Introduction

Cushion-forming species, hereafter referred to as cushions, are a growth form adapted to alpine and polar environments (Aubert et al. 2014). Cushion plants retain dust and litter thanks to their compact, often dome-shaped canopy, moderate temperature, and moisture regime inside the canopy (Molenda et al. 2012), thus improving soil fertility (Zhao and An 2021). Because these plants are decoupled from the atmosphere due to their low stature and high stem density, they act as efficient heat traps within the canopy (Körner 2021). These characteristics allow cushion plants to act as nurse plants in arctic and alpine environments, not only with respect to higher plants (Reid et al. 2010) but also with respect to arthropods and soil microbiota (Aubert et al. 2014). In this regard, and in combination with the individual longevity of adult specimens, cushion plants are considered baseline species or ecosystem engineers because they create positive feedbacks for their own benefit and for the benefit of other species by acting as local micro-refugia facilitating less stress-tolerant species.

Species migration and ecosystem regime shifts are expected to become more sudden and frequent under current and projected human-induced climate change. A rapid increase in temperature and changes in precipitation regimes, as well as a reduction in snowpack, may be critical for alpine plants (Körner 2021). Temperature rise affects the length of the growing season of plants at middle and high elevations, as their growth is primarily temperature limited, and promotes greening of previously bare ground, as recently demonstrated in the Alps (Choler et al. 2021). However, periodic heat waves can affect vegetation differently depending on growth form and ecological adaptation. For example, in 2003, Europe experienced its warmest summer in over 500 years (Jolly et al. 2005), with significant negative impacts on the economy, agriculture, and forestry. Cushion plants, which act as heat traps and normally facilitate growth at high elevations, can suffer from extremely high temperatures that can be lethal to active tissues, especially when coupled with summer drought that limits evaporative cooling (Körner 2021). Dahl (1951) suggests that such outstretched cushion plants cannot grow and survive at low elevations because of the pronounced disconnection from the atmosphere and the heat-trapping effect that would damage plant tissues.

Recently, collapse of foundation species caused by climate change has been reported (Bergstrom et al. 2021a). A notable example is the old-growth cushion plant Azorella macquariensis Orchard (Apiaceae) on subantarctic Macquarie Island, which has been decimated in the last decade by climate change that led to a sudden shift in the regime on the fellfield (Bergstrom et al. 2015). The dieback of A. macquariensis has been linked to an increase in wind speed, hours of sunshine, and evapotranspiration demand, resulting in a significant water deficit for the plant. Recent studies revealed a possible role of soil-borne plant pathogens that are more prevalent in areas with fewer frost days and higher relative humidity (Dickson et al. 2021). However, with the exception of the well-studied collapse of A. macquariensis on a subantarctic island, no evidence of large-scale dieback of cushions has been reported to date.

Silene acaulis (L) Jacq. subsp. bryoides (Jord.) Nyman (hereafter Silene) is an alpine cushion plant that is widespread throughout the Northern Hemisphere (Körner 2021) and probably the best studied (Aubert et al. 2014). Silene has a dome-shaped, compact, and hemispherical canopy that acts as an efficient heat trap (Bonanomi et al. 2016). In addition, Silene is known as a nurse plant due to its ability to buffer microclimatic conditions by releasing warmer temperatures, creating more stable soil moisture, and forming a fertility island within its canopy (Molenda et al. 2012; Kjær et al. 2018). During a field survey in summer 2022, we observed extensive senescence and dieback of Silene in the Appennines (Fig. 1). Our overall goal is to quantify the extent and distribution of Silene dieback to provide a basis for future studies that will focus on causal and mechanistic hypotheses. To this end, we studied Silene dieback along a 500 m elevation transect from 1900 to 2400 m a.s.l. in the Sibillini mountain group, part of the Apennines. Furthermore, we investigated the putative role of the summer 2022 heat wave that hit the Apennines in the dieback of Silene. The specific objectives of our study were (i) to quantify Silene dieback along an altitudinal gradient and (ii) to assess the possible impact of the summer heat wave on Silene dieback.

Fig. 1
figure 1

Selected images of the study site at ~ 2200 m a.s.l. A and specimens of Silene acaulis with close-up of healthy and green plants B, C, dying and yellow plants D, E and scar, grey plants F, G. Pictures by G. Bonanomi

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Materials and methods

Study site description

The Apennines Mountain range is ~ 1200 km long, running down the Italian peninsula from north to south and ranging in latitude from ~ 38°N to ~ 44°N. This study was conducted in the Monti Sibillini group, part of central Apennines, having as highest peak Monte Vettore (2476 m a. s. l.m,; 42°49′27.60′′ N, 13°16′29.26′′E). Sibillini had the lowest average treeline in central Italy (Bonanomi et al. 2020), being characterized by very ample and characteristic altitudinal grasslands (Allegrezza et al. 2013) with Fagus sylvatica forests often limited to very steep and rocky slopes. Mountain and subalpine grasslands are still exploited for agricultural purposes at altitudes up to 2000 m a.s.l.

The altitude of the study sites ranged between 1900 m and 2400 a.s.l. on the north-facing face of the mountains and Mount Argentella (2201 m a.s.l.), Cima del Redentore (2448 m a.s.l.), and Monte Vettore. The substrate is exclusively calcareous belonging to the Umbria-Marche limestone succession and specifically to the Corniola Limestone Formation characterized by high primary and secondary permeability (cracking, karst, etc.) (Regione Marche 2003). Poorly developed soil, classified as lithosol, is characterized by the presence of a small thickness of superficial calcareous debris originating by gelifluction phenomena in situ. The total mean annual rainfall at the Monte Bove meteorological station located at 1904 m a.s.l. at ~ 10 km from the study site is 801 mm, but with summer drought. The mean annual temperature is 5.9 °C, with monthly temperatures that range between 15.3 °C (August) and –1.5 °C (January).

The vegetation has a very low cover value (25–30%) and it is represented by a dwarf-cushions community characterized by Silene acaulis subsp. bryoides referred to the habitat code 6170 “Alpine and subalpine calcareous grasslands” (Habitat Directive 92/43/EEC, Annex I).

Assessment of Silene dieback.

Silene dieback was quantified during a vegetation survey conducted from 6 to 10 August 2022. The degree of dieback in Silene was assessed in 3 m × 3 m quadrats across 30 sites. Sites were distributed along a gradient of six elevations, i.e. 1900, 2000, 2100, 2200, 2300, and 2400 m a.s.l. At each elevation were randomly selected five 3 m × 3 m quadrats with a minimal distance of 50 m.

Three stages of plant status were observed: healthy and “green” stem and leaf, dying stem with “yellow” leaf and old and “grey”, with erosional plant surface, indicating death prior to the previous growing season (Fig. 1). Grey erosional plant surface were not classified as dieback (Bergstrom et al. 2015). Estimates of the proportion of “green”, “yellow”, and “grey” cover of Silene were visually estimated for each individual within the 30 selected plots.

Quantification of summer 2022 heatwave

Meteorological data were obtained from the network of Protezione Civile of Regione Marche (https://www.regione.marche.it/Regione-Utile/Protezione-Civile). The meteorological station that lies at 1904 m a.s.l. at only ~ 10 km from the study site has hourly resolution for temperature and daily resolution for rainfall for the period 2005 to present day. Daily mean maximum and minimum temperature values were calculated through hourly observations, excluding days with missing observations.

Monthly mean values for maximum and minimum temperatures were calculated from daily values. Months with more than ten missing daily mean values were excluded from the analysis. The occurrences of summer heat waves were assessed comparing monthly temperatures in summer months with long-term meteorological data collected from the last 17 years (from 2005 to 2021). Moreover, we used the daily values in order to identify sequences of consecutive days with particularly high temperatures above the long-term average. Concerning rainfall, we compared monthly values of May, June, July, and August with the long-term average calculated from 2005 to 2021.

Results

Silene dieback

During the growing season, healthy Silene cushions appear deep green and usually are firm to touch and resistant to hand compression because of the high stem density (Fig. 1) (Bonanomi et al. 2016). The portion of the cushions that died in previous seasons appear grey, dry to the touch and devoid of the leaves (Fig. 1). Instead, the parts of the plain subject to dieback in the current season are yellow–brown and with the leaves still present (Fig. 1). Dieback in Silene was not evenly present across the full elevation gradient, being widespread at 1900 and 2000 m a.s.l. and progressively decreasing with the increase in altitude (Fig. 2). In detail, dieback surface was 40.7% and 38.4% at 1900 and 2000 m a.s.l., respectively, but less than 1% at an elevation higher than 2300 m a.s.l. As a result, green plant surface was over 70% at an elevation higher than 2100 m a.s.l., but lower than 45% at 1900 and 2000 m a.s.l. (Fig. 2). Finally, the grey died plant portion was lower than 20% of surface at all elevations, with the highest values recorded at 2000 m a.s.l.

Fig. 2
figure 2

Silene acaulis dieback in 2022 along a 500 m elevation gradient. Plant status is expressed as fraction of healthy and green, dying, and yellow, and scar and grey plant surface

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Summer heatwave

Monthly maximum and minimum temperatures were higher in 2022 compared to long-term average in May, June, and July (Fig. 3). In detail, the maximum air temperature in 2022 was 3.7, 4.5, and 3.4 °C higher in May, June, and July 2022 than the respective long-term average. A similar trend was recorded for minimum temperature that was 3.7, 3.8, and 2.9 higher in May, June, and July 2022 than long-term average. Notably, July monthly maximum (21.5 °C) and minimum (14.6 °C) are the highest ever recorded since the start of the meteorological station in 2005. Concerning daily maximum temperature, in July 2022 we found three consecutive days with temperature exceeding 25 °C (24th, 25th, and 26th). Temperature over 25 °C was recorded only four times in the previous 17 years (one day in 2010, another one in 2017 and two days in 2021) (Online Resource 1, Fig. S1). Moreover, in 2022 we recorded five days with temperature exceeding 24 °C (from 22nd to 26th July) and 16 days with temperature exceeding 20 °C (from 15 to 30th July). Consecutive days with such high temperatures have never been measured in the previous 17 years (Online Resource 1, Fig. S1).

Fig. 3
figure 3

Minimum (above) and maximum (below) monthly air temperatures recorded during the whole 2022 compared with the average of the years from 2005 to 2021 at Monte Bove meteorological station (1904 m a.s.l. at ~ 10 km from the study site)

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Concerning precipitation, in the growing season from May to August, the rainfall was 180 mm against a long-term average of 255 mm, resulting in a 30% reduction. On a monthly scale, June was rainier than the long-term average (+ 45%), while August (− 17%), May (− 58%) but above all July (− 72%) were less rainy (Fig. 4). In detail, in July 2022, only 15.2 mm of rain fell against a long-term average of 54.3 mm.

Fig. 4
figure 4

Rainfall recorded during the 2022 growing season compared with the average of the years from 2005 to 2021 at Monte Bove meteorological station (1904 m a.s.l. at ~ 10 km from the study site)

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Discussion

In the summer of 2022, we found that the ecosystem engineer, key-stone species, the cushion plant Silene, suffered a sudden and widespread dieback. The intensity of the dieback was found to increase with decreasing elevation, and it was particularly severe below 2000 m a.s.l., where about 40% of the plant area was affected. Although we noted that some plants were grey and already dead, suggesting that they had died in previous years, the intensity of dieback observed in 2022 is unprecedented for Silene along the Apennine chain.

Several cases of dieback of cushion species have been reported in various geographic areas over the past decade, including A. macquariensis in subantarctic Macquarie Island (Bergstrom et al. 2015) and Lyallia kerguelensis in the Kerguelen Islands (Marchand et al. 2021). To date, the causes of dieback have been studied in detail only in the case of A. macquariensis. Early studies identified water stress as the primary cause of dieback due to long-term climatic changes (Bergstrom et al. 2015). Specifically, the climate on Macquarie Island has become more stormy, and the number of heavy precipitation events and annual rainfall increased, but at the same time, increases in sunshine hours, frequency of windy days, wind speed intensity, and evapotranspiration rates (Adams 2009) have resulted in significant increases in plant water deficit. Subsequent studies have found the presence of several pathogens in dying plants, including Rhizoctonia and Rosellinia (Bergstrom et al. 2021b). However, the causal relationship has not been established because these pathogens are polyphagous and often attack plants weakened by other abiotic stresses (Agrios 2005). The relative importance of water stress caused by long-term climatic changes and secondary pathogens in the dieback of A. macquariensis remains to be determined.

For Silene, dieback was most severe and advanced at the lower end of the elevational gradient below 2000 m a.s.l., suggesting a change in microclimatic conditions. Detailed analysis of climate data from the Monte Bove meteorological station, which is only ten kilometres from the study area and at a similar elevation, clearly shows that June and especially July 2022 were the warmest months since the data were collected. July, in particular, was not only the warmest month on record but also recorded numerous consecutive days of unprecedented day-time and night-time temperatures. Another stressor was the lack of rainfall which totalled only 15.2 mm in July, a figure that was below the long-term average of 72%. The combination of several consecutive days of very high temperatures combined with scarce water availability may have resulted in thermal stress for Silene, which tends to retain heat due to its cushion-like structure (Körner 2021) and therefore could be damaged by excessive temperatures. Our data suggest a shift in climate away from the fundamental niche of the cushion plant Silene, at least during the summer months. To test this hypothesis and obtain robust and direct information on the putative causes of dieback, soil water content, plant water status, and quantification of transpiration fluxes during summer months need to be examined.

In a larger context, the sudden occurrence of Silene dieback demonstrates the vulnerability of high-altitude vegetation to climatic changes. The loss of cover cushions, especially for Silene populations in its southern biogeographic range, is significant and alarming for the survival of this long-lived but very slow-growing plant (Morris et al. 1998). The species could find refuge as demonstrated for other plant species in the Alps and other mountains at higher altitudes (Randin et al. 2009; Gómez et al. 2015), but in the case of the Apennines this ecological possibility is limited to Gran Sasso (2912 m a.s.l.) and Majella (2793 m a.s.l.) due to the relatively low altitude of most peaks, which are usually below 2500 ma.s.l. If the dieback of Silene will continue in the next few years, this plant community would be replaced by grasslands currently present at lower elevations, such as Sesleria juncifolia and Sesleria nitida communities. In the near future, it will be important to monitor the health of Silene populations in other areas of the Apennine chain, especially at the lower limit of altitudinal distribution, in order to plan appropriate conservation strategies.