COMMUNITY AND ECOSYSTEM ECOLOGY

Identification and Diel Activity Patterns of Predators Attacking

Helicoverpa zea (Lepidoptera: Noctuidae) Eggs in Soybean
and Sweet Corn
R. S. PFANNENSTIEL1 AND K. V. YEARGAN
Department of Entomology, University of Kentucky, Lexington, KY 40546

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Environ. Entomol. 31(2): 232Ð241 (2002)
ABSTRACT Predation on lepidopteran eggs in soybean and corn and the temporal partitioning of
predation among the predator species were examined in soybean Glycine max (L.) and sweet corn
Zea mays (L.). The complex of predators feeding on lepidopteran eggs [Helicoverpa zea (Boddie)]
and the key predators discovered in this study were different in each crop. The dominant predator
in each crop was consistent from year to year but the secondary predators varied in importance. Nabids
were the dominant predator group in soybean contributing 51 and 50% of the observed predation
events in 1993 and 1994, respectively. The coccinellid, Coleomegilla maculata (DeGeer), was the
dominant predator in corn contributing 43.9 and 46.3% of the observed predation events in 1993 and
1994, respectively. Other predators causing ⱖ10% of the observed predation events included Geocoris
punctipes Say and the Phalangiidae in soybean, and the nabids, Orius insidiosus Say and Lygus lineolaris
(Palisot de Beauvois) in sweet corn. All predators observed feeding exhibited taxa speciÞc diel patterns
of predation. C. maculata, O. insidiosus and G. punctipes were primarily day active, with 75, 85.7, and
100% of observed predation events occurring during daylight hours, respectively. Nabids were
primarily nocturnal with 84.2% of predation events happening at night. Phalangiids, Clubiona abbotii
Koch, Lygus lineolaris, and the elaterids were only observed preying upon H. zea eggs nocturnally.
Because the dominant predators and their diel activity varied between crops, the period of peak egg
predation did also. Egg predation was usually higher during the day in corn and at night in soybean.
Crop, date, and time of day all affected intensity of predation on H. zea eggs. Predation in both crops
increased through the beginning of August and then declined on the last sampling date. Predation was
usually higher in corn than in soybean (three of four sample dates). However, when anthesis was
occurring in corn plots, predation rates in soybean and corn were similar. Apparently the availability
of sweet corn pollen as an alternative food source for C. maculata caused a reduction in egg predation.

KEY WORDS Helicoverpa zea, Hemiptera, Coccinellidae, predation, diel activity, diurnal

IDENTIFYING THE PREDATOR species feeding on speciÞc
insect pests is an important step in determining the
impact predation may have on pest populations. Stud-
ies have attempted to identify predators attacking lep-
idopteran pests in Þeld crops such as corn, Zea mays
(L.) (Andow 1990), cotton (Gossypium hirsutum L.)
(Whitcomb and Bell 1964, Whitcomb 1967, McDaniel
and Sterling 1979, Nuessly and Sterling 1994, Ruberson
and Greenstone 1998), and soybean, Glycine max (L.)
[Leguminoseae] (Buschman et al. 1977, McCarty et al.
1980, Richman et al. 1980, Godfrey et al. 1989). How-
ever, studies that used direct observation (Whitcomb
and Bell 1964, Buschman et al. 1977) inadequately
addressed nocturnal predation, and studies using ra-
dioactive labeling may produce biased results due to
intraguild predation (i.e., predation on predators)
1
Current address: Subtropical Agricultural Research Center,
USDA-ARS, 2413 E. Highway 83, Weslaco, TX 78596 (e-mail:
rpfannenstiel@weslaco.ars.usda.gov).
(McCarty et al. 1980). The use of immunological tech-
niques (Ruberson and Greenstone 1998) may suffer
from quick degradation of antigens within the pred-
ator (Sansone and Smith 2001). Few of the studies that
previously used direct observation to determine pre-
dation events in crops partitioned diel patterns of
predation. Godfrey et al. (1989) included nocturnal
observations in their study, but spent proportionally
little time conducting nocturnal observations (4 of
16 h per date in 1981 and 2 of 14 h per date in 1982)
and did not partition their results by time of day.
It appears that the complex of predators that feed on
lepidopteran eggs may vary temporally. In separate
studies in soybean, the dominant predators recorded
by direct observation during the daylight (primarily
Formicidae and Dermaptera with 39.4 and 27.4% of the
observations, respectively) differed from those dis-
covered in studies using radioactive labeling (primar-
ily Nabidae and Chrysopidae with 31.3 and 25% of the
observations, respectively) (Buschman et al. 1977).
April 2002 PFANNENSTIEL AND YEARGAN: H. zea EGG PREDATION
Cottrell and Yeargan (1998a, 1998b) showed that Co-
leomegilla maculata (DeGeer) (Coleoptera: Coccinel-
lidae) was primarily day active, although larvae would
continue to feed through the night. Other than the
studies by Cottrell and Yeargan (1998a, 1998b) in
sweet corn, the taxa causing egg predation of lepidop-
teran pests in particular habitats have not been ade-
quately described. Also, predator populations may
vary between different crops, even over a small spatial
scale (Pfannenstiel and Yeargan 1998). We wanted to
simultaneously determine the important predators of
a single pest in multiple habitats. In this study, we
identiÞed the important predators of lepidopteran
eggs in soybean and sweet corn using eggs of the
common pest Helicoverpa zea (Boddie) (Lepidoptera:
Noctuidae). We also determined the diel patterns of
predation by each important predator species and the
impact of these predators on egg survival in soybean
and sweet corn.
Materials and Methods
Predation on lepidopteran eggs was evaluated in
soybean (ÔFlyerÕ), and sweet corn (ÔGolden QueenÕ)
during 1993 and 1994. Crop establishment and main-
tenance practices for these studies are essentially the
same as those used in previous studies on predator
abundance (Pfannenstiel and Yeargan 1998). Soybean
and sweet corn were planted in plots (11.1 by 11.1 m)
in a completely randomized design with four replicate
plots of each crop. Plots were established in May 1993
and 1994 by practices typical for production of each
crop. Soybean and corn were directly seeded with a
mechanical planter on 0.92- and 1.03-m row spacings.
For weed control within plots, we applied herbicides
appropriate for the production of each crop; Alachlor
(8.35 kg/ha) and metribuzin (1.05 kg/ha) were ap-
plied preemergence in soybean, alachlor (8.35 kg/ha)
and cyanazine (4.37 kg/ha) were applied preemer-
gence for corn. All herbicides were applied with a
backpack sprayer to the soil surface. There were 3.1-m
bare ground buffers surrounding all plots and edges of
the Þeld. Hoeing and hand weeding were conducted
throughout the season to supplement weed control
within each plot. Buffer maintenance was conducted
by rototilling, hoeing, and spot treatment with herbi-
cide (glyphosate). The crop layout used in 1993 was
rerandomized for 1994. No pesticides were used dur-
ing the course of this study. Twelve sampling stations
were chosen in each plot along the length of two rows
approximately one-third and two-thirds the distance
from the edge row, respectively. Six stations were
placed 1.5 m apart and 1.5 m from ends of the plot in
each of these two rows and marked with a ßag.
Helicoverpa zea colonies were maintained in the
laboratory by modiÞed methods of Ignoffo (1965).
Adults were placed in 3.8-liter ice cream cartons lined
with green ßorist paper for oviposition; a 10% sucrose
solution was provided as a food source. Eggs were
collected daily; paper on which eggs had been laid was
cut into small (3Ð20 cm2) sections containing 10 H. zea
eggs each. Egg groups were then placed in a refrig-
233
erator at 4⬚C to stop development until used or dis-
carded after 4 d. Groups of 10 eggs (as opposed to one
egg) were used to extend the amount of time a pred-
ator feeds, thus increasing the probability of observing
predation events. Although it is possible that this tech-
nique may have biased estimates of predation because
of the locally high density of eggs, the potential for bias
was not tested in this study. Lepidopteran pests that
deposit eggs singly (e.g., H. zea) lay a disproportionate
number of eggs on speciÞc plant parts (Terry et al.
1987, Eckel et al. 1992), which can result in a clumped
distribution of eggs. Also, the use of green ßorists
paper, instead of afÞxing eggs to the natural substrate,
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has the advantage that these pieces of paper are more
likely to retain potential kairomones associated with
oviposition (moth scales, accessory gland secretions,
pheromone residues) than would eggs removed from
the original oviposition site and glued on the plants.
Moth scales in particular have been observed to affect
localized searching by egg parasitoids (Jones et al.
1973, Beevers et al. 1981, Zaborski et al. 1987, Shu et
al. 1990). Predators of lepidopteran eggs are likely to
use similar cues. Furthermore, the technique used
here does not require the use of “foreign” adhesives
such as egg albumin or an artiÞcial glue which might
in themselves be attractive or alternatively repellent
to predators.
Eggs were transported to the Þeld in an ice chest
with ice and then attached to plants at 1200 hours by
stapling the groups in the desired locations. Noon was
used for deployment of eggs for purely logistical pur-
poses. H. zea eggs typically take 3 d or more to develop
in the Þeld in Kentucky and would be available to
predators throughout this time (R.S.P., unpublished
data). Paper sections containing eggs were not used if
any of the eggs were dislodged during transportation.
Egg groups were attached to the top of a soybean leaf
⬇45Ð55 cm above the ground (⬇55Ð70% of plant
height) or to one of the small leaves (husk terminals)
directly adjacent the silks on the primary ear of a corn
plant. Pest of Þeld crops such as soybean often deposit
their eggs on the foliage of the middle to upper parts
of the plant (Terry et al. 1987, Sappington et al. 2001;
R.S.P., unpublished data) although often on the un-
dersides of leaves. Placing the eggs on the top of leaves
was done to facilitate observation. There are prelim-
inary indications that egg predation rates on the upper
surface of leaves of Þeld crops may be similar to that
of eggs placed on the underside of leaves (R.S.P.,
unpublished data). Most H. zea eggs deposited on corn
plants are laid on the silks although some are also laid
on the leaves and ears (Barber 1936, Archer and By-
num 1994). Eggs were attached to corn plants as close
to corn silks (when present) as possible.
Egg groups were observed at 3-h intervals (1500,
1800, 2100, 2400, 0300, 0600, 0900, and 1200 hours
EDT) for the following 24 h. This distribution of sam-
pling times results in 4 d (0900, 1200, 0300, and 0600
hours) and four night samples (2100, 2400, 0300, and
0600 hours EDT). Sunrise occurred as the 0600 sample
was being Þnished and sunset occurred just before the
2100 hours sample was initiated, allowing for equal
234 ENVIRONMENTAL ENTOMOLOGY Vol. 31, no. 2

Table 1. Frequency of observation of arthropods feeding upon H. zea eggs in soybean and corn

Soybean Corn
1993 1994 1993 1994
Hemiptera Nabis spp. adults 7 11 3 9
Nabis spp. nymphs 46 26 10 2
G. punctipes adults 6 1 4 0
G. punctipes nymphs 12 0 2 0
Orius insidiosus 3 2 11 19
Lygus lineolaris 0 1 2 12
Acrosternum hilare 1 0 0 0
Coleoptera C. maculata adults 0 2 20 33
C. maculata larvae 0 5 27 24
Elateridae 0 1 3 9

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Carabidae 0 3 2 3
Diabrotica virgifera 0 0 0 4
Miscellaneous (⬍5mm) 0 1 12 2
Orthoptera Tettigoniidae 8 1 0 0
Hymenoptera Formicidae 0 2 2 0
Neuroptera Hemerobiidae 0 0 0 1
Arachnida Phalangiidae 14 13 2 0
Clubiona abbotii 7 2 7 3
Mites 0 3 0 2
Total 104 74 107 121

numbers of day and night samples despite a photo-
phase lasting about 14 h. H. zea eggs take about 3 d to
develop; due to their prompt refrigeration, eggs used
during this study did not approach hatching at any
time. At each observation period, predators observed
feeding on the H. zea eggs were collected for subse-
quent identiÞcation. All egg groups that had been fed
upon (missing one or more eggs) were replaced at
each observation period. Replacing any egg groups
that had been fed upon kept the probability of ob-
serving predation at each site during each time period
equal throughout the 24 h. The identiÞcation of the
important predators and their diel activity patterns
was the primary focus of this study and took prece-
dence to estimation of predation rates. This experi-
ment was conducted on three dates in 1993 and four
dates in 1994. In 1993, the three samples were col-
lected over an 8-d period when corn was at the mature
ear stage and soybean was at growth stage R-4/R-5
(full pod/beginning seed) (Fehr and Caviness 1977).
In 1994, the Þrst two sample dates in corn coincided
with tasseling and the third and fourth were done at
the mature ear stage. The growth stages of soybean in
1994 by sample date were; R-1 (beginning bloom), R-2
(full bloom), R-3/R-4 (pod formation), and R-4/R-5
(full pod/beginning seed), respectively (Fehr and
Caviness 1977). SpeciÞc sample dates were 18 Ð19,
23Ð24, and 25Ð26 August in 1993, and 11Ð12 and 18 Ð19
July, and 1Ð2 and 8 Ð9 August in 1994. In 1994, the
number of egg groups fed upon and the number of
eggs missing from each group since the previous ob-
servation period were recorded to estimate levels of
predation in each crop. All sample periods for esti-
mation of predation rates could be ascribed to day
(0900, 1200, 1500, and 1800 hours) or night (2400, 0300,
and 0600 hours) except the 2100 hours sample for
which the estimate of predation resulted from preda-
tion events occurring during both day and night.
The temporal distribution of predation events was
analyzed to determine if each predator taxon was
diurnal or nocturnal. Observations of a taxon were
combined from both crops. Observed predation
events were divided into two groups for analysis: ei-
ther occurring during daylight (0900, 1200, 1500, and
1800 hours) or at night (2100, 2400, 0300, and 0600).
Deviation of the frequency of predation events from
the expectation of a random distribution between
these two periods was analyzed for all taxa with a
sample size ⬎10 with the test of signiÞcance of a
binomial proportion (Snedecor and Cochran 1989).
Percent predation on egg groups and the percent of
total eggs consumed was analyzed using a doubly-
repeated measures analysis of variance (ANOVA) (re-
peated over date and time within a date) to determine
signiÞcance of main effects and all possible interac-
tions of the crop, date and time treatments (SAS In-
stitute 1985). Estimates of 24-h egg predation rates
were determined by subtracting the 24-h survival rate
of eggs from one. The estimated 24-h survival rate for
eggs was calculated by multiplying the mean propor-
tion of eggs surviving in each plot in each crop for all
3-h periods on each sample date. All percentages were
transformed by arcsine [square root (⫻/100)] before
analysis.
Results and Discussion
Identification of Predators of H. zea Eggs. A total of
406 predation events was observed during this study.
In 1993, 104 and 107 observations were made in soy-
bean and corn, respectively (Table 1). In 1994, 74 and
121 observations were made in soybean and corn,
respectively. Although there was overlap among the
taxa feeding on H. zea eggs in soybean and corn, the
frequency of observed predation for many taxa dif-
fered considerably between these two crops.
Nabis spp., predominantly Nabis roseipennis Reuter
but including smaller numbers of Nabis americoferus
Caryon and Nabis rufusculus Reuter (all Hemiptera:
Nabidae), were the most frequent predators in soy-
April 2002 PFANNENSTIEL AND YEARGAN: H. zea EGG PREDATION
bean, responsible for 51.0 and 50.0%, respectively, of
the predation events in 1993 and 1994 (Table 1). N.
roseipennis was consistently the most abundant nabid
in soybean in this area (Braman and Yeargan 1990,
Pfannenstiel and Yeargan 1998). The next most com-
monly observed predator in soybean in 1993 was Geo-
coris punctipes (Say) (Hemiptera: Lygaeidae), which
was responsible for 17.3% of observed feeding events;
however, predation by this species was rare in 1994.
The Phalangiidae (Arachnida: Opiliones) were the
third most frequently observed predators in soybean
in 1993, and second most frequently observed in 1994
with 13.4 and 17.6%, respectively, of the feeding
events. No other predators contributed ⬎10% of the
predation events in either 1993 or 1994 in soybean.
Previous studies also have shown that nabids are
often dominant predators in soybean. Using visual
observations, Godfrey et al. (1989) found nabids to be
the most common predator of small larvae of Antic-
arsia gemmatalis Hübner (Lepidoptera: Noctuidae) in
Florida soybean during 1980 and 1981. Several studies
have used autoradiography to determine the predators
of lepidopteran eggs in soybean. Buschman et al.
(1977), found that Nabis spp. made up 45.5% of the
labeled predators recovered after feeding on eggs of A.
gemmatalis in soybean. McCarty et al. (1980) reported
that N. roseipennis was the most frequently marked
predator of H. zea eggs and small larvae in soybean,
making up about half of the labeled predators col-
lected, with 17Ð30% of the total N. roseipennis col-
lected containing 32P. G. punctipes also were recorded
as predators of eggs by McCarty et al. (1980) and
Godfrey et al. (1989), but they were not observed by
Buschman et al. (1977). The Phalangiidae are not
known as important predators of lepidopteran eggs in
most agricultural systems although they have been
observed feeding on Leptinotarsa decemlineata Say
(Coleoptera: Chrysomelidae) eggs (Hazzard and
Ferro 1991).
In corn, the predator most frequently observed
feeding on H. zea eggs was C. maculata, which was
responsible for 43.9 and 46.3% of the observed preda-
tion events in 1993 and 1994, respectively (Table 1).
C. maculata is an important predator in corn, partic-
ularly of O. nubilalis eggs (Conrad 1959; Andow 1990,
1992). The second most commonly observed predator
for the two years was Orius insidiosus Say (Hemiptera:
Anthocoridae), which made up 10.3 and 15.4% of the
observed predation in 1993 and 1994, respectively.
Like C. maculata, O. insidiosus is an important pred-
ator of lepidopteran eggs in corn (Barber 1936, Dicke
and Jarvis 1962, Reid 1991, Coll and Bottrell 1992).
Cottrell and Yeargan (1998a, 1998b) also observed C.
maculata and O. insidiosus to be the dominant pred-
ators of H. zea eggs in sweet corn in Kentucky. Nabids
accounted for 12.1 and 8.9% of the observed predation
events in 1993 and 1994, but unlike C. maculata and O.
insidiosus they are not a numerically abundant pred-
ator in corn (Pfannenstiel and Yeargan 1998). It is
possible that these species colonized corn plots be-
cause of their proximity to nearby soybean plots (3.1
m distant); however, in previous studies the proximity
235
of soybean to corn did not result in higher nabid
densities (Pfannenstiel and Yeargan 1998). Lygus line-
olaris (Palisot de Beauvois) (Hemiptera: Miridae)
contributed 9.9% of the observed feeding events in
1994, and was the third most common arthropod ob-
served feeding on H. zea eggs that year. Although L.
lineolaris generally is known as an herbivore, it also
will readily feed on eggs and larvae of Heliothis vire-
scens (F.) (Lepidoptera: Noctuidae) (Cleveland
1987) and other soft-bodied arthropods (Lindquist
and Sorenson 1970, Wheeler 1976).
These observations on the predator complex feed-
ing on lepidopteran eggs indicate which predator taxa
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are important mortality agents of H. zea eggs. This
study also revealed several arthropod taxa not previ-
ously reported as important mortality agents, such as
the Phalangiidae and Clubiona abbotii L. Koch (Ara-
neae: Clubionidae) in soybean and Nabis spp. in corn.
However, this sampling technique may introduce a
bias to the proportion of egg mortality that can be
credited to each predator. In particular, predators that
take longer to feed are more likely to be observed in
the act of feeding than predators that consume all of
the eggs quickly. Therefore, smaller, slower-feeding
predators such as mites and O. insidiosus may be less
important than the proportion of observed feeding
events suggests, whereas larger predators that feed
quickly may be more important (R.S.P., unpublished
data). It is likely that C. maculata is responsible for a
larger portion of the H. zea egg mortality in corn than
visual observations indicated. C. maculata adults were
observed to eat all 10 eggs quickly (e.g., in 10 Ð20 min).
On 1 August 1994, supplementary observations of eggs
placed in corn were made about midway between
regular observations. Numerous cases of C. maculata
feeding were observed; in all cases the eggs at those
stations were consumed and the predator was gone
before the next observation period. Individual mites
have been observed feeding on eggs at a single site
over two observation periods (⬎3 h) (R.S.P., unpub-
lished data). The probability of observing a predator
such as C. maculata (adult) that might eat 10 eggs in
about 15 min (or less) would be ⬇8% (15 min/3 h ⫽
1/12 or 8.3%). The probability of observing a mite that
might take 3 h to eat 1Ð3 eggs would be near 100%.
Therefore, in this extreme case, we would get a good
estimate of the number of mites feeding on eggs in any
3-h period, but might only observe ⬇8% of the C.
maculata feeding events. This is just one possible ex-
ample and further studies are planned to examine the
relationship between feeding rate and likelihood of
observing a predator feeding in the Þeld. Also, this
study only examined the predators attacking H. zea
eggs at one location on each crop. It is possible, that
both the predators observed and the predation pres-
sure would change with location on the plant.
Diel Patterns of Predator Activity. The predators
observed feeding on the H. zea eggs in both corn and
soybean varied with the time of day (Figs. 1 and 2); all
predators for which the number of observations was
sufÞcient for analysis exhibited a signiÞcant deviation
from a random distribution (Table 2). Changes in
236 ENVIRONMENTAL ENTOMOLOGY Vol. 31, no. 2

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Fig. 1. Temporal distribution of observed predation events on H. zea eggs in soybean and corn, 1993. See Table 1 for list,
including “Minor Species.”
April 2002 PFANNENSTIEL AND YEARGAN: H. zea EGG PREDATION 237

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Fig. 2. Temporal distribution of observed predation events on H. zea eggs in soybean and corn, 1994. See Table 1 for list,
including “Minor Species.”

frequency of observed predation probably reßect
temporal changes in searching activity. The nabids
tended to be nocturnal, with 86.8 and 84.8% of the
observed feeding events in 1993 and 1994, respec-
tively, occurring between dusk and dawn. Observa-
tions of egg predation by nabid nymphs peaked at
2400, but were common from 2100 to 0300; nabid
adults were observed most frequently at 0300 and 0600
hours (Fig. 3). G. punctipes was diurnally active and
was observed only during the 1200, 1500, and 1800
hour observation periods (Fig. 1). Hutchison and Pitre
(1983) were able to collect signiÞcantly larger num-
bers of G. punctipes on cotton plants by sweepnet in
the afternoon. G. punctipes may be most active on
238 ENVIRONMENTAL ENTOMOLOGY Vol. 31, no. 2

Table 2. Diel activity periods of the common predators in Table 3. Repeated measures ANOVA procedure to compare
soybean and corn effects of crop, date, and time of sampling on egg predation in
soybean and corn, 1994
Frequency
Taxa Year observed ␹2 P Egg groups
Eggs consumed
Day Night Effect df attacked
F P F P
Nabis spp. 1993 9 57 34.9 ⬍0.001
1994 9 39 18.8 ⬍0.001 Crop 1 22.9 0.0030 21.6 0.0035
G. punctipes 1993 24 0 24.0 ⬍0.001 Date 3 16.6 ⬍0.0001 13.8 ⬍0.0001
C. maculata 1993 37 11 14.1 ⬍0.001 Crop ⫻ Date 3 1.4 0.2660 1.8 0.1760
1994 47 17 14.1 ⬍0.001 Error 18
O. insidiosus 1993 13 1 10.3 ⬍0.001 Time 7 7.3 ⬍0.0001 7.6 ⬍0.0001
1994 17 4 8.0 ⬍0.005 Crop ⫻ Time 7 6.9 ⬍0.0001 7.7 ⬍0.0001
C. abbotii 1993 0 14 14.0 ⬍0.001 Error 42

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Phalangiidae 1993 0 16 16.0 ⬍0.001 Date ⫻ Time 21 2.7 0.0004 2.6 0.0006
1994 0 13 13.0 ⬍0.001 Crop ⫻ Date ⫻ Time 21 0.9 0.5874 1.1 0.3756
Error 126

plants in the afternoon or may prefer the lower sec-

tions of the plant or the ground at other times. C.
maculata was most frequently observed during day-
light hours (77.1 and 73.4% in 1993 and 1994, respec-
tively), although feeding by larvae until midnight was
not uncommon, especially on warm nights (Figs. 1 and
2). Cottrell and Yeargan (1998a, 1998b) observed that
C. maculata adults were diurnally active, whereas lar-
vae remained active throughout the night as well. In
this study, feeding by all stages of C. maculata de-
creased during the 0300 and 0600 hour sampling pe-
riods. Another predator, O. insidiosus, was observed
during the afternoon with 94.1 and 85.7% of predation
events observed in daylight in 1993 and 1994, respec-
tively. Most of the other predators in both crops were
nocturnal. The Phalangiidae, C. abbotii, elaterids,
carabids, L. lineolaris, and others, were observed pri-
marily after dark (2100, 2400 and 0300 hours samples),
but with predation usually declining to a low just
before sunrise (0600 hours) in corn, possibly corre-
lating to cooling temperatures and the formation of a
heavy dew (R.S.P., unpublished data). Predation in
soybean did not decline until 0900 hours because of
the continued activity of nabids during the cool pre-
dawn hours.
Fig. 3. Diel observations of Nabis sp. adults and nymphs
feeding on H. zea eggs in soybean and corn. Combined
observations from 1993 and 1994.
The composition of the predator complex observed
feeding on H. zea eggs varied depending on the time
of day. To accurately characterize the predators at-
tacking particular prey, it is important to investigate
predation during nighttime as well as during daytime
hours. Buschman et al. (1977), using both diurnal
visual observations and radioactive labeling studies,
discovered very different complexes using each sam-
pling method. Diurnal observations revealed earwigs
and ants to be the dominant predators and conversely
the radio-labeling studies (which would include noc-
turnal predation) showed the nabids and chrysopid
larvae to be the most important predators. Studies
using primarily diurnal visual observations (e.g., Whit-
comb 1967, Godfrey et al. 1989) probably did not
identify a signiÞcant proportion of the important pred-
ators due to inadequate observation of nocturnal pre-
dation events.
Impact of Predators on H. zea Eggs. The predation
events observed accounted for only a portion of the
overall predation on eggs. Levels of predation varied
with the crop, date, and the time of sampling (Table
3; Fig. 4). Overall predation varied temporally in soy-
bean and corn. In corn, peak predation typically oc-
curred from 0900 to 1200 hours, then declined some-
what before increasing to a second minor peak at 2100
or 2400 hours (Fig. 4). The only sampling period for
which predation was low throughout the season in
corn was from 0300 to 0600 hours. The pattern in
soybean was different, with peak predation occurring
at night between 2100 and 0300 hours. During the
middle of the season there was also a period of rela-
tively higher predation during the day at 1200 or 1500
hours (18 Ð19 July and 1Ð2 August, respectively). Pre-
dation in soybean was lowest throughout the season
during the 0600 Ð 0900 hours period.
Predation increased through the season on both
soybean and corn in 1994, with mean 3-h predation
rates peaking on 1Ð2 August, then declining somewhat
by 9 Ð10 August (Fig. 5). Estimated 24-h rates of pre-
dation on egg groups ranged from 24.2 to 81.7% in
soybean and 53.4 to 97.3% in corn (Fig. 6). Predation
was higher in corn than in soybean on three of four
dates in 1994. Studies of egg predation have yielded a
wide range of estimated predation rates. Anderson
April 2002 PFANNENSTIEL AND YEARGAN: H. zea EGG PREDATION
Fig. 4. Diel variation in total predation of H. zea eggs in
soybean and corn on four sampling dates in 1994. Data are
presented as means ⫾ SEM
and Yeargan (1998) observed 24-h predation rates on
H. zea eggs in soybean from 50 to 63% in July 1994 and
60 to 80% in July and August 1995, although they did
see a decline in predation to ⬇30% in August 1994 and
50 to 60% in 1995. Buschman et al. (1977) reported
lower average predation rates of ⬇26% in Florida
soybean. In corn, Cottrell and Yeargan (1998b) ob-
served predation on H. zea to increase through the
season in 1996 (from ⬇30 to 60% mortality/24 h) but
not in 1995 (mortality near 60%/24 h). Andow (1992)
Fig. 5. Predation of H. zea eggs in soybean and corn on
four dates in 1994
239
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Fig. 6. Estimated 24-h predation rates on H. zea eggs in
soybean and corn in 1994. Total 24-h predation was estimated
by subtracting the proportion of eggs estimated to survive
24 h from 1. The estimated proportion of eggs surviving each
24-h period was calculated as the product of the mean pro-
portion surviving within each crop in each 3-h sample period
calculated from all 3-h sample periods on each date.
observed low levels of predation of O. nubilalis egg
masses in Minnesota. In a study of predation on H. zea
eggs in Texas cotton, Nuessley and Sterling (1994)
demonstrated average 24-h predation rates ⬎80%.
Clearly, predation on lepidopteran eggs can vary
widely among crops and locations, but in many loca-
tions egg predators do cause signiÞcant mortality.
On one date in 1994, egg predation was not higher
in corn than in soybean (Figs. 5 and 6). The change in
the pattern of predation may have been a result of the
stage of the corn. From 12 to 19 July, the corn was
tasseling, and pollen was abundant on all parts of the
plants. During the 18 Ð19 July sample, C. maculata
made up only 18.2% of the predators observed feeding
on H. zea eggs, the only sample where C. maculata was
responsible for ⬍48% of the predation events in corn.
Additionally, on 11Ð12 July, nine of the 14 C. maculata
observed feeding were in the single plot where the
corn had not begun to tassel and shed pollen. The
average number of C. maculata observed feeding in
the three plots where the corn had begun to tassel was
1.7. Corn pollen is a preferred food of C. maculata
(Smith 1965), the dominant predator in corn. During
the short time pollen was available, a large proportion
of the observed feeding events by C. maculata were on
corn pollen (R.S.P., unpublished data). Cottrell and
Yeargan (1998b) demonstrated that an abundance of
corn pollen in sweet corn could divert C. maculata
from carnivory and reduce overall predation of H. zea
eggs.
Numerous arthropods feed on lepidopteran eggs in
soybean and corn. This complex causes signiÞcant
mortality, which probably is important in reducing
populations of lepidopteran pests in both crops. Al-
though many arthropod species contributed to the
overall high egg mortality rate, only a few were re-
sponsible for most of the observed mortality. Daylight
observations might have correctly identiÞed the dom-
inant predator(s) in corn (C. maculata and O. insid-
240 ENVIRONMENTAL ENTOMOLOGY
iosus); however, they would not have correctly iden-
tiÞed the two dominant predators in soybean (Nabis
spp. and the phalangiids). Consideration of nocturnal
predation might change our perception of the domi-
nant predators and their impact on particular pests in
many crops. The dominant predators identiÞed in this
study, particularly Nabis spp. in soybean and C. macu-
lata in corn, should be the focus of further studies to
characterize their ecology and improve our under-
standing of the factors contributing to the mortality of
lepidopteran pests in these two crops.
Acknowledgments
We thank R. Rizk for Þeld assistance. R. J. Barney, J. M.
Baskin, P. L. Cornelius, K. F. Haynes, R. López, B. C. Pass,
D. A. Potter, A. Sih (all University of Kentucky), D. Horton,
and T. Unruh (USDA-ARS, Yakima) provided reviews of
early drafts of the article. This is publication number 00 Ð
08 Ð57 of the University of Kentucky Experiment Station.
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Received for publication 6 December 2000; accepted 9 No-
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