Acta Ecologica Sinica 34 (2014) 325336

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Acta Ecologica Sinica

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / c h n a e s

Interactions between plants and herbivores: A review of plant defense

Bin Gong a, Guangfu Zhang a,b,*
a
b

Jiangsu Key Laboratory of Biodiversity and Biotechnology, School of Life Sciences, Nanjing Normal University, Nanjing 210023, China
State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS), Nanjing 210008, China

A R T I C L E

I N F O

Article history:
Received 7 January 2013
Revised 5 June 2013
Accepted 23 July 2013
Available online
Keywords:
Herbivore
Plant anti-herbivore defense
Plantanimal interaction
Resistant
Tolerance
Escape strategies

A B S T R A C T

Ecologists have long ignored or underestimated the importance of plantherbivore interactions owing
to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briey
discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores. Selective forces of herbivore pressures have led to the evolution of various defensive mechanisms
in plants, which can be classied into (i) resistance traits that reduce the amount of damage received,
including physical, chemical, and biotic traits; (ii) tolerance mechanisms that decrease the impact of herbivore damage, and (iii) escape strategies that reduce the probability of plants to be found by herbivores.
These strategies have been studied at different levels from molecular genetics and genomics, to chemistry and physiology, to community and ecosystem ecology. We summarized the development of the
methodology for studying plant defenses against herbivores. Particularly, 24 of those hypotheses and models,
which are inuential in the international community concerning the relationship between plants and
herbivores, including the defensive mimicry hypothesis, the compensatory continuum hypothesis, the
slow-growth-high-mortality hypothesis, etc, were introduced and grouped into four categories according to plant defense strategies in the present review. Finally, we also reviewed the research progress of
plantherbivore interactions in China, and discussed the perspectives of studies on plantherbivore
interactions.
2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

1. Introduction
The interactions between plants and herbivores are among the
most important ecological interactions in nature [1]. As primary producers, almost all plants inevitably avoid being eaten by herbivores
[2]. Thus, these relationships will affect nutrient cycles and energy
ows of food chains [3]. It is reported that these herbivores consume
over 15% of the whole plant biomass produced annually in temperate and tropical ecosystems. Accordingly, this makes herbivory
the major conduit by which energy enters food chains [1,4].
More than three-quarters of animals are herbivores in nature, which
play a signicant role in shaping ecosystem structure and function
[5,6]. Herbivores have a strong effect on their distributions and abundances by consuming plants [7,8]. They also exert a strong selective
pressure on plant population by increasing its mortality and depleting biomass which can be used for plant growth and reproduction
[9]. On the contrary, such habitat conditions as community type, plant
density and light intensity, will result in spatial variation of planteating insects. Therefore, the interactions between plants and

* Corresponding author. Jiangsu Key Laboratory of Biodiversity and Biotechnology,

School of Life Sciences, Nanjing Normal University, Nanjing 210023, China. Tel:
+86-25-13915978931; fax: +86-25-85891839.
E-mail address: zhangguangfu@njnu.edu.cn (G. Zhang).

herbivores not only affect the structure and dynamics of plant populations, but also affect community composition and diversity, as well
as ecosystem through food web and nutrient cycles [10].
When attacked by herbivores, plants can take various defensive
measures, which are essential in the research eld of interactions
between plants and herbivores. Firstly, plant defense has played a
critical role in the long-term co-evolution of plants and herbivores.
For this reason, understanding the evolution and ecology of plant
defenses is nearly equivalent to understanding the origin and function of extant ecosystems [1]. Secondly, the plant defense research
deals with multiple subdisciplines and different scales, for example,
from genetics and genomic to chemistry and physiology, to community ecology, ecosystem sciences and global patterns of herbivory
and defense [1]. Another reason for studying plant defense against
herbivores is that every year herbivory causes world economies to
lose billions of dollars of revenue related to agriculture, horticulture and forestry [11]. Therefore, the study of plant defense is
particularly necessary. It is quite common to carry out studies about
plant defense characteristics, defense mechanisms and other respects abroad; however, there are very few related researches at home.
In this review, we briey discussed the categories of herbivores. Then we reviewed the major types of plant defenses against
herbivores from an ecological point of view, classied them into
three categories including resistance traits, tolerance mechanisms
and escape strategies. We also summarized the development of the

http://dx.doi.org/10.1016/j.chnaes.2013.07.010
1872-2032/ 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

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G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

methodology for studying plant defenses against herbivores. Numerous theoretical models and hypotheses, which are inuential
in the international community concerning the relationship between
plants and herbivores, were introduced in the present review. They
can be grouped into four categories according to plant defense strategies; meanwhile most of them were reviewed within each category.
Finally, we also reviewed the research progress of plantherbivore
interactions in China, and then discussed the perspectives of studies
on plantherbivore interactions to provide a theoretical basis for
our future research.
2. Categories of herbivores
2.1. According to zoological classication criteria
According to zoological classication criteria, herbivores can be
divided into herbivorous vertebrates and invertebrates. Most part
of the former is generally herbivorous mammals (mainly ungulates), which is widely recognized as an important factor in
maintaining the biodiversity of grasslands [1214]. Meanwhile the
latter mainly consists of Arthropoda (including herbivorous insects
and crustaceans) and Mollusca (usually Gastropoda, such as snails,
slugs, etc.). Initially many authors reported important relationships between mammalians and plants. By contrast, little attention
was paid to the role of invertebrate herbivores in shaping plant community and population dynamics. However, such studies becoming
a great part of ecology have been well documented in the literature in the past decades. Many studies have demonstrated that
invertebrate herbivores have an important effect on secondary succession of plant communities [1520].
Most mammals and mollusks feed on plant seedlings while
insects do great damage to adult plants in the eld. Interaction
between plants and insects from different forest ecosystems has been
widely carried out. Because of their different mouthparts, leaf
damages by insects include chewing, skeletonizing, insect galling,
mining, rolling, and sucking [21]. Plants and insects comprise most
part of the organisms on Earth, and their interactions have profound implications not only for both ecological and evolutionary
processes [2224], but also for ecosystem nutrient cycling and energy
ow [22,25]. Currently, researches on interactions between mollusks and plants are not as many as those relationships between
insects and plants, but most studies on mollusk herbivory have suggested that mollusks, consuming little biomass, do enhance seedling

Zoological classification criterion

mortality of subdominant herbs [14,26]. Generally mollusks are likely

to feed on seedlings instead of adult plants, causing a great inuence on plant individuals which is disproportionate to the biomass
removed [27,28]. For example, a mollusk can kill a whole seedling
with the removal of one bite of the hypocotyl while a similar bite
to a mature leaf would have a negligible effect on the survival of
the plant [29]. Therefore mollusks have a great impact on community composition of herb layer [30,31], especially for seedlings since
their establishment is the crucial point in a species life cycle [3133].
Lodge [34] once pointed out that aquatic herbivores had little
effect on the aquatic plants. However, studies hereafter have shown
that aquatic herbivores have a strong impact on aquatic plant
biomass [35] and species composition [36]. As common aquatic herbivores, some snails (from Gastropoda) and crustaceans (from
Crustacea), like crayshes, are distributed widely in the eld. Nowadays, most of them have been applied as generalist herbivores
during bioassay experiment to elucidate the relationship between
aquatic herbivores and plants [8,3739].

2.2. According to herbivores preference for plant species

According to herbivores preference for plant species, herbivores can be divided into generalists and specialists (including
oligophagous and monophagous). Most herbivorous mammals and
mollusks usually belong to generalist consumers while most planteating insects belong to specialist consumers [39]. For example,
crayshes (from crustacean) are often used as generalist herbivores in experiments (Fig. 1). Generalist herbivores refer to animals
that can feed on most plants, and will not give up feeding on some
certain plant species because of their special feeding preferences.
Plant defenses and natural enemies are widely believed to be the
main reasons why specialist herbivores only rely on one food source
[3].
In view of the fact that generalists and specialists have different dependence and effect on plants [40], there are two viewpoints:
some scholars believe that generalist consumers have greater effects
on plant tness and community composition [8,39,41,42]. On the
contrary, other scholars hold that specialist consumers cause more
damage to plants because they have superiority to generalists in foodsearching and food utilization, food location and detoxifying, with
fewer chance of being exposed to natural enemies [43]. Such disparity may be attributed to the different research content which is

Herbivorous vertebrates

Mammals (mainly)

Herbivorous

Herbivores

Molluscs

Arthropod

Crustacea

Insecta
Herbivores preference for plants

Specialist herbivores
(Oligophagous and monophagous)

Generalist herbivores
Fig. 1. Categories of herbivores.

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

focused on generalists or specialists, as well as to the evolutionary

stage of plants.
In temperate forest ecosystems, generalists take up a large proportion of herbivores while in tropical forest ecosystems, specialists
take up a large proportion of herbivores. Basset [44] pointed out
that this may be related with higher leaf palatability in temperate
forest. Take for example the toughness of mature or immature leaves
in tropical forest, which was twice as much as that in temperate
forest; however, both nitrogen and water contents of mature leaves
in tropical forest were signicantly lower than those in temperate
forest [45].
3. Plant defense strategies
In general, herbivores have negative impacts on plant tness
[46,47]. The damage caused by them is a kind of natural selection
pressure, which enables plants constantly to develop effective defense
strategies against herbivores in the long-term interactive and coevolutionary process. As a rule, each plant species has more than
one defense characteristics. Based on the resource allocation tradeoffs
between different body parts, plant species may well have various
defense characteristics coexisting in different individuals instead of
investing all defensive features in one individual. Agrawal and
Fishbein (2006) predicted that a continuum of anti-herbivory defense
contained three types of syndromes: (1) poorly defended plants with
phenological escape mechanisms; (2) plants with nutritious, edible
leaves having physical and chemical defenses; and (3) plants with
tough and inedible leaves [48]. In addition, plants can change their
defense features across life-history stages to meet the requirements of resource allocation.
In this paper, in light of the latest classication posed by Boege
et al. [49], plant defense strategies will be divided into the following three categories: resistance traits, tolerance mechanisms and
escape strategies (Fig. 2).
3.1. Resistance traits
Resistance traits include physical features (e.g., trichomes, spines,
thorns or leaf toughness), chemical features (main secondary metabolites), or biotic features (e.g., maintaining or enhancing the
activity of natural enemies of herbivores), and all these traits can
be used to reduce the amount of damage from herbivores.
3.1.1. Physical resistance traits
Physical resistance traits refer to morphological or structural
modications that plant species make when attacked by herbi-

vores [50]. One of the most possible parts is leaf blade owing mainly
to its structure, such as trichomes, LMA (leaf mass per area), thickness, texture and cell structure [51]. Among them, LMA, which is
often used as indicators of leaf physical defense, is one of the most
widely measured functional traits [52,53]. In addition, leaf thickness is considered to be the best effective defense measure [54]
because many studies have shown that leaf toughness is negatively correlated with herbivory [24,49,55,56]. It is worthy to note that
some plant species own physical mimicry in structure, like some
orchid owers, which are able to mimic bees or wasps to deter large
herbivorous mammals and insects [57]. However, such kinds of
ower traits may positively or negatively inuence foraging preferences of pollinators to a great extent. For instance, root herbivory
might positively inuence pollinator behavior; nevertheless, herbivore damage to leaves and owers might negatively affect foraging
preferences of pollinators [58].
3.1.2. Chemical resistance traits
Chemical resistance traits refer to physiological modications that
plant species make when attacked by herbivores [50], which chiey
involve a great variety of plant secondary metabolites (PSMs). The
total number of PSMs whose structures have been elucidated is about
50 000, and this is only a small fraction of all PSMs existing in nature
[59,60]. According to Kang [61], the chemical defense components, which are produced by plants against herbivores, can be
divided into seven categories: terpenoids; phenolic compounds; nitrogen compounds; tannins, lignin and cellulose; plant hormones
and lectin; protease inhibitors; and volatile compounds. Of all, phenol
and terpene are secondary metabolites with carbon but without nitrogen, and both of them are made to defend herbivores when there
is redundant carbon in plants. The total phenolic within a plant individual can be used as indicators showing chemical defense capacity,
and the content of tannin and protein is correlated with carbon or
nitrogen-based plant defense [51]. Studies concerning other secondary metabolites such as saponin, alkaloids, amino acids, cyanide
and other studies are still very few. In recent years, many scholars
have focused on the effect of plant enzymes (such as amino acid
degrading enzymes, proteases, etc.) on herbivores after feeding. Some
amino acids cannot be synthesized by herbivores, and therefore they
must be obtained from the diet. If these essential amino acids are
destroyed by plant enzymes in the gut of herbivores, their development will be impaired [60]. The role of anthocyanins in plant
defense against herbivores has been a disputed topic for a long time,
in which some scholars believe that the development of anthocyanin is a response against pathogens [54]. Furthermore, some owers
are able to emit carrion and dung odors, an olfactory mimicry of a

Physical resistance (Leaf thickness, leaf texture, physical mimicry, etc.)

Resistance traits

Chemical resistance (Tannins, alkaloids, chemical mimicry, etc.)

Strategies of plant

Biological resistance (Mututalistic and non-mututalistic indirect defenses)

Tolerance mechanisms

Increases in photosynthetic area, stored resources, bud bank, etc.

Temporal escape

Lag time in the herbivore colonization of young

trees and phenology, etc.

Escape strategies
Spatial escape

327

Associational resistance and Janzen-Connell

hypothesis, etc.

Fig. 2. Categories of plant defense against herbivores (Adapted from Reference 49).

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G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

danger of predators, through chemical mimicry defense to deter the

attack of mammalian herbivores [62].
3.1.3. Biological resistance traits
There are two types of chemical resistance traits. (1) Indirect defenses involving defensive mutualisms. It means that plant species
are able to attract herbivores natural enemies (predators and parasitoids) by providing food rewards, nesting space or chemical cues
so that they can defend themselves against herbivores. The most
famous case is myrmecophytism which involves plantant
mutualisms. In this case, the myrmecophytic plants provide nesting
space for ants, and sometimes offer extraoral nectar or nutritious food [63]. In return, ants protect host plants from herbivores
[6467]. Such defensive mutualisms also occur between wasps and
plants, and in these cases the plant provides nectar for wasps as a
reward to obtain protection [68]. (2) Non-mututalistic indirect
defense. In some cases, plant species are defended by animals that
are not engaged in mutualistic interactions with the plant. Compared with the rst type, this type has small probability of
occurrence. van Bael et al. (2003) investigated how predators affected herbivore abundance and levels of herbivory in saplings and
adult trees in three tropical tree species. By using cages to prevent
access to bird predators, they found that the practice of caging signicantly decreased herbivore abundance and levels of herbivory
on trees but had no effect on saplings [69]. Boege and Marquis [70]
compared the effect of caging and non-caging on saplings and mature
trees, and found that the foraging intensity of bird predators in
mature trees was signicantly higher than in samplings. Furthermore, Boege [71] noted that foraging of parasitoid wasps was almost
restricted to the canopies of mature trees in rain forest.
3.2. Tolerance mechanisms
Tolerance mechanisms are dened as the capacity of plants to
reduce the negative effects of damage on tness [72]. During the
long-term evolution, plants are likely to establish tolerance mechanisms to reduce the impact of herbivore damage once it has occurred.
Early research on this respect regarded plant tolerance as a part of
defense mechanism [73], but later studies have shown that there
is a tradeoff between tolerance and defense [7476]. Although plants
are able to resist herbivores through defense mechanisms, they can
hardly reduce the damage. By contrast, tolerance mechanisms can
enable plants to compensate or replace damaged tissues, e.g., enhancing photosynthetic eciency, activating dormant meristems,
making use of reserved resource, changing resource allocation mode,
etc. Generally, seedlings that experience signicant reductions in
growth following herbivory are unable to compensate for lost tissues.
Later on as juveniles develop from seedlings to saplings, they can
show signicant increases in compensation for herbivory, probably due to increases in photosynthetic area, stored resources, and
abundant bud bank. Finally, mature plants may experience lower
compensation for herbivory than saplings because of having relatively more senescent leaves [49]. Besides, on the basis of tradeoff
between defense and tolerance, plants at the stage of reproduction will have much more tolerance than vegetative growth [76],
because they will allocate more resources to their reproduction with
low investment in other respects. Though many a scholar assume
that compensation mechanisms may enable plants to increase their
tness, there are few related studies and it remains unclear which
mechanism is the most important [77]. Therefore, plant tolerance
mechanisms still need further study. For instance, injured plants can
increase their photosynthetic eciency, but are unlikely to achieve
the same level as the uninjured plants. In fact, the lack of knowledge about the mechanisms of tolerance has constrained the study
of tolerance in real ecological condition, limited the experimental
and genetic manipulation of tolerance to herbivory indoors, and

impeded understanding the role of environmental factors and genetic

backgrounds in tolerance research [72]. In view of the fact that there
are much more theoretical reasons than experimental explanations, experimental researches should be strengthened in order to
supplement and improve the tolerance mechanisms of plants.
3.3. Escape strategies
The reason why plants develop escape strategies during evolution is to reduce the probability of plants to be found by their
consumers. There are a variety of escape strategies, including associational resistance, distance from conspecic trees, lag time in
the herbivore colonization of young trees, phenology, and limited
access to trees as they grow. All these strategies often show biogeographical variation of patterns.
It seems that associational resistance is especially important for
seedlings which lack their own resistance or tolerance to herbivory [78]. Associational resistance occurs when highly susceptible
plants grow close to well-defended plants so as to escape from herbivory. Such plants are called nurse plants, providing physical defense
[7880] and chemical defense [81] for small and/or young plants
that obtain associational resistance from neighbors [82].
Spatial distance between individuals within species is also important for escape from herbivory. As proposed by the Janzen
Connell hypothesis [83,84], seedlings and juveniles growing close
to conspecic adults may suffer more damage from specialist herbivores than those adult trees, resulting in relatively high mortality
near adults and a decrease of herbivory and mortality with distance from conspecic adults. This pattern occurs commonly in
tropical forests. In contrast, tree species tend to have higher survival nearby conspecic adults in temperate forests because parent
trees can produce genetically variable offspring. Meanwhile compared to the adult trees, the surviving seedlings have distinct
secondary chemical components, and herbivores usually consumed only those seedlings with components similar to their parent
trees, leaving chemically differentiated seedlings to survive.
According to associational resistance and JanzenConnell hypothesis, plant species can escape from herbivory in terms of space.
Likewise, they can also do so in terms of time, such as changes in
leaf phenology. Specically, most plants can reduce their damage
from herbivores through the following three main methods: early
leaf expansion, synchronous leaf expansion, and rapid leaf expansion [85,86]. Another pattern is that in tropical forests many species
can resort to delayed greening to escape herbivores [3]. Furthermore, recent studies have demonstrated that Arabidopsis
synchronizes jasmonate-mediated defense with circadian behavior of cabbage loopers (Trichoplusia ni) to protect themselves from
herbivory [87].
4. Methodology of plant defenses against herbivores
There are numerous research approaches and techniques concerning plantherbivore relationships which deal with different
interdisciplines and is conducted at different scales. Overall, current
methodology covers the following three key issues for plant defenses against herbivores.
4.1. Molecular genetics
Plants have evolved a great number of defensive characteristics for resistance or tolerance to herbivory, due to the marked
selection pressure produced by herbivores to plants. Accordingly,
to reveal the molecular mechanisms of plant defense, traits can contribute to further understanding of the evolution of plant defense.
Ecogenomics, a new interdisciplinary approach proposed in recent
years, plays an increasingly important role in revealing molecular

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

mechanisms of plant defense traits. It integrates across disciplines

including evolutionary biology, ecology, and genetics so it can be
adopted to explain genetic and phenotypic variation in intraspecies and interspecies, and to analyze the genetic structure of plant
defense traits. Its common methods mainly include quantitative trait
loci (QTL) mapping, transcription proling, population genomics and
transgenic approaches [88].
In addition, epigentic variation, other than phenotypic variation, is an alternative important resource of plant variations because
plants can produce noticeable defensive phenotypes in different generations under the attack of herbivores or pathogens. Some chemical
modications such as DNA methylation, chemical modication of
histones and siRNA may cause transgenerational defense initiation of plants. And it has been proved that this kind of
transgenerational defense can last in many generations [89]. In view
of the fact that DNA sequence variation and epigenetic variation
covary in most natural systems, it becomes much dicult to test
the phenotypic effects of epigenetic variation of plant species. At
present, there are four testing methods: to study natural epialleles,
to manipulate DNA methylation, to study systems that naturally lack
DNA sequence variation, and to study epigenetic recombinant inbred
lines [90]. Recent epigentic research with respect to plant defense
suggests that there are three approaches adopted widely in experiment: bisulte conversion method, anity chromatography and
immunoprecipitation [89].
4.2. Chemistry and physiology
Many secondary metabolites are essential for the survival of the
plant individual [91]. Among them, tannin and jasmonic acid are
widely used in plant defense. In most cases, tannin is considered
to be one of the most important secondary metabolites in plant defenses against herbivores. Tannin is changeable in molecular
structure, and hence there are a variety of tannins in plants. Polycondensation tannin is easy to be tested, and its commom measuring
approach is spectrophotometric method. With the ability of producing a variety of hydrolyzate by hydrolysis, hydrolyzed tannin is
usually measured by the rhodanine assay, the sodium nitrite method
and the modied potassium iodate technique. And oxidized tannin
is generally measured by Forint-phenol colorimetric test [91].
Jasmonic acid also plays an important role in plant chemical defenses. It can be produced by plants attacked by herbivores, leading
to decreased photosynthetic electron transport and gas exchange,
and inducing plants to produce other secondary metabolites. In this
way, plants thereby can resist herbivores. Such methods as gas exchange, chlorophyll uorescence and thermal spatial patterns are
generally applied to test the defensive effects of jasmonic acid [92].
Recently, the reserach of Arabidopsis thaliana defenses against two
herbivores has indicated that jasmonic acid and salicylic acid pathways may well have considerable interaction effect, and its research
method is mass spectrometry [93].

329

each sampling tree, certain leaves are collected and leaf traits are
measured respectively to explain the plant defense characteristics
[51,56,96]. In this way, the interaction of plants and herbivores can
be analyzed. This method can truly reect the plant survival and
plant defense against different herbivores in the eld, but seems difcult to explain the effect of a specic herbivore on plants.
Consequently, this would limit the application of relationships
between plants and herbivores to solve ecological problems. In contrast, experimental manipulation in laboratory can make up the
shortfall in eld observation to a great extent. This method is used
to assess the anti-herbivore traits in laboratory by calculating palatability index (PI) of each plant species. Specically, this approach
is devised as follows: rst, to use insects, slugs, or other generalist
animals to make bioassay experiments; second, to measure leaf traits
of the plants; then to analyze the correlation of PI with leaf traits
[8,38,39,97]. This method is appicable to those generalist herbivores that are small in size, move slowly, with a limited range of
activity. Currently, there has been little research in which such generalists are used as tested animals in China, suggesting that the need
for making such studies is becoming much urgent.
5. Theoretical models and hypotheses concerning interactions
between plants and herbivores
The interactions between plants and herbivores are related with
plant invasion, ontogeny, dynamics and evolution of plant population and community, and therefore numerous hypotheses and
theoretical models have been proposed by a large number of researchers at different times over the past few decades (see Table 1).
Some of them seem contradictory, resulting from the various
ecosystem-types, plant communities at different successional stages
from which plant species are sampled, herbivores varying from invertebrates to vertebrates in different research papers. For example,
Xiong et al. found that a native generalist snail (Radix swinhoei)
showed preference for feeding on native aquatic plants from local
lakes [8]. On the contrary, experiments from Morrison and Hay [39]
demonstrated that local snails, as generalist herbivores, preferred
consuming exotic aquatic plants. The contradictory results can be
mainly ascribed to the fact that the tested plant species came from
totally different stages of succession, and that plants from early stage
were more susceptible to herbivory since during that time they had
not yet evolved defensive characteristics effective enough to resist
herbivores. The experiment conducted by Parker and Hay [38] is also
contrary to Xiong et al., owing probably to a different animal taxon
which was used as a generalist. In fact, they used craysh
(Procambarus spiculifer) which was a generalist herbivore, instead
of snail. Last but not least, lacking a unied theory concerning plant
defenses at present is an underlying reason, leading to miscellaneous seemingly conicting hypotheses. Indeed, every hypothesis
or theoretical model plays an important role within its own eld.
5.1. Aspects of resistance traits

4.3. Community and ecosystems

Currently, at the community and ecosystem scales, research approaches concerning the relationships of plants and herbivores are
eld observations and indoor control experiments. Field observation is one of the most ecacious methods of plant defense
researches in forest ecosystems, which has two categories, namely,
discrete random sampling and continuous xed-site observation
[22,94,95]. With the recent advance in data collection, eld observation method has improved. For example, each target tree species
can be classied into two categories: observation trees and sampling trees. For each observation tree, several randomly selected
branches are located and then herbivore damages are recorded at
xed periods through continuous observation. At the same time for

The hypotheses which can be applied to aspects of resistance

traits are the defensive mimicry hypothesis, the carbonnutrient
balance hypothesis, the oxidative stress hypothesis, the defensive
mutualisms hypothesis, the natural enemies hypothesis, the biotic
resistance hypothesis, the adaptive convergence hypothesis, the
optimal defense theory, and the induced defense theory.
The defensive mimicry hypothesis is applicable for physical resistance. It refers to the fact that some plants can eciently resist
against herbivores by mimicking the shape of animals or leaf trace
after chewing by herbivores, and by emitting carrion and dung odors
[98]. It has been almost neglected for a long time except that plant
defensive Batesian mimicry was believed to have an effect on plant
pollination based on eld observation or theoretical reason. But

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G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

Table 1
The major theories or hypotheses of interactions between plants and herbivores.
Application

Name

Literature source

Resistance defense

The defensive mimicry hypothesis

The carbonnutrient balance hypothesis
The oxidative stress hypothesis
The defensive mutualisms hypothesis
The natural enemies hypothesis
The biotic resistance hypothesis
The adaptive convergence hypothesis
The optimal defense theory
The induced defense theory
The compensatory continuum hypothesis
The limiting resource model
The JanzenConnell hypothesis
The trees and grazer satiation hypothesis
The herbivore-adaptation hypothesis
The plant-predictability hypothesis
The slow-growth-high-mortality hypothesis
The switching of defensive mechanisms during ontogeny
The escape/defense continuum hypothesis
The co-evolution hypothesis
The growth rate model
The resource availability hypothesis
The grazing optimization hypothesis
The growthdifferentiation balance hypothesis
The nutrition hypothesis

Benson et al. (1975) [98]

Bryant et al. (1983) [99]
Appel (1993) [100]
Janzen (1966) [64]
Crawley (1997) [47]
Maron and Vila (2001) [101]
Agrawal and Fishbein (2006) [48]
Feeny (1975) [102]
Agrawal (1998) [103]
Maschinski and Whitham (1989) [104]
Wise and Abrahamson (2005) [105]
Janzen (1970) [83]; Connell (1971) [84]
Silvertown (1980) [106]
Rathcke (1985) [107]
Rathcke (1985) [107]
Clancy and Price (1987) [108]
Boege et al. (2011) [49]
Kursar and Coley (2003) [24]
Ehrlich and Raven (1964) [109]
Hilbert et al. (1981) [110]
Coley et al. (1985) [9]
Williamson et al. (1989) [111]
Herms and Mattson (1992) [112]
Koyama et al. (2004) [113]

Tolerance mechanisms
Escape strategies

Others

recently, more and more evidence has indicated that plant mimicry
plays a signicant role in plant defense [57]. Studies show that
owers of plants in several orchid genera have the ability to mimic
female bees, by producing similar pheromone or pretending to be
them in appearance. Interestingly, what attracts the male bees to
pollinate is the specic chemical mimicry, rather than the ower
color or appearance polymorphism [114] which can cause the male
bees to misrecognize the deceptive owers, leading to lack of pollination [115,116]. In fact, recent studies indicate that mimicry ower
in color or shape is crucial for orchids to prevent herbivorous
mammals and insects from attacking [57].
The carbonnutrient balance hypothesis and the oxidative stress
hypothesis are applicable for chemical defense. The former means
that under the condition of high light and lower nitrogen, plant
species can invest excess carbon in plant defense if carbohydrates
are more than requirements for development. If not, plants will
reduce their defense with decreasing carbohydrates [99]. The latter
means that oxidative activation of phenolics in ecological interactions can be used to explain plant defense at the levels of individuals
and ecosystems, and that measurements of oxidative conditions can
improve predicting the activity of phenolic derivatives [100].
The defensive mutualisms hypothesis, the natural enemies hypothesis, and the biotic resistance hypothesis are applicable for
biological resistance. The defensive mutualisms hypothesis refers
to traits facilitating the visitation or colonization of mutualistic
animals that defend the plants against herbivores, such as plant food
rewards, nesting space or chemical cues that can attract herbivores natural enemies (predators and parasitoids) [64]. This is one
of the most famous indirect defenses. Seedlings and juveniles are
susceptible to herbivory because they can hardly provide extra nectar
or nesting space. Therefore, this hypothesis is probably not applicable to young plants. Instead, plants during juvenile stage will rely
mainly on direct defense [67,117]. Researchers propose different hypotheses concerning how to explain the successful invasion of exotic
plants, of which the enemy release hypothesis and the biotic resistance hypothesis are inuential and contradictory. The enemy
release hypothesis postulates that non-native plants entering novel
environments will escape their co-evolved, native enemies and that
this escape may free resources and facilitate the spread of exotic
plants [47]. The biotic resistance hypothesis contends that native

species can function as natural enemies (consumers, pathogens, competitors) of non-native invaders and suppress their establishment
and spread in the new habitat [101]. Accordingly the effects of herbivores on the invading plants may be determined by the net effect
of escaping old herbivores and obtaining new ones [39]. Upon invading a new habitat, a non-native plant will escape many specialist
herbivores from its previous habitat (enemy release), but it may also
encounter many new generalist herbivores to deter (biotic resistance). Therefore, this net effect may depend to a great extent on
the relative impact of generalist versus specialist herbivores on plant
tness [118]. Apparently, however, all these disputes seem ultimately to boil down to the question of whether generalist or
specialist herbivores have more effect on plants. If generalists play
a more signicant role, the leading mechanism is the biotic hypothesis; otherwise, it is the enemy release hypothesis.
The adaptive convergence hypothesis, the optimal defense theory,
and the induced defense theory may be involved in more than one
type of resistance traits. The adaptive convergence hypothesis means
that association with specic ecological interactions can result in
convergence on suites of covarying defensive traits. It predicts that
plant defense traits can consistently covary across species, due to
shared evolutionary ancestry or adaptive convergence [48]. According to its characteristics, this hypothesis can be applicable to the
species-rich plant communities, as well as closely related species
in different evolutionary lineages. Agrawal and Fishbein found that
three different shrub communities shared similar plant defenses with
convergence characteristic [48]. The optimal defense theory and the
induced defense theory are very important within the eld of
induced plant defense. The former means that the susceptible plant
tissues contain high constitutive defense and low induced defense
while insusceptible ones contain low constitutive defense and high
induced defense [102]. The latter means that compared to unaffected plants, the initially attacked plants by herbivores are induced
to develop new plant defense, enabling other plants to effectively
resist subsequent attacks [103].
5.2. Aspects of tolerance mechanisms
There are two theoretical model and related hypotheses concerning tolerance mechanisms due to few current researches. Firstly,

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

the compensatory continuum hypothesis refers to a continuum of

compensatory responses to vertebrate herbivory, depending on plant
competition, nutrient availability, and timing of grazing [104]. Secondly, the limiting resource model means that confronted with
consuming of herbivores, plant species will have seven pathways
to three potential outcomes: greater tolerance, equal tolerance, or
lower tolerance in low- vs high-resource environments [105].
5.3. Aspects of escape strategies
The hypotheses which can be applied to aspects of escape strategies are the JanzenConnell hypothesis, the trees and grazer
satiation hypothesis, the herbivore-adaptation hypothesis, the plantpredictability hypothesis, and the slow-growth-high-mortality
hypothesis. The JanzenConnell hypothesis means that seedlings
and juveniles growing near conspecic adults receive high loads of
specialist herbivores from nearby adult trees, leading to relatively
high mortality near adults [83,84]. This hypothesis indicates that
plant species can escape from herbivory in terms of space. The trees
and grazer satiation hypothesis means that all trees of one species
within a region can produce large crops of seeds at odd intervals
mast years and that seed predators cannot respond fast enough
reproductively, so many seeds survive and sprout [106].
Thereafter Rathcke proposed the herbivore-adaptation hypothesis and the plant-predictability hypothesis [107]. The former means
that from the herbivores point of view, herbivores should evolve
to consume the most available (i.e., most predictable) plants in their
environments. In other words, predictable plants should be the most
acceptable to herbivores. The latter means that from the plants point
of view, the most predictable plants should have the greatest risk
of herbivory and have evolved the most effective defenses. That is,
predictable plants should be the least acceptable to herbivores. Additionally, according to the slow-growth-high-mortality hypothesis,
plant species can escape herbivores by prolonging development in
herbivorous insects, which results in greater exposure to natural
enemies such as predators or parasites and a subsequent increase
in mortality [108].
5.4. Other respects
The switching of defensive mechanisms during ontogeny is associated with resistance defense, tolerance mechanisms, and escape
strategies. Plant species can switch from one defensive strategy to
another as they develop under a variety of environmental conditions, or individuals of the same species in different environments
can take distinct plant defense strategies [49]. Take arbores for
example; from seeds to adult trees, plants have undergone tremendous change in morphological and physiological features. As a rule,
during seed or seedling stage plant resources mainly rely on endosperm or cotyledons, and at that time plants can hardly allocate
energy to develop defensive characteristics. Therefore, as explained above, it seems likely that trees can be defended through
associational resistance, a certain distance away from the same individuals, production of secondary metabolites or early leaf
expansion as seedlings, and then switch from escape to secondary
chemistry, physical defenses or tolerance later in development [119].
With the development of seedlings, plants will achieve dominant
position by giving priority to investment in the rapid growth of the
individuals. At this moment, plants may well resort to tolerance
mechanisms. For example, plants then will increase the rate of photosynthesis or activate dormant meristems if their leaves are
damaged by herbivores. In fact, when seedlings then become juveniles and mature trees, switches between tolerance and chemical
defense are also likely to occur, driven by the risk of attack and resource allocation tradeoffs between growth and defense [120,121].
It is found that the level of secondary metabolites probably de-

331

crease with individual age [53]. When plants reach adulthood,

accumulated plant resource becomes abundant enough to enable
plants to invest more energy in physical defensive characteristics,
such as enhancing leaf toughness, offering extraoral nectar or
nesting space to attract herbivores natural enemies. Thus plants
defend themselves against herbivores through various direct and
indirect defense mechanisms [67,68], depending on different ontogeny. Plants in different habitats can also switch from one defensive
strategy to another, or change their resource allocation. For instance, the indirect defense of adult plants with canopies was
different from counterparts without canopies. Under the cover of
canopies the predators of herbivores were much fewer than those
without canopies [67], leading plant individuals with canopies to
invest more resources in defensive measures. The studies by Cates
[122] demonstrated that Asarum caudatum would invest more energy
in defense, otherwise it would invest in growth and reproduction.
When entering a new habitat, plant species would allocate more
resources to develop morphological structure and synthesize chemical composition relative to the consumption of generalist herbivores
[123].
The escape/defense continuum hypothesis is associated with plant
escape and defense. Plant species may take two extreme kinds of
defensive mechanisms: at one extreme are species with a defense
strategy, and at the other extreme are escape species. Actually, most
species fall along an escape/defense continuum in the eld [24].
The co-evolution hypothesis is associated with plant evolution. It refers to such an evolution of two or more species in which
the evolutionary changes of each species inuence the evolution
of the other species [109].
Besides those stated above, there are some other hypotheses proposed to explain the relationship between plant growth and defense,
including the growth rate model, the resource availability hypothesis, the grazing optimization hypothesis, and the growth
differentiation balance hypothesis. The growth rate model means
that under certain conditions plant growth rate, especially for
aboveground biomass, increases with an increase in grazing intensity; under other conditions, very large increases in relative growth
rate after grazing can occur but the biomass may not increase, or
even less than that of ungrazed plants [110]. The resource availability hypothesis refers to cause and effect between intrinsic growth
rate and plant defense characteristics against herbivores. When the
resource is limited, plants with low growth rate will allocate more
energy to resist herbivores than those with high growth rate [9].
The grazing optimization hypothesis suggests that the grazing intensity within a reasonable range will incite plants to enhance their
net productivity [111]. The growthdifferentiation balance hypothesis holds that plants have to make a tradeoff between growing fast
and defending herbivores and pathogens eciently because they
are confronted with the dilemma: to grow or defend during their
development [112].
The nutrition hypothesis can be used to explain the formation
of aphid galls. Koyama et al. reported that some aphid species
induced leaf galls, which had to accumulate high concentrations of
amino acids and provide the aphids with sucient nutrients. So
those aphids would have survival advantage over the counterparts consuming leaves [113].
6. Current issues and problems of plant defense in China
Researches of plantherbivore relationships abroad are fulledged relatively to counterparts in China. The studies abroad cover
diversied plant defensive characteristics, involving numerous herbivores applied in bioassay experiment and a wide variety of
ecosystem types in the eld. Qin [124] discussed insectplant
interactions and their co-evolution in his famous book The Relationship between Insects and Plants, which can be recognized as a

332

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

18
16

SCI

Number of reviews

CNKI
14
12
10
8
6
4
2
0
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Year
Fig. 3. The comparison of review number from domestic and international mainstream ecology journals concerning plantherbivore interactions.

milestone, causing a signicant impact in China. Hereafter one after

another herbivory research cases popped out, including the relation of interaction between insects and plants to evolution [125,126];
anti-herbivore defenses of young leaves in tropical forests [54];
leaves positive effect and their defensive mechanism under the stress
of phytophagous insects [127]; effects of plant on insect diversity
[128]; feeding level of folivorous insects in forest canopy [129]; interactions between herbivores and plant diversity in grassland
ecosystem [130]; new discovery about plant defense: plantplant
communication [131]. Based on comparing the reviews at home and
abroad concerning plant defense published in mainstream ecological journals during the past ten years, it is noted that there are much
fewer papers in China than those abroad, in several years lacking
reviews at home (Fig. 3). Consequently, this suggests that related
researches should be strengthened in China.
6.1. Categories of herbivores
In most cases, recently there have been few herbivorous species
used in plant defense researches at home except phytophagous
mammals like cows [132], grazing sheep [133,134] and goats [135]
from grassland ecosystem or Radix swinhoei from aquatic ecosystem [8]. The vast majority of studies in this area have concentrated
on insect-eating patterns, herbivory intensity and dynamics
[2,10,94,96,136138], and most of them have focused on forest ecosystem, rather than other ecosystems. In addition, Zhu et al. reported
the effects of large herbivore grazing on meadow steppe plant and
insect diversity [139].
6.2. Plant defense strategies
Studies concerning plant defense strategies focus on forest ecosystems in China. In tropical areas, Cai and Cao [54] reviewed the
advances in anti-herbivore defenses of tropical forest plants. In frigid
zone, Deng [140] reported the effects of volatile chemical substances on needles of Pinus massoniana seedlings. However, the
majority of plant defense studies are conducted in the subtropical
forests. Liu et al. found that there existed effects of early-season herbivory on leaf traits of Schima superba and subsequent insect attack
in Mt. Meihua, southern China. Sun et al. found out a direct relationship between herbivory and leaf expansion of Castanopsis fargesii
from evergreen broad-leaved forest in Tiantong National Forest Park
of Zhejiang, China [86]. Liu et al. compared leaf mass per area, photosynthetic capacity and chemical defense traits of four evergreen

broad-leaved tree species under different light conditions, and demonstrated that there was a tradeoff between physical and chemical
defense strategies [51]. Liu et al. found that there was a correlation between leang phenology and leaf traits of woody species of
evergreen broad-leaved forests in subtropical China, suggesting that
plants with different leaf size probably took different defense measures against herbivores [141]. Xia et al. found that leaf herbivory
damage differed between the rst and second sets of shoots in ve
evergreen woody species from Tiantong National Forest Park of Zhejiang, China [142].
Just as stated above, it is obvious that most studies are related
to resistance defense and escape strategies. As far as the contents
are concerned, physical and chemical defenses are the main issues
in these studies of resistance defense; leaf phenological escape is
the main issue in these studies of escape strategies. Actually, there
is little research concerned with tolerance mechanisms, biotic resistance pertaining to the category of resistance defense, and other
escape strategies except leaf phenology.
6.3. Research approaches
It seems that no study of plant defense at the genetic level has
been reported in China so far. But at the chemical and physiological levels, such approaches of measuring leaf tannin or total phenolic
content are widely used to analyze plant defense strategies [51,143].
Main approaches at the community and ecosystem levels are eld
observation of leaf damage by herbivory, coupled with measuring
leaf traits at laboratory [51,86,96,136,141]. Nevertheless, herbivory experiment indoors is particularly few besides the study made
by Xiong et al. in which Radix swinhoei was cultured as generalist
herbivore [8]. Therefore, herbivory experiment indoors and study
of plant defense at the genetic level are extremely insucient in
China, suggesting that we should make efforts to adopt laboratory
techniques in molecular biology in future research of plant defense.
6.4. Theoretical models and hypotheses
Scholars abroad have proposed a number of theoretical models
and hypotheses concerning the relationships of plants and herbivores over the past few decades, facilitating the development in this
eld. Until recently, China has begun research on this area. Most
of the scanty studies at home are carried out to test one or two of
the hypotheses above. For example, the result of experiment performed by Xiong et al. supported the natural enemies hypothesis

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325336

[8]. It remains unclear whether those models and hypotheses are

applicable to Chinese situations where there are various ecosystem types with rich species diversity. Accordingly, the lack of
theoretical progress in relationships of plants and herbivores may
restrict in-depth understanding of plant defense mechanisms. Therefore, it is necessary to carry out theoretical research in this area.
In summary, it seems likely that current herbivory studies in
China are characterized by much few herbivorous animals used in
experiment, only little and poor means and technique, and the lack
of original theoretical models and hypotheses. All of them will constrain the development of herbivory research in China. In addition,
other characteristics are as follows: current researches focus on herbivory from forest or grassland ecosystem, few from other
ecosystems; herbivory researches focus on species in tree and shrub
layers, few in herb layer; these researches focus on the plant
insect and plantmammal relationships, few on the other
relationships. Therefore, the relationships between plants and herbivores in China should be strengthened in the future.
7. Research prospects
Considerable progress about plantherbivore relationships have
been made in China in the past decades. However, there still exists
a big gap in this respect between China and the developed countries in the world. For example, compared with other countries, it
is much later for China to conduct researches concerning interactions of plants and herbivores. Based on the current research status,
we recommend that future researches should be focused on the following aspects:
(1) Selections for experimental herbivores should be diversied. Different herbivores have different effect on plant species.
In general, vertebrates have an important role in maintaining the biodiversity of grassland, insects can increase plant
community richness by feeding on dominant species to reduce
their productivity, and mollusks may signicantly affect the
species richness of herb layer [14]. In view of the fact that
current researches are mainly focused on plantmammal or
plantinsect relationships in China with a high plant and
animal species diversity, therefore we highly recommend that
coming researches of plantmollusk and plantcrustacean relationships should be stimulated in the future.
(2) Experimental manipulation and eld observation should be
combined in practice. Many environmental factors may inuence plant tness in the wild. Actually, most current
researches are conducted by sampling for one time rather than
continuous observation, so we suggest that it is of importance to make continuous observation in a xed site to reect
the consuming dynamics of herbivores in realty. Besides,
efforts should be made to nd out the mechanisms of certain
herbivores to plants. The big advantage of experimental manipulation in laboratory is that it can make up the shortfall
in eld observation of interaction between herbivores and
plants. In the present use, eld observation is one of the few
research approaches for plantherbivore relationship in China;
in contrast the lack of experimental manipulation may seriously affect the related researches of plant defense
mechanisms against herbivores. Therefore, a trend in plant
defensive mechanisms seems likely to combine experimental manipulation with eld observation in China.
(3) Researches of plantherbivore relationships across different
ecosystems should be encouraged in China where there are
diversied ecosystem types with rich ora and fauna, especially for herbivore types and plant species. However, current
researches of plantherbivore relationships only focus on those
species from forest or grassland ecosystem, so we should

333

strengthen interactions of species from water ecosystem and

other systems. In addition, due to human-induced ecosystem perturbations it is worthy to carry out the studies on
how the relationships between plants and herbivores alter
under the man-made treatments and in unaffected nature
within the same ecosystem.
(4) Future researches should also be encouraged to assess the herbivory in the scenario of global climate change. Human
activities are severely changing the composition and function of ecosystems at the global level [144]. For example,
climate warming and increased atmospheric nitrogen deposition may exert strong bottom-up effects on primary
producers and ecosystems; moreover, it probably depends on
herbivores that respond differently to these changes [145].
Thus, there is an urgent requirement to improve our understanding of the herbivory under climate change.
(5) More attention should be paid to plant roots during the studies
of interactions between plants and herbivores. Currently, our
knowledge about the interaction mostly comes from
aboveground herbivory (AGH), rather than the below ground
herbivory (BGH) which has long been neglected in the past
decades. Actually, recent study shows that belowground herbivores have substantial damage to the roots by signicantly
impacting overall plant tness. Furthermore, roots play a signicant role in defending against aboveground herbivory.
Roots can be used as useful organ not only to store the toxic
substances, but also photoassimilates, enabling plants to tolerate the herbivory. In addition, the interaction between roots
and rhizosphere microorganisms can also affect plant
herbivore relationships [146]. Therefore, a better
understanding of the contribution of roots to aboveground
herbivory will shed light on the mechanisms by which plants
and herbivores interact intertwiningly.
Acknowledgements
This study was supported by the Project for National Basic Science
Personnel Training Fund (J1103507 and J1210025), Priority Academic Program Development of Jiangsu Higher Education Institutions
(PAPD), and State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) (No:
083111). We are also grateful to Professor Rodolfo Dirzo for kindly
providing us with some useful articles, and in particular to Professor Sun Shucun for critically reviewing the abstract.
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Note: Reviews of SCI are searched from database Web of Science

(WoS) (from 2000 to 2013), with topic words herbivore * plant
defense * review in English. Reviews at home are searched from
database CNKI (Chinese National Knowledge Infrastructure) (from
2000 to 2013), with key words plant defense and herbivory in
Chinese.