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Temperature-Dependent Life History of Eretmocerus eremicus (Hymenoptera:
Aphelinidae) on Two Whitefly Hosts (Homoptera: Aleyrodidae)
Author(s): S. M. Greenberg, B. C. Legaspi, W. A. Jones, and A. Enkegaard
Source: Environmental Entomology, 29(4):851-860. 2000.
Published By: Entomological Society of America
DOI: http://dx.doi.org/10.1603/0046-225X-29.4.851
URL: http://www.bioone.org/doi/full/10.1603/0046-225X-29.4.851
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BIOLOGICAL CONTROL
Temperature-Dependent Life History of Eretmocerus eremicus
(Hymenoptera: Aphelinidae) on Two Whitefly Hosts
(Homoptera: Aleyrodidae)
S. M. GREENBERG,
1
B. C. LEGASPI, JR.,
2
W. A. JONES, AND A. ENKEGAARD
3
BeneÞcial Insects Research Unit, Kika de la Garza Subtropical Agricultural Research Center, ARSÐUSDA,
2413 East Highway 83, Weslaco, TX 78596
Environ. Entomol. 29(4): 851Ð860 (2000)
ABSTRACT The effects of temperature on insect life history were studied for two whiteßy hosts
(Homoptera: Aleyrodidae), the silverleaf whiteßy, Bemisia argentifolii Bellows & Perring, and the
greenhouse whiteßy, Trialeurodes vaporariorum (Westwood), as well as the parasitoid, Eretmocerus
eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae) attacking both hosts. Mean egg numbers
as a function of time were Þtted to models for age-speciÞc oviposition for each whiteßy. For B.
argentifolii, numbers of eggs laid increased with time at 15, 21, and 24⬚C. At 28 and 32⬚C, the curve
declined after 6 d, although the model Þt was poor. The model did not Þt the oviposition data at 32⬚C.
Maximal oviposition rate occurred at 24⬚C (12 eggs per 48-h period), and the model was almost linear.
For T. vaporariorum, the model closely Þt mean eggs laid, with highest rates of ⬇12 eggs per 48 h
at 21 and 24⬚C. Numbers of whiteßy eggs as a function of time and temperature were described by
a three-dimensional surface model that was also used to estimate temperature thresholds for
oviposition (12.5⬚C for B. argentifolii and 10.9⬚C for T. vaporariorum). Increasing temperatures
produced decreased preoviposition periods in B. argentifolii, whereas temperature extremes resulted
in longer periods for T. vaporariorum. Development times from egg to adult, percentage mortality,
and estimated degree-days for development were measured at 15, 21, 24, 28, and 32⬚C for both
whiteßies, and for E. eremicus reared on both hosts. Development rate was higher for B. argentifolii
than T. vaporariorum at 24 and 28⬚C. Development of E. eremicus was faster using B. argentifolii as
hosts than T. vaporariorum at 24, 28, and 32⬚C. By extrapolation of development rates, lower
developmental thresholds (⬚C) were estimated as follows: T. vaporariorum, 2.92; B. argentifolii, 10.32;
E. eremicus on T. vaporariorum, 5.44; and E. eremicus on B. argentifolii, 8.7. Mean degree-day
requirements for egg to adult development were calculated for T. vaporariorum, 483.4; B. argentifolii,
319.7; E. eremicus on T. vaporariorum, 417.3; and, E. eremicus on B. argentifolii, 314.4. Percentage
mortality also was signiÞcantly affected by temperature in both species of whiteßy. For T. vapo-
rariorum, higher temperatures caused higher levels of mortality, with almost 98% killed at 32⬚C. The
reverse occurred in B. argentifolii, where highest levels of mortality were found at the lowest
temperatures. Mortality patterns in E. eremicus reßected those of the host: increasing with tem-
perature on T. vaporariorum, while decreasing on B. argentifolii. The life history of E. eremicus was
profoundly affected by that of its host.
KEY WORDS Bemisia argentifolii, Eretmocerus eremicus, Trialeurodes vaporariorum, temperature-
dependent, life history
Eretmocerus eremicus ROSE & Zolnerowich is a newly
described biparental parasitoid of the Bemisia tabaci
complex, previously referred to as E. californicus
Howard, E. sp. nr. californicus, or E. haldemani
Howard (Rose and Zolnerowich 1997). This species is
the most common indigenous parasitoid of the Bemisia
tabaci complex on cotton (Gossypium hirsutum L.) in
the desert areas of Arizona and California (Hoelmer
et al. 1998, Headrick et al. 1999). In greenhouse ex-
periments, E. eremicus found patches of host silverleaf
whiteßy, Bemisia argentifolii Bellows & Perring (Ho-
moptera: Aleyrodidae) more effectively and killed
more nymphs than Encarsia formosa Gahan (ÔBelts-
villeÕ strain) (Hymenoptera: Aphelinidae) on poin-
settia (Euphorbia pulcherrima Willd. ex Klotzsch)
(Hoddle et al. 1998a, Hoddle and van Driesche 1999).
Levels of whiteßy control by E. eremicus are affected
both by release rate (Hoddle et al. 1998b) and timing
(Hoddle et al. 1999). Interestingly, better control was
apparently achieved by host feeding rather than par-
asitization (Hoddle et al. 1999).
This article reports the results of research only. Mention of a
commercial or proprietary product does not constitute an endorse-
ment or recommendation by the USDA or the Texas A&M University
System for its use.
1
Current address: Integrated Farming and Natural Resources Re-
search Unit, Kika de la Garza Subtropical Agricultural Research Cen-
ter, USDAÐARS, 2413 East Highway 83, Weslaco, TX 78596.
2
Texas Agricultural Experiment Station, 2413 East Highway 83,
Weslaco, TX 78596.
3
Danish Institute of Agricultural Sciences, Department of Crop
Protection, Research Centre Flakkebjerg, DK-4200 Slagelse, Den-
mark.
Many researchers have studied the effects of the
physical and biological factors on the development
and reproduction of whiteßies and their parasitoids.
However, direct comparisons among published re-
ports are complicated by such factors as taxonomic
confusion in the genus Eretmocerus (Rose et al. 1996,
Rose and Zolnerowich 1997) and the Bemisia complex
(Brown et al. 1995), and differences in experimental
protocols employed. In previous studies, parasitization
levels by E. eremicus were not signiÞcantly different
between the whiteßy hosts B. argentifolii and Trialeu-
rodes vaporariorum (Westwood) (Homoptera: Aley-
rodidae) (W.A.J. and S.M.G., unpublished data). In
this article, we used common experimental protocols
that allowed direct comparisons of important life his-
tory characteristics between these two whiteßy hosts
and a common native parasitoid, E. eremicus.
Materials and Methods
Host Plant and Insect Cultures. Sweet potato, Ipo-
moea batatas (L.) Lam., was the host plant used in
these tests. Sweet potato was selected as the test plant
because it served as a suitable host for both species of
whiteßy tested (W.A.J. and S.M.G., unpublished
data). Test leaves used were excised and each leaf
petiole was placed in a ßoral aquapic with hydroponic
solution (Aqua-Ponics International, Los Angeles,
CA). Excised sweet potato leaves readily rooted and
did not deteriorate under ßuorescent lighting (20-W
Vita-Lite, Duro-Test Lighting, Elk Grove, IL) within
an incubator. We observed that roots appeared 7.2 ⫾
0.5 d after the leaf petiole was placed in the aquapic
and 78.0 ⫾13.0% of the excised leaves had rooted.
These leaves could be used for ⬇10 wk under labo-
ratory conditions.
The B. argentifolii culture was originally started
from individuals collected from cabbage in Hidalgo
County, TX, in 1994 (identiÞcation conÞrmed by J.
Brown, University of Arizona), and maintained in a
greenhouse, primarily on tomato, Lycopersicon escu-
lentum Miller. The T. vaporariorum culture originated
from individuals received from the culture maintained
at Cornell University (Ithaca, NY) on Phaseolus vul-
garis L. Before experimentation, we reared whiteßy
species as described above on sweet potato for three
generations. Our colony of E. eremicus (identiÞcation
conÞrmed by D. Vacek, USDA APHIS, Mission, TX,
through RAPD-polymerase chain reaction originated
from the cultures at Novartis BCM North America
(Oxnard, CA) where they were reared on B. argenti-
folii. Cultures of E. eremicus were reared on B. argen-
tifolii using sweet potato leaves in ßoral aquapics Þlled
with hydroponic solution.
Effects of Temperature on Whitefly Reproduction
and Preovipositional Period. The effects of tempera-
ture on whiteßy age-speciÞc oviposition rates were
compared between both species of whiteßy. Newly
emerged (⬍24 h) females of both species (n⫽15 per
whiteßy species) were conÞned individually to the
undersides of sweet potato leaves using clip cages.
Oviposition was measured under constant tempera-
tures of 15, 21, 24, 28, and 32⬚C(⫾0.5⬚C) in environ-
mental chambers (Percival ScientiÞc, Boone, IA), 55Ð
65% RH, under a photoperiod of 16:8 (L:D) h, at
1,400Ð1,725 lux. Leaves were visually inspected at 2-d
intervals over a period of 10 d. All eggs laid during the
48-h interval were totaled and removed using an en-
tomological pin.
Nonlinear regression was used to estimate models
for (1) mean numbers of whiteßy eggs as a function of
time for each temperature and whiteßy species; and
for (2) mean numbers of whiteßy eggs as a function of
time and temperature for each species. Regressions
described in (1) produced two-dimensional curves
describing oviposition with time at each temperature;
whereas regressions in (2) produced three-dimen-
sional surfaces describing the combined effects of time
and temperature. The following two models were
used: (1) for each species and temperature, numbers
of eggs laid over time was modeled according to the
equation: egg mean ⫽ad exp (-ed); where egg mean is
mean numbers of eggs laid over the 48-h period and d
is time (days); and (2) for each species, numbers of
eggs laid was Þtted to the model: egg mean ⫽(p⫹qT)
dexp(⫺wTd); where Tis temperature (⬚C). The pa-
rameter adescribes how quickly maximum oviposition
is reached, and ehow quickly it decelerates back to
zero. The parameters (p⫹q) and wdescribe the
effects of temperature on aand e, respectively (En-
kegaard 1993). The second equation was also used to
estimate T
0
⫽⫺(a/b), the lower threshold tempera-
ture for oviposition. Temperature effects on preovi-
positional period were measured in a fresh batch of
newly emerged (⬍24 h) females of both species (n⫽
15 per species). Whiteßies were conÞned individually
to the undersides of sweet potato leaves using clip
cages. Prevovipositional period was measured by vi-
sual inspection at 12-h intervals, until individuals
started to oviposit. Temperatures tested for B. argen-
tifolii were 15, 21, 24, 28, and 32⬚C(⫾0.5⬚C). However,
for T. vaporariorum, only 15, 24, and 28⬚C(⫾0.5⬚C)
were used to determine preoviposition period.
Temperature-Dependent Life History in White-
flies and Parasitoid. Temperature effects on whiteßy
mortality and developmental time from egg to adult
were measured using ⬇50 adults of each species. The
whiteßies were transferred to test leaves after chilling
for several minutes in a plastic vial placed inside a
refrigerator to reduce movement. Whiteßy adults
were conÞned together within a 4.5-cm-diameter clip
cage to the underside of each excised test leaf and
allowed to oviposit for 24 h at 25 ⫾1⬚C. The numbers
of eggs were counted and each rooted leaf with eggs
was placed in a polystyrene tissue culture dish (120 by
25 mm, Corning, Corning, NY) covered with polyester
organdy for ventilation. Hydroponic solution was
added to the ßoral aquapics as required. Dishes were
kept in environmental chambers (Percival ScientiÞc)
set at 15, 21, 24, 28, and 32⬚C(⫾0.5⬚C); 55Ð65% RH;
and a photoperiod of 16:8 (L:D) h at 1,400Ð1,725 lux.
After an initial 14-d incubation period, test leaves were
examined daily for whiteßy development and emer-
gence. Time for development from eggs to adult was
852 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 4
recorded for each individual nymph. Whiteßy mor-
tality was calculated as number of eggs that did not
hatch divided by the initial number of whiteßy eggs ⫻
100.
Temperature effects on parasitoid mortality and de-
velopmental time were compared in E. eremicus
reared on T. vaporariorum versus B. argentifolii. Before
experimentation, subcolonies of E. eremicus were es-
tablished where the parasitoid was reared for three
generations on the respective whiteßy host to be
tested. Sweet potato leaves were infested with either
of the whiteßy species as described above. After
whiteßies had developed to the second instar, all but
⬇35 nymphs were carefully removed using an ento-
mological pin. Subsequently, one mated (mating ob-
served) female parasitoid (⬍2 d old) was released and
conÞned with the nymphs in a clip cage at 25 ⫾1⬚C.
Nymphs containing developing parasitoids were
readily observable inside the host. After 24 h, parasi-
toids were removed using an aspirator, and the leaves
with parasitized nymphs were placed in chambers at
test temperatures (15, 21, 24, 28, and 32⬚C⫾0.5⬚C).
Leaves were checked daily; newly emerged adult
parasitoids were removed using an aspirator. Devel-
opmental time from egg to adult parasitoid emergence
and percentage parasitoid mortality were calculated
using the methods for the whiteßy species, as de-
scribed above.
Lower developmental threshold temperatures (T
0
)
for preimaginal development were estimated by
weighted linear regression on mean developmental
rates (reciprocal of mean developmental times, the
weight being the number of individuals) against tem-
perature, i.e., v⫽a⫹bT, where vis development rate,
and aand bare constants and T
0
⫽⫺(a/b). Degree-
days (DD) needed for development was calculated as
DD ⫽(T ⫺T
0
)D, where Tis temperature tested (⬚C);
T
0
is lower temperature threshold; and Dis mean
development time in days at temperature T.
Statistical Analysis. Nonlinear regressions were per-
formed using SAS (SAS Institute 1988). Percentage
data were transformed using the arcsine-square root
method, but are presented as nontransformed means
(Sokal and Rohlf 1994). Development rates were com-
pared statistically using a general linear model with
development rate as the dependent variable; factors
were temperature and insect species with species be-
ing a categorical variable (SPSS 1988).
Voucher specimens of E. eremicus are available at
USDAÐAPHIS Mission Plant Protection Center, Mis-
sion, TX.
Results
Effects of Temperature on Whitefly Reproduction
and Preovipositional Period. Mean egg number as a
function of time together with Þtted model curves are
shown for B. argentifolii and T. vaporariorum in Figs.
1 and 2, respectively. Parameter estimates for the
curves are given in Table 1. In B. argentifolii, numbers
of eggs laid increased with time at temperatures of 15,
21, and 24⬚C (Fig. 1 AÐC). At 28 and 32⬚C, the curve
declined after 6 d, although the model Þt was poor
(R
2
⫽0.169, Table 1). The model did not Þt the data
at 32⬚C (Fig. 1E; Table 1). Maximal oviposition oc-
curred at 24⬚C (12 eggs per 48-h period at day 8), and
the model was almost linear (Fig. 1C). The oviposition
model closely described the mean egg numbers for T.
vaporariorum (Fig. 2; Table 1). Highest oviposition
rates of ⬇12 eggs per 48 h were found at 21 and 24⬚C
at days 8Ð10 (Fig. 2 B and C).
Numbers of B. argentifolii eggs as a function of time
and temperature were described by the surface equa-
tion egg mean ⫽(⫺2.30462 ⫹0.185154T)dexp
(⫺0.0043727Td)(R
2
⫽0.654) (parameter standard
error values ⫽0.701124, 0.041358, 0.00087, respec-
tively) (Fig. 3A). Estimated T
0
for oviposition was
12.5⬚C. Numbers of T. vaporariorum eggs as a function
of time and temperature were described by egg
mean ⫽(⫺2.8967 ⫹0.26742T)dexp (⫺0.005046Td)
(R
2
⫽0.702) (parameter standard error values ⫽
0.944117, 0.05969, 0.00093, respectively) (Fig. 3B). Es-
timated T
0
for oviposition was 10.9⬚C.
The effects of temperature on preoviposition peri-
ods of both whiteßy species are shown in Fig. 4. In T.
vaporariorum, the temperature effect showed an ap-
parent nonlinear relationship (Y⫽21.496 ⫺1.9747X⫹
0.0465
2
; analysis of variance not possible because of
perfect Þt; n⫽15), whereas in B. argentifolii, higher
temperatures produced a linear decline in preovipo-
sition period (Y⫽9.2783 ⫺0.2802X;F⫽19.6; df ⫽1,
3; P⫽0.02; adj R
2
⫽0.82; n⫽15).
Temperature-Dependent Life History in White-
flies and Parasitoid. The effect of temperature on de-
velopmental times and mortalities for both whiteßy
hosts and E. eremicus on both hosts are shown in Table
2. Higher temperatures resulted in signiÞcant declines
in the developmental times of both species of whiteßy
(T. vaporariorum: F ⫽12,566.0, df ⫽4, P⬍0.01; B.
argentifolii: F ⫽3,772.6, df ⫽4, P⬍0.01), and in E.
eremicus on T. vaporariorum (F⫽6,674.5, df ⫽4, P⬍
0.01) and B. argentifolii (F⫽8,165.4, df ⫽4, P⬍0.01).
B. argentifolii had a longer developmental time than
T. vaporariorum at the two lowest and the highest
temperature, whereas the situation was reversed at
temperatures of 24 and 28⬚C. A similar pattern was
observed for E. eremicus that had longer developmen-
tal times at the two lowest temperatures when para-
sitizing B. argentifolii than compared with T. vaporari-
orum. At temperatures above 21⬚C, the situation was
reversed.
The weighted regressions for development of the
three species is shown in Fig. 5. For T. vaporariorum,
the regression was Y⫽⫺0.0058 ⫹0.00199T, where Y
is the reciprocal of development time, and Tis tem-
perature (⬚C) (F⫽64.3, df ⫽4, P⬍0.01; SE of
intercept ⫽0.00567, P⫽0.38; SE of slope ⫽0.00025,
P⬍0.01). The estimated lower threshold temperature
for development was T
0
⫽2.92⬚C. Because of the
nonlinearity in development rates for B. argentifolii,
only the three lowest temperatures were used. The
corresponding equation was Y⫽⫺0.0358 ⫹0.00347T
(F⫽614.3, df ⫽2, P⬍0.05; SE intercept ⫽0.0032, P⫽
0.06; SE slope ⫽0.00014, P⬍0.05), yielding a thresh-
August 2000 GREENBERG ET AL.: TEMPERATURE EFFECTS ON E. eremicus AND TWO HOSTS 853
old temperature of 10.32⬚C. Using T. vaporariorum as
the host, the development rate equation for E. eremi-
cus was Y⫽⫺0.0136 ⫹0.0025T(F⫽60.7, df ⫽4, P⬍
0.01; SE intercept ⫽0.0081, P⫽0.19; SE slope ⫽
0.00032, P⬍0.01), yielding T
0
⫽5.44⬚C. On B. argen-
tifolii, the corresponding equation was Y⫽⫺0.0287 ⫹
0.0033T(F⫽170.9, df ⫽4, P⬍0.01; SE intercept ⫽
0.0066, P⬍0.05; SE slope ⫽0.00025, P⬍0.01), with
T
0
⫽8.7⬚C.
Degree-day requirements for insect development
were calculated at each temperature (Table 2). Al-
though estimated degree-days should be a species-
speciÞc constant, some variability was recorded at
different temperatures. Mean degree-days (⫾SE;
n⫽5) were T. vaporariorum, 483.4 ⫾17.9; B. argen-
tifolii, 319.7 ⫾20.8; E. eremicus on T. vaporariorum,
417.3 ⫾26.2; and E. eremicus on B. argentifolii, 314.4 ⫾
9.2.
Fig. 1. Oviposition of B. argentifolii at Þve temperatures. Data points are numbers of eggs laid in 48-h periods (mean ⫾
SE, n⫽15). The line Þtted is as follows: egg mean ⫽ad exp (-ed); where egg mean is mean numbers of eggs laid over the
48-h period; dis time (d); aand eare parameters. Parameter estimates are given in Table 1.
854 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 4
Percentage egg to adult mortality also was signiÞ-
cantly affected by temperature in both species of
whiteßy (T. vaporariorum: F ⫽258.7; df ⫽4, 18; P⬍
0.01; B. argentifolii: F ⫽76.9; df ⫽5, 15; P⬍0.01) and
in E. eremicus on T. vaporariorum (F⫽18.7; df ⫽4, 24;
P⬍0.01) and B. argentifolii (F⫽64.2; df ⫽4, 20; P⬍
0.01). In T. vaporariorum, higher temperatures caused
higher levels of mortality. The reverse occurred in
B. argentifolii, where highest levels of mortality
were found at the lowest temperatures. Mortality
patterns in E. eremicus reßected those of the host;
increasing with temperature on T. vaporariorum, de-
creasing on B. argentifolii (Table 2). Interestingly,
E. eremicus parasitizing T. vaporariorum at 32⬚C suf-
fered only 53.3% mortality, much lower than the 97.8%
mortality of the host at this temperature. High mor-
tality in T. vaporariorum was incurred in the later host
stages, whereas E. eremicus parasitized second-instar
nymphs, which suffered lower mortalities at this tem-
perature.
Discussion
Direct comparisons in studies of insect life history
are often complicated by the use of different experi-
mental protocols and taxonomic confusion in the in-
sect groups being studied. By adopting identical ex-
perimental procedures in this study, we were able to
make direct comparisons between the effects of tem-
perature on the life histories of two species of whiteßy.
Furthermore, we compared temperature-dependent
life histories in a parasitoid attacking both whiteßy.
Fig. 2. Oviposition of T. vaporariorum at four temperatures (data for 32⬚C excluded because of excessive mortality). Data
points are numbers of eggs laid in 48-h periods (mean ⫾SE, n⫽15). The line Þtted is as follows: egg mean ⫽ad exp (-ed);
where egg mean is mean numbers of eggs laid over the 48-h period; dis time (d); aand eare parameters. Parameter estimates
are given in Table 1.
August 2000 GREENBERG ET AL.: TEMPERATURE EFFECTS ON E. eremicus AND TWO HOSTS 855
hosts. Such studies are uncommon (but see Henter
and van Lenteren 1996).
Published lifetime fecundities of B. tabaci (Genna-
dius Biotype ÔBÕ, ⫽B. argentifolii) are extremely var-
ied, ranging from ⬇40 to ⬎300 (Byrne and Bellows
1991, and references cited therein), although 50Ð200
are typical (e.g., Tsai and Wang 1996). Differences are
attributed to environmental conditions and host plant,
as well as the speciÞc strain being tested. With a
lifetime fecundity ⬎300 eggs per female, the Sudanese
strains of B. tabaci are apparently more fecund than
counterparts from other parts of the world (Byrne and
Bellows 1991). Using different host plants, Costa et al.
(1991) recorded means of 41.3Ð128.3 eggs laid within
a 48-h period by groups of 10 B. tabaci females at 27⬚C.
The per capita oviposition rate of 4.3Ð12.8 in 48 h
approximates our Þndings ⬇4 eggs per day in both
B. argentifolii and T. vaporariorum at 28⬚C. However,
Costa et al. (1991) allowed no further oviposition after
the initial 48-h period, whereas we report means av-
eraged over 10 d (daily means of Þve oviposition
periods of 48-h duration each).
Ambient temperature strongly affects insect re-
productive biology. The temperature-dependent age-
speciÞc fecundities of B. tabaci (Biotype ÔBÕ) were
described by Enkegaard (1993) who found an increase
in fecundity from 16 to 28⬚C, which is similar to the
pattern we observed. In B. tabaci on cotton, Butler et
al. (1983) found that mean number of eggs per female
declined from 81 at 26.7⬚C to 72 at 32.2⬚C. We found
similar inhibitory effects of increasing temperature
at 28⬚C and higher in both species of whiteßy (Figs. 1
and 2). Burnett (1949) reported that fecundity of
T. vaporariorum was zero at 9⬚C, 49 at 12⬚C, then
declined from 319.5 at 18⬚C to 5.5 at 33⬚C. Lifetime
and daily oviposition rates found by Burnett (1949)
are higher than reported here. In this study, highest
oviposition rates of ⬇12 eggs per 48 h were found at
21 and 24⬚CinT. vaporariorum and 24⬚CinB. argen-
tifolii. The oviposition thresholds of 12.5 and 10.9⬚C for
B. argentifolii and T. vaporariorum, respectively, are
slightly lower than T
0
values of 14.4 and 14.0⬚C for
B. tabaci reared on tobacco and poinsettia, respec-
tively (Enkegaard 1993), using the same estimation
procedure.
Fig. 3. Effects of temperature on age-speciÞc oviposition rates of (A) B. argentifolii and (B) T. vaporariorum after 2, 4,
6, 8, and 10 d. Temperatures tested were 15, 21, 24, 28, and 32⬚C for both species, except for 32⬚CinT. vaporariorum because
of excessive mortality. Data points represent mean numbers of eggs laid (n⫽15) over a 48-h period. Equations for the surfaces
are: egg mean ⫽(⫺2.30462 ⫹0.185154T)dexp (⫺0.0043727Td) and egg mean ⫽(⫺2.8967 ⫹0.26742T)dexp (⫺0.005046Td)
for B. argentifolii and T. vaporariorum, respectively. The surface for T. vaporariorum is not extended beyond 28⬚C because
of excessive mortality at 32⬚C.
Table 1. Parameter estimates for oviposition of B. argentifolii
and T. vaporariorum at different temperatures
T(⬚C) aSE (a)eSE (e)R
2
B. argentifolii
15 0.7736332 0.1011362 0.1109628 0.0176854 0.878
21 0.9880624 0.1472035 0.0804489 0.0195166 0.931
24 1.3863327 0.5853436 0.0154389 0.0512172 0.813
28 4.3222045 0.4356139 0.1779345 0.0150583 0.169
32 3.6758767 1.5930419 0.1491291 0.0621251 ⬍0.1
T. vaporariorum
15 1.0082471 0.1836011 0.1062234 0.0247036 0.758
21 3.8340153 0.5146747 0.1113621 0.0185207 0.852
24 3.7235169 0.1194447 0.1088922 0.0043684 0.994
28 3.0878699 0.3683194 0.1161595 0.0164160 0.899
The oviposition model is given as egg mean ⫽ad exp (-ed); where
egg mean is mean numbers of eggs laid over the 48-h period; dis time
(d); aand eare parameters (Enkegaard 1993).
856 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 4
The two whiteßy species displayed interesting dif-
ferences in the effect of temperature on preoviposi-
tion periods. Increasing temperatures produced de-
creased preoviposition periods in B. argentifolii,
whereas temperature extremes resulted in longer pe-
riods in T. vaporariorum. Both of these effects have
been found in other arthropods. Preoviposition period
decreased with increasing temperature in the pear
rust mite (max ⫽25⬚C), Epitrimerus pyri (Nalepa)
(Acari: Eriophyidae) (Bergh 1994); two Australian
ticks (Acari: Ixodidae), Amblyomma limbatum Neu-
mann and Aponomma hydrosauri (Denny) (Chilton
and Bull 1994); and the tropical horse tick, Demacentor
(Anocentor)nitens (Neumann) (Despins 1992). Pro-
longed preoviposition at temperature extremes was
found in the stable ßy, Stomoxys calcitrans (L.)
(Diptera: Muscidae), at maximum temperatures of
35⬚C (Lysyk 1998). For T. vaporariorum, Burnett
(1949) obtained results similar to those reported here:
preoviposition of 1.2 d at 18⬚C,0.4dat24⬚C, and 1.6 d
at 27⬚C. Enkegaard (1993) reported declining preovi-
position period with temperature in B. tabaci reared
on poinsettia, which are also similar to results reported
here for B. argentifolii.
The effect of temperature on development of the
Bemisia complex has been studied by many research-
ers (e.g., von Arx et al. 1983, Powell and Bellows 1992a,
Enkegaard 1993, Tsai and Wang 1996, Wang and Tsai
1996, and Drost et al. 1998). Wagner (1995) studied
B. tabaci (Biotype ÔBÕ) on cotton under 31 constant
temperatures and reported results comparable to
those obtained in this study (median development
times from egg to adult: 26.6 d at 22⬚C; 22.6 at 23.8⬚C;
16.9 at 28⬚C; and, 19.4 d at 32⬚C). Temperature-
dependent development in T. vaporariorum was re-
ported by Burnett (1949), Osborne (1982), and Drost
et al. (1998). Development rates of B. tabaci (different
biotypes) and T. vaporariorum (on different host
plants) are similar to those in this study, i.e., ⬇0.02 at
15⬚C, and increasing to ⬇0.06 at 30⬚C (Drost et al.
1998).
Relatively little research has focused on the life
history of species of Eretmocerus (e.g., McAuslane and
Nguyen 1996). Lopez and Botto (1997) studied a
South American population of Eretmocerus sp. attack-
ing T. vaporariorum on tomatoes and found develop-
mental times of 19.8 d at 26⬚C and 19.3 d at 29⬚C.
Interpolation of the weighted regression presented in
this article for E. eremicus on T. vaporariorum yields
19.5dat26⬚C and 17.0 d at 29⬚C. Powell and Bellows
(1992b) compared life histories in two populations of
Eretmocerus (undetermined arrhenotokous and the-
lytokous species) attacking B. tabaci at different tem-
peratures. Developmental periods ranged from 15.2 d
in males from an arrhenotokous population at 29⬚C, to
Fig. 4. Preoviposition period in T. vaporariorum and B.
argentifolii (mean ⫾SE, n⫽15 per species) as affected by
temperature. In T. vaporariorum, the relationship is quadratic
(Y⫽21.496 ⫺1.9747X⫹0.0465
2
), whereas in B. argentifolii,
it is linear (Y⫽9.2783 ⫺0.2802X).
Table 2. Developmental times (d, egg to adult), degree-days required for development, and mortality (%, egg to adult) (means ⴞSE)
for T. vaporariorum, B. argentifolli, and E. eremicus on both hosts at different temperatures
Temp, ⬚CT. vaporariorum B. argentifolii
Development
a
DD
b
n
c
Mortality
d
n
e
Development
a
DD
b
n
c
Mortality
d
n
e
15 43.7 ⫾0.1a 527.9 932 10.8 ⫾0.02c 235 63.3 ⫾0.13a 296.2 33 78.7 ⫾0.034a 147
21 24.1 ⫾0.18b 435.7 171 16.3 ⫾0.025bc 219 26.4 ⫾0.16b 281.9 69 60.6 ⫾0.037b 176
24 22.4 ⫾0.05c 472.2 777 22.4 ⫾0.027b 235 21.1 ⫾0.16c 288.7 211 23.1 ⫾0.033c 167
28 20.8 ⫾0.07d 521.7 922 30.2 ⫾0.038b 145 19.2 ⫾0.2d 339.5 72 8.0 ⫾0.022d 153
32 15.8 ⫾0.37e 459.5 5 97.8 ⫾0.01a 219 18.1 ⫾0.16e 392.4 169 9.6 ⫾0.024d 148
Eretmocerus eremicus on host:
15 54.0 ⫾0.28a 516.2 88 30.8 ⫾0.043b 114 55.2 ⫾0.16a 347.8 81 68.2 ⫾0.038a 148
21 23.1 ⫾0.12b 359.4 187 23.6 ⫾0.027bc 237 24.3 ⫾0.14b 298.9 212 53.7 ⫾0.039b 160
24 21.6 ⫾0.12c 400.9 297 10.5 ⫾0.018c 291 20.2 ⫾0.2c 309.1 183 26.6 ⫾0.032c 187
28 17.9 ⫾0.13d 403.8 166 25.1 ⫾0.033bc 178 15.4 ⫾0.07d 297.2 514 23.5 ⫾0.032c 171
32 15.3 ⫾0.11e 406.4 157 53.3 ⫾0.042a 143 13.7 ⫾0.14e 319.2 152 17.8 ⫾0.034c 129
a
Means followed by different letters in a column are signiÞcantly different (Tukey HSD, P⬍0.01).
b
Degree-days required to complete development; ⫽developmental time ⫻(temperature Ð threshold temperature).
c
Number of insects measured for developmental times.
d
Means followed by different letters in a column are signiÞcantly different (Tukey HSD, P⬍0.05). SE ⫽公(pg/n),where pis proportion,
q⫽1Ðp, and nis initial number of individuals.
e
Number of insects measured for mortality.
August 2000 GREENBERG ET AL.: TEMPERATURE EFFECTS ON E. eremicus AND TWO HOSTS 857
36.4 d in arrhenotokous females at 20⬚C (both on
cucumber). Interpolated estimates using our data are
17.0 and 27.5 d at 29 and 20⬚C, respectively. SigniÞcant
differences were found in preimaginal development,
indicating that the thelytokous population would af-
ford better biological control of B. tabaci at higher
temperatures.
Lower threshold temperatures were estimated by
extrapolating linear development rates to tempera-
tures at which development rate is 0. This method may
provide reasonably reliable estimates of T
0
using the
limited data available. However, caution should be
taken when the experimental temperature range is
distant to the estimated lower threshold, or when
nonlinearities exist, especially at the lower tempera-
tures. T
0
values previously reported appear higher
than those in the current study: T. vaporariorum, 8.3⬚C
(Osborne 1982); B. argentifolii, ⬇12⬚C (Wang and Tsai
1996); and B. tabaci, 10.8⬚C (von Arx et al. 1983), 12⬚C
(Enkegaard 1993), 14Ð17⬚C (Powell and Bellows
1992a). No T
0
values were found in the literature for
Eretmocerus species. Knowledge of T
0
values may be
used in assessing overwintering ability or cold toler-
ance of pest species. Eggs of B. argentifolii may be
more cold-tolerant than adults and nymphs at tem-
peratures of ⫺2to⫺10⬚C (Simmons and Elsey 1995).
In the case of parasitoids, T0 values may be used to set
temperatures for storage or shipment.
Estimates of developmental degree-day require-
ments for egg to adult development are as follows: B.
tabaci, 327 (Enkegaard 1993) and 368.5 (Zalom and
Natwick 1987); T. vaporariorum, 380.7 (Osborne
1982); and 252Ð315 (Wang and Tsai 1996, estimated
from their data). Our estimate for B. argentifolii
(319.7) compares favorably with degree-day require-
ments previously published for Bemisia species. How-
ever, our estimate for T. vaporariorum (483.4) is
higher than that of Osborne (1982) because of our low
T
0
value for this species. We were unable to locate
degree-day estimates for the development of species
of Eretmocerus. As a comparison, degree-days from
oviposition to adult eclosion has been given as 188.9 in
Encarsia formosa Gahan (Hymenoptera: Aphelinidae)
attacking T. vaporariorum (Osborne 1982), which is
much lower than our estimates for E. eremicus.
The effect of temperature on preimaginal mortality
has been studied in the host whiteßy species. In T.
vaporariorum, Burnett (1949) found that mortality
increased with temperature, from 6.6% at 18⬚C, rising
to 32.4% at 27⬚C. In B. tabaci on poinsettia, Enkegaard
(1993) reported a negative relationship, from 95% at
16⬚C, declining to 6.1% at 28⬚C. Wagner (1995) found
low preimaginal mortality (⬍25%) in B. tabaci on
cotton between 15 and 30⬚C, increasing to nearly 100%
mortality ⬇34⬚C. However, no consistent relationship
is evident in data presented in Powell and Bellows
(1992a) for B. tabaci on cucumber and cotton at 20Ð
32⬚C. For B. argentifolii on eggplant, mortality was
⬇60% at temperature extremes of 15 and 35⬚C, and
lowest at 11.3% at 25⬚C (Wang and Tsai 1996). We
were unable to locate similar studies in the literature
for Eretmocerus species. Like Burnett (1949), we
found that mortality increased with temperature in
T. vaporariorum, from 10.8% at 15⬚C, rising to a max-
imum of 97.8% at 32⬚C. In contrast, mortality declined
with temperature in B. argentifolii, decreasing
from 78.7% at 15⬚C to a minimum of 8% at 28⬚C, similar
to the Þnding of Enkegaard (1993) for B. tabaci.
The temperature effects of preimaginal mortality of
the parasitoid were different on the two hosts. On
T. vaporariorum, mortality of E. eremicus immatures
was highest at the extreme temperatures of 15 and
32⬚C (30.8 and 53.3%, respectively), and lowest at the
midpoint temperature of 24⬚C (10.5%). However, on
B. argentifolii, preimaginal mortality declined from
68.2% at 15⬚C to 17.8% at 32⬚C. Clearly, temperature
effects on preimaginal mortality are variable, and no
prevalent relationship exists in the literature. More-
over, analysis of parasitoid mortality is perhaps com-
plicated by confounding effects caused by mortality of
the host. The life history of E. eremicus appears pro-
foundly affected by temperature effects on its host.
Furthermore, Henter and van Lenteren (1996) sug-
gest that parasitism rates in different populations of
Fig. 5. Development rate (1/development time, mean ⫾
SE) as a function of temperature for (A) whiteßies, B. ar-
gentifolii and T. vaporariorum; and (B) E. eremicus on both
whiteßy hosts. B. argentifolii (⌬), B. argentifolii regression
(.......
), T. vaporariorum (F), T. vaporariorum regression
(ÑÑ).
858 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 4
E. formosa may differ as a result of conditioning effects
when reared on T. vaporariorum or B. tabaci.
The data contained in this study are a useful con-
tribution to the knowledge of the whiteßy hosts and
their common parasitoid E. eremicus. The information
can be useful in designing mass-rearing protocols, in
helping to make decisions in augmentative release
trials, and in the development of predictive modeling
efforts.
Acknowledgments
We are grateful to T.-X. Liu (Texas Agricultural Experi-
ment Station, Weslaco), J. A. Goolsby (ARS Australian Bio-
logical Control, Indooroopilly, Queensland, Australia), and
two anonymous reviewers for helpful comments. J. P. Sand-
erson (Department of Entomology, Cornell University,
Ithaca, NY) provided specimens of T. vaporariorum from
which we established colonies for experimentation, and
D. Cahn (Novartis BCM North America, Oxnard, CA) pro-
vided the founders for our colony of E. eremicus. Approved
for publication by the director of the Texas Agricultural
Experiment Station.
References Cited
Bergh, J. C. 1994. Pear rust mite (Acari: Eriophyidae) fe-
cundity and development at constant temperatures. En-
viron. Entomol. 23: 420Ð424.
Brown, J. K., D. R. Frohlich, and R. C. Rosell. 1995. The
sweetpotato or silverleaf whiteßies: biotypes of Bemisia
tabaci or a species complex? Annu. Rev. Entomol 40:
511Ð534.
Butler, G. D. Jr., T. J. Henneberry, and T. E. Clayton. 1983.
Bemisia tabaci (Homoptera: Aleyrodidae): development,
oviposition, and longevity in relation to temperature.
Ann. Entomol. Soc. Am. 76: 310Ð313.
Burnett, T. 1949. The effect of temperature on an insect
host-parasite population. Ecology 30: 113Ð134.
Byrne, D. N., and T. S. Bellows, Jr. 1991. Whiteßy biology.
Annu. Rev. Entomol. 36: 431Ð437.
Chilton, N. B., and C. M. Bull. 1994. Inßuence of environ-
mental factors on oviposition and egg development in
Amblyomma limbatum and Aponomma hydrosauri (Acari:
Ixodidae). Int. J. Parasitol. 24: 83Ð90.
Costa, H. S., J. K. Brown, and D. N. Byrne. 1991. Life history
traits of the whiteßy, Bemisia tabaci (Homoptera: Aley-
rodidae) on six virus-infected on healthy plant species.
Environ. Entomol. 20: 1102Ð1107.
Despins, J. L. 1992. Effects of temperature and humidity on
ovipositional biology and egg development of the tropical
horse tick, Dermacentor (Anocentor) nitens. J. Med. En-
tomol. 29: 332Ð337.
Drost, Y. C., J. C. van Lenteren, and H.J.W. van Roermund.
1998. Life-history parameters of different biotypes of
Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to
temperature and host plant: a selective review. Bull. En-
tomol. Res. 88: 219Ð229.
Enkegaard, A. 1993. The poinsettia strain of the cotton
whiteßy, Bemisia tabaci (Homoptera: Aleyrodidae),
biological and demographic parameters on poinsettia
(Euphorbia pulcherrima) in relation to temperature. Bull.
Entomol. Res. 83: 535Ð546.
Headrick, D. H., T. S. Bellows, and T. M. Perring. 1999.
Development and reproduction of a population of Eret-
mocerus eremicus (Hymenoptera: Aphelinidae) on Bemi-
sia argentifolii (Homoptera: Aleyrodidae). Environ. En-
tomol. 28: 300Ð306.
Henter, H. J., and J. van Lenteren. 1996. Variation between
laboratory populations in the performance of the para-
sitoid Encarsia formosa on two hosts, Bemisia tabaci and
Trialeurodes vaporariorum. Entomol. Exp. Appl. 80: 427Ð
434.
Hoddle, M. S., and R. G. Van Driesche. 1999. Evaluation of
inundative releases of Eretmocerus eremicus and Encarsia
formosa Beltsville strain in commercial greenhouses for
control of Bemisia argentifolii (Hemiptera: Aleyrodidae)
on poinsettia stock plants. J. Econ. Entomol. 92: 811Ð824.
Hoddle, M. S., R. G. van Driesche, J. S. Elkinton, and J. P.
Sanderson. 1998a. Discovery and utilization of Bemisia
argentifolii patches by Eretmocerus eremicus and Encarsia
formosa (Beltsville strain) in greenhouses. Entomol. Exp.
Appl. 87: 15Ð28.
Hoddle, M. S., R. G. van Driesche, J. P. Sanderson, and
O.P.J.M. Minkenberg. 1998b. Biological control of
Bemisia argentifolii (Hemiptera: Aleyrodidae) on poin-
settia with inundative releases of Eretmocerus eremicus
(Hymenoptera: Aphelinidae): do release rates affect par-
asitism? Bull. Entomol. Res 88: 47Ð58.
Hoddle, M. S., J. P. Sanderson, and R. G. van Driesche. 1999.
Biological control of Bemisia argentifolii (Hemiptera:
Aleyrodidae) on poinsettia with inundative releases of
Eretmocerus eremicus (Hymenoptera: Aphelinidae): does
varying the weekly release rate affect control? Bull. En-
tomol. Res 89: 41Ð51.
Hoelmer, K. A., W. J. Roltsch, C. C. Chu, and T. J. Hen-
neberry. 1998. Selectivity of whiteßy traps in cotton for
Eretmocerus eremicus (Hymenoptera: Aphelinidae), a na-
tive parasitoid of Bemisia argentifolii (Homoptera: Aley-
rodidae). Environ. Entomol. 27: 1039Ð1044.
Lopez, S. N., and E. N. Botto. 1997. Biology of a South
American population of Eretmocerus sp. (Hymenoptera:
Aphelinidae) attacking the greenhouse whiteßy. Biol.
Control 9: 1Ð5.
Lysyk, T. J. 1998. Relationships between temperature and
life-history parameters of Stomoxys calcitrans (Diptera:
Muscidae). J. Med. Entomol. 35: 107Ð119.
McAuslane, H. J., and R. Nguyen. 1996. Reproductive biol-
ogy and behavior of a thelytokus species of Eretmocerus
(Hymenoptera: Aphelinidae) parasitizing Bemisia argen-
tifolii (Homoptera: Aleyrodidae). Ann. Entomol. Soc.
Am. 89: 686Ð693.
Osborne, L. S. 1982. Temperature-dependent development
of greenhouse whiteßy and its parasite Encarsia formosa.
Environ. Entomol. 11: 483Ð485.
Powell, D. A., and T. S. Bellows, Jr. 1992a. Preimaginal de-
velopment and survival of Bemisia tabaci on cotton and
cucumber. Environ. Entomol. 21: 359Ð363.
Powell, D. A., and T. S. Bellows, Jr. 1992b. Development
and reproduction of two populations of Eretmocerus spe-
cies (Hymenoptera: Aphelinidae) on Bemisia tabaci
(Homoptera: Aleyrodidae). Environ. Entomol. 21: 651Ð
658.
Rose, M., and G. Zolnerowich. 1997. Eretmocerus Haldeman
(Hymenoptera: Aphelinidae) in the United States, with
descriptions of new species attacking Bemisia (tabaci
complex) (Homoptera: Aleyrodidae). Proc. Entomol.
Soc. Wash. 99: 1Ð27.
Rose, M., G. Zolnerowich, and M. S. Hunter. 1996. System-
atics, Eretmocerus, and biological control, p. 477Ð497. In
D. Gerling and R. T. Mayer (eds.) Bemisia 1995: taxon-
omy, biology, damage, control and management. Inter-
cept, Andover, UK.
August 2000 GREENBERG ET AL.: TEMPERATURE EFFECTS ON E. eremicus AND TWO HOSTS 859
SAS Institute. 1998. JAS/STAT UserÕs guide, release 6.03 ed.
SAS Institute, Cary, NC.
Simmons, A. M., and K. D. Elsey. 1995. Overwintering and
cold tolerance of Bemisia argentifolii (Homoptera: Aley-
rodidae) in coastal South Carolina. J. Entomol. Sci. 30:
497Ð506.
Sokal, R. R., and F. J. Rohlf. 1994. Biometry: the principles
and practice of statistics in biological research. Freeman,
San Francisco, CA.
SPSS. 1998. Systat 8.0, Statistics, Chicago, IL.
Tsai, J. H., and K. Wang. 1996. Development and reproduc-
tion of Bemisia argentifolii (Homoptera: Aleyrodidae) on
Þve host plants. Environ. Entomol. 25: 810Ð816.
von Arx, R., J. Baumga¨rtner, and V. Delucchi. 1983. Devel-
opmental biology of Bemisia tabaci (Genn.) (Stenorrhyn-
cha, Aleyrodidae) on cotton at constant temperatures.
Mitt. Schweiz. Entomol. Ges. 56: 389Ð399.
Wagner, T. L. 1995. Temperature-dependent development,
mortality, and adult size of sweetpotato whiteßy Biotype
B (Homoptera: Aleyrodidae) on cotton. Environ. Ento-
mol. 24: 1179Ð1188.
Wang, K., and J. H. Tsai. 1996. Temperature effect on
development and reproduction of silverleaf whiteßy
(Homoptera: Aleyrodidae). Ann. Entomol. Soc. Am. 89:
375Ð384.
Zalom, F. G., and E. T. Natwick. 1987. Developmental time
of sweetpotato whiteßy (Homoptera: Aleyrodidae) in
small Þeld cages on cotton plants. Fla. Entomol. 70: 427Ð
431.
Received for publication 20 October 1999; accepted 24 April
2000.
860 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 4
