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Ecological turmoil in evolutionary dynamics of

plantinsect interactions: defense to offence
ARTICLE in PLANTA JULY 2015
Impact Factor: 3.38 DOI: 10.1007/s00425-015-2364-7 Source: PubMed

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DOI 10.1007/s00425-015-2364-7

REVIEW

Ecological turmoil in evolutionary dynamics of plantinsect

interactions: defense to offence
Manasi Mishra1,2 Purushottam R. Lomate1,3 Rakesh S. Joshi1,4
Sachin A. Punekar5,6 Vidya S. Gupta1 Ashok P. Giri1

Received: 16 May 2015 / Accepted: 1 July 2015

Springer-Verlag Berlin Heidelberg 2015

Abstract
Main conclusion Available history manifests contemporary diversity that exists in plant-insect interactions.
A radical thinking is necessary for developing strategies
that can co-opt natural insect-plant mutualism, ecology
and environmental safety for crop protection since
current agricultural practices can reduce species richness and evenness. The global environmental changes,
such as increased temperature, CO2 and ozone levels,
biological invasions, land-use change and habitat fragmentation together play a significant role in re-shaping
the plant-insect multi-trophic interactions. Diverse
natural products need to be studied and explored for
their biological functions as insect pest control agents.
In order to assure the success of an integrated pest

M. Mishra, P. R. Lomate, R. S. Joshi contributed equally.

& Ashok P. Giri
ap.giri@ncl.res.in
1

Plant Molecular Biology Unit, Division of Biochemical

Sciences, CSIR-National Chemical Laboratory, Dr. Homi
Bhabha Road, Pune 411 008, MS, India

Institute of Organic Chemistry and Biochemistry, Academy

of Sciences of the Czech Republic, Prague, Czech Republic

Department of Entomology, Iowa State University, Ames,

IA 50011, USA

Institute of Bioinformatics and Biotechnology, Savitribai

Phule Pune University, Ganeshkhind, Pune 411007, MS,
India

Biospheres, Eshwari, 52/403, Laxminagar, Parvati,

Pune 411 009, MS, India

Naoroji Godrej Centre for Plant Research, Godrej & Boyce

Mfg. Co. Ltd., Lawkim Motor Group, Gat No. 431,
Shindewadi Post, Satara 412 801, MS, India

management strategy, human activities need to be

harmonized to minimize the global climate changes.
Plantinsect interaction is one of the most primitive and coevolved associations, often influenced by surrounding
changes. In this review, we account the persistence and
evolution of plantinsect interactions, with particular focus
on the effect of climate change and human interference on
these interactions. Plants and insects have been maintaining
their existence through a mutual service-resource relationship while defending themselves. We provide a comprehensive catalog of various defense strategies employed
by the plants and/or insects. Furthermore, several important
factors such as accelerated diversification, imbalance in the
mutualism, and chemical arms race between plants and
insects as indirect consequences of human practices are
highlighted. Inappropriate implementation of several
modern agricultural practices has resulted in (i) endangered
mutualisms, (ii) pest status and resistance in insects and
(iii) ecological instability. Moreover, altered environmental
conditions eventually triggered the resetting of plantinsect
interactions. Hence, multitrophic approaches that can harmonize human activities and minimize their interference in
native plantinsect interactions are needed to maintain
natural balance between the existence of plants and insects.
Keywords Plantinsect interaction
Co-evolution

Human interference
Ecosystem
Climatic change

Introduction
Plantinsect interactions are considered to be one of the
most primitive and co-evolved systems (Ehrlich and Raven
1964; Bronstein 1994; Bronstein et al. 2006). There is

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Angiosperm

Plant Diversity

Cycads (Gymnosperm)
Conifers (Gymnosperm)
Ginkgos (Gymnosperm)
Ferns (Seedless)
Mosses (Land)
Algae (Aquac)
Cambrian

Ordovician

Silurian

Devonian

Carboniferous

Permian

Triassic

Jurassic

Paleozoic
440

Cambrian

Ordovician

Silurian

Mesozoic
Million years before present (Approx.)

400

Devonian

Cretaceous

Carboniferous

Terary

Quaternary

Cenozoic

200

Permian

Triassic

Jurassic

Cretaceous

Terary

Quaternary

Archaeognatha
Homoptera, Hemiptera
Detrivory

Simple Plant
Piercing

Hymenoptera
Thysanoptera

Early leaf eang,

Gall forming

Coleoptera

Leaf mining

Lepidoptera

Insect Diversity

Pollen, nectar
consuming

Diptera
Pollinaon

Fig. 1 Plant and insect evolution and various feeding habits developed by insects throughout the evolutionary timescale. Plant evolution and diversity is shown in the upper half, whereas insect orders
and their evolution is given in the lower half. Arrows directed towards

the lower side show insect feeding habits during respective time
periods. The information on the evolutionary time scale and insect
feeding habits was gathered from Niklas et al. (1983), Tahvanainen
and Niemela (1987), and references therein

considerable debate on the timeline and the reasons behind

the genesis or the establishment of plantinsect interactions. However, the general consensus is that the evolution
of various interactions resulted in the diversification of
plant and insect species (Kasting and Catling 2003). Several factors, including climate, geography, and species
abundance/distribution may have contributed to the timely
and the reciprocal evolution of plantinsect interactions
(Shear 1991; Scott et al. 1992; Nisbet and Sleep 2001).
Climatic changes have influenced, shifted, and fragmented the taxonomic composition as well as the geographic distributions of plants and insects and they are the
key drivers for the evolution of plantinsect interactions
(McElwain and Punyasena 2007; Wilf 2008). Figure 1
gives an account of real-time development of diverse plant
and insect forms along with the adaptive evolution of the
insect feeding habits across the evolutionary timeline.
Evolution of vascular plant reproduction aided by seed
dispersal could have been a major factor involved in the
attraction between the insect partners (Niklas et al. 1983;
Scott et al. 1985; 1992; Takhtajan 1991; Taylor and Taylor
1992). For example, flowering plants (Angiosperm)

diversified in the latter half of the Mesozoic era (around

200 million years ago) and this perhaps guided the burst of
pollinator and herbivore insect diversity (Wilf and Labandeira 1999; Currano et al. 2008) (Fig. 1). During the
PaleoceneEocene era, the accumulation of carbon in the
atmosphere due to high temperature conditions could have
elevated the C:N ratio in plants, which in turn triggered the
burst of insect herbivore diversity. These drastic changes in
the host plant diversity and availability might have directly
influenced the balance between speciation and extinction of
associated insect herbivores. More specifically, the profound
diversity of plants and phytophagous insects in the tropics
implies a strong relationship between climatic temperatures
and herbivory, which is also evident from the fossil records
(Wilf and Labandeira 1999; Nelson et al. 2013).
The fossil records provide information about the taxonomic groups of producers and consumers. From the early
Devonian to Permian era, insect herbivores probably have
evolved various feeding habits such as spore feeding,
piercing, and sucking (Labandeira 1998, 2013; Stone et al.
2009; Wappler et al. 2009) (Fig. 1). The spectacular
interplay of plantinsect co-evolution can be seen in terms

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of pollination. The development of floral tubes during the

Cretaceous period gave rise to highly specialized pollinators such as Hymenoptera, Diptera, and Lepidoptera.
Consequently, pollinators promoted the evolution of early
angiosperms for facilitating the genetic exchange between
individuals or spread of pollens to distantly placed individuals. It is thus suggested that the late evolution of
angiosperms is closely related to that of insect evolution
(Zavada 1984; Crane et al. 1995; Crepet 2008). In this
review, we discuss the history of plantinsect interactions
and its current status in the native system. Further, we have
highlighted the adverse effects of human activities on these
interactions and scope to improve and harmonize with the
ecosystem. In conclusion, we emphasize the use of
knowledge of plantinsect interactions to design sustainable strategies to protect crop plants from insect
infestations.

Myriad and diverse plantinsect interactions

Right from the beginning of evolutionary timescale, a
strong materialistic association of plants and insects is
evident due to their interdependent nature of service and
resource availability (Fig. 2). Plants receive pollination
services from insects and in turn most of these pollinators
receive food from plants in the form of pollen and/or
nectar. However, some other pollinators like bees obtain
gum, resin, and wax from plants to build their hives
(Michener 2007). Ant-mediated seed dispersal known as
myrmecochory and dissemination of the seeds of the
flowering plants by termites are apparent examples of
services provided by the insects.
Plant structures also serve as shelter for development and
reproduction of insects. However, many times cheating
behaviors are observed by interacting partners and exploiting the mutualism (Bronstein et al. 2006). For instance,
certain species of carpenter bees and bumble bees known as
nectar thieves enter the flower to obtain nectar, but do not
pollinate due to their morphological incompatibility. Similarly, plants also deceive the insects and receive pollination
services. For example, the orchid family and a few members
of the monocot family, Araceae, having an unusually high
occurrence of non-rewarding flowers exhibit food deception or sexual deception mechanisms. To deceive insect
pollinators orchids advertise floral signals like inflorescence
shape, flower color, and scent in the absence of the nectar
(Jersakova et al. 2006; Vogel and Martens 2000). Insectivorous plants like Venus-fly trap (Dionaea muscipula) or
Bladderworts (Utricularia spp.), which are deprived of
nitrogen for their metabolism, capture the insects to use them
as nitrogen source (Slack and Gate 2000).

Diversification for fitness and survival: coevolution of traits

Plants acquire a range of adaptations to improve their own
reproduction and survival and to reduce the dependency of
insects during the course of co-evolution. They exhibit
several mechanical barriers like direct defense mechanisms, which restrict insects by deterring and/or injuring
them (Fernandes 1994). Deterrents include certain compounds released on the plants surface, namely, resins,
lignins, silica, and wax. The wax secreted by several terrestrial plants change the texture of plant tissue, making it
difficult for the insects to consume (Fernandes 1994). Such
examples of mechanical and morphological defenses of
plants that restrict growth and feeding of the insects are
listed in Fig. 3.
In addition to mechanical defenses, plants use a dynamic
range of chemical defense strategies against herbivores by
constitutive and/or induced production of defensive compounds (Walling 2000; Kessler and Baldwin 2001;
Mithofer and Boland 2012). For example, the secondary
metabolites of the plants that are part of defense machinery
directly affect the insects by either repelling or deterring
them. This counter action of plants results in the reduction
of insect feeding, survival, and reproduction (Karban and
Baldwin 1997; Mithofer et al. 2009; Mithofer and Boland
2012; Ali and Agrawal 2012; Dawkar et al. 2013). Interestingly, the diversity and complexity of plant secondary
metabolites have amplified over the evolutionary timescale
resulting in increased adaptive pressure on the herbivores
(Becerra et al. 2009). Another important example of
molecular co-evolution of plants and insects is the interplay
of insect gut proteases and their proteinaceous inhibitors
expressed by plants. Proteinase inhibitors expressed in
plant tissues retard the growth and development of insects
by disturbing their digestive metabolism (Green and Ryan
1972; Tamhane et al. 2005, 2007). In terms of indirect
defense mechanisms many plant species develop extrafloral nectaries in order to attract natural enemies of herbivores such as ants (Oliveira and Freitas 2004). Plants emit
numerous volatile compounds upon the damage that act as
signals to alert neighboring tissues and plants. These
volatiles also attract predators and consequently involve in
plants indirect defenses (Baldwin et al. 2006).
On the other hand, herbivores also have various means
of manipulating their host plants such as modification of
microhabitats to counter plant defenses and gain better use
of the resources (Potting et al. 1995). Insects display
adaptations to certain plant chemicals by developing
mechanisms to metabolize, sequester, excrete, or selectively binds plant defense compounds (Fig. 3). Sequestration is an important strategy to detoxify harmful

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metabolites, which insects often use for their own benefit

against predators (Krieger et al. 1971; Nishida 2002; Opitz
and Muller 2009; Mithofer and Boland 2012). Recently,
Strauss et al. (2013) described how ABC transporters
transport the toxic metabolites from gut to defensive glands

123

of Chrysomela populi via hemolymph and use them against

predators. Similarly, a specific Cytochrome P450 oxidase
(CYP6B46) was observed to mediate the sequestration of
nicotine in M. sexta (Kumar et al. 2014). Other than
cytochrome P450 oxidases, insects use several enzymes,

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b Fig. 2 Plethora of plantinsect interactions. a Rice Swift (Borbo

cinnara), a skipper butterfly feeding on Ipomoea; b Peacock pansy

(Junonia almana) butterfly feeding on Leea indica; c Honey bee (Apis
cerana indica) feeding on Smithia setulosa; d Fly (Milichiidae)
pollination in Brachystelma malwanense; e Fly (Phoridae) with
Ceropegia pubescens pollinarium; f Banded blister beetle (Mylabris
pustulata) feeding on Alysicarpus pubescens; g Scarab Beetles
(Onthophagus sp.) pollination inAmorphophallus commutatus var.
anshiensis; h Root grub beetle (Rutelinae) feeding on stinky
appendage; i Plain tiger (Danaus chrysippus) butterfly caterpillar
feeding on leaves of Ceropegia maharashtrensis; j Red tree ants
(Oecophylla smaragdina) harvesting honey dew from mealybugs;
k Crab spider (Thomisidae), an ambush predator with fly on
Ceropegia rollae; l Gall induced by plant bug (Mangalorea hopeae)
in Hopeaponga; m Bee orchid (Cottoniapeduncularis) an excellent
mimic of bee; n Hymenopterans harvesting resin from Canarium
strictum; o Pagoda ant nest built by Crematogaster ants using plant
material

such as glutathione s-transferases and esterases for the

detoxification of plant toxic compounds (Snyder and
Glendinning 1996; Feyereisen 1999; Mithofer and Boland
2012). The insects have developed several protease isoforms with diverse specificities to combat against the plant
protease inhibitors (Broadway 1996; Jongsma et al. 1996;
Bown et al. 1997; Giri et al. 1998; Patankar et al. 2001;
Chougule et al. 2005; Lomate and Hivrale 2010, 2011;
Mahajan et al. 2013).
The adaptive responses in diverse herbivorous insects
may depend on the type of plant toxin and its mode of
action, which may result in convergence at molecular
levels. Dobler et al. (2012) demonstrated an example of
Fig. 3 Account of
morphological and molecular
adaptations of plants and insects
during evolution of mutual
interaction. Plants and insects
use various strategies to get
benefit and overcome on each
others defense. For example,
although plants can produce
various anti-feedent and toxic
compounds to avoid insect
damage, insects possess an
adapted detoxification
machinery to surmount the plant
toxins

convergent molecular evolution in cardenolide-resistant

herbivorous insects belonging to different genera and
orders. Cardenolide-resistant insect species from 15 genera
within 4 orders (Coleoptera, Lepidoptera, Diptera, and
Hemiptera) were found to have same amino acid substitution (position 122; N122H) in the extracellular loop of
(Na??K?) ATPase, the target metabolic enzyme. Such
prevalent adaptive responses to a common selective agent
shown by a diverse subset of herbivorous insects demonstrate a link between molecular, functional, and ecological
convergence in insects. Thus, there are numerous defense
strategies being used by plants and insects against each
other for their survival (Fig. 3).

Human intervention through domestication

and agriculture
Human activities such as agriculture and industrialization
have significantly influenced the ecosystem and its components. Likewise, plantinsect interactions and their
evolutionary dynamics have been also affected by these
environmental alterations. Yield-based targeted selection
and domestication of nutritionally superior crop lines have
apparently many folds accelerated the genetic evolution as
compared to their wild relatives (Gepts 2002; Harter et al.
2004; Brown et al. 2009). Monoculturing of crops has
further substituted ecological diversity, which consequently has led to insect outbreaks and introduction of

Behavioral and morphological

adaptaons

Molecular adaptaons
Molecular strategies against plant
defense compounds

Behavioral tacc against plant defense

compounds

Adapve and protecve structures

Avoidance
Ulizaon of alternave hosts
Increased consumpon rate
Change in feeding habits
Development of specialized mouth parts

Cell wall carrier

Cucle
Trichomes
Thorns
Silica deposion
Extraoral nectaries

Sequestraon of toxic compounds

Improved detoxicaon mechanisms
Detoxifying and Anoxidave enzymes
Regulaon and modicaon of digesve
enzymes

Direct and indirect defense metabolites

Secondary metabolites Proteins

Terpenoids
Lecns
Phenolics
Chinases
Flavonoids
Enzyme inhibitors
Quinones
Defensive enzymes
Alkaloids
Extraoral nectar ( to aract parasitoids)

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pests into new favorable areas causing destruction of natural biotic communities, altered behaviors, and population
distributions (Altieri et al. 1984). For example, the moths
of Bombyx mori, a fully domesticated insect, exhibit
inability to fly and survive in wild habitats due to their
migratory restriction in search of food (Mitterboeck and
Adamowicz 2013). Recent increment in bark beetle activity beyond a critical threshold and its altered interaction
with conifers has been correlated with anthropogenic
activities (Raffa et al. 2008). Elevated global temperatures
and atmospheric carbon dioxide (CO2) have directly
influenced the beetle development, survival, and in turn the
host-tree allocation pattern.
Over the last decades there has been an impressive
growth in food production due to the development of highyielding, disease-resistant varieties of crops. Despite these
remarkable developments in agricultural technology
important for successfully catering the demands of
increased food supply, they have also raised some crucial
ecological concerns. Increased nitrogen uptake by highyielding crop varieties in response to fertilizers upsets the
plants carbon/nitrogen balance. This may result in metabolic problems that may force the plants to take up extra
water, which eventually influence the herbivory patterns
(Hosokawa et al. 2007; Cherif and Loreau 2013).
Some soil organisms, insects, weeds, and parasites are
beneficial for agriculture while some pose severe threat to
crop yield (Christou and Twyman 2004). Insect pests cause
damage to crop plants in a variety of ways, such as mining
leaves, eating fruits and seeds, sucking sap, serving vector
for transfer of diseases, gall formation, and much more.
Approximately, 600 species of insects, several species of
nematodes and fungi are considered as pests in agriculture
(Klassen and Schwartz 1985). Management of pests has
become crucial for preventing the losses in crop yield and
quality.

Effects of pesticides on plantinsect ecosystems

Use of chemical insecticides/pesticides is the most popular
way to control insect pests and eventually avoid the crop
losses (Heckel 2012). However, pesticides (or xenobiotics)
usually influence entire population of organisms, thus
changing the stability of species interactions in an
ecosystem (Heckel 2012). The natural agro-ecosystem is
evolved to maintain at least a specific set of plant diversity
by negative density-dependent mechanisms mediated by
pathogens and insects. However, extensive use of fungicides and insecticides may interfere with these natural
mechanisms resulting in the loss of plant/insect diversity
and alteration in species composition (Bagchi et al. 2014).
Perhaps, excess pesticide applications indirectly result in

123

the reduction of population of pests, parasites, and predators. This may favor other species of arthropods, which can
emerge as serious pests in the fields. A large fraction of
pesticides used in the field get mixed with soil that can
directly or indirectly affect the population of decomposing
arthropods in the soil (Pimentel and Edwards 1982;
Pimentel et al. 1992; Frampton 1999). Furthermore, some
cross-pollinator insect species, such as honeybees and wild
bees, are extremely prone to insecticides (Price et al. 1986;
Theiling and Croft 1988).
Excess use of pesticides has also made plants more
reliant on artificial defense treatments which make use of
natural and synthetic stimulants (Chemical analog of Sialic
acid, like S -methyl benzo [1,2,3] thiadiazole-7-carbothioate) of plant immunity (Von Rad et al. 2005). As a result,
offensive traits of insects have turned out to be stronger by
developing rapid resistance to plant defense mechanisms
(Magdoff et al. 2000). For instance, insect enzymes typically associated with pesticide detoxification including
cytochrome P450 s, esterases, and glutathione s-transferases (GSTs) display extensive modification and diversification in their expression and activities (Dawkar et al.
2013). The increased number of insecticide-resistant
insects might be a threat to host plants or other insect
species and their predators.

Ecological impacts of recombinant DNA

technology
Expression of recombinant insecticidal proteins in transgenic crops may exert direct and/or indirect effects on the
striking complexity of biotic interactions and food web
relationships in Agro-ecosystems. Bacillus thuringiensis
(Bt) insecticidal toxins are the most commonly used proteins for generating insect-resistant transgenic plants
(Hofte and Whiteley 1989; Bravo et al. 2011). In the mid1990s, commercial introduction of genetically modified
maize, potato, and cotton plants expressing Bt toxin was
the most prominent landmark in crop improvement, which
revolutionized agriculture by increasing productivity.
However, the ecological risk assessment of insect-resistant
transgenic crops have always suggested that the accumulation of recombinant Bt toxin in the terrestrial food chain
may affect associated arthropod parasites and predator
populations (Duan et al. 2010).
For instance, the emergence of resistance against
transgenic Bt crops in insects due to the modification of
their toxin receptor site indicates a plausible ecological
threat (Gahan et al. 2010). Furthermore, physiochemical
modulation of non-specific target insects or organisms by
the transgenic insecticide presents the obverse ecological
hazard (Duan et al. 2010; Malone and Burgess 2000;

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OCallaghan et al. 2005; Schluter et al. 2010). For example, the use of protease inhibitor for developing insectresistant transgenic crops has remained as a moot point due
to their efficacy against ever adapting insects (Jongsma
et al. 1996; Giri et al. 1998). However, transgenic cotton
plants expressing a combination of protease inhibitors
showed significant protection from insect damage in the
fields (Duan et al. 2010). Appropriate use of such natural
plant defensive molecules for crop protection yet remains a
challenge to biotechnologists in near future.

On the edge of ecological emergency

Revising the strategies
The increased selection pressure and resurgence of pesticide resistance in insects is one of the key drawbacks of the
insect pest management strategies, which poses a severe
threat to the overall stability of the plantinsect ecosystems. Thus, in this scenario, it is extremely important to
understand and realize the differences between natural
plant defense mechanisms and the existing agricultural
strategies employed to control insect pests. All the natural
plant defense mechanisms are aimed at reducing the direct
or indirect impact of insect pests on their survival and
reproduction. Humanistic approaches, however, are mostly
aimed toward complete eradication or wiping out of the
insect populations.
Introduction of exotic and extraneous plants into the
native population could result in disturbed habitats, which
might exert negative impact on the distribution pattern of
specific herbivores. As a consequence, overpopulation of
these plant and/or insect species directly or indirectly could
wipe out the local indigenous plants and may subsequently
fade the dependent insect communities (Spafford and
Lortie 2013). Besides this, introduction of extraneous
plants into the ecosystem might instigate misbalancing
fluctuations in the systems, such as hypervariability in C
and N pools (Liao et al. 2007). Thus, invasive species
threaten the stability of native ecosystems and potentially
affect the ecosystem (Gordon 1998). For example,
enhanced non-native populations of the honeybee Apis
mellifera in the Bonin Islands affected the interactions of
native bees with the native plants (Traveset and Richardson
2006).
Global climate change triggers resetting of plant
insect interactions
Global climatic change directly affects insect herbivores by
influencing their physiology, behavior, phenology, life
cycle, growth, development rates, and distribution in

distinct geographic locations (Scherber et al. 2013). Temperature and water are the two most significant components
of the environment that directly influence plantinsect
interactions (Jamieson et al. 2012; Scherber et al. 2013).
Under a warm weather condition insects exhibit an accelerated metabolism, which leads to higher food consumption, growth, and development. In addition to this, reduced
reproduction time and less exposure to natural enemies
ultimately result in population outbreaks (Jamieson et al.
2012). Recent examples of population outbreaks in spruce
beetles (Dendroctonus rufipennis) and pine beetles (D.
ponderosae) have been linked to climate change (Logan
et al. 2003; Powell and Bentz 2009). More often, these
effects are indirect and act via changes in the nitrogen
content and plant secondary compounds. Indirectly, climate change can also affect predators, parasitoids, and
pathogens by influencing their performance, phenology,
behavior, and fitness.
Owing to altered climatic conditions due to human
activities, plants are facing different environmental conditions such as elevated CO2 and O3 concentrations, high
temperature, and UV radiation. Elevated CO2 and O3 levels
impact on physical leaf defense, leaf carbohydrates, and
phenolic concentrations, while elevated temperature is
responsible for reduced nitrogen (N) content and variable
concentration of terpenoids (Percy et al. 2002; Lindroth
2010). These changes collectively alter the nutritional
quality of plant, which in turn influences pest performance,
development time, survival, and life time fecundity of
associated herbivores and/or the predators at the third
trophic level. Elevated CO2 suppresses jasmonic acid (JA)
while stimulating the production of salicylic acid (SA),
which increases the susceptibility of plants towards
chewing insects. Zavala et al. (2008, 2013) have reported a
47 % reduction in constitutive PI production and downregulation of JA signaling pathway genes in soybean
growing under elevated CO2 conditions. This effect may
compromise the natural plant defense against insects. If the
CO2 levels continue to increase the impact on plant defense
machinery pest management would be heavily compromised (Tylianakis et al. 2008; van der Putten et al. 2010).
Increased UV radiations due to ozone depletion results in
the altered visual behavior of many insects. This may
interfere with their interactions with plants (Raviv and
Antignus 2004). Population-level effects of trophic mismatch caused by differential phenological shifts among the
species have been documented in detail across diverse
consumerresource pairings, including invertebrate herbivores and plants as well as insect pollinators and flowering
plants (Visser and Holleman 2001; Memmott et al. 2007;
Hegland et al. 2009; Scaven and Rafferty 2013) (Fig. 4).
Therefore, such global environmental changes will have
adverse effects at various levels of plantinsect interactions

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Fig. 4 Schematic diagram of
effects of climate change on
plantinsect interactions and
entire community/ecosystem.
Excess release of CO2, O3, and
other toxicants from industry,
temperature, and water content
variations cause direct and
indirect effects on plants,
insects, and their interaction
networks. These effects may
scale up from individual plant/
insect species to entire
communities

CLIMATE

CHANGE

ENTIRE ECOSYSTEM
Community scale trophic exchanges
Invasions at local or global scale
Diversity, composion and distribuon

CO2

O3

PLANT AND INSECT

COMMUNITIES
Associated predators and parasitoids

Temperature

Water

INSECTS
Insect herbivore performance
Foraging acvity
Body size, life span, life cycle
Reproducve output and
populaon densies
Service-resource pairings

Phenological mismatches

Plant-pollinator networks

Populaon-level changes

Plant phenology
Flower producon-number
and ming
Floral nectar, pollen producon
Plant phytochemistry
Plant defenses

PLANTS

and may lead to enhanced problems of food security and

imbalance of the ecosystem.
3.

Conclusions and future directions

1.

2.

Plants and insects evolved with huge diversity. Their

co-dependence represents a classic example of coevolution and mutualism. Comprehensive historical
studies on plantinsect interactions using available
fossil records provide a background for contemporary
biodiversity analysis of their interaction.
Examination and accurate identification of insect
damage in fossil floras can provide minimal Geochronological information on associations between
plants and insects. This temporal and ecological
information can be utilized to test hypotheses generated by host-herbivore analogy or micro-evolutionary
studies for the timing of origin and macro-evolutionary
history of plantinsect interactions. A radical rethinking is necessary for developing methods that can coopt natural insect-plant mutualism, ecology, and environmental safety while increasing the crop protection.
Sophisticated use of time-calibrated phylogenies need
to be made in understanding the actual timing and rate
of diversification and to link such events to other

123

4.

important biotic or abiotic factors in the most conclusive manner.

Extensive use of broad-spectrum chemical insecticides
and agricultural pest management practices often leads
to altered communities with reduced species richness
and evenness. Besides global environmental changes,
such as increased temperature, CO2, and ozone levels,
biological invasions, land-use change, and habitat
fragmentation together, play a significant role in reshaping the plantinsect multitrophic interactions at
various levels.
Diverse natural products need to be studied and
explored for their biological functions. They might
be useful as insect pest control agents and maximize
the use of natural strategies for targeting insect pests.
There may be a need to focus on multitrophic
interactions that indirectly affect plants and herbivores
and regulate their population buildup. In order to
assure the success of an integrated pest management
strategy, human activities need to be harmonized to
minimize the global climate changes.

Author contribution statement APG evolved theme of the

project. MM, PRL and RSJ performed literature survey and
prepared draft. SP contributed in developing ecological
aspects and collected pictures for figure 2. APG and VSG

Planta

edited and finalized the draft. All authors contributed in

revision and finalizing the manuscript.
Acknowledgments We thank Dr. Kiran Kulkarni and Dr. D. Shanmugam from CSIR-National Chemical Laboratory, India, and Dr.
Samuel Bocobza, Weizmann Institute of Science, Israel for critical
suggestions in the manuscript. MM and RSJ acknowledge the fellowship from the Council of Scientific and Industrial Research (CSIR)
and University Grants Commission, Government of India, New Delhi,
respectively. PRL is a recipient of Research Associateship of
Department of Biotechnology (DBT), and SP is a recipient of SERBDST Young Scientist Scheme, Department of Science and Technology (DST), Government of India, New Delhi. RSJ would like to
acknowledge financial support from Savitribai Phule Pune University,
under the DRDP scheme for year 20152016. Project funding under
CSIR network programs in XII plan (BSC0107 and BSC0120) to
CSIR-National Chemical Laboratory is greatly acknowledged.

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