气候变化对作物矿质元素利用率影响研究进展

作物矿质元素利用率对气候变化的响应是目前全球变化研究中既重要、又复杂,且认知最少的科学领域。这个科学问题的研究关系到解密或预测陆地植物及农作物矿质胁迫对全球气候变化响应的机理,为将来农业投入提供理论依据,是应对气候变化的当务之急。目前只有少数研究,通过模拟试验,探索性地开展了CO_2浓度或温度升高的环境条件下,矿质元素在土壤-植物系统迁移、分布和储存特征的研究。从相关的文献报道来看,CO_2浓度升高环境条件下,小麦和水稻作物籽粒中大量和痕量元素的富集水平一般呈下降趋势。但温度升高情况下,作物各器官对对矿质元素的吸收情况则更为复杂。正由于气候因素与植物矿质元素利用率之间关系的复杂性,在气候变化背景下,解密作物矿质胁迫对全球气候变化响应的科学问题,尚需改进试验方法、手段,从土壤性质、作物生态生理,以及农业生态系统中矿质元素在土壤-作物系统中迁移转化的过程,全面考察作物矿质元素利用率对气候变化的响应机理。     

Responses of seagrass to anthropogenic and natural disturbances do not equally translate to its consumers

Coastal communities are under threat from many and often co‐occurring local (e.g., pollution, eutrophication) and global stressors (e.g., climate change), yet understanding the interactive and cumulative impacts of multiple stressors in ecosystem function is far from being accomplished. Ecological redundancy may be key for ecosystem resilience, but there are still many gaps in our understanding of interspecific differences within a functional group, particularly regarding response diversity, that is, whether members of a functional group respond equally or differently to anthropogenic stressors. Herbivores are critical in determining plant community structure and the transfer of energy up the food web. Human disturbances may alter the ecological role of herbivory by modifying the defense strategies of plants and thus the feeding patterns and performance of herbivores. We conducted a suite of experiments to examine the independent and interactive effects of anthropogenic (nutrient and CO₂ additions) and natural (simulated herbivory) disturbances on a seagrass and its interaction with two common generalist consumers to understand how multiple disturbances can impact both a foundation species and a key ecological function (herbivory) and to assess the potential existence of response diversity to anthropogenic and natural changes in these systems. While all three disturbances modified seagrass defense traits, there were contrasting responses of herbivores to such plant changes. Both CO₂ and nutrient additions influenced herbivore feeding behavior, yet while sea urchins preferred nutrient‐enriched seagrass tissue (regardless of other experimental treatments), isopods were deterred by these same plant tissues. In contrast, carbon enrichment deterred sea urchins and attracted isopods, while simulated herbivory only influenced isopod feeding choice. These contrasting responses of herbivores to disturbance‐induced changes in seagrass help to better understand the ecological functioning of seagrass ecosystems in the face of human disturbances and may have important implications regarding the resilience and conservation of these threatened ecosystems.     

On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds

Species comparisons are a cornerstone of biology and there is a long tradition of using the comparative framework to study the ecology and evolution of plant defensive traits. Early comparative studies led to the hypothesis that plant chemistry plays a central role in plant defence, and the evolution of plant secondary chemistry in response to insect herbivory remains a classic example of coevolution. However, recent comparative work has disagreed with this paradigm, reporting little connection between plant secondary chemicals and herbivory across distantly related plant taxa. One conclusion of this new work is that the importance of secondary chemistry in plant defence may have been generally overstated in earlier research. Here, we attempt to reconcile these contradicting viewpoints on the role of plant chemistry in defence by critically evaluating the use and interpretation of species correlations as a means to study defence–herbivory relationships. We conclude that the notion that plant primary metabolites (e.g. leaf nitrogen content) are the principal determinants of herbivory (or the target of natural selection by herbivores) is not likely to be correct. Despite the inference of recent community‐wide studies of herbivory, strong evidence remains for a prime role of secondary compounds in plant defence against herbivores.     

Sources of variation in plant responses to belowground insect herbivory: a meta-analysis

Growing interest in belowground herbivory and the remarkable diversity of the accumulated information on this topic inspired us to quantitatively explore the variation in the outcomes of individual studies. We conducted a meta-analysis of 85 experimental studies reporting the effects of root-feeding insect herbivores (36 species) on plants (75 species). On average, belowground herbivory led to a 36.3% loss of root biomass, which was accompanied by a reduction in aboveground growth (-16.3%), photosynthesis (-11.7%) and reproduction (-15.5%). The effects of root herbivory on aboveground plant characteristics were significant in agricultural and biological control studies, but not in studies of natural systems. Experiments conducted in controlled environments yielded larger effects on plants than field experiments, and infestation experiments resulted in more severe effects than removal studies employing natural levels of herbivory. Simulated root herbivory led to greater aboveground growth reductions than similar root loss imposed by insect feeding. External root chewers caused stronger detrimental effects than sap feeders or root borers; specialist herbivores imposed milder adverse effects on plants than generalists. Woody plants suffered from root herbivory more than herbaceous plants, although root loss was similar in these two groups. Evergreen woody plants responded to root herbivory more strongly than deciduous woody plants, and grasses suffered from root herbivory more than herbs. Environmental factors such as drought, poor nutrient supply, among-plant competition, and aboveground herbivory increased the adverse effects of root damage on plants in an additive manner. In general, plant tolerance to root herbivores is lower than tolerance to defoliating aboveground herbivores.     

Interactions between above- and belowground insect herbivores as mediated by the plant defense system

Plants are frequently attacked by both above- and belowground arthropod herbivores. Nevertheless, studies rarely consider root and shoot herbivory in conjunction. Here we provide evidence that the root-feeding insect Agriotes lineatus reduces the performance of the foliage feeding insect Spodoptera exigua on cotton plants. In a bioassay, S. exigua larvae were allowed to feed on either undamaged plants, or on plants that had previously been exposed to root herbivory, foliar herbivory, or a combination of both. Previous root herbivory reduced the relative growth rates as well as the food consumption of S. exigua by more than 50% in comparison to larvae feeding on the undamaged controls. We found no effects in the opposite direction, as aboveground herbivory by S. exigua did not affect the relative growth rates of root-feeding A. lineatus . Remarkably, neither did the treatment with foliar herbivory affect the food consumption and relative growth rate of S. exigua in the bioassay. However, this treatment did result in a significant change in the distribution of S. exigua feeding. Plants that had been pre-exposed to foliar herbivory suffered significantly less damage on their young terminal leaves. While plant growth and foliar nitrogen levels were not affected by any of the treatments, we did find significant differences between treatments with respect to the level and distribution of plant defensive chemicals (terpenoids). Exposure to root herbivores resulted in an increase in terpenoid levels in both roots as well as in mature and immature foliage. Foliar damage, on the other hand, resulted in high terpenoid levels in young, terminal leaves only. Our results show that root-feeding herbivores may change the level and distribution of plant defenses aboveground. Our data suggest that the reported interactions between below- and aboveground insect herbivores are mediated by induced changes in plant secondary chemistry.     

Climate change disproportionately increases herbivore over plant or parasitoid biomass

All living organisms are linked through trophic relationships with resources and consumers, the balance of which determines overall ecosystem stability and functioning. Ecological research has identified a multitude of mechanisms that contribute to this balance, but ecologists are now challenged with predicting responses to global environmental changes. Despite a wealth of studies highlighting likely outcomes for specific mechanisms and subsets of a system (e.g., plants, plant-herbivore or predator-prey interactions), studies comparing overall effects of changes at multiple trophic levels are rare. We used a combination of experiments in a grassland system to test how biomass at the plant, herbivore and natural enemy (parasitoid) levels responds to the interactive effects of two key global change drivers: warming and nitrogen deposition. We found that higher temperatures and elevated nitrogen generated a multitrophic community that was increasingly dominated by herbivores. Moreover, we found synergistic effects of the drivers on biomass, which differed across trophic levels. Both absolute and relative biomass of herbivores increased disproportionately to that of plants and, in particular, parasitoids, which did not show any significant response to the treatments. Reduced parasitism rates mirrored the profound biomass changes in the system. These findings carry important implications for the response of biota to environmental changes; reduced top-down regulation is likely to coincide with an increase in herbivory, which in turn is likely to cascade to other fundamental ecosystem processes. Our findings also provide multitrophic data to support the general concern of increasing herbivore pest outbreaks in a warmer world.     

Induced responses in three tropical dry forest plant species – direct and indirect effects on herbivory

Induced changes in plant quality are hypothesized to reduce herbivore numbers and subsequent damage to the plant. The resultant decrease in herbivory may be due to direct negative impacts on herbivores, through the reduction in foliage quality as food, or due to indirect effects of plant-induced traits interacting with the third trophic level, increasing predation and parasitism rates on herbivores. The relative importance of induced responses as direct and/or indirect defenses has not been evaluated in natural systems. Moreover, few studies have evaluated the influence of early-season damage on late-season herbivory in natural systems, particularly in the tropics. The presence of induced responses and subsequent impact on folivory as a consequence of early-season damage were evaluated in three plant species ( Croton pseudoniveus , Bursera instabilis and Piper stipulaceum ) in a tropical dry forest in Mexico. A two-factorial experiment was applied to determine if induced responses influenced subsequent herbivory directly, by reducing foliage quality, or indirectly, through their interaction with parasitoids and predatory arthropods. Plants from all three species with reduced early-season damage had higher herbivory rates through the rest of the growing season, compared to plants that were damaged during leaf expansion. Chemical analyses showed that early-season damage induced the production of total phenolics and condensed tannins for C. pseudoniveus and B. instabilis , respectively. The mechanism by which these compounds affected subsequent herbivory was most likely by directly reducing foliage quality as food for herbivores, given that predatory arthropods and parasitoids had no effects on herbivory in this study. I conclude that early-season damage in these three species influenced later-season herbivory through the induction of plant responses that may act to reduce plant quality as food for herbivores.     

Above‐ and belowground insect herbivores mediate the impact of nitrogen eutrophication on the soil food web in a grassland ecosystem

Insect herbivores are important drivers of ecosystem processes in grasslands, and can mediate the grassland's response to environmental change. For example, recent evidence shows that above‐ and belowground herbivory, individually and in combination, can modify how a plant community responds to nitrogen (N) eutrophication, an important driver of global change. However, knowledge about how such effects extend to the associated soil food web is lacking. In a mesocosm experiment, we investigated how communities of soil nematodes – an abundant and functionally important group of soil organisms – responded to above‐ and belowground insect herbivory at contrasting N levels. We found that the strongest influence of above‐ and belowground herbivory on the nematode community appeared at elevated N. The abundance of root‐feeding nematodes increased when either above‐ or belowground insect herbivores were present at elevated N, but when applied together the two herbivore types cancelled out one another's effect. Additionally, at elevated N aboveground herbivory increased the abundance of fungal‐feeders relative to bacterial‐feeders, which indicates changes in decomposition pathways induced by N and herbivory. Belowground herbivory increased the abundance of omnivorous nematodes. The shifts in both the herbivorous and detrital parts of the soil food web demonstrate that above‐ and belowground herbivory does not only mediate the response of the plant community to N eutrophication, but in extension also the soil food web sustained by the plant community. We conclude that feedbacks between effects of above‐ and belowground herbivory mediate the response of the grassland ecosystem to N eutrophication.     

Tracking sucking herbivory with nitrogen isotope labelling: Lessons from an individual trait-based approach

Response and effect traits help to understand how changes in ecological communities (e.g. in response to land use) relate to changes in ecosystem functioning. In grasslands, plants and insect herbivores are involved in many ecosystem processes such as herbivory and plant biomass production. Simultaneous changes in the trait composition of both plants and herbivores should affect herbivory rates, with consequences for plant growth and potentially biomass production. The mechanisms underlying these links are little understood for grasses and sucking insects, which build a major part of grassland communities. In a mesocosm experiment, we manipulated the composition of grasses and sucking herbivores (Hemiptera) to study the role of plant traits, herbivore traits and their interaction on herbivory and plant growth. Because sucking herbivory is generally difficult to quantify, we developed a novel experimental setting, in which we labelled plants with ¹⁵N isotope. This allowed to quantify ¹⁵N uptake and thus sucking rates of individuals. We found that herbivory and simultaneous plant growth reduction are most strongly linked to herbivore species identity. Unexpectedly, herbivory did not increase with herbivore size, but was highest for small species and for thin-bodied Heteroptera. Additionally, herbivory and plant growth reduction depended on the interacting herbivore and plant species, indicating trait matching, which could, however, not be explained with commonly used traits. This indicates that mechanisms linking ecological communities and ecosystem processes are highly context-specific. To understand how global change affects ecosystem functioning, studies need to cover all functionally relevant groups, including plant sap suckers.     

Invertebrate herbivory along a gradient of plant species diversity in extensively managed grasslands

Increasing plant diversity has long been hypothesized to negatively affect levels of invertebrate herbivory due to a lower number of specialist insect herbivores in more diverse sites, but studies of natural systems have been rare. We used a planned comparison to study herbivory in a set of 19 semi-natural montane grasslands managed as hay meadows. Herbivory was measured in transects through the plant communities, and in individuals of Plantago lanceolata and Trifolium pratense that were transplanted into each meadow. In addition, plant community biomass and arthropod abundances were determined in the grasslands. Before the first mowing in June, mean herbivory levels correlated negatively with plant species richness, as predicted by theory, but they were also significantly affected by plant community biomass and plant community composition. After mowing, herbivory levels were only significantly related to plant community composition. Damage levels in the transplants were lower than herbivory levels in the established plant communities. Most insect herbivores were generalists and not specialists. The number of insect herbivores and spiders were positively correlated and tended to increase with increasing plant species richness. Herbivory levels were correlated negatively with spider abundances. We conclude that while the predicted negative relationship between plant species richness and insect herbivory can be found in grasslands, the underlying mechanism involves generalist rather than specialist herbivores. Our data also suggest a role of natural enemies in generalist herbivore activities.Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .     

Warming the tundra: reciprocal responses of invertebrate herbivores and plants

Rapid warming in northern ecosystems is simultaneously influencing plants, herbivores and the interactions among them. Recent studies suggest that herbivory could buffer plant responses to environmental change, but this has only been shown for vertebrate herbivores so far. The role of invertebrate herbivory in tundra ecosystems is often overlooked, but can be relevant in determining the structure and dynamics of tundra plant communities and may also affect how plants respond to warming. Invertebrate herbivores are also likely to respond more rapidly to warming than vertebrates because their behaviour and life cycles strongly depend on temperature. We investigated the effects of current season warming on Arctic moth caterpillars, their herbivory rates, and the subsequent responses of two common tundra plants, Salix arctica and Dryas octopetala. We manipulated both herbivore presence and temperature in a full‐factorial field experiment at two elevations, using enclosures and passive warming chambers. Changes in temperature achieved through elevation and/or experimental warming directly affected caterpillars, herbivory and the responses of plants. Caterpillars performed worse (higher respiration rates and lower growth rates) in warmer, lower elevation plots and shifted their diets towards more nutritious foods, such that the relative intensity of herbivory changed for the two studied plants. Within‐season responses of both forage plant species were weak, but invertebrate herbivores affected the responses of plants to elevation or experimental warming. Our results suggest that increased temperatures can reduce the performance of cold‐adapted invertebrate herbivores, with potential consequences to the longer term responses of tundra plants to warming due to changes in herbivory rates and selective foraging.     

Plant diversity and insect herbivores: effects of environmental change in contrasting model systems

There is increasing concern over the potential impact of anthropogenic factors (e.g. increasing nutrient inputs, global climate change) on the rate of loss of diversity in ecosystems. Such losses may affect ecosystem processes. In addition, a change in diversity of one group of organisms may influence the diversity of species of the next trophic level. We examined the extent to which plant species richness influences that of insect herbivores in two systems: a long‐term field experiment on heather moorland and a model community in the Ecotron controlled environment facility. We examined the response of these two plant communities to environmental change, specifically increased levels of nutrients, grazing and atmospheric CO₂. We measured the indirect effects of changes in these factors on insect herbivores, both above‐ and below‐ground. In the moorland system, grazing was the largest influence on plant community structure. The community was dominated by one species, Calluna vulgaris, and loss of cover under heavy grazing allowed competing species to invade. However, grazing regime was not a major influence on the species richness of the insect herbivore community. Site was more important: there were a greater number of Hemiptera species on sites with more mineral soils than on peat sites, possibly because a greater variety of grass and herb species was present on the former sites. In the Ecotron, below‐ground factors were also important drivers of community change: elevated CO₂ increased carbon availability in the soil and there were simultaneous changes in the community composition of soil biota. Above‐ground, some plant species increased in abundance and others decreased, leading to interaction‐specific effects on the insect herbivores. In two very different studies of the effects of environmental change on the interactions between plants and their herbivores, several similar conclusions can be drawn: (1) effects are likely to be site‐ and interaction‐specific; (2) outcomes are likely to be strongly dependent on the initial state and the dominant species of the plant community; and (3) indirect effects, often mediated by below‐ground factors, may have a bigger influence on insect‐plant interactions than more direct effects of above‐ground factors.     

Community structure and abundance of insects in response to early‐season aphid infestation in wild cabbage populations

1. Changes in the arthropod community structure can be attributed to differences in constitutively expressed plant traits or those that change depending on environmental conditions such as herbivory. Early‐season herbivory may have community‐wide effects on successive insect colonisation of host plants and the identity of the initially inducing insect may determine the direction and strength of the effects on the dynamics and composition of the associated insect community. 2. Previous studies have addressed the effect of early infestation with a chewing herbivore. In the present study, the effect of early infestation was investigated with a phloem‐feeding aphid [Brevicoryne brassicae L. (Hemiptera, Aphididae)] on the insect community associated with three wild cabbage (Brassica oleracea L.) populations, which are known to differ in defence chemistry, throughout the season in field experiments. 3. Aphid infestation had asymmetric effects on the associated insect community and only influenced the abundance of the natural enemies of aphids, but not that of chewing herbivores and their natural enemies. The effect size of aphid infestation further depended on the cabbage population. 4. Aphid feeding has been previously reported to promote host‐plant quality for chewing herbivores, which has been attributed to antagonism between the two major defence signalling pathways controlled by the hormones salicylic acid (SA) and jasmonic acid (JA), respectively. Our results show no effects of early infestation by aphids on chewing herbivores, suggesting the absence of long‐term JA–SA antagonism. 5. Investigating the effects of the identity of an early‐season coloniser and genotypic variation among plant populations on insect community dynamics are important in understanding insect–plant community ecology.     

Carbon storage in terrestrial ecosystems: do browsing and grazing herbivores matter?

Large mammalian herbivores manifest a strong top‐down control on ecosystems that can transform entire landscapes, but their impacts have not been reviewed in the context of terrestrial carbon storage. Here, we evaluate the effects of plant biomass consumption by large mammalian herbivores (>10 kg adult biomass), and the responses of ecosystems to these herbivores, on carbon stocks in temperate and tropical regions, and the Arctic. We calculate the difference in carbon stocks resulting from herbivore exclusion using the results of 108 studies from 52 vegetation types. Our estimates suggest that herbivores can reduce terrestrial above‐ and below‐ground carbon stocks across vegetation types but reductions in carbon stocks may approach zero given sufficient periods of time for systems to respond to herbivory (i.e. decades). We estimate that if all large herbivores were removed from the vegetation types sampled in our review, increases in terrestrial carbon stocks would be up to three orders of magnitude less than many of the natural and human‐influenced sources of carbon emissions. However, we lack estimates for the effects of herbivores on below‐ground biomass and soil carbon levels in many regions, including those with high herbivore densities, and upwards revisions of our estimates may be necessary. Our results provide a starting point for a discussion on the magnitude of the effects of herbivory on the global carbon cycle, particularly given that large herbivores are common in many ecosystems. We suggest that herbivore removal might represent an important strategy towards increasing terrestrial carbon stocks at local and regional scales within specific vegetation types, since humans influence populations of most large mammals.     

Insect herbivory and ontogeny: How do growth and development influence feeding behaviour,morphology and host use?

Herbivorous insects exploit many different plants and plant parts and often adopt different feeding strategies throughout their life cycle. The conceptual framework for investigating insect–plant interactions relies heavily on explanations invoking plant chemistry, neglecting a suite of competing and interacting pressures that may also limit herbivory. In the present paper, the methods by which ontogeny, feeding strategies and morphological characters inhibit herbivory by mandibulate holometabolous insects are examined. The emphasis on mechanical disruption of plant cells in the insect digestive strategy changes the relative importance of plant ‘defences’, increasing the importance of leaf structure in inhibiting herbivory. Coupled with the implications of substantial morphological and behavioural changes in ontogeny, herbivores adopt a range of approaches to herbivory that are independent of plant chemistry alone. Many insect herbivores exhibit substantial ontogenetic character displacement in mandibular morphology. This is tightly correlated with changes in feeding strategy, with changes to the cutting edges of mandibles increasing the efficiency of feeding. The changes in feeding strategy are also characterized by changes in feeding behaviour, with many larvae feeding gregariously in early instars. Non‐nutritive hypotheses considering the importance of natural enemies, shelter‐building and thermoregulation may also be invoked to explain the ontogenetic consequences of changes to feeding behaviour. There is a need to integrate these factors into a framework considering the gamut of potential explanations of insect herbivory, recognizing that ontogenetic constraints are not only viable explanations but a logical starting point. The interrelations between ontogeny, size, morphology and behaviour highlight the complexity of insect–plant relationships. Given the many methods used by insect herbivores to overcome the challenges of consuming foliage, the need for species‐specific and stage‐ specific research investigating ontogeny and host use by insect herbivores is critical for developing general theories of insect–plant interactions.     

Elevated carbon dioxide concentrations indirectly affect plant fitness by altering plant tolerance to herbivory

Global environmental changes, such as rising atmospheric CO₂ concentrations, have a wide range of direct effects on plant physiology, growth, and fecundity. These environmental changes also can affect plants indirectly by altering interactions with other species. Therefore, the effects of global changes on a particular species may depend on the presence and abundance of other community members. We experimentally manipulated atmospheric CO₂ concentration and amounts of herbivore damage (natural insect folivory and clipping to simulate browsing) to examine: (1) how herbivores mediate the effects of elevated CO₂ (eCO₂) on the growth and fitness of Arabidopsis thaliana; and (2) how predicted changes in CO₂ concentration affect plant resistance to herbivores, which influences the amount of damage plants receive, and plant tolerance of herbivory, or the fitness consequences of damage. We found no evidence that CO₂ altered resistance, but plants grown in eCO₂ were less tolerant of herbivory—clipping reduced aboveground biomass and fruit production by 13 and 22%, respectively, when plants were reared under eCO₂, but plants fully compensated for clipping in ambient CO₂ (aCO₂) environments. Costs of tolerance in the form of reduced fitness of undamaged plants were detected in eCO₂ but not aCO₂ environments. Increased costs could reduce selection on tolerance in eCO₂ environments, potentially resulting in even larger fitness effects of clipping in predicted future eCO₂ conditions. Thus, environmental perturbations can indirectly affect both the ecology and evolution of plant populations by altering both the intensity of species interactions as well as the fitness consequences of those interactions.     

Herbivory and plant resource competition: a review of two interacting interactions

This review discusses the prevalence and potential for interactive effects between herbivory and competition on plant growth and biomass, and it is apparent that such effects typically arise when there is a mismatch between the spatial scale of herbivore behaviour (food or patch choice) and the spatial heterogeneity of the plant community. Historically, such interactive effects have been examined using two approaches. Studies using the first approach have excluded plant neighbors and herbivores in a factorial experiment, and scored effects on plant biomass. Studies using the second approach have observed herbivore abundance or herbivory on plants with or without plant neighbors, and have identified a large number of mechanisms underlying such interactive effects. The two types of studies have produced somewhat conflicting results, where interactive effects have been commonly observed in studies using the second approach and only rarely in studies using the first approach. This is most likely a consequence of a biased choice of study systems, where studies using the first approach have primarily studied mammalian herbivory while studies using the second approach have been more focussed on insect herbivory. Moreover, studies using the first approach have typically been very small-scale manipulations and this probably precludes most possible interactive effects in systems with mammalian herbivory. This points to the fact that studies examining interactive effects of herbivory and plant competition should more carefully consider the behaviour and life history of herbivores included in the study prior to the design of removal experiments.     

Does Plant Origin Influence the Fitness Impact of Flower Damage? A Meta-Analysis

Herbivory has been long considered an important component of plant-animal interactions that influences the success of invasive species in novel habitats. One of the most important hypotheses linking herbivory and invasion processes is the enemy-release hypothesis, in which exotic plants are hypothesized to suffer less herbivory and fitness-costs in their novel ranges as they leave behind their enemies in the original range. Most evidence, however, comes from studies on leaf herbivory, and the importance of flower herbivory for the invasion process remains largely unknown. Here we present the results of a meta-analysis of the impact of flower herbivory on plant reproductive success, using as moderators the type of damage caused by floral herbivores and the residence status of the plant species. We found 51 papers that fulfilled our criteria. We also included 60 records from unpublished data of the laboratory, gathering a total of 143 case studies. The effects of florivory and nectar robbing were both negative on plant fitness. The methodology employed in studies of flower herbivory influenced substantially the outcome of flower damage. Experiments using natural herbivory imposed a higher fitness cost than simulated herbivory, such as clipping and petal removal, indicating that studies using artificial herbivory as surrogates of natural herbivory underestimate the real fitness impact of flower herbivory. Although the fitness cost of floral herbivory was high both in native and exotic plant species, floral herbivores had a three-fold stronger fitness impact on exotic than native plants, contravening a critical element of the enemy-release hypothesis. Our results suggest a critical but largely unrecognized role of floral herbivores in preventing the spread of introduced species into newly colonized areas.     

Responses of insect herbivores and herbivory to habitat fragmentation: a hierarchical meta‐analysis

Loss and fragmentation of natural habitats can lead to alterations of plant–animal interactions and ecosystems functioning. Insect herbivory, an important antagonistic interaction is expected to be influenced by habitat fragmentation through direct negative effects on herbivore community richness and indirect positive effects due to losses of natural enemies. Plant community changes with habitat fragmentation added to the indirect effects but with little predictable impact. Here, we evaluated habitat fragmentation effects on both herbivory and herbivore diversity, using novel hierarchical meta‐analyses. Across 89 studies, we found a negative effect of habitat fragmentation on abundance and species richness of herbivores, but only a non‐significant trend on herbivory. Reduced area and increased isolation of remaining fragments yielded the strongest effect on abundance and species richness, while specialist herbivores were the most vulnerable to habitat fragmentation. These fragmentation effects were more pronounced in studies with large spatial extent. The strong reduction in herbivore diversity, but not herbivory, indicates how important common generalist species can be in maintaining herbivory as a major ecosystem process.     

A quantitative evaluation of major plant defense hypotheses, nature versus nurture, and chemistry versus ants

Variation in plant secondary metabolite content can arise due to environmental and genetic variables. Because these metabolites are important in modifying a plant’s interaction with the environment, many studies have examined patterns of variation in plant secondary metabolites. Investigations of chemical defenses are often linked to questions about the efficacies of plant defenses and hypotheses on their evolution in different plant guilds. We performed a series of meta-analyses to examine the importance of environmental and genetic sources of variation in secondary metabolites as well as the antiherbivore properties of different classes of defense. We found both environmental and genetic variation affect secondary metabolite production, supporting continued study of the carbon-nutrient balance and growth-differentiation balance hypotheses. Defenses in woody plants are more affected by genetic variation, and herbaceous plant defenses are more influenced by environmental variation. Plant defenses in agricultural and natural systems show similar responses to manipulations, as do plants in laboratory, greenhouse, or field studies. What does such variation mean to herbivores? A comparison of biotic, physical, and chemical defenses revealed the most effective defensive strategy for a plant is biotic mutualisms with ants. Fast-growing plants are most often defended with qualitative defenses and slow-growing plants with quantitative defenses, as the plant apparency and resource availability hypotheses predict. However, we found the resource availability hypothesis provides the best explanation for the evolution of plant defenses, but the fact that there is considerable genetic and environmental variation in defenses indicates herbivores can affect plant chemistry in ecological and evolutionary time.