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.     

Plants as green phones: Novel insights into plant-mediated communication between below- and above-ground insects

Plants can act as vertical communication channels or ‘green phones’ linking soil-dwelling insects and insects in the aboveground ecosystem. When root-feeding insects attack a plant, the direct defense system of the shoot is activated, leading to an accumulation of phytotoxins in the leaves. The protection of the plant shoot elicited by root damage can impair the survival, growth and development of aboveground insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and insects that develop in the aboveground ecosystem. The interactions between spatially separated insects below- and aboveground are not restricted to root and foliar plant-feeding insects, but can be extended to higher trophic levels such as insect parasitoids. Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked by root-feeding insects are significantly less attractive for the parasitoids of foliar-feeding insects.Key words: above-belowground interactions, green phones, multitrophic plant-insect interactions, plant defense, plant volatiles, parasitoids     

Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis

Aims

Arbuscular mycorrhizal (AM) fungi associate with the majority of terrestrial plants, influencing their growth, nutrient uptake and defence chemistry. Consequently, AM fungi can significantly impact plant-herbivore interactions, yet surprisingly few studies have investigated how AM fungi affect plant responses to root herbivores. This study aimed to investigate how AM fungi affect plant tolerance mechanisms to belowground herbivory.

Methods

We examined how AM fungi affect plant (Saccharum spp. hybrid) growth, nutrient dynamics and secondary chemistry (phenolics) in response to attack from a root-feeding insect (Dermolepida albohirtum).

Results

Root herbivory reduced root mass by almost 27%. In response, plants augmented investment in aboveground biomass by 25%, as well as increasing carbon concentrations. The AM fungi increased aboveground biomass, phosphorus and carbon. Meanwhile, root herbivory increased foliar phenolics by 31% in mycorrhizal plants, and increased arbuscular colonisation of roots by 75% overall. AM fungi also decreased herbivore performance, potentially via increasing root silicon concentrations.

Conclusions

Our results suggest that AM fungi may be able to augment plant tolerance to root herbivory via resource allocation aboveground and, at the same time, enhance plant root resistance by increasing root silicon. The ability of AM fungi to facilitate resource allocation aboveground in this way may be a more widespread strategy for plants to cope with belowground herbivory.

     

Root herbivory induces an above-ground indirect defence

Indirect plant defences have largely been studied within the scope of above‐ground interactions. Here we provide novel evidence that root herbivory can induce an above‐ground indirect defence. Cotton plants (Gossypium herbaceum) exposed to root‐feeding wireworms (Agriotes lineatus) increased their foliar extrafloral nectar production ten‐fold in comparison to undamaged control plants. Mechanical root damage also yielded an increase in nectar production. In nature, extrafloral nectar production allows plants to recruit predators, which in turn protect the plant against above‐ground insect herbivores. Our results show that root‐feeding herbivores may alter such above‐ground defensive interactions.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

Does mother know best? The preference–performance hypothesis and parent–offspring conflict in aboveground–belowground herbivore life cycles

1. A substantial amount of research on host‐plant selection by insect herbivores is focused around the preference–performance hypothesis (PPH). To date, the majority of studies have primarily considered insects with aboveground life cycles, overlooking insect herbivores that have both aboveground and belowground life stages, for which the PPH could be equally applicable. 2. This study investigated the factors influencing the performance of the root‐feeding vine weevil (Otiorhynchus sulcatus) larvae and whether this was linked to the oviposition behaviour of the maternal adult living aboveground. 3. Maternal insects feeding aboveground reduced root biomass by 34% and increased root carbon by 4%. Larvae feeding on plants subjected to aboveground herbivory had reduced mass. Irrespective of the presence of maternal herbivory, larval mass was positively correlated with root biomass. 4. Larval mass was also reduced by conspecific larvae, previously feeding on roots (19% reduction). However, the mechanism underpinning this effect remains unclear, as in contrast to maternal herbivory aboveground, prior larval feeding did not significantly affect root biomass or root carbon concentrations. 5. Maternal insects did not distinguish between plants infested with larvae and those that were free of larvae, in terms of their egg‐laying behaviour. Conversely, maternal insects tended to lay eggs on plants with smaller root systems, a behaviour that is likely to negatively affect offspring performance. 6. The PPH is not supported by our findings for the polyphagous vine weevil feeding on the host plant raspberry (Rubus idaeus), and in fact our results suggest that there is the potential for strong parent–offspring conflict in this system.     

Effects of belowground vertical distribution of a herbivore on plant biomass and survival in Lolium perenne

Root herbivory affects plant performance, but the effects are not well understood. We tested the effects of the vertical distribution of a root-feeding beetle larva (Anomala cuprea) by restricting its access to the top, middle, or bottom zone in pots of perennial ryegrass (Lolium perenne) or by allowing unrestricted access. We predicted that plant mortality, biomass, and biomass allocation should change with the zone of root herbivory, because both the magnitude of root loss and the consequences of such loss are specific to the point of damage. Seven of nine plants died in each treatment in which the larvae had access to the top zone. In contrast, no plants died when larvae occupied the middle or bottom zones. Plants were killed when the larvae grazed the root base and severed the shoots from the roots. Moreover, total plant biomass and biomass allocation to roots were significantly lower when the larvae were confined to the top and middle feeding zones. The greatest number of roots were removed when the larvae occupied the top feeding zone. Thus, the vertical distribution of a belowground herbivore is crucially important to plant fate. In nature, most belowground herbivores are concentrated near the soil surface, and thus the effects of belowground herbivory are often more severe than the effects of aboveground herbivory.     

Delayed local responses of downy birch to damage by leafminers and leafrollers

Recent findings suggest that impacts of endemic herbivory on forest ecosystems over the long term may exceed impacts of herbivore outbreaks. However, responses of trees to minor and local damage imposed by small arthropod herbivores, especially by those mining or skeletonising individual leaves, remain poorly understood. We studied the delayed effects of injuries by several leafmining and leafrolling insects on the performance of downy birch shoots. Insect feeding did not affect survival of shoots or survival of individual axillary buds in long shoots. In the year following the damage, shoots produced an average of 13.8% more biomass than undamaged shoots of the same tree. The magnitude of this effect increased with an increase in the leaf area injured during the previous year, but it did not differ among four localities in subarctic and boreo‐nemoral forests, between herbivore feeding guilds, or among herbivores imposing damage in early, mid and late summer. We also found that herbivores attacked the next‐year foliage produced by damaged shoots less frequently than they attacked the next‐year foliage produced by undamaged shoots of the same tree. Thus, our study demonstrated delayed local compensatory growth and increased antiherbivore defence in downy birch shoots following local damage by insect feeding. We suggest that this pattern reflects evolutionary adaptations of plants to permanently acting minor, dispersed and spatially unpredictable damage imposed by endemic herbivory. Local responses are less costly and represent a more sustainable strategy to maintain plant fitness under low levels of herbivory than constitutive resistance or systemic responses.     

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.     

The effect of herbivore density on host plant mediated interactions between two insects

Recent work suggests that foliar- and root-feeding insects can interact in a novel plus-minus fashion. However, the effects of herbivores may be different at different densities. This paper describes two laboratory experiments investigating the effect of increasing insect density on plant performance and the host-plant mediated interaction between a leaf-mining fly and root-feeding chafer larvae. Above- and below-ground insect herbivory decreased plant performance. The effects of the root feeder were, for some parameters, different between the two densities of chafer larvae. Leaf mining significantly decreased the performance of the chafer larvae, while root herbivory was found to increase the pupal weight (related to fecundity) of the leaf miner. The effects of root herbivory suggest that the relationships between herbivore density and plant performance may be curved as the greater chafer density had no significant increased effect on the plants or foliar-feeding insects.     

Response of Pisum sativum (Fabales: Fabaceae) to Sitona lineatus (Coleoptera: Curculionidae) infestation: effect of adult weevil density on damage, larval population, and yield loss

Sitona lineatus L. (Coleoptera: Curculionidae) is an invasive pest in North America and its geographical range is currently expanding across the Canadian prairies. Adults and larvae of S. lineatus feed upon the foliage and root nodules, respectively, of field pea, Pisum sativum L. (Fabales: Fabaceae), and may contribute to economic losses when population densities are high. Integrated pest management (IPM) programs that incorporate economic thresholds should be used to manage S. lineatus populations in a sustainable manner. The impact of nitrogen fertilizer on field pea yield and the relationships between adult weevil density and above- and below-ground damage and yield were investigated in southern Alberta, Canada using exclusion cages on field pea plots. In each cage, 32 field pea plants were exposed to weevil densities ranging from zero to one adult weevil per plant. Nitrogen-fertilized plants yielded 16% more than unfertilized plants. Nitrogen-fertilized plants had fewer root nodules than unfertilized plants, but fertilizer had no effect on foliar feeding by S. lineatus. Adult density affected foliar feeding damage, with increases in above-ground damage associated with increases in S. lineatus density. Adult density did not affect root nodule damage, larval density, foliar biomass or seed weight. Overall, these results indicate that terminal leaf damage may be used to estimate adult weevil density but cannot be used to predict larval density or yield loss. Further research is required to better understand the impact of larval damage on yield and determine if economic thresholds can be developed using data from large-scale production systems.     

Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions

Most ecologists acknowledge that plants are subject to complex interactions between both below- and aboveground dwelling animals. However, these complex interactions are seldomly investigated simultaneously. In a factorial common garden experiment we tested single and combined effects of decomposers, root herbivores and leaf herbivores on the growth, flower visitation, and abundance of naturally colonizing aphids and parasitoids on wild mustard ( Sinapis arvensis ). We found that the individual presence of either root herbivores or decomposers resulted in increased aphid abundance, demonstrating that the same aboveground plant–insect interaction can be released by different belowground processes. Enhanced aphid densities caused higher numbers of parasitoids. Furthermore, decomposers increased plant growth and plant fitness (measured as the number of seeds produced), indicating that mustard may benefit from nutrients provided by decomposers, regardless whether plants are attacked by root herbivores or leaf herbivores, or both simultaneously. More flower visits were observed in plants attacked by root herbivores but without leaf herbivores than in plants with both herbivores, suggesting that root herbivory can modify flower attractivity to pollinators. Our results suggest that patterns in plant–insect interactions above the ground are not only affected by aboveground factors but also by a wealth of different belowground processes mediated by the plant.     

Interactive effects of soil fertility and herbivory on Brassica nigra

Soil nutrient availability may affect both the amount of damage that plants receive from herbivores and the ability of plants to recover from herbivory, but these two factors are rarely considered together. In the experiment reported here, I examined how soil fertility influenced both the degree of defoliation and compensation for herbivory for Brassica nigra plants damaged by Pieris rapae caterpillars. Realistic levels of defoliation were obtained by placing caterpillars on potted host plants early in the life cycle and allowing them to feed until just before pupation on the designated plant. Percent defoliation was more than twice as great at low soil fertility compared to high (48.2% and 21.0%, respectively), even though plants grown at high soil fertility lost a greater absolute amount of leaf area (38.2 cm² and 22.1 cm², respectively). At both low and high soil fertility, total seed number and mean mass per seed of damaged plants were equivalent to those of undamaged plants. Thus soil fertility did not influence plant compensation in terms of maternal fitness. However, the pathways used to achieve compensation in seed production were different at low and high soil fertility. At low soil fertility, relative leaf growth rates (area added per inital area per day) of damaged plants were drastically reduced over the second week of caterpillar feeding. Damaged plants recovered the leaf area lost to herbivory in the two weeks following insect removal by increasing leaf relative growth rates above the levels seen for undamaged plants, but the replacement of leaf tissue lost to herbivory came at the expense of stem biomass. At high soil fertility, relative leaf growth rates of damaged plants were similar to those of undamaged plants both over the second week of caterpillar feeding and following caterpillar removal, and stem biomass was not affected by herbivory. These results suggest that higher levels of soil nutrients increased the ability of plants to stay ahead of their herbivores as they were being eaten. Because damaged plants at high soil fertility were able to maintain leaf growth rates to a greater extent than damaged plants at low soil fertility, they did not fall as far behind undamaged plants over the period of insect feeding and did not have as much catching up to do after feeding ended to compensate for herbivory.     

Reciprocal feeding facilitation between above- and below-ground herbivores

Interspecific interactions between insect herbivores predominantly involve asymmetric competition. By contrast, facilitation, whereby herbivory by one insect benefits another via induced plant susceptibility, is uncommon. Positive reciprocal interactions between insect herbivores are even rarer. Here, we reveal a novel case of reciprocal feeding facilitation between above-ground aphids (Amphorophora idaei) and root-feeding vine weevil larvae (Otiorhynchus sulcatus), attacking red raspberry (Rubus idaeus). Using two raspberry cultivars with varying resistance to these herbivores, we further demonstrate that feeding facilitation occurred regardless of host plant resistance. This positive reciprocal interaction operates via an, as yet, unreported mechanism. Specifically, the aphid induces compensatory growth, possibly as a prelude to greater resistance/tolerance, whereas the root herbivore causes the plant to abandon this strategy. Both herbivores may ultimately benefit from this facilitative interaction.     

Effect of belowground herbivory on parasitoid associative learning of plant odours

Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root‐infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root‐infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours.     

Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age

Aims Plants use different types of responses such as tolerance and induced defense to mitigate the effects of herbivores. The direction and magnitude of both these plant responses can vary with plant age. However, most studies have focused on aboveground herbivory, whereas important feeding occurs belowground. Here, we tested the hypothesis that plant tolerance and defense following shoot damage or root herbivory depends on plant age.     

Invasive plants and their escape from root herbivory: a worldwide comparison of the root-feeding nematode communities of the dune grass <Emphasis Type="Italic">Ammophila arenaria</Emphasis> in natural and introduced ranges

Invasive plants generally have fewer aboveground pathogens and viruses in their introduced range than in their natural range, and they also have fewer pathogens than do similar plant species native to the introduced range. However, although plant abundance is strongly controlled by root herbivores and soil pathogens, there is very little knowledge on how invasive plants escape from belowground enemies. We therefore investigated if the general pattern for aboveground pathogens also applies to root-feeding nematodes and used the natural foredune grass Ammophila arenariaas a model. In the late 1800s, the European A. arenariawas introduced into southeast Australia (Tasmania), New Zealand, South Africa, and the west coast of the USA to be used for sand stabilization. In most of these regions, it has become a threat to native vegetation, because its excessive capacity to stabilize wind-blown sand has changed the geomorphology of coastal dunes. In stable dunes of most introduced regions, A. arenaria is more abundant and persists longer than in stabilized dunes of the natural range. We collected soil and root samples and used additional literature data to quantify the taxon richness of root-feeding nematodes on A.␣arenaria in its natural range and collected samples from the four major regions where it has been introduced. In most introduced regions A. arenaria did not have fewer root-feeding nematode taxa than the average number in its natural range, and native plant species did not have more nematode taxa than the introduced species. However, in the introduced range native plants had more feeding-specialist nematode taxa than A. arenaria and major feeding specialists (the sedentary endoparasitic cyst and root knot nematodes) were not found on A. arenaria in the southern hemisphere. We conclude that invasiveness of A. arenaria correlates with escape from feeding specialist nematodes, so that the pattern of escape from root-feeding nematodes is more alike escape from aboveground insect herbivores than escape from aboveground pathogens and viruses. In the natural range of A. arenaria, the number of specialist-feeding nematode taxa declines towards the margins. Growth experiments are needed to determine the relationship between nematode taxon diversity, abundance, and invasiveness of A. arenaria.     

Secondary plant succession: how is it modified by insect herbivory?

The effects of foliar- and root-feeding insects on the dynamics of an early successional plant community, representing the first four years of colonisation, were examined. Subterranean insect herbivores were found to increase in density with increasing successional age of the plant community. In early succession, chewing insects mainly Coleoptera (Scarabaeidae) and Diptera (Tipulidae) were dominant. This was in direct contrast to the foliar-feeding insects, which were dominated by sap-feeders (mainly Auchenorrhynchan Hemiptera).Reduction of both foliar- and root-feeding insects with appropriate insecticides had different, but dramatic, consequences for the plant community. Reducing foliar herbivory resulted in large increases in perennial grass growth, with plant species richness being reduced as the grasses outcompeted the forbs. Reducing subterranean herbivory prolonged the persistence of annual forbs, greatly increased perennial forb colonisation and, as a consequence, plant species richness. Foliar-feeding insects thus act to delay succession by slowing grass colonisation. In contrast, root-feeding insects accelerate succession by reducing forb persistence and colonisation. The structure of early successional plant communities is therefore modified by the two modes of herbivory.This paper was presented at the Vth International Congress of Ecology (INTECOL), Japan, 1990, entitled Successional Communities of Plants and Insects.     

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.