ECOLOGY AND POPULATION BIOLOGY
Climate Change and Bemisia tabaci (Hemiptera: Aleyrodidae): Impacts
of Temperature and Carbon Dioxide on Life History
LEVI B. CURNUTTE,1 ALVIN M. SIMMONS,2,3
AND
SHAABAN ABD-RABOU4
Ann. Entomol. Soc. Am. 107(5): 933Ð943 (2014); DOI: http://dx.doi.org/10.1603/AN13143
ABSTRACT Climate change is relevant to life around the globe. A rise in ambient temperature and
carbon dioxide (CO2) may have various impacts on arthropods such as altered life cycles, modiÞed
reproductive patterns, and changes in distribution. The sweetpotato whiteßy, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a global pest responsible for signiÞcant losses of agricultural
yields annually. This study was conducted to determine the impacts of changing temperature and CO2
levels on selected life history parameters of B. tabaci biotype B. Populations were established at three
temperature regimes (25, 28, and 33⬚C), and each population was evaluated in all three environments.
Collard, Brassica oleracea ssp. acephala de Condolle (Brassicaceae), was used as the host. These results
were based on data from 5 to ⬇30 generations. Oviposition, nymphal survival, and reproduction were
signiÞcantly affected by temperature, with net reproductive success declining to 36.4% at 33⬚C.
Overall, 28⬚C was most favorable for whiteßy Þtness. However, the optimal temperature for B. tabaci
reproduction may be between 28 and 33⬚C. There were no temperature effects on total nonstructural
carbohydrate concentrations in collard, and impacts of the host plant on whiteßy development in the
different environments were determined to be minimal. An environment of enriched CO2 (750 ppm)
was not observed to have an adverse effect on whiteßy reproduction. Temperature was negatively
correlated with adult body size. Length and width of males and females were affected by temperature.
Data regarding population dynamics of B. tabaci in response to climate change are important for
accurate predictions and improving management practices.
KEY WORDS Bemisia tabaci, climate change, carbon dioxide, temperature, life history
The current trend of atmospheric enrichment of carbon dioxide (CO2) is a global concern, as increases in
CO2 promote increases in surface temperatures. Combustion of fossil fuels, as well as other primary causes
such as widespread deforestation, has aided atmospheric concentrations of CO2 to increase by 31% over
the past 200 yr (Hance et al. 2007), and CO2 levels
have exceeded 400 ppm for the Þrst time in the modern era as of May 2013 (National Oceanic and Atmospheric Administration 2013). Global surface temperatures have increased 0.74 ⫾ 0.18⬚C during the last
century, and low- and high-emission scenarios are
predicted to yield up to 4.0 and 11.0⬚C temperature
increases, respectively, by the year 2100 (United
States Global Climate Research Program 2009). Cold
days, cold nights, and frost events have become less
frequent, whereas hot days, hot nights, and heat waves
have become more common (Intergovernmental
Panel on Climate Change 2007). In addition, increases
in the extremity of such weather events are likely.
1 Environmental Studies Program, College of Charleston, Charleston, SC 29424.
2 USDAÐARS, U.S. Vegetable Laboratory, 2700 Savannah Highway,
Charleston, SC 29414.
3 Corresponding author, e-mail: [email protected].
4 Ministry of Agriculture, ARC, Plant Protection Research Institute,
7 Nadi El-Seid, Dokki, Giza, Egypt.
Because organisms are not adapted to rapid and
drastic increases in temperature or CO2, signiÞcant
changes in insects, plants, and their relationships are
expected with continued global warming (Porter et al.
1991, Zvereva and Kozlov 2006, Legaspi et al. 2011).
Rising temperatures have altered ßowering times of
plants along with temporal and spatial distribution
patterns of both plants and insects (Parmesan 2006).
Overall, biomass and carbohydrate concentrations
typically increase in foliage grown under elevated
CO2, which may increase plant C: N ratios by an
average of 19% and dilute N concentrations by 15Ð25%
(Stiling and Cornelissen 2007, Robinson et al. 2012).
Physical characteristics of leaves, including surface
waxes, secretory canals, and leaf toughness, may also
respond to elevated CO2 levels (DeLucia et al. 2012).
These factors may have implications for herbivores.
Studies that have focused on CO2 enrichment suggest
that the performance of herbivores in these environments has generally been dependent on their modes
of feeding (Porter et al. 1991, Bezemer and Jones 1998,
Hamilton et al. 2004). The responses of phloem feeders to elevated atmospheric CO2 concentrations are
inconsistent; however, reductions in performance of
defoliators, leaf miners, and xylem feeders have been
observed (Bezemer and Jones 1999). Studies by Bezemer et al. (1999) and Hughes and Bazzaz (2001)
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suggested that the responses of phloem feeders, such
as whiteßies to elevated CO2 levels, vary with the
species of insects and host plants, the biological levels
(population or individual), and the experimental duration (number of generations).
The sweetpotato whiteßy, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a global polyphagous pest of agricultural crops (Greathead 1986, Basu
1995, Oliveira et al. 2001, Simmons et al. 2008) and is
particularly abundant in cultivated and uncultivated
subtropical and tropical habitats (McKenzie et al.
2004). Thought to originate from sub-Saharan Africa
(Dinsdale et al. 2010), anthropogenic inßuence and
mild winters have allowed B. tabaci to expand its
distribution around the globe, adapt to more northern
areas, develop resistance to insecticides, and develop
new biotypes (Prabhaker et al. 1985, Byrne et al. 1990,
Perring et al. 1993, Horowitz et al. 2005). B. tabaci
(synonymous with Bemisia argentifolii Bellows and
Perring), is known to vector ⬎100 viruses (Jones
2003) and feed on ⬎1,000 plant species (Simmons et
al. 2008, Abd-Rabou and Simmons 2010). Moreover, of
the ⬎1,500 different whiteßy species within Aleyrodidae (Martin and Mound 2007), B. tabaci, along with
Trialeurodes vaporiorum (Westwood), are the two
species that cause the majority of economic losses to
agriculture worldwide (Martin 1987, Byrne et al. 1990,
Brown 1994).
Several studies have demonstrated that life cycles of
whiteßies can vary greatly depending on temperature,
relative humidity, and host plant (Lopez-Avila 1986,
Enkegaard 1993, Simmons 1994, Simmons and Elsey
1995, Drost et al. 1998, Simmons and Mahroof 2011).
Temperature is the primary limiting factor for whiteßy
populations affecting reproduction, mortality, and
their ability to exploit particular host plants (Naranjo
et al. 2010). However, studies on the effects of temperature on development, survival, and reproduction
of B. tabaci were documented almost exclusively
based on single generations (Nava-Camberos et al.
2001). Only a few studies have reported the effects of
elevated CO2 on whiteßies. There has been considerable variation in conclusions relating to elevated
CO2 and any effect it may have on whiteßy Þtness
(Ward and Kelly 2004).
Accurate determination of how whiteßy populations, host plants, competitors, and predators respond
to the changing climate is fundamental to understanding their population dynamics. It is essential for identifying future successful management techniques. This
study provides insight on whether selected populations differ in their biological responses to changes in
ambient temperature and CO2 within otherwise similar environments. We examined several life history
parameters in populations of B. tabaci that were previously adapted to distinct environments.
Materials and Methods
Insects and Plants. Separate populations of whiteßies were established to represent populations that
were adapted to three different climate regimes.
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Table 1. Mean ⴞ SEM environmental conditions within research chambers and cages for laboratory life history experiments
on B. tabaci
Arena
Temp. (⬚C)
25⬚C chambers
28⬚C chambers
33⬚C chambers
Low CO2 cages
High CO2 cages
25.1 ⫾ 0.04
28.2 ⫾ 0.03
33.0 ⫾ 0.02
28.1 ⫾ 0.02
28.1 ⫾ 0.01
Relative
VPD
CO2 (ppm)
humidity (%) (kPa)
58.2 ⫾ 0.3
61.8 ⫾ 0.98
64.0 ⫾ 0.27
30.3 ⫾ 0.1
30.8 ⫾ 0.1
1.3
1.5
2.0
2.6
2.6
458 ⫾ 1.38
449 ⫾ 1.63
455 ⫾ 0.76
424 ⫾ 0.34
753 ⫾ 3.03
Whiteßies (B. tabaci biotype B) used in all experiments were obtained from a greenhouse colony maintained at the U.S. Vegetable Laboratory, U.S. Department of AgricultureÐAgricultural Research Service
(USDA-ARS), Charleston, SC. Colony B. tabaci were
reared on assorted vegetable crops, primarily collard,
Brassica oleracea ssp. acephala de Condolle, in a greenhouse as described by Simmons (1994). “Georgian”
collard plants were used as the host for all assays
herein. Collard seedlings were established in Jiffy
starter pellets (Jiffy Products of America, Batavia, IL)
within an insect-free growth chamber at 28⬚C, 60%
relative humidity (RH; 1.5 kPa vapor pressure deÞcit
[VPD]), and photoperiod of 16:8 (L:D) h. Seedlings
were allowed to reach the 3Ð5 leaf stage. The cotyledons were removed. The plants along with the starter
pellets were then transplanted into 10-cm-diameter
pots containing Metro-Mix 360 growth medium (Sun
Gro Horticulture, Agawam, MA). Each plant with pot
was placed in an interlocking plastic bag and was then
loosely sealed around the base of the stem. The bags
were used to limit moisture release into the environmental chamber as well as to retain moisture within
pots. Water was added within the plastic bags as
needed. Once potted and sealed, 12 collards were
added to each 24-cm3 clear vinyl, Þne-mesh BugDorm
cage (BioQuip Products, Rancho Dominguez, CA)
within each of three environmental chambers (model
I-36VL, Percival, Perry, IA). Three separate temperature conditions were established, representing relatively warm (33⬚C), moderate (28⬚C), and cool (25⬚C)
climate conditions (Table 1) with a photoperiod of
16:8 (L:D) h. For a given experimental trial, environmental conditions were randomly rotated among six
chambers throughout the study. Lighting in each
chamber was by four 32-W ßuorescent lamps oriented
vertically along two opposite walls. Moisture conditions within chambers were maintained at ⬇60% RH,
yielding a VPD of ⬇2.0, 1.5, and 1.3 kPa for the warm,
moderate, and cool temperatures, respectively (Table
1). Three 500-count mixed-age adult B. tabaci samples
were collected from the greenhouse colony in separate vials. The cage within each climate treatment was
infested with a vial of whiteßies that were allowed to
disperse freely upon the collard seedlings. The populations of whiteßies were left to self-sustain, effectively yielding three temperature-adapted base populations designated as P25, P28, and P33 for the 25, 28,
and 33⬚C environments, respectively. New pots of
collard seedlings were added as needed to maintain a
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Fig. 1. Flow chart of laboratory temperature-dependent
assays on life history of B. tabaci. Whiteßies from a common
greenhouse colony were released into three separate temperature regimes, and after multiple generations, each population was assayed in three environments.
source of food. Assays were conducted after 5 and up
to ⬇30 generations on these populations.
Oviposition Assay. A laboratory experiment to determine the effects of temperature on oviposition
among the three above-described populations of B.
tabaci was performed. A random sample of 10 adult
female whiteßies from each population was placed in
a separate smaller cage, an open 18-cm-deep by 20cm-diameter clear plastic cylinder. Each cage contained three 2Ð3 leaf collard seedlings. The starter
pellet and bottom of each plant were placed within an
interlocking plastic bag as described above in Insects
and Plants section. The sample of whiteßies was released into the cage, which was then covered with
Þne-mesh screening and secured by a pair of rubber
bands. Three cylindrical cages per population treatment were placed into the environmental chambers
with cool (25⬚C), moderate (28⬚C), and warm (33⬚C)
climate conditions (Fig. 1). Hence, this allowed an
assay of all population treatments at each of the three
temperatures. After 24 h, the females were removed
from the cages and the number of eggs deposited on
the top and lower leaf surfaces of each plant was
recorded with the aid of a microscope. This assay was
repeated four times.
Egg Hatch and Nymphal Survival Assays. A laboratory experiment on the effects of temperature on
egg hatch, nymphal survival, and survival to the adult
stage by B. tabaci was conducted, using the three
whiteßy population treatments. Three collard seedlings were placed in each Þne-mesh-covered cage as
described in Insects and Plants. A random sample of 10
adult female B. tabaci was collected from each respective treatment chamber and released in separate
mesh-covered cages containing collard seedlings as
described in Insects and Plants. Three cages per treatment were used and set up within the environmental
chambers with respective temperatures of 25, 28, and
33⬚C. The females were removed following an ovipo-
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sitional period of 24 h. Eggs on the upper and lower
leaf surfaces were counted under a microscope. To
minimize additional duration of exposure to laboratory conditions, only one cage was removed at a time
from a given treatment chamber for all developmental
stage counts and then returned to its respective chamber. A red dot (made with a Þne-point permanent
marker; Sharpie, Series No. 30000; Stanford Corporation, Bellwood, IL) was used to designate the location
on leaves near a given egg for simplicity of reexamination. Egg hatch was monitored daily. Survival to the
adult stage was determined based on the number of
empty pupal cases present. This experiment was repeated four times.
Adult Body Size. Random samples of 100 live
mixed-gender adult whiteßies from each of the three
base populations were aspirated and placed in a vial
containing ethyl alcohol. The whiteßies were then
pipetted into a 10-depression glass plate and examined
with a Zeiss Axio Zoom.V16 microscope (Carl Zeiss
Microscopy GmbH, Jena, Germany). Size and gender
were determined at a 20⫻ magniÞcation, and measurements were performed within the default Axiovision desktop Zeiss microscope software program.
Ten adult males and 10 adult females from each base
population were randomly chosen and measured.
Length measurements were determined from the vertex of the head to the tip of the genitalia. Width was
determined by measuring laterally across the middle
of the thorax. This procedure was repeated Þve times
early during the study and three times solely using
females about a year after the Þrst Þve replicates were
done.
An additional experiment was conducted on the
three base populations to assay the effects of climate
change on adult body size of the Þrst generation (F1)
of whiteßy offspring. Three random samples of 10
female adult whiteßies from each of the three base
populations were aspirated and placed in separate
mesh-covered cylindrical cages within each of the
cool, moderate, and warm climate conditions as described in Insects and Plants (Fig. 1). Each cage contained three 2Ð3 leaf collard seedlings. After 24 h, all
adults were removed from the plants, and the infested
caged plants were held to allow complete adult emergence. The resulting live adult whiteßies from each
population were then aspirated and measured under
the microscope as described above in Adult Body Size
section. Randomly, 10 female adults were chosen for
length measurements. This experiment was repeated
four times.
Plant Quality. Three random samples of ⬇225 collard seedlings at the 3Ð5 leaf stage and 25 d old were
each taken from the insect-free growth chambers. The
cotyledons were removed and the plants were placed
in interlocking plastic bags as described in Insects and
Plants. Each sample of 225 plants was placed into
individual whiteßy-free BugDorm cages within separate environmental treatments of 25, 28, and 33⬚C.
Approximately 75 seedlings were removed thereafter
from each environmental chamber at 15-d intervals,
with the Þnal sample at 45 d. This sample period
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
allowed an assessment of plant quality over a time in
excess of a complete generation of whiteßy reproduction for insects held at all of the above-described
environments. Once the predetermined interval was
reached, plants were removed from environmental
chambers at the same time of day and all above-ground
plant mass was removed with scissors. Individual
plants were assigned a sample number, weighed,
and placed into 5.7 by 8.9 cm No. 1 coin envelopes
(Quality Park Products, St. Paul, MN). Plants were
dried in an oven (model #13-261-28A; Fisher, Hampton, NH) at 60⬚C for 48 h. Upon removal, the dry
weight of each plant was recorded. Plants were then
randomly sorted into groups of Þve, composing one
sample for a given combination of temperature treatment and duration. Relative water content for collard
seedlings within all treatment combinations was calculated. Once individually weighed, each sample was
Þnely ground by hand with a mortar and pestle in
preparations for measurements of nonstructural carbohydrate (NSC) concentrations including the individual components of glucose, sucrose, and fructose.
Assays for NSC concentrations were performed using
a microplate enzymatic assay method described by
Zhao et al. (2010), and this entailed using a test-tubescale glucose kit (GAHK-20) and ethanol-based solutions. Total NSC assays were performed on 10 samples
for each combination of temperature treatment and
duration.
Carbon Dioxide Assay. A laboratory assay concerning the effects of elevated CO2 levels on select life
history parameters of B. tabaci was performed. Five
collard seedlings were established in 10-cm-diameter
pots as described in Insects and Plants and placed
within two cages that were located on a portable
three-level aluminum laboratory bench. A ßuorescent
lighting Þxture (Underwriters Laboratories, Northbrook, IL) containing four 32-W bulbs as previously
mentioned was horizontally mounted 20 cm above the
cages. A T100 series electromechanical time switch
(Intermatic Inc., Spring Grove, IL) was used to establish a photoperiod of 16:8 (L:D) h cycle. Because
temperature of the laboratory ranged from 21 to 23⬚C,
a remote-controlled commercial propagation heating
pad (International Greenhouse Company, Danvile,
IL) was placed under the cages and was used to maintain a moderate environment of 28 ⫾ 0.02⬚C for the
ambient CO2 treatment and 28 ⫾ 0.01⬚C for the enriched CO2 treatment (Table 1). Mean relative humidities for the ambient and enriched treatments
were 30.3 ⫾ 0.1 and 30.8 ⫾ 0.1%, respectively, resulting
in a VPD of 2.6 kPa throughout the experiment (Table
1). The cages consisted of a 45 by 45 by 46 cm Plexiglas
container, with one 30 by 40 cm hinged door and two
4-cm-diameter openings covered by Þne mesh for
ventilation. One cage was used as a control with a CO2
level of 424 ⫾ 0.34 ppm, while an enriched CO2 treatment cage was maintained at a CO2 level of 753 ⫾ 3.03
ppm (Table 1). Four cages were used to rotate treatment conditions randomly throughout the experiment. The enriched CO2 treatment cage was supplied
with CO2 from a compressed CO2 gas tank. CO2 air-
Vol. 107, no. 5
ßow into the cage was administered by a set of Titan
Controls (Sunlight Supply Inc., Vancouver, WA) instruments consisting of an Atlas-3 dayÐnight CO2 monitor and controller and a CO2 greenhouse regulator.
For CO2 transfer, a 0.64-cm-diameter clear plastic tubing connected to the regulator was inserted into the
top of the cage and cotton Þber was used to seal the
hole for the tube. A Boston 10.2-cm personal fan (ElmerÕs Products Inc., Westerville, OH) was placed
within each cage to allow for adequate circulation and
ventilation. Within each cage, in situ CO2 levels were
monitored using a Telaire 7001 digital monitor and
recorder (Telaire, Goleta, CA) and Hobo recorder
(Onset Corporation, Bourne, MA). Temperature and
relative humidity measurements were monitored with
a separate Hobo recorder. Oviposition, egg hatch, and
nymphal survival assays were performed for each CO2
treatment as previously described. This experiment
was repeated Þve times.
Statistical Analyses. All data were analyzed with
SAS version 9.3 (SAS Institute 2012, Cary, NC). Fixed
effects within laboratory assays relating to host plant
quality and whiteßy reproduction were temperature,
CO2, VPD, and time (plants). Dependent variables
within these assays were the number of eggs deposited, egg hatch, immature survival, net reproductive
rate, body size, plant water content, and total NSC
(plants). Oviposition data within assays on oviposition
and immature survival were combined in the analyses
for either temperature effect or CO2 effect. All analyses performed on insect variables excluded plants
that did not contain eggs. In addition, unhatched eggs
were excluded in determining any effects upon
nymphal survival. Percentage data on egg hatch and
immature survival were arcsine-transformed before
the analysis, but the results are presented on backtransformed data. SigniÞcantly different means for
these data were separated using the StudentÐNewmanÐKeuls test. Body size for F1 adult females were
analyzed separately from the base population data. All
data, excluding assays involving CO2 and the assay
comparing base population body size, were further
analyzed by using the MIXED procedure. No statistical test was performed for any possible effects because of environmental chamber rotations during the
study; however, there was very little variation among
conditions within environmental chambers (Table 1).
Results
Temperature Effects on B. tabaci Reproduction.
The number of eggs deposited by the three populations of B. tabaci was signiÞcantly affected by temperature (F ⫽ 5.63; df ⫽ 2, 419; P ⬍ 0.0038). Within
populations reared at 25 and 28⬚C, oviposition tended
to increase as temperature increased (Fig. 2A). There
was not a case in which a whiteßy population deposited the highest average number of eggs within the
temperature where it had been reared for multiple
generations. Populations that were acclimated to 25,
28, and 33⬚C (P25, P28, and P33) were responsible for
depositing signiÞcantly different (F ⫽ 5.19; df ⫽ 2, 419;
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CURNUTTE ET AL.: CLIMATE CHANGE AND B. tabaci
937
Fig. 2. Mean ⫾ SEM (A) number of eggs per collard plant by 10 females during 24 h, (B) percentage egg hatch, (C)
percentage nymphal survival, and (D) net reproductive success of B. tabaci in three different temperatures by three
populations of whiteßies. Means with different letters within a population are signiÞcantly different at P ⬍ 0.05 (StudentÐ
NewmanÐKeuls test). Note: No means within Fig. 2B are signiÞcantly different.
P ⬍ 0.0059) means of 12.6, 14.0, and 9.3 eggs per plant
across all temperature treatments, respectively. Egg
hatch success was ⬎89% in all temperature treatments,
but temperature did not have a signiÞcant effect on
egg hatch per plant (F ⫽ 0.05; df ⫽ 2, 192; P ⬍ 0.952;
Fig. 2B). However, there was a signiÞcant population
effect (F ⫽ 4.61; df ⫽ 2, 192; P ⬍ 0.011), with P25
having the highest egg hatch success across all temperature treatments.
Temperature had a signiÞcant effect on nymphal
survival (F ⫽ 38.4; df ⫽ 2, 178; P ⬍ 0.0001). Differences
of up to 44.5% were observed in the success of
nymphal survival when undergoing development
within the cool and warm temperature environments
(Fig. 2C). A signiÞcant negative correlation (r ⫽
⫺0.516; df ⫽ 190; P ⬍ 0.0001) was seen between
nymphal survival to the adult stage and temperature.
When considering the number of adults produced
from the entire set of eggs (net reproduction; Fig. 2D),
the pattern of variation was similar to nymphal survival
(Fig. 2C). There was a signiÞcant negative correlation
between temperature and net reproduction (r ⫽
⫺0.473; df ⫽ 192; P ⬍ 0.0001). Whiteßy development
was favored by the cool (25⬚C) or the moderate
(28⬚C) temperatures (Fig. 2D), with 28⬚C being the
most favorable treatment. On average, the warm temperature regime (33⬚C) yielded less than one adult per
two eggs laid in all populations. Peak success for net
reproduction occurred when P25 was reared at 28⬚C
(81% survival). Decreases in temperature generally
allowed for higher reproductive success for a given
population. This was especially evident within P33, as
net reproductive success nearly doubled in a temperature that was 8⬚C cooler than the temperature in
which it was acclimated (Fig. 2D). Overall, offspring
survival from the egg to adult stage varied signiÞcantly
owing to temperature (F ⫽ 27.9; df ⫽ 2, 180; P ⬍
0.0001), but no population effect was observed (F ⫽
0.59; df ⫽ 2, 180; P ⬎ 0.590). In all circumstances, net
reproductive success was greater in a different temperature than in the temperature in which the populations were reared for at least Þve generations.
Body Size. A strong degree of sexual size dimorphism was present within each of the B. tabaci treatment populations. Body length decreased with increasing temperature in both adult male (F ⫽ 9.13;
df ⫽ 2, 149; P ⬍ 0.0002) and adult females (F ⫽ 37.0;
df ⫽ 2, 149; P ⬍ 0.0001; Fig. 3A). The maximum observed body length for males (0.94 mm) and females
(1.12 mm) were observed in populations assayed
within the cool temperature regime of 25⬚C. Moreover, temperature had a signiÞcant effect on body
width for both adult males (F ⫽ 8.36; df ⫽ 2, 149; P ⬍
0.0004) and adult females (F ⫽ 5.18; df ⫽ 2, 149; P ⬍
0.0067). An assessment of female body length of the
population treatments ⬇1 yr after the initial assess-
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Vol. 107, no. 5
Fig. 3. Mean ⫾ SEM (A) length and (B) width of adult males and females, and (C) length of F1 adult female B. tabaci
populations adapted to three different temperature regimes reared on collard plants. Means with different letters across
populations for a given gender represent signiÞcant differences at P ⬍ 0.05 (StudentÐNewmanÐKeuls test).
ment was similar (P25, P28, and P33 were 0.94, 0.92,
and 0.87 mm, respectively) compared with the initial
length estimate for females (Fig. 3A).
Results from the assay performed to determine
whether population or temperature affect the body size
of the F1 generation of adults indicated a similar trend to
that of the base population data (Fig. 3C). Temperature
had a signiÞcant effect (F ⫽ 40.5; df ⫽ 2, 915; P ⬍ 0.0001)
upon adult female body length. There was a negative
correlation (r ⫽ ⫺0.26; df ⫽ 927; P ⬍ 0.0001) between
body length and ambient temperature. The greatest
mean length measurement was for the P25 offspring
(0.92 mm) within its familiar temperature of 25⬚C.
Within their respective temperature treatments, mean
female body length of cool and moderate whiteßy population treatments decreased 0.06 and 0.05 mm, respec-
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CURNUTTE ET AL.: CLIMATE CHANGE AND B. tabaci
Fig. 4. Mean ⫾ SEM microgram of total NSC (nonstructual carbohydrates), sucrose, fructose and glucose content
per gram collard plant tissue at different temperatures over
time (starting age of plants is 25 d). All data on the y-axes are
not on the same scale.
tively, within the F1 generations. There was no differ-
939
ence in mean body length for the P33 population F1
offspring. In addition, there was a signiÞcant replication
effect (F ⫽ 24.6; df ⫽ 3, 915; P ⬍ 0.0001).
Plant Quality. Percent water content of collard
above-ground plant matter varied by time (F ⫽ 92.3;
df ⫽ 2, 72; P ⬍ 0.0001) and temperature (F ⫽ 33.8; df ⫽
2, 72; P ⬍ 0.0001). Mean water content in each of the
15-, 30-, and 45-d intervals was 83.6, 85.0, and 76.3%,
respectively. In addition, a signiÞcant time ⫻ treatment interaction effect was observed (F ⫽ 17.91; df ⫽
4, 72; P ⬍ 0.0001). Analyses of all temperature and
duration combinations revealed that 28⬚C was the
most favorable temperature for water retention.
Total NSCs varied across treatment temperatures
and exposure time; yet, some trends were evident. For
glucose and total NSC, there is evidence of an undulation as concentrations decreased from day 15 to day
30, followed by a subsequent increase at day 45 (Fig.
4). However, statistical differences observed in mean
glucose concentrations were solely due to differences
in time of development (F ⫽ 7.43; df ⫽ 2, 72; P ⬍
0.0012). Fructose and sucrose concentrations were
similar as the exposure time at each temperature increased (Fig. 4). Fructose concentrations contributed
the least to the total volume of NSC and were similar,
but were signiÞcantly affected by both treatment duration (F ⫽ 3.42; df ⫽ 2, 72; P ⬍ 0.038) and temperature
(F ⫽ 3.39; df ⫽ 2, 72; P ⬍ 0.039; Fig. 4). Sucrose
concentrations were also signiÞcantly affected by
both treatment duration (F ⫽ 17.9; df ⫽ 2, 72; P ⬍
0.0001) and temperature (F ⫽ 4.41; df ⫽ 2, 72; P ⬍
0.0155; Fig. 4). The lowest observed total concentrations of total NSC occurred when the duration of
treatment lasted 30 d at 25⬚C (28.6 ␮g/g tissue), while
15 d at 28⬚C yielded the highest concentrations (46.7
␮g/g tissue). Time of exposure had a signiÞcant effect
upon total NSC concentrations (F ⫽ 6.1; df ⫽ 2, 72; P ⬍
0.0036), but not temperature (F ⫽ 0.89; df ⫽ 2, 72; P ⬎
0.4177).
Effects of CO2 on B. tabaci Reproduction. CO2 did
not signiÞcantly affect the life history of B. tabaci (Fig.
5). Oviposition within cages of ambient and enriched
Fig. 5. Mean ⫾ SEM success rates (%) for selected reproductive parameters of B. tabaci within cages containing an
ambient (⬇425 ppm) or elevated (⬇750 ppm) CO2 concentration held on caged collard plants located on laboratory benches
at 28.1 ⫾ 0.02⬚C. Means are not signiÞcantly different at P ⬎ 0.05 (StudentÐNewmanÐKeuls test).
940
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
CO2 were not signiÞcantly different (F ⫽ 0.08; df ⫽ 1,
30; P ⬍ 0.784). Mean oviposition over a 24-h period in
the ambient environment was 18.6 ⫾ 3.1 eggs per
plant, while the enriched environment yielded a mean
of 18.7 ⫾ 2.8 eggs per plant. Mean egg hatch (⬇ 90%)
also was unaffected by CO2 concentrations (F ⫽ 0.16;
df ⫽ 1, 14; P ⬍ 0.698). Results pertaining to nymphal
survival to the adult stage and the success of offspring
to complete the life cycle from egg to adult (net
reproductive rate) were similar. However, neither
nymphal survival to the adult stage (F ⫽ 0.08; df ⫽ 1,
13; P ⬎ 0.780) or net reproduction (F ⫽ 0.01; df ⫽ 1,
14; P ⬎ 0.905) were signiÞcantly different between
treatments (Fig. 5).
Discussion
As the climate continues to change, it is essential
that the scientiÞc and agricultural community understand its ramiÞcations on pests. Earlier reports, including Butler et al. (1983), Verma et al. (1990), and Wang
and Tsai (1996), indicated that development by B.
tabaci may be optimal at ⬇27⬚C. More recent studies
have focused on developing up-to-date thermal tolerance and threshold values, with results suggesting
that favorable temperatures for B. tabaci development
may be closer to 32⬚C (Muniz and Nombela 2001,
Bonato et al. 2007). Among the temperatures in our
study, 28⬚C yielded the highest reproductive success
for B. tabaci. Consistent with several previous studies
(Butler et al. 1983, Muniz and Nombela 2001, NavaCamberos et al. 2001), decreases in success were observed with increasing temperatures. Nymphal survival (36%) at 33⬚C on collard was lower than that seen
by Nava-Camberos et al. (2001) on two cotton cultivars at 32⬚C (48%). It has been recognized that 33⬚C
is near the sublethal temperatures that whiteßies endure (Muniz and Nombela 2001, Guo et al. 2012). A
study by Guo et al. (2012) examined B. tabaci for up
to Þve generations at four separate temperatures.
Their results indicated that although the rate of survival between the Þrst two generations was the same
for temperatures between 27 and 35⬚C, the survival
rate was signiÞcantly different among the third to Þfth
generations. This suggests that long-term exposure to
these higher temperatures may have decreased Þtness
for these populations.
In the current study, using population data from up
to ⬇30 generations, the Þtness of the P33 whiteßy
population at lower temperatures (25 and 28⬚C) was
reduced as compared with the populations adapted to
these lower temperatures. Evidence of this is supported by a comparison of Þtness across the three
populations at the cool and moderate temperatures of
25 and 28⬚C, respectively. The P33 population maintained the capability of successfully reproducing at
higher levels within cooler temperatures, yet, Þtness
levels were still not up to par with those of P25 and P28
in the same temperatures (Fig. 2D). In no circumstance did the whiteßy population have the highest
level of reproductive capability within the temperature in which it had been reared. Thus, treatment
Vol. 107, no. 5
populations did not maintain higher Þtness levels
within temperatures in which they were previously
acclimated.
The frequency, duration, and extremity of cold
snaps and heat waves are predicted to be altered
(Intergovernmental Panel on Climate Change 2007).
As weather events are likely to vary by location, climate data will demand attention when researchers
attempt to model whiteßy population dynamics. An
8⬚C (25Ð33⬚C) rise in temperature can be depicted as
one example of a predicted short-term heat event. In
a simulation of this event, we observed increases in
oviposition of up to 35% (Fig. 2A). An increase in the
number of eggs may allow for a higher number of
adults to be produced within areas of similar climate
patterns that were simulated in this study. Conversely,
decreases in temperature yielded higher levels of reproductive success in populations acclimated to 33⬚C
(Fig. 2D). When experiencing the higher temperature
of 33⬚C, populations acclimated to 25 and 28⬚C maintained over a 40% reproductive success rate, but it is
unknown how subsequent generations may have performed. At higher temperatures, the data suggest a
beneÞt from one or more aspects of reproduction
within whiteßy communities. Hence, the optimal temperature for B. tabaci reproduction may fall between
28 and 33⬚C. Further studies are needed to explore the
acclimation responses of whiteßy populations to rapid
changes in temperature over time, as well as short- and
long-term population effects of B. tabaci exposure to
high temperatures as these factors may play a large
part in future management decisions.
Consistent with previous whiteßy studies (Perring
et al. 1993, Brown et al. 1995, De Barro et al. 2000a,b),
sexual size dimorphism and a negative correlation
with increasing temperatures was present within all
treatment populations (Fig. 3AÐC). VPD may have
had a role on body size, although this affect was not
directly measured in this study. Increases in temperature, as well as decreases in humidity, at otherwise
similar environments increased the ambient VPD (Table 1). Simmons and Mahroof (2011) studied the effect of VPD on B. tabaci reproduction under various
levels (0.5Ð2.7 kPa). They concluded that increases in
VPD signiÞcantly decreased body size of both F1 and
F2 generations and limited reproductive success. At
33⬚C, body size and reproductive success of each
whiteßy population was signiÞcantly reduced by
higher VPD. However, we found that longer exposures to a high temperature did not further suppress
body size. Decreases in overall body size may be
correlated with reductions in overall performance and
Þtness (Simmons and Mahroof 2011). Any relationship between body size and Þtness within B. tabaci
populations requires further investigation.
Temperature can affect the relationship between an
herbivore and its host plant by inßuencing the performance of either organism. Herbivores often avoid
water-stressed plants (Waring and Cobb 1992), as
plant water-stress can affect numerous interactions
with insects (Holtzer et al. 1988). Adequate water
availability within plants is beneÞcial for most herbiv-
September 2014
CURNUTTE ET AL.: CLIMATE CHANGE AND B. tabaci
orous insects because it aids in the digestion and assimilation of nutrients, particularly nitrogen (Scriber
1984). Data herein support that water content within
plants was relatively constant until the 45 d sample.
However, the observed decrease may have had only a
minor impact because adult emergence was completed within 30 d for most of the whiteßies.
Plant quality, including physical and chemical properties, is an essential component in determining insect
population dynamics. There is solid evidence that host
plant type affects B. tabaci life history (Greathead
1986, Simmons 1994, Drost et al. 1998, Nava-Camberos
et al. 2001, Simmons et al. 2008). Within the plant
quality assay herein, the variability in quality of collard
plants across treatments may have been owing to a
period of rapid growth for the seedlings (Fig. 4).
However, we do not suspect plant quality among treatments had a signiÞcant impact on whiteßy reproduction. B. tabaci has been observed to regulate carbohydrate intake contingent on the available concentration
within the plant source (Salvucci et al. 1997). With evidence of whiteßies performing better in lower temperatures in combination with total NSC concentrations
exhibiting similar concentration throughout the assay,
NSC availability may not have been a limiting factor to
whiteßy performance within this study.
Results from our study did not support an impact of
CO2 enrichment on whiteßy oviposition and reproduction over a single generation. This observation is
common in the literature. Many studies have concluded that CO2 enrichment did not affect the life
history of hemipterans (e.g., Butler et al. 1983, Diaz et
al. 1998, Held et al. 2001, Hughes and Bazzaz 2001,
Chong et al. 2004). In environments of elevated CO2,
we observed several cases of mortality when developing adults failed to successfully puncture or emerge
from the case (body and wings visible through the
opaque pupae case). It is not known whether a threshold effect may have been present within the latter
stages of instar development in environments of CO2
enrichment. Predicted increases in leaf thickness and
water retention due to increases in CO2 (DeLucia et
al. 2012) may render existing feeding habits of herbivores less efÞcient. In turn, behavior may be altered by
insects to gain adequate nutrient uptake (Legaspi et al.
2011), and it is unknown how these changes may
additionally alter life history of insects in the future.
To achieve comprehensive analyses of whiteßy performance, studies incorporating the use of similar host
plant type, multi-generational, and long-term approaches to examine any direct impacts on life history
to varying levels of temperature and CO2 enrichment
are necessary. In addition, host plant quality and nutrient information should be considered in impacts on
insect performance. Data describing how B. tabaci
communities will respond to changing climate is essential for effective management, and the results contribute to the general understanding of how insects
respond to climate change.
941
Acknowledgments
We thank Bradford Peck, April Bisner, Zachary Powe,
Zanard Choice, Brian Ward, and Shawna Rodgers for their
technical assistance, and D. Michael Jackson and Amnon Levi
for suggestions on earlier versions of the manuscript. This
study was supported by the U.S.-Egyptian Science and Technology Joint Fund (STDF) in cooperation with the U.S.
Department of Agriculture and Egyptian Ministry of Agriculture under Project 3732. This article reports the results of
research only. Mention of a proprietary product does not
constitute an endorsement or a recommendation for its use
by USDA.
References Cited
Abd-Rabou, S., and A. M. Simmons. 2010. Survey of reproductive host plants of Bemisia tabaci (Hemiptera: Aleyrodidae) in Egypt, including new host records. Entomol.
News 121: 456 Ð 465.
Basu, A. N. 1995. Bemisia tabaci (Gennadius): Crop pest and
principal whiteßy vector of plant viruses. Westview Press,
Boulder, CO.
Bezemer, T. M., and T. H. Jones. 1998. Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82: 212Ð222.
Bezemer, T. M., K. J. Knight, J. E. Newington, and T. H. Jones.
1999. How general are aphid responses to elevated atmospheric CO2? Ann. Entomol. Soc. Am. 92: 724 Ð730.
Bonato, O., A. Lurette, C. Vidal, and J. Fargues. 2007. Modeling temperature-dependent bionomics of Bemisia
tabaci (Q-biotype). Physiol. Entomol. 32: 50 Ð55.
Brown, J. K. 1994. Current status of Bemisia tabaci as a plant
pest and virus vector in agroecosystems worldwide. FAO
Plant Prot. Bull. 42: 3Ð32.
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:
511–534.
Butler Jr., G. D., 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: 310 Ð313.
Byrne, D. N., T. S. Bellows Jr., and M. P. Parrella. 1990.
Whiteßies in agricultural systems, pp. 227Ð261. In D. Gerling (ed.), Whiteßies: their bionomics, pest status, and
management. Intercept Ltd., Andover, Hants, United
Kingdom.
Chong, J., M. van Iersel, and R. D. Oetting. 2004. Effects of
elevated carbon dioxide levels and temperature on the
life history of the Madeira mealybug (Hemiptera:
Pseudococcidae). J. Entomol. Sci. 39: 387Ð397.
De Barro, P. J., F. Driver, I. D. Naumann, G. M. Clarke, S.
Schmidt, and J. Curran. 2000a. Descriptions of three
species of Eretmocerus Haldeman (Hymenoptera: Aphelinidae) parasitizing Bemisia tabaci (Gennadius)
(Hemiptera: Aleyrodidae) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in Australia based on morphological and molecular data. Austral.
J. Entomol. 39: 259 Ð269.
De Barro, P. J., P. J. Hart, and R. Morton. 2000b. The biology
of two Eretmocerus spp. Haldeman and three Encarsia
spp. Forster and their potential as biological control
agents of Bemisia tabaci biotype B in Australia. Entomol.
Exp. Appl. 94: 91Ð102.
DeLucia, E. H., P. D. Nabity, J. A. Zavala, and M. R. Berenbaum. 2012. Climate change: resetting plant-insect interactions. Plant Physiol. 160: 1677Ð1685.
942
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Diaz, S., L. H. Fraser, J. P. Grime, and V. Falczuk. 1998. The
impact of elevated CO2 on plant-herbivore interactions:
experimental evidence of moderation effects at the community level. Oecologia 117: 177Ð186.
Dinsdale, A., L. Cook, C. Riginos, Y. M. Buckley, and P. J. De
Barro. 2010. ReÞned global analysis of Bemisia tabaci
(Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann. Entomol. Soc. Am.
103: 196 Ð208.
Drost, Y. C., J. C. van Lenteren, and H.J.W. Roermund. 1998.
Life history parameters of different biotypes of Bemisia
tabaci (Hemiptera: Alelyrodidae) in relation to temperature and host plants: a selective review. Bull. Entomol.
Res. 88: 219 Ð230.
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.
Greathead, A. H. 1986. Host plants. In M.J.W. Cock (ed.),
Bemisia tabaci: a literature survey on the cotton whiteßy
with an annotated bibliography, pp. 17Ð25. CAB International Institute of Biological Control, Ascot, United
Kingdom.
Guo, J., L. Cong, Z. Zhong-Shi, and W. Fang-Hao. 2012.
Multi-generation life tables of Bemisia tabaci (Gennadius) Biotype B (Hemiptera: Aleyrodidae) under hightemperature stress. Environ. Entomol. 41: 1672Ð1679.
Hamilton, J. G., A. R. Zangerl, M. R. Berenbaum, J. Pippen,
M. Aldea, and E. H. DeLucia. 2004. Insect herbivory in
an intact forest understory under experimental CO2 enrichment. Oecologia 138: 566 Ð573.
Hance, T., J. van Baaren, P. Vernon, and G. Boivin. 2007.
Impact of extreme temperatures on parasitoids in a climate change perspective. Annu. Rev. Entomol. 52: 107Ð
126.
Held, D. W., D. A. Potter, R. S. Gates, and R. G. Anderson.
2001. ModiÞed atmosphere treatments as a potential disinfestation technique for arthropod pests in greenhouses.
J. Econ. Entomol. 94: 430 Ð 438.
Holtzer, T. O., T. L. Archer, and J. M. Norman. 1988. Host
plant suitability in relation to water stress, pp. 11Ð138. In
E. A. Heinrichs (ed.), Plant stress-insect interactions.
Wiley, New York, NY.
Horowitz, A. R., S. Konstedalov, V. Khasdan, and I. Ishaaya.
2005. Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance.
Arch. Insect Biochem. Physiol. 58: 215Ð225.
Hughes, L., and F. A. Bazzaz. 2001. Effects of elevated CO2
on Þve insect-plant interactions. Entomol. Exp. Appl. 99:
87Ð96.
Intergovernmental Panel on Climate Change. 2007. Summary for policymakers. In S. Solomon, D. Qin, M. Manning, A. Chen, M. Marquis, K. B. Averyt, M. Tignor, and
H. L. Miller (eds.), Climate change 2007: the physical
science basis. Contribution of Working Group I to the
Fourth Assessment Report of the Intergovernmental
Panel on Climate Change. Cambridge University Press,
Cambridge, United Kingdom and New York.
Jones, D. R. 2003. Plant viruses transmitted by whiteßies.
Eur. J. Plant Pathol. 109: 195Ð219.
Legaspi, J. C., B. C. Legaspi, Jr., and A. M. Simmons. 2011.
Recent research trends in the use of predators for biological control, pp. 95Ð122. In N. M. Rosas-Garcia (ed.),
Biological control of insect pests. Stadium Press, Houston,
TX.
Vol. 107, no. 5
Lopez-Avila, A. 1986. Taxonomy and biology, pp. 3Ð11. In
M. J. Cock (ed.), Bemisia tabaci; a literature survey on the
cotton whiteßy with an annotated bibliography. International Institute of Biological Control, Chameleon Press,
London, United Kingdom.
Martin, J. H. 1987. An identiÞcation guide to common
whiteßy pest species of the world (Homoptera: Aleyrodidae). Trop. Pest Manage. 33: 298 Ð322.
Martin, J. H., and L. A. Mound. 2007. An annotated check
list of the worldÕs whiteßies (Insecta: Hemiptera: Aleyrodidae). Zootaxa 1492: 1Ð 84.
McKenzie, C. L., P. K. Anderson, and N. Villarreal. 2004. An
extensive survey of Bemisia tabaci (Homoptera: Aleyrodidae) in agricultural ecosystems in Florida. Fla. Entomol. 87: 403Ð 407.
Muniz, M., and G. Nombela. 2001. Differential variation in
development of the B- and Q- biotypes of Bemisia tabaci
(Homoptera: Aleyrodidae) on sweet pepper at constant
temperatures. Environ. Entomol. 30: 720 Ð727.
Naranjo, S. E., S. J. Castle, P. J. De Barro, and S. S. Liu. 2010.
Population dynamics, demography, dispersal and spread
of Bemisia tabaci, pp. 185Ð226. In P.A. Stansly and S.E.
Naranjo (eds.), Bemisia: bionomics and management of a
global pest. Springer, Dordrecht, The Netherlands.
National Oceanic and Atmospheric Administration. 2013.
Carbon dioxide at NOAAÕs Mauna Loa Observatory
reaches new milestone: tops 40 ppm. Earth System Research Laboratory, National Oceanic and Atmospheric
Administration. 10 May 2013. (http://www.esrl.noaa.
gov/news/2013/CO2400/) (accessed 15 June 2013).
Nava-Camberos, U., D. G. Riley, and M. K. Harris. 2001.
Temperature and host plant effects on development, survival, and fecundity of Bemisia argentifolii (Homoptera:
Aleyrodidae). Environ. Entomol. 30: 55Ð 63.
Oliveira, M.R.V., T. J. Henneberry, and P. Anderson. 2001.
Host, current status, and collaborative research projects
for Bemisia tabaci. Crop Prot. 20: 709 Ð723.
Parmesan, C. 2006. Ecological and evolutionary responses
to recent climate change. Annu. Rev. Ecol. Syst. 37: 637Ð
669.
Perring, T. M., A. D. Cooper, R. J. Rodriguez, C. A. Ferrar,
and T. S. Bellows. 1993. IdentiÞcation of a whiteßy species by genomic and behavioral studies. Science 259:
74 Ð77.
Porter, J. H., M. L. Parry, and T. R. Carter. 1991. The potential effects of climate change on agricultural insect
pests. Agric. For. Meteor. 57: 221Ð240.
Prabhaker, N., D. L. Coudreit, and D. E. Meyerdirk. 1985.
Insecticide resistance in the sweetpotato whiteßy, Bemisia tabaci (Homoptera: Aleyrodidae). J. Econ. Entomol.
78: 748 Ð752.
Robinson, E. A., G. D. Ryan, and J. A. Newman. 2012. A
meta-analytical review of the effects of elevated CO2 on
plant-arthropod interactions highlights the importance of
interacting environmental and biological variables. New
Phytol. 194: 321Ð336.
Salvucci, M. E., G. R. Wolfe, and D. L. Hendrix. 1997. Effect
of sucrose concentration on carbohydrate metabolism in
Bemisia argentifolii: Biochemical mechanism and physiological role for trehalulose synthesis in the silverleaf
whiteßy. J. Insect Physiol. 43: 457Ð 464.
SAS Institute. 2012. SAS/STAT version 9.3. SAS Institute,
Cary, NC.
Scriber, J. M. 1984. Host plant suitability, pp. 159 Ð202. In:
R. T. Carde and W. J. Bell (eds.), Chemical ecology of
insects. Chapman & Hall, London, United Kingdom.
September 2014
CURNUTTE ET AL.: CLIMATE CHANGE AND B. tabaci
Simmons, A. M. 1994. Oviposition on vegetables by Bemisia
tabaci (Homoptera: Aleyrodidae): temporal and leaf surface factors. Environ. Entomol. 23: 382Ð389.
Simmons, A. M., and K. D. Elsey. 1995. Overwintering and
cold tolerance of Bemisia argentifolii (Homoptera: Aleyrodidae) in coastal South Carolina. J. Entomol. Sci. 30:
497Ð506.
Simmons, A. M., and R. M. Mahroof. 2011. Response of
Bemisia tabaci (Hemiptera: Aleyrodidae) to vapor pressure deÞcit: Oviposition, immature survival, and body
size. Ann. Entomol. Soc. Am. 104: 928 Ð934.
Simmons, A. M., H. F. Harrison, and K. S. Ling. 2008. Fortynine new host plant species for Bemisia tabaci (Hemiptera:
Aleyrodidae). Entomol. Sci. 11: 385Ð390.
Stiling, P., and T. Cornelissen. 2007. How does elevated
carbon dioxide (CO2) affect plant- herbivore interactions? A Þeld experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob. Chang. Biol. 13: 1823Ð1842.
United States Global Climate Research Program. 2009.
Global climate change impacts in the United States. In
R. K. Thomas, M. M. Jerry, and C. P. Thomas (ed.), United
States Global Change Research Program. Cambridge University Press, New York, NY.
943
Verma, A. K., S. S. Ghatak, and S. Mukhopadhyay. 1990.
Effect of temperature on development of whiteßy (Bemisia tabaci) (Homoptera: Aleyrodidae) in West Bengal.
Indian J. Agric. Sci. 60: 389 Ð399.
Wang, K., and J. H. Tsai. 1996. Temperature effect on development and reproduction of silverleaf whiteßy (Homoptera: Aleyrodidae). Ann. Entomol. Soc. Am. 89: 375Ð
384.
Ward, J. K., and J. K. Kelly. 2004. Scaling up evolutionary
responses to elevated CO2; lessons from Arabidopsis.
Ecol. Lett. 7: 427Ð 440.
Waring, G. L., and N. S. Cobb. 1992. The impact of plant
stress on herbivore population dynamics, pp. 167Ð226. In
E. A. Bernays (ed.), Insect-plant interactions, vol. 4. CRC,
Boca Raton, FL.
Zhao, D., C. T. MacKown, P. J. Starks, and B. K. Kindiger.
2010. Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays. Crop Sci. 50: 1537Ð1545.
Zvereva, E. L., and M. V. Kozlov. 2006. Consequences of
simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta-analysis.
Glob. Chang. Biol. 12: 27Ð 41.
Received 13 September 2013; accepted 8 July 2014.