Abstract Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxonomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and mid-summer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.

Citation: Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, et al. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12(10): e0185809. https://doi.org/10.1371/journal.pone.0185809 Editor: Eric Gordon Lamb, University of Saskatchewan, CANADA Received: July 28, 2017; Accepted: September 19, 2017; Published: October 18, 2017 Copyright: © 2017 Hallmann 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: All relevant data are within the paper and its Supporting Information files. Funding: CH and EJ were supported by the Netherlands Organization for Scientific Research (NWO grants 840.11.001 and 841.11.007), and NH by the Triodos Foundation. The investigations of the Entomological Society Krefeld and its members are spread over numerous individual projects at different locations and in different years. Grants and permits that have made this work possible are listed below: Bezirksregierungen Düsseldorf & Köln, BfN - Bundesamt für Naturschutz, Land Nordrhein-Westfalen - Europäische Gemeinschaft ELER, Landesamt für Agrarordnung Nordrhein-Westfalen, Landesamt für Natur, Umwelt und Verbraucherschutz Nordrhein-Westfalen, Landesamt für Umwelt Brandenburg, Landesamt für Umwelt Rheinland-Pfalz, LVR - Landschaftsverband Rheinland, Naturschutzbund Deutschland, Nordrhein-Westfalen Stiftung, RBN Bergischer Naturschutzverein, RVR - Regionalverband Ruhr, SGD Nord Rheinland-Pfalz, Universitäten Bonn, Duisburg-Essen & Köln, Untere Landschaftsbehörden: Kreis Düren, Kreis Heinsberg, Kreis Kleve, Kreis Viersen, Kreis Wesel & AGLW, Stadt Düsseldorf, Stadt Köln, Stadt Krefeld, Rheinisch Bergischer Kreis, Rhein Kreis Neuss & Rhein-Sieg-Kreis. Members of the Entomological Society Krefeld and cooperating botanists and entomologists that were involved in the empirical investigations are greatly acknowledged: U.W. Abts, F. Bahr, A. Bäumler, D. & H. Beutler, P. Birnbrich, U. Bosch, J. Buchner, F. Cassese, K. Cölln, A.W. Ebmer, R. Eckelboom, B. Franzen, M. Grigo, J. Günneberg, J. Gusenleitner, K. Hamacher, F. Hartfeld, M. Hellenthal, J. Hembach, A. Hemmersbach, W. Hock, V. Huisman-Fiegen, J. Illmer, E. Jansen, U. Jäckel, F. Koch, M. Kreuels, P. Leideritz, I. Loksa, F. B. Ludescher, F. J. Mehring, G. Milbert, N. Mohr, P. Randazzo, K. Reissmann, S. Risch, B. Robert, J. de Rond, U. Sandmann, S. Scharf, P. Scherz, J. Schiffer, C. Schmidt, O. & W. Schmitz, B. P. & W. Schnell, J. L. Schönfeld, E. Schraetz, M. Schwarz, R. Seliger, H. W. Siebeneicher, F. & H. Sonnenburg W. J. S. & P. Sorg, A. Ssymank, H. Sticht, M. Weithmann, W. Wichard and H. Wolf. Competing interests: The authors have declared that no competing interests exist.

Introduction Loss of insects is certain to have adverse effects on ecosystem functioning, as insects play a central role in a variety of processes, including pollination [1, 2], herbivory and detrivory [3, 4], nutrient cycling [4] and providing a food source for higher trophic levels such as birds, mammals and amphibians. For example, 80% of wild plants are estimated to depend on insects for pollination [2], while 60% of birds rely on insects as a food source [5]. The ecosystem services provided by wild insects have been estimated at $57 billion annually in the USA [6]. Clearly, preserving insect abundance and diversity should constitute a prime conservation priority. Current data suggest an overall pattern of decline in insect diversity and abundance. For example, populations of European grassland butterflies are estimated to have declined by 50% in abundance between 1990 and 2011 [7]. Data for other well-studied taxa such as bees [8–14] and moths [15–18] suggest the same trend. Climate change, habitat loss and fragmentation, and deterioration of habitat quality have been proposed as some of the prime suspects responsible for the decline [9–11, 13, 18–22]. However, the number of studies on insect trends with sufficient replication and spatial coverage are limited [10, 23–25] and restricted to certain well-studied taxa. Declines of individual species or taxa (e.g. [7, 26]) may not reflect the general state of local entomofauna [27]. The total insect biomass would then be a better metric for the status of insects as a group and its contribution to ecosystem functioning, but very few studies have monitored insect biomass over an extensive period of time [28]. Hence, to what extent total insect biomass has declined, and the relative contribution of each proposed factor to the decline, remain unresolved yet highly relevant questions for ecosystem ecology and conservation. Here, we investigate total aerial insect biomass between 1989 and 2016 across 96 unique location-year combinations in Germany, representative of Western European low-altitude nature protection areas embedded in a human-dominated landscape (S1 Fig). In all years we sampled insects throughout the season (March through October), based on a standardized sampling scheme using Malaise traps. We investigated rate of decline in insect biomass, and examined how factors such as weather, habitat and land use variables influenced the declines. Knowledge on the state of insect biomass, and it’s direction over time, are of broad importance to ecology and conservation, but historical data on insect biomass have been lacking. Our study makes a first step into filling this gap, and provides information that is vital for the assessment of biodiversity conservation and ecosystem health in agricultural landscapes.

Discussion Our results document a dramatic decline in average airborne insect biomass of 76% (up to 82% in midsummer) in just 27 years for protected nature areas in Germany. This considerably exceeds the estimated decline of 58% in global abundance of wild vertebrates over a 42-year period to 2012 [56, 57]. Our results demonstrate that recently reported declines in several taxa such as butterflies [7, 25–27, 58], wild bees [8–14] and moths [15–18], are in parallel with a severe loss of total aerial insect biomass, suggesting that it is not only the vulnerable species, but the flying insect community as a whole, that has been decimated over the last few decades. The estimated decline is considerably more severe than the only comparable long term study on flying insect biomass elsewhere [28]. In that study, 12.2m high suction traps were deployed at four locations in the UK over the time period 1973–2002, and showed a biomass decline at one of the four sites only. However, the sampling designs differ considerably between the two studies. Suction traps mainly target high-flying insects, and in that study the catches were largely comprised of flies belonging to the Bibionidae family. Contrary, malaise traps as used in the present study target insects flying close to the ground surface (up to 1 meter), with a much wider diversity of taxa. Future investigations should look into how biomass is distributed among insect species, and how species trends contribute to the biomass decline. Although the present dataset spans a relatively large number of years (27) and sites (63), the number of repetitions (i.e. multiple years of seasonal distributions at the same locations) was lower (n = 26). We are however confident that our estimated rate of decline in total biomass resembles the true rate of decline, and is not an artifact of site selection. Firstly, our basic model (including an annual rate of decline) outperformed the null-model (without an annual rate of decline; ΔDIC = 822.62 units; Table 3), while at the same time, between-plot variation (i.s. σ site ) and residual variation (v) decreased by 44.3 and 9.7% respectively, after incorporating an annual rate of decline into the models. Secondly, using only data from sites at which malaise traps were operating in at least two years, we estimated a rate of decline similar to using the full dataset (Fig 4), with the pattern of decline being congruent across locations (S4 Fig). Taken together, there does not seem to be evidence that spatial variation (between sites) in this dataset forms a confounding factor to the estimated temporal trend, and conclude that our estimated biomass decline is representative for lowland protected areas in west Germany. In light of previously suggested driving mechanisms, our analysis renders two of the prime suspects, i.e. landscape [9, 18, 20] and climate change [15, 18, 21, 37], as unlikely explanatory factors for this major decline in aerial insect biomass in the investigated protected areas. Habitat change was evaluated in terms of changes in plant species composition surrounding the standardized trap locations, and in plant species characteristics (Ellenberg values). Land use changes was evaluated in terms of proportional surface changes in aerial photographs, and not for example changes in management regimes. Given the major decline in insect biomass of about 80%, much stronger relationships would have been expected if changes in habitat and land use were the driving forces, even with the somewhat crude parameters that were at our disposal. The decline in insect biomass, being evident throughout the growing season, and irrespective of habitat type or landscape configuration, suggests large-scale factors must be involved. While some temporal changes in climatic variables in our study area have taken place, these either were not of influence (e.g. wind speed), or changed in a manner that should have increased insect biomass (e.g temperature). However, we have not exhaustively analysed the full range of climatic variables that could potentially impact insect biomass. For example prolonged droughts, or lack of sunshine especially in low temperatures might have had an effect on insect biomass [59–62]. Agricultural intensification [17, 20] (e.g. pesticide usage, year-round tillage, increased use of fertilizers and frequency of agronomic measures) that we could not incorporate in our analyses, may form a plausible cause. The reserves in which the traps were placed are of limited size in this typical fragmented West-European landscape, and almost all locations (94%) are enclosed by agricultural fields. Part of the explanation could therefore be that the protected areas (serving as insect sources) are affected and drained by the agricultural fields in the broader surroundings (serving as sinks or even as ecological traps) [1, 63–65]. Increased agricultural intensification may have aggravated this reduction in insect abundance in the protected areas over the last few decades. Whatever the causal factors responsible for the decline, they have a far more devastating effect on total insect biomass than has been appreciated previously. The widespread insect biomass decline is alarming, ever more so as all traps were placed in protected areas that are meant to preserve ecosystem functions and biodiversity. While the gradual decline of rare insect species has been known for quite some time (e.g. specialized butterflies [9, 66]), our results illustrate an ongoing and rapid decline in total amount of airborne insects active in space and time. Agricultural intensification, including the disappearance of field margins and new crop protection methods has been associated with an overall decline of biodiversity in plants, insects, birds and other species in the current landscape [20, 27, 67]. The major and hitherto unrecognized loss of insect biomass that we report here for protected areas, adds a new dimension to this discussion, because it must have cascading effects across trophic levels and numerous other ecosystem effects. There is an urgent need to uncover the causes of this decline, its geographical extent, and to understand the ramifications of the decline for ecosystems and ecosystem services.

Acknowledgments CH and EJ were supported by the Netherlands Organization for Scientific Research (NWO grants 840.11.001 and 841.11.007), and NH by the Triodos Foundation. The investigations of the Entomological Society Krefeld and its members are spread over numerous individual projects at different locations and in different years. Grants and permits that have made this work possible are listed below: Bezirksregierungen Düsseldorf & Köln, BfN—Bundesamt für Naturschutz, Land Nordrhein-Westfalen—Europäische Gemeinschaft ELER, Landesamt für Agrarordnung Nordrhein-Westfalen, Landesamt für Natur, Umwelt und Verbraucherschutz Nordrhein-Westfalen, Landesamt für Umwelt Brandenburg, Landesamt für Umwelt Rheinland-Pfalz, LVR—Landschaftsverband Rheinland, Naturschutzbund Deutschland, Nordrhein-Westfalen Stiftung, RBN—Bergischer Naturschutzverein, RVR—Regionalverband Ruhr, SGD Nord Rheinland-Pfalz, Universitäten Bonn, Duisburg-Essen & Köln, Untere Landschaftsbehörden: Kreis Düren, Kreis Heinsberg, Kreis Kleve, Kreis Viersen, Kreis Wesel & AGLW, Stadt Düsseldorf, Stadt Köln, Stadt Krefeld, Rheinisch Bergischer Kreis, Rhein Kreis Neuss & Rhein-Sieg-Kreis. Members of the Entomological Society Krefeld and cooperating botanists and entomologists that were involved in the empirical investigations are greatly acknowledged: U.W. Abts, F. Bahr, A. Bäumler, D. & H. Beutler, P. Birnbrich, U. Bosch, J. Buchner, F. Cassese, K. Cölln, A.W. Ebmer, R. Eckelboom, B. Franzen, M. Grigo, J. Günneberg, J. Gusenleitner, K. Hamacher, F. Hartfeld, M. Hellenthal, J. Hembach, A. Hemmersbach, W. Hock, V. Huisman-Fiegen, J. Illmer, E. Jansen, U. Jäckel, F. Koch, M. Kreuels, P. Leideritz, I. Loksa, F. B. Ludescher, F. J. Mehring, G. Milbert, N. Mohr, P. Randazzo, K. Reissmann, S. Risch, B. Robert, J. de Rond, U. Sandmann, S. Scharf, P. Scherz, J. Schiffer, C. Schmidt, O. & W. Schmitz, B. P. & W. Schnell, J. L. Schönfeld, E. Schraetz, M. Schwarz, R. Seliger, H. W. Siebeneicher, F. & H. Sonnenburg W. J. S. & P. Sorg, A. Ssymank, H. Sticht, M. Weithmann, W. Wichard and H. Wolf.