Conservation management has been an effective tool to counteract diversity loss at local scales (Bobbink and Willems 1993; Hobbs and Norton 1996; Pykälä 2003; Pöyry et al. 2004), but its effects on regional biodiversity remain little studied (but see Doxa et al. 2012). Using a unique dataset of species presence/absence data before and after 17 years of conservation management for a wide range of taxonomic groups, we evaluated the effects of conservation actions on both local and regional diversity patterns. Shifts in local and regional biodiversity were highly correlated, indicating that there was no discrepancy between local and regional conservation success. However, diversity shifts differed markedly between taxonomic groups, with some taxa decreasing in local and regional diversity, while others became more diverse over time.
Local diversity shifts
Over 17 years of conservation management, local species richness changed significantly for half of the eight investigated taxonomic groups, with increased richness and decreased richness each occurring in two taxonomic groups. Conservation management in Dutch calcareous grasslands has thus not resulted in the anticipated increase in local species richness across taxonomic groups. A lack of response to conservation measures is often attributed to slow recovery of plant and arthropod communities (Huxel and Hastings 1999; Woodcock et al. 2012). However, considering the long time-span of our study (17 years), we would expect to have picked up even relatively slow responses. The lack of recovery may, in part, reflect a lack of source populations in the landscape. Our sampling sites comprised all calcareous grassland sites of reasonable quality and more than 1 ha. in size within the landscape. Species not present in any of these sites may have been completely absent from the landscape and therefore unable to recolonize restored locations. The large variation in species composition between sites, however, indicates that this is not the only explanation. In the absence of control sites that did not receive conservation management, we cannot automatically attribute observed shifts in diversity patterns (or the lack thereof) to the implemented conservation management. Other factors that have affected the study sites simultaneously, e.g. ongoing agricultural intensification in the wider landscape, may have equally contributed to observed patterns, or may have cancelled out positive effects of conservation management. Given the generally negative trend of (specialist) species in northwestern European agricultural landscapes (Green et al. 2005; Kleijn et al. 2009; Potts et al. 2010) and the considerable impact of the implemented conservation management on vegetation structure and microclimate (Willems 2001; van Noordwijk et al. 2012a, b) it is likely that local species richness would have declined in the absence of conservation management. The fact that local species richness remained stable or increased for six out of eight taxonomic groups, could therefore be seen as (moderate) conservation success. For the two remaining groups, carabid beetles and weevils, the implemented conservation management has not prevented local diversity loss. The management may even have directly contributed to their decline, for example by causing increased mortality, food shortages or unfavourable microclimatic conditions (van Klink et al. 2015).
Regional diversity and compositional variation
Local diversity shifts were strongly correlated to regional diversity shifts and were generally paralleled by shifts in compositional variation. We found increased community differentiation in millipedes, which increased in local species richness, while carabid beetles, which decreased in local species richness, became increasingly homogenized. This implies that observed changes in compositional variation were caused predominantly by changes in local species richness, rather than replacement of species (Baeten et al. 2014). We found no evidence for increased biotic homogenization resulting from a limited set of species profiting from the creation of similar environmental conditions across sites. This is an encouraging result for site managers as it shows that there is not necessarily a conflict of interest between local and regional conservation goals. Introducing similar conservation management across sites thus does not necessarily compromise regional biodiversity conservation by leading to sites becoming more similar in species composition.
Differences between taxonomic groups
In our study, we observed both increases and decreases in local and regional biodiversity over 17 years of conservation management, depending on the taxonomic group under study. Relatively few studies have simultaneously investigated biotic homogenization patterns (Devin et al. 2005; Shaw et al. 2010) or the effects of conservation management (Kruess and Tscharntke 2002; Oertli et al. 2005) on more than one taxonomic group. Studies that do have a wide taxonomic scope, generally report differential responses between taxonomic groups (Kruess and Tscharntke 2002; Devin et al. 2005; Oertli et al. 2005; Shaw et al. 2010), in line with our results. The reason for this variation in response between taxonomic groups is that species’ distributions are affected by many different factors, including habitat fragmentation, regional land use, (micro)climatic conditions, biomass production and vegetation structure (Morris 2000; Sala 2000). The relative importance of each of these factors differs among taxonomic groups (Dormann et al. 2007). In addition, taxa also differ in their response to conservation management itself (van Klink et al. 2015). The eight taxonomic groups we investigated differ in many respects, including dispersal ability, trophic position, body plan and development pathway, which all play a role in determining species’ responses to their environment (Verberk et al. 2008, 2013). We have not formally tested which factors explain the differences in diversity shifts between taxonomic groups, because there are more potential factors than the number of taxonomic groups in our study, which leaves insufficient statistical power for formal testing. However, in our highly fragmented study system, dispersal ability is likely to play a role. Fragmentation has repeatedly been demonstrated to hamper restoration of plant communities (Ozinga et al. 2005; Smits 2010), poorly dispersing beetles (Woodcock et al. 2010b) and ants (van Noordwijk et al. 2012a). This potentially explains why these groups did not increase in local and regional diversity in our study. True bugs, which showed the largest increase in richness over the study period, are generally better dispersers and have been shown previously to respond strongly to site conditions and not landscape factors (Kőrösi et al. 2012). Interestingly, the well-developed dispersal ability of many true bug species did not lead to increased biotic homogenization. In fact, no single true bug species was present in all study sites. This implies that either habitat characteristics differed between restored sites (causing species sorting), or that distances between sites were too large to ensure colonization of all sites, even for relatively good dispersers.
Contrary to our expectations, differences in trophic position did not seem to play a direct role in determining the response of taxonomic groups. Predominantly predatory groups showed negative (carabid beetle) and neutral (spiders and ants) changes in local biodiversity, while first order consumers responded positively (true bugs) and negatively (weevils). Interestingly, within both first order consumers and predators, the strongest decrease in diversity was found for holometabolous taxonomic groups (carabid beetles and weevils), while hemimetabolous groups responded more positively (true bugs and spiders). Holometabolous species generally have a more strongly synchronised life-cycle and their immature stages are less mobile and need different environmental conditions than the adult stages. This makes holometabolous species particularly sensitive to management timing, intensity and scale (van Noordwijk et al. 2012b; van Klink et al. 2015), indicating that too intensive management may have hampered restoration of carabid beetle and weevil communities.
It should be noted here that our study design, with only two sampling periods, makes it impossible to conclude unequivocally whether observed diversity changes represent ongoing shifts or mere year to year fluctuations. For example, carabid beetles are known to exhibit considerable annual population fluctuations (Baars and Van Dijk 1984; den Boer 1985, 1990; Brooks et al. 2012), presenting an alternative explanation for their observed decline in local and regional diversity. However, even if the observed diversity decline for carabid beetles is caused by annual population fluctuations rather than a decreasing trend, there is still reason for concern. The small size of individual sites (<5 ha.) and the large distance between sites, make species with large population fluctuations especially prone to local extinction (Henle et al. 2004; van Noordwijk et al. 2015).
In addition to the variation in responses between taxonomic groups, species within each group also differ in life-history, and hence in vulnerability to all the different factors affecting biodiversity (Stearns 1976; Southwood 1977). This causes a multitude of responses within each group, which are likely to cancel each other out and obscure overall patterns. Analyzing species’ traits may help to disentangle such contrasting effects and our species-level analysis provides a unique opportunity to investigate consistent trait patterns. Conservation management is primarily aimed at improving conditions for characteristic species. A greater increase in characteristic calcareous grassland species, compared to habitat generalists, was indeed found for spiders. The fact that the replacement of non-characteristic spiders by characteristic species did not result in overall changes in compositional variation among sites, means that replacement was independent of the initial occurrence. Indeed, if both rare and prevalent characteristic species increase over time, there is no net-effect on the compositional variation. For weevils we found an effect of food type specialization with food specialists like Sibinia pyrrhodactyla, Strophosoma fulvicorne, Trachyphloeus alternans, Trichosirocalus troglodytes and Tychius squamulatus increasing more in occupancy than food generalists. This implies that conditions generally improved for these food specialists, which all feed on forbs that are well adapted to dry, nutrient poor conditions (Spergula arvensis, Calluna vulgaris, Helianthemum nummularium, Plantago lanceolata and Lotus corniculatus). The lack of increase in habitat- and food specialists in other groups (spiders, true bugs and carabid beetles) indicates that either conditions for specialists did not improve (at least not more so than for habitat generalists) or that specialists did not reach improved sites because of dispersal barriers. Our trait analysis revealed some evidence, albeit weak, for the existence of such dispersal barriers. The significant interaction between habitat affinity and dispersal ability for changes in compositional variation among spiders (see Fig. 4a) is caused by the fact that poorly dispersing habitat specialists occur in fewer sites than good dispersers and habitat generalists. This indicates that habitat fragmentation limits the dispersal of these spider species. For vascular plants, we found a trend towards interaction between habitat affinity and dispersal ability with respect to changes in occupancy: characteristic species tended to increase more if they had long-distance dispersal mechanisms, although this effect was not significant (p = 0.06). For woodlice we found a strong correlation between occurrence change and body size, which was used as a proxy for dispersal ability. Large bodied species (>10 mm), like Armadillidium vulgare, Porcellio dilatatus, Porcellio scaber and Trachelipus rathkii increased in occurrence, while small-bodied species such as Platyarthrus hoffmannseggi and Trichoniscus pusillus declined. This could indicate that species recovery was limited by habitat isolation and fragmentation. However, no hard conclusions can be drawn from this relationship, as body size is equally related to other responses, including drought or heat resistance (Calder 1984; Peters 1986). Small species tend to be more vulnerable to drought (Kaspari 1993; Kærsgaard et al. 2004; Dias et al. 2012) and heat (Peters 1986) than larger species, presenting an alternative explanation for the observed relationship. The lack of a coherent effect of dispersal ability across taxonomic groups may be caused by the fact that the absolute dispersal ability of ‘good’ and ‘poor’ dispersers varies considerably between groups. True bugs classified as ‘good dispersers’ (i.e. species capable of active flight) are likely to reach much longer distances in a single generation than ‘good dispersing’ plants, which was defined as those with a long distance dispersal strategy. Moreover, trait variation within some taxonomic groups may be too small to have an effect.
Overall, the explanatory power of single traits in our study was generally low. This is likely to be partly due to the crude trait categories we adopted, due to a lack of more accurate autecological data for some of the studied taxonomic groups. However, there is also a more fundamental reason for the lack of trait-environment responses. The adaptive value of a specific trait is contingent upon a species’ body-plan and its other traits (Verberk et al. 2013). This means that the vulnerability of a species to a specific environmental factor depends on the effect of all its traits combined. More elaborate analyses, incorporating a wide range of traits and explicit trait interactions, e.g. through the use of life-history strategies, are likely to generate better insight (van Noordwijk et al. 2012a; Verberk et al. 2013; van Noordwijk 2014).
Conclusions and implications
In all, our results indicate that 17 years of conservation management in Dutch calcareous grasslands has not led to the anticipated overall increase in local species richness across all taxonomic groups. However, considering the ongoing biodiversity decline in agricultural landscapes, our results do indicate moderate conservation success (lack of decline among plants, ants, spiders and woodlice, increased richness of millipedes and true bugs and increases in characteristic spiders and weevil food specialists). Local biodiversity conservation seems to have been limited in particular by species’ inability to recolonize suitable habitat in this highly fragmented landscape. In addition, the management regime seems to have been insufficient to create favorable habitat conditions for some characteristic species, particularly carabid beetles and weevils. Intensive autumn management in Dutch calcareous grasslands may cause particular obstacles for their larval stages, as was previously demonstrated for ants (van Noordwijk et al. 2012a) and butterflies (van Noordwijk et al. 2012b).
An encouraging result of our study is that local diversity shifts were generally paralleled by shifts in regional diversity and compositional variation in the same direction. Implementation of relatively uniform conservation management at the regional scale, consisting of intensive autumn grazing and/or mowing, did not lead to a uniform change in species composition. This suggests that the management succeeded in maintaining or even enhancing the unique character of each site, attracting different species to different sites. Although this is certainly a positive result, it may in fact partially reflect the high level of fragmentation of the study landscape. If species are only able to recolonize restored sites over short distances, then regional introduction of uniform conservation management is indeed unlikely to lead to biotic homogenization. In addition, the spider data in our study demonstrate that successful management (in terms of increased occurrence of characteristic species) does not always lead to increased compositional variation among sites. Theoretically, successful conservation management can even contribute to biotic homogenization in a positive way, e.g. if it causes characteristic species to be present in all study sites (recall Fig. 1). Therefore, biotic homogenization should not by definition be considered as a process that needs to be avoided and countered. Instead, providing a range of environmental conditions to suit different species is paramount for safeguarding regional biodiversity, irrespective of whether these conditions are present in the same or in separate sites.
In line with earlier studies (Kruess and Tscharntke 2002; Devin et al. 2005; Oertli et al. 2005; Shaw et al. 2010), our results demonstrate that diversity shifts differ markedly among taxonomic groups. This demonstrates the need to adopt a wide taxonomic scope when evaluating strategies to tackle diversity loss and the need to understand underlying mechanisms. Although the explanatory power of our single trait analyses was generally low, it did shed some light on the mechanisms underlying observed diversity shifts, particularly highlighting dispersal constraints. In addition, we found that holometabolous taxonomic groups declined more than hemimetabolous arthropods. This intriguing observation warrants further investigation.