Indirect plant defenses: volatile organic compounds and extrafloral nectar

Abstract

Indirect plant defense is an important component in regulating population dynamics and the structure of numerous communities in different ecosystems. These defenses mainly involve the emission of volatile organic compounds (VOCs) induced after damage by an herbivore. VOCs can play several ecological roles, such as help natural enemies locate prey or hosts, attract or repel other herbivores, mediate communication between neighboring plants and among different parts of the same plant, and affect the behavior of pollinators and seed dispersers. In addition to VOCs, some plants produce extrafloral nectar, which can enhance plant defense, by attracting, retaining, and increasing the efficiency of some natural enemies; however, among the associated costs, these compounds can attract other herbivorous species and exclude some natural enemies due to competition. Many factors can influence the production of indirect defenses by plants, such as the individual species, life stage, density of herbivores, age, abiotic factors, as well as the association of plants with symbiotic microorganisms. The potential of indirect plant defenses to reduce herbivory and increase the plant fitness has been well demonstrated. Indirect plant defenses may have ecological costs but can express phenotypic plasticity, as plants can reduce or increase the production of defenses according to the associated herbivory rate. Such variable expression of characteristics provides a barrier against the evolution of resistance by the associated herbivores. In this article, we intend to provide a review on volatile organic compounds and extrafloral nectar as indirect plant defenses, including some costs and benefits of these defense mechanisms.

Full text

Vol.:(0123456789)
1 3
Arthropod-Plant Interactions
https://doi.org/10.1007/s11829-021-09837-1
REVIEW PAPER
Indirect plant defenses: volatile organic compounds andextrafloral
nectar
RannaHeidySantosBezerra1 · LeandroSousa‑Souto1 · AntônioEuzébioGoulartSantana2 ·
BiancaGiulianoAmbrogi1
Received: 21 July 2020 / Accepted: 28 April 2021
© The Author(s), under exclusive licence to Springer Nature B.V. 2021
Abstract
Indirect plant defense is an important component in regulating population dynamics and the structure of numerous commu-
nities in different ecosystems. These defenses mainly involve the emission of volatile organic compounds (VOCs) induced
after damage by an herbivore. VOCs can play several ecological roles, such as help natural enemies locate prey or hosts,
attract or repel other herbivores, mediate communication between neighboring plants and among different parts of the same
plant, and affect the behavior of pollinators and seed dispersers. In addition to VOCs, some plants produce extrafloral nectar,
which can enhance plant defense, by attracting, retaining, and increasing the efficiency of some natural enemies; however,
among the associated costs, these compounds can attract other herbivorous species and exclude some natural enemies due
to competition. Many factors can influence the production of indirect defenses by plants, such as the individual species, life
stage, density of herbivores, age, abiotic factors, as well as the association of plants with symbiotic microorganisms. The
potential of indirect plant defenses to reduce herbivory and increase the plant fitness has been well demonstrated. Indirect
plant defenses may have ecological costs but can express phenotypic plasticity, as plants can reduce or increase the production
of defenses according to the associated herbivory rate. Such variable expression of characteristics provides a barrier against
the evolution of resistance by the associated herbivores. In this article, we intend to provide a review on volatile organic
compounds and extrafloral nectar as indirect plant defenses, including some costs and benefits of these defense mechanisms.
Keywords Induced volatile organic compounds· EFN· Herbivores· Natural enemies
Introduction
Plants have developed a complex diversity of direct and indi-
rect defense mechanisms (Pinto-Zevallos etal. 2013; Chen
etal. 2020). This complex defense arsenal is more evident
when we examine its function in tritrophic interactions
(interactions involving the host plant, its herbivores, and
their natural enemies). Direct mechanisms act on herbivores
and include physical and chemical barriers. Physical barriers
include the cuticle, trichomes, thorns, and leaf toughness
that interfere with arthropod mobility and feeding (Dudareva
etal. 2006; Howe and Jander 2008). The chemical barri-
ers consist of the production of toxic secondary metabolites
and defense proteins that can repel, suppress oviposition and
feeding, and hinder the digestion of herbivores (Arimura
etal. 2005). Indirect mechanisms involve the attraction of
parasitoids and predators through structures that offer food
and protection (e.g., extrafloral nectaries and domatia) and
by the emission of volatile organic compounds (VOCs)
induced by herbivory (Chen 2008; Aljbory and Chen 2018).
A wide range of recent studies indicate that VOCs emit-
ted by plants are an eco-sustainable strategy to increase
both protection and plant productivity (Brilli etal. 2019).
The dissemination of VOCS through the air allows rapid
defense signaling, not only at the level of the individual
plant (Heil and Silva-Bueno 2007) or at plant–plant level
Handling Editor: Heikki Hokkanen.
* Bianca Giuliano Ambrogi
bianca.ambrogi@gmail.com
1 Laboratório de Ecologia Química, Departamento de
Ecologia, Programa de Pós Graduação em Ecologia
e Conservação, Universidade Federal de Sergipe,
SãoCristóvão, SE, Brazil49100-000
2 Laboratório de Pesquisas em Recursos Naturais
(LPqRN), Campus de Engenharias e Ciências Agrárias
(CECA), Universidade Federal de Alagoas, Maceió, AL,
Brazil57100-000

R.H.S.Bezerra et al.
1 3
(Baldwin etal. 2006), but also through the mediation of the
complex network of interactions between plants and other
organisms, including arthropods, pathogens, and soil symbi-
onts. In addition, VOCs can “prepare” the defense system of
plants for greater resistance to environmental stressors, such
as sudden changes in temperature, droughts, and air pollu-
tion (Conrath etal. 2002; Bolsoni etal. 2018). However, the
study of tritrophic interactions of VOCs have received more
focus (Turlings and Erb 2018; Pekas and Wäckers 2020).
In recent years, studies on tritrophic interactions have
made great progress, especially in relation to indirect defense
(Rodríguez-Saona 2012; Gebreziher 2018; Turlings and Erb
2018; Pekas and Wäckers 2020). To understand how these
interactions occur, the defense mechanisms of plants and
how they influence these relationships must be understood.
Several studies have been carried out using mechanisms of
plant resistance against herbivory, to observe their influence
on the behavior and biology of the natural enemies (Taka-
bayashi and Dicke 1996; Rasmann etal. 2005; Takabayashi
and Shiojiri 2019) and the herbivores (De Moraes etal.
2001; Reisenman etal. 2013), most of which are related to
the defenses induced after herbivore damage.
Induced defenses mainly involve the emission of vola-
tile compounds after herbivore damage, and they can repel
(de Moraes etal. 2001; Verheggen etal. 2013; Veyrat etal.
2015) or attract herbivores (Robert etal. 2012; McCormick
etal. 2016; Shivaramu etal. 2017) as well as attract preda-
tors and parasitoids (Takabayashi and Dicke 1996; Paré and
Tumlinson 1997; Horiuchi etal. 2003; Oliveira and Pareja
2014; Pinto-Zevallos etal. 2018) (Table1). In addition to
volatile compounds, plants can also provide food and shel-
ter that can help recruit natural enemies of these herbivores
(Chen 2008). These defense mechanisms can alter the
dynamics and the trophic chains of the community (Dicke
and Baldwin 2010), which are decisive for the development
and maintenance of the species interactions and ecosystem
structure. This article provides a review on indirect plant
defense, including some costs and benefits to plant survival
and fitness (Fig.1).
Plant volatiles induced byherbivores
intritrophic interactions
Volatile organic compounds play an important role as a com-
munication signal that plants use to interact with the sur-
rounding environment (Dudareva etal. 2006). These VOCs
can be produced constitutively, without herbivore attack, or
be induced by damage to plant tissues, such as herbivory
and/or oviposition (Paré and Tumlinson 1999; Arimura etal.
2005).
Constitutively produced VOCs defend the plant against
stress, oxidation, and high temperatures (Pinto-Zevallos
etal. 2013). They mediate interactions between plants and
the environment by attracting pollinators, seed dissemina-
tors, and herbivores (Pichersky and Gershenzon 2002; Rein-
hard etal. 2004); repelling herbivores; and protecting against
microorganisms (Pichersky and Gershenzon 2002; Pinto-
Zevallos etal. 2013). VOCs induced by herbivory can play
several ecological roles, such as help natural enemies locate
prey or hosts, attract or repel other herbivores, and medi-
ate communication between neighboring plants or between
different parts of the same plant (Dicke etal. 1990, 1999;
Horiuchi etal. 2003; Verheggen etal. 2013; Mutyambai
etal. 2016).
These compounds are often related to defense (Price etal.
1980), as their release in the environment signal the presence
of resources, allowing a natural enemy to locate the prey or
host (de Moraes etal. 2000; Kessler and Baldwin 2001). The
attractive or repellent responses of herbivores and natural
enemies to induced VOCs depend on the level of damage
to the plant (Maeda and Takabayashi 2001; Horiuchi etal.
2003) and the ability of organisms to discriminate between
different volatile mixtures (Dicke 1999).
Most studies have found that the release of VOCs is
greater when the plant is damaged by herbivores than when
the damage is produced mechanically or in healthy plants
(Paré and Tumlinson 1999; Shiojiri etal. 2010; Kappers
etal. 2011). These volatiles constitute about 1% of the sec-
ondary metabolites of plants and are mainly terpenoids, phe-
nylpropanoids, benzenoids, and derivatives of fatty acids and
amino acids (Dudareva etal. 2004), which are synthesized
through different metabolic pathways (War etal. 2011).
These mixtures of induced VOCs can contain more than 200
different compounds (Dicke and Van Loon 2000). In a recent
review, Guo and Wang (2019) summarize the progresses in
characterization of herbivore-induced plant volatiles and the
olfactory mechanisms underlying tritrophic interactions in
the last three decades.
The induction of VOCs after herbivory or oviposition
occurs through the activation of metabolic routes that
involve the recognition of elicitors; phytohormones, mainly
jasmonic acid, salicylic acid, and ethylene (Thaler etal.
2012; Aljbory and Chen 2018); and genes that can trigger a
local and/or systemic defensive response in the plant (Kes-
sler and Baldwin 2002). The eliciting substances are usually
in the oral secretions and oviposition fluids of the herbi-
vores that enter the plant through injuries caused by them,
which then initiates chemical reactions that culminate in the
synthesis of VOCs (Dicke 1999; Aljbory and Chen 2018).
Induction can also be reproduced through the exogenous
application of elicitors and plant hormones, such as jasmonic
acid and salicylic acid (Dicke and Van Loon 2000).
The first eliciting substance to be identified was volicitin
N-(17-hydroxylinolenoyl)-L-glutamine present in the oral
secretion of Spodoptera exigua (Lepidoptera: Noctuidae),

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
Table 1 Examples of the influence of induced volatiles on the behavior of natural enemies and herbivores
Inductors Plants Volatile compounds Attracts References
Natural enemies
Tetranychus urticae Phaseolus lunatus Linalol, β-ocimene, (3E)-
DMNT, methyl salicylate Phytoseiulus persimilis Dicke etal. (1990)
T. urticae P. lunatus Linalol, methyl salicylate Amblyseius potentillae Dicke etal. (1990)
T. urticae P. lunatus (E)-DMNT, methyl salicy-
late P. persimilis Dicke etal. (1999)
Manduca quinquemacu-
lata, Dicyphus minimus,
Epitrix hirtipennis
Nicotiana attenuata Cis-α-bergamotene, methyl
jasmonate Geocoris pallens Kessler and Baldwin (2001)
Diabrotica virgifera
virgifera Zea mays (E)-β-caryophyllene Heterorhabditis megidis Rasmann etal. (2005);
Rasmann and Turlings
(2007); Hiltpold etal.
(2011)
Spodoptera littoralis + D.
virgifera Z. mays (E)-β-caryophyllene Cotesia marginiventris Rasmann and Turlings
(2007)
T. urticae Cucumis sativus (E)-β-ocimene, (E,E)-TMTT
and others P. persimilis Kappers etal. (2011)
Chilo partellus Z. mays (R)–linalol, (E)-DMNT,
methyl salicylate and
others
Cotesia sesamiae Tamiru etal. (2012)
Glomus mosseae + T.
urticae Phaseolus vulgaris β-ocimene, β-caryophyllene P. persimilis Schausberger etal. (2012)
Trichoderma longibra-
chiatum + Macrosiphum
euphorbiae
Solanum lycopersicum Cis-3-hexen-1-ol,
α-pinene, methyl
salicylate, longifolene, and
β-caryophyllene
Aphidius ervi Battaglia etal. (2013)
C. partellus Z. mays (E)-DMNT, limonene and
decanal Trichogramma bournieri, C.
sesamiae Mutyambai etal. (2016)
Spodoptera frugiperda Zea spp. (Z)-3-hexenol, (Z)-3-hexenyl
acetate, linalool, DMNT,
(E)-β-caryophyllene, and
(E)-β-farnesene
Campoletis sonorensis Lange etal. (2018)
T. urticae Manihot esculenta (1Z)-methyl propanol
oxime and 2-methyl-butyl
aldoxime, (E)-β-ocimene,
indole, methyl-O-amin-
obenzoate, (E)-geranyl
acetone, β-caryophyllene,
α-farnesene and nerolidol
Neoseiulus idaeus Pinto-Zevallos etal. (2018)
Tuta absoluta S. lycopersicum (Z)-3-hexen-1-ol, β-pinene,
β-myrcene, γ-terpinene,
γ-elemene, guaidiene-6, 9,
nonanal and decanal
Trichogramma cordubense Milonas etal. (2019)
T. urticae + Frankliniella
insularis Rosa spp. 3-hexenyl acetate, methyl
salicylate, caryophyllene,
β-nerolidol and supraene
Orius insidiosus Souza etal. (2019)
Inductors Plants Volatile compounds Attract Repels References
Herbivores
Heliothis virescens Nicotiana tabacum (Z)-3-hexenyl butyrate,
(Z)-3-hexenyl isobu-
tyrate, (Z)-3-hexenyl
acetate, (Z)-3-hexenyl
tiglate
–H. virescens de Moraes etal. (2001)
M. quinquemaculata, D.
minimus, E. hirtipennis N. attenuata Linalol – M. quinquemaculata Kessler and Baldwin
(2001)
D. virgifera Brassica rapa (E)-β-caryophyllene D. virgifera – Robert etal. (2012)

R.H.S.Bezerra et al.
1 3
which induces the emission of VOCs in corn, Zea mays
(Poaceae) and attracts the parasitic wasps Cotesia mar-
giniventris and Microplitis croceipes (Hymenoptera: Bra-
conidae) (Alborn etal. 1997; Turlings etal. 2000). Other
elicitors have been identified in different insect species,
including β-glucosidase found in the oral secretion of Pieris
brassicae (Lepidoptera: Pieridae) that causes the release of
VOCs, which attract the parasitic wasp Cotesia glomerata
(Hymenoptera: Braconidae) (Mattiacci etal. 1995); N-lino-
lenoyl-glutamine isolated from the regurgitant of Manduca
sexta (Lepidoptera: Sphingidae) that induces the emission
in tobacco, Nicotiana attenuata (Solenaceae) (Halitschke
etal. 2001); inceptins produced through digestion of veg-
etable proteins in the intestine of Spodoptera frugiperda that
induce emission in Phaseolus vulgaris (Fabaceae), Vigna
unguiculata (Fabaceae), and Z. mays (Schmelz etal. 2006,
2007); and alkaline phosphatase present in the saliva of
Bemisia tabaci (Hemiptera: Aleyrodidae) (Funk 2001).
According to Paré and Tumlinson (1999), four identified
metabolic pathways involved in the production of induced
VOCs are mevalonate; methyl erythritol-phosphate, which
leads to terpenes; lipoxygenase, which leads to the volatiles
of green leaves; and shikimic acid, which leads to phenyl-
propanoids and benzenoids.
Green leaf volatiles (GLVs) are released immediately
after damage, regardless of the causative agent (Turlings
etal. 1998), and are emitted mainly when the damage is
mechanical (Pinto-Zevallos etal. 2013). Terpenoids are
the most diverse group of induced VOCs and are produced
later than GLVs in response to damage caused by her-
bivory, and are generally released not only in damaged
tissue, but also in undamaged plant parts, through systemic
induction (Paré and Tumlinson 1999). Phenylpropanoids
Table 1 (continued)
Inductors Plants Volatile compounds Attract Repels References
S. littoralis B. rapa Ethylene – D. virgifera Robert etal. (2012)
Manduca sexta S. lycopersicum (−)-linalol – M. sexta Reisenman etal.
(2013)
Myzus persicae B. rapa (E)-2-hexenol, β-pinene,
sec-butyl isothiocyanate,
and 4-pentenyl isothio-
cyanate, (E)-β-farnesene
and others
–M. persicae Verheggen etal.
(2013)
Acyrthosiphon
pisum + arbuscular
mycorrhizal
Vicia faba (Z)-3-hexenyl acetate,
naphthalene, (R)-germa-
crene
A. pisum – Babikova etal. (2014)
Ectropis obliqua Camellia sinensis benzyl alcohol, (Z)-3-hexe-
nyl hexanoate, (Z)-
3-hexenal, (Z)-3-hexenyl
acetate
E. obliqua – Sun etal. (2014)
S. littoralis Gossypium hirsutum (E)-(DMNT) – S. littoralis Hatano etal. (2015)
Epiphyas postvittana Malus domestica nitrile, benzyl alcohol,
2-phenylethanol, and
acetic acid
E. postvittana – El-Sayed etal. (2016)
Spilonota ocellana M. domestica benzyl nitrile and acetic
acid S. ocellana – El-Sayed etal. (2016)
Choristoneura rosaceana M. domestica 2-phenylethanol C. rosaceana – El-Sayed etal. (2016)
Scirtothrips dorsalis Capsicum annuum δ-3-Carene, Octadecane
and n-Docosane S. dorsalis – Shivaramu etal.
(2017)
T. absoluta S. lycopersicum hexanal, (Ζ)-3-hexen-1-ol,
methyl salicylate and
indole
–S. lycopersicum Anastasaki etal.
(2018)
Phratora laticollis Hybrid aspen (P.
tremula × tremu-
loides)
syn-3-methylbutyl aldox-
ime, 2-methyl butaneni-
trile, isobutyronitrile,
benzyl nitrile, phenethyl
acetate, 2-phenylethanol,
salicylaldehyde, (E)-β-
ocimene, (Z)-3-hexenyl
isovalerate and 2-methyl
butanol
P. laticollis – Li etal. (2020)

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
and benzenoids are another large class of induced VOCs
(War etal. 2011). One of the most frequent VOCs in the
mixture induced after herbivory is methyl phenylpropa-
noid salicylate, which was reported in the profile emitted
by bean (Dicke etal. 1990; Maeda and Tabakayashi 2001),
apple (Takabayashi etal. 1991), cucumber (Kappers etal.
2011), kale (Mumm etal. 2008), cassava (Pinto-Zevallos
etal. 2018), and other plants. The derivatives of fatty acids
and amino acids, as well as the other classes of VOCs,
play an important role in the plant defense by recruiting
natural enemies. The derivatives of fatty acids are formed
from linolenic acid and released immediately after herbi-
vore damage. Amino acid derivatives include aldehydes,
alcohols, esters, acids, and compounds containing nitrogen
and sulfur (War etal. 2011).
These VOCs can vary depending on the density of herbi-
vores (Maeda and Takabayashi 2001; Kappers etal. 2011;
Pinto-Zevallos etal. 2018), the type of herbivore causing the
damage, the feeding habit and the stage of lifespan (Taka-
bayashi and Dicke 1996; Silva etal. 2017), the presence of
different species of herbivores in the same plant (Magal-
hães etal. 2018; Hodge etal. 2019), plant age and genotype
Fig. 1 Costs and benefits of
indirect plant defenses

R.H.S.Bezerra et al.
1 3
(Takabayashi etal. 1994; Krips etal. 2001; Kappers etal.
2011), and abiotic factors such as soil texture and density,
air humidity, temperature, and light intensity (Takabayashi
etal. 1994; Gouinguené and Turlings 2002; Dudareva etal.
2006; Truong etal. 2014). In addition to these factors, recent
studies have demonstrated that the association of plants with
root symbionts, such as rhizobacteria and mycorrhizal fungi,
can influence the emission of constitutive and induced VOCs
and the expression of plant defense mechanisms, with con-
sequences on the performance of herbivores and natural
enemies (Schausberger etal. 2012; Babikova etal. 2014;
Malik etal. 2018; Pappas etal. 2018; Rusman etal. 2018).
Volatile emissions are generally not restricted to the
injured site, but also occur in undamaged tissues, character-
izing systemic induction, thereby increasing the detectability
of the signal (Dicke etal. 1990; Dicke 2009). The ability of
natural enemies to recognize and respond to VOCs induced
by herbivory indicates that VOCs emitted by herbivore-
damaged plants are distinguishable from those emitted in
response to other factors, such as mechanical injuries (Paré
and Tumlinson 1999). These volatiles alert natural enemies
that the plant is being consumed by their prey/hosts, increas-
ing their chances of success in the search for food, and are
more reliable than those constitutively produced, since they
indicate the possible presence of prey or host (Kessler and
Baldwin 2001; Rodríguez-Saona 2012). Thus, VOCs play an
important role as a signal during the search (Vet and Dicke
1992) and can be used to indicate prey density or select
oviposition sites (Shiojiri etal. 2010).
Influence ofherbivore‑induced VOCs
onthebehavior ofnatural enemies
The adoption of herbivore-induced VOCs by natural enemies
depends on how easy these compounds are to detect in the
environment and on the reliability of information about the
presence and quality of the resource (Vet and Dicke 1992).
VOCs emitted by herbivores themselves are reliable indica-
tors of their presence; however, due to the small biomass of
herbivores compared to plants, these compounds are pro-
duced in small quantities and are thus difficult for natural
enemies to detect over long distances. In addition, herbivores
are constantly adapting to try not to be detected (Dicke and
Van Loon 2000). On the other hand, their greater biomass
allows plants to produce greater amounts of VOCs, which
are more easily detected by natural enemies; however, they
are less reliable (Vet and Dicke 1992). The adaptation of
natural enemies to induced VOCs is advantageous for plants,
predators, and parasitoids (Pinto-Zevallos etal. 2013).
The first studies that demonstrated the production of
herbivore-induced VOCs in plants and their role in attract-
ing natural enemies were carried out with herbivorous mites
and their predators (Sabelis and Van de Baan 1983; Dicke
and Sabelis 1988; Dicke etal. 1990; Takabayashi and Dicke
1996). Dicke etal. (1990) observed that lima bean plants,
Phaseolus lunatus, infested with Tetranychus urticae (Acari:
Tetranychidae), produced a volatile mixture that attracts
the predatory mite Phytoseiulus persimilis (Acari: Phyto-
seiidae), which does not occur in plants without herbivore
damaged or with only mechanical damage. Subsequently,
cucumber plants, Cucumis sativus (Cucurbitaceae) and apple
trees, Malus sp. (Rosaceae), also respond to T. urticae her-
bivory by producing VOCs that attract P. persimilis (Taka-
bayashi and Dicke 1996).
These studies have encouraged several works that
explored how the induced VOCs affect the interactions
between plants, herbivores, and their natural enemies,
mainly by attracting predators and parasitoids to specific
compounds induced by their prey/hosts (Horiuchi etal.
2003; Pinto-Zevallos etal. 2018).
The attraction of natural enemies has been evidenced in
several tritrophic systems (Horiuchi etal. 2003; Zhong etal.
2011; Oliveira and Pareja 2014; Silva etal. 2016; Pinto-
Zevallos etal. 2018; Xiu etal. 2019). Eggplant, Solanum
melongena (Solanaceae); pepper, Capsicum annuum (Sola-
naceae); and tomato, Solanum lycopersicum, plants emit
volatiles in response to the Frankliniella occidentalis (Thy-
sanoptera: Thripidae) herbivory, which attract Neoseiulus
cucumeris (Acari: Phytoseiidae) (Zhong etal. 2011). Simi-
larly, Brassica juncea (Brassicaceae) plants damaged by
the aphid Myzus persicae (Hemiptera: Aphididae) or under
simultaneous herbivory of the aphid and Plutella xylostella
(Lepidoptera: Plutellidae) were more attractive to the natu-
ral enemies Chrysoperla externa (Neuroptera: Chrysopidae)
and Aphidius colemani (Hymenoptera: Braconidae) than
healthy plants (Silva etal. 2016).
As in the aerial part of plants, the emission of VOCs from
the roots can also contribute to belowground defense, acting
as antimicrobial or anti-herbivory substances and attracting
natural enemies (Rasmann etal. 2005; Hiltpold etal. 2011;
Ali etal. 2012; Tonelli etal. 2016). Species of nematodes,
such as Heterorhabditis indica and Steinernema carpocap-
sae (Rhabditida: Heterorhabditida) were attracted to sugar-
cane roots injured by Mahanarva fimbriolata (Hemiptera:
Cercopidae) compared to undamaged plants (Tonelli etal.
2016). The application of volatiles from Swingle citrumelo
(Citrus paradisi x Poncirus trifoliata) (Rutaceae) roots dam-
aged by the feeding of Diaprepes abbreviatus (Coleoptera:
Curculionidae) and the isolated compound pregeijerene
(1,5-dimethylcyclodeca-1,5,7-triene), attracted entomopath-
ogenic nematodes and increased the mortality of beetle lar-
vae compared to control plants. In addition, the application
of the same compound in blueberry orchards attracted native
entomopathogenic nematodes, increasing the mortality of
Galleria mellonella (Lepidoptera: Pyralidae) and Anomala
orientalis (Coleoptera: Scarabaeidae) (Ali etal. 2012).

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
The presence of more than one species simultaneously
consuming the same plant can also alter the response of
natural enemies to induced VOCs, which may increase or
decrease their attraction (Rasmann and Turlings 2007; de
Boer etal. 2008; Bukovinszky etal. 2012; Peñaflor etal.
2017). Studies using corn plants under leaf herbivory by
Spodoptera littoralis, and plants with root herbivory by
Diabrotica virgifera virgifera (Coleoptera: Chrysomeli-
dae), found that C. marginiventris and Heterorhabditis
megidis were strongly attracted by plants damaged by their
hosts; however, this attraction was significantly reduced
when both herbivores were simultaneously on the plant
(Rasmann and Turlings 2007). In this case, dual herbivory
reduced the emission of (E)-β-karyophylene, the main com-
pound involved in the attraction of H. megidis, and caused
a non-significant reduction in other minor compounds that
may be involved in the attraction of C. marginiventris. In
other study, however, the parasitic wasp Cotesia flavipes was
more attracted to VOCs emitted by sugarcane plants infested
simultaneously by Diatraea saccharalis (Lepidoptera: Pyral-
idae) and S. frugiperda than to plants infested only by their
host D. saccharalis (Peñaflor etal. 2017).
Simultaneous herbivory did not alter the attraction
response of natural enemies in some tritrophic systems
(Oliveira and Pareja 2014; Souza etal. 2019). For exam-
ple, the generalist predator Orius insidiosus (Hemiptera:
Anthocoridae) did not discriminate the odors of rose plants,
Rosa sp. (Rosaceae), infested by T. urticae or Frankliniella
insularis from plants with both species, although volatiles of
plants infested with one or two species differed qualitatively
and quantitatively (Souza etal. 2019).
Similar to herbivory, the mechanical damage caused by
the oviposition of herbivores can also induce the emission
of VOCs that attract predators or egg parasitoids (Picher-
sky and Gershenzon 2002; Tamiru etal. 2012; Mutyambai
etal. 2016; Milonas etal. 2019), allowing the plant to defend
itself before herbivore eggs hatch. Studies have found that
the oviposition of Chilo partellus (Lepidoptera: Cambridae)
in two varieties of corn plants induces the emission of VOCs
that attract Cotesia sesamiae (Tamiru etal. 2012). Another
study with Z. mays demonstrated that Trichogramma bourni-
eri (Hymenoptera: Trichogrammatidae) and C. sesamiae
prefer the plant volatiles induced by oviposited and unovi-
posited neighboring plants, compared to the control (Muty-
ambai etal. 2016).
From the plant’s point of view, the attraction of preda-
tors to induced VOCs can result in a direct and immediate
benefit, through the population reduction of the herbivore by
predators, which decreases or stops the damage. However,
attracting parasitoids to the plant does not usually imme-
diately stop the consumption by the herbivore (Dicke and
Van Loon 2000; Dicke and Baldwin 2010), because the host
continues to feed until the parasitoid hatches, delaying the
benefit (Dicke and Sabelis 1989; Dicke and Baldwin 2010).
A few studies have demonstrated an increase in plant fitness
after parasitoid-mitigated herbivory (Gols etal. 2015; Cuny
etal. 2018; Lange etal. 2018; Bustos-Segura etal. 2020).
Influence ofherbivore‑induced VOCs onherbivore
behavior
In addition to the indirect effects of plant-emitted VOCs
on herbivores by attracting natural enemies (Vet and Dicke
1992; Paré and Tumlinson 1997; Kessler and Baldwin
2001), these compounds can directly benefit some species
of herbivores, by attracting them to host plants for feeding or
mating partners (Robert etal. 2012; McCormick etal. 2016;
Shivaramu etal. 2017; Peñaflor etal. 2019) or by repelling
them to avoid intraspecific competitions and displacement
to locations that natural enemies could be attracted (Hori-
uchi etal. 2003; Verheggen etal. 2013; Anastasaki etal.
2018). However, negative effects can also be observed, since
VOCs can directly affect the physiology and behavior of her-
bivores, due to their toxic, repellent, or deterrent properties
on feeding and oviposition (De Moraes etal. 2001; Kessler
and Baldwin 2001; Veyrat etal. 2015; Gasmi etal. 2019).
Plants infested with herbivores can emit information
about the presence of resources (De Moraes etal. 2000) and
activation of plant defense. However, VOCs can also indi-
cate that plant defenses have been overcome by herbivores
and that those plants are consequently weakened and more
susceptible to attack (Dicke and Van Loon 2000).
The emission of induced VOCs results in differential
responses among members of the community (Dicke and
Baldwin 2010). Several studies have investigated their influ-
ence on the behavior of different species (de Moraes etal.
2001; Kessler and Baldwin 2001; Reisenman etal. 2013).
Many herbivores can be attracted by induced VOCs
(Kalberer etal. 2001; Robert etal. 2012; Sun etal. 2014;
Shivaramu etal. 2017). For example, Scirtothrips dorsalis
(Thysanoptera: Thripidae) was significantly more attracted
to pepper plants infested with cospecifics than VOCs from
healthy plant or by the insect odor (Shivaramu etal. 2017).
Similarly, D. virgifera virgifera larvae were more attracted
and had greater growth in corn roots previously attacked by
cospecifics (Robert etal. 2012). The feeding of the larvae
induces the emission of (E)-β-caryophyllene that can be used
as a signal to locate more suitable plants (Robert etal. 2012).
In such cases, the emission of induced VOCs can increase
herbivory rates, harming the plant.
On the other hand, induced VOCs can repel some spe-
cies of herbivores. The aphid M. persicae had a significant
preference for the volatiles of undamaged Brassica rapa
compared to those damaged by cospecifics and with the
caterpillar Heliothis virescens (Lepidoptera: Noctuidae).
The reduced attraction may be associated with changes in

R.H.S.Bezerra et al.
1 3
the composition of VOCs, including the emission of (E)-β-
farnesene by aphid-infested plants, a compound generally
found in alarm pheromones of some species (Verheggen
etal. 2013).
In addition to attraction and repellency, studies have
shown that the induced VOCs can discourage the oviposi-
tion of some herbivore species, as occurs for H. virescens (de
Moraes etal. 2001), M. sexta (Reisenman etal. 2013), and
Tuta absoluta (Lepidoptera: Gelechiidae) (Anatasaki etal.
2018) in plants damaged by cospecifics. Kessler and Bald-
win (2001) observed that the oviposition rate of Manduca
quinquemaculata was reduced by the emission of VOCs
induced both by cospecifics as well as by Dicifo minimus
(Heteroptera: Miridae) and Epitrix hirtipennis (Coleoptera:
Chrysomelidae) on tobacco plants.
Depending on the ecological context, the same species of
herbivore can be attracted or repelled by VOCs induced in
different plant species. For example, T. urticae is repelled
by P. lunatus plants infested with cospecifics (Dicke 1986),
but in cotton, Gossypium hirsutum (Malvaceae), this mite
prefers healthy plants compared to the infested ones (Har-
rison and Karban 1986). In contrast, another study reported
a slight preference of T. urticae for cucumber plants infested
by cospecifics, but the same mite was repelled by plants
infested with F. occidentalis (Pallini etal. 1997).
Influence ofherbivore‑induced VOCs onplant–plant
communication
Induced VOCs can also represent some important com-
munication signals between neighboring plants or within
the same plant (Karban etal. 2006). They can mediate
plant–plant interactions, inducing the expression of defense
genes and emission of VOCs by healthy parts in the same
plant or in neighboring non-damaged plants, increasing their
attractiveness to natural enemies and decreasing their sus-
ceptibility to the herbivore (Dicke etal. 1990; Moreira etal.
2016; Mutyambai etal. 2016; Meents and Mithöfer 2020;
Timilsena etal. 2020). Exposure to VOCs can also induce
the production of extrafloral nectar (see below), which help
the survival and maintenance of natural enemies in plants
(Kost and Heil 2006).
The exposure of plants to induced VOCs prepares them
to express the induced defenses more quickly and intensely
against the subsequent attack of an herbivore (Kessler etal.
2006; Pinto-Zevallos etal. 2013; Aljbory and Chen 2018).
In this way, plants that can activate their defenses according
to information derived from their neighbor have an advan-
tage over plants that cannot use this information (Kost and
Heil 2006), since it reduces the investment of the receiving
plant in chemical defenses until the onset of nearby herbi-
vore damage (Engelberth etal. 2004; Kessler etal. 2006).
The first experiments that demonstrated the interaction
between plants mediated by induced VOCs were done by
Baldwin and Schultz (1983). They observed that maple,
Acer saccharum (Sapindaceae), and poplar trees, Populus
euroamericana (Salicaceae), damaged by the removal of part
of the leaf area, exhibited higher concentrations of phenolic
compounds in response to the injury. The same occurred in
the nearby undamaged plants, indicating that these signals
from damaged tissues may stimulate biochemical changes
in neighboring plants.
Since that pioneering study, an increasing number of
studies with different species have reported that plants can
perceive VOCs emitted by neighboring plants (Kost and Heil
2006; Heil and Silva-Bueno 2007; Ali etal. 2013; Moreira
etal. 2016; Mutyambai etal. 2016; Ninkovic etal. 2020;
Timilsena etal. 2020). For example, healthy bean plants
exposed to VOCs from conspecifics infested with T. urticae
emitted a similar group of volatiles as the damaged plants.
The same work observed that leaves infested with T. urti-
cae, which had previously been exposed to the volatiles of
induced leaves, emitted more VOCs and were more attrac-
tive to the predator P. persimilis than the leaves infested by
T. urticae exposed to volatiles of non-infested leaves (Choh
etal. 2004).
Influence ofherbivore‑induced VOCs onpollinator
behavior
In addition to influencing the behavior of herbivores and
natural enemies, plant-induced responses to herbivory can
mediate not only tritrophic interactions but also interactions
involving other actors in the community, for example, modi-
fying the attraction behavior and choice of resources by pol-
linators (Bruinsma etal. 2014; Rusman etal. 2019), which
can confer ecological costs (Rusman etal. 2019). These eco-
logical costs may have a negative impact on plant fitness due
to the response induced by herbivores (Kessler etal. 2011;
Poelman and Kessler 2016), such as the reduced attraction
of pollinators (Heil and Baldwin 2002; Kessler etal. 2011).
As herbivore-induced plant responses can be expressed
in a systemic way, leaf and root herbivory also affects floral
traits (Kessler and Halitschke 2009; Lucas-Barbosa etal.
2016; Rusman etal. 2019), since many resources are allo-
cated to defense at the expense of growth and reproduction
(Herms and Mattson 1992; Lehtilä and Strauss 1999; Strauss
etal. 2002), or by the presence of repellent and toxic com-
pounds in flowers and floral rewards (Irwin and Adler 2006;
Zangerl and Berenbaum 2009; Schiestl etal. 2014). These
changes in floral characteristics can affect the behavior of
both mutualistic and antagonistic visitors (Kessler and Hal-
itschke 2009; Kessler etal. 2011, 2015; Schiestl etal. 2014).
Pollinator visitation is influenced by visual and olfactory
cues that can indicate the quantity and quality of pollen and

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
nectar, such as the odor and color of flowers (Bruinsma etal.
2014; Lucas-Barbosa etal. 2016; Agren 2019; Barragán-
Fonseca etal. 2020). Hence, changes in flower characteris-
tics and in the rewards offered can negatively influence the
visitation of pollinators and consequently reduced seed and
fruit production (Bruinsma etal. 2014).
Herbivory can affect pollinator behavior instantly, when
pollinators avoid flowers damaged by herbivores due to
altered floral characteristics (Muola etal. 2017; Rusman
etal. 2019) or avoid contact with herbivores in flowers
(Lohman etal. 1996). During and soon after the attack,
herbivores-induced metabolic changes in plants can mod-
ify the quality of floral rewards (Adler etal. 2006) and the
chemical information that mediates interactions (Kessler and
Halitschke 2009; Kessler etal. 2011; Schiestl etal. 2014;
Cozzolino etal. 2015).
The several studies have demonstrated that the effects
induced by herbivory include reduced number of flowers
(Hambäck 2001; Barber etal. 2015), smaller flower size
(Steets and Ashman 2004; Poveda etal. 2005), reduced
quantity and quality of floral rewards (Adler etal. 2006;
Chautá etal. 2017; Rusman etal. 2019), changes in flow-
ering phenology (Poveda etal. 2003; Kessler etal. 2010;
Hoffmeister etal. 2016), and changes in sexual expression
of flowers (Krupnick and Weiss 1998; Lehtilä and Strauss
1999). Herbivory can also alter floral chemistry, increas-
ing the amount of secondary defense metabolites in nectar
(Adler etal. 2006; Kessler and Baldwin 2007), modifying
the emission of floral VOCs (Bruinsma etal. 2014; Lucas-
Barbosa etal. 2016), increasing the emission of induced
VOCs with repellent properties (Kessler and Halitschke
2009; Zangerl and Berenbaum 2009; Kessler etal. 2011),
or reducing the emission of alluring floral VOCs (Bruinsma
etal. 2014; Schiestl etal. 2014).
Most studies demonstrate that plant responses induced
by herbivory can reduce pollinator attraction and visitation
(Schiestl etal. 2014; Barber etal. 2015; Chautá etal. 2017);
however, other studies found increased attraction (Poveda
etal. 2003, 2005; Cozzolino etal. 2015) or neutral effects
(Hladun and Adler 2009; Bruinsma etal. 2014; Lucas-Bar-
bosa etal. 2016). The exposure of mustard plants Brassi-
canigra (Brassicaceae), to the herbivory of different her-
bivore functional groups (chewing herbivores, sap-feeding
herbivores, and root herbivores) induced changes in multi-
ple flower traits and affected pollinator behavior. Except for
flower color, the induced changes were herbivore species-
specific and beyond feeding guild. Thus, the response of
plants to herbivores can have positive, negative, or neutral
effects on pollinator behavior (Rusman etal. 2019).
Another study demonstrated that the damage caused by
locusts on the leaves of Palicourea angustifolia (Rubiaceae)
resulted in flowers with shorter styles and less nectar, which
reduced the visitation of two species of hummingbird and
two species of pollinating bees (Chautá etal. 2017).
Therefore, the study of the clues explored by pollinators
is fundamental to understand how the responses of plants
induced by herbivory can influence the behavior of pollina-
tors and other members of the community, affecting plant
fitness (Bruinsma etal. 2014; Barber etal. 2015; Cozzolino
etal. 2015; Rusman etal. 2019).
Influence ofplant‑symbiotic root interactions
onVOC emission induced byherbivores
Below or above ground, organisms can interact and alter
each other’s fitness through direct and indirect effects medi-
ated by the host plants they share (Rasmann and Turlings
2007; Erb etal. 2008; Babikova etal. 2014; Chagas etal.
2018). Several studies have shown that the association of
plants with root symbionts organisms, including arbuscular
mycorrhizal fungi, rhizobia, symbiotic bacteria, detritivores,
and decomposers, can alter the result of their interactions
with herbivores (Babikova etal. 2014; Kaling etal. 2018)
and natural enemies (Guerrieri etal. 2004; Schausberger
etal. 2012; Pappas etal. 2018). These associations can help
plant fitness by significantly increasing nutrient absorption,
growth, and stress tolerance (Smith etal. 2010; Berendsen
etal. 2012; Pineda etal. 2013; Zeilinger etal. 2016). Fur-
thermore, these symbionts can increase tolerance to patho-
gens (Whipps 2004; de La Peña etal. 2006) and induce the
systemic resistance of the plant against herbivores (Campos-
Soriano etal. 2012; Jung etal. 2012; Pieterse etal. 2014).
Root symbionts can also alter and improve the indirect
defense of the plant by changing the size/vigor of the plant,
the primary and secondary metabolism of the plant, and the
emission of VOCs (Rasmann etal. 2017). Although most
evidence of a positive influence from underground mutu-
alists on the inducibility of defense mechanisms in plants
comes from arbuscular mycorrhizal fungi, the importance of
other groups, such as rhizobia, for induced plant responses
has recently been better understood (Ballhorn etal. 2013).
Plant-symbiotic root interactions can trigger important
changes in the primary and secondary metabolism, such as
the accumulation of defense compounds and phytohormones
(López-Raéz etal. 2010; Cappellari etal. 2017; Kaling etal.
2018). Although still poorly studied, the effects of symbiotic
organisms on the emission of VOCs include several mecha-
nisms. Symbionts can alter plant volatiles by changing the
amount of some compounds, producing their own VOCs or
by metabolizing those emitted by the plant (Farré-Armengol
etal. 2016). For example, the association of the mycorrhi-
zal fungus Glomus mosseae with P. vulgaris increased the
emission of β-ocimene and β-karyophylene in plants sub-
mitted to herbivory by T. urticae. This increase influenced
their attractiveness to the predatory mite P. persimilis, which

R.H.S.Bezerra et al.
1 3
preferred mycorrhizal plants compared to non-mycorrhizal
plants (Schausberger etal. 2012). In another study, Pappas
etal. (2018) reported the influence of the endophytic fun-
gus Fusarium solani on the tritrophic interaction between
tomato, the herbivorous mite T. urticae, and the zoophy-
tophagous predator Macrolophus pygmaeus (Hemiptera:
Miridae). In the study, colonization by F. solani triggered the
differentiated expression of genes related to plant defense,
in response to the attack by T. urticae. Colonization by
F. solani also triggered the indirect defense of the plant,
through significant differences between the VOCs emitted by
the colonized plants and control plants, resulting in a greater
attraction of predators to plants colonized with this fungus.
In addition to the symbiotic fungi, rhizobacteria can also
influence tritrophic interactions through the emission of
VOCs. For example, Ballhorn etal. (2013) demonstrated
that rhizobia colonization of lima bean, plants resulted in
the alteration of jasmonic acid-induced volatile blends. Such
changes resulted in a greater olfactory preference of the
Mexican bean beetle, Epilachna varivestis (Coleoptera: Coc-
cinellidae), which is a specialist herbivore insect, for non-
induced plants when they grew in symbiosis with rhizobia.
Root symbionts not only affect the expression of VOCs
(Vannette and Hunter 2013; Malik etal. 2018), but also alter
other defense mechanisms, such as the production of extra-
floral nectar, affecting superior trophic levels and evidencing
the complexity of the ecological effects of these mutualists
(Rasmann etal. 2017; Tao etal. 2017).
These organisms can also affect the emission of differ-
ent VOC groups in the same plant. Pangesti etal. (2015)
observed that the colonization of the rhizobacterium Pseu-
domonas fluorescens in Arabdopsis thaliana (Brassicaceae)
suppressed the emission of the terpene (E)-α-bergamotene
and the aromatics methyl salicylate and lilial in response
to the feeding of the caterpillar Mamestra brassicae (Lepi-
doptera: Noctuidae). However, even with the suppression of
volatiles, inoculated plants were more attractive to parasitic
wasp Microplitis mediator (Hymenoptera: Braconidae) com-
pared to control plants. Thus, by simultaneously affecting a
set of defensive characteristics of the plant, associations with
root symbionts can modulate the interactions of plants with
different trophic levels above and belowground. However,
this modulation depends on the particular species of insect
herbivores and their natural enemies considered.
Ecological costs ofplant‑symbiotic root interactions
In essence, the mutualistic interaction between plant and
root symbionts is supported by the sugar (carbon) supplied
by the host plant in exchange for mineral nutrients and water.
The tradeoff in allocation of plant resource between root
mutualists and indirect defense rewards may explain the
reduced attractiveness of natural enemies in some cases.
For example, root symbionts can affect the protocooperation
between ants and their host plant, reducing the production of
extrafloral nectaries and nectar, which impairs protection by
ants against herbivores (Laird and Addicott 2007; Godschalx
etal. 2015).
By changing the VOC expression by plants, microbial
root mutualists can increase the attractiveness of the host
plant to associated herbivores. For example, Fontana etal.
(2009) observed that in the presence of arbuscular myc-
orrhizal fungi, herbivore-induced sesquiterpenes were
reduced, which influence the recruitment of parasitoids after
herbivory.
The carbon costs associated with hosting root symbionts
also affect plant nutritional status by changes in vegetative
and/or reproductive characteristics, which can reduce not
only VOC emissions but also plant fitness (Koricheva etal.
2009; Babikova etal. 2014) and indirectly affect predators
and parasitoids aboveground in different ways (Tao etal.
2017).
Extraoral nectar intritrophic interactions
Extrafloral nectaries are nectar-producing structures that are
a predictable and abundant source of food, especially rich in
carbohydrates. Similar to VOCs induced by herbivores, nec-
taries can act in the indirect defense of the plant by increas-
ing the attraction, retention, and efficiency of some natural
enemies (Cortesero etal. 2000).
More than 100 plant families have extrafloral nectaries
(Marazzi etal. 2013; Weber and Keller 2013), including
ferns, gymnosperms, and angiosperms (Heil 2008). They
can vary in abundance, shape, and distribution throughout
the plant, and can be present in any aerial part such as leaves,
stipules, inflorescences, pedicels, and external floral organs,
but are never found on the roots (Marazzi etal. 2013). Nec-
taries can be either anatomically visible or invisible struc-
tures (Heil 2015).
Extrafloral nectar (EFN) is an aqueous solution rich in
mono and disaccharides, as well as amino acids, lipids, and
enzymes with an attractive and nutritious function for its
consumers (Nicolson and Thornburg 2007). The availabil-
ity of this resource influences the presence and abundance
of some arthropods, especially ants (Leal etal. 2006; Kop-
tur etal. 2013), along with other predators and parasitoids,
such as wasps (Wäckers 2001; Jamont etal. 2014), spiders
(Ruhren and Handel 1999; Whitney 2004), beetles (Krakos
etal. 2011), and mites (Bakker and Klein 1993; Kost and
Heil 2005), which can participate in the indirect defense of
the plant by disturbing, attacking, or consuming herbivores
and seed consumers (Marazzi etal. 2013).

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
Little is known about the mechanisms that involve EFN
synthesis, induction, and regulation (Escalante-Pérez and
Heil 2012; Orona-Tamayo etal. 2013). It is widely accepted
that floral and extrafloral nectar are produced through the
same general mechanisms, and the influence of jasmonic
acid and an invertase of the cell wall play a role in the dis-
charge of sucrose in the phloem (Orona-Tamayo etal. 2013;
Heil 2015). In addition, sucrose availability in phloem has
been shown as a limiting factor for EFN secretion (Millán-
Cañongo etal. 2014). However, although phloem sap can
be thought of as ‘pre-nectar’ for many plant species (Roy
etal. 2017), recent studies have demonstrated a biochemical
complexity, such as the presence of sugars and amino acids,
which does not originate from phloem (Escalante-Pérez
etal. 2012; Orona-Tamayo etal. 2013).
In the myrmecophytic plant, Acacia cornigera (Fabaceae),
Orona-Tamayo etal. (2013) observed that nectar and phloem
sap significantly differed in their chemical composition, par-
ticularly in terms of hexoses and dominate nectar proteins
(nectarins). Among the six functionally important genes
in the synthesis of nectar components that were analyzed,
five were expressed only in the nectary tissue, excluding
the phloem as the direct source of sugars and proteins from
EFN (Orona-Tamayo etal. 2013). Similarly, genes related to
exocytosis, hormone metabolism and sugar metabolism were
over-expressed in extrafloral nectaries of the hybrid aspen
Populus tremula × Populus tremuloides (Ptt) (Salicaceae)
compared to the leaf tissue (Escalante-Perez etal. 2012).
Other studies have been developed with the aim of identify-
ing and understanding the genes and mechanisms involved
in EFN synthesis (Jaborsky etal. 2016; Chatt etal. 2019;
Hu etal. 2020).
EFN is secreted in greater quantities in the most suscepti-
ble stages of plant growth (Bentley 1977), mainly in the most
valuable organs that contribute to fitness and demand higher
energy costs, such as young leaves and developing fruits,
and when the pressure of the herbivore increase according
to the predictions of the Optimal Defense Theory (Rhoades
and Cates 1976; Rostás and Eggert 2007; Millán-Cañongo
etal. 2014; Heil 2015; Calixto etal. 2020). Bentley (1977)
associated the highest rates of EFN and consequently greater
visitation of ants to the most vulnerable stage of develop-
ment of the Bixa orellana (Bixaceae), when its flower buds
were generally more damaged by herbivores. Plants with
higher visitation rates and extrafloral nectaries produce more
fruit, suggesting that the presence of ants reduced herbivory
and increased plant fitness.
Plants can produce EFN in a constitutive manner (Wäck-
ers 2001; Turlings and Wäckers 2004), but studies have
shown that its production can also be induced and increased
after the damage caused by herbivores, either in relation
to volume (Heil etal. 2001; Choh and Takabayashi 2006)
or the number of nectaries (Mondor and Addicott 2003).
In addition to responding to damage, EFN production can
vary according to the species of herbivore (Carrillo etal.
2012; Nam 2018); the age of the plant (Radhika etal. 2008;
Kwok and Laird 2012; Jones and Koptur 2015) and its leaves
(Heil etal. 2000); climatic conditions, such as temperature
and precipitation (Calixto etal. 2020); the period of the day
(Raine etal. 2002; Dáttilo etal. 2015; Lange etal. 2017);
and the presence of light (Radhika etal. 2010). Jones and
Koptur (2015) observed that EFN production in Senna mexi-
cana (Fabaceae) plants is higher at night and by older plants.
In addition, they found that EFN production increased in
response to mechanical damage (mainly to young leaves)
and that the damage resulted in an increased rate of visita-
tion by ants in the field.
Influence ofVOCs induced byherbivores
onthesecretion ofextrafloral nectar
As previously mentioned, the production of EFN can be
induced and increased by herbivory. Some studies have
shown that this increase in nectar production after herbivory
is probably related to the exposure to induced VOCs (Choh
etal. 2006; Heil and Silva-Bueno 2007; Blande etal. 2010;
Choh and Takabayashi 2010; Li etal. 2012). EFN induction
was observed after exogenous application of jasmonic acid
(Kost and Heil 2008; Hernandez-Cumplido etal. 2016) and
the exposure of plants to induced VOCs (Choh etal. 2006;
Choh and Takabayashi 2006; Heil and Silva-Bueno 2007),
which can prepare the plant to secrete EFN more quickly and
in greater quantities to attract natural enemies (Choh etal.
2006; Kost and Heil 2006) compared to unexposed plants.
The increase in EFN secretion was observed in healthy
lima bean plants exposed to VOCs induced by the herbivory
of Cerotoma ruficornis and Gynandrobrotica guerreroensis
(Coleoptera: Chrysomelidae) (Heil and Silva-Bueno 2007).
This exposure to VOCs also reduced the damage caused by
herbivores and lead to a higher growth rate of plants, com-
pared to plants that were not exposed. Later, non-infested
lima bean plants exposed to VOCs induced by phytopha-
gous mites attracted more predatory mites and produced
more EFN than unexposed plants. Then, when subjected to
herbivory for two days, the exposed plants attracted more
predators and secreted more EFN than the plants that were
not exposed; however, this difference was not observed when
the plants were infested for four days (Choh and Takabayashi
2010), suggesting that EFN production in response to her-
bivory is short-term.
On the other hand, exposure of healthy hybrid aspen
plants to VOCs of infested cospecifics induced secretion of
EFN but did not induce the emission of volatile terpenes (Li
etal. 2012). However, these authors reported that after herbi-
vore attack, the plants previously exposed to induced VOCs

R.H.S.Bezerra et al.
1 3
released significantly more terpenes and more quickly than
unexposed plants, while EFN secretion did not increased.
These results indicate that induced VOCs prepare plants to
emit VOCs in response to damage. Thus, the exposure of
healthy plants to induced VOCs can improve the response of
plants, increasing the attraction of natural enemies compared
to plants without previous exposure.
Influence ofextrafloral nectar onthebehavior
ofnatural enemies
The role of EFN as an indirect defense mechanism of the
plant is well documented and most studies reveal that its
presence can increase the attraction and retention of natu-
ral enemies (Jones and Koptur 2015; Mathews etal. 2016;
Hernadez-Cumplido etal. 2016; Kautz etal. 2017) with the
consequent reduction of the damage caused by herbivores,
increasing the fitness of the plant. By allowing defensive
interactions between plants and natural enemies through the
availability of resources in exchange for protection against
herbivores, EFN secretion can increase the success of plants
by shaping the composition of the community and structur-
ing arthropod communities (Marazzi etal. 2013), facilitating
the evolution of mutualistic interactions between plants and
different species (Bronstein etal. 2006).
The defensive interaction between plants and ants was
first described by Thomas Belt (1874), when he observed
the presence of hollow spines, extrafloral nectaries, and food
bodies in A. cornigera, which serve as shelter and food for
Pseudomyrmex ferruginea (Hymenoptera: Formicidae). The
ant, in turn, responds aggressively to any approach by herbi-
vores and leaf-cutting ants, indicating that these structures
serve for their attraction and maintenance in the acacia.
Subsequently, several studies have reinforced this type
of interaction (Bentley 1977; Leal etal. 2006; Koptur etal.
2015; Fagundes etal. 2017; Pereira etal. 2020). The pres-
ence of extrafloral nectaries in the fern, Pleopeltis crass-
inervata (Polypodiaceae), for example, coincided with a
higher rate of visitation by ants and consequently greater
removal of caterpillars compared to plants that had their
nectaries covered (Koptur etal. 2013). Similarly, Kautz
etal. (2017) found that mechanically damaged Prunus
laurocerasus (Rosaceae) significantly increased its EFN
production increasing recruitment of ants that reduced the
presence of the weevil, Otiorhynchus sulcatus (Coleoptera:
Curcuionidae).
Besides the damage caused to the aerial parts of plants,
root herbivory can induce a systemic response, increasing
EFN secretion (Wäckers and Bezemer 2003; Mathur etal.
2012; Huang etal 2015). Root feeding by D. radicum lar-
vae in Brassica juncea (Brassicaceae) plants increased EFN
production compared to undamaged plants. In addition, the
parasitoid, Trybliographa rapae (Hymenoptera: Figitidae),
significantly preferred the plant’s EFN when subjected to a
choice between the nectar and water solution (Mathur etal.
2012).
Mechanical damage and the exogenous application of
phytohormones, such as jasmonic acid, can also induce EFN
secretion in some plant species (Heil etal. 2001; Hernan-
dez-Cumplido etal. 2016; Kautz etal. 2017; Williams etal
2017; Stefani etal. 2019), increasing the attraction of natural
enemies, even in the absence or low prey density. The secre-
tion of EFN by Macaranga tanarius (Euphorbiaceae) in the
field increased after the herbivory of Xenocatantops humi-
lis (Orthoptera: Acrididae), mechanical damage, or exog-
enous application of jasmonic acid, with a greater number
of natural enemies and less herbivores in plants that have
suffered the application of jasmonic acid (Heil etal. 2001).
Another study observed that the application of jasmonic acid
in lima bean plants induced the secretion of EFN, resulting
in increased attraction of ants compared to untreated plants
(Hernandez-Cumplido etal. 2016).
The presence of EFN can influence not only the attrac-
tion and retention of natural enemies, but also help their
survival, development, and reproduction (Gnanvossou etal.
2005; Mathews etal. 2016; Xiu etal. 2017). The presence
of extrafloral nectar in Hibiscus cannabinus (Malvaceae)
helped maintain the adult population of Harmonia axyridis
(Coleoptera: Coccinelidae) in the field, even when the popu-
lations of aphids were low or absent. In addition, laboratory
experiments have demonstrated a significant increase in the
longevity of predators when fed with a combination of EFN
and aphids compared to aphids only (Xiu etal. 2017).
Although most evidence reports an increase in EFN pro-
duction, some studies show that, depending on the ecologi-
cal context, the damage caused by the herbivore may not
affect (Yoshida etal. 2017; Nam 2018; Abdala-Roberts etal.
2019) or even reduce nectar secretion due to reduced photo-
synthetic area, nectar consumption, and damage or predation
of extrafloral nectaries (Li etal. 2012; Ballhorn etal. 2014;
Gish etal. 2015; Yoshida etal. 2017; Nam 2018).
Mechanical damage and the application of jasmonic acid
or Spodoptera litura (Lepidoptera: Noctuidae) regurgite
did not affect EFN production in Impatiens balsamia (Bal-
saminaceae), while the damage caused by aphid feeding,
Impatientinum impatiens (Hemiptera: Aphididae), decreased
nectar production, suggesting that secretion can be altered
by the species and type of herbivore feeding (Nam 2018).
Another study observed that feeding by Epirrita autumnata
(Lepidoptera: Geometridae) larvae on hybrid aspen plants
not only significantly reduced EFN secretion by infested
leaves but also caused a reduction in systemic non-infested
leaves (Li etal. 2012).
Although the role of EFN in attracting natural enemies is
well established, few studies have demonstrated beneficial
effects on plant fitness (Ruhren and Handel 1999; Cuautle

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
and Rico-Gray 2003; Rudgers 2004; Mathews etal. 2007,
2009; Dutton etal. 2016; Hernandez-Cumplido etal. 2016;
Pereira etal. 2020). Ants exclusion experiments showed that
peach plants, Prunus persica (Rosaceae), with extrafloral
nectaries had fewer Grapholita molesta (Lepidoptera: Tort-
ricidae) caterpillars when the ants were present and that trees
with EFN had a 90% reduction in fruit injuries caused by the
caterpillar (Mathews etal. 2007). Subsequently, the authors
observed that trees with EFN showed lower rates of her-
bivory and increased stem growth, fruit and bud production,
and greater diversity of arthropods (Mathews etal. 2009).
More recently, Dutton etal. (2016) found that Turnera
ulmifolia (Turneraceae) plants that produce EFN had more
seeds removed by ants than plants that do not, suggesting
that nectar may also play a role in seed dispersal.
Influence ofextrafloral nectar onpollinator
behavior
The effects of EFN on plant-pollinator interactions are
context dependent. Some ants attracted by EFN can repel
floral visitors and seed dispersers due to their presence or
aggressiveness, representing ecological costs for plants (Vis-
ser etal. 1996; Altshuler 1999; Ness 2006; Assunção etal.
2014). For example, a reduction in the population of ten of
the eleven insect taxa found in Protea repens (Proteacea)
was observed when the ant Linepithema humile (Hymenop-
tera: Formicidae) was abundant, which can delay pollina-
tion and the reproductive capacity of the plant (Visser etal.
1996). Another study noted that the presence of Ectatomma
ruidum and Ectatomma tuberculatum (Hymenoptera: For-
micidae) on the leaves of Psychotria limonensis (Rubiaceae)
improved the pollination and fruiting rates of the plants but
had a negative effect on the removal of fruits by fruit birds,
influencing its dispersion (Altshuler 1999).
Negative impacts have also been reported on Ferocac-
tus wislizeni (Cactaceae) plants when Solenopsis xyloni
(Hymenoptera: Formicidae) was associated with extrafloral
nectaries. The visits and the length of stay of bees reduced
due to the aggressiveness and abundance of the ants. In addi-
tion, the plants produced fruits with a significantly lower
total seed mass (Ness 2006). Sousa-Lopes etal. (2020) also
observed that floral visitors decrease the time spent during
visits on the extrafloral nectaries bearing Declieuxia fruti-
cosa (Rubiaceae) with the presence of ants. However, in this
case, the ants can be beneficial to the plants as they induce
pollinators to do shorter visits and search for other flow-
ers or other plants, so this behavior may contribute to plant
outcrossing. A study in Turnera subulata (Turneraceae)
bearing extrafloral nectaries, also found that the presence of
ants decreased the frequency of flower visitation but did not
affect plant reproductive success (Santos and Leal 2019).
On the other hand, the EFN in Sambucus javanica (Adox-
aceae) attracts both ants and flying pollinators, significantly
increasing the frequency of visiting pollinators, and had no
effect on the final fruit production (Jiang etal. 2019).
Recently, Villamil etal. 2019 examining the ecological
functions of EFN further noted that extrafloral nectaries
located near flowers may prevent ants from stealing flo-
ral nectars during the crucial pollination period, thereby
reducing ant-pollinator conflicts and thus increasing plant
reproductive success. Another hypothesis considered in a
few studies is that ants could also function as pollinators,
because when in search of EFN, they vector pollen (Ashman
and King, 2005; Ohm and Miller 2014).
Ecological costs ofproducing extrafloral nectar
Although EFN can increase the attraction, retention, and effi-
ciency of natural enemies, some studies report that the pres-
ence of EFN can also cost plants by attracting herbivores and
arthropods that do not provide plant protection, excluding
natural enemies through competition (Heil etal. 2004) and/
or reducing the attraction of pollinators and seed dispersers
(Visser etal. 1996). Laboratory experiments demonstrated,
for example, that Pseudoplusia includens (Lepidoptera:
Noctuidae), oviposited significantly more in cotton that had
EFN compared to plants without, attributing the increased
fertility and fecundity of the herbivore to the use of EFN
(Beach etal. 1985).
A negative interaction was also observed in the myrme-
cophilic M. tanarius plant. Ants and other species of arthro-
pods were found, especially the flies Grammicomya sp. and
Mimegralla sp. (Diptera: Micropezidae) among the visitors
to the nectaries. Flies actively excluded beneficial arthro-
pods, causing ecological costs by reducing the presence of
ants that consume EFN and defend plants, since flies have
no defensive effect (Heil etal. 2004).
Despite the negative effects, most studies have shown that
the presence of EFN can play an important role in indirect
defenses (Heil etal. 2001), as a wide variety of natural ene-
mies can benefit from the supply of EFN, and many of them
can affect herbivores. Thus, EFN secretion can have multiple
effects on the level of entire ecosystems (Heil 2015).
Challenges andfuture perspectives
The ecological role of VOCs and EFN in the modulation
of tritrophic interactions is fundamental and recent studies
have shown that the processes involved in this modulation
are multiple and complex. Unfortunately, part of the benefits
is offset by costs that are directly involved with the multi-
functionality of VOCs and EFN (such as the attraction of
herbivores and other undesirable arthropods) or with factors

R.H.S.Bezerra et al.
1 3
often neglected by current protocols and bioassays. Such
factors are still poorly understood and represent important
challenges to be overcome (Brilli etal. 2019; Takabayashi
and Shiojiri 2019). For example, in natural field conditions,
a plant is usually infested by more than one species of her-
bivore, leading to the emission of a different mix of VOCs
from that released by a plant infested with a single species
(Stam etal. 2014). The difference in the blends emitted may
be one of the reasons why some results observed in labora-
tory studies are not reproduced in field conditions (Bruce
etal. 2015; Pickett and Khan 2016; Takabayashi and Shiojiri
2019).
The difficulties mentioned above can be minimized by
including in future studies more detailed data of all com-
pounds found in the blends, quantitative measurements of
VOC emissions from a broader spectrum of plant functional
groups (i.e., herbs, shrubs, and trees), and the different func-
tional groups of herbivores (Faiola and Taipale 2020). It has
been found, for example, that fewer studies have examined
VOCs emission induced by sucking insects than VOCs emit-
ted in response to chewing insects (Faiola and Taipale 2020).
In addition to the need for studies that address the specific
effects of species in field conditions, more in-depth studies
are needed on the range of action by blends (Meents and
Mithöfer 2020), as well as the effect of climatic conditions
on the emission of volatiles and EFN (Loreto etal. 2014).
Recent studies have pointed to the implication of plant-
induced VOCs in atmospheric chemical processes. Some
highly reactive VOCs are particularly important for their
effects on atmospheric composition and air quality (Loreto
etal. 2014). According to Faiola and Taipale (2020), models
about VOC emissions can be improved with the inclusion
of some variables, such as the accurate emission of these
compounds in natural environments, the temporal dynamics
of induced-VOC emissions after the onset of the herbivore
population outbreak, and the analysis of VOC emissions
after the plant is subjected to multiple stressors. Instruments
to detect, characterize, and quantify the emission rates of
induced VOCs from plants in the field have been developed
and improved, and can provide valuable data that will fill
many of these gaps indicated and a significant advance in
current knowledge. Within these new analytical technolo-
gies, the "Time-of-Flight" mass spectrometry of high resolu-
tion proton transfer (PTR-TOF-MS) enables the instant and
highly sensitive detection of the entire spectrum of VOCs
with high resolution power (Graus etal. 2010). According to
Brilli etal (2019), an advantage of the PTR-TOF-MS tech-
nique would be to provide a complete and invivo measure-
ment of all the blends of VOCs emitted by the plant.
New perspectives also involve more in-depth studies on
how the induction of defense mechanisms (VOCs and EFN)
can influence the plant fitness (number of seeds, fruits, and
descendants), since plant hormones and metabolic pathways
involved in indirect defense have other functions in plant
physiology, such as regulating growth, development, and dif-
ferentiation of tissues (Aljbory and Chen 2018). Researchers
have already observed that the induction of defense mecha-
nisms can affect floral traits, which reduces the quality of
floral rewards and increases the amount of defense metabo-
lites in the nectar, making floral odors repellent or simply
unattractive to pollinators (Rusman etal. 2019). Conse-
quently, an undesirable effect was a decrease in the number
of seeds and fruits. Therefore, studies are needed to verify
the impact, for the plants themselves, the manipulation of
hormonal pathways, and the artificial release of VOCs in
the field.
The perspectives for the use of VOCs include realistic
and promising strategies in the agronomic and biotechno-
logical areas. Despite the great potential of VOCs, little has
been effectively applied in the field. Some hypotheses that
justify this are the high volatility and reactivity of VOCs
with other compounds (Brilli etal. 2019) and the various
environmental factors, as already mentioned above, limit-
ing the persistence of these compounds in the field. Another
important limitation is related to the high costs associated
with formulation, mass production, registration, and com-
mercialization of synthetic VOCs (Blum etal. 2011), making
it difficult even to finance field research, especially in devel-
oping countries. However, Brilli etal. (2019) pointed out
that the current growing demand for ecologically friendly
and sustainable solutions to protect crops and increase their
productivity may accelerate future investments the use of
VOCs in modern agriculture, especially in greenhouses,
where the emission can be controlled more effectively.
More recently, VOCs have also been used to induce or
strengthen the immune system of plants, a technique called
“green vaccination” (Luna-Diez 2016). Green vaccination
in pest control has great potential, since it is relatively inex-
pensive, with the use of plant compounds that are generally
benign and in low doses, which can increase the attractive-
ness of a plant to natural enemies (Luna-Diez 2016; Bruce
etal. 2017). In addition to the “green vaccination”, the appli-
cation of VOCs and EFN in the field, although incipient,
indicates a high potential of these compounds to improve
other relatively recent strategies, such as the direct applica-
tion of VOCs (e.g., methyl salicylate “MeSa”, Limonene,
and/or JA) in the crop (Rodriguez-Saona etal. 2011; Con-
boy etal. 2020). For example, MeSA is reported to have
an attractive effect on several species of natural enemies,
such as predatory insects, ladybugs, hoverflies, and chrys-
opids (Rodriguez-Saona etal. 2011), and has shown promis-
ing effects against sucking insects, such as the greenhouse
whitefly (Conboy etal. 2020), spider mites, and aphids
(Pinto etal. 2007; Coppola etal. 2018).
Among the various techniques usually applied in agricul-
ture, the “push–pull strategy” has received special attention

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
(Turlings and Erb 2018; Mofikoya etal. 2019). It is a system
of intercropping between plants that emit VOCs able to repel
(“push”) herbivores, surrounded by plants that emit VOCs
that can attract (“pull”) pest insects away from the target
crop plants (Picket and Khan 2016). The plants responsible
for “pulling” herbivores can also be particularly useful for
the early detection of the presence of pests.
In conclusion, VOCs and NEF could be as important tools
for use in modern agriculture. Again, the most important
challenge in the field is that the simultaneous occurrence of
different biotic and abiotic stressors hinders our understand-
ing of how plants adjust their defensive priorities, which
makes it difficult to obtain an effective and broad-spectrum
response.
Author contributions BGA and RHSB conceived of the presented idea.
RHSB wrote the manuscript with support from BGA and LS-S. All
authors discussed the results and contributed to the final manuscript.
BGA supervised the project. LS-S and AEGS provided critical feed-
back and helped shape the manuscript.
Funding The research was supported by the Coordenação de Aper-
feiçoamento de Pessoal de Nível Superior (CAPES) and the Fundação
de Apoio à Pesquisa e Inovação Tecnológica do Estado de Sergipe
(FAPITEC-SE) (project CAPES/FAPITEC-88881.157451/2017–01)
and the INCT-Semioquímicos na Agricultura (CNPq [465511/2014-7]
and FAPESP [2014/50871-0]).
Data availability The references used for writing this article are prop-
erly cited in the text and the articles are available for consultation in
their respective journals.
Declarations
Consent to participate All authors agreed to participate in the article.
Consent for publication All authors consent to the publication of this
article.
References
Abdala-Roberts L, Reyes-Hernández M, Quijano-Medina T, Moreira
X, Francisco M, Angulo DF, Parra-Tabla V, Virgen A, Rojas JC
(2019) Effects of amount and recurrence of leaf herbivory on the
induction of direct and indirect defences in wild cotton. Plant
Biol 21:1063–1071. https:// doi. org/ 10. 1111/ plb. 13022
Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutri-
ents increase nectar alkaloids. Ecol Lett 9:960–967. https:// doi.
org/ 10. 1111/j. 1461- 0248. 2006. 00944.x
Agren J (2019) Pollinators, herbivores, and the evolution of floral traits.
Science 364:122–123. https:// doi. org/ 10. 1126/ scien ce. aax16 56
Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tum-
ilson JH (1997) An elicitor of plant volatiles from beet army-
worm oral secretion. Science 276:945–949. https:// doi. org/ 10.
1126/ scien ce. 276. 5314. 945
Ali JG, Alborn HT, Campos-Herrera R, Kaplan F, Duncan LW, Rod-
ríguez-Saona C, Koppenhöfer AM, Stelinski LL (2012) Subter-
ranean, herbivore-induced plant volatile increases biological con-
trol activity of multiple beneficial nematode species in distinct
habitats. PLoS ONE 7:e38146. https:// doi. org/ 10. 1371/ journ al.
pone. 00381 46
Ali M, Sugimoto K, Ramadan A, Arimura G (2013) Memory of plant
communications for priming anti-herbivore responses. Sci Rep
3:1872. https:// doi. org/ 10. 1038/ srep0 1872
Aljbory Z, Chen M (2018) Indirect plant defense against insect her-
bivores: a review. Insect Sci 25:2–23. https:// doi. org/ 10. 1111/
1744- 7917. 12436
Altshuler DL (1999) Novel interactions of non-pollinating ants with
pollinators and fruit consumers in a tropical forest. Oecologia
119:600–606. https:// doi. org/ 10. 1007/ s0044 20050 825
Anastasaki E, Drizou F, Milonas PG (2018) Electrophysiological and
oviposition responses of Tuta absoluta females to herbivore-
induced volatiles in tomato plants. J Chem Ecol 44:288–298.
https:// doi. org/ 10. 1007/ s10886- 018- 0929-1
Arimura G, Kost C, Boland W (2005) Herbivore-induced indirect plant
defense. Biochim Biophys Acta 1734:91–111. https:// doi. org/ 10.
1016/j. bbalip. 2005. 03. 001
Ashman T-L, King EA (2005) Are flower-visiting ants mutualists or
antagonists? A study in a gynodioecious wild strawberry. Am J
Bot 92:891–895. https:// doi. org/ 10. 3732/ ajb. 92.5. 891
Assunção MA, Torezan-Silingardi HM, Del-Claro K (2014) Do ant
visitors to extrafloral nectaries of plants repel pollinators and
cause an indirect cost of mutualism? Flora 209:244–249. https://
doi. org/ 10. 1016/j. flora. 2014. 03. 003
Babikova Z, Gilbert L, Bruce T, Dewhirst SY, Pickett JA, Johnson
D (2014) Arbuscular mycorrhizal fungi and aphids interact by
changing host plant quality and volatile emission. Funct Ecol
28:375–385. https:// doi. org/ 10. 1111/ 1365- 2435. 12181
Bakker FM, Klein ME (1993) Host plant mediated coexistence of pred-
atory mites: the role off extrafloral nectar and extrafoliar domatia
on cassava. In: Bakker FM (ed) Selecting phytoseiid predators
for biological control, with the emphasis on the significance of
tritrophic interacions, PhD thesis University of Amsterdam,
Amsterdam, pp 33–63
Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry
induced by damage: evidence for communication between plants.
Science 221:277–279. https:// doi. org/ 10. 1126/ scien ce. 221. 4607.
277
Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA
(2006) Volatile signaling in plant–plant interactions: “talking
trees” in the genomics era. Science 311:812–815. https:// doi.
org/ 10. 1126/ scien ce. 11184 46
Ballhorn DJ, Kautz S, Schädler M (2013) Induced plant defense via
volatile production is dependent on rhizobial symbiosis. Oeco-
logia 172:833–846. https:// doi. org/ 10. 1007/ s00442- 012- 2539-x
Ballhorn DJ, Kay J, Kautz S (2014) Quantitative effects of leaf area
removal on indirect defense of lima bean (Phaseolus lunatus)
in nature. J Chem Ecol 40:294–296. https:// doi. org/ 10. 1007/
s10886- 014- 0392-6
Barber NA, Milano NJ, Kiers ET, Theis N, Bartolo V, Hazzard RV,
Adler LS (2015) Root herbivory indirectly affects above- and
below-ground community members and directly reduces plant
performance. J Ecol 103:1509–1518. https:// doi. org/ 10. 1111/
1365- 2745. 12464
Barragán-Fonseca KY, Van Loon JJA, Dicke M, Lucas-Barbosa D
(2020) Use of visual and olfactory cues of flowers of two bras-
sicaceous species by insect pollinators. Ecol Entomol 45:45–55.
https:// doi. org/ 10. 1111/ een. 12775
Battaglia D, Bossi S, Cascone P, Digilio MC, Prieto JD, Fanti P, Guer-
rieri E, Iodice G, Lingua L, Lorito H, Maffei ME, Massa N,
Ruocco H, Sasso R, Trotta V (2013) Tomato below ground-above

R.H.S.Bezerra et al.
1 3
ground interactions: Trichoderma longibrachiatum affects the
performance of Macrosiphum euphorbiae and its natural antago-
nists. Mol Plant Microbe Interact 26:1249–1256. https:// doi. org/
10. 1094/ MPMI- 02- 13- 0059-R
Beach RM, Todd JW, Baker SH (1985) Nectaried and nectariless
cotton cultivars as nectar sources for the adult soybean looper.
J Entomol Sci 20:233–236. https:// doi. org/ 10. 18474/ 0749-
8004- 20.2. 233
Belt T (1874) The naturalist in Nicaragua. University Press of the
Pacific, Londres
Bentley BL (1977) Extrafloral nectaries and protection by pugna-
cious bodyguards. Annu Rev Ecol Syst 8:407–428. https:// doi.
org/ 10. 1146/ annur ev. es. 08. 110177. 002203
Berendsen R, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere
microbiome and plant health. Trends Plant Sci 17:478–486.
https:// doi. org/ 10. 1016/j. tplan ts. 2012. 04. 001
Blande JD, Holopainen JK, Li T (2010) Air pollution impedes plant-
to-plant communication by volatiles. Ecol Lett 13:1172–1181.
https:// doi. org/ 10. 1111/j. 1461- 0248. 2010. 01510.x
Blum B, Nicot PC, Köhl J, Ruocco M (2011) Identified difficul-
ties and conditions for field success of biocontrol: 4. Socio-
economic aspects: market analysis and outlook. In: Tei F (ed)
Classical and augmentative biological control against diseases
and pests: critical status analysis and review of factors influ-
encing their success. IOBC/WPRS Publications, Athens, pp
62–67
Bolsoni VP, Oliveira DP, Pedrosa GS, Souza SR (2018) Volatile
organic compounds (VOC) variation in Croton floribundus (L.)
Spreng. related to environmental conditions and ozone concen-
tration in an urban forest of the city of São Paulo, São Paulo
State Brazil. Hoehnea 45:184–191. https:// doi. org/ 10. 1590/ 2236-
8906- 60/ 2017
Brilli F, Loreto F, Baccelli I (2019) Exploiting plant volatile organic
compounds (VOCs) in agriculture to improve sustainable defense
strategies and productivity of crops. Front Plant Sci 10:264.
https:// doi. org/ 10. 3389/ fpls. 2019. 00264
Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant–insect
mutualisms. New Phytol 172:412–428. https:// doi. org/ 10. 1111/j.
1469- 8137. 2006. 01864
Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, Doherty
A, Sparks CA, Woodcock CM, Birkett MA, Napier JA, Jones
HD, Pickett JA (2015) The first crop plant genetically engineered
to release an insect pheromone for defence. Sci Rep 5:11183.
https:// doi. org/ 10. 1038/ srep1 1183
Bruce TJA, Smart LE, Birch NE, Blok VC, Mackenzie K, Guerrieri
E, Cascone P, Luna E, Ton J (2017) Prospects for plant defence
activators and biocontrol in IPM—concepts and lessons learnt
so far. Crop Prot 97:128–134. https:// doi. org/ 10. 1016/j. cropro.
2016. 10. 003
Bruinsma M, Lucas-Barbosa D, Ten Broeke CJM, Van Dam NM,
Van Beek TA, Dicke M, Van Loon JJA (2014) Folivory affects
composition of nectar, floral odor and modifies pollinator
behavior. J Chem Ecol 40:39–49. https:// doi. org/ 10. 1007/
s10886- 013- 0369-x
Bukovinszky T, Poelman EH, Kamp A, Hemerik L, Prekatsakis G,
Dicke M (2012) Plants under multiple herbivory: consequences
for parasitoid search behaviour and foraging efficiency. Anim
Behav 8:501–509. https:// doi. org/ 10. 1016/j. anbeh av. 2011. 11. 027
Bustos-Segura C, Cuny MAC, Benrey B (2020) Parasitoids of leaf her-
bivores enhance plant fitness and do not alter caterpillar-induced
resistance against seed beetles. Funct Ecol 34:586–596. https://
doi. org/ 10. 1111/ 1365- 2435. 13478
Calixto ES, Lange D, Bronstein J, Torezan-Silingardi HM, Del-Claro
K (2020) Optimal defense theory in an ant–plant mutualism:
extrafloral nectar as an induced defence is maximized in the most
valuable plant structures. J Ecol. https:// doi. org/ 10. 1111/ 1365-
2745. 13457
Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbus-
cular mycorrhizal symbiosis promotes the systemic induction
of regulatory defence-related genes in rice leaves and confers
resistance to pathogen infection. Mol Plant Path 13:579–592.
https:// doi. org/ 10. 1111/j. 1364- 3703. 2011. 00773.x
Cappellari LR, Chiappero J, Santoro MV, Giordano W, Banchio E
(2017) Inducing phenolic production and volatile organic com-
pounds emission by inoculating Mentha piperita with plant
growth-promoting rhizobacteria. Sci Hortic 220:193–198.
https:// doi. org/ 10. 1016/j. scien ta. 2017. 04. 002
Carrillo J, Wang Y, Ding J, Siemann E (2012) Induction of extrafloral
nectar depends on herbivore type in invasive and native Chinese
tallow seedlings. Basic Appl Ecol 13:449–457. https:// doi. org/
10. 1016/j. baae. 2012. 07. 006
Chagas FO, Pessotti RC, Caraballo-Rodríguez AM, Pupo MT (2018)
Chemical signaling involved in plant–microbe interactions.
Chem Soc Rev 47:1642–1704. https:// doi. org/ 10. 1039/ c7cs0
0343a
Chatt EC, Mahalim S-N, Mohd-Fadzil N-A, Roy R, Klinkenberg PM,
Horner HT, Hampton M, Carter CJ, Nikolau BJ (2019) Systems
analyses of key metabolic modules of floral and extrafloral nec-
taries of cotton. BioRxiv 139:322–364. https:// doi. org/ 10. 1101/
857771
Chautá A, Whitehead S, Amaya-Márquez M, Poveda K (2017) Leaf
herbivory imposes fitness costs mediated by hummingbird and
insect pollinators. PLoS ONE 12:e0188408. https:// doi. org/ 10.
1371/ journ al. pone. 01884 08
Chen M (2008) Inducible direct plant defense against insect herbivores:
a review. Insect Sci 15:101–114. https:// doi. org/ 10. 1111/j. 1744-
7917. 2008. 00190.x
Chen S, Zhang L, Cai X, Li X, Bian L, Luo Z, Li Z, Chen Z, Xin Z
(2020) (E)-nerolidol is a volatile signal that induces defenses
against insects and pathogens in tea plants. Hortic Res 7:52.
https:// doi. org/ 10. 1038/ s41438- 020- 0275-7
Choh Y, Takabayashi J (2006) Herbivore-induced extrafloral nectar
production in lima bean plants enhanced by previous exposure to
volatiles from infested conspecifics. J Chem Ecol 32:2073–2077.
https:// doi. org/ 10. 1007/ s10886- 006- 9130-z
Choh Y, Takabayashi J (2010) Herbivore-induced plant volatiles prime
two indirect defences in lima bean. In: Sabelis M, Bruin J (eds)
Trends in Acarology. Springer, Dordrecht, pp 255–258
Choh Y, Shimoda T, Ozawa R, Dicke M, Takabayashi J (2004) Expo-
sure of lima bean leaves to volatiles from herbivore-induced con-
specific plants results in emission of carnivore attractants: active
or passive process? J Chem Ecol 30:1305–1317. https:// doi. org/
10. 1023/B: JOEC. 00000 37741. 13402. 19
Choh Y, Kugimiya S, Takabayashi J (2006) Induced production of
extrafloral nectar in intact lima bean plants in response to vola-
tiles from spider mite-infested conspecific plants as a possible
indirect defense against spider mites. Oecologia 147:455–460.
https:// doi. org/ 10. 1007/ s00442- 005- 0289-8
Conboy NJ, McDaniel T, George D, Ormerod A, Edwards M, Donohoe
P, Gatehouse AMR, Tosh CR (2020) Volatile organic compounds
as insect repellents and plant elicitors: an integrated pest man-
agement (IPM) strategy for glasshouse whitefly (Trialeurodes
vaporariorum). J Chem Ecol 46:1090–1104. https:// doi. org/ 10.
1007/ s10886- 020- 01229-8
Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant-
pathogen interactions. Trends Plant Sci 7:210–216. https:// doi.
org/ 10. 1016/ S1360- 1385(02) 02244-6
Coppola M, Manco E, Vitiello A, Di Lelio I, Giorgini M, Rao R, Pen-
nacchio F, Digilio MC (2018) Plant response to feeding aphids
promotes aphid dispersal. Entomol Exp Appl 166:386–394.
https:// doi. org/ 10. 1111/ eea. 12677

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manip-
ulating plant attributes to enhance biological control. Biol Con-
trol 17:35–49. https:// doi. org/ 10. 1006/ bcon. 1999. 0777
Cozzolino S, Fineschi S, Litto M, Scopece G, Trunschke J, Schiestl FP
(2015) Herbivory increases fruit set in Silene latifolia: a conse-
quence of induced pollinator-attracting floral volatiles? J Chem
Ecol 41:622–630. https:// doi. org/ 10. 1007/ s10886- 015- 0597-3
Cuautle M, Rico-Gray V (2003) The effect of wasps and ants on the
reproductive success of the extrafloral nectaried plant Turnera
ulmifolia (Turneraceae). Funct Ecol 17:417–423
Cuny MAC, Gendry J, Hernandez-Cumplido J, Benrey B (2018)
Changes in plant growth and seed production in wild lima bean
in response to herbivory are attenuated by parasitoids. Oecolo-
gia 187:447–457. https:// doi. org/ 10. 1007/ s00442- 018- 4119-1
Dáttilo W, Aguirre A, Flores-Flores RV, Fagundes R, Lange D,
García-Chávez J, Del-Claro K, Rico-Gray V (2015) Secretory
activity of extrafloral nectaries shaping multitrophic ant-plant-
herbivore interactions in an arid environment. J Arid Environ
114:104–109. https:// doi. org/ 10. 1016/j. jarid env. 2014. 12. 001
De Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey
and non-prey arthropods sharing a host plant: effects on
induced volatile emission and predator attraction. J Chem Ecol
34:281–290
De Moraes CM, Lewis WJ, Tumlinson JH (2000) Examining plant-
parasitoid interactions in tritrophic systems. An Soc Entomol
Bras 29:189–203. https:// doi. org/ 10. 1590/ S0301- 80592 00000
02000 01
De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-
induced nocturnal plant volatiles repel conspecific females.
Nature 410:577–579. https:// doi. org/ 10. 1038/ 35069 058
De la Peña E, Echeverría SR, van der Putten WH, Freitas H, Moens
M (2006) Mechanism of control of root-feeding nematodes by
mycorrhizal fungi in the dune grass Ammophila arenaria. New
Phytol 169:829–840. https:// doi. org/ 10. 1111/j. 1469- 8137. 2005.
01602.x
Dicke M (1986) Volatile spider-mite pheromone and host-plant kair-
omone, involved in spaced-out gregariousness in the spider mite
Tetranychus urticae. Physiol Entomol 11:251–262. https:// doi.
org/ 10. 1111/j. 1365- 3032. 1986. tb004 12.x
Dicke M (1999) Are herbivore-induced plant volatiles reliable indica-
tors of herbivore identity to foraging carnivorous arthropods?
Entomol Exp Appl 91:131–142. https:// doi. org/ 10. 1046/j. 1570-
7458. 1999. 00475.x
Dicke M (2009) Behavioural and community ecology of plants that
cry for help. Plant Cell Environ 32:654–665. https:// doi. org/ 10.
1111/j. 1365- 3040. 2008. 01913.x
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-
induced plant volatiles: beyond the ‘cry for help.’ Trends Plant
Sci 15:167–175. https:// doi. org/ 10. 1016/j. tplan ts. 2009. 12. 002
Dicke M, Sabelis MW (1988) How plants obtain predatory mites as
bodyguards. Neth J Zool 38:148–165. https:// doi. org/ 10. 1163/
15685 4288X 00111
Dicke M, Sabelis MW (1989) Does it play plants to advertize for body-
guards? Towards a cost-benefit analysis of induced synomone
production. In: Lambers H, Cambridge ML, Konings H, Pons
TL (eds) Causes and consequences of variation in growth rate
and productivity of higher plants. SPB Academic Publishing,
The Hague, pp 341–358
Dicke M, Van Loon JJA (2000) Multitrophic effects of herbivore-
induced plant volatiles in an evolutionary context. Entomol Exp
Appl 97:237–249. https:// doi. org/ 10. 1046/j. 1570- 7458. 2000.
00736.x
Dicke M, Van Beek TA, Posthumus MA, Ben Don N, Vanbokhoven
H, De Groot AE (1990) Isolation and identification of a volatile
kairomone that affects acarine predator-prey interaction: involve-
ment of host plant in its production. J Chem Ecol 16:381–396
Dicke M, Gols R, Ludeking D, Posthumus MA (1999) Jasmonic acid
and herbivory differentially induce carnivore-attracting plant
volatiles in lima bean plants. J Chem Ecol 25:1907–1922. https://
doi. org/ 10. 1023/A: 10209 42102 181
Dudareva N, Pishersky E, Gershenzon J (2004) Biochemistry of plant
volatiles. Plant Physiol 135:1893–1902. https:// doi. org/ 10. 1104/
pp. 104. 049981
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant vola-
tiles: recent advances and future perspectives. Crit Rev Plant
Sci 26:417–440. https:// doi. org/ 10. 1080/ 07352 68060 08999 73
Dutton EM, Shore JS, Frederickson ME (2016) Extrafloral nectar
increases seed removal by ants in Turnera ulmifolia. Biotropica
48:429–432. https:// doi. org/ 10. 1111/ btp. 12342
El-Sayed AM, Knight AL, Byers JA, Judd GJR, Suckling DM (2016)
Caterpillar-induced plant volatiles attract conspecific adults in
nature. Sci Rep 6:37555. https:// doi. org/ 10. 1038/ srep3 7555
Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Air-
borne signals prime plants against insect herbivore attack. PNAS
101:1781–1785. https:// doi. org/ 10. 1073/ pnas. 03080 37100
Erb M, Ton J, Degenhardt J, Turlings TCJ (2008) Interactions between
arthropod-induced aboveground and belowground defenses in
plants. Plant Physiol 146:867–874. https:// doi. org/ 10. 1104/ pp.
107. 112169
Escalante-Pérez M, Heil M (2012) Nectar secretion: its ecological
context and physiological regulation. In: Vivanco J, Baluska F
(eds) Secretions and exudates in biological systems signaling and
communication in plants. Springer, Berlin, pp 187–220
Escalente-Pérez M, Jaborsky M, Lautner S, Fromm J, Müller T,
Dittrich M, Kunert M, Boland W, Hedrich R, Ache P (2012)
Poplar extrafloral nectaries: two types, two strategies of indi-
rect defenses against herbivores. Plant Physiol 159:1176–1191.
https:// doi. org/ 10. 1104/ pp. 112. 196014
Fagundes R, Dáttilo W, Ribeiro SP, Rico-Gray V, Jordano P, Del-Claro
K (2017) Differences among ant species in plant protection are
related to production of extrafloral nectar and degree of leaf her-
bivory. Biol J Linn Soc 122:71–83. https:// doi. org/ 10. 1093/ bioli
nnean/ blx059
Faiola C, Taipale D (2020) Impact of insect herbivory on plant stress
volatile emissions from trees: a synthesis of quantitative meas-
urements and recommendations for future research. Atmos Envi-
ron X 5:100060. https:// doi. org/ 10. 1016/j. aeaoa. 2019. 100060
Farré-Armengol G, Filella I, Peñuelas J (2016) Bidirectional interaction
between phyllospheric microbiotas and plant volatile emissions.
Trends Plant Sci 21:854–860. https:// doi. org/ 10. 1016/j. tplan ts.
2016. 06. 005
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009)
The effects of arbuscular mycorrhizal fungi on direct and indi-
rect defense metabolites of Plantago lanceolata L. J Chem Ecol
35:833–843. https:// doi. org/ 10. 1007/ s10886- 009- 9654-0
Funk CJ (2001) Alkaline phosphatase activity in whitefly salivary
glands and saliva. Arch Insect Biochem Physiol 46:165–74.
https:// doi. org/ 10. 1002/ arch. 1026
Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings
TCJ, Erb M, Herrero S (2019) Can herbivore-induced volatiles
protect plants by increasing the herbivores susceptibility to
natural pathogens? Appl Environ Microbiol 85:e01468-e1518.
https:// doi. org/ 10. 1128/ AEM. 01468- 18
Gebreziher HG (2018) The role of herbivore-induced plant volatiles
(HIPVs) as indirect plant defense mechanism in a diverse plant
and herbivore species; a review. Int J Agric Environ Food Sci
2:139–147. https:// doi. org/ 10. 31015/ jaefs. 18024
Gish M, Mescher MC, De Moraes CM (2015) Targeted predation
of extrafloral nectaries by insects despite localized chemical
defences. Proc Royal Soc B 282:20151835. https:// doi. org/ 10.
1098/ rspb. 2015. 1835

R.H.S.Bezerra et al.
1 3
Gnanvossou D, Hanna R, Yaninek JS, Toko M (2005) Comparative life
history traits of three neotropical phytoseiid mites maintained
on plant-based diets. Biol Control 35:32–39. https:// doi. org/ 10.
1016/j. bioco ntrol. 2005. 05. 013
Godschalx AL, Schädler M, Trisel JA, Balkan MA, Ballhorn DJ (2015)
Ants are less attracted to the extrafloral nectar of plants with
symbiotic, nitrogen-fixing rhizobia. Ecology 96:348–354. https://
doi. org/ 10. 1890/ 14- 1178.1
Gols R, Wagenaar R, Poelman EH, Kruidhof HM, Van Loon JJA, Har-
vey JA (2015) Fitness consequences of indirect plant defence in
the annual weed, Sinapis arvensis. Funct Ecol 29:1019–1025.
https:// doi. org/ 10. 1111/ 1365- 2435. 12415
Gouinguené SP, Turlings TC (2002) The effects of abiotic factors
on induced volatile emissions in corn plants. Plant Physiol
129:1296–1307. https:// doi. org/ 10. 1104/ pp. 001941
Graus M, Müller M, Hansel A (2010) High resolution PTR-TOF: quan-
tification and formula confirmation of VOC in real time. J Am
Soc Mass Spectrom 21:1037–1044. https:// doi. org/ 10. 1016/j.
jasms. 2010. 02. 006
Guerrieri E, Lingua G, Digilo MC, Massa N, Berta G (2004) Do inter-
actions between plant roots and the rhizosphere affect parasitoid
behaviour? Ecol Entomol 29:753–756. https:// doi. org/ 10. 1111/j.
0307- 6946. 2004. 00644.x
Guo H, Wang CZ (2019) The ethological significance and olfac-
tory detection of herbivore-induced plant volatiles in interac-
tions of plants, herbivorous insects, and parasitoids. Arthro-
pod Plant Interact 13:161–179. https:// doi. org/ 10. 1007/
s11829- 019- 09672-5
Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001)
Molecular interactions between the specialist herbivore Manduca
sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana
attenuata. III. Fatty acid-amino acid conjugates in herbivore oral
secretions are necessary and sufficient for herbivore-specific
plant responses. Plant Physiol 125:711–717. https:// doi. org/ 10.
1104/ pp. 125.2. 711
Hambäck PA (2001) Direct and indirect effects of herbivory: feeding
by spittlebugs affects pollinator visitation rates and seedset of
Rudbeckia hirta. Écoscience 8:45–50. https:// doi. org/ 10. 1080/
11956 860. 2001. 11682 629
Harrison S, Karban H (1986) Behavioural response of spider mites
(Tetranychus urticae) to induced resistance of cotton plants. Ecol
Entomol 11:181–188. https:// doi. org/ 10. 1111/j. 1365- 2311. 1986.
tb002 93.x
Hatano E, Saveer AM, Borrero-Echeverry F, Strauch M, Zakir A,
Bengtsson M, Ignell R, Anderson P, Becher P, Witzgall P, Dek-
ker T (2015) A herbivore-induced plant volatile interferes with
host plant and mate location in moths through suppression of
olfactory signalling pathways. BMC Biol 13:75. https:// doi. org/
10. 1186/ s12915- 015- 0188-3
Heil M (2008) Indirect defence via tritrophic interactions. New Phytol
178:41–61. https:// doi. org/ 10. 1111/j. 1469- 8137. 2007. 02330.x
Heil M (2015) Extrafloral nectar at the plant-insect interface: a spot-
light on chemical ecology, phenotypic plasticity, and food webs.
Annu Rev Entomol 60:213–232. https:// doi. org/ 10. 1146/ annur
ev- ento- 010814- 020753
Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerg-
ing experimental support for a slippery concept. Trends Plant Sci
7:61–67. https:// doi. org/ 10. 1016/ S1360- 1385(01) 02186-0
Heil M, Silva-Bueno JC (2007) Within-plant signaling by volatiles
leads to induction and priming of an indirect plant defense in
nature. PNAS 104:5467–5472. https:// doi. org/ 10. 1073/ pnas.
06102 66104
Heil M, Fiala B, Baumann B, Linsemair KE (2000) Temporal, spatial
and biotic variations in extrafloral nectar secretion by Macaranga
tanarius. Funct Ecol 14:749–757. https:// doi. org/ 10. 1046/j. 1365-
2435. 2000. 00480.x
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair K (2001)
Extrafloral nectar production of the ant-associated plant, Maca-
ranga tanarius, is an induced, indirect, defensive response elic-
ited by jasmonic acid. PNAS 98:1083–1088. https:// doi. org/ 10.
1073/ pnas. 98.3. 1083
Heil M, Hilpert A, Krüger R, Linsenmair KE (2004) Competition
among visitors to extrafloral nectaries as a source of ecological
costs of an indirect defence. J Trop Ecol 20:201–208. https:// doi.
org/ 10. 1017/ S0266 46740 30011 0X
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or
defend. Q Rev Biol 67:283–335. https:// doi. org/ 10. 1086/ 417659
Hernandez-Cumplido J, Forter B, Moreira X, Heil M, Benrey B (2016)
Induced floral and extrafloral nectar production affect ant-pol-
linator interactions and plant fitness. Biotropica 48:342–348.
https:// doi. org/ 10. 1111/ btp. 12283
Hiltpold I, Erb M, Robert CAM, Turlings TCJ (2011) Systemic root
signalling in a belowground, volatile-mediated tritrophic interac-
tion. Plant Cell Environ 34:1267–1275. https:// doi. org/ 10. 1111/j.
1365- 3040. 2011. 02327.x
Hladun KR, Adler LS (2009) Influence of leaf herbivory, root her-
bivory, and pollination on plant performance in Cucurbita mos-
chata. Ecol Entomol 34:144–152. https:// doi. org/ 10. 1111/j. 1365-
2311. 2008. 01060.x
Hodge S, Bennett M, Mansfield JW, Powell G (2019) Aphid-induc-
tion of defence-related metabolites in Arabidopsis thaliana is
dependent upon density, aphid species and duration of infesta-
tion. Arthropod Plant Interact 13:387–399. https:// doi. org/ 10.
1007/ s11829- 018- 9667-0
Hoffmeister M, Wittköpper N, Junker RR (2016) Herbivore-induced
changes in flower scent and morphology affect the structure
of flower-visitor networks but not plant reproduction. Oikos
125:1241–1249. https:// doi. org/ 10. 1111/ oik. 02988
Horiuchi J, Ozawa R, Arimura G, Nishioka T (2003) A comparison of
the responses of Tetranychus urticae (Acari: Tetranychidae) and
Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted
from lima bean leaves with different levels of damage made by
T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl
Entomol Zool 38:109–116. https:// doi. org/ 10. 1303/ aez. 2003. 109
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu
Rev Plant Biol 59:41–66. https:// doi. org/ 10. 1146/ annur ev. arpla
nt. 59. 032607. 092825
Hu W, Qin W, Jin Y, Wang P, Yan Q, Li F, Yang Z (2020) Genetic and
evolution analysis of extrafloral nectary in cotton. Plant Biotech-
nol J 8:2081–2095. https:// doi. org/ 10. 1111/ pbi. 13366
Huang W, Siemann E, Carrillo J, Ding J (2015) Below-ground her-
bivory limits induction of extrafloral nectar by above-ground
herbivores. Ann Bot 115:841–846. https:// doi. org/ 10. 1093/ aob/
mcv011
Irwin RE, Adler LS (2006) Correlations among traits associated with
herbivore resistance and pollination: implications for pollina-
tion and nectar robbing in a distylous plant. Am J Bot 93:64–72.
https:// doi. org/ 10. 3732/ ajb. 93.1. 64
Jaborsky M, Maierhofer T, Olbrich A, Escalente-Pérez M, Müller HM,
Simon J, Krol E, Cuin TA, Fromm J, Ache P, Geiger D, Hedrich
R (2016) SLAH3-type anion channel expressed in poplar secre-
tory epithelia operates in calcium kinase CPK-autonomous man-
ner. New Phytol 210:922–933. https:// doi. org/ 10. 1111/ nph. 13841
Jamont M, Dubois-Pot C, Jaloux B (2014) Nectar provisioning close
to host patches increases parasitoid recruitment, retention and
host parasitism. Basic Appl Ecol 15:151–160. https:// doi. org/
10. 1016/j. baae. 2014. 01. 001
Jiang X, Deng Hui-Ni QuJ, Zeng H, Guo-Xing C (2019) The function
of extrafloral nectaries in the pollination and reproduction of

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
Sambucus javanica. Plant Species Biol 34:53–60. https:// doi. org/
10. 1111/ 1442- 1984. 12234
Jones IM, Koptur S (2015) Dynamic extrafloral nectar production: the
timing of leaf damage affects the defensive response in Senna
mexicana var. chapmanii (Fabaceae). Am J Bot 102:58–66.
https:// doi. org/ 10. 3732/ ajb. 14003 81
Jung SC, Martinez-Medina A, López-Ráez JA, Pozo MJ (2012) Myc-
orrhiza-induced resistance and priming of plant defenses. J Chem
Ecol 38:651–664. https:// doi. org/ 10. 1007/ s10886- 012- 0134-6
Kalberer NM, Turlings TCJ, Rahier M (2001) Attraction of a leaf beetle
(Oreina cacaliae) to damaged host plants. J Chem Ecol 27:647–
661. https:// doi. org/ 10. 1023/A: 10103 89500 009
Kaling M, Schimidt A, Moritz F, Rosenkranz M, Witting M, Kasper
K, Janz D, Schmitt-Kopplin P, Schnitzler J, Polle A (2018)
Mycorrhiza-triggered transcriptomic and metabolomic networks
impinge on herbivore fitness. Plant Physiol 177:2639–2656.
https:// doi. org/ 10. 1104/ pp. 17. 01810
Kappers IF, Hoogerbrugge H, Bouwmeester HJ, Dicke M (2011) Vari-
ation in herbivory-induced volatiles among cucumber (Cucumis
sativus L.) varieties has consequences for the attraction of car-
nivorous natural enemies. J Chem Ecol 37:150–160. https:// doi.
org/ 10. 1007/ s10886- 011- 9906-7
Karban R, Shiojiri K, Huntzinger M, Mccall AC (2006) Damage-
induced resistance in sagebrush: volatiles are key to intra- and
interplant communication. Ecology 87:922–930. https:// doi. org/
10. 1890/ 0012- 9658(2006) 87[922: DRISVA] 2.0. CO;2
Kautz S, Williams T, Ballhorn DJ (2017) Ecological importance of
cyanogenesis and extrafloral nectar in invasive english laurel,
Prunus laurocerasus. Northwest Sci 91:214–221. https:// doi. org/
10. 3955/ 046. 091. 0210
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced
plant volatile emissions in nature. Science 291:2141–2144.
https:// doi. org/ 10. 1126/ scien ce. 291. 5511. 2141
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the
emerging molecular analysis. Annu Rev Plant Biol 53:299–328.
https:// doi. org/ 10. 1146/ annur ev. arpla nt. 53. 100301. 135207
Kessler A, Baldwin IT (2007) Making sense of nectar scents: the
effects of nectar secondary metabolites on floral visitors of Nico-
tiana attenuata. Plant J 49:840–854. https:// doi. org/ 10. 1111/j.
1365- 313X. 2006. 02995.x
Kessler A, Halitschke R (2009) Testing the potential for conflicting
selection on floral chemical traits by pollinators and herbivores:
predictions and case study. Funct Ecol 23:901–912. https:// doi.
org/ 10. 1111/j. 1365- 2435. 2009. 01639.x
Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant
defense responses in nature by airborne signaling between Arte-
misia tridentate and Nicotiana attenuata. Oecologia 148:280–
292. https:// doi. org/ 10. 1007/ s00442- 006- 0365-8
Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a
means of escaping herbivores. Curr Biol 20:237–242. https://
doi. org/ 10. 1016/j. cub. 2009. 11. 071
Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollina-
tor limitation: negative impacts of induced volatiles on plant–pol-
linator interactions. Ecology 92:1769–1780. https:// doi. org/ 10.
1890/ 10- 1945.1
Kessler D, Kallenbach M, Diezel C, Rothe E, Murdock M, Baldwin
IT (2015) How scent and nectar influence floral antagonists and
mutualists. e-Life 4:e07641. https:// doi. org/ 10. 7554/ eLif e. 07641.
001
Koptur S, Palacio-Rios M, Díaz-Castelazo C, Mackay WP, Rico-Gray
V (2013) Nectar secretion on fern fronds associated with lower
levels of herbivore damage: field experiments with a widespread
epiphyte of Mexican cloud forest remnants. Ann Bot 111:1277–
1283. https:// doi. org/ 10. 1093/ aob/ mct063
Koptur S, Jones IM, Peña JE (2015) The influence of host plant extra-
floral nectaries on multitrophic interactions: an experimental
investigation. PLoS ONE 10:e0202836. https:// doi. or g/ 10. 1371/
journ al. pone. 01381 57
Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi
on insect herbivores: a meta-analysis. Ecology 90:2088–2097.
https:// doi. org/ 10. 1890/ 08- 1555.1
Kost C, Heil M (2005) Increased availability of extrafloral nectar
reduces herbivory in lima bean plants (Phaseolus lunatus,
Fabaceae). Basic Appl Ecol 6:237–248. https:// doi. org/ 10. 1016/j.
baae. 2004. 11. 002
Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an
indirect defence in neighbouring plants. J Ecol 94:619–628.
https:// doi. org/ 10. 1111/j. 1365- 2745. 2006. 01120.x
Kost C, Heil M (2008) The defensive role of volatile emission and
extrafloral nectar secretion for lima bean in nature. J Chem
Ecol 34:1–13. https:// doi. org/ 10. 1007/ s10886- 007- 9404-0
Krakos KN, Booth GM, Gardner JS, Neipp MG (2011) Nectar for
plant defense: the feeding of the non-native coccinellid beetle,
Curinus coeruleus, on extra-floral nectaries of Hawaiian native
Hibiscus brackenridgei. Int J Insect Sci 3:11–21. https:// doi.
org/ 10. 4137/ IJIS. S7162
Krips OE, Willems PEL, Gols R, Posthumus MA, Gort G, Dicke M
(2001) Comparison of cultivars of ornamental crop Gerbera
jamesonii on production of spider mite-induced volatiles, and
their attractiveness to the predator, Phytoseiulus persimilis.
J Chem Ecol 27:1355–1372. https:// doi. org/ 10. 1023/A: 10103
13209 119
Krupnick GA, Weis AE (1998) Floral herbivore effect on the sex
expression of an andromonoecious plant, Isomeris arborea
(Capparaceae). Plant Ecol 134:151–162. https:// doi. org/ 10.
1023/A: 10097 62415 520
Kwok KE, Laird RA (2012) Plant age and the inducibility of extraflo-
ral nectaries in Vicia faba. Plant Ecol 213:1823–1832. https://
doi. org/ 10. 1007/ s11258- 012- 0138-x
Laird RA, Addicott JF (2007) Arbuscular mycorrhizal fungi reduce
the construction of extrafloral nectaries in Vicia faba. Oecolo-
gia 152:541–551. https:// doi. org/ 10. 1007/ s00442- 007- 0676-4
Lange D, Calixto ES, Del-Claro K (2017) Variation in extrafloral
nectary productivity influences the ant foraging. PLoS ONE.
https:// doi. org/ 10. 1371/ journ al. pone. 01694 92
Lange ES, Farnier K, Degen T, Gaudillat B, Aguilar-Romero R,
Bahena-Juárez F, Oyama K, Turlings TCJ (2018) Parasitic
wasps can reduce mortality of teosinte plants infested with
fall armyworm: support for a defensive function of herbivore-
induced plant volatiles. Front Ecol Evol 6:1–13. https:// doi.
org/ 10. 3389/ fevo. 2018. 00055
Leal IR, Fischer E, Kost C, Tabareli M, Wirth R (2006) Ant protec-
tion against herbivores and nectar thieves in Passiflora coc-
cinea flowers. Écosience 13:431–438. https:// doi. org/ 10. 2980/
1195- 6860(2006) 13[431: APAHAN] 2.0. CO;2
Lehtilä K, Strauss S (1999) Effects of foliar herbivory on male and
female reproductive traits of wild radish, Raphanus raphan-
istrum. Ecology 80:116–124. https:// doi. org/ 10. 1890/ 0012-
9658(1999) 080[0116: EOFHOM] 2.0. CO;2
Li T, Holopainen JK, Kokko H, Tervahauta AI, Blande JD (2012)
Herbivore-induced aspen volatiles temporally regulate two
different indirect defences in neighbouring plants. Funct Ecol
26:1176–1185. https:// doi. org/ 10. 1111/j. 1365- 2435. 2012.
01984.x
Li T, Grauer-Gray K, Holopainen JK, Blande JD (2020) Herbivore
gender effects on volatile induction in Aspen and on olfactory
responses in leaf beetles. Forests 11:638. https:// doi. org/ 10. 3390/
f1106 0638
Lohman D, Zangerl A, Berenbaum M (1996) Impact of floral herbivory
by parsnip webworm (Oecophoridae: Depressaria pastinacella
Duponchel) on pollination and fitness of wild parsnip (Apiaceae:

R.H.S.Bezerra et al.
1 3
Pastinaca sativa L.). Am Midl Nat 136:407–412. https:// doi. org/
10. 2307/ 24267 44
López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C,
Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles
highlight common and differential host responses to arbuscular
mycorrhizal fungi and the regulation of the oxylipin pathway. J
Exp Bot 61:2589–2601. https:// doi. org/ 10. 1093/ jxb/ erq089
Loreto F, Dicke M, Schnitzler J-P, Turlings TCJ (2014) Plant volatiles
and the environment. Plant Cell Environ 37:1905–1908. https://
doi. org/ 10. 1111/ pce. 12369
Lucas-Barbosa D, Sun P, Hakman A, Van Beek TA, Van Loon JJA,
Dicke M (2016) Visual and odour cues: plant responses to pol-
lination and herbivory affect the behaviour of flower visitors.
Funct Ecol 30:431–441. https:// doi. org/ 10. 1111/ 1365- 2435.
12509
Luna-Diez E (2016) Using green vaccination to brighten the agro-
nomic future. Outlooks Pest Manag 27:136–140. https:// doi. org/
10. 1564/ v27_ jun_ 10
Maeda T, Takabayashi J (2001) Production of herbivore-induced
plant volatiles and their attractiveness to Phytoseiulus persimi-
lis (Acari: Phytoseiidae) with changes of Tetranychus urticae
(Acari: Tetranychidae) density on a plant. Appl Entomol Zool
36:47–52. https:// doi. org/ 10. 1303/ aez. 2001. 47
Magalhães DM, Borges M, Laumann RA, Blassioli MC (2018) Influ-
ence of multiple- and single-species infestations on herbivore-
induced cotton volatiles and Anthonomus grandis behavior. J Pest
Sci 91:1019–1032. https:// doi. org/ 10. 1007/ s10340- 018- 0971-3
Malik RJ, Ali JG, Bever JD (2018) Mycorrhizal composition influences
plant anatomical defense and impacts herbivore growth and sur-
vival in a life-stage dependent manner. Pedobiologia 66:29–35.
https:// doi. org/ 10. 1016/j. pedobi. 2017. 12. 004
Marazzi B, Bronstein JL, Koptur S (2013) The diversity, ecology and
evolution of extrafloral nectaries: current perspectives and future
challenges. Ann Bot 111:1243–1250. https:// doi. org/ 10. 1093/
aob/ mct109
Mathews CR, Brown MW, Bottrell DG (2007) Leaf extrafloral nectar-
ies enhance biological control of a key economic pest, Grapholita
molesta (Lepidoptera: Tortricidae), in peach (Rosales: Rosaceae).
Environ Entomol 36:383–389. https:// doi. org/ 10. 1603/ 0046-
225x(2007) 36[383: lenebc] 2.0. co;2
Mathews CR, Bottrell DG, Brown MW (2009) Extrafloral nectaries
alter arthropod community structure and mediate peach (Prunus
persica) plant defense. Ecol Appl 19:722–730. https:// doi. org/
10. 1890/ 07- 1760.1
Mathews CR, Brown MW, Wäckers FL (2016) Comparison of peach
cultivars for provision of extrafloral nectar resources to Har-
monia axyridis (Coleoptera: Coccinellidae). Environ Entomol
45:649–657. https:// doi. org/ 10. 1093/ ee/ nvw035
Mathur V, Wagenaar R, Caissard J-C, Reddy AS, Vet LEM, Cortesero
A-M, Van Dam NM (2012) A novel indirect defence in Brassi-
caceae: structure and function of extrafloral nectaries in Brassica
juncea. Plant Cell Environ 36:528–541. https:// doi. org/ 10. 1111/j.
1365- 3040. 2012. 02593.x
Mattiacci L, Dicke M, Posthumus MA (1995) β-glucosidase: an elici-
tor of herbivore-induced plant odor that attracts host-searching
parasitic wasps. PNAS 92:2036–2040. https:// doi. org/ 10. 1073/
pnas. 92.6. 2036
McCormick AC, Reinecke A, Gershenzon J, Unsicker SB (2016)
Feeding experience affects the behavioral response of poly-
phagous gypsy moth caterpillars to herbivore-induced poplar
volatiles. J Chem Ecol 42:382–393. https:// doi. org/ 10. 1007/
s10886- 016- 0698-7
Meents AK, Mithöfer A (2020) Plant–plant communication: is there
a role for volatile damage-associated molecular patterns? Front
Plant Sci 11:583275. https:// doi. org/ 10. 3389/ fpls. 2020. 583275
Millán-Cañongo C, Orona-Tamayo D, Heil M (2014) Phloem sugar
flux and jasmonic acid-responsive cell wall invertase control
extrafloral nectar secretion in Ricinus communis. J Chem Ecol
40:760–769. https:// doi. org/ 10. 1007/ s10886- 014- 0476-3
Milonas PG, Anastasaki E, Partsinevelos G (2019) Oviposition-induced
volatiles affect electrophysiological and behavioral responses of
egg parasitoids. Insects 10:437–450. https:// doi. org/ 10. 3390/
insec ts101 20437
Mofikoya AO, Bui TNT, Kivimäenpää M, Holopainen JK, Himanen
SJ, Blande JD (2019) Foliar behaviour of biogenic semi-vol-
atiles: potential applications in sustainable pest management.
Arthropod Plant Interact 13:193–212. https:// doi. org/ 10. 1007/
s11829- 019- 09676-1
Mondor EB, Addicott JF (2003) Conspicuous extra-floral nectaries
are inducible in Vicia faba. Ecol Lett 6:495–497. https:// doi.
org/ 10. 1046/j. 1461- 0248. 2003. 00457.x
Moreira X, Nell CS, Katsanis A, Rasmann S, Mooney KA (2016)
Herbivore specificity and the chemical basis of plant–plant
communication in Baccharis salicifolia (Asteraceae). New
Phytol 220:703–713. https:// doi. org/ 10. 1111/ nph. 14164
Mumm R, Posthumus MA, Dicke M (2008) Significance of terpe-
noids in induced indirect plant defence against herbivorous
arthropods. Plant Cell Environ 31:575–585. https:// doi. org/ 10.
1111/j. 1365- 3040. 2008. 01783.x
Muola A, Weber D, Malm LE, Egan PA, Glinwood R, Parachnow-
itsch AL, Stenberg JA (2017) Direct and pollinator-medi-
ated effects of herbivory on strawberry and the potential for
improved resistance. Front Plant Sci 8:823. https:// doi. org/ 10.
3389/ fpls. 2017. 00823
Mutyambai DM, Bruce TJA, Van den Berg J, Midega CAO, Pickett
JÁ, Khan ZR (2016) An indirect defence trait mediated through
egg-induced maize volatiles from neighbouring plants. PLoS
ONE 11:e0158744. https:// doi. org/ 10. 1371/ journ al. pone. 01587
44
Nam K-J (2018) Effects of insect herbivory on extrafloral nectar pro-
duction of Impatiens balsamina. J Wetl Res 20:131–135. https://
doi. org/ 10. 17663/ JWR. 2018. 20.2. 131
Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant
bodyguards also deter pollinators. Oikos 113:506–514. https://
doi. org/ 10. 1111/j. 2006. 0030- 1299. 14143.x
Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicol-
son SW, Nepi M, Pacini E (eds) Nectaries and nectar, 1st edn.
Springer, Dordrecht, pp 215–263
Ninkovic V, Markovic D, Rensing M (2020) Plant volatiles as cues and
signals in plant communication. Plant Cell Environ. https:// doi.
org/ 10. 1111/ pce. 13910
Ohm JR, Miller TEX (2014) Balancing anti-herbivore benefits and anti-
pollinator costs of defensive mutualists. Ecology 95:2924–2935.
https:// doi. org/ 10. 1890/ 13- 2309.1
Oliveira MS, Pareja M (2014) Attraction of a ladybird to sweet pepper
damaged by two aphid species simultaneously or sequentially.
Arthropod Plant Interact 8:547–555. https:// doi. org/ 10. 1007/
s11829- 014- 9336-x
Orona-Tamayo D, Wielsch N, Escalente-Pérez M, Svatos A, Molina-
Torres J, Muck A, Ramirez-Chávez E, Ádame-Alvarez R-M, Heil
M (2013) Short-term proteomic dynamics reveal metabolic fac-
tory for active extrafloral nectar secretion by Acacia cornigera
ant-plants. Plant J 73:546–554. https:// doi. org/ 10. 1111/ tpj. 12052
Pallini A, Janssen A, Sabelis MW (1997) Odour-mediated responses
of phytophagous mites to conspecific and heterospecific com-
petitors. Oecologia 110:179–185. https:// doi. org/ 10. 1007/ s0044
20050 147
Pangesti N, Weldegergis BT, Langendorf B, Van Loon JJA, Dicke M,
Pineda A (2015) Rhizobacterial colonization of roots modulates
plant volatile emission and enhances the attraction of a parasitoid

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
wasp to host-infested plants. Oecologia 178:1169–1180. https://
doi. org/ 10. 1007/ s00442- 015- 3277-7
Pappas ML, Liapoura M, Papantoniou D, Avramidou M, Kavroulakis
N, Weinhold A, Broufas GD, Papadopoulou KK (2018) The ben-
eficial endophytic fungus Fusarium solani strain K alters tomato
responses against spider mites to the benefit of the plant. Front
Plant Sci 9:1603. https:// doi. org/ 10. 3389/ fpls. 2018. 01603
Paré PW, Tumlinson JH (1997) Induced synthesis of plant volatiles.
Nature 385:30–31. https:// doi. org/ 10. 1038/ 38503 0a0
Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against
insect herbivores. Plant Physiol 121:325–331. https:// doi. org/ 10.
1104/ pp. 121.2. 325
Pekas A, Wäckers FL (2020) Bottom-up effects on tri-trophic interac-
tions: plant fertilization enhances the fitness of a primary para-
sitoid mediated by its herbivore host. J Econ Entomol 113:2619–
2626. https:// doi. org/ 10. 1093/ jee/ toaa2 04
Peñaflor MFGV, Gonçalves FG, Colepicolo C, Sanches PA, Bento JMS
(2017) Effects of single and multiple herbivory by host and non-
host caterpillars on the attractiveness of herbivore-induced vola-
tiles of sugarcane to the generalist parasitoid Cotesia flavipes.
Entomol Exp Appl 165:83–93. https:// doi. org/ 10. 1111/ eea. 12623
Peñaflor MFGV, Andrade FM, Sales L, Silveira EC, Santa-Cecília
LVC (2019) Interactions between white mealybugs and red spi-
der mites sequentially colonizing coffee plants. J Appl Entomol
143:957–963. https:// doi. org/ 10. 1111/ jen. 12683
Pereira CC, Boaventura MG, Castro GS, Cornelissen T (2020) Are
extrafloral nectaries efficient against herbivores? Herbivory
and plant defenses in contrasting tropical species. J Plant Ecol
13:423–430. https:// doi. org/ 10. 1093/ jpe/ rtaa0 29
Pichersky E, Gershenzon J (2002) The formation and function of plant
volatiles: perfumes for pollinator attraction and defense. Curr
Opin Plant Biol 5:237–243. https:// doi. org/ 10. 1016/ S1369-
5266(02) 00251-0
Pickett JA, Khan ZR (2016) Plant volatile-mediated signalling and its
application in agriculture: successes and challenges. New Phytol
212:856–870. https:// doi. org/ 10. 1111/ nph. 14274
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees
SCM, Bakker PAHM (2014) Induced systemic resistance by ben-
eficial microbes. Annu Rev Phytopathol 52:347–375. https:// doi.
org/ 10. 1146/ annur ev- phyto- 082712- 102340
Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes
in a changing environment: are they always helping plants to deal
with insects? Funct Ecol 27:574–586. https:// doi. org/ 10. 1111/
1365- 2435. 12050
Pinto DM, Blande JD, Nykänen R, Dong W-X, Nerg A-M, Holopainen
JK (2007) Ozone degrades common herbivore-induced plant
volatiles: does this affect herbivore prey location by predators
and parasitoids? J Chem Ecol 33:683–694. https:// doi. org/ 10.
1007/ s10886- 007- 9255-8
Pinto-Zevallos DM, Martins CBC, Pellegrino AC, Zarbin PHG (2013)
Compostos orgânicos voláteis na defesa induzida das plantas
contra insetos herbívoros. Quím Nova 36:1395–1405. https://
doi. org/ 10. 1590/ S0100- 40422 01300 09000 21
Pinto-Zevallos DM, Bezerra RHS, Souza SR, Ambrogi BG (2018)
Species- and density-dependent induction of volatile organic
compounds by three mite species in cassava and their role in
the attraction of a natural enemy. Exp Appl Acarol 74:261–274.
https:// doi. org/ 10. 1007/ s10493- 018- 0231-5
Poelman EH, Kessler A (2016) Keystone herbivores and the evolution
of plant defenses. Trends Plant Sci 21:477–485. https:// doi. org/
10. 1016/j. tplan ts. 2016. 01. 007
Poveda K, Steffan-Dewentwer I, Scheu S, Tscharntke T (2003) Effects
of below- and above-ground herbivores on plant growth, flower
visitation and seed set. Oecologia 135:601–605. https:// doi. org/
10. 1007/ s00442- 003- 1228-1
Poveda K, Steffan-Dewentwer I, Scheu S, Tscharntke T (2005) Floral
trait expression and plant fitness in response to below- and above-
ground plant–animal interactions. Perspect Plant Ecol Evol Syst
7:73–83. https:// doi. org/ 10. 1016/j. ppees. 2005. 02. 002
Price PW, Bouton CE, Gross P, Mcpheron BA, Thompson JN, Weis
AE (1980) Interactions among three trophic levels: Influence
of plants on interactions between insect herbivores and natural
enemies. Annu Rev Ecol Syst 11:41–65. https:// doi. org/ 10. 1146/
annur ev. es. 11. 110180. 000353
Radhika V, Kost C, Bartram S, Heil M, Boland W (2008) Testing the
optimal defence hypothesis for two indirect defences: extraflo-
ral nectar and volatile organic compounds. Planta 228:449–457.
https:// doi. org/ 10. 1007/ s00425- 008- 0749-6
Radhika V, Kost C, Mithöfer A, Boland W (2010) Regulation of
extrafloral nectar secretion by jasmonates in lima bean is light
dependent. PNAS 107:17228–17233. https:// doi. org/ 10. 1073/
pnas. 10090 07107
Raine NE, Willmer P, Stone GN (2002) Spatial structuring and floral
avoidance behavior prevent ant–pollinator conflict in a mexican
ant-acacia. Ecology 83:3086–3096. https:// doi. org/ 10. 1890/
0012- 9658(2002) 083[3086: SSAFAB] 2.0. CO;2
Rasmann S, Turlings TCJ (2007) Simultaneous feeding by above-
ground and belowground herbivores attenuates plant-medi-
ated attraction of their respective natural enemies. Ecol
Lett 10:926–936. https:// doi. org/ 10. 1111/j. 1461- 0248. 2007.
01084.x
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuh-
lmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of
entomopathogenic nematodes by insect-damaged maize roots.
Nature 434:732–737. https:// doi. org/ 10. 1038/ natur e03451
Rasmann S, Bennett A, Biere A, Karley A, Guerrieri E (2017) Root
symbionts: powerful drivers of plant above and belowground
indirect defenses. Insect Sci 24:947–960. https:// doi. org/ 10. 1111/
1744- 7917. 12464
Reinhard J, Srinivasan M, Zhang S (2004) Olfaction: scent-triggered
navigation in honeybees. Nature 427:411–411. https:// doi. org/
10. 1038/ 42741 1a
Reisenman CE, Riffel JA, Duffy K, Pesque A, Mikles D, Goodwin B
(2013) Species-specific effects of herbivory on the oviposition
behavior of the moth Manduca sexta. J Chem Ecol 39:76–89.
https:// doi. org/ 10. 1007/ s10886- 012- 0228-1
Rhoades DF, Cates RG (1976) Toward a general theory of plant anti-
herbivore chemistry. In: Wallace JW, Mansell RL (eds) Biochem-
ical interaction between plants and insects, 1st edn. Springer,
Boston, pp 168–213
Robert CAM, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings
TCJ (2012) Herbivore-induced plant volatiles mediate host selec-
tion by a root herbivore. New Phytol 194:1061–1069. https:// doi.
org/ 10. 1111/j. 1469- 8137. 2012. 04127.x
Rodriguez-Saona C (2012) La ecología química de interacciones tri-
tróficas. In: Rojas JC, Malo EA (eds) Temas selectos en ecología
química de insectos, 1st edn. El Colegio de la Frontera Sur, Méx-
ico, pp 315–342
Rodriguez-Saona C, Vorsa N, Singh A, Johnson-Cicalese J, Szendrei
Z, Mescher M, Frost CJ (2011) Tracing the history of plant traits
under domestication in cranberries: potential consequences on
anti-herbivore defences. J Exp Bot 62:2633–2644. https:// doi.
org/ 10. 1093/ jxb/ erq466
Rostás M, Eggert K (2007) Ontogenetic and spatio-temporal patterns of
induced volatiles in Glycine max in light of the optimal defence
hypothesis. Chemoecology 18:29–38. https:// doi. org/ 10. 1007/
s00049- 007- 0390-z
Roy R, Schmitt AJ, Thomas JB, Carter CJ (2017) Review: nectar biol-
ogy: from molecules to ecosystems. Plant Sci 262:148–164.
https:// doi. org/ 10. 1016/j. plant sci. 2017. 04. 012

R.H.S.Bezerra et al.
1 3
Rudgers JA (2004) Enemies of herbivores can shape plant traits: selec-
tion in a facultative ant–plant mutualism. Ecology 85:192–205.
https:// doi. org/ 10. 1890/ 02- 0625
Ruhren S, Handel SN (1999) Jumping spiders (Salticidae) enhance the
seed production of a plant with extrafloral nectaries. Oecologia
119:227–230. https:// doi. org/ 10. 1007/ s0044 20050 780
Rusman Q, Lucas-Barbosa D, Poelman EH (2018) Dealing with mutu-
alists and antagonists: specificity of plant-mediated interactions
between herbivores and flower visitors, and consequences for
plant fitness. Funct Ecol 32:1022–1035. https:// doi. org/ 10. 1111/
1365- 2435. 13035
Rusman Q, Poelman EH, Nowrin F, Polder G, Lucas-Barbosa D
(2019) Floral plasticity: Herbivore-species-specific-induced
changes in flower traits with contrasting effects on pollinator
visitation. Plant Cell Environ 42:1882–1896. https:// doi. org/
10. 1111/ pce. 13520
Sabelis MW, Van de Baan HE (1983) Location of distant spider mite
colonies by phytoseiid predators: demonstration of specific kai-
romones emitted by Tetranychus urticae and Panonychus ulmi.
Entomol Exp Appl. https:// doi. org/ 10. 1111/j. 1570- 7458. 1983.
tb032 73.x
Santos ATF, Leal LC (2019) My plant, my rules: bodyguard ants of
plants with extrafloral nectaries affect patterns of pollinator
visits but not pollination success. Biol J Linn Soc 126:158–
167. https:// doi. org/ 10. 1093/ bioli nnean/ bly165
Schausberger P, Peneder S, Jürschik S, Hoffmann D (2012) Mycor-
rhiza changes plant volatiles to attract spider mite enemies.
Funct Ecol 26:421–449. https:// doi. org/ 10. 1111/j. 1365- 2435.
2011. 01947.x
Schiestl FP, Kirk H, Bigler L, Cozzolino S, Desurmont GA (2014)
Herbivory and floral signaling: phenotypic plasticity and trade-
offs between reproduction and indirect defense. New Phytol
203:257–266. https:// doi. org/ 10. 1111/ nph. 12783
Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey
PM, Alborn HT, Teal PEA (2006) Fragments of ATP synthase
mediate plant perception of insect attack. PNAS 103:8894–8899.
https:// doi. org/ 10. 1073/ pnas. 06023 28103
Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PEA (2007)
Cowpea (Vigna unguiculata) chloroplastic ATP synthase is
the source of multiple plant defense elicitors during insect her-
bivory. Plant Physiol 144:793–805. https:// doi. org/ 10. 1104/ pp.
107. 097154
Shiojiri K, Ozawa R, Kugimiya S, Uefune M, Van Wijk M, Sabelis
MW, Takabayashi J (2010) Herbivore-specific, density-depend-
ent induction of plant volatiles: honest or “cry wolf” signals?
PLoS ONE 5:e12161. https:// doi. org/ 10. 1371/ journ al. pone.
00121 61
Shivaramu S, Jayanthi PDK, Kempraj V, Anjinappa R, Nandagopal
B, Chakravarty AK (2017) What signals do herbivore-induced
plant volatiles provide conspecific herbivores? Arthropod Plant
Interact 11:815–823. https:// doi. org/ 10. 1007/ s11829- 017- 9536-2
Silva SEB, França JF, Pareja M (2016) Olfactory response of four
aphidophagous insects to aphid- and caterpillar-induced plant
volatiles. Arthropod Plant Interact 10:331–340. https:// doi. org/
10. 1007/ s11829- 016- 9436-x
Silva DB, Weldegergis BT, Van Loon JJA, Bueno VWP (2017) Qualita-
tive and quantitative differences in herbivore-induced plant vola-
tile blends from tomato plants infested by either Tuta absoluta or
Bemisia tabaci. J Chem Ecol 43:53–65. https:// doi. org/ 10. 1007/
s10886- 016- 0807-7
Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in
stressful environments: interpreting new and established knowl-
edge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20.
https:// doi. org/ 10. 1007/ s11104- 009- 9981-5
Sousa-Lopes B, Calixto ES, Torezan-Silingardi HM, Del-Claro K
(2020) Effects of ants on pollinator performance in a distylous
pericarpial nectary-bearing. Sociobiology 67:173–185. https://
doi. org/ 10. 13102/ socio biolo gy. v67i2. 4846
Souza ALV, Silva DB, Silva GG, Bento JMS, Peñaflor MFGV, Souza
B (2019) Behavioral response of the generalist predator Orius
insidiosus to single and multiple herbivory by two cell content-
feeding herbivores on rose plants. Arthropod Plant Interact
14:227–236. https:// doi. org/ 10. 1007/ s11829- 019- 09729-5
Stam JM, Kroes A, Li Y, Gols R, van Loon JJA, Poelman EH, Dicke M
(2014) Plant interactions with multiple insect herbivores: from
community to genes. Annu Rev Plant Biol 65:689–713. https://
doi. org/ 10. 1146/ annur ev- arpla nt- 050213- 035937
Steets JA, Ashman T (2004) Herbivory alters the expression of a
mixed-mating system. Am J Bot 91:1046–1091. https:// doi. org/
10. 3732/ ajb. 91.7. 1046
Stefani V, Alves VN, Lange D (2019) Induced indirect defence in a
spider–plant system mediated by pericarpial nectarines. Aus-
tral Ecol 44:1005–1012. https:// doi. org/ 10. 1111/ aec. 12766
Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and eco-
logical costs of resistance to herbivory. Trends Ecol Evol
17:278–285. https:// doi. org/ 10. 1016/ S0169- 5347(02) 02483-7
Sun X, Wang G, Gao Y, Zhang X, Xin Z, Chen Z (2014) Volatiles
emitted from tea plants infested by Ectropis obliqua larvae are
attractive to conspecific moths. J Chem Ecol 40:1080–1089.
https:// doi. org/ 10. 1007/ s10886- 014- 0502-5
Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through
herbivore-induced carnivore attractants. Trends Plant Sci
1:109–113. https:// doi. org/ 10. 1016/ S1360- 1385(96) 90004-7
Takabayashi J, Shiojiri K (2019) Multifunctionality of herbivory-
induced plant volatiles in chemical communication in tritrophic
interactions. Curr Opin Insect Sci 32:110–117. https:// doi. org/
10. 1016/j. cois. 2019. 01. 003
Takabayashi J, Dicke M, Posthumus MA (1991) Variation in compo-
sition of predator attracting allelochemicals emitted by herbi-
vore-infested plants: relative influence of plant and herbivore.
Chemoecology 2:1–6. https:// doi. org/ 10. 1007/ BF012 40659
Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-
induced terpenoids in plant-mite interactions: variation caused
by biotic and abiotic factors. J Chem Ecol 20:1329–1354.
https:// doi. org/ 10. 1007/ BF020 59811
Tamiru A, Bruce TJA, Midega CAO, Woodcock CM, Birkett MA,
Pickett JA, Khan ZR (2012) Oviposition induced volatile
emissions from African smallholder farmers’ maize vari-
eties. J Chem Ecol 38:231–234. https:// doi. org/ 10. 1007/
s10886- 012- 0082-1
Tao L, Hunter MD, de Roode JC (2017) Microbial root mutualists
affect the predators and pathogens of herbivores above ground:
Mechanisms, magnitudes, and missing links. Front Ecol Evol
5:160. https:// doi. org/ 10. 3389/ fevo. 2017. 00160
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jas-
monate and salicylate signal crosstalk. Trends Plant Sci 17:60–
270. https:// doi. org/ 10. 1016/j. tplan ts. 2012. 02. 010
Timilsena BP, Seidl-Adams I, Tumlinson JH (2020) Herbivore-spe-
cific plant volatiles prime neighboring plants for nonspecific
defense responses. Plant Cell Environ 43:787–800. https:// doi.
org/ 10. 1111/ pce. 13688
Tonelli M, Peñaflor MFGB, Leite LG, Silva WD, Martins F, Bento
JMS (2016) Attraction of entomopathogenic nematodes to
sugarcane root volatiles under herbivory by a sap-sucking
insect. Chemoecology 26:59–66. https:// doi. org/ 10. 1007/
s00049- 016- 0207-z
Truong DH, Delory M, Vanderplanck M, Brostaux Y, Vandereycken A,
Heuskin S, Delaplace P, Francis F, Lognay G (2014) Tempera-
ture regimes and aphid density interactions differentially influ-
ence VOC emissions in Arabidopsis. Arthropod Plant Interact
8:317–327. https:// doi. org/ 10. 1007/ s11829- 014- 9311-6

Indirect plant defenses: volatile organic compounds andextrafloral nectar
1 3
Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbi-
vore-induced plant volatiles: mechanisms, ecological relevance,
and application potential. Annu Rev Entomol 63:433–452.
https:// doi. org/ 10. 1146/ annur ev- ento- 020117- 043507
Turlings TCJ, Wäckers FL (2004) Recruitment of predators and para-
sitoids by herbivore-injured plants. In: Cardé RT, Millar JG (eds)
Advances in insect chemical ecology, 1st edn. Cambridge Uni-
versity Press, Cambridge, pp 21–75
Turlings TCJ, Lengwiller UB, Bernasconi ML, Wechsler D (1998)
Timing of induced volatile emissions in maize seedlings. Planta
207:146–152. https:// doi. org/ 10. 1007/ s0042 50050 466
Turlings TCJ, Alborn HT, Loughrin JH, Tumlinson JH (2000) Volici-
tin, an elicitor of maize volatiles in oral secretion of Spodop-
tera exigua: isolation and bioactivity. J Chem Ecol 26:189–202.
https:// doi. org/ 10. 1023/A: 10054 49730 052
Vannette RL, Hunter MD (2013) Mycorrhizal abundance affects the
expression of plant resistance traits and herbivore performance.
J Ecol 101:1019–1029. https:// doi. org/ 10. 1111/ 1365- 2745. 12111
Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2013)
Aphid responses to volatile cues from turnip plants (Brassica
rapa) infested with phloem-feeding and chewing herbivores.
Arthropod Plant Interact 7:567–577. https:// doi. org/ 10. 1007/
s11829- 013- 9272-1
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural
enemies in a tritrophic context. Annu Rev Entomol 37:141–172.
https:// doi. org/ 10. 1146/ annur ev. en. 37. 010192. 001041
Veyrat N, Robert CAM, Turlings TCJ, Erb M (2015) Herbivore intoxi-
cation as a potential primary function of an inducible volatile
plant signal. J Ecol 104:591–600. https:// doi. org/ 10. 1111/ 1365-
2745. 12526
Villamil N, Boege K, Stone GN (2019) Testing the distraction hypoth-
esis: do extrafloral nectaries reduce ant-pollinator conflict? J Ecol
107:1377–1391. https:// doi. org/ 10. 1111/ 1365- 2745. 13135
Visser D, Wright MG, Giliomee JH (1996) The effect of the Argentine
ant, Linepithema humile (Mayr) (Hymenoptera, Formicidae) on
flower-visiting insects of Protea nitida Mill. (Proteaceae). Afr
Entomol 4:285–287
Wäckers FL (2001) A comparison of nectar- and honeydew sugars
with respect to their utilization by the hymenopteran parasitoid
Cotesia glomerata. J Insect Physiol l47:1077–1084. https:// doi.
org/ 10. 1016/ S0022- 1910(01) 00088-9
Wäckers FL, Bezemer TM (2003) Root herbivory induces an above-
ground indirect defence. Ecol Lett 13:9–12. https:// doi. org/ 10.
1046/j. 1461- 0248. 2003. 00396.x
War AR, Sharma HC, Paulraj MG, War MY, Ignacimuthu S (2011)
Herbivore induced plant volatiles: their role in plant defense for
pest management. Plant Signal Behav 6:1973–1978. https:// doi.
org/ 10. 4161/ psb.6. 12. 18053
Weber MG, Keeler KH (2013) The phylogenetic distribution of extra-
floral nectaries in plants. Ann Bot 111:1251–1261. https:// doi.
org/ 10. 1093/ aob/ mcs225
Whipps JM (2004) Prospects and limitations for mycorrhizas in bio-
control of root pathogens. Can J Bot 82:1198–1227. https:// doi.
org/ 10. 1139/ b04- 082
Whitney KD (2004) Experimental evidence that both parties benefit
in a facultative plant-spider mutualism. Ecology 85:1642–1650.
https:// doi. org/ 10. 1890/ 03- 0282
Williams L III, Rodríguez-Saona C, Castle del Conte SC (2017) Methyl
jasmonate induction of cotton: a field test of the ‘attract and
reward’ strategy of conservation biological control. AoB Plants.
https:// doi. org/ 10. 1093/ aobpla/ plx032
Xiu C-L, Pan H-S, Ali A, Lu Y-H (2017) Extrafloral nectar of Hibiscus
cannabinus promotes adult populations of Harmonia axyridis.
Biocontrol Sci Technol 27:1009–1013. https:// doi. org/ 10. 1080/
09583 157. 2017. 13646 97
Xiu C, Dai W, Pan H, Zhang W, Luo S, Wyckhuys KAG, Yang Y, Lu
Y (2019) Herbivore-induced plant volatiles enhance field-level
parasitism of the mirid bug Apolygus lucorum. Biol Control
135:41–47. https:// doi. org/ 10. 1016/j. bioco ntrol. 2019. 05. 004
Yoshida T, Kakuta H, Choh Y (2017) Pea aphids (Acyrthosiphon pisum
Harris) reduce secretion of extrafloral nectar in broad bean (Vicia
faba). Ecol Entomol 43:134–136. https:// doi. org/ 10. 1111/ een.
12476
Zangerl AR, Berenbaum MR (2009) Effects of florivory on floral
volatile emissions and pollination success in the wild parsnip.
Arthropod Plant Interact 3:181–191. https:// doi. org/ 10. 1007/
s11829- 009- 9071-x
Zeilinger S, Gupta VK, Dahms TES, Silva RN, Singh HB, Upadhyay
RS, Gomes EV, Tsui CKM, Nayak SC (2016) Friends or foes?
emerging insights from fungal interactions with plants. FEMS
Microbiol Rev 40:182–207. https:// doi. org/ 10. 1093/ femsre/
fuv045
Zhong F, He Y, Gao Y, Qi G, Zhao C, Lu L (2011) Olfactory responses
of Neoseiulus cucumeris (Acari: Phytoseiidae) to odors of host
plants and Frankliniella occidentalis (Thysanoptera: Thripidae)–
plant complexes. Arthropod Plant Interact 5:307–314. https:// doi.
org/ 10. 1007/ s11829- 011- 9135-6
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.