Black Pecan Aphid (Hemiptera: Aphididae) Management on Pecan When Gibberellic Acid Is Applied Concurrently With Broad-Spectrum Insecticides
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Journal of Economic Entomology, 115(2), 2022, 611–617
https://doi.org/10.1093/jee/toac009
Advance Access Publication Date: 4 March 2022
Research
Horticultural Entomology
Black Pecan Aphid (Hemiptera: Aphididae) Management
on Pecan When Gibberellic Acid Is Applied Concurrently
With Broad-Spectrum Insecticides
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Ted E. Cottrell1,
USDA, Agricultural Research Service, Southeastern Fruit and Tree Nut Research Laboratory, 21 Dunbar Road, Byron, GA 31008,
USA and 1Correspondence address, e-mail: Ted.Cottrell@usda.gov
Subject Editor: Hannah Burrack
Received 30 September 2021; Editorial decision 16 January 2022
Abstract
Aphids (Hemiptera: Aphididae) are serious pests of pecan foliage (Carya illinoinensis [Wangenh.] K. Koch).
The black pecan aphid, Melanocallis caryaefoliae (Davis) (Hemiptera: Aphididae), feeds on pecan foliage
and elicits leaf chlorosis that can cause defoliation. In contrast, the blackmargined aphid, Monellia caryella
(Fitch) (Hemiptera: Aphididae), and yellow pecan aphid, Monelliopsis pecanis Bissell (Hemiptera: Aphididae),
feed on pecan foliage but do not elicit chlorotic feeding injury. Application of gibberellic acid (GA3) to pecan
foliage reduces chlorotic foliar injury and nymphal populations of the black pecan aphid. GA3 has potential to
manage black pecan aphid later in the season when broad-spectrum insecticides are used to control direct pests
of pecan nuts but also inadvertently induce aphid outbreaks. Here, broad-spectrum insecticides were used with
GA3 or aphicides in orchard trials for 2 yr. Populations of aphids and natural enemies along with chlorotic
feeding injury on foliage were assessed. When used concurrently with GA3 or aphicides, broad-spectrum in-
secticides did not flare black pecan aphid populations. However, combined populations blackmargined aphids
and yellow pecan aphids were higher in treatments with GA3 than with an aphicide or in the control treat-
ment during one of two years. Application of GA3 or the aphicide often led to significantly less chlorotic injury
than observed in the control. Surprisingly, natural enemies were not significantly affected by broad-spectrum
insecticides when applied concurrently with GA3. These results show that GA3 can be used as part of a late-
season IPM strategy to protect foliage from localized chlorotic leaf injury elicited by the black pecan aphid.
Key words: chlorosis, phytohormone, bioregulator, growth regulator
The black pecan aphid, Melanocallis caryaefoliae (Davis) (Hemiptera: Additionally, accumulation of leaf chlorosis damage results in pre-
Aphididae), is one of three aphid species attacking the foliage of mature defoliation.
pecan, Carya illinoinensis (Wangenh.) K. Koch (Juglandaceae), and Leaf feeding by the black pecan aphid involves it actively breaking
causing economic harm (Tedders 1978, Wood et al. 1987). The down chlorophyl and feeding on the resulting catabolites (Tedders
black pecan aphid injures foliage when it elicits leaf chlorosis during 1978; Cottrell et al. 2009, 2010). Using the knowledge that pecan
feeding (Lakin 1972, Cottrell et al. 2009). This species is the most cultivars exhibited varying degrees of susceptibility to the black pecan
serious pest of the three aphid species because host injury occurs aphid but yet that all cultivars were similarly susceptible later in the
at a lower pest density than for the other two species (Lakin 1972, season, Cottrell et al. (2010), theorized that endogenous levels of cer-
Tedders 1978). In fact, it is known that the black pecan aphid is tain senescence-retarding plant bioregulators in pecan foliage were af-
dependent on elicitation of leaf chlorosis during feeding for normal fecting cultivar and seasonal susceptibility to the black pecan aphid.
development. When elicitation of leaf chlorosis is prevented, aphid Those authors found that pecan foliage treated with gibberellic acid
mortality increases, survivors take longer to complete develop- (GA3) and the combination of GA3 + chlorforfenuron lessened the in-
ment, and the body length of adults is shorter (Cottrell et al. 2009). cidence of leaf chlorosis elicited by the black pecan aphid. As a proof
of concept for orchard usage, Cottrell and Wood (2021) applied GA3
Published by Oxford University Press on behalf of Entomological Society of America 2022. 611
This work is written by (a) US Government employee(s) and is in the public domain in the US.612 Journal of Economic Entomology, 2022, Vol. 115, No. 2
(chlorforfenuron is not labeled for use on pecan) to the canopy of insecticides used to target direct pests. To understand aphid popula-
pecan orchards during late summer and early autumn resulting in sig- tions dynamics under these treatments, all three pecan-feeding spe-
nificantly less chlorotic injury to foliage by the black pecan aphid. cies were sampled. To determine the effect of GA3 on leaf chlorosis
It is likely that endogenous levels of senescence-retarding plant elicited by the black pecan aphid, chlorotic leaf area was measured.
bioregulators, including GA3, decline in mature pecan foliage as the Additionally, species of the dominant aphid predator guild and an
season progress thus increasing the ability of the black pecan aphid aphid parasitoid were sampled concurrently with aphids.
to elicit senescence-like injury when feeding. In the orchard study by
Cottrell and Wood (2021), numbers of black pecan aphid nymphs
were significantly lower on foliage treated with GA3 compared with
Materials and Methods
the nontreated control. However, no effect of GA3 application was
detected regarding numbers of adult black pecan aphid nor nymphs This orchard study was done during 2016 and 2017 with methods
+ adults of the other two aphid species, i.e., the blackmargined aphid, similarly as described by Cottrell and Wood (2021) using the same
Monellia caryella (Fitch) (Hemiptera: Aphididae), and yellow pecan mature pecan orchards (USDA, ARS, Southeastern Fruit and Tree
aphid, Monelliopsis pecanis Bissell (Hemiptera: Aphididae). Nut Research Laboratory, Byron, GA), spray equipment (DW
Management of aphids on pecan generally coincides with late- 3210 orchard airblast sprayer, Durand Wayland Machinery, Inc.,
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season management of nut-attacking pests such as the pecan weevil, Reedley, CA) applying 935.4 l/ha, and insect sampling procedures.
Curculio caryae (Horn) (Coleoptera: Curculionidae), hickory Predominantly ‘Stuart’ and ‘Schley’ cultivar trees in these nearly
shuckworm, Cydia caryana (Fitch) (Lepidoptera: Tortricidae), and 100-yr-old orchards were on an 18.3 × 18.3 m spacing and tree
stink bugs (Hemiptera: Pentatomidae). Broad-spectrum insecticides, height ranged from 18 to 23 m. Four replicates, each with four 1-ha
including carbaryl and pyrethroids, are used to manage these pests, treatment plots, were used. The four treatments, described below,
especially pecan weevil and stink bugs (Wells 2020). However, the were randomly assigned to plots within a replicate.
use of broad-spectrum insecticides can flare aphid populations thus Black pecan aphid management was necessary in these orchards
requiring concurrent use of aphicide products (Wilson et al. 1999, before the treatments for late-season direct pests began. Therefore,
Chapman et al. 2009). GA3 alone was applied to all treatment plots, except the nontreated
Although it is now known that GA3 does negatively impact the control plots, each year (Table 1). Three late-season treatment re-
black pecan aphid (Cottrell et al. 2010, Cottrell and Wood 2021), it gimens and a nontreated control were used in this orchard study
is not known if GA3 will have a similar positive effect when applied during 2016 and 2017. These treatments were applied to pecan can-
to pecan orchards concurrently with insecticides that potentially opies on multiple dates (Table 1) during the late season. The treat-
flare aphid populations. Late-season black pecan aphid management ments used each year included a grower standard spray regimen
is important considering that defoliation by this pest negatively (standard) and two alternative spray regimens (BPA Alt1 and
impacts the nut crop the following season and aphid resistance to BPA Alt2) for management of late-season direct pests and aphids.
neonicotinoid insecticides is suspected in many grower orchards. A nontreated control was also included. The standard treatment in-
Thus, the objective of this study was to examine whether two dif- cluded aphicides for management of all pecan-feeding aphid species
ferent rates of GA3 could be used to manage the black pecan aphid but BPA Alt1 and BPA Alt2 used GA3 specifically targeting the black
when applied to the pecan canopy concurrently with broad-spectrum pecan aphid (Table 1).
Table 1. Application date and broad-spectrum insecticide treatments applied to manage late-season direct pests of pecan when used with
either a standard aphicide program or two different rates of gibberellic acid for black pecan aphid management
Treatment
Year Application date Standard BPAa Alt1b BPA Alt2c
2016 15 Jul. GA3d GA3 GA3
04 Aug. GA3 GA3 GA3
19 Aug. Carbaryle + Imidaclopridf Carbaryl + GA3 Carbaryl + GA3
23 Aug. Bifenthring + Flonicamidh Bifenthrin + GA3 Bifenthrin + GA3
31 Aug. Carbaryl + Imidacloprid Carbaryl + GA3 Carbaryl + GA3
14 Sep. Bifenthrin + Flonicamid Bifenthrin + GA3 Bifenthrin + GA3
28 Sep. Imidacloprid GA3 GA3
2017 28 Jul. GA3 GA3 GA3
14 Aug. Carbaryl + Sulfoxaflori Carbaryl + GA3 Carbaryl + GA3
25 Aug. Bifenthrin + Imidacloprid Bifenthrin + GA3 Bifenthrin + GA3
08 Sep. Carbaryl + Sulfoxaflor Carbaryl + GA3 Carbaryl + GA3
22 Sep. Bifenthrin + Imidacloprid Bifenthrin + GA3 Bifenthrin + GA3
a
BPA, black pecan aphid, Melanocallis caryaefoliae (Hemiptera: Aphididae).
b
Alt1, alternative 1 using gibberellic acid applied at 49.5 g active ingredient/ha.
c
Alt2, alternative 2 using gibberellic acid applied at 98.8 g active ingredient/ha.
d
GA3, gibberellic acid.
e
Carbaryl applied at 5.6 kg active ingredient/ha.
f
Imidacloprid applied at 105.1 g active ingredient/ha.
g
Bifenthrin applied at 112.5 g active ingredient/ha.
h
Flonicamid applied at 196.2 g active ingredient/ha.
i
Sulfoxaflor applied at 34.6 g active ingredient/ha.Journal of Economic Entomology, 2022, Vol. 115, No. 2 613
The standard regimen used rotation of the broad-spectrum 7.0, Media Cybernetics, Inc., Rockville, MD) per methodology of
insecticides carbaryl (Carbaryl 4L, 0.48-kg active ingredient/l, Cottrell et al. (2010) and Cottrell and Wood (2021).
Loveland Products, Inc., Greeley, CO) and bifenthrin (Fanfare 2EC, To meet assumptions of normality, insect data were transformed
0.24 kg active ingredient/l, Makhteshim Agan of North America, using log (X + 1) and a univariate repeated-measures ANOVA com-
Inc., Raleigh, NC) with imidacloprid (Mana Alias 4F, 0.48 kg ac- pared treatment effects across dates for the following: black pecan
tive ingredient/l, Makhteshim Agan of North America, Inc., Raleigh, aphid nymphs, black pecan aphid adults, adults and nymphs of
NC or Wrangler, 0.48 kg active ingredient/l, Loveland Products, Inc., both the blackmargined aphid and the yellow pecan aphid, the com-
Greeley, CO), flonicamid (Carbine 50WG, 0.5 g active ingredient/g, bined life stages of lady beetles and lacewings, and aphid mummies.
FMC Corporation, Philadelphia, PA), or sulfoxaflor (Closer SC, Furthermore, cumulative data for black pecan aphid nymphs, black
0.24 kg active ingredient/l, Corteva Agriscience, Wilmington, DE). pecan aphid adults, and combined adults and nymphs of both the
BPA Alt1 and BPA Alt2 also used carbaryl and bifenthrin in rotation blackmargined pecan aphid and the yellow pecan aphid, and the
but each of these treatment regimens used a different rate of GA3 combined life stages of lady beetles and lacewings, and aphid mum-
(ProGibb LV Plus, 0.068 g active ingredient/ml, Valent Biosciences mies were subjected to one-way analysis of variance (ANOVA) fol-
Corporation, Libertyville, IL; Table 1). The two rates of GA3 used lowing data transformation, i.e., log (X+1), to meet assumptions of
in the current study fall within the range of rates for GA3 prod- normality. If a significant treatment effect was detected (P ≤ 0.05),
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ucts labeled for use on pecan (24.71–98.84 g a.i./ha). Treatment mean separation was done using Tukey’s Honestly Significant
regimens began on 15 July 2016 and 28 July 2017, but the first Difference (HSD) test. For each leaf collection date during 2016 and
broad-spectrum insecticide was not used until 19 August 2016 and 2017, a one-way ANOVA was used to examine treatment effects on
14 August 2017, coinciding with adult pecan weevil emergence. The percentage leaf chlorosis. Mean separation was done with Tukey’s
last application was on 28 September 2016 and 22 September 2017 Honestly Significant Difference (HSD) test (JMP 1989–2021) if a
(Table 1). significant treatment effect was detected (P ≤ 0.05). All analyses were
Each time after treatments were applied, nymphs and adults of conducted using JMP (1989–2021).
all pecan-feeding aphid species were sampled. Predominant natural
enemy species, i.e., species of lacewings (Neuroptera: Chrysopidae)
and lady beetles (Coleoptera: Coccinellidae), were sampled concur- Results
rently on foliage. The same number of days elapsing between treat- Black pecan aphid nymph sampling showed a significant treatment ×
ment application and insect sampling each time was not possible date interaction across the season during 2016 (F = 3.30; df = 18, 72;
because of inclement weather and availability of articulating boom P = 0.0002; Fig. 1A) and 2017 (F = 45.79; df = 12, 48; P < 0.0001;
lifts (450 AJ, JLG Industries, Inc., McConnellsburg, PA) for sam- Fig. 1B). A significant treatment effect on black pecan aphid nymphs
pling. Thus, sampling was done 9.7 or 13.4 d after treatment in 2016 was seen when cumulative data were analyzed during 2016 (F = 7.06;
and 2017, respectively, with the final sample taken 20 or 25 d after df = 3, 9; P = 0.0098), with higher counts in both the control and
the final treatment, respectively. During 2017, heavy rain and strong BPA Alt1 treatments than in the standard treatment (Fig. 2A). Counts
winds from Hurricane Irma prevented a planned sample date during for the BPA Alt2 treatment were similar to all treatments (Fig. 2A).
mid-September. All insect samples were taken from 6 to 7.5 m above A similar significant treatment effect was observed during 2017
ground where pecan foliage receives the expected treatment volume (F = 58.56; df = 3, 9; P < 0.0001), with significantly higher black
from the sprayer (when compared with a lower volume reaching pecan aphid nymph numbers in the control than the other treatments.
the upper pecan canopy; Bock et al. 2015). Low limbs reachable However, black pecan aphid nymph numbers in BPA Alt1 and BPA
from the ground were not sampled because their availability on Alt2 were low like the standard treatment (Fig. 2B).
every tree was not consistent. Ten compound leaves from around the Similar to nymphs, adult black pecan aphids had a signifi-
tree periphery were randomly selected from each of four trees within cant treatment × date interaction across dates in 2016 and 2017
the center of each plot. Adults and nymphs of each aphid species (F = 3.75; df = 18,72; P < 0.0001 and F = 25.13; df = 12, 48;
were counted separately except for nymphs of the blackmargined P < 0.0001, respectively; Fig. 1C and D). There was no treatment ef-
aphid and the yellow pecan aphid which were combined. Under field fect for cumulative black pecan aphid adults during 2016 (F = 1.23;
sampling conditions, the nymphs of the blackmargined aphid and df = 3, 9; P = 0.3453), but there was for 2017 (F = 24.31; df = 3, 9;
yellow pecan aphid are difficult to separate. At the same time, all P = 0.0001). Numbers of black pecan aphid adults were significantly
stages of lady beetles and lacewings were recorded. In all, aphids greater in the control than other treatments during 2017 (Fig. 2C
and predators were sampled on seven and five dates during 2016 and D).
and 2017, respectively. During 2017 only, aphid mummies resulting In contrast with the black pecan aphid nymphs and adults, no
from blackmargined aphids and yellow pecan aphids parasitized by significant treatment × date interaction was observed in 2016 or
Aphelinus perpallidus Gahan (Hymenoptera: Aphelinidae) were also 2017 (F = 3.83; df = 18, 72; P < 0.0001 or F = 5.89; df = 12, 48;
counted; hymenopteran parasitoids of the black pecan aphid are P < 0.0001, respectively) for all life stages of the blackmargined aphid
not known. and the yellow pecan aphid combined (Fig. 1E and F). However, a
Leaf chlorosis elicited through black pecan aphid feeding was significant treatment effect on these aphids was revealed from cumu-
examined on two dates both years (13 September and 5 October lative data analyses for 2016 (F = 17.80; df = 3, 9; P = 0.0004), but
2016 and 26 August and 26 September 2017). The damage was as- not 2017 (F = 1.72; df = 3, 9; P = 0.2316; Fig. 2E and F). During
sessed on compound leaves randomly selected from the insect sample 2016, their numbers were significantly higher for BPA Alt1 and BPA
trees in a plot (n = 16 leaves per treatment). All leaves were selected Alt2 than in the control or standard treatments (Fig. 2E).
from the same height from which insects were sampled. The leaves Most predator samples were comprised of Olla v-nigrum
were brought into the laboratory, scanned (HP Scanjet 8300 Digital (Mulsant) (Coleoptera: Coccinellidae), Harmonia axyridis (Pallas)
Flatbed Scanner, Hewlett-Packard Inc., Palo Alto, CA) and per- (Coleoptera: Coccinellidae), and lacewings, predominantly
centage leaf chlorosis measured (Image Pro Plus, Software version Chrysoperla rufilabris Burmeister (Neuroptera: Chrysopidae).614 Journal of Economic Entomology, 2022, Vol. 115, No. 2
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Fig. 1. 2016 and 2017 seasonal means for black pecan aphid (BPA) nymphs (A, B) and adults (C, D), combined blackmargined aphids and yellow pecan aphids
(BMA and YPA) (E, F), and predators (G, H). Pecan foliage was treated with a broad-spectrum insecticide and gibberellic acid at two rates (i.e., black pecan aphid
alternative 1 [BPA Alt1] and black pecan aphid alternative 2 [BPA Alt2]) or an aphicide (i.e., standard) on four dates beginning 19 August in 2016 and 14 August
in 2017. Aphids were sampled 9.7 and 13.4 d after treatment application during 2016 and 2017, respectively. Gibberellic acid only was applied to BPA Alt1, BPA
Alt2, and standard treatments on 15 July and 4 August in 2016 and 28 July in 2017. A late-season application of gibberellic acid (BPA Alt1 and BPA Alt2) and an
aphicide (standard) was applied on 28 September in 2016.
Combined life stages of all predators sampled across dates had a for 26 August (F = 18.39; df = 3, 9; P = 0.0004) and 26 September
significant treatment × date interaction in 2016 (F = 2.34; df = 18, (F = 107.30; df = 3, 9; P < 0.0001; Fig. 4C and D).
72; P = 0.0059) and 2017 (F = 9.74; df = 12, 48; P < 0.0001; Fig.
1G and H). However, no treatment effect on predators was detected
Discussion
during 2016 (F = 2.53; df = 3, 9; P = 0.1223) or 2017 (F = 2.25;
df = 3, 9; P = 0.1521) when cumulative data were analyzed (Fig. 2G Application of GA3 to pecan foliage is a unique method to lessen
and H). No treatment × date interaction or effect of treatment alone chlorotic foliar injury resulting from the feeding activity of the black
was detected for the combined number of parasitized blackmargined pecan aphid (Cottrell et al. 2010, Cottrell and Wood 2021). However,
aphids and yellow pecan aphids during 2017 (F = 1.71; df = 12, 48; this beneficial effect had not been tested when applied concurrently
P = 0.0931 or F = 1.84; df = 3, 12; P = 0.1934). However, sample with broad-spectrum insecticides used to control late-season pests of
date did have a significant effect on parasitized aphids (F = 9.97; pecan nuts. Generally, aphid management is needed when applying
df = 4, 48; P < 0.0001) when significantly more mummies were sam- these broad-spectrum insecticides because of the negative impact on
pled on 25 August than on 4 and 19 October (Fig. 3A). No effect of natural enemies often leading to subsequent aphid population in-
treatment on numbers of aphid mummies was observed when cumu- creases on the treated crop. Dutcher and Payne (1983) documented
lative data were analyzed (F = 2.99; df = 3, 15; P = 0.0885; Fig. 3B). aphid resurgence on pecan following carbaryl treatment for pecan
Significantly less leaf chlorosis was observed for BPA Alt1 weevil. The approach to black pecan aphid management in the cur-
when compared with the nontreated control for the 13 September rent study used GA3 similarly as pecan growers would use an aphi-
and 5 October leaf collection dates during 2016 (F = 4.72; df = 3, cide when applying broad-spectrum insecticides.
9; P = 0.0303 and F = 15.40; df = 3, 9; P = 0.0007, respectively). The black pecan aphid is most often a late-season pest, but,
However, no difference in leaf chlorosis was detected between BPA in some years, economically injurious populations precede pecan
Alt1, BPA Alt2, and the standard treatment for either date (Fig. 4A weevil emergence and require management (Moznette 1933, Cottrell
and B). During 2017, BPA Alt1, BPA Alt2, and the standard treat- and Wood 2021). Therefore, GA3 was applied to treatment plots, but
ment had significantly less leaf chlorosis than the nontreated control not control plots, before pecan weevil emergence. It is unlikely thatJournal of Economic Entomology, 2022, Vol. 115, No. 2 615
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Fig. 2. 2016 and 2017 mean (± SE) of cumulative black pecan aphid (BPA) nymphs (A, B) and adults (C, D), combined blackmargined aphids and yellow pecan
aphids (BMA and YPA) (E, F), and predators (G, H) on pecan foliage. Pecan foliage was treated with a broad-spectrum insecticide and gibberellic acid at two
rates (i.e., black pecan aphid alternative 1 [BPA Alt1] and black pecan aphid alternative 2 [BPA Alt2]) or an aphicide (i.e., standard) on four dates beginning 19
August in 2016 and 14 August in 2017. Aphids were sampled 9.7 and 13.4 d after treatment application during 2016 and 2017, respectively. Gibberellic acid only
was applied to BPA Alt1, BPA Alt2, and standard treatments on 15 July and 4 August in 2016 and 28 July in 2017. A late season application of gibberellic acid (BPA
Alt1 and BPA Alt2) and an aphicide (standard) was applied on 28 September in 2016. Different letters above columns indicate significant difference (P < 0.05,
Tukey’s HSD) between treatments.
residual effects of this early GA3 application affected later results pecan aphid. Cottrell and Wood (2021) found that orchard applica-
when GA3 was applied with broad-spectrum insecticides (T.E.C., un- tion of GA3 significantly reduced populations of black pecan aphid
published data). Using an aphicide with systemic or translaminar nymphs, but not adults. In the current study, both GA3 treatment
activity or even a broad-spectrum insecticide may have led to longer rates (i.e., BPA Alt1 and BPA Alt2) had lower black pecan aphid
residual activity against aphids or possibly flaring aphid popula- nymph and adult populations than the control during 2017, but not
tions, thus GA3 was the best solution. during 2016. Except for BPA Alt1 (i.e., the lower rate of GA3) during
Because black pecan aphid nymphs require 2–3 d of sedentary 2016, populations of nymphs and adults were like the standard
behavior at a feeding site to begin chlorophyl breakdown, GA3 has treatment. Conversely, cumulative combined blackmargined aphid
a more pronounced effect on nymphs than adults (Cottrell 2010, and yellow pecan aphid abundance was significantly higher in BPA
Paulsen et al. 2013, Cottrell and Wood 2021). Nymphs able to elicit Alt1 and BPA Alt2 treatments than the control during 2016, but
leaf chlorosis develop faster and result in larger adults than those not during 2017. Their higher abundance was not surprising because
nymphs deprived of feeding on chlorotic foliage (Cottrell et al. the blackmargined aphid and yellow pecan aphids do not elicit leaf
2009). To increase survival by remaining sedentary, about 50% of chlorosis and thus GA3 has no direct effect on them.
first instars practice a bet-hedging strategy by moving to the upper As indicated by numbers for the controls, aphid populations
leaf surface, similarly as described by Hopkins and Dixon (1997), varied between the two years. All aphid species experienced a similar
to avoid natural enemies that spend more time searching the lower late August peak during 2017 that was not as pronounced for those
leaf surface of pecan foliage (Paulsen et al. 2013). Alate black pecan treatments that included insecticides. This likely indicates that
aphids occur more frequently on the lower leaf surface as do the the broad-spectrum insecticides, in addition to the aphicide in the
nymphs and adults of the blackmargined aphid and the yellow standard treatment, had a negative effect on aphids. When observing616 Journal of Economic Entomology, 2022, Vol. 115, No. 2
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Fig. 3. (A) Seasonal occurrence and (B) mean (± SE) of cumulative mummies
of blackmargined aphids and yellow pecan aphids parasitized by Aphelinus
perpallidus (Hymenoptera: Aphelinidae). Foliage was treated concurrently
with a broad-spectrum insecticide and two rates of gibberellic acid (i.e.,
black pecan aphid alternative 1 [BPA Alt1] and black pecan aphid alternative
2 [BPA Alt2]) or an aphicide (i.e., standard) on four dates beginning 14 August
2017. Mummies were sampled 13.4 d after treatment application. Gibberellic
acid only was applied to BPA Alt1, BPA Alt2, and standard treatments on 28
July. Different letters above columns indicate significant difference (P < 0.05,
Tukey’s HSD) between treatments.
Fig. 4. Percentage leaf chlorosis elicited by the black pecan aphid on (A) 13
black pecan aphid nymph and adult populations across the season, September 2016, (B) 5 October 2016, (C) 26 August 2017, and (D) 26 September
numbers in the BPA Alt1 and BPA Alt2 treatments were generally 2017. Foliage was treated concurrently with a broad-spectrum insecticide and
higher than numbers in the control. It is likely that their numbers two rates of gibberellic acid (i.e., black pecan aphid alternative 1 [BPA Alt1]
and black pecan aphid alternative 2 [BPA Alt2]) or an aphicide (i.e., standard)
were flared by the broad-spectrum insecticides later in the season
on four dates beginning 19 August in 2016 and 14 August in 2017. Different
during 2016, but not during 2017. letters above columns indicate significant difference (P < 0.05, Tukey’s HSD)
Cumulative predator data in the control and in the treatments with between treatments.
broad-spectrum insecticides were always similar. Except for lagging,
natural enemy population changes tended to mirror aphid changes treatment was less than the control, except for the first sample date
across the season for each respective treatment. Similarly, numbers of in 2016. The standard treatment never resulted in less chlorotic fo-
mummies of the blackmargined aphid and yellow pecan aphid (para- liar injury than either BPA Alt1 or BPA Alt2. Without examining
sitized by A. perpallidus) were not significantly different among treat- leaf chlorosis, black pecan aphid abundance does not provide a true
ments. In fact, a sharp decline in mummies in all treatments mirrored a measure of this pest when using GA3.
similar decline in aphid numbers. Where insecticides were used, aphid This study demonstrates the utility of GA3 as part of a pest man-
presence presumably allowed A. perpallidus to persist. In fact, Slusher agement program for black pecan aphid management in pecan or-
et al. (2021) reported no differences in adult A. perpallidus and aphid chards. Results from this study indicate that the lower rate of GA3
mummies between nontreated trees and trees treated with the aphicides (i.e., BPA Alt1) affects the black pecan aphid similarly as the higher
flonicamid, sulfoxaflor, or afidopyropen. D’Ávila et al. (2018) suggest rate. Whether used alone (Cottrell and Wood 2021) or concurrently
that because of low toxicity of the insecticide lambda-cyhalothrin with broad-spectrum insecticides, exogenous application of GA3 in-
to the aphid parasitoid, Aphidius colemani Viereck (Hymenoptera: creases pecan foliage tolerance to the black pecan aphid by reducing
Braconidae), both can be used in IPM programs against aphids. Even if detrimental chlorosis, senescence, and abscission processes of leaves.
the insecticides used in this study had a negative effect on A. perpallidus, It is likely that this unique application of a plant bioregulator for
it is possible that higher aphid abundance in these plots attracted and/ pest management may extend to other insect species eliciting chlor-
or arrested A. perpallidus from nearby pecan orchards thus masking otic feeding injury to host plants.
the effect of the insecticides on A. perpallidus.
It is interesting that regardless of aphid numbers (except for
BPA Alt2 on the first leaf sample date of 2016) percentage chlor-
Acknowledgments
otic leaf area was significantly less for BPA Alt1 and BPA Alt2 than The author would like to thank Merry Bacon, Rebekah Hartley,
the control. Similarly, the percentage chlorotic area for the standard Chace Morrill, and Saleah Starks (USDA, ARS, Southeastern FruitJournal of Economic Entomology, 2022, Vol. 115, No. 2 617
and Tree Nut Research Laboratory, Byron, GA) for technical as- D’Ávila, V. A., W. F. Barbosa, R. N. C. Guedes, and G. C. Cutler. 2018. Effects
sistance. Funding for this research was provided in part by the of Spinosad, imidacloprid, and lambda-cyhalothrin on survival, para-
Georgia Agricultural Commodity Commission for Pecans. The U.S. sitism, and reproduction of the aphid parasitoid Aphidius colemani. J.
Econ. Entomol. 111: 1096–1103.
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cense in and to any copyright of this article. This article reports
methoate, and dialifor on foliar and nut pests of pecan orchards. J.
the results of research only. Mention of trade names or commercial
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the U.S. Department of Agriculture. JMP®, SAS Institute Inc., Cary, NC. 1989–2021. Version 14.3.
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