Mitigating the Precipitous Decline of Terrestrial European Insects: Requirements for a New Strategy
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Biodiversity and Conservation (2019) 28:1343–1360 https://doi.org/10.1007/s10531-019-01741-8 REVIEW PAPER Mitigating the precipitous decline of terrestrial European insects: Requirements for a new strategy Jan Christian Habel1,2 · Michael J. Samways3 · Thomas Schmitt4,5 Received: 27 December 2018 / Revised: 8 March 2019 / Accepted: 11 March 2019 / Published online: 22 March 2019 © Springer Nature B.V. 2019 Abstract Severe decline in terrestrial insect species richness, abundance, fying biomass, and local extinctions across Europe are cause for alarm. Here, we summarize this decline, and iden- tify species afected most. We then focus on the species that might respond best to mitiga- tion measures relative to their traits. We review apparent drivers of decline, and critically refect on strengths and weaknesses of existing studies, while emphasising their general signifcance. Generality of recent scientifc fndings on insect decline have shortcomings, as results have been based on irregular time series of insect inventories, and have been car- ried out on restricted species sets, or have been undertaken only in a particular geographi- cal area. Agricultural intensifcation is the main driver of recent terrestrial insect decline, through habitat loss, reduced functional connectivity, overly intense management, nitrogen infux, and use of other fertilisers, as well as application of harmful pesticides. However, there are also supplementary and adversely synergistic factors especially climate change, increasingly intense urbanisation, and associated increase in trafc volume, artifcial light- ing and environmental pollution. Despite these various synergistic impacts, there are miti- gating factors that can be implemented to stem the precipitous insect decline. Science can provide the fundamental information on potential synergistic and antagonistic mechanisms of multiple drivers of insect decline, while implementation research can help develop alter- native approaches to agriculture and forestry to mitigate impacts on insects. We argue for more nature-friendly land-use practices to re-establish Europe’s insect diversity. Keywords Biodiversity crisis · Insect decline · Species richness · Abundance · Agricultural intensifcation · Habitat fragmentation · Habitat degradation · Pesticides · Climate change · Insect conservation Communicated by P. Ponel. * Jan Christian Habel [email protected] Extended author information available on the last page of the article Vol.:(0123456789)1 3 1344 Biodiversity and Conservation (2019) 28:1343–1360 Introduction Europe’s insect diversity was recorded as declining in the 19th century, when it was described as ‘heartlessly being swept away in this era of steam and telegraphy’ (Swin- ton 1880). Since then, the situation has worsened, with accelerating velocity of losses across Europe since the 1950s. This decline has been documented for various, mainly charismatic insect groups, such as lepidopterans (Maes et al. 2001; Conrad et al. 2004; Thomas et al. 2004; Thomas 2005; Fox 2013) and carabid beetles (Brooks et al. 2012). However, these well-studied groups are not unique, but refect a general decline in insects (Sánchez-Bayo and Wyckhuys, 2019; Samways 2019). Overall, Europe has seen a signifcant and on-going loss of general insect species richness (Thomas et al. 2004; Conrad et al. 2006; Müller et al. 2012; Habel et al. 2016; Simons et al. 2017). For example, the European Red List of Butterfies indicates a decline in these insects at the continental scale (Van Swaay et al. 2010). Similar trends have occurred at regional and local scales. Macro- and micro-lepidopterans of the fed- eral state of Bavaria in southern Germany have experienced losses of >13% since the year 2000 (Haslberger and Segerer 2016), and in south-western Germany, Luxembourg, and north-eastern France, butterfies and carabid beetles associated with calcareous grassland patches have declined precipitously in the last 50 years (Augenstein et al. 2012; Filz et al. 2013; Habel et al. 2016). In addition to decline in species richness, there have also been temporal shifts in species composition, as for example among but- terfies (Filz et al. 2013; Habel et al. 2016), wild bees (Potts et al. 2010), and carabid beetles (Augenstein et al. 2012). These species losses and assemblage shifts are often associated with declines in abundance of specifc taxa, and decreases in total biomass. Hallmann et al. (2017) showed a biomass reduction of 75% in fying insects at various sites in Germany over three decades, while similar negative trends have been recorded for other parts of Europe (Conrad et al. 2004; Shortall et al. 2009; Knowler et al. 2016; Storkey et al. 2016). Although these studies have temporal and spatial restrictions, they have the same conclusions: (1) reduction of insect species richness, (2) shift in species assemblages, with reduced species evenness, and (3) decline in many species’ abun- dance, i.e. losses of biomass. These conclusions lead to three general questions, which we explore in the following: 1. Which taxon traits are sufering the most, and which are not afected, or alternatively, beneft from the continuing environmental changes? 2. What are the main drivers leading to these negative trends? 3. How can science, policy, and management mitigate further insect decline, or preferably, reverse this negative trend? We focus here specifcally on above-ground terrestrial insects, rather than aquatic insects, which face diferent (e.g. alien fsh predation, channelization, damming of riv- ers, functionally signifcant reduced leaf litter), but sometimes overlapping (e.g. pesti- cide impact, increased nitrogen and fertilizer input, fragmentation of habitats) threats and stressors. In turn, soil insects are subject to some diferent (e.g. loss of leaf lit- ter, soil erosion, changes in soil fungi composition) and some similar (e.g. changing microhabitats, landscape fragmentation, impact of invasive alien vegetation) impacts. All three realms, terrestrial, freshwater and soil, are afected by the pervasive efect of climate change, directly, or indirectly through changes in interaction networks. 1 3 Biodiversity and Conservation (2019) 28:1343–1360 1345 Trait analyses to discriminate losers from winners Application of morphological, life-history, and physiological traits is useful for ana- lysing changes in patterns and abundance of biodiversity (Cleary et al. 2007; Mayfeld et al. 2010; Gossner and Müller 2011; Gossner et al. 2013; Thorn et al. 2015; Simons et al. 2016, 2017), and decreases in evenness, and hence homogenisation, of insect assemblages (Gossner et al. 2016). Thus, identifying response traits (e.g. life-history and feeding-related traits) to environmental changes may help to explain why certain species become less (or more) abundant over time. An underlying assumption is that the drivers act as flters allowing certain species to survive or remain in high abundance, and others not. Furthermore, trait analyses are informative for understanding commu- nity assembly rules (Mouchet et al. 2010; Vandewalle et al. 2010). For example, when analysing the characteristics of communities in response to land-use intensity, average insect body size decreases, and fight ability increases, with higher land-use intensity in grasslands (Simons et al. 2016). Consequently, more rapidly developing and mobile taxa are less afected than others. Furthermore, an increase in mobile species, and a decrease in sedentary species, indicates a response to increasing habitat isolation through higher mobility safeguarding species survival in a fragmented landscape (Thomas 2016). Spe- cies relying on specifc microhabitat structures and/or resources can sufer greatly from their reduction or loss. Consequently, deterioration of habitat quality can be as rele- vant as decreasing habitat size and increasing habitat isolation (Dennis and Eales 1997; Thomas et al. 2001). This means that a mechanistic understanding of how land-use changes afect arthropod assemblages can be achieved by trait-based analyses of com- munity shifts (Birkhofer et al. 2015). As species equipped with specialised traits are the ones sufering the most, it is essential to identify the specifc drivers causing disappear- ance of specifc taxa, as well as shifts in species composition. Highest rate of regional extinction in Danish butterfies has been among sedentary habitat specialists overwin- tering as eggs, while the most severe local-scale declines have occurred among seden- tary host plant specialists overwintering as larvae. In contrast, mobile generalists with a mature overwintering larval stage, have been least afected (Eskildsen et al. 2015). Trait-based analyses identify the following four drivers, which have diverging efects on diferent taxa, depending on their respective ecological requirements (Fig. 1). Habitat loss Habitat losses, e.g. of semi-natural habitats like grasslands, hedgerows, small set-aside areas, which were once integral components of traditional low-intensity agriculture, are greatly reducing regional species diversity (Reidsma et al. 2006). Loss of these habitats has severely afected extreme specialists, whose combination of traits does not allow any shift to alternative habitats. An example is the great loss of monophagous species through having lost their specialized bog habitats (Ebert and Rennwald 1991; Gelbrecht et al. 2016). The severe decline, and even regional extinction, of the highly specialised Maculinea butterfies, with their extraordinarily complex