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Article
Intercropping Rosemary (Rosmarinus officinalis) with Sweet
Pepper (Capsicum annum) Reduces Major Pest Population
Densities without Impacting Natural Enemy Populations
Xiao-wei Li 1, Xin-xin Lu 1, Zhi-jun Zhang 1, Jun Huang 1, Jin-ming Zhang 1, Li-kun Wang 1,
Muhammad Hafeez 1, G. Mandela Fernández-Grandon 2and Yao-bin Lu 1,*
Citation: Li, X.-w.; Lu, X.-x.; Zhang,
Z.-j.; Huang, J.; Zhang, J.-m.; Wang,
L.-k.; Hafeez, M.; Fernández-Grandon,
G.M.; Lu, Y.-b. Intercropping Rosemary
(Rosmarinus officinalis) with Sweet
Pepper (Capsicum annum) Reduces
Major Pest Population Densities
without Impacting Natural Enemy
Populations. Insects 2021,12, 74.
https://doi.org/10.3390/insects
12010074
Received: 7 December 2020
Accepted: 13 January 2021
Published: 15 January 2021
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional clai-
ms in published maps and institutio-
nal affiliations.
Copyright: © 2021 by the authors. Li-
censee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products,
Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences,
Hangzhou 310021, China; lixiaowei1005@163.com (X.-w.L.); lxx2026383726@126.com (X.-x.L.);
zhijunzhanglw@hotmail.com (Z.-j.Z.); junhuang1981@aliyun.com (J.H.); zhanginsect@163.com (J.-m.Z.);
wanglikun1314@sina.cn (L.-k.W.); drhafeez@webmail.hzau.edu.cn (M.H.)
2Natural Resources Institute, University of Greenwich, Chatham Maritime, Kent ME4 4TB, UK;
m.fernandez-grandon@greenwich.ac.uk
*Correspondence: luybcn@163.com; Tel./Fax: +86-517-8640-4225
Simple Summary:
Due to the harmful effects of pesticides on the environment and human health,
alternative control methods have become more favored in vegetable pest management. Intercropping
and natural enemy release are two widely implemented environmentally friendly control methods.
In this study, the impact of sweet pepper/rosemary intercropping on pest population suppression
was evaluated under greenhouse conditions and the effect of rosemary intercropping on natural
enemy population dynamics was investigated. The results showed that intercropping rosemary with
sweet pepper significantly reduced the population densities of three major pest species on sweet
pepper, Frankliniella intonsa,Myzus persicae, and Bemisia tabaci, but did not affect the population
densities of released natural enemies, predatory bug Orius sauteri, and parasitoid Encarsia formosa.
Significant pest population suppression with no adverse effect on released natural enemy populations
in the sweet pepper/rosemary intercropping system suggests this could be an approach for integrated
pest management of greenhouse-cultivated sweet pepper.
Abstract:
Intercropping of aromatic plants provides an environmentally benign route to reducing pest
damage in agroecosystems. However, the effect of intercropping on natural enemies, another element
which may be vital to the success of an integrated pest management approach, varies in different
intercropping systems. Rosemary, Rosmarinus officinalis L. (Lamiaceae), has been reported to be
repellent to many insect species. In this study, the impact of sweet pepper/rosemary intercropping on
pest population suppression was evaluated under greenhouse conditions and the effect of rosemary
intercropping on natural enemy population dynamics was investigated. The results showed that
intercropping rosemary with sweet pepper significantly reduced the population densities of three
major pest species on sweet pepper, Frankliniella intonsa,Myzus persicae, and Bemisia tabaci, but did not
affect the population densities of their natural enemies, the predatory bug, Orius sauteri, or parasitoid,
Encarsia formosa. Significant pest population suppression with no adverse effect on released natural
enemy populations in the sweet pepper/rosemary intercropping system suggests this could be
an approach for integrated pest management of greenhouse-cultivated sweet pepper. Our results
highlight the potential of the integration of alternative pest control strategies to optimize sustainable
pest control.
Keywords:
aromatic plants; habitat manipulation; biological control; pest densities; natural en-
emy densities
Insects 2021,12, 74. https://doi.org/10.3390/insects12010074 https://www.mdpi.com/journal/insects
Insects 2021,12, 74 2 of 13
1. Introduction
Due to the harmful effects of synthetic pesticides on the environment and human
health, in addition to reduced efficacy due to resistance within pest populations, alternative
control methods have become more favored in the framework of integrated pest manage-
ment (IPM) [
1
]. Two widely implemented systems within IPM are the “push–pull” strategy
and the introduction of biological control agents to achieve sustainable control [
2
,
3
]. The ma-
nipulation of insect behavior via plant volatiles is one of the key components of push–pull
strategies [
4
–
6
]. Insects use plant volatiles to locate and recognize potential plant hosts for
feeding and oviposition [
7
,
8
]. Accordingly, some non-host plants (e.g., aromatic plants)
emit volatiles with repellent or deterrent properties as a defense against attack [
9
] and could
be used to develop insect repellents, antifeedants, or insecticides [
10
,
11
]. Alternatively,
non-host plants could disrupt host-plant finding and host-plant acceptance behavior by
providing insects with a choice of green surfaces on which to land (host and non-host plant
leaves), according to the ‘appropriate/inappropriate landings theory’ [
12
–
14
]. For these
reasons, aromatic plants have been frequently used as intercrops to reduce pest damage
to cultivated plants [
15
–
19
]. Intercropping aromatic plants could also increase the effi-
ciency of biological control by attracting natural enemies to the area [
20
,
21
], providing food
resources [
15
,
17
], or offering shelter and oviposition sites [
21
]. However, intercropping
does not invariably result in an improvement in biological control [
22
,
23
]. For instance,
in wheat-based intercropping systems, although pest abundance was significantly reduced,
regulation through natural enemies was not necessarily enhanced [
24
]. Another study
demonstrated that intercropping actively reduces the nocturnal biological control of aphids
in a collard greens/parsley plants intercropping system [
25
]. Consequently, in order to
optimize pest control in intercropping systems, the effects of intercropped plants on both
pests and natural enemies should be evaluated and implemented on a case-by-case basis.
Rosemary (Rosmarinus officinalis L.) (Lamiaceae) is an aromatic plant mainly cul-
tivated in the Mediterranean region. The plant, and its essential oil, are widely used
for ornamental, culinary, cosmetic, and medicinal purposes [
26
–
28
]. The volatile com-
pounds released by rosemary and its essential oils have been elucidated through several
studies [
29
–
34
]. Although their composition varies among different studies [
29
–
34
], a com-
mon feature is that they all show
α
-pinene, eucalyptol (1,8-cineole), camphor, camphene,
and verbenone as the most abundant compounds. The behavioral response of several
pests to rosemary volatiles has been evaluated with an aim to develop an effective push–
pull strategy [
35
,
36
]. Rosemary volatiles have been reported to be repellent to spider
mites Tetranychus urticae Koch (Acari: Tetranychidae) [
37
], aphids Myzus persicae (Sulzer),
and Neotoxoptera formosana (Takahashi) (Hemiptera: Aphididae) [
38
–
40
], whitefly Bemisia
tabaci Gennadius (Hemiptera: Aleyrodidae) [
32
], thrips Thrips tabaci Lindeman and Franklin-
iella occidentalis (Thysanoptera: Thripidae) [
31
,
41
,
42
], the tea green leafhopper Empoasca
vitis Gothe (Hemiptera: Cicadellidae) [
33
], and the tea geometrid Ectropis obliqua (Prout)
(Lepidoptera: Geometridae) [
34
]. Consequently, rosemary has been used as an intercrop
for reducing insect damage in the agricultural and horticultural systems in sweet pepper
(Capsicum annuum L., Solanaceae) [
43
,
44
] and tea [Camellia sinensis (L.) O. Kuntze, Theaceae]
fields [
33
,
34
]. A study in tea plantations found no effect of rosemary on generalist predator
populations (spiders, ladybirds, and lacewings) [
33
]; however, beyond this example, previ-
ous studies have overlooked the implications rosemary may have on natural enemies with
none exploring impacts on parasitoid success.
Sweet pepper (Capsicum annuum L., Solanaceae) is one of the most important hor-
ticulture crops globally [
45
]. It is susceptible to a range of pests, with thrips, whiteflies,
and aphids considered the most important [
45
]. Currently, sustainable pest management in
greenhouse-cultivated sweet pepper is mainly based on biological control [
46
,
47
]. Predatory
bugs from the Orius genus are not only the most important natural enemies for thrips [
48
],
but also contribute to the control of whiteflies [
49
] and aphids [
50
]. In addition to the Orius
species, the parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae) has been used
successfully to control whiteflies, including Trialeurodes vaporariorum Westwood and Bemisia
Insects 2021,12, 74 3 of 13
tabaci Gennadius (Hemiptera: Aleyrodidae) [
51
,
52
]. Biological control is primarily used as
part of an IPM approach and therefore its compatibility with other control methods could
be key to sustainable suppression of the pest populations. In the present study, we com-
bined rosemary intercropping and the release of biological control agents (predatory bug,
Orius sauteri (Poppius) (Hemiptera: Anthocoridae), and parasitoid, Encarsia formosa) to con-
trol pests on sweet pepper. The impacts of these two control strategies on pest population
suppression were evaluated. In addition, the effect of rosemary intercropping on natural
enemies’ population dynamics was investigated. This study confirms the viability of this
strategy for IPM in sweet pepper systems.
2. Materials and Methods
2.1. Field Setup
This study was conducted in a greenhouse (45 m
×
15 m) at the Experimental Station
of Zhejiang Academy of Agricultural Sciences, Jiaxing, Zhejiang, China (120
◦
24
0
38.70” E,
30
◦
27
0
4.28” N) in 2020. The experimental area in the greenhouse was divided into 12 plots
(Figure 1). Plots (1 m
×
12 m) were spaced 2 m apart from each other based on the results
from previous studies [
42
,
44
]. The two planting systems, sweet pepper monoculture and
sweet pepper/rosemary intercropping, were alternatingly represented throughout the
glasshouse providing six plots of each (Figure 1).
Insects2021,12,xFORPEERREVIEW3of13
beenusedsuccessfullytocontrolwhiteflies,includingTrialeurodesvaporariorumWest‐
woodandBemisiatabaciGennadius(Hemiptera:Aleyrodidae)[51,52].Biologicalcontrol
isprimarilyusedaspartofanIPMapproachandthereforeitscompatibilitywithother
controlmethodscouldbekeytosustainablesuppressionofthepestpopulations.Inthe
presentstudy,wecombinedrosemaryintercroppingandthereleaseofbiologicalcontrol
agents(predatorybug,Oriussauteri(Poppius)(Hemiptera:Anthocoridae),andparasitoid,
Encarsiaformosa)tocontrolpestsonsweetpepper.Theimpactsofthesetwocontrolstrat‐
egiesonpestpopulationsuppressionwereevaluated.Inaddition,theeffectofrosemary
intercroppingonnaturalenemies’populationdynamicswasinvestigated.Thisstudycon‐
firmstheviabilityofthisstrategyforIPMinsweetpeppersystems.
2.MaterialsandMethods
2.1.FieldSetup
Thisstudywasconductedinagreenhouse(45m×15m)attheExperimentalStation
ofZhejiangAcademyofAgriculturalSciences,Jiaxing,Zhejiang,China(120°24′38.70″E,
30°27′4.28″N)in2020.Theexperimentalareainthegreenhousewasdividedinto12plots
(Figure1).Plots(1m×12m)werespaced2mapartfromeachotherbasedontheresults
frompreviousstudies[42,44].Thetwoplantingsystems,sweetpeppermonocultureand
sweetpepper/rosemaryintercropping,werealternatinglyrepresentedthroughoutthe
glasshouseprovidingsixplotsofeach(Figure1).
Figure1.Schematicrepresentationoftheexperimentalgreenhouse.Theexperimentalareainthegreenhousewasdivided
into12plots(1m×12m),whichwerespaced2mapartfromeachother.Ineachplot,sweetpepperplantswereseparated
by40cmanddistributedamongtworowsspacedat40cm.Rosemaryplantswereplantedattheouteredgesofeach
intercroppingplot,witha30cmdistancefromthesweetpepperand40cminrows.
Sweetpepperplants(Capsicumannuumvar.Luojiaochengyan115)weresowninplas‐
ticnurserypotson15April2020inaseparategreenhousenurseryandtransplantedinto
theexperimentalgreenhouseon18May2020,whentheseedlingswereatthefourtosix
trueleavesstage.Ineachplot,sweetpepperplantswereseparatedby40cmanddistrib‐
utedamongtworowsspacedat40cm.Rosemary(R.officinalisvar.Zhili)seedlings(one
totwoyearsold,15–20cminheight)wereboughtfromanurseryinShouguang,Shan‐
dong,China.Rosemaryplantsweretransplantedtotheouteredgesofeachintercropping
plot,witha30cmdistancefromthesweetpepperand40cminrows.Duringtheexperi‐
ment,conventionalfertilizationandirrigationwerecarriedout,andnoinsecticides,fun‐
gicides,orherbicideswereusedintheexperimentalarea.
Figure 1.
Schematic representation of the experimental greenhouse. The experimental area in the greenhouse was divided
into 12 plots (1 m
×
12 m), which were spaced 2 m apart from each other. In each plot, sweet pepper plants were separated
by 40 cm and distributed among two rows spaced at 40 cm. Rosemary plants were planted at the outer edges of each
intercropping plot, with a 30 cm distance from the sweet pepper and 40 cm in rows.
Sweet pepper plants (Capsicum annuum var. Luojiaochengyan115) were sown in plastic
nursery pots on 15 April 2020 in a separate greenhouse nursery and transplanted into the
experimental greenhouse on 18 May 2020, when the seedlings were at the four to six true
leaves stage. In each plot, sweet pepper plants were separated by 40 cm and distributed
among two rows spaced at 40 cm. Rosemary (R. officinalis var. Zhili) seedlings (one to
two years old, 15–20 cm in height) were bought from a nursery in Shouguang, Shandong,
China. Rosemary plants were transplanted to the outer edges of each intercropping plot,
with a 30 cm distance from the sweet pepper and 40 cm in rows. During the experiment,
conventional fertilization and irrigation were carried out, and no insecticides, fungicides,
or herbicides were used in the experimental area.
Insects 2021,12, 74 4 of 13
2.2. Natural Enemies Release
Predatory bug Orius sauteri adults and nymphs were purchased from Henan Jiyuan
Baiyun Industrial Co., Ltd. (Jiyuan, China). Orius sauteri individuals were evenly released
to all the plots at the second and third weeks (June 1 and June 8, to ensure the colonization
of O. sauteri in the field) after transplantation at a release density of three individuals/m
2
(plot area). Adults of the parasitoid Encarsia formosa were purchased from Woofutech
Bio-control Co., Ltd. Trialeurodes vaporariorum nymph cards with parasitoids were evenly
released to all the plots when the whitefly density was five individuals (adults and nymphs)
per leaf on sweet pepper leaves (June 29). The release density was 20 individuals/m
2
(plot area).
2.3. Sampling of Pests and Natural Enemies on Sweet Pepper
The pest infestation samplings were conducted every week after transplantation until
the end of the experiment (11 weeks). The major pests on sweet pepper in our greenhouse
were thrips (Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae)), aphids (Myzus persi-
cae), and whiteflies (Bemisia tabaci). In each plot, three sweet pepper plants were randomly
selected (at least four plants away from edges) and the number of M. persicae (adults and
nymphs), B. tabaci (adults) and parasitoids E. formosa (adults) on five leaves at different
directions of each plant were recorded. Because F. intonsa and predator bug O. sauteri
were mainly distributed in sweet pepper flowers, 15 flowers (one to two flowers per plant,
10 to 15 plants in total) were randomly selected in each plot (at least four plants away
from edges) and the number of thrips (adults and nymphs) and O. sauteri (adults and
nymphs) were recorded. The mean number of individuals of each species per leaf or flower
was calculated.
2.4. Statistical Analysis
Statistical analyses were conducted with SPSS statistical software (version 22.0) [
53
]
and the R program (version 4.0.3) [
54
]. Since the majority of pests and natural enemies’
density data were not normally distributed according to non-parametric Kolmogorov–
Smirnov tests in SPSS, differences in the densities of pests and natural enemies between
sweet pepper monoculture and sweet pepper/rosemary intercropping treatments during
the whole sampling duration (11 weeks) were determined using Generalized Linear Mixed
Models (package ‘lme4’, function ‘glmer’) [
55
] with Poisson error distribution in the R
program (p< 0.05). Treatment was included as a fixed factor, and sampling date as a
random factor. Differences in the densities of pests and natural enemies on each sampling
date between two cropping patterns were analyzed using Mann–Whitney Utests in SPSS
(
p< 0.05
). Linear regressions were used to analyze the relationships between pest and
natural enemy abundance. For F. intonsa,M. persicae,B. tabaci, and O. sauteri, the total
abundance in each plot (in both treatments) was summed from the second week of O. sauteri
release to the end of the experiments (June 8 to August 3), then linear regressions between
the abundance of the three pest species and O. sauteri were analyzed. For B. tabaci and
E. formosa, total abundance in each plot (in both treatments) was summed from the second
week of E. formosa release to the end of the experiments (July 6 to August 3) with linear
regressions between the abundance B. tabaci and E. formosa analyzed.
3. Results
3.1. Effect of Rosemary Intercropping on Population Dynamics of Pest Species
Frankliniella intonsa densities throughout the sampling period were significantly lower
in the sweet pepper/rosemary intercropping treatment compared to the sweet pepper
monoculture treatment (
χ2
=
−
9.469, p< 0.0001) (Figure 2A). Specifically, F. intonsa den-
sities for the intercropped treatment were lower than those of the monoculture on June 1
(
U= 3194.0
,p= 0.008), June 8 (U= 2951.0, p< 0.0001), July 6 (U= 3531.5, p= 0.014), July 20
(U= 3380.5, p= 0.006), and July 27 (U= 3550.0, p= 0.050) (Figure 2A).
Insects 2021,12, 74 5 of 13
Insects2021,12,xFORPEERREVIEW5of13
Myzuspersicaedensitiesthroughoutthesamplingperiodweresignificantlylowerin
thesweetpepper/rosemaryintercroppingtreatmentcomparedtothesweetpeppermon‐
oculturetreatment(χ2=−7.307,p<0.0001)(Figure2B).Specifically,M.persicaedensities
fortheintercroppedtreatmentwerelowerthanthoseofthemonocultureonJuly13(U=
3510.0,p<0.0001),July20(U=3780.0,p=0.013),July27(U=3735.0,p=0.007),andAugust
3(U=3555.0,p=0.001)(Figure2B).
Bemisiatabacidensitiesthroughoutthesamplingperiodweresignificantlylowerin
thesweetpepper/rosemaryintercroppingtreatmentcomparedtothesweetpeppermon‐
oculturetreatment(χ2=−30.526,p<0.0001)(Figure2C).Specifically,B.tabacidensitiesfor
theintercroppedtreatmentwerelowerthanthoseofthemonocultureonJuly6(U=
3364.5,p=0.046),July20(U=2970.5,p=0.002),July27(U=2689.0,p<0.0001),andAugust
3(U=2213.0,p<0.0001)(Figure2C).
Figure2.Meanpopulationdensitiesofpestsonsweetpepperplantsinsweetpeppermonoculture
andsweetpepper/rosemaryintercroppingtreatments.(A)Frankliniellaintonsa;(B)Myzuspersicae;
(C)Bemisiatabaci.Asterisksindicatesignificantdifferencesinpestdensityatagivensamplingdate
betweensweetpeppermonocultureandsweetpepper/rosemaryintercroppingtreatments(p<0.05).
Figure 2.
Mean population densities of pests on sweet pepper plants in sweet pepper monoculture
and sweet pepper/rosemary intercropping treatments. (
A
)Frankliniella intonsa; (
B
)Myzus persicae;
(
C
)Bemisia tabaci. Asterisks indicate significant differences in pest density at a given sampling date
between sweet pepper monoculture and sweet pepper/rosemary intercropping treatments (p< 0.05).
Myzus persicae densities throughout the sampling period were significantly lower
in the sweet pepper/rosemary intercropping treatment compared to the sweet pepper
monoculture treatment (
χ2
=
−
7.307, p< 0.0001) (Figure 2B). Specifically, M. persicae
densities for the intercropped treatment were lower than those of the monoculture on July
13 (U= 3510.0, p< 0.0001), July 20 (U= 3780.0, p= 0.013), July 27 (U= 3735.0, p= 0.007),
and August 3 (U= 3555.0, p= 0.001) (Figure 2B).
Bemisia tabaci densities throughout the sampling period were significantly lower in
the sweet pepper/rosemary intercropping treatment compared to the sweet pepper mono-
culture treatment (
χ2
=
−
30.526, p< 0.0001) (Figure 2C). Specifically, B. tabaci densities for
the intercropped treatment were lower than those of the monoculture on July 6 (
U= 3364.5
,
p= 0.046), July 20 (U= 2970.5, p= 0.002), July 27 (U= 2689.0, p< 0.0001), and August 3
(U= 2213.0, p< 0.0001) (Figure 2C).
Insects 2021,12, 74 6 of 13
3.2. Effects of Rosemary Intercropping on Population Dynamics of Natural Enemies
The density of the predatory bug, O. sauteri, throughout the whole sampling period
was not significantly different between the intercropped and monoculture treatments
(
χ2= 1.396
,p= 0.163) (Figure 3A). The same result was also found for population densities
of parasitoid, E. formosa, between the two treatments (χ2=−2.472, p= 0.064) (Figure 3B).
Insects2021,12,xFORPEERREVIEW6of13
3.2.EffectsofRosemaryIntercroppingonPopulationDynamicsofNaturalEnemies
Thedensityofthepredatorybug,O.sauteri,throughoutthewholesamplingperiod
wasnotsignificantlydifferentbetweentheintercroppedandmonoculturetreatments(χ2
=1.396,p=0.163)(Figure3A).Thesameresultwasalsofoundforpopulationdensitiesof
parasitoid,E.formosa,betweenthetwotreatments(χ2=−2.472,p=0.064)(Figure3B).
Figure3.Meanpopulationdensitiesofnaturalenemiesonsweetpepperplantsinsweetpepper
monocultureandsweetpepper/rosemaryintercroppingtreatments.(A)PredatorbugOriussauteri;
adultsandnymphsofO.sauteriwerereleasedonJune1andJune8.(B)ParasitoidEncarsiaformosa;
hostnymphcardswithE.formosawerereleasedonJune29.
3.3.EffectofNaturalEnemyReleaseonPestDensitiesandPest‐NaturalEnemyRegressions
ThenumberofF.intonsadecreasedsharplyafterthereleaseofO.sauteri(Figure2A)
andwerenegativelycorrelatedwiththedensitiesofO.sauteri(F1,11=8.102,p=0.017,R2=
0.4476)(Figure4A).AlthoughthenumberofM.persicaedecreasedafterthereleaseofO.
sauteri(Figure2B),thedensitiesofM.persicaeandO.sauteriwerenotcorrelated(F1,11=
0.069,p=0.799,R2=0.0068)(Figure4B).ThedensityofB.tabaciwasnotcorrelatedwith
thedensityofO.sauteri(F1,11=0.497,p=0.497,R2=0.0474)(Figure4C),butpositivelycor‐
relatedwiththedensityoftheparasitoidE.formosa(F1,11=66.145,p<0.0001,R2=0.8687)
(Figure5).ThereleaseofO.sauteriinhibitedpopulationgrowthofB.tabaciuntilJune29
(Figure2C).WhenthepopulationdensityofO.sauteribecamelow(June29)(Figure3A),
Figure 3.
Mean population densities of natural enemies on sweet pepper plants in sweet pepper monoculture and sweet
pepper/rosemary intercropping treatments. (
A
) Predator bug Orius sauteri; adults and nymphs of O. sauteri were released
on June 1 and June 8. (B) Parasitoid Encarsia formosa; host nymph cards with E. formosa were released on June 29.
3.3. Effect of Natural Enemy Release on Pest Densities and Pest-Natural Enemy Regressions
The number of F. intonsa decreased sharply after the release of O. sauteri (Figure 2A)
and were negatively correlated with the densities of O. sauteri (F
1,11
= 8.102, p= 0.017,
R2= 0.4476
) (Figure 4A). Although the number of M. persicae decreased after the release
of O. sauteri (Figure 2B), the densities of M. persicae and O. sauteri were not correlated
(
F1,11 = 0.069
,p= 0.799, R
2
= 0.0068) (Figure 4B). The density of B. tabaci was not correlated
with the density of O. sauteri (F
1,11
= 0.497, p= 0.497, R
2
= 0.0474) (Figure 4C), but posi-
tively correlated with the density of the parasitoid E. formosa (F
1,11
= 66.145, p< 0.0001,
R2= 0.8687
) (Figure 5). The release of O. sauteri inhibited population growth of B. tabaci
until June 29 (Figure 2C). When the population density of O. sauteri became low (June 29)
(
Figure 3A
), the population density of B. tabaci started increasing dramatically (Figure 2C).
The parasitoid, E. formosa, was released on June 29 and the density of B. tabaci started to
decrease two weeks later (from July 13) (Figure 2C).
Insects 2021,12, 74 7 of 13
Insects2021,12,xFORPEERREVIEW7of13
thepopulationdensityofB.tabacistartedincreasingdramatically(Figure2C).Thepara‐
sitoid,E.formosa,wasreleasedonJune29andthedensityofB.tabacistartedtodecrease
twoweekslater(fromJuly13)(Figure2C).
Figure4.LinearregressionsbetweenFrankliniellaintonsa(A),Myzuspersicae(B),andBemisiatabaci
(C)andOriussauteridensities.Thedensitiesofeachspeciesarethesumsof1620observations.
Figure 4.
Linear regressions between Frankliniella intonsa (
A
), Myzus persicae (
B
), and Bemisia tabaci
(C) and Orius sauteri densities. The densities of each species are the sums of 1620 observations.
Insects 2021,12, 74 8 of 13
Insects2021,12,xFORPEERREVIEW8of13
Figure5.LinearregressionbetweenBemisiatabaciandEncarsiaformosadensities.Thedensitiesof
eachspeciesarethesumsof1080observations.
4.Discussion
IntercroppingwithrosemarysignificantlydecreasedthepopulationdensityofM.
persicaeonsweetpepper,whichisconsistentwithapreviousfieldstudybyBenIssaetal.
[44].Moreover,thepopulationdensitiesoftwootherpests,F.intonsaandB.tabaci,were
alsosignificantlysuppressedbyrosemaryintercropping.Therepellentchemicalhypoth‐
esis,whichstatesthatnon‐hostplantvolatilesdisrupthostlocationandfeedingbyherbi‐
vores,couldexplainwhypestdensitiesintheintercroppedtreatmentwerelowerthanin
thoseinthesolecrop[56].Ithasbeenreportedpreviouslythatrosemaryvolatileswere
repellenttoM.persicaebothinthelaboratoryandscreenhouse[38,40].Rosemaryvolatiles
arealsorepellenttoB.tabaci[32]andmorerecentworkhasindicatedrepellenceforthree
thripsspecies,includingF.intonsainlaboratory‐basedolfactometerandhostplantselec‐
tionbioassays[42].However,thepersistentvalueofthisrepellenteffectinfieldconditions
needsfurtherstudy.Itisrecognizedthatcontributingfactorsaremyriadandthevolatile
interactionbetweennon‐hostplantsandhostplantsmightresultindifferentbehavioral
responsesinpestsfordifferentsystems[57].Inaddition,thereleaseofsemiochemicals
fromtheintercropplantscanbeaffectedbymanyfactors,suchasvarieties,growthstages,
andseason[32,34,40].Ourresultsconfirmedthatrosemaryiseffectiveinsuppressing
aphid,thrips,andwhiteflypopulationsonsweetpepperinthefieldandcouldbeagood
candidateasarepellentintercropplant.
Anotherpossiblemechanismresponsibleforlowerpestdensitiesintheintercrop‐
pingsystemisthedisruptionofinsecthost‐plantfindingandacceptancebehaviorsug‐
gestedbythe‘appropriate/inappropriatelandingstheory’[12,14].Thistheorysuggests
thatitisjustthenumberofalternativegreenobjects(non‐hostplants)surroundingahost
plantthatreducescolonizationbypestinsectsratherthanthereleaseofvolatilechemicals
thatdeterthepestsfromlanding[13].Thetheoryisbasedondetailedstudiesofthecab‐
bagerootfly[DeliaradicumL.(Diptera:Anthomyiidae)]andsuggeststhatthecomplete
systemofhostplantselectioninvolvesathree‐linkchainofeventsinwhichthefirstlink
isgovernedbycuesfromvolatileplantchemicals,thecentrallinkbyvisualstimuli,and
thefinallinkbycuesfromnon‐volatileplantchemicals[12].Itispossiblethatintheinter‐
croppingtreatmentinthisstudy,host‐plantfindingandacceptanceweredisruptedbya
Figure 5.
Linear regression between Bemisia tabaci and Encarsia formosa densities. The densities of
each species are the sums of 1080 observations.
4. Discussion
Intercropping with rosemary significantly decreased the population density of M. per-
sicae on sweet pepper, which is consistent with a previous field study by Ben Issa et al. [
44
].
Moreover, the population densities of two other pests, F. intonsa and B. tabaci, were also
significantly suppressed by rosemary intercropping. The repellent chemical hypothesis,
which states that non-host plant volatiles disrupt host location and feeding by herbivores,
could explain why pest densities in the intercropped treatment were lower than in those in
the sole crop [
56
]. It has been reported previously that rosemary volatiles were repellent
to M. persicae both in the laboratory and screenhouse [
38
,
40
]. Rosemary volatiles are also
repellent to B. tabaci [
32
] and more recent work has indicated repellence for three thrips
species, including F. intonsa in laboratory-based olfactometer and host plant selection
bioassays [
42
]. However, the persistent value of this repellent effect in field conditions
needs further study. It is recognized that contributing factors are myriad and the volatile
interaction between non-host plants and host plants might result in different behavioral
responses in pests for different systems [
57
]. In addition, the release of semiochemicals
from the intercrop plants can be affected by many factors, such as varieties, growth stages,
and season [
32
,
34
,
40
]. Our results confirmed that rosemary is effective in suppressing
aphid, thrips, and whitefly populations on sweet pepper in the field and could be a good
candidate as a repellent intercrop plant.
Another possible mechanism responsible for lower pest densities in the intercropping
system is the disruption of insect host-plant finding and acceptance behavior suggested
by the ‘appropriate/inappropriate landings theory’ [
12
,
14
]. This theory suggests that it is
just the number of alternative green objects (non-host plants) surrounding a host plant that
reduces colonization by pest insects rather than the release of volatile chemicals that deter
the pests from landing [
13
]. The theory is based on detailed studies of the cabbage root fly
[Delia radicum L. (Diptera: Anthomyiidae)] and suggests that the complete system of host
plant selection involves a three-link chain of events in which the first link is governed by
cues from volatile plant chemicals, the central link by visual stimuli, and the final link by
cues from non-volatile plant chemicals [
12
]. It is possible that in the intercropping treatment
in this study, host-plant finding and acceptance were disrupted by a proportion of the pests
landing on the rosemary (alternative green surfaces) instead of the sweet pepper plants.
Insects 2021,12, 74 9 of 13
However, further studies on the behavior of these three pest species are needed to test this
possible hypothesis.
It has been reported that increasing crop biodiversity, such as intercropping, can en-
hance pest natural enemies in agroecosystems [
20
]. However, the effect of intercrops on
natural enemies varies when different intercrops are used. In our study, intercropping with
rosemary did not affect the population densities of predatory bug, O. sauteri, or parasitoid,
E. formosa, on sweet pepper. Similarly, it has been reported that rosemary intercropping
did not affect the population densities of generalist predators in tea plantations [
33
]. Sev-
eral possible reasons might contribute to the above results. No enhancement of natural
enemy success in rosemary intercropping treatment in our study, or a previous study [
33
],
might indicate that rosemary did not have any behavioral effect on natural enemies. Alter-
natively, rosemary volatiles might manipulate the behavior of natural enemies, as reported
by Bennison et al. [
41
], who showed rosemary leaves and volatiles were repellent to preda-
tory bug Orius laevigatus in an olfactometer. However, in this environment, it may be
that herbivore-induced plant volatiles (HIPVs), which are known to attract natural ene-
mies
[58–61]
, are sufficiently detectable and take precedent over any attraction the natural
enemies might otherwise have to rosemary. Further study on the behavioral response of
O. sauteri and E. formosa to rosemary volatiles and sweet pepper HIPVs are required to
elucidate the details of this interaction.
Our results showed that in both intercropping and monoculture treatments, the pop-
ulation densities of F. intonsa and M. persicae decreased as O. sauteri population density
increased. Although we could not rule out other factors that contributed to pest population
suppression because no control treatment without natural enemy releases was included
in our study, predation of F. intonsa and M. persicae by O. sauteri could be the most likely
reason. The population suppression of thrips and aphids by O. sauteri reported here is
consistent with that of previous studies [
62
–
64
]. These results provide further evidence for
the benefits of predatory bugs from the Orius genus as an effective control method for thrips
and aphids [
48
,
65
]. Sequential release of O. sauteri and E. formosa was also effective in the
control of B. tabaci in both intercropping and monoculture treatments. These results were
similar to those of a previous study, in which the combination of O. sauteri and E. formosa
was shown to effectively control B. tabaci in the greenhouse [
66
]. Our results showed the
population decrease in B. tabaci occurred two weeks following the release of E. formosa.
The reason might be that, unlike predators which immediately kill the host, such as a
koinobiont parasitoids, E. formosa does not usually cause the immediate death of the host,
requiring the host to be alive for the early stages of larval development [
67
]. In our study,
F. intonsa density was negatively correlated with the density of O. sauteri regardless of the
cropping system, which was consistent with the negative correlation between predator
and prey in other studies [
68
,
69
]. However, in another study, the abundance of predator
hoverfly larvae was positively correlated with the number of aphids [
70
]. Unlike the nega-
tive correlation between predator and prey in our study, B. tabaci density was positively
correlated with the density of its parasitoid E. formosa. Different relationships between
pests and natural enemies might be due to different host selection and foraging behavior
of predators or parasitoids. Moreover, interactions between host plants, pests, and natural
enemies vary considerably among different systems. Further studies on chemical commu-
nications and insect behavior manipulations in different plant–prey–predator or plant–host
pest–parasitoid systems are needed.
Natural enemy release has been widely used in greenhouse pest control, unlike in-
tercropping, which is more commonly used in open fields and orchards [
16
,
17
,
33
,
68
,
71
].
Less research has explored its possible use in greenhouse pest control. Our study showed
that rosemary intercropping is feasible in the greenhouse because it can be successfully es-
tablished under vegetable-growing conditions without additional farming practices being
implemented. Although the intercropping of rosemary plants would compete for nutrients
and/or water with target crop plants, they also provide economic value as ornamental,
culinary, cosmetic, or medicinal plants [
26
–
28
], and could provide a minor additional
Insects 2021,12, 74 10 of 13
revenue for growers. Furthermore, significant pest population suppression and the lack
of adverse effect on natural enemies in the sweet pepper/rosemary intercropping system
suggest the potential of this combination in the IPM framework. However, because field
conditions were complicated, and our study was only conducted for one growing season,
further investigations are needed to confirm the validity of the results. Moreover, additional
studies are needed to investigate whether this is effective in different spatial configurations
of the two plants and in open field settings. Nevertheless, enhanced pest suppression
by combining the two alternative control strategies reported here provides a promising
direction for improving sustainable pest management.
Author Contributions:
Conceptualization, X.-w.L. and Y.-b.L.; Methodology, X.-w.L. and Z.-j.Z.;
Software, X.-w.L. and X.-x.L.; Validation, X.-w.L. and Y.-b.L.; Formal Analysis, J.H. and J.-m.Z.;
Investigation, X.-x.L., J.H., J.-m.Z. and L.-k.W.; Resources, Y.-b.L. and J.H.; Data Curation, X.-x.L.
and Z.-j.Z.; Writing—Original Draft Preparation, X.-w.L.; Writing—Review & Editing, M.H. and
G.M.F.-G.; Visualization, X.-w.L.; Supervision, Y.-b.L.; Project Administration, X.-w.L.; Funding
Acquisition, X.-w.L., Z.-j.Z. and Y.-b.L. All authors have read and agreed to the published version of
the manuscript.
Funding:
This work was supported by the National Key R&D Program of China (2017YFD0200400);
the Key R&D Program of Zhejiang Province (2018C02032); the National Natural Science Foun-
dation of China (31901885; 31672031); the Zhejiang Provincial Natural Science Foundation of
China (LQ18C140003).
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: The data presented in this study are available in article.
Conflicts of Interest: The authors declare no conflict of interest.
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