Food webs and biological control: A review of molecular tools used to reveal trophic interactions in agricultural systems (original) (raw)

Food webs and biological control. A review of molecular tools used to reveal trophic interactions in agricultural systems Food webs and biological control. A review of molecular tools used to reveal trophic interactions in agricultural systems

Modern monocultural agro-ecosystems can be perceived as a simplification of natural ecosystems, where a single plant species is usually grown over vast areas. In these systems, it has historically been assumed that the concept of a food chain can describe the relationships between an insect pest and a single biocontrol agent. In reality, multiple potentially complex ecological interactions are involved, and these comprise food webs. However, identifying, analysing and quantifying the relative strengths of these multi- trophic interactions are very difficult using orthodox methods such as dissection and subsequent visual gut-content identification. An emerging field of study using molecular tools to analyse prey DNA in predators as well as parasitoid DNA within their hosts can now begin to address these impediments and help to better understand multi-trophic dynamics and improve biological control. In this article, we review the scientific literature published between 2000 and 2015 related to the use of molecular tools to analyse trophic interactions in agroecosystems in the context of biological control, using the ISI Web of Science search engine. A total of 213 articles were found and a steady increase in the volume of this literature occurred over the period studied. Based on the analysis of those publications, we propose future avenues in which advanced molecular tools can contribute to a mechanistic understanding of biological control, suggesting how this approach could help design agricultural systems based on agroecological techniques.

Identifying Molecular-Based Trophic Interactions as a Resource for Advanced Integrated Pest Management

Insects, 2021

Simple Summary With increasing human populations and the need for ecosystem services to work in synergy with the production of specialty crops, the maintenance of biodiversity is becoming increasingly important. The aims of this study were to review the current literature employing molecular analysis to reveal the roles of species in providing biological control in agricultural systems. Decrypting the trophic networks between biological control agents and agricultural pests is essential to build eco-friendly strategies that promote the natural management of pests before any mediations, such as chemical control strategies, are required. It was found, during the review process, that our understanding of biological control communities is lacking in many agricultural systems, including common fruit and vegetable production, both in terms of what species are doing for crop production, and how various environmental challenges (i.e., land-use and habitat management concepts, such as wildfl...

Molecular detection of trophic links in a complex insect host-parasitoid food web

Molecular Ecology Resources, 2011

Previously, host-parasitoid links have been unveiled almost exclusively by time-intensive rearing, while molecular methods were used only in simple agricultural host-parasitoid systems in the form of species-specific primers. Here, we present a general method for the molecular detection of these links applied to a complex caterpillar-parasitoid food web from tropical rainforest of Papua New Guinea. We DNA barcoded hosts, parasitoids and their tissue remnants and matched the sequences to our extensive library of local species. We were thus able to match 87% of host sequences and 36% of parasitoid sequences to species and infer subfamily or family in almost all cases. Our analysis affirmed 93 hitherto unknown trophic links between 37 host species from a wide range of Lepidoptera families and 46 parasitoid species from Hymenoptera and Diptera by identifying DNA sequences for both the host and the parasitoid involved in the interaction. Molecular detection proved especially useful in cases where distinguishing host species in caterpillar stage was difficult morphologically, or when the caterpillar died during rearing. We have even detected a case of extreme parasitoid specialization in a pair of Choreutis species that do not differ in caterpillar morphology and ecology. Using the molecular approach outlined here leads to better understanding of parasitoid host specificity, opens new possibilities for rapid surveys of food web structure and allows inference of species associations not already anticipated.

Supplementary material 1 from: Lefort M, Wratten S, Cusumano A, Varennes Y, Boyer S (2017) Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing. Metabarcoding and Metagenomics 1: e13709. https://doi.org/10.3897/mbmg.1.13709

2017

The lack of understanding of complex food-web interactions has been a major gap in the history of biological control. In particular, a better understanding of the functioning of pest food-webs and how they vary between native and invaded geographical ranges is of prime interest for biological control research and associated integrated pest management. Technical limitations associated with the deciphering of complex food-webs can now be largely overcome by the use of high throughput DNA sequencing techniques such as Illumina MiSeq. We tested the efficiency of this next generation sequencing technology in a metabarcoding approach, to study aphid food-webs using the cabbage aphid as model. We compared the variations in structure and composition of aphid food-webs in the species' native range (United Kingdom, UK) and in an invaded range (New Zealand, NZ). We showed that Illumina MiSeq is a well suited technology to study complex aphid food-webs from aphid mummies. We found an unexpectedly high top down pressure in the NZ cabbage aphid food-web, which coupled to a large ratio of consumer species / prey ‡, § § | ¶ #, ‡ © Lefort M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. species and a lack of potential inter-specific competition between primary parasitoids, could cause the NZ food-web to be more vulnerable than the UK one. This study also reports for the first time the occurrence of a new hyperparasitoid species in NZ, as well as new associations between hyperparasitoids parasitoids and the cabbage aphid in this country. We conclude that the complexity of aphid food-webs in agricultural systems could often be underestimated, particularly at higher trophic levels; and that the use of high throughput DNA sequencing tools, could largely help to overcome this impediment.

Editorial: Molecular and isotopic approaches to food webs in agroecosystems

a r t i c l e i n f o Available online xxxx This special issue comprises seven papers: one review, one opinion and five experimental papers. Together, these articles illustrate how molecular tools and isotope analyses are improving our understanding of food-web structure and dynamics in agricultural systems. The papers collated here make use of the PCR-based DNA barcoding approach, protein-marking ELISA and the analysis of isotopic ratios to investigate a wide range of ecological questions. These studies advance our understanding of biodiversity and food-web dynamics in agroecosystems, provide direction on how to improve biological control of pests, detail the movement of energy and nutrient fluxes in soil food webs, and quantify anthropogenic disturbances in agroecosystems.

Empirically Characterising Trophic Networks

Ecological Networks in an Agricultural World, 2013

Food webs in agricultural systems are complex and trophic linkages are difficult to track using conventional methodologies. Here, we review three alternative approaches that allow empirical assessment of feeding interactions: DNA-based techniques, and stable isotope and fatty acid analyses. DNA-based methods, namely multiplex PCR and nextgeneration sequencing, allow identification of food types and host-parasitoid linkages, resulting in taxonomically highly resolved feeding networks. Stable isotopes and fatty

Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing

The lack of understanding of complex food-web interactions has been a major gap in the history of biological control. In particular, a better understanding of the functioning of pest food-webs and how they vary between native and invaded geographical ranges is of prime interest for biological control research and associated integrated pest management. Technical limitations associated with the deciphering of complex food-webs can now be largely overcome by the use of high throughput DNA sequencing techniques such as Illumina MiSeq. We tested the efficiency of this next generation sequencing technology in a metabarcoding approach, to study aphid food-webs using the cabbage aphid as model. We compared the variations in structure and composition of aphid food-webs in the species' native range (United Kingdom, UK) and in an invaded range (New Zealand, NZ). We showed that Illumina MiSeq is a well suited technology to study complex aphid food-webs from aphid mummies. We found an unexpectedly high top down pressure in the NZ cabbage aphid food-web, which coupled to a large ratio of consumer species / prey ‡, § § | ¶ #, ‡

DNA Metabarcoding as a Tool for Disentangling Food Webs in Agroecosystems

Insects, 2020

Better knowledge of food webs and related ecological processes is fundamental to understanding the functional role of biodiversity in ecosystems. This is particularly true for pest regulation by natural enemies in agroecosystems. However, it is generally difficult to decipher the impact of predators, as they often leave no direct evidence of their activity. Metabarcoding via high-throughput sequencing (HTS) offers new opportunities for unraveling trophic linkages between generalist predators and their prey, and ultimately identifying key ecological drivers of natural pest regulation. Here, this approach proved effective in deciphering the diet composition of key predatory arthropods (nine species.; 27 prey taxa), insectivorous birds (one species, 13 prey taxa) and bats (one species; 103 prey taxa) sampled in a millet-based agroecosystem in Senegal. Such information makes it possible to identify the diet breadth and preferences of predators (e.g., mainly moths for bats), to design a ...

Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats

The ecosystem service of insect pest regulation by natural enemies, such as primary parasitoids, may be enhanced by the presence of uncultivated, semi-natural habitats within agro-ecosystems, although quantifying such host-parasitoid interactions is difficult. Here, we use rRNA 16S gene sequencing to assess both the level of parasitism by Aphidiinae primary parasitoids and parasitoid identity on a large sample of aphids collected in cultivated and uncultivated agricultural habitats in Western France. We used these data to construct ecological networks to assess the level of compartmentalization between aphid and parasitoid food webs of cultivated and uncultivated habitats. We evaluated the extent to which uncultivated margins provided a resource for parasitoids shared between pest and nonpest aphids. We compared the observed quantitative ecological network described by our molecular approach to an empirical qualitative network based on aphid-parasitoid interactions from traditional rearing data found in the literature. We found that the molecular network was highly compartmentalized and that parasitoid sharing is relatively rare between aphids, especially between crop and noncrop compartments. Moreover, the few cases of putative shared generalist parasitoids were questionable and could be due to the lack of discrimination of cryptic species or from intraspecific host specialization. Our results suggest that apparent competition mediated by Aphidiinae parasitoids is probably rare in agricultural areas and that the contribution of field margins as a source of these biocontrol agents is much more limited than expected. Further large-scale (spatial and temporal) studies on other crops and noncrop habitats are needed to confirm this.

Complementary molecular information changes our perception of food web structure

Proceedings of the National Academy of Sciences, 2014

How networks of ecological interactions are structured has a major impact on their functioning. However, accurately resolving both the nodes of the webs and the links between them is fraught with difficulties. We ask whether the new resolution conferred by molecular information changes perceptions of network structure. To probe a network of antagonistic interactions in the High Arctic, we use two complementary sources of molecular data: parasitoid DNA sequenced from the tissues of their hosts and host DNA sequenced from the gut of adult parasitoids. The information added by molecular analysis radically changes the properties of interaction structure. Overall, three times as many interaction types were revealed by combining molecular information from parasitoids and hosts with rearing data, versus rearing data alone. At the species level, our results alter the perceived host specificity of parasitoids, the parasitoid load of host species, and the webwide role of predators with a cryptic lifestyle. As the northernmost network of host-parasitoid interactions quantified, our data point exerts high leverage on global comparisons of food web structure. However, how we view its structure will depend on what information we use: compared with variation among networks quantified at other sites, the properties of our web vary as much or much more depending on the techniques used to reconstruct it. We thus urge ecologists to combine multiple pieces of evidence in assessing the structure of interaction webs, and suggest that current perceptions of interaction structure may be strongly affected by the methods used to construct them. trophic interaction | Hymenoptera | Lepidoptera | DNA barcode H ow networks of ecological interactions are structured has major implications on how they function (1), how they react to external stressors (2, 3) and how they return to their original state after disturbance (4, 5). Quantitative descriptions of who interacts with whom (e.g., refs. 6 and 7) may then be used to formulate testable hypotheses for basic questions concerning, for example, the fundamental strength of indirect interactions (8, 9), or how a community will respond to invasive species, habitat modification, or climate change (e.g., refs. 10-14). In applied biology, quantifications of interaction structure have increasingly been used to examine the success of, for example, habitat restoration and management, the biological control of pests, and the conservation of biodiversity (6). Global comparisons of food web structure are underway, comparing the linking structure of local webs described from different latitudes with highly different species richness .