Consistent population declines but idiosyncratic range shifts in Alpine orchids under global change

Mountains are plant biodiversity hotspots considered particularly vulnerable to multiple environmental changes. Here, we quantify population changes and range-shift dynamics along elevational gradients over the last three decades for c. two-thirds of the orchid species of the European Alps. Local extinctions were more likely for small populations, after habitat alteration, and predominated at the rear edge of species’ ranges. Except for the most thermophilic species and wetland specialists, population density decreased over time. Declines were more pronounced for rear-edge populations, possibly due to multiple pressures such as climate warming, habitat alteration, and mismatched ecological interactions. Besides these demographic trends, different species exhibited idiosyncratic range shifts with more than 50% of the species lagging behind climate warming. Our study highlights the importance of long-term monitoring of populations and range distributions at fine spatial resolution to be able to fully understand the consequences of global change for orchids.


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Life sciences Behavioural & social sciences Ecological, evolutionary & environmental sciences
For a reference copy of the document with all sections, see nature.com/documents/nr-reporting-summary-flat.pdf Ecological, evolutionary & environmental sciences study design All studies must disclose on these points even when the disclosure is negative. We analysed population survival, trends in population size, and range shift dynamics of Alpine orchids over 28 years in one of the plant diversity hot-spots of Europe. The historical dataset included 50,074 records for 60 orchid species recorded across the entire orchid elevational range of an Alpine region (66-2,970 m) over 28 years. However, we present results from analyses with 49,303 records for 44 species that meet our criteria for inclusion in the study. In addition, we selected a subset of sites (463) to resurvey orchid populations to detect evidence of survival or local extinction.
The historical dataset on orchid occurrence and abundance was collected by GP (Giorgio Perazza) and collaborators. All the data were stored in the private database of GP and in the GIS-inventory database of the Museo Civico di Rovereto (Rovereto, Trento, Italy).
Orchids are one of the most threatened groups of plants and population declines are well documented worldwide. However, previous research on mountain floras has focused on warming impacts on common taxa, while the response of rare and threatened species to global change has been largely overlooked due to data limitations. Our database is unique in describing the regional distribution of a rare, highly diverse and threatened group of plants because of its massive sampling effort compared to the relatively large spatial and temporal extent, spanning almost three decades.
The aims of the sampling of the historical database were to describe the regional orchid species distribution at a very fine spatial resolution, and to provide a network of sites to investigate orchids' population dynamics. In 2018, starting from the historical database, we selected a subset of sites to resurvey orchid populations to detect evidence of survival or local extinction. The selection of the sites was performed using a stratified random sampling in a GIS environment. The strata were the four major habitat types occurring across the elevational gradient: forests, alpine areas, semi-natural grasslands and wetlands. Further criteria of site selection were: 1) to include the whole elevational distribution of each resurveyed species, 2) to exclude sites with the occurrence of a single individual, 3) to cover most of the geographical area of the historical survey.
GP and collaborators collected data by sampling 21,601 sites, systematically covering the whole area of Trento Province. Each site was visited only once. Having identified a potentially suitable area in the field (i.e. natural or semi-natural habitats corresponding to open grassland, wetland or the woodland understorey), using a GPS they marked the site (point), recorded all the orchid species occurring in the close surroundings (c. 50 m), and counted the number of individuals per species. The general small size of orchid populations and the patchy distribution of individuals allowed estimates of population size in the field with relatively low uncertainty. The sites were not physically marked as true permanent plots but the centre of each site was georeferenced using a GPS (c. 5-10 m precision) and high-resolution topographical maps. At each site, the following variables were also collected: date of sampling, elevation, detailed site description (vegetation, proximity to roads or constructions etc.) and slope. All the data were stored in the private database of GP and in the GIS-inventory database of the Museo Civico di Rovereto (Rovereto, Trento, Italy). In spring and summer 2018 and 2019, GM and CG revisited the 463 sites following the sampling methodology of the first observer (GP), who constantly helped verifying baseline data, confirming species identification, relocating the sites and assessing habitat alterations. The sites were only visited once either in 2018 or in 2019. The re-survey was performed by actively searching the whole area around the sites surveyed in the historical survey (c. 50 m around the originally referenced point). Orchid species and number of individuals were recorded. Along with the orchid data, the following parameters were recorded: date, elevation, habitat type, and description of any local alteration occurred between the two periods. For the latter, we reported if a local disturbance (e.g. construction sites, touristic activities) or a habitat type change occurred in the second survey by comparing the description of the sites in the initial survey with the current conditions.
The historical dataset was collected starting from 1990 to 2017, while the re-survey took place in spring and summer 2018-2019. Data collection took place on a daily basis as long as weather conditions permitted it. Orchid populations were recorded throughout Trento Province, NE Italy (6207 km2, elevation range 66-3769 m), the historical dataset comprehends 21,601 sites, while te re-survey 463 sites.
1) To reduce model uncertainty, we excluded species with less than 30 records in both historical and current periods when testing the effects of elevation and time on population size and when computing range shift; 2) From re-survey analyses, a) we excluded observations with more than 30 day differences between surveys in the two periods to match species phenology, b) we excluded 11 observations for 9 species recorded less than 5 times (either singletons or doubletons) in the initial surveys because models included species as random factor and we could not test our covariates at the species level, and c) we excluded sites revisited after less than 5 years. The original design of the resurveys aimed at comparing historical vs. current conditions using this threshold. However, during the re-surveys some sites were resurveyed just because they were close to others matching our inclusion criteria. Therefore, they were excluded for consistency. However, results would have not changed by including these sites; 3) to estimate range shift rates with relatively low uncertainty using the network of re-surveyed sites, we excluded species with less than 10records in the first and 10 records in the second survey.
Not applicable since our study is not experimental (i.e. manipulative).
1) Randomization is not relevant for our study when we analysed the historical database. However, we performed in-depth analysis