Using network ecology to understand and mitigate long‐term insect declines

Atmospheric Nitrogen Dioxide data from the UK Environmental Change Network (ECN) terrestrial sites. These data (weight of NO2) are collected by diffusion tubes at all of ECN's terrestrial sites using a standard protocol. They represent continuous fortnightly records from 1993 to 2015. ECN is the UK's long-term environmental monitoring programme. It is a multi-agency programme sponsored by a consortium of fourteen government departments and agencies. These organisations contribute to the programme through funding either site monitoring and/or network co-ordination activities. These organisations are: Agri-Food and Biosciences Institute, Biotechnology and Biological Sciences Research Council, Cyfoeth Naturiol Cymru - Natural Resources Wales, Defence Science & Technology Laboratory, Department for Environment, Food and Rural Affairs, Environment Agency, Forestry Commission, Llywodraeth Cymru - Welsh Government, Natural England, Natural Environment Research Council, Northern Ireland Environment Agency, Scottish Environment Protection Agency, Scottish Government and Scottish Natural Heritage.

The greenbug, Schizaphis graminum (Rondani), is a major pest of cereals in some parts of the world and is of particular concern because it can be resistant to some insecticides and overcome the resistance of crops. In the UK, it has never been found on crops, but two rather little-known and closely-related species (Schizaphis holci and Schizaphis agrostis) are associated with the wild grasses, Holcus lanatus and Agrostis stolonifera. Since 1987, winged (alate) aphids morphologically resembling the greenbug have been found in increasing numbers in 12.2m high suction-trap samples of the Rothamsted Insect Survey (RIS); hence, studies were undertaken to establish their identity. Clones (=asexual lineages) established from populations collected from H. lanatus in southern England showed strong preference for Holcus over Agrostis and Hordeum in laboratory tests and produced sexual morphs when transferred to short-day conditions, the males being apterous, as expected for S. holci. Multivariate morphometric comparisons of alatae caught in UK RIS suction traps in 2007 and 2011 with named specimens from museum collections, including S. graminum from many countries, indicated that the suction-trapped alatae were mostly S. agrostis and S. holci. Cytochrome c oxidase subunit I (COI) mtDNA obtained from 62 UK specimens from suction-traps had 95.4-100% sequence identity with US specimens of S. graminum. Two of the UK specimens had identical COI sequence to the US sorghum-adapted form of S. graminum, and these specimens also had 100% identity with a 640bp fragment of nDNA CytC, indicating that this form of S. graminum may already be present in the UK. Present and future economic implications of these results are discussed.

<p>Long-term monitoring data that considers a wide array of environmental variables provides key insights to environmental change because responses of ecosystem functions and services to environmental drivers are inherently long-term and strongly interlinked. To ensure that the data are reliable for analysis and interpretation, they must undergo quality assurance procedures. However, the expected or acceptable range of data values vary greatly as the state of the ecosystem changes. Current quality assurance procedures for environmental data take no consideration of the system state at which each measurement is made, and provide the user with little contextual information on the probable cause for a measurement to be flagged out of range. We propose the use of data science techniques to tag each measurement with an identified system state. The term “state” here is defined loosely and they are identified using k-means clustering, an unsupervised machine learning method. The meaning of the states is open to specialist interpretation. Once the states are identified, state-dependent prediction intervals can be calculated for each observational variable. This approach provides the user with more contextual information to resolve out-of-range flags and derive prediction intervals for observational variables that considers the changes in system states. Our highly flexible and efficient approach is applicable to any point data time series in earth and environmental sciences, regardless of their sub-discipline. Such advantage is particularly relevant when conducting simultaneous analysis of multiple processes and feedbacks, where a wide variety of data is used.</p><p>We illustrate our approach using the moth and butterfly data from the UK Environmental Change Network (ECN), where meteorological variables are used to define system states. A web application is publicly available to allow users to explore the method on various ECN site, while a generic is also available for users to upload their own data files. Our work contributes to the ongoing development of a better data science framework that allows researchers and other stakeholders to find and use the data they need more readily and reliably.</p><p> </p>

1. Aphids represent a significant challenge to food production. The Rothamsted Insect Survey (RIS) runs a network of 12·2-m suction-traps throughout the year to collect migrating aphids. In 2014, the RIS celebrated its 50th anniversary. This paper marks that achievement with an extensive spatiotemporal analysis and the provision of the first British annotated checklist of aphids since 1964.2. Our main aim was to elucidate mechanisms that advance aphid phenology under climate change and explain these using life-history traits. We then highlight emerging pests using accumulation patterns.3. Linear and nonlinear mixed-effect models estimated the average rate of change per annum and effects of climate on annual counts, first and last flights and length of flight season since 1965. Two climate drivers were used: the accumulated day degrees above 16 °C (ADD16) indicated the potential for migration during the aphid season; the North Atlantic Oscillation (NAO) signalled the severity of the winter before migration took place.4. All 55 species studied had earlier first flight trends at rate of β = −0·611 ± SE 0·015 days year−1. Of these species, 49% had earlier last flights, but the average species effect appeared relatively stationary (β = −0·010 ± SE 0·022 days year−1). Most species (85%) showed increasing duration of their flight season (β = 0·336 ± SE 0·026 days year−1), even though only 54% increased their log annual count (β = 0·002 ± SE <0·001 year−1).5. The ADD16 and NAO were shown to drive patterns in aphid phenology in a spatiotemporal context. Early in the year when the first aphids were migrating, the effect of the winter NAO was highly significant. Further into the year, ADD16 was a strong predictor. Latitude had a near linear effect on first flights, whereas longitude produced a generally less-clear effect on all responses. Aphids that are anholocyclic (permanently parthenogenetic) or are monoecious (non-host-alternating) were advancing their phenology faster than those that were not.6. Climate drives phenology and traits help explain how this takes place biologically. Phenology and trait ecology are critical to understanding the threat posed by emerging pests such as Myzus persicae nicotianae and Aphis fabae cirsiiacanthoidis, as revealed by the species accumulation analysis.

Genetic diversity is the determinant for pest species’ success and vector competence. Understanding the ecological and evolutionary processes that determine the genetic diversity is fundamental to help identify the spatial scale at which pest populations are best managed. In the present study, we present the first comprehensive analysis of the genetic diversity and evolution of Rhopalosiphum padi, a major pest of cereals and a main vector of the barley yellow dwarf virus (BYDV), in England. We have used a genotyping‐by‐sequencing approach to study whether (a) there is any underlying population genetic structure at a national and regional scale in this pest that can disperse long distances; (b) the populations evolve as a response to environmental change and selective pressures; and (c) the populations comprise anholocyclic lineages. Individual R. padi were collected using the Rothamsted Insect Survey's suction‐trap network at several sites across England between 2004 and 2016 as part of the RIS long‐term nationwide surveillance. Results identified two genetic clusters in England that mostly corresponded to a North–South division, although gene flow is ongoing between the two subpopulations. These genetic clusters do not correspond to different life cycle types, and cyclical parthenogenesis is predominant in England. Results also show that there is dispersal with gene flow across England, although there is a reduction between the northern and southern sites with the south‐western population being the most genetically differentiated. There is no evidence for isolation by distance and other factors such as primary host distribution, uncommon in the south and absent in the south‐west, could influence the dispersal patterns. Finally, results also show no evidence for the evolution of the R. padi population, and it is demographically stable despite the ongoing environmental change. These results are discussed in view of their relevance to pest management and the transmission of BYDV.

Changing patterns of morph frequency in three moth species (Biston betularia, Odontoptera bidentata and Apocheima pilosaria) have been investigated using data from the Rothamsted Insect Survey. All three exhibited industrial melanism during the period of high atmospheric pollution in Britain. Three historical and habitat types are compared, the old industrial north of England, rural Scotland, Wales and South-West England, and a southern English intermediate region of high human population density but generally low industrialization. Between 1974 and 1999 the carbonaria morph of B. betularia declined in frequency in the industrial region and is nearly absent from rural areas. It is the form which most closely tracks atmospheric change. It is shown that the insularia forms of B. betularia and the melanic morphs in the other two species have decreased in the industrial region, commencing later than carbonaria, but have maintained their presence and possibly reached equilibrium elsewhere. They may be non-industrial polymorphisms. B. betularia is rarer than the other species and all three species are at lower densities in industrial than in non-industrial regions.

Regional variation in the number of pea aphids caught in the suction traps of the Rothamsted Insect Survey (RIS) was associated with the proportion of each region under pea crops. The degree of infestation of crops was similar in areas of high and low pea production as the mean annual abundance of aphids per hectare of crop remained constant. Yearly variation in abundance was loosely associated with temperature from January to July. Cold weather in January and February resulted in large numbers of aphids. Warm weather in February led to early colonization, and emigration from, pea crops as well as making early sowing of the crop more likely. A forecast of the time of first appearance of Acyrthosiphon pisum in the aerial plankton can be made, based on February temperature. Populations of A. pisum on peas appear to be regulated by alata production. High densities of aphids resulted in almost all the nymphs developing into alatae which, on reaching maturity, emigrated, causing populations on the crop to decline. This explains population crashes of the pea aphid observed at early growth stages of the crop, on vining and combining peas. Late sowing of peas, a probable effect of cold winters, results in higher aphid densities at flowering. The probable explanation for this is that late‐sown crops are colonized at an earlier growth stage, so that the aphid population has a longer period of time in which to develop.

Indirect Mutualism: Variations on a Theme by Stephen Levine

An indicator highlights seasonal variation in the response of Lepidoptera communities to warming

Biomass production and plant species diversity in grassland in southern England was monitored before and after a change from conventional to organic farming. Our 18-year study, part of the UK's Environmental Change Network long-term monitoring programme, showed that the cessation of artificial fertiliser use on grassland after conversion to organic farming resulted in a decrease in biomass production and an increase in plant species richness. Grassland productivity decreased immediately after fertiliser application ceased, and after two years the annual total biomass production had fallen by over 50%. In the subsequent decade, total annual grassland productivity did not change significantly, and yields reached 31–66% of the levels recorded pre-management change. Plant species richness that had remained stable during the first 5 years of our study under conventional farming, increased by 300% over the following 13 years under organic farm management. We suggest that the change in productivity is due to the altered composition of species within the plots. In the first few years after the change in farming practice, high yielding, nitrogen-loving plants were outcompeted by lower yielding grasses and forbs, and these species remained in the plots in the following years. This study shows that grassland can be converted from an environment lacking in plant species diversity to a relatively species-rich pasture within 10–15 years, simply by stopping or suspending nitrogen additions. We demonstrate that the trade-off for increasing species richness is a decrease in productivity. Grassland in the UK is often not only managed from a conservation perspective, but to also produce a profitable yield. By considering the species composition and encouraging specific beneficial species such as legumes, it may be possible to improve biomass productivity and reduce the trade-off.

An overview of the results from the first 20 years of the monitoring and research at ECN Rothamsted. Originally published 2014, updated and reprinted 2015.

The observed insect decline, which threatens agricultural productivity and ecosystem stability, calls for comprehensive international insect monitoring. Monitoring implementation demands standardisation and the integration of new and innovative methods. Therefore, we compared two quantitative butterfly survey methods – the commonly applied transect counts (or ‘Pollard walks’) and more extensive area-time counts. We evaluated the influence of the two methods on the estimation of biodiversity variables such as species richness and species abundance to examine whether they could be applied alternatively for the calculation of butterfly trend indicators. During 576 surveys we conducted 5-minute transect counts and 25-minute area-time counts simultaneously at 144 different sites in Western Austria. The estimated relative butterfly abundance of the two methods for 119 observed species showed a strong linear relationship. While we found 2.4 times more species per site with the more extensive area-time counts than with the transect counts, we also observed a strong correlation between estimates of local abundance (Pearson’s r = 0.85) and observed species richness (Pearson’s r = 0.81) based on the two methods. Area-time counts provide thorough assessments on a given location, enabling a close connection to specific habitat types and facilitating comparability with other plot-based biodiversity assessments. They are more suitable than transect counts when aiming to analyse the drivers of temporal and spatial variability in butterfly occurrence. Furthermore, area-time counts can be used synergistically for the calculation of international butterfly abundance trends (e.g., European butterfly indicators), as we found strong linear relationships for all applied indicators with both methods.

Wolbachia are a group of cytoplasmically inherited bacteria that cause reproduction alterations in arthropods, including parthenogenesis, reproductive incompatibility, feminization of genetic males and male killing. Previous general surveys of insects in Panama and Britain found Wolbachia to be common, occurring in 16-22% of species. Here, using similar polymerase chain reaction methods, we report that 19.3% of a sample of temperate North American insects are infected with Wolbachia, a frequency strikingly similar to frequencies found in two other studies in widely separated locales. The results may indicate a widespread equilibrium of Wolbachia infection frequencies in insects whose maintenance remains to be explained. Alternatively, Wolbachia may be increasing in global insect communities. Within each of the three geographic regions surveyed, Hymenoptera are more frequently infected with A group Wolbachia and Lepidoptera more frequently infected with B group Wolbachia.

Sticky colored traps have been widely used for sampling of harmful insects in wild and cultivated plants worldwide. Colored sticky traps could be a simple and a low-cost method for determining the relative abundance of harmful and beneficial insects, including pollinators. However, knowledge about catches of nontargeted insects such as pollinators by colored traps is rudimentary. Trials were conducted to evaluate the attractiveness of various colors (white, yellow, blue, and green) to some pollinating insects in apple in Adana Province, Turkey, during 2011 and 2012. Colored plates were hung at about 1.70 m from ground level of the exterior canopy of the selected trees at the beginning of their blooming and they were positioned toward the 4 cardinal directions. A total of 7 insect species belonging to the families Syrphidae (6 species, Diptera) and Apidae (1 species, Hymenoptera) were identified. Pollinating hoverfly Eristalis tenax L. and honey bee Apis mellifera L. were frequently captured, and significantly more of them were captured on white traps (P &amp;amp;lt; 0.05). Blue and green colored traps were less attractive to both pollinator species. Cardinal directions did not have a significant effect on catches of E. tenax and A. mellifera on white traps. The use of white sticky traps may provide more ecological data for pollinators. However, using white colored traps for mass trapping of harmful insect species in fruit orchards may be risky due to reducing their numbers, particularly during blooming periods of the fruit orchards. Arrangements of sticky trap use prior to peak occurrence of the pollinators would be a better approach in terms of conservation of pollinators and sustainability of ecosystems.

Autumn control of rosy apple aphid, Dysaphis plantaginea (Passerini), with aphicides