Our results show rapid and far-reaching changes in the vascular flora of southernmost Sweden, both during the 1900s and during the most recent decades. A majority of all plant species have experienced a change in frequency since 1938, and this turnover of the species pool appears to have continued in recent decades. In previous analyses of data from the same surveys but using species-specific traits as proxies for environmental drivers, the main drivers of floristic changes during 1938–1996 were inferred to be eutrophication/nitrogen deposition and increasing drainage of the landscape (Tyler and Olsson 1997), while the main drivers of changes during 1987–2015 appeared to be climatic warming and decreasing management and disturbance from grazing and agricultural practices (Tyler et al. 2018). A recent study based on data from other provinces of Sweden also concluded that climatic changes have had a significant effect on changes in the flora during the last century (Auffret and Thomas 2019). The spread of recently introduced/immigrated species that may be considered invasive make up for a large proportion of the changes observed (and was also identified as a major factor in the analyses of Tyler et al. 2018); however, it is difficult to analyse to what extent their expansion is related to changes in the environment or caused by the simple fact that they have not been present and thus not able to spread before (Tyler et al. 2015, 2018).
The species showing the most dramatic declines during the most recent decades (Fig. 2 and Supplementary Material) are mostly a mixture of arable weeds of relatively less fertile soils (e.g. Anthemis arvensis, Galeopsis speciosa, Crepis tectorum, Lamium amplexicaule, Thlaspi arvense, Erysimum cheiranthoides, Raphanus raphanistrum) and species of mown or grazed seminatural grasslands (e.g. Nardus stricta, Carex pairae, Galium uliginosum, G. boreale, Briza media, Succisa pratensis, Botrychium lunaria, Dactylorhiza maculata subsp. maculata). This excludes forest species or other species that are not associated with the agricultural or urban landscape, stressing the importance of changes in land use for the changes observed (Bernes 2011–2012; Auffret and Thomas 2019).
Also many very common species in open/agricultural landscapes show significant declines, although to a smaller relatively degree (Supplementary Material). Species like Alopecurus geniculatus, Euphorbia helioscopia, Caltha palustris, Solidago virgaurea, Festuca ovina, Draba verna, Fallopia convolvulus and Achillea ptarmica were recorded in almost all grid-squares during 1987–2006, but have since declined by 10–16% and are now absent from parts of the province. In contrast, the vast majority of the most rapidly increasing species (Fig. 2 and Supplementary Material) represent escapes from cultivation that thrive under somewhat shaded conditions in hedges and forests, e.g. Scilla luciliae, Galanthus nivalis, Lysimachia nummularia and L. punctata, and woody species that are spreading from cultivated stands, e.g. Mahonia aquifolium, Taxus spp., Ligustrum vulgare, Prunus cerasifera, Cornus sericea, Spiraea spp., Amelanchier spp. and Cotoneaster spp. Among woody cultivated species, it is notable that it is mostly those with bird-dispersed red fleshy fruits that show very rapid increases (Tyler 2019). All these species are considered as invasive alien species in the region (Tyler et al. 2015), but their rapid increase in frequency may at the same time be indicative of changes in the environment and land use. The only species with a pre-1700 history in the province that have increased by more than 100% in recent decades are Filago vulgaris, growing on sandy–gravelly waste lands and rapidly expanding since its near-extinction in the late 1900s, and Echinochloa crus-gallii and Cardamine flexuosa, which are both weeds of gardens and other cultivated lands and based on their historic geographic ranges and phenology they may be assumed to be strongly favoured by longer and warmer summers and milder winters, respectively. However, some native species of forests and shrublands also show significant increases, e.g. Chelidonium majus, Alliaria petiolata, Campanula persicifolia and Allium ursinum. Furthermore, it should be pointed out that since the analysis is based on a fixed number of relatively large grid-squares, increases for already very common species may be difficult to detect.
The species showing large changes between 1938 and 1996 were thoroughly discussed already by Tyler and Olsson (1997). They concluded that ca. 50% of the biggest “losers” were species confined to tree-less fens, but several arable weeds and species confined to limnic habitats or managed heathlands were also in this group. In contrast, the biggest “winners” were found to be a mixture of species with widely different colonization histories and ecological demands, but with an overrepresentation of ruderals, garden weeds, recent immigrants, fertile hybrids, and species strongly favoured by high nitrogen availability or construction sites (Tyler and Olsson 1997).
Many of the species showing drastic changes in Scania during the 1900s have similar trends elsewhere in Sweden (e.g. Oredsson 1989; Maad et al. 2009; Sundberg 2014; Hedwall and Brunet 2016; Auffret and Thomas 2019) and other parts of Europe (Mennema et al. 1980–1989; Benkert et al. 1996; Rich and Woodruff 1996; Nielsen et al. 2019). However, most of the latter trends were observed in long-term studies over many decades. We know of no studies on a comparable geographic scale conducted over the very last decades with which the present results can be compared in terms of changes for individual species. Our results strongly advocate the need of performing broad-scale monitoring of floristic diversity over both short- and long-term time periods.
We found a strong connection between the changes in frequency for individual species 1938–1996 and 1987–2015. However, it was only the decreasing species that tended to have the same trend during the two periods; the species shown to have increased during the 1900s did, on average, not continue to increase after this period (Fig. 1). This may be interpreted either as a sign that the drivers that caused species to decline during the 1900s are still acting, a scenario only partly corroborated by the results of Tyler et al. (2018), or as the result of an extinction debt or a general delay in how regional floras adapt to new conditions (Eriksson et al. 2002; Bertrand et al. 2011). Since most plant species are relatively long-lived, either as mature individuals or in the seed bank, and may thus persist as slowly decreasing populations under suboptimal conditions, the latter explanation appears more plausible. In contrast, apart from the consistent tendency of newly immigrated species to expand, the ecological drivers that cause species to increase appear to be largely different today compared to the 1900s. In view of the results of Tyler et al. (2018), Hedwall and Brunet (2016) and Auffret and Thomas (2019), it may be concluded that climate warming is currently a major driver for increasing species in the region. Indeed, in Scania the last decade has been 0.9–1.6 °C warmer with 60–80 mm higher precipitation than the reference period in the mid-1900s (based on climate data from the Swedish Meteorological and Hydrological Institute). In particular, current winter temperatures tend to stay slightly above rather than below the freezing point for most of the season, a factor with potentially large consequences for plant growth and survival (e.g. Birgander et al. 2012). Several epiphytic bryophytes with oceanic distributions, presumably strongly favoured by mild and wet winters have also shown remarkable increases and range expansions in Scania during recent decades (Tyler 2018). From a conservation perspective, when only records from earlier and longer time periods are available, it may generally be assumed that species shown to decline during the 1900s are still at risk; by contrast, it should not be assumed that previously increasing species are still increasing.
However, the fact that the surveys here compared each encompassed two or more decades makes it somewhat difficult to associate the floristic changes observed with changes in the environment. Although we believe that such cases may at most be rare exceptions, we cannot rule out the possibility that some individual species may have experienced contrasting trends during the first and last years of the same survey period resulting in ambiguous conclusions when the accumulated survey results are compared. On the other hand, this may also be regarded as a strength of studies spanning long and partially overlapping time periods since erroneous conclusions based on short-term changes due to, e.g. the weather conditions of individual years or naturally cyclic changes in predator populations, can be avoided.
Trends for vegetation types
The vegetation types showing the largest average decreases of associated species (Figs. 4, 5) during the most recent decades are almost all tree-less, while the vegetation types performing the best are wooded or at least shaded by woody plants. With very few exceptions, different types of forests represent climax ecosystems of the region, and thus, all of the declining vegetation types are to some degree dependent on human activities and management. It is widely established that the study region has undergone significant increases in forest cover (Cousins et al. 2005; Hedwall and Brunet 2016; free data from the Swedish Forest Inventory) and in the abundance of trees in the open agricultural landscape (Fredh et al. 2012; Blomberg 2013), combined with decreases in agricultural activities and in the number of grazing animals (cf. Cui et al. 2014; free data from the Swedish Board of Agriculture), especially in the less fertile upland areas. Thus, it may not come as a surprise that overgrowth and cessation of traditional management constitute major drivers of changes in the Scanian flora, as also shown by the analyses of Tyler et al. (2018) and that species thriving in shaded conditions increase relative to species of open managed habitats. Most of the forests of the region are either monospecific plantations or intensively managed for production of timber and other biomass, which is a potential threat to many organisms in forests (The Swedish Species Information Centre 2015). Yet, modern forestry practices appear to be less problematic for the vascular ground flora in Scania. Similar conclusions were reached by Maad et al. (2009) based on analyses of floristic data from more northern areas in Sweden.
The continuing concentration of arable land and pastures to the most productive areas is also reflected in our results. Species of fens, bogs, low-productive grasslands, oligotrophic waters and base-poor wastelands all show larger average declines than those of more productive vegetation types (Figs. 4, 5). Furthermore, among the arable weeds, the steepest declines seem to characterize species preferring less-productive soils (e.g. Raphanus raphanistrum, Brassica rapa subsp. campestris, Erysimum cheiranthoides, Crepis tectorum, Anthemis arvensis). Approximately 20–35% of all species associated with low-productive treeless vegetation such as heaths and acidic and intermediate fens have declined over the very last decades. This should be particularly alarming as these formerly widespread vegetation types and their associated species are important for a wide range of other organisms, in particular insects that provide pollination services (Carvell et al. 2006). Only political actions improving the profitability and reducing regulations imposed on farmers managing less-productive lands, combined with raising consumer demands for their products, can halt this process. Education campaigns directed towards land owners may also be beneficial since some species and habitats of protective value, but of little economic value, are today lost simply owing to the ignorance of the land owners.
The dramatic decrease documented for species in oligotrophic waters throughout northern Europe (Sand-Jensen et al. 2018) is most probably caused by the ongoing humification of previously clear acidic waters that has been observed throughout northern Europe (Kritzberg and Ekström 2012; Garmo et al. 2014). Submerged plants in humified waters rapidly disappear when light penetration of the water column decreases and the mineral sediments on the bottoms become buried under organic matter (Arts 2002). Since the underlying drivers of humification are still under debate (e.g. Kalbitz et al. 2017), it is difficult to propose counteractive measures, but increased disturbance from e.g. cattle grazing (Sand-Jensen et al. 2018) and reduced tree-cover along shorelines would most probably promote many of the plant species concerned. In contrast, plants of eutrophic waters show only a modest decrease during recent decades, numerically comparable to their increase observed during the 1900s (Fig. 4).
When comparing the relative rank of the changes estimated for different vegetation types between the two time periods considered (Figs. 4, 5), both similarities and dissimilarities become apparent. In this context, it has to be kept in mind that the grid-squares available for the first time period are not randomly distributed geographically; however, all inland vegetation types were reasonably well represented. All vegetation types that showed increases during the very last decades also increased in the 1900s, but it is clear that species of wooded or forested vegetation types have performed relatively better in recent years while species of open vegetations strongly influenced by human activities (e.g. waste lands and ruderal vegetation) show only minimal increases over the same time interval. Similarly, although the decreasing vegetation types remain largely the same, their internal rank order is much altered. It is, for example, notable that species of sand-steppes and steppe-like meadows, as well as rich fens, i.e. those vegetation types that have attained most attention and enjoyed most active measures from regional conservationists during recent decades (e.g. Bager and Persson 2009; Rosquist 2017), although still declining, appear to perform relatively better now than during the 1900s, while species of vegetation types that have received less attention, e.g. arable land, poor fens, oligotrophic waters, heaths and low-productive meadows now comprise the most rapidly declining ones. There may be other explanations for this pattern, but it is tempting to conclude from our results that conservation measures actually do have positive effects also on broad-scale biodiversity.
The different approaches to calculate changes at the level of vegetation types attempted here may be expected to give somewhat different results. The mean over species change (Fig. 4) gives equal weight to all species, thus in effect up-weighting rare ones, while the “weighted approach” (Fig. 5) weights the changes proportionally to the frequency of the species. While it may be argued that rare species contribute only little to broad-scale biodiversity, up-weighting common ones may be problematic since these tend to be habitat generalists present in multiple vegetation types and thus not necessarily valid indicators for particular vegetation types. In particular, frequent species common to both widespread and rare vegetation types may provide false estimates of the trends of the latter. Furthermore, the weighted approach gives the same weight to all grid-squares, possibly introducing errors for those vegetation types that are geographically restricted to parts of the province while on the other hand being more relevant for changes at the scale of the province as a whole. However, for most vegetation types the two approaches suggest largely the same trends (compare Figs. 4, 5) and the same biggest winners and loosers. As expected, it is the geographically most restricted and species-poor vegetation types (boreal conifer forest, raised bog, sand-steppe and sandy sea-shores) that show the largest relative differences between the unweighted and the weighted estimates.
It must also be stressed that neither approach is able to differentiate between changes caused by changes in the areas covered by vegetation types and those caused by changes in the species richness of the vegetation types per area unit. In theory, a decrease in the area covered by a particular vegetation type can be compensated for by an increase in species richness at remaining sites. Still, we believe that mean changes and proportions of decreasing vs increasing species may be highly informative for giving priority to and choosing between conservation efforts.
Consequences for general plant biodiversity
While the proportion of rapidly declining vegetation types may be alarming, it must be stressed that several of the most species-rich vegetation types have performed well over the past decades, decreasing general losses of plant biodiversity at the landscape scale. In a recent study from Denmark overall plant species richness was found to have increased over the last centuries at the same time as the geographic diversity/differentiation of the species pool had decreased (Nielsen et al. 2019) and similar trends are suggested by a study with data from further north in Sweden (Auffret and Thomas 2019). Hedges, shrublands, wood margins, groves, waste lands, yards, gravel-pits, road verges and ruderal vegetation may not obtain the highest interest from conservationists, but together house more than one third of all species in Scania and all these vegetation types have either increased or remained stable in frequency. Thus, loss of vegetation types does not necessarily imply a reduction in total species diversity. Still, based on our data from the most recent decades (surveys 2 and 3), the number of decreasing species far outnumbers the number of increasing species. There may of course be differences in the completeness of all surveys, but the volunteers that participated in the field works of the two most recent surveys all got the same instructions, many of them participated during both surveys and the identity of critical species were checked by experts (cf. Tyler et al. 2018). In contrast, the comparison between the two first surveys conducted during the 1900s is inconclusive in this respect as only relative changes could be estimated. Still, a general reduction of species richness at the scale of the 2.5 × 2.5 km grid-squares appear highly probable given the general intensification, up-scaling and regional homogenisation of the land use seen during the last century (Bernes 2011–2012; Nielsen et al. 2019) and the results of local studies within the region (Oredsson 1989).