Energy Drain by Three Pecan Aphid Species
(Homoptera: Aphididae) and Their Influence on
In-shell Pecan Production
B. W. WOOD, W. L. TEDDERS, ANDJ. D. DUTCHER
Southeastern Fruit and Tree Nut Research Laboratory,
Agricultural Research Service, U.S. Department of Agriculture,
Byron, Georgia 31008
Environ. Entomol. 16(5): 1045-1056 (1987)
ABSTRACT An estimate of the energy requirements of the three speciesof aphids, Monellia
caryella (Fitch), Monelliopsis pecanis Bissell, and Melanocallis caryaefoliae (Davis), that
feed on pecan, Carya illinoensis (Wangenh.) K. Koch, indicated that during a lifetime, an
individual of M. caryella consumes 8.4-fold more energy (301 J) than that of M. pecanis
(36.1 J) and ca. 7-fold that of M. caryaefoliae (44.8 J). When expressed as an average-age
individual typical of a season-long field population, M. caryella extracts ca. 8-fold more
energy than M. pecanis or M. caryaefoliae. Most energy consumed by all three species was
excreted as honeydew. Growth efficiency was low for all three species, but was highest for
M. caryaefoliae (25%), followed by M. pecanis (19%) and M. caryella (5%). Regression
models were derived to estimate the cumulative level of energy consumed by aphids of
various ages for growth, respiration, excretion, and total energy removal. Determination of
the season-long standing-aphid population (and aphid-days) in two different aphid management programs within a 70-yr-old 'Stuart' pecan orchard and influence of these populations
on nut yield indicated that all three species are highly detrimental to nut production;
extraction of 1 x 10" J, via feeding by M. pecanis or M. caryella, reduced in-shell nut
production by 58.7 g per 70-yr-old 'Stuart' tree. A season-long standing population of one
individual of M. pecanis per leaf of such trees reduced in-shell nut yield by 2.41 kg; 18.13
kg was lost because of the same level of M. caryella.
KEY WORDS Monellia caryella, Monelliopsis
illinoensis, energy drain, pecan production
pecanis, Melanocallis caryaefoliae,
Carya
INCONSISTENTFRUIT production, commonly referred to as alternate bearing, is associated with
changes in reserve energy levels within the tree
(Sitton 1931, Sparks & Brack 1972, Worley 1979a, b,
Wood & Tedders 1982) and is exhibited by essentially all commercially important pecan cultivars.
aphids and the quantification of their influence on
nut productivity of pecan trees. Such information
would give an estimate of the economic impact of
aphids on pecan trees and provide a basis for establishing economic injury levels. This investigation reports estimates of the energy budgets of in-
Thus, factors reducing energy reserves contribute
digenous pecan aphid species, per-annum energy
to alternate bearing or induce a decline in tree
productivity (Sparks 1979). The blackmargined
aphid, Monellia caryella (Fitch); the yellow pecan
aphid, Monelliopsis pecanis Bissell; and the black
pecan aphid, Melanocallis caryaefoliae (Davis),
which feed from the foliar vascular system of pecans (Tedders 1978, Wood et al. 1985), can influence energy reserves by reducing leaf net photosynthesis (Wood et al. 1985), depleting carbohydrate
reserves in stem tissue (Wood & Tedders 1982),
and by reducing leaf chlorophyll and leaf area
(Tedders et al. 1981, Wood & Tedders 1982, Tedders & Wood 1985). Aphid populations have also
been observed to reduce pecan nut yield (Stone &
Watterson 1981, Dutcher et al. 1984, Tedders &
Wood 1985), presumably because of the depletion
of tree energy reserves by feeding and their influence on tree growth and physiology. In spite of this
information, there is a dearth of knowledge relating to the amount of energy extracted by pecan
loss of trees due to aphid populations, influence of
high populations on nut production, and the estimated effects of aphids on pecan tree productivity.
Materials
and Methods
Energy Consumption by Individual Aphids. Energy consumption by an aphid feeding on foliage
can be represented by a modification of the generalized equation described by Petrusewicz as reported by Llewellyn (1972), such that:
E, = G,
+ R, + F, +
V,
(1)
Energy consumed by an individual aphid (E,) is
equal to the summation of energy associated with
aphid growth per developmental stage (G,) (G, =
body growth [G,o] + reproductive growth [G,,] +
exuviae production [G'e)), respiration (R,), and fecal (F,) and nitrogenous excretory products (V.).
G" (also R,) of embryonic aphids is included in the
1046
Table
ENVIRONMENT
1.
Developmental
Species
M. pecanis
M. caryella
M. caryaefoliae
and reproductive
Developmental
stage
1st instar
2nd instar
3rd instar
4th instar
Adult
1st instar
2nd instar
3rd instar
4th instar
Adult
1st instar
2nd instar
3rd instar
4th instar
Adult
parameters
i ageh
(d)
Vol. 16, no. 5
AL ENTOMOLOGY
for pecan aphids"
Duration of
life stagee
(d)
1.0
3.0
4.5
6.0
13.9
1.0
2.5
4.0
5.5
20.2
1.0
3.0
4.5
6.5
13.8
2.0
2.0
1.0
2.2
13.4
1.8
1.2
1.8
1.5
28.2
2.0
2.0
1.2
2.8
11.7
Composition
of field aphid
populationsd
(%)
52.6
31.7
8.1
4.5
2.7
23.6
19.7
27.5
18.7
10.2
32.3
31.2
18.6
11.7
5.9
i age of
field
population
(d)
3.8
2.5
3.7
Energy content
(J/mg dry wt)'
22.4
22.4
22.4
18.1
18.7
21.6
21.6
21.6
20.6
21.6
18.0
17.2
17.3
19.0
18.7
LSD
=
0.8
" Data taken from Tedders (1978).
b Mean age of aphids from field environment composing each developmental
stage.
e Mean number of progeny produced per adult aphid per day.
d Mean makeup of field aphid populations at anyone time as determined over a 2-yr period.
e Based on ca. 100 aphids per measurement.
growth estimates of the adults. This was necessary
because it was not practical to separate adults with
and without embryos or to remove embryos for
measurements. It is also impossible to distinguish
between F, and V, of pecan aphids, because both
are eliminated as honeydew by each of the three
pecan aphid species. They are therefore considered
in toto (F, + VJ
Estimate of Aphid Growth (G,). Dry weight of
individual aphids of the various instars feeding on
pecan trees in the orchard environment was determined by weighing 100+ individuals from each
developmental stage of each species. The average
age of aphids within each of the five stages was
estimated from previously published data by Tedders (1978) in which aphids were measured from
the field environment. Regression of dry weight on
estimated aphid age resulted in equations with a
high level of significance (P ::5 0.01) for each of
the three aphid species. The equations for these
lines were then used to predict the dry-weight
growth characteristics of individuals of any age for
each species.
Energy content of aphids was determined by the
combustion of freeze-dried aphids (100 aphids per
datum) in a microbomb calorimeter (Phillipson
1964). The total dry-weight increase of the respective aphid population, as described above, was
then multiplied by the appropriate energy (joules)
value obtained for each species. The exuviae from
the four molts of developing aphids were not included in the estimate of aphid energy content.
Energy content of exuviae is probably similar to
that of the lime aphid, Eucallipterus titiae L., as
reported by Llewellyn (1972, 1975) and would,
thus, probably be of relatively little consequence
in regard to the total amount of energy removed
from the tree.
The energy directly consumed by G, was then
determined using the above derived regression
equations and aphid energy content. G, (expressed
as joules per aphid per day per life stage) was then
determined for each developmental stage of each
species by first multiplying y (aphid dry weight)
by the appropriate energy content of each aphid
stage (i.e., joules per milligram of aphid dry weight
[see Table 1]). This value (joules per aphid per
developmental stage) was adjusted, to give joules
per aphid per day for each developmental stage,
by subtracting the energy content of the previous
life stage and then dividing by the duration of the
life stage of concern (see Table 1).
Respiration (R,). Energy utilized in aphid respiration was estimated by measuring CO2 evolution
and conversion to energy equivalents. Groups of
100 field-collected aphids for each developmental
stage and for each species were placed in a chamber
(333 cm3) of a portable photosynthetic system (LICOR 6000). Aphid respiration was measured at
23°C. Energy equivalents were determined by
measuring the rate of CO2 evolution and converting to metabolic energy loss based on a respiratory
quotient (R.Q.) of 1.00. Pecan aphids feed by sucking phloem sap containing carbohydrates and nitrogenous compounds; thus, their diet seems to consist largely of carbohydrates, and an R.Q. of ca.
1.00 would be expected (Llewellyn 1972).
The energy consumed by R, was determined using the above derived regression equations. R, (expressed as joules per aphid per day per life stage)
was then determined for each developmental stage
of each species by multiplying y by the appropriate
October 1987
WOOD
1047
ET AL.: ENERGY DRAIN BY PECAN APHIDS
dry weight (in micrograms [derived from Fig. 1
and Table 1]) of that life stage.
Defecation (F) and Excretion (U). Pecan aphids
excrete surplus nutrients as honeydew composed
primarily of sugars with a small amount of organic
nitrogen (Tedders et al. 1981). Because defecation
and excretion occur together as honeydew exudate,
honeydew was taken to represent F, + V;. Honeydew sugars on pecan are almost entirely monoand polysaccharides (Tedders et al. 1981); thus,
energy content was estimated by adapting previous
research findings by Tedders & Wood (1987) in
which the amount of energy in honeydew produced in a 24-h period in the field environment
by each aphid developmental stage was determined for each species. Individual aphids were
caged on leaves in the field, and their honeydew
was collected on a nylon-mesh cloth within the
cage. Honeydew was washed from the cloth with
hot 70% ethanol, dried in vacuo and treated with
invertase to convert nonreducing sugars to their
reducing moieties. These moieties were measured
colorimetrically using Nelson's modification of
Somogy's method (Hodge & Hofreiter 1962). Moiety levels were converted to molar glucose equivalents, with the associated energy content being
calculated by converting moles of glucose to joules.
Energy content of the honeydew was then regressed against aphid age (determined by substituting the average chronological age of each developmental stage as described above) and the
results utilized to predict the amount of energy
contained in the honeydew of individuals of various ages of each species.
The energy removed in the form of honeydew
(F, + V,) was then determined using the appropriate regression equation derived from the above
determination. Two equations were developed for
each species because the energy content of the
honeydew increased in the earlier stages of development and then decreased. The appropriate equation was used for the determination of F, + U,.
Joules per life stage (E,) was then determined
by the summation of daily C" R" and U, + F, and
multiplication of this value by the number of days
within each life stage. Joules per aphid life span
was then determined by the summation of the above
life-stage components.
The regression equations for C" R" and F, + V,
were then used to calculate cumulative E, for aphids
of any age throughout the aphid's lifetime. These
points were then fitted by regression equations using SAS GLMP (SAS Institute 1985) and plotted,
thus providing a means of determining the cumulative amount of energy removed by an individual aphid at any point in its lifetime.
Energy Consumption by Field Aphid Populations. The amount of energy consumed by a field
population of aphids feeding on trees in the commercial orchard environment was also estimated
using the generalized equation reported by Llewellyn (1972), and is stated as follows:
Ep = Cp
+
Rp
+ Fp +
Vp
(2)
Energy consumed by an aphid population (Ep) is
equal to the summation of energy associated with
the biomass growth of the population (Cp) (where
Cp = population body growth [Cpb] + population
reproductive growth [Cpr] + population exuvia
production [Gpe]), population respiration (Rp), and
population fecal (Fp) and population nitrogenous
excretory products (Vp). As in the previously described procedure for E" Cp and Rp of embryonic
aphids is only partially included in the growth estimates. Fp and Vp are considered in toto as honeydew.
Estimates of Ep in this paper carry a small inaccuracy in that the standing-aphid population was
based on population counts made at 7-d intervals
(rather than daily), with these levels assumed to
remain constant until the next count. This method,
of course, assumes that immigration and birth are
offset by emigration and death.
Influence of Field Aphid Populations on Tree
Energy Drain and Nut Production. The influence
of aphids on energy drain was determined under
orchard conditions using a randomized completeblock design consisting of two aphid treatments and
three replicates of 4.7 ha (140 trees) of 70-yr-old
'Stuart' pecan trees per replicate. Treatments were
a full-season insecticide spray program in which
trees were sprayed as needed using a spray threshold of 20 aphids per compound leaf; and a lateseason aphicide spray program in which trees were
not sprayed for the spring aphid populations but
were sprayed from mid-July to frost on the same
dates as the full-season treatment. Trees of both
treatments received the same fungicide (using triphenyltin hydroxide) spray program used for pecan scab control. Fertilization was based on leaf
and soil analyses according to Georgia Cooperative
Extension Service guidelines. Based on leaf analysis, both treatments were maintained at horticulturally equal levels of nutrient element nutrition.
Pretreatment soil and leaf analyses indicated that
macro- and micronutrients were similar in all plots
and were within the recommended range. All treatments received at least 2.54 cm of water each week,
either from rainfall or sprinkle irrigation. In-shell
nut yields were determined by harvesting all 70
trees per experimental unit.
An estimation of Ep by the season-long field
populations was determined by measuring aphid
species composition and population density
throughout the growing season via weekly aphid
counts from five randomly selected terminal shoots
(7-11 compound leaves per shoot) located along
the outer canopy (8 m high) of a randomly selected
tree of typical size and shape from each replication
of the two aphicide management treatments. Because pecan aphids are reported to be uniformly
distributed relative to tree height or quadrant
(Edelson & Estes 1983) and distributions are similar
between trees of the same cultivar (personal ob-
1048
ENVIRONMENTAL
Vol. 16, no. 5
ENTOMOLOGY
10
300
0.59
I
I
r
lC
Y-7.'S.
:E
c.
«l
c.
200
0>
3
0
~
,.,
-0
100
:E
c.
0«
f
'"
..,~ ~
.•
f
/
a
2
/"
8
7
":;
6
0
g
8
M. pecenis
10
6
e
10
12
.4
16
18
20
Fig. 2. Energy consumption by respiration of M.
pecanis, M. caryaefoliae, and M. caryella as related to
aphid age. Regressions are significant (P < 0.05). Standard error of the estimate for M. caryaefoliae, M. pecanis, and M. caryella is ±0.0l, ±0.02, and ±O.03, respectively.
M. caryella
-----
4
Aphid age (days)
M. cBryaefollae
• .•••...........•
6
•
5
j
.,/
4
--_
9
0
...
;::<~ / .
•••••••••
0
I
• --
i
I
M. co'yaelolla
M. pecanls
"
:c0. :;
«
•
/. /'
>-
.~ i;
/ / ,.~::."..
!
0>
'(jj
o
c:
.~
f
.c:;
."
.•
0.50 .•.
I
I
b I
I
I
I
I
I
I
."
Q;
Y"5.7Be
>.
~
~
12
14
19 20
Aphid age (days)
Fig. 1. Dry weight of M. caryaefoliae, M. pecanis,
and M. caryella in relation to age. The relationship between aphid dry weight (y) is expressed as a power model
of aphid age (x). Standard error of the estimate for M.
caryaefoliae, M. pecanis, and M. caryella is ±l.lO, ±O.62,
and ±O.44, respectively.
servations), these counts were, therefore, taken to
be representative of the season-long field aphid
population. The average age (or corresponding developmental stage) of the field aphid population,
at each of the weekly sampling dates throughout
the growing season, was then determined from previously published data (see Table 1, information
from Tedders [1978]).
To estimate energy loss of a whole tree, a single
70-yr-old tree was measured for foliage characteristics. In early July, the total leaf area and number
of leaves on one tree, judged representative of the
trees in the aphid treatments, was measured by
stripping the tree of leaves. These leaves were then
counted and areas measured with a leaf area meter
(LI-COR),
The assimilation of the above-mentioned information regarding E, for aphids of any age or species,
season-long population level, age and species makeup of the population, and the number of aphids
per tree facilitates the estimation of the amount of
Ep a standing population of aphids can remove
from a pecan tree. The mean numbers of aphids
per species per compound leaf per growing season
(standing aphids) were determined from the weekly aphid counts and are presented in Table 4 (derived from Table 3). The age composition of these
standing-aphid populations was estimated from
previous data reflecting a 2-yr average of field populations of all three species (Table 1). This information provides a species-specific breakdown of
the average number of aphids inhabiting a com-
pound leaf throughout the growing season plus the
life stage or the composition of this population. Ep
was then estimated by determining the amount of
energy consumed by each standing aphid per life
stage per species using the regression equations for
cumulative energy consumption in Fig. 4-6. These
values were then added to the energy consumed
by each average standing aphid (representing the
different ages) during each I-d period of the 217-d
growing season. For M. pecanis from the full-season aphid control treatment in 1982, the standing
population was 1.88 aphids per compound leaf or
0.99,0.60,0.15,0.08, and 0.05 aphids per first instar
to adult life stages, respectively; these aphids averaged 1, 3, 4.5, 6, and 13.9 d old per respective
life stage. The age values were then utilized in the
regression equations in Fig. 4-6 to determine the
energy consumed to reach that particular age. These
standing aphids represent a statistical average, so
the energy consumed by aphids of the respective
standing-aphid life-stage (or age) category was determined by utilizing the equations of Fig. 4-6 to
estimate the total amount of energy consumed between ±0.5 d of the mean ages of individuals from
each of the respective life stages (0.5-1.5 and 2.53.5 d, for the first and second instars, respectively).
The sum of these two consumption values was then
multiplied by 217 to obtain the energy consumed
per compound leaf per growing season per aphid
population. This then estimated season-long Ep per
compound leaf; season-long Ep per 70-yr-old tree
was estimated by multiplying by the number of
compound leaves (l20,474 leaves per 70-yr-old tree)
per tree, giving an estimation of the joules removed
by the season-long standing-aphid population (Table 4). This value was determined annually for each
of the two aphid treatments over a 3-yr period
(Table 4).
Estimation of the In8uence of Aphids on Inshell Nut Yield. The impact of aphid feeding on
in-shell nut yield was estimated by dividing the
October
1987
WOOD ET AL.: ENERGY DRAIN BY PECAN APHIDS
1049
Table 2. Energy removed" by the various developmental stages of the three pecan aphid species
Speciesand
developmental
stage
J per aphid/d
J/life stag.!>
J/life span
Ratio
0.91
1.49
2.35
2.86
1.69
1.82
2.98
2.35
6.29
22.65
36.09
1.0
0.65
0.93
1.13
1.20
0.62
0.84
1.42
1.87
3.47
2.42
1.68
2.84
2.24
9.72
28.31
44.79
1.2
9.58
38.26
52.97
12.15
6.64
9.83
38.78
54.00
14.98
8.38
17.69
46.53
97.20
41.94
98.05
301.41
8.4
Growth
Respiration
Excretion
Total
0.08
0.14
0.52
0.32
0
0.07
0.18
0.37
0.77
1.39
0.76
1.16
1.47
1.77
0.30
0.11
0.30
0.35
1.26
0
0.08
0.19
0.39
1.01
1.80
0.13
0.26
0.43
1.45
0
0.12
0.26
0.60
1.38
1.74
M. pecanis
1st instar
2nd instar
3rd instar
4th instar
Adult
M. caryaefo/iae
1st instar
2nd instar
3rd instar
4th instar
Adult
M. caryella
1st instar
2nd instar
3rd instar
4th instar
Adult
" Derived from actual measured values from aphids of each of the five developmental stages of each species.
/.Energy removed by an individual aphid during its total amount of time in each developmental stage. Tbis value is the product
of total joules per aphid per day (column 4, Table 3) and the number of days (column 2, Table 1) the aphid was in the respective
developmental stage.
difference in in-shell yield between the two aphid
treatments
by the difference
in energy removed
by the season-long standing-aphid
populations
of
the two treatments
(Tables 4 and 5). Therefore,
the removal of an estimated
334 MJ from 70-yrold 'Stuart' trees was associated with the loss of 19.6
kg of in-shell nuts per tree, or 58.7 g per megajoule
(Table 5). Because M. caryaefoliae was essentially
absent from the aphid populations
during all 3 yr
of the study (Tables 3 and 4), this yield loss was
associated
with feeding
by the "yellow"
aphid
complex (M. pecanis and M. caryella).
The influence of the two "yellow" aphid species
on nut production
was then estimated
by multi-
plying megajoules consumed in the growing season
by a population of one standing aphid (for each of
the two species) on each compound
leaf of the tree
(Table 4) by the in-shell nut loss associated with
the removal of a megajoule of energy (58.7 g per
megajoule [Table 5]) by the feeding aphids.
Results
Growth Estimates (G,). The dry-weight
increase
of all three aphid species was rapid as they passed
through the first four developmental
stages of their
life span. Maximum
weight was reached at the
early adult stage (after ca. 6-8 d, depending
upon
species) (Fig. 1). Growth was curvilinear,
with the
relationship
of dry weight (y) to age (x) during the
first half of the aphid's life span described by exponential-type
regression models (M. caryaefoliae:
y = 5.78e05Ox, r2 = 0.87, P < 0.05; M. caryella: y =
7.15eo59" r2 = 0.97, P < 0.05; M. pecanis: y =
r2 = 0.96, P < 0.05). Energy content for
each instar is given in Table 1.
Respiration
Estimates
(E). Aphid respiration
consumed from 6.3 x 10-3 to 9.6 X 10-3 J I J.Lgof
aphid dry weight per day, depending
on species
and age (Fig. 2). The relationship
of respiration
(y = 10-3 JIJ.Lg dry wt per day) to aphid age (x =
mean age in days within each developmental
stage)
was curvilinear,
with respiratory energy consumption per microgram
of aphid declining with aphid
age (joules per aphid for M. caryaefoliae,
M. caryella, and M. pecanis was y = 8.20x-°'1O [r2 = 0.93],
y = 9.54x-OI4 [r2 = 0.90], and y = 9.75x-009 [r2 =
0.89], respectively).
Respiration by M. pecanis had
a tendency to be higher than that of either M.
4.37e051"
caryella or M. caryaefoliae.
Excretion
Estimates
(F;
+ UJ. The energy associated with aphid honeydew exudate was much
greater for M. caryella than for M. pecanis or M.
caryaefoliae (Fig. 3). Levels of energy excreted in
the form of honeydew (y) increased with aphid age
(x) up to 4 d for M. caryella (y = 9,587 + 31,307
In x, r2 = 0.91) and to 6 d for M. pecanis (y =
201x + 561, r2 = 0.99) and M. caryaefoliae (y =
138x + 511, r2 = 0.96). After these ages, energy
levels in honeydew decreased.
These relationships
were best described
by a curvilinear
logarithmic
regression model for M. caryella and linear regression models for the other two species. All regressions were significant (P < 0.05).
Daily Energy Expenditure
(E,). The daily E; of
aphids representative
of the various developmental
stages of each species, as determined
from the
above-mentioned
regression equations, is given in
1050
ENVIRONMENTAL
Vol. 16, no. 5
ENTOMOLOGY
M. caryella
•••. pecanls
200
Life
stage
190
150
/
/
/
/
100
/
150
/
Y=12.
/
2 .•. 0 19X3
13 1 X •. 305X
/
/
/
50
/
r2o; .99
/
/
/
•...
'"'as
-
"C
CIl
Gl
/
110
:;
M. <sryelle
E-
-
"C
Ql
o
C
...
Ql
Ql
~
U
Ql
•..
..
//
30
Ql
--.,
1100
>-
900
Ql
,2 •. 87
/
/
,2= .99
/
Tolal---
Respiration
c::
)(
20
Growth
,-
-.-.-.-
I
.••...•.•......••.
,/
Q)
>
c:
Excrement
iii
c:
y
o
u
...
/
/1
E
1300
V=10.832X+.l03X2-.003X3
/
>
E
Ol
70
o
Gl
'0
///\
/
N
I
-
/
/
/
/
0
1500
.8673+31307
,2 •• S1
U
V=-.008 X+.100X2-
Ql
c:
,/
,-I
,,,-
~
E
~
Inlf
I
_
.00 1X3 ,
W
M. caryaefollae
200
10
,2= .99
~
//,/
,,-
..".·.•.:·<·· ·..·..
150
•.•••••;,:./.
100
Y=.400X+.07
-:.:..:::..~.;.:.;.,,'
f· · · · .
1X2 -.005X3
,2= .99
o
o
50
4
6
Aphid
,2 •. 80
,2 •.
eo
o
o
2
4
6
8
10
12
14
16
Aphid age (days)
Fig. 3. Energy content of honeydew excreted per
day by individual M. pecanis, M. caryaefoliae, and M.
caryella aphids as related to aphid age. The relationship
between the energy content of excreted honeydew (y)
is expressed as linear or log models of aphid age (x).
Standard error of the estimate for the early phase curve
for M. caryaefoliae, M. pecanis, and M. caryella is ±1.6,
±1.4, and ±35, respectively; that of the late phase curve
is ±0.07, ±1.5, and ±33, respectively.
Table 3. In all three species, the greatest amount
of energy consumed in the first four life stages was
in the honeydew (34-97% of the total), followed
by growth (1-36%), and then respiration (1-28%).
E for adults of M. pecanis and M. caryaefoliae
was primarily due to respiration, whereas for M.
j
2
8
age
10
12
14
(days)
Fig. 4. Estimated cumulative energy consumption
by M. caryella at various ages and developmental stages.
Curves are for energy utilized in growth, respiration,
and excretion, and the summation of these factors (total).
Regression equations are significant (P < 0.05) using SAS
GLMP (SAS Institute 1985, 433-507).
caryella it was due to excretion. Thus, pecan aphids
assimilate relatively little of the energy they ingest.
Energy use increased with instar, but declined at
the adult stage. Growth efficiency (joules utilized
in growth divided by those consumed until adulthood) of the aphids was 19% for M. pecanis, 25%
for M. caryaefoliae, and 5% for M. caryella. When
energy removal from the host tree is expressed by
reflecting the number of days within each developmental stage, individuals of M. caryella remove
far more energy than individuals of the other
species. Individuals of M. caryella extracted 301 J
per aphid per lifetime or ca. 6.7- and 8.4-fold more
than individuals of M. caryaefoliae and M. pecan-
October 1987
WOOD ET AL.: ENERGYDRAIN BYPECAN APHIDS
1051
Table 3. Monthly mean population density or pecan aphids on 70-yr-old 'Stuart' pecan trees receiving rull-season
lind late-season aphicide spray programs
f
Year
Month
Full
1982
1983
1984
Mar.
Apr.
May
June
July
Aug.
Sept.
Oct.
Nov.
Mar.
Apr.
May
June
July
Aug.
Sept.
Oct.
Nov.
Mar.
Apr.
May
June
July
Aug.
Sept.
Oct.
Nov.
no.of aphidsper compoundleaf
M. caryella
M. pecanis
0.24
0.52
5.80
4.35
0.05
0.59
0.33
2.39
0.24
0.05
9.24
4.71
0.57
1.93
1.71
0.49
0.14
7.86
4.05
0.23
0.03
1.04
0.67
4.00
±
±
±
±
±
±
±
±
±
0
±
±
±
±
±
±
±
±
0
±
±
±
±
±
±
±
0.05
0.22
4.32
2.81
0.01
0.37
0.29
1.33
0.06
0.02
5.81
1.01
0.09
0.82
0.70
0.15
0.03
7.32
1.56
0.07
0.02
0.63
0.36
2.48
Full
Late
0.28
1.03
24.56
21.12
0.05
0.13
± 0.04
± 0.58
± 0.41
± 15.03
± 0.01
± 0.03
om
0.69 ± 0.14
0.14 ± 0.02
0
0.01
24.03 ± 19.22
62.34 ± 18.88
0.49 ± 0.31
0.69 ± 0.27
0.80 ± 0.31
0.47 ± 0.27
0.30 ± 0.10
0
8.27 ± 7.76
5.2 ± 2.23
0.12 ± 0.06
0.04 ± 0.01
0.36 ± 0.21
0.66 ± 0.40
4.38 ± 0.98
0.03
0.17
0.25
3.24
0.05
3.39
0.14
0.08
0.38
0.91
0.13
1.89
2.96
0.44
0.42
±
±
±
±
±
±
±
±
0
0
0
±
±
±
±
±
±
±
0
±
±
±
±
om
0.02
0.20
2.82
0.2
2.10
0.01
0.02
0.17
0.22
0.01
0.95
1.73
0.20
0.11
3.03
2.37
0.57
0.12
0.06
0.05
0.06
0.02
6.91 + 3.73
2.18 ± 1.15
9.99 ± 6.21
M. caryaefoliae
Late
0
0.01
3.74 ± 2.79
4.24 ± 2.81
0.14 ± 0.05
0.82 ± 0.37
0.18 ± 0.04
0.08 ± 0.03
0
0
0
1.47 ± 1.21
10.97 ± 3.71
0.08 ± 0.05
0.87 ± 0.43
1.93 ± 0.58
0.38 ± 0.17
0.47 ± 0.19
0
3.40 ± 2.67
1.01 ± 0.67
0.03 ± 0.02
0.04 ± 0.02
3.92 ± 1.98
2.96 ± 1.93
15.84 ± 6.55
Full
Late
0
0
0
0
0
0
0
0
0
0
0.02
0.13 ± 0.02
0
0
0
0
0.01
0
0
om ± 0
0
0
0
0.14 ± 0.07
0
0
0
0
0
0
0
0
0
0
0
0
0.16 ± 0.03
0.98 ± 0.27
0.10 ± 0.26
0
0
0.01
0
0
0
0.05 ± 0.02
0
0
0
0.07 ± 0.02
0
0
Full-seasontreatmentreceivedaphicidesprayson 29 March,26 April,11 May,2 and 17 June, 16 July, 11 and 26 August,and 13
September,and on 27 April,16 May,2 and 23 June,7, 14, and 21 July, 11 and 22 August,8 September,and 3 Octoberin 1982 and
1983, respectively.
Part-seasontreatmentwaslate-seasonaphidcontrolwithsprayson 16 July, 11 and 26 August,and 13 September,
and on 14 and 21 July, 10 and 22 August,8 September,and 3 Octoberin 1982 and 1983, respectively.
is, respectively. This indicates that, when compared in terms of the level of energy removed per
aphid lifetime from a tree by an individual aphid,
M. caryella is by far the most detrimental of the
three aphid species.
Population Energy Consumption (Ep). The cumulative energy removed by an aphid over its life
span is given in Fig. 4-6, and the seasonal abundance of aphids is shown in Table 3. This information, combined with a record of nut production
from the two aphid treatments, provided a method
of estimating the influence of aphids on nut production.
The near absence of the highly injurious (Wood
& Tedders 1986) M. caryaefoliae during the period
of study means that yield loss was due to M. pecan is
and M. caryella, thus giving a unique opportunity
to estimate the influence of energy removal and
"yellow" (refers to either M. pecanis or M. caryella, or both) aphid numbers on tree nut production. To understand the influence of aphids on pecan nut production, it is first necessary to recognize
two important points about the nature of nut production. First, it is the level and composition of
assimilate reserves accumulated during the previous growing season that largely regulate nut production, and second, because of the high demand
for assimilate by a developing crop, nut production
is cyclic, with a relatively large nut crop being
followed by a light crop, and vice versa; this response is termed alternate bearing (Sparks 1979,
Monselise & Goldschmidt 1982). The bearing cycle
of trees in the two aphid treatments of this study
were synchronous before the establishment of aphid
treatments. Therefore, with other variables being
constant, any yield differences between the two
treatments would be expected to be due to the
season-long aphid population.
In 1982, the season-long standing-aphid population of 1.61 M. pecanis and 0.82 M. caryella per
compound leaf from the full-season aphicide treatment extracted an estimated energy equivalence
of 320 x 106 J per tree and 533 x 106 J were
removed in the late-season insecticide treatment
with a standing population of 5.33 M. pecanis and
1.02 M. caryella (Table 4). In 1983, the standing
population removed 330 x 106 and 963 x 106 J
per tree from the full-season and late-season treatments, respectively. Such an apparent loss in tree
energy reserves, and associated feeding damage,
by the standing-aphid population would be expected to reduce tree nut productivity. The standing-aphid population of the 1982 treatments did
not differentially influence 1982 nut production.
1052
ENVIRONMEJ\TAL
Vol. 16, no. 5
ENTOMOLOGY
M. caryaefoliae
M. pecanis
50
Life
Life
50
stage
stage
adull
r2~.99
Tolal---
40
-----
•..•
16X 3
III
Ql
30
:;
2:
'0
Ql
30
"C
Ql
>
o
E
>
o
E
~
•..
Ql
>-
>Cl
Qj
~
Cl
Ql
;
-.-.-.-
..•...............
Excrement
----Y=.3 7 4X+.350X2-.0
::I
o
Growth
.
Excremenl
Ql
Respiration
-.-.---
Growth
••
Total---
40
Respiration
\
20
ffi
20
Ql
Ql
.~
>
tij
:;
E
::I
U
10
10
, \
.
. .' -' : ~.
o
o
o
2
4
6
Aphid
8
age
10
12
14
(days)
o
2
4
6
8
10
12
14
Aphid age (days)
Fig. 5. Estimated cumulative energy consumption
by M. pecanis at various ages and developmental stages.
Curves are for energy utilized in growth, respiration,
and excretion, and the summation of these factors (total).
Regression equations are significant (P < 0.05) using SAS
GLMP (SAS Institute 1985, 433-507).
Fig. 6. Estimated cumulative energy consumption
by M. caryaefoliae at various ages and developmental
stages. Curves are for energy utilized in growth, respiration, and excretion, and the summation of these factors
(total). Regression equations are significant (P < 0.05)
using SAS GLMP (SAS Insitute 1985, 433-507).
As previously explained, this would be expected
because a tree's nut crop is primarily influenced
by factors affecting energy accumulation during
the previous growing season, and trees of both
treatments were exposed to an equal number of
aphids in 1981 and in earlier years. The 1982 aphid
population would then have its major influence on
the 1983 nut crop. Because trees of both treatments
were on the same bearing cycle, 1983 yield would
be equal if aphids had no effect; however, yield
was reduced in 1983 by 55.4 kg per tree (Table 4),
primarily by a standing-aphid population of 3.72
(5.33 minus 1.61) M. pecanis and 0.20 (1.02 minus
0.82) M. caryella in 1982. It is entirely possible that
the 1983 aphid population could also influence 1983
yield; however, the exact degree of influence is
unknown, and based on previous observations
(Tedders & Wood 1985), would probably be small
relative to that of the 1982 population.
In 1984, there was no yield difference between
aphid treatments, with yield being less than in 1983.
Trees of the full-season treatment would be expected to be in the light-crop phase of the alternately bearing cycle in 1984 because of the large
crop produced the previous growing season. This
yield drop was indeed observed. Yield was also less
October
1987
WOOD ET AL.: ENERGY DRAIN BY PECAN APHIDS
1053
Table 4. Estimated influence of full- and late-season aphid control and subsequent standing aphid populations on
energy removal and tree yield from a 70-yr-old 'Stuart' pecan tree
No. of aphids"
Treatment/species
1983
1982
SA
AD
SA
1984
AD
SA
AD
Estimated energy
removed by a~hid
population
(MJ/tree)
1982 1983 1984
Full-seasoncontrol
M. pecanis
M. caryella
M. caryaefoliae
1.61
0.82
0
349
178
0
2.09
0.79
0.02
454
171
4
1.98
2.53
0.09
430
549
20
66
254
0
320
85
244
1
330
81
782
1
864
5.33
1.02
0
1,157
221
0
9.90
1.80
0.17
2,148
391
37
2.11
3.02
0.08
458
655
17
218
315
0
533
405
557
1
963
86
934
1
1,021
Total
La te-seasoncontrol
M. pecanis
M. caryella
M. caryaefoliae
Total
In-shell nut yieldC
(kg/tree)
1982
1983
1984
44.9b
102.9c
28.6a
41.2b
47.5b
28.9a
" Mean number of aphids per compound leaf per growing season.One standing aphid (SA)per compound leaf per growing season
e(~uals120,474standing aphids per 70-yr-old 'Stuart' tree per seasonor over 26 x 106 aphid-days (AD) per tree per growing season.
Energy values estimated using regression equations for average-aged individuals of each life stage of each aphid species in the
field population. These values were then multiplied by the number of standing aphids of each class.number of compound leaves per
tree, and days per growing season to estimate total energy removed per seasonby the aphid population.
C Means among columns and rows followed by the same letter are not significantlydifferent (P > 0.05; Duncan's [1955]multiple
range test).
than that of the 1982 nut crop, perhaps additionally
reflecting the influence of aphid feeding in 1983
and 1984. In the late-season control treatment, yield
in 1984 was lower than in 1982, probably because
of the very high aphid numbers in 1983. The lack
of a 1984 yield difference between the two aphid
control treatments
is, therefore,
as would be expected given the bearing nature of pecan and the
detrimental
influence of aphid feeding.
The influence of the two species of aphids on
nut production
is consequently
best estimated
by
utilizing the means of nut production
and aphid
population
data for 1982-84. Thus, the mean differential in nut production
between the two aphid
management
programs during 1982,1983, and 1984
resulted in an in-shell nut yield loss of 19.6 kg per
tree (58.8 minus 39.2) and was associated with an
estimated energy removal of 334 x 106 J (838 minus 504) per tree (Table 5). Therefore,
the removal
of 1 x lQ6 per tree reduced yields by an average
of 58:7 g (19,600 g divided by 334 MJ) of in-shell
nuts per tree. The average individual (average aphid
age was 3.8 d for M. pecanis and 2.5 d for M.
caryella) M. caryella extracts ca. 8.3-fold (derived
from Tables 1 and 2) more energy from the tree
than does the average individual of M. pecanis and,
therefore,
populations
of M. caryella might be ca.
8.3-fold more detrimental
than equivalent
numbers of M. pecanis.
The average-aged
individual
of M. pecanis or
M. caryella is estimated to remove 40.4 and 309
MJ, respectively, during the growing season (or 217
aphid-days).
A well-managed
70-yr-old 'Stuart' pecan tree was estimated
to have ca. 120,474 compound leaves; therefore,
a season-long aphid population of one aphid per compound
leaf would be
J
120,474 aphids (or rather 26 x 106 aphid-days)
per
tree. This number of M. pecan is would reduce inshell nut production
from such a tree by 2,406 g
(58.7 g nuts per megajoule
x 40 MJ per aphid),
but M. caryella would reduce it by 18,128 g (58.7
g nuts per megajoule
x 309 MJ per aphid). This
relationship
of the standing-aphid
population
and
aphid-days
to in-shell yield reduction is represented in Fig, 7, where it is presented
in the form of
simple equations
that reflect the aphid-induced
yield loss of the 'Stuart' trees in our study. This
relationship
was such that for M. pecanis the kilograms of in-shell nut loss per tree (y) was equal
to the product of the number of season-long standing aphids per compound
leaf (x) and 2.41, or
the product of the number of aphid-days
per compound leaf (x) and 0.011. For M. caryella, this
Table 5. Estimated annual yield reduction of in-shell
nuts in 70-yr-old 'Stuart' pecan trees due to specific levels
of energy removed by "yellow" aphids
Treatment
Full-seasoncontrol
Late-seasoncontrol
Difference
X annual
In-shell
energy
nut yield
x annual
removed
lossper
in-shell
nut yield" by "yellow" unit energy
b
aphids
removedc
(kg/tree)
(M])
(g/MJ)
58.8
39.2
19.6
504
838
334
58.7
Mean of nut yield in 1982, 1983, and 1984.
Mean of energy removed by M. caryella and M. pecanis in
1982, 1983,and 1984. Values are from Table 4.
C 19,600g divided by 395 MJ = 58.7 g in-shell nuts per 106 J
of energy removed by aphid feeding.
a
b
1054
ENVIRONMENTAL
Predicted
(kg
100
In-shell
loss
nutS/tree)
M. pecanls
M. caryell8
Aphld811eaf
:
y=
Aphld-days/leat:
18.13
y
II
V:O.083x
=
..•..
.•..•..
2.41 •.....
y= 0.011.
80
60
40
o
2
3
4
6
5
Standing aphids per compound leaf
217
434
651
868
1085
1302
Aphid -days per compound leal
Fig. 7. Estimated reduction in in-shell nuts per 70yr-old 'Stuart' pecan tree by either a season-longstanding
population (per compound leaf) or season-long aphiddays (per compound leaf) of M. pecanis or M. caryella.
A 70-yr-old 'Stuart' pecan tree was determined to have
120,474 leaves; therefore, one aphid per compound leaf
equals 120,474standing aphids per tree. This isalsoequal
to 217 aphid-days per compound leaf or 26 x 106 aphiddays per tree per growing season. Because of the great
difference in the ratio of leaf area to fruit between a 70yr-old tree and a much younger tree, these predictions
of aphid impact on yield would be considerably less in
younger 'Stuart' trees.
relationship was y = 18,13x for standing aphids per
leaf and y = O.083x for aphid-days (Fig. 7). These
simple prediction equations are undoubtedly oversimplistic, especially in the sense that the influence
of aphids on yield reduction is likely not directly
proportional to the number of aphid-days or the
standing population. They are, however, presented
with the intention of providing, for the first time,
a reasonable estimate of the influence of "yellow"
aphids on pecan nut production and as a reference
point for determining the influence of aphids on
pecan nut production.
Discussion
All three pecan aphid species are capable of extracting large amounts of energy from a pecan tree,
with the vast majority being excreted in the form
of honeydew. This results in a low growth efficiency, and is similar to that reported for other aphid
ENTOMOLOGY
Vol. 16. no. 5
species (Dixon 1975). Because individuals of M.
caryella remove several times more energy than
M. pecanis, their control should be of greater interest to pest managers and their economic threshold should be roughly 8.4-fold lower than that of
M. pecanis. This conclusion, of course, assumes that
they have equal influences on tree physiology, which
may not be true. Currently, their influence on tree
physiology is unknown, except that both species
induce clogging of phloem cells and reduce leaf
net photosynthesis and dark respiration by approximately equal amounts per individual aphid
(Wood et al. 1985). Because the influence of a single
aphid on net photosynthesis is small (Wood & Tedders 1986) and probably insignificant relative to
the degree of energy loss via M. caryella honeydew,
it seems that the M. caryella threshold level should
indeed be considerably less than that of M. pecanis.
They are currently considered to be equally damaging and are not treated separately by pest managers. Perhaps there is some justification for this
action in that the numbers of M. pecanis normally
exceed those of M. caryella by 2- to 4-fold (Table
3) when considered for the entire growing season.
Therefore, it may be invalid to conclude that normal field populations of M. pecanis are less damaging than those of M. caryella. M. caryaefoliae
must be considered separately because it causes
severe leaf damage, greatly reduces photosynthesis,
induces leaf abscission, and must be held at low
population levels to prevent damage (Wood & Tedders 1986).
The influence of pecan aphids on the direct loss
of tree energy reserves, or photosynthate, may not
directly account for all of the large loss in tree yield
due to aphid infestation. There could also be adverse influences on tree physiological processes. Such
influences have been reported for other aphid
species and may be due to a redistribution of stored
products (Dixon 1975) or to the injection of growthregulating substances into the tree, as has been
previously observed for other aphid species (Dixon
1971a,b).
The predictions of the detrimental influence of
M. pecanis (y = 2.4lx) and M. caryella (y = 18.13x)
(where y = in-shell nut production and x = aphids
per leaf or aphid-days per leaf) on in-shell nut
production have been derived for well-managed
70-yr-old 'Stuart' trees and would not be expected
to apply strictly to trees of other ages, cultivars, or
management programs. Because the fruit/leaf area
ratio (sink to source) of a large mature tree such
as that utilized in this study is generally much less
for younger trees (as much as 8-fold), it would be
a reasonable assumption to expect that a young
tree could tolerate a proportionately greater number of M. pecanis and M. caryella aphids without
additional yield reductions. Thus, aphid thresholds
of 5- to 20-yr-old trees should be expected to be
considerably greater than those of 70-yr-old trees.
The estimates represented in this report have
been made with the intention of providing a rea-
October
1987
WOOD
ET AL.: ENERGY DRAIN BY PECAN APHIDS
sonably accurate measure of the energetics of pecan aphids and the influence of such aphids on tree
nut production.
The energetics estimates excluded
the energy contained
in exuviae, eggs, and noncarbohydrate
compounds
in honeydew;
thus, our
reported estimate of the energy consumed by aphid
populations
probably
slightly underestimates
actual energy consumption.
The estimates of the impact of standing aphids or aphid-days
on nut production
should
also be interpreted
with the
understanding
that such influences are probably
acted upon by a variety of variables in a subtle and
complex manner. A few of the important questions
that remain unanswered
address issues such as the
possibility
of differential
influences
of "yellow"
aphids on tree physiology and productivity
(other
than that of energy removal), the relative impact
of "yellow" aphids depending
upon season of infestation, the relative contribution
to nut production of infested leaves in different portions of the
tree crown, and the interaction
of "yellow" aphids
and other factors limiting photosynthesis.
Although the loss of 58.7 g of in-shell nuts per
10" J removed from the tree by feeding aphids is
an estimate of "yellow" aphid impact on 70-yr-old
'Stuart' trees, it is the first attempt
to determine
such information
in pecan culture and seems to be,
according to our experience,
representative
of observations of such orchards. Our data indicate that
aphid feeding can severely retard tree nut production, presumably
because of the removal of an
immense amount of energy from the tree and possible influences on tree physiology. Such an influence would be expected to have a major effect on
alternate
bearing and nut quality. This information, plus the knowledge of the amount of energy
removed by individual aphids, provides a first-time
estimate of the impact of different aphid levels on
nut production.
It also provides fundamental
quantitative data useful for the establishment
of both
aphid and economic threshold levels for aphicide
spra y programs.
References
Cited
Dixon, A. F. G. 1971a. The role of aphids in wood
formation. I. The effect of the sycamore aphid, Drepanosiphyan platanoides (Schr.) (Aphididae), on the
growth of sycamore, Acer pseudoplatanus
(L.). J.
Appl. Ecol. 8: 165-179.
1971b. The role of aphids in wood formation. II. The
effect of the lime aphid on the growth of lime. J.
Appl. Ecol. 8: 393-399.
1975. Aphids and translocation, pp. 154-170. In M.
H. Zimmerman & J. A. Milburn [eds.], Transport in
plants. I. Phloem transport. Springer, Berlin.
Duncan, D. B. 1955. Multiple range and multiple F
tests. Biometrics 11: 1-42.
Dutcher, J., R. Worley, J. Daniell, R. Moss & K. Harrison.
1984. Impact of six insecticide-based arthropod pest management strategies on pecan yield,
quality, and return bloom under four irrigationjsoilfertility regimes. Environ. Entomol. 13: 1644-1653.
1055
Edelson, J. & P. Estes. 1983. Intracanopy distribution
and seasonal abundance of the yellow pecan aphids
Monellia caryella and Monelliopsis nigropunctata
(Homoptera: Aphididae). Environ. Entomol. 12: 862867.
Hodge, J. & B. Hofreiter.
1962. Determination of
reducing sugars and carbohydrates, pp. 300-394. In
R. L. Whistler & J. L. Wolfrom [eds.], Methods in
carbohydrate chemistry, vol. 1. Academic, New York.
Llewellyn, M. 1972. The effects of the lime aphid,
Eucallipterus titiae L. (Aphididae), on the growth of
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ENTOMOLOGY
Received for publication
30 Apr/I
19B?
Vol. 16, no. 5
2 December 1985; accepted