Insect Plant Insteractions

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

DOWNLOADS

62

VIEWS

68

6AUTHORS,INCLUDING:

PurushottamRLomate

IowaStateUniversity

19PUBLICATIONS59CITATIONS

SEEPROFILE

RakeshJoshi

SavirtibaiPhulePuneUniversity

17PUBLICATIONS42CITATIONS

SEEPROFILE

VidyaShrikantGupta

CSIR-NationalChemicalLaboratory,Pune

190PUBLICATIONS3,614CITATIONS

SEEPROFILE

AshokPGiri

CSIR-NationalChemicalLaboratory,Pune

102PUBLICATIONS2,309CITATIONS

SEEPROFILE

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

[email protected]

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

Planta

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;

Planta

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