Insects as stem engineers: interactions mediated by the twig-girdler Oncideres albomarginata chamela enhance arthropod diversity

Background

Ecosystem engineering may influence community structure and biodiversity by controlling the availability of resources and/or habitats used by other organisms. Insect herbivores may act as ecosystem engineers but there is still poor understanding of the role of these insects structuring arthropod communities.

Methodology/Principal Findings

We evaluated the effect of ecosystem engineering by the stem-borer Oncideres albomarginata chamela on the arthropod community of a tropical dry forest for three consecutive years. The results showed that ecosystem engineering by O. albomarginata chamela had strong positive effects on the colonization, abundance, species richness and composition of the associated arthropod community, and it occurred mainly through the creation of a habitat with high availability of oviposition sites for secondary colonizers. These effects cascade upward to higher trophic levels. Overall, ecosystem engineering by O. albomarginata chamela was responsible for nearly 95% of the abundance of secondary colonizers and 82% of the species richness.

Conclusions/Significance

Our results suggest that ecosystem engineering by O. albomarginata chamela is a keystone process structuring an arthropod community composed by xylovores, predators and parasitoids. This study is the first to empirically demonstrate the effect of the ecosystem engineering by stem-boring insects on important attributes of arthropod communities. The results of this study have important implications for conservation.     

Preferences, patterns and consequences of branch removal on the dioecious tropical tree Spondias purpurea (Anacardiaceae) by the insect borer Oncideres albomarginata chamela (Cerambycidae)

Most studies of plant–herbivore interactions in dioecious species have evaluated foliar herbivory. In this studie we evaluated preferences of branch removal by the insect borer Oncideres albomarginata chamela in the tropical dioecious tree Spondias purpurea L. The objectives were to determine the preferences and patterns of the removal of branches, to evaluate the effect of branch removal in the vegetative regeneration of branches, and to evaluate the effect of branch removal on the regeneration of fertile branches of male and female trees of S. purpurea . During three consecutive years of study, damage caused to branches by the girdled borer was associated with plant gender. The proportion of branches removed by the insect was greater for female than for male trees. The effects of branch removal were evaluated in attacked regenerated and unattacked branches. Removed branches regenerated a year after the insect borer attacked them. Branch removal affected the probability of producing fertile branches. The preference by O. a. chamela is apparently associated with the nutritional quality of the host.     

Developmental responses of individual Onobrychis plants to spatial heterogeneity

An experimental study was undertaken to assess the extent to which better-situated branches correlatively inhibit other branches on the same plant which are growing in relatively inferior conditions. The experiments were carried out on naturally-grown Onobrychis squarrosa L. (Papilionaceae), a dominant annual plant of the Mediterranean region of Israel. Treatments were carried out (i) on young plants that only had a seminal shoot, and (ii) on plants after lateral branches had started growing. Differential shade conditions were achieved by the repeated removal of neighbours on one side of the plants. The plants were either left intact or damaged by removing different parts of their branch system. In intact plants, growth responses to the differential light conditions which were expressed by the number of branches, leaves and fruits showed some evidence for support of the shaded branches by the exposed branches on the same plant. In contrast, heterogeneous treatments of both shade and branch damaging led to development that reflected marked correlative inhibition of the shaded parts of the plant. The results show that a latent potential for correlative inhibition between branches exists throughout plant development and that in Onobrychis it can be readily realised when plants are damaged. This could depend on known traits of auxin acting as a correlative signal of growing branches. The observed responses of Onobrychis can be understood as an adaptive strategy which reflects the low reliability of environmental signals and the high cost of changing the course of development, especially in short-lived annual plants.     

How to induce defense responses in wild plant populations? Using bilberry (Vaccinium myrtillus) as example

Inducible plant defense is a beneficial strategy for plants, which imply that plants should allocate resources from growth and reproduction to defense when herbivores attack. Plant ecologist has often studied defense responses in wild populations by biomass clipping experiments, whereas laboratory and greenhouse experiments in addition apply chemical elicitors to induce defense responses. To investigate whether field ecologists could benefit from methods used in laboratory and greenhouse studies, we established a randomized block‐design in a pine‐bilberry forest in Western Norway. We tested whether we could activate defense responses in bilberry (Vaccinium myrtillus) by nine different treatments using clipping (leaf tissue or branch removal) with or without chemical treatment by methyljasmonate (MeJA). We subsequently measured consequences of induced defenses through vegetative growth and insect herbivory during one growing season. Our results showed that only MeJA‐treated plants showed consistent defense responses through suppressed vegetative growth and reduced herbivory by leaf‐chewing insects, suggesting an allocation of resources from growth to defense. Leaf tissue removal reduced insect herbivory equal to the effect of the MeJa treatments, but had no negative impact on growth. Branch removal did not reduce insect herbivory or vegetative growth. MeJa treatment and clipping combined did not give an additional defense response. In this study, we investigated how to induce defense responses in wild plant populations under natural field conditions. Our results show that using the chemical elicitor MeJA, with or without biomass clipping, may be a better method to induce defense response in field experiments than clipping of leaves or branches that often has been used in ecological field studies.     

Sink strength manipulation in branches of a Mediterranean woody plant suggests sink-driven allocation of biomass in fruits but not of nutrients in seeds

The relative autonomy of branches within an individual plant may favor different resource allocation responses after reproductive losses. The assessment of these reproductive strategies at the branch level before their integration at the plant level would provide more insight into how plants deal with reproductive losses. Here, we present a field experiment to assess changes in the allocation strategies at the branch level after sink strength manipulation in a Mediterranean woody plant (Cistus ladanifer). We applied three levels of removal of developing fruits (75, 25 and 0 %) on branches of the same plants, and measured their effects on resource allocation (biomass, nitrogen and phosphorus) and seed production after controlling for the effects of branch diameter and leaf weight per branch. Our results suggest that after experimental fruit thinning, C. ladanifer branches presented a sink-driven allocation of biomass to fruits but this was not the case for the allocation of nutrients to seeds, which could be driven by competition with leaf biomass. Reductions in biomass per fruit resulted in a reduction in seed output since the average weight per seed remained constant. From these results, it could be suggested that an heterogeneous distribution of fruit losses among the branches within a crown would produce a higher impact on reproductive output than a more equitable distribution.     

Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites

Induced defenses mediate interactions between parasites sharing the same host plant, but the outcomes of these interactions are challenging to predict because of spatiotemporal variation in plant responses and differences in defense pathways elicited by herbivores or pathogens. Dissecting these mediating factors necessitates an approach that encompasses a diversity of parasitic feeding styles and tracks interactions over space and time. We tested indirect plant-mediated relationships across three tomato (Solanum lycopersicum) consumers: (1) the fungal pathogen—powdery mildew, Oidium neolycopersici; (2) a sap-feeding insect—silverleaf whitefly, Bemisia tabaci; and (3) a chewing insect—the leaf miner, Tuta absoluta. Further, we evaluated insect/pathogen responses on local vs. systemic leaves and over short (1 day) vs. long (4 days) time scales. Overall, we documented: (1) a bi-directional negative effect between O. neolycopersici and B. tabaci; (2) an asymmetrical negative effect of B. tabaci on T. absoluta; and (3) an asymmetrical positive effect of T. absoluta on O. neolycopersici. Spatiotemporal patterns varied depending on the species pair (e.g., whitefly effects on leaf miner performance were highly localized to the induced leaf, whereas effects on pathogen growth were both local and systemic). These results highlight the context-dependent effects of induced defenses on a diverse community of tomato parasites. Notably, the outcomes correspond to those predicted by phytohormonal theory based on feeding guild differences with key implications for the recent European invasion by T. absoluta.     

Central place foraging by beavers (Castor canadensis): a test of foraging predictions and the impact of selective feeding on the growth form of cottonwoods (Populus fremontii)

Summary Several predictions of central place foraging theory were tested. As predicted, beavers foraged more selectively at increasing distance from the central place. With increasing distance from the river's edge, beavers cut fewer branches and deleted small branches from their diet. Large branches were favored at all distances, which differs from patterns observed in previous studies of beaver foraging. This difference, however, is expected and supports Schoener's (1979) predictions which are based on differences between provisioning costs and item size.The selective harvesting of branches predicted by foraging theory affects plant growth form and may influence plant reproductive patterns. High rates of branch removal caused cottonwoods to develop a shrubby architecture. The importance of selective branch choice by beavers on patterns of cottonwood reproduction (i.e., delayed sexual maturity and induced cloning) is discussed.     

光照条件、植株冠层结构和枝条寿命的关系——以桂花和水杉为例

根据衰老理论的代谢率假说,生物寿命与其代谢率有关,个体大小相同的生物体,在质量较好的微生境中通常比较差生境中具有更高的代谢速率。因此,生物体在资源供给较差的生境中通常比资源供给较充足的生境中具有更长的寿命。枝条是木本植物植冠构建的基本单元之一,如果枝条遵循代谢率假说,则可推测在光照较好环境下的植物枝条或小枝将比其在遮荫环境下具有更短的寿命,即枝条寿命与光照条件成反比。以常绿物种桂花(Osmanthus fragrans)和落叶物种水杉(Metasequoiaglyptostroboides)为研究对象,通过测量不同光照环境下,植株大小(株高和胸径)、冠层深度、冠层轮廓(冠层深度/冠层宽度)、相对冠层宽度(冠层宽度/植株高度)以及植株凋落枝条寿命等性状,探讨了光照条件对成年植株冠层形态结构和植株枝条寿命的影响。调查发现:1)枝条的寿命在遮荫条件下显著高于全光照条件下,与理论预测吻合;2)随遮荫程度增加,植株冠层深度和冠层轮廓增加,相对冠层宽度减小;3)枝条的平均寿命与植株冠层深度和冠层轮廓成正比,与植株相对冠层宽度成反比。这表明光照条件可能通过改变植株冠层结构来影响枝条寿命。未来需要进一步研究枝条生物量分配、叶片光合能力和呼吸速率在不同生活型物种之间的差异,以便更全面的理解枝条寿命与生境质量之间的关系。     

Ecosystem Engineering by Plants on Wave-Exposed Intertidal Flats Is Governed by Relationships between Effect and Response Traits

In hydrodynamically stressful environments, some species—known as ecosystem engineers—are able to modify the environment for their own benefit. Little is known however, about the interaction between functional plant traits and ecosystem engineering. We studied the responses of Scirpus tabernaemontani and Scirpus maritimus to wave impact in full-scale flume experiments. Stem density and biomass were used to predict the ecosystem engineering effect of wave attenuation. Also the drag force on plants, their bending angle after wave impact and the stem biomechanical properties were quantified as both responses of stress experienced and effects on ecosystem engineering. We analyzed lignin, cellulose, and silica contents as traits likely effecting stress resistance (avoidance, tolerance). Stem density and biomass were strong predictors for wave attenuation, S. maritimus showing a higher effect than S. tabernaemontani. The drag force and drag force per wet frontal area both differed significantly between the species at shallow water depths (20 cm). At greater depths (35 cm), drag forces and bending angles were significantly higher for S. maritimus than for S. tabernaemontani. However, they do not differ in drag force per wet frontal area due to the larger plant surface of S. maritimus. Stem resistance to breaking and stem flexibility were significantly higher in S. tabernaemontani, having a higher cellulose concentration and a larger cross-section in its basal stem parts. S. maritimus had clearly more lignin and silica contents in the basal stem parts than S. tabernaemontani. We concluded that the effect of biomass seems more relevant for the engineering effect of emergent macrophytes with leaves than species morphology: S. tabernaemontani has avoiding traits with minor effects on wave attenuation; S. maritimus has tolerating traits with larger effects. This implies that ecosystem engineering effects are directly linked with traits affecting species stress resistance and responding to stress experienced.     

Large herbivores facilitate an insect herbivore by modifying plant community composition in a temperate grassland

Large herbivores often co‐occur and share plant resources with herbivorous insects in grassland ecosystems; yet, how they interact with each other remains poorly understood. We conducted a series of field experiments to investigate whether and how large domestic herbivores (sheep; Ovis aries) may affect the abundance of a common herbivorous insect (aphid; Hyalopterus pruni) in a temperate grassland of northeast China. Our exclosure experiment showed that 3 years (2010–2012) of sheep grazing had led to 86% higher aphid abundance compared with ungrazed sites. Mechanistically, this facilitative effect was driven by grazing altering the plant community, rather than by changes in food availability and predator abundance for aphids. Sheep significantly altered plant community by reducing the abundance of unpalatable forbs for the aphids. Our small‐scale forb removal experiment revealed an “associational plant defense” by forbs which protect the grass Phragmites australis from being attacked by the aphids. However, selective grazing on forbs by sheep indirectly disrupted such associational plant defense, making P. australis more susceptible to aphids, consequentially increasing the density of aphids. These findings provide a novel mechanistic explanation for the effects of large herbivores on herbivorous insects by linking selective grazing to plant community composition and the responses of insect populations in grassland ecosystems.     

Ecosystem engineers maintain a rare species of butterfly and increase plant diversity

We evaluated whether ecosystem engineers can accomplish two conservation goals simultaneously: (1) indirectly maintain populations of an endangered animal through habitat modification and (2) increase riparian plant diversity. We tested for effects of a prominent ecosystem engineer, the beaver Castor canadensis, on populations of St. Francis' satyr butterfly Neonympha mitchellii francisci and plant species richness and composition. We performed our test by surveying riparian vegetation communities in all stages of beaver‐influenced wetland succession. We found that beavers created wetland habitats that supported plant species not found elsewhere in riparian zones and increased plant species diversity across the landscape by creating a novel combination of patch types. Our results confirmed what others have found about engineering effects on plant diversity, but these results further demonstrated a case where ecosystem engineers indirectly maintain populations of rare animals by modifying the composition and diversity of plant communities within wetlands. Our research demonstrates how an ecosystem engineer can influence habitat availability and composition of plant communities important for an endangered insect, and maintain overall plant species diversity by increasing habitat heterogeneity.     

Linking belowground and aboveground phenology in two boreal forests in Northeast China

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVY^NTN, PVY^NO and PVY^O) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVY^NTN induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVY^NTN infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect–plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.     

Effects of the mermithid nematode Ovomermis sinensis on the hemocytes of its host Helicoverpa armigera

Little is known about the mechanism by which mermithid nematodes avoid encapsulation responses of insect hosts. In this study, we investigated the influence of the mermithid nematode Ovomermis sinensis on host Helicoverpa armigera hemocyte number, encapsulation activity, spreading behavior and cytoskeleton. Parasitism by O. sinensis caused a significant increase in the total hemocyte counts (THC) and plasmatocyte numbers of H. armigera. However, in vivo encapsulation assays revealed that hemocyte encapsulation abilities of H. armigera were suppressed by O. sinensis. Moreover, parasitism by O. sinensis changed the spreading behavior and cytoskeletons of the host hemocytes. The results suggested that O. sinensis could actively suppress the hemocyte immune response of its host, possibly by destroying the host hemocyte cytoskeleton. This is the first report of a possible mechanism by which mermithid nematodes suppress encapsulation responses of insect hosts.     

Effect of spikelet removal on the whole plant senescence of rice

The rice (Oryza sativa L.) cultivar IET 1444 showed a nonsequential mode of senescence as evident from the decline in chlorophyll and protein of the flag and second leaves at the senescent stage. Removal of 50,75 and 100 % spikelets from the panicle of rice plant or emasculation of the panicle by hot water treatment induced the development of secondary branch from the axil of second leaf but 25 % removal had no effect. Similarly, removal of 75 and 100 per cent spikelets from the panicle of secondary branch induced tertiary branch development, while 25 and 50 per cent removal had no such effect. Similar treatments on tertiary branch had no effect on further branch production. The pattern of leaf senescence of the untreated (control) main tiller, secondary and tertiary branches was identical, i. e. nonsequential, which could be changed into the sequential type only by the development of additional sinks (i. e. side branch). The leaf area and the seed number of secondary and tertiary branches were gradually reduced and reached a critical value in the tertiary branch. The removal of spikelets or emasculation delayed leaf senescence of the main tiller and the secondary and tertiary branches. Also the longevity of the whole plant could be increased by 40 d i. e., up to the senescence of the tertiary branch. Both leaves and reproductive parts control side branch production, which, in turn, controls the longevity of the whole rice plant.     

Plant responses following grazing removal at different stocking rates in an Inner Mongolia grassland ecosystem

Grazing removal is widely used in grassland management. Plant responses following grazing removal at different organizational levels, however, are not well understood. We examined plant responses at different stocking rates in an Inner Mongolia grassland ecosystem dominated by Leymus chinensis and Stipa grandis. Our results indicated that plant response patterns differed significantly among stocking rates, at different levels of organization, and between wet and dry years. Community aboveground net primary production (ANPP) recovered more quickly at low and moderate stocking rates than those at high stocking rates. Response of aboveground net primary production (R_ANPP) was significantly positively correlated with both individual biomass and density responses of L. chinensis. Overcompensation of L. chinensis after grazing removal contributed greatly to positive R_ANPP at the community level. Significant compensatory effects were found between the two dominant species and between dominant species and the remaining non-dominant species. Variation in precipitation significantly affected community ANPP, relationships between community and species responses, and compensatory effects between species. Our study suggests that periodic grazing removal is likely to be a useful method for grassland management and that a combination of species with compensatory effects can be advantageous for reseeding practices in grassland restoration.     

Strategy for shoot meristem proliferation in plants

Shoot apical meristem (SAM) of plants harbors stem cells capable of generating the aerial tissues including reproductive organs. Therefore, it is very important for plants to control SAM proliferation and its density as a survival strategy. The SAM is regulated by the dynamics of a specific gene network, such as the WUS-CLV interaction of A. thaliana. By using a mathematical model, we previously proposed six possible SAM patterns in terms of the manner and frequency of stem cell proliferation. Two of these SAM patterns are predicted to generate either dichotomous or axillary shoot branch. Dichotomous shoot branches caused by this mechanism are characteristic of the earliest vascular plants, such as Cooksonia and Rhynia, but are observed in only a small minority of plant species of the present day. On the other hand, axillary branches are observed in the majority of plant species and are induced by a different dynamics of the feedback regulation between auxin and the asymmetric distribution of PIN auxin efflux carriers. During evolution, some plants may have adopted this auxin-PIN system to more strictly control SAM proliferation.     

Impact of the flower-galling midge,Dasineura rubiformis Kolesik,on the growth of its host plant,Acacia mearnsii De Wild,in South Africa

Acacia mearnsii (black wattle), although recognised as being extremely invasive and problematic in South Africa, is cultivated as an important commercial plant in parts of the country. Following the introduction of a flower-galling midge, Dasineura rubiformis (Cecidomyiidae), into the Western Cape Province for biological control of A. mearnsii, trials to confirm that galling would not affect growth rates of the host-plant were necessitated before the midge could be more-widely distributed. Insecticide exclusion of the midge from selected branches of the plant enabled comparison of growth rates of branches with high and low levels of galling. Over fifteen months the increment in branch diameter was greater on highly galled branches than on lightly galled branches with pods. This result indicates that D. rubiformis, while reducing seed set to very low levels, does not negatively affect growth of its host and that the midge will have no detrimental effect on the wattle forestry industry in South Africa.     

Biomass partitioning and water content relationships at the branch and whole-plant levels and as a function of plant size in Elaeagnus mollis populations in Shanxi, North China

Understanding of the biomass (dry weight) allocation and water relations in populations will provide useful information on the growth patterns and resource-allocation dynamics. By destructive sampling, foliage, branch and root biomass were measured in the endangered shrub Elaeagnus mollis populations growing in Shanxi province, North China. Biomass partitioning and water content relationships were compared at the branch and whole-plant levels, and as a function of basal diameter (plant size). The biomass was mainly distributed in the bigger branches at the branch level, and in the branch wood at the whole-plant level, and branch biomass (but not foliage or root biomass) increases significantly with increasing basal diameter. As a result, branch wood became the major biomass pool, even though considerable biomass was also allocated to the roots. However, the relative water content decreased from the periphery of the crown to the interior of the shrub at the branch level, and from the aboveground to the belowground at the whole-plant level though no significant variation among foliage, branches, and roots. Yet it increased significantly for the whole-plant with increasing basal diameter. The ratio of belowground to aboveground biomass was smaller than 1.0, even as a function of basal diameter. These growth responses indicated a strong adaptation to the shrub’s growing conditions. Biomass was primarily allocated above the ground and the aboveground components grew faster than the belowground one.     

Distinct roles of jasmonates and aldehydes in plant-defense responses

Background

Many inducible plant-defense responses are activated by jasmonates (JAs), C₆-aldehydes, and their corresponding derivatives, produced by the two main competing branches of the oxylipin pathway, the allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches, respectively. In addition to competition for substrates, these branch-pathway-derived metabolites have substantial overlap in regulation of gene expression. Past experiments to define the role of C₆-aldehydes in plant defense responses were biased towards the exogenous application of the synthetic metabolites or the use of genetic manipulation of HPL expression levels in plant genotypes with intact ability to produce the competing AOS-derived metabolites. To uncouple the roles of the C₆-aldehydes and jasmonates in mediating direct and indirect plant-defense responses, we generated Arabidopsis genotypes lacking either one or both of these metabolites. These genotypes were subsequently challenged with a phloem-feeding insect (aphids: Myzus persicae), an insect herbivore (leafminers: Liriomyza trifolii), and two different necrotrophic fungal pathogens (Botrytis cinerea and Alternaria brassicicola). We also characterized the volatiles emitted by these plants upon aphid infestation or mechanical wounding and identified hexenyl acetate as the predominant compound in these volatile blends. Subsequently, we examined the signaling role of this compound in attracting the parasitoid wasp (Aphidius colemani), a natural enemy of aphids.

Principal Findings

This study conclusively establishes that jasmonates and C₆-aldehydes play distinct roles in plant defense responses. The jasmonates are indispensable metabolites in mediating the activation of direct plant-defense responses, whereas the C₆-aldehyes are not. On the other hand, hexenyl acetate, an acetylated C₆-aldehyde, is the predominant wound-inducible volatile signal that mediates indirect defense responses by directing tritrophic (plant-herbivore-natural enemy) interactions.

Significance

The data suggest that jasmonates and hexenyl acetate play distinct roles in mediating direct and indirect plant-defense responses. The potential advantage of this “division of labor” is to ensure the most effective defense strategy that minimizes incurred damages at a reduced metabolic cost.