Integrating associational resistance into arable weed management

Agriculture, Ecosystems and Environment 142 (2011) 129–136

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Review

Integrating associational resistance into arable weed management Richard M. Gunton ∗ Institute of Integrative and Comparative Biology, University of Leeds, LS2 9JT, UK

a r t i c l e

i n f o

Article history: Received 2 June 2010 Received in revised form 19 May 2011 Accepted 20 May 2011 Available online 25 June 2011 Keywords: Agroecology Diversity Herbivore Natural enemy Resource concentration Spatial scale

a b s t r a c t This review considers how natural weedy vegetation affects herbivory in arable crops, and how such ‘associational effects’ may be set against other factors affecting crop yield that are better understood, such as competition for resources. Natural vegetation may reduce or increase herbivory by three broad categories of mechanisms: (1) directly, by altering the behaviour of herbivores, (2) indirectly by altering the behaviour of natural enemies or (3) indirectly by altering crop plants’ growth and physiology. The first category includes natural vegetation diverting herbivores away from crop plants, which appears to be the most beneficial effect, but this is sensitive to the spatial scales at which herbivores forage. There is little evidence that mechanisms in the second category significantly affect crop performance. The viability of crops is critically dependent on the dynamics of plant–plant interactions (the third category) and their interactions with associational effects. While few published studies demonstrate the potential for weedy vegetation to improve crop yields, there is clear scope for optimising weed management with regard to economics, pesticide use and conservation. © 2011 Elsevier B.V. All rights reserved.

Contents 1. 2.

3. 4.

5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanisms for associational resistance and associational susceptibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Herbivore behaviour: density and distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Enemies effects: a chain of hypotheses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Plant-quality effects: closing the feedback loop . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Multitrophic interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Associational resistance from additional natural vegetation – a viable proposition? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other effects of natural vegetation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Optimising crop–weed interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Timing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Spatial arrangement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Species composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Arable weeds often interfere with crop production by competing for resources (Lampkin, 2002), but natural vegetation that colonises crop stands can also reduce herbivory. Associational resistance occurs if plants growing in more-diverse stands of vegetation suffer less herbivory (Andow, 1991a). It has been scientifically investigated since the 1960s (van Emden, 1965; Smith, 1969) and may

∗ Tel.: +44 0113 3438215; fax: +44 0113 3431407. E-mail address: [email protected] 0167-8809/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2011.05.022

129 130 130 130 131 131 132 132 132 132 134 134 134 134 134

be attributed to a wide range of ecological processes. However, little work has been done on interactions between associational resistance and competitive interference, perhaps because it is difficult to disentangle these effects experimentally. The effects of diversifying field vegetation on crop yields have been reviewed by Andow (1991b) and Poveda et al. (2008), but improved understanding of where associational resistance occurs (Barbosa et al., 2009), of the economics of plant defences (Agrawal, 2011) and of the conservation value of agriculture (Jackson et al., 2007) together highlight the need to explore how natural vegetation can be managed to maximise associational resistance and minimise competition.

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This paper considers the range of mechanisms that may link crop yield to the presence of natural vegetation that develops in fields and field margins. This focus excludes intercropping (Vandermeer, 1989), which normally concerns substitution of one crop type for another, although some of this literature is relevant. The conclusions should contribute to integrated pest management (Kogan, 1998), besides wide-ranging conservation and aesthetic benefits. The relative importance of different mechanisms for associational effects is considered first, followed by the question of how cropping systems may be manipulated to obtain more benefits from natural vegetation at lower cost. 2. Mechanisms for associational resistance and associational susceptibility Two general hypotheses, first formulated by Root (1973), may explain reduced herbivory in more-diverse plant stands. The resource concentration hypothesis says that less-pure, less-dense or smaller stands of a herbivore’s host plants are less attractive to herbivores and therefore suffer less damage, while the enemies hypothesis says that more complex habitats support more predators and parasitoids, leading to increased herbivore mortality. A third set of hypotheses involves plant quality (Theunissen, 1994), where physiological or morphological changes induced by neighbouring plants make focal plants more resistant or less attractive to herbivores. This phenomenon, also termed “bottom-up effects” (Hooks and Johnson, 2003), is closely linked with plant competition. Combined hypotheses may also be tested, such as resource concentration effects on root herbivores leading to plant-quality effects on above-ground herbivores (Moore et al., 2003), or plant-quality effects via natural enemies (Ninkovic and Pettersson, 2003). Diversifying plant stands does not always reduce herbivore damage. In a recent meta-analysis, the presence of heterospecific neighbours was associated with increased and decreased damage to plants in similar numbers of cases; overall there was a significant reduction in herbivore abundance but not in plant damage (Barbosa et al., 2009). A review of arable studies found that pest pressure declined significantly in 52% of cases but increased in 12%, while crop yield increased significantly in 32% of cases but declined in 29% (Poveda et al., 2008). The phenomenon of increased herbivory in diversified plant stands is termed “associational susceptibility” (Brown and Ewel, 1987) and may be explained by another set of hypotheses concerning herbivore behaviour, natural enemy effects and plant quality effects. For arable crops, associational resistance is best documented by entomological studies using sown companion plants (Andow, 1991b; Tonhasca and Byrne, 1994). The following three sections therefore combine ecological reasoning with evidence from several meta-analyses to explore the possible associational effects of additional natural vegetation on all kinds of herbivory. The aim is to identify the mechanisms that are most conducive to sustained yields by first considering herbivore behaviour, natural enemy effects and plant quality effects in turn, and then considering a conceptual model for multitrophic interactions and competition. 2.1. Herbivore behaviour: density and distribution A large number of mechanisms have been proposed for direct effects of plant diversity on herbivores (e.g. Finch and Collier, 2000; Norris and Kogan, 2000; Hambäck and Beckerman, 2003; Barbosa et al., 2009). However, an important distinction should be made between effects on population density and on distribution. The combined effect of crop and non-crop plants may attract herbivores to a field, repel them from it or stimulate population growth or decline – affecting population densities. At the same time, the

juxtaposition of different plant species, or of plant stands differing in composition, may lead to herbivores discriminating between the different qualities of habitats on offer – altering their distributions. The distinction is similar to the “coarse-grained” vs. “fine-grained” habitat distinction introduced by Levins and Macarthur (1966). The relative importance of these effects for herbivores and natural enemies will depend on their foraging behaviours and the spatial arrangement of crops, and may vary with different stages of life-cycles and foraging. Herbivore densities can be affected by repulsive volatiles. In some cases herbivores may be repelled by non-host-plant volatiles – as, e.g., for ovipositing cabbage white Pieris rapae (Hern et al., 1996), though not for foraging cabbage root fly Delia radicum and onion root fly D. antique (Finch et al., 2003). Masking of host plant odours by other plants has been widely proposed but rarely demonstrated (but see Thiery and Visser, 1986), though it may be conceptually inseparable from repellence (Schroeder and Hilker, 2008). Such effects support the resource concentration hypothesis (Root, 1973) so long as non-crop plants are close enough to crop plants to prevent herbivores discriminating between emitting and non-emitting plants. The resource concentration hypothesis may also be attributed to altered herbivore distributions. Non-crop seedlings can divert limited local populations of slugs away from crop seedlings among which they are interspersed (Cook et al., 1997; Frank and Barone, 1999; Brooks et al., 2005) – also described as a dilution effect. For specialist airborne insect herbivores, the appropriate/inappropriate landings theory (Finch and Collier, 2000) proposes that herbivores land indiscriminately on green surfaces once olfactory cues from a host plant are present; it has been supported in studies of cabbage and onion root flies, where foraging is disrupted by weeds covering bare soil and extending to at least 50% of the height of the crop (Finch and Collier, 2000). At the wholefield scale, strips of suitable “barrier” or “trap” vegetation bordering a crop can be effective for impeding invasion by aphids (Hooks and Fereres, 2006). The push–pull strategy (Shelton and Badenes-Perez, 2006; Cook et al., 2007) combines two elements: sacrificial crop stands, bordering or interspersed with a main crop, attract herbivores, while companion plants within the crop repel them (Khan et al., 2008). This may be the best approach for protecting crops from mammal herbivory (Bilenca et al., 2007), although it may be too species-dependent to work with natural vegetation. Importantly, associational susceptibility may arise if weeds increase the density of herbivores by providing supplementary food resources or cover. For example, a palatable cover crop such as red clover may increase populations of generalist herbivores such as slugs (Vernava et al., 2004) – both by attracting individuals and by facilitating reproduction. Associational susceptibility could also result from altered herbivore distributions if herbivores were attracted to crop stands in proportion to the amount of vegetation cover, as they might be by a visual cue, and were then repelled from the non-crop vegetation onto the crop. Some evidence suggests that host plants in smaller patches suffer more herbivory (Hambäck et al., 2010). It is not clear whether additional vegetation would effectively fragment a crop into small patches for this purpose and the resource dilution hypothesis (Otway et al., 2005) needs further investigation for arable habitats. 2.2. Enemies effects: a chain of hypotheses Meta-analyses of field experiments have found positive effects of habitat diversity on natural enemy abundances (Langellotto and Denno, 2004; Bianchi et al., 2006). However, an early review of agricultural studies found little evidence that natural enemies effectively reduce herbivory (Risch et al., 1983), and this conclusion was recently upheld (Jonsson et al., 2008). Moreover, studies com-

R.M. Gunton / Agriculture, Ecosystems and Environment 142 (2011) 129–136

paring natural enemies with resource concentration effects suggest that natural enemies tend to be relatively ineffectual (Kemp and Barrett, 1989; Rämert and Ekbom, 1996; Bjorkman et al., 2010). Nevertheless, crop damage was reduced or yield increased in 22 out of 31 studies that directly manipulated generalist natural enemies with non-intrusive methods (Symondson et al., 2002). This leaves the questions (i) whether the causal chain from diversification through to reduced herbivory via natural enemies is strong enough to be useful in field conditions and (ii) whether it can be promoted by natural vegetation without causing unacceptable yield loss. Regarding the latter, vegetation that supports generalist predators over winter (Frank, 2010) or in field margins may occupy land that could otherwise be cropped, and can be a source of weed invasions (De Cauwer et al., 2008). Regarding the former, a scale-specific meta-analysis found that increased predator densities resulted from diversifying plant stands in plots of between 16 and 256 m2 , but not in larger plots (Bommarco and Banks, 2003), suggesting a local displacement of natural enemies from uniform to diversified experimental plots. Given the rarity of field-scale experiments, this casts some doubt on the reliability of natural enemies effects at whole-field scales, since the density response of natural enemies observed in fine-scale experiments may partly depend on altered distributions at broader scales. In addition, the spatial aggregation of predators to prey may not be sustained across whole fields (Pearce and Zalucki, 2006). The distinction between effects on population density and on distribution applies to natural enemies as it does to herbivores. The possibility of associational susceptibility due to natural vegetation repelling, inhibiting or diverting natural enemies has been considered conceptually (Norris, 2005) and occasionally reported (e.g. Kemp and Barrett, 1989). This could result from non-crop plants either attracting natural enemies away from crop plants at a fine scale, or repelling them and reducing their densities in the whole stand, either way allowing herbivores to escape attack. 2.3. Plant-quality effects: closing the feedback loop When plants are competing for resources, they grow more slowly and affect each other’s architecture, morphology and metabolism. Norris and Kogan (2000) cite cases of weeds reducing the nutritive value of crop plants to herbivores, which could result in associational resistance with severely reduced yield. Competition may also inhibit crops’ herbivory defences, producing associational susceptibility. The expression of trypsin inhibitors by Brassica napus plants can be decreased by competition (Cipollini and Bergelson, 2001), resulting in increased susceptibility to herbivory (Cipollini and Bergelson, 2002). Indeed, Bukovinszky et al. (2004) showed that Brussels sprouts plants stunted by competition were both more attractive and more nourishing to Pieris brassicae larvae. However, competition need not be symmetric (Freckleton and Watkinson, 2001), so in favourable conditions the effects of crop on non-crop plants could be more significant than vice versa. If stunted plants are more attractive to certain herbivores (e.g. boring and sucking insects, Koricheva et al., 1998), there is the possibility of additional vegetation acting as an uncompetitive sink for such pests. However, the widely-supported plant vigour hypothesis (Price, 1991; Cornelissen et al., 2008), which says that herbivores prefer more vigorous plants, suggests that crop–weed competition can only be detrimental if it affects herbivore distributions at the scale of individual plants. Even competition with neighbouring plants does not necessarily compromise a plant’s resource allocation to herbivore defences (Cipollini, 2004). Some secondary metabolites appear to be adaptive to both challenges (Lankau and Kliebenstein, 2009), so that mild competitive stress may simultaneously increase plants’ defences against herbivory (Siemens et al., 2003). If this is the case

Association of crop and noncrop plants

(1) Herbivore preference for non-crop plants

131

Heterospecific competition

(2) Defences level of crop relative to non-crop plants

(3’) Herbivory of non-crop relative to crop plants

(3)

Competitive advantage of crop over noncrop plants

Growth of crop relative to noncrop plants

Crop yield

Fig. 1. A model of possible interactions in the allocation of resources between crop and non-crop plants. Each rectangular box represents a comparison between crop and non-crop plants for herbivore behaviour (left column) and plant responses (right column). Solid arrows indicate effects assumed to be positive; dotted arrows indicate effects that could be either positive or negative (with numbers referring to hypotheses in the text). All the effects being positive could lead to increased crop yield.

for crop plants then the additional cost of competition could be minimal in situations with frequent herbivore attack (Gurevitch et al., 2000; Parmesan, 2000; Haag et al., 2004). Similarly, the impact of herbivory on fitness depends on the extent to which growthlimiting resources are lost or foregone (Wise and Abrahamson, 2007). For example, a crop suffering leaf herbivory may not be at much competitive disadvantage if growth were mostly limited by competition for water. However, herbivory must ultimately reduce a plant’s fitness (Crawley, 1997, p. 443). 2.4. Multitrophic interactions Interactions among herbivory and competition could lead to self-reinforcing dynamics. The conceptual model in Fig. 1 shows how positive feedback may arise (the bracketed numbers below refer to arrows in Fig. 1). Supposing that (1) additional vegetation alongside crop plants diverts herbivores away from the crops and (2) the crop plants’ systemic responses to heterospecific neighbours also have a defensive effect against herbivory, both of which give the crop an early competitive advantage, while (3) herbivores prefer more stressed plants (i.e. the additional vegetation, or marginal crop plants): then sustained yield increases could result. By contrast, if (1) additional vegetation increases herbivore pressure on crop plants and (2) heterospecific competition compromises crops’ herbivory defences, both reducing the crop’s competitive advantage, and (3) whatever responses the crop does have to herbivore attack divert resource allocation away from crop growth, then com-

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plete crop failure could ensue. Theoretical studies probing some of these factors in a food web with two plant species and a herbivore (Grover and Holt, 1998) and a predator (Caron-Lormier et al., 2009) show the complexity of such systems and suggest a framework for further investigation of crop–weed–herbivore dynamics. Some experimental studies already show the potential for complex tritrophic interactions (Ninkovic and Pettersson, 2003) and the persistent effects of altered plant quality during a season (Bukovinszky et al., 2010). 2.5. Associational resistance from additional natural vegetation – a viable proposition? This review of associational resistance mechanisms suggests that (a) additional natural vegetation often affects herbivory but the outcome in a particular case (associational resistance or associational susceptibility) is difficult to forecast or control; (b) direct herbivore effects are probably greater and more predictable than enemies effects; (c) the plant-quality effects of additional vegetation are critical and their dynamics in the field need further investigation; (d) the distinction between density and distribution effects highlights the importance of studies at appropriate spatial scales; and (e) detailed knowledge of the prevalence and ecology of specific crops, weeds, herbivores and natural enemies will be required for predicting outcomes in a given situation. To date, few experiments on associational resistance using additional natural vegetation have reported final crop yield, and those that do mostly report reduced yields (Table 1). There may additionally be a reporting bias against negative effects on yields, since severe herbivore damage can render crop yield unmeasurable (e.g. HansPetersen et al., 2010). However, for economic purposes, crop quality must be considered alongside yield. The market for vegetable crops has low tolerance of herbivore damage (Grundy et al., 2003), so that the ideal balance between associational resistance and yield loss through competition may not be that which maximises gross yield (Theunissen et al., 1995; Theunissen and Schelling, 1998). Growers of high-value Brassica crops are especially likely to benefit, since herbivory has a large effect on their market value, and wild Brassica species may offer important trap-cropping effects (Altieri and Gliessman, 1983; Ahuja et al., 2010). 3. Other effects of natural vegetation Natural vegetation may have other benefits such as improving soil structure, reducing erosion and fixing nitrogen (Lampkin, 2002). Vegetation present before a crop emerges and again after harvest may provide such benefits without directly affecting crops. Natural vegetation that develops during fallow periods may have important effects on soil-dwelling invertebrates, and may be preferable to cover crops for limiting the abundance of nematodes (Gruver et al., 2010). The risks of natural vegetation, besides those of competition, include weeds interfering with the application of sprays such as fungicides to crop tissues, contaminating the harvest or interfering with harvesting machinery (Caussanel, 1989) – problems mostly resulting from severe infestations (Lampkin, 2002; Grundy et al., 2003) or problematic weed–crop combinations. Allelopathic properties may also be common among arable weeds (Om et al., 2002; Chon and Nelson, 2010). Weeds may increase the incidence of fungal diseases by acting as vectors or by their effects on microclimate (Duffus, 1971; Wisler and Norris, 2005; but see Iannetta et al., 2010). On the other hand, herbivores such as aphids can also be vectors of pathogens, so associational resistance may be accompanied by reduced incidence of diseases (Hooks and Fereres, 2006).

Regardless of the potential for yield improvement, additional natural vegetation is unavoidable in agriculture, so understanding the relationship between its associational, competitive and other effects is important.

4. Optimising crop–weed interactions Extensive work in both theoretical and agronomic contexts has shown that the size, proximity and species identity of plants are important for competition (e.g. Benjamin and Aikman, 1995; Hock et al., 2006; Schneider et al., 2006). Whereas conventional weed management aims to reduce natural vegetation densities until competitive impacts become negligible (Canner et al., 2009), an appreciation of associational effects, as reviewed above, may suggest alternative approaches and thresholds. This section considers how the phenology, spatial arrangement and species composition of natural vegetation could each be optimised with respect to associational and competitive effects. In view of the conclusions above, the main focus is on using natural vegetation to affect herbivore behaviour while minimising competition between crop and non-crop plants.

4.1. Timing When crops are planted, the relative sizes of crop and non-crop plants become very important because size-asymmetric competition can magnify initial differences in plant sizes (Weiner and Damgaard, 2006). This insight is elaborated in the concept of critical periods for weed control (Nieto, 1960). Assuming crops are sown into bare ground, the critical period is defined as the window of time following crop emergence that starts when emerging weeds would inflict significant yield losses if not removed, and finishes when the crop is big enough to be unaffected by newly emerging weeds. Assuming post-emergence weeding techniques are available, the critical period is thus the minimum period during which non-crop vegetation should be removed in order to avoid significant loss of crop yield (Knezevic et al., 2002) or quality (Merotto et al., 2009). Considering associational effects raises the question whether noncrop plants can reduce herbivory even if they are removed at an early stage or if they occur low in a competitive hierarchy later in the growing period. Where non-crop vegetation covers bare ground and deters oviposition early in the growing season, it is probably effective before the crop canopy closes over. Examples include the protection from slugs afforded by early-emerging weeds to young wheat plants (Cook et al., 1997) and plant-quality effects accrued from natural vegetation before crops are planted (den Belder et al., 2000). The potential for late-germinating companion plants to provide associational resistance is illustrated by studies where Brassica crops suffered less herbivory and no yield loss when mustard was sown 1 week after the crop was planted (Kloen and Altieri, 1990), or when weeds were allowed to develop 2 or 4 weeks after planting (Altieri and Gliessman, 1983). Similarly, Finch and colleagues (Finch and Kienegger, 1997; Finch and Collier, 2000; Finch et al., 2003) found that low-growing plant cover reduced oviposition by Delia spp. However, Asman et al. (2001) found that clipping clover down to 10 cm instead of 30 cm removed its deterrent effect on Plutella xylostella oviposition. Where associational resistance depends on tall companion plants it would be difficult to obtain without significant yield loss, but these results suggest it could be economical to modify the timing of weed-removal from recommendations based purely on studies of competition. Optimising the critical period approach will depend on understanding the ecology of the weed species present (Section 4.3; Norris, 2007).

Table 1 Reported effects of weeds on crop yield (comparisons with weed-free monoculture; medians calculated where rows summarize several experiments). Crop

Amount/type of weed cover at harvest or last sampling

Sugar beet

Effects on herbivore abundances and/or herbivorya

Effects on natural enemy abundancesa

Fewer Brachycaudus helichrysi −2

*

181 gm

Greater populations of 9 out of 11 taxa; no reduction in herbivory

Alfalfa

145 gm−2

−44%* Hypera brunneipennis

Collards

Brassicaceae spp.

−9% herbivory

Brussels sprouts

Did not overtop crop plants

−20%# Pieris rapae eggs; −54%# larval survival

Collards

Non-Brassica ceae spp.

−24% herbivory

Sugar cane

49 gm−2 (grasses)

Sugar cane

80 gm−2 (mixed spp)

Maize

34–47% cover

Oilseed rape

170 plants m−2 b

Sugar cane

45 gm−2 (forbs)

Oilseed rape

180 plants m−2 b −2

Greater populations of 9 out of 14 taxa

Number of years’ data used

Reference

−71%*

1

Dewar et al. (2000)

−61%

2

Showler and Greenberg (2003)

−54%

1

Norris et al. (1984)

*

+240% (carabids and coccinellids; no effects on parasitoids) +450%* Harpalus rufipes (carabid); no effects on parasites +720%* (taxa as above)

−41%

1

Schellhorn and Sork (1997)

−37%#

1

Dempster (1969)

−19%

1

Schellhorn and Sork (1997)

+28%* ground-based prey; +71%* foliage-based prey +36%* ground-based prey; +61%* foliage-based prey Fewer* Spodoptera frugiperda, aphids and nitidulid beetles Less damage by Delia sp. larvae

+8% (ground-based); +29% (foliage-based) +37% (ground-based); +16% (foliage-based) More* carabid beetles

−19% (−25% financial return) −5.8% (−16% financial return) −4.4%

3

Ali and Reagan (1985)

3

Ali and Reagan (1985)

1

Penagos et al. (2003)

−1.3%

2

Dosdall et al. (2003)

+14%* ground-based prey; +11%* foliage-based prey Less damage by Delia sp. larvae

+18% (ground-based); −4% (foliage based)

+1.9% (+5.7% financial return) +4.8%

3

Ali and Reagan (1985)

2

Dosdall et al. (2003)

*

Collards

440 gm

−81% Phyllotreta cruciferae; −45% [proportion of leaves damaged after 45 d]

+6%

1

Altieri and Gliessman (1983)

Collards

55 gm−2 b (only from 14 d after planting)

−15%* Phyllotreta cruciferae; −18% [proportion of leaves damaged after 45 d]

+14%

1

Altieri and Gliessman (1983)

Collards

52 gm−2 b (only from 28 d after planting)

−14%* Phyllotreta cruciferae; −18% [proportion of leaves damaged after 45 d]

+69%

1

Altieri and Gliessman (1983)

*

R.M. Gunton / Agriculture, Ecosystems and Environment 142 (2011) 129–136

Cotton

*

Change in harvest yield (mean for all years)

# No significance test reported; * P < 0.05. a The herbivore and enemies data are means over all survey dates reported. b In these experiments, crops were kept weed-free for part of the season.

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4.2. Spatial arrangement For maximum yields, associational resistance should ideally be obtained from non-crop plants growing at some distance from crop plants. The natural enemies hypothesis is relevant here because it refers to polyphagous predators that are sufficiently mobile to move between crop and non-crop resources. In a model where natural enemies moved by diffusion, spacing of habitat strips had large effects on their abundances in the crop, depending on dispersal rates, which are highly variable (Corbett and Plant, 1993). However, doubts about the viability of exploiting natural enemies were raised above (Section 2.2). Trap-cropping studies suggest using a border of trap crop around the edge of a field and further blocks within it, amounting to 10% of the crop area (Hokkanen, 1991). In an experiment where long narrow beds of broccoli were interrupted by bands of weeds at three different spacings (Banks, 1998), flea beetle Phyllotreta cruciferae colonisation was reduced by bands four m apart more than by larger spacings. Here the contrasting treatments were separated by strips of just 3 m, so the beetle may also have been locally diverted from less- to more-favourable treatments. In general, animal distributions are easiest to manipulate at fine spatial scales, where vegetation creates alternative microhabitats. A meta-analysis of herbivore abundance analyses (Bommarco and Banks, 2003) found that experiments with plots of the smallest class (<16 m2 ) showed the greatest reductions in herbivore abundance in diversified plots; it is reasonable to assume that these plots were closer together than those in experiments using larger plots. More scale-conscious experimental studies confirm the decay of diversion responses with increasing spatial separation between contrasting habitats (e.g. Hambäck et al., 2009).

4.3. Species composition Although wild species closely related to the crop may be effective in diverting herbivores, promoting them can be technically difficult and they carry the risk of increasing herbivore densities overall and of spill-over into the crop; they may also attract additional herbivores (Capinera, 2005) and compete strongly for resources (Silvertown, 2004). Other wild species can still promote associational resistance, and entirely unrelated species may certainly divert generalist herbivores such as slugs (Cook et al., 1997; Kozlowski and Kozlowska, 2000). To evaluate the usefulness of different floras for fully integrated pest management, a catalogue of the functional ecology of different weed species is needed. Growth rates and competitive indices have been calculated for common British weeds (Storkey, 2004) and there is some information on allelopathic interference via chemical secretions and residues, e.g. from couch grass Agropyron repens (Sagar and Ferdinandez, 1976) and wild oats Avena sativa (Perez and Ormenonunez, 1991). It is also possible to propose useful species for promoting enemies effects (Marshall et al., 2003; Storkey, 2006) – e.g. Cerastium fontanum, with many associated invertebrates but no pest species and a low competitive index. Useful species should be capable of attracting predators far more than pests (“selective food plants”; cf Baggen et al., 1999). In general, naturally-occurring floras are related to local conditions, tillage and fertilisation regimes and the weeding technologies employed (McCloskey et al., 1996; Ghersa et al., 2000; Légère et al., 2005), and the complex interplay of these factors makes local knowledge invaluable (Shennan, 2008). The availability of selective weed management techniques will increase the value of knowing which species are most valuable for integrated pest management. At the same time it may be economical to select crop cultivars that

are more competitive (Efthimiadou et al., 2009) and that complement the local flora (Smith et al., 2010). 5. Conclusions Although natural vegetation can be a liability for farmers, it may serve to divert herbivores away from crop plants. This may produce agronomic benefits, especially with crops that are less sensitive to competition and where market value is subject to cosmetic criteria. Studies are needed that help to disentangle associational effects from competitive effects, that discriminate among the different hypotheses for associational resistance and susceptibility, and that report market values of crops with and without additional vegetation. Associational effects should be considered at all policy levels, from agronomic decision-making to public planning, so that effective associational resistance mechanisms are combined with strategies to limit yield loss through competition. This could increase the economic advantages of agri-environment schemes, organic farming systems and agricultural enterprises in general, bringing benefits for agricultural efficiency, conservation and scientific understanding. Acknowledgements I thank Gareth Davies and Andrea Grundy for input in earlier stages of this review, and Kristin Hanzlik and two anonymous reviewers for helpful suggestions. The opportunity to begin this review was provided by a student bursary from the Henry Doubleday Research Association (now Garden Organic). I declare no involvement of funding organisations. References Agrawal, A.A., 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25, 420–432. Ahuja, I., Rohloff, J., Bones, A.M., 2010. Defence mechanisms of Brassicaceae: implications for plant–insect interactions and potential for integrated pest management. A review. Agron. Sustain. Dev. 30, 311–348. Ali, A.D., Reagan, T.E., 1985. Vegetation manipulation impact on predator and prey populations in Louisiana sugarcane ecosystems. J. Econ. Entomol. 78, 1409–1414. Altieri, M.A., Gliessman, S.R., 1983. Effects of plant diversity on the density and herbivory of the flea beetle, Phyllotreta cruciferae, in California collard, Brassica oleracea, cropping systems. Crop Prot. 2, 497–501. Andow, D.A., 1991a. Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36, 561–586. Andow, D.A., 1991b. Yield loss to arthropods in vegetationally diverse agroecosystems. Environ. Entomol. 20, 1228–1235. Asman, K., Ekbom, B., Ramert, B., 2001. Effect of intercropping on oviposition and emigration behaviour of the leek moth (Lepidoptera, Acrolepiidae) and the diamondback moth (Lepidoptera, Plutellidae). Environ. Entomol. 30, 288–294. Baggen, L.R., Gurr, G.M., Meats, A., 1999. Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol. Exp. Appl. 91, 155–161. Banks, J.E., 1998. The scale of landscape fragmentation affects herbivore response to vegetation heterogeneity. Oecologia 117, 239–246. Barbosa, P., Hines, J., Kaplan, I., Martinson, H., Szczepaniec, A., Szendrei, Z., 2009. Associational resistance and associational susceptibility: having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40, 1–20. Benjamin, L.R., Aikman, D.P., 1995. Predicting growth in stands of mixed species from that in individual species. Ann. Bot. 76, 31–42. Bianchi, F., Booij, C., Tscharntke, T., 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. Lond. B: Biol. 273, 1715–1727. Bilenca, D.N., Gonzalez-Fischer, C.M., Teta, P., Zamero, M., 2007. Agricultural intensification and small mammal assemblages in agroecosystems of the Rolling Pampas, central Argentina. Agr. Ecosyst. Environ. 121, 371–375. Bjorkman, M., Hamback, P.A., Hopkins, R.J., Ramert, B., 2010. Evaluating the enemies hypothesis in a clover-cabbage intercrop: effects of generalist and specialist natural enemies on the turnip root fly (Delia floralis). Agr. Forest Entomol. 12, 123–132. Bommarco, R., Banks, J.E., 2003. Scale as modifier in vegetation diversity experiments: effects on herbivores and predators. Oikos 102, 440–448.

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