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Abstract and Figures

Recent reports of local extinctions of arthropod species 1 , and of massive declines in arthropod biomass 2 , point to land-use intensification as a major driver of decreasing biodiversity. However, to our knowledge, there are no multisite time series of arthropod occurrences across gradients of land-use intensity with which to confirm causal relationships. Moreover, it remains unclear which land-use types and arthropod groups are affected, and whether the observed declines in biomass and diversity are linked to one another. Here we analyse data from more than 1 million individual arthropods (about 2,700 species), from standardized inventories taken between 2008 and 2017 at 150 grassland and 140 forest sites in 3 regions of Germany. Overall gamma diversity in grasslands and forests decreased over time, indicating loss of species across sites and regions. In annually sampled grasslands, biomass, abundance and number of species declined by 67%, 78% and 34%, respectively. The decline was consistent across trophic levels and mainly affected rare species; its magnitude was independent of local land-use intensity. However, sites embedded in landscapes with a higher cover of agricultural land showed a stronger temporal decline. In 30 forest sites with annual inventories, biomass and species number-but not abundance-decreased by 41% and 36%, respectively. This was supported by analyses of all forest sites sampled in three-year intervals. The decline affected rare and abundant species, and trends differed across trophic levels. Our results show that there are widespread declines in arthropod biomass, abundance and the number of species across trophic levels. Arthropod declines in forests demonstrate that loss is not restricted to open habitats. Our results suggest that major drivers of arthropod decline act at larger spatial scales, and are (at least for grasslands) associated with agriculture at the landscape level. This implies that policies need to address the landscape scale to mitigate the negative effects of land-use practices.
Contribution of individual years to overall trends a, To assess the contribution of individual years to the overall trend, we repeated the linear mixed models for overall biomass, abundance and number of species, and excluded one year each time. The distribution of t and z values for the effect of the year from subset models (white), and from the full models including all years (black), are shown (11 models for grasslands and 10 models for forests). Grey bars denote effect of the year 2008 (the year with the strongest effect on overall trend estimates). b, In addition, we tested whether the observed effect of year differed from a random expectation by randomizing the order of years 100× for forests and grasslands before modelling. The distribution of t and z values for the effect of the year from models with randomly ordered years (white) and models with the years ordered correctly (black) are shown (101 models each for grasslands and forests). Vertical dashed lines indicate levels of significance with P < 0.05. The results in a show that both weaker and stronger temporal trends could be detected when single years were excluded from the analysis, compared to the full model including all years. Results in b show that models with the years ordered randomly produced effects of the year that were normally distributed around zero, and only the models with years ordered correctly generated strong temporal trends. For a more detailed discussion, see Supplementary Information section 3.
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Effect of tree mortality on arthropod trends a, The relative change in the number of arthropod species between the first two and the final two study years was similar for managed (n = 19) and unmanaged (n = 9) forest sites (z = 0.648, P = 0.517, derived from a linear mixed model with relative difference in species number as response, harvesting category as fixed and region as random effect). Dots show raw data per site. Boxes represent data within the 25th and 75th percentile, black lines show medians, and whiskers show 1.5× the interquartile range. b, When considering actual tree mortality between forest inventories in 2009 and 2016, declines in the number of arthropod species were weaker at sites with higher tree mortality (z = 2.536, P = 0.011, derived from a linear mixed model with relative difference in species number as response, tree mortality as fixed and region as random effect). Dots show raw data per site. The blue line visualizes the significant relationship between the change in the number of arthropod species and tree mortality based on the linear mixed model, and the shaded area represents confidence intervals. This suggests that changes in habitat conditions and heterogeneity linked to tree mortality—such as increasing canopy openness, herb cover or deadwood availability—moderated declines in the number of arthropod species. More research is needed to identify mechanistic relationships. Tree mortality included both natural mortality and timber harvesting. Forest sites had a stand age of, on average, 116 years (minimum of 30 years and maximum of 180 years) and therefore did not include overmature stands. Owing to stand age and because management was abandoned 20 to 70 years before this study started, natural tree mortality was low even in unmanaged stands. We expect increasingly positive effects of natural tree mortality and associated increased structural diversity and heterogeneity⁴⁰ on arthropod trends with increasing stand age, but further research is required. In Germany, harvesting is usually conducted as shelterwood cutting. In our sites, the harvested amount over the course of our study reached a maximum of 1% of the standing volume per year. More intense harvesting systems (such as clear cutting), which lead to less heterogeneous habitat conditions, may not have similar moderating effects on arthropod declines.
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Nature | Vol 574 | 31 October 2019 | 671
Article
Arthropod decline in grasslands and forests
is associated with landscape-level drivers
Sebastian Seibold1,2*, Martin M. Gossner3, Nadja K. Simons1,4, Nico Blüthgen4, Jörg Müller2,5,
Didem Ambarlı1,6, Christian Ammer7, Jürgen Bauhus8, Markus Fischer9, Jan C. Habel1,10,
Karl Eduard Linsenmair11, Thomas Nauss12, Caterina Penone9, Daniel Prati9, Peter Schall7,
Ernst-Detlef Schulze13, Juliane Vogt1, Stephan Wöllauer12 & Wolfgang W. Weisser1
Recent reports of local extinctions of arthropod species1, and of massive declines in
arthropod biomass2, point to land-use intensication as a major driver of decreasing
biodiversity. However, to our knowledge, there are no multisite time series of
arthropod occurrences across gradients of land-use intensity with which to conrm
causal relationships. Moreover, it remains unclear which land-use types and arthropod
groups are aected, and whether the observed declines in biomass and diversity are
linked to one another. Here we analyse data from more than 1million individual
arthropods (about 2,700species), from standardized inventories taken between 2008
and 2017 at 150grassland and 140forest sites in 3regions of Germany. Overall gamma
diversity in grasslands and forests decreased over time, indicating loss of species
across sites and regions. In annually sampled grasslands, biomass, abundance and
number of species declined by 67%, 78% and 34%, respectively. The decline was
consistent across trophic levels and mainly aected rare species; its magnitude was
independent of local land-use intensity. However, sites embedded in landscapes with a
higher cover of agricultural land showed a stronger temporal decline. In 30forest sites
with annual inventories, biomass and species number—but not abundance—decreased
by 41% and 36%, respectively. This was supported by analyses of all forest sites sampled
in three-year intervals. The decline aected rare and abundant species, and trends
diered across trophic levels. Our results show that there are widespread declines in
arthropod biomass, abundance and the number of species across trophic levels.
Arthropod declines in forests demonstrate that loss is not restricted to open habitats.
Our results suggest that major drivers of arthropod decline act at larger spatial scales,
and are (at least for grasslands) associated with agriculture at the landscape level. This
implies that policies need to address the landscape scale to mitigate the negative
eects of land-use practices.
Much of the debate surrounding the human-induced biodiversity crisis
has focused on vertebrates
3
, but population declines and extinctions
may be even more substantial in small organisms such as terrestrial
arthropods
4
. Recent studies have reported declines in the biomass of
flying insects
2
, and in the diversity of insect pollinators
5,6
, butterflies
and moths
1,7–10
, hemipterans
11,12
and beetles
7,13,14
. Owing to the associated
negative effects on food webs
15
, ecosystem functioning and ecosystem
services
16
, this insect loss has spurred an intense public debate. However,
time-series data relating to arthropods are limited, and studies have
so far focused on a small range of taxa11,13,14, a few types of land use and
habitat
12
—or even on single sites
1,17
. In addition, many studies lack species
information
2
or high temporal resolution
2,12
. It therefore remains unclear
whether reported declines in arthropods are a general phenomenon
that is driven by similar mechanisms across land-use types, taxa and
functional groups.
The reported declines are suspected to be caused mainly by human
land use
2
. Locally, farming practices can affect arthropods directly by
application of insecticides
18,19
, mowing
20
or soil disturbance, or indirectly
via changes in plant communities through the application of herbi-
cides or fertilizer
21
. Forestry practices can also affect local arthropod
https://doi.org/10.1038/s41586-019-1684-3
Received: 8 February 2019
Accepted: 16 September 2019
Published online: 30 October 2019
1Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Technical University of Munich, Freising, Germany. 2Field Station Fabrikschleichach, Department of
Animal Ecology and Tropical Biology, Julius-Maximilians-University Würzburg, Würzburg, Germany. 3Forest Entomology, Swiss Federal Research Institute WSL, Birmensdorf, Switzerland.
4Ecological Networks, Department of Biology, Technical University of Darmstadt, Darmstadt, Germany. 5Bavarian Forest National Park, Grafenau, Germany. 6Department of Agricultural
Biotechnology, Faculty of Agricultural and Natural Sciences, Düzce University, Düzce, Turkey. 7Silviculture and Forest Ecology of the Temperate Zones, University of Göttingen, Göttingen,
Germany. 8Institute of Forest Sciences, Faculty of Environment and Natural Resources, University of Freiburg, Freiburg, Germany. 9Institute of Plant Sciences, University of Bern, Bern,
Switzerland. 10Evolutionary Zoology, Biosciences, Salzburg University, Salzburg, Austria. 11Department of Animal Ecology and Tropical Biology, Julius-Maximilians-University Würzburg,
Würzburg, Germany. 12Faculty of Geography, Philipps-University Marburg, Marburg, Germany. 13Max Planck Institute for Biogeochemistry, Jena, Germany. *e-mail: sebastian.seibold@tum.de
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... While most studies of temporal trends focus on species richness and/or abundance or occupancy of single groups (e.g., Habel et al., 2019;Janousek et al., 2023;Jönsson et al., 2021), other studies focus solely on the biomass of overall patterns without further taxonomic classification (Hallmann et al., 2017;Müller et al., 2023). The simultaneous assessment of temporal trends in species richness, abundance and biomass is rare (but see Fürst et al., 2022;Seibold et al., 2019). However, evaluating insect diversity trends and their potential consequences for ecosystem functioning and service provisioning is only possible with the joint analysis of richness, abundance and biomass data (Hallmann et al., 2021). ...
... The unmanaged study sites were composed of six unstocked, open study sites and six sites in unmanaged forests. Since patterns in insect trends have been shown to differ between habitats (Seibold et al., 2019), the analysis was conducted separately for the three habitat types. We considered temperature and precipitation as weather-related factors while we employed the normalised difference vegetation index (NDVI) as a land-use related factor. ...
... Our findings seem to contradict the common finding of declining insect richness with time (e.g., Hallmann et al., 2021;Homburg et al., 2019;Powney et al., 2019). For both overall diversity patterns (Hallmann et al., 2017;Seibold et al., 2019) and for different insect taxa, declining patterns are common, also during the 8 years we covered (Habel et al., 2019;Halsch et al., 2021;Janousek et al., 2023). ...
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... The DINA project was initiated to detect causes of insect decline as well as to develop measures to mitigate the decline of flying insects in NPA in Germany (Diversity of Insects in Nature protected Areas, [45]). Previous studies provide support for the assumption that agricultural practices are related to the decline in flying insect biomass [13,53]. Therefore, only NPA with neighbouring or integrated agricultural areas were included in the experimental design to determine if agricultural impact could be verified. ...
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... Consequently, the status of insects is critical for the functioning of many ecosystems, and their decline can have strong cascading effects on other trophic levels (e.g., Rosenberg et al., 2019). Such declines, both in abundance and diversity, have been well documented for the past half-century, especially in temperate regions of North America and Europe (Hallmann et al., 2017;Seibold et al., 2019;van Klink et al., 2020;Wagner, 2020). ...
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Along with the global decline of species richness goes a loss of ecological traits. Associated biotic homogenization of animal communities and narrowing of trait diversity threaten ecosystem functioning and human well‐being. High management intensity is regarded as an important ecological filter, eliminating species that lack suitable adaptations. Below‐ground arthropods are assumed to be less sensitive to such effects than above‐ground arthropods. Here, we compared the impact of management intensity between (grassland vs. forest) and within land‐use types (local management intensity) on the trait diversity and composition in below‐ and above‐ground arthropod communities. We used data on 722 arthropod species living above‐ground (Auchenorrhyncha and Heteroptera), primarily in soil (Chilopoda and Oribatida) or at the interface (Araneae and Carabidae). Our results show that trait diversity of arthropod communities is not primarily reduced by intense local land use, but is rather affected by differences between land‐use types. Communities of Auchenorrhyncha and Chilopoda had significantly lower trait diversity in grassland habitats as compared to forests. Carabidae showed the opposite pattern with higher trait diversity in grasslands. Grasslands had a lower proportion of large Auchenorrhyncha and Carabidae individuals, whereas Chilopoda and Heteroptera individuals were larger in grasslands. Body size decreased with land‐use intensity across taxa, but only in grasslands. The proportion of individuals with low mobility declined with land‐use intensity in Araneae and Auchenorrhyncha, but increased in Chilopoda and grassland Heteroptera. The proportion of carnivorous individuals increased with land‐use intensity in Heteroptera in forests and in Oribatida and Carabidae in grasslands. Our results suggest that gradients in management intensity across land‐use types will not generally reduce trait diversity in multiple taxa, but will exert strong trait filtering within individual taxa. The observed patterns for trait filtering in individual taxa are not related to major classifications into above‐ and below‐ground species. Instead, ecologically different taxa resembled each other in their trait diversity and compositional responses to land‐use differences. These previously undescribed patterns offer an opportunity to develop management strategies for the conservation of trait diversity across taxonomic groups in permanent grassland and forest habitats.
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