Publications by authors named "Michael Traugott"

51 Publications

Handling of targeted amplicon sequencing data focusing on index hopping and demultiplexing using a nested metabarcoding approach in ecology.

Sci Rep 2021 09 30;11(1):19510. Epub 2021 Sep 30.

Applied Animal Ecology, Department of Zoology, University of Innsbruck, Technikerstraße 25, 6020, Innsbruck, Austria.

High-throughput sequencing platforms are increasingly being used for targeted amplicon sequencing because they enable cost-effective sequencing of large sample sets. For meaningful interpretation of targeted amplicon sequencing data and comparison between studies, it is critical that bioinformatic analyses do not introduce artefacts and rely on detailed protocols to ensure that all methods are properly performed and documented. The analysis of large sample sets and the use of predefined indexes create challenges, such as adjusting the sequencing depth across samples and taking sequencing errors or index hopping into account. However, the potential biases these factors introduce to high-throughput amplicon sequencing data sets and how they may be overcome have rarely been addressed. On the example of a nested metabarcoding analysis of 1920 carabid beetle regurgitates to assess plant feeding, we investigated: (i) the variation in sequencing depth of individually tagged samples and the effect of library preparation on the data output; (ii) the influence of sequencing errors within index regions and its consequences for demultiplexing; and (iii) the effect of index hopping. Our results demonstrate that despite library quantification, large variation in read counts and sequencing depth occurred among samples and that the sequencing error rate in bioinformatic software is essential for accurate adapter/primer trimming and demultiplexing. Moreover, setting an index hopping threshold to avoid incorrect assignment of samples is highly recommended.
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http://dx.doi.org/10.1038/s41598-021-98018-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8484467PMC
September 2021

Endpoint PCR coupled with capillary electrophoresis (celPCR) provides sensitive and quantitative measures of environmental DNA in singleplex and multiplex reactions.

PLoS One 2021 23;16(7):e0254356. Epub 2021 Jul 23.

Department of Zoology, University of Innsbruck, Innsbruck, Austria.

The use of sensitive methods is key for the detection of target taxa from trace amounts of environmental DNA (eDNA) in a sample. In this context, digital PCR (dPCR) enables direct quantification and is commonly perceived as more sensitive than endpoint PCR. However, endpoint PCR coupled with capillary electrophoresis (celPCR) potentially embodies a viable alternative as it quantitatively measures signal strength after PCR in Relative Fluorescence Units (RFU). Provided comparable levels of sensitivity are reached, celPCR permits the development of cost-efficient multiplex reactions, enabling the simultaneous detection of several target taxa. Here, we compared the sensitivity of singleplex and multiplex celPCR to dPCR for species-specific primer pairs amplifying mitochondrial DNA (COI) of fish species occurring in European freshwaters by analyzing dilution series of tissue extracts as well as field-collected water samples. Both singleplex and multiplex celPCR and dPCR displayed comparable sensitivity with reliable positive amplifications starting at two to 10 target DNA copies per μl extract. celPCR was suitable for quantifying target DNA and direct inference of copy numbers from RFU was possible after accounting for primer effects in linear mixed-effects models and calibration via dPCR. Furthermore, multiplex celPCR and dPCR were successfully used for the detection and quantification of fish-eDNA in field-collected water samples, confirming the results of the dilution series experiment and exemplifying the high sensitivity of the two approaches. The possibility of detection and quantification via multiplex celPCR is appealing for the cost-efficient screening of high sample numbers. The present results confirm the sensitivity of this approach thus enabling its application for future eDNA-based monitoring efforts.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0254356PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8301609PMC
November 2021

Landscape complexity promotes resilience of biological pest control to climate change.

Proc Biol Sci 2021 05 26;288(1951):20210547. Epub 2021 May 26.

Department of Ecology, Swedish University of Agricultural Sciences, 75751 Uppsala, Sweden.

Increased climate variability as a result of anthropogenic climate change can threaten the functioning of ecosystem services. However, diverse responses to climate change among species (response diversity) can provide ecosystems with resilience to this growing threat. Measuring and managing response diversity and resilience to global change are key ecological challenges. Here, we develop a novel index of climate resilience of ecosystem services, exemplified by the thermal resilience of predator communities providing biological pest control. Field assays revealed substantial differences in the temperature-dependent activity of predator species and indices of thermal resilience varied among predator communities occupying different fields. Predator assemblages with higher thermal resilience provided more stable pest control in microcosms where the temperature was experimentally varied, confirming that the index of thermal resilience developed here is linked to predator function. Importantly, complex landscapes containing a high number of non-crop habitat patches were more likely to contain predator communities with high thermal resilience. Thus, the conservation and restoration of non-crop habitats in agricultural landscapes-practices known to strengthen natural pest suppression under current conditions-will also confer resilience in ecosystem service provisioning to climate change.
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http://dx.doi.org/10.1098/rspb.2021.0547DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8150070PMC
May 2021

The resilience of weed seedbank regulation by carabid beetles, at continental scales, to alternative prey.

Sci Rep 2020 11 9;10(1):19315. Epub 2020 Nov 9.

Agroécologie, AgroSup Dijon, INRAE, Université de Bourgogne Franche-Comté, 17 rue Sully, BP 86510, 21065, Dijon Cedex, France.

Carabids are generalist predators that contribute to the agricultural ecosystem service of seedbank regulation via weed seed predation. To facilitate adoption of this ecosystem services by farmers, knowledge of weed seed predation and the resilience of seedbank regulation with co-varying availability of alternative prey is crucial. Using assessments of the seedbank and predation on seed cards in 57 cereal fields across Europe, we demonstrate a regulatory effect on the soil seedbank, at a continental scale, by groups formed of omnivore, seed-eating (granivore + omnivore) and all species of carabids just prior to the crop-harvest. Regulation was associated with a positive relationship between the activity-density of carabids and seed predation, as measured on seed cards. We found that per capita seed consumption on the cards co-varied negatively with the biomass of alternative prey, i.e. Aphididae, Collembola and total alternative prey biomass. Our results underline the importance of weed seedbank regulation by carabids, across geographically significant scales, and indicate that the effectiveness of this biocontrol may depend on the availability of alternative prey that disrupt the weed seed predation.
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http://dx.doi.org/10.1038/s41598-020-76305-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7652833PMC
November 2020

Fish as predators and prey: DNA-based assessment of their role in food webs.

J Fish Biol 2021 Feb 8;98(2):367-382. Epub 2020 Jul 8.

Applied Animal Ecology, Department of Zoology, University of Innsbruck, Innsbruck, Austria.

Fish are both consumers and prey, and as such part of a dynamic trophic network. Measuring how they are trophically linked, both directly and indirectly, to other species is vital to comprehend the mechanisms driving alterations in fish communities in space and time. Moreover, this knowledge also helps to understand how fish communities respond to environmental change and delivers important information for implementing management of fish stocks. DNA-based methods have significantly widened our ability to assess trophic interactions in both marine and freshwater systems and they possess a range of advantages over other approaches in diet analysis. In this review we provide an overview of different DNA-based methods that have been used to assess trophic interactions of fish as consumers and prey. We consider the practicalities and limitations, and emphasize critical aspects when analysing molecular derived trophic data. We exemplify how molecular techniques have been employed to unravel food web interactions involving fish as consumers and prey. In addition to the exciting opportunities DNA-based approaches offer, we identify current challenges and future prospects for assessing fish food webs where DNA-based approaches will play an important role.
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http://dx.doi.org/10.1111/jfb.14400DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7891366PMC
February 2021

Monitoring spawning migrations of potamodromous fish species via eDNA.

Sci Rep 2019 10 28;9(1):15388. Epub 2019 Oct 28.

Research Department for Limnology, University of Innsbruck, Mondsee, Austria.

Potamodromous fish are considered important indicators of habitat connectivity in freshwater ecosystems, but they are globally threatened by anthropogenic impacts. Hence, non-invasive techniques are necessary for monitoring during spawning migrations. The use of environmental DNA (eDNA) potentially facilitates these efforts, albeit quantitative examinations of spawning migrations remain so far mostly uncharted. Here, we investigated spawning migrations of Danube bleak, Alburnus mento, and Vimba bream, Vimba vimba, and found a strong correlation between daily visual fish counts and downstream eDNA signals obtained from filtered water samples analysed with digital PCR and end-point PCR coupled with capillary electrophoresis. By accounting for daily discharge fluctuations, it was possible to predict eDNA signal strength from the number of migrating fish: first, the whole spawning reach was taken into account. Second, the model was validated using eDNA signals and fish counts obtained from the upper half of the examined river stretch. Consequently, fish counts and their day-to-day changes could be described via an eDNA-based time series model for the whole migration period. Our findings highlight the capability of eDNA beyond delivering simple presence/absence data towards efficient and informative monitoring of highly dynamic aquatic processes such as spawning migrations of potamodromous fish species.
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http://dx.doi.org/10.1038/s41598-019-51398-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6817844PMC
October 2019

Resilience of ecosystem processes: a new approach shows that functional redundancy of biological control services is reduced by landscape simplification.

Ecol Lett 2019 Oct 16;22(10):1568-1577. Epub 2019 Jul 16.

Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

Functional redundancy can increase the resilience of ecosystem processes by providing insurance against species loss and the effects of abundance fluctuations. However, due to the difficulty of assessing individual species' contributions and the lack of a metric allowing for a quantification of redundancy within communities, few attempts have been made to estimate redundancy for individual ecosystem processes. We present a new method linking interaction metrics with metabolic theory that allows for a quantification of redundancy at the level of ecosystem processes. Using this approach, redundancy in the predation on aphids and other prey by natural enemies across a landscape heterogeneity gradient was estimated. Functional redundancy of predators was high in heterogeneous landscapes, low in homogeneous landscapes and scaled with predator specialisation. Our approach allows quantifying functional redundancy within communities and can be used to assess the role of functional redundancy across a wide variety of ecosystem processes and environmental factors.
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http://dx.doi.org/10.1111/ele.13347DOI Listing
October 2019

Molecular analysis indicates high levels of carabid weed seed consumption in cereal fields across Central Europe.

J Pest Sci (2004) 2019 9;92(3):935-942. Epub 2019 Apr 9.

3Institute of Interdisciplinary Mountain Research, IGF, Austrian Academy of Sciences, Technikerstraße 21a, 6020 Innsbruck, Austria.

Carabid beetles are abundant in temperate agroecosystems and can play a pivotal role as biocontrol agents. While there is good knowledge regarding their effects on invertebrate pests in some systems, comparably little is known on the rate of seed feeding under field conditions. Molecular approaches are ideally suited for investigating carabid feeding interactions; to date, however, they have only been applied to animal prey. We sampled adult carabid beetles in organic cereal fields in three regions along a Central European transect. Regurgitates from populations of the three most common species, and , were screened for plant DNA, cereal aphids, collembolans and earthworms. The frequency of carabid individuals positive for plant DNA was high (> 70%) and independent of carabid species, sex, region and the time point of sampling. Detections for non-pest and pest prey were comparably lower, with 21.6% for collembolans, 18.1% for earthworms and 4.2% for aphids, respectively. Despite the prolonged detection period of plant DNA in carabid guts, as compared to animal prey, these first results suggest that weed seeds form an important part of the adult carabid diet. It would also lend support to the hypothesis that seed-feeding carabids are biocontrol agents of weeds, with effects of regulation on the weed seedbank that depend on behavioural and contextual factors including carabid species preferences for weed seed species, their life stage and tillage practices.
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http://dx.doi.org/10.1007/s10340-019-01109-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6528783PMC
April 2019

A broadly applicable COI primer pair and an efficient single-tube amplicon library preparation protocol for metabarcoding.

Ecol Evol 2018 Dec 11;8(24):12335-12350. Epub 2018 Dec 11.

Mountain Agriculture Research Unit Institute of Ecology University of Innsbruck Innsbruck Austria.

The nucleotide variation in the cytochrome c oxidase subunit I (COI) gene makes it ideal for assigning sequences to species. However, this variability also makes it difficult to design truly universal primers. Here, we present the forward primer "Sauron-S878," specifically designed to facilitate library preparation for metabarcoding. This primer is modified to improve the coverage of terrestrial species compared to the primer mCOIintF, optimized for aquatic systems, which raised the in silico coverage from 74.4% to 98.3% of available NCBI sequences (perfect match in 3' region, up to three mismatches in remaining primer). When paired with the reverse primer "jgHCO2198" (fragment length ~313 bp), these primers amplified 98.4% of 255 tested DNA extracts from various taxa, which are better than many other common COI barcoding primers. Furthermore, a single-tube protocol was developed, wherein these primers amplify the target gene, and attach MIDs and Illumina sequencing adapters in one reaction. This eliminates the need for re-amplification or enzymatic ligation during library preparation while keeping the flexibility to modularly combine primers and MIDs. Using the single-tube approach, three replicates of three mock samples were sequenced on a MiSeq platform with no adverse effects compared to commercial Nextera indexing kits. From this run, 75% of all included taxa could be recovered, with no considerable bias among taxonomic groups. Despite the fact that 98.4% of the extracts were confirmed to amplify in vitro, this number was lower than expected. A reason for this discrepancy was a clear link between the relative concentration of a specific DNA type in the template and the number of returned reads for this DNA. We would argue that such a bias may be especially problematic in metabarcoding where samples usually contain trace DNA in unknown amounts. However, how this affects the completeness of metabarcoding results has yet been poorly investigated.
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http://dx.doi.org/10.1002/ece3.4520DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6308894PMC
December 2018

The effect of plant identity and mixed feeding on the detection of seed DNA in regurgitates of carabid beetles.

Ecol Evol 2018 Nov 25;8(22):10834-10846. Epub 2018 Oct 25.

Institute of Interdisciplinary Mountain Research, IGF Austrian Academy of Sciences Innsbruck Austria.

Carabids are abundant in temperate agroecosystems and play a pivotal role as biocontrol agents for weed seed and pest regulation. While there is good knowledge regarding their effects on invertebrate pests, direct evidence for seed predation in the field is missing. Molecular approaches are ideally suited to investigate these feeding interactions; however, the effects of an omnivorous diet, which is characteristic for many carabid species, and seed identity on the detection success of seed DNA has not yet been investigated. In a series of feeding experiments, seeds of six different Central European weed species were fed to beetles of the species , to determine post-feeding seed DNA detection rates and how these are affected by plant identity, meal size, and chemical seed composition. Moreover, we investigated the effect of a mixed diet of seeds and mealworm on prey DNA detection. Four out of six seed species were detectable for up to five days after consumption, and seed species identity significantly affected post-feeding detection rates. Detectability was negatively influenced by protein content and seed mass, whereas oil content and meal size had a positive effect. The mixed diet led to both increased detection rates and post-feeding detection intervals of seed DNA. This suggests that mixed feeding leads to an enhancement of food detection intervals in carabid beetles and that seed identity, their chemical composition, and meal size can affect DNA detection of consumed seeds. These aspects and potential implications of this non-invasive approach are discussed as they can become highly relevant for interpreting field-derived data.
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http://dx.doi.org/10.1002/ece3.4536DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262922PMC
November 2018

When to use next generation sequencing or diagnostic PCR in diet analyses.

Mol Ecol Resour 2019 Mar 4;19(2):388-399. Epub 2019 Feb 4.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

Next-generation sequencing (NGS) is increasingly used for diet analyses; however, it may not always describe diet samples well. A reason for this is that diet samples contain mixtures of food DNA in different amounts as well as consumer DNA which can reduce the food DNA characterized. Because of this, detections will depend on the relative amount and identity of each type of DNA. For such samples, diagnostic PCR will most likely give more reliable results, as detection probability is only marginally dependent on other copresent DNA. We investigated the reliability of each method to test (a) whether predatory beetle regurgitates, supposed to be low in consumer DNA, allow to retrieve prey sequences using general barcoding primers that co-amplify the consumer DNA, and (b) to assess the sequencing depth or replication needed for NGS and diagnostic PCR to give stable results. When consumer DNA is co-amplified, NGS is better suited to discover the range of possible prey, than for comparing co-occurrences of diet species between samples, as retested samples were repeatedly different in prey detections with this approach. This shows that samples were incompletely described, as prey detected by diagnostic PCR frequently were missed by NGS. As the sequencing depth needed to reliably describe the diet in such samples becomes very high, the cost-efficiency and reliability of diagnostic PCR make diagnostic PCR better suited for testing large sample-sets. Especially if the targeted prey taxa are thought to be of ecological importance, as diagnostic PCR gave more nested and consistent results in repeated testing of the same sample.
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http://dx.doi.org/10.1111/1755-0998.12974DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446722PMC
March 2019

Sex-specific prey partitioning in breeding piscivorous birds examined via a novel, noninvasive approach.

Ecol Evol 2018 Sep 14;8(17):8985-8998. Epub 2018 Aug 14.

Institute of Ecology University of Innsbruck Innsbruck Austria.

Piscivorous birds frequently display sex-specific differences in their hunting and feeding behavior, which lead to diverging impacts on prey populations. Cormorants (Phalacrocoracidae), for example, were previously studied to examine dietary differences between the sexes and males were found to consume larger fish in coastal areas during autumn and winter. However, information on prey partitioning during breeding and generally on sex-specific foraging in inland waters is missing. Here, we assess sex-specific prey choice of Great Cormorants () during two subsequent breeding seasons in the Central European Alpine foreland, an area characterized by numerous stagnant and flowing waters in close proximity to each other. We developed a unique, noninvasive approach and applied it to regurgitated pellets: molecular cormorant sexing combined with molecular fish identification and fish-length regression analysis performed on prey hard parts. Altogether, 364 pellets delivered information on both, bird sex, and consumed prey. The sexes differed significantly in their overall prey composition, even though , , and spp. represented the main food source for both. Albeit prey composition did not indicate the use of different water bodies by the sexes, male diet was characterized by higher prey diversity within a pellet and the consumption of larger fish. The current findings show that female and male cormorants to some extent target the available prey spectrum at different levels. Finally, the comprehensive and noninvasive approach has great potential for application in studies of other piscivorous bird species.
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http://dx.doi.org/10.1002/ece3.4421DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6157673PMC
September 2018

Resolving the predator first paradox: Arthropod predator food webs in pioneer sites of glacier forelands.

Mol Ecol 2019 01 7;28(2):336-347. Epub 2018 Sep 7.

Department of Ecology, University of Innsbruck, Innsbruck, Austria.

Primary succession on bare ground surrounded by intact ecosystems is, during its first stages, characterized by predator-dominated arthropod communities. However, little is known on what prey sustains these predators at the start of succession and which factors drive the structure of these food webs. As prey availability can be extremely patchy and episodic in pioneer stages, trophic networks might be highly variable. Moreover, the importance of allochthonous versus autochthonous food sources for these pioneer predators is mostly unknown. To answer these questions, the gut content of 1,832 arthropod predators, including four species of carabid beetles, two lycosid and several linyphiid spider species caught in early and late pioneer stages of three glacier forelands, was screened molecularly to track intraguild and extraguild trophic interactions among all major prey groups occurring in these systems. Two-thirds of the 2,310 identified food detections were collembolans and intraguild prey, while one-third were allochthonous flying insects. Predator identity and not successional stage or valley had by far the strongest impact on the trophic interaction patterns. Still, the variability of prey spectra increased significantly from early to late pioneer stage, as did the niche width of the predators. As such the structure of pioneer arthropod food webs in recently deglaciated Alpine habitats seems to be driven foremost by predator identity while site and early successional effects contribute to a lesser extent to food web variability. Our findings also suggest that in these pioneer sites, predatory arthropods depend less on allochthonous aeolian prey but are mainly sustained by prey of local production.
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http://dx.doi.org/10.1111/mec.14839DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6378689PMC
January 2019

Ecosystem function in predator-prey food webs-confronting dynamic models with empirical data.

J Anim Ecol 2019 02 7;88(2):196-210. Epub 2018 Sep 7.

Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

Most ecosystem functions and related services involve species interactions across trophic levels, for example, pollination and biological pest control. Despite this, our understanding of ecosystem function in multitrophic communities is poor, and research has been limited to either manipulation in small communities or statistical descriptions in larger ones. Recent advances in food web ecology may allow us to overcome the trade-off between mechanistic insight and ecological realism. Molecular tools now simplify the detection of feeding interactions, and trait-based approaches allow the application of dynamic food web models to real ecosystems. We performed the first test of an allometric food web model's ability to replicate temporally nonaggregated abundance data from the field and to provide mechanistic insight into the function of predation. We aimed to reproduce and explore the drivers of the population dynamics of the aphid herbivore Rhopalosiphum padi observed in ten Swedish barley fields. We used a dynamic food web model, taking observed interactions and abundances of predators and alternative prey as input data, allowing us to examine the role of predation in aphid population control. The inverse problem methods were used for simultaneous model fit optimization and model parameterization. The model captured >70% of the variation in aphid abundance in five of ten fields, supporting the model-embodied hypothesis that body size can be an important determinant of predation in the arthropod community. We further demonstrate how in-depth model analysis can disentangle the likely drivers of function, such as the community's abundance and trait composition. Analysing the variability in model performance revealed knowledge gaps, such as the source of episodic aphid mortality, and general method development needs that, if addressed, would further increase model success and enable stronger inference about ecosystem function. The results demonstrate that confronting dynamic food web models with abundance data from the field is a viable approach to evaluate ecological theory and to aid our understanding of function in real ecosystems. However, to realize the full potential of food web models, in ecosystem function research and beyond, trait-based parameterization must be refined and extended to include more traits than body size.
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http://dx.doi.org/10.1111/1365-2656.12892DOI Listing
February 2019

Facultative bacterial endosymbionts shape parasitoid food webs in natural host populations: A correlative analysis.

J Anim Ecol 2018 09 16;87(5):1440-1451. Epub 2018 Jul 16.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

Facultative bacterial endosymbionts can protect their aphid hosts from natural enemies such as hymenopteran parasitoids. As such, they have the capability to modulate interactions between aphids, parasitoids and hyperparasitoids. However, the magnitude of these effects in natural aphid populations and their associated parasitoid communities is currently unknown. Moreover, environmental factors such as plant fertilization and landscape complexity are known to affect aphid-parasitoid interactions but it remains unclear how such environmental factors affect the interplay between aphids, parasitoids and endosymbionts. Here, we tested whether facultative endosymbionts confer protection to parasitoids in natural populations of the English grain aphid, Sitobion avenae, and if this is affected by plant fertilization and landscape complexity. Furthermore, we examined whether the effects of facultative endosymbionts can cascade up to the hyperparasitoid level and increase primary-hyperparasitoid food web specialization. Living aphids and mummies were collected in fertilized and unfertilized plots within 13 wheat fields in Central Germany. We assessed the occurrence of primary parasitoid, hyperparasitoid and endosymbiont species in aphids and mummies using a newly established molecular approach. Facultative endosymbiont infection rates were high across fields (~80%), independent of whether aphids were parasitized or unparasitized. Aphid mummies exhibited a significantly lower share of facultative endosymbiont infection (~38%). These findings suggest that facultative endosymbionts do not affect parasitoid oviposition behaviour, but decrease parasitoid survival in the host. Facultative endosymbiont infection rates were lower in mummies collected from fertilized compared to unfertilized plants, indicating that plant fertilization boosts the facultative endosymbiont protective effect. Furthermore, we found strong evidence for species-specific and negative cascading effects of facultative endosymbionts on primary and hyperparasitoids, respectively. Facultative endosymbionts impacted parasitoid assemblages and increased the specialization of primary-hyperparasitoid food webs: these effects were independent from and much stronger than other environmental factors. The current findings strongly suggest that facultative endosymbionts act as a driving force in aphid-parasitoid-hyperparasitoid networks: they shape insect community composition at different trophic levels and modulate, directly and indirectly, the interactions between aphids, parasitoids and their environment.
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http://dx.doi.org/10.1111/1365-2656.12875DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6099228PMC
September 2018

High Redundancy as well as Complementary Prey Choice Characterize Generalist Predator Food Webs in Agroecosystems.

Sci Rep 2018 05 23;8(1):8054. Epub 2018 May 23.

Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

Food web structure influences ecosystem functioning and the strength and stability of associated ecosystem services. With their broad diet, generalist predators represent key nodes in the structure of many food webs and they contribute substantially to ecosystem services such as biological pest control. However, until recently it has been difficult to empirically assess food web structure with generalist predators. We utilized DNA-based molecular gut-content analyses to assess the prey use of a set of generalist invertebrate predator species common in temperate agricultural fields. We investigated the degree of specialization of predator-prey food webs at two key stages of the cropping season and analysed the link temperature of different trophic links, to identify non-random predation. We found a low level of specialization in our food webs, and identified warm and cool links which may result from active prey choice or avoidance. We also found a within-season variation in interaction strength between predators and aphid pests which differed among predator species. Our results show a high time-specific functional redundancy of the predator community, but also suggest temporally complementary prey choice due to within-season succession of some predator species.
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http://dx.doi.org/10.1038/s41598-018-26191-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5966386PMC
May 2018

Habitat heterogeneity induces rapid changes in the feeding behaviour of generalist arthropod predators.

Funct Ecol 2018 03 10;32(3):809-819. Epub 2018 Jan 10.

Mountain Agriculture Research UnitInstitute of Ecology University of Innsbruck Innsbruck Austria.

The "habitat heterogeneity hypothesis" predicts positive effects of structural complexity on species coexistence. Increasing habitat heterogeneity can change the diversity (number of species, abundances) and the functional roles of communities. The latter, however, is not well understood as species and individuals may respond very differently and dynamically to a changing environment.Here, we experimentally test how habitat heterogeneity affects generalist arthropod predators, including epigaeic spiders, carabid and staphylinid beetles, under natural conditions by assessing their diversity and directly measuring their trophic interactions (which provide a proxy for their functional roles). The experiment was conducted in spring barley fields in Southern Sweden where habitat heterogeneity was manipulated by increasing within-field plant diversity.Increased habitat heterogeneity triggered rapid changes in the feeding behaviour of generalist predators characterized by lower trophic specialization at both network (H', degree of interaction specialization in the entire network) and species level (d', degree of interaction specialization at the species level). We presume that this is because spatial separation resulted in relaxed competition and allowed an increased overlap in resources used among predator species. Predators collected from heterogenous habitats also showed greater individual-level dietary variability which might be ascribed to relaxed intraspecific competition.Our results provide conclusive evidence that habitat heterogeneity can induce rapid behavioural responses independent of changes in diversity, potentially promoting the stability of ecosystem functions. A plain language summary is available for this article.
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http://dx.doi.org/10.1111/1365-2435.13028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5887929PMC
March 2018

Comparing three types of dietary samples for prey DNA decay in an insect generalist predator.

Mol Ecol Resour 2018 Mar 6. Epub 2018 Mar 6.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

The rapidly growing field of molecular diet analysis is becoming increasingly popular among ecologists, especially when investigating methodologically challenging groups, such as invertebrate generalist predators. Prey DNA detection success is known to be affected by multiple factors; however, the type of dietary sample has rarely been considered. Here, we address this knowledge gap by comparing prey DNA detection success from three types of dietary samples. In a controlled feeding experiment, using the carabid beetle Pterostichus melanarius as a model predator, we collected regurgitates, faeces and whole consumers (including their gut contents) at different time points postfeeding. All dietary samples were analysed using multiplex PCR, targeting three different length DNA fragments (128, 332 and 612 bp). Our results show that both the type of dietary sample and the size of the DNA fragment contribute to a significant part of the variation found in the detectability of prey DNA. Specifically, we observed that in both regurgitates and whole consumers, prey DNA was detectable significantly longer for all fragment sizes than for faeces. Based on these observations, we conclude that prey DNA detected from regurgitates and whole consumers DNA extracts are comparable, whereas prey DNA detected from faeces, though still sufficiently reliable for ecological studies, will not be directly comparable to the former. Therefore, regurgitates and faeces constitute a useful, nonlethal source for dietary information that could be applied to field studies in situations when invertebrate predators should not be killed.
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http://dx.doi.org/10.1111/1755-0998.12775DOI Listing
March 2018

Species composition and seasonal dynamics of aphid parasitoids and hyperparasitoids in wheat fields in northern China.

Sci Rep 2017 10 25;7(1):13989. Epub 2017 Oct 25.

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.

Parasitoids are important natural enemies of aphids in wheat fields of northern China, and interest in them has increased in recent years. However, little is known regarding parasitoids of wheat aphids, which has hindered the study and understanding of aphid-parasitoid interactions. In the present study, three primary parasitoids and 15 hyperparasitoids were collected in wheat fields during a 2-year survey in northern China (2014, 2015) and a 2-year investigation at Langfang, Hebei Province (2015, 2016). Among them, Aphidius uzbekistanicus Luzhetski was found most frequently among the primary parasitoids, while Pachyneuron aphidis (Bouché) dominated the hyperparasitoid community. Investigation of the dynamics of wheat aphids and parasitoids revealed that the primary parasitoids appeared early in the growing period and that the hyperparasitoids appeared later. Analysis of the seasonal dynamics revealed that growth of the parasitoid population followed that of the aphid population and that the parasitism rates were highest in the late growing period.
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http://dx.doi.org/10.1038/s41598-017-14441-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5656665PMC
October 2017

Evaluation of an automated protocol for efficient and reliable DNA extraction of dietary samples.

Ecol Evol 2017 08 7;7(16):6382-6389. Epub 2017 Jul 7.

Mountain Agriculture Research Unit Institute of Ecology University of Innsbruck Innsbruck Austria.

Molecular techniques have become an important tool to empirically assess feeding interactions. The increased usage of next-generation sequencing approaches has stressed the need of fast DNA extraction that does not compromise DNA quality. Dietary samples here pose a particular challenge, as these demand high-quality DNA extraction procedures for obtaining the minute quantities of short-fragmented food DNA. Automatic high-throughput procedures significantly decrease time and costs and allow for standardization of extracting total DNA. However, these approaches have not yet been evaluated for dietary samples. We tested the efficiency of an automatic DNA extraction platform and a traditional CTAB protocol, employing a variety of dietary samples including invertebrate whole-body extracts as well as invertebrate and vertebrate gut content samples and feces. Extraction efficacy was quantified using the proportions of successful PCR amplifications of both total and prey DNA, and cost was estimated in terms of time and material expense. For extraction of total DNA, the automated platform performed better for both invertebrate and vertebrate samples. This was also true for prey detection in vertebrate samples. For the dietary analysis in invertebrates, there is still room for improvement when using the high-throughput system for optimal DNA yields. Overall, the automated DNA extraction system turned out as a promising alternative to labor-intensive, low-throughput manual extraction methods such as CTAB. It is opening up the opportunity for an extensive use of this cost-efficient and innovative methodology at low contamination risk also in trophic ecology.
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http://dx.doi.org/10.1002/ece3.3197DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5574753PMC
August 2017

The influence of meal size on prey DNA detectability in piscivorous birds.

Mol Ecol Resour 2017 Nov 14;17(6):e174-e186. Epub 2017 Oct 14.

Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

Molecular methods allow noninvasive assessment of vertebrate predator-prey systems at high taxonomic resolution by examining dietary samples such as faeces and pellets. To facilitate the interpretation of field-derived data, feeding trials, investigating the impacts of biological, methodological and environmental factors on prey DNA detection, have been conducted. The effect of meal size, however, has not yet been explicitly considered for vertebrate consumers. Moreover, different noninvasively obtained sample types remain to be compared in such experiments. Here, we present a feeding trial on abundant piscivorous birds, Great Cormorants (Phalacrocorax carbo), to assess meal size effects on postfeeding prey DNA detection success. Faeces and pellets were sampled twice a day after the feed of large (350-540 g), medium (190-345 g) and small (15-170 g) fish meals contributing either a large (>79%) or small (<38%) share to the daily consumption. Samples were examined for prey DNA and fish hard parts. Molecular analysis of faeces revealed that both large meal size and share had a significantly positive effect on prey DNA detection rate postfeeding. Furthermore, large meals were detectable for a significantly longer time span with a detection limit at ~76 hr and a 50% detection probability at ~32 hr postfeeding. In pellets, molecular methods reliably identified the meal consumed the previous day, which was not possible via morphological analysis or when examining individual faeces. The less reliable prey DNA detection of small meals or meal shares in faeces signifies the importance of large numbers of dietary samples to obtain reliable trophic data.
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http://dx.doi.org/10.1111/1755-0998.12706DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5725817PMC
November 2017

An effective molecular approach for assessing cereal aphid-parasitoid-endosymbiont networks.

Sci Rep 2017 06 9;7(1):3138. Epub 2017 Jun 9.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

Molecular approaches are increasingly being used to analyse host-parasitoid food webs as they overcome several hurdles inherent to conventional approaches. However, such studies have focused primarily on the detection and identification of aphids and their aphidiid primary parasitoids, largely ignoring primary parasitoid-hyperparasitoid interactions or limiting these to a few common species within a small geographical area. Furthermore, the detection of bacterial secondary endosymbionts has not been considered in such assays despite the fact that endosymbionts may alter aphid-parasitoid interactions, as they can confer protection against parasitoids. Here we present a novel two-step multiplex PCR (MP-PCR) protocol to assess cereal aphid-primary parasitoid-hyperparasitoid-endosymbiont interactions. The first step of the assay allows detection of parasitoid DNA at a general level (24 primary and 16 hyperparasitoid species) as well as the species-specific detection of endosymbionts (3 species) and cereal aphids (3 species). The second step of the MP-PCR assay targets seven primary and six hyperparasitoid species that commonly occur in Central Europe. Additional parasitoid species not covered by the second-step of the assay can be identified via sequencing 16S rRNA amplicons generated in the first step of the assay. The approach presented here provides an efficient, highly sensitive, and cost-effective (~consumable costs of 1.3 € per sample) tool for assessing cereal aphid-parasitoid-endosymbiont interactions.
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http://dx.doi.org/10.1038/s41598-017-02226-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5466676PMC
June 2017

Evaluation of three molecular markers for identification of European primary parasitoids of cereal aphids and their hyperparasitoids.

PLoS One 2017 31;12(5):e0177376. Epub 2017 May 31.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Innsbruck, Austria.

Aphids are major pests of cereal crops and a suite of hymenopteran primary parasitoids play an important role in regulating their populations. However, hyperparasitoids may disrupt the biocontrol services provided by primary parasitoids. As such, understanding cereal aphid-primary parasitoid-hyperparasitoid interactions is vital for a reliable parasitoid-based control of cereal aphids. For this, the ability to identify the different primary and hyperparasitoid species is necessary. Unfortunately, this is often difficult due to a lack of morphologically diagnostic features. DNA sequence-based species identification of parasitoids can overcome these hurdles. However, comprehensive DNA sequence information is lacking for many of these groups, particularly for hyperparasitoids. Here we evaluate three genes [cytochrome c oxidase subunit I (COI), 16S ribosomal RNA (16S) and 18S ribosomal RNA (18S)] for their suitability to identify 24 species of primary parasitoids and 16 species of hyperparasitoids associated with European cereal aphids. To identify aphelinid primary parasitoid species and hyperparasitoids, we found 16S to be more suitable compared to COI sequences. In contrast, the Aphidiinae are best identified using COI due to better species-level resolution and a more comprehensive DNA sequence database compared to 16S. The 18S gene was better suited for group-specific identification of parasitoids, but did not provide resolution at the species level. Our results provide a DNA sequence database for cereal aphid primary parasitoids and their associated hyperparasitoids in Central Europe, which will allow further improvement of our understanding of cereal aphid-primary parasitoid-hyperparasitoid interactions in relation to aphid biological control.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0177376PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451020PMC
September 2017

Diet analysis in piscivorous birds: What can the addition of molecular tools offer?

Ecol Evol 2017 Mar 23;7(6):1984-1995. Epub 2017 Feb 23.

Institute of Ecology University of Innsbruck Innsbruck Austria.

In trophic studies on piscivorous birds, it is vital to know which kind of dietary sample provides the information of interest and how the prey can be identified reliably and efficiently. Often, noninvasively obtained dietary samples such as regurgitated pellets, feces, and regurgitated fish samples are the preferred source of information. Fish prey has usually been identified via morphological analysis of undigested hard parts, but molecular approaches are being increasingly used for this purpose. What remains unknown, however, is which dietary sample type is best suited for molecular diet analysis and how the molecular results compare to those obtained by morphological analysis. Pellets, feces, and regurgitated fish samples of Great Cormorants () were examined for prey using both morphological hard part analysis and molecular prey identification. The sample types and methods were compared regarding number of species detected (overall and per sample) as well as the prey species composition and its variability among individual samples. Via molecular analysis, significantly higher numbers of prey species were detected in pellets, feces, and fish samples. Of the three sample types, pellets contained the most comprehensive trophic information and could be obtained with the lowest sampling effort. Contrastingly, dietary information obtained from feces was least informative and most variable. For all sample types, the molecular approach outperformed morphological hard part identification regarding the detectable prey spectrum and prey species composition. We recommend the use of pellets in combination with molecular prey identification to study the diet of piscivorous birds.
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http://dx.doi.org/10.1002/ece3.2790DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5355203PMC
March 2017

Diet of generalist predators reflects effects of cropping period and farming system on extra- and intraguild prey.

Ecol Appl 2017 06 16;27(4):1167-1177. Epub 2017 Mar 16.

Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, 75007, Uppsala, Sweden.

The suppression of agricultural pests by natural enemies, including generalist arthropod predators, is an economically important regulating ecosystem service. Besides pests, generalist predators may also consume non-pest extraguild and intraguild prey, which can affect their impact on pest populations. This may either reduce the impact of generalist predators on pest populations, because they are diverted from pest predation, or increase it, as it helps them survive periods of low pest availability. However, the availability of pest prey and alternative, non-pest prey can vary over the crop growing season and between farming systems, potentially affecting predator-prey interactions and the levels of biological control. We have limited information about how farming systems and environmental variation over the crop growing season influence predator diets. This limits our ability to predict the importance of generalist predators as natural enemies of agricultural pests. Here we utilize molecular gut content analyses to assess detection frequencies of extra- and intraguild prey DNA in generalist predator communities in replicated organically and conventionally managed cereal fields at two key periods of the cropping season for aphid biological control. This is done in order to understand how farming system, crop season, prey availability and predator community composition determine the composition of predator diets. Aphid pests and decomposers (springtails) were equally important prey for generalist predators early in the growing season. Later in the season, the importance of aphid prey increased with increasing aphid densities while springtail predation rates were positively correlated to abundance of this prey at both early and late crop growth stages. Intraguild predation was unidirectional: carabids fed on spiders, whereas spiders rarely fed on carabids. Carabids had higher detection frequencies for the two most common spider families in organically compared to conventionally managed fields. Our study documents that predation by generalist predator communities on aphid pests increases with pest numbers independently of their generally widespread consumption of alternative, non-pest prey. Therefore, conservation strategies in agricultural fields could promote biological control services by promoting high levels of alternative non-pest prey for generalist predator communities.
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http://dx.doi.org/10.1002/eap.1510DOI Listing
June 2017

Diagnostic PCR assays to unravel food web interactions in cereal crops with focus on biological control of aphids.

J Pest Sci (2004) 2016;89:281-293. Epub 2015 Aug 11.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstraße 25, 6020 Innsbruck, Austria.

Successful biological control of agricultural pests is dependent on a thorough understanding of the underlying trophic interactions between predators and prey. Studying trophic interactions can be challenging, particularly when generalist predators that frequently use multiple prey and interact with both pest and alternative prey are considered. In this context, diagnostic PCR proved to be a suitable approach, however at present, prey-specific PCR primers necessary for assessing such interactions across trophic levels are missing. Here we present a new set of 45 primers designed to target a wide range of invertebrate taxa common to temperate cereal crops: cereal aphids, their natural enemies such as carabid beetles, ladybeetles, lacewings, and spiders, and potential alternative prey groups (earthworms, springtails, and dipterans). These primers were combined in three 'ready to use' multiplex PCR assays for quick and cost-effective analyses of large numbers of predator samples. The assays were tested on 560 carabids collected in barley fields in Sweden. Results from this screening suggest that aphids constitute a major food source for carabids in cereal crops (overall DNA detection rate: 51 %), whereas alternative extraguild and intraguild prey appear to be less frequently preyed upon when aphids are present (11 % for springtails and 12 % for earthworms; 1 % for spiders and 4 % for carabids). In summary, the newly developed molecular assays proved reliable and effective in assessing previously cryptic predator-prey trophic interactions, specifically with focus on biological control of aphids. The diagnostic PCR assays will be applicable manifold as the targeted invertebrates are common to many agricultural systems of the temperate region.
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http://dx.doi.org/10.1007/s10340-015-0685-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4757624PMC
August 2015

Food Web Designer: a flexible tool to visualize interaction networks.

J Pest Sci (2004) 2016;89:1-5. Epub 2015 Aug 9.

Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstraße 25, 6020 Innsbruck, Austria.

Species are embedded in complex networks of ecological interactions and assessing these networks provides a powerful approach to understand what the consequences of these interactions are for ecosystem functioning and services. This is mandatory to develop and evaluate strategies for the management and control of pests. Graphical representations of networks can help recognize patterns that might be overlooked otherwise. However, there is a lack of software which allows visualizing these complex interaction networks. Food Web Designer is a stand-alone, highly flexible and user friendly software tool to quantitatively visualize trophic and other types of bipartite and tripartite interaction networks. It is offered free of charge for use on Microsoft Windows platforms. Food Web Designer is easy to use without the need to learn a specific syntax due to its graphical user interface. Up to three (trophic) levels can be connected using links cascading from or pointing towards the taxa within each level to illustrate top-down and bottom-up connections. Link width/strength and abundance of taxa can be quantified, allowing generating fully quantitative networks. Network datasets can be imported, saved for later adjustment and the interaction webs can be exported as pictures for graphical display in different file formats. We show how Food Web Designer can be used to draw predator-prey and host-parasitoid food webs, demonstrating that this software is a simple and straightforward tool to graphically display interaction networks for assessing pest control or any other type of interaction in both managed and natural ecosystems from an ecological network perspective.
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http://dx.doi.org/10.1007/s10340-015-0686-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4757606PMC
August 2015

Maximizing dietary information retrievable from carcasses of Great Cormorants using a combined morphological and molecular analytical approach.

Ibis (Lond 1859) 2016 Jan 15;158(1):51-60. Epub 2015 Dec 15.

Institute of Ecology University of Innsbruck Technikerstraße 25 6020 Innsbruck Austria.

Avian carcasses can provide important information on the trophic ecology of birds. Usually, the number of carcasses available for examination is limited and therefore it is important to gain as much dietary information per specimen as possible. In piscivorous birds and raptors, the stomach has been the primary source of dietary information, whereas the gut (intestine) has so far been neglected as it usually contains only a few morphologically identifiable hard parts of prey. Molecular approaches have the potential to retrieve dietary information from the gut, although this has not yet been verified. As well as identifying the prey, it is important to estimate any secondary predation to avoid food web errors in dietary analyses. The assignment of accidentally consumed prey is notoriously difficult regardless of the prey identification approach used. In the present study, morphological and molecular analyses were, for the first time, combined to maximize the dietary information retrievable from the complete digestive tract of Great Cormorants . Moreover, a novel approach based on predator-prey size ratios was applied to these piscivorous birds to minimize the number of samples that might contain secondarily predated prey. The stomach contents of the examined birds were found to provide the most dietary information when morphological and molecular analyses were used in combination. However, compared with the morphological approach, the molecular analysis increased the number of fish species detected by 39%. The molecular approach also permitted the identification of fish DNA in the Cormorant guts. Predator-prey size ratios derived from morphological analysis of fish hard parts can reduce the incidence of potential confounding influence of secondarily predated prey by 80%. Our findings demonstrate that a combination of morphological and molecular approaches maximizes the trophic information retrievable from bird carcasses.
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http://dx.doi.org/10.1111/ibi.12337DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4739555PMC
January 2016

Trophic and Non-Trophic Interactions in a Biodiversity Experiment Assessed by Next-Generation Sequencing.

PLoS One 2016 9;11(2):e0148781. Epub 2016 Feb 9.

Agroecology, Department of Crop Sciences, Georg-August University Goettingen, Grisebachstr. 6, 37077, Goettingen, Germany.

Plant diversity affects species richness and abundance of taxa at higher trophic levels. However, plant diversity effects on omnivores (feeding on multiple trophic levels) and their trophic and non-trophic interactions are not yet studied because appropriate methods were lacking. A promising approach is the DNA-based analysis of gut contents using next generation sequencing (NGS) technologies. Here, we integrate NGS-based analysis into the framework of a biodiversity experiment where plant taxonomic and functional diversity were manipulated to directly assess environmental interactions involving the omnivorous ground beetle Pterostichus melanarius. Beetle regurgitates were used for NGS-based analysis with universal 18S rDNA primers for eukaryotes. We detected a wide range of taxa with the NGS approach in regurgitates, including organisms representing trophic, phoretic, parasitic, and neutral interactions with P. melanarius. Our findings suggest that the frequency of (i) trophic interactions increased with plant diversity and vegetation cover; (ii) intraguild predation increased with vegetation cover, and (iii) neutral interactions with organisms such as fungi and protists increased with vegetation cover. Experimentally manipulated plant diversity likely affects multitrophic interactions involving omnivorous consumers. Our study therefore shows that trophic and non-trophic interactions can be assessed via NGS to address fundamental questions in biodiversity research.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0148781PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4747541PMC
August 2016
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