Understory plant communities represent the majority of plant diversity in temperate forest ecosystem and play a central role in a number of ecosystem services and processes, such as tree regeneration, nutrient cycling, and pollination (Landuyt et al. 2019). In addition, many of these plants have a large indicator potential and may serve as an early warning system for global-change impacts on forests in temperate and boreal biomes (Hedwall et al., 2021). Therefore, research on understory community responses to different drivers of vegetation change (e.g., stand structure dynamics, macroclimate warming, herbivory, and nitrogen deposition) are currently representing one of the major research topics in vegetation science. Long-term research sites in different types of natural and semi-natural environments enable answering on both theoretical and applied ecological questions in relation to different global-change scenarios (de Bello et al. 2020).
By testing a priori hypotheses concerning the direction of forest vegetation change, this study aimed at detecting the signal of climate change, nitrogen deposition, forest disturbances and deer browsing in ground vegetation (GV) of different forest types across Slovenia in the period from 2004/05 to 2019/2020. Rather than observing a strong signal of environmental drivers, we found high variability in magnitude and direction of GV changes at different sites. Site-specific factors (e.g., soil type, stand structure, tree composition) may cause differential temporal response in GV under comparable external pressure (Verstraeten et al. 2013). Temporal trends in ecological indicator values (EIVs) were highly site-specific. However, taking the whole spectrum of IM sites in Slovenia, temporal trends in GV were not completely random. This resulted in an interesting pattern of “ecological contraction”, which can be described as decrease in range of EIVs and tendency towards intermediate conditions when first survey and resurvey periods were compared. This process was induced by divergent response of GV at different sites: colder sites became warmer and warmer sites became colder; sites with acidic and nutrient-poor soils experienced increase in EIV for soil reaction and soil nutrients whereas more basophilic and nutrient-rich sites tend to change in the opposite direction (i.e., decrease in EIV-R and EIV-N). This kind of opposing changes resulted in range shrinkage of ecological gradients across the entire spectrum of studied forest types. Hülber et al. (2008) have reported a homogenization in the species composition from acid, wet sites and base-rich, dry sites toward more intermediate conditions. We showed that the level of impact of these environmental changes may strongly depend on initial site conditions.
In the absolute terms, compositional changes in GV between the first survey and last resurvey were of small to moderate magnitude. The lack of directional change over time in GV species composition can be explained by several factors. First, our resurvey spanned a relatively short time period and compared only two snapshots in time. Second, the response of GV to anticipated environmental changes may be buffered by tree layer canopy. Such effects seem to be particularly important in case of global warming (microclimate buffering) and atmospheric nitrogen deposition (canopy interception; however, canopies can accumulate high amounts of dry deposit which is then flushed by rainfall). Third, majority of GV communities studied are composed of perennial forest plant species which are known for their relatively high local persistence owing to clonal reproduction. All these factors contribute to time lags in response of forest plants to environmental change (De Pauw et al. 2022). Because environmental drivers act over long time periods, the response of vegetation could be delayed in time. This is particularly evident in forest understory vegetation due to buffering capacity of overstory canopy. Lastly, the fact that multiple environmental drivers are likely operating simultaneous might induce interactions between multiple drivers (Naaf and Kolk 2016; Hedwall et al. 2021). For example, forest disturbances creating canopy gaps have been proposed to amplify thermophilization of tree communities (Brice et al. 2019) and understory plant communities (Stevens et al. 2015; Dietz et al. 2020).
Slovenian IM sites are getting warmer with an average warming rate of 0.25 ºC per decade in the last ~ 70 years. Annual amount of precipitation has decreased in the period 1950–2018 by 2.4% per decade. Therefore, we anticipated GV to show increase in EIV-T and decrease in EIV-F. Across all vegetation plots at each site, the expected increase in EIV-T were confirmed for seven sites. The largest increase was detected for high-elevation spruce site (1-KK) and two montane beech forests (2-FO and 8-LO). It has been previously observed that GV is shifting towards more thermophilic composition at higher altitudes compared to lowlands (Küchler et al. 2015). In contrast, two lowland oak-hornbeam forest sites (11-MŠ and 10-KG) experienced decrease in EIV-T. Detected trends of decreasing EIV-T values may be explained by confounding influence of local stand dynamics. One additional factor controlling herb layer cover is the variability in the shrub and lower tree layer. More open tree canopies in the upper tree layer due to dieback of Quercus robur trees (mainly caused by changed hydrological regime, i.e., lowered groundwater levels) benefited juvenile tree growth (especially of Carpinus betulus with high lateral spread and shade-casting ability of canopy) and therefore increase shading and cooling of understory plants. Similar effects likely occurred at site 3-GB where abundant ingrowth of native deciduous tree species (Fraxinus ornus, Ostrya carpinifolia) induced microclimate buffering and consequently decrease in EIV for temperature in the herb layer. Discrepancy between the changes in abiotic environment and observed shifts in plant-derived indicators can be hence explained by confounding influence of forest stand dynamics, which were recognized as key drivers of long-term changes in understory diversity in old-growth forests (Nagel et al. 2019).
The shifts in EIV for soil moisture were on average the least pronounced (in terms of magnitude) among all ecological gradients studied. The values decreased at eight sites, with two sites at the Pohorje mountains (6-KL and 12-TR) exhibiting the largest decline. Lower EIV-F values can be interpreted as an influence of summer droughts and decline in snow precipitation amount, but these two high-altitude forests grow on siliceous bedrock with generally high water-storage capacity of the soil. Therefore, the declining trend in EIV-F was likely a consequence of changes in relative abundance of resident plant species because only few taxa were recognized as winners and there were no losers at these two species-poor sites which could explain observed trends. Two IM sites were exceptional in the other direction as they showed prominent increase in moisture values: 4-BR and 10-KG. These are two completely different forest ecosystems. The 4-BR is a Pinus sylvestris forest with packed understory dominated by dwarf shrubs, tall grasses and ferns adapted to acidic, infertile soil. The composition shifted towards higher dominance of graminoids and ferns while dwarf shrubs evidently declined. The 10-KG is an oak-hornbeam forest where some species with higher soil moisture demands increased (according to ISA). For example, the colonization of Carex pendula and Aegopodium podagraria might be related to microsites on skid trails where soil is more compacted, and thus moisture is elevated in the topsoil layers (Closset-Kopp et al. 2019). Another explanation for increase in EIV-F might be that soils in small canopy gaps are usually wetter due to lower evapotranspiration from trees (Helm et al., 2017) and this effect may be possible reason for increase of EIV-F at 9-GO (Dinaric fir-beech forest) experiencing some local openings in the canopy due to natural and management disturbances.
Nitrogen deposition can induce both eutrophication and acidification of GV. The most profound increase in EIV-N was observed for three sites on acidic (dystric) soil: 12-TR (acidophilous beech forest), 4-BR (acidophilous pine forest) and 6-KL (acidophilous spruce forest). This observation is in line with the hypothesis that forest sites on nutrient-poor soil are more susceptible to nitrogen deposition (Reinecke et al. 2014; Roth et al. 2022) compared to more nutrient-rich sites where nitrogen is not a limiting factor. The site 4-BR, naturally N limited forest dominated by Pinus sylvestris with relatively open canopy and acidic low-nutrient soils, is located in densely populated landscape where agricultural inputs (arable fields with high amounts of nitrogen fertilization) are potential reason for strongest eutrophication signal at this site. Previous studies also stressed that eutrophication of GV can be context-dependent (Perring et al. 2018). The nitrogen depositions may not be the primary cause for shifts towards higher EIV-N values. Changes in tree species composition and canopy closure can contribute to GV being composed of more nitrophilous species. Tree species with higher litter quality (e.g., noble broadleaves) facilitate faster decomposition of the litter and thus greater nutrients availability for herb-layer plants (Verheyen et al. 2012). The accumulation of slowly decomposing litter in a forest floor will lead to soil acidification (Vanhellemont et al. 2014). However, such effects are unlikely to be the leading cause of the observed increase in acidic forests at our IM sites. At the other side of the productivity gradient, two lowland oak-hornbeam sites (11-MŠ and 10-KG) experienced decrease in EIV for nutrients. According to ISA results, both sites showed the highest degree of species loss, with earl-flowering species (geophytes) being the most frequent among losers. Geophytes are considered as important indicators of overall naturalness of forest stands and these taxa mostly occur on fertile soils (i.e., have higher EIV-N values).
Because EIV-N and EIV-R values in European flora tend to be positively correlated, sites that showed eutrophication signal tend to also increase in EIV-R values. Acidification of GV mainly happened on more nutrient-rich (oak-hornbeam forests) and on calcareous IM sites. The decrease in EIV-R was observed for spruce forest on mixed bedrock (1-KK) where the topsoil acidification due to thick litter layer (needles) over otherwise more limestone bedrock is likely responsible for creating favourable conditions for acidic-tolerant species (Oxalis acetosella and Melampyrum sylvaticum were winners). In addition, Pokljuka plateau in the Julian Alps receives high rainfall amount and is continuously exposed to wind-induced remote transport of pollutants coming from industrial and agricultural areas in the northern Italy (Bragazza et al. 2005). The drop in EIV-R values was also recorded for two beech-dominated forests on limestone (2-FO) and dolomite (8-LO) parent material. Both sites had two common loser species, i.e., Cardamine enneaphyllos and Cyclamen purpurascens which are known to prefer basophilic substrate. The decline of these species likely contributed to lower EIV-R values. In addition, increase of acidophilous and/or decrease of basophilous plant species may have resulted from long-term deposition of airborne sulphur (Hülber et al. 2008) which is in declining trend at all IM sites where measurements are available (data not shown).
Forest disturbances can open overstory layer, weakening the shading and colling effects and thus act as triggers for more rapid changes of the forest GV (Helm et al. 2017). Increasing forest disturbances were earlier identified as the dominant factor shaping the changes in GV across Slovenian IM sites (Kutnar et al. 2019). Sites experiencing higher intensity of disturbances also shifted more in overall GV composition. By modifying the cover of tree layer and thus light availability at the forest floor, anthropogenic and natural disturbances play an important role in the context of global environmental changes as they can modulate the response of GV (Hedwall et al. 2021). Three sites experienced increase in EIV-L, namely 11-MŠ, 3-GB (Pinus nigra forest) and 9-GO. Interestingly, the first two mentioned sites showed decrease in EIV-T, contradicting the assumption than more light should result in warmer microclimate in the understory. All three sites decreased in canopy cover but not on all plots. Disturbances were mainly limited to smaller spatial scale due to mortality of individual trees or management interventions. In this sense, disturbances likely increased environmental heterogeneity where closed stands are mixed with small-scale canopy gaps. Nevertheless, in the majority of sites canopy cover still remained high enough to buffer GV against macroclimate warming and nitrogen depositions. In the absence of disturbance events, natural succession towards late-successional stages causes tree layer canopy to become denser and light availability at forest floor to decrease (e.g., studies dealing with abandonment of traditional management practices such as coppicing; Kopecký et al. 2013)
Overall, the observed changes in GV can be mainly attributed to local changes in ecological conditions. This is why the overall impacts of global and regional drivers has not yet come to full expression. Local changes (e.g., in canopy cover and composition) may mimic or counterbalance the effects of regional or global drivers (Naaf and Kolk 2016). Many studies concluded that local factors (forest stand dynamics) are responsible for temporal trends while the signal of global change drivers (climate change) was less evident, possibly due to time lags in response of GV. Ascribing changes in GV to environmental drivers in a reliable manner is a challenging task (Staubli et al. 2021). In the absence of in situ measurements of abiotic parameters (microclimate, edaphic conditions), it is difficult to relate observed compositional shifts in species assemblages to particular driver. Causality for changes is also not uniform and multiple drivers simultaneously act on plant communities in a synergistic or antagonistic manner. Caution should be taken when relating observed changes in GV to presumed environmental drivers. The inclusion of broad spectrum of forest types in our study permitted us to improve the understanding of context dependency, as has been emphasized for the response of forest plant communities to global change (Hedwall et al. 2021), especially for potential nitrogen deposition effects (Verheyen et al. 2012; Perring et al. 2018).
The comparison of fenced and unfenced plots may suggest impact of deer browsing on GV temporal dynamics. Increase in graminoids and ferns in our study can be interpreted as browsing effects because the plant functional groups are less (grasses, sedges) or even completely (ferns) disfavoured by ungulates. Similar to our observations, many resurvey studies found an increase in woody species presence. Seedlings of tree species constitute an important part of GV, but their temporal dynamics is also dependent on mast years (Vanhellemont et al. 2014). The most evident was the difference in frequency of more palatable tree species in the herb and shrub layer. Natural regeneration of deciduous forests is likely to be threatened by intensive browsing pressure if appropriate measures are not applied (e.g., fencing in our case). One of simple proxies for this influence is evident discrepancy in abundance of key tree species in the herb layer (height < 0.5 m) and the shrub layer (height > 0.5 m) which is in many cases dominated by dense thickets of strongly competitive beech. Inadequate ingrowth to higher vegetation layers is serious management problems and poses one of the greatest threats to the naturalness and conservation status of various forest habitats in Slovenia (Veselič 2017; Kermavnar et al. 2023b). Such direct effects are accompanied with indirect impacts. Deer browsing can also act as a biotic filter for some more palatable herbaceous plants with nutritious leaves. Herbaceous species with higher SLA values are, according to literature (Wilson in sod. 1999), more palatable to deer. Shade-tolerant forbs with higher SLA and thinner leaves and foliage less resistant to decay (i.e., species with more nutrient-rich, easily decomposable aboveground parts) but also more susceptible to browsing.
Different forest sites with contrasting ecological backgrounds are expected to response differently to individual environmental driver. Besides differences in site characteristics, site history (former land use or silvicultural system applied) and initial site conditions like soil nutrients status may also play an important role in shaping responses of temperate forest plant communities to environmental changes (Naaf and Kolk 2016). Presented results are in line with the assumption that signals of environmental drivers are likely to be more pronounced at sites which are at the opposite end of the ecological gradients. For example, climate warming is expected to cause vegetation thermophilzation in more cold-adapted communities (higher altitudes) compared to thermophilous forests. Similarly, atmosperhic deposition of nitrogen is presumed to cause nitrophilous plants colonization in N-limited ecosystems rather than in forest on nutrient well-supplied soils (Hedwall et al. 2021).
Averaged across all sites, our analysis provided only weak evidence of an effect of environmental changes on GV. Shrinking effect was evident for all ecological gradients. Shifts towards the middle of the gradients (process of ecological contraction) was likely driven by the decline of ecological specialists and their replacement by species with greater ecological amplitudes and intermediate requirements for resources. More extreme forest sites (positioned at both ends of the gradient) are thus losing their unique character and are becoming more similar to communities positioned in the middle of the ecological gradient (Kopecký et al. 2013). Contrasting directions of shifts, site-specific changes and overall weak signal of environmental drivers suggest relatively high degree of stochasticity rather than deterministic (directional) changes in GV. The shrinkage effect can be perceived as some form of homogenization (ecological convergence) and should be monitored in the future.
Differences in traits between winners and losers reflect impacts of environmental change. Taxa showing declining trend or lost from the total species pool were labelled as losers. They were significantly lower in stature and had (insignificantly) higher specific leaf area (SLA) values compared to winners. This suggest that vegetation is shifting toward taller and more conservative communities. Such trends can be interpreted as effects of disturbances and/or thermophilization (Stevens et al. 2015; Govaert et al. 2021b). Drought-tolerant species have lower SLA (Stevens et al. 2015).
The observed ecological contraction could suggest that ecological specialists are disappearing and are being gradually replaced by species with broader ecological niches (generalists). This corroborates with our previous study (Kutnar et al. 2019). The loss of rare species can lower compositional variation within a site (Vanhellemont et al. 2014) and could lead to floristic homogenization (Naaf and Wulf 2010; Durak and Holeksa 2015). In addition, plants with early-spring phenology were frequently observed among losers. Geophytes have been recognized as important indicator of conservation status of forest habitats and as a functionally distinct species group in understory communities of temperate deciduous forests (Durak and Durak 2021). They mostly occur on nutrient-rich soils and prefer higher soil moisture and relative humidity. The highest representativeness of geophytes at our sites was in lowland oak-hornbeam forests and in beech-dominated communities. A possible reason for observed decline of geophytes in our study might be in climate warming. It is feasible to assume that geophytes are now starting to develop earlier in the late winter/early spring compared to 15 years ago, due to milder winters and higher temperature. Negative effects of winter and spring warming on the seedling emergence and overall regeneration of forest geophytes has been experimentally tested by Vangansbeke et al. (2022). Lack of precipitation in this period may also contribute to their decrease. Another evidence why geophytes may be particularly vulnerable to climate change comes from studies in North America. A mismatch between understory and overstory phenology may lead to a reduction of understory light levels in the early spring, which is a critical period when many spring-flowering forest herbs achieve highest photosynthetic rates (Miller et al. 2023). Such effects reduce carbon budgets of geophytes under climate change (Heberling et al. 2019). In contrast to our results, Nagel et al. (2019) reported long-term increase in geophytes in fir-beech forest reserves, which was likely driven by decline of silver fir and subsequent increase in cover of beech in the lower tree and shrub layer, enabling higher light levels at the forest floor during early spring.
We recommend continuation of regular GV monitoring, expanding the research to broader extent (ICP-Forests Level II plots) and, if possible, evaluation of potential effects of environmental changes using data for other plant groups (e.g., bryophytes). Given the relatively high variation in response of local communities (individual plots within a site), it is feasible to perform surveys using different plot sizes (10 × 10 m vs. 2 × 2 m in our case) to capture full environmental heterogeneity within a forest stand. Specific microsites might be occupied by habitat specialists which are apparently showing decline in occurrence. Monitoring of GV should be complemented with in situ measurements of climate, soil properties, atmospheric nitrogen deposition and other variables that can be than used as explanatory factors. Mid- and long-term observational studies are required in order to unravel individual and aggregated impacts of multiple stressors on forest vegetation composition and diversity. While resurvey of historical plots became popular approach to infer global change impacts, regular monitoring in permanent plots included in broad-scale monitoring networks (e.g., ICP-Forests) have several advantages, manifested in standardized protocols and harmonized monitoring, enabling more robust cross-site comparisons of plant diversity and community composition.