Chemical information transfer between plants:: back to the future
Introduction
All organisms are under selective pressure to maximize reproductive success. To exploit the prevailing environmental conditions to their full extent, organisms can take advantage of information. An important form of information consists of chemical cues. It has been well established that chemical information plays an essential role in the ecology of such diverse organisms as protozoa (Kuhlmann et al., 1999), crustaceans (Tollrian and Dodson, 1999), insects (Cardé and Bell, 1995; Roitberg and Isman, 1992), and vertebrates (Kats and Dill, 1998; Tollrian and Harvell, 1999). Likewise, there is a rich literature on the emission of chemical information by plants and its use by arthropods (Schoonhoven et al., 1998; Chadwick and Goode, 1999), by fungi (Nagashi and Douds, 1999) and by plant-parasitic plants (Estabrook and Yoder, 1998). In addition, allelopathic effects of plant compounds on neighbouring plants have been amply documented (Pellisier and Souto, 1999; Mallik and Romeo, 2000). The role of chemical information in interactions between damaged and undamaged plants, however, remained controversial ever since the first scientific publications appeared in the early 1980s (Baldwin and Schultz, 1983; Rhoades, 1983; Fowler and Lawton, 1985). Some studies found no evidence for transfer of information between damaged and undamaged plants (Myers and Willams, 1984; Williams and Myers, 1984; Fowler and Lawton, 1985; Lin et al., 1990; Preston et al., 1999). Many others presented evidence supporting the hypothesis of information conveyance between damaged and undamaged plants (Rhoades, 1983; Haukioja et al., 1985; Rhoades, 1985; Zeringue, 1987; Dicke et al., 1990; Farmer and Ryan, 1990; Bruin et al., 1992; Shulaev et al., 1997; Arimura et al., 2000; Dolch and Tscharntke, 2000; Karban et al., 2000) and several stimulating reviews have been published in the past five years (Bruin et al., 1995; Shonle and Bergelson, 1995; Karban and Baldwin, 1997).
Yet, studies on plant-to-plant communication are often received with scepticism. The major issues raised by critics are, in random order: (1) data suffer from statistical flaws such as pseudoreplication, (2) the dose of the chemical cues applied in experiments was unrealistically high, (3) the mechanism is unknown or alternative mechanisms may explain the data, (4) ubiquitous cues cannot be meaningful information in interactions between damaged and undamaged plants, and (5) experiments under realistic field conditions are lacking (Fowler and Lawton, 1985; Firn and Jones, 1995; Karban and Baldwin, 1997). Although related to very different aspects of experimental studies, each of these issues is important and should be considered in studies on information conveyance between damaged and undamaged plants. They should stimulate scientists to improve their experimental protocols, to investigate alternative mechanisms, to determine costs and benefits, and to assess the impact on population dynamics—in short they should stimulate continual investigation of a phenomenon with good potential. After all, there is abundant evidence that chemical information from damaged plants is available to undamaged plants.
Section snippets
Plants ‘talk’: characteristics of volatiles from damaged plants
In the past two decades it has been well documented that plants respond to damage and herbivory with the emission of a bouquet of volatiles (see e.g. Takabayashi and Dicke, 1996; Chadwick and Goode, 1999; Dicke and Vet, 1999; Sabelis et al., 1999 for reviews). These volatiles are usually emitted in considerable quantities and the bouquet is often dominated by compounds that are not emitted when the plant is undamaged or mechanically damaged (Boland et al., 1999; Dicke, 1999b). In other cases
Why would plants ‘listen’?
In discussions of communication between plants the emphasis is often placed on the benefits to the emitter. However, given that chemical information from damaged plants is available, the important question is: do downwind neighbours exploit this information to their own benefit? After all, the wind that transfers the information from damaged to undamaged plants can also transport attackers such as pathogens and small herbivores such as mites and insects. The mere presence of damage-related
Past evidence
Various groups have published data that support the hypothesis that chemical information conveyance occurs between damaged and undamaged plants, although shortcomings may still be present (Table 1). Some critics will say that not a single study has met all criteria needed to support the hypothesis for a single system. Several studies have enclosed plants in small airtight bell jars or other types of containers for considerable periods of time (e.g. Farmer and Ryan, 1990; Shulaev et al., 1997;
Variation in plant responses
An important question is whether we expect to find information conveyance between damaged and undamaged plants for all plant species. And if plants of a certain species exhibit the ability, a relevant question is whether individuals of that species should always respond to information from damaged neighbours (Bruin et al., 1995). Such questions are common in other fields related to phenotypic plasticity such as learning in insects (Papaj and Prokopy, 1989; Vet et al., 1995). Can we identify
Above versus below-ground transfer of information
Most research on interactions between damaged and undamaged plants addresses the role of plant volatiles (Bruin et al., 1995; Shonle and Bergelson, 1995; Karban and Baldwin, 1997) and specific experiments have been designed to exclude below-ground communication (Zeringue, 1987; Farmer and Ryan, 1990; Bruin et al., 1992; Karban et al., 2000). However, interactions between plants and other organisms may also be mediated by chemical information in root exudates (Estabrook and Yoder, 1998). One
Comparison with research on the use of chemical information by animal receivers
In the study of chemical information transfer between plants, much can be learned from research on chemical information in interactions between animals. Optimal foraging theory assumes that animals are omniscient and take optimal decisions accordingly (Stephens and Krebs, 1986). Although this assumption has often been criticized as being unrealistic, there is growing evidence that animals exploit many sources of information to adjust their behavioural decisions (e.g., Milinski, 1990; Janssen et
Contributions to this special issue
Considering the importance of chemical information in the ecology of protozoa, invertebrate and vertebrate animals (Roitberg and Isman, 1992; Cardé and Bell, 1995; Kats and Dill, 1998; Kuhlmann et al., 1999; Tollrian and Harvell, 1999) and plant-parasitic plants (Estabrook and Yoder, 1998), it is important to investigate whether and how plants can perceive chemicals from damaged neighbours. At present the research field of plant-to-plant communication is mostly involved in such mechanistic
Acknowledgments
The authors thank Ian T. Baldwin, Erkki Haukioja, Arne Janssen, Rick Karban, John Pickett, Jack C. Schultz, and Teja Tscharntke for constructive comments on a previous version of the manuscript. MD was partially supported by the Uyttenboogaart-Eliasen Foundation, Amsterdam.
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