Journal of Plant EcologyPAGES 1–10

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A systematic review of the attractant-decoy and repellent-plant hypotheses: do plants with heterospecific neighbours escape herbivory?

Ally Ruttan* and Christopher J. Lortie

Department of Biology, York University, 4700 Keele Street, Toronto, Ontario M3J1P3, Canada*Correspondence address. Department of Biology, York University, 4700 Keele Street, Toronto, Ontario M3J1P3, Canada. Tel: +1-416-736-2100 ext. 33053; Fax: +1-416-736-5698; E-mail: aruttan@yorku.ca

Abstract

AimsThis systematic review highlights the relative support and implica-tions of the attractant-decoy and repellent-plant hypotheses, discuss-ing important linkages between these theories and the opportunity for novel integration into ecological and applied research.

MethodsAn extensive systematic review of the current literature on the attract-ant-decoy and repellent-plant hypotheses was done to describe the following attributes of the research to date: (i) the geographic extent (country and biome) of studies on this topic, (ii) the scope of experi-mental designs used, (iii) the level of support for these hypotheses with respect to the breadth of ecological niches tested, (iv) the level of support for these hypotheses with respect to the classes of herbi-vores examined and, lastly, (v) the ecological impact or purpose of these studies. Herein, we summarize important research gaps in the empirical literature on this topic and identify novel opportunities for critical linkages between ecological and applied theories.

Important FindingsA total of 37% of experiments testing these two associated hypoth-eses were done in North America, frequently in either temperate broadleaf (26% of studies) or taiga ecosystems (15% of studies).

The majority of these studies involved experimental manipulations such as removing and transplanting vegetation and either tracked or excluded mammalian herbivores. Ecological implications were primarily examined (59% of studies), but there were also implica-tions described for agriculture and commercial forestry in 22% of studies. The repellent-plant hypothesis was well supported in many ecological systems, particularly for mammalian herbivores, but the attractant-decoy hypothesis has been less frequently tested, thereby representing an important research gap. Insect herbivores were under-represented in all categories except in applied contexts such as commercial forestry and agriculture. There is a clear need for studies to connect these two ecological hypotheses with the man-agement of agriculture and restoration efforts in many ecosystems. Research on the co-evolution and facilitation between palatable and unpalatable plants also represents another novel area of future study.

Keywords: associated plant defence, attractant-decoy, herbivory, neighbour, repellent-plant, systematic review

Received: 15 April 2014, Revised: 13 October 2014, Accepted: 20 October 2014

INTROducTIONHerbivores present a major obstacle to plant survival. As such, many plants have developed defensive features to secure pro-tection from herbivore pressure. Plant defence mechanisms may include one or sometimes several of the following strategies:

chemical defences, mechanical defences, mimicry and/or an escape from herbivory in time or space (Atsatt and O’Dowd 1976; Baraza et al. 2006; Barton and Koricheva 2010; Littler et  al. 1986). A  recent meta-analysis on plant defences con-cluded that the strength and type of defence utilized by a plant depends on many factors including plant ontogeny, life-history

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strategy and the primary herbivore among other potential fac-tors (Barton and Koricheva 2010). Chemical resistance typi-cally includes the production of secondary metabolites and is a common defence mechanism in plants (Bryant et al. 1994; Dyer et al. 2001; Herms and Mattson 1992; Levin 1976; Rohner and Ward 1997; Wink 1988). These defences often use com-pounds such as alkaloids, non-protein amino acids, cyanogenic glycosides, glucosinolates and terpenes, which can either be continuously present in the plant or production can be induced when the plant is injured by herbivory for example (Bennett and Wallsgrove 1994; Wink 1988). These compounds offer protection through species-specific digestion inhibiting anti-nutritional effects and/or varying levels of toxicity, which deter herbivores especially when more suitable vegetation is avail-able (Bennett and Wallsgrove 1994; Palo 1985). Morphological features such as spines, thorns and barbs can be found on the stems and leaves of some plants as a form of mechanical defence against herbivory (Atsatt and O’Dowd 1976; Fernandes 1994; Jones et al. 2005; Lucas et al. 2000; Rohner and Ward 1997). These characters make it difficult for a herbivore to browse veg-etation as they can reduce the rate of food intake, cause physi-cal harm to the animal’s oral cavity and digestive tract as well as significantly (and prematurely) wear down their molars to the point where grinding food becomes difficult (Bee et al. 2009; Cooper and Owen-Smith 1986; Fernandes 1994). As an alter-native to morphological adaptations in plant structure, some plants secrete substances such as waxes or resins that change the texture of the plant to make them appear unattractive to herbivores (Levin 1976). Additionally, the production of sap that is secreted upon damage to the plant is often employed in areas where insects are the dominant herbivores, as it traps them and prevents further damage and burrowing of the insect into the plant tissue (Fernandes 1994; Levin 1976). Mimicry of toxic plants (or occasionally insects, e.g. some orchids) in sight (shape and colour), smell and taste has also been sug-gested as a means of herbivore avoidance in plants though it is not well documented (Barrett 1987; Eisner and Grant 1981; Launchbaugh and Provenza 1993; Lev-Yadun and Ne’eman 2012; Wiens 1978). Collectively, this body of research has demonstrated that while defences against herbivores are often effective, there are also energy costs associated with their pro-duction that can negatively impact plant growth and reproduc-tion (Agrawal 2000; Agrawal et al. 2002; Puentes and Ågren 2013). Co-evolution between plants and herbivores/predators is also common and can reduce the efficiency of these defences through the development of counter-defences or the evolution of tolerance for specific plant defences (Ali and Agrawal 2012; Ehrlich and Raven 1964; Mithöfer and Boland 2012). Specialist herbivores frequently co-evolve with their preferred plants to the extent that they may use the secondary metabolites pro-duced for defence as host recognition cues or even nutrient sources (Bennett and Wallsgrove 1994). However, there is another subset of defences less commonly studied in the plant–animal literature that are equally as important—associational defences.

While direct mechanisms can provide protection from herbivory, they also come with inherent trade-offs. As was previously mentioned, energy that would normally be allo-cated towards vegetative growth and reproduction is being reallocated for the production of anti-herbivory mechanisms including secondary metabolites, additional plant parts (e.g. thorns) and secretions (e.g. wax and resin) (Agrawal 2000; Agrawal et  al. 2002; Fine et  al. 2006; Puijalon et  al. 2011; Strauss et al. 2002). The avoidance of these costs is thus a set of selection pressures that can function to reduce or even eliminate these defences in some plant species. For instance, some plants do not possess individual-level defence mecha-nisms even in areas of high-intensity grazing but instead ben-efit from the use of anti-herbivory mechanisms of associated neighbouring plants (Atsatt and O’Dowd 1976; Barbosa et al. 2009; Wahl and Hay 1995). Two dominant hypotheses have been put forth in order to explain this escape strategy: the attractant-decoy hypothesis and the repellent-plant hypoth-esis (Atsatt and O’Dowd 1976; McNaughton 1978; Miller et al. 2007; White and Whitham 2000). Both hypotheses comprise part of the ecological research subdisciplines of associational resistance and associational plant refuges (APR), which pro-pose that herbivore consumption can be avoided by associ-ating with neighbouring plants that are of either higher or lower palatability levels (Feldman et  al. 2004; Hjalten et  al. 1993; Pfister and Hay 1988; Tahvanainen and Root 1972). The attractant-decoy hypothesis suggests that plants may be able to avoid consumption by herbivores if they neighbour more preferred, highly palatable plants (Bergman et al. 2005; Erickson et  al. 2012; Tahvanainen and Root 1972). These plants provide alternative food choices for the herbivore and act as ‘decoys’ that draw the herbivore away from the less-pal-atable plant, thereby protecting it from herbivory (Atsatt and O’Dowd 1976; Tahvanainen and Root 1972). Conversely, the repellent-plant hypothesis proposes that relatively palatable plants associated with low-palatability/highly defended plants receive protection from herbivory through patch avoidance (Atsatt and O’Dowd 1976; Bee et al. 2009; Tahvanainen and Root 1972). Plants with low palatability are naturally avoided by herbivores and therefore neighbouring plants that are asso-ciated with them are also avoided (Atsatt and O’Dowd 1976; Root 1973). Chemical and mechanical defences as well as the nutritional content of neighbouring plants play an impor-tant role in whether or not the focal plant will be browsed (Bee et al. 2009; Miller et al. 2009). Plants that exhibit dense branching or foliage patterns or that have thorns, barbs or irritating chemicals physically deter herbivores from grazing and offer similar protection for the species that surround them (Bee et al. 2009; Bergström 1992; Frid and Turkington 2001; Miller et al. 2009; Rousset and Lepart 2003). Likewise, focal plants with neighbours that have a low nutritive value are frequently avoided by herbivores even if access is unlimited, as the entire quality of the patch is reduced (Bee et al. 2009; Kuijper and Bakker 2008; Pietrzykowski et al. 2003; Valone and Giraldeau 1993). Consumption of these plants reduces

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the efficiency of grazing, thereby requiring the herbivore to increase their total food intake (Bee et  al. 2009; Bergman et al. 2005). While browsers with a diet consisting primarily of lower availability vegetation such as leaves, twigs, bark and fruit do selectively forage, grazers can afford to be espe-cially selective because they forage primarily on readily avail-able grasses and forbs (Augustine and McNaughton 1998; Glendinning 1994; Hofmann and Stewart 1972). To maximize efficiency, herbivores tend to forage in dense patches of palat-able vegetation (Pfister and Hay 1988). Thus, avoiding a patch of mostly low-nutrient plants altogether is beneficial to both the herbivore and neighbouring (often palatable) plants when there are other food choices present. Hence, the ecological framework is well established for the potential capacity for plants to avoid paying direct costs in developing defences by capitalizing on the defences of adjacent plants. However, the extent of the empirical tests and reported support for these plant–animal interactions has not been synthesized to date. By collectively examining these studies, we can further the potential for these ecological hypotheses to inform restoration techniques, sustainable agriculture and forestry practices and co-evolutionary dynamics in general.

This review uses formalized synthesis tools (Lortie 2013) to systematically examine the research on the attractant-decoy and repellent-plant hypotheses. This approach provides a clear assessment of the research scope including the presence of research gaps. The geographic/ecosystem range of these studies globally, level of reported support for these hypotheses with respect to the breadth of ecological niches and herbivore classes tested, the disciplinary biases and the scope of experi-mental designs used to test these hypotheses are examined. Description of this body of literature enhances understand-ing of the mechanisms of associational resistance and speaks to co-evolutionary theory (Ali and Agrawal 2012; Ehrlich and Raven 1964; Mithöfer and Boland 2012) and trade-offs in plants (Agrawal et al. 2002; Fine et al. 2006; Puijalon et al. 2011; Strauss et  al. 2002). Positive plant–plant interactions generally focus on habitat amelioration and abiotic pressures, but consumer pressure is also an important driver of popu-lation and community dynamics and thus an essential focus of facilitation literature (Daleo and Iribarne 2009; Graff and Aguiar 2011; Graff et al. 2007; Maestre et al. 2009; McIntire and Fajardo 2014). Accordingly, this review examines the capacity for plant–plant interactions to inform our under-standing of plant defence strategies and their application to many applied fields.

METHOdSLiterature search method

To determine the current state of primary, peer-reviewed research on the attractant-decoy and repellent-plant hypotheses, a systematic review was done using Thomson Reuters Web of Knowledge in February 2014. An initial search for publications was executed utilizing the search

terms ‘attractant-decoy’, ‘repellent-plant’, ‘associat* AND resistance AND herbiv*’, ‘associat* AND resistance AND herbiv* AND choice’, ‘defense AND guild AND herbiv*’ and ‘neighbo* AND herbiv* AND choice’. Following this, the references of relevant articles were scanned manu-ally to screen for additional studies producing a total of 323 possible publications (Supplementary Appendix 1). All articles underwent a preliminary title and abstract scan for relevance. The full text of articles that remained was processed, and articles that did not test the mechanisms of the attractant-decoy or repellent-plant hypotheses and secondary studies without primary data were excluded (see Supplementary Appendices 1 and 2). Articles that focused on indirect effects of herbivory (i.e. associational resistance mediated by the attraction of natural enemies) were also excluded because these mechanisms do not rely on the indi-vidual-level defence strategies of the neighbouring plant, and this review was focused only on the direct pathways of neighbour-mediated herbivore avoidance. Of the initial 323 articles that were sourced, 269 were not incorporated in this review due to duplication (24) or relevance (245) (Supplementary Appendix 1). The remaining 54 studies were composed of experiments from 1972 to 2013. A large proportion of studies were published in 2006 (13%), 2011 (13%) and 2012 (17%). All articles that were included in this review were published in English (or had an English manuscript) in a total of 24 different peer-reviewed jour-nals. Oecologica published the highest number of articles at 17%, followed by Oikos (13%) and then by Ecology (9%).

Analysis of the literature

Studies were coded by the country and biome under study, the type of experiment performed (lab trial, patch manipula-tion, field study/no manipulation), the ecological region and class of herbivore used (Mammalia, Insecta, Actinopterygii, Echinoidea and Malacostraca) and the purpose/discipline of the research (general ecology, agriculture, commercial forestry, invasion biology, biological control and restora-tion). Additionally, the author-reported level of support for the attractant-decoy and/or repellent-plant hypotheses was recorded as either ‘support’, ‘mixed’ or ‘no support’, where mixed support indicated that the authors reported support for one or both of the hypotheses in some instances but not in others. Studies spanning more than one category were coded as multiple instances and allotted half a database entry each so as not to inflate the importance of one particular study.

RESulTSGeographic range and biomes

Studies examining the attractant-decoy and repellent-plant hypotheses were conducted in 5 continents (North America, South America, Europe, Asia and Australia) comprising 18 countries (Fig.  1). The majority of studies were done in Europe and North America (Fig.  1). Both terrestrial and

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aquatic ecosystems were studied, but the majority of experi-ments were done in temperate broadleaf followed by taiga biomes (Fig. 2).

Types of experiments

There were three main types of experiments used to test the attractant-decoy and repellent-plant hypotheses in the stud-ies summarized herein. The first and most common type of experiment was ‘patch manipulation’ (66.67%) that directly altered patches of vegetation through removals, clippings, plantings or the addition of entire areas of vegetation (Fig. 3). Three ‘patch manipulation’ studies utilized captive herbivores, and two studies also used artificial food choices (e.g. pelleted feed) instead of plants in a cafeteria-style feeding experiment

(Bergvall et al. 2006; Rautio et al. 2008). Field studies com-prised 28.70% of the research and included observational surveys using existing vegetation and predators (Fig.  3). Finally, the least frequent experimental approach used lab tri-als at only 4.63% of the total studies and all were focused on herbivory in aquatic, marine environments (Fig. 3).

Ecosystems and herbivore classes

The attractant-decoy hypothesis was tested in only five eco-systems (artificial, grassland, coniferous forest, mixed forest and mangrove forest) with author-interpreted support in only artificial systems and mixed support in mangrove systems (Fig. 4A). The repellent-plant hypothesis has been tested in 11 ecosystems with author-interpreted support in 67.68% of

0 2 4 6 8 10 12 14 16

Tropical rainforestTemperate steppe

Temperate broadleafTaiga

Subtropical moist forestSubtropical dry forest

Sub-alpineSemi-arid grassland

Salt marshMountain forest

MediterraneanMarine

FreshwaterDry Steppe

CostalArid desert

Arctic

Number of Studies

Biom

e

Figure 2: the number of studies the attractant-decoy and repellent-plant hypotheses summarized by biome. The population of studies (n = 54) was generated using a formalized systematic review in Web of Science (see Methods for details).

Figure 3: the percentage of studies in this review (n = 54) that uti-lized a lab trial, patch manipulation or field study in their research of the attractant-decoy and/or repellent-plant hypotheses. The popula-tion of studies was generated using a formalized systematic review in Web of Science (see Methods for details).

Figure 1: a world map showing the geographic extent and number of studies of the attractant-decoy and repellent-plant hypotheses globally. Colours denote different numbers of studies conducted (total number of studies = 54). The population of studies was generated using a formal-ized systematic review in Web of Science (see Methods for details).

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studies (Fig.  4A). A  total of 65.67% studies that concluded support for the repellent-plant hypothesis were from grass-land, temperate broadleaf or ‘other’ ecosystems (marine, salt marsh, sand dune, wetland and tropical) (Fig. 4A). Note, vote-count support does not imply strength of evidence within studies (Koricheva et al. 2013) and is reported herein only as an indication to the reader of the consensus by researchers on the hypotheses tested within this subdiscipline.

A total of five classes of animal were used to test the attractant-decoy and repellent-plant hypotheses (Mammalia, Insecta, Malacostraca, Actinopterygii and Echinoidea) though Actinopterygii and Echinoidea were only used to test the latter hypothesis in aquatic environ-ments. Mammals were the dominant herbivore in 57.01% of the 54 studies with insects as the second most dominant predator class comprising 34.58% of the studies (Fig. 4B). Author-interpreted support was highly varied for the attractant-decoy hypothesis for all classes studied. Support was reported much more frequently for the repellent-plant hypothesis for all five animal classes (Mammalia: 72.73%, Insecta: 52.78%, Malacostraca: 100%, Actinopterygii: 100% and Echinoidea: 100%) (Fig. 4B).

Ecological purposes/discipline of studies

There were six general categories of application/disciplinary research that tested the attractant-decoy and repellent-plant

Figure 4: the varying levels of support (no support, mixed support, support) for the attractant-decoy and repellent-plant hypotheses with respect to (A) ecosystem type, which included alpine, artificial, coniferous forest, grassland, mixed forest, temperate broadleaf forest, or if there were two or less studies done there, other (mangrove, marine, rainforest, riparian, salt marsh, sand dune, semi-arid shrub land, tropical and wetland) and (B) the class of animal studied. The population of studies (n = 54) was generated using a formalized systematic review in Web of Science (see Methods for details).

Figure 5: a summary of the studies (n = 54) in this review by the class of animal studied (Insecta, Mammalia or other) classified by pri-mary research focus including ecological study, agriculture, commer-cial forestry, invasion biology, restoration and biological control. Full details of classification and search terms are listed in Methods.

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hypotheses: ecological, agricultural, commercial forestry, inva-sion biology, restoration and biological control (Fig. 5). Ecological studies directly tested the mechanisms of the attractant-decoy and repellent-plant hypotheses in 62% of the studies (Fig. 5). Applied research in fields such as agricultural, commercial forestry and restoration was infrequently tested (Fig.  5). Biological control was the least common category of study for the attractant-decoy and/or repellent-plant hypotheses with only one study published to date linking these ideas (Fig. 5). Mammals were most heav-ily utilized in studies testing the ecological framework of these hypotheses (64.18%) with insects used only 25.37% of the time (Fig.  5). In applied studies such as those involving agriculture and commercial forestry, insects were studied more frequently at 83.33% for agriculture and 50% for commercial forestry (Fig. 5).

dIScuSSIONThe attractant-decoy and repellent-plant hypotheses have been studied for their application in numerous fields including ecology, agriculture and commercial forestry (among others). This subdiscipline of plant defence strategies is becoming an increasingly important area of study for both the management of threatened, native species and for its economic importance to the commercial agriculture and forestry industries. These hypotheses have also been applied to the majority of natural ecosystems globally and have examined the most dominant herbivore classes suggesting their versatility in many ecologi-cal contexts. While there is diversity in the scope of the studies on this topic, there is nonetheless a significant bias towards mammalian herbivores in temperate ecosystems. The under-representation of insect herbivores is unfortunate because they are among the most important and damaging herbivores in many terrestrial systems (Coley and Barone 1996)—par-ticularly with respect to agricultural crops. Consequently, it is surprising that there were not more studies combining insect herbivores with these hypotheses in these systems.

The greatest proportion of the studies involving insect her-bivores were centred on biological control and the agricul-tural and commercial forestry industries. However, insects are important in many other respects and would be valuable for the study of the ecological and evolutionary theory associated with the attractant-decoy and repellent-plant hypotheses. Their short generation times (Belovsky and Slade 2000), cosmopoli-tan distribution and ability to alter plant distribution patterns (Louda and Rodman 1996; Maron and Crone 2006) make them suitable for the study of these hypotheses, especially with regard to their application to plant–herbivore co-evolution. While previous reviews have found that associational resist-ance is more prevalent with mammalian herbivores relative to insects (Barbosa et al. 2009), most studies that utilized insect herbivores reported support for the repellent-plant hypothesis (Karban 2007; Kostenko et al. 2012; Sholes 2008). This indi-cates that plant associations may have the capacity to mitigate and control insect population dynamics though more research testing the ecological mechanisms of this hypothesis is needed.

The repellent-plant hypothesis has received the most attention of the two mechanisms with most studies report-ing either full or mixed support (see Methods for definition) and only six instances where no support was found (e.g. see Letourneau 1995; Moravie et al. 2006; Plath et al. 2012; Rautio et  al. 2008). Support was reported by authors for a wide demographic and was not limited to any one ecosystem or animal class though support for mammalian herbivores was most frequently reported (e.g. see Bossuyt et  al. 2005; Boughton et al. 2011; Callaway et al. 2000, 2005; Cushman et  al. 2011). Even in instances where support was docu-mented, many studies discussed a growth trade-off between protection from herbivory and competition when herbivores are not present (Hay 1986; Kostenko et al. 2012; Pfister and Hay 1988). However, the benefits of having an unpalatable neighbour often constituted a net benefit toward the target plant (Levine 2000). Though support for the repellent-plant hypothesis is frequently reported, it is likely not applicable to all scenarios and may vary by species, ecosystem and overall resource availability. In species with individual (as opposed to patch) level foraging techniques, these hypotheses may not be a viable defence strategy. Herbivores in these complexes use the presence of individual palatable plants to forage and thus plant–plant interactions are less likely to be important (Danell et al. 1991; Jia et al. 1997).

The attractant-decoy hypothesis has received much less attention than the repellent-plant hypothesis to date. Additionally, of the few studies conducted, there has been little evidence for this hypothesis overall (e.g. see Bergman et  al. 2005; Erickson et  al. 2012; Frid and Turkington 2001; Hjalten et  al. 1993), with only two instances of support reported (Miller et al. 2006; Parker et al. 2007). In the study by Parker et al. (2007), Sparganium americanum, a plant with relatively low palatability to beavers, was only susceptible to herbivory in situations where palatable Polygonum densiflorum was unavailable. This suggests that the P.  densiflorum is act-ing as a ‘decoy’ for the beavers, drawing them away from plants of other species. Miller et  al. (2006) similarly found that seedlings were least vulnerable to herbivory when they were growing in patches of highly palatable species. In many instances where there was no support reported for the attract-ant-decoy hypothesis, associated susceptibility was proposed as an alternative mechanism (e.g. see Beckstead et al. 2008; Moravie et al. 2006; Rautio et al. 2008). Associated suscepti-bility suggests that palatable plants do not act as decoys for herbivores (as the attractant-decoy hypothesis states) but instead act as magnets and attract herbivores not only to the palatable plant but also to the neighbouring plants, increasing their likelihood of damage (Beckstead et al. 2008; Bee et al. 2009; Frid and Turkington 2001; Moravie et al. 2006; Rousset and Lepart 2003). While the attractant-decoy hypothesis is infrequently reported as an explanatory pattern for defence, it is nonetheless reasonable to propose that the strong mam-malian bias and near absence of studies on insect herbivores negatively skew the likelihood of detecting these effects. If it

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is applicable to insects, the attractant-decoy hypothesis will have important implications for managing insect pests in agri-cultural systems and in informing ecological theory of the capacity for plant–plant interactions to mediate plant–insect interactions. These are important opportunities for novel research associated with positive plant interactions (Brooker et al. 2008; McIntire and Fajardo 2014)

Most of the literature regarding the attractant-decoy and repellent-plant hypotheses was conducted in terrestrial habi-tats such as temperate broadleaf forests or grassland ecosys-tems. Interestingly, ‘other’ ecosystems such as mangrove, marine, rainforest, riparian, salt marsh, sand dune, semi-arid shrub land, tropical and wetland habitats frequently reported support for the repellent-plant hypothesis even though each was represented by less than two studies. These ecosystems can be highly stressed and have significant herbivore loads and, therefore, represent an important research gap. Gómez et al. (2001) proposed that systems such as the Mediterranean provide ideal systems to examine associational resist-ance because they are highly diverse in species at all scales. Mediterranean habitats are highly populated with a variety of herbivore groups, many of them generalists, and are therefore optimal for this type of study (Gómez et al. 2001). Freshwater systems (represented by only one article in this review) could also benefit from more research because the plant material provides an important source of organic matter and, subse-quently, nutrients for the system (Parker et al. 2007). Beavers, like many other terrestrial and marine herbivores, are selec-tive consumers of palatable plants and can alter the composi-tion of their habitats both directly and indirectly (e.g. through the change in plant composition leading to a change in nutri-ent content of the litter and soil) (Lubchenco and Gaines 1981). Beavers will frequently deplete areas so that only the most unpalatable plant species remain (Barnes and Mallik 2001). If palatable plant species secure refuge from herbivory through associated resistance (Parker et al. 2007), then novel management theory and planning associated with the pro-tection of wetlands in particular should consider these plant-mediated effects on trophic dynamics.

Similarly, herbivory rates are assumed to be higher in tropical versus temperate areas with the majority of damage being inflicted by insects on young, developing plants (Coley and Barone 1996). Mangrove habitats are among the most sensitive (and degraded) coastal, tropical systems globally (Chen et  al. 2009), and the attractant-decoy and repellent-plant hypotheses can provide experimentally testable predic-tions in terms of providing refuges (using other species or the addition of palatable/unpalatable plants) to reduce herbivore impacts on threatened species (Erickson et al. 2012). To the best of our knowledge, this is untested as a management tool. Importantly, regeneration is slow in these low-productivity systems making restoration of these areas challenging. Many current mangrove restoration projects resemble monoculture plantations and lack the diversity that a true mangrove sys-tem requires (Chen et al. 2009; Ellison 2000). Erickson et al.

(2012) demonstrated that the repellent-plant hypothesis could be utilized to protect sensitive seedlings that begin to grow post-disturbance. If the concepts of associational resist-ance could be applied to these systems in order to protect fragile seedlings or make use of decoy species, the entire sys-tem may have an increased capacity for natural regeneration. There are of course numerous limitations to both approaches including introductions of palatable/non-palatable non-native species to protect native species, but conceptually these hypotheses can be used to explore and define appropriate sets of alternatives. Plant–plant interactions can be a critical driver of community assembly in general, and we cannot afford to overlook the capacity for mediation of herbivore impacts in many impacted systems globally.

The implication of the repellent-plant hypothesis for applied research is a major research gap. For example, grazing of commercial seaweed by fish and sea urchins was drasti-cally reduced when neighbouring plants were less palatable (Ganesan et al. 2006). Nearly 10% of all commercial seaweed is commonly destroyed through herbivory, thereby cutting into profit margins (Ganesan et  al. 2006). Similar findings have been reported in commercial forestry wherein unattrac-tive, non-host trees lessened the colonization of Thaumetopoea pityocampa on host trees in the same area (Dulaurent et  al. 2012). It has also been suggested that the concepts of the repellent-plant hypothesis can be used to improve vegeta-tive and ecosystem restoration projects (Erickson et al. 2012; Smit et al. 2007) as described above. Smit et al. (2007) dem-onstrated that patches of unpalatable vegetation provide an important refuge for young shrub saplings in forests. These saplings are relatively unprotected as juveniles, but grow to become thorny and therefore unpalatable, acting as nurse plants for future tree saplings (Smit et al. 2007; Soliveres et al. 2014). The initial herbivore avoidance achieved through their association with other unpalatable plants is important long term for the regeneration of critical (and vulnerable) tree species (Smit et al. 2007; Soliveres et al. 2014). Studying the mechanisms associated with APR such as the repellent-plant hypothesis could also be very beneficial in reducing herbivory on food crops and commercial forests.

Research opportunities and novel concepts

Applied research and an expanded range of ecosystems are important extensions to the attractant-decoy and repellent-plant hypotheses because of their potential incorporation into the protection of crop plants and the restoration of degraded ecosystems. High-sensitivity regions and overgrazed systems could be ideal for the integration of associational resistance management tools. Most of the studies on this topic focused on mammalian herbivores, but there is every indication that the attractant-decoy and repellent-plant hypotheses can also be applied to invertebrates or other classes of animals. Lastly, we propose that there is a novel link between the attractant-decoy and repellent-plant hypotheses and the potential for co-evolu-tion between palatable and unpalatable plants. The occurrence

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of neighbour-mediated selection is dependent on whether a plant has a higher risk of being consumed within a group of other plants (palatable or unpalatable) or standing alone (Rautio et al. 2012). If a defended (i.e. unpalatable) plant does not experience a higher risk of consumption in the presence of a palatable plant than it would on its own, and the undefended (i.e. palatable) plant experiences a lower risk of herbivory in the presence of the defended plant than it would on its own, then the strength of both the defence and the plant–plant associations is subject to positive selection (Rautio et al. 2012). By furthering these two hypotheses, facilitation theory between plants can be extended to consumer pressure gradients in addition to environmental pressures even on evolutionary timescales.

FuNdINGNSERC Discovery Grant to C.J.L.

SuPPlEMENTARy MATERIAlSupplementary material is available at Journal of Plant Ecology online.Conflict of interest statement. None declared.

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