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Narrow Environmental Niches Predict Land-Use Responses And Wehner et al. BMC Ecol Evo (2021) 21:15 BMC Ecology and Evolution https://doi.org/10.1186/s12862-020-01741-1 RESEARCH ARTICLE Open Access Narrow environmental niches predict land-use responses and vulnerability of land snail assemblages Katja Wehner1* , Carsten Renker2, Nadja K. Simons1, Wolfgang W. Weisser3 and Nico Blüthgen1 Abstract Background: How land use shapes biodiversity and functional trait composition of animal communities is an impor- tant question and frequently addressed. Land-use intensifcation is associated with changes in abiotic and biotic con- ditions including environmental homogenization and may act as an environmental flter to shape the composition of species communities. Here, we investigated the responses of land snail assemblages to land-use intensity and abiotic soil conditions (pH, soil moisture), and analyzed their trait composition (shell size, number of ofspring, light prefer- ence, humidity preference, inundation tolerance, and drought resistance). We characterized the species’ responses to land use to identify ‘winners’ (species that were more common on sites with high land-use intensity than expected) or ‘losers’ of land-use intensity (more common on plots with low land-use intensity) and their niche breadth. As a proxy for the environmental ‘niche breadth’ of each snail species, based on the conditions of the sites in which it occurred, we defned a 5-dimensional niche hypervolume. We then tested whether land-use responses and niches contribute to the species’ potential vulnerability suggested by the Red List status. Results: Our results confrmed that the trait composition of snail communities was signifcantly altered by land-use intensity and abiotic conditions in both forests and grasslands. While only 4% of the species that occurred in forests were signifcant losers of intensive forest management, the proportion of losers in grasslands was much higher (21%). However, the species’ response to land-use intensity and soil conditions was largely independent of specifc traits and the species’ Red List status (vulnerability). Instead, vulnerability was only mirrored in the species’ rarity and its niche hypervolume: threatened species were characterized by low occurrence in forests and low occurrence and abun- dance in grasslands and by a narrow niche quantifed by land-use components and abiotic factors. Conclusion: Land use and environmental responses of land snails were poorly predicted by specifc traits or the spe- cies’ vulnerability, suggesting that it is important to consider complementary risks and multiple niche dimensions. Keywords: Gastropoda, Land snails, Land-use intensity, Biodiversity Exploratories, Forests, Grasslands Background Reduction of habitat and microhabitat heterogeneity Land use disturbs natural environments, changes may lead to a homogenization of plant and animal com- local geographical landscape structure and alters local munities, trigger a reduction in functional diversity and biotic and abiotic conditions, e.g. microclimate [1–6]. thus lower the capacity of an ecosystem to bufer distur- bances [7, 8]. Homogenization of animal communities by increasing land-use intensity has been shown for several *Correspondence: [email protected] taxa; e.g., in managed grasslands, 34% of plant- and leaf- 1 Ecological Networks, Technische Universität Darmstadt, hoppers species were signifcant losers (i.e. species that Schnittspahnstraße 3, 64287 Darmstadt, Germany Full list of author information is available at the end of the article were signifcantly less abundant under conditions of high © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wehner et al. BMC Ecol Evo (2021) 21:15 Page 2 of 23 (See fgure on next page.) Fig. 1 Trait distribution (a shell size, b number of ofspring, c light preference, d humidity preference, e drought resistance, f inundation tolerance) of snail communities among forest (grey) and grassland (white) habitats in the Swabian Alb, the Hainich-Dün and the Schorfheide-Chorin. Traits are given as community weighted mean (CWM). Diference among habitats per region are tested using an ANOVA (asterisks), diferences between regions are tested by a posthoc Tukey test (letters). Signifcances: ns not signifcant, *p < 0.05, **p < 0.01, ***p < 0.001 land-use intensity) of land-use intensifcation, particu- In the present study, we investigated land snail com- larly increases in mowing frequency had a negative efect munities at forest and grassland sites in diferent regions [9]. of Germany, which were characterized by diferent land- Land snails are an important macroinvertebrate group use types and intensities. We aimed to test whether the that is directly and indirectly involved in ecosystem pro- trait composition of the snail community is infuenced by cesses such as litter decomposition or nutrient cycling land-use intensity (and soil conditions). We then tested [10, 11]. Tere is a natural north–south and west–east the responses of each snail species to land-use intensity; gradient of snail species distributions and abundances ‘winners’ signifcantly increase in abundance and occur- within Europe; species richness increases from north to rence with land-use intensity, whereas ‘losers’ signif- south and to a lesser extent from west to east which is cantly decrease compared to the null model [9, 39]. We linked to regional and ecological diferences and the land- than compared these responses with the snail species’ use history [12]. Snail species also difer in their tolerance habitat association; i.e. we asked whether species that to abiotic factors (pH, soil moisture), and vary greatly in only occasionally occur in forests are more afected by life-history parameters (e.g., lifespan, development, num- forest management than species that are specialized to ber of ofspring, food requirement, shell size) and general forest habitats. On the other hand, do species that are behavior [13] which also afect their distribution. Varia- grassland specialist sufer less from grassland manage- tion in body size and diet seems to be especially impor- ment than those only occasionally occurring in grass- tant for structuring snail communities [14] as well as the lands? Finally, we compared our fndings of the land-use species-specifc tolerance to a variety of environmental efects and the ‘winner/loser’ status of a species with its factors which can result in nested communities at a spe- putative vulnerability (Red List status), to test if losers cifc site [15, 16]. of land-use intensifcations in forests and grasslands are Studies on trait composition of snail communities in those species that are classifed as vulnerable. Sweden pointed to the importance of the species’ niche- width and the importance of local environmental condi- Results tions over spatial variables [17]. While tolerance-related Response to land use traits such as humidity preference or inundation toler- Te trait composition of land snail communities dif- ance were positively associated with abiotic soil moisture, fered strongly between forests and grasslands within a large amount of variation remained unexplained [17], regions, indicated by a strong diferentiation of commu- which may be related to land use. Te impact of land nity-weighted mean trait values (CWMs). Assemblages use and its intensity on land snail communities is less of forest species consisted of larger species, consistently intensively investigated although most land snail species showed lower light and higher humidity preference, are characterized by a limited mobility and therefore are lower drought resistance and mostly lower inundation vulnerable to human introduced habitat changes [15, 18– tolerance than grassland assemblages; diferences in the 20]. Changes in abiotic factors such as soil pH, soil mois- number of ofspring were inconsistent among forest and ture, soil calcium content, leaf litter depth, soil surface grassland habitats (Fig. 1). structure or the type of vegetation have been shown to In forests, land-use intensity and abiotic conditions sig- alter snail communities [15, 21–25]. Also land-use factors nifcantly infuenced the CWMs of all traits investigated, such as the proportion of wood harvested in forests or the although often in a diferent way across regions (Table 1, amount of grazing livestock in grasslands can infuence Additional fle 1: Appendix 1; see interaction terms with snail communities directly and/or indirectly [20, 26, 27]. region). Similarly, in grasslands the trait composition of In addition, disturbances
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