1. home and garden
2. pest control

BIOLOGICAL AND MICROBIAL CONTROL
Trichogramma Releases in North Carolina Cotton: Why Releases Fail
to Suppress Heliothine Pests
CHARLES P.-C. SUH,1 DAVID B. ORR,
AND
JOHN W. VAN DUYN
Department of Entomology, North Carolina State University, Raleigh, NC 27695Ð7613
J. Econ. Entomol. 93(4): 1137Ð1145 (2000)
ABSTRACT Field studies were conducted in 1996 and 1997 to determine the fate of naturally
oviposited F3 heliothine eggs in cotton plots treated with augmentative releases of Trichogramma
exiguum Pinto & Platner and nontreated plots. Four cohorts of newly oviposited eggs (⬍24 h old)
were followed in 1996 and two cohorts in 1997. In 1996, mean ⫾ SD percent parasitism, estimated
by in-Þeld studies following the fate of naturally oviposited eggs, ranged from 7 ⫾ 7 to 61 ⫾ 8% in
T. exiguum release plots and 0 ⫾ 0 to 35 ⫾ 13% in control plots. The mean ⫾ SD percent of eggs
hatched in T. exiguum release plots ranged from 1 ⫾ 2 to 11 ⫾ 4% and 7 ⫾ 4 to 28 ⫾ 10% in control
plots. In 1997, mean ⫾ SD percent egg parasitism ranged from 27 ⫾ 4 to 40 ⫾ 3% in T. exiguum release
plots and 15 ⫾ 18 to 25 ⫾ 8% in control plots. The mean ⫾ SD percent of eggs hatched in T. exiguum
release plots ranged from 7 ⫾ 3 to 12 ⫾ 2% and 18 ⫾ 6 to 28 ⫾ 8% in control plots. Despite increased
parasitism and reduced egg hatch in T. exiguum release plots, overall, there was no signiÞcant
difference in larval density (all instars combined) between T. exiguum release and control plots.
Combined analysis of the heliothine larval populations and egg fate data revealed that the additional
egg mortality produced by released T. exiguum was offset by lower larval mortality in release plots.
Because of the occurrence of compensatory mortality, the egg stage of heliothines is not an
appropriate target for biological control using Trichogramma wasp releases.
KEY WORDS Trichogramma exiguum, heliothines, egg fate, compensatory mortality
NATURAL FIELD POPULATIONS of insect predators and
parasitoids alone, if undisturbed, can substantially reduce heliothine pest populations in cotton. A large
proportion of heliothine eggs are consumed by predators, parasitized, or removed by rain and wind before
hatching (Fletcher and Thomas 1943, Fye 1979, Mabbett and Nachapong 1983, Nuessly 1986). Fletcher and
Thomas (1943) observed that 15.3Ð32.9% of tagged
Heliothis armigera Hu¨ bner eggs on cotton were destroyed by predators. Wene and Sheets (1962) found
that natural populations of predators helped maintain
bollworm populations below destructive levels in cotton. Based on data reported by some of these authors
and others (e.g., Quaintance and Brues 1905, Bell and
Whitcomb 1964), Ridgway and Lingren (1972) estimated that 50 Ð90% of heliothine eggs and larvae in
cotton were consumed or parasitized by natural populations of insect predators and parasitoids. Additionally, abiotic factors (e.g., rain and leaf abrasion resulting from wind) can substantially contribute to
heliothine mortality, particularly during the egg stage
(e.g., Fletcher and Thomas 1943, Fye 1979, Nuessly
1986).
Parasitoids also contribute to heliothine mortality
during the egg stage. Johnson (1985) reported that as
much as 59% of bollworm eggs in cotton were parasitized by natural populations of Trichogramma wasps.
1
Current address: USDA- ARS at Southern Plains Agriculture Research Center, College Station, TX 77845.
Segers et al. (1984) reported natural egg parasitism
levels ranging from 0 to 92% in cotton during peak
bloom and Þrst open boll stages. Several studies (e.g.,
Stinner et al. 1974; Jones et al. 1977, 1979; King et al.
1985; Lopez and Morrison 1985; Suh et al. 1998) demonstrated that bollworm egg parasitism in cotton could
be substantially increased with augmentative releases
of Trichogramma wasps. However, despite increases in
parasitism levels of heliothine eggs, several authors
(Jones et al. 1979, Luttrell et al. 1980, King et al. 1985,
Suh et al. 1998) found heliothine larval populations
were not adequately suppressed with Trichogramma
releases.
The variability of these results led several authors
(e.g., Knipling and McGuire 1968, King et al. 1985) to
suggest that Trichogramma spp. were not suitable candidates for biological control in cotton. However, the
underlying reasons for the variability in results with
Trichogramma have not been examined.
Initially, we speculated that poor Trichogramma
quality, species selection, variable experimental designs, and disadvantageous experimental procedures
were responsible for the variable, and for the most
part, poor parasitism levels reported in prior studies.
However, results from a previous study with these
variables minimized (see Suh et al. 2000) suggested
that some other factor(s) was responsible for the lack
of larval and damage suppression achieved in cotton
with augmentative releases of Trichogramma.
0022-0493/00/1137Ð1145$02.00/0 䉷 2000 Entomological Society of America
1138
JOURNAL OF ECONOMIC ENTOMOLOGY
The objectives of this study were to determine the
fate of naturally oviposited heliothine eggs and the
structure of larval populations in cotton Þelds exposed
to natural and augmented populations of Trichogramma wasps. Analysis of these data could then be
used to fulÞll an overall goal of developing an understanding of why augmented Trichogramma populations in cotton have not consistently reduced heliothine larval populations and damage to an acceptable
level.
Materials and Methods
Experimental Design. The experiment was designed as a complete block with systematic placement
of treatments. There was one treatment and one control plot located at three Þeld sites with sites serving
as blocks and replications. In 1996, two Þeld sites were
located on the Hudson Farm and the third site on the
Sid Hassel Farm. In 1997, one Þeld site was located on
the Hudson Farm, another on the Tidewater Research
Station, and the third on the Sid Hassel Farm. All Þeld
sites were located near Plymouth, NC. The treatment
was T. exiguum Pinto & Platner release. Control plots
were not treated with T. exiguum or foliar heliothine
insecticides. Within each Þeld site, Trichogramma release plots were located downwind (based on prevailing wind direction for that area) ⬇300 m from control
plots to reduce possibility of parasitoid dispersal into
control plots. Release and control plots were each
⬇0.4 ha in size, and separated by Þeld corn at each
Þeld site.
Plot Management. (see Suh et al. 2000).
Plot Characterization. A leaf area index value
(square meter of leaf surface area per square meter of
soil surface area) and mean plant height were determined for each T. exiguum release and control plot
near the beginning and end of the month ßight since
plant size has been shown to affect Trichogramma
parasitism (Need and Burbutis 1979).
Trichogramma Source. The T. exiguum used for the
1996 and 1997 Þeld releases were initiated from parasitized H. zea and H. virescens eggs collected from
cotton Þelds located near Plymouth, NC. Parasitoids
identiÞed as T. exiguum by John Pinto (University of
California at Riverside) were shipped to BIOTOP for
mass production and formulated for Þeld release (see
Suh et al. 2000).
Trichogramma exiguum Release. Nine releases averaging 108,357 females per hectare per release were
made in each release plot during 1996 and six releases
each containing two cohorts of T. exiguum averaging
193,366 females per hectare per cohort per release
were made in 1997 (see Suh et al. 2000).
Quality Control. To ensure that high quality parasitoids were used throughout the experiment, Þeld and
laboratory quality control samples were taken for each
released cohort (see Suh et al. 2000). Measured parameters included percentage of emergence under
laboratory and Þeld conditions, sex ratio, percentage
of female brachyptery, and female longevity under
laboratory conditions.
Vol. 93, no. 4
Heliothine Egg Density. Heliothine (H. zea ⫹ H.
virescens) egg density was measured at 3- to 4-d intervals in each T. exiguum release and control plot
from 17 July through 30 August in 1996, and 29 July
through 2 September in 1997. Egg density in each plot
was determined by counting the number of eggs occurring on 100 terminals (top 15 cm of the plant)
randomly selected throughout the plot.
Heliothine Egg Fate. Within each T. exiguum release and control plot, heliothine eggs were marked at
25 sites evenly distributed (spaced ⬇8 m apart) within
the center portion of the plot. At each site, heliothine
eggs (⬍24 h old; creamy white appearance) located in
the top 30% of the plant were marked by tying a white
paper tag (3.5 by 5 cm) around the base of the structure supporting the egg. The exact location of the egg
was marked with a descriptive picture on the tag.
Tagged eggs were checked with a hand lens (10⫻
magniÞcation) 2, 4, 7, 9, 11, and 13 d after discovery
until a Þnal fate had been determined for each egg. In
doubtful cases, eggs were examined in the Þeld under
a compound microscope. Final fate classiÞcations
were as follows: hatched, preyed upon, dislodged,
nonviable, and parasitized. Based on prior laboratory
and Þeld observations, hatched eggs were distinguished from preyed upon eggs by the amount and
shape of the remaining egg chorion. Eggs with remaining chorions that appeared crescent-shaped and
mostly intact were classiÞed as hatched. Eggs with
only a very small circular remnant of the chorion
remaining, usually where the egg was attached to the
plant structure, or chorions that were completely intact but appeared conical in shape (produced by sucking insects) were classiÞed as preyed upon. Also, chorions of hatched eggs appeared white and translucent,
whereas preyed upon eggs had chorions that appeared
discolored (yellowish to tan in color). Eggs classiÞed
as dislodged may have been carried off by predators or
may have been removed from plants by abiotic factors
(e.g., rain, action of wind). In any case, there was no
trace of the egg chorion. Eggs classiÞed as nonviable
appeared yellowish or tannish in color, and did not
produce viable larvae nor turn black to indicate parasitism. Eggs that took on a black shiny appearance
were classiÞed as parasitized, and each was followed
until a Þnal fate was determined. ClassiÞcations for
parasitized eggs were as follows: parasitized and
preyed upon, parasitized and washed off, and parasitized with adult parasitoid emergence.
In 1996, the dates and number of eggs tagged in each
plot were 29 July, n ⫽ 30; 5 August, n ⫽ 75; 12 August,
n ⫽ 75; and 19 August, n ⫽ 30. In 1997, the dates and
number of eggs tagged in each plot were 11 August,
n ⫽ 25 and 18 August, n ⫽ 75. On each of these dates,
cohorts of eggs were found and tagged between 0630
and 1200 hours in all plots.
Larval Infestation. Heliothine larval infestation was
assessed in each T. exiguum release and control plot on
multiple dates in 1996 and 1997. Samples were taken
from 25 sites evenly distributed throughout the central
portion of each plot. For each plot, the sampling dates
and structures sampled in 1996 were 5 August, 50
August 2000
SUH ET AL.: Trichogramma RELEASES FAIL IN COTTON
1139
Table 1. Fate of F3 heliothine (predominantly H. zea) eggs naturally oviposited in T. exiguum-treated and control cotton plots.
Plymouth, NC, 1996
Datea
Treatment
29 July
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
5 Aug.
12 Aug.
19 Aug.
Overall
% of heliothine eggsb
Hatched
Preyed upon
Dislodgedc
Parasitized
1.3 ⫾ 2.3a
7.0 ⫾ 0.4b
3.6 ⫾ 0.8a
27.8 ⫾ 9.5b
5.0 ⫾ 2.1a
8.2 ⫾ 2.6a
10.4 ⫾ 3.6a
7.0 ⫾ 3.7a
5.1 ⫾ 3.9a
12.5 ⫾ 10.3b
17.8 ⫾ 5.1a
34.4 ⫾ 18.7a
15.6 ⫾ 10.7a
32.7 ⫾ 4.5a
15.7 ⫾ 3.8a
15.1 ⫾ 3.9a
10.2 ⫾ 5.6a
13.8 ⫾ 6.0a
14.8 ⫾ 6.5a
24.0 ⫾ 13.3b
73.8 ⫾ 6.3a
58.6 ⫾ 19.1a
17.5 ⫾ 5.2a
18.8 ⫾ 5.5a
53.6 ⫾ 5.8a
57.8 ⫾ 2.2a
32.0 ⫾ 9.6a
42.6 ⫾ 5.8a
44.2 ⫾ 23.1a
44.5 ⫾ 19.0a
7.1 ⫾ 6.7a
0.0 ⫾ 0.0a
60.5 ⫾ 8.1b
19.3 ⫾ 8.8a
25.7 ⫾ 3.7a
18.8 ⫾ 3.7a
47.4 ⫾ 12.2a
35.4 ⫾ 13.3a
35.2 ⫾ 22.5b
18.4 ⫾ 14.8a
For each date, values within a column followed by different letters are signiÞcantly different (ANOVA, P ⫽ 0.05).
Represents date cohorts of eggs were initially marked.
Less than 2% of eggs were classiÞed as nonviable, therefore this classiÞcation was not included in table.
c
Dislodged indicates that egg was removed from plant by predator, rain, or action of wind; no trace of egg chorion.
a
b
terminals and 50 terminal squares; 12 August, 100 small
squares and 100 large squares; 19 August 100 large
squares, 100 small bolls, and 100 large bolls; and 28
August, 100 large squares, 100 small bolls, and 100 large
bolls. In 1997, sampling dates and structures were 11
August, 100 terminal squares (match-head) and 100
small squares; 18 August, 100 small squares and 100
small bolls; 25 August 100 small and 100 large bolls; 2
September, 100 small and 100 large bolls; 9 September,
100 small and 100 large bolls.
Data Analysis. Plot means were calculated for each
egg fate category and larval densities. Analysis of variance (ANOVA) was carried out on plot means to
compare treatments (Abacus Concepts 1991). Analysis of the fate and larvae data indicated that there was
a substantial date effect and date by treatment interaction (PROC GENMOD, SAS Institute 1996); therefore, a repeated measures analysis was not performed.
Instead, fate and larvae data were presented for each
date. A square-root transformation was performed on
larval counts before analysis. Data collected from determination of the fate of parasitized eggs and egg
densities per hectare in T. exiguum release plots allowed estimation of Trichogramma recycling. The average daily egg density per 100 terminals between
initial oviposition and peak oviposition was estimated
by summing the number of eggs within this period and
dividing this number by the number of days from
initial to peak oviposition. This number was multiplied
by three to account for eggs laid on other parts of the
plant (Farrar and Bradley 1985) then divided by 100
to estimate density on a per plant basis. This number
was then multiplied by the estimated number of plants
per hectare (46,770 plants per hectare) to yield egg
density on a hectare basis. A larval mortality index,
calculated as [1 Ð (instar 5 larval density on day n ⫹
15) (neonate density on day n)⫺1] ⫻ 100, was determined for each plot. Because of the difÞculty in sampling for Þrst instars, neonate density was estimated
from egg density and fate data as the number of
hatched eggs per 100 plants. The relationship between
larval mortality index and neonate density (hatched
eggs) on 9 August (average of density on 5 and 12
August) was analyzed for the 1996 data using linear
regression (Abacus Concepts 1992). The 1997 data
were analyzed similarly using the densities of hatched
eggs on 18 August and numbers of Þfth instars on 2
September The dates on which neonate densities (estimated by egg hatch densities) were used to assess
compensatory mortality were selected because they
occurred at the peak egg laying period in each year
and Þeld site, providing some form of standardization
between Þelds and years. The dates on which Þfth
instars were sampled to assess compensatory mortality
were selected because development from the egg
stage to Þfth instars takes about 2 wk under conditions
typically found in North Carolina cotton.
Results
Plot Characterization, Trichogramma Quality Control, and Heliothine Egg Density. Plants in release and
control plots were similar in size (see Suh et al. 2000).
High quality T. exiguum were released throughout the
study in 1996 and 1997 (see Suh et al. 2000). Egg
densities within T. exiguum release and control plots
were similar during 1996 and 1997; however, there
were substantial differences between years in terms of
the timing, duration, and intensity of the F3 egg-laying
period (see Suh et al. 2000).
Heliothine Egg Fate. In 1996, for egg cohorts
marked on 29 July, only the percentage of eggs
hatched was signiÞcantly different (F ⫽ 17.63; df ⫽ 1,
4; P ⫽ 0.014) between T. exiguum release (1.3 ⫾ 2.3)
and control plots (7.0 ⫾ 0.4) (Table 1). The majority
of eggs were dislodged from plants or lost to predation.
For egg cohorts marked on 5 August, the percentage
of eggs lost to parasitism was signiÞcantly higher (F ⫽
35.82; df ⫽ 1, 4; P ⫽ 0.004) in T. exiguum release plots
(60.5 ⫾ 8.1%) than in control plots (19.3 ⫾ 8.8%) and
the percentage of hatched eggs was signiÞcantly lower
(F ⫽ 19.31; df ⫽ 1, 4; P ⫽ 0.012) in T. exiguum release
plots (3.6 ⫾ 0.8%) than in control plots (27.8 ⫾ 9.5%).
For egg cohorts marked on 12 August, a majority of
eggs were dislodged from plants in T. exiguum release
(53.6 ⫾ 5.8%) and control plots (57.8 ⫾ 2.2%). For egg
1140
JOURNAL OF ECONOMIC ENTOMOLOGY
Table 2. Fate of parasitized F3 heliothine eggs naturally oviposited in T. exiguum-treated and control cotton plots. Plymouth,
NC, 1996
Datea
Treatment
29 July
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
5 Aug.
12 Aug.
19 Aug.
Overall
% of parasitized heliothine eggsb
Preyed upon
Dislodgedc
Recycledd
0.0 ⫾ 0.0
NA
14.5 ⫾ 4.5a
7.4 ⫾ 6.5a
6.7 ⫾ 5.8a
9.9 ⫾ 4.1a
2.0 ⫾ 3.4a
4.8 ⫾ 8.3a
6.4 ⫾ 6.9a
8.2 ⫾ 7.2a
75.0 ⫾ 35.4
NA
69.4 ⫾ 15.0a
69.9 ⫾ 4.7a
64.3 ⫾ 20.7a
42.4 ⫾ 13.1a
53.3 ⫾ 8.0a
70.9 ⫾ 16.3a
65.8 ⫾ 17.5a
65.7 ⫾ 19.0a
25.0 ⫾ 35.4
NA
15.4 ⫾ 10.2a
17.9 ⫾ 4.9a
29.0 ⫾ 15.4a
43.2 ⫾ 18.2a
37.8 ⫾ 8.1a
14.8 ⫾ 17.0a
27.8 ⫾ 17.5a
26.1 ⫾ 18.6a
For each date, values within a column followed by different letters
are signiÞcantly different (ANOVA, P ⫽ 0.05). NA, no parasitized
eggs found on this date in control plots.
a
Represents date cohorts of eggs were initially marked.
b
Percentages based on eggs that were classiÞed as parasitized in
Table 1.
c
Dislodged indicates that parasitized egg was removed from plant by
predator, rain, or action of wind; no trace of egg chorion.
d
Recycled indicates that adult Trichogramma successfully emerged
from egg.
cohorts marked on 19 August, almost half of the eggs
in release plots were lost to parasitism (47.4 ⫾ 12.2%),
where as almost half of the eggs in control plots were
dislodged from plants (42.6 ⫾ 5.8%).
Overall (all dates combined) in 1996, egg hatch was
signiÞcantly lower in T. exiguum release plots than in
control plots (F ⫽ 5.40; df ⫽ 1, 22; P ⫽ 0.030), with an
overall egg hatch reduction of 59% (Table 1). Almost
half of the eggs were dislodged from plants in both T.
exiguum release (44.2 ⫾ 23.1%) and control plots
(44.5 ⫾ 19.0%). Overall, the percentage of eggs preyed
upon in T. exiguum release plots (14.8 ⫾ 6.5%) was
signiÞcantly lower (F ⫽ 4.60; df ⫽ 1, 22; P ⫽ 0.043) than
in control plots (24.0 ⫾ 13.3%) The percentage of eggs
lost to parasitism was signiÞcantly higher in T. exiguum- treated plots than in control plots (F ⫽ 4.67;
df ⫽ 1, 22; P ⫽ 0.042). Approximately 27% of eggs
classiÞed as parasitized in T. exiguum release and control plots produced viable adult Trichogramma (Table
2). The remainder were either dislodged or preyed
upon.
Vol. 93, no. 4
In 1997, for eggs marked on 11 August, only the
percentage of eggs hatched was signiÞcantly different
(F ⫽ 21.25; df ⫽ 1, 4; P ⫽ 0.010) between T. exiguum
release (6.7 ⫾ 2.8%) and control plots (28.3 ⫾ 7.6%)
(Table 3). The majority of eggs in release plots were
parasitized (40.0 ⫾ 3.0%), whereas the majority of
eggs in control plots were dislodged (38.3 ⫾ 17.6%)
from plants before hatching. For the cohort of eggs
marked on 18 August, there were no signiÞcant differences between T. exiguum release and control plots
for all egg classiÞcations.
Overall (both dates combined) in 1997, egg hatch
was signiÞcantly lower (F ⫽ 13.72; df ⫽ 1, 10; P ⫽
0.004) in T. exiguum release plots (9.5 ⫾ 3.7%) than in
control plots (23.2 ⫾ 8.2%) with an overall egg hatch
reduction of 59% in T. exiguum release plots (Table 3).
Nearly half of the eggs were dislodged from plants in
T. exiguum release (43.2 ⫾ 11.3%) and control plots
(43.7 ⫾ 15.0%). The percentage of eggs lost to parasitism was not signiÞcantly different between T. exiguum release and control plots (F ⫽ 4.48; df ⫽ 1, 10;
P ⫽ 0.060); however, the average percentage of eggs
lost to parasitism was substantially higher (68%) in T.
exiguum release plots. Approximately 48% of eggs classiÞed as parasitized in T. exiguum release and control
plots produced viable adult Trichogramma, whereas
the remainder were mostly dislodged (Table 4).
Larval Infestation. In 1996, larval densities on four
assessment dates were statistically analyzed (Table 5).
On 5 August there were no signiÞcant differences in
number of ÞrstÐsecond (F ⫽ 0.07; df ⫽ 1, 4; P ⫽ 0.809)
or thirdÐfourth instars (F ⫽ 1.00; df ⫽ 1, 4; P ⫽ 0.374)
between T. exiguum release and control plots. No Þfth
instars were found on this date so comparisons could
not be made. On 12 August there were no signiÞcant
differences in number of ÞrstÐsecond instars (F ⫽ 2.25;
df ⫽ 1, 4; P ⫽ 0.208) or thirdÐfourth instars (F ⫽ 1.50;
df ⫽ 1, 4; P ⫽ 0.288) between T. exiguum release and
control plots. No Þfth instars were found on this date
so comparisons could not be made. There was no
signiÞcant difference in number of larvae (all instars
combined) between T. exiguum release and control
plots (F ⫽ 3.71; df ⫽ 1, 4; P ⫽ 0.126). On 19 August
there were no signiÞcant differences in number of
ÞrstÐsecond (F ⫽ 1.37; df ⫽ 1, 4; P ⫽ 0.307), thirdÐ
Table 3. Fate of F3 heliothine (predominantly H. zea) eggs naturally oviposited in T. exiguum-treated and control cotton plots.
Plymouth, NC, 1997
Datea
Treatment
11 Aug.
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
18 Aug.
Overall
Percentage of heliothine eggsb
Hatched
Preyed upon
Dislodgedc
Parasitized
6.7 ⫾ 2.8a
28.3 ⫾ 7.6b
12.3 ⫾ 1.5a
18.0 ⫾ 5.6a
9.5 ⫾ 3.7a
23.2 ⫾ 8.2b
15.7 ⫾ 18.5a
16.7 ⫾ 7.6a
11.3 ⫾ 2.5a
7.7 ⫾ 5.1a
13.5 ⫾ 12.0a
12.2 ⫾ 7.6a
37.7 ⫾ 15.0a
38.3 ⫾ 17.6a
48.7 ⫾ 1.5a
49.0 ⫾ 13.1a
43.2 ⫾ 11.3a
43.7 ⫾ 15.0a
40.0 ⫾ 3.0a
15.0 ⫾ 18.0a
27.0 ⫾ 3.6a
25.0 ⫾ 7.8a
33.5 ⫾ 7.7a
20.0 ⫾ 13.6a
For each date, values within a column followed by different letters are signiÞcantly different (ANOVA, P ⫽ 0.05).
Represents date cohorts of eggs were initially marked.
Less than 2% of eggs were classiÞed as non-viable, therefore this classiÞcation was not included in table.
c
Dislodged indicates that egg was removed from plant by predator, rain, or action of wind; no trace of egg chorion.
a
b
August 2000
SUH ET AL.: Trichogramma RELEASES FAIL IN COTTON
Table 4. Fate of parasitized F3 heliothine eggs naturally oviposited in T. exiguum-treated and control cotton plots. Plymouth,
NC, 1997
Table 6. Mean ⴞ SD number of heliothine (H. zea ⴙ H.
virescens) larvae found on fruiting structures in T. exiguum-treated
and control plots. Plymouth, NC, 1997
Percentage of parasitized eggsb
Datea
Treatment
Preyed
upon
Dislodged
Recycled
11 Aug.
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
0.0 ⫾ 0.0a
7.0 ⫾ 9.9a
12.3 ⫾ 4.9a
11.0 ⫾ 2.6a
6.2 ⫾ 7.4a
9.4 ⫾ 5.7a
71.7 ⫾ 12.7a
68.0 ⫾ 25.5a
24.0 ⫾ 10.8a
23.0 ⫾ 11.8a
47.8 ⫾ 28.2a
41.0 ⫾ 29.0a
28.3 ⫾ 12.7a
25.0 ⫾ 35.4a
63.7 ⫾ 6.5a
66.0 ⫾ 9.5a
46.0 ⫾ 21.3a
49.6 ⫾ 29.4a
18 Aug.
Overall
c
d
For each date, values within a column followed by different letters
are signiÞcantly different (ANOVA, P ⫽ 0.05).
a
Represents date cohorts of eggs were initially marked.
b
Percentages based on eggs that were classiÞed as parasitized in
Table 3.
c
Dislodged indicates that parasitized egg was removed from plant
by predator, rain, or action of wind; no trace of egg chorion.
d
Recycled indicates that adult Trichogramma successfully emerged
from egg.
fourth (F ⫽ 5.10; df ⫽ 1, 4; P ⫽ 0.087), or Þfth instars
(F ⫽ 0.00; df ⫽ 1, 4; P ⫽ 0.973) between the T. exiguum
release and control plots. There was no signiÞcant
difference in the number of larvae when all instars
were combined between T. exiguum release and control plots (F ⫽ 4.88; df ⫽ 1, 4; P ⫽ 0.092). On 28 August
there were no signiÞcant differences in numbers of
ÞrstÐsecond (F ⫽ 0.01; df ⫽ 1, 4; P ⫽ 0.927), thirdÐ
fourth (F ⫽ 1.47; df ⫽ 1, 4; P ⫽ 0.293), and Þfth instars
(F ⫽ 0.18; df ⫽ 1, 4; P ⫽ 0.748), or all combined instars
(F ⫽ 2.19; df ⫽ 1, 4; P ⫽ 0.213) between T. exiguum
release and control plots.
In 1997, larval densities on the last four dates of
assessments were statistically analyzed (Table 6). On
18 August there were no signiÞcant differences in
numbers of ÞrstÐsecond (F ⫽ 0.39; df ⫽ 1, 4; P ⫽ 0.565)
or thirdÐfourth instars (F ⫽ 0.05; df ⫽ 1, 4; P ⫽ 0.828)
between T. exiguum release and control plots. Comparisons of Þfth instars could not be made because
none were found at this time. There was no signiÞcant
difference in the number of larvae when all instars
Table 5. Mean ⴞ SD number of heliothine (H. zea ⴙ H.
virescens) larvae found on fruiting structures in T. exiguum-treated
and control plots. Plymouth, NC, 1996
Date
Treatment
5 Aug.
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
12 Aug.
19 Aug.
28 Aug.
Number of heliothine
(H. zea ⫹ H. virescens) larvaea
Instars 1Ð2
Instars 3Ð 4
Instar 5
1.3 ⫾ 1.2a
2.0 ⫾ 2.0a
4.3 ⫾ 2.5a
7.7 ⫾ 3.1a
7.0 ⫾ 3.0a
10.0 ⫾ 3.5a
2.7 ⫾ 1.6a
3.3 ⫾ 4.9a
0.3 ⫾ 0.0a
0.3 ⫾ 0.6a
0.3 ⫾ 0.6a
3.7 ⫾ 4.7a
15.3 ⫾ 9.5a
28.7 ⫾ 2.3a
10.0 ⫾ 6.6a
17.7 ⫾ 8.5a
0.0 ⫾ 0.0
0.0 ⫾ 0.0
0.0 ⫾ 0.0
0.0 ⫾ 0.0
2.7 ⫾ 3.1a
2.7 ⫾ 2.5a
17.1 ⫾ 6.1a
17.1 ⫾ 10.5a
For each date, values within a column followed by different letters
are signiÞcantly different (ANOVA, P ⫽ 0.05); values transformed
(square root) prior to analysis.
a
Number of larvae present in a total of 100 squares, 100 small bolls
(⬇2 cm diameter) and 100 large bolls (⬇3 cm diameter) per plot.
1141
Date
Treatment
18 Aug.
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
T. exiguum
Control
25 Aug.
2 Sept.
9 Sept.
Number of bollworm
(H. zea ⫹ H. virescens) larvaea
Instars 1Ð2
Instars 3Ð 4
Instar 5
3.3 ⫾ 4.0a
4.3 ⫾ 2.3a
0.3 ⫾ 0.6a
1.0 ⫾ 1.0a
0.0 ⫾ 0.0
0.0 ⫾ 0.0
0.7 ⫾ 0.6b
0.0 ⫾ 0.0a
1.0 ⫾ 0.0a
2.0 ⫾ 2.0a
1.3 ⫾ 1.5a
7.7 ⫾ 5.7b
3.0 ⫾ 1.0a
7.0 ⫾ 7.0a
2.7 ⫾ 3.1a
10.0 ⫾ 6.6a
0.0 ⫾ 0.0
0.0 ⫾ 0.0
1.0 ⫾ 1.0a
1.0 ⫾ 0.0a
2.0 ⫾ 2.0a
3.0 ⫾ 2.0a
0.3 ⫾ 0.6a
1.7 ⫾ 1.5a
For each date, values within a column followed by different letters
are signiÞcantly different (ANOVA, P ⫽ 0.05); values transformed
(square root) prior to analysis.
a
Number of larvae found in fruiting structures; 18 August sample
consisted of 100 squares and 100 small bolls (⬇2 cm diameter) per
plot; remaining dates consisted of 100 small bolls and 100 large bolls
(⬇3 cm diameter) per plot.
were combined between T. exiguum release and control plots (F ⫽ 0.63; df ⫽ 1, 4; P ⫽ 0.471). On 25 August,
no signiÞcant differences in number of ÞrstÐsecond
(F ⫽ 0.77; df ⫽ 1, 4; P ⫽ 0.429), thirdÐfourth (F ⫽ 5.00;
df ⫽ 1, 4; P ⫽ 0.089), or Þfth instars (F ⫽ 0.22; df ⫽ 1,
4; P ⫽ 0.666) were detected between T. exiguum release and control plots. There was no signiÞcant difference in the number of larvae when all instars were
combined between T. exiguum release and control
plots (F ⫽ 4.58; df ⫽ 1, 4; P ⫽ 0.099). On 2 September,
no ÞrstÐsecond instars were found, so comparisons of
these instars could not be made. There were no signiÞcant differences in numbers of instars thirdÐfourth
(F ⫽ 0.88; df ⫽ 1, 4; P ⫽ 0.401), Þfth instars (F ⫽ 0.56;
df ⫽ 1, 4; P ⫽ 0.497), or all instars combined (F ⫽ 0.77;
df ⫽ 1, 4; P ⫽ 0.430) between T. exiguum release and
control plots. On 9 September there were no signiÞcant differences in numbers of ÞrstÐsecond (F ⫽ 4.00;
df ⫽ 1, 4; P ⫽ 0.116), thirdÐfourth (F ⫽ 3.49; df ⫽ 1,
4; P ⫽ 0.135), or Þve instars (F ⫽ 1.30; df ⫽ 1, 4; P ⫽
0.318) between T. exiguum release and control plots.
There was no signiÞcant difference in the number of
larvae when all instars were combined between T.
exiguum release and control plots (F ⫽ 3.63; df ⫽ 1, 4;
P ⫽ 0.130).
Combined analysis of the 1996 egg fate and larval
population data revealed a relationship (r2 ⫽ 0.69, P ⫽
0.041) between the larval mortality index and neonate
density (Fig. 1). As the neonate population increased,
the larval mortality index also increased. This relationship was not found in 1997 (r2 ⬍ 0.01, P ⫽ 0.993)
(Fig. 2).
Discussion
In past studies (e.g., Stinner et al. 1974, Jones et al.
1977, Luttrell et al. 1980, King et al. 1985) parasitism
levels were estimated from collections of tan-colored
eggs (⬇48 h old) held under laboratory conditions.
Unfortunately, estimates of percent parasitism based
on collection of eggs at a single point in time will often
1142
JOURNAL OF ECONOMIC ENTOMOLOGY
Vol. 93, no. 4
Fig. 1. Relationship between larval mortality index ([1 ⫺ (5th instar density on 27 August) (neonate density on 12
August)⫺1] ⫻ 100) and neonate density on 12 August in cotton. Plymouth, NC, 1996.
overestimate impact (Hassell and Waage 1984). Several approaches, including stage-speciÞc life tables
have been used successfully to more accurately assess
impacts of parasitoids on their host populations (Bellows et al. 1992). In our study, we chose the latter
approach and examined the fate of naturally oviposited heliothine egg cohorts within T. exiguum release
and control plots.
In each year of our study. T. exiguum releases substantially increased the percentage of heliothine eggs
lost to parasitism, although this increase was statistically signiÞcant only in 1996. Overall (1996 and 1997
combined), the percentage of eggs lost to Trichogramma parasitism was increased by 84% in T. ex-
iguum release plots. Increased parasitism signiÞcantly
reduced egg hatch, indicating that the additional parasitism from T. exiguum releases contributed mortality
from the egg stage to the Þrst larval instar.
In our study the percentage of eggs lost to parasitism
in control plots was relatively low during the initial
stages of the F2 heliothine ovipositional period, but
steadily increased throughout the ovipositional period. This trend has been observed in control plots
from other Trichogramma augmentation studies in cotton that reported parasitism data based on collection
of tan colored eggs (Stinner et al. 1974; Jones et al.
1977, 1979; Ables et al. 1979; Luttrell et al. 1980; King
et al. 1985). This suggests that T. exiguum releases have
Fig. 2. Relationship between larval mortality index ([1 ⫺ (5th instar density on 2 September) (neonate density on 18
August)⫺1] ⫻ 100) and neonate density on 18 August in cotton. Plymouth, NC, 1997.
August 2000
SUH ET AL.: Trichogramma RELEASES FAIL IN COTTON
more of an impact on heliothine eggs laid early in the
ovipositional period than on eggs laid later in the
period.
In addition to Trichogramma parasitism, predators
also contribute to heliothine egg mortality. In our
study the overall (1996 and 1997) average percentage
of eggs lost to predation for egg cohorts sampled
ranged from 10 to 18% in T. exiguum release plots and
8 to 34% in control plots. These ranges are consistent
with those reported by Fletcher and Thomas (1943),
who followed the fate of H. armigera eggs in cotton.
Similarly, Bell and Whitcomb (1964), using artiÞcially
placed H. zea eggs, reported that predators destroyed
between 10 and 28% of the eggs within 24 h after eggs
were placed on cotton plants.
Another factor contributing to heliothine egg mortality in our study was dislodgment of eggs from plants
by abiotic and biotic forces. Abiotic factors such as rain
and wind both have been shown to be important
mortality factors of heliothine eggs in cotton (Quaintance and Brues 1905, Fye 1979, Nuessly 1986). Under
Þeld conditions, Fletcher and Thomas (1943) reported that 11Ð 44% of H. armigera eggs were dislodged
from cotton plants by wind, rain, cultivation, or other
unknown sources. Additionally, some predators in cotton have been observed to carry H. zea eggs away at
times (Bell and Whitcomb 1964), leaving no evidence
of predation.
In our study, the percentage of heliothine eggs dislodged in T. exiguum release and control plots were
very similar for each cohort of eggs whose fate was
determined, but varied among cohorts, ranging from
18 to 74% in T. exiguum release plots and 18 to 59% in
control plots. The discrepancies among cohorts may
have resulted from each cohortÕs different exposure to
weather conditions. Nuessly et al. (1991), under simulated conditions, demonstrated that the impact of
rain and wind on heliothine egg dislodgment from
plants was dependent on the amount and duration of
these events. This may also explain the discrepancy
between the ranges reported in our study and those
reported by Fletcher and Thomas (1943).
We also examined the fate of blackened (parasitized) eggs to estimate the level of Trichogramma recycling. The recycling of parasitoids is considered
crucial for the economic success of augmentative Trichogramma releases. If enough Trichogramma are recycled early on, the number of subsequent releases
and release rates could be reduced.
Overall (both years and treatments combined), predation of eggs in our study before hatch averaged 16%,
whereas those that turned black (indicating parasitism) were preyed upon an additional 8%. Lingren and
Wolfenbarger (1976) reported that Orius insidiosus
(Say) attacked H. virescens eggs parasitized by T. pretiosum Riley as readily as nonparasitized eggs. Others
have suggested that predation of parasitized eggs may
be higher than for unparasitized eggs because of the
extended period they are exposed to predators, greatly
reducing the potential of parasitized eggs recycling
Trichogramma (Jones et al. 1977, King et al. 1985). The
percentage of parasitized eggs in our study (1996 and
1143
1997 combined) that produced adult Trichogramma
was identical in T. exiguum release and control plots,
⬇33%. However, because numbers of eggs classiÞed as
parasitized were higher in T. exiguum release plots, the
percentages of tagged eggs that produced adult Trichogramma were also higher in T. exiguum release
plots. Trichogramma adult eclosion (1996 and 1997
combined) took place in ⬇11% of the original eggs
tagged in T. exiguum release plots, whereas only 6% of
eggs tagged in control plots produced viable adult
Trichogramma. The average daily F3 heliothine egg
density from initial oviposition to peak oviposition
(1996 and 1997 combined) in T. exiguum release plots
was estimated to be 42,376 eggs per hectare. Assuming
11% of these eggs recycled T. exiguum and each produced two female, ⬇9,323 adult female Trichogramma
per hectare emerged daily from heliothine eggs oviposited between the initial and peak heliothine egg
laying period. In comparison, daily adult female T.
exiguum emergence from release capsules (1996 and
1997 combined) during the release period averaged
34,183 females per hectare. Thus, the contribution of
recycling in our study was negligible, indicating that
releases would have to be continued throughout the
heliothine ovipositional period to sustain parasitism
levels, particularly if natural populations of Trichogramma are not present in high numbers.
In our study, the combination of parasitism, predation, and abiotic factors produced high levels of heliothine egg mortality. Overall (1996 and 1997 combined), the percentage of eggs that hatched was
signiÞcantly reduced by 60% in T. exiguum release
plots compared with control plots. Based on egg hatch
data, it follows that the density of neonate larvae in T.
exiguum release plots was also signiÞcantly reduced by
60%. We elected to use egg density and fate data
instead of direct counts to estimate neonate densities
caused by the difÞculties in sampling for neonates.
Although neonate populations (based on egg density and fate data) in T. exiguum release plots were
signiÞcantly reduced, further examination of the larval
population structure through time revealed only a
slight reduction in density of thirdÐfourth instars in T.
exiguum release plots, and virtually no reduction in
density of Þfth instars. Combined analysis of 1996 egg
fate and larval population data revealed a correlation
between a larval mortality index (see Materials and
Methods) and neonate density (based on hatched egg
density), suggesting that density-related mortality occurred during the larval stage. However, there appeared to be no relationship between neonate density
and larval mortality in 1997, and the reason for this is
unknown. One possibility may be related to the small
number and range of neonates and Þfth instars found
in 1997, which may have limited our analysis. Another
possibility is that the factors responsible for densitydependent mortality in 1996 were not present in 1997.
Regardless of the reason, the fact that there was a
strong relationship between larval mortality and neonate density (i.e., density-related larval mortality) in
1 yr of our study, but not the other, may help explain
1144
JOURNAL OF ECONOMIC ENTOMOLOGY
why results from past Trichogramma release studies
have been so variable.
Several authors (e.g., Morrison and Strong 1980,
Stiling 1987, Walde and Murdoch 1988) noted that
inverse density dependence or density independence,
in general, was reported more frequently in the literature than direct density dependence for insect hostparasitoid systems. The existence and timing of density-dependent mortality relative to parasitism has a
dramatic impact on the success of parasitoid releases
(Hassell and Waage 1984). If density-dependent mortality occurs in a stage after parasitism, the effect of
parasitism on host population regulation may be compensated for by reduced mortality in the subsequent
stage (Van Driesche and Bellows 1996).
There is apparently very little information in the
literature concerning density dependence of mortality factors affecting heliothine larvae under Þeld conditions in cotton. The only case found involved spatial
density dependence in parasitism of H. virescens by
Microplitis croceipes (Cresson) (Hopper et al. 1991).
Simulations with several models using population dynamics of M. croceipes and heliothine species showed
that density-dependent mortality after parasitism
greatly reduced the impact of parasitoids on host dynamics (Hopper 1989).
In the few other cropping systems where larval
mortality has been examined in host populations following Trichogramma releases, results have varied. A
model incorporating Trichogramma parasitism and
density-dependent larval mortality of graminaceous
stalk borers Chilo partellus (Swinehoe) (van Hamburg
1980) indicated that density-dependent larval mortality can compensate for parasitism, even negating the
impact of parasitism, or worse, increase the size of
surviving larval populations (van Hamburg and Hassell 1984). In contrast, Andow et al. (1995) found a
strong relationship between Ostrinia nubilalis (Hu¨ bner) egg mass parasitism by T. nubilale Ertle & Davis
and larval population reduction in sweet corn, and
detected no evidence of density-dependent larval
mortality under Þeld conditions. They found that for
every 1% increase in egg mass parasitism, there was a
1% reduction in larval density, regardless of the initial
larval density.
Thus, it appears that the effect of Trichogramma
releases on pest and damage suppression depends
heavily on the occurrence and timing of density-dependent mortality. In our study, H. zea was the predominant heliothine species, and it is apparent that
density-related larval mortality factors such as parasitism, cannibalism, competition for feeding sites, or
predation had an offsetting effect on the neonate mortality contributed by Trichogramma egg parasitism.
Our study showed that releases of high quality T.
exiguum signiÞcantly increased heliothine egg parasitism and signiÞcantly reduced heliothine egg hatch.
However, reduction of egg hatch did not result in a
proportional reduction in Þfth-instar populations. It is
likely that density-related larval mortality had an offsetting effect on the additional egg mortality produced
by Trichogramma parasitism. This interaction (com-
Vol. 93, no. 4
pensatory mortality) may explain the lack of boll damage suppression reported in a prior study (see Suh et
al. 2000) as well as in past Trichogramma release studies in cotton. Because of the apparent occurrence of
compensatory mortality, the egg stage of heliothines is
not an appropriate target for biological control efforts
in cotton using Trichogramma wasp releases.
Acknowledgments
Appreciation is extended to J. R. Bradley and Fred Gould
(Department of Entomology, NCSU) for their insight, advice, and critical review of the manuscript. We also thank
Rebeca Rufty (Department of Crop Science, NCSU) for her
review of the manuscript. Special thanks to Jay Rosenheim
(Department of Entomology, UC at Davis) and Cavell
Brownie (Department of Statistics, NCSU) for their advice.
We are grateful to Firouz Kabiri and Jacque Frandon
(BIOTOP) for providing insects and materials. We also thank
Dan Borchert, Wayne Modlin, and Andrew Summerlin for
their technical assistance.
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Received for publication 22 September 1999; accepted 16
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