Influence of Temperature on Reproduction~ Development~ and

Intrinsic Rate of Increase of Russian Wheat Aphid~

Greenbug~ and Bird Cherry-Oat Aphid
(Homoptera: Aphididae)

G. J. MICHELS, JR., AND R. W. BEHLE

Texas Agricultural Experiment Station,
Texas A&M Research and Extension Center,
Amarillo, Texas 79106

J. [Link].82(2):439-444(1989)
ABSTRACT The effects of constant (1O"C)and fluctuating (5-15°C and I-19°C) temper-
ature regimes on the reproduction, development, and intrinsic rate of increase of the Russian

Downloaded from [Link] at New York University on September 7, 2015

wheat aphid, Diuraphis noxia (Mordvilko), greenbug, Schizaphis graminum Rondani, and
the bird cherry-oat aphid, Rhopalosiphum padi Fitch, were studied in the laboratory at an
average-temperature regime (1O"C)that is common in the spring when all three of these
aphids are found in small grain fields in the Texas Panhandle. Significant differences in
nymphal development and total lifespan were observed among species within a temperature
regime and among temperature regimes for a species. Natality was highest for D. noxia and
R. padi at 5-15°C; S. graminum natality was highest at I-19°C. Estimates of the intrinsic
rate of increase (r",) for the three aphid species were highest at I-19°C (0.188 for D. noxia,
0.144 for S. graminum, and 0.200 and for R. padi).

KEY WORDS Insecta, Diuraphis noxia, Schizaphis graminum, Rhopalosiphum padi

THE RUSSIAN WHEAT APHID, Diuraphis noxia S. graminum, and R. padi. The three temperature
(Mordvilko), is a recently introduced pest of small regimes chosen for this study reflected the average
grains in the United States. It was officially detected temperature found in the Texas Panhandle during
in the Texas Panhandle in 1986, although there is the spring when these aphids are found in wheat
evidence that it was probably present as early as fields.
1985 (Stoetzel 1987). According to Pakendorf
(1984), D. noxia can cause yield losses in small
Materials and Methods
grains of up to 90% through feeding damage.
Additional information concerning the intro- The studies were done at the Texas Agricultural
duction of D. noxia and the damage it causes has Experiment Station, Amarillo Research and Exten-
been previously addressed by Kieckhefer & Elliott sion Center Agronomy Laboratory at Bushland,
(in press) and Michels & Behle (1988). In the Texas Tex., in 1986 and 1987.
Panhandle, D. noxia occurs on small grains in con- Diuraphis noxia, S. graminum, and R. padi used
junction with other aphid pests, notably the green- in these studies were obtained from stock colonies
bug, Schizaphis graminum Rondani, and the bird that had been reared in a greenhouse on winter
cherry-oat aphid, Rhopalosiphum padi Fitch (Tur- wheat, Triticum aestivum (cv. Scout 66), at ap-
ney & Hoelscher 1986; G.J.M., unpublished data). proximately 20"C and the naturally occurring pho-
Although other recent papers have examined the toperiod. The stock colonies were obtained from
effects of either constant (Michels & Behle 1988) wheat, fields in the Texas Panhandle near Bush-
or fluctuating (Kieckhefer & Elliott in press) tem- land, Tex., in the fall of 1986 and had been main-
peratures on D. noxia development, natality, and tained in the greenhouse for approximately 9 mo
mortality, neither has addressed how these results before the studies began.
relate to the population dynamics of other small Adult aphids from these colonies were removed
grain aphids that normally occur in the fields at from the wheat in the greenhouse and placed in
the same time. To establish proper laboratory pro- Petri dishes containing a wheat leaf ('Scout 66')
cedures for further studies, it would be beneficial whose ends were inserted in moist paper towels,
to compare the effect of constant temperature and following the techniques of Michels et a1. (1987).
temperature ranges that fluctuate about the mean Wheat leaves were changed every 3-4 d. The Petri
of the constant temperature regime. Therefore, to dishes were placed in environmental chambers
elucidate similarities and differences between D. (Percival I30-BLL, Boone, Iowa) at a lOoe con-
noxia and other small grain aphids, we conducted stant, 5-15°e fluctuating, or 1-19°e fluctuating
laboratory experiments to examine the effects of temperature. The fluctuating temperature regimes
fluctuating and constant temperature on D. noxia, were set on a 12-h, square-wave cycle, and the

0022-0493/89/0439-0444$02.00/0
© 1989Entomological
Societyof America
440 JOURNAL OF ECONOMIC ENTOMOLOGY V 01. 82, no. 2

photoperiod was set at 12:12 (L:D). The temper- regime by analyses of covariance procedures in the
ature regimes and photoperiod were selected to GLM and a t test of all combinations of slopes for
reflect the normal average temperature and pho- estimates of a common slope (Steel & Torrie 1960).
toperiod in the Texas Panhandle in the spring when Age-specific survival and age-specific fecundity
all three aphid species are present in wheat fields. were recorded daily. From these data, the follow-
Newly deposited nymphs from these acclimated ing life table statistics (Andrewartha & Birch 1954)
adults were used to begin the studies. Each first were derived: intrinsic rate of increase (r",), net
instar was placed on wheat in a separate Petri dish reproductive rate (Ro), mean generation time (T),
as described above. The Petri dishes were then and mean survival time (MST).
placed in the environmental chambers at the re-
spective temperature regime. Individual nymphs
Results and Discussion
were observed daily for molting and survivorship.
The presence of exuviae was used to determine Development and reproduction were observed
molting. After the aphids reached the adult stage, for all species at all temperature regimes. There
the number of progeny per adult and adult mor- was considerable, expected variation in develop-
tality were recorded daily. There were 50 aphids ment among species and temperature regimes (Ta-

Downloaded from [Link] at New York University on September 7, 2015

per species per temperature regime, run concur- ble 1). There was no significant difference in total
rently. nymphal development time between D. noxia or
Data were analyzed using the SAS Statistical S. graminum at a given temperature regime. Total
Analysis System for Personal Computers, version nymphal development time for R. padi was sig-
6 (SAS Institute 1985). Various procedures and op- nificantly faster than D. noxia or S. graminum at
tions available in the general linear model (GLM) each temperature regime. At 1000e,adult lifespan
(SAS 1985, 433-506) portion of this system were was significantly different for each species, with D.
used for all analyses. The selection of statistical noxia having the shortest duration, followed by R.
methods for analyzing the data followed that of padi and S. graminum. Diuraphis noxia and R.
Ballou et al. (1986). With the exception of the mor- padi had significantly longer adult lifespans than
tality data, which included all individuals reared S. graminum at 5-15°e, and adult lifespan was
at a specific temperature regime, only those indi- similar among all species at I-19°C. The overall
viduals that completed development to the adult total lifespan at a given temperature regime was
stage were included in the analyses. longest for S. graminum at lODe, D. noxia at 5-
Developmental data (each stadium), adult lon- 15°e, and S. graminum at I-19°C.
gevity, and total lifespan of the aphids were ana- Within a species among temperature regimes,
lyzed separately by one-way analyses of variance 5-15°e seemed to be optimal for D. noxia and R.
for all species at each temperature regime and then padi nymphal development and adult lifespan.
for all temperature regimes for each species. Sig- Nymphal development was significantly faster at
nificant means were separated using the Student- 1-19°e for both species. Adult lifespan was signif-
Newman-Keuls multiple range test (P = 0.05). icantly shorter for D. noxia and shorter, although
Variations in natality over time for temperature not significantly so, for R. padi at 10"C. For S.
regimes within a species were analyzed as a fourth- graminum, 1-19°e seemed to be optimal for
order polynomial regression with natality as the nymphal development and adult lifespan. S. gra-
dependent variable and temperature and age as minum nymphs developed significantly faster at
discrete, independent variables. Variations in na- lOoe and adult lifespan was significantly shorter at
tality over time among species at each temperature 5-15°C.
regime and at a composite temperature (mean Least-square means of natality for all three
nymphs per day per species at all regimes) were species are presented in Table 2. No significant
analyzed in the same manner. Temperature re- differences in natality were found across temper-
gimes were assigned as class variables in all anal- ature regimes for D. noxia or R. padi. S. graminum
yses. Temperature effects were analyzed using least- natality was significantly higher at 5-15°e and 1-
squares means to adjust for the polynomial age 19°e than at 10"C. At a specified temperature re-
effects. These means of natality were then sepa- gime, R. padi had significantly higher natality than
rated with options available in the GLM. Age ef- D. noxia. This same difference was reflected in the
fects were analyzed separately and independent composite natality, an average natality of all tem-
comparisons were made of the means within a tem- perature regimes for a species. The natality result
perature regime using the Student-Newman-Keuls for D. noxia at lOoe is very similar to that reported
multiple range test. by Michels & Behle (1988) at lOoe constant tem-
Mortality data were analyzed separately for each perature, 0.90 (±0.20) nymphs per day in this ex-
species at each temperature regime as a simple periment compared with 0.91 (±0.07) nymphs per
linear regression with the percentage of surviving day in the previous research.
adults as the dependent variable and age as the Fig. 1-3 illustrate natality over time for each
independent variable. Separate comparisons of the species and temperature regime. Each species
slopes were made for all temperature regimes with- demonstrated a specific natality pattern that was
in a species and for all species within a temperature discernable across temperature regimes. D. noxia
 April 1989 MICHELS & BEHLE: INFLUENCE OF TEMPERATURE ON SMALL GRAIN APHIDS 441

Table 1. Development of tbree small grain aphids at three temperature regimes

Days in stadia Total Overall

Species nO
1st 2nd 3rd 4th Pre-pupa Nymph Adult total
1O"C
D. nona 15 5.1Aa 5.1Aa 6.0Aa 6.4Aa 5.1Aa 27.7Aa 16.1Cb 43.8Bc
S. gramlnum 33 4.0Ab 4.1 Bb 4.6Bb 5.2Bb [Link] 19.9Ab 33.9Aa 53.8Ab
R. padl 40 3.7Ba 3.4Ca 3.7Cb 4.4Ca 1.4Bb 16.6Ba 25.0Ba 41.6Ba
5-15OC
D. nona 21 4.6Aab 5.4Aa 5.6Aa 6.1Aa 4.9Aa 26.6Aa 35.1Aa 61.8Aa
S. gramlnum 30 4.1Bb 3.4Bc 5.2Aab 6.3Aa 2.1Bb 21.1Aa 21.0Bb 42.1Bc
R. padl 35 3.6Ba 2.3Ca 4.2Ba 3.8Bb 1.9Ba 15.8Ba 29.7Aa 45.6Ba
l-l9OC
D. nona 14 4.0Bb 4.6Aa 4.4Bb 5.5Ba 3.6Ba 22.1Ab 32.2Aa 54.3Ab
S. gramlnum 21 4.6Aa 5.4Aa 5.6Aa 6.1Aa 4.9Aa 26.6Aa 36.3Aa 63.0Aa
R. padl 40 [Link] 2.7Aa 3.1Cc 3.2Cc 0.8Cc 12.0Bb 26.1Aa 37.6Bb

Meansin a column followedby the same upper-case letter are not significantlydifferent among specieswithin a temperature regime.

Downloaded from [Link] at New York University on September 7, 2015

Means in a column followed by the same lower-caseletter are not significantlydifferent among temperature regimes within a species
(P = 0.05, Student-Newman Keuls).
on, number of aphids from original cohort surviving to adult reproductive stage.

had a much "flatter" age-specific natality curve S. graminum, which was significantly higher than
that extended for a much longer period of time D. noxia.
than R. padi, with nymphs being produced for as Life table statistics are found in Table 4. The
long as 90 d. This result is again consistent with intrinsic rate of increase (r oJ can be used as a com-
that reported by Michels & Behle (1988) for D. parative statistic across temperature regimes and
noxia reared at a constant lOGe. R. padi natality species, because it is composed of a number of
was characterized by very high initial natality, factors that contribute to population growth, name-
ranging as high as five nymphs per day, followed ly the net reproductive rate (R.), immature devel-
by an extremely steep drop as the adult population opment rates, and mean generation time (T)
aged, with very few nymphs produced after 40 d. (Kieckhefer & Elliott in press).
Age-specific natality for S. graminum fell between An examination of the factors that compose r m

R. padi and D. noxia. S. graminum produced more gave an indication of the effect of temperature
nymphs per day over time than D. noxia, but did regimes on aphid population growth patterns. The
not have the high initial output found in R. padi. highest r no for all three aphids was found at I-19°C.
S. graminum natality also occurred over a greater Although T for D. noxia increased at5-15°e, when
timespan than R. padi, but not as long as D. noxia. compared with 10"C and 1-19°e, Ro at 5-15°e was
Less variation in day-to-day natality was found much higher than at lOOe or I-19°C. On the other
at 5-15OC for D. noxia and R. padi. S. graminum hand, for S. graminum and R. padi, T decreased
had less day-to-day variation at lOGe. All species
had a high degree of variation in day-to-day na- Table 2. Least square means of natality for three small
tality at 1-19°e. This variation in natality at 1- grain aphids reared at three temperature regimes
19°e was very noticeable for R. padi.
Mortality regressions are found in Table 3. The Avg. nymphs
Tem- per day
Avg. nymphs
t test comparisons of the mortality regression slopes perature
Species per day composite over
declared no significance if the slopes associated regime (±SE) temperature
(OC)
with two regressions were estimates of the same (±SE)"
slope, but did not indicate if the two regressions D. nox/a 10 0.90Ba (0.20) 0.89A (0.03)
being compared were estimates of the same line. 5-15 0.98Ba (0.05)
Therefore, these analyses allowed comparisons of 1-19 0.89Ba (0.05)
the rate of decline in the parent population over S. gramlnum 10 0.97Ba (0.06) 1.36B (0.02)
time. 5-15 1.57Ab (0.07)
The rate of decline for D. noxia was significantly 1-19 1.67Ab (0.07)
more rapid at loGe than at 5-15°e or 1-19°e. The R. padl 10 1.30Aa (0.11) 1.52B (0.07)
rate of decline for S. graminum was significantly 5-15 1.67Aa (0.08)
1-19 1.49Aa (0.10)
slower at 5-15°e than at looe or 1-19°e, and there
were no significant differences in rate of decline Meansin a column followed by the same upper-case letter are
for R. padi at the three temperature regimes. With- not significantlydifferent among speciesat the specifiedtemper-
in a specific temperature regime, D. noxia and R. ature regime. Means in a column followed by the same lower-
case letter are not significantlydifferent among temperature re-
padi had a significantly higher rate of decline than gimes for the specifiedspecies(P = 0.05,Student-Newman-Keuls).
S. graminum at lOGe; at 5-15°e and 1-19°e, R. o Means in a column followed by the same letter are not sig-
padi had a significantly higher rate of decline than nificantly different (P = 0.05, Student-Newman-Keuls).
442 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 82, no. 2

!:i D. noxia 10 C s. graminum 10 C

~ 5

0
:I:
4

Q.
::E 3
>-
Z
W 2
o
~
a:l
o !p 00
W (f>8:? oo{?°J
~ , o 0 0
o
o 10 20 30 40 50 60 70 60 90 100 110 10 20 30 40 50 60 70 60 go 100 110
COHORT AGE IN DAYS COHORT AGE IN DAYS

Downloaded from [Link] at New York University on September 7, 2015

D. noxia 5-15 .C s. graminum 5-15 C

ID ro ~ ~ 00 00 ro 00 00 ~ 00 ID ro ~ ~ 00 ~ ro 00 go _ 00

COHORT AGE IN DAYS COHORT AGE IN DAYS

!:i D. noxia 1-19 C s. graminum 1-19 C

55
...04
-<
~ 0
::E3
>-
Z
W2 0 ~@l 0
~ CD
a: c;,,_~1ID Do CD
W 1 ~~rnn 0 0 lj¥l 0

~ '1JCD
o
o ID~ ro~ 00 00 ro 00 00 ~ 00 ID ro ~ ~ 00 ~ ro 00 go _ 00

COHORT AGE IN DAYS COHORT AGE IN DAYS

Fig. 1. Average number of nymphs produced per Fig. 2. Average number of nymphs produced per
adult per day by cohort age for Diuraphis nona reared adult per day by cohort age for Schizaphis graminum
under three temperature regimes. reared under three temperature regimes.

or remained nearly the same, and Ro increased spread out over the entire adult lifespan. The higher
from IO"C through I-l9°C. These results indicate r associated with S. graminum and R. padi at 1-
m

that a wider fluctuation in temperature was more 19°C also was associated with the highest day-to-
beneficial to S. graminum and R. padi than it was day variability in natality over the three temper-
for D. noxia, but rearing at constant temperature ature regimes, whereas D. noxia's at I-19°C was
rOIl

had deleterious effects on Ro for all three species. associated with moderate day-to-day variability in
It is interesting to note that mean survival time natality.
(MST) for D. noxia was much higher at its highest Extrapolating these results to the field is difficult,
r"" than S. graminum and R. padi at their highest as with most laboratory data, but there are con-
r m' s. These differences are easily explained by Fig. clusions that can be drawn from the results that
1, which indicates that S. graminum and R. padi are useful for laboratory and field. If D. noxia, S.
concentrated their reproductive effort in early graminum, or R. padi are being reared in the lab-
adulthood, whereas D. noxia reproduction was oratory, especially for production (such as cocci-
April1989 MICHELS & BEHLE: INFLUENCEOF TEMPERATUREON SMALLGRAIN APHIDS 443

a Table 3. Mortality regression analyses for three small

!:i [Link] 10 C grain aphids reared at three temperature regimes

~a Tem-
..•. pera-
en. Intercept
r2
:z: Species ture
(±SE)
Slope (±SE)a
Q. regime
~3 0 ("C)
>- ~
Z D. noria 10 99.55 (1.13) -1.80 (O.03)Aa 0.98
W2 ~°crC 5-15 84.90 (0.88) -0.91 ([Link])Cb 0.97
0019 1-19 62.55 (1.71) -0.71 (0.03)Cb 0.85
~ 0
-1.34 (0.03)Ba
W1 o @ S. graminum 10 108.73 (1.29) 0.97
~ 00 5-15 116.11 (2.03) -1.17 (0.05)Bb 0.95
0
~ 1-19 98.46 (1.38) -1.25 (O.03)Ba 0.96
0 10 20 30 .0 60 60 70 80 90 100 110
R. padi 10 101.22 (1.44) -1.66 (0.04)Aa 0.97
COHORT AGE IN DAYS
5-15 103.81 (1.00) -1.42 (0.02)Aa 0.98
1-19 112.76 (1.87) -1.82 (O.06)Aa 0.95
8

Downloaded from [Link] at New York University on September 7, 2015

!:i [Link] 5-15 C
a Slope means in a column followed by the same upper-case
letter are not significantly different among species at the specified
~6 temperature regime. Means in a column followed by the same
..•. 0 lower-case letter are not significantly different among temperature
en. 00 regimes for the specified species (t test of slopes for estimate of a
:z: 0
common slope [Steel & Torrie 1960]).
Q. 0000
~3 o 0
>-
Z
o 0o~
o () lowed by a similar increase in S. graminum, while
W2

~ ° 0 D. noxia remain at lower densities for a time. Be-

cause of different reproductive strategies among
ffil
~
the three species, D. noxia may not seem to be a
~ ~&, 0 problem in the field early in the spring, because
0
0 10 20 30 .0 60 60 70 60 90 lOa 110 its Ro is smaller than those for S. graminum and
COHORT AGE IN DAYS R. padi. But, given the proper climatic condition
and the ability to produce nymphs at a somewhat
6
steady rate for a longer period than S. graminum
!:i or R. padi, D. noxia should eventually equal and
0 0 [Link] 1-19 C probably surpass S. graminum and R. padi.
~6 0 0
We realize that these results point out differences
..•. 0
associated only with temperature, and that factors
en. @CD ~
:z: 0
such as host plant cultivar, other climatic variables,
Q.
~3 ~ and predation ana parasitism also affect the pop-
>- 0
ulation growth rates for these aphids. In addition,
Z 0
W2 we recognize that D. noxia and S. graminum may
0 be more damaging to small grains in the spring,
~1 ~ because of their toxicogenic effects, than R. padi.
W

~ 0 However, these results do demonstrate the major

0
0 10 20 30 40 60 60 70 80 90 100 110
COHORT AGE IN DAYS Table 4. Age-specific life table statistics for three small
Fig. 3. Average number of nymphs produced per grain aphids reared at three temperature regimes
~dult per day by cohort age for Rhopalosiphum padi
reared under three temperature regimes. Temperature regime
Species Statistic"
1000C 5-15"C 1-19"C

nellid prey), these data indicate that alternating D. noxia Ro 5.5 20.1 14.1
rrn 0.045 0.062 0.188
temperatures were much better for aphid produc- T(d) 38.2 48.3 43.4
tion than constant temperatures, and that S. gra- MST(d) 55.3 93.3 88.1
minum and R. padi natality benefited from a wider 52.1
S. graminum Ro 30.0 33.6
fluctuation in temperature than did D. noxia. The rm 0.098 0.105 0.144
peak reproductive period for S. graminum and R. T (d) 34.7 33.5 27.5
padi was early in their life, whereas D. noxia pro- MST(d) 81.1 99.2 78.8
duced fewer nymphs on a day-to-day basis, but R. padi Ro 23.4 48.0 54.2
produced them over a longer period of time. These rm 0.118 0.146 0.200
T (d) 26.8 26.6 20.4
data indicate that in the field, especially during MST(d) 61.0 73.1 62.0
the spring, there should be a pattern in aphid den-
sities when these three species are present. One a Ro. net reproductive rate; r m. intrinsic rate of increase: T,
would expect an initial "bloom" of R. padi, fol- mean generation time; MST, mean survival time; d, days.
444 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 82, no. 2

role temperature plays in regulating aphid popu- Michels, G. J., Jr., T. J. Kring, R. W. Behle, A. C.
lation growth. Bateman & N. M. Heiss. 1987. Development of
the greenbug (Homoptera: Aphididae) on corn: geo-
graphic variations in the host-plant range of biotype
Acknowledgment E. J. Econ. Entomol. 80: 394--397.
Pakendorr, K. W. 1984. The research program for
We extend our sincere thanks and appreciation to combatting the Russian wheat aphid (Diuraphis nox-
Rene Chase and Matt Peters for their technical assistance. ia) in South Africa, pp. 164-170. In Barley yellow
This paper was approved as TX No. 23604 by the Di- dwarf-a proceedings of the workshop. CIMMYT
rector of the Texas Agricultural Experiment Station. (International Maize and Wheat Improvement Cen-
ter), Mexico City.
SAS Institute. 1985. SAS user's guide: statistics. SAS
References Cited
Institute, Cary, N.C.
Andrewartha, H. G. & L. C. Birch. 1954. The dis- Steel, R. G. D. & J. H. Torrie. 1960. Principles and
tribution and abundance of animals. University of procedures of statistics. McGraw-Hill, New York.
Chicago Press, Chicago. Stoetzel, M. B. 1987. Information on and identifica-
Ballou, J. K., J. H. Tasi & T. D. Center. 1986. Effects tion of Diuraphis noxia (Homoptera: Aphididae) and

Downloaded from [Link] at New York University on September 7, 2015

of temperature on the development, natality and lon- other aphid species colonizing leaves of wheat and
gevity of Rhopalosiphum nymphae (L.) (Homoptera: barley in the United States. J. Econ. Entomol. 80:
Aphididae). Environ. Entomol. 15: 1096-1099. 696-704.
Kieckherer, R. W. & N. C. Elliott. In press. Russian Turney, H. A. & C. E. Hoelscher. 1986. Managing
wheat aphid (Homoptera: Aphididae) immature de- insect and mite pests of Texas small grains. Texas
velopment and age-specific life tables under fluc- Agricultural Extension Service Bulletin B-1251.
tuating temperatures. J. Econ. Entomol.
Michels, G. J., Jr., & R. W. Behle. 1988. Reproduc- Received for publication 16 May 1988; accepted 2
tion and development of Dim'aphis noxia (Homop- December 1988.
tera: Aphididae) at constant temperatures. J. Econ.
Entomol. 81: 1097-1101.