Introduction
The cessation of grazing is a common feature of the European landscape
and is expected to rise sharply over the next decade (Eurostat 2018),
especially in low-productivity, mountainous areas where previously
extensively grazed lands are increasingly being taken out of
agricultural production (MacDonald et al. 2000; Cramer et
al. 2008; Kuemmerle et al. 2016; Lasanta et al. 2017;
Eurostat 2018). Extensively managed, semi-natural grasslands are
widespread across Europe, often grazed since Roman or even pre-Roman
times (Prins 1998; Hejcman et al. 2013), and support an important
component of regional biodiversity, delivering multiple ecosystem
functions and services (Hector et al. 1999; Schröter et
al. 2005; Hautier et al. 2018). This has resulted in grassland
ecosystems with spatially heterogeneous vegetation (Adler et al.2001). Based on studies focused on plants, there is widespread concern
that the cessation of grazing in these ecosystems is causing biotic
homogenization due to a loss of rare specialist species and an increase
in common generalists, as well as overall declines in plant biodiversity
(McKinney & Lockwood 1999; Olden et al. 2004; Clavel et
al. 2011; Newman et al. 2014; Epelde et al. 2017; Oggioniet al. 2020). Further, biotic homogenization and associated loss
of biodiversity resulting from grazer exclusion is likely to impact
ecosystem functioning (Plieninger et al. 2014; Johansen et
al. 2019; Oggioni et al. 2020).
Despite the prevalence of grazer removal from historically grazed
ecosystems, major uncertainties exist regarding its impact on
biodiversity and ecosystem functioning. One particular uncertainty
concerns its impact on different components of biodiversity, which have
been observed to operate independently of each other. Species richness
at the local, plot scale (ɑ-diversity) is likely driven by changes in
land management (Socolar et al. 2016), whereas compositional
(between plot) variation (β-diversity), which includes variation in the
taxonomic composition of communities across sites, is driven by a range
of factors that operate from small to larger scales (Anderson et
al. 2011). Therefore, while ɑ-diversity may be stable or increasing in
some areas, β-diversity could be decreasing due to biotic
homogenization, i.e. communities from different sites become more
similar in composition (Dornelas et al. 2014; McGill et
al. 2015; Beauvais et al. 2016). There is mounting evidence that
the cessation of livestock grazing influences these different attributes
of biotic homogenisation of aboveground communities, including plants
(Bühler & Roth 2011; Newman et al. 2014; Beauvais et al.2016) and insects (Carvalheiro et al. 2013; van Noordwijket al. 2017), but far less is known regarding the effects on
communities of belowground organisms. Soil biodiversity regulates a
number of key ecosystem functions and services, for instance organic
matter decomposition, plant nutrient availability, nutrient leaching,
and soil structural stability (Bais et al. 2006; Mendes et
al. 2011; Berendsen et al. 2012; Philippot et al. 2013;
Turner et al. 2013; Schrama & Bardgett 2016). While some studies
have examined the effects of cessation of livestock grazing on
belowground communities in grasslands (Heyde et al. 2017; Oggioniet al. 2020), these studies generally focussed on specific groups
of soil organisms (but see (Bardgett et al. 1997; Bardgettet al. 2001; Epelde et al. 2017), short time spans since
grazing removal (Epelde et al. 2017) or a narrow range of climate
and soil conditions (Bardgett et al. 2001). Given this, there is
a clear need for an improved understanding of the long-term impact of
the cessation of grazing on the composition and diversity of belowground
communities.
Here, we explore how cessation of grazing impacts ɑ- and β-diversity of
both plants and belowground communities, by analysing resulting changes
in vegetation and a wide range of soil faunal and microbial groups. We
used a series of 12 montane grassland sites positioned along an 800-km
north-south gradient of the United Kingdom, and covering several of the
UK’s main montane grassland regions, each with several paired plots that
were either subject to historical grazing by sheep or had livestock
grazers excluded by fencing for 10-65 years. We focussed on montane
grasslands because they are a prominent feature of the European
landscape and have been grazed by sheep for centuries, forming the
backbone of the sheep farming industry across Europe (Rodwell 1990).
Further, the cessation of livestock grazing is commonplace in mountain
regions of Europe, including the United Kingdom, and is recognised as a
key aspect of land abandonment (Eurostat 2018) and rewilding (Pereira &
Navarro 2015), with the potential to have multiple, but largely unknown,
effects on local diversity and compositional variation in belowground
communities among sites (Figure 1; after (van Noordwijk et al.2017)).
Changes in ɑ- and β-diversity can occur simultaneously and have
positive, neutral or negative relationships. As such, we tested a range
of hypotheses, namely that: (1) increased ɑ-(plot-based) diversity
occurs when cessation of grazing results in a higher degree of local
environmental variation, and an increased availability of niches
supports more species (scenario C, E and H in Figure1); (2) decreased
ɑ-diversity happens when grazer exclusion results in a reduction in
local environmental heterogeneity, causing loss of rare species and/or
gain of generalist species (scenario A, D and F in Figure 1); (3) a
decrease in β-(site-based) diversity may occur independently of changes
in ɑ-diversity, which is expected when the removal of grazing has a
homogenizing effect on the composition of local communities within a
given area, independent of the effect on local soil community species
richness (scenarios A, B and C in Figure 1); (4) if current land
management causes strong homogenization of soil communities, we expect
that cessation of grazing will increase β-diversity through a gradual
divergence of communities, which may happen independently of changes in
ɑ-diversity by changing communities in various directions through
differential species losses and gains (scenario F, G and H in Figure 1).
We tested these hypotheses using our unique dataset of different
components of the belowground food web from long term paired grazed and
ungrazed exclosures across the United Kingdom.