Interactions between plants and herbivores: A review of plant defense

Acta Ecologica Sinica 34 (2014) 325–336

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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 Plant–animal interaction Resistant Tolerance Escape strategies

A B S T R A C T

Ecologists have long ignored or underestimated the importance of plant–herbivore interactions owing to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briefly 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 classified 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 influential 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 plant–herbivore interactions in China, and discussed the perspectives of studies on plant–herbivore 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 flows 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 significant 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: [email protected] (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 field 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 briefly discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores from an ecological point of view, classified 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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methodology for studying plant defenses against herbivores. Numerous theoretical models and hypotheses, which are influential 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 plant–herbivore interactions in China, and then discussed the perspectives of studies on plant–herbivore interactions to provide a theoretical basis for our future research. 2. Categories of herbivores 2.1. According to zoological classification criteria According to zoological classification 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 [12–14]. 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 [15–20]. Most mammals and mollusks feed on plant seedlings while insects do great damage to adult plants in the field. 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 [22–24], but also for ecosystem nutrient cycling and energy flow [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 influence 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 [31–33]. 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 crayfishes, are distributed widely in the field. Nowadays, most of them have been applied as generalist herbivores during bioassay experiment to elucidate the relationship between aquatic herbivores and plants [8,37–39].

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, crayfishes (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 fitness 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 Herbivore’s preference for plants

Specialist herbivores (Oligophagous and monophagous)

Generalist herbivores Fig. 1. Categories of herbivores.

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325–336

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 significantly lower than those in temperate forest [45]. 3. Plant defense strategies In general, herbivores have negative impacts on plant fitness [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 classification 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 modifications 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 flowers, which are able to mimic bees or wasps to deter large herbivorous mammals and insects [57]. However, such kinds of flower traits may positively or negatively influence foraging preferences of pollinators to a great extent. For instance, root herbivory might positively influence pollinator behavior; nevertheless, herbivore damage to leaves and flowers might negatively affect foraging preferences of pollinators [58]. 3.1.2. Chemical resistance traits Chemical resistance traits refer to physiological modifications that plant species make when attacked by herbivores [50], which chiefly 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 flowers 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

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Associational resistance and Janzen-Connell hypothesis, etc.

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

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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 plant–ant mutualisms. In this case, the myrmecophytic plants provide nesting space for ants, and sometimes offer extrafloral nectar or nutritious food [63]. In return, ants protect host plants from herbivores [64–67]. 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 first 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 significantly 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 significantly 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 defined as the capacity of plants to reduce the negative effects of damage on fitness [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 [74–76]. 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 efficiency, activating dormant meristems, making use of reserved resource, changing resource allocation mode, etc. Generally, seedlings that experience significant reductions in growth following herbivory are unable to compensate for lost tissues. Later on as juveniles develop from seedlings to saplings, they can show significant 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 fitness, 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 efficiency, 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 conspecific 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 [78–80] 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 conspecific 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 conspecific adults. This pattern occurs commonly in tropical forests. In contrast, tree species tend to have higher survival nearby conspecific 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 Janzen–Connell 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. Specifically, 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 plant–herbivore 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

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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 profiling, 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 modifications such as DNA methylation, chemical modification 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 difficult 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: bisulfite conversion method, affinity 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 modified 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 fluorescence 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].

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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 reflect the plant survival and plant defense against different herbivores in the field, but seems difficult to explain the effect of a specific 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 field 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. Specifically, this approach is devised as follows: first, 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 crayfish (Procambarus spiculifer) which was a generalist herbivore, instead of snail. Last but not least, lacking a unified theory concerning plant defenses at present is an underlying reason, leading to miscellaneous seemingly conflicting hypotheses. Indeed, every hypothesis or theoretical model plays an important role within its own field. 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 field observations and indoor control experiments. Field observation is one of the most efficacious methods of plant defense researches in forest ecosystems, which has two categories, namely, discrete random sampling and continuous fixed-site observation [22,94,95]. With the recent advance in data collection, field observation method has improved. For example, each target tree species can be classified 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 fixed 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 carbon–nutrient 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 efficiently 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 field observation or theoretical reason. But

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

Name

Literature source

Resistance defense

The defensive mimicry hypothesis The carbon–nutrient 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 Janzen–Connell 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 growth–differentiation 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 significant role in plant defense [57]. Studies show that flowers 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 specific chemical mimicry, rather than the flower color or appearance polymorphism [114] which can cause the male bees to misrecognize the deceptive flowers, leading to lack of pollination [115,116]. In fact, recent studies indicate that mimicry flower in color or shape is crucial for orchids to prevent herbivorous mammals and insects from attacking [57]. The carbon–nutrient 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 influential 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 fitness [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 significant 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 specific 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 field 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,

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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 Janzen–Connell hypothesis, the trees and grazer satiation hypothesis, the herbivore-adaptation hypothesis, the plantpredictability hypothesis, and the slow-growth-high-mortality hypothesis. The Janzen–Connell hypothesis means that seedlings and juveniles growing near conspecific 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 herbivore’s 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 plant’s 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-

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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 extrafloral 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 field [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 influence 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 growth–differentiation balance hypothesis holds that plants have to make a tradeoff between growing fast and defending herbivores and pathogens efficiently 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 sufficient 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 plant–herbivore relationships abroad are fullfledged relatively to counterparts in China. The studies abroad cover diversified plant defensive characteristics, involving numerous herbivores applied in bioassay experiment and a wide variety of ecosystem types in the field. Qin [124] discussed insect–plant interactions and their co-evolution in his famous book The Relationship between Insects and Plants, which can be recognized as a

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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 plant–herbivore interactions.

milestone, causing a significant 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: plant–plant 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 [2,10,94,96,136–138], 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 leafing 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 first and second sets of shoots in five 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 field 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 insufficient 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 field. 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

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[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 plant–mammal 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 plant–herbivore 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 diversified. 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 significantly affect the species richness of herb layer [14]. In view of the fact that current researches are mainly focused on plant–mammal or plant–insect relationships in China with a high plant and animal species diversity, therefore we highly recommend that coming researches of plant–mollusk and plant–crustacean relationships should be stimulated in the future. (2) Experimental manipulation and field observation should be combined in practice. Many environmental factors may influence plant fitness 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 fixed site to reflect the consuming dynamics of herbivores in realty. Besides, efforts should be made to find 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 field observation of interaction between herbivores and plants. In the present use, field observation is one of the few research approaches for plant–herbivore 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 field observation in China. (3) Researches of plant–herbivore relationships across different ecosystems should be encouraged in China where there are diversified ecosystem types with rich flora and fauna, especially for herbivore types and plant species. However, current researches of plant–herbivore relationships only focus on those species from forest or grassland ecosystem, so we should

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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 significantly impacting overall plant fitness. Furthermore, roots play a significant 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. References [1] M.T.J. Johnson, Evolutionary ecology of plant defences against herbivores, Funct. Ecol. 25 (2) (2011) 305–311. [2] Z.G. Liu, Y.L. Cai, K. Li, L. Yang, C. Sun, Insect herbivory patterns on leaves of Castanopsis fargesii during leaf expansion in evergreen broad-leaved forest in eastern China, Chin. J. Plant Ecol. 33 (5) (2009) 919–925. [3] P.D. Coley, J.A. Barone, Herbivory and plant defenses in tropical forests, Annu. Rev. Ecol. Syst. 27 (1) (1996) 305–335. [4] A.A. Agrawal, Current trends in the evolutionary ecology of plant defence, Funct. Ecol. 25 (2) (2011) 421–433. [5] N. Huntly, Herbivores and the dynamics of communities and ecosystems, Annu. Rev. Ecol. Syst. 22 (1) (1991) 477–503. [6] J. Cebrian, Role of first-order consumers in ecosystem carbon flow, Ecol. Lett. 7 (3) (2004) 232–240. [7] J.E. Houlahan, C.S. Findlay, Effect of invasive plant species on temperate wetland plant diversity, Conserv. Biol. 18 (4) (2004) 1132–1138. [8] W. Xiong, D. Yu, Q. Wang, C.H. Liu, L.G. Wang, A snail prefers native over exotic freshwater plants: implications for the enemy release hypotheses, Freshw. Biol. 53 (11) (2008) 2256–2263. [9] P.D. Coley, J.P. Bryant III, F.S. Chapin, Resource availability and plant antiherbivore defense, Science 230 (4728) (1985) 895–899. [10] H. Jiang, Y.L. Cai, K. Li, H. Wang, L. Wang, Intensity and patterns of leaf area eaten of Lithocarpus glaber by insects, at Tiantong Forest Park, Zhejiang, Chin. J. Ecol. 24 (9) (2005) 989–993.

334

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325–336

[11] E.C. Oerke, H.W. Dehne, Safeguarding production-losses in major crops and the role of crop protection, Crop Prot. 23 (4) (2004) 275–285. [12] S.J. McNaughton, M. Oesterheld, D.A. Frank, K.J. Williams, Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats, Nature 341 (6238) (1989) 142–144. [13] S.L. Collins, A.K. Knapp, J.M. Briggs, J.M. Blair, E.M. Steinauer, Modulation of diversity by grazing and mowing in native tallgrass prairie, Science 280 (5364) (1998) 745–747. [14] E. Allan, M.J. Crawley, Contrasting effects of insect and molluscan herbivores on plant diversity in a long-term field experiment, Ecol. Lett. 14 (12) (2011) 1246–1253. [15] H. McBrien, R. Harmsen, A. Crowder, A case of insect grazing affecting plant succession, Ecology 64 (5) (1983) 1035–1039. [16] P.J. Edwards, M.P. Gillman, Herbivores and plant succession, in: A.J. Gray, M.J. Crawley, P.J. Edwards (Eds.), Colonization, Succession and Stability, The 26th Symposium of the British Ecological Society Held with the Linnean Society of London, Blackwell Scientific Publications, Oxford, 1987, pp. 295– 314. [17] C.W.D. Gibson, V.K. Brown, M. Jepson, Relationships between the effects of insect herbivory and sheep grazing on seasonal changes in an early successional plant community, Oecologia 71 (2) (1987) 245–253. [18] V.K. Brown, A.C. Gange, Differential effects of above- and below-ground insect herbivory during early plant succession, Oikos 54 (1) (1989) 67–76. [19] V.K. Brown, A.C. Gange, Secondary plant succession: how is it modified by insect herbivory? Vegetatio 101 (1) (1992) 3–13. [20] M.E. Hanley, M. Fenner, P.J. Edwards, An experimental field study of the effects of mollusc grazing on seedling recruitment and survival in grassland, J. Ecol. 83 (4) (1995) 621–627. [21] D.C. Allen, J.E. Coufal, Introduction to Forest Entomology: A Training Manual for Forest Technicians, Syracuse University Press, Syracuse, 1984. [22] P.D. Coley, Herbivory and defensive characteristics of tree species in a lowland tropical forest, Ecol. Monogr. 53 (2) (1983) 209–233. [23] S.E. Hartley, T.H. Jones, Plant diversity and insect herbivores: effects of environmental change in contrasting model systems, Oikos 101 (1) (2003) 6–17. [24] T.A. Kursar, P.D. Coley, Convergence in defense syndromes of young leaves in tropical rainforests, Biochem. Syst. Ecol. 31 (8) (2003) 929–949. [25] C.M. Herrera, O. Pellmyr, Plant Animal Interactions: An Evolutionary Approach, Wiley, Oxford, 2002. [26] H. Buschmann, M. Keller, N. Porret, H. Dietz, P.J. Edwards, The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland, Funct. Ecol. 19 (2) (2005) 291–298. [27] C.M.G. Duthoit, Slugs and food preferences, Plant Pathol. 13 (2) (1964) 73–78. [28] M. Fenner, M.E. Hanley, R. Lawrence, Comparison of seedling and adult palatability in annual and perennial plants, Funct. Ecol. 13 (4) (1999) 546–551. [29] R. Dirzo, J.L. Harper, Experimental studies on slug-plant interactions. II. The effect of grazing by slugs on high density monocultures of Capsella bursapastoris and Poa annua, J. Ecol. 68 (3) (1980) 999–1011. [30] M.J. Crawley, Insect herbivores and plant population dynamics, Annu. Rev. Entomol. 34 (1) (1989) 531–564. [31] P.E. Hulme, Seedling herbivory in grassland: relative impact of vertebrate and invertebrate herbivores, J. Ecol. 82 (4) (1994) 873–880. [32] P.E. Hulme, Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory, J. Ecol. 84 (1) (1996) 43–51. [33] U. Scheidel, H. Bruelheide, Effects of slug herbivory on the seedling establishment of two montane Asteraceae species, Flora 200 (4) (2005) 309–320. [34] D.M. Lodge, Herbivory on freshwater macrophytes, Aquat. Bot. 41 (1–3) (1991) 195–224. [35] M. Søndergaard, L. Bruun, T. Lauridsen, E. Jeppensen, T.V. Madsen, The impact of grazing waterfowl on submerged macrophytes: in situ experiments in a shallow eutrophic lake, Aquat. Bot. 53 (1–2) (1996) 73–84. [36] E. van Donk, Switches between clear and turbid water states in a biomanipulated lake (1986 – 1996): the role of herbivory on macrophytes, in: E. Jeppensen, M. Sondergaard, M. Sondergaard, K. Christoffersen (Eds.), The Structuring Role of Macrophytes in Lakes, Springer-Verlag, New York, 1998, pp. 290–297. [37] G. Cronin, D.M. Lodge, M.E. Hay, M. Miller, M.A. Hill, T. Horvath, et al., Crayfish feeding preferences for freshwater macrophytes: the influence of plant structure and chemistry, J. Crustacean Biol. 22 (4) (2002) 708–718. [38] D.J. Parker, E.M. Hay, Biotic resistance to plant invasions? Native herbivores prefer non-native plants, Ecol. Lett. 8 (9) (2005) 959–967. [39] W.E. Morrison, M.E. Hay, Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve, PLoS ONE 6 (3) (2011) e17227. [40] W.G. Abrahamson, Plant-animal Interactions, McGraw-Hill Inc, New York, 1989, pp. 123–162. [41] A.A. Agrawal, P.M. Kotanen, C.E. Mitchell, A.G. Power, W. Godsoe, J. Klironomos, Enemy release? An experiment with congeneric plant pairs and diverse aboveand belowground enemies, Ecology 86 (11) (2005) 2979–2989. [42] J.D. Parker, D.E. Burkepile, M.E. Hay, Opposing effects of native and exotic herbivores on plant invasions, Science 311 (5766) (2006) 1459–1461. [43] T.S. Zhang, Insect Diversity in Subtropical Evergreen Broad-leaved Forests [PDR], East China Normal University, Shanghai, 2008.

[44] Y. Basset, Palatability of tree foliage to chewing insects: a comparison between a temperate and a tropical site, Acta Oecologica 15 (1994) 181–191. [45] P.D. Coley, T.M. Aide, Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests, in: P.W. Price, T.M. Lewinsohn, G.W. Fernandes, W.W. Benson (Eds.), Plant-animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, Wiley & Sons, New York, 1991, pp. 25–49. [46] J.L. Harper, Population Biology of Plants, The Blackburn Press, Caldwell, 2010. [47] M.J. Crawley, Plant-herbivore dynamics, in: M.J. Crawley (Ed.), Plant Ecology, 2nd ed., Blackwell Science, Cambridge, 1997, pp. 401–475. [48] A.A. Agrawal, M. Fishbein, Plant defense syndromes, Ecology 87 (2006) S132–S149. [49] K. Boege, K.E. Barton, R. Dirzo, Influence of tree ontogeny on plant-herbivore interactions, in: F.C. Meinzer, B. Lachenbruch, T.E. Dawson (Eds.), Size- and Age-related Changes in Tree Structure and Function, Tree Physiology 4, Springer Science and Business Media, Berlin, 2011, pp. 193–214. [50] J.H. Gowda, Physical and chemical response of juvenile Acacia tortilis trees to browsing: experimental evidence, Funct. Ecol. 11 (1) (1997) 106–111. [51] F.J. Liu, S. Xiang, X.C. Yang, S.C. Sun, Comparison of leaf mass per area, photosynthetic capacity and chemical defense traits of four evergreen broad-leaved tree species under contrasting light conditions, Chin. J. Appl. Environ. Biol. 16 (4) (2010) 462–467. [52] C.H. Lusk, P.B. Reich, R.A. Montgomery, D.D. Ackerly, J. Cavender-Bares, Why are evergreen leaves so contrary about shade? Trends Ecol. Evol. 23 (6) (2008) 299–303. [53] B.L. Webber, I.E. Woodrow, Chemical and physical plant defence across multiple ontogenetic stages in a tropical rain forest understorey tree, J. Ecol. 97 (4) (2009) 761–771. [54] Z.Q. Cai, K.F. Cao, Advances in the studies on anti-herbivore defenses of tropical forest plant young leaves, Guihaia 22 (5) (2002) 474–480. [55] P.V.A. Fine, I. Mesones, P.D. Coley, Herbivores promote habitat specialization by trees in Amazonian forests, Science 305 (5684) (2004) 663– 665. [56] E.G. Pringle, R.I. Adams, E. Broadbent, P.E. Busby, C.I. Donatti, E.L. Kurten, et al., Distinct leaf-trait syndromes of evergreen and deciduous trees in a seasonally dry tropical forest, Biotropica 43 (3) (2011) 299–308. [57] S. Lev-Yadun, G. Ne’eman, Does bee or wasp mimicry by orchid flowers also deter herbivores? Arthropod Plant Interact. 6 (3) (2012) 327–332. [58] D. Lucas-Barbosa, J.J.A. van Loon, R. Gols, T.A. van Beek, M. Dicke, Reproductive escape: annual plant responds to butterfly eggs by accelerating seed production, Funct. Ecol. 27 (1) (2013) 245–254. [59] V. De Luca, B. St Pierre, The cell and developmental biology of alkaloid biosynthesis, Trends Plant Sci. 5 (4) (2000) 168–173. [60] M.S. Chen, Inducible direct plant defense against insect herbivores: a review, Insect Sci. 15 (2) (2008) 101–114. [61] L. Kang, The chemical defenses of plants on phytophagous insects, Chin. Bull. Bot. 12 (4) (1995) 22–27. [62] S. Lev-Yadun, G. Ne’eman, U. Shanas, A sheep in wolf’s clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores? Bioessays 31 (1) (2009) 84–88. [63] B. Fiala, U. Maschwitz, Food bodies and their significance for obligate antassociation in the tree genus Macaranga (Euphorbiaceae), Bot. J. Linn. Soc. 110 (1) (1992) 61–75. [64] D.H. Janzen, Coevolution of mutualism between ants and acacias in Central America, Evolution 20 (3) (1966) 249–275. [65] E.W. Schupp, Azteca protection of Cecropia: ant occupation benefits juvenile trees, Oecologia 70 (3) (1986) 379–385. [66] B. Fiala, H. Grunsky, U. Mashwitz, K.E. Linsenmair, Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association, Oecologia 97 (2) (1994) 186–192. [67] M. Heil, D. McKey, Protective ant-plant interactions as model systems in ecological and evolutionary research, Annu. Rev. Ecol. Syst. 34 (2003) 425–453. [68] E. Narbona, R. Dirzo, A reassessment of the function of floral nectar in Croton suberosus (Euphorbiaceae): a reward for plant defenders and pollinators, Am. J. Bot. 97 (4) (2010) 672–679. [69] S.A. van Bael, J.D. Brawn, S.K. Robinson, Birds defend trees from herbivores in a neotropical forest canopy, Proc. Natl Acad. Sci. U.S.A. 100 (14) (2003) 8304–8307. [70] K. Boege, R.J. Marquis, Plant quality and predation risk mediated by plant ontogeny: consequences for herbivores and plants, Oikos 115 (3) (2006) 559–572. [71] K. Boege, Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture, Oecologia 143 (1) (2005) 117–125. [72] J. Fornoni, Ecological and evolutionary implications of plant tolerance to herbivory, Funct. Ecol. 25 (2) (2011) 399–407. [73] R.H. Painter, Resistance of plants to insects, Annu. Rev. Entomol. 3 (1958) 367–390. [74] J. Fornoni, P.L. Valverde, J. Nuñez-Farfán, Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium, Evolution 58 (8) (2004) 1696–1704. [75] R. Leimu, J. Koricheva, A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies, Oikos 112 (1) (2006) 1–9.

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325–336

[76] K. Boege, R. Dirzo, D. Siemens, P. Brown, Ontogenetic switches from plant resistance to tolerance: minimizing costs with age?, Ecol. Lett. 10 (3) (2007) 177–187. [77] P. Tiffin, Mechanisms of tolerance to herbivore damage: what do we know? Evol. Ecol. 14 (4–6) (2000) 523–536. [78] C. Vandenberghe, C. Smit, M. Pohl, A. Buttler, F. Freléchoux, Does the strength of facilitation by nurse shrubs depend on grazing resistance of tree saplings? Basic Appl. Ecol. 10 (5) (2009) 427–436. [79] O. Rousset, J. Lepart, Positive and negative interactions at different life stages of a colonizing species (Quercus humilis), J. Ecol. 88 (3) (2000) 407–412. [80] E. Baraza, R. Zamora, J.A. Hódar, Conditional outcomes in plant-herbivore interactions: neighbours matter, Oikos 113 (1) (2006) 148–156. [81] C. Smit, J.D. Ouden, H. Müller-Schärer, Unpalatable plants facilitate tree sapling survival in wooded pastures, J. Appl. Ecol. 3 (2) (2006) 305–312. [82] W.A. Niering, R.H. Whittaker, C.H. Lowe, The saguaro: a population in relation to environment, Science 142 (3588) (1963) 15–23. [83] D.H. Janzen, Herbivores and the number of tree species in tropical forests, Am. Nat. 104 (940) (1970) 501–527. [84] J.H. Connell, On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees, in: P.J.D. Boer, G.R. Gradwell (Eds.), Dynamics of Populations, Centre for Agricultural Publication and Documentation, Wageningen, 1971, pp. 298–312. [85] T.M. Aide, Patterns of leaf development and herbivory in a tropical understory community, Ecology 74 (2) (1993) 455–466. [86] C. Sun, Y.L. Cai, Z.G. Liu, L. Yang, Leaf growth of Castanopsis fargesii in evergreen broad-leaved forest in Tiantong National Forest Park of Zhejiang, China, J. Ecol. Rural Environ. 26 (3) (2010) 215–219. [87] D. Goodspeed, E.W. Chehab, A. Min-Venditti, J. Braam, M.F. Covington, Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior, Proc. Natl Acad. Sci. U.S.A. 109 (12) (2012) 4674–4677. [88] J.T. Anderson, T. Mitchell-Old, Ecological genetics and genomics of plant defences: evidence and approaches, Funct. Ecol. 25 (2) (2011) 312–324. [89] L.M. Holeski, G. Jander, A.A. Agrawal, Transgenerational defense induction and epigenetic inheritance in plants, Trends Ecol. Evol. 27 (11) (2012) 618–626. [90] Y.Y. Zhang, M. Fischer, V. Colot, O. Bossdorf, Epigenetic variation creates potential for evolution of plant phenotypic plasticity, New Phytol. 197 (11) (2013) 314–322. [91] J.P. Salminen, M. Karonen, Chemical ecology of tannins and other phenolics: we need a change in approach, Funct. Ecol. 25 (2) (2011) 325–338. [92] P.D. Nabity, J.A. Zavala, E.H. DeLucia, Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata, J. Exp. Bot. 64 (2) (2013) 685–694. [93] P.J. Zhang, C. Broekgaarden, S.J. Zheng, T.A.L. Snoeren, J.J.A. van Loon, R. Gols, et al., Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana, New Phytol. 197 (4) (2013) 1291–1299. [94] Z. Zheng, X.D. Chen, H.W. Mao, Q. Zheng, F. Yun, Leaf growth and herbivory dynamics of saplings in tropical seasonal rainforest gaps in Xishuangbanna, Acta Phytoecologica Sin. 25 (6) (2001) 679–686. [95] L.R. Fox, P.A. Morrow, Estimates of damage by herbivorous insects on Eucalyptus trees, Aust. J. Ecol. 8 (2) (1983) 139–147. [96] Z.G. Liu, Y.L. Cai, K. Li, C. Sun, Herbivory in relation to leaf development during leaf expansion in Rhododendron latoucheae (Ericaceae), Ecol. Environ. Sci. 18 (4) (2009) 1443–1448. [97] R. Dirzo, Experimental studies on slug-plant interactions: I. The acceptability of thirty plant species to the slug Agriolimax caruaneae, J. Ecol. 68 (1980) 981–998. [98] W.W. Benson, K.S. Brown, L.E. Gilbert, Co-evolution of plants and herbivores: passion flower butterflies, Evolution 29 (4) (1975) 659–680. [99] J.P. Bryant III, F.S. Chapin, D.R. Klein, Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory, Oikos 40 (3) (1983) 357–368. [100] H.M. Appel, Phenolics in ecological interactions: the importance of oxidation, J. Chem. Ecol. 19 (7) (1993) 1521–1552. [101] J.L. Maron, M. Vila, When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses, Oikos 95 (3) (2001) 361–373. [102] P. Feeny, Biochemical coevolution between plants and their insect herbivores, in: L.E. Gilbert, P.H. Raven (Eds.), Coevolution of Animals and Plants, University of Texas Press, Austin, 1975, pp. 3–19. [103] A.A. Agrawal, Induced responses to herbivory and increased plant performance, Science 279 (5354) (1998) 1201–1202. [104] J. Maschinski, T.G. Whitham, The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing, Am. Nat. 134 (1) (1989) 1–19. [105] M.J. Wise, W.G. Abrahamson, Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory, Oikos 109 (3) (2005) 417–428. [106] J.W. Silvertown, The evolutionary ecology of mast seeding in trees, Biol. J. Linn. Soc. 14 (2) (1980) 235–250. [107] B. Rathcke, Slugs as generalist herbivores: tests of three hypotheses on plant choices, Ecology 66 (3) (1985) 828–836. [108] K.M. Clancy, P.W. Price, Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox, Ecology 68 (3) (1987) 733–737. [109] P.R. Ehrlich, P.H. Raven, Butterflies and plants: a study in coevolution, Evolution 18 (4) (1964) 586–608.

335

[110] D.W. Hilbert, D.M. Swift, J.K. Detling, M.I. Dyer, Relative growth rates and the grazing optimization hypothesis, Oecologia 51 (1) (1981) 14–18. [111] S.C. Williamson, J.K. Detling, J.L. Dodd, M.I. Dyer, Experimental evaluation of the grazing optimization hypothesis, J. Range Manage. 42 (2) (1989) 149–152. [112] D.A. Herms, W.J. Mattson, The dilemma of plants: to grow or defend, Q. Rev. Biol. 67 (3) (1992) 283–335. [113] Y. Koyama, I. Yao, S. Akimoto, Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation, Entomol. Exp. Appl. 113 (1) (2004) 35–44. [114] N.J. Vereecken, F.P. Schiestl, On the roles of colour and scent in a specialized floral mimicry system, Ann. Bot. (Lond) 104 (6) (2009) 1077–1084. [115] F.P. Schiestl, On the success of a swindle: pollination by deception in orchids, Naturwissenschaften 92 (6) (2005) 255–264. [116] A.C. Gaskett, M.E. Herberstein, Colour mimicry and sexual deception by Tongue orchids (Cryptostylis), Naturwissenschaften 97 (1) (2010) 97–102. [117] E. del-Val, R. Dirzo, Does ontogeny cause changes in the defensive strategies of the myrmecophyte Cecropia peltata? Plant Ecol. 169 (1) (2003) 35–41. [118] K.J.F. Verhoeven, A. Biere, J.A. Harvey, W.H. van der Putten, Plant invaders and their novel natural enemies: who is naïve? Ecol. Lett. 12 (2) (2009) 107–117. [119] K. Seiwa, Changes in leaf phenology are dependent on tree height in Acer mono, a deciduous broad-leaved tree, Ann. Bot. (Lond) 83 (4) (1999) 355–631. [120] H. Nykänen, J. Koricheva, Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis, Oikos 104 (2) (2004) 247–268. [121] J.A. Hódar, R. Zamora, J. Castro, J.M. Gómez, D. García, Biomass allocation and growth responses of Scots pine saplings to simulated herbivory depend on plant age and light availability, Plant Ecol. 197 (2) (2008) 229–238. [122] R.G. Cates, The interface between slugs and wild ginger: some evolutionary aspects, Ecology 56 (2) (1975) 391–400. [123] J. Hitchmough, M. Wagner, Slug grazing effects on seedling and adult life stages of North American Prairie plants used in designed urban landscapes, Urban Ecosyst. 14 (2) (2011) 279–302. [124] J.D. Qin, The Relationship between Insects and Plants: Insect-Plant Interactions and Their Coevolution, Science Press, Beijing, 1987. [125] J.D. Qin, C.Z. Wang, The relation of interaction between insects and plants to evolution, Acta Entomol. Sin. 44 (3) (2001) 360–365. [126] D.L. Wang, Progress in the coadaptation and coevolution between plants and herbivores, Acta Ecol. Sin. 24 (11) (2004) 2641–2648. [127] Y. Gao, K. Li, T. Tian, Leaves’ positive effect and their defensive mechanism under the stress of phytophagous insects, Chin. J. Appl. Environ. Biol. 10 (4) (2004) 512–514. [128] H. Zhu, Y.Y. Peng, D.L. Wang, Effects of plant on insect diversity, Chinese J. Ecol. 27 (12) (2008) 2215–2221. [129] X.W. Wang, L.Z. Ji, X.G. Wang, L.L. An, L.B. Yan, Feeding level of folivorous insects in forest canopy: quantitative methods and research advances, Chin. J. Ecol. 30 (7) (2011) 1403–1410. [130] D.L. Wang, L. Wang, Interactions between herbivores and plant diversity (review), Acta Agrestia Sin. 19 (4) (2011) 699–704. [131] S.F. Zhang, Z. Zhang, H.B. Wang, X.B. Kong, New discovery about plant defense: plant-plant communication, Chin. J. Plant Ecol. 36 (10) (2012) 1120–1124. [132] D.L. Wang, The response characteristics of grassland vegetation structure to grazing intensities with cows, J. Northeast Norm. Univ. (Natural Science Edition) 33 (3) (2001) 73–79. [133] J.S. Liu, L. Wang, D.L. Wang, S.P. Bonser, F. Sun, Y.F. Zhou, et al., Plants can benefit from herbivory: stimulatory effects of sheep saliva on growth of Leymus chinensis, PLoS ONE 7 (1) (2012) e29259. [134] Y. Huang, L. Wang, D.L. Wang, Y.X. Li, D.G. Alves, The effect of plant spatial pattern within a patch on foraging selectivity of grazing sheep, Landsc. Ecol. 27 (6) (2012) 911–919. [135] X. Wang, D.L. Wang, Y. Liu, L. Ba, W. Sun, B.T. Zhang, Intake mass and diet selection for grazing goats on Leymus chinensis grassland, Acta Ecol. Sin. 22 (5) (2002) 662–667. [136] X.D. Yu, Z.H. Zhou, T.H. Luo, Patterns of damage by phytophagous insects on leaves of Quercus liaotungensis, Acta Phytoecologica Sinica 25 (5) (2001) 553–560. [137] H.W. Wang, Y.L. Cai, K. Li, H. Jiang, Y.P. Tian, Insect herbivory patterns on leaves of 11 plant species in the evergreen broad-leaved forests of Tiantong National Forest Park, Zhejiang, Biodivers. Sci. 14 (2) (2006) 145–151. [138] X.D. Fan, Y.S. Ji, J.J. Ling, Y.J. Gu, Intensity and patterns of Castanopsis sclerophylla leaf eaten by insects, at Qiandao Lake, Zhejiang, J. Ecol. Rural Environ. 23 (4) (2007) 1–5. [139] H. Zhu, D.L. Wang, L. Wang, Y.G. Bai, J. Fang, J. Liu, The effects of large herbivore grazing on meadow steppe plant and insect diversity, J. Appl. Ecol. 49 (5) (2012) 1075–1083. [140] W.H. Deng, Y.B. Shen, Z.Y. Li, X.N. Jiang, Effects of insect-damaged, MeJA and terpenes treatment on the induction of phenolic acids in needles of Pinus massoniana seedlings, J. Beijing For. Univ. 32 (1) (2010) 39–43. [141] Z.G. Liu, K. Li, Y.L. Cai, Y. Fang, Correlations between leafing phenology and traits: woody species of evergreen broad-leaved forests in subtropical China, Pol. J. Ecol. 59 (3) (2011) 463–473. [142] Y.J. Xia, J.Q. Tang, G.F. Zhang, C. Huang, F.Q. Meng, S.C. Sun, First and second sets of shoots in five evergreen woody species from Tiantong National Forest Park of Zhejiang, China, Chin. J. Plant Ecol. 37 (3) (2013) 220–229.

336

G. Bin, Z. Guangfu/Acta Ecologica Sinica 34 (2014) 325–336

[143] Z.G. Liu, Y.L. Cai, Y. Fang, J. Jing, K. Li, Induced response in Schima superba: effects of early-season herbivory on leaf traits and subsequent insect attack, Afr. J. Biotechnol. 9 (51) (2010) 8731–8738. [144] N. Eisenhauer, S. Cesarz, R. Koller, K. Worm, P.B. Reich, Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity, Glob. Change Biol. 18 (2) (2012) 435–447. [145] E.R.D. Moise, H.A.L. Henry, Interactions of herbivore exclusion with warming and N addition in a grass-dominated temperate old field, Oecologia 169 (4) (2012) 1127–1136. [146] V.J. Nalam, J. Shah, P. Nachappa, Emerging role of roots in plant responses to aboveground insect herbivory, Insect Sci. 20 (3) (2013) 286–296.

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.