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Insect Plant Insteractions
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Seediscussions,stats,andauthorprofilesforthispublicationat:http://www.researchgate.net/publication/279989279
Ecologicalturmoilinevolutionarydynamicsofplant–insectinteractions:defensetooffence
ARTICLEinPLANTA·JULY2015
ImpactFactor:3.38·DOI:10.1007/s00425-015-2364-7·Source:PubMed
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6AUTHORS,INCLUDING:
PurushottamRLomate
IowaStateUniversity
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RakeshJoshi
SavirtibaiPhulePuneUniversity
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VidyaShrikantGupta
CSIR-NationalChemicalLaboratory,Pune
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AshokPGiri
CSIR-NationalChemicalLaboratory,Pune
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Availablefrom:RakeshJoshi
Retrievedon:09September2015
REVIEW
Ecological turmoil in evolutionary dynamics of plant–insectinteractions: 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 contem-
porary 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 rich-
ness and evenness. The global environmental changes,
such as increased temperature, CO2 and ozone levels,
biological invasions, land-use change and habitat frag-
mentation 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
management strategy, human activities need to be
harmonized to minimize the global climate changes.
Plant–insect interaction is one of the most primitive and co-
evolved associations, often influenced by surrounding
changes. In this review, we account the persistence and
evolution of plant–insect 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 rela-
tionship while defending themselves. We provide a com-
prehensive 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 plant–insect
interactions. Hence, multitrophic approaches that can har-
monize human activities and minimize their interference in
native plant–insect interactions are needed to maintain
natural balance between the existence of plants and insects.
Keywords Plant–insect interaction � Co-evolution �Human interference � Ecosystem � Climatic change
Introduction
Plant–insect 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
M. Mishra, P. R. Lomate, R. S. Joshi contributed equally.
& Ashok P. Giri
1 Plant Molecular Biology Unit, Division of Biochemical
Sciences, CSIR-National Chemical Laboratory, Dr. Homi
Bhabha Road, Pune 411 008, MS, India
2 Institute of Organic Chemistry and Biochemistry, Academy
of Sciences of the Czech Republic, Prague, Czech Republic
3 Department of Entomology, Iowa State University, Ames,
IA 50011, USA
4 Institute of Bioinformatics and Biotechnology, Savitribai
Phule Pune University, Ganeshkhind, Pune 411007, MS,
India
5 Biospheres, Eshwari, 52/403, Laxminagar, Parvati,
Pune 411 009, MS, India
6 Naoroji Godrej Centre for Plant Research, Godrej & Boyce
Mfg. Co. Ltd., Lawkim Motor Group, Gat No. 431,
Shindewadi Post, Satara 412 801, MS, India
123
Planta
DOI 10.1007/s00425-015-2364-7
considerable debate on the timeline and the reasons behind
the genesis or the establishment of plant–insect interac-
tions. However, the general consensus is that the evolution
of various interactions resulted in the diversification of
plant and insect species (Kasting and Catling 2003). Sev-
eral factors, including climate, geography, and species
abundance/distribution may have contributed to the timely
and the reciprocal evolution of plant–insect interactions
(Shear 1991; Scott et al. 1992; Nisbet and Sleep 2001).
Climatic changes have influenced, shifted, and frag-
mented the taxonomic composition as well as the geo-
graphic distributions of plants and insects and they are the
key drivers for the evolution of plant–insect 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 Laban-
deira 1999; Currano et al. 2008) (Fig. 1). During the
Paleocene–Eocene 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 taxo-
nomic 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 plant–insect co-evolution can be seen in terms
Paleozoic Mesozoic Cenozoic0200400440 Million years before present (Approx.)
Cambrian Ordovician Silurian Devonian Carboniferous Permian Triassic Jurassic Cretaceous Ter�ary Quaternary
Insect Diversity
Detrivory Simple PlantPiercing
Early leaf ea�ng,Gall forming
Leaf mining
Pollen, nectar consuming
Pollina�on
Homoptera, Hemiptera
Archaeognatha
Hymenoptera
Thysanoptera
Coleoptera
Lepidoptera
Diptera
Algae (Aqua�c)
Mosses (Land)
Ferns (Seedless)
Ginkgos (Gymnosperm)
Conifers (Gymnosperm)
Cycads (Gymnosperm)
AngiospermPlant Diversity
Cambrian Ordovician Silurian Devonian Carboniferous Permian Triassic Jurassic Cretaceous Ter�ary Quaternary
Fig. 1 Plant and insect evolution and various feeding habits devel-
oped by insects throughout the evolutionary timescale. Plant evolu-
tion 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
Planta
123
of pollination. The development of floral tubes during the
Cretaceous period gave rise to highly specialized pollina-
tors 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 indi-
viduals. 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 plant–insect 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 plant–insect interactions to design sustain-
able strategies to protect crop plants from insect
infestations.
Myriad and diverse plant–insect 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 exploit-
ing 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. Simi-
larly, 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 decep-
tion’ 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). Insectiv-
orous 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: co-evolution 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 mecha-
nisms, which restrict insects by deterring and/or injuring
them (Fernandes 1994). Deterrents include certain com-
pounds released on the plant’s surface, namely, resins,
lignins, silica, and wax. The wax secreted by several ter-
restrial 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 com-
pounds (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). Inter-
estingly, 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 extraflo-
ral nectaries in order to attract natural enemies of herbi-
vores 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
plant’s 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 selec-
tively binds plant defense compounds (Fig. 3). Sequestra-
tion is an important strategy to detoxify harmful
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123
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
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,
Planta
123
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 iso-
forms 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
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 substi-
tution (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 demon-
strate 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 domesticationand agriculture
Human activities such as agriculture and industrialization
have significantly influenced the ecosystem and its com-
ponents. Likewise, plant–insect 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 conse-
quently has led to insect outbreaks and introduction of
bFig. 2 Plethora of plant–insect 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
Behavioral and morphological adapta�ons Molecular adapta�ons
Adap�ve and protec�ve structures• Cell wall carrier• Cu�cle• Trichomes• Thorns• Silica deposi�on• Extrafloral nectaries
Secondary metabolites• Terpenoids• Phenolics• Flavonoids• Quinones• Alkaloids• Extrafloral nectar ( to a�ract parasitoids)
Proteins• Lec�ns• Chi�nases• Enzyme inhibitors• Defensive enzymes
Direct and indirect defense metabolites
Behavioral tac�c against plant defense compounds • Avoidance• U�liza�on of alterna�ve hosts• Increased consump�on rate• Change in feeding habits• Development of specialized mouth parts
Molecular strategies against plant defense compounds• Sequestra�on of toxic compounds• Improved detoxifica�on mechanisms• Detoxifying and An�oxida�ve enzymes• Regula�on and modifica�on of diges�ve
enzymes
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
Planta
123
pests into new favorable areas causing destruction of nat-
ural 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 activ-
ity 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 high-
yielding, 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 high-
yielding crop varieties in response to fertilizers upsets the
plants’ carbon/nitrogen balance. This may result in meta-
bolic 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 plant–insect 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 fungi-
cides 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
the reduction of population of pests, parasites, and preda-
tors. 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-carboth-
ioate) 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 typi-
cally associated with pesticide detoxification including
cytochrome P450 s, esterases, and glutathione s-trans-
ferases’ (GSTs) display extensive modification and diver-
sification 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 DNAtechnology
Expression of recombinant insecticidal proteins in trans-
genic 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 pro-
teins for generating insect-resistant transgenic plants
(Hofte and Whiteley 1989; Bravo et al. 2011). In the mid-
1990s, 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 accumu-
lation 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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123
O’Callaghan et al. 2005; Schluter et al. 2010). For exam-
ple, the use of protease inhibitor for developing insect-
resistant 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 pesti-
cide 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 plant–insect ecosys-
tems. 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). Tem-
perature and water are the two most significant components
of the environment that directly influence plant–insect
interactions (Jamieson et al. 2012; Scherber et al. 2013).
Under a warm weather condition insects exhibit an accel-
erated metabolism, which leads to higher food consump-
tion, 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, cli-
mate 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 condi-
tions 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 down-
regulation 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 compro-
mised (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 mis-
match caused by differential phenological shifts among the
species have been documented in detail across diverse
consumer–resource pairings, including invertebrate herbi-
vores 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 plant–insect interactions
Planta
123
and may lead to enhanced problems of food security and
imbalance of the ecosystem.
Conclusions and future directions
1. Plants and insects evolved with huge diversity. Their
co-dependence represents a classic example of co-
evolution and mutualism. Comprehensive historical
studies on plant–insect interactions using available
fossil records provide a background for contemporary
biodiversity analysis of their interaction.
2. Examination and accurate identification of insect
damage in fossil floras can provide minimal Geo-
chronological information on associations between
plants and insects. This temporal and ecological
information can be utilized to test hypotheses gener-
ated by host-herbivore analogy or micro-evolutionary
studies for the timing of origin and macro-evolutionary
history of plant–insect interactions. A radical rethink-
ing is necessary for developing methods that can co-
opt natural insect-plant mutualism, ecology, and envi-
ronmental 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
important biotic or abiotic factors in the most conclu-
sive manner.
3. 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 re-
shaping the plant–insect multitrophic interactions at
various levels.
4. 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
• Plant phenology• Flower produc�on-number and �ming• Floral nectar, pollen produc�on• Plant phytochemistry• Plant defenses
• Insect herbivore performance• Foraging ac�vity• Body size, life span, life cycle• Reproduc�ve output and popula�on densi�es
• Associated predators and parasitoids
• Community scale trophic exchanges• Invasions at local or global scale• Diversity, composi�on and distribu�on
PLANTS
INSECTS
PLANT AND INSECT COMMUNITIES
ENTIRE ECOSYSTEM
Phenological mismatches
Popula�on-level changes
Service-resource pairings
Plant-pollinator networks
C L I M A T E C H A N G E
CO2
Temperature
O3
Water
Fig. 4 Schematic diagram of
effects of climate change on
plant–insect 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
Planta
123
edited and finalized the draft. All authors contributed in
revision and finalizing the manuscript.
Acknowledgments We thank Dr. Kiran Kulkarni and Dr. D. Shan-
mugam 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 fel-
lowship 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 SERB-
DST Young Scientist Scheme, Department of Science and Technol-
ogy (DST), Government of India, New Delhi. RSJ would like to
acknowledge financial support from Savitribai Phule Pune University,
under the DRDP scheme for year 2015–2016. Project funding under
CSIR network programs in XII plan (BSC0107 and BSC0120) to
CSIR-National Chemical Laboratory is greatly acknowledged.
References
Ali JG, Agrawal AA (2012) Specialist versus generalist insect
herbivores and plant defense. Trends Plant Sci 17:293–302
Altieri MA, Letourneau DK, Stephen J (1984) Vegetation diversity
and insect pest outbreaks. CRC Crit Rev Plant Sci 2:131–169
Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE,
Freckleton RP, Lewis OT (2014) Pathogens and insect herbi-
vores drive rainforest plant diversity and composition. Nature
506:85–88
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
Becerra JX, Noge K, Venable DL (2009) Macroevolutionary chem-
ical escalation in an ancient plant-herbivore arms race. Proc Natl
Acad Sci USA106:18062–18066
Bown DP, Wilkinson HS, Gatehouse JA (1997) Differentially
regulated inhibitor-sensitive and insensitive protease genes from
the phytophagous insect pest, Helicoverpa armigera, are mem-
bers of complex multigene families. Insect Biochem Mol Biol
27:625–638
Bravo A, Likitvivatanavong S, Gill SS, Soberon M (2011) Bacillus
thuringiensis: a story of a successful bioinsecticide. Insect
Biochem Mol Biol 41:423–431
Broadway RM (1996) Dietary proteinase inhibitors alter complement
of midgut proteases. Arch Insect Biochem Physiol 32:39–53
Bronstein JL (1994) Our current understanding of mutualism. Q Rev
Biol 69:31–51
Bronstein JL, Alarcon R, Geber M (2006) The evolution of plant–
insect mutualisms. New Phytol 172:412–428
Brown TA, Jones MK, Powell W, Allaby RG (2009) The complex
origins of domesticated crops in the Fertile Crescent. Trends
Ecol Evol 24:103–109
Cherif M, Loreau M (2013) Plant–herbivore–decomposer stoichio-
metric mismatches and nutrient cycling in ecosystems. Proc Biol
Sci. 280:20122453
Chougule NP, Giri AP, Sainani MN, Gupta VS (2005) Gene
expression patterns of Helicoverpa armigera gut proteases.
Insect Biochem Mol Biol 35:355–367
Christou P, Twyman RM (2004) The potential of genetically
enhanced plants to address food insecurity. Nutr Res Rev
17:23–42
Crane PR, Friis EM, Pedersen KR (1995) The origin and early
diversification of angiosperms. Nature 374:27–33
Crepet WL (2008) The fossil record of angiosperms: requiem or
renaissance? Ann Mo Bot Gard 95:3–33
Currano ED, Wilf P, Wing SL, Labandeira CC, Lovelock EC, Royer
DL (2008) Sharply increased insect herbivory during the
paleocene-eocene thermal maximum. Proc Natl Acad Sci USA
105:1960–1964
Dawkar VV, Chikate YR, Lomate PR, Dholakia BD, Gupta VS, Giri
AP (2013) Molecular insights into resistance mechanisms of
lepidopteran insect pests against toxicants. J Proteome Res
12:4727–4737
Dobler S, Dalla S, Wagschal V, Agrawal AA (2012) Community-
wide convergent evolution in insect adaptation to toxic carde-
nolides by substitutions in the Na?K?-ATPase. Proc Natl Acad
Sci USA 109:13040–13045
Duan JJ, Lundgren JG, Naranjo S, Marvier M (2010) Extrapolating
non-target risk of Bt crops from laboratory to field. Biol Lett
6:74–77
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in
coevolution. Evolution 18:586–608
Fernandes GW (1994) Plant mechanical defenses against insect
herbivory. Rev Bras Entomol 38:421–433
Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol
44:507–533
Frampton GK (1999) Spatial variation in non-target effects of the
insecticides chlorpyrifos cypermethrin and pirimicarb on
Collembola in winter wheat. Pestic Sci 55:875–886
Gahan LJ, Pauchet Y, Vogel H, Heckel DG (2010) An ABC
transporter mutation is correlated with insect resistance to
Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 6:e1001248
Gepts PA (2002) Comparison between crop domestication classical
plant breeding and genetic engineering. Crop Sci 42:1780–1790
Giri AP, Harsulkar AM, Deshpande VV, Sainani MN, Gupta VS,
Ranjekar PK (1998) Chickpea defensive proteinase inhibitors
can be inactivated by podborer gut proteinases. Plant Physio
116:393–401
Gordon DR (1998) Effects of invasive, non-indigenous plant species
on ecosystem processes: lessons from Florida. Ecol Appl
8:975–989
Green TR, Ryan C (1972) Wound-induced proteinase inhibitor in
plant leaves: a possible defense mechanism against insects.
Science 175:776–777
Harter AV, Gardner KA, Falush D, Lentz DL, Bye RA, Rieseberg LH
(2004) Origin of extant domesticated sunflowers in eastern North
America. Nature 430:201–205
Heckel DG (2012) Insecticide resistance after silent spring. Science
337:1612–1614
Hegland SJ, Nielsen A, Lazaro A, Bjerknes A, Totland O (2009) How
does climate warming affect plant-pollinator interactions? Ecol
Lett 12:184–195
Hofte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus
thuringiensis. Microbiol Rev 53:242–255
Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T (2007) Obligate
symbiont involved in pest status of host insect. Proc Biol Sci
22:1979–1984
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012)
Consequences of climate warming and altered precipitation
patterns for plant–insect and multitrophic interactions. Plant
Physiol 160:1719–1727
Jersakova J, Johnson SD, Kindlmann P (2006) Mechanisms and
evolution of deceptive pollination in orchids. Biol Rev
81:219–235
Jongsma MA, Stiekema WJ, Bosch D (1996) Combatting inhibitor-
insensitive proteases of insect pests. Trends Biotechnol
14:331–333
Karban R, Baldwin IT (1997) Induced responses to herbivory.
University of Chicago Press, Chicago
Kasting JF, Catling D (2003) Evolution of a habitable planet. Annu
Rev Astron Astrophys 41:429–436
Planta
123
Kessler A, Baldwin IT (2001) Defensive function of herbivore-
induced plant volatile emissions in nature. Science
1291:2141–2144
Klassen W, Schwartz PH (1985) AARS Research Program in
Chemical Insect Control,@ Agricultural Chemicals of the
Future, BARC Symposium 8, James L. Hilton (ed), Rowman
& Allanheld, Totowa
Krieger RI, Feeny PP, Wilkinson CF (1971) Detoxification enzymes
in the guts of caterpillars: an evolutionary answer to plant
defenses? Science 172:579–581
Kumar P, Pandit SS, Steppuhn A, Baldwin IT (2014) Natural history-
driven plant-mediated RNAi-based study reveals CYP6B46’s
role in a nicotine-mediated antipredator herbivore defense. Proc
Natl Acad Sci USA 111:1245–1252
Labandeira CC (1998) Early history of arthropod and vascular plant
associations. Annu Rev Earth Planet Sci 26:329–377
Labandeira CC (2013) A paleobiological perspective on plant–insect
interactions. Curr Opin Plant Biol 16:414–421
Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2007)
Altered ecosystem carbon and nitrogen cycles by plant invasion:
a meta-analysis. New Phytol 177:706–714
Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on
forests: phytochemistry trophic interactions and ecosystem
dynamics. J Chem Ecol 36:2–21
Logan JA, Regniere J, Powell JA (2003) Assessing the impacts of
global warming on forest pest dynamics. Front Ecol Environ
1:130–137
Lomate PR, Hivrale VK (2010) Partial purification and characteri-
zation of Helicoverpa armigera (Lepidoptera: Noctuidae) active
aminopeptidase secreted in midgut. Comp Biochem Physiol-B
155:164–170
Lomate PR, Hivrale VK (2011) Differential responses of midgut
soluble aminopeptidases of Helicoverpa armigera to feeding on
various host and non-host plant diets. Arthropod Plant Interact
5:359–368
Magdoff F, Foster JB, Buttel FH, (2000) Hungry for profit: The
agribusiness threat to farmers, food, and the environment. NYU
Press, New York
Mahajan NS, Mishra M, Tamhane VA, Gupta VS, Giri AP (2013)
Plasticity of protease gene expression in Helicoverpa armigera
upon exposure to multi-domain Capsicum annuum protease
inhibitor. Biochim Biophys Acta 1830:3414–3420
Malone LA, Burgess EPJ (2000) Interference of protease inhibitors on
non-target organisms. In: Michaud D (ed) Recombinant protease
inhibitors in plants. Landes Bioscience, Georgetown, pp 89–106
Mcelwain JC, Punyasena S (2007) Mass extinction events and the
plant fossil record. Trends Ecol Evol 22:548–557
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming
and the disruption of plant–pollinator interactions. Ecology Lett
10:710–717
Michener CD (2007) The bees of the world, 2nd edn. The John
Hopkins University Press, Baltimore
Mithofer A, Boland W (2012) Plant defense against herbivores:
chemical aspects. Annu Rev Plant Biol 63:431–450
Mithofer A, Boland W, Maffei ME (2009) Chemical ecology of
plant–insect interactions. In: Parker J (ed) Plant disease resis-
tance. Wiley, Chichester, pp 261–291
Mitterboeck TF, Adamowicz SJ (2013) Flight loss linked to faster
molecular evolution in insects. Proc Biol Sci 280:20131128
Nelson WA, Bjornstad ON, Yamanaka T (2013) Recurrent insect
outbreaks caused by temperature-driven changes in system
stability. Science 341:796–799
Niklas KJ, Tiffney BH, Knoll AH (1983) Pattern in vascular land
plant diversification. Nature 303:614–616
Nisbet EG, Sleep NH (2001) The habitat and nature of early life.
Nature 409:1083–1091
Nishida R (2002) Sequestration of defensive substances from plants
by Lepidoptera. Annu Rev Entomol 47:57–92
O’callaghan M, Glare TR, Burgess EPJ, Malone LA (2005) Effects of
plants genetically modified for insect resistance on non-target
organisms. Annu Rev Entomol 50:271–292
Oliveira PS, Freitas AV (2004) Ant–plant–herbivore interactions in the
neotropical cerrado savanna. Naturwissenschaften 91:557–570
Opitz SE, Muller C (2009) Plant chemistry and insect sequestration.
Chemoecology 19:117–154
Patankar AG, Giri AP, Harsulkar AM, Sainani MN, Deshpande VV,
Ranjekar PK, Gupta VS (2001) Complexity in specificities and
expression of Helicoverpa armigera gut proteinases explains
polyphagous nature of the insect pest. Insect Biochem Mol Biol
31:453–464
Percy KE, Awmack CS, Lindroth RL, Kubiske ME, Kopper BJ,
Isebrands JG, Pregitzer KS, Hendrey GR, Dickson RE, Zak DR,
Oksanen E, Sober J, Harrington R, Karnosky DF (2002) Altered
performance of forest pests under atmospheres enriched by CO2
and O3. Nature 420:403–407
Pimentel D, Edwards CA (1982) Pesticides and ecosystems. BioS-
cience 32:595–600
Pimentel D, Acquay H, Biltonen M, Rice P, Silva M, Nelson J, Lipner
V, Giordano S, Horowitz A, D’amore M (1992) Environmental
and economic costs of pesticide use. BioScience 42:750–760
Potting RP, Vet LE, Dicke M (1995) Host microhabitat location by
stem-borer parasitoid Cotesia flavipes: the role of herbivore
volatiles and locally and systemically induced plant volatiles.
J Chem Ecol 21:525–539
Powell JA, Bentz BJ (2009) Connecting phenological predictions
with population growth rates for mountain pine beetle an
outbreak insect. Landscape Ecol 24:657–672
Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN,
Mobley K (1986) Parasite mediation in ecological interactions.
Annu Rev Ecol Evol Syst 17:487–505
Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG,
Romme WH (2008) Cross-scale drivers of natural disturbances
prone to anthropogenic amplification: the dynamics of bark
beetle eruptions. Bioscience 58:501–517
Raviv M, Antignus Y (2004) UV radiation effects on pathogens and
insect pests of greenhouse-grown crops. Photochem Photobiol
79:219–226
Scaven VL, Rafferty NE (2013) Physiological effects of climate
warming on flowering plants and insect pollinators and potential
consequences for their interactions. Curr Zool 59:418–426
Scherber C, Gladbach DJ, Stevnbak K, Karsten RJ, Schmidt IK,
Michelsen A, Albert KR, Larsen KS, Mikkelsen TN, Beier C,
Christensen S (2013) Multifactor climate change effects on
insect herbivore performance. Ecol Evol 3:1449–1460
Schluter U, Benchabane M, Munger A, Kiggundu A, Vorster L,
Goulet M, Cloutier C, Michaud D (2010) Recombinant protease
inhibitors for herbivore pest control: a multitrophic perspective.
J Exp Bot 61:4169–4183
Scott AC, Chaloner WG, Paterson S (1985) Evidence of pteridophyte-
arthropod interactions in the fossil record. Proc Biol Sci 86:133–140
Scott AC, Stephenson J, Chaloner WG (1992) Interaction and
coevolution of plants and arthropods during the Palaeozoic and
Mesozoic. Philos Trans R Soc Lond B Biol Sci 335:129–165
Shear WA (1991) The early development of terrestrial ecosystems.
Nature 351:183–189
Slack A, Gate J (2000) Carnivorous plants. MIT Press, Cambridge
Snyder MS, Glendinning JI (1996) Causal connection between
detoxification enzyme activity and consumption of a toxic plant
compound. J Comp Physiol A 179:255–261
Spafford RD, Lortie CJ (2013) Sweeping beauty: is grassland
arthropod community composition effectively estimated by
sweep netting? Ecol Evol 3:3347–3358
Planta
123
Stone GN, Hernandez-lopez A, Nicholls JA, Di pierro E, Pujade-villar
J, Melika G, Cook JM (2009) Extreme host plant conservatism
during at least 20 million years of host plant pursuit by oak gall
wasps. Evolution 63:854–869
Strauss AS, Peters S, Boland W, Burse A (2013) ABC transporter
functions as a pacemaker for sequestration of plant glucosides in
leaf beetles. eLife 2:e01096
Takhtajan A (1991) Evolutionary trends in flowering plants.
Columbia University Press, New York
Tamhane VA, Chougule NP, Giri AP, Dixit AR, Sainani MN, Gupta
VS (2005) In vivo and in vitro effect of Capsicum annum
proteinase inhibitors on Helicoverpa armigera gut proteinases.
Biochim Biophys Acta 1722:156–167
Tamhane VA, Giri AP, Sainani MN, Gupta VS (2007) Diverse forms
of Pin-II family proteinase inhibitors from Capsicum annuum
adversely affect the growth and development of Helicoverpa
armigera. Gene 403:29–38
Tahvanainen J, Niemela P (1987) Biogeographical and evolutionary
aspects of insect herbivory. Ann Zool Fennici 24:239–247
Taylor EL, Taylor TN (1992) Reproductive biology of the Permian
Glossopteridales and their suggested relationship to the flower-
ing plants. Proc Natl Acad Sci USA89:11495–11497
Theiling KM, Croft BA (1988) Pesticide side-effects on arthropod
natural enemies: a database summary. Agric Ecosyst Environ
21:191–218
Traveset A, Richardson DM (2006) Biological invasions as disruptors
of plant reproductive mutualisms. Trends Ecol Evol 21:208–216
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global
change and species interactions in terrestrial ecosystems. Ecol
Lett 11:1351–1363
Van der putten WH, Macel M, Visser ME (2010) Predicting species
distribution and abundance responses to climate change:why it is
essential to include biotic interactions across trophic levels.
Philos Trans R Soc Lond B Biol Sci 365:2025–2034
Visser ME, Holleman LJ (2001) Warmer springs disrupt the
synchrony of oak and winter moth phenology. Proc Biol Sci
268:289–294
Vogel S, Martens J (2000) A survey of the function of the lethal kettle
traps of Arisaema (Araceae) with records of pollinating fungus
gnats from Nepal. Bot J Linn Soc 133:61–100
Von Rad U, Mueller MJ, Durner J (2005) Evaluation of natural and
synthetic stimulants of plant immunity by microarray technol-
ogy. New Phytol 165:191–202
Walling LL (2000) The myriad plant responses to herbivores. J Plant
Growth Regul 19:195–216
Wappler T, Currano ED, Wilf P, Rust J, Labandeira CC (2009) No
post-Cretaceous ecosystem depression in European forests? Rich
insect-feeding damage on diverse middle Palaeocene plants
Menat France. Proc Biol Sci 276:4271–4277
Wilf P (2008) Insect-damaged fossil leaves record food web response
to ancient climate change and extinction. New Phytol
178:486–502
Wilf P, Labandeira CC (1999) Response of plant-insect associations
to paleocene-eocene warming. Science 284:2153–2155
Zavada MS (1984) Angiosperm origins and evolution based on
dispersed fossil pollen ultrastructure. Ann Mo Bot Gard
71:444–463
Zavala JA, Casteel CL, Delucia EH, Berenbaum MR (2008)
Anthropogenic increase in carbon dioxide compromises plant
defense against invasive insects. Proc Natl Acad Sci USA
105:5129–5133
Zavala JA, Nabity PD, Delucia EH (2013) An emerging understand-
ing of mechanisms governing insect herbivory under elevated
CO2. Annu Rev Entomol 58:79–97
Planta
123