show, larger larvae are more difficult to kill
than smaller larvae.
Another factor is deactivation of B. thuringiensis by sunlight. In assays of B. thu-
ringiensis sprayed on other crops it had an activity half-life of approximately 2 days
(Ali & Young 1993). In the tests reported here, leaves were collected immediately after
spray deposits dried (usually less than 30 min). This minimized potential degradation
of B. thuringiensis deposits by sunlight. In addition, once treated leaves were picked,
brought to the laboratory, and placed in cups, test larvae fed throughout the 3 d leaf-
exposure period on undegraded B. thuringiensis. In the field tests of Steinkraus &
Young (1994) and Young & Steinkraus (1996), in spite of the fact that the B. thuring-
iensis products were applied in late afternoon to minimize UV degradation, the
B. thuringiensis deposits would still have been exposed to several hours of sunlight
before the P. unipuncta larvae fed. Armyworms typically feed at night and rest on the
ground during the day. Thus, in field tests with feral P. unipuncta larvae B. thuring-
iensis residues would be increasingly degraded by sunlight each day throughout the
duration of a test.
A third possible explanation of the failure of B. thuringiensis products to reduce
field armyworm populations, as reported by Steinkraus & Young (1994) and Young &
Steinkraus (1996), could be movement of larvae between plots in field tests. It is pos-
sible that between the day of application, and assessments of larval populations 4 d
later, armyworms moved between plots. If so, larvae counted in treated plots may
have originated from outside treated areas and have been unexposed to B. thuringien-
sis. Such a situation could result in no significant differences in larval numbers be-
tween treated and control plots. Further tests are needed to fully explain the failure
of B. thuringiensis to control P. unipuncta on heading wheat.
ENDNOTE
We thank G. Boys for field and laboratory assistance and R. McNew for statistical
assistance. Thanks go to T. Kring and W. Yearian (Department of Entomology, Univer-
sity of Arkansas, Fayetteville) for reviewing the manuscript. This research was sup-
ported in part by USDA-CSRS Grants No. 89-34195-4378 and 92-34195-7162.
Published with the approval of the Director, Arkansas Agricultural Experiment Sta-
tion, Fayetteville, manuscript # 98037.
REFERENCES CITED
ABBOTT, W. S. 1925. A method of computing the effectiveness of an insecticide. J. Econ.
Entomol. 18: 265-267.
ALI, A., AND S. Y. YOUNG. 1993. Effects of rate and spray volume of Bacillus thuring-
iensis var. kurstaki on activity against Heliothis virescens (Lepidoptera: Noctu-
idae) and persistence on cotton. J. Econ. Entomol. 86: 735-738.
BREELAND, S. G. 1958. Biological studies on the armyworm, Pseudaletia unipuncta
(Haworth) in Tennessee (Lepidoptera: Noctuidae). J. Tenn. Acad. Sci. 33: 263-
347.
BURTON, R. L. 1969. Mass rearing the corn earworm in the laboratory. USDA, ARS,
No. 33-134. 8 pp.
CLARK, M. S., J. M. LUNA, N. D. STONE, AND R. R. YOUNGMAN. 1994. Generalist pred-
atory consumption of armyworm (Lepidoptera: Noctuidae) and effect of preda-
tor removal on damage in no-till corn. Environ. Entomol. 23: 617-622.
218 Florida Entomologist 82(2) June, 1999
GUPPY, J. C. 1961. Life history and behavior of armyworm, Pseudaletia unipuncta
(Haw.) (Lepidoptera: Noctuidae) in eastern Ontario. Can. Entomol. 93: 1141-
1153.
JOHNSON, D. R., AND B. F. JONES. 1996. 1995-1996 insecticide recommendations for
Arkansas. Arkansas Cooperative Extension Service MP 144.
SAS INSTITUTE. 1990. SAS/STAT user's guide: version 6.0, 4th ed. SAS Institute,
Cary, NC.
STEINKRAUS, D. C., AND S. Y. YOUNG. 1994. Evaluation of microbial insecticides for
control of armyworm on winter wheat, 1993. Arthropod Management Tests 19:
297.
YOUNG, S. Y., AND D. C. STEINKRAUS. 1996. Control of armyworm on heading wheat
with Bacillus thuringiensis products and baculoviruses, 1994. Arthropod Man-
agement Tests 21: 318-319.
ZADOKS, J. C., T. T. CHANG, AND C. F. KONZAK. 1974. A decimal code for the growth
stage of cereals. Weed. res. 14: 415-421.
Florida Entomologist 82(2)
June, 1999
LATE SEASON BEET ARMYWORM
(LEPIDOPTERA: NOCTUIDAE) INFESTATIONS ON COTTON:
DEFOLIATION, FRUIT DAMAGE, AND YIELD LOSS
V. J. MASCARENHAS1, D. COOK2, B. R. LEONARD3 E. BURRIS2 AND J. B. GRAVES1
Louisiana State University Agricultural Center
1Department of Entomology, Baton Rouge, LA 70803
2Northeast Research Station, St. Joseph, LA 71366
3Macon Ridge Location, Northeast Research Station, Winnsboro, LA 71295
ABSTRACT
Field cage studies were conducted in 1996 and 1997 to measure the effects of late
season beet armyworm, Spodoptera exigua (Htbner), infestations (0, 1, 3, and 6 egg
masses per 5.1 m row) on defoliation, fruit damage, and yield of cotton. Significantly
higher light penetration through the cotton canopy was observed in most infested
plots compared with non-infested control plots. A trend for higher numbers of dam-
aged fruiting forms (squares and bolls) with increases in egg mass density was ob-
served. There were no significant differences in the number of damaged fruiting forms
among treatments, however, plots infested with 1, 3, or 6 egg masses had 2.3, 2.4, and
3.3-fold more damaged fruiting forms than the control plots. In all infested plots, a sig-
nificantly higher percentage of shed fruiting forms were damaged compared with the
control plots in 1996. In 1997, only plots infested with 6 egg masses had a significantly
higher percent of the cumulative fruiting forms damaged compared with the control
plots. In both years, there were no significant differences in seed cotton yield among
treatments.
Armyworm Symposium '98: Mascarenhas et al.
Key words: Gossypium hirsutum L., Plant Damage, Yield Loss, Spodoptera exigua
RESUME
Se realizaron experiments en 1996 y 1997 con jaulas en campos de algod6n para
medir el efecto de infestaciones de fin de temporada de Spodoptera exigua (Htibner),
(con 0, 1, 3, y 6 masas de huevecillos por cada 5.1 m de hilera) en la defoliaci6n, dano
del fruto, y rendimiento del algod6n. Se observe una cantidad significativamente mas
alta de penetraci6n de luz a trav6s del follaje del algod6n en la mayoria de las parcelas
infestadas en comparaci6n con las parcelas no infestadas. Se observe una correlacion
positive entire el numero de 6rganos fructiferos (cuadros y bellotas) dahados y la den-
sidad de masas de huevecillos. No se documentaron diferencias significativas en el nu-
mero de frutos entire los tratamientos; sin embargo, parcelas infestadas con 1, 3, o 6
masas de huevecillos tenian 2.3, 2.4, y 3.3 veces mas de frutos que las parcelas control.
En todas las parcelas infestadas, un porcentaje significativamente mas alto de frutos
tirados estaba dahado por el gusano de Spodoptera exigua en comparaci6n con las par-
celas control de 1996. En 1997, s6lo parcelas infestadas con 6 masas de huevecillos tu-
vieron un por ciento acumulado significativamente mas alto de frutos dahados en
comparaci6n con las parcelas control. No hubo ninguna diferencia significativa entire
los tratamientos en ambos ahos en el rendimiento de semilla de algod6n.
The beet armyworm, Spodoptera exigua (Htbner), has been an occasional pest of
cotton in the U.S. since the early 1900s (Sanderson 1905) causing damage primarily
as a defoliator (Smith 1989, Leser et al. 1996). Injury to cotton associated with beet
armyworm has traditionally been feeding on the foliage and flower buds, as well as
etching on the bracts of fruiting forms (Smith 1989). These insects occasionally feed
on squares and small bolls late in the growing season, but this injury typically has not
resulted in economic yield losses, because fruiting forms that are produced late in the
growing season generally do not significantly contribute to yield (Jenkins et al. 1990).
Beet armyworm population outbreaks occurred in the mid to late 1980's in Ala-
bama (Smith 1989) and in 1993 in Mississippi (Layton 1994). In these areas, this pest
uniformly infested fields, and larvae fed almost exclusively on squares, flowers, and
young bolls during the fruiting stages of plant development rather than on foliage
(Smith 1989, Layton 1994). During outbreaks in Alabama and Mississippi, many cot-
ton producers sustained severe yield losses despite extensive control efforts, the cost
of which exceeded $371 per hectare in some areas. Similar devastation by beet army-
worm outbreaks has occurred in areas of Georgia (Douce & McPherson 1991, 1992)
and Texas (Summy et al. 1996).
The economic impact of beet armyworm infestations include yield losses and costs
associated with insecticide applications. Beet armyworms are tolerant to most regis-
tered classes of insecticides and control costs can become prohibitive when severe out-
breaks occur (Layton 1994). The cost of insecticides targeted at beet armyworms
exceeded $44 per application per hectare during the beet armyworm outbreaks in the
Lower Rio Grande Valley of Texas in 1995 (Williams 1996).
Cotton production in Louisiana has not been threatened by severe beet armyworm
outbreaks. Isolated economic infestations have been reported every two to three years
since the mid 1980s (Burris et al. 1994), but cotton yield losses associated with beet
armyworm injury have been less severe than in other states. However, during the past
4 years, this pest infested more than 500 thousand hectares of cotton in the state (Wil-
liams 1994, 1995, 1996, 1997).
Florida Entomologist 82(2)
June, 1999
Chlorpyrifos and thiodicarb are the only two insecticides currently recommended
for beet armyworm control on cotton in Louisiana (Bagwell et al. 1997). Unsatisfac-
tory efficacy of these insecticides against beet armyworm populations has been re-
ported across most of the mid-south and southeastern U.S. (Elzen 1989, Burris et al.
1994, Layton 1994, Smith 1994, Graves et al. 1995, Mascarenhas et al. 1996, Sparks
et al. 1996).
A Boll Weevil Eradication Program was implemented in Louisiana in August,
1997. The intensive insecticide regime associated with this program could release
beet armyworms from their natural enemies (Evellens et al. 1973, Gaylor & Graham
1991, Ruberson et al. 1994), and cause widespread population outbreaks. The poten-
tial yield losses associated with beet armyworm damage to cotton have not been well
studied. Therefore, the objective of this study was to determine the combined effects
of late-season defoliation and fruit injury by beet armyworm on cotton yields.
MATERIALS AND METHODS
Studies were conducted at the Northeast Research Station near St. Joseph, Loui-
siana during 1996 and 1997. Plots consisted of three adjacent rows (approximately 1
m centers) by 1.7 m in length covered by a translucent 32 mesh nylon cage (Synthetic
Industries, Greenville, Georgia) measuring 1.7 x 3.4 x 1.7 m. Plots were planted to
'Stoneville 474' cotton, an early maturing variety, on 1 May in 1996 and on 4 June in
1997. In both years, plots were arranged in a randomized block design with 4 replica-
tions. Plots were treated as needed with insecticides to minimize defoliation and fruit
damage by other insect pests. Insecticides that were selected for these applications
were those with negligible activity against beet armyworms and short residual activ-
ity. Insecticide applications were initiated at first square and ended 7-10 d before plots
were infested. Before covering the plots with cages, a combination of methyl par-
athion and acephate was applied to reduce populations of natural enemies within the
caged area 24 h before artificial infestations.
Field-collected beet armyworm strains were used to infest plots. Beet armyworm
larvae collected from cotton in Tift County, Georgia on 20 and 21 June were used in
1996, while larvae collected from cotton near St. Joseph, Louisiana on 7 and 8 August
were used in 1997. Field-collected larvae were transported to the Department of En-
tomology at Louisiana State University Agricultural Center in Baton Rouge, LA and
reared using an artificial wheat-germ and soybean protein diet (King & Hartley
1985). Egg masses of the F2 and F1 generation were used in field infestations during
1996 and 1997, respectively.
Cotton plots were infested when plants reached 5 nodes above white flower
(NAWF) stage and had accumulated approximately 300 heat units (Oosterhuis et al.
1993). Heat unit accumulation was calculated according to Bagwell & Tugwell (1992).
Infestations were made on 2 and 27 August in 1996 and 1997, respectively. The center
row of each plot was artificially infested with 0, 1, 3, or 6 egg masses. Egg masses on
wax paper oviposition sheets were attached with a paper clip to the lower surface of
fully expanded leaves in the middle one-third of the cotton canopy. Larval numbers
were thinned to approximately 60-80 insects per egg mass 2-3 d after larval hatching
(DAH). Larval survival and development was monitored through the duration of the
experiment.
All shed fruiting structures were removed from the soil surface within the cages
immediately before infestation. Square and boll damage was estimated by collecting
all shed fruiting structures two times per week and examining them for larval feeding.
Shed fruiting forms were categorized into two groups based on feeding signs on the
fruit. Fruiting forms that were shed but had no signs of fruit feeding were categorized
Armyworm Symposium '98: Mascarenhas et al.
as undamaged, while those that were shed and had signs of fruit feeding were catego-
rized as damaged. Fruiting forms in which the bracts were etched, but no feeding signs
were evident on the petals or carpel walls were recorded as undamaged. Fruit damage
was monitored until most larvae (>90%) had pupated in the soil (20-22 DAH).
Defoliation was estimated by measuring the photosynthetically active radiation
(PAR) that penetrated through the cotton canopy. A 1-m light ceptometer (Decagon
Devices, Inc. Pullman, Washington) probe equipped with 80 independent light sensors
was used to measure PAR. All PAR sampling was conducted between the hours of
11:00 am and 1:30 pm to minimize the effects of sun position on PAR data. Six PAR
samples were taken above the canopy by placing the ceptometer probe parallel to the
top of the cages and perpendicular to the cotton rows. This measurement supplied the
base level of PAR inside the cage. PAR samples below the canopy were taken by plac-
ing the probe perpendicular to the rows at the base of the cotton plants. Samples be-
low the canopy were taken at 10 different locations within the cage. Sampling PAR
above and below the canopy was conducted sequentially within a cage. Light penetra-
tion through the canopy was estimated by dividing the PAR below the canopy by the
PAR above the canopy and multiplying that number by 100. Visual defoliation ratings
after all larvae had pupated also were used to estimate foliage injury by beet army-
worms. The percent of the leaf area consumed in infested plots were visually com-
pared to that in the control plots. Cotton yields were determined by manually
harvesting the plots and measuring seed cotton weights. Data were analyzed by
ANOVA and means were separated according to Fisher's Protected LSD (P = 0.05)
(SAS Institute 1988). Statistical comparisons (a = 0.05) were done within sampling
date and across infestation densities.
RESULTS
Defoliation
Light penetration through the cotton canopy was significantly higher in plots in-
fested with beet armyworm eggs masses compared with control plots on most sam-
pling dates (Table 1). In 1996, all beet armyworm infested plots had significantly more
(1.5 to 1.7-fold) light penetrating the canopy than the control plots at 9 DAH. At 13
DAH, all infested plots, except for those infested with 3 egg masses, had significantly
more light penetration (1.3 to 1.5-fold) than the control plots. At 16 DAH, all infested
plots, except for those infested with 1 egg mass, had significantly higher light pene-
tration (1.2 to 1.4-fold) than the control plots. In 1997, only the plots infested with 3
egg masses had significantly more (1.5-fold) light penetrating the canopy than the
control plots at 9 DAH. At the remaining sampling dates (12, 16, and 19 DAH), plots
infested with 3 and 6 egg masses had significantly more light penetrating through the
canopy than the control plots. At 12, 16, and 19 DAH, plots infested with 3 egg masses
had 1.6, 1.8, and 1.9-fold more light penetration than the control plots, respectively.
Similarly, plots infested with 6 egg masses had 1.6, 1.8, and 2.2-fold more light pene-
tration than the control plots at 12, 16, and 19 DAH, respectively.
Visual defoliation ratings in 1996 showed that only the plots infested with 6 egg
masses had significantly higher defoliation (14%) than the control plots (4%) (Table
1). In 1997, there were no significant differences in visual defoliation ratings between
infested and control plots, despite a greater range in defoliation estimates.
Fruiting Form Damage 1996
Cumulative numbers of damaged fruiting forms in plots infested with 1, 3, or 6 egg
masses was 2.4, 3.0, and 3.3-fold higher than that in the control plots (Fig. 1). Although
TABLE 1. LIGHT PENETRATION IN COTTON PLOTS INFESTED WITH 0, 1, 3, OR 6 BEET ARMYWORM EGG MASSES. PLOTS WERE INFESTED WHEN COTTON
REACHED NAWF = 5 PLUS 300 HEAT UNITS.
% Light Penetration2 (1996) % Light Penetration (1997) Visual % Defoliation
Number of
Egg Masses' 9 DAH3 13 DAH 16 DAH 9 DAH 12 DAH 16 DAH 19 DAH 1996 1997
0 4.94 b 5.77 b 7.76 b 7.90 b 9.38 b 9.24 b 10.00 b 4.0 b 14.3 a
1 7.78 a 8.44 a 9.44 a 10.52 ab 11.52 ab 10.98 b 13.74 b 7.8 ab 32.5 a
3 7.47 a 7.66 ab 10.42 a 11.61 a 14.86 a 16.72 a 19.37 a 6.3 b 40.0 a
6 8.62 a 8.38 a 10.64 a 9.05 ab 14.86 a 16.67 a 22.37 a 13.8 a 56.7 a
F 3.4 2.8 3.0 2.9 4.7 12.1 14.9 4.2 0.9
df (3,153) (3,153) (3,153) (3,132) (3,126) (3,127) (3,123) (3,9) (3,6)
P 0.02 0.04 0.03 0.04 <0.01 <0.01 <0.01 0.04 0.51
Means within a column not followed by a common letter differ significantly (Fisher's Protected LSD; P = 0.05).
Larvae in each egg mass were thinned to 60-80 insects per egg mass.
Light penetration measured in Photosynthetic Active Radiation (PAR) using light ceptometer. % Light penetration = (PAR bottom canopy/PAR top canopy) x 100.
DAH = days after larval hatching.
Armyworm Symposium '98: Mascarenhas et al.
S0 Egg Mass n 1 Egg Mass E 3 Egg Masses E 6 Egg Masses
300
E 250 a
200
100
0
Total Shed Undamaged Damaged
Fig. 1. Numbers of total shed, undamaged, and damaged fruiting forms in plots in-
fested with 0, 1, 3, and 6 beet armyworm masses in 1996. Statistical comparisons
within a category were made across egg mass densities. Different letters above bars
indicate significant differences LSD (P = 0.05).
a trend for increased numbers of damaged fruiting forms with increases in egg mass
density was observed, the cumulative numbers of damaged fruiting forms in infested
plots were not significantly (a = 0.05) different from that in the control. In addition,
there were no differences in the cumulative numbers of undamaged or total shed (un-
damaged + damaged) fruiting forms between infested and control plots (Fig. 1).
In all infested plots, a significantly higher percentage of the shed fruiting forms
was damaged compared with the control plots at 6, 9, 13, and 16 DAH (Table 2). In ad-
dition, plots infested with 6 egg masses had a significantly higher percentage of shed
fruiting forms that were damaged than the plots infested with 1 egg mass at 6 and 16
DAH. No differences were observed in the percentage of shed fruiting forms that were
damaged between infested and control plots at 20 DAH. Similar results were obtained
in the percentage of cumulative shed fruiting forms that were damaged (Table 2). All
infested plots had a significantly higher percentage of the cumulative shed fruiting
forms that were damaged than in the control plots.
Fruiting Form Damage 1997
The cumulative numbers of damaged fruiting forms in plots infested with 1, 3, or
6 egg masses were 2.1, 1.8, and 3.3-fold higher than that in the control plots (Fig. 2).
Although a trend for increased numbers of cumulative damaged fruiting forms with
increases in egg mass density was noted, no significant (a = 0.05) differences were ob-
served. In addition, there were no significant differences in the cumulative numbers
of undamaged or total shed fruiting forms between infested and control plots (Fig. 2).
The percentage of shed fruiting forms that were damaged tended to increase with
increases in egg mass density. However, there were no significant differences among
treatments on 3 of the 4 sampling dates. At 12 DAH, plots infested with 6 egg masses
had a significantly higher percentage of the shed fruiting forms that were damaged
TABLE 2. PERCENT OF SHED FRUITING FORMS (SQUARES AND BOLLS) DAMAGED BY BEET ARMYWORM LARVAE IN PLOTS INFESTED WITH 0, 1, 3, AND
6 BEAT ARMYWORM EGG MASSES.
% Damaged Fruiting Forms (1996)2 % Damaged Fruiting Forms (1997)2
No. Egg
Masses' 6 DAH3 9 DAH 13 DAH 16 DAH 20 DAH Cumulative 9 DAH 12 DAH 16 DAH 20 DAH Cumulative
0 10.9 c 18.4 b 14.7 b 16.5 c 9.9 a 16.3 c 2.4 a 3.2 b 6.4 a 1.0 a 3.2 b
1 18.7 b 36.5 a 35.0 a 29.5 b 15.6 a 31.5 b 10.0 a 3.4 b 33.3 a 25.0 a 6.0 b
3 21.7 ab 38.8 a 39.2 a 38.1 a 22.1 a 36.9 ab 16.4 a 6.7 b 31.3 a 33.3 a 22.2 b
6 25.3 a 36.3 a 42.9 a 40.4 a 19.5 a 38.3 a 26.4 a 36.5 a 25.0 a 41.7 a 54.0 a
F 17.3 12.4 15.6 19.1 1.5 23.3 2.2 .38 0.5 1.5 6.4
df (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) (3,9) 00
P <0.01 <0.01 <0.01 <0.01 0.29 <0.01 0.16 0.05 0.74 0.28 0.01
Means within a column not followed by a common letter differ significantly according to Fisher's Protected LSD (P = 0.05).
Numbers of larvae in each egg mass were thinned to 60-80 insects per egg mass.
Percent damage fruiting forms = (No. damaged fruiting forms/No, total shed fruiting forms)* 100.
DAH = days after larval hatching.
Armyworm Symposium '98: Mascarenhas et al.
I 0 Egg Mass E 1 Egg Mass E 3 Egg Masses F 6 Egg Masses:
Total Shed Undamaged Damaged
Fig. 2. Numbers of total shed, undamaged, and damaged from fruiting forms in
plots infested with 0, 1, 3, and 6 beet armyworm egg masses in 1997. Statistical com-
parisons within a category were made across egg mass densities. Different letters
above bars indicate significant differences LSD (P = 0.05).
than control plots, as well as plots infested with 1 or 3 egg masses (Table 2). Similar
results were obtained in the percentage of cumulative numbers of shed fruiting forms
that were damaged. Plots infested with 6 egg masses had a significantly higher per-
centage of the cumulative shed fruiting forms that were damaged than the control
plots and those infested with 1 or 3 egg masses.
Yield
There were no significant differences (a = 0.05) in seed cotton yield between in-
fested and non-infested control plots in 1996 or 1997 (Fig. 3).
Larval Development and Survival
Larval development and survival was normal in both years. Egg masses hatched 2-
3 d after they were pinned to the leaves. Neonate larvae fed gregariously on the un-
derside of leaves near the egg mass. Larvae began to disperse throughout the infested
plant 3-4 d after they hatched, and 8 d after hatching, larvae were found throughout
the cage environment. Larval survival to pupation was estimated at greater than 50%.
DISCUSSION
Yield losses associated with beet armyworm damage may result from direct dam-
age to fruiting forms, as well as indirect damage from larvae feeding on foliage. Foli-
age feeding can indirectly affect yield by reducing the leaf area that produces
photosynthates required to mature bolls. In previous studies, Kerby et al. (1988)
showed that cotton can withstand up to 57% defoliation (artificial removal of leaves)
before first square without significant reduction in lint yield. Additionally, Russell et
al. (1993) conducted simulated defoliation studies in which cotton was repeatedly de-
Florida Entomologist 82(2)
June, 1999
0 Egg Mass D 1 Egg Mass E 3 Egg Masses 0 6 Egg Masses
5000 -
a
S4000 a a a
3000 a
a a
e 2000 j
1000
0 --
1996 1997
Fig. 3. Seed cotton yield in plots infested with 0, 3, and 6 beet armyworm egg
masses in 1996 and 1997. Statistical comparisons were made across egg mass densi-
ties. Different letters above bars indicate significant differences LSD (P = 0.05).
foliated (20%) over a period of 7 consecutive weeks, from early squaring to mid-bloom,
with no effect on yield. However, Russell et al. (1993) suggested that severe defoliation
(>20%) during boll maturation could significantly impact yield by reducing the pro-
duction of photosynthates in leaves necessary for maximum boll development.
The beet armyworm densities used in these studies ranged from 2.7 to 16.7-fold
higher than the threshold of 6 hits (egg masses or clusters of small larvae) per 91.5
meter of row currently recommended in Louisiana (Bagwell et al. 1997). At the infes-
tation densities used in these studies, a significant increase in the amount of light
penetrating the canopy was generally observed in plots infested with 3 or 6 egg
masses, which suggests a significant decrease in leaf area in those plots. Visual defo-
liation ratings in plots infested with 1, 3, or 6 egg masses were an average (1996 and
1997) of 2.1, 2.2, and 3.8-fold higher than the control plots, respectively. However,
these levels of foliage loss at NAWF < 5 plus 300 heat units were not sufficient to re-
duce yield in these plots compared with the control plots. These data are similar to re-
search by Guitierrez et al. (1975), that showed cotton defoliation by beet armyworms
and cabbage looper, Trichoplusia ni (HuIbner), late in the growing season had little ef-
fect on yield. Similar results also were reported by Torrey et al. (1997) where removal
of all foliage from the bottom 1/3 of the cotton canopy (33% defoliation) did not signif-
icantly reduce yields when plant development was at NAWF < 5 plus 350 heat units.
Results obtained in this study could have been caused by a compensatory effect (Oost-
erhuis et al. 1991), where plants were able to produce new leaf material at a rate in
which the demands for photosynthates by the maturing bolls were met. Thus, no re-
duction in yield was observed. Alternatively, defoliation at this late stage of plant ma-
turity (NAWF < 5 plus 300 heat units) may not have affected yield because there was
sufficient leaf area remaining to mature bolls. Cotton plants appear relatively unaf-
fected by moderate (<40%) defoliation from early season to mid-flowering (Kerby et al.
1988, Russell et al. 1993). After plants have reached 5 NAWF and have accumulated
heat units in excess of 300, late season defoliation low in the canopy also has little ef-
fect on yields (Torrey et al. 1997).
Armyworm Symposium '98: Mascarenhas et al.
Although beet armyworms historically are recognized as defoliators, their direct
feeding on fruiting forms often is of a much greater yield consequence (Smith 1989,
Layton 1994). In 1996, a definite trend for increasing fruit damage occurred with in-
creases in egg mass density. During the period that this study was conducted (one lar-
val cycle or approximately 22 d), larvae in plots infested with 1, 3, or 6 egg masses
damaged approximately 60, 70, and 90 fruiting forms, respectively (Fig. 1). However,
these levels of fruit damage observed (1996) had no significant effect on yield. In fact,
a trend for slight seed cotton yield increases with increased egg mass density was ob-
served in 1996 (Table 1). A similar trend also was observed in the cumulative number
of total shed fruiting forms (Fig. 1). In these studies, some level of fruit abscission may
have occurred due to shading effects caused by the cage. Inside the cage, the light in-
tensity was 60% of that recorded outside of the cage under direct sunlight. Guinn
(1982) reported high rates (>90%) of fruit abscission when cotton plants were exposed
to dim light (4 pEm's 1) for 3 d. Although abscission rates for young bolls (4-8 d old)
was near 100%, abscission rates declined very rapidly for older bolls. Bolls that were
15 d past anthesis when exposed to dim light were virtually immune to abscission
(Guinn 1982). In this study, a significant portion of undamaged young bolls did abscise
in all treatments (Fig. 1). However, most of the older bolls were sufficiently matured
(> 8 d old) and were not likely to abscise due to the shading caused by the cages. By
having a slightly higher incidence of shed fruiting forms, plants in infested plots may
have been able to concentrate their photosynthate resources on older fruiting forms,
thus producing slightly bigger bolls than produced in the control plots. Small fruit ab-
scission can be beneficial because it allows for the maturation of bigger bolls which the
plant already has invested time and energy (Hake et al. 1989). The lack of differences
in the cumulative numbers of total shed fruiting forms (Fig. 1), and the significantly
higher percentage of shed fruiting forms damaged in infested plots (Table 2), indicates
that the majority of the fruiting forms damaged by beet armyworm larvae were those
that the plant would have naturally shed in the absence of insect damage.
The trends observed in fruit shedding and damage during 1996 were not repeated
during 1997. A combination of late planting, poor early season growing conditions,
and abnormally hot and dry late season growing conditions in 1997 likely impacted
the outcome of this study. The overall yield potential of the plants was probably re-
duced due to stresses during the seedling and boll development stages. Differences in
plant condition (fruit load and canopy mass) between 1996 and 1997 likely had some
influence on the feeding behavior of beet armyworms.
The numbers of total shed fruiting forms was extremely different between the
1996 and 1997 studies. In the control plots, the number of total shed (undamaged +
damaged) fruiting forms in 1996 was 4.8-fold higher than in 1997. Similarly, in plots
infested with 1, 3, or 6 egg masses, the number of total shed fruiting forms in 1996 was
9.5, 11.5, and 13.5-fold higher than in 1997, respectively. Some of the fruiting forms
in the 1997 test plots had suffered considerable damage from other insects and were
aborted before cages were in place. This decreased the available numbers of fruiting
forms susceptible to damage and shed from beet armyworm feeding. Most fruit shed-
ding occurred at the first two sampling dates in all plots. After those fruiting forms
were shed, remaining bolls may have been mature enough to avoid damage by beet ar-
myworm larvae (Adamczyk et al. 1998). Nevertheless, there was a general trend for
increased numbers of damaged fruiting forms with increases in egg mass density in
1997 (Fig. 2). However, no significant differences among treatments in seed cotton
yield were observed in either year.
In summary, results indicate that neither defoliation nor fruit damage caused by
late season beet armyworm infestation levels as high as 16.7 times the current
threshold of 6 hits per 91.5 meters of row significantly affected cotton yields in these
Florida Entomologist 82(2)
June, 1999
studies. Further research is needed to determine the consequences of beet armyworm
infestations that may occur earlier in the growing season, when cotton bolls may be
more susceptible to damage by this pest. In addition, this research was conducted dur-
ing only a single generation of the larval stage of this insect pest. Continuous damage
caused by overlapping generations of beet armyworms can be considerably greater
than that tested herein, thus potentially resulting in economic yield losses.
ENDNOTE
The financial support of Cotton Incorporated is gratefully acknowledged. We thank
Dr. Gary Herzog and Russ Ottens for supplying field-collected insects. The critical re-
view of this manuscript by Dr. Blake Layton, and Dr. Alton Sparks is gratefully acknowl-
edged. We also thank Larry Daigle, Chad Comeaux, David Nyagah, and Shae Robinson
for their help in insect rearing. This manuscript is approved for publication by the Di-
rector of the Louisiana Agricultural Experiment Station as Manuscript No. 98-76-0069.
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Florida Entomologist 82(2)
June, 1999
TOXICITY OF SELECTED INSECTICIDES TO FALL
ARMYWORMS (LEPIDOPTERA: NOCTUIDAE)
IN LABORATORY BIOASSAY STUDIES
J. J. ADAMCZYK, JR., B. R. LEONARD AND J. B. GRAVES
Louisiana State University Agricultural Center
Department of Entomology, Baton Rouge, LA 70803
ABSTRACT
Efficacy of conventional and experimental insecticides against the fall armyworm,
Spodoptera frugiperda (J. E. Smith), was evaluated in laboratory bioassays. In a lab-
oratory diet bioassay, third instars of a laboratory-strain were more susceptible to
novel insecticides, including chlorfenapyr, methoxyfenozide, spinosad, and
tebufenozide, than to a recommended insecticide, thiodicarb. In other laboratory bio-
assays, fall armyworms were fed field grown cotton leaves, white flowers, or bolls
treated with one of two recommended insecticides, L-cyhalothrin or thiodicarb, or one
of four experimental insecticides, chlorfenapyr, emamectin benzoate, methoxy-
fenozide, or spinosad. First instar mortality was significantly greater on leaves
treated with chlorfenapyr, L-cyhalothrin, or thiodicarb than for the untreated control
at 24 h after infestation (HAI). First instar mortality was significantly greater on
leaves treated with all insecticides, with the exception of methoxyfenozide, than for
the untreated control at 48 HAI. Likewise, first instar mortality was significantly
greater on white flowers treated with all insecticides, with the exception of methoxy-
fenozide, than for the untreated control at 24 HAI. First instar mortality on white
flowers treated with all insecticides was significantly greater than the untreated con-
trol at 48 HAI. Fifth instar mortality on bolls was not significantly different among
treatments at 1 day after infestation (DAI). At 3 and 5 DAI, fifth instar mortality was
significantly greater on bolls treated with all insecticides, with the exception of meth-
oxyfenozide and spinosad, than for the untreated control. At 7 DAI, fifth instar mor-
tality was significantly greater on bolls treated with all insecticides, with the
exception of spinosad, than for the untreated control. These data indicate that these
recommended and experimental insecticides are effective in controlling early fall ar-
myworm instars on cotton if larvae come in contact with these insecticides.
Key Words: Spodoptera frugiperda, efficacy, chemical control, insecticides
RESUME
La eficacia de insecticides convencionales y experimentales contra el gusano cogo-
llero del maiz, Spodoptera frugiperda (J. E. Smith), se evalu6 con bioensayos de labo-
ratorio. En un experiment de dieta, se document que instares terceros de una
colonia de laboratorio eran mas susceptibles a los insecticides nuevos, incluyendo a
chlorfenapyr, methoxyfenozide, spinosad, y tebufenozide, que a un insecticide reco-
mendado, thiodicarb. En otros experiments de laboratorio, los gusanos cogolleros se
alimentaron con hojas de algod6n, flores blancas, o bellotas tratadas con uno de dos in-
secticidas recomendados, L-cyhalothrin o thiodicarb, o uno de cuatro insecticides ex-
perimentales, chlorfenapyr, emamectin benzoate, methoxyfenozide, o spinosad. La
mortalidad del primer instar fue significativamente mayor en hojas tratadas con
chlorfenapyr, L-cyhalothrin, o thiodicarb que en hojas control no tratadas 24 h des-
pues de la infestacion (HAI, "hours after infestation"). La mortalidad del primer ins-
tar fue significativamente mayor a las 48 HAI en hojas tratadas con cualquiera de los
insecticides, con la excepci6n de methoxyfenozide, que con cualquier hoja control no
tratada. Igualmente, la mortalidad del primer instar fue significativamente mayor a
las 24 HAI en flores blancas tratadas con cualquiera de los insecticides, con la excep-
Armyworm Symposium '98:Adamczyk et al.
ci6n de methoxyfenozide, que con el control. La mortalidad del primer instar a las 48
HAI en flores blancas tratadas con cualquiera de los insecticides fue significativa-
mente mayor que en los controls no tratados. La diferencia en la mortalidad del
quinto instar en bellotas entire los tratamientos en el dia 1 de la infestacion (DAI, "day
of infestation") no fue significativa. En los DAI 3 y 5, la mortalidad del quinto instar
fue significativamente mayor en bellotas tratadas con cualquiera de los insecticides,
con la excepci6n de methoxyfenozide y spinosad, que con el control no tratado. En el
DAI 7, la mortalidad del quinto instar fue significativamente mayor en botones trata-
dos con cualquiera de los insecticides, con la excepci6n de spinosad, que en el control
no tratado. Estos datos indican que los insecticides recomendados y experimentales
mencionados aquf son eficaces para el control de instares pequenos del gusano de Spo-
doptera frugiperda en algod6n si las larvas contactan estos insecticides.
The fall armyworm, Spodoptera frugiperda (J. E. Smith), is a pest of many crops
in the southern United States, including rice, Oryza sativa L.; field corn, Zea mays L.;
soybean, Glycine max (L.) Merr.; and cotton, Gossypium hirsutum L. (Young 1979).
Historically, this insect is considered as a sporadic pest on cotton, but it has become
an annual economic cotton pest in Georgia, Alabama, and Florida (Smith 1985). In
1977, this pest caused significant damage to cotton throughout the southeastern
United States (Bass 1978), and in 1984, caused economic damage in the Winter Gar-
den region of Texas (King et al. 1986). In 1985, it was the single most damaging cotton
pest reported in Mississippi (King et al. 1986). Recently, local outbreaks of fall army-
worms have been reported on transgenic Bacillus thuringiensis (Bt) cotton cultivars
in Alabama and Georgia (Hood 1997, Smith 1997).
Fall armyworms on cotton are difficult to control with insecticides. Larvae are usu-
ally distributed low in the plant canopy (Ali et al. 1990), and inadequate insecticide
deposition in the lower portions of the cotton plant seems to be one limiting factor in
controlling this pest (Mink & Luttrell 1989). Insecticides that are used to control the
tobacco budworm, Heliothis virescens (F.), and the cotton bollworm, Helicoverpa zea
(Boddie), often are ineffective against fall armyworms (Smith 1985). Pyrethroids may
have some effect on young fall armyworm larvae, but in general provide little overall
control, while carbaryl and methyl parathion are completely ineffective for controlling
this pest on cotton (Smith 1985). Although the CrylA (c) a-endotoxin is expressed
throughout genetically engineered transgenic Bt cotton plants, this particular S-en-
dotoxin should be classified as sublethal to fall armyworm larvae (Jenkins et al. 1992,
Jenkins et al. 1997, Adamczyk et al. 1998). In addition, many studies have shown that
fall armyworms are resistant to a number of compounds including carbaryl, methyl
parathion, trichlorfon, and numerous pyrethroids (Young & McMillian 1979, Wood et
al. 1981, McCord & Yu 1987, Yu 1991), which further complicates control of this pest
on cotton. The purpose of these studies was to examine the toxicity of selected conven-
tional and experimental insecticides to fall armyworm larvae in laboratory bioassays.
MATERIALS AND METHODS
Diet Bioassay with Experimental Insecticides
A fall armyworm colony consisting of the corn-associated strain (Pashley 1986),
which had been reared in the laboratory for at least 30 generations, (obtained from Dr.
H.W. Fescemyer, Clemson University, Department of Entomology) was tested with a
Florida Entomologist 82(2)
June, 1999
recommended insecticide, thiodicarb (Larvin 3.2F [flowable], Rh6ne-Poulenc Ag.
Co., Research Triangle Park, North Carolina), as well as four novel compounds includ-
ing chlorfenapyr (Pirate 3SC [soluble concentrate], American Cyanamid, Princeton,
New Jersey), methoxyfenozide (Intrepid 80WP wettablee powder], Rohm & Haas
Co., Philadelphia, Pennsylvania), spinosad (Tracer 4SC, Dow AgroSciences, India-
napolis, Indiana), and tebufenozide (Confirm 2F, Rohm & Haas Co., Philadelphia,
Pennsylvania).
The surface-treated diet bioassay methods were similar to those described by Joyce
et al. (1986), Chandler & Ruberson (1994), and Mascarenhas et al. (1996). Three ml of
a soybean/protein meridic diet (King & Hartley 1985) were pipetted into 30 ml cups
and allowed to cool at room temperature for approximately 1 h. For each insecticide
tested, serial dilutions of formulated material (100 pl aliquots) were pipetted onto the
diet surface, agitated to distribute evenly, and allowed to dry for approximately 30 min.
Third instar fall armyworms (30-45 mg) were placed into a series of cups that con-
tained 4-5 different concentrations (ppm) of formulated insecticide, along with untreated
controls to determine the LCs, for a given insecticide. Each cup contained one larva. The
cups were sealed with corresponding lids and bioassays were conducted under constant
light at 22 + 1C and 40 + 5% RH. A minimum of 30 larvae per dose were tested for each
insecticide, and mortality was assessed at 120 h after treatment (HAT). Larvae were
considered dead if no movement was observed after prodding with blunt forceps for 10 s.
Control mortality never exceeded 5%. LCs0's were considered significantly different from
one another if the 95% confidence limits did not overlap. Data were analyzed and LC50's
generated with POLO-PC using probit analysis (LeOra Software 1987).
Toxicity of Cotton Plant Parts Treated with Insecticides to Fall Armyworm Larvae
Fall armyworm larvae were collected from field corn in May 1997 at the Macon
Ridge Location of the Northeast Research Station (Louisiana State University Agricul-
tural Center, Louisiana Agricultural Experiment Station) near Winnsboro, LA. F, gen-
eration larvae were used in all tests. Cotton plants (cv. DP 5690 1.0 m tall) were
sprayed with selected foliar insecticides using a high clearance sprayer, and com-
pressed air system, calibrated to deliver 56.1 L total spray/ha through Teejet TX-8 hol-
low cone nozzles (2/row) at 3.3 kg/cm2. Selected insecticides included methoxyfenozide,
L-cyhalothrin (Karate 1EC [emulsifiable concentrate], Zeneca Ag. Products, Wilming-
ton, Delaware), thiodicarb, chlorfenapyr, emamectin benzoate (Proclaim 5SG [soluble
granule], Novartis, North Carolina), and spinosad. Treatments were arranged in a ran-
domized complete block design (RCB) and replicated 4 times. Plots consisted of 4 rows
(1.0 m centers) x 15.2 m. Cotton leaves, white flowers, and bolls, were removed from the
lower 0.5 m of treated plants 2 HAT, and transported to the laboratory for each test.
The toxicity of insecticide-treated cotton leaves and white flowers to first instar (1-
d-old) fall armyworms was evaluated. Five first position white flower subtending
leaves, and entire white flowers, were removed from treated plants within the center
2 rows of each plot. Individual leaves were placed into 9.0 cm plastic Petri dishes, and
entire white flowers were placed into individual 236.6 ml paper Solo cups. A moist-
ened filter paper was placed into each dish or cup to delay plant tissue desiccation.
Fall armyworm larvae were reared on artificial diet for 24 hours to minimize disease
effects, and healthy larvae transferred to treated leaves or white flowers. Five larvae
were placed in each dish or cup (5 larvae/5 dishes or cups/plot, and replicated 4 times
= 100 larvae/treatment) using a small camel-hair brush. The dishes or cups were
sealed with corresponding lids. Both dishes and cups were maintained at 25' 1C
and 40 + 5% RH. Larval mortality was assessed at 24 and 48 h after infestation (HAI)
and were considered dead if no movement was observed after being probed gently
Armyworm Symposium '98:Adamczyk et al.
with a camel-hair brush for 5 s. Mean mortality was calculated for each dish or cup,
and these means were analyzed using ANOVA and treatments separated using the
Waller-Duncan k-ratio t-test (PRM 1995).
The toxicity of insecticide-treated cotton bolls to fifth instar (200-350 mg) fall ar-
myworms was evaluated using similar methods. Cotton bolls were age-classed using
the methods described in Adamczyk et al. (1997a). White flowers from the lower 0.5
m from plants were tagged at anthesis and heat unit (HU) accumulation was re-
corded. Bolls had accumulated 187.0 HU at the time insecticides were applied. These
bolls were removed from the plants and placed into individual 110.9 ml plastic cups.
One fifth instar was placed in each cup (10 bolls/plot and replicated 4 times = 40 lar-
vae/treatment), and the cups were sealed with corresponding lids. These containers
were maintained in an environmental chamber at 26 + 1C and a photoperiod of 14:10
(L:D) h. Larval mortality was assessed from 1-9 days after infestation (DAI) and were
considered dead if no movement was observed after being probed with blunt forceps
for 10 s. Results were analyzed using ANOVA and treatments separated using the
Waller-Duncan k-ratio t-test (PRM 1995).
RESULTS AND DISCUSSION
Diet Bioassay with Experimental Insecticides
The fall armyworm consists of two host-associated strains that widely differ in
their susceptibility to insecticides (Adamczyk et al. 1997b). Therefore, it is essential
that fall armyworm insecticide efficacy studies identify the host from which the test
insects were collected. Our data contain baseline susceptibility information for corn-
associated fall armyworms treated with four novel insecticides which can be used in
the future for monitoring insecticide susceptibility. LC0, values ranged from 4.4 ppm
for spinosad, to 492.9 ppm for thiodicarb (Table 1). The four novel insecticides (chlor-
fenapyr, methoxyfenozide, spinosad, and tebufenozide) were more toxic than the rec-
ommended insecticide, thiodicarb. The LC,0 values for these new insecticides are
similar to those reported by Mascarenhas et al. (1996) for the beet armyworm,
Spodoptera exigua (Htibner), using these same methods.
Toxicity of Cotton Plant Parts Treated with Insecticides to Fall Armyworm Larvae
First instar mortality was significantly greater on cotton leaves treated with chlo-
rfenapyr, L-cyhalothrin, or thiodicarb than for the untreated control at 24 HAI (Table
2). At 48 HAI, mortality for all treatments, with the exception of methoxyfenozide,
was significantly greater than for the untreated control.
First instar mortality was significantly greater on white flowers for all treatments,
with the exception of methoxyfenozide, than for the untreated control at 24 HAI (Ta-
ble 2). At 48 HAI, mortality for all treatments was significantly greater than for the
untreated control.
Fifth instar mortality on bolls was not significantly different among treatments at
1 DAI (Table 3). Larval mortality for all treatments, with the exception of methoxy-
fenozide and spinosad, was significantly greater than for the untreated control at 3
and 5 DAT. Fall armyworm larval mortality for all treatments, with the exception of
spinosad, was significantly greater than for the untreated control at 7 DAT.
Most of the insecticides tested against fall armyworms were equally effective.
While spinosad was very effective against first instars, the activity against fifth in-
stars was numerically lower compared to methoxyfenozide, L-cyhalothrin, thiodicarb,
Florida Entomologist 82(2)
June, 1999
TABLE 1. SUSCEPTIBILITY OF THIRD INSTAR FALL ARMYWORMS FROM A LABORATORY
STRAIN1 AFTER FIVE DAYS OF EXPOSURE TO DIET TREATED WITH SELECTED IN-
SECTICIDES.
95% Confidence Limits
No. LC502
Insecticide Tested (ppm) Low High Slopes (SE) X2
Chlorfenapyr 150 8.3 7.0 9.7 10.47 (1.75) 4.15
Methoxyfenozide 130 197.9 138.8 294.9 1.82 (0.42) 1.83
Spinosad 135 4.4 1.7 6.8 1.43 (0.42) 1.72
Tebufenozide 135 30.1 20.0 40.6 2.09 (0.44) 0.63
Thiodicarb 135 492.9 357.7 602.6 3.55 (0.74) 0.62
Clemson University, Department of Entomology.
LC0's significantly different if 95% confidence limits do not overlap.
chlorfenapyr, and emamectin benzoate. An insect growth regulator, methoxyfenozide,
was very effective against both larval stages, but required considerably longer to max-
imize mortality compared to the other insecticides. In bioassays using field treated
cotton parts, the pyrethroid, L-cyhalothrin, and carbamate, thiodicarb, were as effec-
tive as the newer compounds.
Our studies generally agree with the results of other fall armyworm research. Fall
armyworms are susceptible to numerous insecticides if the larvae are exposed to the
TABLE 2. TOXICITY OF INSECTICIDE RESIDUES ON COTTON LEAVES AND WHITE FLOWERS'
TO FIRST INSTAR FALL ARMYWORMS.
% Mortality
Leaves White Flowers
Rate
Treatment (kg AI/ha) 24 HAP2 48 HAI 24 HAI 48 HAI
Chlorfenapyr 0.34 69.7 a 84.1 a 47.7 ab 87.3 ab
Emamectin benzoate 0.01 54.3 ab 81.5 a 67.0 a 92.0 a
L-cyhalothrin 0.04 54.7 a 77.6 a 74.4 a 91.4 ab
Methoxyfenozide 0.51 25.6 c 54.7 b 31.0 bc 77.3 b
Spinosad 0.10 52.6 ab 85.8 a 50.3 ab 94.8 a
Thiodicarb 0.84 58.6 a 87.8 a 54.8 ab 86.5 ab
Untreated 30.7 bc 43.7 b 11.8 c 44.6 c
F value 4.3 5.9 4.6 11.7
(P >F)ANOVA <0.01 <0.01 <0.01 <0.01
Means in a column followed by the same letter are not significantly different (O = 0.05; Waller-
Duncan k-ratio t-test).
tLeaves and white flowers removed 2 hours after insecticide treatment.
Hours After Infestation.
Armyworm Symposium '98:Adamczyk et al.
TABLE 3. TOXICITY OF INSECTICIDE RESIDUES ON COTTON BOLLS' TO FIFTH INSTAR FALL
ARMYWORMS.
% Mortality
Rate
Treatment (kg AI/ha) 1 DAI 3 DAI 5 DAI 7 DAI
Chlorfenapyr 0.34 10.0 a 42.5 a 52.5 a 57.5 a
Em. benzoate 0.01 10.0 a 32.5 a 50.0 a 50.0 ab
L-cyhalothrin 0.04 20.0 a 32.5 a 40.0 ab 45.0 ab
Methoxyfenozide 0.51 5.0 a 10.0 b 35.0 abc 55.0 a
Spinosad 0.10 5.0 a 7.5 b 12.5 bc 22.5 bc
Thiodicarb 0.84 25.0 a 42.5 a 47.5 a 52.5 a
Untreated 0.0 a 2.5 b 7.5 c 15.0 c
F value 2.4 6.6 4.3 3.8
(P > F) ANOVA 0.07 <0.01 <0.01 <0.01
Means in a column followed by the same letter are not
Duncan k-ratio t-test).
'Bolls removed 2 hours after insecticide treatment.
'Hours After Infestation.
significantly different (a = 0.05; Waller-
insecticide (Mink & Luttrell 1989), but first instars are more susceptible to insecti-
cides compared to later instars (Yu 1983). In addition, inadequate penetration of in-
secticide sprays to the lower portions of the cotton plant continues to be a limiting
factor in controlling this pest (Mink & Luttrell 1989, Ali et al. 1990). Thus, it may be
beneficial for a producer to manage excessive plant height with plant growth regula-
tors (PGR s) in geographical areas where fall armyworms are an annual cotton pest.
ENDNOTE
The authors would like to thank Cotton Incorporated for financial support of this
project. We would like to thank Larry Daigle, Jon Holloway, Victor Mascarenhas, and
David Nyagah for their assistance in many aspects of these studies. This manuscript
is approved for publication by the Director of the Louisiana Agricultural Experiment
Station as Manuscript No. 98170068.
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ing the period of boll susceptibility to fall armyworm injury in cotton, pp. 941-943
in Proc. Beltwide Cotton Conf., National Cotton Council, Memphis, Tennessee.
ADAMCZYK, J. J., JR., J. W. HOLLOWAY, G. E. CHURCH, B. R. LEONARD, AND J. B.
GRAVES. 1997b. Susceptibility of fall armyworm collected from different plant
hosts to selected insecticides and transgenic Bt cotton. J. Cotton Sci. 1: 21-28.
ADAMCZYK J. J., JR., J. W. HOLLOWAY, G. E. CHURCH, B. R. LEONARD, AND J. B.
GRAVES. 1998. Larval survival and development of the fall armyworm (Lepi-
doptera: Noctuidae) on normal and transgenic cotton expressing the Bacillus
thuringiensis CryIA(c) a-endotoxin. J. Econ. Entomol. 91: 539-545.
ALI, A., R. G. LUTTRELL, AND H. N. PITRE. 1990. Feeding sites and distribution of fall
armyworm (Lepidoptera: Noctuidae) larvae on cotton. Environ. Entomol. 19:
1060-1067.
Florida Entomologist 82(2)
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BASS, M. H. 1978. Fall armyworm: evaluation of insecticides for control. Auburn Univ.
Leafl. 93: 7.
CHANDLER, L. D., AND J. R. RUBERSON. 1994. Comparative toxicity of four commonly
used insecticides to field-collected beet armyworm larvae from the southeast-
ern United States, pp. 860-864 in Proc. Beltwide Cotton Conf., National Cotton
Council, Memphis, Tennessee.
HOOD, E. 1997. The fall armyworm: and I thought I had it made, pp. 1223-1224 in
Proc. Beltwide Cotton Conf., National Cotton Council, Memphis, Tennessee.
JENKINS, J. N., W. L. PARROTT, AND J. C. MCCARTY, JR. 1992. Effects of Bacillus thu-
ringiensis genes in cotton on resistance to lepidopterous insects, p. 606 in Proc.
Beltwide Cotton Conf., National Cotton Council, Memphis, Tennessee.
JENKINS, J. N., J. C. MCCARTY, JR., R. E. BUEHLER, J. KISER, C. WILLIAMS, AND
T. WOFFORD. 1997. Resistance of cotton with a-endotoxin genes from Bacillus thu-
ringiensis var. kurstaki on selected Lepidopteran insects. Agron J. 89: 768-780.
JOYCE, J. A., R. J. OTTENS, G. A. HERZOG, AND M. H. BASS. 1986. A laboratory bioas-
say for thiodicarb against the tobacco budworm, bollworm, beet armyworm and
fall armyworm. J. Agric. Entomol. 3: 207-212.
KING, E. G., AND G. G. HARTLEY. 1985. Diatraea saccharalis, pp. 265-270 in P. Singh
and R. F. Moore [eds.], Handbook of Insect Rearing, vol. 2. Elsevier, Amster-
dam, Netherlands.
KING, E. G., J. R. PHILLIPS, AND R. B. HEAD. 1986. 39th annual conference report on
cotton insect research and control, pp. 126-135 in Proc. Beltwide Cotton Prod.
Res. Conf., National Cotton Council, Memphis, Tennessee.
LEORA SOFTWARE. 1987. POLO-PC a user's guide to Probit or Logit analysis. LeOra
Software, Berkeley, California 94707.
MASCARENHAS, V. J., B. R. LEONARD, E. BURRIS, AND J. B. GRAVES. 1996. Beet army-
worm (Lepidoptera: Noctuidae) control on cotton in Louisiana. Florida Ento-
mologist 79: 336-343.
MCCORD, E., AND S. J. YU. 1987. The mechanism of carbaryl resistance in the fall ar-
myworm, Spodoptera frugiperda (J. E. Smith). Pestic. Biochem. Physiol. 27:
114- 122.
MINK, J. S., AND R. G. LUTTRELL. 1989. Mortality of fall armyworm, Spodoptera fru-
giperda (Lepidoptera: Noctuidae) eggs, larvae and adults exposed to several in-
secticides on cotton. J. Entomol. Sci. 24: 563-571.
PASHLEY, D. P. 1986. Host-associated genetic differentiation in fall armyworm: a sib-
ling species complex? Ann. Entomol. Soc. Am. 79: 898-904.
PRM 1985. Pesticide Research Manager (PRM), Version 5.0 for IBM and IBM compat-
ible computers. Grylling Data Management, Inc., Brookings, SC 57006.
SMITH, R. H. 1985. Fall and beet armyworm control, pp. 134-136 in Proc. Beltwide
Cotton Prod. Res. Conf., National Cotton Council, Memphis, Tennessee.
SMITH, R. H. 1997. An extension entomologist's 1996 observations of Bollgard (Bt)
technology, pp. 856-857 in Proc. Beltwide Cotton Conf., National Cotton Coun-
cil, Memphis, Tennessee.
WOOD, K. A., B. H. WILSON, AND J. B. GRAVES. 1981. Influence of host plant on the
susceptibility of the fall armyworm to insecticides. J. Econ. Entomol. 74: 96-98.
YOUNG, J. R. 1979. Fall armyworm: control with insecticides. Florida Entomol. 62:
130-133.
YOUNG, J. R., AND W. W. MCMILLIAN. 1979. Differential feeding by two strains of fall
armyworm larvae on carbaryl treated surfaces. J. Econ. Entomol. 72: 202-203.
YU, S. J. 1983. Age variation in insecticide susceptibility and detoxification capacity of
fall armyworm (Lepidoptera: Noctuidae) larvae. J. Econ. Entomol. 76: 219.
YU, S. J. 1991. Insecticide resistance in the fall armyworm, Spodoptera frugiperda
(J. E. Smith). Pestic. Biochem. Physiol. 39: 84-91.
Armyworm Symposium '98: Carpenter & Wiseman
COMPARISONS OF LABORATORY AND FERAL STRAINS
OF SPODOPTERA FRUGIPERDA AND HELICOVERPA ZEA
(LEPIDOPTERA: NOCTUIDAE) IN LABORATORY
AND FIELD BIOASSAYS
J. E. CARPENTER AND B. R. WISEMAN
USDA-ARS, Insect Biology and Population Management
Research Laboratory, Tifton, GA 31793-0748
ABSTRACT
The effects of resistant corn entries and resistant silk-diets on the growth and de-
velopment of fall armyworm and corn earworm from a laboratory and a 3/4 wild colony
were compared in laboratory and field studies. For both species, there were significant
interactions between insect strain and diet treatments. Compared to the laboratory
strains, the 3/4 wild strains produced lighter larvae and required longer developmental
times when reared on diets with and without resistant silks. Larval growth of both in-
sect strains was significantly retarded by the addition of resistant silks to the diets.
In field studies, the 3/4 wild strains generally performed better than the laboratory
strains. For both insect species, interactions between insect strains and corn lines
were observed. Strain differences for all measured parameters were greater for the
corn earworm than for the fall armyworm. Results from these studies indicate that re-
search on plant resistance for the fall armyworm and the corn earworm would better
predict the relative levels of resistance among different corn lines and among differ-
ent silk diets if 3/4 wild colonies were established annually, and if insects from these 3/4
wild colonies were used in conducting laboratory and field bioassays.
Key Words: Plant Resistance; maize; corn silks; meridic diets
RESUME
Los efectos de la introducci6n de lines resistentes de maiz y de dietas con estig-
mas resistentes en el crecimiento y desarrollo del gusano cogollero del maiz y del gu-
sano del elote del maiz de una colonia de laboratorio y de una colonia 3/4 salvaje fueron
comparadas en studios de laboratorio y de campo. Para ambas species se notaron in-
teracciones significativas entire el tipo de insecto y los tratamientos de dieta. En com-
paraci6n con las colonies de laboratorio, las colonies 3/4 salvajes produjeron larvas mas
ligeras y que requirieron periods de desarrollo mas largos cuando se criaron en die-
tas con o sin estigmas resistentes. El crecimiento larval de ambos tipos de insecto fue
significativamente retardado por la adici6n de estigmas resistentes a las dietas. En
studios de campo, las colonies 3/4 salvajes resultaron mejores que las colonies de la-
boratorio. En ambas species se observaron interacciones entire los tipos de insecto y
las lines de maiz. En todos los parametros medidos las diferencias entire las colonies
fueron mas grandes para el gusano del elote que para el gusano cogollero. Los resul-
tados de estos studios indican que investigaciones sobre resistencia del maiz contra
el gusano cogollero y el gusano del elote podrian predecir mejor los niveles relatives
de resistencia entire lines diferentes de maiz y entire diferentes dietas de estigmas si
se establecieran anualmente colonies 3/4 salvajes y si insects de estas colonies 3/4 sal-
vajes se utilizaran para conducir bioensayos de laboratorio y de campo.
Florida Entomologist 82(2)
June, 1999
The fall armyworm, Spodoptera frugiperda (J. E. Smith), and the corn earworm,
Helicoverpa zea (Boddie), are two of the most destructive pests of corn, Zea mays L.,
in the United States. The use of corn varieties resistant to these insect pests is an
ideal method to reduce losses caused by insect feeding and to reduce the population
density of insect pests developing on corn. Resistant corn varieties can be used as the
primary method of insect control or as a component of an integrated pest manage-
ment scheme (Wiseman et al. 1983). Corn germplasm resistant to the fall armyworm
(Wiseman et al. 1976, Williams & Davis 1997a, Wiseman et al. 1981) and to the corn
earworm (Straub & Fairchild 1970, Wiseman & Davis 1990) have been discovered.
Rearing fall armyworm and corn earworm in laboratory colonies has been an im-
portant part of research programs developing corn varieties resistant to these insect
pests (Davis & Guthrie 1992). Laboratory reared insects are used to artificially infest
corn plants in the field, and fresh leaves and silk diets and reconstituted leaf and silk
diets in the laboratory (Davis et al. 1989, Williams & Davis 1997b, Wiseman et al.
1981, Wiseman et al. 1983, Wiseman & Wilson 1987). Although natural populations
or field collections of fall armyworm and corn earworm can be useful to researchers in
plant resistance, laboratory colonies of these pests provide a reliable source of insects
for these studies and thereby allow for an expanded research program. Because labo-
ratory colonies of fall armyworm and corn earworm are relied upon by many research-
ers to conduct plant resistance studies, it is important that the insects in the
laboratory colonies are physiologically and behaviorally equivalent to their wild coun-
terparts (Davis & Guthrie 1992). The infusion of new genes from wild insects into lab-
oratory colonies can improve the field performance of laboratory-reared insects
(Young et al. 1975). As a precautionary measure, some researchers start new labora-
tory colonies or infuse new genes into their laboratory colony each year (Davis &
Guthrie 1992). In this study, our objectives were to compare the performance of a lab-
oratory colony and a 3/4 wild colony of the corn earworm and fall armyworm when
reared on silk-diets or on corn plants in the field with varying levels of resistance.
MATERIALS AND METHODS
Laboratory corn earworm and fall armyworm larvae were obtained from cultures
maintained on a corn-soy-milk solids and pinto bean diets, respectively, (Perkins
1979; Burton & Perkins 1989) at the Insect Biology and Population Management Re-
search Laboratory, Tifton, GA. The laboratory corn earworm culture is sustained in a
heterozygous state by maintaining a series of carefully controlled crosses (Young et al.
1976). A 3/4 wild strain was developed for both the corn earworm and fall armyworm
by crossing wild males with laboratory females. Female progeny (V2 wild) from these
crosses were mated with wild males (Young et al. 1975). Wild corn earworm males
were collected in light traps during early and late October, 1996. Wild fall armyworm
males were collected as larvae from whorl corn during late August and late Septem-
ber, 1996.
Laboratory studies were conducted on the 3/4 wild, corn earworm strain during the
2nd and 3rd generation. Field studies were conducted on the 3/4 wild, corn earworm
strain during the 5th and 6th generation. Laboratory studies were conducted on the
3/4 wild, fall armyworm strain during the 3rd and 4th generation, and field studies
were conducted during the 7th and 8th generations.
Two laboratory experiments, one for the corn earworm and the other for the fall ar-
myworm, were conducted as a split plot design with 30 replications and 1 cup per rep-
lication. Whole plots were the laboratory strain insects and the 3/4 wild strain insects,
and subplots were diet treatments. Diets were made using 50 and 25 mg 'Zapalote
Armyworm Symposium '98: Carpenter & Wiseman
Chico' (resistant) and 50 mg 'Stowell's Evergreen' sweet corn oven dried silks mixed
(per 1 ml diluted diet) in pinto bean diet diluted at a rate of 3 ml of bean diet/2 ml of
water. Controlled diets for each experiment were regular pinto bean diet (Burton &
Perkins 1989) and a celufil check at the rate of 50 mg celufil/ml of dilute diet. The diet
mixtures were dispensed into 30 ml plastic diet cups of -10 ml per cup. The diets were
allowed to cool for -2 h, after which 1 neonate was introduced into each cup and the
cup was capped. Weight of larvae (8 d for the corn earworm and 9 d for the fall army-
worm), days to development to pupation and weight of pupae were recorded. Both ex-
periments were held in a controlled environment room maintained at 28 + 2C and 75
+ 2% RH with a photoperiod of 14:10 (L:D).
Two field experiments with two planting dates each were conducted in 1997 for the
corn earworm and fall armyworm. Four dent corn entries (resistant 'MpSWCB-4' and
'GT-FAWCC(C5)' or susceptible 'Cacahuacintle X's' and 'Pioneer 3369A') were selected
for comparison against the fall armyworm. Zapalote Chico and 'Zimmerman Z-63W'
(resistant) and Stowell's Evergreen and Pioneer 3369A (susceptible) were selected for
comparison against the corn earworm.
The fall armyworm tests were seeded on 13 May, 1997 and 29 May, 1997 at Tifton,
GA. The corn earworm tests were seeded on 2 April, 1997 and 22 April, 1997 at Tifton,
GA. Test plots consisted of single rows 6.1 m long and 0.9 m apart. Plants were
thinned to ca. 30 cm apart. Recommended agronomic practices were followed for both
tests and planting dates.
A split plot design with 6 replications was used with whole plots being a check plot
with no infestation, infested with the 3/4 wild strain and infested with the laboratory
culture of the fall armyworm or corn earworm, respectively. Subplots were corn en-
tries.
Whorl stage plants (10 leaves) were infested with a total of 30 fall armyworm ne-
onates (2 applications of 15/plant on the same day) using the 'Bazooka' method (Wise-
man 1989). Counts of larvae and weight of biomass were made per 5 plants at 7 d after
infestation (DAI) and rated at 7 and 14 DAI using a visual rating scale of 0-9 (Davis
et al. 1992), where 0 = no damage and 9 = whorl destroyed.
Corn earworm larvae were infested on two-day-old silks at the rate of 5 larvae/silk
mass. Counts of larvae and weight of their biomass per 5 ears were made at 7 DAI and
injury ratings were made at 18 DAI (Wiseman 1989).
Data from laboratory tests and field tests were analyzed by PROC GLM (SAS In-
stitute 1989). When significant differences were indicated, means were separated by
least significant differences (LSD) at P = 0.05 (SAS Institute 1989).
RESULTS AND DISCUSSION
Laboratory Experiments
Studies with the corn earworm revealed a significant interaction between insect
strain and diet treatments for the 8-d larval weights (Table 1). Larvae from the labo-
ratory colony performed significantly better on the bean diet than on the celufil and
susceptible diets. Larvae from the 3/4 wild colony performed significantly better on the
celufil diet than on the bean and susceptible diets. Larval growth of both insect
strains was significantly retarded by the addition of resistant silks to the diets. In
general, the 8-d larval overall diet weights of the 3/4 wild strain were about half the 8-
d larval weights of the laboratory strain. The mean 8-d larval weight across diet treat-
ments was 169.4 mg for the laboratory strain and 80.3 mg for the 3/4 wild strain. There
was a significant interaction between insect strain and diet treatments for the devel-
Florida Entomologist 82(2)
June, 1999
TABLE 1. EFFECT OF DIET TREATMENTS AND CORN EARWORM STRAIN ON WEIGHT (MG) OF
8-D-OLD LARVAE, DEVELOPMENTAL TIME OF LARVAE (DAYS TO PUPATION), AND
PUPAL WEIGHT (MG).
Diet Treatment'
Insect
Strain BNCK CLCK SEG25 ZC25 ZC50 Mean
Weight (mg) of 8-d-old larvae
Laboratory 278.9 Aa 221.4 Ab 202.9 Ab 102.3 Ac 32.8 Ad 169.4
3/4 Wild 103.6 Bb 139.9 Ba 106.5 Bb 36.1 Bc 7.6 Ad 80.3
Mean 201.4 180.6 159.2 70.5 20.9
Developmental time of larvae (days to pupation)
Laboratory 13.1 Ad 14.3 Acd 15.4 Ac 17.7 Ab 26.9 Aa 17.0
3/4 Wild 18.3 Bc 18.8 Bc 18.9 Bc 21.2 Bb 37.3 Ba 21.6
Mean 15.1 16.4 16.9 19.3 30.7
Pupal weight (mg)
Laboratory 554.6 Aa 531.3 Aa 528.9 Aa 467.8 Ab 287.3 Ac 484.9
3/4 Wild 398.5 Bb 414.9 Bab 432.2 Bab 437.3 Aa 321.7 Ac 409.0
Mean 495.6 478.6 488.3 453.9 299.8
'BNCK= Bean check diet; CLCK= Celufil check; SEG25 = 'Stowell's Evergreen' 25 mg silks; ZC25 = 'Zapalote
Chico' 25 mg silks; ZC50 = 'Zapalote Chico' 50 mg silks. Horizontal means followed by the same lowercase letter
are not significantly different, and column means for each parameter followed by the same uppercase letter are
not significantly different (PoeO.05) as separated by LSD (SAS Institute 1989).
opmental time of corn earworm to pupation (Table 1). The laboratory strain required
significantly more time to develop on diet containing susceptible silks than on the
bean diet; however, there was no difference in the developmental time for the 3/4 wild
strain on these two diets. The number of days to pupation for both insect strains was
significantly increased by the addition of resistant silks to the diets. The 3/4 wild strain
required a greater number of days to pupate on each diet treatment than did the lab-
oratory strain. There also was a significant interaction between insect strain and diet
treatments for the weight of corn earworm pupae (Table 1). Addition of resistant silks
to the diet significantly reduced the weight of pupae for the laboratory strain. How-
ever, 3/4 wild strain pupae that developed on the diet with the lower concentration of
resistant silks were significantly heavier than pupae that developed on the bean diet.
Except for the diet with the higher concentration of resistant silks, each diet treat-
ment yielded heavier laboratory strain pupae than 3/4 wild strain pupae.
Studies with the fall armyworm also showed a significant interaction between in-
sect strain and diet treatments for the 9-d larval weights (Table 2). Larvae from both
fall armyworm strains performed significantly better on the bean diet than on the ce-
lufil and susceptible diets. Larval growth of both insect strains was significantly re-
tarded by the addition of resistant silks to the diets. Larvae from the 3/4 wild strain
weighed about 84% the weight of larvae from the laboratory strain when reared on
the bean diet, and weighed about 50% the weight of larvae from the laboratory strain
when reared on the resistant silk-diets. There was a significant interaction between
insect strain and diet treatments for the developmental time of fall armyworm to pu-
pation (Table 2). The number of days to pupation for both insect strains was signifi-
Armyworm Symposium '98: Carpenter & Wiseman
TABLE 2. EFFECT OF DIET TREATMENTS AND FALL ARMYWORM STRAIN ON WEIGHT OF 9-
D-OLD LARVAE, DEVELOPMENTAL TIME (DAYS TO PUPATION), AND PUPAL
WEIGHT (MG).
Diet Treatments'
Insect
Strain BNCK CLCK SEG25 ZC25 ZC50 Mean
Weight (mg) of 9-d-old larvae
Laboratory 212.OAa 187.1Ab 155.5 Ac 35.1 Ad 6.1Ae 119.2
3/4 Wild 177.1 Ba 148.4 Bb 92.1 Bc 17.4 Ad 3.2 Ad 87.6
Mean 194.5 167.8 a 123.8 26.2 4.6
Developmental time of larvae (days to pupation)
Laboratory 14.4 Aa 15.5 Aab 16.1 Ab 20.4 Ac 27.2 Ad 18.7
3/4 Wild 15.9 Ba 17.1 Bab 17.9 Bb 22.2 Bc 33.7 Bd 21.4
Mean 15.2 16.2 17.0 21.3 30.4
Pupal weight (mg)
Laboratory 305.4 A 273.2 A 272.6 A 243.4 A 159.9 A 159.7 a
3/4 Wild 297.9 A 281.7 A 297.4 B 247.1 A 176.7 A 274.5 b
Mean 301.3 a 277.5 b 285.7 b 245.3 c 165.8 d
'BNCK= Bean check diet; CLCK = Celufil check; SEG25 = 'Stowell's Evergreen' 25 mg silks; ZC25 = 'Zapalote
Chico' 25 mg silks; ZC50 = 'Zapalote Chico' 50 mg silks. Horizontal means followed by the same lowercase letter
are not significantly different, and column means for each parameter followed by the same uppercase letter are
not significantly different (P s 0.05) as separated by LSD (SAS Institute 1989).
cantly increased by the addition of resistant silks to the diets. Developmental time on
bean diet for 3/4 wild larvae was about 1.5 d longer than the developmental time for
laboratory larvae. When larvae were reared on the more resistant silk-diet, the devel-
opmental time for 3/4 wild larvae was about 6.5 d longer than the developmental time
for laboratory larvae. Pupae from the 3/4 wild strain were significantly heavier than
pupae from the laboratory strain (Table 2). Larvae that developed on bean diet pro-
duced significantly heavier pupae than did larvae that developed on the celufil and
susceptible silk diets. Resistant silk diets produced significantly lighter pupae than
the other diet treatments.
Field Experiments
The number of corn earworm larvae collected from 5 corn ears 7 d after infestation
was significantly influenced by insect strain and corn line (Table 3). There was a sig-
nificant interaction between corn line and insect strain for the first planting date but
not for the second planting date. For each planting date, more larvae were found in the
3/4 wild strain treatment than in the laboratory strain treatment. More larvae were
produced on Stowell's Evergreen than the other corn lines for the first planting date,
and more larvae were produced on P3369A than the other corn lines for the second
planting date. The weight of larvae per 5 corn ears was similar to the number of larvae
per 5 corn ears. Again, there was a significant interaction between corn line and insect
strain for the first planting date but not for the second planting date (Table 4). Also,
Florida Entomologist 82(2)
June, 1999
TABLE 3. EFFECT OF CORN LINES AND CORN EARWORM STRAIN ON LARVAL SURVIVAL AT
7 DAYS AFTER INFESTATION (NO. OF LARVAE/5 EARS).
Corn Line'
Insect Strain SEG ZC Z63W P3369A Mean
First Planting Date (2 April)
Check 3.3 Aa 1.5 Aa 1.3 Aa 1.8 Aa 2.0
Laboratory 8.2 Ba 2.2 Ab 2.8 ABb 2.8 Ab 4.0
3/4 Wild 13.3 Ca 4.5 Ab 5.5 Bb 3.8 Ab 6.8
Mean 8.3 2.7 3.2 2.8
Second Planting Date (22 April)
Check 3.2 Ab 0.2 Ac 7.0 Aa 9.8 Aa 5.0 A
Laboratory 7.2 Ba 1.8 Ab 6.3 Aa 8.3 Aa 5.9 AB
3/4 Wild 11.3 Ca 2.8 Ab 7.5 Ab 10.5 Aa 8.0 B
Mean 7.2 b 1.6 c 6.9 b 9.6 a
'SEG= 'Stowell's Evergreen'; ZC = 'Zapalote Chico'; Z63W= 'Zimmerman Z-63W'; P3369A= 'Pioneer 3369A'.
Horizontal means followed by the same lowercase letter are not significantly different, and column means for
each planting date followed by the same uppercase letter are not significantly different (P s 0.05) as separated
by LSD (SAS Institute 1989).
for each planting date, the weight of larvae per 5 corn ears was greater for the 3/4 wild
strain than for the laboratory strain, however, the difference was not significant. For
each planting date, the weight of larvae per 5 corn ears was significantly greater for
TABLE 4. EFFECT OF CORN LINES AND CORN EARWORM STRAIN ON WEIGHT OF LARVAE 7
DAYS AFTER INFESTATION [WEIGHT (MG) OF LARVAE/5 EARS].
Corn Line'
Insect Strain SEG ZC Z63W P3369A Mean
First Planting Date (2 April)
Check 115.7 Aa 56.3 Aa 2.7 Aa 15.3 Aa 47.5
Laboratory 274.8 Ba 30.3 Ab 86.8 Ab 32.3 Ab 106.1
3/4 Wild 349.5 Ba 126.5 Abc 24.0 Abc 9.7 Ac 127.4
Mean 246.7 71.1 37.8 19.1
Second Planting Date (22 April)
Check 222.7 Aa 0.5 Ab 99.7 Aab 152.5 Aab 118.8 A
Laboratory 244.3 Aa 21.2 Ab 179.7 Aab 135.5 Aab 145.2 A
3/4 Wild 321.5 Aa 192.7 Aab 81.8 Ab 100.0 Ab 174.0 A
Mean 262.8 a 71.4 b 120.4 b 129.3 b
'SEG= 'Stowell's Evergreen'; ZC = 'Zapalote Chico'; Z63W= 'Zimmerman Z-63W'; P3369A= 'Pioneer 3369A'.
Horizontal means followed by the same lowercase letter are not significantly different, and column means for
each planting date followed by the same uppercase letter are not significantly different (P 0.05) as separated
by LSD (SAS Institute 1989).
Armyworm Symposium '98: Carpenter & Wiseman
Stowell's Evergreen than for the other corn lines. Measurements of the depth of ear
penetration 18 d after infestation for the first planting date revealed that larvae from
the 34 wild strain penetrated significantly deeper into the ear than did the larvae from
the laboratory strain or larvae from natural infestation (Table 5). Depth of ear pene-
tration was significantly greater for Stowell's Evergreen than for the other corn lines.
Results of ear penetration for the second planting date was similar except that there
was a significant interaction between corn line and insect strain.
Results from the field study with fall armyworm showed significant interactions
between corn lines and insect strain for each of the measured parameters for each
planting date. For the first planting date the mean number of 34 wild larvae per 5
plants was about twice the number of laboratory larvae per 5 plants (Table 6). The
mean number of larvae per plant for the second planting date was similar for the 3/4
wild and laboratory strains (18.6 and 21.9, respectively). No larvae were found in the
check plots. More larvae were found in the susceptible corn plots than in the resistant
corn plots for both planting dates. The weight of larvae per 5 plants for each corn line
was greater for the laboratory strain than for the 34 wild strain for the second planting
date (Table 7). Also, the weight of larvae per 5 plants was greater for susceptible corn
lines than for resistant corn lines. Weight of larvae per 5 plants was not recorded for
the first planting date. The 7-d visual damage rating for the 34 wild strain was greater
than the 7-d visual damage rating for the laboratory strain for the first planting date
(Table 8). For the second planting date the 7-d visual rating was similar for the 34 wild
and laboratory strains (2.5 and 2.7, respectively). No damage was found in the check
plots. Damage ratings were higher in the susceptible corn plots than in the resistant
corn plots for both planting dates. The visual damage ratings after 14 d were higher
in each case than the damage ratings taken after 7 d (Table 9). Otherwise, the 14-d
damage ratings were similar to the 7-d damage ratings when comparing between in-
sect strains and among corn lines.
TABLE 5. EFFECT OF CORN LINES AND CORN EARWORM STRAIN ON DEPTH (CM) OF LAR-
VAL PENETRATION INTO THE EAR 18 DAYS AFTER INFESTATION.
Corn Line'
Insect Strain SEG ZC Z63W P3369A Mean
First Planting Date (2 April)
Check 3.8 Aa 2.6 Ab 1.6 Ac 2.5 Abc 2.5 A
Laboratory 3.6 Aa 2.5 Ab 1.9 Ab 2.8 Aab 2.7 A
3/4 Wild 5.1 Ba 3.1 Ab 2.7 Ab 2.8 Ab 3.4 B
Mean 4.1 a 2.7 b 2.1 c 2.5 bc
Second Planting Date (22 April)
Check 5.5 Aab 2.6 Ac 4.7 Ab 6.1 Aa 4.7
Laboratory 7.6 Ba 3.2 ABc 4.8 Ab 5.9 Ab 5.4
3/4 Wild 8.1 Ba 4.4 Bb 5.1 Ab 5.8 Ab 5.9
Mean 7.1 3.4 4.9 5.9
'SEG= 'Stowell's Evergreen'; ZC = 'Zapalote Chico'; Z63W= 'Zimmerman Z-63W'; P3369A= 'Pioneer 3369A'.
Horizontal means followed by the same lowercase letter are not significantly different, and column means for
each planting date followed by the same uppercase letter are not significantly different (P s 0.05) as separated
by LSD (SAS Institute 1989).
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