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Current Issue. Previous Issues. Editorial Board. Submit a Manuscript. Guide to Authors. More recently, the number of studies showing that herbivore induced belowground volatiles trigger predator attraction in the soil has increased. Belowground investigations began with two key studies which demonstrated for the first time that unknown cues were responsible for attracting entomopathogenic nematodes to insect damaged roots Boff et al. Tritrophic interactions with belowground herbivore-induced plant volatiles HIPV signaling have been described both in agricultural systems Rasmann et al.

Because of the extensive literature focused on aboveground plant volatiles and methods, here we describe the techniques used for belowground assessment, focusing our attention on the advances related to agroecosystems and their application in the control of insect pests. Factors in addition to VOCs are known to influence both behavior of herbivores and their natural enemies belowground. Root exudates also influence spatial distribution of root feeders Johnson and Gregory, ; Johnson and Nielsen, ; Gfeller et al. Some recent techniques were developed to measure root exudates that influence herbivore behavior using LESA liquid extraction surface analysis Robert et al.

Thus, far VOCs have been a major candidate for use in biological control and also to explain multitrophic cascades both above and below ground Kaplan, a , b ; Poelman et al. The technical difficulties associated with dynamics of the soil ecosystem have been a major limitation in studying belowground multitrophic interactions. Soil is a complex, tri-phasic medium making the analysis of individual factors and their interactions considerably difficult, and hence, most research has been based on in vitro analysis of individual factors Rasmann et al.

Spatial Pattern Analysis in Plant Ecology : Mark R. T. Dale :

New approaches to evaluate root volatiles have only recently been developed and applied in researches on chemical and evolutionary ecology. As mentioned earlier, all of these can serve as signals and cues for herbivores and their natural enemies. However, in this review we focus on HIPVs as they are often shown to be involved in multitrophic interactions that include natural enemies and have been shown to be detectable from intact plants.

Although methods exists for the evaluation of additional exudates from intact plant roots i. Rasmann et al. Briefly, an adsorbent-coated fused silica fiber with properties similar to a gas chromatography column can collect volatile compounds from the headspace of a sample. The volatile compounds once fixed to the SPME fiber can then be thermally desorbed in an injection port of a gas chromatograph. SPME is a rapid and simple extraction method that does not require the use of solvents and its detection limits can reach parts per trillion ppt levels for certain compounds Pawliszyn, However, one of the limitations of this technique is that it is a destructive method of sampling root material: both the plant and herbivore must be separated and volatiles from this interaction can only be examined after harvesting and crushing the plant tissues.

Ali et al. In this case, volatiles can be collected and extracted by elution of an adsorbent with low boiling point solvents. Adsorbent traps are usually made of glass tubes filled with the granulated adsorbent, held in place by stainless steel mesh, glass wool plugs, or Teflon fitted rings.


By connecting the adsorbent trap to a vacuum pump and pulling air through glass chambers containing intact citrus plants either with or without feeding larvae Ali et al. The volatiles collected on this trap are rinsed using a non-polar e. This methodology allows for the sample to be retained in a solvent, which can be analyzed multiples times.

Additionally, the solvents containing root volatiles were also tested in sand-filled two-choice bioassays chambers. By using this approach, Ali et al. Moreover, a soil probe was recently used to sample soil volatiles in Florida citrus groves at a depth of 20 cm Figure 1 Ali et al. This soil probe was developed to collect the compound on adsorbent traps by using a vacuum pump to pull air from the soil. Recently, a non-destructive method similar to the one used by Ali et al. Figure 1.

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Representation of soil probe design used to sample volatiles belowground. Probe is inserted into soil and connected to a vacuum pump.

420.639 Landscape Ecology

By using this technique, organic compounds such as ketones, aldehydes, alcohols, oxygenated aromatic and aliphatic compounds will be readily protonated Danner et al. Proton transfer utilizes a soft ionization method, so it generally leads to less overall fragmentation of the product ions, which is a tremendous advantage, and also the mass of the product ion equals the VOC mass plus one de Gouw and Warneke, ; Danner et al.

At the end of the drift tube, the reagent and product ions are measured by a quadrupole mass spectrometer.

1 Introduction

The product ion signal is proportional to the VOC mixing ratio. PTR-MS can monitorize numerous VOCs with a high sensitivity 10— pptv and rapid response time 1—10 s de Gouw and Warneke, , although regular calibration with the gas mixture is required for accurate and reproducible quantification of trace gases Danner et al.

The more common methods of collecting plant VOCs on to filters with polymer adsorbents makes it necessary to preconcentrate the sample before analysis by collecting volatiles during a range of minutes to hours; this reduces the ability to resolve the timing of VOC emission measurements Danner et al. Furthermore, solvents used to elute VOCs from the adsorbents may introduce contamination before GC analysis. It is clear that isomers cannot be distinguished, and the interpretation of mass spectra is further complicated by the formation of cluster ions and the fragmentation of product ions.

Two recent examples show its promise as a technique to evaluate belowground interactions in preliminary PTR-MS results on herbivore-induced root responses in Brassica species. Danner et al. Nancy during infestation with a belowground herbivore, Delia radicum , the larvae of the cabbage root fly.

The resulting mass scans found that the intensities of several molecular masses were enhanced in root fly infested B. In a second example, Danner et al. Initially, they detected only a low emission rate of compounds, which steadily increased with longer feeding times of the root flies. In control plants, the VOC emissions remained at a very low level, allowing a clear distinction between control and infested plants within a few hours after infestation Danner et al.

In general, these techniques are informative and effective in different manners. For example, the non-destructive sampling techniques are useful in evaluating belowground interactions in situ. Also, they may potentially prove useful in additional contexts. However, the properties of the surrounding soil might interfere and, hence, make resolution difficult with the potential for significant background. The combination of techniques and refinements of approaches might produce the best resolution for the target individual system.

The considerable advances in research on molecular mechanisms and ecological signaling of insect herbivore induced VOCs launch promising prospects of manipulating the release of these compounds in order to enhance crop protection. Encouraging examples from both laboratory and field experiments support this approach to develop novel ecologically drive crop protection strategies. On the agricultural side, at the moment, the best-known belowground tritrophic interaction is the maize system, described for the first time by Rasmann et al.

This compound is a highly attractive HIPV to the entomopathogenic nematode Heterorhabidtis megidis in the laboratory as well as in the field Rasmann et al.

In fact, it is among the less costly terpenoid that could be travelling within the soil Hiltpold and Turlings, , and that is under selection Kollner et al. Another example of highly complex volatile blends in agroecosystems was described by using the roots of cotton Gossypium herbaceum and the larvae of the chrysomelid beetle Diabrotica balteata. The sesquiterpenoid aristolene was discussed as being a good candidate for playing a major role in Heterorhabditis megidis nematode attraction, although future studies might confirmed it Rasmann and Turlings, These authors also tested the nematode preference against damaged roots of cowpea Vigna unguiculata plants.

In contrast to the other crops, corn and cotton, cowpea plants emitted almost undetectable amounts of volatiles that also resulted in lower nematode attractions Rasmann and Turlings, More recently, Ali et al. Using belowground olfactometers Ali et al. However, Ali et al. Consequently, this may reduce the exploitation of citrus induced VOCs emission in biological control strategies targeting Diaprepes abbreviates if rootstocks are not truely resistant to T.

Most recently, Ali et al. At this moment, there are very few published examples of cue-based behavioral manipulation in belowground contexts. The use of natural products to enhance biocontrol is typically compatible with integrated pest management; deploying HIPVs aboveground by controlled release dispensers has been shown to increase plant recruitment and retention of beneficial parasites or predators Thaler, ; James and Grasswitz, After identification of herbivore-induced compound attractive to natural enemies, it is possible genetically manipulate the plant in order to i make a plant more attractive to beneficial predators or parasitoids or ii to restore the phenotype that was lost due to natural or human selection Rasmann et al.

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The first examples of such an approach are aboveground Kappers et al. Most of the European maize varieties and Teosinte produce this sesquiterpene whereas American varieties do not Rasmann et al. This indicates a shift in the gene activity through breeding selection Kollner et al.

Degenhardt et al. This constituted the first demonstration in the field that plant genotype engineering could enhance biological control. Entomopathogenic nematodes appear as good candidates for an inundative biological control strategy. At the moment, there are knowledge of key attractants for specific entomopathogenic nematodes species Hallem et al. Hiltpold et al. Using root-zone olfactometers, a population of the nematode Heterorhabditis bacteriophora was successfully selected. Interestingly, the establishment and the persistence in the field were not influenced by the selection process Hiltpold et al.

Here we see the great potential of selecting beneficial organisms for a better and faster response, which also resulted in higher infection rates. Recent advances are showing the potential of belowground organisms to interact with aboveground food webs. In this regard, Pineda et al. In laboratory studies, they combined ecological, molecular, and chemical approaches to study how the rhizobacterial colonization modified the complex composition of the HIPV.

They observed that the compounds produced by the rhizobacteria-aphids-plant treatment negatively influenced the behavior of the aphid-parasitoid when compared with the effect of the blend induced by just aphid-plant. These authors have demonstrated that the non-pathogenic rhizobacteria effect on parasitoid activity is mediated by jasmonic acid pathways that associate with plant volatile production.

In contrast, work by Robert et al. Thus, manipulation of these blends and studies in more natural conditions might provide additional insight on the complex multitrophic interactions occurring above- and belowground, and it should be acknowledged the effects and responses in one subsystem of the plant can have very different roles on other systems. During the past several decades, new technologies and spatial statistics offer a number of tools for point pattern analysis, which provide improved detection and characterization of spatial heterogeneity such as gradient or clustering Perry et al.

Earlier two-dimensional maps of spatial patterns were developed for plants and for relatively immobile organisms Diggle, Meanwhile, the spatial information of mobile organisms was restricted to counts in traps at specific locations Perry, Initially, the methods used to describe spatial patterns focused on the intensity of aggregation and were based on the relationship between the sample mean and variance Taylor, ; Iwao, Spatial information provided by these methods was criticized by Perry and Hewiit for not considering geographic location of each sample unit, and in consequence, these indices could not be used for comparing or mapping the spatial patterns of populations.

Currently available technologies i. Notwithstanding the utility of geostatistical procedures to characterize spatial patterns, they do not provide tests to assess the statistical significance of the estimated patterns. To overcome this limitation, Perry and Hewiit developed a new method, SADIE, which uses the spatial information in the sample in ways that permit inference testing in order to make the information more understandable from a theoretical biological perspective. Despite this advantage, SADIE is used infrequently compared to geostatistical methods for community studies.

Accordingly, we describe the method here with some examples of its application to agroecology. The method evolved from a spatial analysis based on a single index to an analysis of count data that are spatially-referenced with two coordinates x, y that can be irregularly spaced and not necessarily on a grid Perry, , The development of new SADIE indices and maps, increased the ability to characterize the spatial information in a sample Perry et al.

Table 3. To assess the magnitude of aggregation, the observed D is compared to those for large numbers of randomly distributed permutations of the counts observed among the sample units.