skip to main content


Title: Environmental context and herbivore traits mediate the strength of associational effects in a meta‐analysis of crop diversity
Abstract

Crop diversification offers a promising solution to meet expanding global food demands while maintaining ecosystem services. Diversification strategies that use mixed planting to reduce pest damage (e.g. intercropping), termed ‘associational effects’ (AE) in the ecological literature, can decrease (associational resistance) or increase (associational susceptibility) herbivore abundance on a focal plant. While application of AE to agroecosystems typically reduces pest abundance, the range of outcomes varies widely.

We conducted a meta‐analysis using 272 estimates of insect herbivore abundance on crops neighbored by a conspecific or heterospecific from 44 studies undertaken on six continents. We focus on four agricultural crops well represented from sites across the globe to test hypotheses related to understanding how herbivore traits (diet breadth, feeding guild, origin), plant traits (crop type, phylogenetic distance to neighbour) and environmental context (climate, experimental design) contribute to variation in the outcomes of AE.

Overall, bicultures provided a strong reduction of insect abundance on the focal crop. Climate and interactions between herbivore traits, particularly diet breadth and origin, and plant traits or environmental context mediated the strength of AE.

Bicultures provided the strongest reductions in insect abundance at low latitudes, and this effect decreased at higher latitudes but only for insects with certain traits. Abundance of generalist herbivores and globally distributed pests tended to be most strongly negatively affected by bicultures, under certain contexts, whereas specialist herbivores and native pests were less affected by neighbours.

Synthesis and application. This meta‐analysis highlights that crop diversification schemes have an overall strongly beneficial effect of reducing pest abundance. However, there was also variability in the outcomes that is determined in part by the interactive effects of herbivore traits and environmental context. The results provide guidance for incorporating beneficial ecological interactions into integrated pest management strategies.

 
more » « less
Award ID(s):
1901552
NSF-PAR ID:
10405202
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Applied Ecology
Volume:
60
Issue:
5
ISSN:
0021-8901
Page Range / eLocation ID:
p. 875-885
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Associational effects—in which the vulnerability of a plant to herbivores is influenced by its neighbors—have been widely implicated in mediating plant–herbivore interactions. Studies of associational effects typically focus on interspecific interactions or pest–crop dynamics. However, associational effects may also be important for species with intraspecific variation in defensive traits. In this study, we observed hundreds ofDatura wrightii—which exhibits dimorphism in its trichome phenotype—from over 30 dimorphic populations across California. Our aim was to determine whether a relationship existed between the trichome phenotype of neighboring conspecifics and the likelihood of being damaged by four species of herbivorous insects. We visited plants at three timepoints to assess how these effects vary both within and between growing seasons. We hypothesized that the pattern of associational effects would provide rare morphs (i.e., focal plants that are a different morph than their neighbors) with an advantage in the form of reduced herbivory, thereby contributing to the negative frequency‐dependent selection previously documented in this system. We found the best predictor of herbivory/herbivore presence on focal plants was the phenotype of the focal plant. However, we also found some important neighborhood effects. The total number of plants near a focal individual predicted the likelihood and/or magnitude of herbivory byTupiochoris notatus,Lema daturaphila, andManduca sexta. We also found that velvety focal plants with primarily sticky neighbors are more susceptible to infestation byTupiochoris notatusandLema daturaphila. This does not align with the hypothesis that associational effects at the near‐neighbor scale contribute to a rare‐morph advantage in this system. Overall, the results of our study show that the number and trichome‐morph composition of neighboring conspecifics impact interactions betweenD. wrightiiand insect herbivores.

     
    more » « less
  2. Abstract

    Forest structure and diversity can regulate tree vulnerability to damage by insects and pathogens. Past work suggests that trees with diverse neighbours should experience less leaf herbivory and less damage from specialist herbivores and diseases, and that the effect of neighbourhood diversity should be strongest at small spatial scales.

    In an early stage temperate tree diversity experiment, we monitored damage from leaf removing herbivores, specialist (gallers and leaf miners) herbivores, and two specialist fungal diseases (maple leaf anthracnose and cedar apple gall rust) over 3 years. The experimental design included treatments that varied independently in phylogenetic and functional diversity and we made our analyses across four spatial scales (1–16 m2).

    Neighborhood diversity simultaneously increased leaf removal for some species, decreased it for others, and had no effect on yet others. Height apparency—the difference between a focal plant’s height and its neighbours’—was the best single predictor of leaf removal across species and spatial scales, but the strength and direction of its effect were also species‐specific.

    Specialist pathogens and fungal foliar diseases showed signs of associational resistance and susceptibility. Oaks (Quercusspp.) were more resistant to leaf miners and maples were more resistant to anthracnose when surrounded by diverse neighbours (associational resistance). In contrast, birches (Betula papyrifera) were more susceptible to leaf miners and eastern red cedars (Juniperus virginiana) were more susceptible to cedar apple gall rust (Gymnosporangium juniperi‐virginianae) infection in diverse environments (associational susceptibility).

    Herbivore and pathogen damage was better predicted by community structure and diversity at small spatial scales (1 and 4 m2) than large scales (9 and 16 m2), suggesting a characteristic spatial scale for these biodiversity‐ecosystem functioning effects.

    Synthesis.Humans control forest diversity through selective harvesting and planting in natural stands and plantations. Our experimental demonstration of the role of local community structure and diversity in suppressing some forms of pest and pathogen damage to trees suggests that forest management can be most effective when diversity is considered at small spatial scales and the underlying biology of particular pests, pathogens, and hosts is taken into account. Pictured here: the “galls” formed by cedar apple gall rust (Gymnosporangium juniperae‐virginiae) on eastern red cedar (Juniperus virginiana) in early spring release wind‐dispersed teleospores. Junipers showed associational susceptibility: greater susceptibility to gall rust with more diverse neighbours.

     
    more » « less
  3. Abstract

    Non‐crop habitats are essential for sustaining biodiversity of beneficial arthropods in agricultural landscapes, which can increase ecosystem services provision and crop yield. However, their effects on specific crop systems are less clear, such as soybean in South America, where the responses of pests and natural enemies to landscape structure have only recently been studied.

    Here, we analysed how native forest fragments at local and landscape scales influenced arthropod communities, herbivory and yield in soybean fields in central Argentina. To do this, we selected soybean fields located in agricultural landscapes with varying proportions of forest cover. At two distances (10 and 100 m) from a focal forest fragment, we sampled natural enemy and herbivore arthropods, and measured soybean herbivory and yield. We focused on herbivore diversity, abundance of key soybean pests in the region (caterpillars and stink bugs), and their generalist and specialist natural enemies.

    Higher abundance of predators, lower herbivory rates and increased yield were found near forests, while overall forest cover in the landscape was positively related with parasitoid and stink bug abundance, soybean yield, and negatively with herbivory. Moreover, yield was positively linked to richness and abundance of generalist and specialist enemies and independent of herbivory according to piecewise Structural Equation Models.

    Synthesis and applications. Our results show positive effects of native forests on biodiversity and yield in soybean crops, highlighting the need for conservation of forest fragments in agricultural landscapes. Moreover, the relation between natural enemies and crop yield suggests that Chaco forests support a diverse and abundant community of natural enemies that can provide sustained levels of ecosystem services and result in positive effects for farmers.

     
    more » « less
  4. Abstract

    Consumer‐resource interactions are often influenced by other species in the community, such as when neighbouring plants increase or reduce herbivory to a focal plant species (known as associational effects). The many studies on associational effects between a focal plant and some neighbour have shown that these effects can vary greatly in strength and direction. But because almost all of these studies measure associational effects from only one or two neighbour species, we know little about the actual range of associational effects that a plant species might encounter in a natural setting. This makes it difficult to determine how important effects of neighbours are in real field settings, and how associational effects might interact with competition and other processes to influence plant community composition.

    In this study, we used a field experiment with a focal species,Solanum carolinense, and 11 common neighbour species to investigate how associational effects vary among many co‐occurring neighbour species and to test whether factors such as neighbour plant apparency, phylogenetic proximity to the focal species, or effects on focal plant defence traits help to explain interspecific variation in associational effect strength.

    We found that some neighbour species affectedS. carolinensedamage and attack by specialist herbivores, but associational effects of most neighbours were weak. Associational effects increased herbivore attack on average earlier in the season (associational susceptibility) and reduced herbivore attack on average later in the season (associational resistance) relative toS. carolinensein monoculture.

    We found some evidence that a neighbour's associational effect was related to its biomass and phylogenetic proximity to the focal species. While neighbour species differed in their effects on physical leaf traits of focal plants (trichome density, specific leaf area, and leaf toughness), these traits did not appear to mediate the effects of neighbours on focal plant herbivory.

    Synthesis. Our results suggest that the distribution of associational effect strengths in natural communities are similar to those observed for other interaction types, and that multiple mechanisms are likely acting simultaneously to shape associational effects of different neighbour species.

     
    more » « less
  5. Abstract

    Access to high‐quality food is a main driver of population dynamics. For herbivores, protein and carbohydrates are key nutrients that are notoriously variable in plants and are affected by land use. However, few studies have linked foraging decisions and performance in the laboratory to the nutritional landscape available in the field.

    Oedaleus senegalensisis a non‐model locust, a grass‐feeder, and the main pest of millet, a subsistence crop in the Sahel. In this study, we examined dietary preference and locust performance across a range of protein:carbohydrate ratios using the Geometric Framework methodology. We then applied a fitness landscape approach to visualize these results with the plant nutrient contents available across four land‐use types: millet, groundnut, fallow, and grazed fields. Finally, we contrasted our results with locust distribution in the field. Several locust species (O. senegalensisincluded) exhibit density‐dependent colour polymorphism; thus, we also reported individual coloration (brown or green).

    We found thatO. senegalensispreferred moderately carbohydrate‐biased food 1:1.6 protein:carbohydrate ratio. All traits recorded (mass gain, development time, growth rate, moult success and performance index) were best near that ratio and declined on either side presenting a ‘hump‐shape’. Fallow fields contained more plants, particularly grasses, that were both abundant and closer to the optimal protein:carbohydrate ratio recorded from the laboratory experiments.

    When we surveyedO. senegalensisabundance and proportion, we found that they were more numerous in the fallow fields. Brown morph individuals, the ones associated with high density, were proportionally more abundant in fallow fields than green individuals.

    Our study provides evidence that variation in nutritional landscapes – relative to an herbivore's optimal nutrient balance – is a key driver of herbivore population distribution and abundance, and can be used to predict bottom‐up effects on herbivore species.

     
    more » « less