Collation of a century of soil invertebrate abundance data suggests long-term declines in earthworms but not tipulids

PLOS ONE RESEARCH ARTICLE Collation of a century of soil invertebrate abundance data suggests long-term declines in earthworms but not tipulids Ailidh E. Barnes ID1*, Robert A. Robinson1, James W. Pearce-Higgins1,2,3 1 British Trust for Ornithology, The Nunnery, Thetford, United Kingdom, 2 Conservation Science Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom, 3 School of Biological Sciences, University of East Anglia, Norwich, United Kingdom a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Barnes AE, Robinson RA, Pearce-Higgins JW (2023) Collation of a century of soil invertebrate abundance data suggests long-term declines in earthworms but not tipulids. PLoS ONE 18(4): e0282069. https://doi.org/10.1371/journal. pone.0282069 Editor: Tunira Bhadauria, Feroze Gandhi Degree College, INDIA Received: August 10, 2022 Accepted: February 7, 2023 Published: April 3, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0282069 Copyright: © 2023 Barnes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The data file collated for this study is available online in the figshare repository: https://doi.org/10.6084/m9.figshare. 21428121. * Abstract Large-scale declines in terrestrial insects have been reported over much of Europe and across the world, however, population change assessments of other key invertebrate groups, such as soil invertebrates, have been largely neglected through a lack of available monitoring data. This study collates historic data from previously published studies to assess whether it is possible to infer previously undocumented long-term changes in soil invertebrate abundance. Earthworm and tipulid data were collated from over 100 studies across the UK, spanning almost 100 years. Analyses suggested long-term declines in earthworm abundance of between 1.6 to 2.1% per annum, equivalent to a 33% to 41% decline over 25 years. These appeared greatest in broadleaved woodlands and farmland habitats, and were greater in pasture than arable farmland. Significant differences in earthworm abundance between habitats varied between models but appeared to be highest in urban greenspaces and agricultural pasture. More limited data were available on tipulid abundance, which showed no significant change over time or variation between enclosed farmland and unenclosed habitats. Declines in earthworm populations could be contributing to overall declines in ecosystem function and biodiversity as they are vital for a range of ecosystem services and are keystone prey for many vertebrate species. If robust, our results identify a previously undetected biodiversity decline that would be a significant conservation and economic issue in the UK, and if replicated elsewhere, internationally. We highlight the need for long-term and large-scale soil invertebrate monitoring, which potentially could be carried out by citizen/community scientists. Introduction After Hallman et al. [1] alerted the world to large-scale declines in the abundance of aerial insects across Germany (76% over 27 years), there has been considerable interest and debate in the extent to which different invertebrate groups have declined, and the causes of any such decline. Whilst some authors highlight growing evidence for large-scale insect declines across PLOS ONE | https://doi.org/10.1371/journal.pone.0282069 April 3, 2023 1 / 25 PLOS ONE Funding: We are extremely grateful to the many BTO donors and members who have funded this project, particularly Simon Cooke and Gillian & Justin Wills and the Penchant Foundation. We are also grateful to Kenneth Trouth whose Gift in Will supported our work on this paper. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Soil invertebrate declines the globe [2–5], others have expressed uncertainty over the extent of these declines [6, 7], in part because population trends appear to differ between taxa and studies [5]. For example, large-scale declines in pollinators [8, 9], including bees [10], macro-moths [11, 12], butterflies [13] and aerial insects [1] have been recorded, whilst other groups including emergent freshwater insects [14] and flying aphids [12] appear to have stable or increasing populations. For many other invertebrate groups, a lack of robust monitoring data has hampered our ability to detect long-term change [7]. Whilst the current focus of the literature has been on terrestrial insect declines, other key invertebrate groups have been largely neglected, again principally due to a lack of long-term monitoring data [15]. One such neglected group are soil invertebrates, which, as important detritivores, underpin many food webs, including important prey for a wide selection of vertebrate predators [16]. They are also critically important in the delivery of a wide range of ecosystem functions including nutrient cycling and soil formation [17, 18]. Despite this, soil invertebrates have been “woefully neglected in many biodiversity assessments and databases” [19]. For example, although earthworms dominate the biomass of most terrestrial ecosystems [20], their populations are not routinely monitored. This is despite them being a prime candidate for monitoring the health of soils [21], with well-established field methods and the potential for citizen science to inform large-scale earthworm monitoring [22, 23]. There is an urgent need to address this monitoring gap. Whilst it is clearly not possible to go back in time and generate monitoring data, soil invertebrates have often been the subject of ecological study generating a potentially accessible record of historical soil invertebrate abundance data, that may be used to infer changes through time [24]. Building on the approach of Robinson & Sutherland [25] who documented long-term declines in the availability of weed seeds on farmland from published studies, and recognising recent developments in generating large biodiversity datasets from previously published studies (e.g. van Klink [3]), we similarly attempt to identify potential long-term signals of changes in soil invertebrate abundance from published studies. The UK has a long history for ecological study, in which long-term changes in some insect populations have already been identified [26]. The fact that populations of many bird species that rely on (...truncated)