Biological Conservation 242 (2020) 108422

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Implications of heathland management for ant species composition and T

diversity – Is heathland management causing biotic homogenization?
Rikke Reisner Hansena, , Knud Erik Nielsena, Joachim Offenberga, Christian Damgaarda,
⁎

David Bille Byrielb, Inger Kappel Schmidtb, Peter Borgen Sørensena, Christian Kjæra,
Morten Tune Strandberga
a
Section for Plant and Insect Ecology, Department of Bioscience, Aarhus University, Vejlsøvej 25, DK-8600 Silkeborg, Denmark
b
Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958 Frederiksberg, Denmark

ARTICLE INFO ABSTRACT

Keywords: Maintaining heathland ecosystems in an early successional stage is a major aim of most management regimes,
Composition such as harvesting, burning or grazing. However, how these types of management affect important ecosystem
Ecosystem engineers engineers such as ants, are poorly understood. We registered the density of ant colonies in managed plots
Heathland management (harvested, burned and grazed) and plots with long succession (so forth unmanaged) across six different dry
Species conservation
lowland heath sites. With these data, we investigated how composition and richness varied across management
Species richness
regimes and elucidated the direct effects of management from the indirect effects of environmental covariates.
Ant species richness was significantly lower in managed plots compared to unmanaged plots. Harvest and
grazing regimes were associated with the lowest richness, while intermediate richness was registered in burned
plots. Smallest variation in species composition was found in the harvested, followed by grazed, burned and
unmanaged heathlands. There was an overall negative association between abundances of organic mound
forming species and all types of management, while non-mound forming species where negatively affected by
grazing. In addition, Non- and organic mound forming species were indirectly affected through decreasing ve-
getation complexity. Only ants with mineral mounds benefitted from grazing and burning, but not from har-
vesting. To promote ant richness and abundance, we propose to downscale the frequency and intensity of
management, as well as designating certain parts of the heathland area for later successional vegetation stages.

1. Introduction
In open terrestrial ecosystems, current management focuses on
keeping the system at an early successional stage and on preventing
nutrient accumulation in the system (Gimingham, 1994; Mobaied et al.,
2015). Plant species are then applied as the model indicator from which
all effects are estimated (Webb, 1998), occasionally with detrimental
costs to arthropod diversity (Klink et al., 2013).
Danish heathland ecosystems are strongly influenced by different
management regimes roughly divided into the following categories: pre-
scribed burning, harvesting, sod cutting and grazing (Degn, 2016). Each of
these aimed at regenerating dwarf shrub vegetation, Calluna vulgaris (L.)
Hull in particular. In the absence of management or naturally occurring
disturbances (i.e. deer grazing, wild fires etc.), tree species like Mountain
and Scots pine (Pinus mugo (Turra) and P. sylvestris (L.), respectively), will
become dominant and the open heathland areas will diminish. Dis-
turbances, whether caused by machinery, fire or large herbivores, will
influence biotic and abiotic variables mostly due to changes in vegetation
complexity (Måren, 2009; Rosa García et al., 2013), and intuitively this
will generate environmental variation. Conversely, when frequently ap-
plying one management regime to larger areas, the risk is a homo-
genization of the biotic as well as the abiotic environment, limiting the
amplitude of available ecological niches (McKinney and Lockwood, 1999;
Harpole and Tilman, 2007; Nordberg and Schwarzkopf, 2019).
The degree to which management can be expected to affect ant
communities, depend upon the frequency, intensity and timing, as well
as the size of the managed parcel (Andersen et al., 2009; Philpott et al.,
2009; Maravalhas and Vasconcelos, 2014). As well as for other ar-
thropods, both abiotic and biotic factors govern the diversity of ants and
determine the species distribution of ants (Cushman et al., 1988;
Hölldobler and Wilson, 1990; Seifert, 2017), rendering them equally
susceptible to management. This occurs both through the direct me-
chanistic forces of management to the colony (Morris, 2000), but also
through the indirect effects on microclimate and vegetation structure

⁎
Corresponding author.
E-mail address: rrh@bios.au.dk (R.R. Hansen).

https://doi.org/10.1016/j.biocon.2020.108422
Received 4 September 2019; Received in revised form 8 January 2020; Accepted 13 January 2020
0006-3207/ © 2020 Elsevier Ltd. All rights reserved.
R.R. Hansen, et al.
Fig. 1. A map of Jutland showing the location and size of the heathlands investigated in the study with the location within Europe depicted with a square in the inset
box in the lower left corner. The inset figure in the lower right corner shows the location of the selected plot within the management parcel, as well as the
experimental design within each plot and heathland site (upper right). Grey circles are subplot locations and the squares shows an example of the randomised
locations for pin-point analyses and environmental covariate registration.
(Andersen, 2018), as well as a reduction of food resources (Blüthgen and
Feldhaar, 2009). Reduced complexity in environmental heterogeneity
may thus lead to a homogenization of ant communities through reduced
species richness. This is then exemplified either through increased
dominance of single species (Moranz et al., 2013; Vonshak and Gordon,
2015) or through a shift in microclimatic conditions favoring warm
temperate species, and filtering out species dependent on accumulation
of organic structures for nest building (Seifert, 2017; Andersen, 2018).
Studies on ant responses to disturbances are widely applied in arid
Australian ecosystems, where wild fires, grazing cattle and mining ac-
tivities are the main source of disturbance (Andersen and Majer, 2004).
Very few studies differentiate between the direct and the indirect effects
of management on ant assemblages in pursuit of the optimal manage-
ment scheme (Heuss et al., 2019). In temperate regions, studies on ant
community responses to management are mostly limited to grassland
habitats, where frequent disturbances are a prerequisite for habitat
conservation (Dauber and Wolters, 2005; Pihlgren et al., 2010; Heuss
et al., 2019), causing disturbance-tolerant ant assemblages (Arcoverde
et al., 2018). However, in temperate and low productive heathland
ecosystems, ant community responses to management-mediated dis-
turbances have been less studied. Because ant species responses have
been shown to differentiate between habitats of differing structural
complexity and hydrological regimes (Arnan et al., 2006; Arcoverde
et al., 2018), we would expect different responses of ant assemblages to
disturbances in arid, acidic and low productive ecosystems.
As abundant and important ecosystem engineers, ants play an im-
portant role as mediators of many ecological processes, including the
decomposition of organic matter, soil turnover and structure, nutrient
cycling, plant protection, seed dispersal, and seed predation (Hölldobler
and Wilson, 1990; Folgarait, 1998;Frouz and Jílková, 2008; Nakamura
et al., 2007). Their role as ecosystem engineers is especially important in
acidic environments where earthworms and other soil-burrowing
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Biological Conservation 242 (2020) 108422
organisms are scarce (Wallwork, 1976; Beylich and Graefe, 2009). Ants'
ability to modulate the environment is exploited by a multitude of other
organisms (Cagnolo and Tavella, 2015), ranging from soil bacteria and
microarthropods (Wagner et al., 1997), to surface active arthropods
(Päivinen et al., 2002), and butterflies (Fiedler et al., 2006). Some or-
ganisms, like birds, rely on ants for food and cleansing of plumage
(Coudrain et al., 2010), while some utilize the warmer microclimate in or
on the mound (Streitberger and Fartmann, 2015). Ants affect vegetation
richness and structure, both positively through predation of herbivorous
insects (Muniz et al., 2012), but also negatively through interactions with
honeydew-producing hemipterans (Wills and Landis, 2018). In addition,
ants increase plant species richness directly via soil disturbance, which
help secure islands for less competitive plant species (Dean et al., 1997).
However, this ecological importance of ants is in stark contrast to the
lack of attention they receive in management planning and conservation.
We studied how current heathland management practices affect ant
species composition and diversity, and quantified how these compo-
nents vary across four management regimes, burning, harvesting,
grazing and unmanaged heathland. Through the appliance of multi-
variate methods in a Bayesian framework, we explored the following
hypothesis. Species assemblages are significantly different across
management treatments. We further explored the hypothesis that spe-
cies with different nesting strategies (i.e mineral, organic or non-nesting
ant species), responds not only to the direct effects of management, but
also indirectly to the altered environmental conditions. For this pur-
pose, we employed structural equation modelling.
2. Methods
2.1. Study system
The study was conducted at six heathland sites in Denmark (Fig. 1).
R.R. Hansen, et al.
The selected study sites were inland dry lowland heaths on acidic, low-
nutrient sandy soils. The parental soil geology of the selected locations
consisted primarily of downwash sandy deposits with elements of
Aeolian sand and glaciofluvial sand and gravel. The locations were
typically dwarf shrub-dominated with patches of grass primarily
dominated by purple moor grass (Molinia caerulea (L.) Moench) or wavy
hair grass (Deschampsia flexuosa (L.) Trin.).
Climatic parameters varied little across the selected heathland sites.
Mean average temperature for 2018 ranged from 9.2 °C to 9.5 °C with
minimum temperature ranging from −10.9 °C to −9.8 °C and max-
imum ranging from 32.3 °C to 33.1 °C across sites. Average yearly
precipitation across sites varied from 666 mm to 726.1 mm. Average
hours of sunshine across Denmark ranged from 1740 to 1830 h.
2.2. Study design
We selected the heathland sites based on four criteria to enable
comparison between managed and unmanaged areas: (1) sites included
an area of heathland unmanaged for > 30 years. (2) Sites should in-
clude a minimum of two areas with different management regimes
(burned, grazed or harvest). (3) The management regime had to be
consistent in type, as well as being applied with less than ten years in
between, and with the latest application within the last four years. (4)
Areas should be large enough to include a 1 ha square plot with a 100 m
edge buffer. Unfortunately, none of the considered Danish heathland
sites included all possible management combinations, which led to an
unbalanced design (Table 1). The different management regimes in-
cluded three areas of prescribed burning, performed in early spring.
Five machine harvested areas, uniformly cut at a height of 5–10 cm.
Three grazed areas, one heavily grazed by red deer, and two grazed by
cattle in the summer with approximately 0.4 animal units per ha (one
animal unit = 550 kg). Six unmanaged areas, where management has
been abandoned > 30 years.
The managed and unmanaged areas which met the criteria were
mapped in QGis Version 2.14.21. Within each site and management
polygon, we randomly established a 1 ha square plot, which we sub-
divided into 100 subplots with each 10 m between. These subplots
formed the basis for ant-colony search. To avoid edge effects, we es-
tablished a buffer of 100 m to the edge of the management polygon.
Each plot was located > 400 m apart to avoid species exchange be-
tween plots. Apart from the subplots, we selected 10 vegetation survey
plots to form the basis for registering environmental variables. These
were randomly distributed within each plot (Fig. 1). Kongenshus
heathland had grazing sheep in all three management types, however,
we estimated that the sheep's use of the selected plots were negligible,
based on presence/absence of sheep feces and bites to the vegetation.
Borris heathland is a military area, where management is carried out
yearly to prevent spontaneous fires caused by exploding artillery.
The design encompasses to different spatial resolution levels of
sampling. One for ant sampling and one for registering environmental
covariates. The reason for this is that we chose a very high-resolution
Table 1
An overview of the selected sites and the management carried out in the se-
lected plots. The number under Burn, Harvest, and unmanaged is the number of
years since the management was last applied. For grazing the number is the
number of years it has been grazed.
Site Burn Harvest Grazing Unmanaged (years)
(years) (years) (years)
Harrild 3 2 > 50
Kongenshus 1 1 > 50
Borris 1 1 > 30
Ovstrup 2 > 50 > 50
Randboel 2 > 30 > 100
Noerholm > 50 > 100
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Biological Conservation 242 (2020) 108422
sampling for ants to enable a density measure. This would require too
many person-hours to replicate for sampling of covariates.
2.3. Ant sampling and identification
Through active search, we manually registered colony abundances
of all ant species in the 17 selected one-hectare plots during two weeks
of similar warm and dry weather conditions in July 2018. At each
subplot, we estimated a circle of four meters in diameter (17 plots with
100 subplots yielding 1700 subplots in total), and inspected all poten-
tial nest habitats, i.e. grass tussocks, mounds, sphagnum moss, soil,
rocks and dead wood. In addition, we inspected three random places
within each circle to detect species leaving few aboveground signs.
Search time varied drastically with structural complexity. Highly
structurally complex plots took an estimated six person-hours, whereas
the more homogenous plots took a maximum of one person-hour. For
the species where field identification was challenging, we sampled a
few individuals from each colony for later identification in the la-
boratory.
All ants were identified to species using the available identification
keys (Seifert, 2000; Abenius et al., 2012; Seifert, 2018). The dataset is
available through the Open Science Framework (Hansen et al., 2019).
2.4. Environmental covariates
We registered plant species composition in each vegetation survey
plot with a 50 cm × 50 cm pinpoint frame with 25 pins in total. At
every pin, we measured vegetation height directly to get a solid base for
averaging across the plot. We inserted a soil corer (Ø = 3 cm) in three
positions close to each vegetation survey plot (center, North and South)
with 1 m apart and registered the depth of each soil horizon. In the
same positions, we measured soil moisture content (Volumetric Water
Content) in the top 5 cm using a HH2 moisture meter with a ML3 Theta
probe attached.
The mean depth for all soil horizons, as well as, mean values for soil
moisture and vegetation height was calculated across each plot.
Pinpoint data were aggregated into five cover classes: Dwarf shrubs,
graminoids, forbs, mosses and lichens and a measure for mean cover
and the degree of spatial aggregation was calculated under the as-
sumption that pin-point plant cover data was beta-binomial distributed
(Damgaard and Irvine, 2019). As environmental covariates were mea-
sured on different scales, they were standardized to a zero mean and
unit variance prior to analysis. All statistical analyses were carried out
in R version 3.5.2.
2.5. Ant species richness
We calculated species richness for each subplot and averaged it
across plots for each management regime to estimate the amount of
species per management regime. To estimate effects of management
regime on species richness at the subplot level, we employed a Bayesian
framework, which estimates credibility intervals of the posterior dis-
tributions of each management regime with site as a random factor. The
statistical inferences were assessed using the calculated 95% percentiles
of the marginal posterior distribution of the parameters (credibility
intervals). For this purpose, we used the ‘R-INLA’ package (version
19.09.03) with default prior setting. (Rue et al., 2009). R-INLA is an R
package that uses the Laplace approximation to calculate the joint
posterior distribution of the model.
2.6. Species composition
To assess how the species assemblages varied within and across
management regimes, we investigated species composition in a multi-
dimensional space. For this purpose, we employed latent variable
modelling through the R package ‘boral’ (Hui, 2016). Latent variable
R.R. Hansen, et al.
modelling is a Bayesian model-based approach that models community
composition through a set of underlying latent variables to account for
residual correlation, for example due to biotic interaction. This method
offers the possibility to adjust the distribution family to e.g., negative
binomial distribution, which better accounts for over-dispersion in
count data (Warton et al., 2012). Thus, it accounts for the increasing
mean-variance relationship without confounding location with disper-
sion (Hui et al., 2015). We created a latent variable model at subplot
level with a negative-binomial distribution and two latent variables to
visualize how the ant communities were distributed. Site was added as
a random factor and management regime as fixed effects. From the
latent variable model, we extracted the posterior median values of the
latent variables which we used as coordinates on ordination axes to
represent species composition at subplot level (Hui et al., 2015). We
drew convex hulls around posterior median values belonging to each
management regime to visualize the difference. For this purpose, we
used the function ‘ordihull’ in the r package ‘vegan’ (Oksanen et al.,
2016).
Because model based ordination lacks resampling, it is not well
suited for hypothesis testing (Francis Hui, Pers. Comm.). We therefore
tested our first hypothesis with a multivariate extension of GLMs as
recommended by Warton et al. (2012), using the function ‘manyglm’
and subsequently ‘anova.manyglm’ in the package ‘mvabund’ (Wang
et al., 2012). This method offers the possibility to model distributions,
and test hypotheses based on multivariate count data by correlating
each row of the dataset to an environmental covariate (column), as-
suming a negative binomial distribution. We ran two models, where we
first tested for an interaction between site and management. In the
second model, site was then included as a random effect, management
regime as a fixed and we subsequently compared all management re-
gimes against each other in a post-hoc comparison test offered via the
function ‘anova.manyglm’ with site included as a random factor.
The model assumptions of mean-variance and log-linearity were
examined, for both models, with residual vs. fitted plot and a normal
quantile plot.
2.7. Effects of environmental variables and management
We calculated abundance-weighted values for three different types
of nest organization following Seifert (2018), which we hypothesized to
be affected both directly and indirectly by management. The selected
types of nest organization were mineral mound forming species (two
species), organic mound forming species (six species) and non-mound
forming species (12 species). An overview of species and their trait
assignments can be found in Appendix (Table A1).
To analyze the direct and indirect effects of management on ant
species assemblages, we fitted a piecewise structural equation model
using the R package “piecewiseSEM” (Lefcheck, 2016). As an important
first step in every SEM model, we first formed an à priori model (Grace
et al., 2010). This conceptual framework was based on available lit-
erature (Philpott et al., 2009; Seifert, 2017; Andersen, 2018; Li et al.,
2018), and our ecological understanding of the three groups. Starting
from hypotheses that species grouped into different nest strategies each
depend on a specific substrate (Seifert, 2017; Andersen, 2018), we se-
lected environmental covariates meaningful for the groups nesting
microhabitat and strata of foraging, as described by Seifert (2017).
Because most organic mound forming species are polydomous and
have limited dispersal and foraging ranges (Seifert, 2017), we hypothe-
sized that their ability to form these large complex structures would be
negatively correlated with a decrease in mean vegetation height, litter
layer, dwarf shrub cover and graminoid cover. This would also mean that
all management forms, causing a direct destruction of their mounds (i.e.
harvesting and burning), would negatively affect them.
The abundances of mineral mound forming species are known to be
promoted by grazing from large herbivores (Li et al., 2018), which we
know decreases the vegetation height and shifts the dominance of the
4
Biological Conservation 242 (2020) 108422
heathlands towards higher forb and graminoid dominance (Newton
et al., 2009). We also predicted that harvesting would have a direct and
negative effect on the mineral mounds, due to the mechanistic impacts
of harvesting, removing the mound construct entirely. Furthermore,
they are often highly abundant on the heathland soils, which are
missing a well-developed hardpan layer or where the eluvial layer (i.e.
the sandy material in the soil horizon with maximum leaching of or-
ganic material and metals) is deep (Pers. Obs.). Consequently, we tested
for indirect effects of mean forb cover, mean depth of the eluvial layer
and mean vegetation height.
The ant species, which do not form mounds, depend on the substrate
in various ways, nesting in grass tussocks, moss pads and dwarf shrub
swards (Groc et al., 2017; Seifert, 2017; Andersen, 2018). Furthermore,
most species hibernate closer to the surface, and rely on a deep eluvial
layer (Seifert, 2018). We therefore tested for indirect effects of mean
depth of eluvial layer, mean depth of litter layer, mean vegetation
height, mean cover of dwarf shrubs, mean cover of graminoids, and
mean cover of mosses. However, as some non-mound-forming species
are thermophilic and dependent on an open environment, we hy-
pothesized grazing, burning and harvesting to have a direct positive
effect.
To account for multicolinearity, we first computed Pearson corre-
lation coefficient between all sets of covariates and tested their sig-
nificance with the function ‘cor test’ in R. When r2 values of the cor-
relations were significant (p < 0.05), we specified a correlated error
between the covariates. Site was included as a random effect and
management regimes as fixed effects. The four management regimes
were modelled by indicator variables. In this way, we test the effect of
one management regime against the other three. We standardized the
path regression coefficients via the latent theoretic approach for bino-
mial models as recommended by Lefcheck (2016). The structure of each
model can be found in the Appendix (Fig. A1) and a correlogram matrix
of the significant covariate correlations Fig. A2. Model adequacy was
verified by examination of residuals.
3. Results
We identified 20 ant species belonging to five genera. A species list
including management and site-specific abundances is included in the
Appendix (Table A1). Boxplots of the measured environmental covari-
ates summarized over management regime can be found in the Ap-
pendix (Fig. A3).
3.1. Ant species richness
When averaged across plots, we found a mean species richness of
4.4 ( ± 1.0 SE) in the harvested plots. The grazed plots had a mean
species richness of 5.3 ( ± 1.5 SE), compared to 9.3 ( ± 1.9 SE) species
in the burned plots and 11.8 ( ± 1.0 SE) in the unmanaged plots
(Fig. 2a). Species richness at the subplot level differed significantly
between some of the management regimes. There was no significant
difference between unmanaged and burned plots, or between the har-
vested and the burned plots, as the credibility intervals of the posterior
distributions overlapped. Burned and unmanaged plots were both sig-
nificantly different from harvested and grazed plots with non-over-
lapping credibility intervals (Fig. 2b).
3.2. Species composition
The latent variable analysis indicated higher species variation
within the unmanaged plots (i.e. beta diversity), followed by the
burned, and less in both the grazed and the harvested plots (Fig. 3). In
the multivariate glm testing for the interaction between site and man-
agement, there was a significant effect of site (p = 0.001) and man-
agement as well as a significant interaction between them (p = 0.001).
Following the inclusion of site as a random effect, management alone
R.R. Hansen, et al. Biological Conservation 242 (2020) 108422

(caption on next page)

5
R.R. Hansen, et al.
Fig. 2. a) A dotplot showing species richness of ants (Mean ± SE) at plot level for each of the four management regimes. b) A boxplot showing species richness at
subplot level for each of the four management regimes and for each of the six sites. Outlayers are depicted as dots, whiskers display minimum and maximum, the box
depicts the first quartile, the median and the third quartile. Letters a and b demonstrates statistical significance between management regimes (p < 0.05).
was no longer significant (p = 0.16). In the subsequent pairwise test
however, all of the management regimes differed significantly from
each other (p = 0.001).
3.3. Effects of environmental variables and management
In the Piecewise SEM all three management regimes exerted sig-
nificant negative impacts on the abundance of organic mound forming
ant species (harvest: β = −4.48, p < 0.0001, grazing: β = −6.16,
p < 0.0001, burning: β = −3.85, p = 0.001) (Fig. 4a). Harvesting and
grazing had indirect effects through the decreased vegetation height
(β = −0.77, p < 0.0001, β = −0.53, p < 0.0001 respectively),
which acted negatively on organic mounds (β = −0.27, p = 0.003).
Grazing furthermore promoted the cover of graminoids (β = 0.54,
p < 0.0001), but decreased the cover of dwarf shrubs (β = −0.55,
p < 0.0001), both of which acted positively on the organic forming
ants (β = 4.93, p < 0.0001, β = 4.49, p < 0.0001, respectively).
Conversely, harvest and burning exerted indirect negative effects by
decreasing the cover of graminoids (β = −0.09, p < 0.0001,
β = −0.13, p < 0.0001, respectively). There was no significant effect
of mean depth of the litter layer (p = 0.16) (Fig. 4b). The model had an
overall r2 value of 0.36.
The abundance of mineral mound forming species were positively
impacted by grazing (β = 6.73, p < 0.0001) and burning (β = 4.38,
p < 0.0001), but negatively by harvesting (β = −3.28, p = 0.02)
(Fig. 4a). In addition, they were positively impacted by an increasing
forb cover (β = 12.94, p < 0.0001), which was also significantly pro-
moted by grazing (β = 0.57, p < 0.0001). Mean depth of the eluvial
layer or mean vegetation height did not have significant effects
(p = 0.72, p = 0.11 respectively) on abundance of mineral mound
forming ant species (Fig. 4b). The model explained 32% of the variation.
For non-mound forming ant species, the SEM showed that grazing
was the only management regime with significant and negative impacts
on the abundance (β = −5.77, p < 0.0001) (Fig. 4a). Harvest and
Fig. 3. Species distribution plot of the best fitted latent variable model showing the mean of the latent variable with a negative binomial distribution. Size of the hulls
indicate the variation in species assemblages within management type.
6
Biological Conservation 242 (2020) 108422
burning had direct and positive effects (β = 7.99, p < 0.0001 and
β = 7.51, p < 0.0001, respectively) Harvest also impacted non-
mounds indirectly as harvest decreased vegetation height (β = −0.77,
p < 0.0001), that acted positively on the non-mound forming ants
(β = 0.99, p < 0.0001). Mean depth of the eluvial and litter layer both
had significant and positive effects on non-mound forming ant species
(β = 0.58, p < 0.0001 and β = 1.54, p < 0.0001, respectively), and
the latter was significantly decreased by all three management regimes
(harvest: β = −0.75, p ≤ 0.0001, grazing: β = −0.77, p ≤ 0.0001,
burning: β = −0.56, p < 0.0001) (Fig. 4b). The total r2 value was
27% for the full model.
4. Discussion
We have presented evidence of homogenization of ant assemblages
caused by heathland management. Both the species richness analysis
and the species composition analysis demonstrated how harvesting and
grazing both exercised heavy impacts on ant communities, while the
effects of burning were modest (Figs. 3–4). Structural equation mod-
elling further showed how organic mound forming species (6 species)
were directly and negatively affected by all three types of management,
whereas the non-mound forming species (12 species) were negatively
affected by grazing and indirectly by harvest. Only the mineral mound
forming ants (two species) benefitted from the management regimes
grazing and burning, directly as well as indirectly.
In previous studies, ants have shown remarkable resilience towards
grazing (Underwood and Christian, 2009; Heuss et al., 2019), but in this
study, we found the studied grazing pressure (0.4 animal units) to have
detrimental effects on overall ant species richness and composition
(Figs. 2–3), but only for abundances of organic and non-mound forming
species (Fig. 4). We believe the organic mound forming species are
impacted because they are poor disperses (Seifert, 2018) and many,
such as Formica rufa (Linnaeus, 1761) and F. pratensis (Retzius, 1783),
are adapted to structurally complex environments. Trampling by
R.R. Hansen, et al. Biological Conservation 242 (2020) 108422

Fig. 4. a) Structural equation model showing direct effects of management types on the abundance weighted nest strategies over all sampled subplots (n = 1700). b)
Structural equation model showing indirect effects of management regimes through environmental covariates on the abundance weighted nest strategies over all
sampled subplots (n = 1700). a and b) Only significant (p < 0.05) interactions between variables are depicted (full lines show positive interactions and stipled show
negative interactions). We report the significant path coefficients as standardized effect sizes on top of the arrows. Boxes feeding into both diagrams is the proportion
of remaining unexplained variation.

grazing cattle further causes soil compaction, which negatively impacts
soil fauna (Schlaghamerský et al., 2007), potentially decreasing the
abundances of important prey items. Concomitantly, trampling would
also directly affect the non-mound forming species as they nest close to
the surface (Seifert, 2018). This was also indicated by a negative re-
sponse in the model. Mineral mound forming ants were positively im-
pacted by grazing and this was manifested by exceptionally high
abundances of Lasius flavus (Fabricius, 1781) in grazed plots (Table A1).
As proposed by Li et al. (2018), this could be explained by reciprocal
facilitation between grazing animals and Lasius species (Li et al., 2018).
The large shift in vegetation cover in the grazed plots towards a more
forb-dominated structure (Fig. A4) had positive effects on mineral
mound abundances (Fig. 4b), and could promote additional suitable
plant hosts for the ant-aphid symbiosis. In the present study, we chose
to keep grazing pressure constant and to select areas with a long con-
tinuity of grazing animals. However, as the response of biodiversity to

7
R.R. Hansen, et al.
grazing is not easily generalizable and often complicated by a multitude
of factors (Milchunas and Lauenroth, 1993; Heuss et al., 2019), there is
an urgent need for controlled experiments to address the impact each
grazing regime.
We detected positive direct effects of harvest and burning on the
non-mound forming species, indicating that some non-mound forming
species benefit from an increase in open patches as generated by
management. The abundances however, were quite low in most sites
(Table A1). The species registered in the harvested plots were pre-
dominately L. niger (Linnaeus, 1758) (mineral mound), Myrmica scab-
rinodis (Nylander, 1846) (non-mound) and M. ruginodis (Nylander,
1846) (non-mound) (Table A1), all quite common species, and known
to be rather tolerant to disturbances (Dauber and Wolters, 2005; Grill
et al., 2008). In contrast to the other two management regimes, har-
vesting leaves a uniform imprint on the area, by consistent biomass
removal in a short time period (Lepš, 2014), forming an environment
with dwarf shrub dominated fields of equal age and height (Fig. A4),
and few suitable nest sites. The overall low abundances and absence of
a majority of species in the harvested plots is then likely to be caused by
a reduction in available nest sites. Increasing vegetation height and
mean depth of litter layer did also exhibit positive effects on the non-
mound forming species and these variables were negatively affected by
harvest, further substantiating this theory. Species, which form large
polydomous colonies, such as F. exsecta (Nylander, 1846) or F. pratensis
are highly vulnerable to the mechanistic forces destroying the nests
(Heuss et al., 2019). This was corroborated in the present study as
harvest affected the abundances of both types of mounds considerably
and we detected no indirect effects.
Burning only posed a direct immediate threat to the abundances of
organic mounds, possibly due to the aboveground structure of the nests
being destroyed in fire events. Furthermore, organic mound forming
species on the heathlands are limited in their ability to rebuild nests by
their short foraging ranges and poor dispersal capacity (Seifert, 2017;
Seifert, 2018). Consequently, colonization from nearby areas is slow in
post fire heathland patches. For non-mound building species the effect
of burning was positive and there was also a positive effect of a deeper
eluvial layer. The depth of the eluvial layer controls the extent of bio-
turbation (Hart and Humphreys, 2004) and thus the horizontal niche
for some species (Seifert, 2018). A deeper eluvial layer may then buffer
the direct effects of fire and control the capacity of non-mound forming
species to evade lethal temperatures. However, long term fire regimes
with short intervals can result in persistent impacts on vegetation
structure, resonating in available nest sites, food resources and even-
tually lead to changes in ant assemblages (Andersen, 2018).
The responses were not consistent across sites, as demonstrated by
the multivariate extension of GLM. This indicates that the responses of
the local assemblages to management rely on the local species com-
position, because prevailing conditions within each site promotes spe-
cific ant assemblages. For instance, available soil moisture may de-
termine the severity of fire on ant communities (Arnan et al., 2006).
Large to small-scale patches are usually left unaffected, due to increased
soil moisture, which may cause ants to be less affected by fire in wetter
sites. In addition, responses to disturbance may also be larger in more
structurally complex habitats (Arcoverde et al., 2018), due to differ-
entiated adaptations in functional trait assemblages. This also presents
as a plausible explanation of the contrasting responses to grazing be-
tween this study and studies from more productive ecosystems. This
study however, did not include an analysis of the surrounding areas,
which is also an important factor shaping local ant communities
(García-Martínez et al., 2017). Further studies should include this
factor.
According to literature, ants are seldom directly affected by dis-
turbances as only parts of the massive colony are affected (Pihlgren
et al., 2010). As such, impacts occur through the changes in vegetation
8
Biological Conservation 242 (2020) 108422
structure and microclimate (Andersen, 2018). Ants are, to some degree,
able to manipulate their nest habitat to accommodate these changes
(Philpott et al., 2009), but when the disruption in available niches is
applied frequently and to large homogenous fields, there are no refuges
and survival depends on dispersal capacity. As such, all three man-
agement types were detrimental to species with limited dispersal ca-
pacity and foraging ranges, as well as, species with complex poly-
domous nesting strategies. This study also demonstrated the importance
of vegetation height and cover, but the importance differentiated
among nest strategies. Contrasting responses between ants with dif-
ferent nesting strategies merely asserts the complexity of ant-ecosystem
interactions and advocates for studies of ant responses at a higher
taxonomic resolution. The unmanaged areas all bore resemblance to
later successional stages with (for some sites) more tree encroachment,
Empetrum dominated dwarf shrub assemblies and a thick litter layer.
These factors will naturally produce a microclimate unsuitable for a
large number of ectotherms, including thermophilic ant species, and
small-scale disturbances may therefore be warranted in these ecosys-
tems. We cannot dismiss the notion that some ant species may be very
persistent under the unmanaged regimes. L. flavus and L. niger, for in-
stance, are able to accommodate the increasing vegetation height
through increased mound size, but tree encroachment would over time
cause them to disappear. To our knowledge, no studies have attempted
to link direct and indirect responses to management with specific life
history traits, such as nest strategies. While this study sampled man-
agement regimes in situ, it was at the cost of replication numbers.
However, the documented ant responses are substantiated by literature
(Seifert, 2017; Andersen, 2018; Seifert, 2018). Because ant diversity
integrates a multitude of traits, we advocate for more studies, aimed at
disentangling the specific drivers of ant responses for species with si-
milar traits.
5. Conclusion
There is an urgent need to rethink current heathland management
practices. Our results demonstrate that allowing heathland areas to
reach later successional stages is pivotal in maintaining a high ant
species diversity. In addition, the differentiated responses of ants with
different nesting strategies, advocates for variation in management re-
gimes. The indirect responses to the altered environment stress the need
for a less frequent interference, while allowing the ecosystem longer
time to regenerate. Hence, we recommend downscaling heathland
management in both frequency, intensity and the size of the managed
parcels. There is a need to study the timeframe in which management
abandonment can persist, while still supporting high biodiversity.
Maintaining high ant abundances and diversity, also maintains many
ecosystem functions and is thus beneficial to other taxonomic groups.
Role of the funding source
All authors acknowledge the substantial funding provided by Aage
V. Jensen foundation without which the project would not have been
realized.
Declaration of competing interest
The authors certify that they have no affiliations with or involve-
ment in any organization or entity with any financial interest (such as
honoraria; educational grants; participation in speakers' bureaus;
membership, employment, consultancies, stock ownership, or other
equity interest; and expert testimony or patent-licensing arrangements),
or non-financial interest (such as personal or professional relationships,
affiliations, knowledge or beliefs) in the subject matter or materials
discussed in this manuscript.
R.R. Hansen, et al. Biological Conservation 242 (2020) 108422

Appendix A

Fig. A1. Detailed description of SEMs used to analyze all direct and indirect effects of management and environmental variables, which were found to be important
to ant species nesting strategy. One model was fitted to each nesting strategy. Site was included as random effect and the Piecewise SEM was modeled with a general
linear mixed effect model for the response variable (nest strategy) with a binomial error distribution, and linear mixed effect models for the environmental covariates.
%~~% means that a correlated error between variables were included.
9
R.R. Hansen, et al. Biological Conservation 242 (2020) 108422

Fig. A2. S3: Correlogram showing the significant (p < 0.05) correlations of the correlation test. The size and color of the circle is scaled after r2 value.

Fig. A3. S3: Boxplots of environmental covariates by mangement type. B = Burn, G = Graze, H = Harvest and U = Unmanaged.

10
R.R. Hansen, et al. Biological Conservation 242 (2020) 108422

Table A1
An overview of total abundances of the colonies registered as summarized over site and management regime (type). B, H, G and U indicate whether the plot was
Burned, Harvested, Grazed or Unmanaged respectively.

Site Total across sites Borris Harrild Kongenshus Noerholm Ovstrup Randboel

Species Nest organization B H G U B H U B H U B H U G U G H U G H U

Formica exsecta Organic mound forming 37 6 34 246 37 0 48 0 0 59 0 0 2 11 39 8 0 22 15 6 76

Formica forsslundi Non-mound forming 6 1 0 16 6 0 9 0 0 1 0 0 0 0 3 0 0 0 0 1 3
Formica fusca Non-mound forming 16 2 4 97 11 0 6 0 1 0 5 0 13 1 19 0 1 50 3 0 9
Formica picea Non-mound forming 28 5 10 133 21 0 35 7 2 44 0 0 0 5 20 0 1 0 5 3 34
Formica pratensis Organic mound forming 0 0 0 7 0 0 0 0 0 0 0 0 0 0 7 0 0 0 0 0 0
Formica pressilabris Organic mound forming 0 0 0 4 0 0 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0
Formica rufa Organic mound forming 0 0 0 3 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0
Formica sanguinea Organic mound forming 4 1 0 3 4 1 1 0 0 1 0 0 1 0 0 0 0 0 0 0 0
Formica uralensis Organic mound forming 0 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0
Lasius flavus Mineral mound forming 152 0 420 77 104 0 43 0 0 0 48 0 8 239 3 40 0 2 141 0 21
Lasius niger Mineral mound forming 64 11 66 12 26 3 2 23 1 0 15 0 9 51 0 7 3 0 8 4 1
Leptothorax acervorum Non-mound forming 0 0 0 11 0 0 4 0 0 1 0 0 2 0 3 0 0 1 0 0 0
Myrmica lobicornis Non-mound forming 6 7 3 30 5 0 2 0 0 4 1 1 3 0 5 0 0 0 3 6 16
Myrmica rubra Non-mound forming 5 2 0 18 3 0 3 1 0 5 1 0 3 0 4 0 0 3 0 2 0
Myrmica ruginodis Non-mound forming 22 47 5 168 10 5 19 8 5 24 4 3 25 0 27 0 1 37 5 33 36
Myrmica sabuleti Non-mound forming 0 0 0 2 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0
Myrmica scabrinodis Non-mound forming 6 13 2 64 4 0 11 1 0 8 1 0 12 0 7 0 0 12 2 13 14
Myrmica schencki Non-mound forming 0 0 0 2 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0
Myrmica sulcinodis Non-mound forming 9 1 0 21 3 0 1 4 0 2 2 0 1 0 0 0 1 17 0 0 0
Tetramorium caespitum Non-mound forming 39 0 0 21 13 0 2 26 0 5 0 0 9 0 0 0 0 5 0 0 0

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