In this study, we investigated potential reasons for the decline of the European populations of the formerly widely distributed band-winged grasshopper B. tuberculata using ecological niche modelling in combination with a basic population genetic assessment. Specifically, we aimed to test if (1) changing climatic conditions over the last 100 years, or (2) changes in land-use and land-cover are responsible for the decline and local extinction. For this we assessed the habitat requirements and the decline of the species and modelled the environmental niche. Furthermore, we tested if (3) the genetic diversity in the Asian core populations is higher than in the European relic populations, which may support the center-periphery hypothesis. We discuss the results in regards of conservation management of the species.
Climate models reveal suitable conditions in extinct locations
We used an ellipsoid envelope approach to estimate the climatic niche of
B. tuberculata and measure the proximity of its populations to their optimum. All sets recovered low distances of the extinct populations to the climatic niche centroid, and none recovered any difference between extinct and extant populations (Figs.
2,
3; SI 6–7).
Set 1 offered higher variation in distances to the centroid (range: 0.417–32.611), possibly due to the higher variation and multi-dimensionality of the principal components included (i.e., 15 variables).
While most extinct populations were located in areas with lower Mahalanobis distance (D
2) to the centroid (i.e., high suitability), two extinct locations with higher values were recorded (D
2 = 22.306 and 17.142; Fig.
2, Table
3). These locations represent a population close to the German-Austrian border in the Berchtesgaden national park (D
2 = 17.142) and a population in Austria close to Ried im Innkreis (D
2 = 22.306). The higher D
2 at these two locations could have several reasons, e.g. imprecise locality data, errors in georeferencing, individuals dispersed from neighboring locations (e.g. migrating individuals; Barton and Hewitt
1982), artefacts of the bioclimatic layers used (e.g. Marchi et al.
2019; Poggio et al.
2018), or even just a high tolerance regarding abiotic conditions (e.g. Preston and Johnson
2020). The last reason is supported by data from Asia with similar D
2 range. Since our models predict areas situated in the distribution gap between the European and Asian populations as climatically suitable, the destruction of natural habitats is a likely reason for the loss of stepping stones and for the extinction of any connecting populations in the area.
Habitat requirements and historical decline of B. tuberculata
Bryodemella tuberculata is a species of open landscapes, preferring habitats with sparse vegetation and open ground. According to our observations, all Russian collection sites in the Altay-Sayan Mountains, the Kulunda Plain (the south-eastern part of West Siberian Plain between the Irtysh and Ob Rivers) and within the south-eastern Ural Mountains (pers. obs. MGS; for further details, see SI 9) were mainly composed of dry meadows and steppes with sparse vegetation (~ 10–30 cm height) and spots of open ground (generally, the vegetation cover was less than 80%). The ground is mostly sandy to rocky, with smaller pebbles. In most cases occurrence sites were close to water systems. The species enters transformed ecosystems, such as the steppe variants with moderate livestock grazing and the dry hayfields. This type of habitat was found at almost all visited collection sites in Central Asia and Europe (for habitat images see Supplementary Information SI 10). In Mongolia, the species is found in low abundance, but in almost all habitats with open spaces and sparse vegetation, mainly covered by shorter plant species up to 30 cm and at the edges to forests (pers. observ., LSD 2015–2019; Dey et al. in press; Supplementary Information SI 10). Pastures for grazing represent the major agricultural use in the country, hence, the landscape is characterized by bare steppe habitats with low vegetation providing good conditions for B. tuberculata.
All extant populations of Central Europe (Southern Germany, Austria) inhabit alpine river valleys with unmodified or little modified flood regimes; specifically zones of alluvial gravel beds with sparse or without any vegetation. Occasionally, individuals may be observed in adjacent structures similar to those described for the Asian populations (Landmann
2017). Since the middle of the 19th century, populations of
B. tuberculata in Europe have been declining (e.g. Reich
1991; Zuna-Kratky et al.
2017). Despite the availability of a large database, we are unable to make any statements about the exact timing of extinction of
B. tuberculata at any particular location, but we provide the last recorded findings for several regions (Fig.
1; Supplementary Information SI 11). Altogether, our data suggest that most Central European extinction events took place between the 1920’s and 1960’s. We therefore suggest that each local extinction event in Central Europe may be closely connected with local landscape changes. Historically, at least in the mountainous regions, the naturally occurring annual floods following snowmelt removed most vegetation growing in the riparian habitats. Anthropogenic reductions of the flood volume, mostly due to the construction of hydroelectric dams, led to the establishment of shrub and tree vegetation in these habitats and a decline of the areas suitable for
B. tuberculata (Reich et al.
2008; Juszczyk et al.
2020). A variety of restoration measures have been put in place over the last decades, including a reduced deduction of water for hydroelectric energy generation, mechanical removal of vegetation, and education of the public; the mid- and long-term efficiency of these measures remains to be demonstrated (Juszczyk et al.
2020). A different type of change to the habitat structure was recorded in Denmark. There, most heathlands in the vicinity of Abild (an extinct location) have been converted to agricultural areas or were overgrown by shrubs (pers. observ. LSD; SI 10). Although the agricultural land-use decreased from 74% in 1915 to 61% in 2015, afforestation and urban expansion still led to a decline of heath areas previously typical for many parts of Denmark (Pedersen and Møllenberg
2017). The species has been listed as extinct in Denmark since the 1950s. Similarly, in Northern Germany, restoration of some old heath landscapes has been performed. Based on literature and museum surveys, we were able to find several records from the Lüneburger Heide heathland areas, for which the gradual conversion to arable land and forests at the end of the 19th century is historically documented (Koopmann
2000). This change in land-use was mainly triggered by a decrease in the local production of wool and honey due to external competitors, making the maintenance of large pastures uneconomic (Naturpark-Lueneburger-Heide.de; Koopmann
2000). During the early 20th century, the first areas were restored to the original heath systems. Nowadays, the Lüneburger Heide is one of the largest heath areas in Northern and Central Germany. Although most heath areas in Central Europe declined through time, some of these cultural landscapes are still intact. Many of them are now under military use and kept open by military activity, which practically equals to legal protection of the landscape. As a result,
B. tuberculata was rediscovered on 03 August 2008 in the Pabradė military training area in Lithuania, where it had been assessed as possibly extinct until 2008 (Budrys et al.
2008; Budrys and Pakalniškis
2007). This was the first record since the first half of the 20th century (Budrys and Pakalniškis
2007); yet, the status of the population remains unknown and it will have to be monitored to check its population establishment. In Northern Europe the population on Øland (Sweden) shows similar habitat preferences for barren land. The implementation of specific conservation measures appears to keep the population relatively stable.
Bryodemella tuberculata needs larger areas with open habitat, often with frequent natural disturbance. Anthropogenic changes of the European landscape in the last centuries (Plieninger et al.
2016; Hersperger and Bürgi
2009; Antrop
2004) likely led to the current patchy distribution of the species and will probably cause the extinction of further populations in the European range. The time series of land-cover plots (Supplementary Information SI 8) supports land-use change as a driver of the decline of
B. tuberculata as it displays a rapid change from grassland and agricultural areas to settlement and reforestation in the middle of the 20th century and still ongoing. This change from open areas to more closed habitat types, and an increase of human pressure due to high-intensity land-use, may have led to the extinction of
B. tuberculata at many Central European locations. Even though some habitats of extinct populations have now been restored, they are highly fragmented, and the dispersal capabilities of
B. tuberculata appear insufficient to allow for quick colonization of these habitats without support. Similar scenarios of decline have been described for many other European species, e.g., carabid beetles with different ecological preferences in Belgium, Denmark and the Netherlands (Kotze and O’Hara
2003); common and widespread butterflies in the Netherlands (Van Dyck et al.
2009); or the ground nesting Black Grouse populations in Lower Saxony, Germany (Ludwig et al.
2009). In turn, the availability of large stretches of natural habitats suitable for
B. tuberculata currently remains much higher in the Asian range. However, vast areas of habitat are also being destroyed in Russia, especially in the European part of the country, due to urbanization, agriculture and mining (Smelansky and Tishkov
2012). This process is much slower due to lower human activity in these areas and simply a larger area, but can also be expected to fragment populations and impact genetic diversity in the near future.
Distribution of genetic diversity and historical demography
While our genetic data is limited, also due to the rareness of the species, it suggests that the majority of genetic diversity is found in Central Asia. The European populations show lower diversity and are nested within the Asian populations. Hence, based on our COI data, European populations only represent a subset of the species’ genetic diversity, as expected for relic populations, which may have gone through a population bottleneck (e.g. Chen et al.
2016; Gaublomme et al.
2013; Hájková et al.
2007; Lucchini et al.
2004). We did not find any evidence supporting the status of these populations as distinct genetic lineages. This may suggest a previously more continuous, potentially panmictic distribution across much of Europe and Asia and a relatively recent fragmentation and decline in Central Europe, as also suggested by our historical distribution data.
The genetic patterns do not support the center-periphery hypothesis, i.e., low genetic variability in areas of low environmental suitability, as low genetic variability was also detected in areas of high environmental suitability. However, due to strong contemporary restrictions on migration, gene flow is likely completely interrupted and the European populations are likely under a drift regime, rendering them prone to extinction. On the other hand, Bayesian Skyline plots provide some evidence that supports the center-periphery hypothesis driven by geographic distance. Our results show that female effective population size is larger in Central Asia and also has been more stable in the last 10 ka (Fig.
5), while the European populations have smaller estimated population sizes and are in decline. The results we obtained match other taxa with similar distributions, e.g., the leaf-beetle
Cheilotoma musciformis, which has some relic populations in Poland. These populations are declining, probably because habitat destruction caused a disjunction from the main distribution, resulting in an observed genetic bottleneck (Kajtoch et al.
2016). Such patterns of loss of genetic diversity associated with habitat destruction, which have led to the disjunction of populations, can also be seen in the decline of the Danish population of the otter
Lutra lutra (Pertoldi et al.
2001), among others (e.g. Cremene et al.
2005; Kotze and O’Hara
2003).
Insufficient genetic samples and lack of more fine-scaled genome-wide markers inhibited the direct assessment of a relationship between genetic diversity and niche centrality. Nevertheless, our results support the findings of Lira‐Noriega and Manthey (
2014), who equally failed to detect any clear relationship between genetic diversity, and geographic and environmental distance to the geographic centroid. However, they did find a strong relationship between genetic diversity and climatic niche centrality. In some taxa, Lira‐Noriega and Manthey (
2014) describe a negative tendency for the relationship of genetic diversity and geographical distance to the source population, reflecting environmental impact on the population dynamics, rather than a fundamental ecological relationship. In case of
B. tuberculata, we suggest a similar effect of habitat destruction in the periphery of the distribution supported by decreasing female effective population size in the European populations (geographically distant from the main distribution; source) in contrast to the stable demography in the Asian populations (geographically close to the source). A more detailed study of other habitat characteristics, especially land-use patterns, may shed light on the reasons for the local decline and could help to manage the conservation activities to save the remaining European populations from decline, which may also facilitate the recolonization of former locations.
Aspects of conservation management
Local conservation efforts for species with isolated and declining populations may often be seen as unsustainable, because these populations may be threatened by the effects of climate change, which cannot be counteracted by localized efforts (e.g. Sinervo et al.
2010, Malcom et al.
2006). Our results show that extinct or threatened European populations of
B. tuberculata are in areas of optimal climatic conditions for this species, whereas some Asian populations appear to be thriving also in areas of poor climatic suitability. This suggests that
B. tuberculata is most likely resilient to the purely climatic effects of global warming in the Central European part of its range. If our results hold true, this means that threatened populations may survive the next decades of changing climate as long as their habitats are locally protected, and that these local efforts can be considered sustainable. This includes not only threatened extant populations, but also means that reintroduction efforts into the localities of extinct populations may be a promising option as long as the habitat structures necessary for
B. tuberculata have been restored and long-term management measures are in place. We suggest that monitoring of extant and potentially translocated populations should be accompanied by genetic studies using deeper population-level sequencing methods, such as microsatellites or RAD sequencing. Once a high-quality whole genome becomes available, genome resequencing may become a viable option.
The speckled buzzing grasshopper is just one species of an assembly of taxa sharing a habitat that is highly threatened by anthropogenic land-cover change. We believe that our study reinforces that status of B. tuberculata as a flagship and umbrella species for this organism community, and we hope that our results help making a case for increased efforts to their protection.