5. Discussion
We assessed the effects of local and landscape environmental
heterogeneity on ant community structure in semi-natural temperate
grasslands. We found that extensively grazed pastures and within-site
heterogeneity in soil moisture and topographic exposition at the local
scale, as well as diversity of land cover types and forest cover at the
landscape scale affected ant community composition and evenness. Our
findings additionally confirmed the importance of local mean air
temperature and mean soil moisture as environmental filters of ant
species establishment in temperate grasslands (Dauber and Wolters 2005,
Seifert 2017, Heuss et al. 2019). Furthermore, our trait-based approach
showed that the response of overall ant community structure to local and
landscape environmental heterogeneity was mediated by a set of species
traits including morphological, ecological and life history features.
5.1. Effects of local and landscape heterogeneity on ant species
composition
Within-site variability of soil moisture affected ant species
composition by promoting nest densities of some species and therefore
total nest density per grassland site, while an increase of mean soil
moisture between grassland sites explained the decrease of nest
densities in our studied system. Although both results on soil moisture
may seem contradictory, they should be interpreted as the effect of soil
moisture as i ) an environmental heterogeneity measure reflecting
variability within grasslands (TWIcv) and ii ) an environmental
means measure showing variability between grasslands sites (TWImean;sensu Stark et al. 2017). High levels of soil moisture have been
reported to adversely affect ant species richness and density in Central
European grasslands, with most ant species having a narrow range of
tolerance to water content in soils (Dahms et al. 2005, Dauber et al.
2005, Seifert 2017, Heuss et al. 2019). In this sense, it seems likely
that a higher environmental heterogeneity in terms of soil moisture
(high TWIcv) exerts a positive effect on ant communities within
grassland sites by providing more niche-spaces to be exploited by a
wider group of species with different tolerances to wetness. On the
other hand, the significant negative effect of mean soil moisture on
ants likely reflects the gradient in humidity between grassland sites in
the study area, where less humid grasslands (lower TWImean) accommodated
more diverse ant communities than more humid grassland sites (higher
TWImean). This is in line with a more regional-scale pattern found
across Central Europe, where ant diversity decreases from warm-dry to
humid-cool grasslands (Dekoninck 2007, Seifert 2017). In contrast to
soil moisture, the effect of mean air temperature was more evident at
species than at entire community level (total nest density per site)
where nest densities of the reportedly thermophilic species L.
niger , L. flavus , M. rubra and Formica cunicularia(cf. Figure A4) increased along with Tmean (Seifert 2017, 2018).
In addition to the role of soil moisture, our findings showed that
extensively managed pastures promote nest density of most of species
compared to extensive meadows, which supports previous results
highlighting the benefits of extensive grazing on biodiversity compared
to annual mowing (Tälle et al. 2016). Although both extensive management
types are expected to be beneficial for biodiversity in semi-natural
grasslands, the mechanisms behind their effect on grassland vegetation
and fauna may differ (Lepš 2014, Tälle et al. 2016). While low intensity
(gradual but continuous) grazing by cattle creates a small-scale mosaic
of disturbances in soil and spatial structure of vegetation (vertical
and horizontal), annual mowing homogenizes the vegetation structure
through consistent and uniform biomass removal in a short period of time
(Olff and Ritchie 1998, Adler et al. 2001, Lepš 2014, Tälle et al.
2016). Thus, grazing disturbance not only enables openness throughout
the sward but also creates a variety of different micro- sites and
micro-climates suitable for a wider group of ground-dwelling insects,
including ants (Cole et al. 2010, Hoffmann 2010, Jerrentrup et al.
2014). The differential effect of management types on grassland
vegetation structure has been shown to affect ants indirectly by
changing micro-habitat and soil moisture conditions (Dahms et al. 2005,
Dauber et al. 2005, Pérez-Sánchez et al. 2018, Heuss et al. 2019), which
correspond to our data showing higher within-site soil moisture
heterogeneity in pastures (TWIcv : mean= 14.7, SD= 5.9) than in
meadows (TWIcv : mean=8.9, SD= 4.5). Thus, both environmental
heterogeneity measures, management type and soil moisture variability,
may address the same synergistic effect of providing favorable
micro-habitat and soil conditions for ant communities.
At the landscape scale, a high diversity of land cover types had a
general positive effect on species composition, while the influence of
the surrounding forest varied among species. The effect of land cover
heterogeneity on ant communities can be interpreted in two different
ways. First, a higher variability in land cover types in the
surroundings of the grassland sites may provide source habitats for new
colonizing species, thereby enriching the local species pool (Benton et
al. 2003, Öckinger et al. 2012). Second, a higher between-habitat
heterogeneity in the surroundings increases the range of abiotic
conditions, particularly along the edges, thus causing ecotonal effects
that may favor thermophilic species near open habitat edges (i.e.
arable, built-up land) or moist-tolerant species near shaded edges (i.e.
forest) within grassland communities (Dauber and Wolters 2004). In our
study region, the higher levels of landscape diversity are located at
intermediate elevations where the land cover matrix transitions from a
built up- to forest-dominated landscape and the proportions of
neighboring arable lands and grasslands reach their peaks (Figure A1).
Supporting the ecotonal effect, the observed species composition in many
of these grasslands was characterized by species with different habitat
preferences: F. fusca (woodland edges), L. acervorum(light forest), F. cunicularia (open verges), L. niger(urban and disturbed open habitats; Seifert 2018). The species-specific
effects of surrounding forests detected in our study further support
this statement, as F. fusca density was positively affected by
%Forest, while densities of L. flavus and F. cuniculariawere negatively affected (Figure A4).
5.2. Effects of local and
landscape heterogeneity on ant community evenness
The effect of environmental heterogeneity on diversity has been
explained by classical niche theory, where habitat heterogeneity is
expected to increase species co-existence and therefore evenness (Stein
and Kreft 2015). However, it has been argued that the high diversity of
species in seemingly homogeneous habitats cannot be explained
exclusively by niche processes, but also by neutral or stochastic
processes related to demography and dispersal events (Hubbell 2001,
Andersen 2008, Brown et al. 2013). In this regard, evenness has been
used as neutrality metric, meaning that habitats with high levels of
community evenness are subject to more neutral than deterministic
processes (Schowalter 2011, Bar-Massada et al. 2014). In our study
system, an important proportion of grassland sites accommodate even
communities, which suggests that neutral processes may also contribute
to structuring ant communities in addition to environmental
heterogeneity. The fact that ant response traits describing colony
reproduction and dispersal constraints in semi-natural grasslands (van
Noordwijk et al. 2012) were important in our fourth-corner analysis
suggest that neutral processes, such as stochastic species dispersal,
may contribute to the local assembly of ant communities. Nevertheless,
these findings, although remarkably interesting, need to be considered
with caution since neutrality levels in species-poor communities are
difficult to interpret as the lower bound of evenness decreases with
richness (1/0D ), and in our studied system
approximately 25% of the grassland sites showed communities with less
than three ant species (Jost 2010, Bar-Massada et al. 2014).
In contrast to our expectations, the effect of environmental
heterogeneity on ant community evenness was variable at local scale and
negative at landscape scale. The effects of TWIcv, TWImean, and SHID on
RLE0,2 were exactly opposite to those observed for
species composition and density, hence their interpretation is
intimately related to our previous discussion. An increase in
within-site soil moisture variability and diversity of surrounding land
cover types certainly supports total nest density, but also benefits
numerical dominant species (i.e. M. scabrinodis or L.
niger ) which may lead to uneven or dominated ant communities in some
grassland sites. Similarly, high levels of soil moisture may promote
community evenness by limiting nest densities of numerical dominant ants
in grasslands, which leads to a more even distribution of species
densities within the community structure (c.f. sites in cluster 2,
Figure 1). Model results additionally showed a positive effect of
within-site surface aspect range (ASPrg) on community evenness. Our
study system contains grasslands mostly facing from east to west through
south azimuths. In grasslands facing east, the soil surface receives
radiation earlier in the day when air temperature and evapotranspiration
are lower leading to moister habitats (Ashcroft et al. 2008); while on
west-facing sites, the soil surface reaches maximum temperatures during
the afternoon when the direct radiation is at its maximum creating
warmer and drier habitats (Bennie et al. 2008). A higher range of
surface exposure within grasslands sites creates highly heterogeneous
habitats for ant species, thereby increasing species co-existence and
promoting ant diversity and community evenness.
5.3. Community structure response
to environmental heterogeneity through species traits
The community structure response to environmental conditions is the
result of different sets of species (response) traits, therefore
quantifying how traits and environment interact provides a mechanistic
understanding of community assembly (Lavorel and Garnier 2002, Zirbel et
al. 2017). Our results show that the response of ant community structure
to local heterogeneity on topography, soil temperature, and management
was strongly related to behavioral dominance and a generalist life
history strategy. Behavioral dominance may be an advantageous trait for
food acquisition and territory defense in open habitats characterized by
patchy vegetation such as pastures (Mtyppasture) with
rugged slopes (SLOcv) where the probability of intra- and inter-specific
competitive encounters is high (Savolainen and Vepsäläinen 1988,
Savolainen et al. 1989, Pérez-Sanchez et al. 2018; but see Stuble et al.
2019). Similarly, species well adapted to deal with low food
availability and variable soil temperatures during nest foundation (life
history strategy G, according to van Noordwijk et al. 2012, cf. Table
2), may be favored in dynamic and heterogeneous habitats such as
extensively managed pastures (Verberk et al. 2010). Surprisingly, we
found a negative relationship between strategy G and within-site solar
radiation range (SRDrg), expected to be positive according to the
environmental heterogeneity hypothesis. We attribute this result to the
overpowering negative effect of within-site soil temperature variability
(SDRrg) on L. flavus densities, rather than the cumulative
effects on all species with life history strategy G (i.e. L.
niger and F. fusca ; van Noordwijk et al. 2012).
Community response to local mean air temperature and soil moisture was
strongly related to worker and colony size traits and, to a lesser
extent, to life history strategies F and T (cf. Table 2). Higher mean
temperatures negatively affected worker size, but positively affected
colony size. The relationship between body size and temperature has been
traditionally related to the heat conservation hypothesis, i.e. a larger
body size has adaptive value in cold temperatures due to lower
surface-to-volume ratios (Cushman et al. 1993, Blackburn et al.1999).
This hypothesis has been questioned for ants, as a larger body size in
ectotherms also reduce the rate of heat gain, which is as important as
decreasing heat loss (Cushman et al. 1993). However, it may be suitable
at the colony level as long as i ) worker body size is positively
correlated to colony size, and ii ) colony size is correlated to
thermoregulatory capabilities (Cushman et al. 1993, Kaspari and Vargo
1995). In our case, some Formica species meet such conditions and
were certainly associated with cooler temperatures in upland sites or
grasslands surrounded by forest (i.e. F. fusca, F. pratensis ).
Nevertheless, it is more likely that this particular result is
influenced by species with small workers but large colonies such asL. flavus and L. niger , which showed high nest densities
in grassland sites with high temperature records. On the other hand, the
interaction of life history strategies with temperature suggests that
grassland sites with high mean air temperatures have a low nutrient
content for ants (strategy F), but may shelter species whose nest
foundation is highly dependent on soil temperature (strategy T; van
Noordwijk et al. 2012).
The strongest interactions between traits and environment were detected
at landscape scale, with a functional response to land cover types
(SHID) similar to local mean air temperature (Tmean). Although both
predictors, Tmean and SHID, did not exceed the collinearity threshold
(|r | < 0.7; Dormann et al.
2013), their effect on ant communities seems to be related. In a
forest-dominated landscape, a high number and even distribution of open
land cover types (i.e. grasslands, arable lands and urban areas) in the
surroundings likely increases air and soil temperature of grasslands;
while a decrease in grassland temperatures can be expected when
surrounding landscape is dominated by forest due to shading (Figure A2;
Krämer et al. 2012, Öckinger et al. 2012, Liivamägi et al. 2014). The
strong and negative relationship between life history strategy T and
%Forest supports this statement, as species depending on high soil
temperature for nest foundation showed low densities or were absent in
grasslands surrounded completely or almost entirely by forest. In this
sense, a high proportion of surrounding forests not only contributes to
grassland isolation by imposing a physical barrier for species
colonization, but also limits abiotic conditions for the establishment
of grassland specialist and thermophilic species (Krämer et al. 2012,
Öckinger et al. 2012).
6. Conclusions
Investigating the impacts of environmental heterogeneity on species
diversity and functional traits at multiple spatial scales is crucial to
better understand community patterns in ecology, and is especially
relevant for biodiversity conservation (Costanza et al. 2011, Ovaskainen
et al. 2017). This study shows that local environmental heterogeneity
within and between grasslands, and the surrounding landscape play a
relevant deterministic role in structuring ant communities in temperate
semi-natural upland grasslands. Heterogeneity in habitat structure
caused by grassland management (i.e. low intensity grazing) and
within-site heterogeneity in soil moisture were the most important local
environmental measures shaping ant species composition and density. At
the landscape scale, a high land cover heterogeneity increased overall
species density within grasslands, although the effect of each
surrounding habitat type depended on species-specific abiotic
requirements. The variation of community evenness against environmental
heterogeneity showed an opposite pattern compared to community
composition due to the inherent relationship between richness and
evenness (Jost 2010). However, this approach revealed that a higher
range of surface aspect (exposure of the slope) within grassland sites
exerts a positive effect on community structure by promoting species
co-existence. Overall, the proportion of even communities was high (54%
of the surveyed sites) compared to uneven (35%) or dominated
communities (11%), suggesting additional (neutral) processes operating
on ant community assembly (Bar-Massada et al. 2014). The response of ant
community structure to environmental heterogeneity at both spatial
scales was mediated by morphological (worker size), ecological (dominant
behavior) and life history (colony size and strategies related with
colony reproduction- dispersal-foundation) traits. The interaction of
the aforementioned response traits and the environment framed in a
fourth-corner scheme proved to be a valuable approach for understanding
how community structure is driven by environmental heterogeneity. We
conclude that ant communities in semi-natural grasslands are not only
driven by environmental heterogeneity but also by complementary neutral
processes related to stochastic habitat colonization, as dispersal
events between isolated grasslands are limited in a forest-dominated
landscape. Both environmental heterogeneity and stochastic explanations
are not exclusive and may represent opposite ends of the same continuous
gradient denoting the relative contributions of both niche and neutral
processes to the assembly of ant communities in temperate semi-natural
grasslands (sensu Gravel et al. 2006).