Enemy Biodiversity Research Articles

The benefits of floral border crops in smallholder rice production depends on agronomic inputs and landscape context

Abstract Ecological intensification (EI) provides an important and increasingly adopted pathway for achieving more sustainable agricultural systems. However, the implementation and success of on‐farm EI practices may vary depending on landscape context and local management practices. We evaluated how EI interventions, including two different agricultural input regimes (high or low use of synthetic pesticides and fertilizers) and floral border crops, affected local natural enemy biodiversity, pest abundance and crop yield, and how this was influenced by the surrounding landscape context across 12 rice fields on smallholder farms in Puducherry, India. Reducing agricultural inputs positively impacted the overall natural enemy assemblage; however, responses to landscape factors varied. For example, coccinellid beetles were negatively correlated with higher densities of field edges (landscape configuration). In contrast, spiders, the most abundant group surveyed, were not significantly influenced by any landscape metric. Furthermore, pest abundance was greatest in fields with reduced inputs but only at sites where floral border crops were not present. Mean rice grain yield was lower across low‐input sites compared with high‐input sites and floral border crops had opposing effects across high‐ and low‐input sites. At low‐input sites, mean yields were 33% higher where floral border crops were present. At high‐input sites, the presence of floral border crops was correlated with a lower mean yield (16%). These findings show that ecological intensification practices can benefit smallholder crop systems but highlight the need to account for variations in landscape context and local management practices for developing effective sustainable management practices.

'Tidy' and 'messy' management alters natural enemy communities and pest control in urban agroecosystems.

Agroecosystem management influences ecological interactions that underpin ecosystem services. In human-centered systems, people’s values and preferences influence management decisions. For example, aesthetic preferences for ‘tidy’ agroecosystems may remove vegetation complexity with potential negative impacts on beneficial associated biodiversity and ecosystem function. This may produce trade-offs in aesthetic- versus production-based management for ecosystem service provision. Yet, it is unclear how such preferences influence the ecology of small-scale urban agroecosystems, where aesthetic preferences for ‘tidiness’ are prominent among some gardener demographics. We used urban community gardens as a model system to experimentally test how aesthetic preferences for a ‘tidy garden’ versus a ‘messy garden’ influence insect pests, natural enemies, and pest control services. We manipulated gardens by mimicking a popular ‘tidy’ management practice–woodchip mulching–on the one hand, and simulating ‘messy’ gardens by adding ‘weedy’ plants to pathways on the other hand. Then, we measured for differences in natural enemy biodiversity (abundance, richness, community composition), and sentinel pest removal as a result of the tidy/messy manipulation. In addition, we measured vegetation and ground cover features of the garden system as measures of practices already in place. The tidy/messy manipulation did not significantly alter natural enemy or herbivore abundance within garden plots. The manipulation did, however, produce different compositions of natural enemy communities before and after the manipulation. Furthermore, the manipulation did affect short term gains and losses in predation services: the messy manipulation immediately lowered aphid pest removal compared to the tidy manipulation, while mulch already present in the system lowered Lepidoptera egg removal. Aesthetic preferences for ‘tidy’ green spaces often dominate urban landscapes. Yet, in urban food production systems, such aesthetic values and management preferences may create a fundamental tension in the provision of ecosystem services that support sustainable urban agriculture. Though human preferences may be hard to change, we suggest that gardeners allow some ‘messiness’ in their garden plots as a “lazy gardener” approach may promote particular natural enemy assemblages and may have no downsides to natural predation services.

Perennial woodlands benefit parasitoid diversity, but annual flowering fallows enhance parasitism of wheat aphids in an agricultural landscape

Agriculture intensification poses serious threats to natural enemy biodiversity and associated ecological services. The conservation or reestablishment of semi-natural habitats is used to counteract negative effects of agriculture intensification on natural enemies. Understanding specific functions of different habitats for natural enemies from a landscape perspective is an important step needed for the development of sustainable agriculture. Here, focusing on parasitoids of wheat aphids, we examined effects of the proportion and connectivity of two main semi-natural habitats (woodlands and fallows) present in landscapes, measured within circular buffer radii of 0.5, 1.0, 1.5, and 2.0 km around sampling sites, on parasitoid (mummy) density, biodiversity (Shannon diversity) and associated services (parasitism rate) in 35 wheat fields. We also compared local vegetation communities of these two semi-natural habitats to test whether plant characteristics can shed light on the potential mechanisms driving parasitoids responses to different landscape habitats. We found that the parasitoid diversity was much higher in landscapes dominated by woodlands, while fallows in the landscape promoted parasitoid density and parasitism. Woodlands connectivity at larger scales (such as 1.5 or 2.0 km) displayed positive effects on parasitoid activities, fallows connectivity at the smaller scale (0.5 km) had a positive effect on the hyperparasitism rate. In terms of vegetation characteristics, fallows provided more flowering plants and floral resources, while woodlands suffered less disturbance across years. Local vegetation composition of the semi-natural habitats indeed help explain their different effects on parasitoids at larger landscape scales. We suggested that future research should investigate the role of different types of semi-natural habitats. Conservation management should combine different habitats, such as perennial and annual habitats, to promote the functional complementarity for beneficial organisms. Based on results from local vegetation survey, we also suggested native flowering plants such as Capsella bursa-pastoris L., Lagopsis supina Steph., and Calystegia hederacea Wall. in fallows could be used as functional plants to conserve wheat aphid parasitoids.

Alternatives to Synthetic Insecticides in the Control of the Colorado Potato Beetle (Leptinotarsa decemlineata Say) and Their Environmental Benefits

In this study, we review the wide range of alternative control methods used to this day to control the Colorado potato beetle (Leptinotarsa decemlineata Say), the biggest potato pest globally. We further categorize and highlight the advantages and disadvantages of each method by comparing them to conventional insecticides. In a second step, we point out the current knowledge about positive and negative impacts of using alternative control methods. By this, we illustrate how alternative control methods, farmers’ activities, and environmental factors (e.g., biodiversity and ecosystem health) are heavily linked in a cycle with self-reinforcing effects. In detail, the higher the acceptance of farmers to use alternative control methods, the healthier the ecosystem including the pest’s enemy biodiversity. The following decrease in pest abundance possibly increases the yield, profit, and acceptance of farmers to use less conventional and more alternative methods. Overall, we try to balance the positive and negative sides of alternative control methods and combine them with current knowledge about environmental effects. In our view, this is a fundamental task for the future, especially in times of high species loss and increasing demand for environmentally friendly agriculture and environmentally friendly products.

Organic farming expansion drives natural enemy abundance but not diversity in vineyard-dominated landscapes.

Organic farming is seen as a prototype of ecological intensification potentially able to conciliate crop productivity and biodiversity conservation in agricultural landscapes. However, how natural enemies, an important functional group supporting pest control services, respond to organic farming at different scales and in different landscape contexts remain unclear. Using a hierarchical design within a vineyard‐dominated region located in southwestern France, we examine the independent effects of organic farming and semi‐natural habitats at the local and landscape scales on natural enemies. We show that the proportion of organic farming is a stronger driver of species abundance than the proportion of semi‐natural habitats and is an important facet of landscape heterogeneity shaping natural enemy assemblages. Although our study highlights a strong taxonomic group‐dependency about the effect of organic farming, organic farming benefits to dominant species while rare species occur at the same frequency in the two farming systems. Independently of farming systems, enhancing field age, reducing crop productivity, soil tillage intensity, and pesticide use are key management options to increase natural enemy biodiversity. Our study indicates that policies promoting the expansion of organic farming will benefit more to ecological intensification strategies seeking to enhance ecosystem services than to biodiversity conservation.

Give predators a complement: Conserving natural enemy biodiversity to improve biocontrol

Natural enemy biodiversity reflects both the number of species attacking pests (species richness) and their relative abundances (species evenness). Recent experimental work suggests that greater enemy biodiversity might lead to stronger pest suppression when natural enemies occupy different, complementary feeding niches. Complementarity can arise from natural enemy species attacking different pest species or stages located in different places or at different times, and/or when enemies use different hunting strategies. However, these benefits can be weakened when predators in diverse predator communities kill one another, which is more likely in simple foraging environments including few prey species. Here, I review our growing understanding of natural enemy biodiversity in agroecosystems while suggesting a range of approaches that conservation biological control (CBC) practitioners might deploy to specifically encourage complementarity and dampen interference. For example, mixing different crop species or allowing crop residue to remain in fields increases prey diversity and the complexity of the foraging environment, both of which are likely to increase partitioning of diet- and spatial-niches among natural enemy species, making intraguild predation less likely. Habitat management alongside fields likewise might be designed to include elements attractive to different natural enemy taxa that fill different feeding niches, explicitly engineering fields to bring together complementary natural enemies. For example, refuge strips could include both bunch grasses that provide refuge to predatory beetles and spiders that forage on the ground, and flowers attractive to generalist predators and parasitoids that forage in plant foliage. Caution is warranted however, as a general enrichment of prey communities might build trophic complexity that dampens overall herbivore suppression. Altogether, the approach suggested here is consistent with a growing realization that CBC efforts that simultaneously encourage multiple ecosystem services will be most likely to be adopted by growers. Furthermore, CBC projects provide an opportunity to examine whether predator biodiversity effects demonstrated in cages or other experimental arenas lead to real-world benefits for biological control, advancing our understanding of biodiversity-ecosystem services relationships more generally. Perhaps the clearest challenges remain in extending what is known about enemy biodiversity effects, and their enhancement through CBC, to species-rich tropical agroecosystems.

Functional diversity of predators and parasitoids does not explain aphid biocontrol efficiency

Many studies demonstrate an important role of natural enemy biodiversity in the regulation of agricultural pests, but the role of different aspects of biodiversity in influencing this crucial ecosystem service remain controversial. We hypothesised that the functional diversity generated by combining divergent consumer groups (roaming coccinellid predators and parasitoid wasps) fosters complementarity, enhancing aphid biocontrol. We tested this using experimental mesocosms containing plants, aphids and natural enemies located in a greenhouse. We compared the aphid control efficiency (final aphid abundance) of low functional diversity treatments (two parasitoid species, or two predator species) with high functional diversity treatments (all four possible predator-parasitoid combinations). We also included all four enemies as single species treatments to allow calculation of the non-additive effects of combining natural enemies. Results showed that biocontrol (final aphid abundance) was driven by the species identity of natural enemies and positive non-additive effects in two treatments in which the most efficient predator species was combined with a parasitoid species and the other predator species, respectively. Functional diversity did not consistently influence biocontrol or non-additive effects. In conclusion, functional diversity, as defined by differences between roaming predator and parasitoid functional groups, failed to consistently explain biocontrol efficiency in our study. This calls for consideration of finer-scale functional traits and how they govern natural enemy interactions and cascading effects across ecosystems.

Effects of biodiversity in agricultural landscapes on the protective microbiome of insects – a review

AbstractSymbiotic bacteria in herbivorous insects can have strong beneficial impacts on their host's survival, including conferring resistance to natural enemies such as parasitoid wasps or pathogens, while also imposing energetic costs on the host, resulting in cost‐benefit trade‐offs. Whether these trade‐offs favour the hosting of symbionts depends on the growth environment of the herbivore. Long‐term experimental grassland studies have shown that increasing plant species richness leads to an increased diversity of associated herbivores and their natural enemies. Such a change in natural enemy diversity, related to changes in plant diversity, could also drive changes in the community of symbionts hosted by the herbivorous insects. Aphids are one model system for studying symbionts in insects, and effects of host‐plant species and diversity on aphid‐symbiont interactions have been documented. Yet, we still understand little of the mechanisms underlying such effects. We review the current state of knowledge of how biodiversity can impact aphid‐symbiont communities and the underlying drivers. Then, we discuss this in the framework of sustainable agriculture, where increased plant biodiversity, in the form of wildflower strips, is used to recruit natural enemies to crop fields for their pest control services. Although aphid symbionts have the potential to reduce biological control effectiveness through conferring protection for the host insect, we discuss how increasing plant and natural enemy biodiversity can mitigate these effects and identify future research opportunities. Understanding how to promote beneficial interactions in ecological systems can help in the development of more sustainable agricultural management strategies.

Biodiversity provides whitefly biological control based on farm management

Management of the whitefly Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) has challenged scientists and famers worldwide because this insect is highly polyphagous and resistant to traditional control methods. Innovative management tools, such as the use of the ecosystem service of biological control, are necessary, especially in a century in which sustainable crop systems are emerging. We investigated how management practices and farm diversity within the property limits affect the relationship between biodiversity conservation and the biological control of B. tabaci. We determined the mortality factors of whitefly nymph cohorts on 33 small farms growing tomatoes. The sampled farms formed a gradient of increasing farm diversity and decreasing management intensity. The diversity of natural enemies increased from conventional to agroecological farms, and predation was identified as the key mortality factor of B. tabaci nymphs on all farm types except the conventional farms. Biological control provided by biodiversity components (predators, parasitoids and pathogens) was enhanced on more diverse and less intensively managed farms. Higher predator richness and abundance resulted in more effective biological control and made it less variable among farms. Different components of natural enemy biodiversity were conserved and acted in a complementary way on agroecological farms, and the enhanced ecosystem services reduced the need for insecticides.

Cityscape quality and resource manipulation affect natural enemy biodiversity in and fidelity to urban agroecosystems

Complex landscapes with high resource availability can support more diverse natural enemy communities and better natural pest control by providing resources and facilitating organism dispersal. Moreover, in agricultural landscapes, local agroecosystem management can support biodiversity maintenance and pest control by adding resources in less complex landscapes with fewer resources. However, we lack an understanding of how local and landscape factors interact to affect natural enemy communities and their site fidelity to agroecosystems in urban landscapes (i.e., cityscapes). To better understand how local and landscape factors influence natural enemies in urban agroecosystems, we used urban community gardens as a model system to test if and how local resource manipulation and differences in cityscape quality affect natural enemy (ladybird beetles, parasitoid wasps) communities and their fidelity to urban habitats. We performed two manipulations. First, we added local floral resources in 6 of 12 gardens situated in different cityscapes to measure differences in natural enemy biodiversity. Second, in those 12 gardens, with and without resource additions, we manipulated populations of a common natural enemy, Hippodamia convergens, to assess fidelity to the gardens. Floral resource additions increased parasitoid abundance and changed community composition, but had little effect on ladybeetle abundance, richness or site fidelity. Rather, ladybeetle fidelity to gardens was lower in gardens in low quality cityscapes with high impervious cover. Cityscape quality influences natural enemies in and fidelity to gardens. Landscape-moderated biodiversity patterns observed in rural landscapes likely differ from urban contexts with implications for pest control.

Natural enemy composition rather than richness determines pest suppression

Natural enemy (NE) biodiversity is thought to play an important role in agricultural pest suppression. However, the relative importance of the number of NE species (species richness), versus the particular combinations of species (species composition), in determining aphid suppression and ultimately crop yields, remains poorly understood. We tested the effects of NE richness and composition on pea aphids Acyrthosiphon pisum (Harris) and broad bean plants Vicia faba (Linn.). We used the larvae of two predator species, the ladybird Adalia bipunctata (Linn.) and the green lacewing Chrysopa carnea (Stephens), and the parasitic wasp Aphidius ervi (Haliday) as enemies. NEs generally reduced aphid density but did not increase final plant biomass, despite a significant negative correlation between aphid density and plant biomass. Among NE treatments, species richness had an inconsistent effect on aphid density. The composition of NEs within richness levels also affected final aphid density: the ladybird was a key species among the treatments in controlling aphid density and was especially effective in combination with the parasitoid. This ladybird/parasitoid combination also appeared to drive the higher level of suppression observed at the two, relative to three, species richness levels. Although these three species of aphid NEs are commonly used in aphid control, this is the first study, to our knowledge, that simultaneously examined these three species and highlighted the composition effect between the A. bipunctata and A. ervi. In conclusion, increasing NE species richness had an inconsistent effect on aphid density. Meanwhile, the presence of a key species (the ladybird) and its combination with a parasitoid was an important determinant of aphid biological control.

Tailored flower strips promote natural enemy biodiversity and pest control in potato crops

Summary Sown flower strips are increasingly implemented within agri‐environment schemes (AES) to increase functional biodiversity and ecosystem services such as pollination or natural pest control, but their effectiveness in achieving these goals remains poorly studied. We tested the performance of experimentally sown annual flower strips specifically designed to promote natural enemies of aphids and their pest control services (tailored flower strips) in adjacent potato crops (n = 8) compared with control fields (n = 10). Flower strips consisted of 11 plant species providing abundant floral and extra‐floral resources. The abundance of key natural enemies of aphids (hoverflies, lacewings and ladybirds) and hoverfly species richness was greatly enhanced in tailored flower strips compared with potato control strips. This resulted in an average increase in the number of eggs deposited by hoverflies and lacewings by 127% and 48%, respectively, and a reduction in the number of aphids by 75% in adjacent potato crops. Synthesis and applications. We conclude that tailored flower strips can be an effective agri‐environmental measure to enhance natural enemies and aphid control in nearby crops. Indeed, tailored flower strips may help to reduce insecticide input in potato production as they significantly decrease the probability that action thresholds are reached. Promoting natural enemy abundance and diversity, as observed for hoverflies, may increase the stability of pest control and provide additional benefits to agro‐ecosystems in terms of natural enemy conservation. We thus recommend establishing tailored flower strips as a promising management option to reconcile the objectives of ecological intensification and biodiversity conservation.

Urban greenspace composition and landscape context influence natural enemy community composition and function

Conservation research has historically been aimed at preserving high value natural habitats, but urbanization and its associated impacts have prompted broader mandates that include the preservation and promotion of biodiversity in cities. Current efforts within urban landscapes aim to support biodiversity and diverse ecosystem services such as storm water management, sustainable food production, and toxin remediation. Arthropod natural enemies provide biocontrol services important for the ecosystem management of urban greenspaces. Establishing habitat for these and other beneficial arthropods is a growing area of urban conservation. Habitat design, resource inputs, management, and abiotic conditions shape the value of greenspace habitats for arthropods. In general, larger patches with diverse plant communities support a greater abundance and diversity of natural enemies and biocontrol services, yet opposing patterns or no effects have also been documented. The surrounding landscape is likely a contributor to this variation in natural enemy response to patch-scale habitat design and management. Looking across rural–urban landscape gradients, natural enemy communities shift toward dominance by habitat generalists and disturbance tolerant species in urban areas compared to rural or natural communities. These changes have been linked to variation in habitat fragmentation, plant productivity and management intensity. In landscape-scale studies focusing solely within cities, variables such as impervious surface area and greenspace connectivity affect the community assembly of natural enemies within a patch. Given these findings, a greater mechanistic understanding of how both the composition and spatial context of urban greenspaces influence natural enemy biodiversity–biocontrol relationships is needed to advance conservation planning and implementation.

Evaluating the Structure of Enemy Biodiversity Effects on Prey Informs Pest Management

Evaluating the structure of enemy biodiversity effects on prey in agroecosystems can provide insights into biological pest control functioning. With this aim, theoretical models that describe biological mechanisms underlying prey suppression can be developed and confronted with experimental data by means of model selection. Here, we confront multiplicative risk models to evaluate the structure of multiple predator effects on the whitefly Trialeurodes vaporariorum provided in tomatoes by two spiders (Oxyopes lineatus and Pityohyphantes phrygianus) and two mirids (Nesidiocoris tenuis and Macrolophus melanotoma). Biologically meaningful parameters retained in the best models showed that several predator traits differently affected pest control: species-specific per capita predation rates, prey use extent, different type of interactions between predators, and the response of predator species to prey density and environmental temperature. Even from a limited perspective of single-pest control and short term experiment, this study suggests that assembly of the four predator species results in predator complementarity across prey life stages and density, interactions of prey and predators with environmental conditions, and interactions between predators that do not result in whitefly control disruption. Such information about enemy biodiversity and whitefly control functioning can drive hypotheses about sustainable pest management options in local agroecosystems.

Species abundance patterns of coccinellid communities associated with olive, chestnut and almond crops in north‐eastern Portugal

The patterns of abundance of coccinellid species associated to the main agricultural tree crops of north‐eastern Portugal namely olive, chestnut and almond were studied. During three to four crop seasons, eight olive, five chestnut and one almond groves were sampled. In each grove, five samples were collected from 10 randomly selected trees using the beating technique and the coccinellids were counted and identified to species. Principal component analysis was used to establish associations among crop and coccinellid species. The mean species richness was higher in chestnut, with 15 ± 3.81 species/grove, followed by olive and almond, with 13 ± 2.76 and 10 ± 2.97 species/grove, respectively. Scymnus mediterraneus was the most abundant species in olive and almond, whereas Scymnus interruptus was dominant in chestnut. Brumus quadripustulatus, Chilocorus bipustulatus, Scymnus subvillosus, S. mediterraneus and Rhyzobius chrysomeloides were associated with olive, whereas S. interruptus, Coccinella septempunctata and Adalia decempunctata were associated with chestnut and Hippodamia variegata, Oenopia conglobata and Adalia bipunctata with almond. Both Stethorus punctillum and Scymnus apetzi species were similarly associated with chestnut and almond. The differences in coccinellid communities could have been related to the kind of prey item present in the different trees. This knowledge can be used to develop integrated pest management programmes that encourage greater natural enemy biodiversity in agroecosystems.

Effects of Natural Enemy Biodiversity on the Suppression of Arthropod Herbivores in Terrestrial Ecosystems

Claims about the role of predator diversity in maintaining ecosystem function and providing ecosystem services such as pest control are controversial, but evaluative tests are beginning to accumulate. Empirical and experimental comparisons of species-rich versus species-poor assemblages of entomophagous arthropods and vertebrates range from strong suppression to facilitative release of herbivorous arthropod prey. Top-down control can be strengthened when natural enemies complement each other, dampened by negative interactions, balanced by both factors, and driven by single influential species. A meta-analytic synthesis shows a significant overall effect of enemy richness increasing top-down control of herbivores, which is consistent in agricultural studies conducted in tropical versus temperate zones, in studies using caged versus open-field designs, but not so in nonagricultural habitats. Synthetic analyses address theory and help set precautionary policy for conserving ecological services broadly, while characterizing uncertainty associated with herbivore response to changes in enemy diversity.

Are the conservation of natural enemy biodiversity and biological control compatible goals?

In conservation biological control (CBC), we attempt to reduce pest problems by increasing the abundance and diversity of the natural enemy community. However, rather than consistently strengthening herbivore suppression, studies show that the conservation of natural enemy species richness sometimes weakens, or has no affect, on biological control. Evidence is mounting that this idiosyncratic mix of positive, negative, and neutral effects of enemy diversity is caused by niche complementarity, intraguild predation, and functional redundancy, respectively. While the balance of evidence suggests that the conservation of natural enemy diversity and biological control are compatible goals, CBC practitioners cannot ignore the fact that conserving intraguild predators can sometimes disrupt biological control. Recent studies have made important progress toward identifying the traits of enemies and their prey that promote intraguild predation, functional redundancy, and niche complementarity. However, intraguild predation has received more attention than niche complementarity, and more theoretical and empirical work is needed rectify this asymmetry. We suggest that a continued focus on natural enemy functional traits, particularly those that are expressed at larger spatiotemporal scales, will increase our ability to identify the “right” kind of diversity and may ultimately improve the practice of conservation biological control.